Fishery Bulletin

^^ATES O^ ^

r

Marine Bioiogicai Laburasor-
LIBRARY

Vol. 78, No. 1

Woods Hole, Mass.

ADAMS, PETER B. Life history patterns in marine fishes and their consequences '

for fisheries management 1

AMBLER, JULIE W. Species of Munidopsis (Crvistacea, Galatheidae) occurring off
Oregon and in adjacent waters 13

MENDELSSOHN, ROY. Using Markov decision models and related techniques for
purposes other than simple optimization: analyzing the consequences of policy
alternatives on the management of salmon runs 35

STOUT, VIRGINIA F. Organochlorine residues in fishes from the northwest Atlan-
tic Ocean and Gulf of Mexico 51

PIETSCH, THEODORE W., and JOHN P. VAN DUZER. Systematics and distribu-
tion of ceratioid anglerfishes of the family Melanocetidae with the description of a
new species from the eastern North Pacific Ocean 59

HUNTER, JOHN R., and CAROL M. KIMBRELL. Early life history of Pacific mack-
erel, Scomber japonicus o9

MORSE, WALLACE W. Spawning and fecundity of Atlantic mackerel. Scomber
scombrus, in the Middle Atlantic Bight 103

WEIHS, DANIEL. Respiration and depth control as possible reasons for swimming
of northern anchovy, Engraulis mordax, yolk-sac larvae 109

POWLES, HOWARD. Descriptions of larval silver perch, Bairdiella chrysoura.
banded drum, Larimus fasciatus, and star drum, Stellifer lanceolatus (Sciaenidae) 119

GRIMES, CHURCHILL B., and GENE R. HUNTSMAN. Reproductive biologj' of
vermilion snapper, Rhomboplites aurorubens, from North Carolina and South
Carolina 137

PETERSON, R. H., P. H. JOHANSEN, and J. L. METCALFE. Observations on ear-
ly life stages of Atlantic tomcod, Microgadus tomcod 147

Notes

HINES, ANSON H., and THOMAS R. LOUGHLIN. Observations of sea otters dig-
ging for clams at Monterey Harbor, California 159

WEIS, PEDDRICK, and JUDITH SHULMAN WEIS. Effect of zinc on fin regener-
ation in the mummichog, Fundulus heteroclitus , and its interaction with methyl-
mercury

163

(Continued on back cover)

J

Seattle, Washington

U.S. DEPARTMENT OF COMMERCE

Philip M. Klutznick, Secretary

NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION

Richard A. Frank, Administrator

Terry L. Leitzell, Assistant Administrator for Fisheries

NATIONAL MARINE FISHERIES SERVICE

Fishery Bulletin

The Fishery Bulletin carries original research reports and technical notes on investigations in fishery science, engineering, and
economics. The Bulletin of the United States Fish Commission was begun in 1881; it became the Bulletin of the Bureau of Fisheries in
1 904 and the Fishery Bulletin of the Fish and Wildlife Service in 1941 . Separates were issued as documents through volume 46; the last
document was No. 1103. Beginning with volume 47 in 1931 and continuing through volume 62 in 1963, each separate appeared as a
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in exchange for other scientific publications.

EDITOR

Dr. Jay C. Quast

Scientific Editor, Fishery Bulletin

Northwest and Alaska Fisheries Center

Auke Bay Laboratory

National Marine Fisheries Service, NOAA

P.O. Box 155, Auke Bay, AK 99821

Editorial Committee

Dr. Elbert H. Ahlstrom Dr. Merton C. Ingham

National Marine Fisheries Service National Marine Fisheries Service

Dr. Bruce B. Collette Dr. Reuben Lasker

National Marine Fisheries Service National Marine Fisheries Service

Dr. Edward D. Houde Dr. Jerome J. Pella

University of Miami National Marine Fisheries Service

Dr. Sally L. Richardson

Gulf Coast Research Laboratory

Kiyoshi G. Fukano, Managing Editor

The Fishery Bulletin (USPS 090-870) is published quarterly by Scientific Publications Office, National Marine Fisheries Service, NOAA,
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The Secretary of Commerce has determined that the publication of this periodical is necessary in the transaction of the public business
required by law of this Department. Use of funds for printing of this periodical has been approved by the Director of the Office of
Management and Budget through 31 March 1982.

Fishery Bulletin

CONTENTS

Vol. 78, No. 1

ADAMS, PETER B. Life history patterns in marine fishes and their consequences
for fisheries management 1

AMBLER, JULIE W. Species of Munidopsis (Crustacea, Galatheidae) occurring off
Oregon and in adjacent waters 13

MENDELSSOHN, ROY. Using Markov decision models and related techniques for
purposes other than simple optimization: analyzing the consequences of policy
alternatives on the management of salmon runs 35

STOUT, VIRGINIA F. Organochlorine residues in fishes from the northwest Atlan-
tic Ocean and Gulf of Mexico 51

PIETSCH, THEODORE W., and JOHN P. VAN DUZER. Systematics and distribu-
tion of ceratioid anglerfishes of the family Melanocetidae with the description of a
new species from the eastern North Pacific Ocean 59

HUNTER, JOHN R., and CAROL M. KIMBRELL. Early life history of Pacific mack-
erel. Scomber japonicus 89

MORSE, WALLACE W. Spawning and fecundity^ of Atlantic mackerel, Scomber
scombrus, in the Middle Atlantic Bight 103

WEIHS, DANIEL. Respiration and depth control as possible reasons for swimming
of northern anchovy, Engraulis mordax, yolk-sac larvae 109

POWLES, HOWARD. Descriptions of larval silver perch, Bairdiella chrysoura,
banded drum, Larimus fasciatus, and star drum, Stellifer lanceolatus (Sciaenidae) 119

GRIMES, CHURCHILL B., and GENE R. HUNTSMAN. Reproductive biology of
vermilion snapper, Rhomboplites aurorubens, from North Carolina and South
Carolina 137

PETERSON, R. H., P. H. JOHANSEN, and J. L. METCALFE. Observations on ear-
ly life stages of Atlantic tomcod, Microgadus tomcod 147

Notes

HINES, ANSON H., and THOMAS R. LOUGHLIN. Observations of sea otters dig-
ging for clams at Monterey Harbor, California 159

WEIS, PEDDRICK, and JUDITH SHULMAN WEIS. Effect of zinc on fin regener-
ation in the m\iTam\c\\og, Fundulus heteroclitus , and its interaction with methyl-
mercury 163

(Continued on next page)

Seattle, Washington
1980

For sale by the Superintendent of Documents. U.S. Government Printing Office. Washington,
DC 20402 — Subscription price per year $12 00 domestic and $15 00 foreign Cost per single
issue $3 00 domestic and $3 75 foreign

Contents-continued

TESTAVERDE, SALVATORE A., and JAMES G. MEAD. Southern distribution of
the Atlantic whitesided dolphin, Lagenorhynchus acutus, in the western North
Atlantic 167

MATARESE, ANN C, and DAVID L. STEIN. Additional records of the sculpin
Psychrolutes phrictus in the eastern Bering Sea and off Oregon 169

ODELL, DANIEL K., EDWARD D. ASPER, JOE BAUCOM, and LANNY H. COR-
NELL. A recurrent mass stranding of the false killer whale, Pseudorca crassi-
dens, in Florida 171

BRANSTETTER, STEVEN, and ROBERT L. SHIPP. Occurrence of the finetooth
shark, Carcharhinus isodon, off Dauphin Island, Alabama 177

BAGLIN, RAYMOND E., JR., MARK I. FARBER, WILLIAM H. LENARZ, and JOHN
M. MASON, JR. Shedding rates of plastic and metal dart tags from Atlantic blue-
fin tuna, Thunnus thynnus 179

HAYNES, JAMES M., and ROBERT H. GRAY. Influence of Little Goose Dam on
upstream movements of adult chinook salmon, Oncorhynchus tshawytscha 185

MORSE, WALLACE W. Maturity, spawning, and fecundity of Atlantic croaker,
Micropogonias undulatus , occurring north of Cape Hatteras, North Carolina 190

MILLER, ROBERT E., DOUGLAS W. CAMPBELL, and PAMELA J. LUNSFORD.
Comparison of sampling devices for the juvenile blue crab, Callinectes sapidus . . . 196

Notices
NOAA Technical Reports NMFS published during the last 6 mo of 1979 199

Vol. 77, No. 4 was published on 23 July 1980.

The National Marine Fisheries Service (NMFS) does not approve, rec-
ommend or endorse 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 pro-
motion which would indicate or imply that NMFS approves, recommends
or endorses any proprietary product or proprietary material mentioned
herein, or which has as its purpose an intent to cause directly or indirectly
the advertised product to be used or purchased because of this NMFS
publication.

LIFE HISTORY PATTERNS IN MARINE FISHES AND
THEIR CONSEQUENCES FOR FISHERIES MANAGEMENT

Peter B. Adams*

ABSTRACT

Natural selection operates at the life history level to maximize the number of surviving offspring. Life
history characteristics will vary in consistent patterns to meet this constraint. When theoretical
patterns in life histories were investigated in terms of r and K selection and compared with actual
trends in life history characteristics of fishes, the agreement between observed and predicted trends
was significant. The effects of harvesting on stocks with these life history trends were investigated
and it was found that K selected type species would be highly sensitive to overfishing and, once
depleted, recovery would require a long time.

The ecological and genetic properties of a species
are intimately linked. The morphological and re-
productive characteristics, population sizes, and
genetic frequencies of species are adjusted to their
environments by natural selection. Species in-
habiting different environments show different
patterns of life history characteristics. The rela-
tionship among habitat, ecological strategies, and
population parameters has been termed r and K
selection (Mac Arthur and Wilson 1967) and/or op-
timal life histories ( Gadgil and Bossert 1970). This
body of theory is based on the assumption that
natural selection operates on these characteristics
in order to maximize the number of surviving
offspring produced. Under an environmental re-
gime with a large component of unpredictable,
nonselective, mortality an organism will allocate
a larger portion of its resources to reproductive
activities (an r strategist). Conversely the optimal
allocation of resources for a population subjected
to a high proportion of predictable, selective mor-
tality will be toward increasing individual fitness,
frequently through competitive ability (a K
strategist). With the number and variability of
factors operating on any particular species, no
species is going to be an r or X strategist in an
absolute sense. A species will only occupy a rela-
tive position on the r and K continuum.

In fisheries biology, the value of comparative
studies of life history parameters has long been
recognized (Holt 1962; Beverton 1963; Gushing
1971; Alverson and Carney 1975). These life his-

' Southwest Fisheries Center Tiburon Laboratory, National
Marine Fisheries Service, NOAA, Tiburon, CA 94920.

tory parameters should vary in a consistent pat-
tern which can be predicted from the theory of r
and K selection. In this paper, these predictions
are tested with life history parameters from major
groups of marine fishes. The theory has implica-
tions for management, particularly when fisheries
are in the initial stages of development.

THEORY OF r AND K SELECTION

The theory of r andX selection is based on two
assumptions about the allocation of a population's
resources between competitive and reproductive
functions (Pianka 1974; Gadgil and Bossert 1970;
Schaffer and Gadgil 1975). The first is that there is
a positive relationship between the amount of re-
sources spent on an offspring and the fitness of
that offspring. The second assumption is that any
species only has a fixed amount of resources avail-
able. This results in an inverse relationship be-
tween the number of offspring produced and their
average fitness. The criterion for success in
natural selection is the number of surviving
offspring that a parent produces (Crow and
Kimura 1970). Therefore, the best reproductive
strategy is a compromise between two conflictmg
demands: production of the largest possible total
number of offspring {r selection), and production of
offspring with the highest possible fitness ^ selec-
tion). The particular point of compromise for any
species will be a function of the selection factors
operating on that species and would be that
species' position on the r and K continuum.

The second part of the theory concerns the rela-
tionship between these life history strategies and

1^

Manuscript accepted September 1979.
FISHERY BULLETIN; VOL. 78, NO. 1. 1980.

FISHERY BULLETIN: VOL. 78, NO. 1

the habitat the species occupies (Southwood et al.
1974; Southwood and Comins 1976). If mortality
factors in an environment are variable and/or un-
predictable, then their effects are likely to be less
selective in terms of population size or of the
phenotype involved. Under these circumstances,
individual competitive fitness is of relatively less
importance. The best strategy would be to place
maximal resources into reproduction and produce
as many offspring as possible (r selection).

The contrasting situation is an environment in
which mortality factors are stable and/or predict-
able. Mortality under these circumstances will re-
sult in strong selection for individual fitness and
there will be pronounced differences between their
effects on different phenotypes. In these stable
environments, the optimal strategy would be to
produce offspring with substantial competitive
ability {K selection). Due to the previously as-
sumed relationship between fitness per offspring
and the number of offspring produced, this also
means the production of fewer offspring.

The two situations described above are end
points of a spectrum. Species will always have a
number of different selective pressures operating
on them, both spatially and temporally. This is
particularly evident in aquatic organisms which
characteristically go through several life history
stages. This again emphasizes that the concept of
r and K selection should be applied only in a
comparative sense. Finally, comparisons must be
made between species of a similar ecological na-
ture. Comparisons between species of different
ecological types is meaningless since fundamen-
tally different types of selective factors will be
operating in those cases.

r AND K SELECTION IN
MARINE FISHES

Natural selection will favor nonreproductive ac-
tivities at the expense of reproductive activities
only when they enhance reproduction at later
stages in the life history and thereby maximize
overall survival (Crow and Kimura 1970).
Changes in allocation of a species' resources from
reproductive to competitive activities will only
occur in habitats where competitive activities en-
hance the survival of future offspring. The result
of this is that organisms under different selection
pressures will have characteristic life history pat-
terns. An r selected species will have life history
strategies which tend toward productivity. Thei^

selected species will have life strategies which
tend toward efficient exploitation of a specific
limiting resource (Pianka 1974). Therefore,
specific combinations of population parameters
can be identified as being characteristic of an r
strategist, while the opposing combination would
be characteristic of aK strategist.

A species which is exposed to a large component
of nonselective or catastrophic mortality (i.e., an r
strategist) would be selected for characteristics
that would increase productivity. Increasing pro-
ductivity through reproductive activity generally
implies: 1) early maturity, 2) rapid growth rates,
3) production of larger numbers of offspring at a
given parental size, and 4) maximum production
of offspring at early age (Gadgil and Bossert 1970).
Other characteristics which are results of the allo-
cation of large portions of resources to reproduc-
tive activity are: 1) small body size, 2) high rates of
mortality, and 3) shorter life span (Pianka 1974;
Gadgil and Solbrig 1972). In terms of commonly
measured population parameters in fishery biol-
ogy, an r selected species would have: 1) a low age
at first maturity, 2) a high value ofk from the von
Bertalanffy growth equation, 3) a small Lx from
the von Bertalanffy growth equation, 4) high rates
of instantaneous natural mortality (M), and 5) low
maximum age.

Even in environments with predictable mortal-
ity sources, increased allocation of resources to
competitive activities will only occur when two
prerequisites are met (Schaffer and Gadgil 1975).
The first is that reproductive potential increases
with some function of age. The second is that there
is some additional mortality risk associated with
reproduction. Under these assumptions, the attri-
butes associated with aK strategist would be: 1)
delayed maturity, 2) reduced growth rates, 3) low
mortality rates, 4) large body size, and 5) longer
life span. Again in terms measured in fishery biol-
ogy, aK selected species would have: 1) a high age
at first maturity, 2) a low k from the von Ber-
talanffy growth equation, 3) a large L-x from the
von Bertalanffy growth equation, 4) lowM, and 5)
a high maximum age.

Using these life history correlates of r and K
selection (summarized in Table 1), it is possible to
predict the signs of a correlation matrix between
life history parameters (Table 2). The predicted
matrix can be compared with actual matrices cal-
culated using Spearman's rank correlation
coefficient. This coefficient only assumes that the
observed data are mutually independent and come

ADAMS: LIFE HISTORY PATTERNS IN MARINE FISHES

Table l .—Summary of hypothetical r and K correlates in life
history parameters of fishes.

Characteristics

r selected

K selected

Body size. L x'
Maximum age
Age at first maturity
Natural mortality, M
Growtti rate./t'

Small
Low
Low
High
High

Large

High

High

Low

Low

'The parameter from the von Bertalanffy growth equation was used to
represent the actual characteristic.

Table 2. — Predicted signs of correlation matrix of life history
parameters in fishes.

Characteristics

Maximum
L rJ age

Age at

first
maturity

M

Body size, L J
Maximum age
Age at first maturity
Natural mortality, M
Growth rate, h'

1.0

1.0

+
+
1.0

1.0

+
1.0

'The parameter from the von Bertalanffy growth equation was used to
represent the actual characteristic.

from a continuous bivariate population (Hollan-
der and Wolfe 1973).

RESULTS

Life history parameters were gathered from the
literature for several major groups of marine
fishes. Often there were multiple sets of data for
the same species from different locations. Each set
of values was used as a separate data case. The
literature citations for the actual parameters are
listed by group in Appendix I. Correlation ma-
trices were calculated for the following groups of
fish: 1) herring and anchovies, Clupeidae and En-
graulidae (Table 3), 2) salmons, Salmonidae (Ta-
ble 4), 3) cods, Gadidae (Table 5), 4) rockfishes,

Table 3. — Correlation coefficients between life-history
parameters for herring and anchovies (families Clupeidae and
Engraulidae). For sources of data see Appendix I. The number in
parentheses represents the significance value for that particular
coefficient since the number of data cases was different for each
correlation.

Age at

Table 4. — Correlation matrix between life-history parameters
for salmons (family Salmonidae). For sources of data see Appen-
dix I. The number in parentheses represents the significance
value for that particular coefficient since the number of data
cases was different for each correlation.

Characteristics

L-x'

Maximum
age

Age at

first
maturity

M

Body size.Lx'
Maximum age
Age at first maturity
Natural mortality, M
Growth rate,/('

10

0.765

0728

-0785

-0.730

(0,001)

(0032)

(0 001)

(0002)

10

0 776

-0 737

-0.674

(0.020)

(0003)

(0.004)

10

-0644

-0812

(0.084)

(0013)

1.0

0 896

(0 001)
1.0

'The parameter from the von Bertalanffy growth equation was used to
represent the actual characteristic.

Table 5. — Correlation matrix between life-history parameters
for cods ( family Gadidae) . For sources of data see Appendix I. The
number in parentheses represents the significance value for that
particular coefficient since the number of data cases was differ-
ent for each correlation.

Characteristics

L-x'

Maximum
age

Age at

first
maturity

M

k-'

Body size, L-x'

1.0

0.795

0.833

-0.647

-0.666

Maximum age

(0.002)
1.0

(0.001)
0.737

(0.022)
-0.654

(0.001)
-0.702

Age at first maturity
Natural mortality, M
Growth rate, k'

(0.014)
1.0

(0.028)
-0.715
(0.035)
1.0

(0.008)
-0.658
(0.008)
0.950
(0.001)
1.0

'The parameter from the von Bertalanffy growth equation was used to
represent the actual characteristic.

Scorpaenidae, genus Sebastodes (Table 6), and 5)
flatfishes, Pleuronectiformes (Table 7).

All of the observed correlations agree with the
predicted correlations in sign (Table 8). Of the
observed correlations, 40 of a possible 46 (or 87%)
were significantly different from zero at a 5%
probability level. If the observed correlation
agreement of coefficients were distributed ran-

TABLE 6. — Correlation matrix between life-history parameters
for rockfishes (family Scorpaenidae, genus Sebastodes). For
sources of data see Appendix I. The number in parentheses
represents the significance value for that particular coefficient
since the number of data cases was different for each correlation.

Characteristics

Ly-:

age

maturity

M

/c'

Characteristics

Lx'

Maximum
age

Age at

first
maturity

Body size, Lx'

ity
M

1.0

0.846
(0.001)
1.0

0.816
(0.001)

0.904
(0.001)

1.0

-0.746
(0.001)

-0.797
(0.001)

-0.702
(0.001)
1.0

-0.720

(0.001)

-0.763

(0.001)

-0.732

(0.001)

0.876

(0.001)

1.0

/('

Maximum age
Age at first matur
Natural mortality.
Growth rate./c'

Body size, L-x'
Maximum age
Age at first maturity
Growth rate, fc'

1.0

0.662
(0.019)
1.0

0.456
(0.088)

0.612
(0.030)

1.0

-0.490
(0.075)

-0.567
(0.040)

-0.651
(0.021)
1.0

'The parameter from the von Bertalanffy growth equation was used to
represent the actual characteristic.

'The parameter from the von Bertalanffy growth equation was used to
represent the actual characteristic.

FISHERY BULLETIN. VOL. 78, NO. 1

Table 7. — Correlation matrix between the life-history
parameters for flatfishes (order Pleuronectiformes). For sources
of data see Appendix I. The number in parentheses represents
the significance value for that particular coefficient since the
number of data cases was different for each correlation.

Characteristics

i-x'

Maximum
age

Age at

first
maturity

M

k'

Body size, Lx'

1.0

0.755

0.956

-0.291

-0.619

Maximum age

(0.001)
1.0

(0.001)
0.824

(0.156)
-0.355

(0.005)
-0.808

Age at first maturity

(0.001)
1.0

(0.142)
-0.630

(0.001)
-0.732

Natural mortality.

M

(0.014)
1.0

(0.001)
0.367

Growttirate,/('

(0.098)
1.0

'Thie parameter from the von Bertalanffy growth equation was used to
represent the actual characteristic.

Table 8. — Summary of the number of agreements between pre-
dicted and observed correlation coefficients among life-history
parameters within selected taxonomic groups.

Level of agreement

Number in
agreement

Number
possible

Percent in
agreement

Sign

5% probability level

1% probability level

46
40

31

46
46
46

100
87
67

domly (i.e., p = probability of agreement = 0.5,
and q = probability of disagreement = 0.5), then
the number of agreements would follow a binomial
distribution. The binomial test (Hollander and
Wolfe 1973 ) can be used to test the hypothesis that
the number of agreements between the predicted
and observed correlations differs from the number
that would have occurred randomly. The number
of agreements is significantly different than would
have occurred randomly iz = 4.86, P<0.001),
when only correlations that were significant at the
5% level were used.

maximum age of a fish. From r andK selection, we
can predict how these parameters will vary. Con-
sider a situation with three hypothetical species:
one species will be more r selected, another species
will be moreK selected, and another will be inter-
mediate between the first two. The biological
parameters will vary as shown in Table 9. Bever-
ton and Holt yield per recruit curves were calcu-
lated for a constant age at first capture {t^ = 4.2 yr)
with varying fishing mortality (Figure 1), and for
a constant fishing mortality (F = 0.25) with a
varying age at first capture (Figure 2).

The yield per recruit analysis points up that
there are specific differences in fisheries based on r
or K selected species. In fisheries based on K
selected species, the maximum yield per recruit
would occur at a lower level of fishing mortality
and at a later age at first entry than in fisheries
based on r selected species. The curves also indi-
cate that K selected species would be much more
sensitive to overfishing both in terms of fishing
mortality and age at first entry.

The surplus production model of Schaefer com-
bines reproductive and mortality functions into
one parameter (Ricker 1975). The biological
parameters in this model are 5x, the maximum
stock size (or carrying capacity in weight), and /e,
the instantaneous rate of increase of the stock at
densities approaching zero. Again these parame-
ters can be predicted for the three hypothetical
species from r and if selection (Table 10). In the
surplus production model analysis (Figure 3), ther
selected species have the highest productivity. As
in the yield per recruit analysis, the maximum
yield occurs at a lower fishing mortality for the A"

RESPONSE OF r AND K SELECTED
SPECIES TO HARVESTING

The interaction of life history characteristics
will have a strong affect on the response of a
species to fishing pressure. The Beverton and Holt
yield per recruit equation estimates the yield that
can be harvested from the growi:h of a cohort. The
model assumes that fish grovvi:h is described by the
von Bertalanffy growth curve and that mortality
processes are exponential (Beverton and Holt
1957; Ricker 1975). The biological parameters in
the model are: 1) M, the instantaneous rate of
natural mortality, 2) Wy-, the mean asymptotic
weight which corresponds to Ly-_, 3) k, the von
Bertalanffy growth coefficient, and 4) t^, the

Table 9. — Biological parameters for use in yield per recruit
analysis for three hypothetical r andK selected species.

r selected

Intermediate

K selected

Biological parameters

species

species

species

Natural mortality, M

0.30

0.20

0.10

Mean asymptotic weight,

w-..

641 g

1,141 g

1,641 g

von Bertalanffy growth

coefficient, fc

0.22

0.14

007

Maximum age, (^

13yr

20 yr

35 yr

Table lO. — Biological parameters for surplus production model
analysis for three hypothetical r and K selected species.

Biological
parameters

r selected
species

Intermediate
species

K selected
species

Maximum stock

size (8 -^J
Rate of

I.54xi08g

2.04- 10«g

2.54y-[Cfig

increase [k)

0.912

0.612

0.312

ADAMS: LIFE HISTORY PATTERNS IN MARINE FISHES

100 .0

FIGURE 1.— The effect of different
levels of fishing mortality with constant
age of recruitment (4.2 yr) on yield per
recruit of three hypothetical fish species
demonstrating the range of r and K
selection.

FIGURE 2.— The effect of different mean
ages of recruitment at constant fishing
mortality (F = 0.25) on yield per recruit
of three hypothetical fish species dem-
onstrating the range of r and K selec-
tion.

<D

3
Ll)

a:

(X
LU
CL

>

° SPECIES a

■

' SPECIES B

90.0

« SPECIES C

BO .0

■

70.0

60 .0

50.0
40.0
30.0

•

1

20.0

"^"^■^^"^

—

10.0

'

0.0,

>-^- — , — ^^ — , — , — , . ._

0.00 .25 .50 .75 1.00 1.25 1.50 1.75 2.00 2.25 2.50

FISHING HDRTPLITY (Fl

200 .0

175 .0

— 150.0
125.0

° SPECIES 0
' SPECIES B
o SPECIES C

4.0 B.O 12.0 16.0 20.0 24.0 2B.0 32.0 36.0

OGE AT FIRST RECRUITMENT

selected species than for the r selected species. The
K selected species is reduced to levels lower than

the maximum sustainable yield by overfishing
much more rapidly than the r selected species.

FISHERY BULLETIN: VOL. 78. NO. 1

Figure 3. — Maximum equilibrium
yields (x 10* g) from Schaefer surplus
production curves as a function of
fishing mortality for three hypothetical
fish species demonstrating the range of
r and K selection.

40 .00

36.10

32 .20 .

2G .30

U3

X; 24.40

X

o

■^ 20.50

16 .60

>

12 .70

B.BO

4 .90

1 .00

° SPECIES «
' SPECIES B
° SPECIES C

0.00 .10 .20 .30 .40 .50 .60 .70 .BO .90 1.00

FISHING MDRTPLITY (F)

DISCUSSION

Life history parameters vary in consistent pat-
terns. These patterns are explainable and predict-
able by the theoretical constructs of r and K selec-
tion. This is not a particularly new or unique idea
in fisheries biology. Beverton and Holt (1959) in-
vestigated a positive relationship between body
size and life span and between mortality and
growth rates. Gushing (1971) suggested that there
is a negative relationship between degree of den-
sity dependent regulation and fecundity. Alverson
and Carney ( 1975) have suggested a positive rela-
tionship between body size and the time when a
cohort maximizes its biomass. In population ecol-
ogy, similar relationships have been investigated
for zooplankton (Allan 1976), plants (Gadgil and
Solbrig 1972; MacNaughton 1975), and animals
(Smith 1954; Bonner 1965). All these empirical
observed trends in life history parameters, along
with the trends described here, are consistent with
r and K selection.

It is important to reemphasize here the com-
parative nature of r andi^ selection. The r and K
continuum is a model and as such occurs only in an
idealized sense. The idealized r selected species
occurs in an ecological vacuum with no density

effects and no competition. The idealized K
selected species occurs in a completely saturated
ecosystem where densities are high compared
with carrying capacities and competition for re-
sources is intense. The problem of applying this
model to any real situation is not a trivial one.
Species are not simply subjected to a single selec-
tive pressure, or even to a single set of selective
pressures. Because of this, r and /C concepts should
only be applied in a comparative sense between
groups of species that have some degree of func-
tional similarity. No species is r selected or K
selected in an absolute sense; it is only relatively
more r selected or K selected than some other
reference species. This theory will only have value
in a situation where the population dynamics of
one member of a species group are fairly well un-
derstood.

The results of the model analysis give several
indications about the reaction to harvesting pres-
sure of species which are more or less r or K
selected. Fisheries based on more r selected
species will be more productive. They can be fished
at younger ages and at higher levels of fishing
mortality. Given a minimum population size,
these fisheries should also have a quicker recovery
from overfishing. Species which are more r

ADAMS: LIFE HISTORY PATTERNS IN MARINE FISHES

selected are likely to be strongly influenced by
physical forces in the environment (Pianka 1974).
Relationships of this type, e.g., between anchovies
and upwelling, should be important considera-
tions in management plans for these species.

Fisheries based on more K selected species will
have a high maximum yield per recruit, but there
will be fewer fish. Maximum equilibrium yield
will occur at later ages of entry into the fishery and
at lower levels of fishing mortality. These fisheries
would be more susceptible to overfishing and stock
depletion. Besides these species' sensitivity to
overfishing, more K selected species are much
more likely to have sophisticated life history
mechanisms (Pianka 1974) which would have to
be recognized in a management plan. These
mechanisms might include parental care systems
such as nesting or live births, mating systems, or
territoriality. The more K selected species are
much more likely to have strong interspecific rela-
tionships, usually competitive ones. The relation-
ship between competition and harvesting has been
dealt with by Larkin (1963) and Tanner (1975).
Additional density independent mortality (fishing
mortality) increases the advantage for the popula-
tion with a higher population growth rate (i.e.,
more r selected). Therefore, even low levels of
fishing pressure can destabilize a previously sta-
ble competitive pair and result in decline of the
harvested species. Interestingly, the opposite re-
sult is also possible; harvesting pressure can
stabilize a previously unstable species pair as
Slobodkin ( 1962) found with experimental popula-
tions of hydra.

Fisheries based on more r selected species are
likely to be of a boom and bust nature. Although in
some years catches in these fisheries will be very
large, they will be characterized by erratic produc-
tion levels. The most efficient form of harvesting
these fisheries will be fleets which are capable of
switching between a number of target species rel-
atively quickly.

Fisheries based on more K selected species, in
contrast to the boom and bust nature of r selected
fisheries, will be characterized by relatively stable
population sizes and therefore catch levels. Given
some initial measure of year class strength, possi-
bly through larval or prerecruitment surveys, the
prediction of future catches from that fishery could
be made with a fair degree of accuracy. However,
once fisheries based on these species become over-
fished, it would require a long period for the stock
to rebuild to levels which can support economical

profitable fisheries. An extremely K selected
species would only be suitable for trophy fisheries.

Fisheries based on r and K selected species have
been discussed in a comparative sense, but preda-
tion (in the case of a fishery , human predation) will
also have effects on an individual species. The
gene pool of any species is going to contain within
it some range of variation of both r and/C selected
traits. The effects of increasing fishing mortality,
which is assumed to be density independent
(Gushing 1975), on life history characteristics has
been theoretically analyzed by Roughgarden
(1971). The general effect is an increase in selec-
tive advantage for the r selected proportions of the
gene pool. This would mean an increase in growth
rates, reduced age at first maturity, and greater
fecundity at age. These trends will be more con-
spicuous in species that are relatively more K
selected. Species that are more strongly r selected
are likely to have less range of variation in this
direction. One example of these effects of preda-
tion pressure is a comparison of lake trout, Sal-
velinus namaycush , populations under heavy pre-
dation pressure from the freshwater harbor seal,
Phoca uitulina, to populations in nearby lakes
without seals (Power and Gregoire 1978). The lake
trout populations which were preyed upon by seals
had faster growth rates, small maximum body
size, reduced maximum age, lower age at sexual
maturity, and greater individual fecundity com-
pared with populations in lakes without seals.
Growth and maturation rates of certain seal
species have also increased where populations
have been reduced by fisheries (Sergeant 1973).
These affects can be attributed to changes in selec-
tion pressure resulting from sustained harvesting.

In summary, r and K selection seems to have
been an important evolutionary trend on marine
fish populations. The basic hypotheses are con-
firmed by the data presented here. The result of
patterns in population parameters which arise
from r and K selection is that different manage-
ment strategies would be appropriate. The value
of this approach is likely to be in initial stages of
development of a fishery. As a fishery becomes
more developed and more specific information be-
comes available, a more refined management
strategy would become possible.

ACKNOWLEDGMENTS

This paper benefited from readings by M. E.
Adams, E. O. Garton, E. S. Hobson, W. H. Lenarz,

FISHERY BULLETIN: VOL. 78, NO. 1

and H. Li. Naturally any errors in the paper are
the sole responsibility of the author.

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1943. Studies on the Pacific pilchard or sardine {Sardinops
caerulea). 5. — A method of computing mortalities and re-

ADAMS: LIFE HISTORY PATTERNS IN MARINE FISHES

placements. U.S. Fish Wildl. Serv., Spec. Sci. Rep. 24,
10 p.
Slobodkin, L. B.

1962. Growth and regulation of animal populations. Holt,
Rinehart and Winston, N.Y., 184 p.
SMITH, F. E.

1954. Quantitative aspects of population growth. InE.J.
Boell (editor). Dynamics of growth process, p. 277-294.
Princeton Univ. Press, Princeton, N.J.

Smith, W.C.

1957. Gonad condition, age and size of Manx herrings,
1945-53, and comparison with earlier years. Annu. Rep.
Mar. Biol. Stn. Pt. Erin. 69:21-28.
SOUTHWOOD, T. R. E., AND H. N. COMINS.

1976. A synoptic population model. J. Anim. Ecol.
45:949-965.

SOUTHWOOD, T. R. E., R. M. May, M. P. Hassell, and G. R.
Conway.

1974. Ecological strategies and population parameters.
Am. Nat. 108:791-804.

SUND, O.

1943a. The age-composition of the Norwegian spawn her-
ring observed during 36 years. Ann. Biol. 1:45-49.
1943b. The size of the Norwegian spawn herring. Ann.
Biol. 1:50-51.
TANAKA, S.

1960. Studies on the djTiamics and the management offish
populations. [In Jpn., Engl, summ.] Bull. Tokai Reg.
Fish. Res. Lab. 28:1-200.
Tanner, J. T.

1975. The stability and the intrinsic growth rates of prey
and predator populations. Ecology 56:855-867.

Taylor, C. C.

1958. Cod growth and temperature. J. Cons. 23:366-370.

Tester, a. L.

1955. Estimation of recruitment and natural mortality
rate from age-composition and catch data in British Co-
lumbia herring populations. J. Fish. Res. Board Can.
12:649-681.

TIBBO, S. N.

1956. Populations of herring (Clupea harengus L.) in New-
foundland waters. J. Fish. Res. Board Can. 13:449-466.

1957a. Herring of the Chaleur Bay area, /n A. H. Leim,
S. N. Tibbo, L. R. Day, L. Lauzier, R. W. Trites, H. B.
Hachey, and W. B. Bailey, Report of the Atlantic herring
investigation committee, p. 85-102. Fish. Res. Board Can.,
Bull. 111.

1957b. Herring populations on the south and west coasts of
Newfoundland. In A. H. Leim, S. N. Tibbo, L. R. Day, L.
Lauzier, R. W. Trites, H. B. Hachey, and W. B. Bailey,
Report of the Atlantic herring investigation committee, p.
153-164. Fish. Res. Board Can., Bull. 111.
TOKAI Regional Fisheries Research Laboratory.

I960. Synopsis on the biology oi Sardinops melanosticta
(Temminck and Schlegel). In H. Rosa, Jr. and G. Mur-
phy (editors), Proc. World Sci. Meet. Biol. Sardines Relat.
Species 2:213-244. FAO, Rome.

Van Cleve, R., and D. E. Bevan.

1973. Evaluation of causes for the decline of the Karluk
sockeye salmon runs and recommendations for rehabilita-
tion. Fish. Bull., U.S. 71:627-649.
Wat AN ABE, K.

1958. Growth of the anchovy in the Japan Sea. Annu.
Rep. Jpn. Sea Fish. Res. Lab. 4:147-152.

APPENDIX I:

LITERATURE CITATIONS FOR POPULATION
PARAMETERS BY SPECIES

Herring and Anchovies,
Families Clupeidae and Engraulidae

Clupea harengus — Lea 1919; Sund 1943a, b; Jen-
sen 1947; Fridriksson 1950, 1951-61; Alander
1950; Tibbo 1956, 1957a, b; Hannerz 1956; Gilis
1957-61; Smith 1957; Day 1957; Gushing 1959;
Nielsen 1960; Burd 1962; Parrish and Craig
1963; Postuma 1963; Bowers 1963.

C. pallasii — Hanamura 1953; Tester 1955; Kicker
1958; Tanaka 1960; Ayushin 1963; Motoda and
Hirano 1963.

Sprattus sprattus — Robertson 1938; Molander
1943; Faure 1950; Elwertowski 1957-60.

Sardinops caerulea — Silliman 1943; Phillips
1948; Mosher and Eckles 1954; Clark and Marr
1955; Murphy 1966; Culley 1971.

S. melanosticta — Tanaka 1960; Tokai Regional
Fisheries Research Laboratory 1960.

S. neopilchardus — Blackburn 1950.

S. ocellata — Davies 1958; De Jager 1960; Culley

1971.
Sardina pilchardus — Hodgson and Richardson

1949; Bough 1952; Hodgson 1957; Larraneta

1960; Cushing 1961; Culley 1971.
Sardinella aurita — Postel 1955; Rossignol 1955;

Richardson et al. 1960; Ben-Tuvia 1960; Bever-

ton 1963.
S. longiceps — Nair 1960.
Engraulis encrasicholus — Fage 1920; Fumestin

1945.
E. japonicus — Hayashi and Kondo 1957;

Watanabe 1958; Tanaka 1960; Hayashi 1961.
E. mordax mordax — Clark and Phillips 1952; Mil-
ler et al. 1955; Miller and Wolf 1958; Culley

1971.
Cetengraulis mysticetus — Barrett and Howard

1961.

11

Salmons, Family Salmonidae

Coregonus clupeaformis — Hart 1931; Hile and
Deason 1934; Kennedy 1943, 1953; Ricker 1949.

Cristivomer namaycush — Kennedy 1954.

Leucichthys artedii — Hile 1936.

L. kiyi — Deason and Hile 1947.

Oncorhynchus kisutch — Shapovalov and Taft
1954; Drucker 1972.

O. nerka — Foerster 1968; Van Cleve and Bevan
1973.

Cods, Family Gadidae

Boreogadus saida — Beverton and Holt 1959.

Gadus callarias — Beverton and Holt 1957; Taylor
1958.

G. macrocephalus — Ketchen 1964.

G. minutus — Menon 1950.

G. morAaa— Fleming 1960; Pinhorn 1969;
Clayden 1972.

G. virens — Beverton and Holt 1959.

Melanogrammus aeglefinus — Raitt 1939; Bever-
ton and Holt 1957.

Merluccius merluccius — Beverton and Holt 1959.

FISHERY BULLETIN: VOL. 78, NO. 1

Rockfishes, Family Scorpaenidae,
Genus Sebastodes

Sebastodes crameri — Phillips 1964.

S. diploproa — Phillips 1964.

S. entomelas — Phillips 1964.

S. /Zaf^fdus— Phillips 1964.

S. ^oodei— Phillips 1964.

S.jordani — Phillips 1964.

S. miniatus — Phillips 1964.

S. paucispinis — Phillips 1964.

S. pinniger — Phillips 1964.

S. saxicola — Phillips 1964.

Flatfishes, Order Pleuronectiformes

Citharichthys sordidus — Arora 1951.
Eopsetta jordani — Ketchen and Forrester 1966.
Hippoglossus platessoides — Powles 1965, 1969;

MacKinnon 1973.
H. vulgaris — Beverton and Holt 1959.
Isopsetta isolepis — Hart 1948.
Pleuronectes platessa — Beverton and Holt 1959.
Pseudopleuronectes americanus — Dickie and

McCracken 1955.
Solea vulgaris — Beverton and Holt 1957.

12

SPECIES OF MUNIDOPSIS (CRUSTACEA, GALATHEIDAE)
OCCURRING OFF OREGON AND IN ADJACENT WATERS

Julie W. Ambler'

ABSTRACT

Twelve species of Munidopsis (Decapoda: Crustacea: Galatheidae) were collected from the continental
slope, Cascadia Basin, and Tufts Abyssal Plain off Oregon and in adjacent waters. Three new species
are described: Munidopsis cascadia, M. tuftsi, and M. yaquinensis . One specimen, Munidopsis sp.,
closely related to M. bairdii, is described but unnamed, pending capture of more specimens. Munidop-
sis chacei is synonymized with M. bairdii and M. geyeri is synonymized with M. subsquamosa . The
ranges of seven previously described species are now extended to Oregon and Washington: M. aries, M.
bairdii, M. beringana, M. ciliata, M. latirostris, M. subsquamosa, and M. verrucosus. The 12 species
occurred between 950 and 4,194 m; 3 species were found on the continental slope (950-2,189 m); 9
species were found on Cascadia Basin (1,900-3,025 m); and 3 species were found on Tvifts Plain
(3,390-4,194 m). Species composition on Cascadia Basin differed from east to west. The highest
densities (number of specimens per trawl) occurred at the base of the continental slope and 40 miles
farther west. One species, M. latirostris, contributed 73.0% of the total number of specimens, and three
other species (M. bairdii, M. ciliata , and M. subsquamosa ) contributed an additional 20 .2% . The species
collected also occur in the Atlantic (M. bairdii, M. aries), tropical Pacific and Indian (M. ciliata),
tropical Pacific (A/, latirostris), Arctic (M. beringana), southern temperate Pacific (M. verrucosus), or
are cosmopolitan (Af. subsquamosa), or are endemic on Cascadia Basin (M. cascadia, M. yaquinensis),
and on Tufts Plain (M. tuftsi).

Species of Munidopsis are found from intertidal
waters to the abyssal plains of the deep sea.
Munidopsis polymorpha is found in saltwater
lakes in caverns connected to the sea in the Ca-
nary Islands (Dinkins 1969). Munidopsis crassa,
the deepest known species, was found at 4,700 m in
the Bay of Biscay (Sivertson and Holthuis 1956).
Recently, an unidentified Munidopsis sp. has been
found near submarine hot springs near the
Galapagos (Corliss and Ballard 1977). In general,
the genus is found in the deep sea with about half
of the known species occurring deeper than 800 m
(Doflein and Balss 1913).

In the eastern Pacific Ocean, the first Munidop-
sis species were collected off Chile by the Chal-
lenger (Henderson 1888) and in the eastern tropi-
cal Pacificby the A /6a^ross (Faxon 1895). Benedict
(1902) described additional new species collected
by the Albatross off southern California and the
Galapagos, and in the Bering Sea. Since then,
Bahamonde (1964) and Khodkina (1973) have
found new species off Chile, and Pequegnat and
Pequegnat ( 1973) described a new species off Baja
California and Costa Rica from the Albatross and

'School of Oceanography, Oregon State University, Corvallis,
Oreg.; present address: Department of Oceanography, Texas
A&M University, College Station, TX 77843.

Manuscript accepted August 1979.
FISHERY BULLETIN; VOL. 78, NO. 1, 1980.

Galathea collections. Little work has been done on
Munidopsis occurring off the west coast of the
United States. Schmitt ( 1921), in a key to Muni-
dopsis species found off California, included M.
verrilli, M. hystrix, M. aspera, and M. quadrata.
Haig (1956) modified this key to include M. de-
pressa.

This paper discusses the taxonomy and distribu-
tion of 12 Munidopsis species collected mainly off
Oregon from 950 to 4,194 m. These depths include
the lower slope and the abyssal plains of Cascadia
Basin and Tufts Plain (Figure 1). Among species
found off Oregon, only M. quadrata has previously
been collected from the west coast of the United
States. Three new species are described: M. cas-
cadia, M. tuftsi, and M. yaquinensis. One species,
Munidopsis sp., is described but left unnamed
until more specimens become available to eluci-
date its relationship to M. bairdii. The ranges of
seven previously described species are extended to
Oregon: M. bairdii, M. beringana, M. ciliata, M.
aries, M. verrucosus, M. latirostris, and M. sub-
squamosa.

METHODS

A total of 803 specimens were collected from 146

13 ^3

FISHERY BULLETIN: VOL. 78, NO. 1

TUFTS
PLAIN

TP-C TP-9 TP-A

Figure l. — Stations sampled in Cascadia Basin and Tufts Plain,
off Oregon and Washington.

benthic otter trawls (0TB, OT) and beam trawls
(BMT) during 13 yr of sampling by Andrew G.
Carey, Jr., School of Oceanography, Oregon State
University. On Cascadia Basin, samples were col-
lected on three north-south lines ranging from the
CP-1 line (Figure 1) at the base of the continental
slope to the CP-3 line 80 mi farther offshore. The
base of the continental slope varies from 1,900 m
on the Astoria Fan at CP-l-A to 2,816 m at CP-l-E.
At the base of the continental slope farther south,
between lat. 43° and 44° N, a small trench occurs
in which depths reach 3,000 m. Stations become
deeper both to the south and to the west in Cas-
cadia Basin. One sample was taken from Gorda
Ridge off California, south of Cascadia Basin. Ten
tows were made in northern Cascadia Basin on
Nitinat Fan off Washington, during a study of
deepwater dumpsites (Carey et al. 1973). Three
areas (TP-C, TP-B, TP-A) were sampled on Tufts
Plain. Station abbreviations are as follows: NAD
= Newport hydrographic line, mainly slope sta-
tions; CP = Cascadia Basin, off Oregon; TP =
Tufts Plain; and DWD = Deepwater dumpsite,
northern Cascadia Basin, off Washington.

The beam trawl is a semiquantitative sampler
(Carey and Heyamoto 1972), with a rigid frame of
steel skids connected by a 3 m aluminum pipe,
with a collecting net of 4.1 cm stretch mesh lined
with 1.3 cm mesh net. The otter trawl is a 7 m
semiballoon Gulf of Mexico shrimp trawl with 4.1
cm stretch mesh with a 1.3 cm mesh liner. Samples
were preserved at sea in 10% formaldehyde and
sorted in the laboratory.

The specimens were examined through a dis-
secting microscope and measured with vernier

calipers usually to the nearest millimeter. The
following measurements were used (Figure 2):

Carapace length (CL) = tip of rostrum to middle
of posterior margin of carapace.

Anterior width of carapace = width between an-
terolateral spines.

Posterior width of carapace = width at posterior
margin of carapace.

Rostrum length = tip of rostrum to rostrum
base, which lies on an imaginary line between
the bases of the ocular peduncles.

Cheliped length = tip of chela to articulation
between ischium and sternum.

Chela length = tip of chela to articulation be-
tween chela and carpus, on the ventral side.

Eyespine length = tip of eyespine to proximal
end of cornea.

Incomplete synonymies are given for each
species. References include original description,
first redescription if the original description was
very short, first figure, and all synonyms.

The specimens from Oregon State University
(OSU) were compared with those borrowed from
the U.S. National Museum (USNM), the Museum
of Comparative Zoology at Harvard (MCZ), and
from Texas A&M University (TAMU). Specimens
of each species are cataloged in the Oregon State
University Benthic Invertebrate Museum
(OSUBI). The holot5^es and a few paratypes of the
new species were deposited at the U.S. National
Museum.

MUNIDOPSIS WHITE AVES 1874

Munidopsis Whiteaves 1874:212 (original de-
scription); Smith 1885:493 (synonomy with
Galacantha); Milne-Edwards and Bouvier
1894:271, 1897:63 (redescriptions); Faxon
1895:81-83 (synonomy with Orophorhynchus,
Elasmonotus, Galathodes, and Anoplonotus);
Chace 1942:69 (synonomy with Galacantha).

Galathodes Milne-Edwards 1880:53 (original de-
scription); Milne-Edwards and Bouvier
1894:276, 1897:94 (redescriptions).

Orophorhynchus Milne-Edwards 1880:58 (origi-
nal description); Milne-Edwards and Bouvier
1894:283, 1897:110 (redescriptions).

Elasmonotus Milne-Edwards 1880:60 (original
description); Milne-Edwards and Bouvier
1894:279, 1897:98 (redescriptions); Henderson
1888:165 (synonomy with GaZaf/iopsis).

14

AMBLER: SPECIES OF A/ l/MDOPS/S OFF OREGON

CHELIPED

SECOND ANTENNAE

INNER EYESPINE
OUTER EYESPINE

ANTEROLATERAL SPINE "^^^^^NAL SPINE

ANTERIOR BRANCH OF CERVICAL GROOVE
FIRST LATERAL SPINE

POSTERIOR BRANCH OF CERVICAL GROOVE

AMBULATORY LEGS

^ ABDOMINAL SEGMENTS

<!M»*

Figure 2. — Generalized drawing of the genus Munidopsis.

Anoplonotus Smith 1883:50 (original description).

Galathopsis Henderson 1885:417 (original de-
scription).

Galacantha Milne-Edwards 1880:52 (original de-
scription); Henderson 1888:166 (redescription,
argues for separate genus); Milne-Edwards and
Bouvier 1894:268, 1897:55 (redescriptions).

Diagnosis. — Integument heavily calcified;
carapace longer than wide, covered with spines,
sometimes with setae, and with rugae often in
transverse rows; dorsal surface of carapace with
well-defined cardiac and gastric areas, gastric
area separated from branchial area by cervical
groove; anterolateral borders of carapace usually
spinose or dentate but occasionally entire; an-
terior border of carapace sometimes with small
supra-antennal spine or tooth, never with a long
supraorbital spine; eyes small, unfaceted, and

devoid of pigment; ocular peduncle sometimes
extended beyond cornea as a spine (eyespine);
rostrum well developed, triangular or spatulate;
antennular peduncle with short flagellum; anten-
nal peduncle four jointed, usually with long flagel-
lum; chelipeds either longer or shorter than next
three ambulatory legs, epipodite present some-
times on chelipeds and occasionally on ambula-
tory legs; moderate number of large eggs, a few
millimeters in diameter.

The genus Munidopsis (including Galacantha)
has about 140 species with 112 of them covered in
checklists by Doflein and Balss (1913) and 101 in a
checklist by Benedict (1902). The genus has been
divided into five groups called either genera, sub-
genera, or groups (Henderson 1888; Milne-Ed-
wards and Bouvier 1894; Alcock 1901; Tirmizi
1966). Faxon (1895) and Chace (1942) recom-
mended a single genus Munidopsis because many

15

FISHERY BULLETIN: VOL. 78, NO. 1

species show characteristics intermediate be-
tween groups.

Several extensive keys exist. Benedict's (1902)
key describes all specimens in the U.S. National
Museum collection at that time. Chace (1942)
wrote a key to the western Atlantic species, which
has been updated by Pequegnat and Pequegnat
(1970, 1971). Other extensive keys were con-
structed by Milne-Edwards and Bouvier (1894)
and Alcock (1901).

Characteristics of
Taxonomic Importance for Species

Although the antennular peduncle, antennal
peduncle, and merus of the third maxilliped are
usually drawn for new species, these characters
are rarely used to identify species.

Carapace. Presence, absence, and number of
spines on the anterior, lateral, and posterior mar-
gins and on the dorsal surface of the carapace.

Presence of the antennal spine variable among
specimens of the same species. The basic type of
ornamentation (ridges, tubercles, crenulations,
spines, setae) on the dorsal surface. Slight differ-
ences in ornamentation, size, and spacing found on
specimens from different geographic locations are
considered varietal differences.

Rostrum. The general shape: triangular or
rounded. Lateral margins armed with spines or
unarmed.

Eyespines. Presence or absence; length in rela-
tion to cornea; sharp or blunt.

Chelipeds. Length compared with carapace
length; ornamentation, especially spines on seg-
ments.

Walking legs. Not as important as chelipeds.
General ornamentation.

Epipodites on chelipeds and legs. Presence or
absence.

Abdomen. Presence or absence of spines on dor-
sal surface.

Key to Species of Munidopsis off Oregon and Washington

la. No epipods on chelipeds 2

lb. Epipods present on chelipeds 5

2a. Eyespines absent; one large spine on second, third, and fourth abdominal segments;

frontal and lateral margin of carapace forms a right angle quadrata

2b. Eyespines present; abdomen unarmed; spine or tooth present at anterolateral corner of

carapace 3

3a. Wide, triangular rostrum; posterior margin of carapace unarmed aries

3b. Narrow rostrum with or without lateral spines; posterior margin of carapace armed with 1

to 10 spines 4

4a. Rostrum with 2-6 lateral spines, posterior margin of carapace armed with 3-10 (usually

4-6) spines; chela with 2 inner spines bairdii

4b. Rostrum with no lateral spines; posterior margin of carapace armed with one spine; chela

without two inner spines sp.

5a. Eyestalks extend beyond eye as definite, sharp spines 6

5b. Eyestalks extend beyond eye as blunt processes 11

6a. Two eyespines present, a longer inner spine and a short outer spine ciliata

6b. Only inner eyespine present 7

7a. Rostrum wide, not triangular, with dorsal carina, rounded at end yaquinensis

7b. Rostrum triangular, with dorsal carina and pointed at end 8

8a. Carapace and legs covered densely with setae; lateral margins of carapace

without spines cascadia

8b. Carapace and legs not covered densely with setae; spines on lateral margins of carapace 9

16

AMBLER: SPECIES OF Wt/MDOPS/S OFF OREGON

9a. Thin, unarmed rostrum strongly upturned beringana

9b. Triangular rostrum armed with spines or teeth, not upturned 10

10a. Rostrum armed laterally with two to four small spines; carapace covered with crenulated
(margin cut into rounded scallops) tubercles; eyespines long, anterolateral spine about
same size as first lateral spine tuftsi

10b. Rostrum armed laterally with minute teeth; carapace covered with semicircular scalelike
tubercles with long setae; eyespines short; anterolateral spine larger than first lateral
spine subsquamosa

11a. Rostrum triangular without dorsal carina; large spine on second, third, and fourth abdom-
inal segments verrucosus

lib. Rostrum wide at base, nearly parallel to eyestalks, with dorsal carina; abdomen with no

large spines latirostris

Munidopsis quadrata Faxon 1893

Munidopsis quadrata Faxon 1893:1888 (original
description); Faxon 1895:97 (redescription), pi.
23,fig. 1, le.

Elasmonotus quadratus Milne-Edwards and
Bouvier 1894:281-282 (under discussion of
genus Elasmonotus, key to Elasmonotus).

Material— OSVBl 00170, gravid female, 11 mm
CL, stn NAD 11, 44°39.0' N, 124°59.9' W, BMT
312, 950 m; OSUBI 00171, male, 13 mm CL, stn
Waldpt., 44°21.7' N, 125°07.9' W, OT 27, 1,000 m;
OSUBI 00182, gravid female, 12 mm CL, male, 11
mm CL, stn NAD 12, 44°38.8' N, 125°09.1 ' W, 0TB
360, 1,170 m; OSUBI 01580, 2 specimens, stn
DWD 5, 48°38.1 ' N, 126°58.1 ' W, BMT 9, 2,189 m.

Distribution. — The range of Munidopsis quad-
rata extends from off Destruction Island, Wash., to
Tres Marias Islands, Mexico, at depths usually
between 620 and 1 ,57 1 m; it has also been found at
86 and 110 m, off Wilmington, Calif., and Los
Coronados Islands, respectively (Rathbun 1904).
These shallow records (86 and 110 m) seem un-
likely when compared with the usual depth range
of 620-1,571 m, although other species of
Munidopsis do occur on the Continental Shelf.
Munidopsis quadrata occurs on the continental
slope off Oregon and on the Nitinat Fan off
Washington at 950-2,189 m, which extends the
known depth range.

Munidopsis aries (Milne-Edwards 1880)

Orophorhynchus aries Milne-Edwards 1880:58
(original description); Milne-Edwards and

Bouvier 1897:111-113 (redescription), pi. 9.
Munidopsis aries. Benedict 1902:316 (genus
changed to Munidopsis).

Materia/.— USNM 171346, female, 43 mm CL, stn
CP-2-E, 44°38.4' N, 126°42.0' W, BMT 270, 2,850
m; OSUBI 00169, female, 29 mm CL, stn CP-3-E
Channel, 44°44.4 ' N, 127°22.1 ' W, BMT 359, 3,025
m. The holotype was not examined.

Remarks. — This species is known from only three
specimens — the type and two Oregon specimens
(Table 1). Munidopsis sundi and M. albatrossae ,
both giant species, are most similar to M. aries in
shape and ornamentation of the carapace.

The description of M. aries (Milne-Edwards and
Bouvier 1897) fits the Oregon specimens except for
the chelipeds. In the Oregon specimens, the merus
of the cheliped has four small spines at the an-
terior border and a row of small spines along the
dorsal ridge; the carpus has four or five small
spines on the dorsal surface with two or three of
these at the anterior border. Milne-Edwards and
Bouvier (1897) described two denticles at the an-
terior border of the merus and the carpus. They did
not describe the inner margin of the merus of the
third maxilliped. In the Oregon specimens three

Table l. — Morphometry of Munidopsis aries. Data on holotype
from Milne-Edwards and Bouvier (1897).

USNM

OSUBI

Measurement (mm)

Holotype

171346

00169

Carapace length

20

43

29

Rostrum length

5.1

12

8

Anterior carapace width

9.7

18

14

Posterior carapace width

10.5

26

18

Width at widest part of carapace

14

29

19

Cheliped length

18

37

24

Rostrum length/carapace length

0.26

0.28

0.28

Cheliped length/ carapace length

0.90

0.86

0.83

17

FISHERYBULLETIN:VOL.78,NO. 1

small spines occur along the posterior half of this
inner margin.

Distribution. — Munidopsis aries appears to be a
rare, deepwater species. The type is from near
Bequia in the Caribbean Sea (lat. 13° N, long. 61.1°
W) at 2,912 m. The Oregon specimens were col-
lected at 2,850 m in Cascadia Basin and at 3,025 m
in Cascadia Channel.

Munidopsis bairdii (Smith 1884)

Galacantha bairdii Smith 1884:356 (original de-
scription).

Munidopsis bairdii. Smith 1886:649 (redescrip-
tion) pi. 5, fig. 2.

Munidopsis chacei. Kensley 1968:288 (original
description) fig. 1.

Materia/.— Holotype, USNM 5717, female, 45 mm
CL, Albatross stn 2106, 37°41.3' N, 73°3.3' W,
2,740 m; USNM 10801, male, Albatross stn 2573,
40°34.3' N, 66°09' W, 3,188 m; USNM 171344,
male, 48 mm CL, male, 41 mm CL, stn CP-2-B,
45°34.5' N, 126°18.5' W, BMT 156, 2,661 m;
OSUBI 00193, female, 28+ mm CL, stn CP-2-E,
44°43.4' N, 126°27.5' W, 0TB 90, 2,772 m; OSUBI
00192, 6 specimens, stn CP-2-C, 45°20.8' N,
126°37.7' W, BMT 264, 2,750 m; OSUBI 00194,
female, 22 m CL, stn CP-2-D, 44°53.7 ' N, 126°33.4'
W, BMT 162, 2,774 m; 51 uncataloged specimens,
smallest ovigerous female 43 mm CL.

Remarks. — The characteristics of Munidopsis
chacei Kensley, are within the range of variation
of M. bairdii and, therefore, M. chacei is here con-
sidered a synonym of M. bairdii. As noted by
Kensley (1968), M. chacei and M. bairdii differ in
the number of spines of the gastric and cardiac
areas and on the posterior margin, and the ratio of
dactyl to propodal length of the ambulatory legs.
However, the range of variation of these charac-
teristics in our specimens of M. bairdii includes
those observed for M. chacei (Table 2).

Munidopsis columbiana Pequegnat and
Pequegnat is a closely related species, with the
following differentiating characteristics: anten-
nal spines present in M. columbiana, absent in M.
bairdii; abdominal segments with spines in M.
columbiana, absent in M. bairdii; and inner mar-
gin of merus of third maxilliped with five to eight
teeth in M. columbiana, three teeth in M. bairdii,
and two to four teeth in our specimens.

Table 2. — Selected spine counts of Munidopsis chacei and M.
bairdii from their type descriptions, compared with data from 46
Oregon specimens.

Gastric

Cardiac

Posterior

Item

area

area

margin

M. chacei:

Kensley (1968)

5

4

4

M. bairdii:

USNM 5717

6

3

10

USNM 10801

5

3

4

Faxon (1895)

4

1

5

Oregon specimens

3-5

2-4

4-6

Pequegnat and Pequegnat (1971) mention two
other characteristics, but these do not separate the
two species. In their key, the presence of more than
seven spines on the carapace separates M. colum-
biana from M. bairdii. In the Oregon specimens,
the number of spines on the carapace ranges from
5 to 11. The number of lateral spines on the ros-
trum is not a distinguishing characteristic.
Munidopsis columbiana can have from two to six
lateral spines, but usually has four. The type of M.
bairdii has six lateral spines. In the Oregon
specimens the number of spines ranges from two to
six, but usually is four.

Distribution. — Munidopsis bairdii occurs at
depths of 2,377-2,940 m in Cascadia Basin. It has
been previously collected in both the Atlantic and
Pacific Oceans: Cape Sable to Cape May (Smith
1886); Cape Hatteras to Nantucket (Smith 1884);
off Panama (Faxon 1895); and off the west coast of
the Cape Peninsula or Cape Point, South Africa
(Kensley 1968).

Munidopsis sp. (Figure 3)

Munidopsis sp. USNM 171345, male, 20 mm CL,
stn NAD 17, 44°31.2' N, 125°15.5' W, OT 23,
1,829 m.

Remarks. — Munidopsis sp. closely resembles
Munidopsis bairdii, but is distinctly different in
some characters. More specimens are needed to
verify species status. The form differs from M.
bairdii in having no lateral spines on the rostrum,
a shorter rostrum, only one spine on the posterior
margin, rugae on carapace much less pronounced,
hairs on carapace thicker, shorter eyespines ex-
tending just beyond the cornea, and the chelae not
armed with two inner spines. However, Munidop-
sis sp. has four spines on the gastric area and three
on the cardiac area, which are within the range
found for M. bairdii.

18

AMBLER: SPECIES OFMUNIDOPSIS OFF OREGON

S^^

J I I I I

cm

Figure 3. — Munidopsis sp. (similar to Munidopsis bairdii)
USNM 171345, dorsal view of carapace.

Distribution. — Munidopsis sp. has only been col-
lected from the lower continental slope at 1,829 m,
which does not overlap with the depth range of M.
bairdii (2,377-2,940 m).

Munidopsis ciliata Wood-Mason 1891

Munidopsis brevimana Henderson 1885:414 (orig-
inal description); Henderson 1888:154 (re-
description), pi. 17, fig. 1, 2.

Munidopsis ciliata Wood-Mason 1891:200 (origi-
nal description); Faxon 1895:84 (synonymy with
M. brevimana, comparison with M. nitida);
Faxon 1895:81-82 (M. ciliata because genus
sjTionomy caused prior usage of M. brevimana),
pi. 18, fig. 3.

Material.— MCZ 4540, female, 27 mm CL, Alba-
tross stn 3392, 7°5.5' N, 79°40.0' W, 2,324 m; MCZ
4541 , male, 19 mm CL, Albatross stn 3393, 7°15.0 '
N, 79°37.0' W, 1,867 m; USNM 171342, female, 13
mm CL, stn CP-l-A, 45°55.3 ' N, 125^36.1 ' W, BMT
194, 2,030 m; USNM 171343, 13 specimens, stn
CP-2-A, 45=52.5' N, 126'40.8' W, BMT 154, 2,666
m; OSUBI 00188, male, 15 mm CL, stn CP-l-E,
44°39.8' N, 125=36.4' W, BMT 184, 2,875 m;
OSUBI 00189, 33 specimens, stn CP-2-D, 44=53.7'
N, 126°33.4' W, BMT 162, 2,774 m; OSUBI 01581,
females, 16 mm CL, stn CP-2-A, 45°48.3' N,
126=28.2' W, BMT 158, 2,651 m; OSUBI 01578,
female, 12 mm CL, stn CP-2-C, 45=18.6' N,
126=31.5' W, BMT 265, 2,750 m.

Comparative material. — Munidopsis nitida:
USNM 21287, female, 21 mm CL, Albatross stn
2140, 17=36.2 ' N, 76=46. 1 ' W, 1,768 m. Munidopsis
verrilli: Holotype, USNM 20556, female, 22 mm
CL, Albatross stn 2923, 32=40.5' N, 117=31.5' W,
1,504 m.

Remarks. — The Oregon specimens differ from
the Albatross specimens by the shorter, stouter
spines on the carapace and legs; shorter setae cov-
ering the carapace and legs; rostrum with a nar-
rower base; and no extra spine between the antero-
lateral and antennal spines, as sometimes occurs
in the Albatross specimens (Figure 4). A small
ventral spine occurs behind the large inner eye-
spine on the Oregon specimens. Carapace
sculpturing is similar in all specimens. I conclude
that the observed differences are racial or varietal
rather than specific. All specimens are from the
Indian and Pacific Oceans.

Munidopsis ciliata is closely related to M. nitida
Milne-Edwards, but has a more sculptured
carapace. Faxon (1895) suggested the differences
may be racial or varietal rather than specific.
Munidopsis nitida has only been found in the At-
lantic Ocean (Milne-Edwards 1880; Pequegnat
and Pequegnat 1970). Because of the distinct
differences in carapace sculpture, I consider M.
ciliata and M. nitida to be separate species.

Both M. ciliata and M. nitida are closely related
to M. verrilli Benedict, but differ in that M. verrilli
has no epipods on the chelipeds or walking legs,
whereas M. ciliata and M. nitida have epipods on
only the chelipeds; M. verrilli has two spines on
the crest of the chela and two spines on the inner
edge of the merus of the cheliped, whereas M.
ciliata and M. nitida do not; M. verrilli does not

19

FISHERY BULLETIN: VOL. 78, NO. 1

I'll L

I cm

FIGURE 4.

-Munidopsis ciliata, dorsal view of
carapace.

have an inner spine on the third segment of the
antennae, which is present in M. ciliata and M.
nitida; and the cheliped is 1.5 times as long as the
carapace length in M. verrilli, but about the same
length in M. ciliata and M. nitida.

Distribution. — Munidopsis ciliata occurs in the
eastern part of Cascadia Basin from 2,030 to 2,875
m, off Panama (Faxon 1895) and off the Arrou
Islands, Indonesia, (Henderson 1888) in the
Pacific Ocean, and the Bay of Bengal, Indian
Ocean (Wood-Mason 1891; Alcock 1901). It occurs
deeper than M. verrilli, which has only been re-
ported off California from San Diego to the Pioneer
Seamount at depths of 805-1,618 m (Goodwin
1952). No M. verrilli have been found at these
depths off Oregon. Goodwin (1952) found M. ver-

rilli on rock samples. In one beam trawl ( BMT 162)
off the Oregon coast, a log was collected at 2,724 m
on which there were 33 M. ciliata, 67% of the total
M. ciliata caught.

Munidopsis yaquinensis n. sp. (Figure 5)

Maierm/. —Holotype, USNM 171340, female,
17.4 mm CL, stn CP-3-A, 45°57.1 ' N, 127^32.9' W,
BMT 321, 2,763 m; Paratypes: OSUBI 01583, 6
males, 12-13 mm CL, stn CP-l-A, 45°56.5' N,
125°52.5' W, BMT 251, 2,377 m.

Diagnosis.— A small species, 12-17 mm CL; large
spatulate rostrum with strong carina, small stout
eyespines hidden by rostrum; carapace with no
spines but covered with small transverse ridges;
antennal and anterolateral points of front
carapace margin separated by semicircular mar-
gin; ambulatory legs with strong anterodorsal
carinae.

Description. — Rostrum wide, spatulate, with
crenulated edges, base of rostrum with notch
around cornea; dorsal surface of rostrum sparsely
covered with setae, strong dorsal median carina
from anterior part of rostrum to center of gastric
area, median carina not extending to tip of ros-
trum; ventral surface of rostrum covered with
small setae and with central ridge; length, 4.9
mm.

Carapace length (17.4 mm) greater than an-
terior carapace width (8.3 mm), posterior carapace
width (11.5 mm), or largest width of carapace (12.2
mm); frontal margin with antennal and antero-
lateral points separated by semicircular border;
lateral margins without spines, forming raised
rounded margin; single ridge at posterior border,
unarmed; carapace surface covered by small
ridges with setae on anterior side, ridges strongly
transverse except for those on anterior branchial
regions, two larger ridges with crenulated edges
on anterior gastric area.

Sternum covered by very small ridges with long
setae.

Abdomen unarmed, covered with setae, very
slight ridges on somites two and three.

Ocular peduncle movable, with a small, stout,
inner eyespine covered by rostrum, eyespine a lit-
tle longer than length of unpigmented cornea.

Basal segment of antennular peduncle with
small anterodorsal spine and anteroventral, jag-
ged, stout tooth.

20

AMBLER: SPECIES OF MUNIDOPSIS OFF OREGON

Figure 5. — Munidopsis yaquinensis,
new species, female holotype, dorsal
view.

'Ill'

cm

Basal segment of antennal peduncle with two
stout teeth; second, third, and fourth segments
without teeth or spines; anterior fourth segment
with outer rounded extension.

Inner margin of third maxilliped smooth.

Chelipeds with epipodites, chelipeds covered
with very small ridges with setae, carpus with
strong inner ridge, merus triangular with strong
dorsal ridge, right finger length 41% of chela
length (6.4 mm), right cheliped length 19.0 mm.
Pereiopods without epipodites, covered sparsely
with only short setae; propodus, carpus, and merus
triangular in cross section, with prominent ridges
on anterodorsal side.

Remarks. — The seven Oregon specimens are
similar in all important characteristics, with the
exception of an OSUBI 01583 specimen, which has
an extra long, apparently deformed, rostrum with
notched sides.

Munidopsis yaquinensis differs distinctly from
all other known species. It most closely resembles
M . platirostris (Milne-Edwards and Bouvier 1897)
and M. liuida (Pequegnat and Pequegnat 1971).

Etymology. — Munidopsis yaquinensis is named
for the Oregon State University oceanographic
ship RV Yaquina.

Distribution.— Occurs at 2,763 and 2,377 m in
Cascadia Basin.

Munidopsis cascadia n. sp. (Figure 6)

Ma^ermZ.— Holotype, USNM 171338, female, 54
mm CL, stn CP-l-E, 44=35.5 ' N, 125=^35.4 ' W, 0TB
112, 2,810 m; Paratypes: USNM 134658, male, 45
mm CL, stn CP-l-E, 44°46.2' N, 125°01.8' W, 0TB
49, 2,800 m; USNM 171339, female, 38 mm CL, stn
CP-2-A, 45°59.1 ' N, 126°40.1 ' W, BMT 256, 2,743

21

FISHERY BULLETIN: VOL. 78, NO. 1

Figure 6. — Munidopsis cascadia, new
species, male holotype, dorsal view.

I ■ ■ ■

cm

m; OSUBI 00177, male, 51 mm CL, stn CP-l-E,
44°32.3' N, 125°41.6' W, 0TB 77, 2,975 m; OSUBI
00178, gravid female, 37 mm CL, stn CP-l-E,
44°48.8' N, 125°36.4' W, BMT 287, 2,743 m;
OSUBI 00179, male, 27 mm CL, stn CP-2-D,
44^53.7' N, 126°33.4' W, BMT 162, 2,884 m;
OSUBI 00180, gravid female, 47 mm CL, stn
CP-l-D, 44°55.4' N, 125°40.6' W, BMT 187, 2,760
m.

Comparative material. — Munidopsis bermudezi
holotype, MCZ 10231, female, 38 mm CL, stn
2967, 19°43.5' N, 74°57.5' W, 2,434-3,020 m.

Diagnosis. — Moderate size (27-54 mm CL);
carapace and legs densely covered with setae;
stout eyespine on immovable eye stalk; two stout
gastric spines; lateral margins of carapace smooth
and slightly convex; resembles Munidopsis ber-
mudezi.

Description. — Carapace length longer than wide,
posterior width slightly greater than anterior
width; strong antennal and anterolateral teeth
separated by semicircular margin, a blunt tooth
distal to anterolateral tooth, another blunt tooth
at end of cervical groove; lateral margins raised

22

AMBLER: SPECIES OF MUNIDOPSIS OFF OREGON

and slightly convex; pair of large, blunt, gastric
spines, one pit behind each gastric spine, each pit
surrounded by a small bare area; dorsal carapace
surface densely covered with setae except for bare
spots posterior to pits on gastric area, on cervical
groove, and on anterior boundary of cardiac re-
gion; with setae removed dorsal surface fairly
smooth except for rounded tubercles of posterior
branchial area; one blunt ridge at unarmed poste-
rior margin.

Rostrum 22'7f of carapace length, triangular in
dorsal view, horizontal in lateral view, covered
with setae, bluntly carinate dorsally.

Abdomen densely pubsecent, unarmed; second,
third, and fourth somites with two blunt trans-
verse ridges.

Sternum with few setae and small tubercles;
with transverse setose ridge opposite legs.

Eyestalks immovable; long, stout, pubescent in-
ternal eye spine much longer than diameter of the
cornea.

Basal segment of antennular peduncle with one
long spine midventrally, one long spine mid-
dorsally, and an inner toothed process.

Basal segment of antennal peduncle covered
with setae, bearing outer ventral tooth and stout,
inner, ventral spine. Second segment with large,
outer, ventral spine and small, inner, ventral
tooth.

Inner margin or merus of third maxilliped has
three main spines, the posterior two have two
points.

Cheliped shorter than carapace length; densely
pubescent; epipods on chelipeds only; ischium
with dorsal and ventral spine at meral articula-
tion and a ventral row of six to seven small spines
(including spine at meral articulation); merus
with five spines at carpal articulation, dorsal row
of six spines (including spine at carpal articula-
tion), and two spines on the inner margin; carpus
with four spines at chela articulation and one
spine on inner dorsal surface; chela without
spines.

Remarks. — Paratypes differ only slightly from
holotype (Table 3). The chelipeds of four paratypes
(USNM 134658, USNM 171339, OSUBI 00177,
and OSUBI 00178) are relatively longer than
those of the holotype and two other paratypes
(OSUBI 00179 and OSUBI 00180), as shown by
the ratio of carapace length to cheliped length in
Table 3. In two specimens (OSUBI 00180 and
USNM 134658), the lateral carapace margins
posterior to the cervical groove have jagged edges
instead of being smooth. The number of spines on
the inner edge of the merus of the third maxilliped
is constant except for one maxilliped of USNM
134658.

The number of spines on the cheliped segments
is usually constant. Only the holotype has five
spines at the carpal-meral articulation — the
paratypes have four. There are four to five spines
of the dorsal row on the merus; usually there are
four on the paratypes. The number of spines on the
ventral row of the ischium is variable, ranging
from three to six. The dorsal inner spine on the
carpus is always present, but is greatly reduced on
paratype OSUBI 00179, and on OSUBI 00177
there are two spines.

A rhizocephalan parasite is present under the
abdomen of USNM 171339.

Munidopsis cascadia was compared with the
type of M. bermudezi. Munidopsis cascadia has
stouter, blunter gastric spines, no spines on the
lateral margin of the carapace, convex rather than
a straight lateral margin of the carapace, and
more pubescence.

Etymology. — Munidopsis cascadia is named from
Cascadia Basin since all the specimens were found
there.

Distribution. — Only seven specimens of M. cas-
cadia are known, all from Cascadia Basin at
2,743-2,926 m. Munidopsis bermudezi has only
been found in the Atlantic Ocean (Chace 1942;

Table 3. — Morphometry of Munidopsis cascadia.

Measurement (mm)

USNM
'171338

USNM
1 34658

USNM
171339

OSUBI
00177

OSUBI OSUBI OSUBI
00178 00179 00180

Carapace length 54 45 38 51

Rostrum length 14 13 10 15

Anterior carapace width 36 21 18 23

Posterior carapace width 38 27 25 32

Cheliped length 43 41 33 49

Chela length 21 19 14 24

Carapace length/ cheliped length 1.26 1.10 1.15 1.04

37

9
17
24
35
12

1.06

27

8

12
16
22
10

1.23

47
13
23
36
37
17
1.27

'Type-specimen.

23

FISHERY BULLETIN; VOL. 78, NO. 1

Sivertson and Holthuis 1956; Pequegnat and
Pequegnat 1970; Laird et al. 1976).

Mutiidopsis heringana Benedict 1902

Munidopsis heringana Benedict 1902:279 (origi-
nal description), fig. 23.

Material— \5^^M 134659, male 32 mm CL,
male, 29 mm CL, female, 29 mm CL, stn Coos Bay
#A, 43°17.3' N, 125°49.3' W, 0TB 76, 3,000 m;
OSUBI 00175, female, 31 mm CL, stn CP-2-E,
44°40.8' N, 126°26.5' W, 0TB 48, 2,800 m; OSUBI
00176, male, 23 mm CL, stn CP-3-D, 44°53.5' N,
127°27.5' W, BMT 332, 2,826 m; 20 uncataloged
specimens, no ovigerous females.

Remarks. — Three Oregon specimens (USNM
134659) were compared with Benedict's syntypes
at the USNM by Henry B. Roberts.^ He found
considerable variation between the Oregon
specimens and the syntypes regarding number of
spines on the gastric area, length and spacing of
the rugae on the carapace, and number of spines
on the lateral edges of the carapace and on the
meri of the chelipeds. The rugae of the Oregon
specimens are, in general, shorter, more promi-
nent, and more widely separated than the rugae of
Benedict's specimens from the Bering Sea. The
number of spines on the gastric area of the Oregon
specimens varied from 4 to 17, on the lateral edge
of the carapace from 2 to 4, and on the meri of the
chelipeds from 7 to 12.

Distribution. — Munidopsis heringana was ob-
tained in the deeper portions of Cascadia Basin
from 2,800 to 3,041 m, on Tufts Plain from 3,354 to
3,990 m, and in the Bering Sea at Alhatross stn
3603, 3,276 m (Benedict 1902).

Munidopsis tuftsi n. sp. (Figure 7)

Materia/.— Holotype, USNM 171336, male, 70
mm CL, stn TP-3, 44°40.8' N, 133°26.3' W, BMT
233, 3,717 m; Paratypes: USNM 171337, male, 36
mm CL, stn TP-4, 44°31.1' N, 134°43.8' W, 0TB
334, 3,858 m; OSUBI 00181, male, 62 mm CL, stn
TP-3, 44°39.8' N, 133°37.2' W, BMT 232, 3,724 m;
OSUBI 00183, gravid female, 67 mm CL, stn TP-7,
44°58.0' N, 133°14.5' W, BMT 302, 3,500 m;

^Henry B. Roberts, Senior Museum Specialist, U.S. National
Museum, Washington, DC 20560, pars, commun. July 1970.

24

OSUBI 01582, male, 15 mm CL, stn TP-6, 44°59.8'
N, 132°12.1' W, BMT 302, 3,585 m.

Comparative material. — Munidopsis crassa:
USNM 8563, female 45+ mm CL, Alhatross stn
2224, 36°16.5' N, 68°21' W, 4,710 m; USNM
10803, female, 43 mm CL, Alhatross stn 2573,
40°34.3' N, 66°09' W, 3,188 m; USNM 19289, male
44 mm CL, Albatross stn 2566, 37°23' N, 68°08' W,
4,795 m. Munidopsis aculeata: USNM 21277,
male 39 mm CL, Alhatross stn 3382, 6°21.0' N,
80°41.0' W, 3,281 m. Munidopsis suhsquamosa:
See M. suhsquamosa.

Diagnosis. — Medium-sized species, 36-70 mm.
CL; triangular rostrum with small lateral spines;
long eyespines; carapace wider posteriorly than
anteriorly, covered with tubercles, first lateral
spine not much larger than anterolateral spine;
similar to Munidopsis crassa.

Description. — Rostrum triangular, bearing six
(two right, four left) small spines laterally on dis-
tal half, upturned distally, dorsal median carina;
dorsal surface with small tubercles; ventral sur-
face smooth; length 267c of carapace length.

Carapace longer than wide, anterior width and
length measured between first lateral spines less
than posterior width; frontal margin bearing an-
tennal spines, anterolateral spine on hepatic re-
gion with three spinules. First lateral spine on an-
terior lobe of branchial region with spinules on
anterolateral spine. Several (five or six) small
spines on lateral edge behind first lateral spine.
Gastric area covered by crenulated tubercles bear-
ing setae; six main spines — four at the base of the
rostrum, two posterior to these — and numerous
slightly smaller spines, smooth spaces between
spines and tubercles. Cardiac and posterior
branchial areas with crenulated transverse ridges
bearing setae, smooth between ridges. Posterior
margin unarmed, double ridge of small tubercles.

Sternum smooth, except for scattered setae on
bumps and lateral ridges with many setae on top.

Abdomen spineless, covered with tubercles;
ridges on somites two to four.

Ocular peduncle slightly moveable, extends
beyond unpigmented cornea as stout inner spine,
about twice the length of diameter of cornea,
spinule on inner side of cornea.

Basal segment of antennular peduncle with one
long slender spine midventrally; one long slender

AMBLER: SPECIES OF MUNIDOPSIS OFF OREGON

Figure 7. — Munidopsis tuftsi, new
species, male holotype, dorsal view.

'Ill

I cm

spine middorsally; a rounded, toothed process on
inner side; and spinule on outer side.

Basal segment of antennal peduncle with two
stout ventral spines. Second segment with outer
spines and a small dorsal tooth. Third segment
with four spines: inner, outer, and smaller dorsal
and ventral spines. Fourth segment with two
small, blunt, dorsal processes.

Inner margin of merus of third maxilliped with
four main spines, plus several spinules.

Chelipeds with epipods. Chelipeds covered with

setae and small tubercles, chela bears no major
spines; carpus with five small spines at distal edge,
and two rows of dorsal spines; merus with three to
five small spines at distal edge, row of six to nine
spines on dorsal surface, and two inner spines
on left merus. Ambulatory legs without epipods,
covered with setae and tubercles, and with spines
on carina of propodus, carpus, and merus.

Remarks. — The three paratypes vary from the
holotype in the number and presence of spinules

25

FISHERY BULLETIN: VOL, 78, NO. 1

and spines. Both the holotype and OSUBI 00181
have spinules on the inner side of the ocular
peduncle; OSUBI 00183 has no inner spinule but
has an outer spinule; USNM 171337 has no
spinules on the ocular peduncle. The number of
small spines on the rostrum varies from two to
seven with the smallest specimen having only two
spines. Paratypes USNM 171337 and OSUBI
00183 have very few spinules on the anterolateral
and first lateral spines compared with the other
two specimens. The number of spines on the inner
margin of the third maxilliped varies from two to
four. The specimens are similar in the ornamenta-
tion of the carapace and in their proportions ( Table
4).

Munidopsis tuftsi belongs to a species complex
including M. crassa, M. aculeata, and M. sub-
squamosa. These species can be separated by ob-
serving several characteristics (Table 5). In this
complex, M. tuftsi most closely resembles M.
crassa, but differs in having a narrower anterior
carapace and narrower width between first lateral
spines compared with the posterior carapace

width; anterolateral and first lateral spines of the
same size; and small spines on the lateral edges of
the rostrum. Although M. tuftsi has some charac-
teristics in common with M. aculeata and M. sub-
squamosa, it has a distinctly more spinous orna-
mentation on the carapace. A very small specimen
of M. tuftsi, OSUBI 01582, differs from the larger
specimens only in the smoother carapace or-
namentation and a larger ratio for anterior
carapace width/posterior carapace width (Table
5). The ratio of cornea diameter divided by eye-
spine length is quite variable for M. subsquqmosa,
but is usually between 0.46 and 0.55 for M. crassa
and M. tuftsi.

Etymology. — Munidopsis tuftsi is named for Tufts'
Plain where all specimens were collected.

Distribution. — The four specimens of M. tuftsi
were collected from Tufts Plain at depths of
3,500-3,858 m. Munidopsis crassa, the most simi-
lar species, has only been found from the Atlantic
Ocean (Laird et al. 1976).

Table 4. — Morphometry of Munidopsis tuftsi.

USNM

OSUBI

USNM

OSUBI

OSUBI

Measurement (mm)

'171336

00181

171337

00183

01582

Carapace length

70

62

36

^67

14.8

Rostrum length

18

17

9

216

4.2

Rostrum length/carapace

length

026

0.27

0.25

0.24

0.27

Anterior carapace width

30

29

18

32

7.6

Posterior carapace width

41

37

22

42

8.2

Width between first

lateral spines

38

36

21

42

8.2

Right cheliped

84

69

43

76

14.1

'Holotype.

2 Rostrum broken at tip

Munidopsis subsquamosa Henderson 1885

Munidopsis subsquamosa Henderson 1885:414
(original description); Henderson 1888:152 (re-
description), pi. 16, fig. 4.

Munidopsis subsquamosa Henderson var. pallida
Alcock 1894:331 (original description); Alcock
1901:268 (redescription).

Munidopsis geyeri Pequegnat and Pequegnat
1970:149 (original description).

Table 5. — Morphometric ratios and spina tion that distinguishes Munidopsis tuftsi, M. crassa, M. aculeata, and M. subsquamosa.

Characteristics

M. tuftsP

M. crassa^

M. aculeata^

M. subsquamosa'

1. Chela length/carapace length

0.41-0.44

0.42-0.45

0.65

0.37-0.46

2. Anterior carapace width/pos-

terior carapace width

0.73-0.93

50.90

0.92

0.80-0,98

3. Width between first lateral

spines/posterior carapace width

0.93-1.00

1.03-1.13

1.05

1.07-1,25

4. Cornea length/eyespine length

0.48-0.55

0.36-0.49

0.89

0.52-0.82

5. First lateral spine compared

with anterolateral spine

Same size

Larger

Same size

Larger

6. Armature on lateral edges of

Small spines

Minute teeth, none

None

Minute teeth and small

rostrum

spines

7. Rostrum turned up sharply

No

No

Yes

No

8. Number of spines on gastric

area

2-6

2-4

6

2-12

9. Ornamentation on gastric area

Tubercles with blunt

Tubercles with blunt

Sparsely covered with

Densely covered with

teeth

teeth

small scalelike
tubercles

large scalelike
tubercles

10. Geographic distribution

Tufts Plain

Off North Carolina. SE
of Martha's Vineyard.
SE of Georges Bank

Gulf of Panama

Gulf of Panama, Cas-
cadia Basin, Gulf
of Mexico, Carrib-
bean

'USNM 171336 (holotype), USNM 171337, OSUBI 00181, OSUBI 00183, OSUBI 01582.

^USNM 9563 (holotype; measurements from Smith (1885) because holotype is in poor condition). USNM 19289. USNM 10803.

^USNM 21277

"USNM 21314 (holotype), USNM 171348, OSUBI 00185, OSUBI 00186. OSUBI 00187, M. geyer/— USNM 299042. TAMU 2-0574, TAMU 2-0575.

^Unknown for holotype.

26

AMBLER: SPECIES OF MUNIDOPSIS OFF OREGON

Material. — Munidopsis subsquamosa: Holotype,
USNM 21314, female 20 mm CL, Albatross stn
3361, 6°10.0' N, 83°6.0' W, 2,692 m; USNM
171348, male, 57 mm CL, stn Coos Bay #A,
43°17.3' N, 125°49.3' W, 0TB 76, 3,000 m; OSUBI
00185, male, 70 mm CL, stn CP-3-C, 45°12.0' N,
127°32.5' W, BMT 324, 2,809 m; OSUBI 00186,
female with parasite, 41 mm CL, stn NAD 20A,
44°30.1 ' N, 125°24.3' W, 0TB 64, 2,772 m; OSUBI
00187, male, 23 mm CL, stn CP-l-E, 44"31.3' N,
125°35.5' W, 0TB H-1, 2,736 m; OSUBI 00184,
male with isopod parasite, stn CP-l-E, 44°40.5' N,
125°40.0' W, 0TB 18, 2,850 m; 46 uncataloged
specimens from off Oregon, smallest ovigerous
female 54 mm CL.

Comparative material. — Munidopsis geyeri:
Holotype, USNM 128812, male, 25 mm CL,
Alaminos stn 69-A-11-92, 23°30' N, 95° W, 2,928-
3,001 m; TAMU 2-0574, female, 38 mm CL, male,
47 mm CL, Alaminos stn 70-A-10-48, 14°29.5' N,
74°28.8' W, 4,154 m; TAMU 2-0575, male, 46 mm
CL, male, 18 mm CL, Alaminos stn 70-A-10-50,
15°50' N, 77°24.5' W, 2,654-2,791 m.

were examined on the Oregon specimens of M.
subsquamosa, the holotype of M. subsquamosa,
and five specimens of M. geyeri, including the
holotype. The range of variations of these charac-
teristics for the Oregon specimens included those
found for M. geyeri, except for the number of teeth
on the lateral edges of the rostrum (Table 6). With
the addition of the Oregon specimens, the
maximum size and range of variation of M. sub-
squamosa is extended. Mayo (1974), who collected
three specimens of M. geyeri, proposed that M.
geyeri might become a synonym of M. sub-
squamosa when more material was available.

Alcock ( 1894, 1901 ) stated that M. subsquamosa
var. pallida differs from M. subsquamosa by the
former having only two spines on the gastric area
of the carapace. Henderson (1885) did not state
how many gastric spines the holotype has; I found
only two.

Five of the Oregon female specimens have
rhizocephalan parasites on the ventral side of the
abdomen. Two other specimens had isopod para-
sites under the carapace on the posterior branchial
area.

Remarks. — Munidopsis geyeri found in the
Caribbean and Gulf of Mexico is here synonymized
with M. subsquamosa from the Pacific and with M.
subsquamosa var. pallida from the Indian Ocean.
When compared with closely related species (M.
tuftsi, M. aculeata, and M. crassa), M. geyeri and
M. subsquamosa are identical (Table 5). Munidop-
sis subsquamosa and M. aculeata have similar
carapace ornamentation, but with M. sub-
squamosa the scalelike tubercles are larger and
closer together. The two species are also distin-
guished by characteristics 1, 3, 5, and 7 of Table 5.
Munidopsis crassa and M. tuftsi have smaller,
more spiny tubercles on the carapace and usually
have longer, stouter eyespines than M. sub-
squamosa.

The distinctions given by Pequegnat and
Pequegnat ( 1970) to distinguish M. geyeri from M.
subsquamosa, and other taxonomic charcteristics

Distribution. — Munidopsis subsquamosa occurs
mainly in the eastern part of Cascadia Basin from
1,829 to 3,000 m. This species is cosmopolitan,
since it has also been collected at 3,431 m off
Yokohama, Japan (Henderson 1888), 1,471 and
1,672 m off Panama (Faxon 1895), 3,299 m in the
Bay of Bengal (Alcock 1894, 1901), 2,938-3,001 m
in the southwest Gulf of Mexico (Pequegnat and
Pequegnat 1970), 4,154 m in the Colombian Basin
(Pequegnat and Pequegnat 1971), 2,790-2,650 m
south of Jamaica (Pequegnat and Pequegnat
1971), and 3,111-3,496 m off Haiti (Mayo 1974).

Munidopsis verrucosus Khodkina 1973

Munidopsis verrucosus Khodkina 1973:1156-1159
(original description), fig. 1, 2.

Material. — Munidopsis verrucosus, USNM

Table 6.— Selected

spine

counts for Mu

midopsis geyeri

and M. subsquamosa.

M.

geyeri

M. si-

ibsquamosa

Type

USNI^ 289042

(n = 1)

TAIVIU 2-0574
TAtvlU 2-0575

(n = 4)

Type

USNM 21314

(n = 1)

Oregon specimens
(n = 20)

Characteristic

Mean

Range

Number of spines on 3d maxilliped (total, right ^ left)

Total number of teeth on lateral edges of rostrum

Number of spines on gastric area of carapace

Number of spines behind anterolateral spine of carapace (total, right +

left)

9

18
2
4

8-10

7-19

'2

4-8

6
6
2
2

7.8
3.1
4.8
9.2

6-11
0-6
2-12
4-12

' Gastric area of carapace cracked on one specimen.

27

171347, gravid female, 25 mm CL, Gorda Ridge,
40°13.4' N, 126°30.0' W, 0TB 104, 4,260 m;
OSUBI 00172, female, 26 mm CL, stn TP-9,
45°01.1' N, 135°12.6' W, BMT 308, 3,932 m.

Remarks. — The Oregon specimens are indistin-
guishable from those described by Khodkina
(1973). Munidopsis verrucosus is very similar to
M. granosa, but differs in having an epipodite on
the cheliped, setae on the tubercles of the
carapace, plumose setae on portions of the
chelipeds and pereiopods, no small antennal tooth,
and no dorsal carina on the rostrum.

Distribution. — Khodkina (1973) collected three
male specimens of M. verrucosus (33.8 mm, 34.8
mm, and 40.6 mm CL) from the Atakamsky
Trench off Antofagasta, Chile, at two stations (lat.
23°47.1' S, long. 71°03.2' W, 4,300 m, and lat.
23°15.1' S, long. 7r39.1' W, 4,880 m). The two
Oregon specimens were also found at great
depths— 3,932 m on Tufts Plain and 4,194 m on
Gorda Ridge off northern California. Alcock
(1901) collected one male specimen of Munidopsis
granosa from 2,812 m in the Bay of Bengal.

Munidopsis latirostris (Henderson)
Faxon 1895

Elasmonotus latifrons. Henderson 1885:416 (orig-
inal description); Henderson 1888:160 (rede-
scription), pi. 19, fig. 1.

Orophorhynchus latifrons. Milne-Edwards and
Bouvier 1894:287 (in key to Orophorhynchus).

Munidopsis latirostris. Faxon 1895:81-82, 99
(changed name because genus synonomy caused
prior usage of M. latifrons).

Material.— USNM 21285, female, 15 mm CL, Al-
batross stn 3381, 4°56.0' N, 80°52.5' W, 3,243 m;
MCZ 4563, female, 16 mm Ch, Albatross stn 3391,
7°15.0' N, 79°36.0' W, 280 m; USNM 171341, 14
specimens, stn CP-l-E, 44°28.2' N, 125°32.3' W,
0TB 50, 2,800 m; OSUBI 00190, 28 specimens, stn
CP-l-E, 44°35.7' N, 125°34.3' W, 0TB 155, 2,830
m; OSUBI 00191, gravid female, 23 mm CL, male,
22 mm CL, male, 20 mm CL, stn C-P-3E Channel,
44°41.2' N, 127°21.2' W, BMT 407, 3,041 m; 541
uncataloged specimens from off Oregon, smallest
ovigerous female 18 mm CL.

Remarks. — The characteristics of the Oregon
specimens agree with those of the USNM and the

FISHERYBULLETIN: VOL. 78, NO. 1

MCZ specimens, but differ slightly from the type
description (Henderson 1888). The "two slightly
rounded elevations" at the base of the rostrum on
the gastric area are blunt spines in the observed
specimens. The "faint median carina" on the ros-
trum is a definite rounded ridge extending from
the end of the rostrum to the blunt gastric spines
(Figure 8).

The following observations are added to Hen-
derson's description of M. latirostris. The basal
segment of the antennular peduncle is swollen
with two outer spines. The basal segment of the
antennal peduncle has an outer tooth and an inner
spine; the second segment has an outer stout tooth.
The meri of the ambulatory legs have dorsal ridges
with setae on the anterior side. Epipods are pre-
sent on the chelipeds only.

I I I I ' «

J

I cm

Figure 8. — Munidopsis latirostris, dorsal view of carapace.

28

AMBLER: SPECIES OF Aff/MDOPS/S OFF OREGON

In all specimens examined, the ocular peduncle
extends beyond the eye as a blunt spine, although
Benedict ( 1902) does not consider it an eyespine in
his key. On the carina of the second, third, and
fourth abdominal somites, there are slight median
projections. Benedict (1902) considers these pro-
jections "armature on the abdomen confined to the
median line."

The main variation of the Oregon and A /6a^ross
specimens is in the shape of the apex of the ros-
trum. Henderson (1888, plate XIX, figure 1) de-
scribes the rostrum as ending in an "acute apex,"
which is true for USNM 21285 and some of the
Oregon specimens. In most of the Oregon speci-
mens and MCZ 4563, the rostrum ends as a spine
(Figure 9).

Rhizocephalan parasites occurred under the ab-
domen in 40 of 444 Oregon specimens; 23 hosts
were females and 17 were males.

Distribution. — Munidopsis latirostris is the most
abundant Munidopsis species found in Cascadia
Basin, with a wide depth range, 1,900-3,021 m.
This species has also been found in the tropical
Pacific Ocean at 280 and 3,243 m off Panama
(Faxon 1895) and at 1,958 m between Papua and
Admiralty Islands (Henderson 1888).

VERTICAL AND GEOGRAPHIC
DISTRIBUTION OF THE SPECIES

Twelve species o{ Munidopsis were captured in
51% or 146 of the total number of tows. Collections
from both otter and beam trawls are included in
the distributional analysis for more complete
coverage. Although samples from otter trawls
have been considered quantitative (number per
hour trawled, Haedrich et al. 1975), beam trawls
were designed to be more quantitative, giving
number per square meter (Carey and Heyamoto

u.

I I I

I cm

Figure 9. — Munidopsis latirostris, variation in rostrum, left
rostrum ends as spine, right rostrum ends as acute apex.

1972). Carney (1976) questioned the reliability of
beam trawl data for area covered and expressed
abundance as number per trawl for samples with
similar wheel readings. In this paper, abundances
are expressed as average number per trawl
(number of specimens/number of trawls towed)
because beam and otter trawls were towed for
approximately the same time. Some specimens
which can escape through 1.3 cm mesh liners are
not sampled adequately. Adult densities of small
species such as M. ciliata, M. quadrata, and M.
yaquinensis , and immature individuals of the
other species are probably underestimated. Imma-
ture specimens included M. subsquamosa, M.
latirostris, M. bairdii,M. tuftsi, and M. beringana.
Cascadia Basin off Oregon was probably the
only area trawled adequately enough to sample all
the species, since most species were collected at
least several times there. The most abundant
species, M. latirostris, contributed 73.0% of the
total number of specimens. Three species together
contributed 20.2% of the total: M. bairdii (7.5%),
M. ciliata (6.2%), and M. subsquamosa (6.5%).
These four species together represented 93.2% of
all specimens, and were only found in Cascadia
Basin. At the deepwater dumpsite stations in
northern Cascadia Basin, all of the above except
M. ciliata were collected. Five additional species
(32 specimens) were also found on Cascadia Basin.
Although 106 tows were taken on the continental
slope off Oregon, only 5 tows yielded a total of
three species (six specimens). Three species (17
specimens) were found on Tufts Plain (Table 7).
Abundances (number per trawl) for all
Munidopsis species were about the same for the
base of the continental slope (CP-1 line) and the
CP-2 line (Table 7). However, the relative abun-
dance of species changed from east to west.
Munidopsis latirostris was the most abundant on
both the CP-1 and CP-2 lines. On the CP-1 line, M.
subsquamosa was second in rank, but on the CP-2
line, M. subsquamosa was fourth, M. ciliata was
second, and M. bairdii was third (Table 7).

Eight of the 12 Munidopsis species were col-
lected in Cascadia Basin, especially below 2,250 m
(Figure 10). The single sample from Gorda Ridge,
south of Cascadia Basin, contained one specimen
of the rare, deepwater form, M. verrucosus. Muni-
dopsis quadrata was the only species occurring
over a wide depth range on the continental slope.
A single tow on the lower part of the continental
slope contained Munidopsis sp. and M. subsqua-
mosa.

29

FISHERY BULLETIN: VOL, 78, NO. 1
Table 7. — Occurrence of Munidopsis species on the continental slope, Cascadia Basin, and Tufts Plain (Figure 1).

Base of conti-

Northern

Tufts Plain

Continental

ner

tal slope

Cascadia Basin

Cascadia Basin

Cascadia

(TP-A,

Gorda

Species

Total

slope

(CP

-l,CP-x)

(CP-2)

(CP-3, CP-4)

(DWD)

TP-B, TP-C)

Ridge

M. latirostris

586

0

362

132 77

15

0

0

M. bairdii

60

0

8

45

4

3

0

0

M. ciliata

50

0

2

48

0

0

0

0

M. subsquamosa

52

1

24

15

1

11

0

0

M. benngana

25

0

7

2

5

0

11

0

M. cascadia

7

0

4

3

0

0

0

0

M yaqutnensis

7

0

6

0

1

0

0

0

M quadrata

6

4

0

0

0

2

0

0

M. tuftsi

5

0

0

0

0

0

5

0

M. aries

2

0

0

1

1

0

0

0

M verrucosus

2

0

0

0

0

0

1

1

Munidopsis sp.

1

1

0

0

0

0

0

0

Total no of Munidopsis

spp

803

6

413

246

89

31

17

. 1

Mean no, 'trawl

2.8

0.1

5.1

6.5

23

3,1

0.9

1.0

Total no. of trawls

289

106

81

38

38

10

18

1

Percent trawls with

Munidopsis spp.

51

5

70

87

79

60

78

trace

DEPTH fmeter-^l

o

o

o

o

o

o

O

o

o

o

o

o

o

o

o

O

o

o

o

in

o

tn

Q

tr

o

T

T

^

n"

^J

r^

^^

Tufts Plain

Base of Slope

Cascadia Basin

Slope

Munidopsis species

M. auadrata 950-2189 m

M. sp. 1829 m

M. subsquamosa 1829-3000 m

M. latirostris 1900-3021 m

M. oiliata 2030-2875 m

M. bairdii 2377-2940 m

M. yaauinensis 2377-2763 m

M. aascadia 2743-2926 m

M. berinaana 2800-3990 m

M. aries 2850-3025 m

M. tuftsi 3500-3858 m

,V. verrucosus 3932-4194 m

Figure lO. — Bathymetry of Munidopsis species from the continental slope, Cascadia Basin, and Tufts Plain off Oregon and

Washington.

Four types of species distribution patterns
emerge when all the stations on Cascadia Basin
and Tufts Plain are considered (Figure 11). Two
species, M. latirostris and M. bairdii, were found

30

at most stations sampled in Cascadia Basin. The
most abundant species, M. latirostris, was also
the most widespread since it occurred at all but
two of the Cascadia Basin stations. It occurred at

AMBLER: SPECIES OF Mt/WDOPS/S OFF OREGON

• M berinqana

O M subsquamosa

1

A M cascadia

e

▲ M ciliala

§

« ** MIsi

^

TUFTS
PL A in

44* 44'

134"

—I

O M bairdii
• M tafirostns

Figure ll. — Distribution of Munidopsis species off Oregon and Washington; upper — M. cascadia, M. ciliata, M. tuftsi, M.

subsquamosa, and M. beringana; lower — M. bairdii and M. latirostris.

CP-4-E, the deepest and most western station on
Cascadia Basin. Three species — M. subsquamosa,
M. cascadia, and M. ciliata — occurred predomin-
antly on the eastern side of Cascadia Basin. Only
M. beringana was taken on both abyssal plains,
notably occurring in Cascadia Basin only at the
deeper, southern stations. Two species occurred
only on Tufts Plain — M. verrucosus and M. tuftsi.

Carney (1976) found greater overlap in species
distributions between Cascadia Basin and Tufts
Plain for holothurians than for Munidopsis
species. He described three basic distribution pat-
terns: 1) present on Cascadia Basin but generally
absent from the base of the continental slope, 2)
present over all of Cascadia Basin extending to the
eastern edge of Tufts Plain, and 3) present in the
deepest and farthest offshore stations of Cascadia
Basin and on Tufts Plain.

Two distributional studies of infauna on Cas-
cadia Basin have shown great variation in species
composition between different stations: Hancock's
(1969) polychaete study along the CP-E line
(Newport hydrographic line) and the gammarid
amphipod study at stations CP-l-E and CP-3-E by
Dickinson and Carey (1978). Carney (1976)
showed that the species composition of poly-
chaetes had greater variability between stations
than that of the holothurians. Of the 20 most
abundant gammarid amphipod species at the two
Cascadia Basin stations, only 6 had similar abun-
dances at both stations, and 10 species only oc-
curred at one station (Dickinson and Carey 1978).
Of the eight Munidopsis species I found on Cas-
cadia Basin, only three occurred at both CP-l-E

and CP-3-E. In all three groups (polychaetes, am-
phipods, galatheid crabs), there are differences in
species composition between stations on either
side of Cascadia Basin, which Dickinson and
Carey (1978) suggested may be caused by decreas-
ing sedimentation rates with increasing distance
offshore, since other environmental conditions are
constant across Cascadia Basin.

Of 65 known abyssal species of Munidopsis,
Doflein and Balss ( 1913) found that a high percent-
age (71%) are endemic to specific oceanic regions.
Since many abyssal species have been described
from single or few specimens, the percentage of
endemism declines with further collecting. My col-
lections off Oregon extended the geographic range
of seven species, three of which were previously
known from only one location: M. beringana from
the Bering Sea, M. aries from the Caribbean, and
M. verrucosus from off Chile.

The number of cosmopolitan Munidopsis
species, those found in all three major oceans, is
small (Doflein and Balss 1913). Only one of the
Oregon species, M. subsquamosa, can be consi-
dered cosmopolitan. Seven of the Oregon species
are found only in the Pacific Ocean; one is also
found in the Indian Ocean (Table 8). However, four
of the Pacific and Indian-Pacific species have sib-
ling species in the Atlantic Ocean, evidence that at
one time the progenitors had broader distribu-
tions.

The four most abundant species from Cascadia
Basin have tropical Pacific affinities (Table 8).
Only one species, M. beringana, has arctic
affinities and is found in the deepest parts of Cas-

31

FISHERY BULLETIN: VOL. 78, NO. 1

Table 8. — Geographic occurrences of Munidopsis species from Cascadia Basin and Tufts Plain (Milne-Edwards 1880; Smith 1884,
1886; Henderson 1888; Faxon 1895; Alcock 1901; Benedict 1902; Rathbun 1904; Kensley 1968; Pequegnat and Pequegnat 1970, 1971;
Khodkina 1973; Mayo 1974; Laird et al. 1976).

Eastern Pacific Ocean

World ocean

Sibling species'

Species

Endemic

North
America

Arctic Tropical Bipolar Pacific

Indian and
Pacific

Atlantic

Species

Ocean

M. aries

M. bairdii

M. beringana +

M. cascadia +

M. ciliata

M. latirostris

M. quadrate +

M. subsquamosa

M. tuftsi +

M. verrucosus

M. yaquinensis +

' Most similar species, as described in this paper.

+
+
+

+
+

M. bermudezi
M. nitida

M. crassa
M. granosa

Atlantic (Laird et al.

1976)
Atlantic (Pequegnat

and Pequegnat 1970)

Atlantic (Laird el al.

1976)
Indian (Alcock 1901)

cadia Basin and on Tufts Plain. Munidopsis ver-
rucosus, another deepwater species, may have a
bipolar distribution since its only other known
occurrence is in the Peru-Chile trench. The three
new species may be endemic, but two of them have
sibling species in the Atlantic Ocean. Munidopsis
quadrata is only found off the west coast of North
America from Washington to Mexico. Of the five
species occurring off California and Mexico
(Schmitt 1921; Haig 1956), M. quadrata is the
only one whose range extends north to Oregon and
Washington.

This research was supported by: the Oceanog-
raphy Section, National Science Foundation, NSF
grant GB-4629; the Atomic Energy Commission,
Contracts AT (45-1)1750 and AT (45-1)2227, Task
Agreement 12; and the Office of Naval Research,
through contract NOOO 14-67-A-0369-0007 under
project NR083-102. Ship support was partially
supplied by the National Science Foundation
Grant OCE 76-00061. The ERDA publication
number is RLO-2227-T12-77.

LITERATURE CITED

ACKNOWLEDGMENTS

I am grateful to James E. McCauley and David
L. Stein for their taxonomic advice and critical
review of the paper, and to Andrew G. Carey for
providing the galatheid crabs for this study. For
loans of specimens, I thank Raymond B. Manning
of the U.S. National Museum, Herbert W. Levi of
the Museum of Comparative Zoology at Harvard
University, and Linda and Willis Pequegnat of
Texas A&M University. I appreciate Linda H.
Pequegnat's review of the manuscript. Ken
Johnson translated a French article, Gary A. Hal-
vorson translated a Russian article, and Kathy
Jefferts latinized names of the new species. My
special thanks go to Norma C. Smallbone for the
excellent drawings.

I thank the following people with pleasure for
their work at sea and in the laboratory over the
years: Mimi Alspaach Alton, Frances Bruce Pope,
Nikki Cummins, Carolyn Kuelthau Evans, Mike
Kyte, Roger Paul, Gene Ruff, and the officers and
crews of the RV Yaquina and RV Cayuse.

ALCOCK, A.

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results of the deep-sea dredging during the season 1890-
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1901. A descriptive catalogue of the Indian deep-sea Crus-
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Bahamonde, N.

1964. Dos nuevos Munidopsis en aguas Chileans (Crus-
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BENEDICT, J. E.

1902. Descriptions of a new genus and forty-six new
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Carey, A. G., Jr., and H. Heyamoto.

1972. Techniques and equipment for sampling benthic
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Carey, A. G., Jr., J. B. Rucker, and R. C. Tipper.

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32

AMBLER: SPECIES OF MUNIDOPSIS OFF OREGON

the first conference on the environmental effects of explo-
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Carney, R. S.

1976. The patterns of abundance and relative abundance
of benthic holothurians (Echinodermata: Holothuroidea)
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Chace, F. a., Jr.

1942. Rep)orts on the scientific results of the Atlantic ex-
peditions to the West Indies, under the joint auspices of
the University of Havana and Harvard University. The
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Corliss, J. B., and R, D. Ballard.

1977. Oases of life in the cold abyss. Natl. Geogr. Mag.
152:441-451.

Dickinson, J. J., and a. G. Carey, Jr.

1978. Distribution of gammarid Amphipoda (Crustacea)
on Cascadia Abyssal Plain (Oregon). Deep-Sea Res.
25:97-106.

DINKINS, S.

1969. Lanzarote the strangest Canary. Natl. Geogr.
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DOFLEIN, F., AND H. BALSS.

1913. Die Galatheiden der Deutschen tiefsee-expedi-
tion. Wiss. Ergeb. dt. Tiefsee-Exped. "Valdivia"
20:130-184.

Faxon, W.

1893. Reports on the dredging operations off the west coast
of Central America to the Galapagos, to the west coast of
Mexico, and in the Gulf of California, in charge of Alexan-
der Agassiz, carried on by the U.S. Fish Commission
Steamer "Albatross," during 1891 Lieut. -Commander Z.
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scriptions of new species of Crustacea. Bull. Mus. Comp.
Zool. 24:149-220.
1895. Reports on an exploration off the west coasts of
Mexico, Central and South America, and off the
Galapagos Islands, in charge of Alexander Agassiz, by the
U.S. Fish Commission Steamer "Albatross," during 1891,
Lieut.-Commander Z. L. Tanner, U.S.N., commanding.
XV. The stalk-eyed Crustacea. Mem. Mus. Comp. Zool.
Harv. 18:1-292.
Goodwin, d. G.

1952. Some decapod Crustacea dredged off the coast of
central California. Proc. Calif. Acad. Sci. 27:393-397.
Haedrich, R. L., G. T. Rowe, and p. T. POLLONI.

1975. Zonation and faunal composition of epibenthic popu-
lations on the continental slope south of New Eng-
land. J. Mar. Res. 33:191-212.
Haig, J.

1956. Notes on two anomuran crustaceans new to Califor-
nia waters. Bull. South. Calif. Acad. Sci. 55(2):79-82.
Hancock, d. R.

1969. Bathyal and abyssal polychaetes (Annelids) from
the central coast of Oregon. M.S. Thesis, Oregon State
Univ., Corvallis, 121 p.

Henderson, j. r.

1885. Diagnoses of the new species of Galatheida collected
during the "Challenger" expedition. Ann. Mag. Nat.
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1888. Report on the anomura collected by H.M.S. Chal-
lenger during the years 1873-76. Rep. Sci. Res. H.M.S.
Challenger, Zoology 27 (part 69):1-221.

KENSLEY, B. F.

1968. Deep sea decapod Crustacea from west of Cape Point,
South Africa. Ann. S. Afr. Mus. 50:283-323.
KHODKINA, I. V.

1973. New species of the genus Munidopsis (Decapoda,
Anomura) from the east Pacific. Zool. Zh. 52:1156-
1167.

Laird, C. E., E. G. Lewis, and P. A. Haefner, Jr.

1976. Occurrence of two galatheid crustaceans, Munida
forceps and Munidopsis bermudezi, in the Chesapeake
Bight of the western North Atlantic Ocean. Fish. Bull.,
U.S. 74:462-463.

Mayo, B. S.

1974. The systematics and distribution of the deep-sea
genus Munidopsis (Crustacea, Galatheidae) in the west-
em Atlantic Ocean. Ph.D. Thesis, Univ. Miami, Coral
Gables, 432 p.

Milne-Edwards, a.

1880. Reports on the results of dredging under the super-
vision of Alexander Agassiz , in the Gulf of Mexico, and in
the Caribbean Sea 1877, 78, '79, by the U.S. Coast Survey
Steamer "Blake," Lieut.-Commander C. D. Sigsbee,
U.S.N., and Commander J. R. Bartlett, U.S.N. , command-
ing. VIII. Etudes preliminaires sur les Crustaces. Bull.
Mus. Comp. Zool. Harv. 8:1-68.

Milne-Edwards, a., and E.-L. BOUVIER.

1894. Considerations generales sur la Famille des

Galatheides. Ann. Sci. Nat., Zool., Ser. 7, 16:191-327.
1897. Reports on the results of dredging, under the super-
vision of Alexander Agassiz, in the Gulf of Mexico (1877-
78), in the Caribbean Sea (1878-79), and along the Atlan-
tic coast of the United States (1880), by the U.S. Coast
Survey Steamer "Blake," Lieut.-Commander C. D.
Sigsbee, U.S.N. , and Commander J. R. Bartlett, U.S.N.,
commanding. XXXV. Description des Crustaces de la
famille des Galatheides recueillis pendant I'expedi-
tion. Mem. Mus. Comp. Zool. Harv. 19:1-141.

Pequegnat, L. H., and W. E. Pequegnat.

1970. Deep-sea anomurans of superfamily Galatheoidea
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biology of the Gulf of Mexico, p. 125-170. Gulf Publ. Co.,
Houston, Tex.

Pequegnat, W. E., and L. H. Pequegnat.

1971. Contributions on the biology of the Gulf of
Mexico. Texas A&M Univ. Oceanogr. Stud. 1 (suppl.),
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1973. Munidopsis albatrossae, a new species of deep-sea
Galatheidae (Decapoda, Anomura) from the eastern
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Rathbun, M. J.

1904 . Decapod crustaceans of the northwest coast of North
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SCHMITT, W. L.

1921. The marine decapod Crustacea of California with
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Zool., 23, 470 p.
SIVERTSEN, E., AND L. B. HOLTHUIS.

1956. Crustacea Decapoda (the Penaeidea and
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N. Atl. Deep-Sea Exped. 5(12):l-54.

33

SMITH, S. I.

1883. Preliminary report on the Brachyura and Anomura
dredged in deep water off the south coast of New England
by the United States Fish Commission in 1880, 1881, and

1882. Proc. U.S. Natl. Mus. 6:1-57.

1884. Report on the decapod Crustacea of the Albatross
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1883. U.S. Comm. Fish Fish., Rep. Comm. 10:345-426.

1885. On some new or little known decapod Crustacea from
recent Fish Commission dredging off the east coast of the
United States. Proc. U.S. Natl. Mus. 7:493-511.

1887. Report on the decapod Crustacea of the Albatross
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FISHERYBULLETIN:VOL.78,NO. 1

summer and autumn of 1884. U.S. Comm. Fish Fish.,
Rep. Comm. 13:605-705.
TlRMlZI, N. M.

1966. Crustacea: Galatheidae. Br. Mus. (Nat. Hist.)
John Murray Exped. 1933-34, Sci. Rep. 11:169-234.
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1874. On recent deep-sea dredging operations in the Gulf
of St. Lawrence. Am. J. Sci., Ser. 3, 7:210-219.

Wood-Mason, J.

1891. Natural history notes from H. M. Indian Marine
Survey Steamer "Investigator" Commander R. F. Hos-
kyn, R.N., commanding.— No. 21. Note on the results of
the last season's deep-sea dredging. Ann. Mag. Nat.
Hist., Ser. 6, 7:186-202.

34

USING MARKOV DECISION MODELS AND RELATED TECHNIQUES

FOR PURPOSES OTHER THAN SIMPLE OPTIMIZATION:

ANALYZING THE CONSEQUENCES OF POLICY ALTERNATIVES

ON THE MANAGEMENT OF SALMON RUNS

Roy Mendelssohn'

ABSTRACT

The mathematics of Markov decision processes and related techniques are used to analyze a model
relevant to salmon management. It is shown that the choice of grid can have a significant effect on the
results obtained. Optimal policies that maximize total expected discounted return may be too variable.
Smoothing costs are included to trade off long-run total return against the smoothness of the year-to-
year fluctuations in the allowed harvest. Simpler, approximate policies that have a smoothing effect
are also found. Preliminary analysis suggests the results are robust against misspecification of the
parameters of the model. Concepts such as maximum sustainable yield would seem to impute a very
high smoothing cost and are probably not practical for fish populations with a significant degree of
randomness.

The history of most managed natural populations
is one of sizable, nondeterministic variations in
the dynamics of the population. This observed
variation tends to have two sources: The first
source is actual randomness in the system, such as
that due to environmental variability, which will
exist no matter how accurate our models become;
and the second source is the inaccurate or incom-
plete specification of the transition probabilities
themselves. Standard production models
(Schaefer 1954; Pella and Tomlinson 1969; Fox
1970, 1971, 1975) assume deterministic dynamics,
as do most recent bioeconomic analyses, as in
Clark (1976) or Anderson (1977). For randomly
varying populations, at best only extremely low
harvests may be sustainable year to year, and it is
not difficult to develop realistic scenarios where
policies that are sustainable in a deterministic
model would cause possible depletion in a stochas-
tic model.

In this paper, the latest tools from stochastic
optimization, particularly in the area of Markov
decision problems (MDFs) are used to analyze a
model relevant to salmon management. The view-
point taken is that of the analyst, who must
analyze trade offs and provide a decision maker
with as few policies as possible that contain the

'Southwest Fisheries Center Honolulu Laboratory, National
Marine Fisheries Service, NOAA, Honolulu, HI 96812.

maximum amount of information, rather than
that of the decision maker, who ultimately decides
if a particular concern or trade off is worthwhile.
The salmon model is used as an example — the goal
is to gain insight into managing randomly varying
populations.

Ricker (1958) appears to be the first to examine
the effects of variability on management. He used
intuition and simulation to arrive at policies that
are of the same general form as many of the
policies to be discussed in this paper. However,
Ricker presented no systematic way of developing
optimal policies and made the incorrect assump-
tion that the long-run stochastic behavior will
have a mean equal to the deterministic equilib-
rium yield, with noise around this mean.

Reed ( 1974) derived qualitative properties of op-
timal policies if the random variable has a mean of
1, if it affects the population dynamics in a multi-
plicative manner, and if it has costs when the
system is shut down (no harvesting) and then
started up again (resumption of harvesting).
Reed's results are not relevant to the model dis-
cussed in this paper, since he assumed the deter-
ministic population model is concave, while the
models examined in what follows are pseudocon-
cave. A more complete treatment of one dimen-
sional stochastic growth models can be found in
Mendelssohn and Sobel (in press).

Walters (1975) and Walters and Hilborn (1976,
1978) discussed a variety of topics as the concerns

Manuscript accepted September 1979.
FISHERY BULLETIN: VOL. 78, NO. 1, 1980.

35

FISHERY BULLETIN: VOL 78, NO. 1

jf this paper. Some of the techniques they dis-
cussed, particularly the filtering techniques (Wal-
ters and Hilborn 1978), are only appropriate if the
model has an additive error term. While a Ricker
spawner-recruit curve can be transformed to an
additive model, many models do not have this fea-
ture.

I am presenting what I feel is an improved way
to smooth out the fluctuations in the year-to-year
harvests as compared with the method suggested
in Walters (1975) and show that the Bayesian
(adaptive) model discussed in Walters and Hilborn
(1976) has an optimal policy with a very simple
form that can be readily calculated.

Moreover, a rigorous approach is taken to define
the model on a grid and the effects of the grid
choice. None of the papers cited deal with this
important question; new results are presented
which show that the most serious effect of the grid
is on the estimates of the long-run (ergodic) prob-
abilities of the population dynamics when follow-
ing a given policy. Particularly the tail properties
of the ergodic distribution, i.e., the long-run prob-
ability of low harvest or low population sizes, are
misestimated. This is a new finding even in the
MDP literature, and has numerical implications,
particularly when calculating the trade off be-
tween the mean harvest of a given policy and the
long-run probability of undesirable events when
following that policy.

THE MODEL

The models to be analyzed were developed by
Mathews (1967) to describe the spawner-recruit
relationships of sockeye salmon, Oncorhynchus
nerka, populations in two rivers that run into Bris-
tol Bay, Alaska. Oceanographic and other factors
affect the number of recruits to a degree where the
relationships can be modeled by the random equa-
tions:

Wood River:

x,^j = expid) (4.077y,) exp(-0.800y,)
d-N(0, 0.2098)

1.1a)

Branch River:

jc^^ = exp(c?) (4.554y,) exp( -1.845y, )
d^N (0,0. 3352)

(1.1b)

where y, is thenumber of spawTiers in period ^ x, + 1
is the (random) number of recruits in period ^4-1,
and d~N{a, b) denotes that <i is a normally dis-

36

tributed random variable, with mean a and var-
iance b.

For deterministic versions of Equation (1.1), the
primary objective of management is MSY
(maximum sustainable yield), which is equivalent
to the largest per period growth of the determinis-
tic model. The stochastic equivalent of this criteri-
on is to maximize the average per period harvest,
or gain optimality. Mathematically, letting E be
the expectation operator, this is

max lim

1 T
T ^ t=i

(xt-y't)

(1.2a)

However, for many decision making situations,
total expected discounted harvest may be a prefer-
able criterion, since a discount factor can repre-
sent a measure of risk or uncertainty about the
system, over and above the variability due to the
random variable d. More formally, if a is a dis-
count factor 0^a<l, the problem is to:

maximize E

^ a'^ip(x,-y,)

t=i

(1.2b)

subject to O^y^^Xf-, and Equation (1.1)

where p is a weighting factor, which could be 1 or
could represent the average weight of the salmon
harvested.

All the results in this paper are for expected
discounted return with « = 0.97. For a = 1, Equa-
tion (1.2a) must be used, since Equation (1.2b) is
infinite for most policies. The choice of a = 0.97 is
arbitrary, though numerical runs for a ranging
from 0.95 to 1.00 produced no significant changes
in the results. When actually implementing a
model, a careful choice of a must be made, and the
sensitivity of the results to changes in the value of
a should be tested. It should be mentioned that a =
1 is just as much a discount factor as any other
value and implies certain temporal preferences
and attitudes towards risk that may not
adequately reflect the decision maker's prefer-
ences.

The shortcomings of Equation (1.1a) or (1.1b)
should also be noted, such as no account is taken of
ocean harvesting of the salmon, particularly by a
foreign nation. This just reinforces the idea that
the purpose of this analysis is not optimization per

MENDELSSOHN: USING MARKOV DECISION MODELS

se, but rather to provide the decision maker with
added insight and reasonable first choices.

Defining the Model on
a Discrete Grid

In order to make Equation (1.2) amenable to
numerical methods, it is necessary to define both
the state space and the action space on a discrete
grid, and then to redefine the transition prob-
abilities, etc., on this grid. Several authors (Fox
1973; Bertsekas 1976; Hinderer 1978; Waldmann
1978; Whitt 1978; Larraneta^) have suggested
techniques to reduce MDP's to a grid and give
bounds on the error due to the approximation. I
have shown elsewhere (Mendelssohn^) that grid
choice can have a significant effect on the analysis.
An optimal policy and the value of an optimal
policy may not be greatlj' affected by the choice of
grid, but the estimated probabilistic behavior of
the population dynamics is affected significantly
by the choice of grid.

A first effort then is to find an adequate grid for
the problem, a grid fine enough for both the de-
sired accuracy and for realistic approximations of
observed population sizes and coarse enough for
computational efficiency. Increased computa-
tional efficiency makes it reasonable to solve
many variations of a given model, which allows for
a more thorough exploration of the management
questions of interest and their sensitivity to key
assumptions.

Several different grids were tried for Equation
(1.2) for both the Branch and Wood Rivers.

To defin e Equation ( 1 .2 ) on a given grid, suppose
a grid of k points has been chosen on which to
discretize the problem and assume, as is reason-
able for this problem, that the reduced action
space (how many spawners to leave) is equivalent
to the state space (how many recruits are observed
at the beginning of the period). From Equation
(1.1), letting /?j and /?2 represent the parameters
of the Ricker equation

P(jc,^i<w|y,) = P[(e^)/?iy,exp(-i?2y<)<w]

= P(d<lnco-lna)

(2.1)

^Larraneta, J. C. 1978. Approaches to approximate Mar-
kov decision processes. Paper presented at Joint National
ORSA/TIMS Meeting, Nov. 13-15, 1978, Los Ang., Calif.

^Mendelssohn, R. 1978. Theeffectsof grid size and approx-
imation techniques on the solutions of Markov decision prob-

where a = [R^y^expi-R 2y, )]. Let ^ be the sj;andard
normal integral for a random variable d = did,
and let x,, x^^ be any two adjacent points on the
grid. Then:

P(d<\nxi-\na) = (I>|

In Xi — In a

a

P(d<Inx,-+i -In a) = ^\

'In jc,+i —In a

o

so that one method of defining the transition prob-
abilities on a grid is:

P{xt^\ = x,+ i \yt) = ^\

'in Xi+i —In a

d,!

a

\nxi —In a

a

The discrete probability when the action is y^ is
equal to the total probability of going to any state
in the interval (jc„ x, + j).

If zero is included as a state, the procedure needs
to be modified slightly. Suppose the probability of
going to Xj is known for each decision _y. Then an
arbitrary fraction of this probability is assigned as
going to the zero state. In this paper, one-half of
the probability in the interval (Q,x^) is assigned to
the zero state. The results have been found not to
be sensitive to the value of the fraction; this is
because zero is an absorbing state. Either there
exists a policy that never reaches (0,a;i) and hence
never reaches zero, or else with probability one the
population goes to zero in finite time. Hence, it is
the size of (0,x^) that most influences the results,
not the fraction of this total that is assigned to
going to the absorbing state.

Adding an absorbing state is sensible if the ab-
sorbing state is thought of as all states at low
enough population levels such that it would take
years for the fishery to recover again, if it recovers
at all. Without the absorbing state, the models in
Equation (1.1a, b) will always recover in fairly
short order. Since fisheries can be depleted, the

lems. SWFC Admin. Rep. 20H, 15 p. Southwest Fish. Cent.
Honolulu Lab., Natl. Mar. Fish. Serv. NOAA, Honolulu, HI
96812.

37

FISHERY BULLETIN: VOL. 78, NO. 1

inclusion of an absorbing state would seem to be a
more realistic assumption. It is included in what
follows.

A coarser grid implies, in a sense, less informa-
tion about the state of the system. As the interval
(0, Xj) becomes large, our information has de-
creased about the true state of the population and
this increased uncertainty is reflected in increased
risk of absorbtion. Similarly, a finer grid implies
more exact information — a grid should not be used
which is finer than the precision of the estimate of
the population size.

Optimal policies for grids of 16, 26, 51, 101, and
501 equally spaced points (including zero) for both
rivers are shown in Table 1. The optimal equilib-
rium population for the equivalent deterministic
models are shown also. All numbers are in units of
millions offish.

The optimal policies are all of the base stock
variety, i.e. it is optimal to harvest to a fixed
number of spawners, or else not to harvest at all. If
the 501-point grid is taken as the standard, it can
be seen that each coarser grid has as its base stock
size the grid point closest to the base stock size for
the 501-point grid.

Figure 1 gives the long-run (ergodic) cumula-
tive distribution of being in any state when follow-
ing an optimal policy on grids of 16, 26, 51, and 101
points. Grid size can be seen to play a crucial part
in estimating the probabilistic behavior of the
population. For the Wood River, extinction with
probability one is predicted on grids of 16 and 26
points, while the probability is zero on grids of 51
and 101 points, so long as zero is not the initial
state. Similar but not identical results are valid
for the Branch River. It should be emphasized that
for a = 1, i.e., when the objective is given by Equa-
tion (1.2a), the estimated average per period har-
vest of any policy depends entirely on the ergodic
distribution that arises from that policy. There-
fore, this variation in estimated long-run behavior
due to changes in grid size is nontrivial.

Probability one of extinction occurs because for
a finite state, irreducible Markov chain with an
absorbing state, the absorbing state is reached in

Table l. — Optimal policies for the different grid sizes.

Wood River

Grid size

Branch River

Vf = min {x,. 0.9333)
Vj = min (xj, 0.840)
/( = min (x^, 0.700)
Yf = min (Xj, 0.770)
/f = min (Xf, 0.742)

Equilibrium stock 0.735

16

26

51

101

501

Deterministic

y, = min (x^, 0.3333)
y = min (x^, 0.4000)
y = min (x,, 0.3000)
y = min (x,, 0.3500)
y = min (Xj, 0.3500)

Equilitxium stock 0.345

STATE (WOOD RIVER)

2 3

STATE (BRANCH RIVER)

Figure l. — Ergodic cumulative distributions for optimal har-
vesting strategies on grid sizes of 16, 26, 51, and 101 points for
the Wood River and the Branch River.

finite time with probability one. However, for the
larger grids, there exist policies that are reducible,
in the sense that if the chain does not start in the
interval (0, x^), it will never enter that interval.
Since P[jC;e(0,Xj )] = 0, and a fraction of this proba-
bility has been assigned to the zero state, then P(jc,
= 0) = 0. When using the smaller grids that induce
Markov chains that are irreducible, the estimated
time till absorption varies greatly also. For exam-
ple, for the Branch River, ifP(Xi = 0) = 0 andP(Xj
= w) = 1/{N-1), where w is a grid point and A^ is
the number of states, then a 16-point grid predicts
absorption with probability one after 2,000 itera-
tions, the 26-point grid predicts only a 76% chance
of absorbtion after 2,000 iterations, and the 51-
point grid predicts only a 17% chance of absorp-
tion.

When maximizing total expected discounted re-
turn, the discounted mean return depends on the
values of these intermediate probability distribu-
tions, so that coarser grids can be expected to un-
derestimate the long-run value of the harvest.

Finally, for the Wood River, note that the 51-
and 101-point grids have similar long-run be-
havior. These results suggest that in order to find

38

MENDELSSOHN: USING MARKOV DECISION MODELS

good policies, it is only necessary to use a grid size
of 26 to 51 points for the problems under consider-
ation. However, to analyze the long-run (prob-
abilistic) behavior of a given policy, it is necessary
to use a grid containing no fewer than 100 points.
It should be reemphasized that the reason for
considering a coarser grid is that a smaller prob-
lem size allows for many problems to be solved at a
small cost. This is desirable to obtain insight into
the sensitivity of the problem. However, it is pos-
sible to solve quite large problems, making use of a
variety of methods to accelerate computations (see
for example Porteus 1971; Hastings and van
Nunen 1977). For example, the 501-point grid for
the Branch River used 1.80 s of CPU (central pro-
cessing unit) time to perform the optimization.
Computations, when smoothing costs are included
(see Policy Analysis section), have 2,601 states.
These used about 5 to 6 min of CPU time to per-
form the computations, but at a cost of about $20.
Our experience is that it is possible to obtain
reasonable estimates using coarse grids and that
this suffices for initial policy investigation. How-
ever, it is worthwhile to reanalyze the final two or
three problems of greatest interest on a finer grid.

POLICY ANALYSIS

For the Wood River, the optimal policy for Equa-
tion (1.2) is given by

y^ = minimum (0.770, x^)

and it produces a mean per period harvest of
1 . 14758, and a standard deviation in the harvest of
0.8963. The median harvest is 0.91, and no harvest
occurs roughly 4.3% of the time. A harvest of 25%
or less of the mean harvest occurs roughly 15% of
the time, while a harvest greater than the mean
harvest occurs approximately 38% of the time.

Similarly, for the Branch River, an optimal pol-
icy for Equation (1.2) is given by

y^ = minimum (0.300, x,)

and it produces a mean per period harvest of
0.6622, and a standard deviation in the harvest of
0.6120. The median harvest is roughly 0.500;
there is a 3.9% chance of no harvest. A harvest of
25% of the mean harvest or less occurs roughly
14.5% of the time, and a harvest greater than the
mean harvest occurs approximately 61% of the
time.

While these policies are similar in form to
policies that are optimal for a deterministic ver-
sion of Equation (1.2), they differ greatly in the
year-to-year dynamics. There are two ways of
finding the optimal deterministic policy. The first
way is to assume a general model of the form:

Xt+i ^ Riyisxpi-Rzyi)

The second method is to assume a general model of
the form:

a:, ^ J =E exp {d)R^y^ exp (-R^ y^ )

where as before, R^ and R^ are the parameters of
the Ricker equation. The second method is prefer-
able since it uses all the information available. As
disa. normal random variable with mean zero and
variance cr^, it is easy to show that exp((i) is a
lognormal random variable with expectation exp
{V2. 0-2). Solving for the optimum sustained yield
(OSY) population size for each river gives:

Wood River

Branch River

^OSY

0.735

0.345

OSY

1.11346

0.63804

Both OSY values are lower than the mean per
period harvests in the stochastic models, but the
variation is too high to allow this amount to be
harvested each year. However, the Xq^y level is a
good estimate of the base stock size, and it is
known a priori from Mendelssohn and Sobel (in
press) that a base stock policy is optimal.

In the deterministic model, oncexQgy is reached,
both the population size and the harvest size are
maintained at steady, equilibrium levels. An op-
timal policy for the stochastic model, however,
produces large fluctuations in both and may allow
no harvesting 1 yr out of 25 in the long run. For
many fisheries, these "boom and bust" conditions
may not be acceptable. Many people, especially
those with interest or mortgage payments, as are
many fishermen, are concerned about smoothness
of income received as well as the total amount
received. The final decision on the acceptable
amount of fluctuation is, of course, up to the deci-
sion maker with appropriate input.

There are several methods available to try to
find a balance between the smoothness of the ran-
dom income stream and its total discounted ex-
pected value. Walters (1975) and Walters and Hil-
born (1978) suggested fixing a given mean harvest

39

FISHERY BULLETIN: VOL 78, NO. 1

u, and then finding a policy that minimizes

'^ This methodology de-

lim

e\; k^ {Zt-uY

pends on the values of u chosen. It also determines
the policy that minimizes the approximate long-
run variance for a given long-run mean harvest.
This is not equivalent to reducing the size of the
year-to-year fluctuations.

A second method is to include "smoothing costs"
into the one-period return. This approach has been
studied analytically by Mendelssohn.'* Let y be the
cost of a unit decrease in the harvest from year to
year, and let e be the cost of a unit increase in the
harvest from year to year.

If 2 was harvested last year, then net revenues
this year, for any harvest 2, , are decreased by

1(2 -Zt)

0

e{Zt-z)

if 2 >2^

Z <2i

Amended to Equation (1.2), this would imply a
one-period net benefit of

pix^ - y^) - y[z - (x^ - yi)V - e[(x^ - y^) -zV

where (a)^ denotes the positive part of a. An alter-
nate form is to let e = (y-e)/2andc = (y+e)/2.Then
the one-period return is:

pix^ -y^) + e(x^-y^)-c\{Xf-yi)-z\ - ez.

One advantage to the smoothing cost approach
over other approaches is that p, e, and c can be
normalized so as to be interpreted as relative
prices. That is, the normalized values p - 1, elp,
and dp can be interpreted as the value of having
the between period harvest "smoothed" by one unit
relative to the value of one unit of additional har-
vest. Actual relative values are often difficult to
determine. But by parameterizing on e and c, it is
possible to present a decision maker not only a
range of possible "optimal" policies and their con-
sequences, but also some feeling for the relative

■•Mendelssohn, R. 1976. Harvesting with smoothing
costs. SWFC Admin. Rep. 9H, 26 p. Southwest Fish. Cent.
Honolulu Lab.. Natl. Mar. Fish, Serv., NOAA, Honolulu, HI
96812.

trade off between total income and the smoothness
of the received income stream.

For the Wood and Branch Rivers, two sets of
computations were performed. The first set as-
sumes that y = e, i.e., there is an equal concern for
increases in allowable harvest as well as for de-
creases. This is equivalent to e = 0.0 and c = y (or
equivalently e). The motivation for this cost struc-
ture is that fishermen typically resist any decrease
in the allowed harvest, hence y>0. However, al-
lowing increases in the harvest size often signals
fishermen to gear up and invest in equipment,
thereby making it even more difficult to decrease
the allowable harvest later on. Therefore this cost
should be equal to a cost due to a decrease in the
harvest.

As a counterbalance to this, a second set of com-
putations were performed with y>0 but e = 0, i.e.,
a cost only if the harvest is decreased. This is
equivalent toe = e = y/2.

For the first set of computations, with e = 0.0
andp = 1.0, values of c of 0.25, 0.50, 0.75, 1.00,
1.25, 1.50, 1.75, and 2.00 were used. These are
equivalent to relative values of Vs, V4, %, ¥2, %, %,
■%, and 1. For the second set of runs, withe = e, and
p = 1.0, values of 0.25, 0.50, 0.75, 1.00 and 1.25
were used. These are equivalent to a ratio of yip
equal to Va, V2, %, 1, VA. The results are sum-
marized in Figure 2(a)-(m) and Figure 3(a)-(m),
which show an optimal policy for each river for
each of these cases. All computations were per-
formed on 26-point grids.

The figures are read as follows. Suppose 2 was
harvested last year and x is the observed popula-
tion size this period. Find the point {x, z) on the
graph and follow the arrow in that zone to the
appropriate boundary as indicated. Then read off
the 2 value of this point; this is the optimal amount
to harvest during this period.

For example, if e = 0.50, e = 0.00, x^ = 0.84, and
the harvest last period was 0.28, Figure 2(b) shows
that the optimal policy for the Wood River is to
harvest 0.28 this period. Note that the dashed line
is the equivalent base stock harvest with no
smoothing costs.

While the policies in Figures 2 and 3 are optimal
for the given relative values of p, e, and c, they are
complex in nature and would be difficult for a
layperson to understand. Practical management
often implies determining simpler, good but sub-
optimal policies that achieve the same objectives.
These policies are often more desirable since they

40

MENDELSSOHN: USING MARKOV DECISION MODELS

are easier to implement and easier to explain the
rationale to the public.

As an example of suboptimal, approximate
policies, the following nine modified base stock
policies were examined:

3) Policy of base stock size of 0.56 till 1.40, then a
base stock size of 0.84.

4) Harvest 0 till 0.28, harvest 0.28 till 0.84, a base
stock size of 0.56 till 2.52, then a base stock size
of 0.84.

Wood River

Branch River

1) Base stock policy, base stock size = 0.84.

2) Policy of base stock size of 0.56 till 2.52, then a
base stock size of 0.84.

5) Base stock policy, base stock size of 0.40.

6) Base stock size of 0.4 till 1.6, then a base stock
size of 0.6.

Figure 2(a-m). — Optimal policy functions for the Wood River for various assumptions about the relative value of smoothing costs. (See

text for details).

41

FISHERY BULLETIN: VOL. 78, NO. 1

7) Base stock size of 0.2 till 0.6, then a base stock
size of 0.4.

8) Base stock size of 0.2 till 1.0, then a base stock
size of 0.4.

9) Base stock size of 0.2 till 0.4, base stock size of
0.4 till 1.2, base stock size of 0.6 after that.

These nine approximate policies were devised
by examining the functions that define the three
regions in Figures 2 and 3. These approximate the
boundaries of the three regions where the smooth-

ing costs are one-fourth to one-half the per unit
value of the harvest. The mean per period harvest,
variance, standard deviation, median per period
harvest, etc. for these nine policies are given in
Table 2.

Policies 3 and 4 for the Wood River and 8 and 9
for the Branch River demonstrate how these ap-
proximate policies tend toward smoothing
policies. For example, policy 4 has the same me-
dian harvest as the optimal base stock harvest,
almost never closes the fishery, significantly de-

,56 1.12 1.68 2.24 2.80 3.36 3.92 4.48 5.04 5.60 6.16 6.72 0 .56 1.12 1.68 2 24 2.80 3.36 3.92 4.48 5.04 5.60 6.16 6.72

Figure 2.— Continued.
42

MENDELSSOHN. USING MARKOV DECISION MODELS

creases the percent of time there are low catches,
and only reduces the mean per period harvest by
33,800 fish. In order to achieve a smoother catch,
"potlatch" harvests from time to time have been
sacrificed.

When looked at closely, these policies are actu-
ally very intuitive and represent an interesting
variant of a base stock policy. These policies re-
place a single base stock size by a dual base stock
size policy. The first base stock size is lower than
the original one, while the second base stock size is

greater than or equal to the original base stock
size. This means that there are fewer states where
there is no harvesting, but also lowers the likeli-
hood of the really big harvests. The mean per period
harvest tends to be very sensitive to these big
harvests, while the median is not, particularly
since the very large harvests are not too frequent.
It is curious that the population dynamics are so
sensitive to such fine tuning, for the difference
between policy 1 and policy 3, say, is quite mar-
ginal. It would be an interesting area of future

0 .56 112 1.68 224 2.80 336 3.92 4.48 5.04 5.60 6.16 6.72 0 .56 1.12 1.68 2.24 2.80 3.36 3.92 4.48 504 5.60 6.16 6.72

X X

Figure 2.— Continued.

43

FISHERY BULLETIN: VOL. 78, NO. 1

672

-

1 1 1 1

I 1 ' 1

1 1 1

6.16

-

(m) C»E« 1.25

7
/

/

5.60

/

5.04

"

/
/

4.48

-

'

/
/

3.92

-

/

/

o

3 36

-

I

/
/

?

2.80

-

/ c n

/ -

2.24

-

X

1.68

_

//

/

-

1.12

[—

/ ■' ^

/

/

^'

\

m

56

/Sr

0

^.Z.

■•'1 1 1 :

1 1 1 1

1 1 I

0 .56 1.12 168 2.24 2.80 3 36 3.92 4 48 5.04 5,60 616 672

X
Figure 2.— Continued.

research to determine guidelines for when fine
tuning would be expected to produce such "trim-
ming" of the tails of the ergodic (long-run probabil-
ity) distribution.

Including smoothing costs also tells us a great
deal about traditional concepts of fisheries man-
agement, such as MSY. It is clear from Figures 2
and 3 that anything close to an MSY policy is
optimal only if the smoothing costs exceed the per
unit value of the harvest. As whole systems of laws
for regulating fisheries have been constructed
around the idea of smooth, constant harvests, it is
clear that this imputes lower average catches, and
a significant preference for constancy of the har-
vest over total amount harvested.

The analysis has assumed that Equation (1.1) or
similar equations are available, and that the
parameter estimates are accurate (in this case,
estimates of R^, R^, and cr^). In the latter case,
management measures would seem more reason-

able if they were known to be robust against mis-
specifying the parameters. This involves knowing
how an optimal policy and total expected value
would vary if the true underlying parameter val-
ues differ from those specified, and also how the
estimate of the long-run probability distribution
differs from the true one.

Walters and Hilbom (1976) have examined a
similar question of trying to solve the Bayes model
of this problem, i.e., where there is an original
prior probability given to each value of the
parameter, and this probability is updated each
period using Bayes theorem and the observed val-
ues during the period. However, they could not
obtain a solution, and Walters and Hilborn ( 1978)
raised questions as to the validity of some of their
numerical approximations.

Fortunately, qualitative results are possible for
this particular class of Bayes problems. Let 6 be
the parameter (or vector of parameters) under
consideration. Let q^iQ) be the initial prior dis-
tribution on 6, and let q^ ( B) be the updated prior
distribution after n period has elapsed. Let Cl be
the set of all possible prior distributions. Then it is
proven in van Hee (1977a) that if the state of the
system is expanded to {Xf,q^), the resulting optimi-
zation problem is Markovian. Following argu-
ments similar to those in Scarf (1959) and van Hee
(1977a) it follows that an optimal Bayes policy
takes the form:

For each element q e Ci, there is an x{q) such
that:

do not harvest ifx^^xiq)

harvest x^ - x{q) ifXf>x(q).

For example, if cr^ in the distribution of c? is itself a
random variable, then each possible probability
distribution of cr^ yields a possibly unique base
stock size policy.

Table 2. — Vital statistics for the nine policies approximating the smoothing cost policies for Wood and Branch Rivers.

Mean per

Variance of

% time

% time

period

per period

Standard

% time

less than

greater than

Median

Relative value:

River

Policy

harvest

harvest

deviation

no catch

25% of mean

mean catch

catch

smoothingprice

Wood

1

1.1357

0.8468

09202

5.6

16.8

39

0.98

0/1

2

1.0993

05460

0.7389

1.7

10.7

39.8

0.98

1/8

3

1.1203

0.6506

08066

1.1

7.7

43.2

0.91

1/4

4

1.1019

0.5758

07588

002

10.47

40

0.98

1/2

Branch

5

0.6528

0.3982

0.6310

9.2

21.8

40

0.500

0/1

6

0.6290

02532

0.5032

9.1

21.5

37.2

0.500

1/4

7

0.6272

0.3077

0.5547

1.2

27.7

31.3

0.400

1/2

8

0.5920

0.2202

0.4693

1.9

35.7

26.3

0.500

3/8

9

0.5995

0.3038

0.5512

0 72

22.83

39.3

0.500

3/4

44

MENDELSSOHN: USING MARKOV DECISION MODELS

Van Hee (1977a) defined a set of policies that he
terms Bayes equivalent policies. For problems
such as the salmon models under discussion, a
Bayes equivalent policy would be found as follows:

1) At the start of the period, the prior probability
distribution is q^( B).

2) The expected transition function (expectation
with respect to O) is calculated, i.e.,

p(d,q) = jp(d\e)q(de)

(4.1)

where p( • | • ) describes the dependence of the ran-
dom variable d on O.

3 )p(d,q) is used to solve a non-Bayesian Markov
decision process, with p{d, q) as the transition
function.

4)The optimal policy from step 3 above is used
for one period.

5) q-l O) is updated using Bayes theorem and the
observations from the last period, and the updated
(?( • ) is used in step 1 at the next time period.

It is worth noting that a Bayes eqivalent policy

8 1.2 1.6 2.0 2.4 2.8 3.2 3.6 4.0 44 4.8

X

Figure 3(a-m). — Optimal policy functions for the Branch River for various assumptions about the relative value of smoothing costs.

(See text for details.)

45

FISHERY BULLETIN: VOL. 78, NO. 1

is adaptive, as the prior distribution is updated
each period. Moreover, it is not the same as fixing
9 at its estimated value, and using a fixed value of
6 in step 3. The difference can be seen in the
integral in Equation (4.1). The reason for consider-
ing Bayes equivalent policies is that van Hee
(1977a, theorem 3.1) proved that for the models
under discussion, when the objective is given by
Equation (1.2a) or (1.2b), then the Bayes equiva-
lent policy is optimal for the full Bayes model. For
example, in Walters and Hilborn (1976), the

parameter 6 is a scalar, i.e., flg ^^ our notation.
Their problem, for which an optimal policy was not
found, can be solved by following a policy outlined
in the five steps above.

Many models will not have the necessary struc-
ture for a Bayes equivalent policy to be optimal for
the full Bayes model, and unlike salmon manage-
ment, estimates of the population size may not be
available every year. A legitimate question is:
suppose the present best estimate of B were to be
used from hereafter. What would be the loss in

MENDELSSOHN: USING MARKOV DECISION MODELS

expected value? Van Hee ( 1977b) gave bounds on
this expected loss that are easy to compute. To
obtain a feel for these bounds, both (r'^ and R^ are
assumed to be random variables. For the Wood
River, /?2 could take on the values -0.6, -0.8 and
-1.0, and for the Branch River R^ could take on the
values -1.5, -1.85, and -2.00. For the Wood River, 0-2
could assume the values of 0.35, 0.45, and 0.55,
and for the Branch River a^ could assume the
values 0.48, 0.58, and 0.68. Three probability dis-
tributions were used as the present prior probabil-

ity of the parameter values. These were (%, Vs, Va,),
(1/4, V2, 1/4), (Vs, %, Vs). The results of the optimiza-
tion using the parameters at each fixed value
(which are needed to calculate the bounds) are
given in Table 3. Table 4 gives the bounds on the
expected loss of value from using the present esti-
mates of the parameters as in Equation (1.1).

Table 3 suggests that as cr^ varies for fixed val-
ues of /?j , /?2 ' the mean per period harvest varies
little, but the variance of the long-term harvest
size distribution increases significantly. As i?2

4.8

-

1 I 1 1 1 1 1 1 1 1 I

44

-

(i) C = E = 0.25 /:

/

4.0

-

/
/

/

3.6

-

/

/

3.2

-

/
/

-

2.8

_

'

/

_

/

24

-

I /
/

-

2.0

-

/

.

1.6

-

/
/

-

1.2

_

/
/

ffl

/

.8

-

/

/

-

4

—

/
/

/
/ 1

1 I i ' ! 1

4.8

-

1

11:11

1 ; 1 1 1

44

-

(J)

C = E = 0.50

/_
/ /
/ /

4.0

/ / -
/ /
/ /

3.6

-

/ /

/ /

3.2

-

/ /

'

2.8

-

/ /
/ /

-

?4

■A

/ /

?0

I

/

'/

^ /

'&/

1.6

-

.

//

-

/ /

1.2

-

/-—^

m

/

.8

-

A
/

/

-

.4

"

^'

-

n

_ ^

Av

i 1 1 1 1

1 1 1 1 1

"1 r

1 r

(k) C = E = 0.75

J I L

"I r

"1 r

"1 r

(I) C=E = I.OO

J I I L

0 4 .8 12 1.6 2.0 2.4 2.8 3.2 3.6 4.0 4.4 4.8 0 4 8 1.2 1.6 2.0 2.4 2.8 3.2 3.6 40 44 4.8

X X

Figure 3.— Continued.

47

FISHERY BULLETIN: VOL. 78, NO. 1

0 4 .8 1.2 1.6 2.0 2 4 2.8 3.2 3.6 4.0 4.1 4.8

X
Figure 3.— Continued.

varies for fixed values ofi?i , cr^, both the mean and
the variance vary significantly. Table 4 reinforces
this impression to a degree. If the mean per period
harvest does not vary significantly with changes
in the value of cr^, it might be expected that the
present estimate of a^ will suffice. This is borne
out by Table 4, where the bounds on the maximum
expected total loss is <0.01, which is <1% of the
optimal Bayes expected value.

Some significant expected loss in value wheni?2
varies is seen, but the loss is less than might be
expected from Table 3. The values in Table 4 when
i?2 varies are all <4% of the true value. These
results suggest that if Equation (1.1) is the correct
form of the model, and the present parameter es-

timates have relatively small variance, then little
is gained in expected value if the more complicated
policy is used. The same may not be true if the
population size is unobserved.

All of these results suggest a model that is fairly
robust to our lack of understanding of nature. A
possible explanation for this can be made from the
discussion on the effect of grid size. As long as
there is some cutoff population size below which no
harvesting is allowed, and this cutoff assures that
the absorbing state cannot be reached with proba-
bility one, then our management can only damage
the stocks to a degree.

All of the policies examined in this paper have
such a minimum cutoff. The rest of the policy will
determine the relative mean and variance of the
harvest, and techniques are presented to examine
these features in detail. Uncertainty about the
values of the parameters will affect the total re-
turn, but present estimates often can give a satis-
factory approximation. The truly risk adverse de-
cision maker can use present estimates of the
parameters that are weighted to be on the cautious
side.

SUMMARY

Uncertainty in fisheries management can be
faced head on. Techniques exist that allow us to
gain much insight on managing randomly varying
populations. Optimization procedures allow us to
reduce our attention to the few best policies, and to
analyze their properties, rather than to pick
policies ad hoc that meet no special criteria.

Optimization under uncertainty can also lead to
a reconsideration of what is valued in managing a

Table 3. — ^Trials with varied parameters.

Rrver

Value CJf fl2

Value of (7

Optimal policy

Mean per
penod harvest

Variance

% time
no harvest

Wood

Wood

Wood

Wood

Branch

Branch

Branch

Branch

0.800

0.35

min (X(, 0.7)

1.0680

0390976

0.79

0.800

0.55

min (Xf, 0.77)

1.2267

1 .2422

7.8

0.600

0.458

mm (x,, 0.980)

1.5108

1.3136

3.8

1.000

0.458

mm (x,. 0.560)

0.9225

0.4839

3.29

1.845

048

mm (Xf. 0.35)

06122

02253

3.54

1.845

0.68

mm (Xf. 0.35)

—

—

—

1.500

0.579

mm (X,, 0-40)

1.989

0.5254

582

2.000

0.579

mm (xf, 0.30)

0.9075

0.3068

5.82

Table 4.

-Largest possible deviation in value of the approximate policy compared with the

true Bayes policy.

Probability
distribution

When Ri is uncertain

When (T is uncertain

1/3, V3, Va

y4,V2,'/4 V8,%,y8

Vj, V3, V3

Vo. V2. Va

Ve, %, Va

Wood River
Branch River

1.4
1.04

0.51 0.5
0.47 0.38

0.04
0.01

0.03
«0.01

0.03
S0.01

48

MENDELSSOHN: USING MARKOV DECISION MODELS

fishery — in the examples considered, some consis-
tency in the amount harvested is a desirable al-
ternative to high year-to-year fluctuations in the
harvest size. But this reduced the average per
period catch. Only in extreme situations, where
the cost of smoothing out the catch is greater than
the unit value of the catch, does any policy re-
sembling MSY become optimal.

Finally, it is possible to obtain an understand-
ing of how robust the management measures are
to misspecifications of the underlying model. This
is important, since the model is only a guide to our
decision making, not the answer. In the models
considered, the "best" policies are robust in view of
this uncertainty.

A question not examined is the assumption that
the population size is observed at the start of each
period. This too is usually costly, and inexact. Re-
cently, I and E. J. Sondik developed an efficient
algorithm that addresses the relative merits of
different sampling intervals for obtaining popula-
tion estimates.^ Together, all of these techniques
allow for an integrated, realistic approach to man-
agement under uncertainty.

ACKNOWLEDGMENTS

Debra Chow provided invaluable assistance in
programming the computer runs. David
Stoutemeyer of the University of Hawaii gave
much useful advice on maximizing the efficiency
of the optimization algorithm used. Lee Anderson,
George Fishman, and Adi Ben-Israel gave impor-
tant comments for improving an earlier version of
this paper. The paper also benefited greatly from
the comments of one of the referees and from C.
Walters who tempered some remarks in a previous
version.

LITERATURE CITED

ANDERSON, L. G.

1977. The economics of fisheries management. The
Johns Hopkins Univ. Press, Baltimore, 214 p.
Bertsekas, D. p.

1976. Dynamic programming and stochastic con-
trol Acad. Press, NY., 396 p.

Clark, C. W.

1976. Mathematical bioeconomics: The optimal manage-

^Mendelssohn, R., and E. J. Sondik. 1979. The cost of in-
formation seeking in the optimal management of random re-
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49

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FISHERY BULLETIN: VOL. 78, NO. 1

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50

ORGANOCHLORINE RESIDUES IN FISHES FROM
THE NORTHWEST ATLANTIC OCEAN AND GULF OF MEXICO

Virginia F. Stouts

ABSTRACT

Residues of SDDT (p,p -DDT and its metabolites p,p -TDE and p,p -DDE), PCB (polychlorinated
biphenyls), dieldrin, and endrin were determined in the flesh of 700 specimens of fishes caught between
1973 and 1975 in the northwestern Atlantic Ocean and northern Gulf of Mexico off the coasts of the
southeastern United States. Species with lowest oil content (<3%) — gag, Mycteroperca microlepis;
black grouper, M. bonaci; red grouper, Epinephelus morio; and red snapper, Lutjanus campechanus —
contained the least amounts of chlorinated hydrocarbon residues. Species with higher oil content —
king mackerel, Scomberomorus cavalla, (3.5%) and Spanish mackerel, S. maculatus, (4.6%) — more
consistently contained residues, but still at low levels. Significant correlations (P<0.05) were found in
red snapper and king mackerel between lipid and size and between lipid and chlorinated hydrocarbon
content. The correlations between lipid and PCB in gag and between lipid and DDT in black grouper
were also significant. The highest mean values for any species were 0.18 ppm SDDT, 0.32 ppm PCB,
0.007 ppm dieldrin, and 0.008 ppm endrin. The highest level in any one composite sample of 10 fish was
1.0 ppm IDDT, 1.8 ppm PCB, 0.026 ppm dieldrin, and 0.026 ppm endrin.

Haifa century ago manufacturers of surface coat-
ings and of electrical equipment found a common
interest in a newly introduced group of or-
ganochlorine chemicals, the PCB.^ These com-
pounds dissolve the inks in carbonless carbon
paper, which duplicates without the use of carbon
paper. They plasticize the waterproof coatings for
dairy silos and fish tanks, and marine antifouling
paint. The thermal and electrical properties of
PCB are highly desirable in dielectric fluids, the
electrical insulators in transformers and
capacitors. The PCB are also highly resistant to
chemical and biological degradation, and these
properties, too, are valued by industrial users.

Immediately following World War II, another
organ ochlorine chemical, DDT, became the magic
tool of the medical profession, deeply concerned
with preventing outbreaks of infectious, insect-
borne diseases. Enormous quantities of DDT were
used to prevent epidemics of typhus and plague in
war-torn Europe. DDT was dramatically effective
in controlling lice and fleas, which carried these

'Northwest and Alaska Fisheries Center Utilization Research
Division, National Marine Fisheries Service, NOAA, 2725
Montlake Boulevard East, Seattle, WA 98112.

^Abbreviations used in this manuscript: DDE = p,p'-di-
chlorodiphenyldichloroethylene; DDMU = p,p'-dichlorodi-
phenylchloroethylene; DDT = p,p'-dichlorodiphenyl-
trichloroethane; PCB = polychlorinated biphenyls; I DDT =
DDT and its metabolites DDE and TDE; TDE = p,p'-
dichlorodiphenyldichloroethane.

Manuscript accepted August 1979.
FISHERY BULLETIN: VOL. 78, NO. 1, 1980.

diseases. The use of this and related compounds
spread rapidly for mosquito and agricultural pest
control. Before insect resistance developed, DDT
reduced the incidence of malaria to a very low
level.

Since PCB and the organochlorine pesticides
are not only stable but also easily dispersed in the
air and through the water, it is not surprising in
retrospect that they are now found even in the
polar regions (Sladen et al. 1966; Risebrough et al.
1976; Bowes and Jonkel 1975) and that chlori-
nated hydrocarbon pollution has become a
worldwide problem. Not until the 1960's did ap-
preciation of the adverse effects of these chlori-
nated hydrocarbons begin to develop. "Silent
Spring" (Carson 1962) described the effects on the
environment of the accumulation of DDT, and
Jensen (Anonymous 1966; Jensen et al. 1969)
found PCB in marine animals. Burdick et al.
(1964) noted reproductive failure in lake trout
when the eggs contained a high level of SDDT.
Aulerich et al. (1973) traced the reproductive fail-
ure and mortality in ranch-grown mink back to
coho salmon, Oncorhynchus kisutch, from Lake
Michigan and ultimately to the PCB they con-
tained. Only recently fin erosion, a disease
associated with municipal and industrial dis-
charges, was related to iDDT (Mearns and Sher-
wood 1977). Montrose Chemical Company re-
leased wastes from DDT manufacture directly into

51

the Los Angeles County sewer system which flows
via sewer outfalls into the marine environment of
southern California. From this unanticipated
source of iDDT pollution, high levels of IDDT
developed throughout the southern California
marine environment from mollusks (Young et al.
1976), crustaceans (Burnett 1971), and fishes
(McDermott-Ehrlich et al. 1978) to marine birds
(Anderson et al. 1975) and cetaceans (Le Boeuf
and Bonnell 1971). Henderson et al. (1969, 1971)
found organochlorine residues in freshwater
fishes throughout the United States. Some species
of freshwater fishes, especially those from the
Great Lakes, contained levels of chlorinated hy-
drocarbons that exceeded the U.S. Food and Drug
Administration guidelines (Reinert 1970; Veith
1975). In recent years, the use of chlorinated hy-
drocarbons has been drastically curtailed, but
concern remains about the continuing occurrence
of these toxic compounds in the marine environ-
ment.

Fishes and shellfishes are excellent organisms
for monitoring chlorinated hydrocarbons.
Shellfishes have been used as indicators of short-
term pollution (Butler 1973; Goldberg et al. 1978)
because they accumulate and depurate these sub-
stances readily. Fishes, on the other hand, reflect
long-term exposure since they lose chlorinated
hydrocarbons slowly, if at all (Lieb et al. 1974).
Butler and Schutzmann (1978) have reported on
pesticides and PCB in yearling estuarine fishes of
the United States. Outside of their study, how-
ever, few data on fishes for human consumption
from the western Atlantic Ocean have been pub-
lished except on fishes from Canadian waters
(Sims et al. 1977). The study reported here was
undertaken to obtain information about levels of
SDDT, PCB, dieldrin, and endrin in fillets from
fishes caught in the northwestern Atlantic Ocean
and northern Gulf of Mexico. Six marine species of
both commercial and sport value have been
examined.

FISHERY BULLETIN: VOL. 78. NO. 1

METHODS

Samples of gag, Mycteroperca microlepis; black
grouper, M. bonaci; red grouper, Epinephelus
morio; red snapper, Lutjanus campechanus; king
mackerel, S comber omor us cavalla; and Spanish
mackerel, S. maculatus, were collected from the
northwestern Atlantic Ocean and northern Gulf of
Mexico, from Beaufort, N.C., south to the Florida
Keys, and west to Aransas Pass, Tex. Sampling
occurred between October 1973 and October 1975,
but mainly in 1975. Specimens were frozen and
held at -18° C. They were thawed for filleting,
grinding, compositing, and refrozen until
analysis. In the aggregate, 70 samples each con-
taining 10 fish of the same species and of similar
size were obtained. Each sample was a composite
of equal weights of ground skinless fillets from the
10 individual fish. At most sites, two or three sam-
ples from different size fish were selected. The
collection sites, size, and lipid content of the
specimens are listed in Table 1.

Extracts were prepared by the procedures of
Reinert (1970). Samples for SDDT and PCB
analysis were extracted with propanol-2/benzene
(1:1), and the extracted materials transferred to
hexane by repeated codistillation of the
propanol-2, benzene, and water with hexane. One
aliquot of the hexane extract was evaporated to
minimum weight for determination of the lipid
content. Another aliquot was cleaned up on
Florisil.^ PCB were separated from TDE, DDT,
and most of the DDE on activated silica gel
(Snyder and Reinert 1971), which also separates
the interfering hydrocarbons, phenanthrene,
fluoranthrene, and pyrene from the PCB (Zitko
1978). At least 90% of the PCB was contained in
the pentane fraction, which also contained part of

^Mention of specific products or companies in this paper does
not imply endorsement by the National Marine Fisheries Ser-
vice, NOAA.

Table l. — Collection sites, size, and lipid content of fishes from the northwest Atlantic Ocean and Gulf of

Mexico.

Species

Gag

Black grouper
Red grouper
Red snapper
King mackerel
Spanish mackerel

No.2

Fork length (cm)
Mean Range^

Weight (kg)

Lipid ci
Mean

ontent (%)

Sites'

Mean

Range^

Range^

1,2,3

8

86

64-108

9.77

3.79-18.32

2.9

0.2-5.9

5,6

6

77

54- 96

7.01

1.98-12.70

0.6

0.2-1.2

1,4, 5, 6

10

68

52- 82

608

2.42-11.50

0.5

0.1-1.0

1,2,3,4.5,

6.

7,8

18

65

45- 83

5.94

1.65-11 35

1.5

0.4-3.9

1,2,3,4,5,

6,

9

18

87

55-119

6.01

1.20-12.91

3.5

0.4-7.5

3,4, 5,6, 7

10

54

45- 64

1.41

0.48- 2.34

4.6

1.7-9.4

' 1 - Beaufort, N.C.; 2 ■ Savannah, Ga.; 3 - Florida, East Coast; 4 - Florida Keys; 5 - Tampa/St. Petersburg, Fla.; 6 - Panama City, Fla.;
7 - Mobile, Ala.; 8 - Pascagoula, Miss.; 9 - Aransas Pass, Tex.
^Number of composites, each consisting of 10 fish.
^Range of means of individual composites.

52

STOUT: ORGANOCHLORINE RESIDUES IN FISHES

the DDE. All of the TDE and DDT eluted into the
benzene fraction. For dieldrin and endrin
analysis, tissues were saponified with KOH in
aqueous ethanol, extracted with hexane, and
cleaned up on Florisil. Since the specimens, origi-
nally collected for trace-metal analysis, were
stored in polypropylene containers (Falcon No.
4014) with polyethylene lids (Falcon No. 4017),
the containers and lids were also analyzed to as-
sure freedom from interfering substances. The de-
tails of our procedures were published previously
(Stout and Beezhold 1979). Blanks carried
through the whole procedure for either PCB and
SDDT or dieldrin and endrin showed no
chromatographic peaks which interfered with
quantitation of the chlorinated hydrocarbons.

The extracts of the fishes were quantitated by
electron-capture gas chromatography. A Varian
600 C gas chromatograph with a titanium tritide
detector was fitted with a 1.5 m (5 ft) x 0.32 cm
(0.125 in) o.d. glass column containing a mixture
of equal parts of 15% QF-1 on 80-100 mesh Gas
Chrom Q and 10% DC-200 on the same support
(Burke and Holswade 1966). Reference standards
of p,p'-DDE, p,p'-DDMU, p,p'-TDE, p,p'-DDT,
dieldrin, and endrin were obtained from the U.S.
Environmental Protection Agency, Health Effects
Research Laboratory, Research Triangle Park,
N.C. Aroclor 1254 obtained from the Monsanto
Company, St. Louis, Mo., was the standard for the
PCB because the residues in the fishes matched
this Aroclor most closely. Standard curves of peak
height versus concentration were used to deter-
mine the concentrations of components in the ex-
tracts. The sensitivity throughout each run was
assured by frequent injections of standard solu-
tions. The quantifiable limit was about 0.003 ppm
for DDE, TDE, DDT, dieldrin, and endrin, and
about 0.04 ppm for PCB depending on daily sen-
sitivity. The mean relative standard deviation for
samples analyzed in duplicate was 11%. The aver-
age recovery of samples spiked with standards was
85%. The values reported were not corrected for
recovery. Residue values were calculated on the
basis of micrograms chlorinated hydrocarbon per
gram wet tissue or parts per million (ppm).

The PCB were quantitated by summing the
peak heights corresponding to the five major peaks
in Aroclor 1254 after omitting the twin peak with
a retention time similar to that of p,p'-DDE. As
Veith ( 1975) also concluded, use of five peaks in-
creased the accuracy of PCB measurement by
reducing the effect of minor variations in concen-

tration of individual components in the samples
(Figure 1).

Since part of the DDE eluted from silica gel with
the PCB fraction and one of the major peaks in
Aroclor 1254 overlapped the DDE peak in the
gas-chromatographic traces, a special technique
was needed to quantitate the DDE in the PCB
fraction. First the gross DDE concentration was
determined in the usual way from the peak height
versus DDE concentration curve. Next, the con-
tribution of PCB to that overlapping peak was
calculated based on the assumption that the
height of Aroclor peak 3, the peak which over-
lapped DDE, was proportional to the heights of the
five PCB peaks used to calculate the concentration
of PCB. To make this calculation, the sum of the
peak heights of the five major PCB peaks exclud-
ing the "DDE" peak was plotted against the peak
height of the "DDE" peak in PCB standards of
increasing concentrations. From the sum of the
five PCB peaks in the sample, the peak height of
the PCB portion of peak 3 in that sample was
determined. This peak height was converted to
concentration of DDE via the peak height versus
concentration curve for DDE. The apparent con-
centration of DDE from PCB peak 3 was sub-
tracted from the gross DDE concentration in the
"DDE" peak to obtain the net concentration of
DDE in the PCB fraction. The elctron-capture de-
tector is so much more sensitive to DDE than PCB
that this method of calculation affected the accu-
racy of DDE determination only to a small extent
(Figure 1). Use of a minicomputer expedited these
calculations.

Confirmation of DDT and its metabolites and
PCB was effected by saponifying separate portions
of tissue (Reinert 1970). DDT is dehydrochlori-
nated by base to DDE, and TDE similarly to
DDMU. PCB are stable to base. The levels of diel-
drin and endrin were too low to warrant confirma-
tion studies.

RESULTS AND DISCUSSION

The marine fishes from the northwestern Atlan-
tic Ocean and northern Gulf of Mexico analyzed in
this study contained relatively low levels of SDDT
and PCB. Of the 70 composite samples, only 29
contained more than 0.05 ppm SDDT and 0. 1 ppm
PCB in the edible portion (skinless fillets), and
only one as much as 1 ppm SDDT and PCB. Red
grouper contained the lowest levels of both chlori-
nated hydrocarbons. The mean IDDT content for

53

FISHERY BULLETIN: VOL. 78, NO. 1

AROCLOR 1254 (1100 pg)

TDE (40 pg)

DDT (40 pg)

Figure l. — Gas chromatographic curves of Aroclor 1254, the
PCB fraction of an extract from Spanish mackerel, and DDT and
its metabolites DDE and TDE; pg = picograms or 10

54

10 sets of red grouper was 0.008 ppm; for most
samples, PCB were not detectable. Black grouper
and gag contained slightly higher levels of iDDT
and PCB. Red snapper also contained little iDDT
(mean 0.039 ppm), but the PCB level in six sam-
ples exceeded 0.1 ppm. Only the two species of
mackerel consistently contained quantifiable
amounts of both SDDT and PCB. The mean levels
of SDDT were 0.144 ppm in Spanish mackerel and
0.177 ppm in king mackerel. The mean PCB level
in both species of mackerel was 0.32 ppm. The
highest levels of both chlorinated hydrocarbons
were found in one composite sample of king mack-
erel from the Florida Keys, 0.996 ppm iDDT and
1.8 ppm PCB. The data are summarized in Table 2.
The limited data in the literature convey a simi-
lar picture. Groupers of the genera Epinephelus
and Mycteroperca from the Gulf of Mexico and the
Grand Bahamas contained 0-0.10 ppm SDDT and
0.003-0.22 ppm PCB in muscle (Giam et al. 1974).
Red snapper from Mobile Bay, Ala., contained
0.086 ppm SDDT and 0.14 ppm PCB in the whole
animal; gray snapper, Lutjanus griseus, from
Jacksonville, Fla., 0.007 ppm SDDT and no PCB
in the whole animal (Markin et al. 1974). Small
Spanish mackerel (306 g) from the Savannah
River estuary in Georgia contained neither SDDT
nor PCB in muscle. (Butler^) Although somewhat
larger than those fish, the smallest fish in the
current study (475 g) contained barely detectable
amounts of these substances (0.008 ppm SDDT
and 0.034 ppm PCB). Markin et al. (1974) found
0.04-0.16 ppm SDDT and <0.01-0.18 ppm PCB in
seven whole Spanish mackerel from the south-
eastern United States. A single sample of king
mackerel muscle from the Gulf of Mexico off
Mexico contained 0.024 ppm SDDT and 0.034 ppm
PCB (Giam et al. 1972). Atlantic mackerel,
Scomber scombrus, collected in 1971-72 in Cana-
dian waters (Sims et al. 1977) contained more
SDDT (0.26 ppm) and PCB (0.41 ppm) in the "edi-
ble portion" (which may have contained skin
and/or bones) than did skinless fillets of either
species of mackerel examined in my study. On the
other hand, muscle from Atlantic mackerel from
the Bay of Fundy-Gulf of Maine contained the
same level of PCB (0.35 ppm) (Zitko et al. 1972).
The proportions of p,p '-DDT and its metabolites
were very similar in the king and Spanish mack-
erel examined in our study. p,p'-DDE is the

-12

g-

"Butler, P. A. 1978. EPA-NOAA Cooperative Estuarine
Monitoring Program, Final Report, Gulf Breeze, Fla., 108 p.

STOUT: ORGANOCHLORINE RESIDUES IN FISHES

Table 2.— iDDT and PCB in fishes from the northwest Atlantic Ocean and Gulf of
Mexico, nq = not queintifiable; nd = none detected.

No.'

iDDT (ppm)

PCB (ppm)

Species

Mean + SD

Range

Mean = SD

Range

Gag

8

0.036^0.013

0.017-0050

0087 = 0.023

nq-0 129

Black grouper

6

0.009r0.007

0.003-0.020

nq

nq-0.059

Red grouper

10

0.008 = 0 007

n.d,-0,025

nd

nd-nq

Red snapper

18

0.039 = 0076

n.d.-0.322

0.121=0.108

nd-0464

King mackerel

18

0.177 = 0.239

0.009-0.996

0322 = 0.414

0,060-1.78

Spanish mackerel

10

0.144 = 0.097

0.008-0.319

0319 = 0.263

0.034-0.821

'Number of composites, each consisting of 10 fish.

major component (—65%) accompanied by about
25% of the parent compound and 10% p,p'-TDE.
Although the composite picture for red snapper
looked markedly different (Table 3), in fact the
DDT residues in that species actually fell into two
categories. In the first group, p,p -TDE and p,p '-
DDT were not quantifiable, and the maximum
content of p,p -DDE was 0.029 ppm. In the second
group, five samples containing >0.029 ppm p,p'-
DDE, both p,p'-TDE and p,p -DDT were quanti-
fiable. In those five samples, the proportions of the
three components were the same as in the mack-
erel. Finfish from the Atlantic coast of Canada
(Sims et al. 1977) contained proportionately much
lessp,p -DDE (45% ) and morep,p -DDT (40% ) and
p,p '-TDE (15%). The increase in the proportion of
p,p -DDE in the present samples may reflect deg-
radation of the parent compound in the environ-
ment before it accumulated in the fishes. Samples
for the Canadian study were collected in 1971 and
1972, soon after usage of DDT had been drastically
curtailed (around 1970) as the result of increasing
insect resistance, problems with indirect con-
tamination of foodstuffs, and concern about effects
of DDT on nontarget species. Several years
elapsed before the samples for the present study
were collected, mainly in 1975. In the interval,
DDT was degrading aerobically to DDE and
anaerobically in the marine environment to TDE.
Alternatively, DDT may metabolize more rapidly
to DDE in the more temperate climate of the re-
gion studied and somewhat less rapidly to TDE.

Table 3. — Mean proportions of 5^DDT present as p,p '-DDE, p,p '-
TDE, and p,p -DDT in fishes from the northwest Atlantic Ocean
and Gulf of Mexico.

p.p DDE (%)
Mean = SO Range

p.p TDE (%)

p.p -DDT (%)

Species

IV1ean=SD

Range

Mean = SD Range

Red snapper,

all

88=18

58-100

3=5

0-15

9 = 13 0-30

Red snapper'

62= 6

58- 72

10 = 3

7-15

28-4 21-32

King mackerel

64= 8

48- 77

8 = 6

0-17

28= 6 16-40

Spanish

mackerel

66 = 19

48-100

12 = 8

0-24

21=12 0-37

'Five samples which contained >0.029 ppm DDE.

The concentration of PCB, when present, was
higher than that of IDDT in all samples but one.
The mean ratio of PCB to SDDT was 1.8 for gag,
2.2 for king and Spanish mackerel, and 2.6 for six
sets of red snapper. In the two other samples of red
snapper with quantifiable levels of PCB, the
PCB/SDDT ratios were 22.7 and 24.3. The con-
centrations of SDDT were below 0.01 ppm in both
cases. The one sample of red snapper in which the
PCB/IDDT ratio was below 1 contained a rela-
tively large amount of SDDT, 0.096 ppm, the sec-
ond highest IDDT value in the 18 samples of red
snapper. In contrast, the PCB concentration was
low both in absolute amount, <0.06 ppm, and in
rank, 14th out of 18 samples.

The chlorinated-hydrocarbon content of the
specimens in this study was, in general terms,
directly related to the lipid content. The groupers,
which contained <1% lipid, contained the least
iDDT and PCB. King and Spanish mackerel had
the highest lipid contents, 3.5 and 4.6%, respec-
tively, and the highest levels of both IDDT and
PCB. In three of the six species, the correlation
between lipid and IDDT was significant, i.e.,
P<0.05. Similarly, in three of the four species for
which PCB were quantifiable the correlation be-
tween lipid and PCB was significant. Possible rela-
tionships between size and chlorinated hydrocar-
bon content were also examined. Although length,
weight, iDDT, and PCB were all studied, in no
case was a significant correlation found in any of
the six species (Table 4). In two of the six species,
the correlations between length and lipid and also
between weight and lipid were significant. In both
species, red snapper and king mackerel, the P
values for lipid versus chlorinated hydrocarbon,
were below 0.01. Giam et al. (1974) noted a rela-
tionship between size and concentration of pollu-
tants in groupers from the Gulf of Mexico, but only
in the area with the highest contamination, i.e. , up
to 0.1 ppm.

SDDT and PCB levels within single species
were compared at the various sites. Fish from the

55

FISHERY BULLETIN: VOL. 78. NO. 1

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Florida Keys contained the greatest amounts of
both substances, indicating that contamination
from agricultural and domestic effluents was
greatest in south Florida, an area of intense ag-
riculture and relatively dense population as well.
Fish caught in the vicinity of Beaufort and Mobile
contained slightly less !iDDT and PCB. Fish from
the other sites contained lower levels of chlori-
nated hydrocarbons, which were not distinguish-
able by site, except that only DDE was quanti-
fiable in the one sample from Pascagoula, Miss.
The Mississippi River, which receives the runoff
from 40% of the land mass of the conterminous
United States, including the corn belt and the
cotton belt, did not seem to be the main source of
either SDDT or PCB.

Low levels of dieldrin and endrin, two highly
toxic organochlorine pesticides, were found in the
fish included in this study. The highest concentra-
tion of either compound was 0.026 ppm. The diel-
drin and endrin content of only the three species
with the highest levels of SDDT and PCB were
determined. Nonetheless, dieldrin and endrin
were quantifiable only in about one-third of the
samples. Two of 18 red snapper, 7 of 18 king mack-
erel, and 6 of 10 Spanish mackerel samples con-
tained quantifiable amounts of both compounds.
The mean levels for Spanish mackerel, the species
with the highest mean concentrations, were 0.007
ppm dieldrin and 0.008 ppm endrin (Table 5). King
mackerel from Aransas Pass contained the high-
est concentration of dieldrin, 0.026 ppm; Spanish
mackerel from Panama City, Fla., the highest
concentration of endrin, also 0.026 ppm. The diel-
drin and endrin concentrations in the three
species followed the same distribution patterns
with relation to species and lipid content as was
observed for SDDT and PCB. Butler (see footnote
4) found no dieldrin in the muscle of small Spanish
mackerel from the Savannah River estuary.

CONCLUSIONS

Residues of SDDT, PCB, dieldrin, and endrin,
although generally low, were found in all species
and all locations except Pascagoula, Miss., where
only DDE was quantifiable. The highest levels of
SDDT and PCB, and the only ones to reach 1 ppm,
were in one composite sample of king mackerel
from the Florida Keys, 0.996 ppm SDDT and 1.8
ppm PCB. The highest level of dieldrin, 0.026 ppm,
was in king mackerel from Aransas Pass, Tex.,
and of endrin, also 0.026 ppm, in Spanish mack-

56

STOUT: ORGANOCHLORINE RESIDUES IN FISHES

Table 5. — Dieldrin and endrin in fishes from the northwest
Atlantic Ocean and Gulf of Mexico, nd = not detected; nq == not
quantifiable.

No.'

Dieldrin i

Ippm) ■

Endnn (ppm)

Species

Mean=:SD

Range

Mean*SD

Range

Red snapper
King mackerel
Spanish
mackerel

18

18

10

nd
0.005 i:0.006

0.007^0.004

nd-nq
nd-0.026

nd-0.014

nd
0.004*0.004

0.008 ±0.010

nd-0.003
nd-0.014

nd-0.026

'Number of composites, each consisting of 1 0 fish.

erel from Panama City, Fla. The species with the
highest Hpid contents contained the highest con-
centrations of chlorinated hydrocarbons. Sig-
nificant correlations (P<0.05) were found between
lipid and size and between lipid and chlorinated
hydrocarbon content in two of the six species. In
two other species the correlation between lipid and
either SDDT or PCB was significant. In all cases
but one, the chlorinated hydrocarbon levels were
substantially below the U.S. Food and Drug Ad-
ministration guidelines: 5 ppm SDDT, 2 ppm PCB,
and 0.3 ppm dieldrin and endrin.

ACKNOWLEDGMENTS

I thank the Southeast Fisheries Center Charles-
ton Laboratory, NMFS, NOAA, for providing the
samples and Laura G. Lewis for technical support
throughout this research. Russell F. Kappenman,
Northwest and Alaska Fisheries Center Fisheries
Data & Management Systems Division, provided
guidance for statistical analyses.

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FISHERY BULLETIN: VOL. 78, NO. 1

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1975. Baseline concentrations of polychlorinated

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ZITKO, V.

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ZiTKO, v., O. HUTZINGER, and P. M. K. CHOI.

1972. Contamination of the Bay of Fundy — Gulf of Maine
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58

SYSTEMATICS AND DISTRIBUTION OF CERATIOID ANGLERFISHES

OF THE FAMILY MELANOCETIDAE WITH THE DESCRIPTION OF

A NEW SPECIES FROM THE EASTERN NORTH PACIFIC OCEAN*

Theodore W. Pietsch and John P. Van Duzer^

ABSTRACT

The ceratioid anglerfish family Melanocetidae is revised on the basis of a study of approximately 600
specimens collected from all oceans. Of the 11 nominal species of Melanocetus based on females, 4 are
recognized: M.johnsoni, with M. krechi, M. rotundatus, M. ferox, M. cirrifer, and M. megalodontis as
synonyms; M. polyactis; M. niger; and M. murrayi , with M. vorax and M. tumidus as synonyms. A fifth
species is newly described from a single female collected from the eastern Pacific Ocean off Mazatlan,
Sinaloa, Mexico. The new form differs most strikingly from its allies in having a larger escal bulb and
shorter jaw teeth.

Melanocetus is widely distributed throughout all the major oceans of the world between about 250 m
and some unknown lower depth limit that exceeds 3,000 m. Melanocetus johnsoni and M. murrayi are
wide ranging forms, whereas M. polyactis and M. niger are apparently restricted to the eastern tropical
Pacific.

Melanocetus murrayi appears to be the most phylogenetically derived member of the family. The four
remaining species are much more closely related to each other than any is to M. murrayi. Melanocetus
johnsoni is perhaps derived in having a relatively long illicium, and in having fewer, but longer jaw
teeth. Melanocetus polyactis and M. niger are similar in having relatively short jaw teeth, a similar
escal morphology, and a sympatric geographic distribution that is limited to the eastern tropical
Pacific. The newly described form is derived in having an extremely large escal bulb, comparable with
no other known ceratioid.

The Melanocetidae include globose, bathypelagic
anglerfishes, easily separated from members of
allied families by having 12 or more dorsal fin rays,
3 or 4 anal rays, and large, fanglike jaw teeth
(Bertelsen 1951; Pietsch 1972a). The only recog-
nized genus of the family was established by
Giinther (1864) with the description of Mel-
anocetus johnsoni, based on a single female
specimen collected in the Atlantic Ocean, off
Madeira. Since that time, 10 additional species
based on females have been described (Table 1).
From a comparison of the characters used to dis-
tinguish these nominal forms, Bertelsen (1951,
table 4) doubted that M. krechi and M. cirrifer
could be maintained and that M. ferox and M.
niger might be synonyms. Melanocetus murrayi
and M. johnsoni were recognized as the only
species known from the Atlantic; M. niger, M.
ferox, and M. polyactis were considered forms re-
stricted to the eastern tropical Pacific. Six larval

'Contribution No. 516 from the College of Fisheries, Univer-
sity of Washington, Seattle, WA 98195.

J'College of Fisheries, University of Washington, Seattle, WA
joiyo.

Manuscri

rio'Ji'4'^"P' accepted September 1979.
nSHERV BULLETIN: Vol. 78, NO. 1,

1980.

specimens from the Gulf of Panama were assigned
to M. polyactis. The remaining larvae (approxi-
mately 600 individuals) were separated into two
groups, representing M. murrayi and M.johnsoni,
on the basis of geographic distribution, fin ray
counts, and a comparison of larval and adolescent
female pigmentation. Despite these allocations,
Bertelsen (1951) made it clear that ". . . the sep-
aration of the species is still very uncertain and
future investigations and material will probably
make it necessary to revise this synopsis."

At the time of Bertelsen's (1951) monograph on
the Ceratioidei, 19 metamorphosed melanocetid
males were known. Of these, 14 had been set up as
tjrpes of 12 separate species, and 5 were uncer-
tainly placed. On the basis of subdermal pigment,
fin ray counts, and geographic distribution, Ber-
telsen (1951) synonymized 6 of these 12 nominal
forms with M. johnsoni and 4 with M. murrayi.
The remaining two species based on males, M.
longirostris and M. nudus, each differing slightly
from the rest of the material, were tentatively
retained (Table 1).

With the vast increase in the amount of mate-
rial of Melanocetus made available in the last 25

59

FISHERY BULLETIN: VOL. 78, NO. 1

Table l. — Reallocation of nominal forms ofMelanocetus. Valid names on right. Synonymy for
species based on males after Bertelsen 1951.

Females:

Melanocetus johnsoni Gunther 1864

Melanocetus krechi Brauer 1 902

Melanocetus rotundatus Gilchrist 1903

Melanocetus ferox Regan 1926

Melanocetus cirrifer Regan and Trewavas 1932

Melanocetus megalodontis Beebe and Crane 1 947

Melanocetus polyactis Regan 1925

Melanocetus niger Regan 1925 (in part)

Melanocetus niger Regan 1925 (in part)

Melanocetus murrayi Gunther 1887

Melanocetus vorax Brauer 1 902

Melanocetus tumidus Parr 1 927
Males:

Centrocetus spinulosus Regan and Trewavas 1 932

Xenoceratias micracanthus Regan and Trewavas 1 932

Xenoceratias heterorhynchus Regan and Trewavas 1932

Xenoceratias laevis Regan and Trewavas 1932

Xenoceratias brevirostris Regan and Trewavas 1 932

Xenoceratias braueri Koefoed 1 944

Rhynchoceratias rostratus Regan 1926 (in part)

Rhynchoceratias leucorhinus Regan 1926 (in part)

Rhynchoceratias acanthlrostris Parr 1927

Rhynchoceratias latirhinus Parr 1927

Rhynchoceratias longipinnis Parr 1 930

Xenoceratias regani Koefoed 1 944

Melanocetus johnsoni Gunther 1 864

Melanocetus polyactis Regan 1 925
Melanocetus niger 1 925

Melanocetus murrayi Gunther 1 887

Melanocetus johnsoni Gunther 1 864

Melanocetus polyactis Regan 1 925
Melanocetus murrayi Gunther 1887

yr, we are able to recognize five species based on
females. Four of these are previously described
forms: M. johnsoni, represented by 346 specimens
collected from all three major oceans of the world;
M. polyactis and M. niger, known from 15 and 6
specimens both restricted to the eastern tropical
Pacific; and M. murrayi, 140 specimens of
worldwide distribution. The fifth is a new species
recently collected by the Velero IV of the Univer-
sity of Southern California in the eastern Pacific
off Mazatlan, Sinaloa, Mexico. It differs strikingly
from its allies in having a considerably larger
escal bulb and shorter jaw teeth.

Although the number of known male specimens
has increased nearly fourfold since Bertelsen's
(1951) work, no new diagnostic data are available.
We have examined 73 individuals (11.5-24 mm
standard length), none of which can be satisfactor-
ily identified to species based on females. As pre-
dicted by Bertelsen (1951), the variation in the
number of denticular teeth is greater than previ-
ously thought and values given in his key overlap
to a much greater extent than is indicated. An
attempt to utilize differences in larval pigmenta-
tion, thought to be more or less retained, at least in
the younger metamorphosed males, failed to sepa-
rate the material into groups that could be as-
sociated with species based on females. Although
Bertelsen's ( 1951 ) synonymies for nominal species
based on males are retained here, additional male
specimens are listed as Melanocetus sp.

METHODS AND MATERIALS

Standard lengths (SL) are used throughout un-
less otherwise stated. Measurements were taken
from the left side whenever possible and rounded
to the nearest 0.5 mm. To ensure accurate fin ray
counts, skin was removed from the pectoral fins
and incisions were made to reveal the rays of the
dorsal and anal fins. Sockets, indicating missing
teeth in the jaws and on the vomer, were included
in total tooth counts. Jaw tooth counts are the sum
of both right and left sides. Head depth is the
distance from the tip of the sphenotic spine to the
base of the quadrate spine. Head width is the dis-
tance between the anterolateralmost margins of
the sphenotic bones. Lower jaw length is the dis-
tance from the symphysial spine to the posterior-
most margin of the articular. Illicium length is the
distance from the articulation of the pterygio-
phore of the illicium and the illicial bone to the
distal surface of the esca, excluding escal append-
ages. The width of the pectoral fin lobe is the
distance between the point of articulation of the
uppermost fin ray to the articulation of the lower-
most fin ray. Terminology used in describing the
various parts of the angling apparatus follows
Bradbury (1967). Definitions of terms used for the
different stages of development follow Bertelsen
(1951). Complete locality data are given for pri-
mary type material only.

The comparative osteological investigation was

60

PIETSCH and VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

based primarily on five female specimens (two M.
murrayi, 75 and 84 mm SL, and three M.johnsoni,
44.5, 60, and 75 mm SL; material representing the
remaining species of the genus was unavailable)
cleared and stained with Alizarin red S following
the trypsin digestion technique (Taylor 1967).
Bone terminology follows Pietsch (1974).

Unless otherwise indicated, all diagnoses and de-
scriptions are based on female specimens >20 mm
SL. For males and larvae see Bertelsen (1951).
Material is catalogued in the following institu-
tions: Australian Museum, Sydney ( AMS); British
Museum (Natural History), London (BMNH);
Bingham Oceanographic Collections, Peabody
Museum of Natural History, Yale University
(BOC); California Academy of Sciences, San Fran-
cisco (CAS); Florida State Museum, University of
Florida, Gainsville (FSM); Institute of Oceanol-
ogy, Academy of Sciences, U.S.S.R., Moscow
(lOAN); Institute of Oceanographic Sciences, Sur-
rey, England (lOS); Institut fiir Seefischerei,
Hamburg (ISH); Natural History Museum of Los
Angeles County (LACM); Museum of Compara-
tive Zoology, Harvard University (MCZ); National
Museum of New Zealand, Wellington (NMNZ);

Royal Ontario Museum, Toronto (ROM); South
African Museum, Cape Town (SAM); University of
Bergen, Zoological Museum (UBZM);University of
Miami Marine laboratory, (UMML); National
Museum of Natural History, Washington, D.C.
(USNM); Virginia Institute of Marine Science,
Gloucester Point (VIMS); Zoological Museum,
Humboldt University, Berlin (ZMHU); Zoological
Museum, University of Copenhagen (ZMUC).

OSTEOLOGY OF FEMALES

The osteology of Melanocetus was partially de-
scribed by Regan (1926, fig. 10), Parr (1930a,
fig. 2-5, male only), Regan and Trewavas (1932,
fig. 19-28), and Bertelsen ( 1951, fig. 13, 14). In the
following account, only those comparative aspects
that need amending or that have not previously
appeared in the literature are discussed.

Cranium (Figures 1-9). — The anterior portion of
the cranium of Melanocetus is considerably wider,
relative to the posterior portion, than in other
ceratioids; the distance between the lateral mar-
gins of the ethmoid cartilage is nearly equal to the

Sphenotic

Posttemporal

Supraethmoid

Vomer

Exoccipital

EpiotJc

Lateral ethmoid

Pterotic

Pterosphenoid

Supraoccipital

Figure l.— Dorsal view of cranium of Melanocetus johnsoni, LACM 32786-1, 75 mm SL. Cartilage stippled, open

spaces solid black.

61

FISHERY BULLETIN: VOL 78, NO. 1

distance between the tips of the sphenotic bones
(Figures 1, 2) The head of the vomer, bearing as
many as 10 recurved teeth, is also unusually wide
(Figures 1, 2, 5-7). The frontals are triradiate in
shape and widely separated from each other along
their dorsal margins, approaching one another on

the midline only at their ventromedial extensions.
A semicircular-shaped pterosphenoid is present
under the posterior extension of each frontal. The
parasphenoid is well separated from the ven-
tromedial extensions of the frontals. Posterome-
dially, the parasphenoid underlies the anterior

Sphenotic

Pterosphenoid

Parietal

Supraethmoid

Vomer

Lateral ethmoid

Posttemporal

Exoccipital

Epiotic

Frontal

Pterotic

Supraoccipital

Figure 2.— Dorsal view of cranium oi Melanocetus murrayi, LACM 31501-3, 84 mm SL. Cartilage stippled, open

spaces solid black.

Pterosphenoid

Sphenotic

/Parietal

Posttemporal

Lateral ethmoid

Vomer

Supraethmoid

Exoccipital

20th pre-ural
centrum

Basioccipital

Parasphenoid

Pterotic

Supraoccipital

Prootic

Figure 3.— Lateral view of cranium of Melanocetus johnsoni , LACM 32786-1, 75 mm SL. Cartilage stippled, open

spaces solid black.

62

PIETSCH and VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

projection of the supraoccipital; posteriorly di-
rected dorsolateral extensions of the parasphenoid
make contact laterally with the respective prootic
(Figures 3, 4).

The large prootics are separated from each other
anteriorly by the anterior process of the supra-
occipital. Ventrally, each prootic forms a rela-
tively large, anterolaterally directed, conical pro-

jection not found in other ceratioids (Figures 3-5,
8).

The supraoccipital is the largest element of the
cranium, making up a considerable portion of the
roof of the cranium. Together with the frontals,
the supraoccipital forms the floor of a deep,
V-shaped illicial trough (Figure 8). An anteriorly
directed extension of the supraoccipital that sep-

Pterosphenoid

Sphenotic

Parietal

Frontal

Supraethmoid

Lateral ethmoid

Vomer

Posttemporal

Exoccipital

20th pre-ural
centrum

Basloccipital

Parasphenoid

Supraoccipital

Pterotic

Prootic

FIGURE 4.— Lateral view of cranium of Melanocetus murrayi, LACM 31501-3, 84 mm SL. Cartilage stippled, open

spaces solid black.

Pterosphenoid

Prootic

Supraethmoid

Pterotic

Parasphenoid

Exoccipital

Vomer

20th pre-ural
centrum

Basioccipital

Lateral ethmoid

Posttemporal

Frontal

Sphenotic

Figure 5.— Ventral view of cranium of Melanocetus murrayi, LACM 31501-3, 84 mm SL. Cartilage stippled, open

spaces solid black.

63

Supraethmold

Frontal

Lateral
ethmoid

Vomer

Figure 6.— Anterior view of anterior half of cranium of
Melanocetus johnsoni, LACM 32786-1, 75 mm SL. Cartilage
stippled.

Supraethmold

Lateral /
ethmoid

Frontal

Vomer

Figure 7. — Anterior view of anterior half of cranium of
Melanocetus murrayi, LACM 31501-3, 84 mm SL. Cartilage
stippled.

arates the prootics on the midline, is narrowly
separated by cartilage from the ends of the
ventromedial extensions of the frontals. The
supraoccipital is not overlapped by the parietals
(Figures 1-5).

The cranium of M. murrayi is considerably more
elongate and compressed compared with that of its
congeners (Figures 3, 4). As a consequence, the
anterior margin of the vomer of M. murrayi is
deeply concave (nearly straight in other forms),
the frontals are more elongate and considerably
lighter in construction, the sphenotics are much
less produced forward, and the parietals do not
extend posteriorly to overlap the posttemporals as
they do in other Melanocetus species (Figures 1, 2).

Mandibular arch (Figures 10, 11). — The anterior
portion of the premaxilla bears a short ascending
process and a slightly longer articular process. A
small (compared with those of oneirodids, Pietsch
1974) symphysial cartilage lies just behind the

FISHERY BULLETIN; VOL. 78, NO. 1

Supraoccipital

Cut surface

of frontal

Epiotic

Pterosplienoid

Cut surface of
supraoccipital

Splienotic

Prootic

Cut surface
of parasplienoid

FIGURE 8. — Anterior view of posterior half of cranium of
Melanocetus murrayi, LACM 31501-3, 84 mm SL, anterior por-
tion removed. Cartilage stippled.

Epiotic

Parietal

Sphenotic

Posttemporal

Pterotic

Exoccipital

20th pre-ural
centrum

Figure 9. — Posterior view of cranium of Melanocetus murrayi,
LACM 31501-3, 84 mm SL. Cartilage stippled.

posteriorly notched symphysis of the premaxillae.
There is no postmaxillary process of the pre-
maxilla. The elongate portion of each premaxilla
may bear up to 89 recurved, depressible teeth of
mixed sizes (Figure 10).

On each side, the posterior ends of the pre-
maxilla and maxilla are united by connective tis-
sue to each other and to the lateral surface of the
ascending process of the articular of the lower jaw,
preventing any forward rotation of the upper jaw
bones to close off the corners of the mouth. There is
no elongate, anterior maxillomandibular liga-
ment originating on the dentary as in oneirodids
(labial cartilage of Le Danois 1964; Pietsch 1972a,
1974).

The dentaries meet on the midline to form a
strong symphysial spine. Each dentary may bear
up to 71 recurved, depressible teeth of mixed sizes
(Figure 11).

Palatine and hyoid arches (Figures 11, 12). — The
distal portion of the palatine arch (including the
mesopterygoid, ectopterygoid, and palatine) is
elongate and slender throughout (Figure 11). The
small mesopterygoid is in contact with the metap-

64

PIETSCH and VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

terygoid. The suspensorium is unusually narrow
and elongate (due largely to the extremely narrow
and elongate quadrate), and directed obliquely
backward. The posterior head of the hyomandibu-
lar is the larger of the two heads forming a broad
articulation with the pterotic. The interhyal is

Maxilla

Premaxilla

Symphyslal
cartilage

FIGURE 10. — Elements of upper jaw of Melanocetus murrayi,
LACM 31501-3, 84 mm SL: A. Maxilla and premaxilla, left
lateral view; B. Symphysis of premaxillae, dorsal view.

short and relatively thick (compared with that of
oneirodids, Pietsch 1974).

The hyoid apparatus (including epihyal,
ceratohyal, and upper and lower hypohyals) is re-
latively short and thick (Figure 12). The lower
hypohyal extends down beyond the ventral mar-
gin of the ceratohyal. In other ways this portion of
the hyoid arch does not differ substantially from
that described for oneirodids (Pietsch 1974).

Opercular apparatus (Figure 11). — The opercu-
lar apparatus is somewhat reduced (compared
with that of oneirodids, Pietsch 1974). The opercle

Dorsal
hypohyal

Ceratohyal

Epihyal

Ventral
hypohyal

' Branchiostegal rays

FIGURE 12. — Lateral view of hyoid apparatus of Melanocetus
murrayi, LACM 31501-3, 84 mm SL, interhyal not shown. Car-
tilage stippled.

Hyomandibular

Symplectic

Interhyal

Palatine

Ectopterygoid

Figure ll. — Lateral view of lower jaw,
suspensorium, and opercular apparatus
of Melanocetus murrayi, LACM 31501-
3, 84 mm SL. Cartilage stippled, open
spaces solid black.

Subopercle

Preopercle

Interopercle

Quadrate

Dentary

Articular

65

is notched posteriorly, but the upper fork of this
bone is considerably shorter than the lower fork
and sometimes absent. The subopercle is narrow
and elongate, the upper part tapering to a fine
point, the lower part rounded with a well-
developed anterior spine or projection. The in-
teropercle is unusually long and slender. The
preopercle is more or less straight.

Branchial arches (Figure 13). — Pharyngobran-
chials I and IV are absent; those of the second and
third arches are well developed, bearing four to
nine recurved and depressible fangs. Epibranchial

FISHERY BULLETIN: VOL. 78, NO. 1

I is reduced lying free in the connective tissue
matrix. Ceratobranchial V is also reduced but
tightly connected to the medial-proximal margin
of ceratobranchial IV. There are three hypo-
branchials, and a single basibranchial ossification
surrounded by a triangular-shaped cartilage.

Vertebrae and caudal skeleton (Figure 14). — The
vertebral column forms a sigmoid curve, dipping
down behind the region of the gut and sloping up
again to support the tail. In the five cleared and
stained specimens examined there are 20 verte-
bral centra (including the half-centrum to which is

Hypobranchial I

Ceratobranchial I

Epibranchial I

Pharyngobranchial II

Basibranchial

Ceratobranchial V

Epibranchial IV

Figure 13.— Branchial arches of
Melanocetus murrayi, LACM 31501-3,
84 mm SL. The ventral portion of the
branchial basket is shown in dorsal
view, the dorsal portion (epibranchials
and pharyngobranchials) is folded back
and shown in ventral view. Cartilage
stippled.

Pharyngobranchial III

Figure 14. — Lateral view of vertebral col-
umn, dorsal and anal fins, and caudal skele-
ton oi Melanocetus murrayi, LACM 31501-
3, 84 mm SL. Cartilage stippled.

66

PIETSCH and VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

fused the hypural plate, Pietsch 1972a) of which
13-15 are caudal vertebrae (those bearing com-
plete haemal arches). Epurals are absent. The
hypural plate is unnotched posteriorly and bears
the overlapping bases of nine principal caudal
rays, the uppermost of which is exceptionally
large. The uppermost and two lowermost caudal
rays are simple, the central rays are bifurcated
distally.

Median fins and illicial apparatus (Figures 14,
15). — There are 13-19 biserial, segmented, and
unbranched dorsal fin rays, the number varying
somewhat among species. The rays are supported
by elongate, closely associated radials, usually one
less than the number of rays. All species of the
genus have 4 anal fin rays (of 353 specimens
counted, only 2 had 3 anal rays, and only 2 had 5
rays) that are like those of the dorsal fin, invari-
ably supported by 3 similar, closely associated ra-
dials (Table 2, Figure 14).

The pterygiophore of the illicium is strongly
compressed with a thin, bladelike ventral expan-
sion. The length of the pterygiophore varies from
17*7^ SL in M. murrayi to 33% SL in M.johnsoni.
The remnant of the second cephalic ray is a minute
ossification lying on the pterygiophore just behind
the articulation with the illicial bone (Figure 15).
The length of the illicial bone varies slightly
among Melanocetus species, becoming longer pro-
portionately with growth.

Pectoral girdle, pectoral fin, and pelvic bone (Fig-
ure 16). — Each posttemporal overlaps the re-
spective pterotic, epiotic, and exoccipital. It is in
turn overlapped by the parietal in M.johnsoni, hut
widely separated from this bone in M. murrayi.

An ossified posteroventral process of the
coracoid is absent but perhaps represented by a
posteroventral cartilaginous extension. There are
four pectoral radials, the lower two of which be-
come completely fused with each other giving the
appearance of only three radials (Regan and Tre-
wavas 1932, fig. 22; Pietsch 1972a).

The pectoral fin lobe of M. murrayi is consid-
erably smaller than that of other Melanocetus
species (Figure 16 A). In other ways the elements
of the pectoral girdle, pectoral fin, and pelvic bone
do not differ substantially from those of oneirodids
(Pietsch 1974).

Skin spines. — Minute dermal spines (approxi-
mately 0.03-0.1 1 mm long) are present in the skin

Illicial
bone

Remnant of 2nd
cephalic ray

Pterygiophore
of illicium

Figure 15. — Bones of illicial apparatus of Melanocetus murrayi,
LACM 31501-3, 84 mm SL, left lateral view. Cartilage stippled.

of the two species examined osteologically. In M.
johnsoni they are most numerous on the side of the
trunk under the dorsal fin ( where there are about 6
spines/mm2)but become progressively more
widely scattered anteriorly and finally disappear
in the area of the upper and lower jaws
(Struhsaker 1962). In the two specimens of M.
murrayi examined osteologically the spines are
confined to the caudal peduncle.

SYSTEMATICS

Family Melanocetidae Regan 1912

Type genus Melanocetus Giinther 1864

Diagnosis. — The metamorphosed females of the
Melanocetidae are distinguished from those of all
other ceratioid families by having the following
combination of characters: jaws equal anteriorly;
supraethmoid present; parietals present; ptero-
sphenoid present; anterior maxillomandibular lig-
ament absent (Pietsch 1972a); hyomandibular
with a double head; hypohyals 2; branchiostegal
rays 6; operculum bifurcate, upper fork reduced;
suboperculum slender, as long as lower fork of
operculum, with strong anterior spine; pharyn-
gobranchials I and IV absent; epibranchial I
reduced; a single ossified basibranchial;
epibranchial and ceratobranchial teeth absent;
epurals absent; only an ossified remnant of second
cephalic ray present; dorsal fin rays 13-17, anal fin

67

FISHERY BULLETIN: VOL 78, NO. 1

Table 2. Fin ray frequencies for females of Melanocetus species.

Species

Melanocetus johnsoni
Melanocetus polyactis
Melanocetus niger
Melanocetus eustalus
Melanocetus murrayi

Total

32
38

Dorsal

12 13 14 15 16 17 3

70
4
3

29

106

64
4
2
1

71

Anal

1 136

13

5

1

62

1 217

Pectoral (both sides)

1

5 15 16 17 18 19 20 21 22 23

1 13 34 69 36 12 2

1 2 3 12 4 2 1

2 2 5 1
2

5 17 37 8 5 1

2 5 19 52 47 88 46 15 3

Supracleithrum

B

^

Radials

Coracoid

Cleithrum

Postcleithrum

Figure 16. — Lateral view of pectoral girdle, pectoral radials, and pelvic
bone: A. Melanocetus murrayi, LACM 31501-3, 84 mm SL; B. M. johnsoni,
LACM 32786-1, 75 mm SL. Cartilage stippled.

Pelvic bone

rays 4 (rarely 3 or 5), caudal fin rays 9 (1-6-2);
ossified posteroventral process of coracoid absent;
pectoral radials 4, fusing to 3 with growth; pelvic
bones expanded distally; esca without denticles;
minute, widely spaced skin spines present in at
least some species.

The metamorphosed males of the Melanocetidae
are distinguished from those of all other ceratioid
families in having the following combination of
characters: free-living; jaw teeth absent; upper
denticular with 2-3 semicircular series of strong,
recurved denticles, fused with a median series of
3-9 enlarged dermal spines that articulate with
the pterygiophore of the illicium; lower denticular
with 10-23 recurved denticles, fused into a median
and two lateral groups; eyes directed laterally,
elliptical in shape, pupil larger than lens; olfac-

tory organs large, nostrils lateral, nasal area un-
pigmented, inflated; dorsal fin rays 12-16, anal fin
rays 4, caudal fin rays 9 (1-6-2); skin spinulose or
naked.

Description. — Females relatively short and deep,
globular (but often appearing highly compressed
apparently due to deformation upon capture, com-
pare Figures 17, 18); head short; mouth large,
nearly vertical, cleft not extending past eye; lower
jaw with a well-developed symphysial spine; oral
valve weakly developed; two nostrils on each side
on distal surface of a rounded papilla; eye small,
subcutaneous, appearing through a circular,
translucent area of integument within a shallow,
orbital pit formed between sphenotic and frontal
bones; gill opening oval in shape, situated posteri-

68

PIETSCH and VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

Figure 17. — Anterior view of Melanocetus johnsoni, LACM
31484-1, 85 mm SL. Drawn by Elizabeth Anne Hoxie.

or to pectoral lobe; all four epibranchials closely
bound together by connective tissue; anterior half
of ceratobranchial I bound to medial surface of
ceratohyal by connective tissue, posterior half
free; gill filaments present on anteriormost tip of
ceratobranchial I and full length of cerato-
branchials II through IV; pseudobranch absent; no
opening behind fourth gill arch; ovaries paired;
pyloric caeca absent.

Illicial length 23.1-60.8^f SL; anteriormost tip
of pterygiophore of illicium exposed, emerging on
snout between eyes, its posterior end concealed
under skin; escal bulb simple, usually with a
rounded or conical, distal prolongation, and often
with posterior and anterior crests; elongate ap-
pendages and filaments absent.

Jaw teeth slender, recurved, and depressible,
some slightly hooked distally, those in lower jaw
less numerous, but slightly longer than those in
upper jaw; number of teeth in lower jaw 32-142, in
upper jaw 29-178; longest tooth in lower jaw 6.9-

FlGURE 18.— Holotype of Melanocetus eustalus, LACM 30037-
12, 111 mm SL, anterior view. Drawn by Elizabeth Anne Hoxie.

69

FISHERY BULLETIN: VOL. 78, NO. 1

25.0'7r SL; vomer with 0-12 teeth; pharyngobran-
chials II and III heavily toothed.

Color in preservative dark brown to black over
entire surface of body (except for distal portion of
escal bulb) and oral cavity; all fins colorless in
specimens less than about 40 mm SL (except for
caudal rays in adolescent M. murrayi, Bertelsen
1951, fig. 161).

Pectoral fin rays 15-23 (Table 2); pelvic fins ab-
sent.

The following measurements, in percent of
standard length, are summarized for females (20-
120 mm SL) of all species: head depth 42.5-82.0;
least outside width between frontals 9.1-28.6;
head width 22.6-45.0; premaxillary length 36.3-
76.0; lower jaw length 36.7-78.0; width of pectoral
fin lobe 6.1-17.8; escal bulb width 1.9-11.3

For description of males see Diagnosis above
and Bertelsen (1951).

Genus Melanocetus Giinther 1864

Females

Melanocetus Giinther 1864:301-302, pi. 25 (type
species Melanocetus johnsoni Giinther 1864, by
monotypy).

Melanocetus (subgenus Liocetus) Giinther
1887:56, pi. 11, fig. A (type species Melanocetus
murrayi Giinther 1887, by monotypy).

Liocetus Goode and Bean 1896: 495-496, fig. 407
(type species Melanocetus murrayi Giinther
1887, by monotypy).

Melanocoetus Smith 1949:429 (erroneous spelling
of Melanocetus, therefore taking the same type
species, Melanocetus johnsoni Giinther 1864).

Linocetus Bertelsen 1951:40, 44 (erroneous spell-
ing of Liocetus, therefore taking the same type
species, Melanocetus murrayi Giinther 1887).

Males

Rhynchoceratias Parr 1927:30-33, fig. 11-12 (in
part; type species Rhynchoceratias brevirostris
Regan 1925, by subsequent designation of
Fowler 1936).

Centrocetus Regan and Trewavas 1932:53, fig. 79
(type species Centrocetus spinulosus Regan and
Trewavas 1932, by monotypy).

Xenoceratias Regan and Trewavas 1932:54-57, fig.
80-84 (type species Xenoceratias longirostris
Regan and Trewavas 1932, by subsequent des-
ignation of Fowler 1936).

Diagnosis and description same as for family.

Key to Species Based on Females

The following key will differentiate female specimens >20 mm SL (for males and larvae see Bertelsen
1951). The key should be used in conjunction with Figures 19-24.

lA.

IB.
2A.

2B.

3A.

3B.

4A.

Escal bulb width 11.3% SL in 111 mm specimen (Figures 18, 28); longest lower jaw tooth
5.9% SL in 111 mm specimen Melanocetus eustalus n. sp. (single known female)

Escal bulb width <10% SL (Figure 17); longest lower jaw tooth 6.9-25.0% SL 2

Anterior margin of vomer deeply concave (Figure 2); least outside width between frontals
9.1-17.8% SL (Figure 19); number of lower jaw teeth 46-142 (>60 in specimens 25 mm
and larger) (Figure 20); escal bulb width 1.9-5.1% SL (<3% SL in specimens >50 mm
SL) Melanocetus murrayi Giinther 1887

Anterior margin of vomer nearly straight (Figure 1); least outside width between frontals
13.5-28.6% SL (Figure 19); number of lower jaw teeth 32-90 (Figure 20); escal bulb width
3.8-8.6% SL (>4% SL in specimens >50 mm SL) 3

Longest lower jaw tooth 8.4-25.0% SL (Figure 21); esca with compressed posterior and

(usually) anterior crests (Figure 25); distribution nearly cosmopolitan

Melanocetus johnsoni Giinther 1864

Longest lower jaw tooth 6.9-13.1% SL (Figure 21); esca without posterior or anterior crests

(Figures 26, 27); distribution restricted to eastern tropical Pacific 4

Number of lower jaw teeth 58-90 (Figure 22); escal bulb width 5.2-8.5% SL (Figure 23);
illicium length 34.6-56.0% SL (Figure 24); escal bulb with a conical, distal prolongation
occasionally pigmented on tip (Figure 26) Melanocetus polyactis Regan 1925

70

PIETSCH and VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

4B. Number of lower jaw teeth 37-57 (Figure 22); escal bulb width 3.8-5.0% SL (Figure 23);
illicium length 29.8-38.8% SL (Figure 24); escal bulb with a low, rounded distal prolon-
gation usually darkly pigmented on tip (Figure 27) Melanocetus niger Regan 1925

20 0

• M.

johnsoni

n

= 107

I I I 1

T -1—

r 1 —

F

°M.

murrayi

n

= 61

c

17 5

• '

o

15 0

■

%

•

•
•

• •

••

•

-

o

12 5
100

■

• • •

••••

•
• •

:/oB

o o

o

o

o ■

■a

3
O

c/>

75
50
2 5

. • • •
•t •

, •• • • o • o8 o o

'm ••° o °o^oo°

Co Q r^ O O

Ooo o ^ °

o

OOo

o
o
o

o

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.

.

1 1 I 1 I 1

1

1

1 1 1 1

,

1 '

1 1

10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100 105 110 115 120

Standard Length in mm

Figure 19. — Relationship between least outside width of frontals and standard length for two species oi Melanocetus.

Melanocetus johnsoni Giinther 1864
Figures 1, 3, 6, 16B, 17, 19-21, 25, 30, 31

Females

Melanocetus johnsoni Giinther 1864:301-303, pi.
25 (original description, single specimen,
holotype BMNH 1864.7.18.6, 64 mm, Madeira,
24 December 1863); Liitken 1871:64, 74 (com-
parison with Oneirodes eschrichtii); Liitken
1872:329-340, 343 (after Liitken 1871); Giinther
1880:473, fig. 211 (after Giinther 1864);
Giinther 1887:56-57 (after Giinther 1864, com-
parison with M. murrayi); Vaillant 1888:346
(after Giinther 1864); Goode and Bean 1896:494,
fig. 406 (description after Gunther 1864); Gill
1909:582, 584, 585, fig. 20 (after Gunther 1864,
Goode and Bean 1896); Regan 1912:286, fig. 60
(cranial osteology); Regan 1913:1096 (descrip-
tion of additional specimen, natural history);
Regan 1926:18, 32, 33, fig. 10 (description of
additional material, cranial osteology; M.
krechi and M. rotundatus synonyms); Parr
1927:29 (description of additional specimen);
Norman 1930:354 (additional record); Regan
and Trewavas 1932:27-29, 49-52, fig. 19-21,
22A, B, 72, 73 (description of additional mate-
rial, osteology, and esca figured, in key); Fowler

1936:1143, 1144, 1346, 1363 (description after
Giinther 1864, Regan 1926, Norman 1930);
Norman 1939:114 (additional material); Koe-
foed 1944:3-5, pi. 1, fig. 1 (description of addi-
tional specimen, comparison with M. murrayi;
Beebe and Crane 1947:152 (description of addi-
tional specimen, color); Fowler 1949:158-159
(listed); Bertelsen 1951:7, 40-41, 43-46, 48-53,
fig. 13, 15, 17-19, tables 4, 6 (description of
females, males, larvae, comparison with all
known material, in key); Grey 1956:235-236
(synonymy; distribution); Monod 1960:687, fig.
80 (pectoral radials); Maul 1961:91-92, fig. 1 (de-
scription of additional material); Maul
1962a:6-7 (description, additional material);
Struhsaker 1962:841-842 (description, addi-
tional specimen, skin spines); Bussing 1965:222
(additional specimen); Fitch and Lavenberg
1968:127, fig. 70 (distinguishing characters,
natural history); Pietsch 1972a:29, 35, 36, 38, 45
(osteological comments); Maul 1973:667
(synonymy, after Bertelsen 1951).
Melanocetus krechi Brauer 1902:293-294 (original
description, single specimen, holotype ZMHU
17688, 45 mm, Valdivia stn. 239, Indian Ocean,
5°42' S, 43°36' E, 0-2,500 m); Brauer 1906:319-
320, pi. 15, fig. 1, 2 (description after Brauer
1902); Gill 1909:583, 584, fig. 21 (after Brauer

71

FISHERY BULLETIN: VOL. 78, NO. 1

1 -» «

-I

T 1 1

1 1

1 1—

T 1

r 1 1

I 1

1 I

1 1 —

140

• M. johnspni n

= 116

0

0°

130

o M. murrayi n

= 66

0

0

80

0
0

120

-

0

0

0

-

110

■

0

r°->

0

0
0

0

0

0

-

100

0 °
0

0

0

0 0^0
0 °

90

0

80

•

0 0

°o

•

•

0 -

70

.0° °

0 0
0

0

0

•

••

0

•
•

•
•

•

•

•

. %

-

60

-

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•• *

•^*

•

•

•

• -

.0 -»^„ •

• 1 •

•

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•

«•

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•

SO
40

•

• •

•

•
•

•
•

•

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•

•

-

30

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J 1 1 —

1

,

1 1

1 1 1

1 1

1 1

1 1 .

10 IS 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100 105 110 115 120

Standard length in mm

Figure 20. — Relationship between number of lower jaw teeth and standard length for two species of Melanocetus.

1902, 1906); Murray and Hjort 1912:87, 614 (in
part, additional specimen, misidentification);
Borodin 1931:84 (additional specimen, misiden-
tification); Regan and Trewavas 1932:49, 52, fig.
74 (misidentification, in key); Fowler 1936:
1143, 1144 (description after Brauer 1902,
1906, in key); Bertelsen 1951:40, table 4 (com-
parison with all known material).

Melanocetus rotundatus Gilchrist 1903:206-208,
pi. 15 (original description, two specimens, both
lost [see Comments, p. 76], the largest about 28
mm, off Cape Point and Natal coast. South Af-
rica, 1,098 m); Gilchrist and Thompson
1917:417 (after Gilchrist 1903); Barnard
1927:1007, pi. 37, fig. 5 (after Gilchrist 1903);
Bertelsen 1951:48 (in synonymy of M. john-
soni).

Melanocoetus rotundatus, Smith 1949:429, fig.
1232 (after Gilchrist 1903); Penrith 1967:187,
188 (type material lost; a synonym of M.
johnsoni).

Melanocetus ferox Regan 1926:33, pi. 9, fig. 1 (orig-
inal description, single specimen, holotype
ZMUC P9257, 78 mm, Dana stn. 1208(14), Gulf
of Panama, 6°48' N, 80°33' W, 3,100 m wire,
1715 h, 16 January 1922); Regan and Trewavas
1932:49, 52, fig. 75 (in part, only holotype, addi-

72

tional material here referred to M. polyactis, in
key); Beebe and Crane 1947:152 (in part, only
holotype); Bertelsen 1951:44, 53, table 4 (in
part, only holotype; comparison with all known
material, in key); Grey 1956:237 (synonymy,
distribution).

Melanocetus cirrifer Regan and Trewavas
1932:52-53, fig. 76A, 77, pi. 2, fig. 1 (original
description, two females, lectotype ZMUC
P9258, 25.5 mm, Dana stn. 3678(2), Banda Sea,
4°05' S, 128°16' E, 4,000 m wire, bottom depth
4,700 m, 1840 h, 24 March 1929, in key); Ber-
telsen 1951:44, 53, table 4 (description, com-
parison with all known material, in key); Grey
1956:237 (synonymy, distribution).

Melanocetus niger, Gregory 1933:400, fig. 272
(misidentification, osteology).

Melanocetus megalodontis Beebe and Crane
1947:152, fig. 1 (original description, single
specimen, holotype CAS-SU 46488 [originally
NYZS 25791], 25.5 mm, Templeton Crocker Ex-
pedition stn. 165 T-3, eastern tropical Pacific,
20°36' N, 115°07' W, 0-915 m, 17 May 1936);
Bertelsen 1951:43, 48, table 4 (description, com-
parison with all known material, in key); Grey
1956:235 (synonymy, distribution); Mead
1958:133 (holotype passed to CAS).

PIETSCH and VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

12 5

1 1 T —

• M. johnsoni
▼ M. polyactis

1 1 1 1 II

n =139

n = i3 ,

1 1

1

1 1 1

1

•

T 1

r

1 1—

1 1—

12 0

A M. niger n

=6

•

-

115

-

•

•

■

110

-

•

•• •

-

10 5

-

«

-

100

"

. •

.

• •

•

• -

95

-

•

•

•

-

90

"

.

«

.

•

-

85

■"

• . • ..

•

-

80

-

•

-

75

-

•• •

•

-

70

■"

. . .
• •

-

65

•

• •••

•

^

-

60

• •

T

-

55

•

•• ••

a

-

50

•

• . • . ▼

-

45

•
•

•

-

40

• .»•:

"

35

•• • .

: -

-

30
2 5

• ... •
IV..

T

-

2 0

-.. .▼ A

-

15
1 n

T

1 1 1 1 1 1

J 1

1

1 1 I .

'

1 1

1 1

1 '

10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100 105 110 115 120

Standard length in mm

Figure 21. — Relationship between length of longest lower jaw tooth £ind standard length for three species oi Melanocetus.

Melanocetus sp. Roule and Angel 1930:121, pi. 6,
fig. 159 (additional material).

Males

Centrocetus spinulosus Regan and Trewavas
1932:53, 54, fig. 79 (original description, two
specimens, lectotype ZMUC P9246, 15.5 mm,

Dana stn. 3847(2), Indian Ocean, 12°02' S,

96°43' E, 3,000 m wire, bottom depth 2,825 m,

2100 h, 11 October 1929).
Xenoceratias macracanthus Regan and Trewavas

1932:11, 12 (erroneous spelling of specific name,

listed).
Xenoceratias micracanthus Regan and Trewavas

1932:54, 55, fig. 81 (original description, single

73

FISHERY BULLETIN: VOL. 78, NO. 1

Figure 22.— Relationship between
number of lower jaw teeth and standard
length in two species oi Melanocetus .

100

90

.c

'a> 80
a>

.2. ''°

a>

S 60 -

o

° 50

40

30

20

▼ M. pojyactis n = i5
A M. niger n=6

»y ▼

I I I 1 L.

I I I 1-

10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85

Standard length in mm

Figure 23.— Relationship between
escal bulb width and standard length in
two species oi Melanocetus .

E
E
c:

4.5

1

-r- ■ 1 1

1

1

1 1

1 1 1

I 1 1

4.0

-

A

M.
M.

polyactis n =
niger n=5

11

A

3.5

-

T

▼

"

3.0

-

▼

A

2.5

-

▼

-

2.0

-

T
W

▼

▼
A

A

-

1.5

-

T

A

-

1.0

-

▼

■

.5
n

-

1

1 r 1

1

1 1

1 1 1

1 J J

10

15 20 25 30 35 40 45 50 55 60 65 70 75 80 85

Standard length in mm

specimen, holotype ZMUC P9250, 28 mm, Dana
stn. 4000(8), eastern tropical Atlantic, 0°31' S,
11°02' W, 4,000 m wire, bottom depth 3,750 m,
0630 h, 4 March 1930, in key); Fowler 1936:1364
(listed).

Xenoceratias heterorhynchus Regan and Tre-
wavas 1932:54, 56, fig. 82 (original description,
single specimen, holotype ZMUC P9248, 27 mm,
Dana stn. 3716(2), South China Sea, 19°18.5' N,
120°13' E, 3,000 m wire, bottom depth 3,225 m,
1400 h, 22 May 1929, in key); Grey 1956:236
(synonymy, distribution).

Xenoceratias laeuis Regan and Trewavas 1932:54,
57, fig. 83 (original description, single specimen,
holotype ZMUC P9249, 23 mm, Dana stn.
3731( 13), South China Sea, 14°37 ' N, 1 19°52 ' E,
2,000 m wire, bottom depth 2,300 m, 0200 h, 17
June 1929, in key).

Xenoceratias brevirostris Regan and Trewavas
1932:54, 57, fig. 84 (original description, single
specimen, holotype ZMUC P9247, 19 mm, Dana
stn. 3739(8), Celebes Sea, 3°20' N, 123°50' E,
3,000 m wire, bottom depth 4,475 m, 0700 h, 2
July 1929, in key).

Xenoceratias braueri Koefoed 1944:6, fig. 2 (origi-
nal description, single specimen, holotype
UBZM 4309, 18.5 mm, Michael Sars North At-
lantic Deep-Sea Expedition stn. 53, central
North Atlantic, 34°59' N, 33°01' W, 2,600 m
wire, bottom depth 2,615-2,865 m, 8-9 June
1910).

Melanocetus johnsoni, Bertelsen 1951:44, 48-53,
fig. 17C, D, F-H, table 6 (synonymy, distribu-
tion, comparison with all known material, in
key); Grey 1956:236 (synonymy, distribution);
Maul 1962b:36-37, fig. 2 (description of addi-

74

PIETSCH and VAN DUZER; SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

FIGURE 24.— Relationship between
Ulicium length and standard length
in two species of Melanocetus.

E
E

e:

32 5

■

— r

T

— r-

M.

pjolyacLis n = i2

I

r r - ■

-» 1 1

A

■

30.0

-

A

M.

niger n = 6

■

275

-

T

A

-

25.0

-

-

225

-

▼

-

20.0

-

▼

-

175

-

▼

A

-

15.0

-

T ▼▼ A

12.5

-

T

▼
T

A

■

10.0

-

T

T
A

-

75

-

■

5.0

9 «i

-

— 1_

I

1 1

_l 1 1

1 1

-

to 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85

Standard length in mm

tional specimen); Maul 1973:667 (synonymy,
after Bertelsen 1951).

Material. — Metamorphosed females, 346 (10-119
mm): AMS, 33 (11-88 mm); BMNH, 16 (13-64 mm);
CAS, 1 (25.5 mm); FSM, 10 (13-76 mm); lOAN, 35
(12-75 mm); lOS, 7 (35-91 mm); ISH, 82 (15-119
mm); LACM, 65 (13.5-83 mm); MCZ, 25 (12-75
mm); NMNZ, 7 (12-55 mm); ROM, 4 (15-56 mm);
SAM, 6 (10-13 mm); UMML, 3 (27-82 mm);
USNM, 15 (12-85 mm); ZMUC, 37 (11.5-89 mm).

Diagnosis. — A species of Melanocetus unique in
having the following combination of characters:
anterior margin of vomer nearly straight (Figure
1); least outside width between frontals 13.5-
28.67c SL (Figure 19); number of lower jaw teeth
32-78 (Figure 20), length of longest lower jaw
tooth 8.4-25.0% SL (Figure 21); width of pectoral
fin lobe 10.7-17.87f SL; escal bulb width 4.3-8.6%
SL; illicium length 32.4-60.8'y^ SL; esca with pos-
terior and (usually) anterior crests (Figure 25);
minute skin spines present over most of body;
integument relatively thick (1.55 mm).

Description. — Escal bulb slightly compressed
with a low, rounded or conical distal prolongation
nearly always darkly pigmented on tip; a com-
pressed posterior crest usually darkly pigmented,

becoming larger and more conspicuous with
growi;h; and a considerably smaller, compressed,
anterior crest present in some specimens (Figure
25); integument relatively thick (cross sections
measure 1.55 mm in thickness), not easily torn,
usually retaining heavy pigmentation during
fixation and preservation.

Number of upper jaw teeth 48-134; dorsal fin
rays 13-15 (rarely 16), pectoral fin rays 17-22
(rarely 23) (Table 2).

Distribution. — Melanocetus johnsoni has a wide
horizontal distribution in tropical and subtropical
waters of all three major oceans of the world (see
Distribution, p. 83). Compared with M. murrayi, it
appears to occupy relatively shallow depths: about
62% of the material (for which data was available)
was captured by open nets fished at maximum
depths of 1,000 m; 827c of the material can be
accounted for by gear fished above 1,500 m, and
98% by gear fished above 2,100 m (see Distribu-
tion, p. 83).

Comments. — Melanocetus krechi Brauer (1902)
was synonymized with M. johnsoni by Regan
(1926), resurrected by Regan and Trewavas
(1932), and tentatively synonymized again with
M. johnsoni by Bertelsen (1951). From the de-
scription and figure given by Brauer (1902, 1906)

75

FISHERY BULLETIN: VOL. 78, NO. 1

I .5 w ,

2 mm

FIGURE 25.— Escae ofMelanocetusjohnsoni: A. ISH 1261/71, 21 mm SL; B. ISH 753/71, 38 mm SL; C. MCZ 49849, 75 mm SL; D. ISH

1534/71, 78 mm SL.

and based on a much greater knowledge of varia-
tion within the genus, there can be little doubt
that this nominal form has been correctly placed
within the synonymy of M. johnsoni.

Melanocetus ferox was described from a single
specimen (78 mm) collected in the Gulf of Panama
(Regan 1926). Two additional specimens of this
nominal form were listed by Regan and Trewavas
(1932). A thorough comparison of all known mate-
rial led Bertelsen ( 1951 , table 4) to suspect that M.
ferox might represent individual variation of M.
niger. The holotype of M. ferox, however, has rela-
tively long lower jaw teeth (longest, 12.0% SL;
Figure 21). In this, and in all other morphometric
and meristic characters used here, it fits well
within the material here recognized as M.
johnsoni. Although the esca of the holotype is in
poor condition, traces of a posterior crest remain.
For these reasons M. ferox is synonymized with M.
johnsoni. The two additional specimens identified
as M. ferox by Regan and Trewavas (1932) (ZMUC
P92210, 30.5 mm; BMNH 1932.5.3.6, 42 mm) have
short jaw teeth; in this and in other ways they fit
well within the material of M. polyactls (see p. 77).

Melanocetus cirrifer Regan and Trewavas
(1932), described on the basis of two small females,
was tentatively maintained by Bertelsen (1951)
because of supposed differences in escal morphol-
ogy and pigmentation which now can easily be

76

shown to be part of the variation found within M.
johnsoni. Melanocetus megalodontis Beebe and
Crane (1947), based on a single specimen, was
distinguished from all other species of the genus
by ". . . the character of the illicium; in the great
length and robustness of the fangs . . . and in the
shortness of the lower jaw. . . ." However, speci-
mens of M. johnsoni may have longer teeth and
individuals of several species of Melanocetus may
have as short a lower jaw (Bertelsen 1951, table 4).
Further (as predicted by Bertelsen 1951), the
"peculiar minute distal flaps" of the esca are arti-
facts. In all ways the holotype of M. megalodontis
fits well within the variation now known to occur
within M. johnsoni. Thus these nominal forms, M.
cirrifer and M. megalodontis , are placed within
the synonymy of M. johnsoni.

Finally, the holotype and paratype of M. rotun-
datus Gilchrist (1903) have been lost. The cir-
cumstances of their demise are the same as for the
holotype of Dolopichthys cornutus described
elsewhere (Pietsch 1972b; see also Barnard 1927,
Penrith 1967). Although Gilchrist's (1903) origi-
nal description is poor, the figure provided by him
shows rather long jaw teeth, a long illicium bear-
ing a relatively large escal bulb, and a large pec-
toral fin lobe. This combination of characters
makes it nearly certain that M. rotundatus is a
synonym of M. johnsoni (Penrith 1967).

PIETSCH and VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

Melanocetus polyactis Regan 1925
Figures 21-24, 26, 30

Females

Melanocetus polyactis Regan 1925:565 (original
description, 3 specimens, lectotype designated
by Bertelsen 1951, ZMUC P9260, 61 mm, Dana
stn. 1206(3), Gulf of Panama, 6°40' N, 80°47' W,
3,500 m wire, 1845 h, 14 January 1922); Regan
1926:34, pi. 8, fig. 2 (description after Regan
1925); Regan and Trewavas 1932:53, fig. 78
(listed, after Regan 1925, 1926); Bertelsen
1951:44, 54-55, tables 4, 7, 8 (description, addi-
tional material, 2 males, 6 larvae, comparison
with all known material, in key); Grey 1956:238
(synonymy, distribution).

Melanocetus niger Regan 1925:565 (in part, 3 of 11
cotypes [see Comments, p. 79], all Gulf of
Panama); Regan 1926:33, pi. 8, fig. 1 (in part,
description, 4 additional specimens); Regan and
Trewavas 1932:53, fig. 76B (in part, listed, after
Regan 1925, 1926); Bertelsen 1951:44, 53, table
4 (in part, description, comparison with all
known material, in key); Grey 1956:237 (in
part, synonymy, distribution).

Melanocetus ferox, Regan and Trewavas 1932:49,
52, fig. 75 (in part, nontype material only, in
key); Bertelsen 1951:44, 53, table 4 (in part,
nontype material only, comparison with all
known material, in key); Grey 1956:237 (in part,
after Bertelsen 1951, synonymy, distribution).

Males

Rhynchoceratias rostratus, Regan 1926:44 (in part,
misidentification).

Rhynchoceratias leucorhinus, Regan 1926:44 (in
part, misidentification).

Material. — Metamorphosed females, 15 (16.5-61
mm): BMNH 1925.8.11.30, 26 mm; BMNH
1925.8.11.32, 42 mm (paralectotype); BMNH
1932.5.3.6, 42 mm; lOAN uncatalogued, 33 mm;
LACM 33603-4, 2 (16.5 and 30 mm); LACM
33574-5, 17 mm; LACM 33624-1, 33 mm; LACM
33629-3, 35 mm; ZMUC P92155, 25 mm (paralec-
totype); ZMUC P921974, 26 mm; ZMUC P9251, 29
mm; ZMUC P92210, 30.5 mm; ZMUC P9253, 47
mm; ZMUC P9260, 61 mm (lectotype).

The following adolescent females, all collected
from the eastern tropical Pacific, are only tenta-

tively referred to M. polyactis: LACM 33618-2, 16
mm; LACM 31119-2, 2 (17 and 18 mm); LACM
31109-2, 18 mm; LACM 31120-20, 2 (18 and 19
mm); LACM 31126-29, 2 (19.5 and 20 mm).

Metamorphosed males, 2: ZMUC P92460, 16
mm (22 mm total length (TL)); ZMUC P92459,
19.5 mm (30 mm TL).

Larvae, 6 (2 males, 4 females, 3-9 mm TL):
ZMUC P92461; ZMUC P92462.

Diagnosis. — A species of Melanocetus unique in
having the following combination of characters:
anterior margin of vomer nearly straight; least
outside width between frontals 18.0-26.0% SL;
number of lower jaw teeth 58-90 (Figure 22);
length of longest lower jaw tooth 9.3-13.1% SL
(Figure 21); width of pectoral fin lobe 10.9-16.0%
SL; escal bulb width 5.2-8.5% SL (Figure 23);
illicium length 34.6-56.0% SL (Figure 24); esca
with a conical, distal prolongation, crests absent
(Figure 26); integument relatively thick.

Description. — Escal bulb not compressed, with
conical distal prolongation nearly always slightly
constricted at base, and usually as long as or
longer than length of escal bulb, pigmented on tip
in some specimens, posterior and anterior crests
absent (Figure 26); integument as in M.johnsoni.
Number of upper jaw teeth 42-120; dorsal fin
rays 14-17; pectoral fin rays 17-21 (rarely 22 and
23) (Table 2).

Distribution. — Melanocetus polyactis appears to
be restricted to the eastern tropical Pacific Ocean
where 15 specimens have been collected between
lat. 10° N and 13° S as far west as long. 88° W (see
Distribution, p. 83). Approximately 67% of the
material was captured by open nets fished at max-
imum depths of 1,000 m or below.

Comments. — Melanocetus polyactis is most easily
confused with M. niger. Both forms are similar in
having exceptionally short lower jaw teeth (Fig-
ure 21). They differ significantly, however, in the
number of lower jaw teeth, escal bulb width, and
illicial length (see Key, Figures 22-24).

Part of the material originally listed as M. niger
has been reallocated to M. polyactis (see Com-
ments, p. 79). Also included with the material of M.
polyactis are two specimens (ZMUC P92210, 30.5
mm; BMNH 1932.5.3.6, 42 mm) previously iden-
tified as M. ferox by Regan and Trewavas (1932).

77

FISHERY BULLETIN; VOL. 78, NO. 1

B

1 mm

Figure 26.— Escae ofMelanocetuspolyacUs: A. LACM 33603-4, 16.5 mm SL; B. Paralectotype, ZMUC P92155, 25 mm SL (lack of distal
pigmentation probably due to abrasion); C. ZMUC P921974, 26 mm SL; D. ZMUC P9251, 29 mm SL (a cotype of M. niger); E. LACM
33603-4, 30 mm SL; F. ZMUC P92210, 30.5 mm SL; G. LACM 33629-3, 35 mm SL; H. Lectotype, ZMUC P9260, 61 mm SL.

Melanocetus niger Regan 1925
Figures 21-24, 27, 30

Melanocetus niger Regan 1925:565 (original de-
scription, in part, 4 of 1 1 cotypes [see Comments,
p. 79] all Gulf of Panama, lectotype hereby des-
ignated, ZMUC P9252, 80 mm, Dana stn.
1208(4), 6°48' N, 80°33 ' W, 3,500 m wire, 0810 h,
16 January 1922); Regan 1926:33, pi. 8, fig. 1 (in
part, description, 4 additional females); Regan
and Trewavas 1932:53, fig. 76B (in part, listed
after Regan 1925, 1926); Beebe and Crane
1947:153-154 (in part, description of 4 addi-
tional females not seen by us); Bertelsen
1951:44, 53, table 4 (in part, description, com-
parison with all known material, in key); Grey
1956:237 (in part, synonymy, distribution).

Ma^erm/. — Metamorphosed females, 6 (22-80
mm): BMNH 1925.8.11.29, 47 mm (paralec-
totype); lOAN uncatalogued, 77 mm; ZMUC

78

P9254, 22 mm (paralectotype); ZMUC P9256, 37
mm (paralectotype); ZMUC P921973, 42 mm
(Galathea stn. 727); ZMUC P9252, 80 mm (lec-
totype).
Males and larvae unknown.

Diagnosis. — A species of Melanocetus unique in
having the following combination of characters:
anterior margin of vomer nearly straight; least
outside width between frontals 14.3-24.3% SL
number of lower jaw teeth 37-57 (Figure 22)
longest lower jaw tooth 6.9-10.5% SL (Figure 21)
width of pectoral fin lobe 9.1-13.5% SL; escal bulb
width 3.8-5.0% SL (Figure 23); illicium length
29.8-38.8% SL (Figure 24); esca without crests
(Figure 27); integument relatively thick.

Description. — Escal bulb not compressed, with a
low, rounded or conical distal prolongation nearly
always pigmented on tip; anterior and posterior

PIETSCH and VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

crests absent (Figure 27); integument as in M.
johnsoni.

Number of upper jaw teeth 29-86; dorsal fin rays
14-15; pectoral fin rays 18-21 (Table 2).

Distribution. — All six known specimens of M.
niger were collected in the Gulf of Panama and
adjacent waters of the eastern tropical Pacific
Ocean as far west as approximately long. 90" W
(see Distribution, p. 83). Eighty-three percent of
the material was captured by open nets fished at
maximum depths of 1,500 m and below.

Comments. — Melanocetus niger was briefly de-
scribed by Regan ( 1925) from seven specimens col-
lected in the Gulf of Panama without type desig-
nation and without a listing of individual sizes,
station numbers, or other means of identification.
Regan (1926) added four more specimens without
providing means of separating the original seven.
All 11 specimens bear labels indicating cotype
status and all are treated here as part of the origi-
nal type material. One of these is designated the
lectotype (ZMUC P9252, 80 mm), three are re-
ferred to M. polyactis (BMNH 1925.8.11.30, 26
mm; ZMUC P9251, 29 mm; ZMUC P9253, 47 mm),
three unidentifiable specimens are listed below as
Melanocetus sp. (ZMUC P9255, 13.5 mm; BMNH
1925.8.11.31, 14 mm; BMNH 1925.8.11.28, 43
mm), and one is unaccounted for and presumed
lost [Dana stn. 1209(3), 37 mm total length). The

remaining three specimens are recognized as
paralectotypes of M. niger.

Melanocetus eustalus n. sp.
Figures 18, 28, 30

Melanocetus ferox, Pietsch 1972b: 10 (misiden-
tification, luminescence); Brewer 1973:25 (after
Pietsch 1972b, distribution).

Melanocetus sp. Pietsch 1976:782, 783 (reproduc-
tion).

Material. — A single female, the holotype, LACM
30037-12, 111 mm, Velero IV stn. 11748, eastern
Pacific off Mazatlan, Sinaloa, Mexico, 21°39' N,
106°58' W, 3 m IKMT, 0-1,675 m, bottom depth
2,820 m, 1320-2136 h, 11 November 1967.

Diagnosis. — A species of Melanocetus unique in
having the following combination of characters:
anterior margin of vomer nearly straight; least
outside width between frontals 18.0% SL; number
of lower jaw teeth 60; longest lower jaw tooth 5.9%
SL; illicium length 30.6% SL; width of pectoral fin
lobe 9.9% SL; escal bulb width 11.3% SL; esca
without crests (Figures 18, 28); integument rela-
tively thick.

Description of holotype. — Escal bulb large
(length 14.4% SL), slightly compressed, with a low
conical distal prolongation, pigment absent; pos-

, 1 mm

Figure 27.— Escae of Melanocetus niger: A. Paralectotype, ZMUC P9256, 37 mm SL; B. Paralectotype, BMNH 1925.8.11.29, 47 mm SL;

lOAN uncatalogued, 77 mm SL; D. Lectotype, ZMUC P9252, 80 mm SL.

79

FISHERY BULLETIN: VOL. 78, NO. 1

terior and anterior crests absent (Figure 28);
integument as in M.johnsoni.

Gill opening exceptionally large, greatest
diameter 23.47f SL; number of upper jaw teeth 91;
vomerine teeth 8; dorsal fin rays 15; pectoral fin
rays 16 (Table 2).

Etymology. — The name eustalus is derived from
the Greek eustales, an adjective meaning well

equipped, in reference to the enormous esca of this
ceratioid.

Luminescence. — Upon capture, the holotype of
Melanocetus eustalus was maintained alive for
several minutes during which the bulb of the esca
glowed continuously with a bright, golden-orange
light. The amount of light actually emitted, how-
ever, appeared to be controlled by an up and down

80

FIGURE 28.-Holotype of Melanocetus eustalus, LACM 30037-12, 111 mm SL, lateral view. Drawn by Elizabeth Anne Hoxie.

PIETSCH and VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

movement of the darkly pigmented, inner wall of
the photophore of the esca. The glowing bulb was
almost entirely covered and uncovered four or five
times within a period of at least 1 min (B. G.
Nafpaktitis^; see Pietsch 1972b). A mechanism of
this kind would provide a rapid means of extin-
guishing light that may not only attract potential
mates and prey, but also predators.

Melanocetiis murrayi Gunther 1887

Figures 2, 4, 5, 7-15,

16 A, 19, 20, 29-31

Females

Melanocetus murrayi Gunther 1887:57, pi. 11, fig.
A (original description, two specimens, lec-
totype BMNH 1887.12.7.17, 71 mm. Challenger
stn. 106, central Atlantic, 1°47' N, 24=26' W,
0-3,386 m); Regan 1926:32 (description, addi-
tional material, in key); Parr 1927:27 (descrip-
tion, additional material); Regan and Trewavas
1932:27, 49-50, fig. 22C, 23, 71 (description, ad-
ditional material; pectoral radials, pelvic bone,
escae figured; in key); Beebe 1932:99-102, fig.
29, 30 (description of postlarvae); Parr 1934:7
(listed); Fowler 1936:1143, 1144-1145, 1346,
1363, fig. 483 (after Gunther 1887; Regan 1926;
in key); Koefoed 1944:3, 5 (description, compari-
son, additional material); Fowler 1949:158
(listed); Bertelsen 1951:40-48, fig. 16, tables 4, 5
(description of females, males, larvae, compari-
son with all known material, in key); Grey
1955:299 (additional material, color); Grey
1956:234 (synonymy; distribution); Monod
1960:687, fig. 80 (pectoral radials); Pietsch
1972a:34, 38 (osteological comments); Maul
1973:667 (synonymy, after Bertelsen 1951).

Melanocetus bispinosus Gunther 1880:473 (name
only); Goode and Bean 1896:495 (in synonymy).

Melanocetus (Liocetus) murrayi Gunther 1887:56
(original description, a distinct subgenus).

Liocetus murrayi, Goode and Bean 1896:495, fig.
407 (new combination, after Gunther 1887); Gill
1909:583, 584, fig. 22 (after Gunther 1887;
Goode and Bean 1896).

Melanocetus vorax Brauer 1902:294 (original de-
scription, single specimen, holotype ZMHU
17710, 85 mm, Valdiuia stn. 63, Gulf of Guinea,

'B. G. Nafpaktitis, Professor, Department of Biological Sci-
ences, University of Southern California, Los Angeles, CA
90007, pers. commun. November 1967.

2°00' N, 8°04' W, 0-2,492 m); Brauer 1906:320-
321, pi. 15, fig. 4 (description after Brauer 1902).
Fowler 1936:1143, 1144 (description after
Brauer 1902, 1906; in key).

Melanocetus johnsoni, Brauer 1906:319 (misiden-
tification); Regan 1926:33 (in part, misiden-
tification); Murray and Hjort 1912:609, 614,
618, fig. 469 (misidentification); Fowler 1936,
fig. 482 (figure after Brauer 1906).

Melanocetus krechi, Murray and Hjort 1912:614,
618 (in part, misidentification).

Melanocetus tumidus Parr 1927:28-29, fig. 10
(original description, single juvenile, holotype
BOC 2022, 15 mm,Pawnee Third Oceanograph-
ic Expedition stn. 11, western North Atlantic,
23°58' N, 77°26' W, 2,135 m wire, 2 March
1927); Regan and Trewavas 1932:49 (men-
tioned); Grey 1956:239 (synonymy, distribution,
a young female M. murrayi).

Melanocetus niger, Parr 1927:29 (misidentifica-
tion); Beebe 1929:18 (misidentification).

Males

Rhynchoceratias acanthirostris Parr 1927:31, fig.

11 (original description, single specimen,
holotype BOC 2011, 20 mm, Pawnee Third
Oceanographic Expedition stn. 22, western
North Atlantic, 23°37' N, 77°15' W, 2,135 m
wire, 12 March 1927); Parr 1930b: 130, 134
(anatomy, life history).

Rhynchoceratias latirhinus Parr 1927:32, 33, fig.

12 (original description, single specimen,
holotype BOC 2012, 15 mm, Pawnee Third
Oceanographic Expedition stn. 33, western
North Atlantic, 24^11' N, 75°37' W, 2,440 m
wire, 22 March 1927).

Rhynchoceratias longipinnis Parr 1930a:7, fig. 2-5
(original description, single specimen, holotype
BOC 2592, 16 mm. Pawnee Third Oceano-
graphic Expedition stn. 59, Bermuda, 32=19' N,
64=32' W, 2,440 m wire, 21 April 1927, osteol-
ogy); Parr 1930b: 129, fig. 1-3, 6, 7 (anatomy, life
history).

Xenoceratias acanthirostris , Regan and Trewavas
1932:54, 55 (new combination; description after
Parr 1927, in key).

Xenoceratias longipinnis, Regan and Trewavas
1932:54, 56 (new combination; description after
Parr 1927, in key).

Xenoceratias latirhinus, Regan and Trewavas
1932:54, 57 (new combination; description after
Parr 1927, in key).

81

FISHERY BULLETIN: VOL. 78, NO. 1

Xenoceratias regani Koefoed 1944:4, 6, pi. 1, fig. 6
(original description, single specimen, holotype
UBNM 4311, 20 mm, Michael Sars North At-
lantic Deep-Sea Expedition stn. 53, central
North Atlantic, 34°59' N, 33°01' W, 2,600 m
wire, bottom depth 2,615-2,865 m, 8-9 June
1910).

Melanocetus murrayi, Bertelsen 1951:44-48, fig.
16A, D, F, H, table 5 (synonymy, description,
comparison with all known material, in key);
Grey 1956:235 (synonymy, distribution); Maul
1962b:37-38, fig. 3 (description of additional
specimen); Maul 1973:667 (synonymy, after
Bertelsen 1951).

Material. — Metamorphosed females, 140 (13.5-
120 mm): BMNH, 8 (21-57 mm); BOC, 1 (15 mm);
CAS, 3 (14.5-51 mm); FSM, 6 ( 13.5-54 mm); lOAN,
5 (14-56 mm); lOS, 6 ( 17-68 mm); ISH, 33 ( 15-120
mm); LACM, 14 ( 13-84 mm); MCZ, 14 (13-84 mm);
UMML, 28 (17-99 mm); USNM, 7 (15-78 mm);
VIMS, 1 (33 mm); ZMUC, 14 (14-80 mm).

Diagnosis. — A species of Melanocetus unique in
having the following combination of characters:
anterior margin of vomer deeply concave (Figure
2); least outside width between frontals 9.1-17.8%
SL (Figure 19); number of lower jaw teeth 46-142
(Figure 20); longest lower jaw tooth 7.7-16.7% SL;
width of pectoral fin lobe 6.1-8.9% SL; escal bulb
width 1.9-5.1% SL; illicium length 23.1-37.2% SL;

esca with crests minute or absent (Figure 29); mi-
nute skin spines restricted to caudal peduncle;
integument relatively thin (0.48 mm).

Description. — Escal bulb not compressed, with a
low, rounded distal prolongation usually unpig-
mented on tip; posterior and anterior crests mi-
nute or absent (Figure 29); integument thin,
easily torn (cross sections measure 0.48 mm in
thickness), pigment readily lost during fixation
and preservation, often transparent, especially in
gill region and over branchiostegal rays.

Number of upper jaw teeth 34-178; dorsal fin
rays 12-14, pectoral fin rays 15-19 (rarely 20) (Ta-
ble 2).

Distribution. — Melanocetus murrayi has a wide
horizontal distribution in the Atlantic and Pacific,
but is apparently absent from the Indian Ocean
(see Distribution, p. 83). Compared with M.
johnsoni, it is a much deeper living form: only 10%
of the material (for which data was available) was
captured in open nets fished at maximum depths of
<l,000m. Approximately 58% of the material was
taken by gear fished at maximum depths of 1,500
m or below, and 45% by gear fished at 2,000 m or
below (see Distribution, p. 83). The relatively thin
integument of M. murrayi (less than one-third the
thickness of that of its congeners) as well as a
lighter, less well-ossified skeleton reflects the
poorer trophic economies of these greater depths
(see Description above).

1 mm

.5 mm

FIGURE 29.— Escae of Melanocetus murrayi: A. ISH 2961/71, 58 mm SL; B. ISH 922/68, 70 mm SL; C. ISH 2961/71, 76 mm SL; D. ISH

c(75/-,3. 120mmSL.
82

PIETSCH and VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

Comments. — Melanocetus vorax Brauer (1902)
was tentatively synonymized with M. murrayi by
Regan (1926). This decision was confirmed by
Regan and Trewavas (1932) and later by Bertelsen
(1951). Melanocetus tumidus Parr 1927 (not men-
tioned by Bertelsen 1951) was based on a single
metamorphosing female (15 mm) that fits well
within the larval and metamorphosing material of
M. murrayi (Bertelsen 1951) in lacking pigment
on the caudal peduncle and having a faintly pig-
mented gill cover. This nominal form is hereby
synonymized with M. murrayi.

Species Incertae Sedis

The following two nominal species based on
males are distinguished from other Melanocetus
males in having the posterior nostril well sepa-
rated from the eye. They are probably not spe-
cifically distinct from each other and are most
likely the males of one of the above recognized
species based on females (Bertelsen 1951, fig. 20).

Melanocetus longtrostris (Regan and Trewavas
1932) Incertae Sedis

Xenoceratias longirostris Regan and Trewavas
1932:54, 55, fig. 80 (original description, single
specimen, holotype ZMUC P9259, 21 mm, Dana
stn. 3751(7), north of New Guinea, 3°40' N,
137°53' E, 3,000 m wire, 1240 h, 12 July 1929);
Fowler 1936:1346 (after Regan and Trewavas
1932; type species designation).

Melanocetus longirostris, Bertelsen 1951:42-44,
54 (new combination, comparison with all
known material, in key); Grey 1956:238
(synonymy, distribution after Bertelsen 1951).

Melanocetus tiudus (Beebe and Crane 1947)
Incertae Sedis

Xenoceratias nudus Beebe and Crane 1947:155,
text fig. 2 (original description, single specimen,
holotype CAS-SU 46495 [originally NYZS
28402J, 21.5 mm. Eastern Pacific Zaca Expedi-
tion stn. 210T-8, south of Cape Blanco, Costa
Rica, 9°12' N, 85°10' W, 915 m, 27 February
1938).

Melanocetus nudus Bertelsen 1951:43-44, 54, fig.
20 (new combination, description of one addi-
tional specimen, comparison with all known
material, in key); Grey 1956:238 (synonymy,
distribution after Bertelsen 1951).

Melanocetus species

The following females, all considered to be part
of the original type material of M. niger (see
Comments, p. 79), are so poorly preserved that
they cannot be referred to any described species of
the genus: BMNH 1925.8.11.31, 14 mm; ZMUC
P9255, 13.5 mm; BMNH 1925.8.11.28, 43 mm (il-
licium absent).

The following males cannot be satisfactorily
identified to species based on females. Variation in
the number of denticular teeth and pectoral fin
rays and in the subdermal pigmentation (Ber-
telsen 1951) is considerably greater than previ-
ously thought (see Diagnosis of family above):
LACM, 73 (11.5-24 mm) (66 from Hawaii at lat.
21°20-30' N, long. 158° 20-30' W; 3 from the Banda
Sea; 2 from the Mid- American Trench at approxi-
mately lat. 18° N, long. 104° W; and 2 from the
Equator at about long. 170° E and 145° W).

DISTRIBUTION

The family Melanocetidae is widely distributed
throughout all three major oceans of the world in a
broad belt limited by the Arctic and Antarctic
Polar Fronts, with northern and southernmost
records at approximately lat. 62° N and 46° S. It is
present in the Gulf of Mexico, but has not been
collected in the Gulf of California or the Med-
iterranean Sea (Figure 30).

Two of the five species of the family are wide
ranging forms: M.johnsoni occurs throughout the
Atlantic, Pacific, and Indian Oceans; M. murrayi
is found throughout the Atlantic and Pacific
Oceans but has so far not been recorded from the
Indian Ocean. Two lesser known species, M.
polyactis and M. niger, are restricted to the east-
ern tropical Pacific Ocean. Melanocetus eustalus is
represented by a single specimen collected in the
eastern Pacific off Mazatlan, Sinaloa, Mexico.

Since the majority of collections of melanocetids
were made with nonclosing nets, the actual depth
of capture is unknown. Furthermore, because
sample sizes are small a statistical treatment of
the nonclosing net data is impossible. Assuming,
however, that most specimens were caught at
depths where gear is fished for the longest period
of time, vertical distributions may be roughly es-
timated by referring to the maximum depth
reached by gear for each capture. On this assump-
tion, members of the Melanocetidae may be taken
anywhere between 250 m and some unknown

83

FISHERY BULLETIN: VOL. 78, NO. 1

Figure 30. — Geographical distribution of Melanocetus species. Symbols may indicate more than one capture.

lower depth limit exceeding 3,000 m, but they are
commonly found between roughly 500 and 2,500
m. Melanocetus johnsoni is most often collected
between 500 and 1,500 m. Melanocetus murrayi is
a considerably deeper dwelling species; the bulk of
the known material was collected between 1,000
and 2,500 m (Figure 31). The relatively thin in-
tegument (see Description above) and lighter, less
well-ossified skeleton of M. murrayi reflects the
poorer trophic economies of these greater depths.
The remaining species of the genus are so poorly
represented in collections that their vertical dis-
tributions cannot be estimated.

EVOLUTIONARY RELATIONSHIPS

The Melanocetidae appears to be a relatively
underived ceratioid family (Bertelsen 1951;
Pietsch 1972a, 1976, 1979). The five species are
characterized by a confusing mosaic of primitive
and derived character states such that an in-
terpretation of interspecific phylogenetic relation-
ships is difficult. In any case, however, it seems
apparent that M. murrayi has split off from the
main line of melanocetid evolution and acquired a
number of unique features that reflect its most
derived position in the genus: 1) depressed
cranium, 2) concave vomer, 3) small pectoral fin, 4)
tiny escal bulb, and 5) thin integument. Living in
considerably deeper strata than its congeners
most probably also reflects a derived condition.

84

The four remaining species are much more
closely related to each other than any is to M.
murrayi. Five characters can be used to distin-
guish these forms: 1 ) number of lower jaw teeth, 2)
longest lower jaw tooth, 3) illicium length, 4) escal
bulb width, and 5) escal morphology. Unfortu-
nately, all but the last of these characters overlap
in variation among the remaining forms of the
genus, and, furthermore, the relative primitive-
ness of character states among these features is
nearly impossible to determine. Melanocetus
johnsoni is perhaps derived in having a relatively
long illicium, and in having fewer, but longer jaw
teeth (see Pietsch 1972b, 1974, 1975). Melanocetus
polyactis and M. niger are similar in having rela-
tively short jaw teeth, a similar escal morphology
lacking anterior and posterior crests, and a sym-
patric geographic distribution that is restricted to
the Gulf of Panama and adjacent eastern tropical
Pacific. Melanocetus eustalus is derived in having
an extremely large escal bulb, comparable with no
other known ceratioid.

ACKNOWLEDGMENTS

We thank E. Bertelsen for critically reading the
manuscript and offering valuable suggestions.
The following people and institutions provided
study material: John R. Paxton (AMS), Alwyne
Wheeler (BMNH), William N. Eschmeyer (CAS),
Carter Gilbert (FSM), N. V. Parin (lOAN), Nigel

PIETSCH and
0

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400

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VAN DUZER: SYSTEMATICS AND DISTRIBUTION OF ANGLERFISHES

1 1 1 1 r— 1 1 r

1 I I I I T r r 1 1 r

cSo •

o

• •• •

• 90 •

• •• • %

o

o

• o«o oo •

• • •

• ^

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o
o

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15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100 105 110 115 120 125

Standard length in mm

Figure 31 . — Relationship between depth of capture (based on maximum depth reached by fishing gear) and standard length for

two species of Melanocetus.

85

FISHERY BULLETIN: VOL. 78, NO. 1

Merrett (lOS), Gerhard Krefft and Alfred Post
(ISH), Robert J. Lavenberg and Jerry W.
Neumann (LACM), Karsten Hartel (MCZ), Jack
Moreland and C. D. Paulin (NMNZ), Allen Emery
(ROM), P. A. Hulley (SAM), C. Richard Robins
(UMML), Robert H. Gibbs and Susan Karnella
(USNM), E. Bertelsen (ZMUC), Thomas A. Clarke
(Hawaii Institute of Marine Biology), Richard E.
Young (University of Hawaii at Manoa), Brett
Stephenson (Auckland Museum, New Zealand),
and Don A. Robertson (Ministry of Agriculture
and Fisheries, Wellington, New Zealand).
Elizabeth Anne Hoxie provided Figures 17, 18,
and 28. The work was supported by National Sci-
ence Foundation Grants GB-40700, DEB 76-
82279 and DEB 7826540, the National Geo-
graphic Society, and PHS Biomedical Research
Support Grant No. RR-07096 administered
through the Graduate School Research Fund of
the University of Washington.

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1888. Poissons. /n A. Milne-Edwards, Expeditions scien-
tifiques du Travailleur et du Tailisman pendant les anees
1880, 1881, 1882, 1883. G. Masson., Paris, 406 p.

87

EARLY LIFE HISTORY OF PACIFIC MACKEREL, SCOMBER JAPONICUS

John R. Hunter and Carol A. Kimbrell^

ABSTRACT

The early life history of Pacific mackerel, Scomber japonicus , is described from laboratory-rearing
studies and examination of stomach contents of sea-caught larvae. At 19° C mackerel eggs hatched in
56 hours, larvae were 3.1 mm standard length with a dry weight of 0.04 mg of which 50% was yolk. First
feeding occurred 46 hours after hatching; all larvae fed by 60 hours (age 2.5 days). Larvae were then 3.6
mm long with fully pigmented eyes and 10% of the yolk remaining. Starvation was irreversible if
larvae were not fed before age 4.5 days. Metamorphosis ( 15 mm standard length) occurred in 24 days at
16.8^ C to 16 days at 22.1° C. Larvae 3-5 days old consumed 87% oftheirbody weight per day and had a
mean gross growth efficiency in dry weight of 33%. Oxygen consumption was 6.1 m1 Qz per milligram
dry weight per hour at 18° C and 11.4 /xl O^ per milligram dry weight per hour at 22° C. Swimming
speeds ranged from 1.3 standard lengths per second for first-feeding \arvae to 3.8 standard lengths per
second for fish at metamorphosis. Fifty percent of the larvae were able to capture a prey when the width
of the prey was 85% of the width of the mouth and 95% were able to do so when the prey was 57% of the
width of the mouth. Cannibalism was common in rearing groups; at 8 mm standard length, 50% of the
larvae became capable of feeding on other fish larvae and cannibalism ceased when schooling com-
menced. Chief food items of sea-caught larvae were stages of copepods; maximum food width increased
rapidly with larval length and was equivalent to the maximum mouth width. Mean prey width was
38% of mouth width. The larger organisms, constituting half of the prey eaten, accounted for 85-90% of
the total voliune of food eaten.

The development and distribution of eggs and lar-
vae of the western Pacific population of the Pacific
mackerel, Scomber japonicus , has been described
(Kramer 1960; Kramer and Smith 1970), but little
information exists on growth, behavior, and
physiology of the larval stages. Incubation times
and other data are known for the Japanese popula-
tion of S . japonicus (Watanabe 1970). This paper
provides some of the information needed to
characterize the early life history of Pacific mack-
erel, including incubation times, yolk absorption,
onset of feeding, vulnerability to starvation,
swimming and feeding behavior, food ration, and
oxygen consumption.

METHODS

Laboratory Experiments and Sea Samples

Eggs were obtained from Pacific mackerel
maintained in spav^ming condition in the labora-
tory and induced to spawn by hormone injection
(Leong 1977). Effects of temperature on incubation
time were determined by placing test tubes con-

'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.

taining 10 eggs and 25 ml of seawater in a temper-
ature block set to produce a temperature gradient
of ll.l°-23.3°±0.2° C (2 SE (standard error))
(Lasker 1964). Hatched eggs were counted at 2-4 h
intervals and time from fertilization to 50% hatch
estimated. Rate of yolk absorption was deter-
mined at 19.4°±0.4° C by measuring the surface
areas of the yolk-sac and oil droplet from tracings
made with an optical comparator (Wolfson 1965).
Six samples, each of 15-25, larvae were taken over
the first 72 h after hatching.

To estimate the time of first feeding at
18.9°±0.3° C, groups of larvae without past feed-
ing experience were transferred to a 100 1 con-
tainer containing 150 rotifers/ml (Brachionus
plicatilus). Four hours later, they were removed
and the percentage of larvae that fed and the mean
number of rotifers in the gut were calculated.
Eight groups of 10-39 larvae were tested at periods
from 18 to 114 h after hatching.

A starvation-based mortality curve was es-
tabilished at 19.0°±0.3° C by starting with 1,000
eggs in each of two 200 1 containers, and counting
and removing dead larvae daily. The age was de-
termined at which starvation became irreversible
in first-feeding larvae. Seven hundred and fifty
eggs were incubated in each of four 200 1 tanks and
the resulting larvae were fed for the first time at

Manuscript accepted October 1979.
FISHERY BULLETIN: VOL. 78, N

NO. 1, 1980.

89

FISHERY BULLETIN: VOL. 78, NO. 1

ages 2.5, 3.5, 4.5, and 5.5 d. The percentage survi-
val was determined on the eighth day. Larvae
were fed rotifers (50/ml) on the first day of feeding,
and rotifers and copepods (Tisbe sp.) thereafter.

VulnerabiHty of newly metamorphosed Pacific
mackerel (mean length 16.7 mm SL (standard
length)) to starvation was tested at 18.9°±0.2° C
by transferring fish from the rearing container to
containers without food. One group of fish was
starved for 4 d, another for 5 d, and a third was fed
Artemia salina nauplii. The two starved groups
were fed at the end of the starvation period.

Tail beat frequency and amplitude of larval
Pacific mackerel (3-5 mm SL) were determined for
routine swimming and burst speeds by analysis of
cine films taken at 100 frames/s using techniques
described by Hunter (1972). Routine swimming
speeds of larval mackerel, at 19° C, were measured
by counting the number of squares crossed by a
larva (3.7-6.6 mm SL) as it swam over a 1 cm grid
on the bottom of the rearing tank for 9-153 s; a 3
cm grid was used for larger larvae (7.9-13.1 mm
SL) with shorter observation times (3-46 s). The
mean of 15-25 visual observations was used as an
estimate of speed for the mean length of the larvae
in the tank on the day of observation; speeds were
adjusted for parallax caused by the difference in
depth between the grid and the fish. Speeds of
juveniles (>19 mm SL) were measured by timing
the fish as they swam a measured distance (35-201
cm) around the perimeter of the rearing tank; in
this case mean speeds were for individual fish and
observation times ranged from 3 to 26 s.

The size at which Pacific mackerel larvae were
capable of ingesting various prey was evaluated
by placing them in a 110 1 container with the prey
and estimating the number that fed by examina-
tion of stomach contents. The type of prey, mean
prey size, prey density, and duration of feeding
respectively were: yolk-sac anchovy larvae, 2.7
mm SL, 8/1, 2 h; A. salina nauplii, 0.2 mm wide,
11/1, 4 h; and anchovy eggs, 0.67 mm wide, 10/1, 2
h. The mouth width, prey width, and standard
length of the larvae were measured and percent-
age feeding success was estimated for size classes
of larval length and mouth width. The number of
fish per size class was >9. Size thresholds for 50%
feeding success and 95% success were estimated
by probit analysis (Finney 1952) and expressed as
a function of mean larval length, or mean prey
width/mean mouth width.

The sizes of food items eaten by Pacific mackerel
larvae in the sea was determined by examination

of the stomachs of 86 larvae taken in routine
ichthyoplankton surveys along the California
coast. We recorded the length of each larva and the
number and maximum width of all identifiable
food items (Arthur 1976; Shirota 1970).

Food requirements were estimated by feeding
the rotifer Brachionus plicatilis to 3-5 d old Pacific
mackerel larvae. Seven to eight samples of 9-16
larvae each were taken over each of three 12-h
feeding days, the number of rotifers in the guts of
each larva were counted, and the counts converted
to equivalent dry weight using the conversion
factor of 0.16 /^g/rotifer (Theilacker and McMaster
1971). Daily changes in larval weight were esti-
mated from mean standard lengths using a
length-dry weight conversion given in the results.
The rate of gastric evacuation for 4 mm SL larvae
was measured. They were allowed to feed for 4 h
and then transferred to a tank without food; sam-
ples of 13-16 larvae were taken at about hourly
intervals until the stomachs were empty. The
number of rotifers in stomachs were counted and
converted to dry weight, and the rate of gastric
evacuation was estimated in terms of dry weight.
The daily ration was estimated from the mean
stomach contents and the rate of gastric evacua-
tion. Gross growth efficiency was estimated in
terms of dry weight from the daily ration and
weight gain over 24 h.

Metabolic requirements of Pacific mackerel lar-
vae were estimated using a Warburg respirometer
and standard manometric techniques (Umbreit et
al. 1964) to measure oxygen consumption. One or
more Pacific mackerel larvae were added to an 18
ml Warburg flask filled with 4.4-8.7 ml of filtered
seawater (salinity 33.58-33.93%o). Larvae >0.06
mg dry weight were tested individually. Twenty-
one tests were made at 18.0°C of larvae or groups
of larvae ranging in length from 3.7 to 17.9 mm SL
(0.038-12.74 mg) and 14 at 22.0° C, of larvae 3.2-
10.5 mm SL (0.025-2.86 mg). Flasks were shaken
at 102 times/min for 5 out of every 30 min; read-
ings were taken after the first 2 h and continued
for 150-360 min. At the end of a test, larvae in each
flask were measured, rinsed in distilled water,
oven dried to a constant weight, and weighed.
Mean weight was obtained for fish tested in
groups. All runs were made under normal room
illumination, about 700 Ix. Logj^ oxygen con-
sumption in microliters Og per hour was regressed
on logio body weight for the 18.0° and 22.0° C
experiments. As the slopes were close to unity,
oxygen consumption was expressed in microli-

90

HUNTER and KIMBRELL: EARLY LIFE HISTORY OF PACIFIC MACKEREL

ters per milligram per hour. Metabolic require-
ments were compared with daily ration by con-
verting oxygen consumption and daily ration to
calories (1 /i.1 Oj = 0.005 cal: one Brachionus

plicatilis
ter 1971).

0.00085 cal, Theilacker and McMas-

Culture of Larvae

Seven groups of Pacific mackerel were reared to
metamorphosis to determine growth rates and ef-
fects of temperature on growth. The rearing con-
tainers were black fiber glass, cylindrical tanks
(122 cm in diameter x 36 cm deep). Culture vol-
ume increased during the rearing period from 200
to 400 1 because of the addition of seawater con-
taining food and algae. Tank temperature was
controlled by a regulated water bath, and groups
were reared at temperatures ranging from 16.8° to
22.1° C. Illumination at the water surface during
the 12-h day was about 2,000 Ix. Tanks were
started with 3,000 eggs/group. Initially, larvae
were fed laboratory-cultured Brachionus
plicatilis. At age 5 d, laboratory-cultured
copepodids and adult copepods (Tishe sp.) were
added; 200,000 copepods were added daily until
metamorphosis. Initially 30 or more rotifers/ml
were added for the first few days of feeding; there-
after the density of rotifers was allowed to decline.
On a diet of rotifers alone, growth slowed after
larvae reached 5 mm SL and few larvae survived
longer than 15 d. Newly metamorphosed juveniles
were fed live and frozen adult A. salina and
minced squid {Loligo opalescens ) and northern an-
chovy. From 1 to 6 1 of algal culture, Tetraselmis
sp. (300,000-500,000 cells/ml), were added daily to
provide food for rotifers and copepods. Samples of
10 or more larvae were taken on alternate days for
length measurements. Some samples were
washed in distilled water, dried, and subsequently
weighed to obtain a relation between length and
dry weight.

RESULTS

Hatching, Onset of Feeding and Starvation

Eggs of Pacific mackerel are transparent
spheres, ranging in diameter from 1.06 to 1.14 mm
(Kramer 1960). Incubation times ranged from 33 h
at 23° C to 117 h at 14° C (Figure 1); eggs did not
hatch below 14° C. The curve for hatching time as
a function of temperature for the western Pacific

population (data from Watanabe 1970) appears to
be the same as the one for the eastern Pacific
population.

I20|-

110-

100-

o 90

<

X

^ 80

O
in

o 70

^ 60

O

X

50

40

H = 3580e-6.50(l-e-00527T)

30^

oV' ' I

_L

J \ I I I I I I I

0 12 14 16 18 20

TEMPERATURE °C

22

24

FIGURE 1. — Incubation time (fertilization to 50% hatch) of
Scomber japonicus eggs. Solid line is for present data, points are
estimated time to 50% hatch of eggs in five test tubes per tem-
perature, dashed line is for data of Watanabe ( 1970). The general
equation was developed by Zweifel and Lasker (1976) and fit to
the 50% values.

At hatching, larvae averaged 3.1 mm SL (Fig-
ure 2B) and weighed 0.040 mg dry weight, of
which 50% was yolk. At 19° C, first feeding oc-
curred 46 h after hatching; by 60 h after hatching,
all larvae had ingested one or more rotifers in 4 h
(Figure 2D). Thus the 50% threshold for onset of
feeding at 19° C occurred at about 50 h (2 d) after
hatching. At this time larvae were 3.6 mm SL, the
eyes were fully pigmented and 10% of the yolk
remained, principally the remnants of the oil drop-
let (Figure 2A, B). Over the threshold for the onset
of feeding, the mean number of rotifers in Pacific
mackerel stomachs increased from 2 at 46 h to 14
at 68 h (Figure 2E). The larvae in each group had
no previous feeding exposure, hence the increase
in feeding activity with time could not be attrib-
uted to experience.

91

FISHERY BULLETIN: VOL. 78, NO. 1

-2 0.0' I I I I I I I I I I I ' I I I I I ' I I I

0 40 80 120 160 200

I 1 r

T-
0

I

1^
2

3

T"
5

7 8

100

T3
O

O

o -

5 60-

>

3
(/)

c
o

Q-

O'l I I I I I I I I I I I I ' I ' VT~f I I
0 40 80 120 160 200

1 1 1

0

3

T"
4

1^

7

8

o
o

e

o
c/5

e

3

' M I I I I M I I I I I
40 80 120 160 200

1 1 r

2 3 4

6

8

38 r

E
E

<u

B

30'| I I I I < I I I I I ' I I I I I I I I I
Hours 0 40 80 120 160 ZOO

1 1 1 1 1 1 1 r

Days 0 1 2 3 4 5 6 7

lOOr

-r

8

I I I > I I I
120 160 200

r

' I I I ' I I I

Hours 0 40 80
1 1 1 1

I f I I I '
120 160

Days 0

I

1^
6

T-1
200

-r
8

Figure 2. — Yolk absorption, onset of feeding, starvation, and point of irreversible starvation in Pacific mackerel larvae at
19° C: A. Rate of yolk absorption — open circles mean area of yolk-sac, solid circles mean area of oil droplet (mm^). B.
Mean length of larvae from hatching through yolk-absorption. C. Percent survival of larvae without food. D. Percent of
larvae tested at various times after hatching that had ingested one or more Brachionus plicatilis in a 4-h test period —
arrow indicates the 50% threshold for the onset of first feeding. E. Mean number of S. plicatilis per positive stomach of
larvae tested at various times after hatching. F. Percentage survival at age 8 d for larvae fed for the first time at age 2.5,
3.5, 4.5, and 5.5 d — percentages are plotted at the time food was first added. Bars in A, B, and E represent ±2 SE of mean.

92

HUNTER and KIMBRELL: EARLY LIFE HISTORY OF PACIFIC MACKEREL

If larvae were not fed, most died between ages 4
and 7 d and none survived longer than 7 d (Figure
2C). Highest survival (on the eighth day after
hatching) occurred when food was added for the
first time at age 2.5 d; survival was somewhat
lower if food was added at 3.5 d and negligible if
added at 4.5 d (Figure 2F). Thus at 19' C starva-
tion appeared irreversible if food was not provided
before 4.5 d.

Pacific mackerel larvae, unlike herring or an-
chovy (Blaxter and Hempel 1963; Lasker et al.
1970), did not cease swimming or feeding at the
time of irreversible starvation. At age 5 d, the
incidence of larvae with rotifers in their stomachs
was relatively high (80%) (Figure 2D), but the
average number of rotifers per positive stomach
was much less than in larvae fed first at age 2 or 3 d
(Figure 2E). Thus at age 5 d, most larvae were still
able to feed, but owing to their weakened condi-
tion, none were able to capture enough prey to
survive.

Vulnerability of larvae to starvation persisted
through metamorphosis. All juvenile Pacific
mackerel appeared emaciated and swam slowly by
the fourth day of starvation. Mortality of 10% oc-
curred in the group starved 4 d; 50% mortality
occurred in those fish starved 5 d. All juveniles
surviving 4 and 5 d of starvation recovered when
food was added; no mortality occurred in the con-
trols. Thus, newly metamorphosed Pacific mack-
erel were able to withstand 1 or 2 d more of starva-

tion than first-feeding larvae, but they were better
able to recover from food deprivation.

Growth

Growth in length of Pacific mackerel larvae was
slow and almost linear over the first 10-15 d until
larvae reached about 6-7 mm SL; there followed a
rapid acceleration through metamorphosis. We
did not fit equations to these data because none of
the standard growth equations gave a good fit to
the entire growth curve. The effect of temperature
on growth was not distinguishable over the initial
growth period, but became obvious during the
period of rapid growth (Figure 3, Table 1). To pro-
vide an index of the effect of temperature on
growth, we expressed the duration of the larvae
period (hatching to metamorphosis, 15 mm) as a
function of temperature (inset in Figure 3). The
Qio was 3.0 when calculated from the equation in
Figure 3 for the temperature range of our observa-
tions ( 16. 8'-22.1° C).

The length-weight relation for Pacific mackerel
larvae and juveniles is shown in Figure 4. The
form of this equation was developed by James
Zweifel and used by Hunter ( 1976) to express the
length-weight relation for northern anchovy lar-
vae. The curvilinear nature of the length-weight
relation, still evident in the log-log plot ( Figure 4),
indicates that if a linear regression of logj^ weight

Table l. — Growth data (millimeters SL) for seven groups of Scomber japonicus larvae reared at different mean temperatures from

hatching through metamorphosis.

Age

22.1=0'

20.4= 0

19.6=0

19.5=0

19.2=0

18.9°0

16.8" 0

(days)

n

X

SD

n

X

SD

n

X

SD

n

X

SD

n

X

SD

n

X

SD

n

X

SD

1

10

3.1

0.24

31

3.5

0.12

2

14

3.3

0.21

16

38

0.06

16

3.7

0.10

15

39

009

15

3.8

006

3

14

3.5

0.30

4
5

10

36

022

18

3.8

026

33

42

0.23

10

4.0

0.17

15

4.0

0.20

10

3.7

0.20

6

10

3.9

0.21

15

4.2

0.41

15

48

0.44

13

4.2

0.14

15

4.4

0.37

10

4.1

0.39

15

4.3

042

7

27

4.5

0.40

8

12

4.5

0.55

15

5.7

0.77

15

6.0

0.39

25

4.7

0.56

15

5.0

0.40

15

5.1

0.43

9

5

5.9

0 13

10

12

6.0

1 13

15

63

091

15

6,6

070

15

4,8

0,43

19

56

0.77

11

5.2

0.45

11

15

6.5

0.70

12
13

22

8.4

1 88

16

82

1.31

15

6,5

0-75

11

5,9

1.08

25

6.4

0.68

12

6.1

0,60

15

7.0

0.50

14

10

89

1,46

10

11.5

1.54

15

8,4

1,12

30

6,4

1,09

15

6.6

0.80

17

7.7

1.40

15

11

8.1

1.08

16

10

14.9

1.45

15

14.1

2.01

15

8.9

1,76

16

8.5

2,21

15

7.1

081

13

7.6

1.50

17

10

10.0

2.71

12

9.0

1.33

15

10.3

2.11

18

15

17.8

1,70

15

10,3

2,48

15

10.3

3.21

13

9.4

1.61

17

10.8

2,84

19

15

24.1

5.81

20

15

12.5

3.18

17

17.7

4.21

15

11.7

2.88

9

11.5

2.81

22

15

17.5

4.51

15

14.6

462

23

15

13.7

1.26

24

24

20.4

5.10

16

18.5

5.38

10

19.8

2.36

25

17

17.1

5.07

'Juvenile growth (age. n.x, and (SD)): 26 d. 13,34.4 mm (4.37); 29 d, 9, 43.9 mm (3.60); 39 d. 5, 55.0 mm (8.74); and 47 d. 9. 67.3 mm (10.30).

93

FISHERY BULLETIN: VOL. 78, NO. 1

24

22

20

18

16

X

14

1-

o

z

1?

Ixl

_J

_l

10

<

>

tr

R

<

_j

6

4

- <

t-

- O

>-
<
o

22.1

E
E
If)

O

I

Q.

cr
o

24
22
20

\

.\

y •

-

\ •

-

\ •

__

•

V

—

D =

51186-

1 593 T

\

-

r2

= 0 706

• \

—

1

1 1

1 1

1 f

15 16 17 18 19 20 21
TEMPERATURE CO

TEMPERATURE (°C)

22.1 +.2
20. 4 + . 5
19.6 +.4
19 . 5 + . 8

19.2 + .1
18-9 + .1
16.8 +.2

8 10 12 14 16 18 20

AGE (DAYS)

22

24 26

Figure 3. — Growth of seven groups of Pacific mackerel larvae reared in the laboratory from hatching (age 0 d) through metamorphosis
(15 mm SL). Lines connect means given in Table 1 ; rearing temperatures ( ±2 SE) given on right side of figure and at end of lines. Inset at
top: elapsed time (days) from hatching to metamorphosis (15 mm), as a function of rearing temperature.

on logjj, length were used, it would produce inac-
curate estimates.

Swimming Behavior

At typical cruising speeds, larval Pacific mack-
erel (3-5 mm SL) have a high tail beat frequency of
about 30 beats/s and a low tail beat amplitude of
0.16 standard length. At slow speeds, tail beat
frequency remained relatively constant but the
amplitude of the tail beat changed. At higher
speeds, both amplitude and frequency changed but
the relative increase in amplitude was much
greater than that of frequency (Table 2). Thus
larval Pacific mackerel, unlike the adults (Hunter

and Zweifel 1971), predominantly modulate tail
beat amplitude to effect changes in speed.

Cruising speeds of Pacific mackerel increased
markedly over the larval period from 0.46 cm/s
(1.3 standard body lengths/s) for first-feeding lar-
vae (3.6 mm SL) to 5.6 cm/s (3.8 standard body
lengths/s) for fish at metamorphosis (Figure 5).
This differs from the pattern in adult fishes where
speed relative to size decreases with an increase in
fish size (Webb 1975).

Feeding Behavior

Upon sighting a prey (rotifer or copepod), a Pa-
cific mackerel larva advanced toward the prey.

94

HUNTER and KIMBRELL: EARLY LIFE HISTORY OF PACIFIC MACKEREL

2000 -

1000 r

500

100

50

^ 10

£

X

C2

UJ

>-
cr

Q

05

01

0.05

001

Ln W= -4.660 + (-672l + 6.333 Ln l)°-S'°

I I h

I I I

2 4 6 8 10 20 40 6080100

STANDARD LENGTH (mm)

Figure 4. — Relation between dry weight (W) of larval and
juvenile Pacific mackerel in milligrams and standard length (L)
in millimeters. Points are observed values for individuals >18
mm and for larvae <18 mm; points are means for groups of 15
larvae.

stopped, drew back the tail, and held it in a
slightly recurved, high amplitude position while
the rest of the body remained relatively straight.

Table 2. — Tail beat frequency and amplitude and speed of 3-5
mm larval Pacific mackerel ix = 4.23 ±0.09 mm SL) expressed as
a function of standard length.

Tail beat

Swimming speed (SUs)
Class interval

18
30
9
3
3
1

0.01-
1.01-
2.01-
3.1 ■
10.1

1.0
2.0
3.0
5.0
15.0

Frequency

Mean

(beats/s)

Amplitude/SL

0.58

33.2

0.12

1.48

30.2

0.16

2.48

30.2

0.17

4.00

37.5

0.18

12.18

39.4

0.29

37.04

38.9

0.33

E
o

Q

UJ
UJ
Q.
Ul

CO

30
20

-

S = 2.780L
r2 = 0.966

753

/

10

_

4

/

8.0

-

/

6.0

-

J

4.0

-

•

7

I

2.0

-

i

/

1.0

—

I

1

0.8

-

*f

0.6

-

?

0.4

-

*

111!

Mil

.3 .4 .5.6.7.8 1.0 2.0 3.0
STANDARD LENGTH (cm)

Figure 5. — Relation between swimming speed and standard
length of Pacific mackerel larvae (log^g scales) at 19° C. Each
point <2.0 cm is the mean of 15-25 observations. For ^2.0 cm,
individual fish were measured.

Feeding involved driving the tail posteriorly and
opening the mouth. Larvae often attacked the
same prey two or more times if the previous strike
was unsuccessful, and repositioned for subsequent
strikes by moving backward. Handling times were
negligible because the prey was engulfed instan-
taneously. Older Pacific mackerel larvae de-
veloped a set of motor patterns for feeding on fish
larvae; larvae were seized from the side and car-
ried crosswise in the mouth. Larger prey were
repeatedly released and grasped until they ceased

95

FISHERY BULLETIN: VOL. 78, NO. 1

struggling, then released and ingested, usually
head first. Handling times increased with prey
size.

The length at which 50% of Pacific mackerel
larvae were capable of capturing and ingesting
anchovy yolk-sac larvae (LD50, Finney 1952) was
8.1 mm SL (95% confidence interval, 7.2-9.5 mm)
(Figure 6). Sibling cannibalism began when the
mean length of the group was about 8 mm SL. At
this size, the mean length of six cannibals was 10.8
mm SL (range 9.9-12.0 mm) and that of their prey
was 6.2 mm SL (range 5.9-6.5 mm). Cannibalism
in rearing containers ended as Pacific mackerel
approached metamorphosis (15 mm SL) and
schooling began. Rearing at higher temperatures
increased the growth rate and thereby decreased
the period over which sibling cannibalism oc-
curred. Consequently, survival at metamorphosis
was higher in groups reared at 20°-22° C (5-6%)
than it was at 19° C or lower temperatures (1-2% ).

Near metamorphosis. Pacific mackerel were
able to eat relatively large fish larvae. Three
Pacific mackerel, 15.4-16.0 mm SL, placed in a
rearing tank with northern anchovy larvae
(12.0-20.6 mm SL) captured and began to ingest
larvae of 11.7-13.5 mm SL, within 6 min. Thus, as
Pacific mackerel larvae grew from 8 mm SL to
metamorphosis, the size of anchovy larvae, they
were able to eat increased from about 3 to 13 mm
SL. This increase in prey size was not closely re-

lated to mouth size of the Pacific mackerel because
the mouth can be greatly expanded when ingest-
ing a larval fish. Mouth size probably was in-
versely related to handling time as in the case for
adult fishes (Kislalioglu and Gibson 1976).

When prey are engulfed rather than seized,
mouth size may give a good indication of the size of
prey a larvae is capable of ingesting. The relation
between mouth width and length in Pacific mack-
erel larvae was slightly curvilinear, and mouth
width increased from 0.216 mm for first-feeding
larvae (3.6 mm SL) to 0.987 mm at metamorphosis
(15mmSL) (Figure 7).

l-4i-

_ LnM= -49419 + (15755 + 5.4815 LnL)

E
X

I-

Q

3
O

8 -

6 -

W/-

J \ \ \ \ L

J \ \ I \ I I I \ I

18 20

6 8 10 12 14 16

STANDARD LENGTH {mm)

en
to

UJ

u
o

CO

UJ
CD
<

UJ
O

PREY

= YOLK-SAC

ANCHOVY

LARVAE

-

S=-2976 + 87ll Log|Q

L

y^

-

S = 7o

IN PROBITS

-

0

yo

-

1

1 1 1 1

1 1 1 1

1 1 1 1

95

90

80
70
60
50
40
30

20

10

6 7 8 9 10 II 12 13

STANDARD LENGTH (mm)

Figure 6.— Percentage of Pacific mackerel larvae (probit scale)
that captured one or more yolk-sac anchovy larvae in relation to
standard length of the mackerel (log,j, scale). The length class
was variable. Larvae were ranked by length and classes set at 10
observation intervals. The LD^^^ was 8.1 mm (95% confidence
interval 7.2-9.5 mm).

Figure 7. — Mouth width as a function of standard length of
Pacific mackerel larvae. Points represent single larva.

The threshold, in terms of length for feeding on
A. salina nauplii, was distinctly different from
that for feeding on anchovy eggs. The 50%
threshold for nauplii was 4.5 mm SL (95% con-
fidence interval, 4.1-4.8 mm) and that for eggs was
12.2 mm SL (11.3-13.1 mm). This could be ex-
pected because anchovy eggs are nearly three
times as large as A. salina nauplii. On the other
hand, when feeding success was expressed as a
function of the ratio, mean prey width/mean
mouth width, the percentage feeding success of
Pacific mackerel fed A. salina was similar to that
of larvae fed eggs (Figure 8). At first feeding, rela-
tive prey size (prey width/mouth width) was near
unity for larvae fed either A. salina or eggs, indi-
cating the width of the mouth established the
upper size limit of prey. Since the 50% threshold
for relative prey size for the combined data given
in Figure 8 was 0.85 (95% confidence interval.

96

HUNTER and KIMBRELL: EARLY LIFE HISTORY OF PACIFIC MACKEREL

95

90 -

80

V. 70

UJ

8 60

^ 50

UJ

^ 40

I-

g 30

^ 20

• •

PREY

O Enqraulis mordox eggs
(minor axis = 0674 mm)

# Artemio solino nauplii
(0238 mm)

5 = 4 322-9580 Log
S= % in probits

10

_L

_L

4 5 6 7 8 9 1.0 1.5

PREY WIDTH /MOUTH WIDTH (R)

Figure 8. — Relation between average feeding success (probit
scale) and average relative prey size (prey width/mouth width),
for larval groups fed Artemia salina nauplii (closed circles) and
northern anchovy eggs (open circles). Each point is the percent-
age success of fish within a mouth width/prey size class, where
n>9. Line is the regression of percentage success probit on log^^
of the prey-width to mouth-width ratio, for A. salina nauplii and
anchovy egg data combined. The LD^p for the combined data was
0.85 (95<7c confidence interval 0.79-0.91).

0.79-0.91) and the 95% threshhold was 0.57
(0.47-0.70), nearly all Pacific mackerel larvae
(95% ) were able to ingest a prey when it was 57% of
the width of the mouth and 50% were able to do so
when it was 85% of the mouth width.

Nearly all prey eaten by Pacific mackerel larvae
in the sea fell within the range of sizes predicted
from the laboratory work; few prey exceeded the
width of the mouth (Figure 9). Fifty-nine percent
of all identifiable food items in the stomachs of
sea-caught larvae were stages of copepods; other
items included cladocerans, oikopleurans, gas-
tropods, invertebrate eggs, diatoms, fecal pellets,
and one fish larvae.

Although laboratory data indicated that 50% of
Pacific mackerel larvae were able to ingest prey
having a width of 85% of the mouth width, the
mean diameter of prey eaten in the sea was
38±2% (2 SE) of the mouth width. Thus, a sub-
stantial number of prey eaten by larvae in the sea
was much smaller than the maximum size of prey
they were capable of ingesting. This may reflect a

shortage of larger prey in the sea. Larger prey
probably are important nutritionally. If one as-
sumes the prey given in Figure 8 to be spherical,
then 50% of the prey items accounted for about
85-90% of the total volume of food, depending on
larval size. Conversely, the small prey items that
contributed 50% by number, contributed only
10-15% of the total volume of prey eaten. This
calculation underestimates the volume of the
larger prey because they are more elongate or less
spherical than smaller ones. Nevertheless, it indi-
cates that prey less than the mean size eaten con-
tributed relatively little nutritionally to the diet of
Pacific mackerel larvae, and that the relatively
large, but more rare, prey probably made the
major contribution to growth.

Ration, Growth Efficiency and Metabolism

Pacific mackerel larvae (age 3-5 d) fed actively
throughout the day; the gut was filled within the
first hour of feeding and it remained full through-
out the remainder of the 12-h feeding day, despite
a high rate of gastric evacuation. Evacuated
Brachionus plicatilis were well digested; only the
lorica remained after digestion. Our measure-
ments of evacuation rates indicated that about
half the gut contents was evacuated in 2 h (Figure
10). Growth of larvae used for ration estimates
was about the same as that for other groups reared
at 19° C (Figure 3). To grow at this rate in the
laboratory, Pacific mackerel larvae (age 3-5 d)
consumed an average of about 87% of their dry
body weight per day, or about 165-538 rotifers/day
(Table 3). This estimate of ration was based on the
dry weight of the mean number of rotifers in
stomachs, adjusted for the rate of evacuation
(Stauffer 1973). The mean gross growth efficiency
in dry weight was 33%, which falls within the
range of estimates for fish larvae and young fishes
(Pandian 1967; Stepien 1976).

Our respiration experiments indicated that
Pacific mackerel larvae at 18.0° C consumed
6.1 ± 1.4 (2 SE) Ml Oa/mg per h (n = 24) and at 22.0°
C they consumed 11.4±3.0 ^tl Og/mg per h (n =
14). By interpolation, the rate at 19° C, the tem-
perature of the ration experiments, is estimated as
7.4 ^x\ Oj/mg per h. This metabolic expenditure,
converted to calories per day (footnote 6, Table 3)
was, on the average, about 18% of the mean daily
ration for larvae given in the table. This is proba-
bly an underestimate of their metabolic require-
ment because the activity of larvae confined in

97

.8

.7

£.6

E

Q
O
O

.5

O

X
Q

.4

.3

.2

FISHERY BULLETIN: VOL. 78, NO. 1

/

/

/

/

/

/

/

/

/

/

/

/

•• ••

• W ••

..4/

/

/

/

oVv

/

/

/

• / /
/ /

/-/ /

/ / • •

/ 'A. . ...

4PX

fi.0.

- - •

- •4, #9"

_4 _ll

mm % »^
m A • • «•
.^ .
Mi w • ^

lb* A"

• « 1^ • «

• • • m

^o:

A
A

y *^S4*

49

10

12

13

14

15

16

17

STANDARD LENGTH (mm)

Figure 9.— Width of foods eaten in the sea by Pacific mackerel larvae of various standard lengths. Each small point is the
width of a single prey; larger points represent multiple points for prey of the same size and number observations. Dashed lines
indicate the prey width equal to 20-80% of the mouth width , or equal to the mouth width ( 100% ) , for Pacific mackerel larvae of
3-16 mm (calculated from data given in Figure 7).

98

HUNTER and KIMBRELL: EARLY LIFE mSTORY OF PACIFIC MACKEREL

005-

LnW = -5 442-0 337 T
r^ =0 970

e

OD

I

^ 0005 -

2
<
liJ

5

001 -

.000

2 3 4 5

ELAPSED TIME (h)

FIGURE 10.— Rate of gastric evacuation of 4.01+0.03 mm SL
Pacific mackerel larvae fed Brachionus plicatilis. Each point
represents the mean dry weight of fi. plicatilis in guts of 13-16
larvae. Dry weight estimated by counting numbers of B.
plicatilis in stomachs and multiplying by the mean dry weight of
one B. plicatilis iO.lSfig) iTheilacker and McMaster 1971).

Warburg flasks was probably less than that of
free-swimming larvae. These respiration mea-
surements do establish a lower limit to food ration,
because the ration would have to exceed the
metabolic requirement just to meet maintenance
costs.

DISCUSSION

The characteristics of the embryonic period (du-
ration of incubation and yolk-sac periods, extent of
yolk reserves, size at first feeding, and ability to
withstand starvation) were similar to other tem-
perate fishes with small pelagic eggs (Lasker et al.
1970; Zweifel and Lasker 1976) and did not differ
greatly from some subtropical species (Houde
1974). Small differences in these characteristics
may be of importance (Houde 1974) but growth,
metabolism, feeding, and swimming behavior are
of more value in characterizing the early life his-
tory of Pacific mackerel.

Pacific mackerel larvae grew rapidly, complet-
ing metamorphosis (15 mm SL) in 2-3 wk. Fast
growth appears to be characteristic of scombroid
larvae and is even more rapid in tropical scom-
broids: Auxis thazard grew to 64 mm SL in 17 d
(Harada, Murata, and Furutani 1973) and A.
tapeinosoma grew to 49 mm SL in 18 d (Harada,
Murata, and Miyashita 1973). Fast growth re-
quires a large food ration; we found that Pacific
mackerel larvae consumed about 877f of their dry

Table 3. — Estimate of ration, metabolism, and growth efficiency of 3-5 d old Pacific mackerel larvae fed Brachionus plicatilis.

Tempera-
ture V 0)

Larval
SL±2SE(mm)

Experimental conditions
Larval weight'

Food density
(no. /ml)

Mean

No.
samp

weight in stomachs^

Larval
age(d)

On day of ration
estimation (;ug)

Gain 1 d after
estimation (^g)

of xr2SE
es= (^g)

3
4
5

X

18.7
19.0
19.4
19.0

3.56-0.03
3.76±0.02
4.38±0.08
3.93

37.8
43.0
84.6
55.1

5.2
14.0
37.5
18.9

157
47

198

134

7
8

7

4.8-0.8
6.9±1.0
15.6-4.5
9.1

Ration"

Ration, metabolism

and growth efficiencies

Metabolic rate^
(cal/d)

Weight gain'
(cal)

Gros

Larval
age (d)

/ug/d

Percent body
welghl'd

5cal;d

;s growth efficiency^
(percentage)

3
4
5

X

26.5
38.1
86.2
50.3

70

89

102

87

0.141
0.203
0.460
0.268

0.0338
0.0384
0.0756
0.0493

0.026
0070
0.188
0.094

20
37
44
33

'Calculated from mean larval length using relation given in Figure 4.

Mean counts of 8. plicatilis in stomach converted to weight using one B. plicatilis = 0.16 ^g (Theilacker and McMaster 1971).
Each sample consisted of 13-16 larvae; sampling began after first hour of feeding.

Ration = (/•■/(• f) - r, where r is mean stomach contents, k is rate of gastric evacuation (0.377), and t is duration of feeding period (12 h). (From G. Stauffer,
unpubl. manuscr. Southwest Fisheries Center. La Jolla. Calif )

Caloric value of B. plicatilis = 5.335 cal/g (Theilacker and McMaster 1971).

Maintenance requirement from; 7.45 /nl 02,mg per h; 1 ^1 O2 = 0.005 cal; time = 24 h; and dry weight of larvae on day ration estimated.

Caloric value of weight gained assumed to equal 5.000 cal/g.

Gross efficiency (dry weight) = weight gam/ration.

99

FISHERY BULLETIN: VOL. 78, NO. 1

weight per day and weight increased from 0.034
mg to 7.5 mg over the larval period. To capture
sufficient numbers of prey to support such rapid
grovvi;h requires that the size of the prey and the
size of the mouth increase rapidly. Our analysis of
sea-caught Pacific mackerel larvae showed that
the maximum size of prey did increase rapidly,
more or less, in proportion to mouth size. The
mean and minimum size of prey eaten by Pacific
mackerel changed more slowly but the smaller
prey, those less than the average size, may consti-
tute <15% of the volume of food eaten. A similar
pattern of rapidly increasing prey size with length
also has been documented for Scomber japonicus
larvae by Shirota (1970) and Yokota et al. (1961).

A dependency on larger prey and fast growth
requires faster swimming to increase the volume
of water searched for prey because abundance de-
clines with increased prey size (Sheldon et al.
1972). The swimming behavior of Pacific mackerel
larvae appeared consistent with this argument.
Cruising speeds increased rapidly with length,
roughly to the 1.8 power, and speeds of the larger
larvae were at the upper end of the range, typical
of larval fishes (3 SL/s) (Blaxter 1969). Higher
speeds require a greater metabolic expenditure.
The rate of oxygen consumption for Pacific mack-
erel (6-11 fx\ Og/mg per h) was above that for other
marine fish larvae (Blaxter 1969) indicating a
higher-than-average metabolic expenditure de-
spite the fact that the rates probably do not reflect
the entire cost of high speed swimming.

Piscivorous feeding was an import".:.;. e-
havioral trait in the early life history of Pacific
mackerel because larvae were no longer limited to
prey sizes equal to or less than the size of an open
mouth. In piscivorous feeding, prey were seized,
manipulated and the mouth greatly expanded
during ingestion, permitting consumption of
much larger diameter foods. In our samples of
sea-caught larvae, only one stomach contained a
larval fish, but the actual incidence may be higher
because larvae are digested rapidly. Cannibalism,
a correlate of piscivorous feeding, was common in
laboratory groups after the larvae reached 8 mm
SL. This also has been observed from stomach
contents of the Atlantic mackerel, S. scombrus
(Lett 1978). Cannibalism appears to be a common
feature of scombroid life history; Mayo (1973) re-
marked that Euthynnus alletteratus , Scom-
beromorus cavalla, S. regalis, and Auxis sp. be-
came cannibalistic at about 5 mm SL. He also
noted that cannibalism ceased as the fish became

100

juveniles which agrees with our observation that
cannibalism ended as Pacific mackerel ap-
proached metamorphosis and began to school. The
extent that cannibalism affected the form of our
laboratory growth curves is unknown. Although
cannibalism was high in all groups, survival was
higher in groups reared at high temperatures be-
cause of the faster growth rate, which meant faster
transit through cannibalistic sizes.

In summary, traits that characterize the early
life history of Pacific mackerel are the interrelated
characteristics of fast growth, fast swimming,
high metabolism, a dependence on increasingly
larger prey, and cannibalism. The high food re-
quirements of the larvae, and the fact that in the
sea they feed upon many prey substantially small-
er than they are capable of eating, indicates that
growth or survival in the sea might be limited by
the availability of larger prey.

LITERATURE CITED

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.

Blaxter, J. H. S.

1969. Development: eggs and larvae. In W. S. Hoar and
D.J.Randall (editors), Fish physiology. Vol. 3, p. 177-252.
Acad. Press, N.Y.

Blaxter, J. H. S., and G. Hempel.

1963. The influence of egg size on herring larvae. J.
Cons. 28:211-240.

Finney, D. J.

1952. Probit analysis: a statistical treatment of the sig-
moid response curve. Univ. Press, Camb., 318 p.
Harada, T., O. Murata, and H. FURUTANI.

1973. On the artificial fertilization and rearing of larvae in
Marusoda, Auxis tapeinosoma. [In Jpn., Engl,
abstr.] J. Fac. Agric, Kinki Univ. 6:113-116.

Harada, T., O. Murata, and S. Miyashita.

1973. On the artificial fertilization and rearing of larvae in
Hirasoda, Aitxjs thazard. [In Jpn., Engl, abstr.] J. Fac.
Agric, Kinki Univ. 6:109-112.

HOUDE, E. D.

1974. Effects of temperature and delayed feeding on
growth and survival of larvae of three species of subtropi-
cal marine fishes. Mar. Biol. (Berl.) 26:271-285.

Hunter, J. R.

1972. Swimming and feeding behavior of larval anchovy
Engraulis mordax. Fish. Bull., U.S. 70:821-838.

1976. Culture and growth of northern anchovy, Engraulis
mordax, larvae. Fish. Bull., U.S. 74:81-88.

Hunter, J. R., and j. r. Zweifel.

1971. Swimming speed, tail beat frequency, tail beat
amplitude, and size in jack mackerel, Trachurus symmet-
ricus, and other fishes. Fish. Bull., U.S. 69:253-266.

Kislalioglu, M., and r. N. Gibson.

1976. Prey 'handling time' and its importance in food

HUNTER and KIMBRELL: EARLY LIFE HISTORY OF PACIFIC MACKEREL

selection by the 15-spined stickleback, Spinachia
spinachia (L.) J. Exp. Mar. Biol. Ecol. 25:151-158.

KRAMER, D.

1960. Development of eggs and larvae of Pacific mackerel
and distribution and abundance of larvae 1952-
1956. U.S. Fish. Wildl. Serv., Fish. Bull. 60:393-438.

Kramer, D., and p. E. Smith.

1970. Seasonal and geographic characteristics of fishery
resources, California Current region — IV. Pacific mack-
eral. Commer. Fish. Rev. 32(10:47-49.
LASKER, R.

1964. An experimental study of the effect of temperature
on the incubation time, development, and growth of
Pacific SEirdine embryos and larvae. Copeia 1964:399-
405.
LASKER, R., H. M. FEDER, G. H. THEILACKER, AND R. C. MAY.
1970. Feeding, growth, and survival of Engraulis mordax
larvae reared in the laboratory. Mar. Biol. (Berl.)
5:345-353.
LEONG, R.

1977. Maturation and induced spawning of captive Pacific
mackerel, Scomber japonicus. Fish. Bull., U.S. 75:205-
211.

LETT, P. F.

1978. A comparative study of the recruitment mechanisms
of cod and mackerel, their interaction and its implication
for dual stock management. Ph.D. Thesis, Dalhousie
Univ., Halifax, 125 p.

MAYO, C. A.

1973. Rearing, growth, and development of the eggs and
larvae of seven scombrid fishes from the Straits of Flori-
da. Ph.D. Thesis, Univ. Miami, 127 p.
Pandian, T. J.

1967. Intake, digestion, absorption, and conversion of food
in the fishes Megalops cyprinoides and Ophiocephalus
striatus. Mar. Biol. (Berl.) 1:16-32.
SHELDON, R. W., A. PRAKASH, AND W. H. SUTCLIFFE, jR.

1972. The size distribution of particles in the
ocean. Limnol. Oceanogr. 17:327-340.

Shirota, a.

1970. Studies on the mouth size of fish larvae. [In Jpn.,
Engl, summ.] Bull. Jpn. Soc. Sci. Fish. 36:353-368.
(Transl. by Fish. Res. Board Can., Transl. Ser. 1978.)

Stauffer, G.

1973. A growth model for salmonids reared in hatchery
environments. Ph.D. Thesis, Univ. Washington, Seat-
tle, 213 p.
Stepien, W. P., JR.

1976. Feeding of laboratory-reared larvae of the sea bream
Archosargus rhomboidalis (Sparidae). Mar. Biol. (Berl.)
38:1-16.
THEILACKER, G. H., AND M. F. MCMASTER.

1971. Mass culture of the rotifer Brachionus plicatilis and
its evaluation as a food for larval anchovies. Mar. Biol.
(Berl.) 10:183-188.

Umbreit, w. w., r. h. Burris, and j. f. stauffer.

1964. Manometric techniques. A manual describing
methods applicable to the study of tissue
metabolism. Burgess, Minneap., 305 p.

Watanabe, T.

1970. Morphology and ecology of early stages of life in
Japanese common mackerel. Scomber japonicus Hout-
tuyn, with special reference to fluctuation of popula-
tion. [InJpn.,Engl. abstr.] Bull. Tokai Reg. Fish. Res.
Lab. 62:1-283.

WEBB, P. W.

1975. Hydrodynamics and energetics of fish propul-
sion. Fish. Res. Board Can., Bull. 190, 158 p.

wolfson, f. h.

1965. The optical comparator as a tool in plankton re-
search. Limnol. Oceanogr. 10:156-157.

YOKOTA, T., M. TORIYAMA, F. KANAI, AND S. NOMURA.

1961. Studies on the feeding habit of fishes. [In Jpn.,

Engl, summ.] Rep. Nankai Reg. Fish. Res. Lab. 14,

234 p.
ZWEIFEL, J. R., AND R. LASKER.

1976. Prehatch and posthatch grow^th of fishes — a general
model. Fish. Bull., U.S. 74:609-621.

101

SPAWNING AND FECUNDITY OF ATLANTIC MACKEREL,
SCOMBER SCOMBRUS, IN THE MIDDLE ATLANTIC BIGHT

Wallace W. Morse '

ABSTRACT

Collections of Atlantic mackerel, Scomfcerscomirus, were made during spring 1977 from Maryland to
Rhode Island. Length-weight relationships were determined for total and fork lengths and total and
gutted weights. Spawning time was determined from gonad somatic indices and peak spawning
occurred between 21 April and 4 May. Egg diameter frequencies from running ripe ovaries indicated
five to seven egg batches are spawned by each female during the spawning season. Fecundity was
estimated and ranged from 285,000 to 1,980,000 for fish between 307 and 438 mm fork length.
Fecundity was related to fork length, gutted weight, and age.

The Atlantic mackerel, Scomber scombrus Lin-
naeus, is a schooling, pelagic species ranging from
the Gulf of St. Lawrence to North Carolina in the
northwest Atlantic and from Norway to Spain in
the northeast Atlantic. The northwest Atlantic
population has been separated into northern and
southern contingents on the basis of size composi-
tion, spawning times, summer distributions, and
tagging studies (Sette 1950; Moores et al. 1975;
MacKay2).The northern contingent spawns in the
southern Gulf of St. Lawrence from about the end
of May to mid-August (Ware 1977). The southern
contingent spawns from mid-April to June from
North Carolina to Massachusetts (Berrien 1978).
Fecundity estimates of northwest Atlantic
mackerel are limited to a few observations rang-
ing from about 500,000 to 1,000,000 eggs (Brice
1898: 208-213; Sette 1943). Fecundity of northeast
Atlantic mackerel ranged from approximately
130,000 to 1,100,000 eggs for fish 28.5-46.0 cm
total length (Macer^; Lockwood'*). This paper pre-
sents the results of a fecundity and spawning time
investigation of the southern contingent.

METHODS

Atlantic mackerel were collected between 9
April and 21 May 1977 from recreational and

'Northeast Fisheries Center Sandy Hook Laboratory, Na-
tional Marine Fisheries Service, NOAA, Highlands, NJ 07732.

^MacKay, K, T. 1973. Aspects of the biology of Atlantic
mackerel in ICNAF Subarea 4. Int. Comm. Northwest Atl.
Fish., Res. Doc. 73/70, 11 p.

^Macer, C. T. 1976. Observations on the maturity and
fecundity of mackerel {Scomber scombrus L.) Int. Counc.
Explor. Sea, CM 1976/H:6, 7 p.

■•Lockwood, S. J. 1978. The fecundity of mackerel. Scomber
scombrus L. Int. Counc. Explor. Sea, CM 1978/H:9, 5 p.

commercial catches from Maryland to Rhode Is-
land (Table 1). Length frequencies of males and
females are shown in Figure 1. All fish were mea-
sured to the nearest millimeter fork length (FL)
and total length (TL), and weighed to the nearest
gram total weight (TW) and gutted or somatic
weight (GW). Otoliths were extracted for age de-
termination. Ovaries of all mature females were
exsected, weighed to the nearest 0.01 g, and pre-
served in 10% Formalin.^

Preliminary observations of eggs from ovaries
in the spawning condition revealed that three egg
types were present: 1) small, translucent eggs; 2)

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

Table l. — Catch data of Atlantic mackerel sampled in 1977.

NumI

bers of

fish examined

Capture

Date

Port

Female

Male

method

9 April

Ocean City, Md.

16

8

Otter trawl

16

Cape May. N.J.

15

10

Hook and line

20

Ocean City

26

26

Otter Trawl

25

Barnegat, N.J.

20

25

Hook and line

27

Greenport. N.Y.

64

36

Pound net

28

Belford, N.J.

10

15

Otter trawl

28

Sheepshead Bay, N.Y.

6

16

Hook and line

30

Sheepshead Bay

9

12

Hook and line

1 May

Sheepshead Bay

6

17

Hook and line

4

Barnegat

16

36

Hook and line

5

Barnegat

39

66

Hook and line

7

Sheepshead Bay

11

19

Hook and line

8

Point Pleasant. N.J.

17

8

Hook and line

9

Point Judith. R.I

42

43

Otter trawl

11

Belmar, N.J.

5

20

Hook and line

14

Sheepshead Bay

12

38

Hook and line

15

Sheepshead Bay

4

33

Hook and line

17

Sandy Hook, NJ.

22

20

Hook and line

18

Point Judith

32

48

Otter trawl

22

Sheepshead Bay

77

21

Hook and line

Totals

449

517

Manuscript accepted August 1979
FISHERV BULLETIN: VOL

103

78, NO. 1, 1980.

FISHERY BULLETIN: VOL. 78, NO. 1

z

UJ

Table 2. — Maturity stages of Atlantic mackerel ovaries.

30 0

Figure l.

32 0 34 0 36 0 38 0 40 0 42 0 44 0

FORK LENGTH 10.5 cm midpoints I

-Length frequencies of male and female Atlantic
mackerel used in this study.

larger opaque, yolked eggs; and 3) large translu-
cent eggs. There appeared to be no clear size sep-
aration between egg types, which is indicative of
serial spawners (Hickling and Rutenberg 1936).
Therefore, the method described by Hislop and
Hall (1974) for whiting, Merlangus merlangus,
was used to determine which eggs would be shed
during the current spawning season. Since yolk
deposition indicates eggs are ripening for spawn-
ing, random samples of 300 eggs were measured
from ovaries at successive maturity stages to de-
termine the average minimum size of yolked eggs.
Eggs 0.20 mm and larger contained yolk and were
included for fecundity estimation. Ovaries were
classified into four maturity stages based upon
macroscopic examination and the occurrence of
mature eggs (Table 2). Egg diameter frequencies
of yolked eggs from ovaries in the developing, ripe,
running ripe, and partially spent condition are
shown in Figure 2.

Ovaries in the ripe condition (Figure 2b) were
used for fecundity estimations. If large translu-
cent eggs (1.00-1.35 mm) were present in the
lumen of the ovary, which is indicative of the run-
ning ripe condition (Figure 2c), the ovary was not
utilized for fecundity because some eggs may have
been shed and fecundity would be underestimated.

Stage

Description

1 . Developing

2. Ripe

3. Running
ripe

4. Partially
spent

Ovary enlarged, usually orange colored with a
granular appearance No translucent eggs,
maximum egg diameters 0,8-0.9 mm.

Ovary fills most of gut cavity, yellow colored,
in advanced stage some translucent eggs are
visible ttirough wall. Maximum egg diameter
1 0-1.2 mm.

Similar in appearance to stage 2, eggs are ex-
truded with pressure on abdomen of fish,
t^aximum egg diameters 1.2-1.4 mm.

Ovary is flaccid, often hemorrhaging is evi-
dent at anterior portion of ovary, some
residual mature eggs (1.1-1.4 mm) present.

^^^

25
20
15
10-

1

InJ

IL

N.nrJI

0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1 12 1.3 1.4

EGG DIAMETER I mm I

Figure 2. — Egg diameter frequencies of Atlantic mackerel ova-
ries in stages: developing (a), ripe (b), running ripe (c), and par-
tially spent (d). Each graph based on 300 egg measurements.

Suitable ovaries were removed from the Formalin
solution, placed in glacial acetic acid for 5 min, and
washed, and the eggs were separated with a gentle

104

MORSE: SPAWNING AND FECUNDITY OF ATLANTIC MACKEREL

stream of water and agitated in a 0.20 mm mesh
sieve. Following removal of the ovarian tissue, the
eggs were air dried on blotter paper for 2-3 min
and weighed (±0.01 g), and two subsamples were
removed and weighed (±0.01 mg). All eggs in each
subsample were counted and the mean used to
calculate total egg numbers based on the weight of
all eggs in the ovary. If the two subsample counts
differed by 10*^ or more, additional samples were
taken until two counts differed by <10%.

Ages were determined from otoliths as de-
scribed by Steven (1952).

RESULTS

The allometric relationships of length-weight
were expressed by the power function:

Y =aX^

(1)

where X is length, Y is weight, and a and h are
constants. Equation (1) was converted to the
linear form by a logarithmic (base 10) transforma-
tion to:

log Y = log a + 61og X

(2)

The interrelationships between length mea-
surements and between weight measurements
were expressed by the linear function:

Y = a + bX

(3)

where Y andX are both length or both weight. All
data were fitted using least-squares regression
techniques.

Predictive regression equations were calculated
using all observations for males and females and
an analysis of covariance applied to determine
possible sex related differences. No significant dif-
ferences iP = 0.05) were indicated between sexes
and sexes were therefore pooled. The pooled re-
gression equations and associated statistics are
presented in Table 3.

To determine the peak spawning time the mean
gonad somatic index (GSI = percent ovary weight
of the gutted weight) was calculated for each week
of the sampling period (Figure 3). It appears that
individual fish attain their maximum GSI just
prior to spawning the first egg batch and a decline
in GSI occurs as successive batches are spawned.
This was shown by comparing the mean GSI of
each maturity stage (Table 4) which showed an

Table 3. — Length and weight relationships of Atlantic mack-
erel collected in the Middle Atlantic Bight, 1977. TW = total
weight (grams); GW = gutted weight I grams); TL = total length
(millimeters); and FL = fork length (millimeters). Symbols refer
to the equation Y = a + bX; n = sample size; r = correlation
coefficient; S = standard deviation about the line.

y a b X n r Sy^

Curvilinear relationships between transformed variates

log TW
log GW
logTW
log GW

TL
TW

-5.767
-5.420
-5.780
-5.374

3.275
3.106
3.334
3.140

log TL
log TL
log FL
logFL

966
966
966
966

0.905
0.924
0905
0.924

Linear relationships between untransformed variates

1.793 1.098 FL 966 0.986

-20.410 1.282 GW 966 0.979

0.036
0.030
0.036
0 030

3.594
22.397

19-25

APRIL

Figure 3. — Mean gonad somatic index (ovary weight as a per-
cent of gutted weight) plotted by week for Atlantic mackerel
sampled in 1977. Numbers in parentheses are sample sizes.

Table 4. — Mean gonad somatic index (GSD and standard devia-
tion for each maturity stage of Atlantic mackerel.

stage

Mean GSI

so

1 . Developing

2. Ripe

3. Running ripe

4. Partially spent

10.4

15.0

24.9

8.6

2.9

68

4.2

247

4.7

41

2.2

93

increase from stage 1 to 3 and a rapid decrease at
stage 4. Similar results were reported by Kaiser
(1973 ) for horse mackerel, Trachurus murphyi. He
found that gonad somatic indices reflected mat-
uration changes of the ovaries and a sharp decline
in the mean GSI coincided with the appearance of
the earliest spawning females. In this study the
weekly mean GSI increased during the first 3 wk
of sampling, peaked between 21 April and 4 May,
and then declined steadily through the end of the
sampling (22 May). All females examined from the
last sampling week were partially spent and indi-
cated spawning was nearly completed within the
study area.

105

FISHERY BULLETIN: VOL. 78, NO. 1

The egg diameter frequencies shown in Figure 2
indicate Atlantic mackerel are serial spawners,
i.e., several batches of eggs are shed by individuals
throughout the spawning season. The presence of
multiple modes in the egg diameter frequencies
(Figure 2a-c) and ripening eggs in partially spent
ovaries (Figure 2d) are indicators of serial spawn-
ing (Clark 1935; MacGregor 1957). A cytological
study by Bara ( 1960) has shown that eggs are not
shed continuously as stated by Cunningham
(1889) but are shed in several batches during the
2-mo spawning period.

The potential number of batches spawned was
estimated by determining the ratio of ripe eggs to
all yolked eggs in six running ripe ovaries. Atlan-
tic mackerel eggs, from plankton samples, ranged
from 1.01 to 1.29 mm diameter (Berrien 1975;
Ware 1977); therefore, in this study, eggs 1.05 mm
and larger were assumed to constitute the next
egg batch to be spawned. The ratios ranged from
13.7 to 21.7% and averaged 17.0%. Thus the po-
tential number of batches spawned per individual
was five to seven and averaged six batches.

Fecundity estimates ranged from 285,000 to
1,980,000 eggs for fish between 307 and 438 mm
FL. Preliminary plots indicated a curvilinear rela-
tionship existed for fecundity-length and a linear
relationship for fecundity-weight and fecundity-
age. However, correlation coefficients (r) were
higher for the logarithmic relationships of
fecundity-weight and fecundity-age, therefore, all
variables were transformed and linear regression
equations of the form log Y = a + b(\og X) were
calculated. Data plots and the equations relating
fecundity to fork length, gutted weight, and age
are shown in Figures 4-6.

DISCUSSION

Spavming by the southern contingent of Atlan-
tic mackerel apparently peaked during the 2-wk
period between 21 April and 4 May 1977. This
2-wk period represents the mean peak spawning
time within the study area (Maryland to Rhode
Island) since there is a north and eastward pro-
gression of spawning during the spring migration
(Bigelow and Schroeder 1953; Berrien 1978). Ber-
rien et al.^ observed the north and east progression

*Berrien,P. L., A. Naplin, and M.R.Pennington. 1979. At-
lantic mackerel, Scomber scombrus, egg production and spawn-
ing population estimates for 1977 in the Gulf of Maine, Georges
Bank, and Middle Atlantic Bight. Int. Counc. Explor. Sea
ICES/ELH Symp./DS:9, 17 p.

1.70

1.50

0 30

log F 8.346 + 5.544llog FLI

N 218

r 0 88

Si X 0.066

360 380

FORK LENGTH(mm)

Figure 4. — Relationship of fecundity and length and the pre-
dictive logarithmic (base 10) regression for Atlantic mackerel
in 1977.

3 0 90

O

log F 1721 + 1.547 Hog GWI

N 218

r 0 81

Sy X 0 081

.'•>::'Vi' '■ ■•

300

400 500 600

GUTTED WEIGHT I g)

700

800

900

Figure 5. — Relationship of fecundity and weight and the pre-
dictive logarithmic (base 10) regression for Atlantic mackerel
in 1977.

in plankton mackerel egg densities. They found
spawming intensity in the Middle Atlantic Bight
was low during mid-April and increased rapidly
by late April, and maximum egg densities oc-
curred about 25 April. Spawning continued at a
reduced rate throughout May and then decreased
steadily during June. Very similar results are in-
dicated from my analysis of gonad somatic indices
during the 1977 spawning season.

106

MORSE: SPAWNING AND FECUNDITY OF ATLANTIC MACKEREL

1.90

log F 5 264+0 840llogAI

N 197

r 0 76

Sy X 0 084

FIGURE 6. — Relationship of fecundity and age and the predic-
tive logarithmic (base 10) regression for Atiantic mackerel
in 1977.

Observations of spawning times of various
temperate-water fish have indicated peak spawn-
ing dates may be relatively fixed. Gushing (1969)
postulated an indirect link between the fixity of
spawning season and the primary production cy-
cle. Ware (1977) investigated the relationship of
spawning time of Atlantic mackerel at St. Georges
Bay, Nova Scotia, to the size and abundance of 80
/xm plankton. He found the mean peak egg produc-
tion date was 1 July ± 1 wk and coincided with the
maximum abundance of summer plankton. It
would appear, at least for the southern contingent,
that the time of peak spawning is more variable
than that indicated for St. Georges Bay. Sette
(1943) determined maximum spawning occurred
during mid-May (1928-32) off Middle Atlantic and
southern New England States. Ichthyoplankton
surveys during the mackerel spawning season in
1966 and 1975-77 (Berrien 1978; Berrien et al. see
footnote 6; Berrien and Anderson') within the
Middle Atlantic Bight indicated spawning peaked
during May in 1966 and 1975 and during April in
1976 and 1977. In fact, eggs were collected as early
as 13 April in 1977. Berrien and Anderson (see
footnote 7) attribute the April 1976 spawning

Bemen, p. L., and E. D. Anderson. 1976. Scomber scom-
brus spawning stock estimates in ICNAF Subarea 5 and Statisti-
1Q7C T ^' ^sed on egg catches during 1966, 1975, and
ly/b. Int. Comm. Northwest Ati. Fish., Res. Doc. 76/XII/140
i-U p.

peak to increased water temperatures within the
study area.

The factors controlling the spawning time of
Atlantic mackerel are unclear. The regularity
shown by Ware (1977) would indicate internal
control or a constant external stimulus such as
photoperiod. Sette (1943) presented evidence indi-
cating water temperature is a limiting factor con-
trolling migration and in turn the timing of
spawning in a fixed location. Gushing ( 1967, 1969)
suggested that some fish spawn at a relatively
fixed date that is linked to planktonic productivity
and that changes in plankton production would
cause dramatic changes in year-class success. It
appears that a variable spawning date, as shown
by the southern contingent— linked to the factors
affecting plankton productivity, e.g., tempera-
ture, photoperiod, nutrient content— would in-
crease the chances for larval survival.

The fecundity estimates presented here must be
considered as maximum potential egg production
because, as reported by Macer (see footnote 3),
resorption may significantly reduce the number of
eggs spawned. Preliminary observations by Macer
indicated an average of 11.4% ofyolked eggs were
being resorbed. Bara (1960) observed degc lera-
tion in a "few" mature eggs though no quantita-
tive data were presented. Studies are needed to
define the extent and possible annual changes of
resorption rates and their relationship to fecun-
dity.

ACKNOWLEDGMENTS

I wish to thank Darryl Ghristensen and others
who provided samples from the recreational
catches throughout the course of this study. I ap-
preciate the critical reviews and comments by E.
Anderson and S. J. Wilk. Special thanks to M.
Montone for typing this manuscript and M. Gox for
preparation of the figures.

LITERATURE CITED

Bara, G.

I960. Histological and cytological changes in the ovaries
of the mackerel, Scomber scombrus L., during the annual
cycle. Rev. Fac. Sci. Univ. Istanbul, Ser. B, 25:49-86.
BERRIEN, P. L.

1975. A description of Atiantic mackerel. Scomber scom-
brus, eggs and early larvae. Fish. Bull., U.S. 73:186-192.
1978. Eggs and larvae of Scomber scombrus and Scomber
japonicus in continental shelf waters between Mas-
sachusetts and Florida. Fish. Bull., U.S. 76:95-115.

107

FISHERY BULLETIN: VOL. 78, NO. 1

BIGELOW, H. B., AND W. C. SCHROEDER.

1953. Fishes of the Gulf of Maine. U.S. Fish Wildl. Serv.,
Fish. Bull. 53, 577 p.
Brice.J. J.

1898. A manual of fish-culture, based on the methods of
the United States Commission of Fish and Fisheries.
Rep. U.S. Comm. Fish Fish. 23:1-261.

CLARK, F. N.

1935. Maturity of the California sardine (Sardina
caerulea), determined by ova diameter measure-
ments. Calif. Dep. Fish Game, Fish Bull. 42:5-49.

Cunningham, J. T.

1889. Studies of the reproduction and development of tele-
ostean fishes occurring in the neighborhood of
Plymouth. J. Mar. Biol. Assoc. U.K. 1:10-54.

Gushing, D. H.

1967. The grouping of herring populations. J. Mar. Biol.

Assoc. U.K. 47:193-208.
1969. The regularity of the spawning season of some

fishes. J. Cons. 33:81-92.

HICKLING, C. F., AND E. RUTENBERG.

1936. The ovary as an indicator of the spawning period in
fishes. J. Mar. Biol. Assoc. U.K. 21:311-316.

HISLOP, J, R. G., AND W. B. HALL.

1974. The fecundity of whiting, Merlangus merlangus(L.),
in the North Sea, the Minch and at Iceland. J. Cons.
36:42-49.

Kaiser, C. E.

1973. Gonadal maturation and fecundity of horse mack-
erel Trachurus murphyi (Nichols) off the coast of
Chile. Trans. Am. Fish. Soc. 102:101-108.
MacGregor,J. S.

1957. Fecimdity of the Pacific sardine (Sardinops caeru-
lea). U.S. Fish Wildl. Serv., Fish. Bull. ?>1A21-AAQ.
Moores, J. A., G. H. Winters, and L. S. Parsons.

1975. Migrations and biological characteristics of Atlantic
mackerel (Scomber scombrus) occurring in Newfound-
land waters. J. Fish. Res. Board Can. 32:1347-1357.
SETTE, O. E.

1943. Biology of the Atlantic mackerel (Scomber scom-
brus) of North America. Part I: Early life history, includ-
ing growth, drift, and mortality of the egg and larval
populations. U.S. Fish Wildl. Serv., Fish. Bull. 50:149-
237.

1950. Biology of the Atlantic mackerel (Scomber scom-
brus) of North America. Part II: Migrations and habits.
U.S. Fish Wildl. Serv., Fish. Bull. 51:251-358.
Steven, G. a.

1952. Contributions to the biology of the mackerel,

Scomber scombrus L. III. Age and growth. J. Mar. Biol.

Assoc. U.K. 30:549-568.
WARE, D. M.

1977. Spawning time and egg size of Atlantic mackerel,

Scomber scombrus, in relation to the plankton. J. Fish.

Res. Board Can. 34:2308-2315.

108

RESPIRATION AND DEPTH CONTROL AS POSSIBLE REASONS FOR
SWIMMING OF NORTHERN ANCHOVY, ENGRAULIS MORDAX,

YOLK-SAC LARVAE

Daniel Weihs'

ABSTRACT

Larval northern anchovy in the yolk-sac (nonfeeding) stage exhibit regular bursts of continuous
swimming during the first 3 days after hatching. It has been suggested that this behavior may have a
respiratory function. A different possibility is depth control, countering the tendency of the larvae to
sink when motionless. This paper includes a theoretical and experimental investigation of the possible
functions of these swimming bouts.

The theoretical approach was to define a model and calculate the oxygen available to the larva
when resting and while moving, and experiments were jjerformed as a check of the theoretical
results. The experiments were conducted on yolk-sac larvae in sealed tanks with varying dissolved
oxygen concentrations to determine the effects of reducing the available oxygen on the frequency and
duration of the swimming bursts. Results of the experiments confirmed the theoretical model. They
indicate that the swimming bouts both help the larva stay at a constant depth and have a respiratory
function when the oxygen concentration in seawater is less than 60% of saturation.

Newly hatched northern anchovy, Engraulis
mordax, larvae exhibit a pattern of regular short
bouts of continuous swimming interspersed with
periods of resting. These larvae are still in the
yolk-sac stage and are not feeding so that the
locomotory behavior must have some other pur-
pose, as these motions are energy consuming and
also endanger the animal by attracting predators
(Lillelund and Lasker 1971). Hunter (1972)
suggested that these swimming bouts might have
a respiratory function. Respiration has to be by
cutaneous diffusion through the 2-3 /xm thick skin
(Lillelund and Lasker 1971) of the larvae as the
gills develop only at a later stage. The purpose of
this paper is to test this hypothesis and another
possibility, depth control, to counter sinking due
to the negative buoyancy, using theoretical and
experimental methods.

First, I develop a theoretical model for oxygen
transport to motionless and swimming yolk-sac
larvae and estimate the possible oxygen uptake.
Next, I describe the experiments to test the predic-
tion of the theory for both proposed mechanisms
and compare their results.

'Southwest Fisheries Center La Jolla Laboratory, National
Manne Fisheries Service, NOAA, La Jolla, Calif.; present ad-
dress: Department of Aeronautical Engineering, Technion,
Hidfa, Israel.

METHODS

Analytical Model

A mathematical model is now introduced to con-
sider the possible respiratory function of the bouts
of continuous swimming of yolk-sac anchovy lar-
vae. First, we calculate the oxygen transport to a
motionless larva. This transport is then compared
with the metabolic requirements. If the metabolic
requirements are not met, larval motion (and the
resulting convective diffusion) is required.

The size of yolk-sac larvae (2.7-4.0 mm total
length) and their swimming speeds (Hunter 1972)
lead to tj^ical Reynolds numbers, based on larval
length (Weihs 1980) of <20. (The Reynolds
number is a nondimensional factor indicating the
relative importance of pressure and viscous effects
on a body moving in a fluid under given circum-
stances— the higher the Reynolds number, the
smaller the influence of the viscosity.) The larvae,
as a direct result of their small size, are in a highly
viscous laminar flow situation in which turbulent
effects can be neglected. Thus, the larvae and
their immediately surrounding water would be
transported together in oceanic turbulent eddies,
which are of the order of tens of centimeters in
diameter. As a result, a nonswimming larva would
stay for a relatively long period in the same mass

Manuscript accepted; July 1979.

FISHERf BULLETIN: VOL. 78, NO. 1, 1980.

109

FISHERY BULLETIN: VOL. 78, NO. 1

of water, even though that mass is convected on a
much larger scale.

The motionless larva and its surrounding water
mass may therefore be analyzed separately, as a
distinct system in the thermodynamic sense.
Within this system, oxygen transport to the larva
is controlled by molecular diffusion because the
gill system is not developed at this stage. This
process is time dependent, beginning when the
larva arrives in a certain location (by swimming)
and rests, ending when swimming begins again.
Initially the oxygen concentration in the water
mass surrounding the larva is uniform, but the
larva now starts acting as an oxygen sink, gradu-
ally depleting the oxygen content of the water
surrounding it. This concept of the larva as an
oxygen sink simplifies the calculations, as knowl-
edge of the exact distribution of oxygen diffusivity
on the animal's surface is not required. The sink
model also is useful here as it averages out the
direction of local transport and the body of the
larva into which the oxygen diffuses can be taken
as an equivalent sphere of equal surface area
(Figure 1).

Diffusion into a sphere is most conveniently
analyzed in the spherical coordinate system. The
governing conservation of mass equation can be
written (Crank 1975) as

dt

= D

c 2 dc

+

dr

(1)

where c is the mass fraction of oxygen (a function
of the distance and time); r is the radial distance,
measured for the center of the equivalent spheri-
cal body (the sink); t is the time; and D is the
diffusion coefficient of oxygen in seawater.

The temporal boundary condition is the initial,
uniform state

c(r,0) = c^
while the spatial conditions are
c(^,0 =Co

(2)

(3)

which states that far from the animal the oxygen
concentration stays unchanged at all times.
Strictly, the condition should be defined at some
finite distance but as that distance is much larger
than the animal equivalent radius, it can be ap-

proximated by ^. Next, the oxygen concentration
boundary condition at the surface of the equiva-
lent sphere r = a is obtained. Muscles and vas-
cularized tissues have much higher oxygen trans-
port rates than seawater, due to internal uptake
augmented by active transport. Thus, oxygen will
be absorbed at the surface of the larva as fast as it
arrives by diffusion from the surrounding water.
The oxygen concentration c at the larva's surface
(r = a) is thus constant, and very low, i.e..

c (a, t) = Cj
where Cj->0 and ^>0.

(4)

Equations (2)-(4) enable solving equation (1)
analytically, by classical methods. The solution
can be written in nondimensional form for the
concentration as

C-Cq

ci -Co

± erfc ^~°

'' 2Vd7

(5)

where the complementary error function, erfc, is
defined as

erfc(2)

2 " — 22

f e dz

\/lT

(6)

Numerical values of the complementary error
function are found in most mathematical tables
(e.g., Abramowitz and Stegun 1965).

The rate of mass transfer (flux) J to the animal
is now obtained from

A O^

dA (surface A)

(7)

where p is the density and A the surface area of the
body. For the equivalent sphere of radius a,A-
Aira"^. dc/dr is assumed spherically symmetric so
that

J = -pDA

dc_
dr

(8)

where the concentration derivative is obtained
from Equation (5). Substituting this, and the
value for the surface area, and setting c^ = 0 as in
Equation (4), the total mass flux per unit time J^ is

110

WEIHS: RESPIRATION AND DEPTH CONTROL IN ENGRAUUS MORDAX

Figure l . — Schematic description of model and spherical coordinate system centered on the center of mass of a northern anchovy larva:
a is the radius of an equivalent sphere of equal surface area (not to scale), I is the larval length, and b and I are the average tail strip
depth and length.

Jd = -pDcQ

Anr^— erfc

^2y/Dt

(9)

and when r = a, this simplifies to

2/1 1

Jd = AnpDcQa'^ (— +

° 2VDt^

(10)

Equation (10) consists of two terms in the brack-
ets, multiplied by a constant factor. The first term
in the brackets is the constant, time-independent
contribution while the second describes the initial

111

FISHERY BULLETIN: VOL. 78, NO. 1

transient. The latter drops rapidly, proportionally
to the square root of time elapsed since arrival of
the larva. Substituting numerical values into
Equation (10), the oxygen flux can be compared
with oxygen requirements of larval anchovy to see
if the swimming motions are required for respira-
tion.

The equivalent radius, a, of the larval anchovy
is found by equating the surface area of the larva
and the equivalent sphere. The larva, at this
yolk-sac stage, is described for diffusion purposes
as a sphere of radius q (the yolk sac) attached to an
almost flat ribbon of length Zj and average breadth
b. The combined surface area of the sphere and
ribbon is then taken to be equal to the area of the
equivalent sphere appearing in Equation (10).
Thus

47ra2 = 2l^b + Anq^.

(11)

Using typical values for these parameters for
newly hatched larvae we obtain /j = 1.4 mm, b =
0.3 mm, and q = 0.3 mm (from drawings by E. H.
Ahlstrom, Senior Scientist, Southwest Fisheries
Center, NMFS, NOAA, La Jolla, CA 92038), i.e., a
= 0.0395 cm. The mass content of oxygen in sea-
water at 20° C is Co =7.8 x IQ-^ g/cm^^ (Prosser
1973), and the mass fraction is obtained by divid-
ing by the density of sea water, which then cancels
out in Equation (10). Finally, the diffusion
coefficient of oxygen is approximately equal for
freshwater and seawater (Riley and Skirrow 1965)
so that a reasonable value for 20° C is 1.8 x 10'^
cm2/s (O'Brien et al. 1978), or D = 1.08 x lO'^
cm^/min. Substituting all these values into Equa-
tion (10) we obtain

J= (4.18 + 2.51 r'/2) 10-^ g/min (12)

when the water is 100% saturated. Reducing the
oxygen content of the water causes the value of the
oxygen flux, J, to go down proportionally, i.e., by
multiplying J from Equation ( 12) by the fraction of
saturation. Some typical values of J appear in
Figure 2 with the percent of saturation as the
parameter.

When the larva starts swimming, two changes
in the oxygen supply occur. First, the animal's
motion produces a convective local flow relative to
the body, thus bringing new, oxygen-rich water
closer and removing the respiratory waste prod-
ucts. Secondly, the absolute motion will bring the
larva to an area where the oxygen concentration is

oo

mm

Figure 2.— Rate of oxygen transport (J) to motionless northern
anchovy larva by diffusion versus time (t). Broken part of curve
shows asymptotic value, after the initial transient has disap-
peared. Parameter is oxygen concentration in percentage of sat-
uration.

still at the initial ambient value, starting the pro-
cess described by Equations (l)-(4) again.

Following this reasoning, even relatively slight
motions causing just a local flow around the ani-
mal's body would suffice for respiratory functions.
Thus, actual swimming would not be required.
However, the yolk-sac larvae are increasingly
negatively buoyant with age (Hunter and Sanchez
1976), which causes them to sink. Therefore, ac-
tive absolute motion is necessary for the larva to
stay at a given depth for feeding and future school-
ing.

When the larva is swimming, the process of
transport of oxygen changes to convective diffu-
sion, and as such is described by a different model
(Daykin 1965). Daykin's work dealt with station-
ary eggs in a moving river environment, but for
mass transfer purposes this is equivalent to a
larva (or egg) moving at constant speed relative to
the water. In the convective diffusion process
(Levich 1962; Daykin 1965), the mass transfer to
the larva can be roughly described by

'^con = 47TaHc„-C^)k

(13)

112

WEIHS; RESPIRATION AND DEPTH CONTROL IN ENGRAULIS MORDAX

where ^ is a diffusion coefficient obtained from
experimental correlations of the diffusional flux
with the Reynolds (Re) and Schmidt numbers (Sc).
(The Schmidt number is the ratio of the kinematic
viscosity to the diffusivity and nondimensionally
indicates the relative importance of these two ef-
fects in a given flow situation.) For the present
circumstances

D

k = — {2 + 0.6 Re '/2 Sc'/3)

2a

(14)

for average swimming speeds of approximately
5 cm/s ( Hunter 1972) and a Schmidt number of 600
we have

J,„„ = 1.27 X 10"^ g/min.

(15)

Hence, oxygen transport due to convective diffu-
sion is over 20 times higher than for the motion-
less larva (Equation ( 12)). The calculation leading
to Equation (15) is approximate, as the larva's
shape will influence the coefficient 0.6 in k (Equa-
tion (14)) and also change the form of Equation
( 13). It is, however, accurate to at least an order of
magnitude (Levich 1962). Thus, once the larva
starts swimming, the mass transfer of oxygen to
its surface increases by at least an order of mag-
nitude. Recently, an additional mechanism for
oxygen transport to stationary eggs was identified
by O'Brien et al. (1978) who showed that under
certain riverbed conditions natural convection,
due to the oxygen and metabolite gradients, may
contribute to the oxygen transfer. This effect may
play a supplementary role in the present (pelagic)
case as the natural convection effects are much
smaller than the forced convection.

Tests with Larvae

Egg batches were obtained once a week from
groups of adult northern anchovy maintained in
the laboratory and induced to spawn. Measure-
ments were made each week during a 6-wk period
to minimize bias due to a single cohort group.
Water temperature ranged from 19° to 21° C, and
overhead fluorescent lighting was used. The 50%
hatching point was determined and defined as
"day 0" for each batch. Experiments were carried
out on age day 0 larvae every week (six times).

A set of five 2,000 ml graduated cylinders filled
with filtered seawater was used for the environ-
mental tests. Oxygen concentrations of 100, 80,

60, 40, and 20% of saturation at the measured
temperature were produced by bubbling nitrogen
through each of the cylinders. After the larvae
were added (about 25 individuals/cylinder), the
cylinders were sealed off with rubber stoppers.
Oxygen concentrations were measured periodi-
cally during the experiments with a Beckman In-
strument Model 160 Physiological Gas Analyzer^
to check on initial values and possible drift;.

Individual fish were monitored for a 5-min
period, and duration and number of swimming
bursts were recorded on a Esterline- Angus Opera-
tion Recorder Model AW. Records were also made
of approximate swimming direction (measured
from horizontal) as well as the change in orienta-
tion of motionless larvae while they were sinking
during the resting periods. Five active larvae were
monitored in each container every week, for both
day 0 and day 1 tests.

After the day 0 experiments were finished each
week, the equipment was reset and the day 1 tests
conducted 24 h later with additional larvae from
the same batch. The latter larvae were kept in
oxygen-saturated water from hatching to
minimize stress due to oxygen starvation.

RESULTS

No appreciable change in the proportion of time
spent in burst swimming was observed when the
measurement at 100% of saturation concentration
of oxygen (which is the oxygen level in the natural
state in the sea because of turbulent interchange
with the atmosphere) was compared with the time
spent in motion at the 80 and 60% oxygen levels
(Figures).

When oxygen levels were <60% of saturation,
large increases in the time spent swimming were
observed. The rate of increase of swimming time in
both ages (day 0 and day 1) were similar. Various
attempts at describing all five data points for each
age-group by means of a single empirical exponen-
tial function were not successful (low coefficients
of determination). Thus, it seems that a different
behavioral mechanism is triggered when oxygen
levels fall below 60%^^ of saturation at the given
temperatures, i.e., much lower than expected oxy-
gen concentrations in the upper layers of the sea,
where the anchovy larvae are usually found.

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

113

FISHERY BULLETIN: VOL. 78, NO. 1

015

0.10

O05

S(0.

Figure 3. — Fraction of time spent actively swimming, ^, versus
oxygen concentration in percentage of saturation. S[02], for
newly hatched (day 0) and 24-h-old (day 1) northern anchovy
larvae. Each point on the full curves is an average of between 20
and 25 individual 5-min observations. Bounds are standard er-
rors. Dashed lines indicate idealized model of constant fraction,
I,, at high S[02l and linearly increasing i at low SLOj].

The duration of bursts increased monotonically
as the oxygen levels decreased, while the number
of bursts dropped significantly to a minimum of
1/min at 60-80%, increasing sharply after that
(Figure 4). No satisfactory explanation has been
found for the drop in the number of bursts at 80%
of saturation. The main result illustrated by Fig-
ure 4 is that both the frequency and duration of
bursts increase markedly at low oxygen concen-
trations, both contributing to the increase in time
spent swimming.

The center of gravity of anchovy larvae is in the
vicinity of the head and therefore they tend to be
oriented in an oblique head-dowm configuration
after swimming ceases. More mature larvae,
which have converted significant amounts of yolk
into denser tissue are negatively buoyant (Hunter
and Sanchez 1976) and tend to sink head down-
ward at rates of approximately 1-2 mm/s. To check
the vertical station-keeping hypothesis, the direc-
tion of swimming was recorded, as well as the body

40% 60%

sLo^]

Figure 4. — Average duration (t) of swimming bouts (full lines)
and number of bouts (n) in 5 min (dashed lines) for day 0 (solid
triangles) and day 1 (solid circles) larvae, versus oxygen in per-
centage of saturation concentration (SIOjl).

orientation, when swimming started. The results
of over 1 ,400 recorded swimming periods appear in
Table 1, which lists average values of the body
angle at the onset of swimming and the direction
of swimming.

No significant variation in swimming direction
with oxygen concentration was found for either
day 0 or day 1 larvae (Table 1). The spread in
results was large, as is noticeable from the stan-
dard errors. The total possible spread of data is
±90°, which suggests that swimming direction is
actually a random phenomenon for day 0 larvae.
At age 1 day, a positive bias was observed in the
swimming direction, still with large variation.
The body inclination at the beginning of the
swimming periods was consistent, at around -65°
with the exception of the day 0, 20% oxygen data,
which is influenced by additional factors, dis-
cussed below.

DISCUSSION

The analytical model predicted that a motion-
less larva would be able to pick up oxygen at a
decreasing rate at any given spot (Equation 12).

Table l. — Initial orientation of the body and duration of swimming during bouts of continuous sv«mming by newly hatched and
1-d-old northern anchovy larvae. Error bounds are standard error. Angles are measured from the horizontal. Positive values indicate
upward motion. Averages of day 0 do not include 20% O^ values as these (indicated by question marks) include different phenomena.

Oxygen concentration

N. number of observed events
Day 0 larvae Day 1 larvae

Orientation of body at start of
swimming period (degrees)

Direction of svifimming relative
to horizontal (degrees)

(% of saturation)

Day 0 larvae

Day 1 larvae

Day 0 larvae

Day 1 larvae

100

80
60
40
20

Weighted average

106
103
109
161
210

157
113
112
140
204

-68.9 = 23.7
-66.3 = 29.4
-72.1=15.6
-61.0=30.3
-45.6 = 36.7(7)

-66.4=25.2

-74.6 = 11.8
-80.0± 9.2
-66.7=17.6
-69.2 = 22.0
-63.8=27.8

-70.2 = 16.9

-4.7 = 56.1
-15.0 = 59.0
-3.9 = 73.6
12.3 = 540
38.7 = 43.3(7)

-2.8 = 58.3

44.7 = 45.8
28,2 = 58.1
51.9=31.9
33.2=45.9
37.4 = 52.3

39.0=48.1

114

WEIHS: RESPIRATION AND DEPTH CONTROL W ENGRAUUS MORDAX

This prediction has now to be compared with the
requirements of the organisms to determine if ad-
ditional oxygen is needed. Data for oxygen con-
sumption at 17° C of late-stage anchovy eggs and
larvae of differing ages as a function of time since
spawning has been obtained by Theilacker,^ by
measurement in a respirometer. These data were
adjusted to 20° C, the temperature at which most
of my experiments were conducted (Figure 5), by
means of a temperature-growth correlation for
larval northern anchovy (Zweifel and Hunter^).
This adjustment was made by calculating the size
of the larvae at 17° C at the ages recorded by
Theilacker, then translating these into age for the
same size at the new temperature, which gave a
smaller size because growth rates increase with
temperature. Thus, an estimate for the oxygen
requirements at 20° C of size-defined larvae was
obtained as a function of their age ( the 20° C line in
Figure 5).

The value of the ratio of oxygen consumption 1 d
after hatching to that at hatching was about 1.6
(Figure 5). Returning now to Figure 3 we see that
the ratio for the average percent of time spent
swimming of the two age-groups is approximately
1.66. I conclude, therefore, that the distance be-
tween the day 0 and day 1 curves in Figure 3 is an
indication of the increased general activity of the
larvae as they grow. This correlation indicated in
Figures 3 and 5 serves as an additional verifica-
tion of both Theilacker's respirometer data and
the present swimming data.

To compare experimental values of oxygen con-
sumption to the prediction of the model we plot the
data as Figure 6, where the horizontal lines show
the range of oxygen requirements (from Theilack-
er's data) at hatching and 24 h later. The steady-
state oxygen available by steady-state diffusion
only (after the initial transient) obtained from the
time-dependent first term in Equation ( 12) is now
superimposed. Figure 6 indicates that pure diffu-
sion supplies all the oxygen required for the day 0
larvae only when <42±47f of the O2 saturation
concentration is available. This changes to 63 ± 4%
of saturation for the day 1 larvae. The sharp dis-
continuity in the swimming data, occurring be-

0.61-

^G. Theilacker, Fishery Biologist, Southwest Fisheries Center
La Jolla Laboratory, National Marine Fisheries Service, NOAA,
La Jolla, CA 92030, pers. commun. November 1978.

"Zweifel, J. R., and J. R. Hunter. 1978. Temperature
specific equations for grovrth and development of anchovy (En-
graulis mordax) during embryonic and larval stages. Unpubl.
manuscr. , 37 p. Southwest Fisheries Center La Jolla Laboratory,
National Marine Fisheries Service, NOAA, La Jolla, CA 92038.

0.5

0.4

0.3

0.2

0.1

/

/ /

20»C / /

/ /

//

/ / 17 'C

/

/
/

/

/ /X"" Hatching

).ol \ L

2 4 6 8 10 12

DAYS

14

Figure 5. — Oxygen consumption by northern anchovy eggs and
larvae versus time elapsed since spawning. Open circles indicate
experimental data for 17° C. The line for 20" C is extrapolated
from the 17^ C data with the aid of the Zweifel and Himter model

(see text).

s[o,]

Figure 6. — Estimated oxygen requirements (J^) of northern
anchovy larvae at day 0 (hatching) and day 1, and steady-state
oxygen supply by diffusion versus oxygen in percentage of sat-
uration concentration (S[02]). The triangle and circle denote
concentrations at which observed swimming behavior changes
at day 0 and day 1, respectively (see Figure 3).

115

FISHERY BULLETIN: VOL. 78, NO. 1

tween 60 and 407f oxygen concentration ( Figure 3 )
can now be understood in terms of the theoretical
results above. When the oxygen concentration in
this water is 60% or higher, diffusion alone can
satisfy the respiratory requirements of both day 0
and day 1 motionless larvae. Thus, the swimming
activity at the higher concentrations is due to
other factors, such as depth control. The measured
activity level (Figure 3) does not change between
60 and lOO'/f oxygen concentration, as expected
from the theoretical model's predictions.

The increased swimming activity observed
when the concentration drops below the 40-60%
level must therefore be a respiratory reaction. Ac-
tive swimming causes convective diffusion (which,
as shown in the Analytical Model section, leads to
much higher oxygen transport rates) and moves
the larva to a new, nondepleted position. As ex-
pected from this mechanism, activity increases
with decreasing ambient oxygen concentration, as
oxygen transport rates drop below the required
level faster at low ambient concentration, initiat-
ing motion more often. The dashed lines in Figure
3 verify this theoretical reasoning and the ob-
tained values of 59% concentration (day 1) and
55% concentration (day 0) for the beginning of
respiration-driven swimming are in very good
agreement with Figure 6, especially considering
the experimental errors involved in the various
data sources.

Next, I consider the significance of swimming
activity at higher oxygen concentration. The most
plausible reason for the swimming behavior is to
keep the larvae, which are negatively buoyant,
from sinking out of the preferred depth zone in the
sea. Day 1 larvae swim at an average angle of 39°
upwards from the horizontal with no significant
variation with oxygen concentration (Table 1).
The large standard error is an indication of the
wide spread of observed directions. The average
swimming speed at this stage is 5.2 ±4.1 cm/s
(Hunter 1972) and the average duration of a
swimming bout (at oxygen concentration of 60-
100%) is about 2.1s (Figure 4). The average verti-
cal component of the distance moved during a
single bout is therefore

/i„p = Vt sin a = 5.2 ■ 2.1 sin 39°

6.9 cm. (16)

The uncertainty in this value is large due to the
standard errors in both the swimming angle and

116

the average swimming speed, but it is probably
accurate at least to an order of magnitude. Be-
tween swimming periods, the larvae sink at a
speed of 0.12 ±0.03 cm/s (Hunter and Sanchez
1976). The average number of swimming bouts per
5-min period was found to be about 7 (Figure 4),
i.e., giving an average sinking time of 43 s. This
leads to a vertical distance of 5.2 cm, which is close
enough to the value of 6.9 cm of Equation (16) to
show that the swimming of day 1 larvae at high
oxygen levels most probably is a depth-control
mechanism.

The newly hatched (day 0) larvae present a dif-
ferent situation. Pelagic eggs are slightly posi-
tively buoyant (Blaxter 1969) while the chorion,
which is shed during hatching, is somewhat nega-
tively buoyant. Thus, while no measurements in-
dependent of the present ones exist, it is reason-
able to assume that these newly hatched larva are
approximately neutrally buoyant due to their
large yolk sac. As the yolk is consumed, the
specific gravity increases and the sinking rates for
day 1 are obtained. The larvae are approximately
neutrally buoyant during the first hours after
hatching so that no net sinking or upward swim-
ming is expected. Table 1 shows that this is actu-
ally the case at day 0, where the average direction
is very close to horizontal and the large error indi-
cates almost random swimming direction. Some
upward swimming may be discerned at the very
low O2 concentration experiments (20% O2). This
may be a result of an inadvertent oxygen gradient
in the tank or a phototactic response induced by
the low oxygen concentration. Phototaxis is prob-
ably the means by which the older larvae choose
swimming direction, and is directed upwards as
light in the present experiments comes from the
surface.

ACKNOWLEDGMENTS

This paper was written while I was a NRC-
NOAA Senior Research Associate, on leave from
the Department of Aeronautical Engineering,
Technion, Haifa, Israel. I would like to thank John
R. Hunter and Reuben Lasker for reading the
manuscript and various discussions, E. H.
Ahlstrom and Gail Theilacker for generously al-
lowing me to use their unpublished data, and Bob
Millman and Steve Lucas for help with the exper-
iments.

WEIHS: RESPIRATION AND DEPTH CONTROL IN ENGRAULIS MORDAX

LITERATURE CITED

ABRAMOWITZ, M., AND I. A. STEGUN (editors).

1965. Handbook of mathematical functions with formulas,
graphs, and mathematical tables. Dover, N.Y., 1046 p.
BLAXTER, J. H. S.

1969. Development: eggs and larvae. In W. S. Hoar and
D. J. Randall (editors), Fish physiology. Vol. 3, p. 177-252.
Acad. Press, N.Y.
Crank, J.

1975. The mathematics of diffusion. 2d ed. Clarendon
Press, Oxf.,414 p.

DA'iKIN, P. N.

1965. Application of mass transfer theory to the problem of
respiration of fish eggs. J. Fish. Res. Board Can.
22:159-171.
HUNTER, J. R.

1972. Swimming and feeding behavior of larval anchovy
Engraulis mordax. Fish. Bull., U.S. 70:821-838.
HUNTER, J. R., AND C. SANCHEZ.

1976. Die! changes in swim bladder inflation of the larvae

of the northern anchovy, En^rau/is mordax. Fish. Bull.,
U.S. 74:847-855.
LEVICH, V. G.

1962. Physiochemical hydrodynamics. Prentice-Hall,
Inc., Englewood Cliffs, N.J., 700 p.
LILLELUND, K., AND R. LASKER.

1971. Laboratory studies of predation by marine copepods
on fish larvae. Fish. Bull., U.S. 69:655-667.

O'Brien, r. n., S. visaisouk, r. Raine, and d. f. Alderdice.
1978. Natural convection: a mechanism for transporting
oxygen to incubating salmon eggs. J. Fish. Res. Board
Can. 35:1316-1321.

Prosser, C.

1973. Comparative animal physiology. W. B. Saunders
Co.,N.Y.,966p.
Riley, J. P., and G. Skirrow.

1965. Chemical oceanography. Academic Press, N.Y.,
Vol. 1., 712 p.
weihs, D.

1980. Energetic significance of changes in swimming
modes during growth of larval anchovy, Engraulis mor-
dax. Fish. Bull., U.S. 77:597-604.

117

DESCRIPTIONS OF LARVAL SILVER PERCH, BAIRDIELLA CHRYSOURA,

BANDED DRUM, LARIMUS FASCIATUS, AND STAR DRUM,

STELLIFER LANCEOLATUS (SCIAENIDAE)'^

Howard Powles^

ABSTRACT

This paper presents descriptions and illustrations of larval Bairdiella chrysoura (3.1-8.8 mm standard
length), Larimus fasciatus (3.0-5.9 mm standard length), and Stellifer lanceolatus (2.8-15.1 mm
standard length). Larimus fasciatus larvae are characterized by brain pigment, pectoral fin pigment,
and early-developing pectoral fin rays. Larval B. chrysoura resemble S. lanceolatus, but B. chrysoura
have a swath of expanded melanophores from nape to cleithral symphysis. These two species also can be
differentiated by the sequence of melanophores in the midventral line posterior to the anus. Off the
southeastern United States, L. fasciatus spawn in continental shelf waters from May to October, andS.
chrysoura and S. lanceolatus spawn in coastal and estuarine waters during late spring and summer.

The perciform family Sciaenidae is represented by
18 species off the southeastern United States (Ta-
ble 1). Taxonomy of adult Sciaenidae of the west-
em North Atlantic has recently been revised by
Chao (1978); nomenclature in the present paper
follows Chao (1978) rather than Bailey et al.
(1970). Studies of larval sciaenids of the east coast
of the United States have been numerous; these
have recently been summarized in several publi-
cations (Scotton et al. 1973; Johnson 1978; Powles
and Stender 1978; Lippson and Moran"*.) Despite
the number of larval studies, their quality has
been uneven; for example, larval series now
known to consist of more than one species have
been described as single species (Menticirrhus
americanus and Stellifer lanceolatus of Hilde-
brand and Cable 1934), damaged or distorted
specimens have been illustrated and described
(Sciaenops ocellata of Pearson 1929; Leiostomus
xanthurus of Hildebrand and Cable 1930), and
illustrations have differed from descriptions of
larvae of the same species in the same publication
(early Stellifer lanceolatus of Hildebrand and
Cable 1934). Further, few detailed developmental

'South Carolina Marine Resources Center Contribution No.
94.

^MARMAP Contribution No. 164.

'Marine Resources Research Institute, Charleston, S.C; pres-
ent address: Gouvemement du Canada, Peches et Oceans, Divi-
sion des Sciences halieutiques.C.P. 15500, Quebec, Canada GIK

"Lippson, A. J., and R. L. Moran. 1974. Manual for iden-
tification of early developmental stages of fishes of the Potomac
River estuary. Md. Dep. Nat. Resour., Power Plant Siting Pro-
gram, PPSP-MP- 13: 1-282.

series of morphometric, meristic, and pigmenta-
tion data have been published, making separa-
tion of larvae to species impossible in the early
stages before complete development of fin ele-
ments. Thus, both description of undescribed or
incompletely described larvae and redescription
of larvae which have been poorly described in the
literature are necessary to specific identification
of sciaenid larvae.

The three species whose larvae are treated in
this paper are generally similar in habitat and
probably in ecology. They are small fishes
(maximum total lengths 20-23 cm) of coastal and
estuarine waters (Hildebrand and Schroeder
1928; Hoese and Moore 1977). None are important
commercial or sport fish, but all are abundant in
estuaries (Dahlberg 1972; Shealy et al. 1974) and
on coastal shrimp grounds (Anderson 1968; Reiser
1976). Because of their abundance and small size,
all may be important prey items for larger, pre-
dacious fishes.

Descriptions of larvae of all three species have
been published. Kuntz (1915) described eggs and
yolk-sac larvae o{ Bairdiella chrysoura from eggs
obtained from a ripe female and further described
larvae and early juveniles from plankton collec-
tions. Since he examined live or fresh material
rather than Formalin-preserved^ material, it is to
be expected that body proportions and pigment
characters of his series might differ from those in

Manuscnpt accepted August 1979

FISHERY BULLETIN; VOL. 78, NO. 1, 1980.

^Reference to trade name does not imply endorsement by the
National Marine Fisheries Service, NOAA.

119

larvae from preserved series. His description was
cited by later authors (Hildebrand and Cable

FISHERY BULLETIN: VOL. 78, NO. 1

1934; Scotton et al. 1973; Johnson 1978; Lippson
and Moran see footnote 4) in compilations of larval

Table l. — Reported meristics of South Atlantic Bight Sciaenidae. Counts in parentheses occur infrequently and semicolon indicates

separate dorsal fins.

Dorsal

Anal

Gill rakers

Species

Source' Spines

Rays

Spines Rays Caudal procurrent Vertebrae^ Upper Lower

Bairdiella chrysoura

Cynoscion nebulosus

C nothus

C regalis

Equetus acuminatus

E. lanceolatus

E. punctatus

E. umbrosus

Larimus fasciatus

Leiostomus xanthurus

Menticirrhus americanus

M. littoralis

M. saxatilis

Micropogonias undulatus

Pogonias cromis

Sciaenops ocellata

Stelliler lanceolatus

1
4
5

7
1
3

4
5

7
9
1
2
3
4
5
7
9
1
4
5
6
7
1
5
7
8
1
5
7
8
1
5
7
8
1
5
7
1
4
5
7
1
4
5
7
1
4
5
7
1
4
5
7
1
4
5
7
1
4
5
7
1
4
5
7
1

4
5
7
1
5
7

X;l

XI-XII

Xl;l

XII

IX-X

X(XI);I

X:l

XI-XII

X;l

X;l
X;l
XI

X:i

X;l

X:i

X-XI;I

XI

VIII-IX;I

X;l

X-XI

IX-X;I

XII-XIII;I

XIV-XVI;I

XIII-XIV

XIII-XIV

XI-XII;I

XI-XII;I

XIII

XI-XII;I

X-XI;I

X;l

IX-X I

X:l

X;l

X;l

XI-XII

IX;I

X;l

X;l

XI-XII

X;l

X;l

X;l

XI

X-XI

X;l

X;l

XI

X;l

X;l

X;l

XI

X;l

X;l

X;l

XI

X;l

X;l

X:l

XI

X;l

X;l

X;l

XI

XI-XII;I

Xl;l

XII-XIII

19-23
19-21

22
19-22
25-28

25
24-26
25-27
24-27
25-27
26-30
27-30(31)
24-28
28-29
27-29
28-30
26-29
26-29
25-28
26-29
24-29
24-28
37-41
38-40
36-40
37-40
47-55

53
46-50
49-55
45-47

46
44-49
45-47
38-40

40
38-39
24-27
24-27
24-26
25-27
29-35
30-34

31
29-32
20-26
24-27
24-25
24-26
19-26
24-26
23-25
24-25
22-27
24-26
26-27
23-25
27-30
28-29
28-29
28-29
19-21
20-22

21
21-23
23-25
23-25

24
23-25
20-24
20-23
21-24

8-10

9-10
10

8-10
10-11
10-12
10-11
10
10-11

9-10

8-10

8-9(10)

8-10
9

9-10
9

9-11
11-13
11-12
11-13
10-12
10-12

7-8
7

6-8

6
5
6

6-8
6-7
7-8

7
7
7

6-8
5-6
6
12-13
12-13
12
12-13
6-8
7-8
7
7-8

7

7

7
7-9
8-9

8
7-8
8-9

8

7

8
5-6
6-7
5-6

6
8-9

8

8
7-8

7-8
7-9

8-9, 5-8

6-9, 5-7

7-8, 6-8

7-9, 5-7

7-8, 6-7

7-8, 6-7

7,5-7

7-8,7

6-7, 4-7

6-8, 6-8

8-9,7

7-8.6

6-8,6

8-9,8

8-9,7

8-10,7-9

7-9, 6-9

12 + 13

11 + 14
(12)13 + 12(13)
25

13 + 12

15 + 12
27(26)

14 + 13
(12)13+12(13)

14-15+10
13 + 12
10 + 15

10 + 15

10+15

10 + 15

10+15

10+15

10 + 15

10 + 15

11 + 14

10+15
10+15

10 + 15
10+15

10 + 15
10+15

10+15
10 + 15

10+15
10 + 15

10+15
10+14

10 + 14
10 + 15

7-8

2-3

4
3-4

4-5

5-6
6

5-6
6

10+15
11 + 14

10+15

4-6

11-13

12

8-12

8

2-3

3-5

3-5

8-10

7
4-6

4
4-5

5

10-13
13

14-16

14-16

16

7-9
8
8

7

6-8
8-10

12-14(15)
12-14
9-
9

10-13
11-13
5 11

9-14
9

10-13
9

10-13
11

10-12

22-25

23-25

24

20-23

22-23

22

0-7
6

0-8
7-8

7

0-7
6

14-18

14-16

16

12-16

14-16
12

7-9
8-9

7

22-23
22

120

POWLES: DESCMPTIONS OF LARVAL SILVER PERCH, BANDED DRUM, AND STAR DRUM
T.\BLE 1. — Continued.

Source'

Dorsal

Anal

Caudal procurrent

Vertebrae

Gill rakers

Species

Spines

Rays

Spines Rays

Upper Lower

Umbhna coroides

1
4
5

X;l
X;l
X;l

26-31

29

27-28

II 6

II 6
II 6-7

11-1-14

5-7 7-10

11

5 9

'Sources:

1. Chao 1978

6.

Lippson and Moran (see text footnote 4)

2. Ginsburg 1929

7

Miller and Jorgensen 1973

3. Hildebrand and Cable 1934

8.

Randall 1968

4. Hildebrand and Schroeder 1928

9

Welsh and Breder 1923.

5. Jordan and Evermann 1896

'Includes urostyle.

sciaenids. Jannke^ illustrated 5. chrysoura of 2.0
and 5.0 mm SL (standard length). Hildebrand and
Cable (1934) described a series identified as
Larimus fasciatus. Although there is some dis-
agreement between illustrations and descriptions
of early larvae in this work, the series appears
to represent a single species and to be correctly
identified. Hildebrand and Cable also described
larvae and juveniles identified as Stellifer
lanceolatus . Their early larvae represent a mixed
series; larvae <4 mm long had pectoral fin pig-
ment and developed pectoral rays, but larvae >4.5
mm long had no pectoral pigment and pectoral
rays that developed at ^5.6 mm. Body proportions
also changed between 4.0 and 4.5 mm. Their series
appears coherent and correctly identified at
lengths 5=5.6 mm. There were also some dis-
crepancies between drawings and descriptions of
early stages in their paper.

The purpose of the present paper is to redescribe
larvae of these three species and to summarize
characters for differentiating between the three
species. In addition, notes are given on time and
place of larval collections and on separation of
larvae of these three species from those of other
marine sciaenids of the southeastern United
States.

METHODS

of North Carolina. Those from continental shelf
waters were collected with Boothbay neuston nets
(mouth 1 m high x 2 m wide, mesh size 0.947 mm,
tow velocity 2.6 m/s), MARMAP neuston nets
(mouth 0.5 X 1.0 m, mesh size 0.505 mm, tow
velocity 1 .0 m/s), and 60 cm bongo nets ( mesh size
0.505 mm, towing velocity 0.8 m/s) towed in a
double oblique pattern between surface and bot-
tom or 200 m depth. Specimens from South
Carolina estuaries were collected with 0.5 m
diameter conical nets (mesh size 0.571 mm, towing
velocity 1.3-1.5 m/s) towed at surface or bottom.
South Carolina tidal passes were sampled with 1.0
m mouth diameter plankton nets (mesh size 0.571
mm) moored to bridges or piers and fished near
bottom for 1 h at early or middle flood tide. Speci-
mens from the Cape Fear River estuary were col-
lected with 1.0 m mouth diameter conical nets
(mesh size 0.760 mm) towed at surface at 0.5 m/s.
The number of samples available from each area
except the Cape Fear River estuary by month (Ta-
ble 2) provides an estimate of seasonal and areal
effort distribution for comparison with data on
time and place of capture of larvae. Tidal pass
sampling was not carried out from August to
January, and estuarine samples from August to
December were not available. All specimens were
preserved in 2% formaldehyde buffered by
saturating with borax. Specimens from continen-

Approximately 50 specimens of each species
were examined. Descriptions are based on the fol-
lowing numbers of specimens: silver perch, Bair-
diella chrysoura, 21; banded drum, Larimus fas-
ciatus, 21; star drum, Stellifer lanceolatus, 26.

Specimens on which descriptions were based
were collected from continental shelf waters of the
South Atlantic Bight, estuaries and tidal passes of
South Carolina, and the Cape Fear River estuary

^Jannke, T. E. 1971. Abundance of young sciaenid fishes
in Everglades National Park, Fla., in relation to season and
other variables. Univ. Miami Sea Grant Tech. Bull. 11:1-128.

Table 2. — Numbers of plankton samples from South Carolina
estuaries (1974), South Carolina tidal passes (1976), and the
South Atlantic Bight continental shelf (1973-76) that were
sorted for larval Sciaenidae.

Estuar

les

Tidal passes

Continen
Neuston

ital shelf

Month

Surface

Bottom

Bongo

Jan.

33

30

30

30

Feb.

17

14

2

30

30

Mar.

17

14

1

47

47

Apr.

33

28

1

52

38

May

19

17

2

48

48

June

17

17

5

—

—

July

16

16

8

—

—

Aug.

—

—

—

40

37

Sept.

—

—

—

39

1

Oct.

—

—

10

11

Nov.

—

—

—

31

16

121

FISHERY BULLETIN: VOL. 78, NO. 1

tal shelf waters were initially fixed by immersing
net cod ends in 8% formaldehyde for 2 min im-
mediately following net washdown.

Measurements were made on the left side of the
body, by ocular micrometer on a dissecting micro-
scope. All measurements were made along or per-
pendicular to the body midline. Measurements are
defined as follows:

Notochord length (NL) — symphysis of upper
jaw to tip of notochord (measured in preflexion
larvae).

Standard length (SL) — symphysis of upper jaw
to posterior edge of hypurals (measured in larvae
undergoing notochord flexion and in postflexion
larvae).

Snout length — symphysis of upper jaw to an-
terior margin of eye.

Eye diameter — horizontal diameter of eye.

Head length — symphysis of upper jaw to pos-
terior margin of opercular membrane.

Preanus length — symphysis of upper jaw to
posterior margin of anus.

Snout to origin of spinous dorsal fin — sym-
physis of upper jaw to anterior margin of first
developed dorsal spine base.

Snout to origin of soft dorsal fin — symphysis of
upper jaw to anterior margin of first developed
dorsal ray base.

Snout to dorsal fin termination — symphysis of
upper jaw to posterior margin of last developed
dorsal ray base.

Snout to anal fin origin — symphysis of upper
jaw to anterior margin of first developed anal ele-
ment base.

Snout to anal fin termination — symphysis of
upper jaw to posterior margin of last developed
anal ray base.

Anus to anal fin — posterior margin of anus to
first developed anal element base.

Snout to pelvic fin insertion — symphysis of
upper jaw to anterior margin of base of pelvic fin.

Depth at cleithral symphysis — vertical dis-
tance between dorsal margin of body and ventral
symphysis of cleithra.

Depth at caudal peduncle — least vertical dis-
tance between dorsal and ventral margins of body
in the area posterior to the terminal dorsal and
anal fin rays and anterior to the hypural bones.

Fin counts include all elements of which any
part (including pterygiophore) was developed.
Counts were made in unstained specimens since

the primary purpose of the study was to permit
identification of specimens from field collections.
Unless otherwise stated, lengths referred to in this
paper are standard lengths.

Data on occurrences of larval Larimus fasciatus
in plankton tows from continental shelf waters
between Martha's Vineyard, Mass., and Palm
Beach, Fla., were provided by Peter Berrien
(Fisheries Biologist, Northeast Fisheries Center
Sandy Hook Laboratory, National Marine
Fisheries Service, NOAA, Highlands, NJ 07732).
Collection methods and station distribution are
given in Clark et al. (1969, 1970).

RESULTS

Bairdiella chrysoura

Morphology. Body proportions change gradually
during larval development (Table 3). Body depth
at the cleithral symphysis increases slightly with
growth and is >30% SL in all specimens
examined. Caudal peduncle depth remains con-
stant through development. Preanus length in-
creases from 40-45% SL in preflexion and flexion
larvae to >50% SL at ^5.7 mm. Positions of the
dorsal, anal, and pelvic fins remain quite constant
as the fins develop, whereas the decrease in length
of the anus-anal fin gap corresponds to the in-
crease in preanus length. Snout length and eye
diameter change little during development,
whereas head length increases from 27-31% NL or
SL in preflexion and flexion larvae to 35% SL in
larvae 4.9 mm.

Lateral and marginal preopercular spines are
present throughout the series, becoming more
numerous with growth until a maximum of five
lateral and four marginal spines are present at
7.0-8.8 mm. A single posttemporal spine is present
at 5.0-7.7 mm, and two such spines are present at
8.8 mm.

Fin development. The pectoral fin is present in
all specimens examined; ray development begins
at 5.7 mm and 16 rays are present by 8.8 mm
(Table 4). Notochord flexion occurs at 4.1-4.4 mm
SL. Development of caudal rays begins at the same
time as notochord flexion. The full complement of
principal rays is developed soon after completion
of notochord flexion. Procurrent caudal rays begin
to form at 5.7 mm and an incomplete procurrent
ray count is present at 8.8 mm. The soft dorsal and
anal fins begin ray development at the start of

122

POWLES: DESCRIPTIONS OF LARVAL SILVER PERCH, BANDED DRUM, AND STAR DRUM

Table 3. — Body proportions (percentage of NL or SL) of larval Bairdiella chrysoura. Specimens between dashed lines undergoing

notochord flexion; lengths are NL above upper dashed line, SL below.

Snout to

Snout

Snout

Anus

Snout

Snout to

Snout to

NLor

Eye

spinous

to soft

to soft

to

to anal

anal fin

pelvic

Body

Caudal

SL

Snout

dia-

Head

Preanus

dorsal

dorsal

dorsal

anal

fin

termina-

fin

depth at

peduncle

(mm)

length

meter

length

length

origin

origin

termination

fin

origin

tion

insertion

cleithrum

depth

3 1
35
36
37
37
38

87
6.8
74
74
63
7.4

100
10.3

9.8
106
10.5

95

30 0

31 0
276
308
273
28.7

425
41 3
404
41 4
400
446

350
31 0
308

31 9

32 1
329

4 1

72

11.7

31.5

468

_

54.1

77,5

15.4

622

74,8

351

8.1

44

106

12.4

372

487

42,5

61 9

83.2

177

664

81 4

372

97

44

89

11 1

30 3

44 6

40 1

57 1

76.7

21.7

663

803

33 9

7 1

48

98

11,4

31 1

45.9

39.3

57,3

78.6

16.3

62.2

73.7

-

336

6.5

49

7.9

103

373

484

38.9

57,1

825

16.7

651

802

357

365

10.3

50

8.6

10.9

352

49.2

39,9

57,8

836

179

67 1

805

359

367

10 1

57

86

11 4

35.7

48.6

386

600

829

17,1

657

800

35.7

37,1

114

57

86

114

35.7

51.4

37 1

58,6

828

114

628

81,4

37.1

37.1

114

70

70

11.6

372

57.0

372

593

825

8,1

65 1

80 2

38 4

37 2

116

75

109

10.9

358

55.4

38 1

59,8

81.5

7.6

63 0

78 3

358

358

10.9

7.5

87

109

369

53.3

39,1

57,6

83.7

11.9

652

79,3

35.8

358

8.7

77

106

10.6

38 3

58.5

43,6

596

829

96

68 1

808

40,4

372

106

88

93

11.2

36.4

56.1

39.3

59,8

85.0

8.4

645

79,5

39,3

36.4

10.3

Table 4. — Fin element counts of larval Bairdiella chrysoura.
Specimens between dashed lines undergoing notochord flexion;
lengths are NL above upper dashed line, SL below.

Caudal

Caudal

NLor

Spinous

Soft

Pec-

prin-

procur-

SL(mm)

dorsal

dorsal

Anal

toral'

Pelvic

cipal

rent

3.1

-

_

_

+

-

-

-

3.5

-

-

-

+

-

-

-

3.6

-

-

-

+

-

-

-

3.7

-

-

-

+

-

-

-

3.7

-

-

-

+

-

-

-

38

-

-

-

+

-

-

-

4.1

_

14

6

+

-

7^6

_

4.4

-

15

8

+

-

7-7

-

4.4

-

18

6

+

-

7^7

-

4.8

_

20

10

+

-

8-7

_

4.9

-

19

1.9

+

-

9*8

-

5.0

-

1.21

1,9

*

-

9-8

-

5.7

XI

21

11,9

+

3

9^8

3,1

5.7

XI

1,21

11.9

6

1,2

9-8

-

7.0

XI

1.21

11,9

11

1,5

9-8

4,3

7.5

XI

1,21

11.9

12

1,5

9-8

5,4

7.5

XI

1,22

11.9

8

1,5

9-8

4,4

7.7

XI

1,21

11,9

12

1,5

9-8

5,4

8.8

XI

1,22

11.9

16

1,5

9-8

6.5

' - = fin present, no developed elements

notochortd flexion and attain adult complements at
>4.8 mm. The spinous dorsal begins development
between 5.0 and 5.7 mm; spine development is
rapid, with the adult complement present at 5.7
mm. Pelvic fins are first present at 5.7 mm and
adult element complements are present at 2^7.0
mm.

Pigmentation. Larvae are characterized by an
oblique swath of internal and external pigment,
paralleling the cleithrum. from nape to cleithral
symphysis (Figure 1). Melanophores of several
areas constitute this swath: in the musculature of

the nape, on the anterior and dorsal surfaces of the
visceral mass, ventral to the brain, and on the
ventral body surface. In small larvae (<5.0 mm),
melanophores in these areas are usually ex-
panded, so that a continuous swath of pigment is
formed. Occasionally melanophores may be con-
tracted, but are always present in the areas listed.
In large larvae (&5.0 mm), melanophores of these
areas are more frequently contracted than in
smaller larvae, and thickening of the body wall
begins to obscure some of the swath pigment.

Pigment of the ventral midline of the tail begins
as a continuous row of small melanophores in the
smallest larvae and develops into a characteristic
sequence of melanophores with growth. About 10
melanophores are present at 3.1-3.8 mm; one of
these (two-thirds of the distance from anus to
notochord tip) is larger than the others. In the
dorsal midline of the tail, a few specimens =£3.5
mm NL have a small melanophore dorsal to the
large melanophore of the ventral midline. At 5^4. 1
mm, melanophores of the ventral row are placed as
follows: one or two anterior to the anal base, one at
the origin of the anal fin, one at its termination,
and three or four posterior to the anal fin. In most
specimens 5=7.0 mm, no pigment is present an-
terior to the anal base, but the rest of the sequence
remains, and small melanophores begin to appear
at the bases of individual rays.

Other head and visceral mass pigmentation
characterizes these larvae. A melanophore is
present at the angle of the lower jaw throughout
the series. Pigment is present at the tip of the

123

FISHERY BULLETIN: VOL. 78, NO. 1

3.5mmNL

4.1mmSL

8.8mmSL

124

Figure l. — Larval Bairdiella chrysoura. Scale equals 1 mm.

POWLES: DESCRIPTIONS OF LARVAL SILVER PERCH, BANDED DRUM, AND STAR DRUM

premaxillary at ^5.7 mm and at the tip of the
lower jaw at ssT.S mm. A melanophore is usually
present on the medial surface of each dentary at
3.1-7.0 mm, while at 5^7.5 mm, one or several
melanophores consistently occur in this position.
Melanophores are present above the anterior part
of the midbrain, and above the eye, at 2^7.0 mm.
Melanophores are present on the surface of the
midbrain at its junction with the hindbrain at
5^5.7 mm, and on the dorsal surface of the fore-
brain at ^7.7 mm. Two melanophores occur in the
midventral line on the ventral surface of the vis-
ceral mass: one midway between the cleithral
symphysis and the anus (between the pelvic fin
bases when these are developed), present at 3=3.3
mm, and another on the anterioventral surface of
the anus, present at 3.1-5.0 mm. A melanophore
midway between these is occasionally present at
3.5-4.7 mm and always present at 224.8 mm. On
the posterior surface of the visceral mass, above
the anus, a melanophore is present at 3=4.9 mm;
this melanophore becomes increasingly branched
and dark at &5.7 mm.

Body surface pigment increases in extent in
late larvae (^7.0 mm). This includes a cluster of
melanophores in the dorsal midline anterior to
the spinous dorsal fin, a group of melanophores
ventral to this cluster, a group on the dorsal sur-
face of the head, and a group on the lateral sur-
face of the visceral mass.

larval S. lanceolatus. Late larvae of this series
have the broadly rounded caudal fin characteristic
of 5. chrysoura (Hildebrand and Schroeder 1928;
Dahlberg 1975) while late larvae of S. lanceolatus
have the lanceolate caudal fin characteristic of the
adult. Finally, larvae of my series are similar in
major characters (the swath of pigment between
head and visceral mass, midventral pigment pos-
terior to the anus) to the larvae described by
Kuntz (1915), which were apparently correctly
identified.

Spawning season and area. Larval B. chrysoura
occurred in six surface and six bottom tows in May
and in five surface and five bottom tows in June
1974 in South Carolina estuaries. None occurred
between January and April or in July. In South
Carolina tidal passes, larvae occurred in two May
samples, one June sample, and one July sample,
and did not occur between February and April. A
single specimen was taken in continental shelf
waters, in a bongo net tow made in 31 m on 8 April
1974 (Figure 2). Thus spawning appears to occur
primarily in coastal and estuarine waters of the
southeastern United States, at least from April
through July. Spawning may occur later in the
year, but no samples after July from coastal and
estuarine waters were examined.

Larimus fasciatus

Identification of the series. This series was iden-
tified as fi. chrysoura by fin ray counts, pigmenta-
tion, caudal fin shape, and similarity to a pub-
lished description. Fin ray counts (dorsal 21-22,
anal 9) of late larvae in the series could have been
attributed to Menticirrhus americanus, M.
saxatilis, or Stellifer lanceolatus as well as B.
chrysoura. A series o^ Menticirrhus larvae (iden-
tified by presence of a single mental barbel at &9.2
mm, tentatively as M. americanus), which I have
examined, is characterized by heavy and exten-
sive body pigment, and the absence of such pig-
ment in larvae of the series described here indi-
cated that it was B. chrysoura rather than M.
americanus. Heavy body pigmentation has been
described for M. americanus (Hildebrand and
Cable 1934) and M. saxatilis (Scotton et al. 1973).
Although species identifications in those descrip-
tions may not be accurate, heavy body pigmenta-
tion is probably characteristic of larvae of the
genus Menticirrhus. Caudal fin shape distin-
guished larvae of the series here described from

Morphology. Body proportions change little dur-
ing development (Table 5). The larvae are deep
bodied (depth at cleithral symphysis >35% SL,
except for a 3.8 mm specimen). Preanus length is
>50% SL in all specimens but one. Positions of the
fins change little during development. Anus to
anal fin distance is variable in length, <6% SL in
most larvae but with a maximum value of 10.2%
SL. Caudal peduncle depth increases with de-
velopment, from <9% SL at «4.2 mm to >9% SL
in most larger specimens.

Preopercular spines are present in all larvae.
Lateral spines are smaller than marginal spines,
and numbers in both series increase with growrth.
One or two small posttemporal spines and a low,
spinous supraorbital ridge are present at ^5.5
mm.

Fin development. The pectoral fins are present
throughout development (Table 6). Pectoral ele-
ments are first present at 3^4.0 mm; elements are
incomplete at 5.9 mm, the largest larva available

125

FISHERY BULLETIN: VOL. 78, NO. 1

Table 5. — Body proportions (percentage of NL or SL) of larval Larimus fasciatus. Specimens between dashed lines are undergoing

notochord flexion. Lengths are NL above upper dashed line, SL below.

NLor

SL
(mm)

Snout
length

Eye
dia-
meter

Head
length

Preanus
length

Snout to

spinous

dorsal

origin

Snout
to soft
dorsal
origin

Snout

to soft

dorsal

termination

Anus

to
anal

fin

Snout
to anal

fin
origin

Snout to
anal fin
termina-
tion

Snout to

pelvic

fin

insertion

Body
depth at
cleithrum

Caudal

peduncle

depth

3.0
3.2

10.4
9.6

10.4
12.0

33.8
36.1

53.2
53.0

-

50.6

68.8

-

-

-

-

50.6
39.8

6.5
7.2

3.6
3.8
4.0

10.9

9.2

10.8

13.0
12.2
12.8

35.9
34.7
38.8

55.4
49.0
56 8

41.3

53.3
52.0

76.1
76.8

4.4

10.2

4.0

59.8
59.2
60.8

71.7
70.4
74.4

39.1
35.6

39.1
33.7
39.6

87
6.1
9.2

4.2

7.3

11.9

36.7

54.1

36.7

50.5

81.7

5,5

59.6

71.6

37.6

37,6

8.3

4.3

10.1

13.8

40.4

57.8

39.4

55.0

81.7

5,5

63.3

74.3

35.8

40.4

92

4.3

8.2

12.7

38.2

57.3

41.8

54.5

85.5

3,6

60.9

71,8

39.1

40.9

82

4.4

9.7

13.3

38.1

58.4

43.4

58.4

89.4

8,9

67,3

75.2

36.3

42.5

10,6

4.5

9.6

13.2

36.8

54,4

40.4

49.1

86.0

96

64,0

76.3

36.0

37.7

88

4.8

8.1

13.8

41.5

65,0

41.5

58.5

87.0

4 1

69,1

78.9

40.7

41 5

10,6

4.9

10.3

14.3

37.3

61.9

40.5

57.1

87.3

0.8

62.7

77,0

39.7

44,4

10,3

5.0

9.4

15.0

40.2

58,3

39.4

55.1

87.4

4,7

63.0

75.6

39.4

46,5

110

5.5

7.5

13.4

35.8

59.7

41,8

56.7

89.6

4,5

64,2

77.6

373

44,8

11,9

5.7

10.3

14.5

37.9

60.0

38.6

57.9

89.0

5,5

65,5

79.3

37.2

44.1

11,0

58

99

127

38.0

60.6

42.3

59.2

87.3

1,6

62.0

74,6

39.4

45.1

11,3

5.9

12.5

13.9

40.3

59.7

44.4

59.7

87.5

5.6

65.3

76.4

37.5

43.1

9.7 •

3rf

2i

jK

(^ Larimus fasciatus
Bairdiella chrysoura

3i

zi

31

30

2tf

28

79"

Table 6. — Fin element counts in larval Larimus fasciatus.
Specimens between dashed lines are undergoing notochord flex-
ion. Lengths are above upper dashed line, SL below.

NLor
SL(mm)

Spinous
dorsal

Soft
dorsal

Anal

Pec-
toral'

Pelvic'

Caudal
prin-
cipal

Caudal

procur-

rent

3.0
32

-

-

-

+
+

-

-

-

3.6
3.8
4.0

-

16
18
19

5

7

+
+
10

-1-
+

6-1-5
3-1-3
9-1-8

-

4.2

-

16

7

-1-

-1-

8-1-6

-

4.3

-

15

6

7

+

4-1-5

-

4.3

-

20

7

6

+

8-1-7

-

4.4

IX

27

11,6

11

1.4

9 + 8

-

4,5

III

22

7

10

+

8+6

-

4,8

X

25

6

10

+

9 + 7

-

4,9

X

27

11,6

12

1,3

9+8

-

5,0

X

26

11,6

10

1,1

9 + 8

-

5.5

X

27

11,6

15

1,5

9 + 8

0,1

5,7

X

27

11,6

14

1,4

9 + 8

0,1

5.8

XI

26

11.6

16

1,5

9 + 8

1,2

5.9

IX

27

11,6

15

1,5

9 + 8

2,2

' + = fin present, no developed elements.

(adult complement 17 in nine adults, 16 in one, all
from South Carolina waters). Caudal flexion is
occurring in specimens of 3.6-4.0 mm. Principal
caudal rays are first seen in flexion specimens and
are usually complete after 4.9 mm. Procurrent
caudal rays appear at 5.5 mm and are incomplete
in the largest specimen available. The soft dorsal
fin base is present in the smallest larva, with no
discernible elements; pterygiophores are count-
able at 3.6 mm and rays are consistently complete
at ^4.8 mm. Dorsal spines first appear at 4.4 mm

FIGURE 2. — Occurrence of larval Bairdiella chrysoura and
Larimus fasciatus in South Carolina-MARMAP plankton tows
in continental shelf waters of the South Atlantic Bight. Num-
bers indicate numbers of Isirvae at stations.

126

POWLES: DESCRIPTIONS OF LARVAL SILVER PERCH, BANDED DRUM, AND STAR DRUM

and are complete in one specimen at 5.8 mm. The
anal fin is first present at 3.6 mm; the complete
anal ray complement is present at ^^4.0 mm and
anal spines are complete consistently at 4.9 mm.
The pelvic fin bud is first present at 3.6 mm, and
the complete element complement consistently
present at 2=5.8 mm.

Pigmentation. Characteristic pigment patterns
of the brain and pectoral fin are useful for iden-
tifying larval L. fasciatus (Figure 3). Melano-
phores are present on the anterior surface of the
forebrain, the anterior and posterior surfaces of
the midbrain, the posterodorsal surface of the
hindbrain, and the ventral surface of the brain
posterior to the eye, throughout the available
series. The midbrain pigment appears to ring the
midbrain when viewed from dorsally. The pec-
toral fin base and membrane are heavily pig-
mented throughout the series. Pigment in the
membrane, diffuse in small larvae, is present be-
tween the rays when these are developed (2=4.3
mm). An expanded melanophore is present on the
visceral mass just ventral to the pectoral fin base
throughout the series; two or more melanophores
may occur here at 2*4.2 mm.

Other head pigment includes two to four
melanophores on the gular isthmus between the
lower jaw rami, melanophores on the preoper-
culum posterior to the eye, a melanophore at the
angle of the lower jaw, and one anterior to the
cleithral symphysis.

In the ventral midline of the visceral mass, early
larvae have three melanophores: one posterior to
the cleithral symphysis (between pelvic fin bases
when present), one midway between cleithral
symphysis and anus, and one on the antero ventral
surface of the anus. At 2=3.6 mm, the anus
melanophore is absent, and at ^4.5 mm, two or
three melanophores may occur at the other two
ventral midline locations. The anterior, dorsal,
and posterior surfaces of the visceral mass are
pigmented throughout the series, and at ^5.0 mm,
melanophores appear and increase in numbers on
the lateral surface of the visceral mass.

In the ventral midline posterior to the anus, a
row of six melanophores is present in the smallest
larva (3.0 mm), the fifth of which, midway between
the anus and notochord tip, is larger than the
others. At ^3.2 mm, two melanophores occur in
the ventral midline, one at the position of the large
melanophore of the original series (at the posterior
end of the anal base when developed) and one

anterior to this (just posterior to the anterior end
of the anal base when developed).

In the dorsal midline, a melanophore is present
anterior to the origin of the finfold or spinous dor-
sal at ^ 3 .8 mm; two or three melanophores may be
present here at ^4.5 mm. Two melanophores, one
on either side of the midline, are present midway
along the spinous dorsal base at >4.8 mm, and a
similar pair of melanophores is present two-thirds
of the distance along the soft dorsal base at >5.9
mm.

On the lateral surface of the body, between the
spinous dorsal base and the visceral mass,
melanophores appear at 4.4 mm and increase in
number with growth.

Identification of the series. This larval series was
identified as L. fasciatus by dorsal and anal fin ray
counts, pigmentation, and by correspondence vdth
a published description of late larval and early
juvenile stages. Fin ray counts (dorsal 26-27, anal
6) observed in late larvae of this series could only
have been of L. fasciatus or M. americanus (Table
1). The absence of heavy, extensive body pigmen-
tation characteristic of Menticirrhus larvae indi-
cated that the series described here was L. fas-
ciatus rather than M. americanus. The pectoral fin
pigment of the series here described is similar to
that of L. fasciatus late larvae and early juveniles
described by Hildebrand and Cable (1934). Al-
though descriptions of early larvae in that paper
are inadequate, late larvae (2=10.5 mm) and
juveniles represent a coherent series apparently
correctly identified.

Spawning season and area. No larval L. fas-
ciatus were present in samples from South
Carolina estuaries or tidal passes throughout the
months sampled, January-July. In MARMAP
tows in shelf waters, larvae were taken in April-
May 1974, August-September 1974, and Sep-
tember 1975; larvae were most frequently taken
on the inner two-thirds of the continental shelf
and occurred from Cape Canaveral to Cape Fear
(Figure 2). Information from plankton collections
made by personnel of Northeast Fisheries Center
Sandy Hook Laboratory (Figure 4) shows larval L.
fasciatus to have been distributed across the width
of the continental shelf and as far south as lat.
27°43' N. Large collections of larvae (6-18 speci-
mens) were common off northern Florida and
southern Georgia. Larval L. fasciatus were taken
in cruises made during May, July, and October off

127

FISHERY BULLETIN: VOL. 78, NO. 1

^C^.

5.8mmSL

Figure 3. — Larval Larimus fasciatus. Scale equals 1 mm.

128

POWLES: DESCRIPTIONS OF LARVAL SILVER PERCH. BANDED DRUM, AND STAR DRUM

80"

34"

33'

32"

31

30

29"

K

77

x:

M

O

M

J /

J M /
CHARLESTON/ ^ ^

IM

M
O

M -

MAY

■NJ

J -

JULY

O -

OCTOBER

J -

1- 5 LARVAE

®-

6-18 LARVAE

CAPE
CANAVERAL

33f

32'

31

30

29

28'

2/

79'

t

Figure 4. — Distribution of captures of larval Larimus fasciatus
during plankton tows conducted by personnel of Northeast
Fisheries Center Sandy Hook Laboratory off the southeastern
United States (data supplied by Peter Berrien, Fishery Biologist,
Northeast Fisheries Center Sandy Hook Laboratory, NMFS,
NOAA, Highlands, NJ 07732).

the southeast United States; larvae were absent
from the cruises made in January-February. On
cruises made north of Cape Lookout, N.C., by
Northeast Fisheries Center Sandy Hook Labora-
tory personnel, larval L. fasciatus were found as
far north as lat. 36°22' N (just south of the mouth
of Chesapeake Bay); larvae were approximately as
widely distributed and as abundant in continental
shelf waters between Cape Lookout and Chesa-
peake Bay as off the southeastern United States

(Berrien'). Larval L. fasciatus were collected in
April to June and August to October on these
"northern section" cruises.

Stellifer lanceolatus

Morphology. Body proportions change little dur-
ing larval development (Table 7). The body is
fairly deep (depth at cleithral symphysis 34-41%
SL in most specimens). Preanus length, 40-50%
SL through most of the series, increases to 55% SL
in most late larvae ( ^ 10.2 mm SL). Fins develop at
the adult positions. The anus-anal fin gap, 12-20%
SL in most specimens <8 mm, decreases with an
increase in preanus length in larvae >10 mm.
Head length increases slightly with development
to the late larval stages; snout length and eye
diameter change little over the size range avail-
able. Depth of the caudal peduncle increases
slightly before and during notochord flexion and
remains constant after flexion is complete.

Small lateral and large marginal preopercular
spines are present throughout the series, as are
premaxillary and dentary teeth. A posttemporal
spine is present at 5.1-7.8 mm; at ^10.2 mm a
"scale bone" with four spinous projections is pres-
ent in the posttemporal region.

Fin development. The pectoral fin, present
throughout the series, first has elements at 6.9
mm and has the complete ray complement consis-
tently at ^14.0 mm, although the complete ray
complement may be present in smaller larvae
(Table 8). Notochord flexion occurs between 3.3
and 4.3 mm. Principal caudal rays are present in
one preflexion larva and are consistently present
during and after flexion; the adult complement is
present at 5=5.5 mm. Procurrent caudal rays first
appear at 5.1 mm and are complete at ^10.2 mm.
Bases of the soft dorsal and anal fins are present,
with no discernible elements, in two preflexion
specimens, and are consistently present with de-
veloped pterygiophores in flexion and postflexion
specimens. Complete anal ray counts occur at
s^3.3 mm, and complete anal spine complements
at &5.5 mm. Dorsal ray complements are consis-
tently complete at 2=5.5 mm although complete
counts may occur at 4.5 mm. Dorsal spines are
occasionally seen at 4.5-5.8 mm and are consis-

^Peter L. Berrien, Fishery Biologist, Northeast Fisheries
Center Sandy Hook Laboratory, National Marine Fisheries Ser-
vice, NOAA, Highlands, NJ 07732, pers. commun. June 1979.

129

FISHERY BULLETIN: VOL. 78, NO. 1

Table 7. — Body proportions (percentage of NL or SL) of larval and juvenile Stellifer lanceolatus . Specimens between dashed lines are
undergoing notochord flexion. Lengths are NL above upper dashed line, SL below.

Snout to

Snout

Snout

Anus

Snout

Snout to

Snout to

NLor

Eye

spinous

to soft

to soft

to

to anal

anal fin

pelvic

Body

Caudal

SL

Snout

dia-

Head

Preanus

dorsal

dorsal

dorsal

anal

tin

termina-

fin

depth at

peduncle

(mm)

length

meter

length

length

origin

origin

termination

fin

origin

tion

insertion

cleithrum

depth

2.8

8.2

11.0

30.1

45.2

-

-

-

-

-

-

-

37.0

6.8

2.9

9.3

10.7

33.3

453

-

506

66.7

13.3

58.6

69.3

-

37.3

6.7

3.1

88

11.4

32.9

41.7

-

48.0

69.6

21.5

63.2

74.6

-

38.0

76

3.1

8.9

11.4

35.4

41.8

-

-

-

-

-

-

-

35.4

76

3.5

6.6

11.0

27.4

39.5

-

-

-

-

-

-

-

34.1

6.6

3.3

5.9

12.9

34.1

47.1

—

61.2

90.5

187

658

84.7

-

41.2

94

3.4

6.9

11.5

36.8

46.0

-

51.7

77.0

13.8

59.8

74.7

-

40.3

8.1

3.8

7.2

9.3

27.8

41.2

-

49.4

70.1

17.6

58.8

73.2

-

35.0

6.2

4.1

7.5

11.3

31.1

45.3

39.6

54.7

86.8

15.1

60.4

79.2

-

39.6

10,4

4.3

8.2

11.8

31.8

45.5

-

53.6

81.8

16.3

61.8

78.2

-

38.2

10.9

4.5

8.7

11.3

34.7

48.7

35.7

57.4

86.1

12.1

60.8

77.3

37.4

40.8

11.3

4.9

8.7

9.5

32.5

42.9

36.5

55.6

83.3

19.0

61.9

80.2

30.2

36.5

8,7

5.1

9.7

12.9

35.5

48.4

35.5

56.4

87.1

12.9

61.3

77.4

35.5

38.7

9,7

5.5

7.5

10.4

32.8

43.3

32.8

49.3

80.6

14.9

58.2

76.1

-

35.8

90

5.5

9.0

10.4

31 3

47.8

34.3

52.2

90.0

11.9

59.7

79.1

-

37.3

9,0

5.8

7.0

14.1

31.0

43.7

35.2

50.7

84.5

15.5

59.2

76.1

32.4

32.4

8.5.

6.2

8.0

8.0

32.0

46.7

34.7

54.7

82.7

12.0

58.7

76.0

32.0

36.0

9.3

6.9

8.3

9.5

34.5

45.2

36.9

54.7

82.1

14.3

59.5

76.2

29.7

33.3

9.5

7.4

10.0

10.0

37.8

54.4

41.1

56.7

84.4

8.9

63.3

77.8

41.1

37.8

10.0

7.6

8.6

8.6

35.4

47.3

37.6

55.9

86.0

11.8

59.1

76.3

31.1

34.4

9-7

7.8

7.4

9.5

32.6

45.3

358

53.6

83.2

12.6

57.9

79,0

30.5

35.8

9,5

10.2

8.8

9.6

38.4

55.2

40.0

59.2

85.6

88

64.0

79.2

38.4

36.0

56

13.1

10.3

9.0

38.5

57.6

38.5

58.9

85.9

6.5

64.1

78.2

39.7

35.8

9,0

13.9

9.6

7.2

39.7

54.2

38.5

59.0

85.5

97

63.9

783

36.1

33.7

9,6

14.0

9.0

9.0

37.3

55.4

36.2

54.1

85.5

8.4

63.8

78.3

385

33.7

9.6

15.1

10.0

8.9

38.9

57.8

36.7

55.5

84.5

7.7

65.5

77.7

38.9

33.3

8.9

tently present at 6.2 mm; the adult complement is
consistently present at S3l0.2 mm. The pelvic fin
bud is first present at 4.9 mm and is consistently
present at ^6.2 mm; adult element complements
are present at ^6.9 mm.

Pigmentation. Pigmentation of the body pos-
terior to the anus is of particular value in iden-
tification of larval S. lanceolatus (Figure 5). In the
ventral midline, small larvae (^=3.1 mm) have a
row of five or six melanophores between the anus
and the notochord tip; one or two of these, two-
thirds of the distance from anus to notochord tip,
are larger than the others. In larger specimens, an
expanded melanophore is present two-thirds of the
distance from anus to notochord tip (at the pos-
terior end of the anal base when developed); this
melanophore branches dorsally , often as far as the
midlateral line. In some specimens (as shown.
Figure 5) two expanded, branching melanophores
are present at the posterior end of the anal fin
base. In most specimens s^3.1 mm, a melanophore
is present (at the anterior end of the anal base
when developed) anterior to this expanded
melanophore. One to three small melanophores
are present posterior to the anal base in most
specimens 3.3-6.2 mm; none are present at 6.9-
10.2 mm, and at >10.2 mm three or four melano-
phores are present here. A small, faint pigment

Table 8. — Fin element counts in larval and juvenile Stellifer
lanceolatus . Specimens between dashed lines are undergoing
notochord flexion. Lengths are NL above upper dashed line, SL
below.

NLor
SL (mm)

Spinous Soft
dorsal dorsal

Anal

Pec-
toral'

Pelvic'

Caudal Caudal
prin- procur-
cipal rent

2.8

-

-

-

+

-

-

-

2.9

-

-

-

+

-

-

-

3.1

-

-

-

+

-

-

-

3.1

-

-

-

+

-

2-1-2

-

3,5

-

-

-

+

-

-

-

3,3

_

15

8

+

_

6-f6

_

3.4

-

19

7

+

-

4-1-5

-

3.8

-

18

8

-1-

-

8-f7

-

4.1

-

17

1.8

-1-

-

8-^7

-

4.3

-

19

8

-t-

-

8-1-6

-

4,5

II

21 1

,8

-1-

-

9+8

-

4.9

-

20

,8

-1-

+

9-f7

-

5.1

V

19 1

,8

+

-

9-1-8

1,1

5.5

-

19

,8

+

-

8-1-7

-

5.5

-

22 1

,9

+

-

9-1-8

1,1

5.8

-

22 1

,8

+

-

9-1-8

-

6.2

VII

22 1

,8

+

+

9-^8

2,2

6.9

XI

1,22 1

,8

7

1,4

9-f8

4,3

7.4

XI

1,23 1

,8

13

1,5

9 + 8

4,4

7.6

XI

1,22 1

.8

7

1,3

9 + 8

5,4

7.8

XI

22 1

,8

13

1,5

9 + 8

6,4

10.2

XI

1,23 1

.8

19

1,5

9 + 8

3,8

13.1

XI

1,22 1

.8

19

1,5

9 + 8

9,8

13.9

XI

1,22 1

,8

15

1,5

9 + 8

9,8

14.0

XI

1.23 1

,8

19

1,5

9+8

9,8

15.1

XI

1,21 1

,8

20

1,5

9 + 8

9,8

fin present, no developed elements.

spot is present in the midlateral line above the
melanophore at the posterior end of the anal base
in some specimens 3.1-5.5 mm, often connected to

130

POWLES: DESCRIPTIONS OF LARVAL SILVER PERCH, BANDED DRUM, AND STAR DRUM

2.9mm NL

4.3mmSL

6.2 mm SL

FIGURE 5. — Larval Stellifer lanceolatus. Scale equals 1 mm.

131

FISHERY BULLETIN: VOL. 78, NO. 1

the dorsal branches of the expanded melanophore.
A melanophore is present in the dorsal midline
dorsal to the melanophore at the anal fin termina-
tion in most specimens 2.9-6.2 mm.

Head and visceral mass pigment is also useful in
identifying larval S. lanceolatus. A large melano-
phore is present on the anterior surface of the
visceral mass, between the cleithra, throughout
development. A similar melanophore appears on
the posterior surface of the visceral mass at ^4.1
mm; this melanophore becomes extensively
branched at >6.9 mm, and additional expanded
melanophores appear dorsal and ventral to this
one at 2^10.2 mm. In the ventral midline of the
visceral mass a melanophore is present midway
from cleithral symphysis to anus at 2.9-6.2 mm
(between pelvic fin bases when present), and a
second melanophore occurs on the anteroventral
surface of the anus at 2.9-5.8 mm. In small larvae
(^3.8 mm), pigment is present in the dorsal mid-
line and internally, on both sides of the notochord,
above the visceral mass. A characteristic pigment
area at the dorsal end of the operculum, which
appears to roof a cavity in this area, is present at
&7.4 mm. Pigment occurs at the angle of the lower
jaw at <6.2 mm and anterior to the cleithral sym-
physis throughout the development.

Further pigment develops in late larvae (>10.2
mm). On the body surface, this includes a scatter-
ing of melanophores between the spinous dorsal
and the visceral mass, four clusters of small
melanophores in the dorsal midline along the dor-
sal fin base, and a few internal melanophores in
the midlateral line above the anal base. Small
melanophores appear in the spinous dorsal mem-
brane and at the tip of the caudal fin at 13.1 mm,
and in the soft dorsal membrane at 15. 1 mm. Even
in late larvae, pigmentation is not particularly
heavy.

Identification of the series. The series was iden-
tified as S. lanceolatus by fin ray counts, pigmen-
tation, caudal fin shape, and similarity to a pub-
lished description of late larvae and juveniles. Fin
ray counts of late larvae in this series (dorsal
21-23, anal 8) could be those of 5. chrysoura, M.
americanus, M. saxatilis, or S. lanceolatus (Table
1). Lack of heavy extensive body pigment indi-
cates that the series is not Menticirrhus . The late
larvae of the series have a lanceolate caudal fin,
characteristic of S. lanceolatus but not of B.
chrysoura (Hildebrand and Schroeder 1928;
Dalhlberg 1975). Late larvae (s=9 mm) and early

juveniles of S. lanceolatus described by Hilde-
brand and Cable (1934) represent a coherent
series leading to a correctly identified young adult;
late larvae of the series described here are similar
to the late larvae of Hildebrand and Cable (1934),
notably in the presence of an area of pigment at
the upper end of the operculum, which appears to
roof a cavity in this area.

Spawning season and area. Larval S. lanceo-
latus occurred in two South Carolina estuary sam-
ples in June and in one in July 1974; all three
samples came from bottom rather than surface
tows. Tidal pass sampling yielded five samples
containing larvae in June and five with larvae in
July; no larvae were taken from February to May.
No S. lanceolatus larvae were taken in continental
shelf tows. Thus, spawning appears to occur in
estuarine and coastal waters, and not in shelf wa-
ters. Spawning occurs in early summer and may
continue later into the year.

DISCUSSION

Comparisons with earlier descriptions

Bairdiella chrysoura

My material is in agreement with the descrip-
tion of Kuntz (1915), except that fin development
occurs at larger sizes in Kuntz's description than
in my material, and some pigment details are dif-
ferent. Kuntz's 5 mm specimen had a flexing noto-
chord, 13 caudal rays, a developing dorsal fin base,
and no anal base; these characters are found in my
larvae of 4.3-4.4 mm. His 7.5 mm specimen is
equivalent to my specimens of about 5.0 mm, hav-
ing about 25 dorsal fin elements, 11 anal elements,
no pelvic fin buds, and the full complement of
caudal rays. Kuntz's larvae of ^7.5 mm had a
melanophore in the dorsal midline above the large
melanophore of the ventral midline, present in
only a few specimens «3.5 mm SL in my series,
and a melanophore anterior to the dorsal fin ori-
gin, present in none of my specimens. These dis-
crepancies may be due to Kuntz's use of fresh
material while I used formaldehyde-preserved
material. Shrinkage of formaldehyde-preserved
larvae could account for the developmental differ-
ences, and melanophores may be contracted dur-
ing preservation or degraded with storage in
formaldehyde. Kuntz probably used total lengths
rather than standard lengths which might par-

132

POWLES: DESCRIPTIONS OF LARVAL SILVER PERCH. BANDED DRUM, AND STAR DRUM

tially account for development rate discrepancies.
Jannke (see footnote 6) illustrated 2.0 mm and
5.0 mm larvae identified as B. chrysoura. The 2.0
mm specimen, smaller than my smallest larva,
does not resemble Kuntz's larvae at similar sizes
nor my earliest specimen in pigmentation. Jann-
ke's 5.0 mm specimen is probably correctly iden-
tified: it has the fin counts and the characteristic
cleithral pigment swath of S. chrysoura but lacks
characteristic pigment of the ventral midline.

Larimus fasciatus

My material agrees fairly well with the only
published description, that of Hildebrand and
Cable (1934). The pigmented pectoral fin, em-
phasized by Hildebrand and Cable (1934), would
appear to confirm identification of all specimens of
their series. The drawings are not in good agree-
ment with the description in their text; for exam-
ple, their drawing of a 4.5 mm specimen shows
none of the pigment described. The pigment of the
brain which I have found characteristic of L. fas-
ciatus larvae was not mentioned by Hildebrand
and Cable; perhaps fading due to preservation was
responsible. The few body proportions given by
Hildebrand and Cable (particularly the position of
the anus at >50% SL) are characteristic of L.
fasciatus.

Stellifer lanceolatus

Hildebrand and Cable's (1934) description of a
series identified as S. lanceolatus was based on a
mixture of that species and L. fasciatus. Early
larvae ( =s3.5 mm SL) had pigmented pectoral fins
and developing pectoral rays characteristic of L.
fasciatus. Later larvae (^4.5 mm SL) lacked pec-
toral fin and brain pigment and showed pectoral
ray development only at >5.6 mm. Body depth and
preanus length values of the early larvae are
closer to those of L. fasciatus than of S. lan-
ceolatus. Characters given by Hildebrand and
Cable (1934) for separating early L. fasciatus and
S. lanceolatus were preopercular spination, mouth
shape, maxillary length, and amount of space
around the brain. However, my observations indi-
cate that none of these characteristics are suitable
for separating these species.

As with L. fasciatus, there are discrepancies
between text and illustrations in the description of
Hildebrand and Cable (1934), particularly in the
early stages. My material agrees fairly well with

that of Hildebrand and Cable (1934) at ^4.5 mm
SL, although I observed a dorsal midline melano-
phore dorsal to the termination of the anal fin in
specimens s=7.0 mm SL, which was not indicated
by those authors.

Spawning Seasons and Areas

Bairdiella chrysoura

Spawning is reported by various authors to
occur in late spring and summer on the east coast
of the United States and the Gulf of Mexico, and
year-round in South Florida. The season appears
to begin later and to be shorter at higher latitudes:
June to August off New Jersey (Welsh and Breder
1923), May to July in Delaware Bay (Thomas
1971) and Chesapeake Bay (Hildebrand and
Schroeder 1928; Joseph et al. 1964), April to Au-
gust at Beaufort, N.C. (Kuntz 1915), April to May
off Georgia (Dahlberg 1972), and April to Sep-
tember off Louisiana (Sabins 1973). Year-round
spawning with peaks in January to February and
April to June is reported in South Florida (Jannke
see footnote 6). Spawning occurs at least April to
July in South Carolina waters, according to data
presented in the present study.

Spawning reportedly occurs primarily in es-
tuarine and coastal waters, and this is indicated
by my data also. Hildebrand and Cable (1930)
reported captures of eggs and early larvae in es-
tuaries and to 19-24 km offshore off Beaufort,
N.C, but the reliability of their identifications is
uncertain. Their descriptions of eggs and early
larvae of 5. chrysoura are insufficiently detailed
to ensure separation from those of other sciaenid
and perciform fishes. Jannke (see footnote 6) and
Sabins (1973) judged from the small size of larvae
caught in tidal passes that spawning must have
occurred nearby in estuarine or coastal waters.
Specimens I examined were mostly taken in South
Carolina estuaries and tidal passes, with only one
specimen coming from continental shelf waters.

Larimus fasciatus

The information I have presented and the lim-
ited literature reports available indicate a long
spawning period, extending at least from May to
October, for L. fasciatus. Although larvae were
more abundant in MARMAP tows made from Au-
gust to September than tows made from April to
May, larvae were abundant in NMFS Sandy Hook

133

FISHERY BULLETIN: VOL. 78, NO. 1

Laboratory plankton tows made in May and in
July. Hildebrand and Cable (1934) took specimens
of length < 5 mm from July to October off Beaufort,
but presence of small juveniles in these months
indicated spawning began in May. Larvae were
taken from April to October in plankton tows be-
tween Chesapeake Bay and Cape Lookout, N.C.
(Berrien et al. 1978).

Spawning apparently occurs in continental
shelf waters. I obtained no larvae from South
Carolina estuaries, but larvae were abundant in
continental shelf plankton tows. Hildebrand and
Cable ( 1934) took larvae from the coast to 22 km
offshore. Larvae were common in plankton tows in
continental shelf waters between Chesapeake Bay
and Cape Lookout (Berrien et al. 1978).

United States, L. fasciatus larvae are easily sepa-
rated from all others by pigmentation, fin de-
velopment sequence, and preanus distance. Fore-
brain pigment and pectoral fin pigment are not
present in early larvae (larvae with dorsal and
anal fin rays undeveloped or incompletely de-
veloped) of other sciaenids of the area, and pig-
ment on the anterior surface of the midbrain ap-
pears earlier than in other sciaenids of the area.
Pectoral fin rays begin development earlier than
in other sciaenids of the area, in fact earlier than
in larvae of most known teleosts. The preanus
distance of >50% SL is greater than in other sci-
aenid larvae of the area.

Bairdiella chrysoura and Stellifer lanceolatus

Stellifer lanceolatus

My data point to spawning at least in June and
July in South Carolina waters; later spawning
may occur but no samples were available from the
second half of the year. Hildebrand and Cable
( 1934) reported presence of small larvae from July
to September, but their small "S. lanceolatus"
were probably L. fasciatus so this report may not
be accurate. Welsh and Breder (1923) reported
spawning in late spring and early summer on the
U.S. east coast, and Dahlberg (1972) reported May
to September spawning off Georgia. Fahay (1975)
reported a 28.2 mm SL specimen taken in October
off Florida.

Spawning in coastal and estuarine waters
rather than continental shelf waters was indi-
cated by my observations. Hildebrand and Cable
(1934) reported small larvae from the coast to 22
km offshore, but again these larvae may have been
misidentified. Larvae have been taken in Georgia
estuaries (Berrien^). Fahay's (1975) single speci-
men was from inshore 7.5 km south of Cape
Canaveral; being relatively large, this specimen
could have originated in another spawning area.

Comparisons With Other Larval Sciaenidae
Larimus fasciatus

Although superficially similar to larvae of sev-
eral other marine sciaenids, of the southeast

These species are treated together because they
are quite similar as larvae, and resemble larvae of
other species, notably Cynoscion regalis (Pearson
1941) and Cynoscion nothus (Stender^). Typical
larvae of B. chrysoura have a well-developed
swath of pigment from nape to cleithral sym-
physis, which is not found in larvae of the other
species; however, melanophores of the swath may
be contracted or faded by preservation. Pigment of
the ventral midline posterior to the anus is the
most reliable character for separation of B.
chrysoura from S. lanceolatus larvae. Both have a
melanophore at the posterior end of the anal fin
base; however, B. chrysoura has a melanophore
anterior to the anal fin base (at 4. 1-7.0 mm SL) and
a melanophore at the anterior end of the anal base,
while S. lanceolatus has no melanophore anterior
to the anal base but has a melanophore just pos-
terior to the anterior end of the anal base (at the
base of the second anal spine when this is
developed).

Larvae of the two Cynoscion species mentioned
can be separated from larval B. chrysoura and S.
lanceolatus by careful attention to pigment of the
midventral line (Stender see footnote 9; pers. ob-
serv.). Identification of small larvae with unde-
veloped anal fin bases may be difficult, since the
characteristic pigment sequences develop (from a
row of small melanophores) at about the same
time as anal-base development. Presence of a
melanophore in the dorsal midline, above the
posterior end of the anal base, in most S. lan-

8Peter L. Berrien, Fishery Biologist, Northeast Fisheries
Center Sandy Hook Laboratory, National Marine Fisheries Ser-
vice, NOAA, Highlands, NJ 07732, pers. commun. May 1975.

134

9Bruce W. Stender, Biologist, South Carolina Wildlife and
Marine Resource Division, P.O. Box 12559, Charleston, SC
29412, pers. commun. February 1978.

POWLES: DESCRIPTIONS OF LARVAL SILVER PERCH, BANDED DRUM, AND STAR DRUM

ceolatus 2.9-6.9 mm SL may also assist in separat-
ing the species; such a melanophore is present in
only a few B. chrysoura at ^3.5 mm SL.

Cynoscion regalis has a single melanophore in
the dorsal midline above the anal fin throughout
development.

ACKNOWLEDGMENTS

I am grateful to Malcolm H. Shealy, Jr., South
Carolina Estuarine Survey Program, Charles
Farmer and Charles Boardman, South Carolina
Crustacean Management Program, and Ronald
Hodson, North Carolina State University, for
permission to use sciaenid specimens from their
collections, and to Peter L. Berrien, Northeast
Fisheries Center Sandy Hook Laboratory, for data
on Larimus fasciatus collections off the south-
eastern United States. Bruce W. Stender has been
a stimulating collaborator on studies of larval sci-
aenids and carefully reviewed the manuscript.
Paul A. Sandifer, Charles A. Barans, and Peter
Berrien also reviewed the manuscript. Hope Mix-
son sorted larvae from samples. Kathleen Meuli
and Lyne Imbeau typed the manuscript. To all
many thanks. This research was supported by the
National Marine Fisheries Service MARMAP
(Marine Resources Monitoring, Assessment and
Prediction) Program under contract number
6-35147.

LITERATURE CITED

ANDERSON, W. W.

1968. Fishes taken during shrimp trawling along the
South Atlantic Coast of the United States, 193 1-35 . U.S.
Fish Wildl. Serv., Spec. Sci. Rep. Fish. 570, 60 p.

Bailey, R. M., J. E. Fitch, E. S. Herald, E. a. Lachner, C. C.

LINDSEY, C. R. ROBINS, AND W. B. SCOTT.

1970. A list of common and scientific names of fishes from
the United States and Canada. 3d ed. Am. Fish. Soc.
Spec. Publ. 6, 149 p.

BERRIEN, P. L., M. p. FAHAY, A. W. KENDALL, JR., AND W. G.

Smith.

1978. Ichthyoplankton from the RV Dolphin survey of con-
tinental shelf waters between Martha's Vineyard, Mas-
sachusetts and Cape Lookout, North Carolina, 1965-
66. U.S. Dep. Commer., NOAA, Sandy Hook Lab. Tech.
Serv. Rep. 15, 152 p.

CHAO, L. N.

1978. A basis for classifying western Atlantic Sciaenidae
(Teleostei: Perciformes). U.S. Dep. Commer., NOAA
Tech. Rep. NMFS Circ 415, 64 p.

CLARK, J., W.G.Smith, A. W.KENDALL, Jr., andM. P. Fahay.

1969. Studies of estuarine dependence of Atlantic coastal
fishes. Data Report I: Northern section. Cape Cod to Cape

Lookout. R.V. Dolphin cruises 1965-66: Zooplankton vol-
umes, mid-water trawl collections, temperatures and
salinities. U.S. Fish Wildl. Serv. Tech. Pap. 28, 132 p.
1970. Studies of estuarine dependence of Atlantic coastal
fishes. Data Report \\: Southern section, New River Inlet,
N.C., to Palm Beach, Fla. R.V. Dolphin cruises 1967-68:
Zooplankton volumes, surface-meter net collections,
temperatures, and salinities. U.S. Bur. Sport Fish.
Wildl. Tech. Pap. 59, 97 p.

Dahlberg, M. D.

1972. An ecological study of Georgia coastal fishes. Fish.

Bull, U.S. 70:323-353.
1975. Guide to coastal fishes of Georgia and nearby states.
Univ. Ga. Press, Athens, 186 p.

Fahay, M. P.

1975. An annoted list of larval and juvenile fishes captured
with surface-towed meter net in the South Atlantic Bight
during four RV Dolphin cruises between May 1967 and
February 1968. U.S. Dep. Commer., NOAA Tech. Rep.
NMFS SSRF-685, 39 p.

GINSBURG, \.

1929. Review of the weakfishes (Cynoscion) of the Atlantic
and Gulf coasts of the United States, with a description of
a new species. Bull. U.S. Bur. Fish. 45:71-85.

Hildebrand, S. F., and L. E. Cable.

1930. Development and life history of fourteen teleosteem
fishes at Beaufort, N.C. Bull. U.S. Bur. Fish. 46:383-488.

1934. Reproduction and development of whitings or
kingfishes, drums, spot, croaker, and weakfishes or sea
trouts, family Sciaenidae, of the Atlantic coast of the
United States. U.S. Bur. Fish, Bull. 48:41-117.
Hildebrand, S. F., and W. C. Schroeder.

1928. Fishes of Chesapeake Bay. Bull. U.S. Bur. Fish. 43
(part 1), 388 p.

HOESE, H. D., AND R. H. Moore.

1977. Fishes of the Gulf of Mexico, Texas, Louisiana, and
adjacent waters. Texas A&M Univ. Press, College Sta-
tion, 327 p.

Johnson, G. D.

1978. Development of fishes of the mid- Atlantic Bight, an
atlas of egg, larval and juvenile stages. Volume IV.
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JORDAN, D. S., AND B. W. EVERMANN.

1896. The fishes of north and middle America: a descrip-
tive catalogue of the species offish-like vertebrates found
in the waters of North America, north of the Isthmus of
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JOSEPH, E. B., W. H. MASSMANN, AND J. J. NORCROSS.

1964. The pelagic eggs and early larval stages of the black
drum from Chesapeake Bay. Copeia 1964:425-434.

Keiser, R. K., Jr.

1976. Species composition, magnitude and utilization of
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KUNTZ, A.

1915. The embryology and larval development of Bair-
diella chrysura and Anchovia mitchilli. Bull. U.S. Bur.
Fish. 33:1-19.
Miller, G. L., and S. C. Jorgenson.

1973. Meristic characters of some marine fishes of the
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1929. Natural history and conservation of redfish and

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FISHERY BULLETIN: VOL 78, NO. 1

other commercial sciaenids on the Texas coast. Bull.
U.S. Bur. Fish. 44:129-214 (Doc. 1046).
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POWLES, H., AND B. W. STENDER.

1978. Taxonomic data on the early life history stages of
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Randall, J. E.

1968. Caribbean reef fishes. T.F.H. Publications Inc.,
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SABINS, D. S.

1973. Diel studies of larval and juvenile fishes of the
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ScoTTON, L. N., R. E. Smith, N. S. Smith, K. S. Price, and D. p.
DE Sylva.

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136

REPRODUCTIVE BIOLOGY OF THE VERMILION SNAPPER,

RHOMBOPLITES AURORUBENS, FROM

NORTH CAROLINA AND SOUTH CAROLINA

Churchill B. Grimes* and Gene R. Huntsman*

ABSTRACT

The vermilion snapper, Rhomboplites aurorubens, a species often associated with Caribbean reefs and
banks, is an important recreational fish of the outer continental shelf of North Carolina amd South
Carolina. Serial spawning occurs from late April through September off the Carolinas at depths
ranging from 31 to 91 m. Most females spawn in the third or fourth year at about 205-275 mm total
length. Larger, older females (age 5-10; up to 530 mm total length) appear to spawn longer each
reproductive season, which may be an optimal strategy for maximizing reproductive biomass (balanc-
ing the physiological costs of somatic and gonadal growth).

Overall sex ratio is unequal in favor of females ( approximately 60% ) , but the ratio is 1 : 1 for small fish
(less than 150 mm total length) and heavily in favor of large females (69-100?J^ for fish greater than 500
mm total length) because they live longer than males. Fecundity of first spawners is estimated at 17-42
thousand eggs, and large females produce 1.5 million eggs.

The vermilion snapper, i?/iom6op/iYesai/rora6ens,
is a small lutjanid which grows to 600 mm total
length (TL) and 2,600 g (illustrated in Bohlke and
Chaplin 1968). It occurs from Cape Hatteras, N.C.,
to Bermuda, southward throughout the Gulf of
Mexico and Caribbean Sea to southeastern Brazil.
The species is abundant, ranking second or third
in weight and numbers in the Carolina headboat^
fishery (which landed between 590 and 730 metric
tons of demersal fishes annually) between 1972
and 1975 (Huntsman 1976).

Vermilion snapper and other reef fishes nor-
mally associated with deep (>70-90 m) Caribbean
reefs and banks occur in two habitats of the outer
continental shelf of the Carolinas (Figure 1). The
most spectacular of the habitats, the shelf break
zone (Struhsaker 1969), occurs at the edge of the
continental shelf (55-180 m) where the gently
sloping bottom plunges abruptly downward as the
continental slope. It is an area of jagged peaks,
precipitous cliffs and rocky ledges associated with
drowned Pleistocene reefs (Maclntyre and Milli-

' Department of Environmental Resources, Cook College and
New Jersey Agricultural Experiment Station, Rutgers Univer-
sity, New Brunswick, NJ 08903.

^Southeast Fisheries Center Beaufort Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 570, Beaufort, NC
28516.

^Headboats are recreational fishing vessels which charge
anglers for a day's fishing on an individual, thus "per head,"
basis.

Manuscript accepted July 1979.

FISHERIES BULLETIN: VOL. 78, NO. 1, 1980.

man 1970). The second habitat (inshore live bot-
tom) occurs at 25-55 m and consists of broken reefs
and rock outcroppings, rocky ledges, and coral
patches dispersed over the continental shelf
shoreward of the shelf break zone.

Knowledge concerning reproduction of the ver-
milion snapper is lacking. Longley and Hilde-
brand (1941) reported gravid specimens about the
Tortugas, Fla., in July and concluded that spawn-
ing takes place in midsummer. Breder (1929)
wTote that vermilion snapper probably spawn in
early spring along the South Atlantic coast of the
United States, and Walker ( 1950) reported spav^oi-
ing off North Carolina in February. Monroe et al.
(1973) collected a ripe female off Jamaica in
November, and Fahay (1975) and Laroche (1977)
recorded larvae off Georgia in July and August.
Erdman (1976) found ripe fish from February
through June in the northeastern Caribbean.

In this paper we describe the seasonality,
spawning frequency, sex ratio, age and size at
maturity, and fecundity of the vermilion snapper
and discuss possible adaptive strategies for its re-
production.

The study area (Cape Hatteras, N.C., to Char-
leston, S.C.) was stratified by depth (i.e., inshore
and offshore, the dividing depth being 55 m), and
specimens were collected throughout. Most fish
were obtained from the recreational fisheries
throughout the Carolinas; however, some speci-
mens were collected by hook and line or trawl from

137

FISHERY BULLETIN: VOL. 78, NO. 1

N.C.

Figure l.— Continental shelf off North
Carolina and South Carolina and important
ba thy metric features that relate to the ver-
milion snapper study.

l)^"^

CAPE LOOKOUT

/

REA 1

Isobath

1

100 km

the RV Onslow Bay and the RV Eastward; most
juveniles were trawled from RV Dolphin.

Temperature was taken by expendable
bathythermograph, and photoperiod was obtained
from the National Ocean Survey tide tables (U.S.
Department of Commerce 1971, 1972, 1973).
Specimens were weighed (nearest gram) and mea-
sured (nearest millimeter). Gonads were removed,
preserved in 10% Formalin"* for at least 1 wk,
washed in tap water for several days, and then
placed in 70% isopropyl alcohol. Frequency dis-
tributions of ovum diameters were plotted by
month to determine seasonality, frequency, and
duration of spawning (Hickling and Rutenberg
1936; Fahay 1954). The diameters of approxi-
mately 100 randomly selected ova from each of two
females per month were measured to the nearest
0.05 mm by dissecting binocular microscope at
25 X . To validate measuring ova from any portion
of an ovary, we determined by analysis of variance
that ova sizes were distributed uniformly (indicat-
ing uniform development) throughout the ovaries
(Table 1).

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

138

Later, the gonads were removed from preserva-
tive and weighed (nearest 0.1 g) after surface
moisture was absorbed by blotting.

A gonosomatic index was used as a measure of
reproductive development (Finkelstein 1969) for
determining spavvTiing seasonality and maturity.
The index was calculated according to the formula
KG =W/TL^ where KG = gonad index, W = pre-
served (blotted dry) gonad weight in grams, TL =
total length in millimeters. We realize that as-
suming the cubic relationship is arbitrary. Quast
(1968) has showm for kelp bass, Paralabrax clath-
ratus, that the percentage of body weight con-
tained in gonads increases with fish length. There-
fore, the true exponent is undoubtedly >3, but
data limitations preclude more accurate
formulation.

Ovaries used for fecundity studies were pre-
served in modified Gilson's fixative (Bagenal and
Braum 1968). The ovarian tunic was removed and
washed free of adhering ova. Additional washings
separated developing ova from undifferentiated
oocytes and follicular material. A small subsam-
ple of ova (about 1,000 or less) was stored wet for
later counting in a gridded Petri dish under a
binocular dissecting scope. Subsamples and origi-

GRIMES and HUNTSMAN: REPRODUCTIVE BIOLOGY OF THE VERMILION SNAPPER

Table l. — Analysis of variance testing the hypothesis that
there is no difference in ovum diameters between anterior, pos-
terior, and center sections of ovaries from three vermilion snap-
per. NS = not significant.

Fish no.

Source of variation

df

MS

F

1

Between sections
Within sections

2
309

1 .0769
2.341

0.46 NS

2

Between sections
Within sections

2
309

0.5417
0.5770

0.97 NS

3

Between sections
Within sections

2
309

29.907
27.3512

1.09 NS

nal ova samples (total sample minus counting
subsample) were drained and dried for 24 h at 40°
C. Subsample and original ova sample dry weights
were determined to 0.001 g on a beam balance, and
the sum of these two weights provided the total
ova sample dry weight. Fecundity was determined
by proportionality where:

fecundity

total ova dry weight

number of ova in subsample
subsample dry weight

Fecundity models were fitted by semilog transfor-
mation (log fecundity = a + 6 x length, weight, or
age) and regressions are the functional regres-
sions of Ricker (1973). The semilog formulation of
fecundity models was used instead of more tradi-
tional log-log models because they fit the data
best.

RESULTS

Seasonality, Frequency, and
Duration of Spawning

Several lines of evidence indicate that spawning
occurs from late spring through early fall. Males
and females with ripe-appearing gonads were col-
lected from late April through September, but few

females were collected with ova loose within the
ovarian tunic. Microscopic examination of pre-
served ovaries showed three types of maturing ova
present during this period (in addition to matur-
ing ova, undifferentiated transparent oocytes
were present and were by far the most numerous):
the smallest developing ova (0.11-0.2 mm in
diameter) were translucent and were the most
numerous developing type; the next largest ova
(0.33-0.43 mm in diameter) were nearly opaque
throughout and less abundant than the preceding;
the largest developing ova (0.46-0.71 mm in
diameter) were typical mature teleost eggs with
opaque cytoplasm occupying one pole of the egg
which also contained transparent to translucent
yolk material and oil globules. We observed these
most mature ova only in ovaries collected from
May to September, although what appeared to be
ripe ovaries were also seen in April; furthermore,
these mature ova occurred in only 7 of 149 ripe-
appearing ovaries examined.

Frequency distributions of maturing ovum
diameters (Table 2) show at least two size modes of
ova present from April to October (three were pre-
sent in one of two June samples), while only one
smaller size mode or undifferentiated oocytes were
present in November, December, and March. No
ova collected in January or February were
examined. These data indicate spawning begins in
late April or May and continues through Sep-
tember or perhaps early October.

Monthly mean gonad index values for 101 sexu-
ally mature females, sampled from May 1972 to
April 1974, also denote late spring to fall spawn-
ing (Figure 2). No fish were collected in January or
February 1973 or 1974; however, adult females
collected in February 1975 had gonad index values
of 0.51 and 0.40 which are consistent with gonad
index trends indicated in Figure 2. Increasing

Table 2. — Developing ovum diameter-frequency distributions (percent) from two female vermilion snapper that were examined

during various months of the study.

0.08 mm

interval

1972

1973

1974

(midpoint)

May

June

July

Aug.

Sept. Oct.

Nov. Mar.

May

June

July

Aug.

Sept.

Oct.

Nov. Dec.

Apr.

0.06

1

0.14

40

45

39

29

35

35

16

17

28

19

80

100

26

0.22

27

13

32

15

8

21

49

22

36

38

12

17

0.30

11

7

7

2

1

10

5

5

11

16

14

0.38

11

10

6

9

12

5

9

17

10

13

6

13

0.46

4

25

2

8

41

28

15

36

9

13

2

27

0.54

4

1

13

3

1

3

6

1

3

0.62

3

5

23

2

0.70

8

4

0.78

2

Total

194

198

172

214

227

179

199

209

200

197

100

100

200

Mean, mm

0.25

0.27

0.27

0.37

0.32 —

— —

0.28

0.29

0.34

0.27

0.27

0.17

0.14 —

0.3

139

FISHERY BULLETIN: VOL. 78. NO. 1

<

at

I?

s
o

Q

o

25 ^
"^ ?
2o

O I

z

\J

I I I I I I I I

\

\

\

\

/

/

/

\.

\

\

/

\

/

/

./

I I I I I I I I I I I

-T— 1 — r I I I I

2 4 0

a

Z

<
z

O 1°

o

5 '0

N = Wl

n=34 .

n=18

I I I I I I I I I I I I I I I I I I I I I I I I
MJJASONOJ fMAMJJASONDJ FMA

MONTHS

Figure 2. — Monthly mean gonad index of female vermilion
snapper collected from May 1972 to April 1974, mean bottom
temperatures at collecting sites, and photoperiod (U.S. Depart-
ment of Commerce 1971, 1972, 1973).

monthly mean gonad index is well correlated with
lengthening photoperiod and increasing bottom
temperature.

The seasonal occurrence of juveniles and the
large size variation within the youngest age-group
provides additional evidence of an extended sum-
mer spawning season. During October and
November 1973, several hundred juveniles rang-
ing from 53 to 227 mm TL were trawled in Long
Bay, N.C. and S.C., and also off Charleston. Aging
of these fish from scales showed the sample to
contain mostly age-groups 0 and 1. Using the
growth rate for the first year of life (Grimes 1978)
for extrapolating backwards, we determined that
the age 0 fish collected in October and November
1973 were spawned throughout the summer
months.

Although actual spawning was never observed,
it probably occurs around rough bottom from 31 to
91 m but may be more concentrated in deeper
areas (55-91 m). Ripe fish were taken over rough
bottom at depths of 31-91 m when bottom temper-
atures were 20.6°-24.8° C. In Raleigh Bay and
northern Onslow Bay, ripe fish were more abun-
dant from 55 to 91 m; however, in the southern
portion of the study area (southern Onslow Bay

and Long Bay) ripe individuals were more equally
distributed with depth.

Reproductive synchrony within schools may be
indicated by hook-and-line sampling. Fish were
usually caught in sudden bursts of fishing activity;
seldom were single individuals encountered.
Gonad indices for fish of similar size caught over a
short time interval (probably from the same
school) were nearly identical, indicating that re-
production within schools may be highly syn-
chronized.

Multiple spawnings each season are indicated
by the relative abundance of ova types (described
earlier) at different times during the spawning
season (Table 2). Maturing ova were present April
through October and spawning apparently takes
place during this period. Early in the spawning
season (May) all three developing ova types were
present in considerable abundance. When ripe ova
were present later in the season (June or July),
fewer smaller developing ova occurred. In August
and September (late in the spawning season) when
ripe ova were present, smaller developing ova
were absent. The total of the developing ova types
may represent all that will be spawned that sea-
son, and at each spawning a female develops only
as many ova as her abdominal capacity will allow.
This process could be repeated a number of times
during the season until all eggs are spawned.

Variation in gonad index during the spawning
period for similar size fish may also indicate frac-
tional spawning. This was evident during the
spawning months of 1972 and 1973 when the
gonad index of both males and females of similar
size varied by as much as a factor of 12 (Figure 3).
The small size of ripe gonads combined with high
fecundity (see subsequent discussion) is additional
evidence for fractional spawning. The mean per-
cent of body weight (observed) for ovaries of ma-
ture females collected during spawning months
was 2.4% (0.6-5.8%, n = 40). Mature males had
testes averaging 1.1% of body weight (0.4-2.4%, n
= 15) during the same months. Also, we fre-
quently observed semiflacid ovaries with no loose
ova (perhaps partially spawned) in large adult
females from June through September.

Maturation

Age and growth data of Grimes (1978) and our
reproductive data indicate that most fish attain
sexual maturity during their third or fourth years
of life (186-256 and 256-324 mm TL), but a few

140

GRIMES and HUNTSMAN: REPRODUCTIVE BIOLOGY OF THE VERMILION SNAPPER

o
z

, Males
I Females

8
6-

4
2

O 4
« 2

May

1972

" ii

. '\ •°.

June

t

10.3

July

° 3 O O I °

. August

September

300 400 500 600 300

TOTAL LENGTH (mm)

April

0

1973

•

a

0 m

May

•
•

•

•

. ° • . 1

_ June

•

0 •

•

•

•
•

. July

1

0

•
o

- August

D

a D

• o

•

1 1 1

_ September

a

. 0 , °

3
0

• •

400

500

600

Figure 3. — Individual gonad index (gonad weight/( total length)^) values for vermilion snapper over the spawTiing months of 1972 and

1973 plotted against total length.

precocious individuals may mature in their second
year (100-186 mm TL) at about 150 mm TL. We
determined age and size at maturity by examining
a plot of monthly mean gonad index of females
collected in the spawning season (June-
September) by total length (Figure 4). Further-
more, spawning season (April-September) gonad
index values for males and females (Figure 3) and
monthly mean gonad index for each age-group of
fish (Figure 5) show that fish age 4-9 0324 mm
TL) ripen earlier (April or May vs. June) and re-
mained in reproductive condition longer (April to
September vs. June to August) than younger
spawning fish.

Sex Ratio

Sex ratio varies significantly from 1:1. From
1972 to 1974 we sexed 874 fish; 546 (62.5%) were
females and 328 (37.5%) were males (1 df; x^ =
54.4; P<0. 001). The total sample was analyzed by

YEARS OF LIFE

-4—1 5 1-

-7*8 — 1-9-|-10-|

6

-

A

5

.

/

\

/

\y

z

S 3

Z

o
o

2

1

/

n

J

-109

138 163 186 213 238 263 288 313 338 363 388 413 438 463 488 513 538 563 588
25mm TOTAL LENGTH INTERVAL

Figure 4.— Mean gonad index plotted by 25 mm TL intervals for
female vermilion snapper during the spawning season (June-
August). Approximate size at age was determined from Grimes
(1978).

year of collection and sex ratios were judged sig-
nificantly different from 1:1 in all years (Table 3).
Higher proportions of females (62.5%) were col-

141

FISHERY BULLETIN; VOL. 78, NO. 1

AGE GROUP 7

I I I I I I I I I

AGE GROUP 8

I I I I I I I I I I

•— "■ AGE GROUP 9

I I I I

I I I

AGE GROUP 10

MAR'aPr'mAy'jUn' JUL'aUg' SEP 'oCt'nOv'dEc' mar' APR 'MAY' JUN' JUL 'AUG' SEP 'OCT-NOVDEC

MONTHS
n = 220

Figure 5. — Monthly mean gonad index (gonad weight/(total length)^') for female vermilion snapper by age-group.

Table 3. — Test of the hypothesis that sex ratios of vermilion
snapper did not vary significantly from 1:1 within years of collec-
tion.

Item

1972

1973

1974

Percentage of females 71.9 59.4 62.5

Sample size 135 424 315

Chi-square value 25.8' 15.1* 20.8*

•P 0 01.

lected at shelf break habitats than inshore Hve
bottom (60.5%), but the hypothesis that sex ratio
and capture depth were independent was not re-
jected (x2P>0.05, n = 852).

There is a significant difference in sex ratio
throughout the Hfe of the fish (as estimated by
total length); however, differences within some
size intervals were not judged significant (Table
4). Contingency-table analysis showed that sex
ratio and size were dependent (x^P>0.05, df = 9)
(i.e., with growth sex ratios were different from 1:1
and changed significantly). In small fish (101-150
mm TL) the number of males and females was
nearly equal, but at 151-200 mm TL the percent-

142

Table 4. — Tests of the hypothesis that sex ratio of vermilion
snapper did not vary significantly from 1:1 within 50 mm TL
intervals.

Total
length
(mm)

Females Chi-
(%) square

Total
length
(mm)

Females Chi-
(%) square

101-150

105

49.5

00096

401-450

102

638

7.19-

151-200

117

63.4

883-

451-500

60

61 7

3.27

201-250

68

49.3

0014

501-550

58

69.2

7.69-

251-300

99

61 2

4.94-

551-600

32

893

17.28-

301-350

90

59.4

3.38

601-650

1

100

351-400

142

65.9

12.7-

•P<0.05.

age of females increased to about 60% , where it
remained somewhat stable until 501-550 mm TL,
when percentage of females began to steadily in-
crease (Table 4). Only one fish >600 mm TL was
collected (618 mm) and it was a female.

Fecundity

Estimates of fecundity ranged from 8,168 to
1,789,998 ova for 41 females ranging from 229 to
557 mm TL (3-8 yr old and 136-2,293 g). Because

GRIMES and HUNTSMAN: REPRODUCTIVE BIOLOGY OF THE VERMILION SNAPPER

females may spawn several times per season,
fecundity estimates were from ovaries collected
early in the spawning season (May and June) and
all classes of maturing ova were counted.

In Table 5, fecundity was separately regressed
on total length (millimeters), weight (grams), and
age (years) and, as expected, fecundity increases
as a function of all three correlates. Fecundity
increases so markedly in larger (older) fish (Figure
6) that semilog models were needed to adequately
describe the relationship between fecundity and
length, weight, and age. Length and weight are
approximately equally good predictors of fecun-
dity (r = 0.864 and 0.863, respectively). First
spawners probably are about 205-275 mm TL and
produce between 16,800 and 41,700 eggs. This es-
timate assumes that spawning extends from late
June through September for young fish (age 2-4),
that first spawning occurs in the third or fourth
year (186-256 or 256-324 mm TL), that scale an-
nuli form in March (Grimes 1978), and that ap-
proximately 25% of annual growth occurs from
annulus formation to late June.

Table 5. — Functional equations for fecundity in vermilion
snapper. Age (A ) determined from scales.

Predictof

Equation

Total length (nnm)
Age (yr)
Weight (g)

F = exp(7.07 + 0.01 ari)

F = exp (7 57 * 0 87aA)
F = exp (10 21 + 0.002VV)

0863

41

0853

41

0.864

41

DISCUSSION

Spawning Seasonality

The conclusion that spawning occurs from late
April through September is corroborated by
Longley and Hildebrand's (1941) statement that
spawning took place in summer around the Tor-
tugas. Powles^ and Fahay (1975) reported that
larvae were collected at the surface off South
Carolina and Georgia in June and July, and
Laroche (1977) described a larval series collected
off Georgia in August. Walker (1950), however,
reports collecting vermilion snapper in spawning
condition off North Carolina in February. Erdman
(1976) sampled 400 vermilion snapper in the
northeastern Caribbean and found fish in spawn-
ing condition January through June. Monroe et al.
(1973) collected a ripe female in November off

^H. Powles, Fishery Biologist, South Carolina Marine Re-
source Center, Charleston, S.C., pers. commun. May 1975.

20

Fecundity - e

15

o

X

o

z

<
>

o

o

z

10

7.065 + .013 TL

n=41
r = .863

• •

_L

J_

0 200 300 400 500 600

TOTAL LENGTH (mm)

Figure 6. — The relationship of fecundity to total length of
female vermilion snapper.

Jamaica and suggested, on the basis of these and
more extensive data for other reef species, that
spawning probably occurs year-round in the
Caribbean, but that peak spawning is in winter
where surface temperature is about 26.5° C. The
larvae reported on by Fahay (1975) and Laroche
(1977) were collected at 27° and 26.5° C, respec-
tively, and we collected ripe fish off North
Carolina when sea surface temperature was be-
tween 26° and 27° C.

It appears that spawning of vermilion snapper
off North Carolina and South Carolina is re-
stricted to warm months (late April or May-
September), yet spawning may occur almost
year-round in the Caribbean (Monroe et al. 1973;
Erdman 1976). Similar life history variations in
response to local environmental conditions are re-
ported by Leggett and Carscadden (1978) for
American shad.

143

FISHERY BULLETIN: VOL. 78. NO. 1

Several authors report fractional spawning in
marine fishes (Starck and Schroeder 1971;
Beaumarriage 1973; de Silva 1973; Macer 1974).
Our inference that variation in gonad index dur-
ing a spawTiing month for similar size fish
suggests fractional spawning is supported by
Starck and Schroeder's (1971) findings on a re-
lated species, Lutjanus griseus, the gray snapper.
They concluded, from variation of ovary lengths
and weights from fish of similar size, that spawn-
ing probably occurs more than once in the same
season in south Florida waters.

In the results, we described three types of
maturing ova and concluded that they indicate
fractional spawning, yet the most mature ova type
was found only in a few ripe-appearing females.
Evidently final ova maturation occurs nearly
simultaneously with spawTiing so that the proba-
bility of catching a completely ripe fish is low.

Maturation

There are no published reports on maturation in
vermilion snapper, but Starck and Schroeder's
(1971) results on gray snapper agree closely. They
wrote that females are mature at age 3 and 190-
200 mm SL. Results for vermilion snapper also
agree with Starck and Schroeder's findings thatL.
griseus females >375-400 mm SL probably spawn
more times each year than smaller ones, and Mos-
ley (1966) observed (from a sample offish 223-456
mm SL) that early in the spawning season, small-
er red snapper, L. campechanus, showed less
gonad development than larger ones, perhaps in-
dicating earlier spawning by larger fish. Also
similar to our results, Quast ( 1968) showed earlier
and longer seasonal gonad maturation with
growth in kelp bass.

Earlier spawning by older fish can probably be
explained via the interplay between somatic and
gonad growth and maintenance. Sexual maturity
marks diminished growth in many fishes (Hubbs
1926; Magnuson and Smith 1963; lies 1974).
Female vermilion snapper older than 5 yr (390
mm TL) are beyond the years of most rapid somat-
ic grov^fth (Grimes 1978) and undoubtedly can af-
ford to put more energy into gonad development,
even though the energy costs of maintenance are
greater for ^arger fish as well.

Cohen (1&76), using a theoretical mathematical
model, predicts that if reproductive success de-
pends upon maximizing reproductive biomass, the
change in the fraction of reproductive growth (di-

144

minished somatic growth and beginning repro-
ductive growth) will occur at a time and mass just
prior to maximum growth rate. We used annual
length increments and a length-weight relation
(Grimes 1978) to derive annual increments in
mass, so that we could evaluate how well vermil-
ion snapper fit the optimal timing of reproduction
model. The greatest annual growth increment
(weight) occurs between age 6 and 7. Age 5, then,
is the year of life the model predicts the growth
change, and Figure 5 shows that fish age 5 and
older reflect the growth change by maturing ear-
lier and being mature for a longer time each re-
productive season.

Sex Ratio

The literature on other lutjanids provides little
help in interpreting our findings that sex ratios of
vermilion snapper vary significantly from 1:1
overall, and throughout life (as measured by
length). Camber's (1955) data on red snapper
showed a greater proportion of males when small
(200-400 mm TL) but a higher percentage of
females among larger fish (400 mm TL). Mosley
(1966) reported 56% males and 44% females
among red snapper (200-400 mm TL). Bradley and
Bryan (1974), however, reported a 1:1 ratio for
1,129 adult red snapper (no size range reported),
and Starck and Schroeder (1971) gave a 1:1 ratio
for 772 gray snapper (including small juveniles to
adults).

Wenner (1972) suggested several possibilities to
account for unequal sex ratios (i.e., differential
mortality, growth, and longevity; sex reversal; sex
difference in activity; and in or out migiration
from sampling area by one sex). There is no evi-
dence to support any of these explanations in ver-
milion snapper, except differential mortality and
longevity. Our results show conclusively that rel-
ative numbers of females begin to increase (to
about 60%) at about 250-300 mm TL, further in-
crease to about 70% at 500-550 mm TL, and even-
tually reach 90% above 550 mm TL (Table 2).
These results indicate that males experience great-
er mortalities above 250-300 mm TL, and Grimes
(1978) demonstrated greater longevity for females
(no male was older than 8 yr, but females reach at
least age 10). It is interesting to note that differen-
tial mortality commences approximately coinci-
den tally with the onset of sexual maturity.

Our fecundity estimates agree reasonably well
with published results for other lutjanids. Starck

GRIMES and HUNTSMAN: REPRODUCTIVE BIOLOGY OF THE VERMILION SNAPPER

and Schroeder ( 1971) estimated fecundity for gray
snapper and found a 354 mm SL female to contain
about 550,000 ova. Using length conversion equa-
tions for vermilion snapper (Grimes 1978), the 354
mm SL is approximately equivalent to a 450 mm
TL vermilion snapper which would contain about
410,000 ova.

ACKNOWLEDGMENTS

We wish to thank the staff members of the
National Marine Fisheries Service (NMFS),
Beaufort, N.C., and Jeflfery Ross, Virginia Insti-
tute of Marine Sciences, for their assistance in
collecting fish and taking of data from specimens.
C. A. Barans, South Carolina Marine Resources
Center, provided juvenile specimens. D. W.
Ahrenholz, D. R. Colby, C. S. Manooch, NMFS,
and W. E. Fahy, University of North Carolina,
Institute of Marine Sciences, contributed much
through helpful discussions and advice.

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1973. Age, growth, and reproduction of king mackerel,
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Bohlke, J. E., AND C. C. G. Chaplin.

1968. Fishes of the Bahamas and adjacent tropical
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1975. Life history and fishery of the red snapper (Lutjanus
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BREDER, CM., Jr.

1929. Field book of marine fishes of the Atlantic coast from
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1955. A survey of the red snapper fishery of the Gulf of
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Cohen, D.

1976. The optimal timing of reproduction. Am. Nat.
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DE SILVA, S. S.

1973. Aspects of the reproductive biology of the sprat,
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ERDMAN, D. S.

1976. Spawning patterns of fishes from the northeastern
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1975. An annotated list of larval and juvenile fishes cap-

tured with surface- towed meter net in the South Atlantic
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and February 1968. U.S. Dep. Commer., NOAA Tech.
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Fahy, W. E.

1954. The life history of the northern greenside darter,
Etheostoma belennioides blennioides Rafmesque. J.
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FINKELSTEIN, S. L.

1969. Age at maturity of scup from New York
waters. N.Y. Fish Game J. 16:224-237.

Grimes, C. B.

1978. Age, growth, and length-weight relationship of
vermilion snapper, Rhomboplites aurorubens, from North
Carolina and South Carolina waters. Trans. Am. Fish.
Soc. 107:454-456.
HICKLING, C. F., AND E. RUTENBERG.

1936. The ovary as an indicator of the spawning period in
fishes. J. Mar. Biol. Assoc. U.K. 21:311-316.
HUBBS, C. L.

1926. The structural consequences of modifications of the
developmental rate in fishes, considered in reference to
certain problems in evolution. Am. Nat. 60:57-81.
Huntsman, G. R.

1976. Offshore headboat fishing in North Carolina and
South Carolina. Mar. Fish. Rev. 38(3):13-23.

ILES, T. D.

1974. The tactics and strategy of growth in fishes. InF.

R. Harden Jones (editor). Sea fisheries research, p. 331-

345. Wiley, N.Y.
Laroche, W. a.

1977. Description of larval and early juvenile vermilion
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75:547-554.

LEGGETT, W. C, AND J. E. CARSCADDEN.

1978. Latitudinal variation in reproductive characteris-
tics of American shad [Alosa sapidissima): evidence for
population specific life history strategies in fish. J. Fish.
Res. Board Can. 35:1469-1478.

Longley, W. H., and S. F. HILDEBRAND.

1941. Systematic catalogue of the fishes of Tortugas, Fla.,
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Macer, C. T.

1974. The reproductive biology of the horse mackerel,
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MACINTYRE, J. G., AND J. D. MILLIMAN.

1970. Physiographic features on the outer shelf and upper
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States. Geol. Soc. Am. Bull. 81:2577-2598.

Magnuson, J. J., AND L. L. Smith, Jr.

1963. Some phases of the life history of the trout-
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1966. Biology of the red snapp)er, Lutjanus aya Bloch, of
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Munro, J. L., V. C, Gaut, R. Thompson, and p. H. reeson.
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1968. Observations on the food and biology of the kelp
hass, Paralabrax dathratus with notes on its sportfishery

145

at San Diego, California. Calif. Fish Game, Fish Bull.
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RICKER, W. E.

1973. Linear regressions in fishery research. J. Fish.
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1969. Demersal fish resources: composition, distribution,
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1971. Tide tables, high and low water predictions, 1972:
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FISHERY BULLETIN: VOL. 78, NO. 1

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1950. Spawning records of fishes seldom reported from
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146

OBSERVATIONS ON EARLY LIFE STAGES OF ATLANTIC TOMCOD,

MICROGADUS TOMCOD

R. H. Peterson,^ P. H. Johansen,^ and J. L. Metcalfe'

ABSTRACT

In southern New Brunswick, tomcod spawn in streams from late December to mid-January. The
benthic eggs hatch and newly hatched larvae drift to sea in mid-March to mid-April at which time
ocean temperatures are beginning to increase. Larval migration to sea is probably aided by active
swimming of larvae to the surface to fill the swim bladder, which must be filled within 24 hours of
hatching. Photopositivity of the larvae may assist in guiding larvae to the surface.

Water content and specific gravity of eggs reared in 0%o were 2.8 mg and 1.030. Eggs reared at
10-30%o had about 2.3 mg water per egg. Specific gravity of eggs incubated in 10%o was constant for 27
days (at 2°-4° C) at 1.038, then decreased to 1.033. This decrease is associated with water uptake of
0.5-0.6 mg per egg and elimination of salt. The specific gravity of eggs incubated in 20%« declined
linearly from 1.044 to 1.037, associated with accumulation of 0.2 mg of water and elimination of a
greater salt load. The specific gravity of eggs incubated at 30%o declined linearly from 1.049 to 1.045,
associated with 0.1 mg water uptake and apparently insufficient salt elimination. Water uptake and
salt excretion problems are minimized for eggs reared in freshwater, and under the experimental
conditions described here. Normal development could not occur in continued exposure to 30%o. In
natural spawning areas, the incubation medium is freshwater for most of the total cycle, with seawater
invading the area only at extreme high tide. The salinity tolerance of tomcod eggs is compared with
that of freshwater and marine fish eggs in general.

Calculation of specific gravity of egg solids may prove a useful indirect way to investigate salt
regulation in fish eggs.

The Atlantic tomcod, Microgadus tomcod (Wal-
baum), is an anadromous species of coastal
streams from Newfoundland to Virginia. Adults
ascend the lower reaches of southern New
Brunswick streams in December and January.
These spawning migrations form the basis for a
recreational ice fishery in some larger rivers. An
annual commercial catch of about 200 t is said to
be taken from inshore waters of the northwest
Atlantic (Scott and Grossman 1973). Local dip net
fishermen take numbers of spawners for both
human and animal consumption.

Details of the life history of the early stages
(e.g., time of hatching, time of descent into saltwa-
ter) have been little studied. Leim (1924) observed
that eggs would hatch in freshwater or saline wa-
ter, but larvae would survive only in saline water.
Booth ( 1967) found sperm motility to be maximal
in low salinities, and that salinities of 0-15%o per-
mitted the highest percentages of eggs to develop

'Fisheries and Environmental Sciences, Fisheries and Oceans
Canada, Biological Station, St. Andrews, NB, E0G2X0, Canada.

^Fisheries and Environmental Sciences, Fisheries and Oceans
Canada, Biological Station, St. Andrews, New Brunswick; pre-
sent address: Department of Biology, Queen's University,
Kingston, ON K7L 3N6, Canada.

Manuscript accepted September 1979.
FISHERY BULLETIN: VOL. 78, NO. 1, 1980.

to the blastula stage. Howe (1971) described the
food habits and growth rates of young tomcod in
the Weweantic River estuary, Mass.

The early stages of tomcod development have
not been studied extensively; therefore, field
studies were performed to obtain information on
spawning habitat, rates of egg development, and
timing of larval descent to saltwater. Tomcod eggs
are deposited in areas subject to variable
salinities, so the embryonic development and
water balance of tomcod eggs reared in several
salinities were also investigated to see how the
responses of this species compare with those of
freshwater and marine species.

METHODS

Field Studies

The mouth and estuary of Frost Fish Creek
(frost fish is a local name for tomcod) were chosen
as a study area because the stream hosts a large
and regular spawning migration of tomcod which
is undisturbed except for some local dip net
fishing. It is a small stream (2-4 m wide) forming a
common estuary with the Digdeguash River in

147

FISHERY BULLETIN: VOL. 78, NO. 1

southwestern New Brunswick, with a midsummer
discharge ca. 80 1/s and a drainage area of 570 ha
(Symons and Martin 1978; Symons and Harding^).
The drainage basin is typical spruce-fir boreal
forest with no human habitation. Portions of it
farther upstream have been recently logged.

Tomcod spawn in a 10 to 1 5 m stretch at the head
of tide in Frost Fish Creek (Figure 1). This area is
freshwater for most of the tidal cycle, but has a
variable bottom salinity (depending upon the
height of the particular tide) during high tide.
Extreme neap tides do not invade the spawning
area. The stream substrate in the spawning area
varies from ledge to boulders and cobbles. Most of
the eggs settle in substrate interstices.

^Symons, P. E. K., and G. D. Harding. 1974. Biomass
changes of stream fishes after forest spraying with the insec-
ticide fenitrothion. Fish. Res. Board Can. Tech. Rep. 432, 47
p. Fisheries and Environmental Sciences, Fisheries and
Oceans Canada, Biological Station, St. Andrews, NB EOG 2X0.

0 7oo -*

I .0%o
13.5 7oo
23.5 7oo

25.0 %o;r^

26.5 7oo-^

\\S\\\\ v\ \

Edge of
Trees

=p^epth ■■ 12 cm

Marsh ;^v'v

Spawning
Area

;^ Depth = 60 cm

3 Metres

Rood
Culvert

Depth Gauge
1977-78

Drift Sampler

977-78

1976-77

rSolt^:
Marsh^

.\\\S\V\S

Figure l. — Diagram of tomcod spawning area in Frost Fish
Creek in the Digdeguash River estuary. New Brunswick. Depths
and salinities are for a "typical" high-tide situation. Salinities
were measured at the stream bottom. Hatched area indicates
spawning area.

148

Drift samples were installed downstream of the
area of egg deposition (Figure 1) near cessation of
spawning (26 Dec. to 2 Jan.) to sample egg and
larval drift. The samplers consisted of a
galvanized-metal funnel, the narrow opening (5 x
20 cm) facing upstream, with a cloth bag attached
to the downstream end (10x20 cm). The eggs and
larvae accumulated in a 250 ml plastic beaker,
with a screened, 2.5 cm diameter hole in one side,
clamped to the bag. The sampler was threaded
onto an iron rod driven into the stream bottom. A
meter stick was installed to measure stream water
levels, and stream salinities were measured with a
salinity meter. Stream temperatures and drift
samples were taken twice weekly at low tide, with
the numbers of eggs collected averaged on a per-
day basis. Eggs and larvae sampled were pre-
served in 10% Formalin^ or 70% ethanol, those
preserved in Formalin being cleared later (Galat
1972) to determine degree of development.

One sample of eggs was taken from the area of
egg deposition with a Surber sampler in January
1977 to see if development of drifting eggs was the
same as those that were not.

Egg Collection

Adults (1 female:2 males) anaesthetized in
MS-222 were stripped of eggs and milt in the field.
Immediately, the eggs were fertilized by the "dry"
method and were washed with stream water 30 s
after mixing (temperature at fertilization near 0°
C). This water was fresh and was taken from a part
of the stream where tomcod were spawning at the
time (although spawning may continue into high
tide conditions when the water would be of vari-
able salinity). After 1 min the water was changed,
and the bottle of eggs was packed in ice and trans-
ported to the laboratory. The eggs were trans-
ferred to the various incubation salinities 30 min
after fertilization. The eggs are weakly adhesive
initially, but this adhesiveness disappears if the
eggs are separated.

Laboratory Studies

Eggs were incubated in columns of PVC pipe
and fittings holding 190 ml of water (Figure 2).
Screened floors and lids retained eggs and larvae.
Water flowed through the columns at 100 ml/min

"Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

PETERSON ET AL.; EARLY UFE STAGES OF ATLANTIC TOMCOD

Water Level
in Tank

Water Level
in Compartment

I I

5 cm

Figure 2. — Diagram of incubation chambers used to rear tom-

cod eggs.

.9!^

4-

2-

. - 30 7oo
o- 10 %o
• - Fresh Water

30 %.

■^«efi

FW.

10

20

?.*Ssf°o "o*^?*"-

.^.^?i ■■•^;^«»*'"°o

_L

10 20 30 40 50

Time ( Days after fertilizotion )

60

(range, 91-111). The columns were immersed in a
freshwater bath cooled (2°-4° C) by recirculation of
water to refrigerated header tanks. Water flowing
to the columns passed through titanium coils in
the bath. Water temperature decreased from 4.5°
C at the beginning of January to 2.0° C in mid-
February (40-d postfertilization), then increased
to 2.5° C by the end of February (Figure 3). Eggs
were incubated in salinities of 0 (2 columns),
10.1 ±0.3 (1 column), 20.2 ±0.6 (1 column), and
30%o (2 columns). About 250-300 eggs were incu-
bated in each column. Temperature and salinities,
by conversion of specific gravity of water with
Knudsen's (1962) hydrographical tables, were
measured daily.

Columns were checked for egg and larval mor-
talities every 2-3 d. Every third day, three eggs
were removed from each salinity and preserved in
10% Formalin for subsequent study of degree of
development. About 100 newly hatched larvae
were measured ( ±0.1 mm) from each salinity and
the percentage of deformed larvae noted.

Water content of 10 eggs (combined) from each
salinity was measured every fifth day by measur-
ing loss of weight after drying for 16 h at 40° C
under vacuum. Specific gravities (sp. gr.) of eggs
were measured by glycerol flotation at 10° C as
described by Peterson and Metcalfe (1977).
Specific gravity of egg solids was calculated from

Figure 3. — Developmental stages and incubation temperatures
for laboratory experiments on tomcod development. Upper
panel: Appearance of developmental stages of tomcod eggs incu-
bated in freshwater. Lower panel: Incubation temperatures for
tomcod eggs at various incubation salinities. Arrows indicate
median hatching dates at each salinity.

total sp. gr. and water content where solid sp. gr. =
egg dry vvrt/(egg vol. - vol. HgO), egg vol. = wet
wt/sp. gr., and vol. H^O = water content/sp. gr. of
HgO. Egg diameters were measured microscopi-
cally to the nearest 10 ^tm. Buoyancies of newly
hatched larvae, due to air content of the swim
bladder, were measured by a Cartesian diver
technique (Saunders 1965).

Photic responses of larvae were observed by
placing groups of five larvae in a Petri dish, half of
which was painted black, on a finger bowl full of
ice. Uniform overhead illumination was used.

Statistical Procedures

Differences in water content and dry weights
among eggs incubated in the various salinities
were tested by one way ANOVA with individual
differences detected by means of Duncan's Multi-
ple Range Test. Changes in water content and dry
weights during larval development were analyzed
by linear regression methods.

149

FISHERY BULLETIN: VOL. 78, NO. 1

RESULTS AND DISCUSSION

Developmental Stages

To assess development of eggs under natural
conditions, a series of embryological stages was
constructed (Table 1; Figure 3, lower) based on
systematically sampled, laboratory-reared eggs.
We attempted to make them consistent with those
published previously for other species (e.g., Bon-
net 1939 for Atlantic cod), although comparisons
were difficult in more advanced embryos. For
example, Atlantic cod lack a well-differentiated
lower jaw at hatching, but it is well developed in
tomcod. The stages are also referred to comparable
figures in Hardy (1978:278-289) where possible
(Table 1). Sampling eggs more frequently would
have been useful in some instances; e.g., many
anatomical features appeared between days 10
and 13, and are grouped into stage 11. The earliest
stages were missed by taking the first sample at 24
h. Stages 3-6 were observed from field samples.

Table 1. — Summary of development stages and day of first
appearance of anatomical features for tomcod eggs incubated at
different salinities. For temperature regime see Figure 3. The
stages are for eggs developing in freshwater. Stages 3-5 and 9
were observed in field-collected material only.

Day of first
appearance at

Corresponding
stage designa-
tion by Hardy
(1978)

stage

Description

0%.

10%o

20%c

30%o

1

Prior to first

cleavage

<1

<1

<1

<1

—

2

2 cells

<1

<1

<1

<1

168B

3

4 cells

<1

<1

<1

<1

—

4

8 cells

<1

<1

<1

<1

168C

5

16 cells

<1

<1

<1

<1

—

3

Large celled morula

<1

<1

<1

<1

168E

7

Small celled morula

4

4

4

4

168H

8

Embryonic axis

7

7

7

7

168J

9

Kupfer's vesicle

and first somite

—

—

—

—

168E

10

Notochord

10

10

10

10

—

Optic vesicle

10

10

10

10

169G

11

Eye lens

13

13

13

16

169K

Ear placode

13

13

13

16

—

Pericardium

13

13

13

19

—

Brain lobes differ-

entiating

13

13

13

22

—

Fin fold

13

13

13

16

—

12

Pectoral fin buds.

axial pigmentation

16

16

16

28

170E

13

Eye faintly

pigmented

19

19

19

19

170G

14

Gill slit

22

22

22

22

—

Swim bladder

22

22

25

28

—

15

Nasal placodes

25

25

31

none

—

16

Beginning of pro-

nounced snout

31

31

31

none

171A

17

Lower jaw, moutti

not opened

34

34

34

34

171B

18

Moutti can be or is

open

37

37

37

—

1710

19

Pigment on lower jaw

45

46

—

—

172A

20

Hatching

—

—

—

—

172A

Irregularities in development were seen in the
later stages of development at 30%o. The snout
failed to develop normally, and the development of
pectoral fin buds and brain lobes was delayed.

Field Observations

Largest numbers of tomcod eggs were sampled
by the drift samplers (Figures 4, 5) in the 15- to
20-d period after spawTiing. The numbers corre-
lated fairly well with stream water level for
1977-78 when water levels were measured ( Figure
5). Largest numbers of drifting eggs may also be
related to spawning activity rather than stream
water levels per se. Typical numbers of eggs col-

*3 0-

o. tl 0

-10

•^""""'y Febfaoty

MofCh

Sea Surfoce Temp

Fresh Water Temp

1000

100

Eqqs ond
Larvae

Larvae

30 45 60

Doys from Dec 29

Figure 4. — Movements of tomcod eggs and larvae out of Frost
Fish Creek. Upper: Environmental conditions and numbers of
sampled tomcod eggs and larvae are shown for the 3 mo of egg
and larval stream residence in 1976-77. Freshwater tempera-
tures (solid line) and sea surface temperatures (dashed line) for
January- April 1976-77. Lower: Histogram of numbers of tom-
cod eggs and larvae caught in drift samplers. Open bars, eggs;
solid bars, eggs and larvae; hatched bars, larvae.

150

PETERSON ET AL.: EARLY LIFE STAGES OF ATLANTIC TOMCOD

Joouor y

Febiuory

Match

Figure 5.— Similar to Figure 4 but for 1977-78. Upper panel
includes water levels (vertical bars). Asterisk indicates occur-
rence of a winter freshet, at which time drift samplers were
washed out.

20

10 -

5 -

C-

lected ranged from a few hundred to a few
thousand per 24 h during these first 15-20 d. In
mid-February, stream flow rates decreased as the
precipitation accumulated in snow and ice. Typi-
cal numbers of eggs sampled/24 h during this
period were 10-100. Hatching occurred in March
and April (Figures 4, 5). Larvae began to be cap-
tured somewhat earlier in 1976-77 and were taken
in greater numbers than in 1977-78. This latter
phenomenon is thought to be because the sampler
was totally submerged in 1977-78, whereas part of
it was emergent in 1976-77. Larvae probably
emigrate into saltwater near the surface im-
mediately after hatching, as will be discussed in a
later section and may have passed over the sub-
merged sampler in 1977-78. Some of the earliest
larvae may have hatched in the samplers as a
result of warming on the return to the laboratory.
These larvae appeared normal and viable. The
hatching period in nature corresponded to rising
stream water levels in late March in 1977-78. Sea
surface temperatures had also risen to 3.0°-4.0° C
during fry emigration. Catches of larvae termi-
nated in early to mid- April of both years.

The earliest stages of development obtained in
the drift samplers were stage 3 and 4 eggs (Figure
6), owing to lag from spawning to sampling. By the
third week of January the embryonic axis was
discernible in most eggs sampled. By mid-
February, eyes and body axis had become pig-
mented, nasal placodes and fin fold were appear-
ing, and the tail had curled past the posterior

Notching

1976-77

1977 -78

16)

(10)

(2)

(I)

(6) (I2)(4) (25)

(4)

(12)

(III

(2)

(4)

T (20)(3I

(3)
I

(9) (7)

(2)
I

(3)

(3)

(2)
I

(3)

T

(5)

(21
I

(5)
I

(3)
I

20

30

January

10 20

February

10 20

March

30

Figure 6. — Stages of embryonic development for eggs sampled from Frost Fish Creek with drift
samples in 1976-77 and 1977-78. Vertical bars indicate ranges of development observed. Numbers
of eggs inspected are in parentheses. Small arrows indicate samples where all eggs were at the
same stage.

151

FISHERY BULLETIN: VOL. 78, NO. 1

margin of the eye. Hatching began in late Feb-
ruary to mid-March. A series of relatively early
stage eggs was also obtained in late February to
mid-March 1978 (Figure 6), indicating a possible
second spawning of tomcod in late January to
early February.

Laboratory Observations

Survival to Hatch and Length at Hatching

Tomcod egg survival to hatching was highest in
freshwater (Table 2). Fifty-eight percent of the
freshwater eggs hatched, compared with 50, 37,
and 13% at 10, 20, and 30%o salinities, respec-
tively. About half of the mortality at 0 and 10%o
occurred at about day 30 (stage 15). Above 10%o
high mortality also occurred at earlier stages of
development.

Table 2.— Percentage survival to hatching, total larval length
at hatching, and median time to hatch for tomcod eggs incubated
at four salinities. Standard deviations are given for larval
lengths.

Item

0%o

10%o

20%«

30%o

Percentage egg survival

to stage 19

70

73

48

21

Percentage hatched

58

50

37

13

Mean length at hatching

(mm)

7.56±0.69

7.25±0.31

6.31 ±0.44

—

Number of larvae

measured

165

104

85

Time to median hatch (d)

54

51

51

38

Larvae hatched in freshwater were significantly
longer than those from higher salinities (7.54 mm
for freshwater vs. 7.25 and 6.31 mm at 10 and
20%o, respectively). Larvae at 30%o had severe spi-
nal curvature and could not be measured accu-
rately. Hatching was earlier at the higher
salinities.

The developmental success of tomcod eggs var-
ied with salinity, so various parameters associated
with water balance were measured on eggs reared
at 0, 10, 20, and 30%o. These parameters are all
interdependent so that changes in one may result
in concomitant changes in others.

Specific Gravity

The sp. gr. of freshwater (FW) eggs was constant
throughout development (Figure 7) at 1.030, im-
plying that weight and volume were not changing
or that they were changing in such a way that the
sp. gr. was constant. In contrast, eggs incubated at
20 and 30%o decreased in sp. gr. throughout de-

152

050

045

1.040

1035

1030

,025

, 30 7oo

20 %o

10 7oo

F W

_L

20 ~
Time (Doys after

40
fertilization )

60

Figure 7 .—Specific gravity of tomcod eggs incubated at various
times from fertilization at various incubation salinities. Each
point is based on the mean of measurements made on 10 eggs.
Lines fitted by eye. FW = freshwater.

velopment. Specific gravity at 10%o was constant
for the first 25 d of incubation, then decreased
linearly. The sp. gr. of water at 10, 20, and 30%o
(10° C) are 1.009, 1.017, and 1.024, so that eggs
were denser than the incubation medium at all
salinities and by approximately the same amount.
For example, the sp. gr. of FW eggs is 1.030 com-
pared with 1.000 for freshwater, a difference of
0.03 sp. gr. units. The sp. gr. of 20%o eggs (extrapo-
lated to 0 time at 20%o from Figure 7) is 1.045
compared with 1.017 for the incubation medium,
again a difference of 0.03 sp. gr. units. Changes in
sp. gr. may be associated with changes in water
content, loss of solids through metabolism, change
of salt content of eggs, or a combination of these
factors.

Water Content

Mean water content of FW eggs was 2.83 mg/egg
(Table 3) with no trends throughout development.
The water content and percentage water content
of FW eggs for the first 27 d of development were
significantly higher than the values obtained at
the other incubation salinities (P<0.05, ANOVA,
Duncan's Multiple Range Test). The percentage
water content increased from 86.4 to 89%o over the
final 25 d of egg development, attributable to de-
creases in egg dry weight (Tables 4, 5).

There were no significant differences among the
percentages of water content of eggs reared at the
three higher incubation salinities for the first 27 d

PETERSON ET AL.: EARLY LIFE STAGES OF ATLANTIC TOMCOD

Table 3. — Water content (milligrams per egg) and percentage
water (parentheses) in tomcod eggs at various incubation
salinities and days from fertilization. Each value represents 10
eggs. Sampling periods were fewer at 20 and 30%o due to earlier
hatch.

Days of
incubation

9
12
17
22

27

27-d mean

32
37
42

47
52
Newly hatched
larvae

0%o

10%o

20%«

2.86(86.7)
2.87(87.2)
2.72(86.6)
2.94(85.5)
2.78(86.1)
2.83(86.4)

2.78(86.8)
2.87(87.5)
2.86(89.4)
2.88(87.8)
2.76(89.0)

1.41(85.5)

2.19(82.3)
2.14(84.3)
2.36(81.9)
2.22(81.5)
2.34(83.9)

2.25(82.8)
240(84.5)
2.44(85.3)
266(86.0)
258(85.4)
2.91(88.2)

250(84.7)
2.48(83.5)
2.47(83.4)
2.39(83.9)
2.30(82.7)

2.43(83.6)
241(84.0)
2.44(84.5)
2.60(86.1)
2.65(85.8)

30%<i

2.35(81.9)
2.32(82.9)
2.54(83.6)
2.29(79.8)
2.40(82.2)
2.38(82.0)

2.42(83.0)
2.55(84.7)

The water content of newly hatched FW larvae
was 1.41 mg (85.5%), so about half of the water in
the FW egg is associated with perivitelline fluid
and zona radiata.

Dry Weight

No measurable change in egg dry weight oc-
curred over the first 27 d of incubation (Table 4). A
one way ANOVA indicated significant differences
among the mean dry weights for the first 27 d of
incubation (F = 3.9, P<0.05). The mean dry
weight of 30%o was significantly greater than
those of FW and 20%o eggs (Duncan's Multiple
Range Test).

Table 4. — Dry weights (mg) for various incubation salinities and times from fertilization
(d). Each value is averaged from 10 pooled eggs. Values to the left of the bracket for the first
27 d of development are means for that period.

Days of
Incubation

Incubation sa

inity (%o)

0

10

20

30

9

/ 0.44

/0.47

/0.45

/0.52

12
17
22

^0.45
-0.03

I 0.42

{ 0.42

0.50

0.47
-0.05

■

0.40
0.52
0.50

0.47
"0.02

0.49
0.49
0.46

^0.52
-0.04

0.48
050
0.58

27

V 0.45

V0.45

*■ 0.48

^ 0.52

32

0.42

0.44

0.46

0.51

37

0.41

0.42

0.46

0.46

42

0.34

0.40

0.42

—

47

0.36

0.44

0.44

—

52

0.34

0.39

—

—

Newly hatched larvae

0.25

—

—

—

Table 5. — Statistical parameters for regressions of percentage
water content vs. time (d) and dry wt vs. time (data given in
Tables 3, 4). Times are for days 27-52, inclusive, b = slope of
regression equation, r = correlation coefficient, df = degrees of
freedom.

Incubation salinity (V)

Regression

eter

0

10

20

% H2O vs. time

b(%/d)

0.10

0.17

0.13

r

0.80

0.91

0.93

df

4

4

3

t

2.72

4.53

4.47

P

-0.05

< 0.025

■=0.05

Dry wt vs. time

fi(mg/d)

-0.0046

-0.0018

-0.0024

r

0.96

0.70

0.83

df

4

4

3

t

3.55

3.92

2.60

P

<0.025

<0.025

<0.1

of incubation. The water content of 10%o eggs in-
creased over the last 25 d of incubation at 0.023
mg/egg per d (P<0. 05, Tables 3, 5), until the water
content at hatching approached that of FW eggs.
The 20%o eggs took up water after 27 d incubation
at 0.018 mg/egg per d (P<0.01), but the water
content of these eggs was still lower than for eggs
incubated in FW and 10%o. The 30%o eggs may
have taken up slight amounts of water, but the
data are insufficient to be tested statistically.

Dry weight decreased significantly over the last
25 d (Tables 4, 5). This decrease was greatest in
freshwater, about 0.1 mg/egg compared with 0.07
and 0.04 at 10 and 20%o, respectively. Although
sample size is inadequate for statistical analysis,
it would appear that the 30%o eggs lost about 0.05
mg/egg. Yolk content of newly hatched larvae was
not measured; however, larvae hatched from
higher incubation salinities appear to have more
yolk (Figure 8), an observation supported by the
fact that hatching is earlier at higher salinities.
The lesser amount of yolk of FW eggs is in agree-
ment with the greater loss of solids by these eggs.

About 25% of the dry weight of FW eggs is lost at
hatching, and is thus contributed by the chorion
and the perivitelline fluid.

Egg Diameter

The diameters of 10 eggs from each incubation
salinity were measured at the time intervals indi-
cated in Table 6. There was no indication of any
change in egg diameter with length of incubation
(Table 6), so that the water uptake at the three

153

Figure 8. — Newly hatched tomcod larvae from various incuba-
tion salinities. Note the larger amounts of yolk remaining, the
higher the salinity of incubation. A. Freshwater; B. 10%o; C.
20%o. Yolks have shrunk due to (Formalin) fixation effects. Mag-
nifications 13 X .

Table 6. — Egg diameters (millimeters) for various incubation
salinities and incubation times. Each value is the mean of 10
measurements, v = calculated egg volume (microliters). Stan-
dard deviations given in parentheses.

Days of
incubation

0%0

1 0%o

20%o

30%o

4

1.85(0.06)

1 .79(0.08)

1 .77(0.05)

1.81(0.09)

12

1.86(0.04)

1.76(0.07)

1 .75(0.06)

1.76(0.04)

17

1 .87(0.05)

1.75(0.05)

1 .79(0.05)

1 .80(0.04)

22

1 .89(0.04)

1.77(0.05)

1.76(0.05)

1.78(0.05)

27

1.84(0.07)

1.75(0.05)

1.76(0.05)

1 .76(0.04)

32

1 .89(0.02)

1.74(0.05)

1.78(0.06)

1.78(0.05)

37

1.90(0.05)

1 .77(0.05)

1 .78(0.05)

1 .78(0.06)

42

1 .93(0.05)

1.82(0.04)

1.81(0.05)

—

47

1.84(0.04)

1.81(0.04)

1.76(0.06)

—

52

1.86(0.07)

1.79(0.05)

—

—

X

1.87

1.78

1.77

1.78

V

3.47

2.86

2.84

2.83

higher salinities toward the end of the incubation
period did not lead to measurable swelling, al-
though slight swelling within experimental error
probably occurred. The mean diameters of FW, 10,
20, and 30%o eggs were 1.87, 1.78, 1.77, and 1.78
mm, respectively. The standard deviations for lots
of 10 eggs varied from 0.02 to 0.09 mm, and were
0.04-0.05 in most cases. The greater diameter of
the FW eggs is no doubt related to the higher
water content of these eggs.

FISHERY BULLETIN: VOL. 78, NO. 1
Specific Gravity of Egg Solids

The sp. gr. of FW egg solids (lipids included) was
constant at 1.27 for the first 27 d of incubation
(Figure 9), then rose linearly to about 1.36 just
before hatching. This increase in sp. gr. of egg
solids may be due to increase in compact tissue,
such as cartilage. It could also reflect a rapid in-
crease in embryonic tissue and a corresponding
decrease in yolk solids. The sp. gr. of solids of
Atlantic salmon alevins also increases during de-
velopment (Peterson and Metcalfe 1977). This was
shown to be due to increase in embryonic mass, the
solids of which had a higher sp. gr. than did yolk
solids.

The sp. gr. of 10%o egg solids was identical to
that of FW eggs throughout. Apparently, in-
sufficient salt penetrated these eggs to change the
solids' sp. gr. measurably. This apparent lack of
difference between FW and 10%o eggs should be
accepted with some caution, since an error of 0.01
mg/egg in estimating dry weight (averaged over
the first five measurements) could result in a shift
in solids' sp. gr. by 0.2 units. Since the dry weight
of 10%o eggs was some 0.02 mg greater than that of
FW eggs (Table 4), some salt may well have en-
tered the 10%o eggs.

The sp. gr.'s of egg solids for 20 and 30%o eggs
during early development were much higher than
for the two lower salinities (Figure 9), and they

L38
1.36

"O

o

CO

^ 1.34

LU
O

^ 1.32

O

•^ 1.30

ir>

I 28

26

30%

«-« — « — ft — ft

_L

J_

10 20 30 40 50

Time from Fertilization (Doys)

60

Figure 9. — The specific gravity of egg solids (as calculated from
water content and egg specific gravity) at various times from
fertilization for various incubation salinities. Lines fitted by eye.

154

PETERSON ET AL.: EARLY LIFE STAGES OF ATLANTIC TOMCOD

decrease with time until a minimum is attained at
27 d postfertilization. The sp. gr. then rose again,
as for eggs reared at 0 and 10%o. The decrease in
egg solids' sp. gr. from fertilization to day 27 at 20
and 30%o may be due to more efficient salt elimina-
tion as the embryo grows. After 27 d the decrease
due to salt elimination is more than balanced by
increases due to factors postulated above for FW
eggs. Apparently, eggs reared at 20%o were suc-
cessful in eliminating salt, because the sp. gr. of
their egg solids tends to converge with that for
eggs reared at lower salinities. At 30%o, however,
the embryos appeared to be unable to eliminate
excess salt successfully because the solids' sp. gr.
never approached those for eggs reared at lower
incubation salinities. The 30%o eggs hatch earlier
than those incubated at lower salinities, perhaps
in response to high salt concentrations. As men-
tioned previously, they were abnormally de-
veloped.

The higher sp. gr. of egg solids at 30%o would
require that 15% of the solids be excess salt (using
the formula 1.27a + 1.8(1 -a) = 1.35; where a =
proportion of egg solids that is not salt; 1 .8 = sp. gr.
of salt, 1.27 = sp.gr. of FW egg solids, 1.35 = sp.gr.
of 30%o egg solids). This amounts to about 0.08 mg.
This is reasonably close to the increase in dry
weight of 30%o eggs over FW eggs (0.07 mg). The
decrease in sp. gr. of 30%o egg solids to its
minimum of 1.33 would require the loss of 0.02 mg
of salt.

Newly hatched larvae in freshwater that did not
have access to the water surface had an sp. gr. of
1.032, which is nearly identical to that of eggs
incubated in freshwater. If larvae were permitted
access to air at the water surface, the sp. gr. de-
clined within 7 h to 1.01, coincident with ingestion
of air into the swim bladder. Newly hatched larvae
were observed swallowing air at the surface. The
filling of the swim bladder was investigated
further with a Cartesian diver technique. Larvae
that had access to air floated at a flotation pressure
(Saunders 1965) of 154 mm Hg (130-170, n = 6)
(0.8 atm). Those that had been denied access to air
for 24 h failed to float at 675 mm Hg (645-685, n =
15), corresponding to 0.1 atm (the greatest vac-
uum attainable with the apparatus). No air was
observed in the swim bladder of these larvae.
These larvae were then allowed access to the sur-
face overnight. When tested subsequently, none
floated at 675 mm Hg, nor was air observed in the
swim bladder. These latter larvae, unlike larvae
with air in the swim bladder (that spend most of

their time near the surface), stayed on the bottom
of the container.

Newly hatched larvae were photopositive as
tested in a half-blackened Petri dish. In two trials,
78% (39/50) and 64% ( 16/25) larvae were observed
in the lighted (unpainted) half of the Petri dish.
When the dish was kept in darkness, 46% (23/50)
and 36% (9/25) larvae were observed in the
unpainted half. Larvae were commonly observed
to aggregate near the lighted sides of rearing
containers.

GENERAL DISCUSSION

The changes that occurred in eggs reared in
various salinities will first be summarized:

Eggs reared in freshwater consisted of 2.8 mg
water, sufficient for the embryo's needs, being con-
stant throughout development. The egg sp. gr. was
also constant despite decrease in solid materials
(ca. 0.1 mg) — the egg diameter should therefore
decrease slightly (about a 1.7% decrease is re-
quired), although this was not observed, as it is
within experimental error.

Eggs reared in 107oo salinity have about 2.2 mg
water for the first month of development, but take
up an additional 0.5-0.6 mg in the later stages of
development, due to the greater water require-
ments of embryonic tissue. Some of this uptake
may also be associated with formation of fluid
filled body cavities (Zotin 1965). This water up-
take was associated with a decreased egg sp.
gr. The 10%o eggs may have a slight salt load
which is probably eliminated in the later de-
velopmental stages. The egg dry weight declined
by only 0.07 mg, and newly hatched 10%o larvae
may have larger yolks than do those in 0%o (Figure
9).

Eggs reared in 20%o salinity had a water content
equal to or greater than that of 10%o eggs in the
early stages of development, but had to tolerate a
higher salt load (ca. 0.04 mg/egg) as a result. Egg
sp. gr. declined throughout development due to
salt elimination as the embryo developed and to
accumulation of about 0.2 mg water during the
later developmental stages. Advanced embryos
eliminated much of the initial salt load as the egg
solid sp. gr. of late stage eggs is nearly identical to
that of eggs reared at lower salinities. The concept
of salt elimination seems reasonable, but is subject
to some uncertainty in these experiments because
the solids associated with the chorion and
perivitelline fluid are included in the estimates of

155

FISHERY BULLETIN: VOL. 78, NO. 1

solids sp. gr. These compartments of the egg obvi-
ously would have no capacity for elimination of
salts. Egg dry weight declined by only 0.04 mg at
hatching as newly hatched 20%o larvae appear to
have even more yolk than 10%o larvae (Figure 8).
The 20%o curve in Figure 9 suggests that salt
elimination began very early and increased as the
embryo grew. It is probable that at least the early
salt elimination had a cellular rather than organ
basis.

Eggs reared in 30%o salinity also had a water
content similar to those reared at 10 and 20%o, but
the salt load was high. Water accumulation dur-
ing the later developmental stages was low (ca. 0. 1
mg). The sp. gr. of egg solids goes down over the
first 27 d of development, indicating some elimina-
tion of salt. The pattern during the later stages of
development is strikingly different from that at
20%o in that the solids' sp. gr. again rose to about
1.37 at 37 d of incubation at which point the larva
hatched. Problems with salt balance and os-
moregulation may have led to the deformities and
early hatching. The dry weight of 30%o eggs de-
creased only slightly during development.

It has been shown, for the eggs and larvae of
some marine organisms, that the salinity in which
fertilization and the earliest stage of development
occur may influence development and growth of
subsequent stages in the life history (Kinne 1962).
It is therefore possible that eggs fertilized in water
of higher salinity might have responded different-
ly to the various experimental salinities. Booth
(1967) obtained data suggesting that fertilization
could occur in salinities as high as 15%o. It is nota-
ble, however, that the eggs of Cyprinodon
macularius in Kinne's experiments were allowed
to develop 3-6 h in the spawning salinity, and at a
higher temperature (27° C) than was the case for
the tomcod experiments. It is probable that the
eggs of C. macularius had developed further be-
fore experimentation.

The tomcod's early life history seems adapted to
the hydrodynamics of streams in which it spawois.
Spawning migrations occur in late December to
early January while water levels are still high
from the fall freshets. The eggs develop through-
out midwinter when water levels are low, thus
minimizing loss of eggs from the stream, then
hatch when water levels are rising coincident with
the early snow melt. The higher water levels dur-
ing hatching would ensure rapid flushing of larvae
into the estuary. Newly hatched larvae probably
rise to the stream surface soon after hatching and

156

ingest air into the swim bladder, with possibly the
positive response to light facilitating surfacing.
This behavior of newly hatched larvae would also
ensure rapid flushing into the estuary.

The continuous drift of eggs out of the stream is
somewhat puzzling. Most eggs taken in the drift
samples were alive and apparently developing
normally. These perhaps are eggs which had been
deposited where they were likely to be taken up
into suspension. In support of this suggestion, egg
drift was positively correlated with stream level.
Whether these eggs continue to develop would de-
pend in part upon the salinity conditions where
they finally settle and the ambient salinity during
earlier development. Laboratory results indicate
that less than full salinities are required for nor- .
mal development from fertilization, but the eff"ects
of variable salinities on tomcod egg development
were not investigated.

The tomcod egg resembled those of freshwater
species (rather than marine species) in regard to
salt tolerance, assuming that the responses re-
ported here are typical. Eggs of brook trout exhibit
increased mortality above 6%o salinity with total
mortality at 12%o (Sutterlin et al.^). Species such
as Abramis will hatch in salinities up to 20%o,
although 2.5-5%o is optimal (Holliday 1969). With
the tomcod, between 20 and 30%o salinity appears
to be the upper limit for production of normal
larvae. By way of contrast, eggs of several marine
species have been hatched in salinities up to 60%o
(cod, herring, plaice), although optima are usually
in the 25-30%o range (Holliday and Blaxter 1960;
Holliday 1965).

Eggs of marine species tend to swell at low
salinities (usually <15%o); above this salinity egg
diameter is constant (Holliday 1965; Solemdal
1967). Tomcod eggs require salinities of <10%o for
noticeable swelling to occur.

Several parameters measured (water content,
dry weight, solids' sp. gr., and egg sp. gr. for 10%o
incubation) begin to change dramatically at about
27 d of incubation. In relation to embryonic de-
velopment it seems probable the embryonic mass
is beginning to increase dramatically at this point,
resulting in the noted physiological changes.
Perhaps these changes are linked to the high mor-
tality occurring at this stage of development.

^Sutterlin, A. M.,P. Harmon, andH. Barchard. 1976. The
culture of brook trout in salt water. Fish. Mar. Serv. Res. Dev.
Tech. Rep. 636, 21 p. Fisheries and Environmental Sciences,
Fisheries and Oceans Canada, Biological Station, St. Andrews,
NB EOG 2X0.

PETERSON ET AL.: EARLY LIFE STAGES OF ATLANTIC TOMCOD

Zotin (1965) reported that eggs of freshwater
teleosts (e.g., loach, zander (Lucioperca)) took up
no water after water hardening until the chorion
began to stretch due to weakening by the hatching
enzyme. The mullet egg took up water during the
second half of development during which time the
perivitelline space first appeared. With the tom-
cod, water uptake occurred in the latter stages of
development in the three higher salinities. It is
not known where this water was distributed
within the egg, but it was probably incorporated
into embryonic tissue.

It is inferred, from calculated specific gravity of
egg solids, that tomcod embryos osmoregulated to
some degree, becoming more proficient as de-
velopment proceeded. This may be simply a func-
tion of embryonic size, resulting in more
osmoregulating tissue. It has been suggested by
Holliday ( 1965) that plaice embryos can regulate
osmotic concentration after gastrulation, which
occurs in 9 d or less in these tomcod eggs. Holliday
(1969) also showed that flounder eggs could regu-
late yolk sodium from fertilization. Unfortu-
nately, we did not make measurements here be-
fore 9 d of incubation.

Holliday and Blaxter (1960) and Forrester and
Alderdice (1966) observed development to proceed
faster at higher salinities for herring and Pacific
cod, respectively. While tomcod hatched earlier at
higher salinities, there is little suggestion that
development occurred more rapidly. Rather, it ap-
peared that the freshwater larvae grew larger
prior to hatching. Some structures were delayed,
or never appeared in 30%o embryos, but this is due
to abnormal development at this salinity. Abnor-
mal development has frequently been recorded at
abnormally high salinities. Usually the defor-
mities are skeletal as are observed for tomcod, or
involved body cavity deformities (Holliday 1965;
Alderdice and Forrester 1971).

Although the tomcod is a physoclist species, the
pneumatic duct is apparently functional in the
newly hatched larva. In <24 h the duct is closed,
and the larva can no longer fill the swim bladder
by air ingestion. Larval loss of the pneumatic duct
has been implied for physoclists generally (Har-
den Jones 1957). Whether or not the duct is
utilized in initial filling of the bladder is apparent-
ly quite variable (Johnston 1953; Schwarz 1971).

ACKNOWLEDGMENTS

We wish to acknowledge P. Harmon for assist-

ing in some aspects of field studies; P. W. G.
McMullon and F. Cunningham for performing the
photography and drafting; A. Sreedharan for pro-
viding statistical analyses of the data; and D. W.
McLeese and M. J. Dadswell for reviewing the
manuscript.

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158

NOTES

OBSERVATIONS OF SEA OTTERS DIGGING

FOR CLAMS AT MONTEREY HARBOR,

CALIFORNIA

Although the feeding behavior of the sea otter,
Enhydra lutris, is frequently observed from the
surface, few underwater observations of foraging
sea otters have been published. Faro (1969) and
Houk and Geibel (1974) described the underwater
behavior and tool use of sea otters when they re-
moved abalone from rock substrates. Shimek
(1977) observed a sea otter foraging for snails and
presumably other invertebrates by patting the
surface of rocks and feeling into cracks. Shimek
also described a sea otter digging up the echiuroid
worm, Urechis caupo, from a silt and cobble sub-
strate. Further deductions about underwater
foraging behavior have been made from collec-
tions of abalone shells with the characteristic "ot-
ter break" hole in the middle (Wild and Ames^)
and from observations of aluminum beverage cans
bitten by otters to remove octopus (McCleneghan
and Ames 1976). Some sea otters can be enticed
underwater to take food offered them (pers. obs).
However, these latter observations of underwater
food manipulation are of limited value because the
otters also take items unpalatable to them (e.g.,
the holothuroid Stichopus californicus) , and be-
cause the otters were clearly interacting with the
diver observer. These accounts of underwater
foraging indicate that sea otters use primarily tac-
tile sensitivity of the forelimbs to locate and cap-
ture prey, whereas all other marine mammals
(pinnipeds and cetaceans) use their jaws to cap-
ture prey. Radinsky (1968) hypothesized that the
sea otter evolved forelimb tactile sensitivity sepa-
rately from the aonychoid otters.

The large impact of sea otters on Pismo clam,
Tiuela stultorum, populations in California has
been documented (Stephenson 1977; Miller et
al.2), and in Prince William Sound, Alaska, 81% of
the food items taken by sea otters were bivalves,
especially Saxidomus gigantea (Calkins 1978).

•Wild, P. W., and J. A. Ames. 1974. A report on the sea
otter, Enhydra lutris L., in California. Calif. Dep. Fish and
Game Mar. Resour. Tech. Rep. 20, 93 p.

=*Miller, D. J., J. E. Hardwick, and W. A. Dahl-
strom. 1975. Pismo clams and sea otters. Calif. Dep. Fish
Game Mar. Resour. Tech. Rep. 31, 49 p.

FISHERY BULLETIN: VOL. 78, NO. 1, 1980.

The Alaskan otters "dug out clams with their
forepaws while maintaining a head downward
position" in intertidal and shallow subtidal water.
However, Shimek's (1977) description is the only
detailed underwater observation of sea otters
foraging on soft substrate. Detailed observations
of sea otters taking prey from soft substrates are
more difficult than those on rock, because the ot-
ter's disturbance of the bottom often results in
clouds of sediment obscuring further vision. In the
present account, we describe underwater ob-
servations of sea otters digging clams in a silty
sand substrate and present information about the
impact of this foraging on the distribution and
abundance of subtidal clams at Monterey Harbor,
Calif.

Observations

In 1976-77 we observed sea otters eating large
numbers of the Washington c\a,va, Saxidomus nut-
talli, primarily in two specific areas of Monterey
Harbor (A and B of Figure 1 ). From vantage points
along the floating boat slips and elevated wharves,
we observed sea otters at the surface feeding on
211 prey items: S. nuttalli (88.6%); the crabs
Pugettia producta (4.2%) and Cancer sp. (3.3% —
probably C. antennarius or C. productus, but not
C. magister); the rock jingle hiwalve Pododesmus
cepio (1.4%); and unidentified items (2.4%). Dur-
ing spring 1976, as many as four sea otters were
foraging at one time in the harbor vicinity, but an
average of about one sea otter was observed on 38
counting trips made to the area.

The underwater path of foraging sea otters
could often be observed from the surface by follow-
ing the trail of air bubbles escaping from their
compressed fur. The paths of foraging dives made
in the inner harbor were often contorted, 50-60 m
or more long, and lasted 45-80 s. These dives usu-
ally produced no prey, but the prey taken were
mostly crabs and rarely clams. On those dives that
resulted in the capture of kelp crabs, sea otters
usually (eight out of nine dives) finished their
search with a swim under 10-20 m of the floating
docks in the inner area of the harbor. During scuba
dives in this area, we repeatedly observed kelp
crabs on the undersides of these floats and rarely
elsewhere. It was difficult to observe the paths of

159

^

1 » 1 »

300 m

N
1

• • • ■
• • •

• •

• •

"^^=^.

i^

""

^^

• • •
• •

Outer

• • >

* *i

Harbor

• • • ,

f^^

^3

• • • • wv,. ^tULu^ ''F ^s

^ Inner

B

• * • • •

Harbor

• • •

«

^^~'^^^~r~-~^

Figure l. — Monterey Harbor, Calif. High densities of clams
were foraged by sea otters in areas A and B. 1 = Fisherman's
Wharf; 2 = Wharf No. 2; 3 = north and east sea wails of the inner
harbor; 4 = breakwater for the outer harbor. (Traced from an
aerial photograph in Haderlie and Donat 1978.)

dives made in the middle of the outer harbor, but
sea otters usually surfaced without prey 50 m or
more from the start of the dive. However, the paths
of feeding dives in the two locations where clams
were taken in abundance were usually quite short,
only 10 m or less.

The usual sequence of dives in the harbor region
began with otters making one to three 50-90 s
dives that produced no prey. After about 10-20 s on
the surface and a little grooming, the otters usu-
ally dove again to the same spot. A series of short
(25-40 s) dives followed the initial dives, and each
of these invariably resulted in a single S. nuttalli
about 10 cm long. The otters took 30-90 s to open
and eat the clams before diving to the same spot.
Sometimes they pounded the clams on a rock anvil
on their chest; other times they simply twisted or
pried the clams open with their teeth. An average
of 6 and as many as 19 clams were taken in a single
series of these dives. Following such a series, ot-
ters usually spent up to 30 min grooming before
they swam away, sometimes to forage in a new
location.

In spring 1976, we conducted an underwater
survey of most of the bottom of the inner and outer
harbor, noting variations in the substrate and
counting protruding clam siphons in haphazardly
tossed y^ m^ quadrats. Depths in the harbor ranged
from 2 to 8 m, with area A being 4.5 m and area B
2-3 m (Figure 1). The substrate in much of the
enclosed inner harbor was black mud and silt, and
most of the rest of the harbor (including areas A
and B) was silty sand. The two areas where otters
fed extensively on clams had high densities of
clam siphons: for area A,x = 13.5/m2, SD = 8.9, n
= 19; for area B,x = 9.3/m2, SD = 7.2, n = 16. The
area under Wharf No. 2 adjacent to area A had
even higher densities of siphons: x = ITA/m.^, SD
= 11.9, n= 18. However, other areas of the harbor
had siphon densities < l.O/m^, and the black mud
of the inner harbor had densities <0.04/m2. ^g
inserted a slender rod down siphon holes in the
substrate until the rod contacted the clam shell,
and, with considerable difficulty, we used a stream
of freshwater from a garden hose to obtain a few
8-14 cm long clams from area A. We used these
specimens to distinguish the two species present
by the morphology of the protruding siphons. The
species composition in areas A, B, and under
Wharf No. 2 were the same: 95% wereS. nuttalli,
5% were the gaper clam, Tresus nuttallii. In this
way we also determined that the clams were lo-
cated 10-50 cm into the substrate and that larger
individuals of both species tended to occur at the
deeper end of this range in the sediment. We re-
corded the densities of clam siphons in area A and
also in the adjacent area of highest density under
Wharf No. 2 at approximately bimonthly intervals
from February 1976 to March 1977. The densities
and proportions of the two species of clams did not
change (ANOVA,P>0.05).

The bottom in the two areas where sea otters
took large numbers of clams was littered with
hundreds of shells, both on the surface and mixed
into the sediments. About 58% of the shells did not
have pairs of connected valves, and about one-
third of the valves were broken. Of 89 shells sam-
pled, 99% wereS. nuttalli and 1% wereT. nuttallii.
The bottom topography was hummocky in these
areas, and there were many craters 0.5-1.0 m
across and 10-15 cm deep. The bottom under
Wharf No. 2, where the density of clam siphons
was highest, was mixed with debris consisting of
chunks of asphalt apparently from resurfacing of
the road on the wharf and of clumps of large bar-
nacle, Balanus nubiluS, tests which had fallen

160

from the massive barnacles encrusting the pihngs.
There were considerably fewer craters in this area
compared with the adjacent area A, and our at-
tempts to dig into the substrate under the wharf
proved difficult as a result of the debris embedded
in the sediment.

Sea otters were in the process of foraging on
clams during several of the scuba dives in area A.
Although these otters were not bothered by our
presence under water, attempts to observe pre-
cisely how they were capturing clams usually
failed because they stirred up large clouds of sedi-
ment that obscured all of their activity. When the
otters stopped foraging and the clouds of sediment
dispersed, a large hole up to 1.0-1.5 m across and
0.5 m deep had obviously resulted from their dig-
ging. The sides of these holes were initially nearly
vertical, but collapsed within minutes.

Details of a sea otter digging for clams were
observed by the first author on a single occasion on
30 March 1977, when a strong current rapidly
dispersed the clouds of sediment. Upon observing
a young male otter begin a typical sequence of
foraging dives in area A, the observer moved along
the bottom and approached the digging site from
an upstream direction. The otter was clearly visi-
ble at a distance of 5 m and was just leaving the
bottom after completing the second longer dive of
the series. He returned to the bottom within 20 s
but abandoned the initial digging site, leaving a
small hole about 0.5 m across and 25 cm deep.
Instead, on this third dive, he moved immediately
to a new spot about 4 m away and began to dig
rapidly with his front paws in a fashion very much
like a dog, producing a large conical cloud of sedi-
ment extending downstream. Digging lasted
about 45 s, followed by a 20 s surface interval. On
the fourth dive the otter resumed digging in the
same spot, and as during all digging periods, he
faced into the current. The observer was able to
approach < 1 m from the sea otter by creeping up in
a prone position on the bottom while the otter
substantially enlarged the hole to a short trench
about 1 m long, 0.5 m across, and 25 cm deep by
digging rapidly with both front paws. His back
flippers were moving at a slower rate, which prob-
ably helped maintain his position and also ap-
peared to assist in digging. Toward the end of the
digging on this dive the otter began to roll re-
peatedly from side to side to enlarge the front end
of the trench laterally, until he apparently en-
countered a clam and suddenly surfaced for 45 s.
On the fifth dive this rapid process of rolling and

lateral digging with the front paws continued
again for about 30 s until another clam was caught
and the activity suddenly stopped. The hole at this
time was over 0.5 m deep and the otter's body was
entirely below the level of the substrate surface
while digging. The otter used this process of lat-
eral digging on three more dives lasting about 30 s
each with 40-60 s surface intervals, before the
observer ran out of air and surfaced. The trench at
that time was over 1.5 m long and remained about
0.5 m wide and deep. The otter terminated the
series of feeding dives with one additional dive
while the observer was at the surface. It paid no
apparent attention to the observer's close presence
during the entire series. Simultaneous observa-
tions by the second author from the surface indi-
cated that none of the first three dives (including
two dives at the first spot) produced a clam, but
that each of the six subsequent dives resulted in a
single clam. The otter did not use a rock to open the
clams.

Discussion

In 1966, prior to the return of sea otters to Mon-
terey Harbor, Calif., Department of Fish and
Game divers made qualitative surveys of the bot-
tom and used a garden hose to remove several
clams from the substrate for identification. The
bottom topography was smooth, clams were abun-
dant, and T. nuttallii was the dominant species
removed from as deep as 50 cm in the substrate
(Ebert^). Follow-up survey dives soon after the
return of sea otters indicated that clams were less
abundant and the bottom topography was hum-
mocky (Ebert, see footnote 3). Although definitive
quantitative data are not available for that period,
and although construction and dredging opera-
tions in the inner marina portion of the harbor
may have had important impact on clam popula-
tions, information in the present report indicates
that sea otters may have limited the abundance
and distribution of S. nuttalli and T. nuttallii and
that T. nuttallii is now only a minor species. The
cause of this apparent shift in dominance from T.
nuttallii toS. nuttalli is unclear. Our limited mea-
surements of the depths of these clams in the sub-
strate indicated that larger individuals were
found deeper (to about 50 cm), but that neither

^E. E. Ebert, Director, Marine Culture Laboratory, California
Department of Fish and Game, Granite Canyon, Coast Route,
Monterey, CA 93940, pers. commun. June 1979.

161

species had a depth refuge from predation by sea
otters, which excavated deeper than 50 cm. Tresus
nuttallii attains larger size than S. nuttalli (pers.
obs.), and if sea otters prefer larger clams, they
may have preyed preferentially upon T. nuttallii.
However, clams remained abundant in small
areas of the harbor in spite of heavy predation by
sea otters. Densities under Wharf No. 2 averaged
about 17 clams/m^; and in this area they appear to
have a partial refuge from sea otters, which may
have found it too difficult to dig through the debris
of chunks of asphalt and clumps of barnacle tests
embedded in the sediment. No such impediment to
digging exists in areas A and B, where clams have
persisted in somewhat lower densities of about 14
and 9/m^, respectively. However, the species com-
position of clams was the same under Wharf No. 2
and in areas A and B, regardless of predation in-
tensity.

By following tagged animals, Loughlin (1977)
showed that certain sea otters made daily foraging
trips to Monterey Harbor from rafting locations as
far as 2 km away. In the present descriptions of
their dive paths, sea otters feeding on items other
than clams apparently located prey in a random
manner similar to Shimek's (1977) description of
an otter patting the surface of rocks and feeling
the cracks. Observations of the bubble paths of
otters taking clams in areas A and B of the harbor,
however, indicated that they usually did not spend
time searching for a suitable place to dig, nor did
visual selection of a patch of clams appear to occur.
If the density of clams in area A averaged 14/m2,
and if an average spot dug up by an otter was 0.5 x
1.5 m (0.75 m^) as observed in this report, then
random digging in area A would produce about 10
clams. This is greater than the average number of
six clams taken by otters on a series of dives.
Perhaps the otters had learned the location of the
clam patches, and because sediment clouds nor-
mally prevented visual cues as soon as the sub-
strate was disturbed, they simply dug haphazard-
ly within the patch. Indeed, Gentry and Peterson
(1967) compared the underwater visual acuity of
sea otters with the sea lion, Zalophus califor-
nianus, and harbor seal, Phoca vitulina, and pro-
posed that vision in otters may be better adapted
for aerial situations of predator detection rather
than for underwater prey location.

The strategy of repeatedly enlarging the hole to
capture clams is a good one, because it makes
efficient use of the labor to start the hole on initial
dives. Anyone who has dug in sand at the seas' --e

knows that it is relatively easy to enlarge a hole,
and it would be advantageous to do this rather
than dig straight down for each individual clam.
The behavior of digging like a dog has also been
reported by Shimek (1977) for a sea otter taking
subtidal echiuroid worms and is apparently simi-
lar to the behavior of sea otters taking clams in
shallow subtidal and intertidal waters in Alaska
(Calkins 1978). The holes reported by these au-
thors were only half the size of freshly dug holes at
Monterey Harbor, however. The first author has
observed similar (1.5 m across and 0.5 m deep)
holes dug by otters in the sand channels in 12 m of
water off kelp forests at Pacific Grove, Calif. In
areas such as Prince William Sound and Monterey
Harbor, where otters forage heavily on clams,
their digging must cause a major disturbance of
the infaunal community.

Sea otters have been termed "keystone pred-
ators" (Estes and Palmisano 1974; Estes et al.
1978), because they regulate populations of
epibenthic invertebrates, perhaps through a pro-
cess of switching between prey species. At Mon-
terey Harbor there is circumstantial evidence that
sea otters have had a major impact on two other
prey items. Surveys by the California Department
of Fish and Game showed C. antennarius and C
productus were taken in abundance by fishermen
from the Monterey wharves prior to the return of
sea otters, but they were rarely taken at Monterey
in 1972-74, while still caught in abundance at
piers north of the range of sea otters (California
Department of Fish and Game"*). Observations on
the scuba dives reported here for 1976-77 confirm
that cancer crabs are rare in the harbor. Mytilus
edulis and M. californianus formed dense clumps
on wharf pilings prior to the return of sea otters
(Haderlie^), but mussels are small and uncommon
there now (Haderlie and Donat 1978). Curiously,
large specimens ofB. nubilus are still abundant on
the pilings and were not taken in appreciable
numbers by sea otters, even though these barna-
cles were taken frequently by otters at other loca-
tions in the Monterey area (pers. obs.). The factors
which regulate prey selection by sea otters remain
poorly understood.

■"California Department of Fish and Game. 1976. A pro-
posal for sea otter protection and research and request for the
return of management to the State of California. Calif. Dep.
Fish Game, Oper. Res. Branch, Vol. 1: Text and summaries,
271 p.

^E. C. Haderlie, Professor, Naval Postgraduate School, Mon-
terey, CA 93940, pers. commun. May 1976.

162

Acknowledgments

John S. Pearse, Ronald Jameson, and an
anonymous reviewer provided advice and critical
discussion for this study. Christopher Harrold
gave technical and diving help. We thank the staff
at Hopkins Marine Station of Stanford University
for their assistance. This work was partially
funded by the U.S. Fish and Wildlife Service.

Literature Cited

Calkins, D. G.

1978. Feeding behavior and major prey species of the sea
otter, Enhydra lutris, in Montague Strait, Prince William
Sound, Alaska. Fish. Bull., U.S.76:125-131.
ESTES, J. A., AND J. F. PALMISANO.

1974. Sea otters: their role in structuring nearshore com-
munities. Science (Wash., D.C.) 185:1058-1060.
ESTES, J. A., N. S. Smith, and J. F. Palmisano.

1978. Sea otter predation and community organization in
the western Aleutian Islands, Alaska. Ecology 59:822-
833.
Faro, J. B.

1969. A survey of subtidal sea otter habitat off Point Pinos,
California. M.A. Thesis, Humboldt State Univ., Areata,
Calif., 278 p.
Gentry, R. L., and R. S. Peterson.

1967 . Underwater vision of the sea otter. Nature (Lend.)
216:435-436.

haderlie, E. C, and W. donat ni.

1978. Wharf piling fauna and flora in Monterey Harbor,
California. Veliger 21:45-69.
HOUK, J. L., AND J. J. GEIBEL.

1974. Observation of underwater tool use by the sea otter,
Enhydra lutris Linnaeus. Calif. Fish Game 60:207-208.
LOUGHLIN, T. R.

1977. Activity patterns, habitat partitioning, and groom-
ing behavior of the sea otter, Enhydra lutris, in Califor-
nia. Ph.D. Thesis, Univ. California, Los Ang., 110 p.
MCCLENEGHAN, K., .A.ND J. A. AMES.

1976. A unique method of prey capture by a sea otter,
Enhydra lutris. J. Mammal. 57:410-412.

Radinsky, L. B

1968. Evolution of somatic sensory specialization in otter
brains. J. Comp. Neurology 134:495-505.

SHIMEK,S. J.

1977. The underwater foraging habits of the sea otter,
Enhydra lutris. Calif. Fish Game 63:120-122.

Stephenson, M. D.

1977. Sea otter predation on Pismo clams in Monterey
Bay. Calif. Fish Game 63:117-120.

ANSON H. HINES

Chesapeake Bay Center for Environmental Studies

Smithsonian Institution

P.O. Box 28, Edgewater, MD 21037

Thomas r. loughlin

Office of Marine Mammals and Endangered Species
National Marine Fisheries Service, NOAA
Washington, D C 20235

EFFECT OF ZINC ON FIN REGENERATION IN

THE MUMMICHOG, FUP^DULUS HETEROCLITVS,

AND ITS INTERACTION WITH

METHYLMERCURY

Methylmercury has been found to retard fin re-
generation in the marsh killifish, Fundulus
confluentus, and striped mullet, Mugil cephalus
(Weis and Weis 1978). In F. confluentus the re-
tarding effect of methylmercury was masked in
water of reduced salinity (9%o). Cadmium, which
also retarded fin regeneration in killifish (Weis
and Weis 1976), interacted antagonistically with
methylmercury so that fish exposed simultane-
ously to the two metals exhibited growth rates
comparable to controls (Weis and Weis 1978).

This paper reports on the effects of zinc on re-
generation in the mummichog, F. heteroclitus ,
and the effects of combinations of methylmercury
and zinc on this process.

Methods

Fish were collected by seining in the vicinity of
Montauk, N.Y. The lower portion of each caudal
fin was amputated with a scalpel, and approxi-
mately 15 fish were placed in each of several all-
glass aquaria with 10 1 of 30%o salinity water. The
temperature was 20°-22° C and the photoperiod
was 14 h light/10 h darkness. Fish were fed com-
merical fish food and live grass shrimp, Palaemo-
netes pugio. Tanks were dosed with methylmer-
curic chloride (I.C.N. Pharmaceuticals, Plainview,
N.Y.i) from a 0.1 mg/ml stock solution in
0.2% NaHCOg to yield a final calculated concen-
tration of 0.050 or 0.025 ppm depending on the
experiment, and/or with ZnClg (Reagent Grade,
Fisher Scientific) from a 1.0 mg/ml stock solution
to yield calculated concentrations of 1.0, 3.0, or
10.0 ppm. Aquaria were washed, refilled, and re-
dosed after 2, 4, 7, 9, and 11 days. Regenerating
fins were measured with a calibrated ocular mi-
crometer in a stereomicroscope at 7, 9, 11, and 14
days. Experiments were terminated at 2 wk be-
cause after that time it became difficult to ascer-
tain the point at which the amputation had been
made. The amputation plane can be seen clearly
in Figure 1, a control fin 1 wk after amputation.

Three experiments were performed. Experi-
ment I involved exposure offish 3.5-4.2 cm stan-

» Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

FISHERY BULLETIN: VOL. 78, NO. 1, 1980.

163

Figure l. — Photograph of regener-
ating caudal fin, 1 wk after amputa-
tion. Measurements were made at A
toB.

mm _

dard length (SL) to 0.05 ppm methylmercury, 1.0,
3.0, or 10.0 ppm zinc or combinations of 0.05 ppm
methylmercury with 1.0, 3.0, or 10.0 ppm zinc.
Experiment II was similar, but used 0.025 ppm
methylmercury and fish 4.1-5.2 cm SL. Experi-
ment III used 0.05 ppm methylmercury and the
same concentrations of zinc, but was performed in
water of reduced salinity (10%o) on fish 4.3-5.1
cm SL.

Fish were frozen at the end of some experi-
ments and later analyzed for metal uptake by
atomic absorption spectrophotometry (cold vapor
technique for mercury, flameless atomic absorp-
tion spectrophotometry for zinc). These analyses
can be considered accurate within 10%.

Results

Table l. — Analysis of variance on effects of methylmercury
and zinc on fin regeneration in Fundulus heteroclitus.

Source of variation

df

SS

MS

Hg

Zn

Hg X Zn

24.778
2.200
0.411

24.778
0.733
0.137

173.671
5.139
0.960

0.001
0.003
0.416

Table 2. — Growth of tail regenerates in Fundulus heteroclitus
e5q)osed to methylmercury and zinc for 14 days in Experiment II
and 11 days in Experiment III.

Experiment II

E:

xperiment III

Exposure

n

mm ±SE

n

mm ±SE

Controls

12

3.62±0.078

12

2. 28^0.069

meHg

15

3.31 ±0.128*

8

1,67±0.125-

meHg + 1 ppmZn

12

3.59±0.099

7

1. 82 ± 0.094*

meHg + 3 ppm Zn

13

3.49±0.116

2

2. 14 ±0.060

meHg + 10 ppmZn

12

3.50^0.084

1

2.24±0.00

1 ppm Zn

13

3.73±0,144

11

2. 43 ±0.098

3 ppm Zn

14

3.86i0.142

9

2.44±0.111

lOppmZn

10

4.18±0.159*

2

2.46±0.020*

*Significantly different from controls (P<0.05) by (-test.

In Experiment I, caudal fin regeneration was
retarded by methylmercury and was accelerated
by zinc in a dose-dependent fashion. The retarda-
tion produced by the mercury could be partially
counteracted by the zinc (Figure 2). Analysis of
variance of day 14 (Table 1) showed significant
effects of mercury, and of zinc, but not of interac-
tion.

Experiment II, using 0.025 ppm methylmer-
cury, produced similar results (Table 2). It can be
seen that zinc again accelerated growth in a
dose-dependent manner and counteracted the
methylmercury-caused depression of growth.
Only the group in methylmercury alone and the

group in 10 ppm zinc were significantly different
from controls (P^0.05) as determined by the
^-test.

In Experiment III (10%o salinity) a similar pat-
tern was seen (Table 2). High mortality due to
interruption in air supply caused the experiment
to be terminated early. The groups in methylmer-
cury, methylmercury + 1 ppm zinc, and in 10
ppm zinc were significantly different from con-
trols, as seen by the ^-test.

Analysis of mercury uptake revealed consider-
able variation (Table 3). However, it seems likely
that the tissue residues are dose dependent and
that zinc does not change the uptake of mercury

164

4r

E
E

c

a>

11

14

Days

Figure 2. — Regenerative growth of tail fin of Fundulus heter-
oclitus exposed to methylmercury and zinc in seawater, Exper-
iment I.

Key: A 10.0 ppm Zn (n = 15), V 3.0 ppm Zn(n = 15), D 1.0 ppm
Zn (« = 15), C Control in = 14), A 0.05 ppm meHg + 10.0 ppm
Zn {n = 11), ▼ 0.05 ppm meHg + 3.0 ppm Zn {n = 12), ■ 0.05
ppm meHg + 1.0 ppm Zn in = 9), • 0.05 ppm meHg (n = 12).

Table 3. — Average mercury uptake (ppm Hg/wet weight ± SE)
by Fundulus heteroclitus.

Control

Hg

Hg + 10 ppm Zn

Item

Uptake

n

Uptake

n

Uptake n

Experiment 1:

Carcass

n.d.'

3

32-5.0

3

37 = 7.2 3

Brain

n.d.

3

11=0.9

3

19 = 4.8 4

Experiment II:

Carcass

n.d.

3

7.4=0.7

3

15.4 = 3.1 5

Brain

n.d.

3

4.8=26

3

9.7 = 1.6 5

Experiment III:

Carcass

n.d.

3

33 = 12

3

25=1.4 3

Brain

n.d.

3

28 = 6.0

3

25±2.5 3

'n.d. = not detectable, <0.03ppm.

into the brain or the rest of the body. Accumula-
tion of zinc was not altered by methylmercury.
Animals in 10 ppm Zn accumulated 246±1.41
ppm; those in 10 ppm Zn + 0.05 ppm meHg ac-
cumulated 250±3.54 ppm. Those in 1 and 3 ppm
Zn accumulated 221±25.2 and 250±4.95 ppm,
showing no clear dose-dependent relationship.

Discussion

The data indicate that in F. heteroclitus, zinc
can accelerate regenerative growth, and, by so
doing, can counteract the retarding effects of
methylmercury. In this species, the regeneration
rate of controls was similar in 30%o and 10%o sa-
linity, and the methylmercury retarded growth at
both salinities. This is in contrast to F. confluen-
tus in which decreased salinities depressed the
regeneration rate, thus masking the effects of
methylmercury in water of 9%o salinity (Weis and
Weis 1978).

Methylmercury has previously been observed to
retard regeneration (Chang et al. 1976; Weis and
Weis 1978) and other developmental processes
(Chang et al. 1974). Its action as an inhibitor of
mitosis (Ramel 1969) could be the cause of these
effects on growth processes. As a potent nerve
poison it could further inhibit regenerative
growth by interfering with the neurotrophic
influence necessary for regeneration.

Previous studies on the effects of zinc on grov^dh
include the work of Hirsch and Hurley (1978) in
which zinc was found to counteract the
teratogenic effects of 6-mercaptopurine in the rat.
They felt that the drug lowered DNA synthesis
and that the zinc counteracted this. Swenerton et
al. (1969) correlated zinc deficiency with reduced
DNA synthesis in rat embryos, and Falchuck et
al. (1975) have associated zinc with promoting cell
division in Euglena gracilis. Thus, if zinc can
promote DNA synthesis and cell division in fish
also, that would account for the observed acceler-
ation of regenerative growi:h. However, previous
studies on fish have not indicated such an effect.
Crandall and Goodnight (1962) reported that 1.15
ppm zinc retarded the growth of newborn gup-
pies. Rachlin and Perlmutter (1969) found that 18
ppm Zn reduced the mitotic index of cultured
rainbow trout, Salmo gairdneri, cells, but that
1.8-10.0 ppm had no effect on the mitotic index.

On the other hand, zinc has often been found to
counteract toxic effects of other heavy metals.
Dixon and Compher (1977) found that zinc could
reverse a cadmium-caused inhibition of regenera-
tion in the nevft. Zinc has been found to coun-
teract the toxic effects of mercury in rats
(Yamane et al. 1977) and to counteract the
teratological effects of methylmercury in killifish
embryos (Weis et al. in press).

In view of reports of fin rot of unknovvTi etiology
in flatfish from polluted environments (Ziskowski

165

and Murchelano 1975), the retardation of growth
by heavy metals may be of significance in inhibit-
ing regeneration of fins eroded by the benthic
substrate.

Addendum

It has recently been demonstrated that, in cer-
tain poeciliid fishes, some environmental vari-
ables which affect general growth rate do not af-
fect the rate of fin regeneration. Factors which do
cause differences in length of regenerated fin
generally affect the time needed for wound heal-
ing and blastema formation, rather than rates of
regeneration per se (E. Zimmerer, Ph.D. disserta-
tion, Rutgers University, 1980). We tested the
data represented in Figure 1 for this possibility.
In regression analysis, the slope equals regenera-
tive rate per se and the elevation (^'-intercept)
represents the time needed for wound healing
and blastema formation. Analysis of covariance
indicates that when Hg treated fish are compared
with control fish, both the slopes and j -intercepts
are significantly different {F = 10.23 and 80.76,
respectively). Similarly, when 10 ppm Zn treated
and control fish are compared, the slopes and
^/-intercepts are significantly different {F = 6.83
and 41.29, respectively). Therefore, it appears
that these heavy metals affect both the initial
wound healing and blastema formation and the
rate of regeneration per se.

Acknowledgments

This work is a result of research sponsored by
NOAA Office of Sea Grant, U.S. Department of
Commerce, under grant No. 04-7-158-44042.
Thanks are extended to J. C. Baiardi of the New
York Ocean Science Laboratory for the use of
facilities for this study, and to J. Seebode Jr., J.
Ricci, and G. Millinger for technical assistance.
We thank S. L. Cheng of the New Jersey Institute
of Technology for the atomic absorption spec-
trophotometry, and J. Chou of the College of
Medicine and Dentistry of New Jersey for statis-
tical assistance.

Literature Cited
Chang, L. W., l. M. Mak, and a. h. Martin.

1976. Dose-dependent effects of methylmercury on limb
regeneration of newts (Triturus viridescens). Environ.
Res. 11:305-309.

Chang, L. W., K. R. Reuhl, and a. W. Dudley, Jr.

1974. Effects of methylmercury chloride on Rana pipiens
tadpoles. Environ. Res. 8:82-91.

Crandall, C. a., and C. J. Goodnight.

1962. Effects of sublethal concentrations of several toxi-
cants on growth of the common guppy, Lebistes re-
ticulatus. Limnol. Oceanogr. 7:233-239.
DIXON, C, AND K. COMPHER.

1977. The protective action of zinc against the deleterious
effects of cadmium in the regenerating forelimb of the
adult newt, Notophthalmus viridescens. Growth
41:95-103.

Falchuck, K. H., D. w. Fawcett, and B. L. Vallee.

1975. Role of zinc in cell division of £ug/en<i graci/is. J.
Cell Sci. 17:57-78.

HiRSCH, K. S., AND L. S. Hurley.

1978. Relationship of dietary zinc to 6-mercaptopurine
teratogenesis and DNA metabolism in the rat. Teratol-
ogy 17:303-314.

RACHLIN, J. W., AND A. PERLMUTTER.

1969. Response of rainbow trout cells in culture to
selected concentrations of zinc sulfate. Prog. Fish-Cult.
31:94-98.
RAMEL.C.

1969. Genetic effects of organic mercury compounds. I.
Cytological investigations on Allium roots. Hereditas
61:208-230.

Swenerton, H., R. Shrader, and l. S. Hurley.

1969. Zinc-deficient embryos: reduced thymidine incorpo-
ration. Science (Wash., D.C.) 166:1014-1015.

WEIS, J. S., P. WEIS, AND J. L. RICCI.

In press. Effects of cadmium, zinc, temperature, and sa-
linity on the teratogenicity of methylmercury to the kil-
lifish, Fundulus heteroclitus . In Second International
Symposium on the Early Life History of Fishes, spon-
sored by International Council for the Exploration of the
Seas, Woods Hole, Mass., April 2-5, 1979.

WEIS, P., AND J. S. WEIS.

1976. Effects of heavy metals on fin regeneration in the
killifish, Fundulus heteroclitus. Bull. Environ. Contam.
Toxicol. 16:197-202.

1978. Methylmercury inhibition of fin regeneration in
fishes and its interaction with salinity and cad-
mium. Estuarine Coastal Mar. Sci. 6:327-334.
YAMANE, Y., H. FUKINO, and M. IMAGAWA.

1977. Suppressive effect of zinc on the toxicity of mer-
cury. Chem. Pharm. Bull. (Tokyo) 25:1509-1518.

ZlSKOWSKI , J. , AND R. MURCHELANO.

1975. Fin erosion in winter flounder (Pseudopleuronectes
americanus) from the New York Bight. Mar. Pollut.
Bull. 6:26-28.

Peddrick Weis

Department of Anatomy
New Jersey Medical School
Newark, NJ 07103

Judith Shulman Weis

Department of Zoology and Physiology
Rutgers, the State University
Newark, N J 07102

166

SOUTHERN DISTRIBUTION OF

THE ATLANTIC WHITESIDED DOLPHIN,

LAGENORHYSCHUS ACUTUS, IN

THE WESTERN NORTH ATLANTIC

Two mass strandings of the Atlantic whitesided
dolphin, Lagenorhynchus acutus, in New
England— Wellfleet, Mass., 11 May 1973 and Ed-
munds, Maine, 6 September 1974 — initiated in-
vestigation at the New England Aquarium, Bos-
ton, into this species' life history and pathobiology.
Previous distribution records for this species in
the United States were reported by Cope (1876),
True ( 1885, 1889), and Schevill ( 1956). Most refer-
ences define this dolphin's southern distribution
as Cape Cod, Mass. We believe this is based on a
206 cm female reported to have been collected near
Portland, Maine, and described by Cope ( 1876) as
L. perspicillatus (= L. acutus). Norton (1930) re-
described the correct collecting site as Cape Cod.

The first confirmed Cape Cod report, although
not a stranding, was on 14 September 1954 when a
school sighting and harpooned specimen were re-
ported by Schevill (1956). This school, about 12
animals, was located 93 km east of Cape Cod in
water 145 m deep (Figure 1, number 3).

The following accounts, arranged in chronologi-
cal order, update our present knowledge of this
species' southernmost known occurrence in the
western North Atlantic. Information is based
upon stranding records of the Smithsonian In-
stitution and the New England Aquarium, along
with an examination of the collections of the
American Museum of Natural History, New York,
N.Y.; Academy of Natural Sciences, Philadelphia,
Pa.; U.S. National Museum, Washington, D.C.;
and the Museum of Comparative Zoology, Har-
vard University, Cambridge, Mass. Paragraph
numbers below correspond to locality numbers in
Figure 1 and to reported body measurements
given in Table 1. Abbreviations for collection
numbers are as follows: MCZ = Museum of Com-
parative Zoology, Harvard University, NEA =
New England Aquarium, USNM = U.S. National
Museum.

1. One male (USNM 22934) captured by the
U.S. Fisheries schooner Grampus 20 mi (37 km)
south of Montauk, Long Island, N.Y. (lat. 40°38'
N, long. 71°49' W), 19 May 1888. This specimen
was reported to have been captured from a school
of about 100 animals.

FISHERY BULLETIN; VOL. 78, NO. 1. 1980.

O Sighting

• Single st randing

A Sighting plus

captured specimens

Figure l. — Southernmost east coast locations of known Atlan-
tic whitesided dolphin sightings. Nximbers refer to specimens
described in Table 1 and in text.

2. One female (USNM 22942), also captured
by the Grampus, taken south of Cape Cod Islands
(lat. 40°43' N, long. 70°32' W). No date recorded
but because of its proximity to the prior animal's
catalog number, we believe this animal was taken
on the same cruise.

3. One female (MCZ 48548) harpooned from a
small school off Cape Cod (lat. 41=35' N, long.
68=55' W), 14 September 1954 (Schevill 1956).

4. One skull (MCZ 48549) collected during the
winter 1954-55 at South Beach, Martha's Vine-
yard, Mass.

5. One specimen washed ashore live at Ocean
Beach, Fire Island, Long Island (lat. 40=39' N,
long. 73°09' W), April 1971. Length estimated at
about 7.5 ft (229 cm), sex undetermined. Skull
measurements: condylobasal length, 391 mm; ros-
trum length, 196 mm; tooth width, up to 4 mm;

33-

dental formula

34-34

167

TABLE 1.— Selected Iwdy measurements, nearest whole centimeter, of Lagenorhynchus acutus from the .southernmost known occur-
rences in the western North Atlantic. Data in parentheses converted from English to metric. Doubtful measurements were not included.
Localities are given in Figure 1 and text. ^

Percentage oi

Locality number and sex

Range

total lengt^

1

Measurement

KM)

2(F)

3(F)

7(M)

9(F)

10(F)

11(M)

12(-)

Range

Mean

Snout to:
Notcti. total length

(150)

(209)
(38)

(137)

225
40

233
32

165
18

224
35

202
30

(241)
(41)

150-241
18-41

10.9-18.2

15.4

Flipper

Tip of dorsal fin

Genital slit

Anus

(109)

87
4

88
153

5
28
23
37

93

112

118

3

119

157

165

5

112

125

141

5

(173)
(182)

87-119

112-173

109-182

3-5

37.8-564

61.9-71 8

69.8-755

1 8-2.5

483

67.2

72.6

2.1

Apex of melon
Center of eye
Angle of mouth
Ear

(22)
(19)

(25)

22

17
16

25

21
33

24
20
29

—

22-28
17-25
16-37

11.2-14.7
9.4-12.7
9.7-15.9

12.6
10.7
13.7

Girth:

Maximum
At axilla
At eye

—

—

—

103
85

91
84

119
106

121
108

—

91-121
84-108

43.8-599
42.1-53.5

530
484

—

—

—

82

68

80

80

—

68-82

35.2-41.2

37.9

Flipper lengths:
Anterior

(24)

(32)

_

34

25

34

28

(36)

24-36

13.9-15.3

15.0

Posterior
Maximum flipper width
Dorsal fin height
Fluke width

25

23

16

25

20

(24)

16-25

9.7-11.2

10.3

(8)
(15)
(35)

(12)
(22)
(57)

24
65

14
55

9
12
36

12
25
55

11
18
43

(13)
(22)

8-14
12-25
35-65

5.3-6.0

7.3-10.7

21 3-28 9

5.5

9.7

244

30-30

30-30

31-29

30-32

33-30

Number of visible teeth

~

31-32

30-30

32-31

30-30

32-31

6. One specimen, length and sex unknown,

found along Patchogue, Long Island ( lat. 40°43' N,

long. 72°57' W), December 1973. Only the head

and the tail were recovered. Estimation of total

length from photographs is 160 cm. Tooth count

-25
from visible teeth was .

-31

7. One dead male found in surf line at Village

Beach, Village of Westhampton Beach, Long Is-
land (lat. 40°48' N, long. 72°38' W), 1 May 1974.
Currently, the skeleton is on display at the New
York Ocean Science Laboratory, Montauk, Long
Island.

8. Decayed carcass of a 150 cm individual
(skull USNM 504292), sex indeterminate, was
examined on the southeastern corner of Pasque
Island, Mass., Nantucket Sound (lat. 41°26' N,
long. 70°51' W), 5 July 1975. According to resi-
dents, this animal had stranded 2 or 3 mo earlier
thereby placing the stranding date in April or
May.

9. A female (NEA MH7622) found live and
later died on the southern side of Nantucket Is-
land, Mass. (lat. 40°14' N, long. 70°00' W), 15
February 1976.

10. A female (NEA MH7670), 127.6 kg,
stranded alive and later died at Marion, Mass.
(lat. 41°42' N, long. 70°46' W), 28 April 1976.

11. One dead male (NEA MH7672), 109 kg,
found on the eastern edge of Easten's Beach, New-
port, R.I. (lat. 41°29' N, long. 71°17' W), 1 May
1976.

12. One decayed specimen (NEA MH76129),
sex unknown, thought to have stranded during
spring 1976. Found early May on the outer side of
Cuttyhunk Island, Nantucket Sound, Mass. (lat.
41°25'N, long. 70°56'W).

13. Three 1976 sightings reported southeast of
Cape Cod along the southeast edge of Georges
Bank by the NOAA Ship Albatross IV , fall survey
76-09:

a. School of 15-20 animals, lat. 41°13' N,
long. 66°15"W, 27 March.

b. Two animals, lat. 40°10' N, long. 67°12' W,
2 April.

c. Five animals, lat. 40°26 ' N, long. 67°03 ' W,
2 August.

14. Four sightings on 2 January 1977 during
U.S. Coast Guard aerial overflights during the
Argo Merchant Oil Spill (Grose and Mattson^):

a. Two animals, lat. 40°21 ' N, long. 66°58 ' W.

b. One animal, lat. 39°29' N, long. 68°20' W.

c. One animal, lat. 40°34' N, long. 66°36' W.

d. One animal, lat. 40°30' N, long. 68°03' W.

15. One female, 248 cm, stranded dead about
2.4 km south of the Virginia-Maryland border on
Chincoteague National Wildlife Refuge in Vir-
ginia (lat. 38°02' N, long. 75°18' W), 27 May 1977.

16. A freshly stranded male animal, 234 cm,
found at Deerfield Lane Beach, Amagonsett, Long

iGrose, P. L., and J. S. Mattson. 1977. The ARGO MER-
CHANT Oil Spill — A preliminary scientific report. U.S. De-
partment of Commerce, Washington, D.C., Special Report, 323 p.

168

Island (lat. 41°00' N, long. 72°05' W), 30 August

1978.
17. On Nantucket Island, Eel Point (lat. 41°17'

N, long. 70°05' W), approximately 200 cm speci-
men (NEA MH78143), sex unknown. The strand-
ing took place on 4 September 1978.

The Virginia stranding extends the southern
distribution approximately 700 km southwest of
Schevill's (1956) sighting. These reportings south
of lat. 41° N indicate that the range of the Atlantic
whitesided dolphin is farther south than the Cape
Cod area thus extending the range into the Middle
Atlantic Bight.

There were two previous published records
which had placed this species farther south than
Schevill's reporting; however, these appear to be
erroneous. True (1885) reported a series of skulls of
L. perspicillatus (= L. acutus) taken in a net
fishery at Fort Macon, N.C. That collection of
skulls, now in the USNM, were examined and
determined to be bottlenosed dolphin, Tursiops
truncatus (Mead 1975). Rhoads (1903) listed L.
acutus as possibly occurring off the coast of New
Jersey based upon an illustration in Godman
( 1828). An examination of the original illustration
indicates that the species depicted was a common
dolphin, Delphinus delphis.

These occurrences, as far south as the
Chesapeake Bight, indicate the southernmost
known extent of the Atlantic whitesided dolphin
distribution along the western North Atlantic. It
appears from this information that the Atlantic
whitesided dolphin has a peak occurrence in the
Mid-Atlantic Region during spring and summer.

This work was supported in part by the U.S.
Marine Mammal Commission, Contract Number
MM5AC008 with the New England Aquarium.

Acknowledgments

The authors wish to express their gratitude to
W. E. Schevill, Woods Hole Oceanographic In-
stitution, for stranding data from the MCZ. We
especially thank P. Connor, New York State
Museum, and A. Cooley, Bellport High School,
Bellport, Long Island, N. Y., for their contributions
of Long Island stranding information. We thank
E. E. Britton, Chincoteague National Wildlife
Refuge for the information of the Virginia strand-
ing and G. K. Mahoney, Fisheries Management
Division, NMFS, NCAA, for his constructive criti-
cism.

Literature Cited
Cope, e. d.

1876. Fourth contribution to the history of the existing
Ceatacea. Proc. Acad. Nat. Sci. Phila., Ser. 3, 28:129-
139.

Godman, J. J.

1828. American natural history. Vol. HI, Part 1, Mas'^lo-
gy. Carey, Lea and Carey, Phila., 264 p.
MEAD, J. G.

1975. Preliminary report on the former fisheries for Tur-
siops truncatus in the western North Atlantic. J. Fish.
Res. Board Can. 32:1155-1162.

Norton, a. h.

1930. The mammals of Portland, Maine, and vicini-
ty. Proc. Portland Soc. Nat. Hist. 4, 155 p.
RHOADS, S. N.

1903. The mammals of Pennsylvania and New Jer-
sey. Privately published, Phila., 206 p.
SCHEVILL, W. E.

1956. Lagenorhynchus acutus off Cape Cod. J. Mammal.
37:128-129.

True, f. w.

1885. The porpoise fishery of Hatteras, N.C. Bull. U.S.

Fish. Conun. 5:3-6.
1889. A review of the Family Delphinidae. Bull. U.S.

Natl. Mus. 36, 191 p.

Salvatore a. Testa VERDE

New England Aquarium

Boston, Mass.

Present address: Fisheries Management Division

National Marine Fisheries Service, NOAA

State Fish Pier, Gloucester, MA 01930

James G. Mead

Division of Marine Mammals
Smithsonian Institution
Washington, DC 20560

ADDITIONAL RECORDS OF THE SCULPIN

PSYCHROLUTES PHRICTUS IN THE EASTERN

BERING SEA AND OFF OREGON

Psychrolutes phrictus Stein and Bond is an unusu-
ally large Psychrolutes known heretofore from
deep water between Monterey, Calif., and north-
ern Oregon. The species can be distinguished from
its only congener, P. paradoxus, by differences in
relative head length, gill raker and pectoral fin
ray counts, and the presence of small cirri on both
head and body. Recent collections in the Bering
Sea and off Oregon supplement the type-
description and contribute new information on
range and early life history.

During a 2-mo period (summer 1978), while a
member of the foreign fisheries observer staff of

fishery BULLETIN: VOL. 78, NO. 1, 1980.

169

the National Marine Fisheries Service, Colin Lau^
subsampled trawl catches northwest of Unalaska
Island on the Japanese fishing vessels Tomi Maru
No. 53 and Eikyu Maru No. 12. Lau often noticed a
cottidlike fish that he was unable to identify with
certainty. Two specimens of this fish, which he
preserved, were accessed into the University of
Washington fish collection and later identified by
the authors as P. phrictus. Collection data for the
two specimens (UW 20762 and 20763) and for two
pelagicjuveniles (OSUO 2437 and 2438), obtained
in an opening-closing midwater trawl off Oregon
(Pearcy et al. 1977), are given in Table 1.

■Colin Lau, College of Fisheries, University of Washington,
Seattle, WA 98195, pers. commun. October 1978.

Confirmation of the identity of these four speci-
mens was made by comparisons with the meristic
and morphometric characters used in the original
description (Table 2). Methods for counting and
measuring are as in Hubbs and Lagler (1964);
measurements were taken to the nearest 0.1 mm
with dial calipers; unpaired fin rays and vertebrae
were counted on radiographs. These specimens
were slightly different from those previously
available. The larger specimen from the Bering
Sea (UW 20763) has an additional caudal vertebra
that may have resulted from development in
colder waters. The two juveniles from off Oregon
have relatively larger heads than reported
previously — evidence of the allometry described
by Stein and Bond (1978).

Table l. — Collection data for Psychrolutes phrictus in the eastern Bering Sea and off Oregon, 1978.

Position

Specimen source

Date

Lat. N

Long. W

Haul Psychrolutes phrictus Subsample

depth (m) Number Weight (l<g) weight (l<g)

Tomi Maru No. 53

19 June

54^31 ■

167''35'

790

1 —

—

25 June

54°29'

16r'25'

685

1 —

—

25 June

54°26'

167°30'

740

—

—

26 June

54"'41 '

167°32'

680

1 —

—

26 June

54°38'

167°29'

660 1

—

—

2 July

54°20'

167°22'

900

—

—

Eikyu Maru No. 12

13 July

54°22'

166°55'

868

5.0

94.7

20 July

54°18'

167°08'

1,240

1 3.5

118.2

21 July

54°21 '

166°50'

925

7.7

135.2

22 July

54°20'

166°53'

1 ,050

5.4

131.1

22 July

54°20'

166°5r

940

8,0

119.2

25 July

54°20'

166°52'

850 2

0.3

96.0

26 July

54° 19'

166^52 '

925 '

^ 11.4

139.1

26 July

54°15'

167°07'

1,320

4.6

133.3

28 July

54°22'

166'55'

865

7.9

132.2

OSUO* 2437

1 Sept.

44°47'

125°50'

495-505 1

—

—

OSUO 2438

2 Sept.

44°37'

125°43'

480-540

—

—

'University of Washington (UW) collection, Seattle, Wash.; (preserved] specimen UW 20762.

^[Preserved] specimen UW 20763.

^Oregon State University Oceanography (OSUO) collection, Corvallis, Oreg.

Table 2. — Meristic and morphometric (measurement in millimeters and percentage within parentheses) characters
of Psychrolutes phrictus from the eastern Bering Sea and off Oregon.

Stein and Bond

Item

UW 20762

UW 20763

OSUO 2438

OSUO 2437

(1978)'

Standard length, mm

113

126

28

30

Fin rays:

Dorsal

VIII, 20

VIII, 20

VIII, 19 or 20

VIII, 19

VII-IX, 19-20

Anal

13

13

13

13

12-14

Pectoral

23

23

24

23

22-26

Pelvic

1,3

1,3

1,3

1,3

1,3

Principal caudal

11

11

11

11

About 13

Gill rakers

11

9

29

29

9-13

Vertebrae:

Total vertebrae

35

36

34

35

33-35

Precaudal

12

12

13

13

Caudal

23

24

21

22

—

Head length^

46.4(41)

65,7(52)

15.9(55)

15.3(48)

(43.5-60.6)

Eye length"

9.6(21)

9.9(15)

3.2(20)

3.4(22)

(8.6-24.3)

Pectoral fin length"

30.2(65)

34.1(52)

7.6(48)

8.0(52)

(44 9-62.3)

Pelvic fin length"

10.2(22)

20.3(31)

4.0(25)

4.8(31)

(23.3-34.7)

Preanal length"

59.8(129)

75.1(114)

15.4(97)

12.7(83)

(93.8-132.2)

'Ranges for data in the

original description.

^May be incomplete.

^Percentage is proportion of standard length.

"Percentage is proportion of head length.

170

Lau's observations on relative abundance of P.
phrictus indicate that this species may constitute
a significant portion of the demersal fish biomass
in the area of the Bering Sea where he sampled.
During a sampling period from 12 to 31 July, 76
hauls were taken, of which 38 were subsampled.
Psychrolutes phrictus was present in subsamples
from 9 of these 38 hauls and ranked 6 of 44 species
found, based on weight. When individuals were
present in subsamples of the catch, they rep-
resented 0.3-8.2% of the subsample weight (Table
1) and 1.8% ofthe overall subsample weight for the
sampling period. Individuals were also observed
casually in hauls where they were not part of the
subsample.

The capture of two juveniles off the Oregon coast
about 2,500 m above the bottom and about 65 km
west ofthe lower continental slope is evidence that
the larvae and juveniles are pelagic. Whether
juveniles normally occur so far offshore, and if so,
whether such individuals survive to reach the bot-
tom, is not known. Psychrolutes phrictus probably
leaves the pelagic zone and becomes demersal at
about 30 mm. The rationale for this is that the
juveniles (28 and 30 mm) reported here were
pelagic, whereas those (30 and 49 mm) reported by
Stein and Bond (1978) were benthic.

Literature Cited

HUBBS, C. L., AND K. F. LAGLER.

1964. Fishes of the Great Lakes Region. Revised
ed. Univ. Mich. Press, Ann Arbor, Mich., 213 p.
Pearcy, W. G., E. E. Krygier, R. Mesecar, and F. Ramsey.

1977. Vertical distribution and migration of oceanic mi-
cronekton off Oregon. Deep-Sea Res. 24:223-245.

Stein, D. L., and C. E. Bond.

1978. A new deep-sea fish from the eastern North Pacific,
Psychrolutes phrictus (Pisces: Cottidae [Psychro-
lutinae]). Nat. Hist. Mus. Los Ang. Cty., Contrib. Sci.
296, 9 p.

ANN C. MATARESE

Northwest and Alaska Fisheries Center
National Marine Fisheries Service, NOAA
2725 Montlake Boulevard East
Seattle, WA 98112

School of Oceanography
Oregon State University
Corvallis, OR 97331

David L. Stein

A RECURRENT MASS STRANDING OF

THE FALSE KILLER WHALE,

PSEUDORCA CRASSIDENS, IN FLORIDA

The false killer whale, Pseudorca crassidens, is
one of the several species of odontocetes known
primarily through its relatively frequent mass
strandings. These strandings offer a large amount
of natural history data but, in most cases, inves-
tigators have been unable, for various reasons, to
thoroughly study these events. As a result, very
few data are available on the natural history of
P. crassidens (Mitchell 1975a, b; Purves and Pil-
leri 1978). Pseudorca crassidens is distributed
worldwide in temperate and tropical waters
(Mitchell 1975b), and frequently strands in large
numbers (Norman and Fraser 1948; Dudok van
Heel 1962), exceeding 800 in one case (Marelli
1953; Tomilin 1957; Reiger 1975). The series ofP.
crassidens mass strandings we describe herein is
the third in Florida in recent years. Caldwell et al.
(1970) reported a stranding of 150-175 false killer
whales near Ft. Pierce on the Atlantic coast of
Florida in January 1970. Little data was collected
and most ofthe animals were apparently buried on
the beach. A heretofore unreported stranding oc-
curred on 18-19 July 1972 on the northeast end of
Sawyer Key (lat. 24°45.6' N, long. 81°33.4' W) in
the lower Florida Keys on the Florida Bay (Gulf of
Mexico) side. This site is approximately 35 km
northeast of Key West (Figure 1). Nineteen ani-
mals were involved. Gordon Hubbell^ estimated
the largest animals to be 460 cm (15 ft) long. He
measured a 320 cm ( 10.5 ft) male, a 376 cm (10.3 ft)
female, and a 427 cm (14.0 ft) female.

Sequence of Events

1. The Florida Marine PatroP reported a whale
stranding near North Captiva Island on the
southwest coast of Florida (Figure 1) on the morn-
ing of 22 July 1976. We found a dead 440 cm
female false killer whale at Redfish Pass (Figure
2) and four live females aground on a sandbar in
Pine Island Sound (Figure 2). We necropsied the
dead animal on the beach and transported the live
animals to Sea World, Orlando, Fla., on 22 July.
At least 29 false killer whales had entered Pine
Island Sound: 1 died; 4 were stranded alive; 24

^Gordon Hubbell, Director, Crandon Park Zoo, Miami, Fla.
33149, pers. commun. 1977.

^Florida Marine Patrol, Officer in Charge, Ft. Myers Office,
pers. commtm. July 1976.

FISHERY BULLETIN: VOL. 78, NO. 1. 1980.

171

i ^^ MARQUESAS

DRY •• ^°°
T0RTU6AS '-k'F

KEY WEST

50 km

X

Figure l. — Outline map of south Florida indicating principal
stranding sites and possible routes of travel of the false killer
whale herd. Fort Pierce is located just north of lat. 27° N on the
east coast of the state. Box represents region covered by succeed-
ing figure.

were photographed exiting Captiva Pass (Lar-
son^). All moved northward in or near the In-
tracoastal Waterway after entering Pine Island
Sound via Redfish Pass. They continued north-
ward and returned to the Gulf of Mexico via Cap-
tiva Pass (Florida Marine Patrol see footnote 2;
Larson see footnote 3) (Figure 2). The animals
originally entered Redfish Pass at about 0830 h.
The tide was rising and near the high point
(Florida Marine Patrol see footnote 2). The exact
time, and thus tidal conditions when the animals
exited Captiva Pass are unknown to us. It is in-
teresting to note that a spinner dolphin, Stenella
longirostris, herd stranded on Casey Key (lat.
27°12'10" N, long. 82°30'30" W) 7 days earlier
(Mead et al.'*). This site is about 75 km north of
North Captiva.

='Peter Larson, Sanibel Island Reporter, Sanibel, Fla., pers.
commun. 1976.

"Mead, J. G., D. K. Odell, R. S. Wells, and M. Scott.
1978. Biological observations on a mass stranding of spinner
dolphins (Stenella longirostris) from the west coast of Flori-
da. Unpubl. manuscr. Division of Mammals, Smithsonian In-
stitution, Washington, DC 20560.

172

GULF

MEXICO

5 km

I 1

Figure 2. — North Captiva Island and vicinity, south Florida,
indicating Redfish Pass and Captiva Pass where the false killer
whales entered and exited Pine Island Sound. The four females
taken to Sea World stranded on a sand bar located off the south-
east side of North Captiva (indicated by an arrow). Intracoastal
waterway is indicated by dashed line in Charlotte Harbor and
Pine Island Sound.

2. A herd of 30 false killer whales stranded on
Loggerhead Key, Dry Tortugas (Figure 1), at ap-
proximately 1300 h on 25 July on a falling tide.
This site is some 235 km south of North Captiva
Island. The herd was divided into two groups at
the time of stranding (Shinn^). The animals were
pushed back into the water and kept wet by U.S.
Coast Guard and National Park Service person-
nel. We measured and sexed the animals and
photographed their dorsal fins and flukes for indi-
vidual identification of the animals on 26 July. We
repeated the measurements and photographs, col-
lected blood samples and marked each animal
with a spaghetti tag (Floy Tag FD-68B^ anchor

*Eugene Shinn, U.S. Geological Survey, Miami, Fla., pers.
commun. 1976.

*Floy Tag & Manufacturing Inc., Seattle, Wash. Reference to
trade names does not imply endorsement by the National Marine
Fisheries Service, NOAA.

tag) on 27 July. A 520 cm male died prior to an
attempt to return all of the animals to offshore
waters. A group effort by Park Service, Florida
Marine Patrol, Coast Guard, and other personnel
successfully forced the remaining 29 out to sea.
Color photographs and a popular description of
this stranding are given by Porter (1977).

3. On 2 August, National Park Service person-
nel found three shark-eaten P. crassidens carcas-
ses floating about 2 km off Cape Sable (Figure 1).
They towed these to shore and Odell examined
them on 3 August.

4. On 23 August, Odell salvaged 20 P. crassi-
dens skulls from carcasses discovered on Cape
Sable by the National Park Service on 18 August.
The whales were severely decomposed when first
discovered and had probably been on the beach for
at least 2 wk. Sex determination and external
measurements were not possible (Odell and
Asper^; Odell et al.^).

Results and Discussion

We measured 29 of the 30 whales that stranded
on Loggerhead Key (total length only). The mean
length (±SD) of 12 males was 458±48 cm, range
377-534 cm and 17 females was 416 ±39 cm, range
328-494 cm. The mean lengths were significantly
different at the 0.01 level. The weight-length data
(250 kg, 297 cm; 327 kg, 338 cm; 359 kg, 358 cm;
773 kg, 475 cm) from the four live females that we
collected at North Captiva Island yielded the fol-
lowing predictive allometric equation corrected
for log transformation bias (Beauchamp and Olson
1973): W = 2.16 x lO'^L^^^^^ where Wis weight in
kilograms andL is length in centimeters.

The length exponent in the above equation is
low when compared with similar equations for
several other marine mammals. Bryden (1972)
summarized the weight- length relationships for a
number of marine mammals. The length expo-
nents for several cetaceans are: Delphinapterus

''Odell, D., and E. Asper. 1977. A summary of information
derived from a mass stranding of P. crassidens in Florida, 1976.
(Abstr.) Marine Mammal Stranding Workshop, Athens, Ga.,
10-12 August, 1977, p. 20-21. U.S. Marine Mammal Commission
contract MM7AC020.

«Odell, D. K., E. D. Asper, J. Baucom, and L. H. Cor-
nell. 1979. A summary of information derived from the re-
current mass stranding of a herd of false killer whales,
Pseudorca crassidens (Cetacea: Delphinidae). In J. R. Geraci
and D. J. St. Aubin (editors). Biology of marine mantmials: in-
sights through strandings, p. 207-222. Final Rep., U.S. Marine
Mammal Commission contract MM7AC020. Available Natl.
Tech. Inf. Serv., Springfield, Va., as PB 293380.

leucas — two populations, males, 2.536 and 2.605
(Sergeant and Brodie 1969); Globicephala
melaena — 2.895; Balaenoptera musculus — 3.25
(Ash 1952); B. physalus— 2.9 (Ash 1952); B.
borealis — two populations, 2.43 and 2.74 (Omura
1950; Fujino 1955); and Megaptera novae-
angliae— 3.1 (Ash 1953). The mean ( ±SD) of these
eight length exponents is 2.807 ±0.283. The rela-
tively low length exponent for P. crassidens could
be due to the small sample size or perhaps to poor
condition of the animals, since we do not know how
long the animals had been without food before
stranding. However, the 95% confidence limits on
the P. crassidens length exponent are
2.437±0.564.

The necropsies of six (four captive, two in field)
recently decreased whales indicated extensive
parasitism. Most apparent in all animals were
hundreds (perhaps thousands) of the acan-
thocephalan worm, Bolbosoma capitatum, at-
tached to the walls of the small intestine (Over-
street^). We found pieces of intestine with
attached acanthocephalans near the Cape Sable
animals. Five of the six animals had hundreds of
the nematode, Stenurus globicephalus, in the
pterygoid sinus complex. Three animals had the
stomach nematode, Anisakis cf. simplex (Over-
street see footnote 9). Four animals had S.
globicephalus in the lungs (Overstreet see footnote
9). Notable was the apparent absence in all six
animals of cestode plerocercoid cysts in the blub-
ber. Histopathology revealed that the ultimate
cause of death of the four captive females was
primarily pneumonia with some parasitic in-
volvement.^" The pathological condition(s) that
led to pneumonia remain speculative. Hall and
Schimpff^^' ^^ examined the brains of the captive
animals and of the male that died on Loggerhead
Key and found them free of major neurologic dis-
ease, although they stated that some animals
exhibited "behavioral symptoms suggestive of

^Robin Overstreet, Gulf Coast Research Laboratory, Ocean
Springs, MS 39564, pers. commun. September 1976.

'"Armed Forces Institute of Pathology, Washington, DC
20306, cases 1579706 and 1579707, pers. commun. October 1976.

"Hall, N.R., and R.D.Schimpff. 1977. Neuropathology in
relation to stranding. 2. Mass stranded whales. (Abstr.) Marine
Mammal Stranding Workshop, Athens, Ga., 10-12 August 1977,
p. 28-29. U.S. Marine Mammal Commission contract
MM7AC020.

i^Hall, N. R., and R. D. Schimpff. 1979. Neuropathology in
relation to strandings: mass strandings. In J. R. Geraci and D.
J. St. Aubin (editors). Biology of marine manomals: insights
through strandings, p. 236-242. Final Rep., U.S. Marine Mam-
mal Commission, contract MM7AC020. Available Natl. Tech.
Inf. Serv., Springfield, Va., as PB 293380.

173

vestibular dysfunction." They also found no
parasitic infiltration of the eighth cranial nerves
or the vestibular cochlear nuclei.

We examined the reproductive organs from the
six fresh carcasses. We judged the male to be sexu-
ally mature on the basis of body length (520 cm),
total testis weight (8,200 g) and histological dem-
onstration of spermatogenesis. We considered
three of the females (body lengths 297, 338, 358
cm) sexually immature. Neither corpora lutea nor
corpora albicantia were found in the ovaries (Har-
rison^^) and ovary weight was low (13.3, 14.0, and
15.1 g, respectively) compared with the other two
females. One female (475 cm) had three corpora
albicantia in the left ovary and five to six corpora
albicantia in the right ovary (Harrison see foot-
note 13). Ovary weight was 46.8 g. We also consid-
ered the 440 cm female from Redfish Pass to be
sexually mature based on ovary weight (65 g) and
the presence of three corpora albicantia in the left
ovary and six in the right.

Few data are available on sexual maturity and
reproduction in P. crassidens. Comrie and Adams
(1938) examined four 425-450 cm female speci-
mens of P. crassidens that were all sexually ma-
ture. Norman and Fraser (1948) and Purves and
Pilleri (1978) stated that sexual maturity was
reached in both sexes at 366-427 cm ( 12-14 ft) long.
Using Norman and Fraser's length range, three
females from the Tortugas stranding would be
considered immature with the lower limit and
nine with the upper limit, and three males would
be considered immature with the upper limit.

Hematology

We took blood from vessels in the flukes, flip-
pers, or dorsal fins. Samples for cell counts and
hemoglobin determinations were collected in an-
ticoagulant tubes. We collected sera from separate
tubes after the blood had clotted, and stored it
frozen until it was analyzed. Cell counts were done
with a Coulter Model D-2 (Coulter Electronics,
Hialeah, Fla.). Serum chemistry analyses were
done with a Clinicard Model 368 (Harleco Div.
American Hospital Supply Co., Gibbstown, N.J.).
This is one of the few (if not the only) times when
blood samples have been collected from an entire
herd of stranded cetaceans. The data from the 30
Loggerhead Key animals are similar to

'^Richard J. Harrison, Anatomy School, Cambridge Univer-
sity, Cambridge, Engl., pers. commun. 1976.

174

hematologic values for other small cetaceans (Ta-
ble 1; Ridgway et al. 1970; Ridgway 1972). Brown
et al. (1966) gave some data on blood cell counts
from the one false killer whale held at Marineland
of the Pacific for 7 yr. Those values are roughly
similar to those presented here, but red cell counts
were higher (4.5-5.2 x 10^/mm^). The blood values
for our four female false killer whales (Table 1)
vary somewhat from the Loggerhead Key group
and undoubtedly reflect their deteriorating condi-
tion. Notable are leucocytosis with an eosinophilia
in both groups (Table 1). Serum calcium levels
were elevated when compared with other odonto-
cetes. Lactic acid dehydrogenase levels were
slightly elevated. All of the above conditions can
be indicative of heat stress, parasitism,
pneumonia, etc. in other odontocetes, and we as-
sume that P. crassidens responds similarly. Al-
kaline phosphatase levels were low, indicating
depletion of reserves. This depletion generally
signals impending death in other odontocetes.
Blood urea nitrogen and glucose levels were
higher in the captives than in the Loggerhead Key
animals and could reflect the fact that captives
were feeding while the other group had probably
not fed for several days. White blood cell counts
and lactic acid dehydrogenase levels were the only
parameters in which males and females differed
significantly (f-test, 0.01 level).

Behavior in Captivity

The four live false killer whales transported to
Sea World appeared to adapt to captivity with
relative ease. When first put into their pool, they
began to swim rapidly around the pool as a group,
swimming in a clockwise direction with the
largest animal (475 cm), apparently leading the
group. They often took food from the hand and
were not easily disturbed by routine handling for
physical examinations. Within 24 h after their
arrival, the largest and the smallest whales were
separated from the other two and placed in an
adjacent pool. The overall swimming patterns of
all the animals remained the same after the sep-
aration. However, their swimming pace slowed
considerably. The general behavior and apparent
rapid adaptation to captivity was quite similar to
that observed in a captive false killer whale (ani-
mal collected at sea) held at Marineland of the
Pacific (Brown et al. 1966).

All of the animals began feeding on mackerel
and herring immediately upon arrival. The 338

Table l. — Blood chemistry analyses from two groups of the false killer wha\e, Pseudorca crassidens, stranded in Florida compared
with data for the bottlenose dolphin, Tursiops truncatus, and the Pacific whitesided dolphin, Lagenorhynchus ohliquidens.

P crassidens^

P. crassidens^

T truncatus^

L ot
N

iliquidens^

Parameter

'N

X

SD

N

X

SD

N

X

X

Hemoglobin (g 100 ml)

26

15 95

0.84

23

1427"

1.29

296

14.73-

67

1861-

Hematocrit (°o)

26

46,04

2.05

23

41.26--

3.22

345

44.04-

79

51.67-

Red cell count (10* mm^)

26

4.01

0.27

23

3.80"

0.29

291

4.05*

64

556-

Mean corpuscular hemoglobin (pg)

26

39.85

2.04

23

37.53"

228

—

^3637

—

53347

Mean corpuscular volume ^l^

26

115.02

4.61

23

108.70"

6.47

—

M 08.74

—

592.93

Mean corpuscular hemoglobin cone, (g dl)

26

34 64

0.95

23

34.56

1 53

—

53345

—

536.02

White cell count (10^ mm^);

Females

15

7.324-

1.765

23

8.842

3.434

167

9.780-

31

6.668-

Males

11

5.922-

1.203

—

—

—

154

10.675-

41

7.922-

Differential white cell count:

Bands (immatures) (%)

26

1.31

202

23

1 83

221

318

1

72

1

Neutrophils (",>)

26

73.31

12.43

23

71.83

1082

318

61

72

42

Lymphocytes (%)

26

13.50

6.59

23

16 96

7.30

318

21

72

29

Eosinophils (°o)

26

13.38

9.65

23

9 17

765

318

14-

72

22

Monocytes (%)

26

0.58

0.86

23

0.43

0.73

318

3

72

5

Basophils(°o)

26

0

0

23

0

0

—

—

—

—

Blood urea nitrogen (mg 100 ml)

29

24.40

4.91

20

46.40"

14.82

232

51-

62

37

Calcium (mg 100 ml)

29

10.67

2.01

17

8.67"

056

166

10

29

10

Creatinine phosphokinase (lU liter)

28

2293

16.09

13

86.77"

134.82

—

—

—

—

Total cholesterol (mg, 100 ml)

29

218.17

47.30

20

305 00"

87.38

301

221

92

154

Lactic acid dehydrogenase (lU liter)

Females

17

566.24

80.65

17

364 65"

76,52

100

113

11

179

Males

12

508.83

56.83

—

—

—

80

130

18

244

Alkaline phosphatase (lU liter)

29

98.72

56.51

20

149.15"

113 80

71

241-

6

256-

Serum glutamic oxaloacetic transaminase

(lU/liter)

29

217.52

88 46

20

382 15"

1 66.82

172

98-

34

110-

Serum glutamic pyruvic transaminase

(lU/liter)

29

43.03

63.58

20

31 89"

2843

88

19

14

45

Glucose (mg 100 ml)

29

80.76

28.76

20

167.10"

52.34

231

129

52

117

Total protein (g 100 ml)

29

7.60

0.56

20

7.32

085

133

8.0

10

9.0

Albumin (g 100 ml)

29

3.55

0.34

20

3.71

0.40

109

34

10

3.9

Globulin (g 100 ml)

29

3.91

0.73

20

3.55

0.75

—

—

—

—

'Animals from Loggerhead Key; each animal sampled once

^The four females held at Sea World; each animal sampled several times.

^Data from Ridgway et al, (1970),

•■Numtjer of determinations made

5Values calculated using mean values for hematocrit, hemoglobin and red cell count.

'Significant difference between males and females, f-test. 0.01 level.

cm female consumed an average (±SD) of 20 ±7.6
kg of mackerel and herring/day, in a ratio of 1.5:1,
from 25 July through 9 August. Food consumption
decreased significantly on 10 August and the ani-
mal died on 13 August. Similarly, the 297 cm
female consumed 15.3 ±4.0 kg of mackerel and
herring (2.2:1) between 24 July and 3 August.
Food consumption dropped to 1.8 kg on 4 August,
rose to 18.6 kg on 8 August when smelt was added
to the diet, and then decreased to 5.4 kg on 13
August. Overall food consumption between 24
July and 13 August was 11.7 ±5.7 kg/day. The
animal died on 14 August. The 358 cm female
consumed 15.1±8.5 kg of mackerel and herring/
day (1.2:1) between 24 July and 7 August. Food
consumption decreased on 4 August and remained
stable through 7 August {x = 9.0 ±2.5 kg/day).
Consumption between 24 July and 3 August was
17.1 ±8.9 kg/day. Smelt was introduced on 8 Au-
gust in place of mackerel and total consumption
was 22.7 kg. Squid was also added on 9 August.
The animal died on 10 August. The 475 cm female

had an erratic food consumption (mackerel and
herring, 19.4 ±16.2 kg/day) between 24 July and
29 July when it died. The individual blood chemis-
try analyses for these four animals reflected their
deteriorating condition (Odell et al. see footnote 8)
and their combined values were significantly
different from the Loggerhead Key animals
(Table 1).

Relationships Among Strandings

It is clear, based on photographs, that some of
the false killer whales that left Pine Island Sound
were the same individuals that stranded on
Loggerhead Key. Low altitude (helicopter) aerial
photographs were taken of the animals leaving
Captiva Pass (Larson see footnote 3). Comparison
of these photographs with photographs of dorsal
fins of the Tortugas animals provided positive
identification of several individuals. Dorsal fin
shapes have been used to identify specific indi-
vidual dolphins over periods of several months

175

(Wiirsig and Wiirsig 1977). Assuming that the
animals left Captiva Pass at about 1200 h on July
22. and that they travelled in a straight line, they
had to travel about 80 km/day to reach
Loggerhead Key at 1300 h on 25 July. When these
animals were escorted away from Loggerhead Key
on 27 July, they apparently headed northeast
(Schimpft"''*). The dead animals we found on Cape
Sable were too decomposed to tell if they were the
Captiva-Tortugas animals. Three large black
whales were seen by a National Park Service pilot
several kilometers east of the Dry Tortugas when
the other animals were stranded. These may be
the first three animals found floating off Cape
Sable on 2 August by Park Service personnel, but
the evidence is only circumstantial.

The sequence of strandings described herein
roughly parallels a series of pilot whale,
Globicephala macrorhynchus , strandings that oc-
curred in the same vicinity on 19-20 August 1971
(Fehring and Wells 1976). Forty-four pilot whales
stranded on Manasota Key and on Gasparilla Is-
land a few kilometers to the south (Figure 1). On
25 August 1971, 12 or 13 pilot whales were found
stranded on the Marquesas Keys east of Key West
(Figure 1). At least one of these was positively
identified to be from the previous stranding.

Fehring and Wells (1976) reported that the pilot
whales observed stranding on Gasparilla Island
made "a deliberate shoreward movement" as op-
posed to "disoriented panic." Eugene Shinn (see
footnote 5) unknowingly photographed the false
killer whales minutes before they beached on
Loggerhead Key while taking aerial photographs
of the reef formations. The photographs show two
close-knit pods of whales heading towards the
beach. Fehring and Wells also reported that the
behavior of the stranded animals changed after
the two largest pilot whales were towed offshore
and held there with ropes around their caudal
peduncles. The remainder of the animals then
showed less tendency to return to shore when
pushed off. Several of the larger Loggerhead Key
whales were forced offshore (headfirst, without
ropes around their tails) in hope that the others
would follow. The animals herded offshore re-
turned to the beach when released. The operation
was only successful when all of the animals were
forced offshore simultaneously and herded to

"Robert Schimpff, Department of Pathology, College of
Medicine, University of Florida, Gainesville, FL 32610, pers
commun. 1977.

176

deeper water, using swimmers and two boats.
While on the Loggerhead Key beach, the whales
were docile, as Fehring and Wells (1976) reported
for the pilot whales. Coast Guard personnel who
followed the animals offshore reported that the
herd split into two groups (one of 17-18 and one of
10 or 11 animals) (Schimpff see footnote 14).

Conclusions

From the veterinary medical standpoint, we
would doubt the ability of those animals that were
necropsied to function normally with the heavy
parasite load in the pterygoid sinus complexes.
The benefits of forcing live stranded animals back
out to sea must be carefully weighed against the
benefits of bringing them into captivity, where
they can be observed closely and thoroughly ne-
cropsied should death occur. If stranded whales are
returned to sea, they should be given permanent,
individual identification marks (e.g., freeze
brands) and, ideally, outfitted for radio tracking.

Acknowledgments

The data presented in this paper could not have
been collected without the generous assistance of
many organizations and individuals, including
the Florida Marine Patrol, U.S. Coast Guard, U.S.
National Park Service, National Marine Fisheries
Service, Wometco Miami Seaquarium, Gary
Davis, Gary Hendrix, Deke Buesse, Ralph Miele,
John Reynolds, and others. Material from the four
captive animals at Sea World was examined as
follows: ovaries - Richard J. Harrison; parasites -
Robin M. Overstreet; histopathology - Armed
Forces Institute of Pathology. Gordon Hubbell
kindly provided the information on the 1972
stranding. Donald Forrester, Robert Schimpff,
and Nicholas Hall commented on an early draft of
this paper. William F. Perrin, James G. Mead, and
Edward D. Houde provided useful criticisms on a
later draft.

Literature Cited

ASH, C. E.

1952. The body weights of whales. [In Engl, and Norw.]
Nor. Hvalfangst-Tidende 41:364-374.

1953. Weights of Antarctic humpback whales. Nor.
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BEAUCHAMP, J. J., AND J. S. OLrfON.

1973. Corrections for bias in regression estimates after
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Brown, D. H., D. K. Caldwell, and M. C. Caldwell.

1966. Observations on the behavior of wild and captive
false killer whales, with notes on associated behavior of
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BRYDEN, M. M.

1972. Growth and development of marine mammals. In
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mammals. Vol. I, p. 1-79. Acad. Press, N.Y.
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51:634-636.

Comrie, L. C, and a. B. Adams.

1938. The female reproductive system eind corpora lutea
of the false killer whale, Pseudorca crassidens
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1962. Sound and Cetacea. Neth. J. Sea. Res. 1:407-507.
Fehring, W. K., and R. S. Wells.

1976. A series of strandings by a single herd of pilot whales
on the west coast of Florida. J. Mammeil. 57:191-194.

FUJINO, K.

1955. On the body weight of the sei whales located in the
adjacent waters of Japan (II). Whales Res. Inst. Sci. Rep.
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1953 . Documentos iconigraficos sobre cetaceos de las costa
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1975a. Porpoise, dolphin, and small whale fisheries of the
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1948. Giant fishes, whales, and dolphins. Putnam,
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Omura, H.

1950. On the body weight of sperm and sei whales located

in the adjacent waters of Japan. Whales Res. Inst. Sci.

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1977. Pseudorca stranding. Oceans 10(4):8-16.
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1978. The functional anatomy and general biology of
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REIGER, G.

1975. Dolphin sacred, porpoise profane. Audubon
77(l):2-29.
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1972. Homeostasis in the aquatic environment. In S. H.

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medicine, p. 590-747. Charles C. Thomas, Springfield, 111.

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GILMARTIN.

1970. Hematologic findings in certain small ceta-
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1977. The photographic determination of group size, com-
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catus). Science (Wash., D.C.) 198:755-756.

DANIEL K. ODELL

Division of Biology and Living Resources
Rosenstiel School of Marine and Atmospheric Science
University of Miami
4600 Rickenbacker Causeway, Miami, FL 33149

EDWARD D. ASPER
Joe Baucom

Sea World, Inc.
7007 Sea World Drive
Orlando, FL 32809

Sea World, Inc.

1720 South Shores Road

San Diego, CA 92109

Lanny H. Cornell

OCCURRENCE OF THE FINETOOTH SHARK,
CARCHARHISLS ISODO^\ OFF
DAUPHIN ISLAND, ALABAMA'

Carcharhinus isodon (Valenciennes) is an in-
frequently encountered species with a poorly
known life history. The literature on this species
covering the western North Atlantic contains
much information on juveniles, but very little on
adults. All lengths discussed herein are total
lengths.

Radcliffe (1916) reported a single specimen
50.8 cm in the Bureau of Fisheries collection at
Beaufort, N.C. Burton's (1940) record of an im-
mature male, 74.4 cm, was the first from South
Carolina waters. Specimens examined by
Bigelow and Schroeder (1948:304-308) ranged
from 46 to 56.7 cm. Springer (1950) examined 20
adult females 147-155 cm collected in December
off Salerno, Fla. Thirteen had from one to six em-
bryos 43-48 cm; the remaining seven had en-
larged flaccid uteri and medium-sized ovarian

^Contribution No. 028, Dauphin Island Sea Lab.
fishery BULLETIN: VOL. 78, NO. 1, 1980. 177

eggs. He suggested a winter pupping period.
Clark and von Schmidt (1965) recorded only a
single female (76 cm) in 9 yr of shark research off
Sarasota, Fla. Dahlberg and Heard (1969) re-
ported the capture of 30 individuals from July
through September 1968 off Georgia. Of these, 29
were between 52 and 94 cm. The other specimen
(144 cm) was probably the only mature indi-
vidual, although there was no mention of sex or
reproductive development. Hoese and Moore
(1977, appendix 5) listed C. isodon as a spring
through fall spawner based on collections of
juveniles at Port Aransas, Texas. Compagno
(1978), in his review of the species, assigned this
species to the genus Carcharhinus.

During longlining operations in the northern
Gulf of Mexico in summer 1978, a gravid
female and two males were collected off Dauphin
Island, Ala. On 2 July 1979 one male and one
female were collected in the mouth of Mobile Bay.
With so few reports of mature C. isodon, these
captures will serve to better define the reproduc-
tive life history of this species.

On 5 June 1978 the gravid female ( 139 cm) was
collected by longline in water about 5 m deep,
approximately 1 km southwest of Sand Island, a
small barrier island approximately 5 km south of
the east end of Dauphin Island. The shark carried
four embryos ranging from 49 to 51 cm. These
appeared to be near-term pups. There were two
pups in each uterus, each positioned with the
head toward the anterior end of the uterus. Each
pup was enveloped by a membrane which was
filled anteriorly with a translucent yellow fluid.
Each had a highly vascularized placenta attached
to the posterior portion of the uterus, and the
connecting umbilical cords measured 20.6-30.0
cm. Where an umbilical cord attached to a
placenta there were three saclike extensions con-
taining a small amount of clear fluid. In earlier
embryonic stages of other species of carcharhinid
sharks these sacs contain the remaining uncon-
sumed portion of the yolk (Gilbert and Schlernit-
zauer 1966). The left uterus contained two males;
the right uterus one male and one female. The
pups and jaws of the female were deposited in the

Table i.-

Item

-Measurements (centimeters; methods after Bass et al. 1973) of the gravid female Carcharhinus

isodon and the four pups.

Gravid
female

Pup no. 1
male

Pup no. 2
male

Pup no. 3
male

Pup no. 4
female

Total length
Fork length!
Standard length
Snout to:

Dorsal 1

Dorsal 2

Pectoral fin

Pelvic fin

Anal fin

(^outh
Mouth breadth
Between nostrils
Eye diameter
Gill lengths:

No.
No.
No.
No.
No,

Dorsal 1 height

Dorsal 1 base

Dorsal 1 free margin

Dorsal 2 height

Dorsal 2 base

Dorsal 2 free margin

Anal height

Anal base

Anal free margin

Pectoral height

Pectoral base

Pectoral free margin

Pelvic anterior margin

Pelvic distal margin

Uppper caudal length

Lower caudal length

Interspace base dorsal 1 to origin dorsal 2

Interspace base dorsal 2 to caudal pit

Origin of pectoral to origin of pelvic

Origin of pelvic to origin of anal

Weight (g)

139

49

51

50.5

50.5

118

38.5

40.5

40

40.5

106

35

37

36

36.5

46

15.7

16.5

16.5

16.5

90

30.2

31.5

31

32.5

31.5

11

12.2

11.9

12.2

74

22.8

25.4

23.8

24.2

88

28.9

31.9

31.3

30.4

9

3.9

3.9

3.8

3.8

13

4.1 ■

4.4

4.2

4.1

7

2.7

2.7

2.7

2.8

1.8

.8

.8

.8

.7

8

2.5

2.3

2.2

2.3

8.6

2.6

2.5

2.4

2.5

9

2.7

2.7

2.6

2.6

8.5

2.5

2.4

2.3

2.4

7.5

2.1

1.8

1.8

1.8

14.7

3.9

3.8

3.5

3.8

14

4.3

4.6

4.6

5.1

5.5

2.0

2.2

1.8

2.0

4.0

1.2

1.4

1.4

1.1

6.5

1.9

2.2

2.2

2.1

5.5

2.0

2.2

1.9

1.9

4.3

1.4

1.5

1.5

1.3

7.4

2.2

2.4

2.4

2.1

4.8

1.9

1.9

1.8

1.8

22

6.0

6.9

6.3

6.5

8

2.5

2.6

2.5

2.5

6.5

2.2

2.4

2.4

2.4

6.5

2.4

2.6

2.7

2.8

8.8

2.8

2.9

2.7

2.8

39

13.8

14.9

14.7

14.1

17.5

5.1

5.5

5.1

5.4

33

10.1

10.2

9.9

10.3

10.5

3.8

3.9

3.4

3.4

42

11.8

13.2

11.9

12.0

16

6.1

6.5

7.5

6.2

—

704

810

737

758

178

University of South Alabama Ichthyological Col-
lection (USAIC 6278). Measurements and
weights are found in Table 1.

Since most records of C. isodon are of juveniles,
there is little information on the reproductive
biology of the species. Based on the cited litera-
ture and these data, pups appear to be 45-55 cm
at birth. However, seasonality is uncertain as the
records of Springer (1950) are not in accord with
those of either Hoese and Moore (1977) or this
report.

Length at maturity can be closely estimated.
One male (112 cm) collected 13 July 1978 was
immature — based on incomplete calcification of
the claspers and incompletely developed siphon
sacs, each sac being 7.5 cm long and 1.0 cm wide.
The other two males ( 120 and 127 cm) collected 2
July 1979 and 28 June 1978 had well-calcified
claspers and fully developed siphon sacs. The only
literature on mature males (Springer 1950) listed
lengths of 140-152 cm. Males apparently mature
between 115 and 120 cm. Maturity in females
must be reached at a larger size. The female col-
lected in July 1979 was 127 cm, yet was imma-
ture with only small undeveloped ovarian eggs.
The gravid female reported here was 139 cm, and
those reported by Springer (1950) were 147-155
cm.

Carcharhinus isodon was only collected when
similarly sized specimens of blacktip shark, C.
limbatus, were caught: 3 C. limbatus ( 126-166 cm)
with the gravid female, 12 C limbatus (102-117
cm) with the 112 cm male, 2 C limbatus (111 and
124 cm) with the 127 cm male, and 12 C. limbatus
(100-130 cm) with the two specimens caught in
1979. If C. isodon is an uncommon straggler into
the northern Gulf of Mexico it may be schooling
with other sharks of like size. Sharks that school
have been noted to do so by sex or size (Ford 1921).

Literature Cited

Bass, a. J., J. D. D' Aubrey, and N. kistnasamy.

1973. Sharks of the east coast of Southern Africa. I. The
genus Carcharhinus (Carcharhinidae). Oceanogr. Res.
Inst. (Durban), Invest. Rep. 33, 168 p.
BIGELOW, H. B., AND W. C. SCHROEDER.

1948. Sharks. In Fishes of the western North Atlantic.
Part one, p. 59-546. Mem. Sears Found. Mar. Res., Yale
Univ. 1.
Burton, E. M.

1940. Aprionodon isodon from South Carolina. Copeia
1940:140.

Clark, E., and K. Von Schmidt.

1965. Sharks of the central Gulf Coast of Florida. Bull.
Mar. Sci. 15:13-83.

COMPAGNO, L. J. V.

1978. Sharks. In W. Fischer (editor), FAO species iden-
tification sheets for fishery purposes: western central At-
lantic. Vol. 5, unpaginated.

Dahlberg, M. C, and R. W. Heard, III.

1969. Observations on elasmobranchs from Georgia. Q.
J. Fla. Acad. Sci. 32:21-25.
FORD, E.

192 1 . A contribution to our knowledge of the life-histories
of the dogfishes landed at Plymouth. J. Mar. Biol. As-
soc. U.K. 12:468-505.

Gilbert, P. W., and D. A. Schlernitzauer.

1966. The placenta and gravid uterus of Carcharhinus
falciformis. Copeia 1966:451-457.

Hoese, H. D., and r. H. Moore.

1977. Fishes of the Gulf of Mexico, Texas, Louisiana, and
adjacent waters. Tex. A&M Univ. Press, College Sta-
tion, 327 p.
Radcliffe, L.

1916. The sharks and rays of Beaufort, North Caroli-
na. Bull. U.S. Bur. Fish. 34:239-284.

Springer, S.

1950. A revision of North American sharks allied to the
genus Carcharhinus. Am. Mus. Novit. 1451, 13 p.

Steven Branstetter

ROBERT L. SHIPP

University of South Alabama
Dauphin Island Sea Lab
P.O. Box 386
Dauphin Island, AL 36528

SHEDDING RATES OF PLASTIC AND

METAL DART TAGS FROM ATLANTIC

BLUEFIN TUNA, THUNNUS THYNMUS^

In 1971, the International Commission for the
Conservation of Atlantic Tunas (ICCAT) recom-
mended that a double-tagging experiment be con-
ducted on Atlantic bluefin tuna, Thunnus thyn-
nus, to determine whether plastic or metal dart
tags were more efficient and to estimate im-
mediate and instantaneous tag shedding rates. A
knowledge of shedding rates is necessary so that
appropriate adjustments can be made when es-
timating mortality rates from tag return data.
This study was begun in 1971 by the National
Marine Fisheries Service (NMFS), the Woods Hole
Oceanographic Institution (WHOI), and the
Fisheries Research Board of Canada (FRBC). The

^Southeast Fisheries Center Contribution Number 80-14M.
FISHERY BULLETIN: VOL. 78, NO. 1, 1980. 179

results obtained through 1972, for 580 double-
tagged bluefin tuna released during 1971 off the
east coast of the United States, were reported by
Lenarz et al. ( 1973). Their results were partially
based on tags supplied by the FRBC, some of which
had longer streamers than the tags supplied by
WHOI. For our present analysis, we used only
data from the WHOI tags.

In this paper we present the overall findings
obtained through 1978 for 3,121 double-tagged
bluefin tuna. These fish were released primarily
from U.S. purse seine vessels fishing off the east
coast of the United States from Virginia to Mas-
sachusetts from 1971 through 1977.

Methods

The U.S. double-tagging program for Atlantic
bluefin tuna was conducted jointly by the NMFS
and WHOI. Tags and tagging procedures were
those described by the Food and Agriculture Or-
ganization (1972). All fish were tagged and re-
leased from U.S. purse seine vessels (98% of all
releases) and from a few sport fishing vessels.
Tagging occurred throughout the purse seine
fishing season during 1971, 1973, and 1974, and at
the end of the season during 1972, 1975, 1976, and
1977. The double-tagging operation was con-
ducted entirely by John Mason during each year
except 1974, when two assistants aided in the dou-
ble tagging. Precise release dates were available
for all of the fish. In a few instances only the month
and year were known for the recapture data. In
these cases, the 15th of the month was arbitrarily
selected to represent the recapture date. The vast
majority of returns fall into an annual cycle dur-
ing which the recapture periods are approxi-
mately 2-3 summer months. The interval mid-
points of the time intervals can be considered to be
on a yearly cycle. Therefore, we grouped returns
into "first year returns," "second year returns,"
etc., and calculated average days out from the
individual days out for each return. Tag shedding
rates were estimated using the notation and
methodology of Bayliff and Mobrand (1972) for
yellowfin tuna, which Lenarz et al. (1973) used for
bluefin tuna and Laurs et al. (1976) used for North
Pacific albacore. Chapman et al. (1965) developed
the original model with the assumption of only one
type of shedding which occurs at a constant in-
stantaneous rate. Bayliff and Mobrand (1972) as-
sumed that there are two types. Type I which oc-
curs immediately after the fish are released and

180

Type II, the type described by Chapman et al.
(1965).

Bayliff and Mobrand's modifications^ of the
Chapman et al. (1965) approximate equations for
tag returns of double-tagged fish are:

nddk^FrNj)Trp^e^p-iF + X + 2L)tk (1)

n^sk = 2FtNd 7rp(l - pexp{-Ltk))

expi-{F + X + L)tk) (2)

where n^^ = number of returns of double-tagged
fish retaining both tags caught dur-
ing the recapture period tk,

n^gi^ = number of returns of double-tagged
fish retaining only one tag caught
during the period ^^ ,

F = instantaneous rate of fishing mortal-
ity,

A^^ = number of double-tagged fish re-
leased,

77 = proportion of tagged fish which re-
main alive after the Type-I mortality
(immediate) has taken place,

p = proportion of the tags which are re-
tained after Type-I shedding (im-
mediate) has taken place,

X = instantaneous rate of mortality due
to natural causes, Type-II tagging
mortality (long term), and emigra-
tion from the fishing grounds,

L = instantaneous rate of tag shedding
(Type II), and

tf^ = time at the middle of the /sth recap-
ture period of length T(k = 1, 2, 3).

From Equations (1) and (2) it follows that
^dsk 2(1 - pexp(-L^fe ))exp(L^fe )

n

ddk

and therefore

ridsk expiLtk)-p exp(L^fe) 2nddk

^^ddk

^^ddk

Rearranging terms yields

^As pointed out by Laurs et al. ( 1976), there was typographical

error in both Bayliffand Mobrand (1972) and Lenarz etal (1973)
in Equation (2).

2n

ddk

and hence In

f^dsk + ^f^ddk
^^ddk

ndsk ■•" 2A2ddfe

= pexp(-Lffe)
= Inp — Ltfj

= y.

where Y^ is an estimate of the natural logarithm
of the proportion of tags retained up to time t/,.
Given n^idk , ^^s* > and t^ , then L and p can be esti-
mated using linear regression. We first estimated
these parameters using the usual least-squares
linear regression which assumes homoscedastic-
ity. We also believed that it would be appropriate
to consider that variability may increase as a func-
tion of time as the number of recoveries decreases.
To accomplish this, a weighting factor was intro-
duced and a weighted least-squares linear regres-
sion model was fitted to calculate values of Inp and
L, as was done by Bayliff and Mobrand (1972). The
weights for each time interval k (k = 1, 2, 3) were
equated to the ratio of the number of returns of
double-tagged fish during interval k to the total
number of returns of double-tagged fish during all
/j -periods. This can be simply expressed as:

GJfe

^ddk + l^dsk
3

2 i^ddi + nasi)

i=l

While we consider this a reasonable first approxi-
mation of the correct weight, further investiga-
tions of the statistical properties of Yf^ to formally

determine the correct weighting procedure are de-
sirable. Estimates of Inp and L were then made
using weighted linear regression.

Results and Discussion

The double-tag releases during 1971 through
1977 and returns in 1971 through 1978 are shown
by tag type (Table 1). A sufficient number of tag
returns existed to allow examination of three
separate recapture periods. Only a few returns
existed from beyond the third recapture period.
There were approximately equal numbers of each
tag type released each year. Table 1 constitutes
the basic data used throughout this study. Using
the basic data, we estimated values of immediate
(Type I) and instantaneous (Type II) shedding
rates for each tag type. Further, we tested several
hypotheses including: 1) equality of return rates
for same year recaptures; 2) equality of return
rates by estimated age; and 3) differences in re-
turns and nonreturns over 2 or 3 yr time periods
for various time intervals.

Using the double-tagging release data for all
years combined (1971-77) the return rate for plas-
tic tags was 5.1% the first year, 8.6% the second
year, and 1.6% the third year. The return rate for
metal dart tags was 5.5% the first year, 9.1% the
second year, and 2.9% the third year. Therefore,
for both types of tags the return rates increased
the second year and decreased the third year. This
should be expected since tagging occurred at the
end of the purse seine season for several of the
release years studied. Chi-square tests (not cor-

Table 1. — Tag releases and returns from northwestern Atlantic bluefin tuna double-tag study. For each of /z = 1, 2, or 3 recapture
periods the number of returns of double-tagged fish retaining both tags is n^^/^ and those retaining only one tags is n^^/^ . The average
number of days-at-large for each period is tf;.

[

Double-tagged

releases

First-year

returns

Second-year

returns

Third-year

returns

Tag type

Year

Number

"dd1

"ds^

t^ (days)

"dd2

"ds2

f2 (days)

"dd3

"ds3

fg (days)

Plastic dart

1971

150

4

0

7.25

20

9

349.07

3

1

724.00

(D-tag)

1972

75

6

0

12.83

17

4

340.52

1

1

726.50

1973

134

18

2

18.45

6

4

354.20

0

1

708.00

1974

629

25

4

12.07

18

12

352.17

4

7

727.82

1975

50

0

1

40.00

1

1

384.50

0

0

0

1976

267

12

2

16.36

2

2

341.00

1

2

707.33

1977

223

3

1

47.50

25

4

361.83

—

—

—

Total

1,528

68

10

16.46

89

36

352.06

9

12

723.10

Metal dart

1971

162

4

1

18.60

10

9

358.63

2

3

724.80

(H-tag)

1972

77

0

1

11.00

9

11

343.55

0

1

740.00

1973

131

12

5

16.88

1

3

373.25

0

2

720.00

1974

666

28

2

10.97

40

13

358.57

15

11

703.19

1975

58

1

0

43.00

4

5

339 11

2

0

687.50

1976

271

23

3

23.08

6

0

311.00

0

4

759.25

1977

228

8

0

36.00

24

2

365.19

—

—

—

Total

1,593

76

12

18.76

94

43

354.71

19

21

712.48

Grand total

3.121

144

22

17.68

183

79

353.44

28

33

716.13

181

rected for continuity) showed that there were no
significant differences at the 0.01 level, with 1
degree of freedom, in return and nonreturn rates
between tag types for fish at liberty for 1, 2, or 3 yr
(Table 2). However, returns were significantly
better at the 0.05 level for metal tags in the third
year. Further, there was no significant difference
at the 0.01 level in the first-year return and non-
return rates between the two types of dart tag,
whether comparing each year individually or
comparing all years combined (Table 3).

We also tested for differences in return and non-
return rates between age-groups. Fish were aged
from unpublished length-age tables (Rivas^).
Chi-square values for fish tagged at ages 1, 2, 3,

^L. R. Rivas, Southeast Fisheries Center Miami Laboratory,
Natl. Mar. Fish. Serv., NOAA, 75 Virginia Beach Drive, Miami,
FL 33149.

and 4 + , were not significant at the 0.01 level (Ta-
ble 4). The results of the chi-square test indicated
that tag types and ages could be combined.

Unweighted and weighted linear regression
models were used to estimate immediate tag shed-
ding rate (1 - p) and instantaneous shedding rate
(L) (Table 5). The unweighted model for both tags
combined yielded an estimate of immediate tag
shedding ( 1 - p) to be 0.040 (0.042 for the weighted
model). The overall estimate of the instantaneous
rate of tag shedding (L) on an annual basis using
the model was 0.205 (0.186 for the weighted
model). (The annual rate analog for L from the
unweighted model is 0.19.) Therefore, the results
from each model were similar. We chose to use the
unweighted results, which give a slightly higher L
value. While results of the chi-square test indi-
cated that tag types could be combined, estimates
were also made for each tag type separately to

Table 2. — Chi-square tests (df = 1) of equality of yearly return and nonreturn rates between double-tagged releases for 1971-77
combined, for A = 1 , 2, or 3 yr at liberty, using plastic or metal dart tags on bluefin tuna in the northwestern Atlantic Ocean. The number
of returns of double- tagged fish retaining both tags is n^^/^ and those retaining only one tag is n^g/i-

Plastic dart tags

Metal dart tags

Return
year (k)

Double-tagged
releases

Total returns k\h year

Return
rate

Double-tagged
releases

Total returns /tth year
^"ddk^"dsk^

Return
rate

Chi-square
value

1
2
3

1.528
1,450
1,325

78
125
21
Average

0.05105
0.08621
0.01585
0.05104

1,593
1,505
1,368

88

137
40

0.05524
0.09103
0.02924
0.05850

0.272
0.213
5.452-

•P«0.05.

T.ABLE 3. — Chi-square tests (df = 1) of equality of return and nonreturn rates between double-tagged releases recaptured the same year
using plastic or metal dart tags on bluefin tuna in the northwestern Atlantic Ocean. The number of returns of double-tagged fish
retaining both tags during the first year after release is n^^j , and those retaining only one tag is n^jgi.

Plastic dart tags

Metal dart tags

Double-tagged

Total returns same year

Return

Double-tagged

Total returns same year

Return

Chi-square

Year

releases

<"ddl ^"dsl>

rate

releases

<"dd1 ^"dsl'

rate

value

1971

150

4

0.02667

162

5

0.03086

0.049

1972

75

6

0 08000

77

1

0.01299

3.884-

1973

134

20

0,14925

131

17

0.12977

0.209

1974

629

29

0.04610

666

30

0.04505

0.008

1975

50

1

0.02000

58

1

0.01724

0.011

1976

267

14

0.05243

271

26

0.09594

3.699

1977

223

4

0.01794

228

8

0.03509

1.280

Total

1,528

78

0.05105

1,593

88

0.05524

0.272

•PsO.05

Table 4. — Chi-square tests (df = 1) of equality of return and nonreturn rates by estimated age between double- tagged releases for all
years 1971-77 combined, recaptured the same year, using plastic or metal dart tags on bluefin tuna in the northwestern Atlantic Ocean.
The number of returns of double- tagged fish retaining both tags during the first year after release is n^j and those retaining only one
tagis«dsl-

Plastic dart tags

Metal dart tags

Estimated age
at release

Double-tagged
releases

Total returns same
("ddl+^dsl'

year

Return
rate

Double- tagged
releases

Total returns same
("ddl ^"dsl'

year

Return
rate

Chi-square
value'

1
2
3

4-I-

641

631

212

44

1.528

29

43

4

_2

78

0.04524
0.0681 5
0.01887
0.04545

647
656
226

64

1,593

31

43

12

_2

88

0,04791
0.06555
0.05310
0.03125

0.052
0.035
3.642
0.148

182

Table 5. — Estimates of immediate (1 - p) and annual instan-
taneous it) tag shedding rates for northwestern Atlantic bluefin
tuna double-tagging study for all years combined (1971-77)
based on a 3-yr return period using unweighted and weighted
linear regression models. (The weights used in the weighted
model were equated to the ratio of the number of returns of
double- tagged fish during each return period to the total number
of returns of double-tagged fish during all periods.)

Model and tag type

1 - P

L (annual)

Linear regression:
Plastic dart
Metal dart

Combined

Weighted linear regression:
Plastic dart
Metal dart
Combined

0.027
0.049

0.040

0.033
0.049

0.042

0 22886
0.19201
0.20452

0.19200
0.18213
0.18596

indicate the magnitude of the variances of the
estimates.

Our estimate of (1 - p) is slightly greater than
the overall estimate of 0.027 given for bluefin tuna
from the northwest Atlantic by Lenarz et al.
(1973). The difference is small relative to the pre-
cision of the estimates. Our estimate of (1 - p) for
northwest Atlantic bluefin tuna is less than the
value of 0.10 reported for Pacific yellowfin tuna by
Bayliff and Mobrand (1972) and the value of 0.12
reported for North Pacific albacore by Laurs et al.
(1976).

Our estimate of L is less than the overall esti-
mate of 0.31 reported by Lenarz et al. (1973) for
bluefin tuna and the L estimate of 0.278 reported
for yellowfin tuna by Bayliff and Mobrand (1972).
Our L estimate is greater than the estimates of
between 0.086 and 0.098 reported for albacore by
Laurs et al. (1976).

As previously noted, there was no significant
difference in return rates found for the two types of
dart tags for 1971-77. However, from examination
of the data presented in Table 1, there appeared to
be changes occurring in the shedding rates of each
type of tag and a difference between the 1971-73
and 1974-77 time intervals. Therefore, we calcu-
lated (1 - p) andL for each time interval and con-
ducted chi-square tests (df = 6) for differences in
returns over three recapture periods ik = 3) be-
tween time intervals and between tag types (Table
6). We found significant differences between time
intervals for each of the tag types and significant
differences between tag types for each of the time
intervals. The plastic dart tags became less
efficient, i.e., L increased over the time intervals,
and the metal dart tags improved, i.e., L decreased
over the time intervals.

The model of Chapman et al. (1965), which was

Table 6. — Estimates of immediate (1 - p) and einnual instan-
taneous (L) tag shedding rates for northwestern Atlantic bluefin
tuna double-tagging study for time intervals 1971-73 and 1974-
77 based on a * = 3-yr return period. (A contingency table, 7x2,
was constructed containing the number of double and single
returns for each of the three recapture periods plus the number of
nonreturns for each tag type and each time interval.) Results of
chi-square tests (df = 6) for differences in double and single tag
returns and total nonreturns between time intervals and tag
types over a 3-yr recapture period are given.

Tag type and
time interval

L (annual)

Chi-square value

Plastic dart:
1971-73
1 974-77

Metal dart:
1971-73
1974-77

1971-73:
Plastic dart
Metal dart

1974-77:
Plastic dart
Metal dart

0 029
0.023

0.140
0.007

0 029

0.140

0.023
0.007

0.14838
0.28455

0.37163
0.17242

0.14838
0.37163

0.28455
0.17242

64.286"
33.489"
18.924"
18.135"

"P«0.01.

modified by Bayliff and Mobrand (1972), assumes
constant L over recapture periods. We decided to
examine values of L over the two pairs of recap-
ture periods k = (1, 2) and k = (2, 3) to determine
how well our data fit the model. Since only two
recapture periods were used, L and ( 1 - p) were
estimated by solving two simultaneous equations.

For the tag types and time intervals examined,
there is an indication that L is not constant (Table
7). In fact, L increased in three out of four cases.
The sequence of events could have happened due
to chance alone, for if the changes in L came from a
binomial distribution with P =0.5, then the prob-
ability of L decreasing in three of the four cases or
L increasing in three of the four cases is ^0.25.
However, L during the second time period is more
than 60% >L in the first time period in three cases
and only 16% <L in the first time period in the
other case. While the data do not provide conclu-
sive evidence that L is not constant, it would be
dangerous to extrapolate beyond the time period
used for analysis.

We previously noted that the 1974 releases were

Table 7. — Estimates of annual instantaneous (L) tag shedding
rates for northwestern Atlantic bluefin tima double-tagging
study for 1971-73 and 1974-77 based on return periods of A = (1,

2) and k = (2, 3).

Tag type and time interval

Return period k

L (annual)

Plastic 1971-73

1,2

0.16017

2.3

0.13421

Plastic 1974-77

1.2

0.09925

2,3

0.45207

Metal 1971-73

1,2

0.27858

2,3

045271

Metal 1974-77

1.2

0.09331

2,3

0.24632

183

unique in that three individuals conducted the
tagging operation, whereas only one individual
tagged and released the remainder of the fish from
the other years. Therefore, we analyzed the data
from the time intervals 1971-73 and 1975-77 sepa-
rately from the 1974 data. For the following
reasons we decided to examine only two recapture
periods, k = (1, 2): 1) 1977 has only two recapture
periods possible (Table 1); 2) the number of single
as well as double returns for ^ =3 for both 1971-73
and 1975-77 constitutes very small sample sizes
(Table 1); and 3) L appears to have been changing
over k = (1, 2) to A; = (2, 3) (Table 7).

Our analysis showed (Table 8) that there was a
significant difference in return and nonreturn
rates between time intervals for each type of dart
tag. Also a significant difference in shedding rates
was found between the plastic and metal type tags
during the time interval 1971-73. A small sample
size may account for the lack of a significant dif-
ference in shedding rates for each type of tag dur-
ing the time interval of 1975-77. There also was no
significant difference found in the shedding rates
between each tag type during 1974. As previously
mentioned, fish were released under different cir-
cumstances during 1974. During the 1971-73 time
interval, plastic tags were found to be superior. We
again found that the metal tag improved (Table 8),
i.e., L decreased, between 1971-73 and 1975-77.

Table 8. — Estimates of immediate (1 - p) and annual instan-
taneous (L) tag shedding rates for northwestern Atlantic bluefin
tuna double-tagging study for 1971-73, 1974, and 1975-77 based
on a * = 2-yr return period. (A contingency table, 7x2, was
constructed containing the number of double and single returns
for each of the three recapture periods plus the number of non-
returns for each tag type and each time interval.) Results of
chi-square tests (df = 4) for differences in double and single tag
returns and total nonreturns between time intervals and tag
types over a 2-yr recapture f)eriod are given. (Results for the
period 1971-72 from Lenarz et al. (1973) are showTi for compari-
son.)

Tag type and

time interval

1 -p

I

Chi-square value

Plastic dart:

1971-73

0.028

0.16017

39.460"

1975-77

0.118

<0.

Metal dart:

1971-73

0.169

0.27858

22.186"

1975-77

0.114

0.05860

1971-73:

Plastic dart

0.028

0.16017

17.323"

Metal dart

0 169

0.27858

1974:

Plastic dart

0.067

0,22615

8.318

Metal dart

0.031

0.12126

1975-77:

Plastic dart

0.118

<0.

6.636

Metal dart

0.114

0.05860

1971-72:

Plastic dart

0.000

0.21615

Metal dart

0.099

0.26278

"PsO.OI.

Also, L -values for the plastic tag decreased, but
results yielded a negative value for the 1975-77
time interval, which is theoretically impossible
and is due to variability in the data.

From our analysis, we cannot conclusively show
that one of the two types of dart tags is better for
bluefin tuna tagging. Both tag types appeared to
improve between 1971-73 and 1975-77. Plastic
tags were significantly better than metal in the
first period and nonsignificantly better in the
second.

We have showTi that tag shedding rates vary
from 1 yr to another. There are some possible
reasons for the observed variability. One reason
may be changes in tag design or quality. To our
knowledge there was no intentional effort made by
the manufacturers to change the design of the
metal or plastic dart tags used in this study. A
different type of glue, however, was used during
1972 through 1977 for the plastic dart tags. Before
using the plastic dart tags, we tested them by
pulling on the barb. On several occasions, we dis-
covered that the barbs were not adequately se-
cured. We reglued these tags before using them. We
also examined the metal dart tags prior to their
use. In general, they appeared to be trouble free.
Several orders of both types of tags were used
during the course of this study. We were unable to
correlate changes in the shedding rates with the
specific batch of tags that were used. The shelf life
of the plastic used in the tags may be another
factor. In some instances we used tags which were
manufactured several years before their actual
use. Since there were no changes in the tagging
method, this reason was discounted. Tagging oc-
curred throughout the purse seine fishing season
during 1971, 1973, and 1974, and at the end of the
season during 1972, 1975, 1976, and 1977. We do
not see why this would have more of an effect on
one type of tag than on the other.

Summary and Conclusions

Return data for double-tagged northwestern At-
lantic bluefin tuna were used to estimate the
shedding rates of plastic and metal dart tags. No
significant difference was found between the re-
turn rates of the plastic and metal tags when the
data were tested for all years combined, but plastic
tags appeared to have lower shedding rates than
metal tags in most cases. We believe that the com-
bining of the data of all years together (1971-77)
probably yields a reasonable approximation to the

184

average shedding rate for each type of tag. Type-I
shedding, which occurs immediately after release,
was estimated to be 0.040 for plastic and metal
dart tags combined. Type-II (instantaneous) shed-
ding was estimated to be 0.205 for plastic and
metal tags combined on an annual basis.

The shedding rates for each type of tag were
found to vary over the time period studied, and
deviations from the assumption of constant shed-
ding throughout the life of the tagged fish were
noted. Due to these differences, one should not be
satisfied with the results of one double-tagging
experiment. We recommend that double tagging
be employed whenever possible, as long as shed-
ding occurs and the rate of shedding is found to
vary. Also, tagged fish, especially the ones which
have been at liberty for a long time, are more
likely to continue to carry at least one tag if they
were originally double tagged. The ones that do
not continue to carry at least one tag are of no
value. Furthermore, relative to the errors inher-
ent in a study of this type we do not feel that there
is really any important difference in shedding
rates between the plastic and metal dart tags.

Since shedding may increase with time from
release, extrapolations based on the assumption of
constant L should be made with caution. Also be-
cause the tag shedding rates that we found are
considerable, efforts should be made to develop a
more efficient type of tag with a lower rate of
shedding.

from yellowfin tuna. [In Engl, and Span.] Inter-Am.
Trop. Tima Comm., Bull. 10:333-352.
FOOD AND AGRICULTURE ORGANIZATION.

1972. Final report of the working party on tuna and
billfish tagging in the Atlantic and adjacent seas. FAO
Fish. Rep. 118, Suppl. 1, 37 p.

Laurs, R. M., W. H. lenarz, and r. n. Nishimoto

1976. Estimates of rates of tag shedding by Non' acific
albacore, Thunnus alalunga. Fish. Bull., U.S. 74:675-
678.
LENARZ, W. H., F. J. Mather m, J. S. Beckett, a. C. Jones,
and J. M. Mason, Jr.

1973. Estimation of rates of tag shedding by northwest
Atlantic bluefin tuna. Fish. Bull., U.S. 71:1103-1105.

Raymond E. Baglin, Jr.

Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA, Miami, Fla.
Present address: National Marine Fisheries Service, NOAA
do Alaska Department of Fish and Game
P.O. Box 686, Kodiak, AK 99615

Mark I. Farber

Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA
75 Virginia Beach Drive, Miami, FL 33149

William H. Lenarz

Southwest Fisheries Center Tiburon Laboratory
National Marine Fisheries Service, NOAA
3150 Paradise Drive, Tiburon, CA 94920

John M. Mason, Jr.

Woods Hole Oceanographic Institution, Woods Hole, Mass.
Present address: Mid-Atlantic Fishery Management Council
Federal Building, North and New Streets
Dover, DE 19901

Acknowledgments

We thank W. H. Bayliff of the Inter-American
Tropical Tuna Commission and J. Wetherall of the
Southwest Fisheries Center Honolulu Laboratory,
NMFS, NOAA, for their helpful comments on the
manuscript. We also thank all captains and crew-
men of commercial and sport fishing vessels,
WHOI personnel, George Bell, NMFS personnel,
Andy Bertolino, and Dennis Lee, who participated
in the bluefin tuna tagging program, and T.
Chewning of the Southeast Fisheries Center for
computer programming assistance.

Literature Cited

Bayliff, W. H., and L. M. Mobrand.

1972. Estimates of the rates of shedding of dart tags from
yellowfin tuna. [In Engl, and Span.] Inter-Am. Trop.
Tuna Comm., Bull. 15:439-462.
Chapman, d. G., B. D. Fink, and E. B. Bennett.

1965 . A method for estimating the rate of shedding of tags

INFLUENCE OF LITTLE GOOSE DAM ON

UPSTREAM MOVEMENTS OF ADULT CHINOOK

SALMON, ONCORHYNCHUS TSHAWYTSCHA

A major environmental and economic concern in
the Pacific Northwest is the continuing decline in
the numbers of Columbia and Snake River sal-
monids. Several investigators (Johnson 1960 and
others) have used biotelemetry to study effects of
hydroelectric dams (Figure 1) on the upstream
movements of adult salmonids. Results indicated
upstream movements were delayed at Bonneville
(Schoning and Johnson^; Monan and Liscom2.3,4,5)^

^Schoning, R. W., and D. R. Johnson. 1956. A measured
delay in the migration of adult chinook salmon at Bonneville
Dam on the Columbia River. Fish. Comm. Oreg., Contrib. No.
23, 16 p.

^Monan, G. E., and K. L. Liscom. 1971. Final report, radio
tracking of adult spring chinook salmon below Bonneville Dam,

fishery BULLETIN: VOL. 78. NO. 1. 1980.

185

Figure l. — Location of Columbia and Snake River hydroelectric dams.

the Dalles (Monan and Liscom see footnote 3), and
Rock Island ( French and Wahle 1956) Dams on the
Columbia River and at Lower Monumental (Mo-
nan and Liscom^; Gray and Haynes'^) and Lower
Granite (Liscom and Monan^) Dams on the Snake

1971. Northwest Fisheries Center, Natl. Mar. Fish. Serv.,
NOAA, Seattle, Wash., 24 p.

^Monan, G. E., and K. L. Liscom. 1973. Final report, radio
tracking of adult spring chinook salmon below Bonneville and
the Dalles Dams, 1972. Northwest Fish. Cent., Natl. Mar. Fish.
Serv., NOAA, Seattle, 37 p.

"Monan, G. E., and K. L. Liscom. 1974. Radio tracking
studies of fall chinook salmon to determine effect of peaking on
passage at Bonneville Dam, 1973. Northwest Fish. Cent., Natl.
Mar. Fish. Serv., NOAA, Seattle, 28 p.

^Monan, G. E., and K. L. Liscom. 1975. Final report, radio
tracking studies to determine the effect of spillway deflectors and
fallback on adult chinook salmon and steelhead trout at Bon-
neville Dam, 1974. Northwest Fish. Cent., Natl. Mar. Fish.
Serv., NOAA, Seattle, 38 p.

«Monan, G. E., and K.L. Liscom. 1974. Final report, radio
tracking of spring chinook salmon to determine effect of spillway
deflectors on passage at Lower Monumental Dam,
1973. Northwest Fish. Cent., Natl. Mar. Fish. Serv., NOAA,
Seattle, 20 p.

■'Gray,R.H.,andJ.M.Haynes. 1976. Upstream movement
of adult salmonids in relation to gas supersaturated water. In
Pacific Northwest Laboratory Annual Report for 1975, p. 73-76.
Vol. I, Life Sciences, Part 2, Ecological Sciences. Battelle,
Pacific Northwest Laboratories, Richland, Wash.

*Liscom, K.L., and G.E. Monan. 1976. Final report, radio

186

River. However, delays of upstream migrants
were generally not considered excessive. We used
radiotelemetry to evaluate effects of Little Goose
Dam on upstream movements of chinook salmon,
Oncorhynchus tshawytscha, in the lower Snake
River, and compared our results with those of pre-
vious studies at other dams.

Materials and Methods

Our telemetry equipment was developed at the
Bioelectronics Laboratory, University of Min-
nesota (Tester and SinifP; Winter et al.^").
Transmitters were pressure-sensitive and permit-
ted determination of salmon location and swim-

tracking studies to evaluate the effects of the spillway deflectors
at Lower Granite Dam on adult fish passage, 1975. Northwest
Fish. Cent., Natl. Mar. Fish Serv., NOAA, Seattle, 18 p.

^Tester, J. R., and D. B. Siniff. 1976. Vertebrate behavior
and ecology progress report for period July 1, 1975-June 30,
1976. COO-1332-123. Prepared for U.S. Energy Research and
Development Administration. Contract No. E(ll-1)-1332. Uni-
versity of Minnesota, Minneapolis, 63 p.

i"Winter, J. D., V. B. Kuechle, D. B. Siniff, and J. R. Tes-
ter. 1978. Equipment and methods for radio tracking fresh-
water fish. Univ. Minn. Agric. Exp. Stn. Misc. Rep. 152-1978,
18 p.

ming depth (Gray and Haynes 1977). Transmit-
ters were individually identifiable and operated
on a carrier frequency of 53 MHz. Transmitter
range varied with depth and transmitter orienta-
tion to a receiving antenna. Transmitter life was
2-3 wk. Receivers were capable of distinguishing
100 discrete crystal-tuned transmitters.

Transmitters used in spring 1976 weighed
about 68 g in water and were 11.5 cm long and 2.7
cm in diameter. Transmitters used in 1977 were
about one-half the weight and two-thirds the vol-
ume of those used initially, weighed about 34 g in
water, and were 7.9 cm long and 1.9 cm in diameter.
In spring 1976 and 1977, chinook salmon
were trapped, anesthetized (tricaine methanesul-
fonate-quinaldine), and tagged externally with
radio and metal-core anchor tags (experimental)
or metal-core anchor tags only (controls). Tagging
was accomplished in cooperation with the Na-
tional Marine Fisheries Service (NMFS) at Little
Goose Dam. Methods of external tag attachment
were reported by Gray and Haynes (1977). After
tagging, salmon were transported 6.4 km down-
stream and released at Texas Rapids (Figure 1).

Total lengths and weights of tagged salmon
ranged from 66 to 100 cm and 3.4 to 11.4 kg and
were consistent with the sizes offish used in other
Columbia River studies (Monan and Liscom see
footnotes 2-6). Fish movements between Lower
Monumental and Lower Granite Dams (Figure 1)
were monitored day and night for the duration of
transmitter life. Tagged fish passing through fish

ladders at Little Goose and Lower Granite Dams
were automatically diverted into fish traps by a
magnetometer-triggered device (Durkin et al.
1969), or observed and recorded at fish-counting
windows. This allowed comparison of travel time
data for control and experimental fish. Total dis-
tance traveled was calculated for each fish by
summing movements between successive loca-
tions.

Results and Discussion

Extensive timing variability among individual
salmon was common throughout the study. How-
ever, travel times of salmon carrying external
radio transmitters and control fish were not sig-
nificantly different (Gray and Haynes 1979). Av-
erage passage delays at Little Goose Dam for
radio-tagged and control salmon (combined) were
216±210 h («=45) in 1976 and 90±57 h{n= 48) in
1977 (Table 1). Passage delays for the same fish at
Lower Granite Dam were <50 ±19 h (n = 3) in
1976 and 58 ±45 h (n = 18) in 1977.

While our observations of delay at Lower Gran-
ite Dam were consistent with previous research at
other Columbia and Snake River Dams (Table 1),
it appears that excessive delays occurred at Little
Goose Dam, especially in 1976. Differences in pas-
sage times at Little Goose Dam compared with
other dams (Table 1) were significant (P<0.05,
Mann- Whitney test).

Several observations indicate extensive salmon

Table l.— Delay of tagged adult chinook salmon below Columbia and Snake River Dams.

Study year(s)

Citation

Tag type'

No. of fish

Tlme2 (h)

Dam

Mean

Range

Bonneville

1948

Schoning and Johnson (text footnote 1)

NT

35

67

62-72

Bonneville

1971

Monan and Liscom (text footnote 2)

R

20

3-63

4-86

Bonneville

1972

Monan and Liscom (text footnote 3)

R

20

141

11-408

Bonneville

1973

Monan and Liscom (text footnote 4)

R

52

''<96

24-384

Bonneville

1974

Monan and Liscom (text footnote 5)

R

42

54

3-540

The Dalles

1972

Monan and Liscom (text footnote 3)

R

30

33

4-69

Rock Island

1954-56

French and Wahle(1956)

NT

2,217

72

48-96

Lower

Monumental

1973

Monan and Liscom (text footnote 6)

R

20

62

—

Lower

Monumental

1975

Gray and Haynes (text footnote 7)

R

20

18

2-42

Little Goose

1975

Gray and Haynes (text footnote 7)

R

10

139

20-288

Little Goose

1976

This study

R, NT

45

216

44-858

Little Goose

1977'

This Study

R, NT

48

90

23-212

Lower Granite

1975

Liscom and Monan (text footnote 8)

R

30

78

—

Lower Granite

1976

This study

R

3

<50

35-72

Lower Granite

1977

This study

R

18

58

2-145

Average passage delays, h:

Little Goose Dam

148.3

±63.5

Other dams

66.0

±31.0

All dams

82.5

±49.9

'R = radio transmitter; NT = nontelemetering fish tag.
^Values averaged over all fish used in a study.
^Time spent in fish ladders only.
^Time from release 6.4 km downstream to dam passage.

187

delays occurred below Little Goose Dam. Radio-
tagged salmon travelled mean distances of 26.5
km in 1976 and 42.0 km in 1977 before crossing
Little Goose Dam, despite its location only 6.4 km
above the Texas Rapids release site. Dropbacks
after arrival of fish in the Little Goose Dam spill
were common, averaging 1 or 2/fish. Delay times
and distances ranged up to 100 h and 40 km/
dropback episode. Radio-tagged (1976-77) salmon
exhibited three movement patterns after release
at Texas Rapids until arrival at Little Goose Dam:
31% (12/39) moved to the dam within 4 to 12 h;
31% ( 12/39) remained within ±5 km of the release
point overnight and moved to the dam the next
day; and 38% (15/39) moved downstream as far as
32 km, and then upstream to the dam 1-6 days
later.

Once an individual salmon began moving up-
stream, it traveled 2-5 km/h and, generally, did
not stop until reaching Little Goose Dam. After
entry into the dam spill, three behavior patterns
were observed: 34% (12/35) crossed the dam 2-5
days after release without dropping back; 40%
(14/35) crossed the dam after averaging 1.6
dropbacks/fish; and 26% (9/35) were not observed
or recorded crossing Little Goose Dam. However,
at least four salmon in the latter group were ob-
served passing Lower Granite Dam or were recov-
ered upstream by anglers or at hatcheries, and
properly belong in the second group.

At Little Goose Dam, especially with continuous
spring 1976 spilling, salmon appeared "confused."
Movements to and from the spill area were com-
mon. Substantial milling, previously reported at
Lower Granite Dam (Liscom and Monan see foot-
note 8), occurred in a large back eddy on the north
side of Little Goose Dam in 1976 and in front of
turbine outflows in 1977. Salmon may use
rheotactic, olfactory and/or acoustical cues to
navigate upstream (Harden Jones 1968). These
cues may be distorted by continuous and heavy
spilling near dams. Milling may be an attempt to
relocate orientation cues (Hasler et al. 1978). In
both study years movements into the fish ladder
were frequent, but salmon frequently fell back and
returned to the spilling basin, especially upon
nearing the trapping facility in midladder.

Periodically, fish trapping operations were
halted to allow large groups of salmon, which were
suspected of accumulating in the spill to pass Lit-
tle Goose Dam (Slatick"). From 26 April to 30
May 1977, the trap was inoperative 17% of the
time (6 of 35 days). However, 30% of all salmon

counted (7,382 of 24,238) at the fish viewing win-
dow by NMFS personnel and 59% (16/27) of our
tagged salmon crossed Little Goose Dam during
nontrapping periods. Daily viewing window
counts of salmon passage averaged 562±497 fish
during trapping and 1,230± 1,040 fish during non-
trapping periods. A ^-test showed these differences
were significant (P<0.05) and indicated trapping
operations at Little Goose Dam impeded chinook
salmon passage.

Other aspects of dam operations affected salmon
passage at Little Goose Dam. One morning in May
1976, spillways were closed for several hours. The
five radio-tagged salmon present left the spill and
moved downstream as far as 16 km. During the 24
h after spilling was restored, fish returned to the
dam. In the absence of spilling in spring 1977,
radio-tagged salmon moved into turbulent areas
created by water leaving power generating tur-
bines at Little Goose and Lower Granite Dams.
When turbine operations were altered, in response
to power generation demands, salmon generally
exited the area and returned after water-flow con-
ditions stabilized. Salmon passage through the
fish ladder was also impeded by turbine operations
(Slatick see footnote 11). Finally, the fish ladder at
Little Goose Dam uses pumped river water rather
than a gravity flow. Of all salmonid species
studied, chinook salmon may be most sensitive to
and least likely to swim through pumped water
(Slatick see footnote 11).

Gray and Haynes (1977) showed that mean
swimming depths of adult chinook salmon in the
Snake River were significantly greater (P<0.05)
in spring 1976 than in spring 1977. However, in
both years, mean swimming depths in the Little
Goose Dam spill were significantly greater
(P<0.05) than in all other sections of the study
area (Haynes 1978). In contrast, swimming depths
in the Lower Granite Dam spill were similar to
those in the open river between dams. As delays
increased in the Little Goose Dam spill, salmon
swimming depths increased. Since fish ladder en-
trances are near the surface, this decreased oppor-
tunities for passage.

Although some delays may have resulted from
tagging, we believe other factors caused the exten-
sive delays observed at Little Goose Dam. First,
our radio-tagged and control salmon had similar
passage times at Little Goose and Lower Granite

•'E. Slatick, National Marine Fisheries Service, Little Goose
Dam, Starbuck, Wash., pers. commun. 1977.

188

Dams in 1976 and 1977 (Gray and Haynes 1979).
Second, the 63*^ passage of internally radio-
tagged salmon in 113 h observed by Liscom and
Monan (see footnote 8) at Lower Granite Dam was
similar to the 699c passage of radio-tagged salmon
in 106 h that we observed in spring 1977 for fish
that crossed Little Goose Dam or were initially
released above it (Haynes 1978).

Our studies provide the first information on
salmon movements near Little Goose Dam. Al-
though they affected salmon movements, spilling
and turbine operations are regular events at all
dams and would not appear to be solely responsi-
ble for excessive delays occurring at Little Goose
Dam. Fish passage delays may have resulted from
tagged salmon being forced to retravel a portion of
their migratory route after release. However, tag-
ging and transport stresses, per se, are common to
all tagging studies. Our salmon (1976-77) moved
to Little Goose Dam in an average of 38 h, a figure
consistent with similar studies at Bonneville Dam
(Monan and Liscom see footnotes 2-5). Thus, our
tagging and handling methods would not appear
to be responsible for extensive delays of salmon
movements upstream.

Dropback and milling of radio-tagged salmon in
the Snake River at Little Goose Dam may be re-
lated to salmon trapping operations. Two factors
that may contribute to trapping effects are the
mechanical aspects of the trap itself and the
possible olfactory sensing of trapped salmon by
other salmon moving up the fish ladder. Trap en-
trances are narrow and steep, the trap emits sharp
noises when operating, and hydraulic fluid may
reach the fish ladder. It is well known that a
human hand in the water of a fish ladder can
interrupt salmon movement. Many authors
(Hasler et al. 1978) have demonstrated great ol-
factory sensitivity among salmon. The presence of
trapped salmon upstream and other disturbances
may inhibit salmon passage through fish ladders.

Extensive passage delays, due to dropback and
milling and greater swimming depths in the spill
below the dam indicate a unique effect of Little
Goose Dam on the upstream migration of chinook
salmon. We observed delays at Little Goose Dam
averaging 148 ±64 h (Table 1). Delays reported at
other dams were significantly less (P<0.05) and
averaged only 66 ±31 h. Cause for great concern is
the 83 ±50 h average delay salmon encounter at
each dam while migrating through the Columbia
and Snake Rivers. Many salmon must pass eight
dams (Figure 1) to reach home spawning areas.

and the additive effects of a 4 wk, multidam pas-
sage delay may significantly influence spawning
success, especially in fall run chinook salmon
which have shown the greatest decline in num-
bers. From 1962 to 1969, before Little Goose Dam
was operational, annual passage of fall chinook
salmon at Ice Harbor Dam averaged nearly 18,000
fish (U.S. Army Corps of Engineers*^). However,
in 1976 and 1977 fall chinook salmon passage at
Ice Harbor Dam was only 1,474 and 1,956 fish
(U.S. Army Corps of Engineersi^-i'*). Little Goose
Dam is 95 km upriver from Ice Harbor Dam (Fig-
ure 1). Since the position of fishways, navigation
locks, and spillways is different at each dam, ef-
fects of each dam must be studied independently.
Only then can methods be devised to increase pas-
sage success throughout the river system.

Acknowledgments

We thank C. D. Becker and the reviewers of the
Fishery Bulletin who criticized the manuscript
and made substantial contributions to its con-
tent; D. W. Crass, S. W. Cubberly, D. D. Dauble,
R. W. Hanf, Jr., J. C. Montgomery, and R. P. Ol-
son, who assisted data collection in the field; and
G. E. Monan, Northwest and Alaska Fisheries
Center, NOAA, Seattle, Wash., and E. Slatick,
Little Goose Dam, Starbuck, Wash., who kindly
provided information on National Marine
Fisheries Service telemetry studies and opera-
tional features of Little Goose Dam. The study was
supported by the U.S. Department of Energy
under Contract EY-76-C-06-1830 with Pacific
Northwest Laboratory, operated by Battelle
Memorial Institute.

Literature Cited

DURKIN, J. T., W. J. EBEL, AND J. R. SMITH.

1969. A device to detect magnetized wire tags in migrating
adult coho salmon. J. Fish. Res. Board Can. 26:3083-
3088.

French, r. r., and r. J. wahle.

1965. Study of loss and delay of salmon passing Rock Is-
land Dam, Columbia River, 1954-56. U.S. Fish. Wildl.
Serv., Fish. Bull. 65:339-368.

12U.S. Army Corps of Engineers. 1969. Annual Fish Pas-
sage Report, Columbia and Snake River Projects, North Pacific
Division. Portland and Walla Walla Districts.

13U.S. Army Corps of Engineers. 1976. Annual Fish Pas-
sage Report. Columbia and Snake River Projects, North Pacific
Division. Portland and Walla Walla Districts.

i-'U.S. Army Corps of Engineers. 1977. Annual Fish Pas-
sage Report. Columbia and Snake River Projects, North Pacific
Division. Portland and Walla Walla Districts.

189

Gray, R. H., and J. M. Haynes.

1977. Depth distribution of adult chinook salmon (On-
corhynchus tshawytscha) in relation to season and gas-
supersaturated water. Trans. Am. Fish. Soc. 106:617-
620.

1979. Spawning migration of adult chinook salmon (On-
corhynchus tshawytscha) carrying external and internal
radio transmitters. J. Fish. Res. Board Can. 36:1060-
1064.
HardenJones, F. R.

1968. Fish migration. Edward Arnold Publ., Lond.,
325 p.
Hasler, a. d., a. T. Scholz, and R. M. HORRALL.

1978. Olfactory imprinting and homing in salmon. Am.
Sci. 66:347-355.

Haynes, J. M.

1978. Movement and habitat studies of chinook salmon
and white sturgeon. Ph.D. Thesis, Univ. Minnesota,
Minneapolis, 168 p.

Johnson, j. H.

I960. Sonic tracking of adult salmon at Bonneville Dam,
1957. U.S. Fish Wildl. Serv., Fish. Bull. 60:471-485.

James M. Haynes

Department of Biological Sciences
State University College
Brockport, NY 14420

ROBERT H. Gray

Freshwater Sciences, Ecosystems Department
Battelle, Pacific Northwest Laboratories
Richland. WA 99352

MATURITY, SPAWNING, AND FECUNDITY OF

ATLANTIC CROAKER, MICROPOGONIAS

UNDULATUS, OCCURRING NORTH OF

CAPE HATTERAS, NORTH CAROLINA

The Atlantic croaker, Micropogonias undulatus, is
an important inshore, bottom fish ranging from
the Gulf of Maine to Bay of Campeche, Mexico
(Chao 1978). United States commercial landings
have reached 50,000 metric tons (t) in recent years
(Gutherz et al. 1975; McHugh 1977), though
dramatic declines in landings have occurred; at
least in the area from Cape Hatteras, N.C., to Cape
Cod, Mass. (Joseph 1972). White and Chittenden
(1977) have postulated the existence of an abrupt
change in life histories and population dynamics
of Atlantic croaker and other species whose ranges
traverse Cape Hatteras. They showed differences
in spawning times, size at maturity, maximum
size and age, and total annual mortality rates of
Atlantic croakers from north and south of Cape
Hatteras and speculated the differences may re-
sult from different temperature regimes.

Few studies exist on reproduction of Atlantic
croaker occurring north of Cape Hatteras. Wallace
(1940) studied size at maturity and sexual de-
velopment offish from Chesapeake Bay and ocean
waters off Virginia and North Carolina. Welsh
and Breder (1923) reported size and age at matur-
ity based on collections from Massachusetts to
Florida. Occurrence of larval stages and gonad
development indicated that spawning occurred
from July through December and peaked during
October and November (Welsh and Breder 1923;
Hildebrand and Schroeder 1928; Wallace 1940).
Haven (1957) and Chao and Musick (1977) found
indications from juvenile length frequencies of
late winter or early spring spawning. The only
report of fecundity was that a 395 mm female
contained approximately 180,000 eggs (Hilde-
brand and Schroeder 1928).

This paper presents size at maturity, spawning
times as indicated by ovarian development, and
fecundity observations of the Atlantic croaker
population north of Cape Hatteras.

Methods

All fish were collected during seven National
Marine Fisheries Service bottom-trawl surveys of
the continental shelf from Cape Hatteras to Block
Island, R.I., during 1973-76 (Table 1). The survey
design and sampling methods were described by
Grosslein (1969). Atlantic croakers were captured
each year between lat. 39°00' N (Cape May, N.J.)
and 35°15' N (Cape Hatteras) in depths from 7 to
131m.

Subsamples of approximately 25 fish, represen-
tative of the length frequency of each catch, were
frozen whole for laboratory examination. Each
fish was weighed (grams), measured (millimeters
total length, TL), sexed, and its maturity stage
was determined using the sexual development
classification and criteria of Wallace (1940).

Table l. — Summary of Atlantic croaker data collected between
Cape May, N.J., and Cape Hatteras, N.C., during 1973-76.

No. of
obser-

Number used In

Collec-

probit analysis

tion no.

Dates

vations

Males

Females

1

9-16 Oct. 1973

556

245

286

2

27-30 Sept 1974

699

324

258

3

16-18 Sept. 1975

79

31

28

4

30Oct.-6Nov. 1975

607

204

145

5

14-17 Dec. 1975

122

—

—

6

6-17 Oct. 1976

438

84

103

7

18 Dec. 1976

16

—

—

Total

2.517

888

820

190

FISHERY BULLETIN: VOL. 78, NO. 1, 1980.

Ovaries in development stage 4 from 1973 and
1974 cruises were exsected, weighed (±0.01 g), and
preserved in a modified Gilson's fluid (Simpson
1951) for subsequent fecundity estimation.

Egg counts for fecundity estimation were made
by a method similar to Bagenal's (1957), but mod-
ified as follows. After 4-6 wk preservation the
ovaries were washed over a 1.0 mm mesh screen
which permitted all the eggs to pass through it but
retained the ovarian tissue. After repeated wash-
ings and decanting the eggs were diluted in water
to a known volume, randomly stirred, and three 10
ml aliquots, each containing from 200 to 400 eggs,
were extracted and the eggs counted using a mi-
croscope. To test the accuracy of the sampling
method two aliquots were extracted from an egg
batch, counted, and replaced until 20 aliquots
were counted. The mean and standard deviation
(SD) of all counts was 255 and 38.3, and the
coefficient of variation (CV) was 15.0%. For the
means of three samples the SD was 20.4 and the
CV was 8.7%. The mean egg number of the three
aliquots times the total dilution volume divided by
the aliquot volume was used to estimate fecundity.

Estimates of length at maturity (length at
which 50% are mature = L^^) were calculated
using probit analysis (Finney 1971). Samples used
in this analysis were collected from September to
November (Table 1; cruises 1-4, 6) which
minimizes the affects of seasonal growth on length
at maturity. The proportion of mature fish for each
centimeter group was calculated for each year by

sex. Table 2 shows the proportion mature by cen-
timeter group for the interval between 0 and 100%
mature. The proportions were transformed to
probits (Fisher and Yates 1964) and the iterative
method was used to calculate the weighted linear
regression equation, Y = a + bX,hy least squares
for the logarithm (base 10) of length iX) and the
probit (7). Chi-square tests indicated no sig-
nificant (x^o.oi ) heterogeneous deviations from the
regression lines; therefore, the regression
coefficients were used to determine L^,.. The var-
iance of L,o was estimated as:

50'

V(L5o) = —

1_
62

l,nw

( Xnwx V

„ / l,nwx\ '
Znwix-— J

\ Lnw /

where n is the number of observations at each
centimeter group, w is the weighting coefficient
(Z2/PQ) (Finney 1971, table II) for probit ( 7), andx
is the logarithm (base 10) of the length.

In order to test for differences in Lg^ between
sexes and between years, 2-values (Natrella 1966)
were calculated using the equation:

'501 ^502

Vv(L50i) + V(L50i)

Table 2. — Percentage mature used in probit analysis by total length group for male (M) and
female (F) Atlantic croaker collected in 1973-76. TV = number of specimens, L^^ = length at 507f

mature, V(L^ )

= variance

of ^50.

and x^ =

for

goodness

of fit of probit regression line.

Total

length

(cm)

1973

1974

1975

1976

M

F

M

F

M

F

M

F

16

0

17

0

0

17

0

18

0

10

0

16

0

13

31

19

17

29

9

0

18

10

67

70

20

69

45

36

10

37

33

89

80

21

90

86

47

23

32

28

91

85

22

94

84

56

35

47

30

90

83

23

89

78

65

47

50

27

100

71

24

92

86

85

74

47

43

94

25

97

94

95

93

78

69

100

26

100

97

98

97

77

79

27

100

100

100

90

82

28

93

100

29

100

N

245

286

324

258

235

173

84

103

^0

19.17

19.81

21.57

22.70

22.35

23.27

18.71

18.52

V(t5c)

0.0190

0.019

0.0357

0.0283

0.0376

0.0356

0 0438

0.0234

X^

15.82

13.82

5.11

3.97

7.07

12.16

4.09

8.66

df

7

9

8

7

11

9

6

7

191

Results and Discussion

Length at Maturity

The matrix of 2-values is shown in Table 3.
Highly significant (2>2.33, P^O.Ol) differences
were found between sexes within years for 1975
and 1976 and between years for each sex except
1973 and 1976 males and 1974 and 1975 females.
This indicates that L^q for males and females was
greater in 1974 and 1975 than in 1973 and 1976.
The greatest difference was found between 1975
and 1976 when L^„ decreased approximately 4.8
cm for females and 3.6 cm for males.

Significant long-term changes in L^^ have oc-
curred since Wallace's (1940) studies of
Chesapeake Bay croakers. The smallest mature
female he observed during 1938-40 was 27.5 cm,
indicating a L^^ of at least 30 cm. His collections
were made during July and August; therefore, due
to additional growth during early fall, 30 cm is an
underestimation of Lg^ for comparison with my
results obtained from September-November.

Spawning

The percentage frequencies of maturity stages
indicate spawning commenced at least as early as
the beginning of September, peaked during Oc-
tober, and ended by late December. The maturity

stages and sample years were combined for
analysis (Table 4). The percentage of ripe ovaries
remained high during September and October,
then dropped to a low level in November. No ripe
females were found in December. As would be
expected the percentage of spawned fish (partially
spent, spent, and resting) increased during the
sampling period and indicated spawning was
nearly completed by mid-December. Because of
difficulty in assigning a specific maturity stage to
testes and since ovarian development was the best
indicator of spawning, males were not analyzed.

The beginning of the spawning season was not
sampled; however, an examination of Wallace's
(1940) maturity stage data for July and August
showed that over 50% of the ovaries were develop-
ing (stages II and III) and <10% were ripe (stage
IV). The remainder was classified as resting (stage
I). Wallace made additional collections in
November which showed that ovaries were either
partially spent (stage VI) or spent (stage VII). His
findings support this study, indicating that
spawning commenced about mid-August and was
completed by the end of December.

The presence of small juveniles (20-40 mm TL)
during April and May have led to speculations of
different spawning populations and a spring
spawning peak. Chao and Musick (1977) appar-
ently detected a modal group "entering" the York
River in May and suggested they may represent

Table 3. — Matrix of 2-values (Natrella 1966) and significance for differences in L,„ (length at which
50% of specimens were mature) of male (M) and female (F) Atlantic croaker collected in 1973-76.

1973

1974

1975

1976

M F

M F

M

F

M

F

1973 M

0.196

7.269" 16.214"

9.632-

17.546**

6.937**

5.779**

F

9.058**

7.544**

3.196**

1974M

4.467**

2.903*

6.367**

6329**

12.546"

F

1.400

12.122**

1975 M

3.400**

8.055**

15.507**

F

9.972**

1976 M

0.729

•PsO.01;

"PsO.OOI.

Table 4. — Percentage frequency of maturity stages of female Atlantic croaker collected between
Cape May, N.J., and Cape Hatteras, N.C., during 1973-76.

Maturity stage

Developing
Ripe

Partially spent
Spent
Resting

Total

Sampling interval

Wallace's

16-18

29 Sept.

5-20

30 Oct-

14-17

stages

Sept.

1 Oct.

Oct. 1973,

6 Nov.

Dec.

(1940)

1975

1974

1976

1975

1975

Hand III

51

29

23

IV and V

46

51

41

12

VI

3

7

13

31

10

VII

11

17

32

28

1

2

6

25

62

42

286

448

196

51

192

progeny from a different spawning population.
Haven (1957) found 20-30 mm fish during April
and concluded the spawning season extended over
almost the entire year with a possible spring peak.
The apparent 9- or 10-mo spawning season may
result from little or no overwinter growth or sam-
pling bias due to differential size distribution or
trawl avoidance (Haven 1957; White and Chitten-
den 1977; Chao and Musick 1977). Maturity ob-
servations made during this study showed essen-
tially all adult fish spawned during August
through December and it is unlikely a spring
spawning peak would occur from the Atlantic
croaker population north of Cape Hatteras.

Fecundity

Fecundity ranged from 100,800 to 1,742,000 for
fish from 196 to 390 mm TL. Preliminary plots of

fish length versus fecundity indicated a curvilinear
relationship and plots of fish weight and ovary
weight versus fecundity appeared linearly re-
lated. Therefore, fish length and fecundity were
transformed to logarithms (base 10) and least
squares regression lines fitted to the data by year
using the equation log fecundity = logo + b (log
length). Fish weight and ovary weight versus
fecundity were related by the linear regression
equation Y =a + bX where Y is fecundity andX is
either fish weight or ovary weight. Analysis of
variance indicated no significant (P«0.05) differ-
ences in variance about the regression between
years for each of fecundity versus length, weight
or ovary weight. Analysis of covariance was used
to test for between years differences in fecundity
relationship. No significant (P = 0.01) difference
was indicated; therefore, regression equations
were calculated for pooled data. Scatter diagrams
and fitted lines are shown in Figures 1-3.

18
17
16
15
14
13

o
o

6 11

o

>

Q

Z

o

Figure l. — Relationship between fecun-
dity and total length for Atlantic croaker
collected in 1973 and 1974.

10
9
8
7
6
5
4
3
2
1

-

•

•

-

log F^-2.586 + 3.361 Hog LI

-

r = 0.86
n=113

-

Syx- 0.1394

-

•

-

•

/

-

f

-

•y

-

-

•

•

jC • •

"

•

_ •

. *. • • ^^

Vt-"^** • . •
^^^-f^ • • ••• •

^ — • • • •• •

J 1 1 1 1 1 ! i : _L

•
•
•

1 \ ^ 1 1 ^ \

190 210 230 250 270 290 310

TOTAL LENGTH imml

330 350

370

193

o
o
o

o
o

Q

z

O
ID

Figure 2. — Relationship between fecun-
dity and fisii weight for Atlantic croaker
collected in 1973 and 1974.

18

17

16

15

14

13

12

11

10

9

8

7

6

5

4

3

2

1

F = -29,175 + 1,624W

r =0.89

n = 113

Sy X =143,755

75 150 225 300 375 450 525 600 675 750 825 900 975 1050
FISH WEIGHT Igl

The correlation coefficients for the relationships
of fecundity to length, weight, and ovary weight
show ovary weight was most closely associated
with the variation of fecundity. Unless the ovaries
are selected, however, ovary weight is the least
reliable predictor of fecundity. It is the most vari-
able parameter and, unless ovaries are collected at
the penultimate development stage, the relation-
ship of ovary weight and fecundity will vary sea-
sonally. Fish weight will also vary seasonally and,
when ovary weight is included with fish weight,
some autocorrelation is present. For general pre-
diction of fecundity, length appears to be the most
reliable measure.

Acknowledgments

I wish to thank the many people who helped
collect samples during National Marine Fisheries
Service cruises and S. J. Wilk and W. G. Smith for

194

their critical reviews of early drafts. Special
thanks to M. Montone for her assistance and typ-
ing of this manuscript and to M. Cox for prepara-
tion of the figures.

Literature Cited

Bagenal, T. B.

1957. The breeding and fecundity of the long rough dab
Hippoglossoides platessoides (Fabr.) and the associated
cycle in condition. J. Mar. Biol. Assoc. U.K. 36:339-375.

Chad, L. N.

1978. A basis for classifying western Atlantic Sciaenidae
(Teleostei: Perciformes). U.S. Dep. Commer., NOAA
Tech. Rep. NMFS Circ. 415, 64 p.
CHAO, L. N., and J. A. MUSICK.

1977. Life history, feeding habits, and functional mor-
phology of juvenile sciaenid fishes in the York River es-
tuary, Virginia. Fish. Bull., U.S. 75:657-702.
FINNEY, D. J.

1971. Probit analysis. 3ded. Camb. Univ. Press, Lond.,
333 p.

o
o
o

d
o

Q

Z

u

UJ

Figure 3. — Relationship between fecun-
dity and ovary weight for Atlantic croaker
collected in 1973 and 1974.

18

17

16

15

14

13

12

11

10

9

8

7

6

5

4

3

2

1

F =8.603 + 19.966V

r 0.98

n =113

Sy x = 67.958

5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85
OVARY WEIGHT Igl

FISHER, R. A., AND F. Yates.

1964. Statistical tables for biological, agricultural and
medical research. 6th ed. Oliver and Boyd, Edinb.,
146 p.
GROSSLEIN, M. D.

1969. Groundfish survey program of BCF Woods
Hole. Commer. Fish. Rev. 31(8-9):22-30.
GUTHERZ, E. J., G. M. RUSSELL, A. R. SERRA, AND B. A. ROHR.
1975. Synopsis of the northern Gulf of Mexico industrial
and food fish industries. Mar. Fish. Rev. 37(7):1-11.
Haven, D. S.

1957. Distribution, growth, and availability of juvenile
croaker, Micropogon undulatus, in Virginia. Ecology
38:88-97.
Hildebrand, S. F., and W. C. SCHROEDER.

1928. Fishes of Chesapeake Bay. Bull U.S. Bur. Fish.
43(1), 366 p.
Joseph, E. B.

1972. The status of the sciaenid stocks of the middle Atlan-
tic coast. Chesapeake Sci. 13:87-100.
MCHUGH, J. L.

1977. Fisheries and fishery resources of New York Bight.
U.S. Dep. Commer., NCAA Tech. Rep. NMFS Circ. 401,
50 p.

NATRELLA, M. G.

1963. Experimental statistics. U.S. Dep. Commer., Natl.
Bur. Stand. Handb. 91, 528 p.
Simpson, a. C.

1951. The fecundity of the plaice. Fish. Invest. Minist.
Agric. Fish. Food (G.B.) Ser. II, 17(5), 27 p.
Wallace, D. H

1940. Sexual development of the croaker, Micropogon un-
dulatus, and distribution of the early stages in
Chesapeake Bay. Trans. Am. Fish. Soc. 70:475-482.
WELSH, W. W., and C. M. BREDER, JR.

1923. Contributions to life histories of Sciaenidae of the
eastern United States coast. Bull. U.S. Bur. Fish.
39:141-201.
White, M. L., and M. E. Chittenden, Jr.

1977. Age determination, reproduction, and population
dynamics of the Atlantic croaker, Micropogonias un-
dulatus. Fish. Bull., U.S. 75:109-123.

Wallace W. Morse

Northeast Fisheries Center Sandy Hook Laboratory
National Marine Fisheries Service, NOAA
Highlands, NJ 07732

195

COMPARISON OF SAMPLING DEVICES FOR

THE JUVENILE BLUE CRAB,

CALLINECTES SAPIDUS^

The behavior of the blue crab, Callinectes sapidus
Rathbun, in the Chesapeake Bay varies consider-
ably with age, temperature, and molting cycle.
These behavioral differences make efforts difficult
to sample effectively the population densities in
the Chesapeake Bay and its tributaries. No single
gear type appears to sample effectively the blue
crab during winter and summer at all depths and
types of bottom. During winter blue crabs burrow
in the mud in the deeper channels of Chesapeake
Bay (Churchill 1917). This pattern is the basis for
an active winter dredge fishery in the lower
portion of the bay (Van Engel 1962). During a 3-yr
survey of blue crabs, Lippson^ found that juveniles
were also present in deeper waters in winter.
Comparative effectiveness of two dredges for
winter sampling of juvenile and adult blue crabs
was reported by Sulkin and Miller (1975).

Blue crabs move about in relatively shallow
water in warm weather presumably because of the
abundance of food here and for protection among
submerged aquatics while in the soft shell
condition. During the summer 7.3 m otter trawls
have been found to be an effective gear to sample
the adult population of blue crabs (Lippson see
footnote 2). The otter trawl, with a small stretch
mesh (0.6 cm) liner in the cod end, is also effective
for catching juveniles in deeper water; however,
juveniles spend much of their time in shallow
waters during the warmer months. The push net
(Figure 1), beach seine, and small otter trawls
have all been used with some degree of success in
this shallow region.

It is the purpose of this study to compare the
effectiveness of the push net, otter trawl, and crab
scrape (Figure 2) in catching juvenile blue crabs in
shallow water.

Methods and Results

Smith Island in the Chesapeake Bay has
extensive grassy (Zostera marina) beds which are
ideal habitats for juvenile crabs (Stevenson and
Confer 1978). This region was chosen to compare

'Contribution No. 992HPEL from the Center for Environmen-
tal and Estuarine Studies, University of Maryland.

^Lippson, R. L. 1969. Blue crab study in Chesapeake
Bay-Maryland. Nat. Resour. Inst. Q. Prog. Rep. 3, Ref No
69-33B:l-13.

the catch effectiveness among a 3.7 m otter trawl,
81.3 cm push net, and a 96.5 cm modified crab
scrape during summer 1975.

The otter trawl opened to a working width of 3.6
m. The gear was towed by the RV Chelae in depths
of 1-2 m for 0.7 km. The cod end was lined with 0.6
cm stretch mesh netting. The trawl door size was
30.5 cm X 61.0 cm and the length of the bridle was
45.7 m.

The push net had a steel frame 81.3 cm wide and
60.9 cm high fitted with a 0.6 cm stretch mesh bag.
The leading edge had a 7 .6 cm diameter pipe which

Figure l. — Push net used for blue crab fishing with the roller
bar on the leading edge.

196

FISHERY BULLETIN: VOL. 78, NO. 1, 1980.

'S*****!

Figure 2. — The crab scrape used for blue crab fishing.

rolled over the bottom. The handle was 1.5 m long.
The net was manually pushed along a 0.7 km
course, waist to chest deep, and parallel to the
shoreline.

The crab scrape, used commercially for catching
shedding crabs, had a metal frame 96.5 cm wide
and 38.1 cm high. The lead bar on the crab scrape
has no teeth, a basic difference between it and a
dredge. A 3.8 cm twine net 182.9 cm long was fitted
to this frame. The crab scrape is towed from a
shallow-draft boat over grassy beds. The crab
scrape used in this study was modified by fitting it
with a 0.6 cm stretch mesh net to retain small (>3
mm) crabs.

The otter trawl and crab scrape were towed
simultaneously beside each other from two small
outboard motorboats for 6 min at an engine speed
of 2,000 r/min. The push net was then pushed
parallel to the trawl and crab scrape tows over the
same distance but closer to shore. The depths for
the trawl and crab scrape tows ranged from 1 to 2
m whereas the push net sampled in depths of
0.6-1.1 m. Eighteen samples were collected for
each gear type.

The sex and size class of crabs were determined
after each tow. Crab size was determined using
carapace width from one lateral spine tip to the
other. Crabs >60 mm wide were excluded from
consideration in this study because they were not
in the most recent year class. Three size classes
were used: class I measured 1 to 20.0 mm; class II,
20.1 to 40.0 mm; and class III, 40.1 to 60.0 mm.

The mean number of crabs per square meter is
shown in Figure 3. It is apparent that the trawl is
comparatively ineffective for classes I and II. The
trawl and push net are about equally as effective
for class III although neither is as effective as the
modified crab scrape for classes I, II, or III. The

TOTAL AREA FISHED
A1552Mi_)08 3 6M^ I2870m2

to

CO

<

u

O

LU
CO

ID

z

24

20

16

12

8

Trawl

Push Net

Crab Scrape

I il ill I II III

SIZE CLASS

I II

Figure 3. — Mean number of blue crabs per square meter for
each haul and total area fished by each gear. Size class (carapace
width) I = 1-20.0 mm, II = 20. 1-40.0 mm, and III = 40. 1-60.0 mm.

crab scrape is the most effective gear for sampling
juvenile blue crabs.

197

Discussion

Acknowledgments

In evaluating various gear for sampling
juvenile blue crabs, a variety of factors should be
considered, such as catch effectiveness, gear cost,
ease of handling, and person hours.

It generally requires two persons to efficiently
operate an otter trawl from a small outboard
motorboat. Handling an otter trawl from a small
outboard motorboat is not only difficult but
dangerous as the net can become fouled in the
propeller. If the net fills with mud or too much
debris, it is impossible to bring the gear on board
and the catch must be sacrificed. The push net is
operable by one person and snags are infrequent.
Mud, as well as high rooted aquatics, makes
pushing the net difficult. The push net is effective
in shallow water (Strawn 1954). Clear shallow
water, however, decreases the effectiveness as
many small crabs see the net approaching and
swim out of its path (pers. obs.). The crab scrape
can be easily handled by one person and seldom
becomes snagged (pers. obs. and observations of
commercial crabbers).

The cost of a 3.7 m otter trawl is about $150.00.
The push net cost varies. They are not available
commercially and must be constructed, usually by
a local blacksmith. The bag may be cut from a
ripped beach seine net. The approximate cost of
the crab scrape is $55.00.

Although gear cost, ease of handling, and hours
involved are considered in gear selection, the most
important factor is catch effectiveness. The push
net was more effective catching small blue crabs
than the trawl but the modified crab scrape was
more effective than either the push net or the
trawl when sampling in shallow water.

Considering all pertinent factors, it would seem
that the crab scrape is the preferred gear for
quantitative studies of juvenile crab abundance.

We thank Fred Dobbs and Marion Ross for their
valuable assistance during the field sampling,
Frances Younger for her technical help in the
preparation of the graphs, and Leo Minasian and
Donna L. Smawley for their photographic
assistance. Our thanks are also extended to Nancy
Robbins and Ida Marbury for their help in the
preparation of the manuscript. This research has
been supported by the National Marine Fisheries
Service and the State of Maryland Fisheries
Administration (Project No. 3-186-R-2, Contract
No. 04-5-043-43).

Literature Cited

Churchill, E. p., Jr.

1917. Life-history of the blue crab of the Chesapeake
Bay. Off. Bull., Conserv. Comm. Md. 2:11-18.
STRAWN, K.

1954. The pushnet, a one-man net for collecting in
attached vegatation. Copeia 1954:195-197.
SULKIN, S. D., AND R. E. MILLER.

1975. Modified commercial crab and oyster dredges as
sampling devices for the blue crab Callinectes sapidus
Rathbun. Chesapeake Sci. 16:137-139.
STEVENSON, J. C, AND N. M. CONFER.

1978. Summary of available information on Chesapeake
Bay submerged vegatation. U.S. Fish Wildl. Serv., Off.
Biol. Serv. FWS/OBS-78/66, 335 p.

Van engel, w. a.

1962. The blue crab and its fishery in Chesapeake Bay.
Part 2 - Types of gear for hard crab fishing. Commer.
Fish. Rev. 24(9):1-10.

ROBERT E. Miller

Horn Point Environmental Laboratories
Center for Environmental and Estuarine Studies
University of Maryland
P.O. Box 775, Cambridge, MD 21613

DOUGLAS w. Campbell
Pamela J. Lunsford

Fisheries Administration

Maryland Department of Natural Resources

Tawes State Office Building

Annapolis, MD 21401

198

NOTICES

NOAA Technical Reports NMFS published during the last 6 mo of 1979.

Circular

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426. Synopsis of biological data on the rock crab.
Cancer irroratus Say. By Thomas E. Bigford. May
1979, V + 26 p., 11 fig., 21 tables. Also FAO Fisheries
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427. Ocean variability in the U.S. Fishery Conserva-
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D. Haynes, editors. July 1979, iv + 362 p.

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Special Scientific Report — Fisheries

735. History of the fishery and summary statistics of
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199

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Fishery Bulletin

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Contents-Continued

.4-.. ■ fi- . ;-^' ilv

TESTA VERDE, SALVATORE A., and JAWfes G. MEAD: Southern distribution of
the Atlantic whitesided dolphin, Lagenorhynchus acutus, in the western North
Atlantic , .- 167

MATARESE. ANN C, and DAVID L. STEIN. Additional records of the sculpin
Psychrolutes phrictus in the eastern Bering Sea and off Oregon 169

ODELL, DANIEL K., EDWARD D. ASPER, JOE BAUCOM, and LANNY H. COR-
NELL. A recurrent mass stranding of the false killer whale, Pseudorca crassi-
dens, in Florida 171

BRANSTETTER, STEVEN, and ROBERT L. SHIPP. Occurrence of the finetooth
shark, Carcharhinus isodon, off Dauphin Island, Alabama 177

BAGLIN, RAYMOND E., JR., MARK I. FARBER, WILLIAM H. LENARZ, and JOHN
M. MASON, JR. Shedding rates of plastic and metal dart tags from Atlantic blue-
fin tuna, Thunnus thynnus 179

HAYNES, JAMES M., and ROBERT H. GRAY. Influence of Little Goose Dam on
upstream movements of adult chinook salmon, Oncorhynchus tshawytscha 185

MORSE, WALLACE W. Maturity, spawning, and fecundity of Atlantic croaker,
Micropogonias undulatus, occurring north of Cape Hatteras, North Carolina 190

MILLER, ROBERT E., DOUGLAS W. CAMPBELL, and PAMELA J. LUNSFORD.
Comparison of sampling devices for the juvenile blue crab, Callinectes sapidus . . . 196

Notices
NOAA Technical Reports NMFS published during the last 6 mo of 1979 199

ft GPO 696-404

'^'-^TES O^ ^

Bulletin

MarineBioiogical Laboratory

LIBRARY

DEC 2 198)

Wood*; Huit!, Ma^ii.

r

Vol. 78, No. 2

April 1980

RANDALL, JOHN E. A survey of ciguatera at Enewetak and Bikini, Marshall
Islands, with notes on the systematics and food habits of ciguatoxic fishes 201

SMYTH, PETER 0. Callinectes (Decapoda: Portunidae) larvae in the Middle Atlan-
tic Bight, 1975-77 251

HUPPERT, D. D. An analysis of the United States demand for fish meal 267

POTTHOFF, THOMAS. Development and structure of fins and fin supports in dol-
phin fishes Coryphaena hippurus and Coryphaena equiselis (Coryphaenidae) 277

KNIGHT, MARGARET D. Larval development of Euphausia eximia (Crustacea:
Euphausiacea) with notes on its vertical distribution and morphological divergence
between populations 313

STONER, ALLAN W. Feeding ecology of Lagodon rhomboides (Pisces: Sparidae):
variation and functional responses 337

MEAD, JAMES G., DANIEL K. ODELL, RANDALL S. WELLS, and MICHAEL D.
SCOTT. Observations on a mass stranding of spinner dolphin, Stenella longiros-
tris , from the west coast of Florida 353

EBELING, ALFRED W., RALPH J. LARSON, WILLIAM S. ALEVIZON, and
RICHARD N. BRAY. Annual variability of reef-fish assemblages in kelp forests
off Santa Barbara, California 361

PIETSCH, THEODORE W, and JEFFREY A. SEIGEL. Ceratioid anglerfishes of
the Philippine Archipelago, with descriptions of five new species 379

RICHARDSON, SALLY L., JEAN R. DUNN, and NANCY ANNE NAPLIN. Eggs
and larvae of butter sole, Isopsetta isolepis (Pleuronectidae), off Oregon and
Washington 401

WEINSTEIN, MICHAEL R, SIDNEY L. WEISS, RONALD G. HODSON, and
LAWRENCE R. GERRY. Retention of three taxa of postlarval fishes in an inten-
sively flushed tidal estuary, Cape Fear River, North Carolina 419

OLIVER, JOHN S., PETER N. SLATTERY, LARRY W. HULBERG, and JAMES W
NYBAKKEN. Relationships between wave disturbance and zonation of benthic
invertebrate communities along a subtidal high-energy beach in Monterey Bay,
California 437

FERRARO, STEVEN R Daily time of spawning of 12 fishes in the Peconic Bays,
New York 455

BULLARD, FERN A., and JEFF COLLINS. An improved method to analyze tri-
methylamine in fish and the interference of ammonia and dimethylamine 465

(Continued on back cover)

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NATIONAL MARINE FISHERIES SERVICE

Fishery Bulletin

The Fishery Bulletin carries original research reports and technical notes on investigations in fishery science, engineering, and
economics. The Bulletin of the United States Fish Commission was begun in 1881; it became the Bulletin of the Bureau of Fisheries in
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Scientific Editor, Fishery Bulletin

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Auke Bay Laboratory

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Fishery Bulletin

CONTENTS

Vol. 78, No. 2 April1980

RANDALL, JOHN E. A survey of ciguatera at Enewetak and Bikini, Marshall
Islands, with notes on the systematics and food habits of ciguatoxic fishes 201

SMYTH, PETER O. Callinectes (Decapoda: Portunidae) larvae in the Middle Atlan-
tic Bight, 1975-77 251

HUPPERT, D. D. An analysis of the United States demand for fish meal 267

POTTHOFF, THOMAS. Development and structure of fins and fin supports in dol-
phin fishes Coryphaena hippurus and Coryphaena equiselis (Coryphaenidae) 277

KNIGHT, MARGARET D. Larval development of Euphausia eximia (Crustacea:
Euphausiacea) with notes on its vertical distribution and morphological divergence
between populations 313

STONER, ALLAN W. Feeding ecology of Lagodon rhomboides (Pisces: Sparidae):
variation and functional responses 337

MEAD, JAMES G., DANIEL K. ODELL, RANDALL S. WELLS, and MICHAEL D.
SCOTT. Observations on a mass stranding of spinner dolphin, Stenella longiros-
tris, from the west coast of Florida 353

EBELING, ALFRED W., RALPH J. LARSON, WILLIAM S. ALEVIZON, and
RICHARD N. BRAY. Annual variability of reef-fish assemblages in kelp forests
off Santa Barbara, California 361

PIETSCH, THEODORE W, and JEFFREY A. SEIGEL. Ceratioid anglerfishes of
the Philippine Archipelago, with descriptions of five new species 379

RICHARDSON, SALLY L., JEAN R. DUNN, and NANCY ANNE NAPLIN. Eggs
and larvae of butter sole, Isopsetta isolepis (Pleuronectidae), off Oregon and
Washington 401

WEINSTEIN, MICHAEL R, SIDNEY L. WEISS, RONALD G. HODSON, and
LAWRENCE R. GERRY. Retention of three taxa of postlarval fishes in an inten-
sively flushed tidal estuary. Cape Fear River, North Carolina 419

OLIVER, JOHN S., PETER N. SLATTERY, LARRY W. HULBERG, and JAMES W.
NYBAKKEN. Relationships between wave disturbance and zonation of benthic
invertebrate communities along a subtidal high-energy beach in Monterey Bay,
California 437

FERRARO, STEVEN R Daily time of spawning of 12 fishes in the Peconic Bays,
New York 455

BULLARD, FERN A., and JEFF COLLINS. An improved method to analyze tri-
methylamine in fish and the interference of ammonia and dimethylamine 465

(Continued on next page)

Seattle, Washington
1980

For sale by the Superintendent of Documents, US. Government Printing Office, Washington,
DC 20402— Subscription price per year: $12.00 domestic and $15.00 foreign. Cost per single
issue: $3.00 domestic and $3.75 foreign.

Contents-continued

O'CONNELL, CHARLES P. Percentage of starving northern anchovy, Engraulis
mordax, larvae in the sea as estimated by histological methods 475

EBEL, WESLEY J. Transportation of chinook salmon, Oncorhynchus tshawytscha,
and stee\h.eaid,Salmo gairdneri, smolts in the Columbia River and effects on adult
returns 491

BENIRSCHKE, K., MARY L. JOHNSON, and ROLF J. BENIRSCHKE. Is ovula-
tion in dolphins, Stenella longirostris and Stenella attenuata, always copulation-
induced? 507

Notes

PEARCY, WILLIAM G. A large, opening-closing midwater trawl for sampling
oceanic nekton, and comparison of catches with an Isaacs-Kidd midwater trawl . . 529

COE, JAMES M., and WARREN E. STUNTZ. Passive behavior by the spotted
dolphin, Stenella attenuata, in tuna purse seine nets 535

KRAEUTER, JOHN N., and MICHAEL CASTAGNA. Effects of large predators on
the field culture of the hard clam, Mercenaria mercenaria 538

PARKER, KEITH. A direct method for estimating northern anchovy, Engraulis
mordax, spawning biomass 541

PITCHER, KENNETH W Food of the harbor seal, Phoca vitulina richardsi, in the
Gulf of Alaska 544

JOHNSON, JAMES H. Production and growth of subyearling coho salmon, On-
corhynchus kisutch, chinook salmon, Oncorhynchus tshawytscha, and steelhead,
Salmo gairdneri , in Orwell Brook, tributary of Salmon River, New York 549

Vol. 78, No. 1 was published on 28 August 1980.

The National Marine Fisheries Service (NMFS) does not approve, rec-
ommend or endorse 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 pro-
motion which would indicate or imply that NMFS approves, recommends
or endorses any proprietary product or proprietary material mentioned
herein, or which has as its purpose an intent to cause directly or indirectly
the advertised product to be used or purchased because of this NMFS
publication.

A SURVEY OF CIGUATERA AT ENEWETAK

AND BIKINI, MARSHALL ISLANDS, WITH NOTES ON

THE SYSTEMATICS AND FOOD HABITS OF CIGUATOXIC FISHES^

John E. Randall^

ABSTRACT

A total of 551 specimens of 48 species of potentially ciguatoxic fishes from Enewetak and 256 specimens
of 23 species from Bikini, Marshall Islands, were tested for ciguatoxin by feeding liver or liver and
viscera from these fishes to mongooses at 10% body weight (except for sharks, when only muscle tissue
was used.) The fishes are representatives of the following families: Orectolobidae, Carcharhinidae,
Dasyatidae, Muraenidae, Holocentridae, Sphyraenidae, Mugilidae, Serranidae, Lutjanidae, Leth-
rinidae, Carangidae, Scombridae, Labridae, Scaridae, Acanthuridae, and Balistidae. The species
selected were all ones for which toxicity can be expected, including the worst offenders from reports of
ciguatera throughout Oceania; only moderate to large-sized adults were tested. In all, 37.3% of the
fishes fi-om Enewetak and 19. 7"%- from Bikini gave a positive reaction for ciguatoxin. Because liver and
other viscera are more toxic than muscle, the percentage of positive reactions at the level which might
cause illness in humans eating only the flesh of these fishes collectively would drop to 16.2 for
Enewetak and 1 .4 for Bikini. This level of toxicity is not regarded as high for Pacific islands, in general .

Because ciguatoxin is acquired through feeding, the food habits of these fishes were investigated.
Most of the highly toxic species, including seven of the eight causing severe illness or death in the test
animals (Lycodontis javanicus , Cephalopholis argus, Epinephelus hoedtii, E. microdon , Plectropomus
leopardus, Aprion virescens, and Lutjanus bohar) are primarily piscivorous. Some such as Lethrinus
kallopterus (which also produced a mongoose death) feed mainly on echinoids and mollusks. Among the
larger herbivorous fishes that were tested, only one individual ofKyphosus and two ofScarus caused a
weak reaction in the test animals.

In view of the importance of correct identification of the ciguatoxic fishes, diagnostic remarks and an
illustration are provided for each of the species tested. Some alteration in scientific names was
necessary for a few of the fishes.

The Marshall Islands are the easternmost islands
of Micronesia and of the Trust Territory of the
Pacific Islands. They consist of 34 low islands,
most of which are atolls, and numerous reefs
which occur between lat. 4° 30' and 15° N and long.
161° and 173° E. They lie in two parallel groups in
a northeast-southwest direction, the easternmost
being the Ratak ("Sunrise") Chain and the west-
ernmost the Ralik ("Sunset") Chain.

Two tj^jes offish poisoning are known from the
Marshall Islands: tetraodontid (puffer) poisoning
(Hiyama 1943; Yudkin 1944; Halstead 1967) and
ciguatera. This paper is restricted to the latter
toxemia. It results from the ingestion of a great
variety of tropical reef and semipelagic fishes.
Ciguatoxin is thermostable, hence unaffected by
cooking or freezing of the fishes. It is not the result
of decomposition but is present to a varying degree

'Contribution of the Mid-Pacific Research Laboratory.
^Bemice P. Bishop Museum, Box 19000-A, Honolulu, HI
96819.

Manuscript accepted October 1979.
FISHERY BULLETIN: VOL. 78, NO. 2, 1980.

in the different tissues of fishes when entirely
fresh. The severity of the illness and the
symptomatology depend upon the concentration of
the toxin and the amount of fish eaten; fatalities
are rare. Symptoms appear about 1-10 h after a
toxic fish is consumed; those most commonly given
are: weakness or prostration; diarrhea; tingling or
numbness of the lips, hands, and feet; confusion of
the sensations heat and cold; nausea; joint and
muscular pain; inability to coordinate voluntary
muscular movements; difficulty in breathing;
burning urination; and itching. Probably the most
common diagnostic symptoms are unpleasant
tingling sensations of the palms of the hands and
soles of the feet on contact with cool materials and
the feeling of heat when cold objects are touched or
cold liquids taken into the mouth. Light cases may
not exhibit these sensations, however.

The Marshall Islands have long been known to
harbor ciguatoxic fishes. The earliest report from
these islands seems to be that of Steinbach ( 1895)
who wrote of fishes being toxic on the west side of

201-

FISHERY BULLETIN: VOL. 78, NO. 2

the lagoon at Jaluit. Becke (1901) recorded
poisonous fishes from Rahk (Ebon), the south-
ernmost atoll in the Marshalls (reference from
Halstead 1967). With the takeover of the Mar-
shalls by Japan at the start of World War I ( 1914),
the documentation of ciguatera at these islands
shifted to the Japanese. Hishikari ( 1921), Matsuo
(1934), and Hiyama (1943) published on poisonous
fishes at Jaluit. Some fishes in the vicinity of
Utirik Island, Utirik Atoll, have been reported as
poisonous (Hydrographic Office, U.S. Navy 1945).

Historically, Jaluit was the principal atoll of the
Marshalls. It was the center of government, had
the greatest shipping activity, and the highest
population (1,683 in 1933). As a result of military
activity during World War II, Kwajalein (the
largest atoll in the world) and Majuro became
more important. Majuro is the District Adminis-
trative Center of the islands. By 1958 the popula-
tion was 3,336 (compared with 783 in 1935),
whereas the population at Jaluit had declined to
1,112 in 1958 (Robson 1959).

Concurrent with the buildup in population and
commerce at Majuro and Kwajalein was the ap-
pearance of ciguatera (or at least the first records
in the literature of its incidence). Halstead and
Lively (1954) reported one death and five persons
seriously ill from the consumption of a moray eel
at Kwajalein. Bartsch et al. (1959, table 2)
documented the marked increase in cases of fish
poisoning at the hospital at Majuro; there were 22
in 1955 (all in the last half of the year), 100 in
1956, and 211 in 1957. Banner and Helfrich ( 1964)
stated that the atolls in the Marshall Islands
where poisonous fishes are most commonly found
are Kwajalein, Mille, Ailinglaplap, Jaluit, and
Majuro. They tested numerous fishes of many
species from Enewetak (formerly spelled
Eniwetok) collected in 1958, but none were found
to be toxic. Balaz,^ on the other hand, interviewed
Chief Johannes, the last remaining traditional
chief of the Enewetak people, at Majuro on 15
March 1974. Johannes stated that poisonous
fishes were known at the atoll at the time of his
departure in 1946 from the islands of the eastern
side between the deep passage and the northern
end. It should be pointed out, however, that a
short-term field survey of ciguatera at an atoll,
such as that carried out by Banner and Helfrich, is
difficult to equate to the continuous human bioas-

'George H. Balaz, Research Associate, Hawaii Institute of
Marine Biology, pers. commun. 1974.

202

say of a population of native people dependent on
fishes as their principal source of protein. One
should also emphasize that even in highly toxic
sectors, the percentage of poisonous fishes that
will cause ciguatera when eaten is small. Never-
theless, only a few cases in an area may be needed
to prevent residents from fishing in that area.

The atolls of Enewetak and Bikini are located at
the northern end of the Ratak Chain 165 mi apart
between lat. 11° and 12° N. The native people of
Bikini were moved from their island to Rongerik
Atoll and later to Kill Island when a series of
nuclear explosion tests were carried out by the
United States beginning in 1946. The people of
Enewetak were transferrred to Ujelang Atoll in
1947 for the same reason. When repatriation of
these Micronesian people was contemplated, a
question arose as to the current level of toxicity of
the food fishes of Bikini and Enewetak.

Fluctuation in the toxicity of fishes in reef
ecosystems has long been recognized (Banner and
Helfrich 1964; Cooper 1964; Halstead 1967; and
Helfrich and Banner 1968). Furthermore, Randall
(1958) hypothesized that disruptions of the marine
environment resulting in the creation of new sur-
faces (particularly the repetitive formation of new
surfaces) in potentially ciguatoxic areas may be
linked to outbreaks of the toxemia. This
hypothesis has received support from Cooper
(1964) who related toxic sectors in the Gilbert Is-
lands to the locations of wrecks and anchorages, by
Helfrich et al. (1968) who documented the first
outbreak of ciguatera at Washington Island, Line
Islands, following the wreck of the MS Southbank
in late 1964, and by Bagnis (1969) who reported
numerous cases of ciguatera at the previously
nontoxic atoll of Hao in the Tuamotu Archipelago
after the atoll was altered as a staging area for
nuclear testing at Mururoa.

de Sylva (1963) misinterpreted this hypothesis.
He stated that Randall found poisonous fishes in
estuarine areas. On the contrary, Randall re-
ported toxic fishes in the Society Islands from cer-
tain areas of slight or intermittent freshwater
drainage which are ordinarily flushed with clear
water from the open sea. During periods of heavy
rain the freshwater runoff to a normally marine
habitat may cause death of stenohaline sessile
marine animals, thus forming a new surface for
benthic growth.

After stating that the basic toxic organism must
be benthic, Randall (1958) wrote, "Since obli-
gately herbivorous fishes and detritus-feeding

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

fishes may be poisonous, the toxic organism would
most likely be an alga, a fungus, a protozoan, or a
bacterium." He added that if it were an alga it
must be fine because certain potentially toxic sur-
geonfishes are unable to feed on coarse types. Of
the algae, he wrote that blue-greens were the most
probable source of ciguatoxin.

Yasumoto et al. (1977), however, have shown
that the "likely culprit" of ciguatera is a di-
noflagellate which lives attached to dead coral or
benthic algae. Though identified initially as a new
species of Diplopsalis, it was later shown (Taylor
1979) to be a new genus as well. Subsequently,
Adachi and Fukuyo (1979) named it Gambierdis-
cus toxicus. Although a fat-soluble toxin, later
identified as ciguatoxin, was isolated from wild
dinoflagellates of this species, this organism pro-
duced "... only meager amounts of ciguatoxin, if
any,. . ." under culture conditions (Yasumoto et al.
1979).

The author first visited Enewetak in 1967, then
in use as the terminus of a missile range by the
United States. The resident personnel had been
informed of the hazard of ciguatera, and local reef
fishes were not served in the mess. In spite of the
warning, some cases of ciguatera still occur, espe-
cially with the crews on supply ships to the island
who sometimes catch and eat fishes, particularly
red snapper, Lutjanus bohar, from the vessels be-
fore they could be informed of the danger. The
most recent case was reported by Roth.'*

In 1968 six residents of the atoll ate a large
reddish brown grouper with small blue spots
(probably Plectropomus leopardus) that one of
them had caught off the garbage pier at the
southwest end of Enewetak Island. They had
asked a cook in the mess hall to prepare the fish for
a meal. The cook refused, explaining that the
species was one which could make them sick. Dis-
believing, the men took the fish to their quarters
and cooked it themselves. They all contracted
ciguatera and were hospitalized (Spillman).

These cases offish poisoning and the knowledge
that the marine environments of both Enewetak
and Bikini have indeed been disrupted underlined
the need for a survey of ciguatera at the two atolls.

The survey was supported by the U.S. Energy

"Robert M. Roth, Capt. USAF, MC, Command Surgeon, Joint
Task Group, Enewetak, described the illness (symptoms typical
of ciguatera) of Francisco Romolor, age 28, a civilian deckhand
on the cargo ship Muskingum, following ingestion of a red snap-
per caught in the lagoon (pers. commun. 2 June 1978).

^Louis C. Spillman, Jr., Chief Medical Officer, Enewetak, pers.
commun. 1968.

Research and Development Administration (now
Department of Energy). The field work at
Enewetak was based at the Mid-Pacific Marine
Laboratory, and the fishing at Bikini was carried
out from the RV Liktahur.^ The testing of fishes
for ciguatoxin was done at the Hawaii Institute of
Marine Biology, University of Hawaii, under the
supervision of A. H. Banner.

Six fishing expeditions of 2 to 4 wk duration
were dispatched from Hawaii to Enewetak within
the period September 1974-May 1978. There were
four fishing cruises to Bikini (fishing periods of 3-7
days at the atoll) from December 1974 to July
1976. In addition, 12 potentially toxic L. bohar
were caught from the Liktanur at the atoll of
Rongelap in November 1975.

Fishes were collected by spearing, hook and
line, trolling lures, explosives, and the ichthyocide
rotenone. The specimens were held in chests of
crushed ice until they were returned either to the
Mid-Pacific Marine Laboratory or the Liktanur.
They were then measured and weighed, tagged
with a metal tag, and a sample taken for testing
which included the liver, other viscera, and mus-
cle. A data sheet was filled out for each specimen;
the upper half of each sheet was used for field data
and the lower half to record the testing for toxicity.
A chart of the atoll was printed on the back of each
data sheet (separate sets of sheets were main-
tained for Enewetak and Bikini) so that the local-
ity of capture could be recorded. At Enewetak the
entire fish was frozen after the sample was taken
for testing. Aboard the Liktanur only the samples
were retained. The Enewetak specimens, which
proved to be highly toxic (rated 4 or 5, see below),
were transported frozen to the University of
Hawaii for use in biochemical and pharmacologi-
cal research on ciguatoxin; the remaining fishes
were either discarded or used as bait or chum.

For the testing, the samples of fish were fed to
mongooses (Herpestes mungo) in single meals at
10% body weight. The mongoose is a good animal
for the bioassay of ciguatoxin (Banner et al. 1960)
because it has a symptomology similar to humans
suffering from ciguatera, it retains a meal of toxic
fishes (in contrast to cats which are prone to re-
gurgitate fish when it is very poisonous), and be-
cause of its availability in Hawaii (where it is
regarded as a pest). The mongoose symptoms were

«The RV Liktanur is a converted U.S. Navy LCM, 115 ft in
length, operated then by the U.S. Energy Research and De-
velopment Administration as a research and supply vessel.

203

FISHERY BULLETIN: VOL. 78, NO. 2

divided into five progressive categories from 1
(diarrhea, slight weakness, and flexion of the
forelimbs) to 5 (death within 48 h). The lack of
symptoms was recorded as 0. The tests which re-
sulted in a reaction of 4 or 5 were repeated on other
mongooses if sufficient material was available.
Also any questionable or unexpected tests were
repeated.

Two tests were run on most of the fishes, one
based on the feeding of liver or liver and viscera to
the mongooses and one on muscle tissue. The liver
of a toxic fish invariably gave a stronger reaction
than muscle. A reaction of 3 to liver feeding would
generally elicit a reaction of 1 with flesh. Helfrich
et al. (1968) found liver more than 50 times as
toxic as the muscle tissue of L. bohar. The remain-
ing viscera are also more toxic than somatic mus-
cle. Since the liver alone was often insufficient in
mass to provide a meal to a mongoose at 10% body
weight, it was usually necessary to combine it
with other viscera (generally alimentary tract
tissue).

The level of toxicity reported herein is from the
liver-viscera feeding, with the exception of sharks.
Shark liver may cause a toxemia from the high
level of vitamin A. Furthermore, it was noted that
mongooses will either not eat shark liver or will
not consume enough to equal 10% of their body
weight. Thus the toxicity data on sharks are based
on muscle tissue alone.

Once a mongoose exhibited symptoms of cigua-
tera, it was not used again for testing. If it showed
no symptoms at all, it was used a second time, but
only after a period of at least 1 wk had elapsed. No
mongooses were fed potentially toxic fish more
than three times even when no symptoms were
elicited. The reason for this is the known tendency
for ciguatoxin to accumulate in a test animal.
Though a fish may cause no illness when eaten, it
may still have some toxin at the subsymptomatic
level. Eating several such fishes in succession
might result in a positive test for the last one, even
though there was insufficient toxin to produce ill-
ness in a mongoose consuming such a fish for the
first time.

The results of our first sampling of potentially
toxic fishes at Enewetak and Bikini did not in-
dicate a high level of toxicity. Only the larger
individuals of the usual offending species' were
poisonous. Most of these species are carnivores,
in particular those feeding heavily on fishes
(Randall 1958). Therefore, subsequent fishing
was concentrated on the larger fishes of these

species. Because of this selectivity, both for spe-
cies and size, more fishing effort was spent per fish
caught; however, this meant less effort expended
later in useless testing.

Prior to the present study, information on the
food habits of ciguatoxic fishes was insufficient for
most species. When a trained marine biologist
familiar with the Marshallese marine biota was
present, an analysis was made of the stomach con-
tents of the fishes that were caught. Since cigua-
toxin is known to pass through food chains to the
larger fishes, where it is concentrated, analyses
of the stomach contents of these fishes are needed
for an understanding of the feeding inter-
relationships.

Some previously unpublished stomach-content

Table l. — Summary of mongoose feeding tests (liver- viscera,
sharks excepted) of fishes collected at Enewetak (0 = nontoxic;
5 = death of test animal).

Intensity of reaction

Species

Nebrius ferrugineus

Carcharhinus albimarginatus

C. amblyrhynchos

C galapagensis

C. Iimbatus

Galeocerdo cuvier

Triaenodon obesus

Taeniura melanospilos

Lycodontis javanicus

Adioryx spinifer

Sphyraena barracuda

Cephalophalis argus

Epinephelus fuscoguttatus

E. hoedtii

E. maculatus

E. microdon

£. socialis

E. tauvina

Plectropomus leopardus

P. melanoleucus

P. truncatus

Variola louti

Aprion virescens

Lutjanus bohar

L. fulvus

L. gibbus

L. monostigmus

Macolor niger

Lethrinus amboinensis

L kallopterus

L. miniatus

L. xanthochilus

Monotaxis grandoculis

Kyphosus cinerascens

Caranx ignobilis

C. lugubris

C. melampygus

C. sexfasciatus

Gymnosarda unicolor

Cheilinus undulatus

Coris aygula

Epibulus insldiator

Hipposcarus harid

Scarus gibbus

S. rubroviolaceus

Acanthurus xanthopterus

Balistoides viridescens

2

4

11

1

2
8
1

6
3
2
2
6
8
8
2
4
12

13

8

56

2

21

1

23

24

14

6

2

4

1

3

11

24

2

7

6

4

5

3

18

3

2

1

4

1
22

2 1

3

4 1

1

8 13

1

8 4

1

1

2

1

11 5

5 2
1 1
2

Totals

346

74

53 37

11

204

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

analyses obtained by the author from localities
other than the Marshall Islands have been in-
cluded in this report. The food habit data are pre-
sented in the species accounts following the assay
of toxicity.

The length measurement most often used for
bony fishes was standard length (SL). This was
taken from the front of the snout to the end of the
hypural plate (hence base of caudal fin). When the
method of measuring length is not specified, stan-
dard length is intended. Fork length (FL) was used
for carangids and scombrids because scutes or
keels laterally on the caudal peduncle prevent the
accurate external determination of the base of the
caudal fin. Total length (TL) was employed for
eels, nurse sharks, and some proportional mea-
surements. The length usually given for requiem
sharks is precaudal length (PCL).

Schultz and collaborators (1953-66) was the
primary reference for the identification of
ciguatoxic fishes and the fishes from their
stomachs. Enewetak and Bikini were among the
islands from which large collections of fishes were
made for this systematic work. When names other
than those given by Schultz and collaborators are
used, an explantion is given in the species
accounts.

The species of ciguatoxic fishes which were
studied are discussed in approximate phylogenetic
sequence below. The results of the mongoose feed-
ing tests are summarized in Table 1 for Enewetak
and Table 2 for Bikini.

RESULTS

Orectolobidae (Nurse Sharks)
Nebrius ferrugineus (Lesson) (Figure 1): Like

Table 2. — Summary of mongoose feeding tests (liver-viscera,
sharks excepted) of fishes collected at Bikini (0 = nontoxic; 5 =
death of test animal).

Intensify of reaction

Species

0

1 2

3 4

5

Carcharhinus amblyrhynchos

1

Galeocerdo cuvier

1

Sphyraena barracuda

1

1 1

S. forsteri

2

Crenimugil crenilabis

3

Epinephelus hoedtii

1

E maculatus

2

E. microdon

2

1 4

1

1

E. tauvina

1

1

Plectropomus leopardus

1

Variola louti

2

Aprion virescens

7

1

Lutjanus bohar

112

15 8

6 2

L gibbus

32

3

L monostigmus

4

1

Lethrinus amboinensis

9

L kallopterus

2

L miniatus

12

L xanthochilus

2

Caranx igriobilis

2

C. melampygus

6

Gymnosarda unicolor

3

Pseudobalistes flavimarginatus

2

Totals

208

22 16

7 2

1

other orectolobids, this shark has a prominent
nasal barbel, relatively small mouth, the fourth
and fifth gill openings over the pectoral base, and
the two dorsal fins set posteriorly on the body. The
teeth, which are small and in numerous rows (the
first three or four functional), have a large central
cusp with four to six smaller cusps on each side
(the teeth of the related genus Ginglymostoma
have an even larger central cusp and only two
small cusps on each side). The two dorsal fins are of
nearly equal size, the first originating slightly an-
terior to the origin of the pelvic fins and the second
distinctly anterior to the origin of the anal fin; the
caudal fin is about 2>Q% TL.

Nebrius concolor Riippell appears to be a junior
synonym. Bass et al. (1975b) employed this name,

Figure l.— Nebrius ferrugineus. 1,080 mm PCL, 1,496 mmTL, 18.1 kg, Enewetak, Marshall Islands.

205

FISHERY BULLETIN: VOL. 78, NO. 2

but admitted that Lesson's ferrugineus might
have priority.

This shark is a shallow-water species, usually
seen at rest on the bottom during daylight hours.
It is not common in the Marshall Islands. Two
specimens were obtained from Enewetak, 1,400
and 1,487 mm TL, weighing 11.7 and 14.1 kg. The
flesh of neither was toxic.

Fourmanoir (1961) stated that the principal
food of this shark consists of octopuses and xanthid
crabs. Gohar and Mazhar (1964) reported
cephalopods, fishes, and parts of corals
(Stylophora) from the stomachs of Red Sea speci-
mens (the corals were probably accidentally in-
gested). Hiatt and Strasburg (1960) found a rab-
bitfish, Siganus sp., in the stomach of one of three
specimens collected at Enewetak.

The stomach of the smaller of the two specimens
taken during the present study contained a sur-
geonfish, Acanthurus glaucopareius, 95 mm SL.
Three other Enewetak specimens and one from the
Tuamotu Archipelago (to 1,615 mm TL, 20.9 kg)
had empty stomachs.

Carcharhinidae (Requiem Sharks)

Carcharhinus albimarginatus (Riippell) (Figure
2): The silvertip shark is one of three carcharhinid
sharks with white on the tips of its fins; the others
are the oceanic whitetip shark, C. maou (Lesson)
(C. longimanus a junior synonym), and the
whitetip reef shark, Triaenodon obesus (Riippell).

The name silvertip has been adopted by Kato et al.
(1967) and others to avoid confusion with the other
two species with white-tipped fins. The white on
the silvertip's fins is not confined to the distal ends
but continues along the posterior margins. The
apex of the first dorsal fin is somewhat pointed
(broadly rounded on C. maou); the origin of this fin
is over the inner edge of the pectoral fin. The pec-
torals are about 18% TL (about 28% on C. maou). A
median interdorsal ridge is present. There are
usually 26 upper and 24 lower teeth. The pre-
caudal vertebrae vary from 115 to 125.

Carcharhinus albimarginatus has not been re-
ported as poisonous [Halstead (1967, pi. VI, fig. 3)
illustrated it but misidentified the figure as
Triaenodon obesus], but it would seem to have the
potential for causing ciguatera because it preys in
part on reef fishes. In the Marshall Islands it was
usually seen on exposed outer reefs in water >30
m, though one individual was observed in the
Enewetak lagoon in water only 2 m deep. Bass et
al. (1973) summarized the depth distribution, not-
ing records to 400 m. This species has attacked
man.

The flesh of four silvertips, 933-1,650 mm PCL
(15.0-73.5 kg), from Enewetak was nontoxic.

Fourmanoir (1961) reported the following wide
variety of fishes from the stomachs of silvertips
from Madagascar: Promethichthys prometheus,
Pristipomoides typus, Seriola songoro, Coris
gaimard, Caesio coerulaureus , Acanthocybium
solandri , Euthynnus pelamis , and Neothunnus al-

FIGURE 2.— Carcharhinus albimarginatus, 1,650 mm PCL, 2,154 mm TL, 73.5 kg, Enewetak, Marshall Islands.

206

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

bacora (= Thunnus albacares). Bass et al. (1973)
examined the stomach contents of 10 specimens of
C. albimarginatus from the western Indian Ocean.
They found teleost fishes (exocoetid, myctophid,
several soleids) in seven sharks; a spotted eagle
ray, Aetobatis narinari, in one; and an octopus in
one.

The stomach of one of the Enewetak silvertips
(1,240 mm PCL, 1,650 mm TL) contained a gray
reef shark, Carcharhinus amblyrhynchos , 483 mm
PCL and 616 mm TL, as well as the dental plates
and pharyngeal mills of three parrotfishes
(Scarus). The stomachs of the other three sharks
were empty.

Carcharhinus amblyrhynchos (Bleeker) Figure
3): This shark, now popularly known as the gray
reef shark, was referred to by Schultz in Schultz
and collaborators (1953) as Carcharhinus
menisorrah (Miiller and Henle). Bass et al. (1973)
and Garrick (in press) are followed in the use of the
name C. amblyrhynchos herein.

The gray reef shark lacks dark pigment distally
on the first dorsal fin, but the tips of the other fins
are broadly blackish, and there is a broad black
margin posteriorly on the caudal fin. The dark
markings on the fins are more evident on live than
on dead specimens. The origin of the first dorsal fin
is over the pectoral axil or anterior part of the
inner edge of the pectoral fin. A short interdorsal
ridge is present or absent. There are 26-28 upper
teeth and 24-26 lower teeth; the precaudal verte-

brae vary from 110 to 117 (two Enewetak speci-
mens had 117).

This shark is abundant in the Marshall Islands.
It occurs in many habitats from lagoons to ocean
reefs, but it is most commonly encountered in deep
channels and outer reef areas. It does not pene-
trate the shallows as readily as C. melanopterus.

The flesh of 11 specimens from Enewetak,
1,017-1,190 mm PCL (17.2-26.3 kg), and 1 from
Bikini (3.6 kg, length not taken) was tested. All
gave a zero reaction for ciguatoxin. The viscera of
one of these, 1,158 mm PCL, from Enewetak pro-
duced a reaction of 2, however.

The stomachs of 74 individuals, 520-1,230 mm
PCL (2.7-32.4 kg), from Enewetak, Fanning and
Palmyra in the Line Islands, Marcus Island,
Johnston Island, Palau Islands, and Ducie and
Henderson in the Pitcairn Group, were examined
for food. Forty-nine stomachs were empty or con-
tained only bait. Three had eaten cephalopods
(two octopus, one squid), and the rest contained
the remains of fishes (in some cases only the lens of
an eye or a few remnants of spines or bones). The
fishes that could be identified to family or genus
were the following: muraenid, belonid, exocoetid,
Fistularia, Decapterus , Trachinotus, Acanthurus,
and another acanthurid (either Acanthurus or
Ctenochaetus).

In spite of its relatively small size, the gray reef
shark constituted a hazard to the personnel of the
survey program, particularly when divers were
spearfishing or collecting with rotenone. Several

Figure 3.— Carcharhinus amblyrhynchos, 1,288 mm PCL, 1,640 mm TL, Tahiti, Society Islands.

207

FISHERY BULLETIN; VOL. 78, NO. 2

of these sharks were killed by powerheads when
their aggressive behavior and proximity war-
ranted. On 12 July 1975 the companion diver of
the author, Russell E. Miller, sustained 7 gashes in
his head requiring 25 stitches as the result of an
attack by a C. amhlyrhynchos of about 1,500 mm
TL. The shark first exhibited threat posturing (see
Johnson and Nelson 1973) at the back of the au-
thor. Miller sounded a warning by rapping on his
scuba tank with his powerhead handle. The shark
immediately turned and swam toward him, re-
peating the exaggerated sinuous swimming of its
threat behavior as it approached. Miller struck the
shark with his powerhead but the shell misfired.
The shark came on to slash his head (and cut the
rubber strap of his face mask) with its upper jaw.
On another occasion Gordon W. Tribble had the
end of his speargun seized by a gray reef shark and
vigorously shaken.

Richard C. Wass ( 1971) has made a comparative
study of the biology of the gray reef shark and the
sandbar shark in the Hawaiian Islands.

Carcharhinus galapagensis (Snodgrass and Hel-
ler) (Figure 4): This shark is circumtropical in
distribution, but as noted by Garrick (1967), it
shows a preference for the sea around oceanic
islands.

The Galapagos shark has no distinctive mark-
ings; it is dark gray dorsally, pale ventrally. The
origin of the first dorsal fin is anterior to the inner
free corner of the pectoral fin. The second dorsal fin
is relatively large for a Carcharhinus, its height
2.4-2.8% TL. A distinctive median interdorsal
ridge is present on the back. There are 26-30 upper

teeth (the anterior upper teeth broadly triangular)
and 26-29 lower teeth. The precaudal vertebrae
range from 103 to 109.

A single specimen, 1,831 mm PCL, 2,426 mm
TL, 41.2 kg, was collected at Enewetak. Its flesh
was nontoxic.

Tester'^ examined the stomach contents of 41
Galapagos sharks caught from the Hawaiian Is-
lands; 51% were empty. Sixty percent of the
sharks had eaten bony fishes, 35% cephalopods,
20% sharks and rays, and 10% crustaceans. He
commented that the larger individuals (maximum
length estimated as 10 ft or 3,048 mm) fed mostly
on larger fishes which were torn into chunks. He
regarded it as a dangerous species; Randall ( 1963)
documented a fatal attack.

Bass et al. ( 1973) found food in 18 of 22 individu-
als of this species; 12 of the stomachs contained
teleost fishes (serranid, Platycephalus , and a
flatfish) and 10 had squids or octopuses (plus the
shell of a bivalve mollusk).

The Enewetak specimen was empty as were
three others 1,460-1,690 mm PCL from the Pit-
cairn Group. One of 1,580 mm PCL from Rapa
contained the head of an unidentified eel.

Carcharhinus limbatus (Valenciennes) (Figure
5): The shark occurs in the Atlantic as well as the
Indo-West Pacific. In the Atlantic it bears the
common name of blacktip shark, a name which is
poor for the species in the Pacific for two reasons.

■'Tester, A. L. 1969. Final Report, Cooperative Shark Re-
search and Control Program, University of Hawaii. Mimeogr.
Rep., 47 + 36 append, p.

Figure a.— Carcharhinus galapagensis, 1,831 mm PCL, 2,426 mm TL, 87 kg, Enewetak, Marshall Islands.

208

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

Figure 5. — Carcharhinus limbatus, 1,415 mm PCL, 1,910 mm TL, 38.2 kg, Enewetak, Marshall Islands.

The tips of the fins of Pacific individuals, particu-
larly adults, are only slightly tipped or edged in
black. Also the common Indo-West Pacific C.
melanopterus has very pronounced black tips on
its fins (see Randall and Helfman 1973, fig. 1, 2).
To avoid confusion in common names, C. melanop-
terus has been referred to by many recent authors
as the blacktip reef shark (though Bass et al. 1973,
call it the blackfin reef shark).

Carcharhinus limbatus is distinctive in lacking
a median ridge on the back between the dorsal
fins, having a relatively long snout, and the cusp of
its teeth notably narrow and erect. It has 29-32
upper, 28-32 lower teeth, and 88-102 precaudal
vertebrae. The color is gray to bronze on the back,
white below, with a long band of the dark dorsal
color extending posteriorly from the last gill open-
ing into the pale ventral color as far as the pelvic
fins.

Two individuals of C. limbatus were caught at
Enewetak during the ciguatera survey; these con-
stitute the first records of the species from the
Marshall Islands. The head of the illustrated
specimen (which was 1,415 mm PCL, 1,910 mm
TL, and weighed 38 kg) has been preserved in the
Bernice P. Bishop Museum under catalog number
18074.

Only the second specimen, which was about
1,700 mm PCL (original data sheet with mea-
surements was lost), was tested for toxicity. The
viscera gave a reaction of 2 when fed to a
mongoose.

Bassetal. (1973) reported on 55 of 101 sharks of
this species with food in their stomachs. Fifty-one
of the sharks had eaten teleost fishes, including:

Scomberomorus commerson, S. leopardus,
Pomadasys sp., Sarpa salpa, Johnius
hololepidosus , Leiognathus equula, Flops saurus,
Tilapia mossambica, and a soleid. Six contained
elasmobranchs, including a small C. obscurus and
aRhinobatus annulatus. Two had eaten Sepia sp.,
and one a spiny lobster, Panulirus homarus.

The two Enewetak specimens had empty
stomachs.

Galeocerdo cuvier (Peron and Lesueur) (Figure
6): The circumtropical tiger shark is readily iden-
tified by its broad bluntly rounded snout, distinc-
tive teeth (heavily serrate, convex on the medial
margin, and deeply notched on the lateral), low
longitudinal keel on the side of the caudal pedun-
cle, and dark bars (though these tend to fade with
age).

The flesh of two tiger sharks from Enewetak,
1,770 and 2,410 PCL (72 and 174 kg), and one from
Bikini, 1,498 mm PCL, was tested. None of these
sharks were toxic. The Bikini specimen was
caught at 4:30 a.m. in only 1.7 m of water.

Bigelow and Schroeder ( 1948) summarized the
literature on food habits, danger to man, etc., of
this shark. Other authors such as Clark and von
Schmidt ( 1965), Bass et al. (1975a), and Tester (see
footnote 7), have added to the list of the great
variety of marine animals (mainly fishes) that this
species will take as food, as well as sundry items of
garbage and refuse discarded into the sea by man.

The stomach of the largest of the Marshall Is-
lands specimens contained the scutes of a green
turtle, Chelonia mydas, estimated to be 500 mm
carapace length and the bait (a gray reef shark).

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FISHERY BULLETIN: VOL. 78, NO, 2

Figure 6. — Galeocerdo cuvier, 2,410 mm PCL, 3,055 mm TL, 175 kg, Enewetak, Marshall Islands.

The stomachs of the other two sharks were empty.
Three other tiger sharks from Enewetak had food
in their stomachs. One of 3,150 mm TL contained
shark vertebrae. The second of 3,581 mm TL had
the scutes of a green turtle and bird feathers. The
third, 3,048 mm TL, was filled with pieces of a
porpoise and the digested remains of shark fins.

A tiger shark of 3,327 mm TL from Ua Huka,
Marquesas Islands, was empty, as was one of 2,895
mm TL from Oahu. Another from Oahu of 3,048
mm had an extremly distended stomach filled with
heads of skipjack tuna (neatly cut by a knife, hence
probably discarded from a fishing boat), plastic
bags of garbage and aluminum foil, a cat, and two
small reef fishes (one a balistid). It also contained
the bait (the head of a calf). A 3,100 mm specimem
weighing 174.6 kg taken by a set line at night at
Rapa had eaten parts of a tiger shark larger than

itself (probably from an individual caught on
another hook), as well as a seabird.

Triaenodon obesus (Riippell) (Figure 7): The
whitetip reef shark, once classified by most
ichthyologists in the family Triakidae, is now re-
corded as a carcharhinid (Compagno 1973). In
spite of its scientific name, it is rather slender
compared with most species of the family. Apart
from its slim form and white-tipped first dorsal fin
and upper caudal lobe, T. obesus is distinctive in
its very blunt snout and teeth which bear a small
cusp on each side of the main central one. It is
widespread throughout the tropical and subtropi-
cal Indo-West Pacific region and ranges to the
eastern Pacific as well. Banner and Helfrich
(1964) and Brock et al. (1965) have reported this
species as poisonous from Johnston Island.

Figure T .—Triaenodon obesus, 1,218 mm PCL, 1,520 mm TL, 23.5 kg, Tahiti, Society Islands.

210

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

The toxicity of eight whitetip reef sharks,
1,003-1,183 mm PCL (8.4-22.4 kg), from
Enewetak was tested. The flesh of all was negative
for ciguatoxin by feeding to mongooses, but the
viscera of two gave positive reactions of 1.

Randall (1977) studied the biology of this
species. He opened the stomachs of 56 specimens
(24 of which were from Enewetak): 33 were empty,
6 had eaten octopuses (2 of these also contained
fishes), and the rest had the remains of reef fishes,
especially scarids and acanthurids.

Dasyatidae (Sting Rays)

Taeniura melanospilos Bleeker (Figure 8): The
specimens collected in the Marshall Islands were
initially called Taeniura brocki Schultz. However,
it now seems more likely that they should be iden-
tified as T. melanospilos Bleeker. Schultz in
Schultz and collaborators (1953) differentiated T.
brocki by its having the venomous spine inserted
". . . at about half length of tail . . ." in contrast to a

little behind the first third on T. melanospilos, in
having the snout contained five times in the
greatest width of the disc (given as six by Bleeker
for T. melanospilos), and in having ". . .very numer-
ous irregularly shaped small brownish to blackish
spots and blotches speckling dorsal surface of disk
...," as opposed to "... numerous rounded black
spots . . ." for T. melanospilos. After noting the
measurements of the position of the spine and the
length of the tail of his only specimens of T. brocki,
Schultz wrote, ". . . end of the tail may have been

bitten off " On the specimen illustrated herein,

the spine is inserted at a point 41% the length of
the tail from the base. From Schultz' measure-
ments, the snout of T. brocki is contained 5.14
times in the width of the disc. The snout of the
specimen illustrated herein is contained about 5.3
times in the disc width. Without knowledge of
variation of this character and perhaps propor-
tional differences with growth, the differentiation
of species on this magnitude of snout length is
questionable. Furthermore, Bleeker's (1853) de-

FIGURE 8.— Taeniura melanospilos, 1,255 mm disc length, 2,008 mm TL, 69 kg, Enewetak, Marshall Islands.

211

FISHERY BULLETIN: VOL. 78, NO. 2

scription of the dark spots of T. melanospilos was
not simply round as Schultz stated, but round and
oblong and variably small, medium, and large.

One stingray of this species from Enewetak with
a disc length of 870 mm (disc width 950 mm; tail
length 950 mm), weighing 19.05 kg, was tested. It
was not poisonous.

The stomach of this ray was empty. Another of
1,255 mm disc length weighing 68.9 kg collected
by the author at Enewetak in 1968 had eaten two
labrid fishes (Xyrichtys) and a parrotfish, Scarus
sp. It was a female with seven embryos.

Muraenidae (Morays)

Lycodontis javanicus (Bleeker) (Figure 9): This
moray is brown with large dark blotches and
numerous small dark spots; the gill opening is in a
large black spot; there are no pale margins on the
fins. It is probably the species of eel reported by
Khlentzos (1950) which poisoned 57 Filipino
laborers at Saipan, Mariana Islands. In spite of
prompt gastric lavage, 14 of these men became
comatose and 2 died.

The severity of illness from the consumption of
moray eels led Halstead and Lively (1954) to re-
gard this as a distinct category of fish toxemia

which they termed "Gymnothorax poisoning."
However, it appears to be principally an acute
form of ciguatera, though there is a possibility of
involvement of one or more other toxins.

Lycodontis javanicus is not common in the Mar-
shall Islands, but it is abundant (for a large carni-
vore) at Johnston Island; in recent years it has
served as the primary source of ciguatoxin for
biochemical and pharmacological study at the
University of Hawaii by a team of scientists
headed by A. H. Banner.

Nine specimens from Enewetak measuring
1,086-1,540 mm TL and weighing 3.6-13.0 kg were
tested. All were toxic, two at the 2 level, one at 3,
three at 4, and three at 5 from the feeding of liver
and viscera to mongooses. The flesh of two of these
eels with a mongoose reaction of 4 was tested; one
was a 1 and the other a 2. One of the eels with a
mongoose test of 5 for liver-viscera gave a reaction
of 3 with flesh.

Brock ( 1972) studied some aspects of the biology
oiL. javanicus, including an analysis of the toxic-
ity at Johnston Island. Of 1,074 specimens, only
158 (14.7%) contained food; 88.8% of the stomach-
content material consisted of fishes (representing
17 different families, the Scaridae predominat-
ing). Among the more interesting prey species was

Figure Q.— Lycodontis javanicus, 732
mm TL, Enewetak, Marshall Islands.

212

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

a whitetip reef shark 465 mm PCL, taken from the
stomach of a 1,422 mm moray. Octopus and spiny
lobster were also eaten.

This is the largest species of moray in the Indo-
Pacific region. Schultz ( 1949) attributed an attack
on the late Vernon E. Brock at Johnston Island by
a moray of about 10 ft (3,048 mm) in length to be
Enchelynassa canina. Following a later interview
with Brock, Randall (1969) reported that the eel
was actually L. javanicus and the length 7-8 ft
(2,134-2,438 mm). Stephens (1963) noted that the
largest moray measured at Johnston during his
stay at the island to be 7 ft 10 in (2,388 mm). The
author tended to disbelieve occasional reports by
divers of individual L. javanicus of 10-12 ft (3,048-
3,658 mm) until he observed one of an estimated
3,000 mm long off Mafia Island, Tanzania, which
was flushed from a cave with rotenone (the eel
recovered from the affect of the rotenone and re-
turned to its cave).

The stomach contents of 1 1 specimens 417-1 ,905
mm TL (the largest weighed 24.5 kg) were
examined during the present study. Six of these
eels were from Enewetak, the rest from Oeno, Pit-
cairn, Johnston, and Truk. Four had empty
stomachs. The smallest contained a crab chela.
The others had eaten fishes (two contained Scarus

sp., one Diodon sp., and another Thalassoma pur-
pureum). The stomach of a 1,540 mm, 13 kg speci-
men was distended with Kyphosus cinerascens,
Acanthurus nigricauda (identified as A. nigricans
by Schultz and Woods in Schultz and collaborators
1953, and as A. gahhm by Randall 1956), and A.
nigroris, all of which totalled 1.5 kg. These fishes
must be discounted as normal prey, however, as
they were undoubtedly eaten as a result of a
dynamite station at the Enewetak garbage pier.
The eel was collected with a powerhead blast im-
mediately after the dynamite explosion when it
was discovered within the area in which many
other fishes had just been killed.

Hoiocentridae (Squirrelfishes)

Adioryx spinifer (Forsskal) (Figure 10): The
largest of the squirrelfishes, this species exceeds
300 mm SL. It has a deep body, the depth about
2.5-2.7 in SL, projecting lower jaw, 40-44 lateral
line scales, and a well-developed venomous spine
at the corner of the preopercle. The color is red and
silvery with a deep red spot behind the eye and
another on the pectoral axil; the fins are yellow
except the spinous dorsal which is deep red. De-
scribed from the Red Sea, the species has since

Figure lO. — Adioryx spinifer, 260 mm SL, Enewetak, Marshall Islands.

213

FISHERY BULLETIN: VOL. 78, NO. 2

been recorded from throughout the tropical
Indo-West Pacific. It is often found in caves.

Randall (1958) reported this species as occa-
sionally toxic in Tahiti. In his review of ciguatoxic
fishes, Halstead (1967) cited this and three other
references.

Six specimens, 232-280 mm SL (0.35-0.66 kg),
were collected for assay of toxicity from Enewetak.
All were nontoxic.

Randall (1958) found fishes in the stomachs of
two adults from Tahiti. Hiatt and Strasburg
(1960) examined the stomachs of nine from
Enewetak, one of which was empty. Crabs (espe-
cially xanthids) dominated the stomach contents
of the other specimens: 12% contained
stoma topods and 12% fishes. The stomachs of five
specimens from Hawaii reported by Hobson ( 1974)
contained crustaceans, mainly caridean shrimps,
and xanthid crabs.

For this food-habit study a total of 31 specimens
ranging from 182 to 280 mm SL were obtained,
principally from Enewetak, but a few from the Red
Sea, Society Islands, Hawaiian Islands, and
American Samoa. Because this species is noctur-
nal, like other holocentrids in general, most
specimens were collected in early morning hours.
Twenty-eight of these fish had food in their
stomachs; 82% by volume consisted of crabs,
mostly xanthids, 5% fishes (including Lycodontis
rueppelliae and a prejuvenile acanthurid), and the
rest shrimps, a hermit crab, unidentified crusta-
ceans (mostly larval), larval moUusks, and an un-
identified worm.

Sphyraenidae (Barracudas)

Sphyraena harracudaa (Walbaum) (Figure 11):
The great barracuda is distinctive in having a few
blackish blotches on the side, especially posterior-
ly and ventrally, and the lowest lateral line scale

count of the genus (76-85). It is the worst offender
for causing ciguatera in the West Indies, due not
only to the high level of toxicity of occasional indi-
viduals but also to its relative abundance there.
The species is far less common in the Indo-West
Pacific.

Seven specimens 563-1,182 mm SL (1.5-13.6 kg)
from Enewetak were tested, and three from Bi-
kini, 640-1,143 mm SL, the largest 15.0 kg. Three
from Enewetak were nontoxic, one was toxic at the
level of 1; two gave a reaction of 2; and one (1,050
mm, 12.7 kg) was a 3. The three from Bikini were
tested at 0, 1, and 2.

de Sylva (1963) made a studv of thesystematics
and life history of the great barracuda, principally
from material from the western Atlantic. He re-
viewed previous papers which presented limited
data on the food habits of this species. Among
them was the report by Ommanney in Wheeler
and Ommanney (1953) on the fishes found in the
stomachs of 5 of 12 specimens of S. commersoni
(now known to be a junior synonym of S. bar-
racuda) from the Seychelles. One of the five con-
tained an unidentified eel and another Lethrinus
ramak. de Sylva mistakenly reported Omman-
ney's five barracuda as all having eaten L. ramak.

de Sylva opened the stomachs of 901 great bar-
racuda, including juveniles, from various
localities in the tropical western Atlantic. Of
these, 529 (58.7%) contained food. Fishes were
found in 82.2% of the stomachs, plant material in
2.8% (probably accidentally ingested with prey),
invertebrates (notably squids and shrimps) in
2.6%, and unidentifiable material in 12.2%. The
Hemiramphidae was the most common family of
fishes found in the stomachs of 446 adult bar-
racuda from Florida, whereas tetraodontid fishes
predominated in the stomach contents of 132
adults from Bimini, Bahamas.

The stomachs of 13 specimens, 560-1,182 mm

Figure ll. — Sphyraena barracuda, 524 mm SL, Palmyra, Line Islands.

214

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

SL, from the Marshall Islands and Line Islands
were examined during the present study. Nine of
these fishes had empty stomachs. The rest con-
tained the remains of fishes.

Sphyraena forsteri Cuvier (Figure 12): This bar-
racuda is readily distinguished from all others by
its large eye, black blotch in the axil of the pectoral
fins, and spiniferous plates on its first gill arch
instead of gill rakers or no trace of rakers at all.

de Sylva (1973:18) wrote that this species of
barracuda has been implicated in poisoning but
added that the examples appear to be misiden-
tifications of S. barracuda. Hiyama (1943, pi. 3,
fig. 9), however, did not confuse his specimens with
■S. barracuda. He reported S. forsteri from the
Marshall Islands as slightly poisonous from feed-
ing flesh to cats and mice.

Only two individuals of this species were caught
during the survey, both from Bikini and both the
same size (610 mm SL, 1.8 kg). Each produced a
toxic reaction of 2.

The stomach of one of these fish contained fish
remains; the other was empty.

Mugilidae (Mullets)

Crenimugil crenilabis (Forsskal) (Figure 13):
This large mullet has a deeply emarginate caudal
fin, a black spot at upper pectoral base, and 37-39
rows of scales between the gill opening and the
caudal base. Widespread in the tropical Indo-West
Pacific region, it is usually seen in small aggrega-
tions in the shallows of lagoons and on outer reef
flats. It appears to feed on fine algae and detritus
from the substratum. After feeding on a sandy
bottom it has been observed to expel sand from its
gill openings. The spawning by a large school at
the surface at night in the Enewetak lagoon was
described by Helfrich and Allen (1975). Cre-
nimugil crenilabis has been reported as poisonous
by Randall (1958) from the Society Islands. It is
probably the species of mullet that Ross (1947)

Figure 12.— Sphyraena forsteri, 540 mm SL, 1.2 kg, Enewetak, Marshall Islands.

Figure 13. — Crenimugil crenilabis, 337 mm SL, Enewetak, Marshall Islands.

215

Fanning, Line Islands (Randall

1 in ee specimens, 248-406 mm
obtained for testing from Bikini.

found toxic at
1958).
Three specimens, 248-406 mm (0.4-0.7 kg), were
n "■'■■ None were toxic.

Serranidae (Groupers)

Cephalopholis argus Bloch and Schneider (Fig-
ure 14): This common brown blue-spotted grouper
has 9 dorsal spines ( in contrast to 1 1 for the group-
ers of the genus Epinephelus). It does not reach
large size, but is has occasionally been implicated
in ciguatera. Although it is most abundant in
outer reef areas, it also occurs on lagoon reefs.

A total of nine specimens from Enewetak were
tested; these ranged from 278 to 390 SL (0.45-1.6
kg). Two were nontoxic, three gave a reaction of 1,
three were recorded as 2, and the largest was a 4.

Randall (1955a) found 8 of 10 individuals of this
grouper from the Gilbert Islands with empty
stomachs; 1 had eaten a fish (probably from
rotenone), and 1 a penaeid shrimp. Randall and
Brock (1960) obtained 280 specimens for food-
habit study, of which 182 were empty; 77.5% con-
tained fishes and the rest crustaceans. Hiatt and
Strasburg (1960) reported on food in five of eight
stomachs from the Marshall Islands as crusta-
ceans, fishes, and polychaetes. Helfrich et al.
(1968) examined the stomachs of 51 from Palmyra;
they found fishes in 89% of the stomachs and crus-
taceans. Harmelin-Vivien and Bouchon (1976)
caught 43 C. argus for stomach-content analyses
in Madagascar. They found fishes 95.7% by

FISHERY BULLETIN: VOL. 78, NO. 2

weight, shrimps 3.9%, and stomatopods 0.4% in
the stomachs.

For the present study the stomachs of 39 speci-
mens, 145-392 mm SL, from Enewetak, Society
Islands, Samoa Islands, Palmyra, Marcus Island,
and Pitcairn, were examined. Twenty-six were
empty, one had eaten a stomatopod, and the rest
contained fishes (two of these were the acronurus
stage of Acanthuridae, one a labrid, one an anten-
nariid, and one Apogon kallopterus).

Epinephelus fuscoguttatus (Forsskal) (Figure
15): The name E. fuscoguttatus was used by
Schultz in Schultz and collaborators ( 1953) for the
more common related species properly called E.
microdon (Bleeker) (systematic clarification by
Randall 1964). The two are similar in morphology
and color. Epinephelus fuscoguttatus has higher
pectoral ray counts (18 or 19, compared with 16 or
17 for E. microdon) and more lower limb gill rak-
ers ( 18-21, including rudiments, compared with 16
or 17 for.E. microdon).

This grouper is a large species; it is not common.
Furthermore, it is the most wary of Marshall Is-
lands groupers. Seven specimens (335-780 mm SL,
3.1-15.4 kg) were taken at Enewetak for testing,
and none at Bikini. Four of the seven were toxic at
the 2 level, and one (710 mm SL) was a 3.

Harmelin-Vivien and Bouchon (1976) caught
four individuals of this species for food-habit study
in Madagascar. The stomachs contained 94.2%
fishes by weight and 5.8% brachyuran crabs.

The stomachs of seven specimens from

Figure U.— Cephalopholis argus, 232 mm SL, Tahiti, Society Islands.

216

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

-Mfc(^

"^

Figure 15. — Epinephelus fuscoguttatus, 551 mm SL, 5.9 kg, Gulf of Aqaba, Red Sea.

Enewetak were examined. Four were empty, one
had an octopus, one had fish remains, and the last
contained unidentified tissue which appeared to
be cephalopod in origin. A specimen 408 mm SL
from the Red Sea had crab remains in its stomach.

Epinephelus hoedtii (Bleeker) (Figure 16):
Schultz in Schultz and collaborators (1953) de-

scribed this fish as new from the Marshall Islands,
naming it E. kohleri. It is relatively deep bodied
and has a slightly emarginate to truncate caudal
fin. He differentiated it from "... all of the 'var-
ieties' of flavocaeruleus described by Boulenger in
having the body spotted with dark blotches in ad-
dition to tiny dark specks." Although more study is
needed of the complex of forms which Boulenger

Figure 16. — Epinephelus hoedtii, 319 mm SL, Enewetak, Marshall Islands.

217

FISHERY BULLETIN: VOL. 78, NO. 2

(1895) regarded as varieties of flauocaeruleus, I
believe that the variety called £^. hoedtii (Bleeker)
is a valid species and that Schultz' E. kohleri is a
junior synonym of it. Adult specimens, such as the
type ofE. kohleri, have the dark blotches, whereas
smaller individuals, such as Bleeker's specimens,
lack them. Hiyama (1943:81, pi. 18, fig. 49) iden-
tified it as Serranus flavocaeruleus (Lacepede).

This grouper was found around isolated coral
heads in the lagoon of Enewetak. Eleven speci-
mens, 348-429 mm SL, 1.36-2.72 kg, were tested.
Six were nontoxic, three gave reactions of 1, one
was a 2, and one (400 mm SL) a 4. A single speci-
men (2 kg) from Bikini was nontoxic.

Hiatt and Strasburg (1960) found fish fragments
in the stomach of one of two specimens from the
Marshall Islands.

The stomachs of the 11 Enewetak specimens
were opened. Five were empty, one (429 mm SL)
contained a 520 mm snake eel, Leiuranus
semicinctus; two had eaten calappid crabs; and the
remaining three contained the digested remains of
fishes.

Epinephelus maculatus (Bloch) (Figure 17):
This dark-spotted grouper was identified as E.
medurensis (Giinther) by Schultz in Schultz and
collaborators (1953). It has also been called E.
fario (Thunberg) by some authors. The oldest valid
name, however, is E. maculatus (Bloch). Though

the author ascertained that the type-specimen is
no longer extant, Bloch's description and illustra-
tion match that of the juvenile of this species,
particularly with reference to the large pale mark-
ings. Adults are distinctive in the rather elevated
third and fourth dorsal spines; also there are two
large dark areas on the dorsal fin and adjacent
back which are separated by a pale area (both dark
and light areas still have the profusion of small
dark spots).

Like E. hoedtii, this species is found mainly
around coral knolls in sandy stretches of atoll la-
goons. Eleven specimens from Enewetak, 270-334
mm SL, 0.45-0.9 kg, were tested. Eight were non-
toxic and three gave reactions of 1. Two from Bi-
kini, 343 and 356 mm SL, were nontoxic.

The stomachs of 13 specimens from Enewetak
and 2 from Bikini, 270-380 mm SL, were
examined. One of 334 mm contained a portunid
crab and unidentified fish remains; another of 345
mm had eaten a calappid crab (15% by volume),
two microdesmid fish 78 and 86 mm SL (identified
as Gunnellichthys monostigma by C. E. Dawson),
and a digested fish; a third (308 mm SL) also con-
tained G. monostigma; a fourth (288 mm SL) an
octopus; and two others fish remains. The remain-
ing nine stomachs were empty.

Epinephelus microdon (Bleeker) (Figure 18):
This is a common species in the Marshall Islands
for a grouper of moderate size. It is found on both

Figure 17. — Epinephelus maculatus, 280 mm SL, Enewetak, Marshall Islands.

218

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

Figure 18.— Epinephelus microdon, 282 mm SL, Enewetak, Marshall Islands.

ocean and lagoon reefs. As mentioned in the ac-
count of E. fuscoguttatus above, it has been con-
fused with this species by Schultz and other
authors.

Thirty-nine specimens from Enewetak were
tested for ciguatera toxin. These ranged from 310
to 470 mm SL and weighed 1.4-3.1 kg. Eight were
nontoxic, 3 were toxic at the 1 level, 8 were 2, 13
were 3, 5 were 4, and 2 were 5 (caused death of test
animals).

Nine specimens from Bikini, 279-508 mm SL,
0.9-4.1 kg, were tested. Two (279 and 342 mm)
were nontoxic, one was poisonous at the 1 level,
four were 2, one was 3, and one was 5 (460 mm
SL).

Randall and Brock (1960) reported on the food
habits of this species (as E. fuscoguttatus) from 33
specimens taken in the Society Islands and
Tuamotu Archipelago. Of 10 with food in their
stomachs, 5 had eaten crustaceans (mainly crabs)
and 5 of them fishes. The eight specimens recorded
by Hiatt and Strasburg (1960) as E. fuscoguttatus
were probably E. microdon. Three fish had empty
stomachs and the remaining five contained fishes
and crustaceans.

Helfrich et al. ( 1968) examined the stomachs of
150 specimens from the Line Islands of which 81
contained food, mainly fishes and crustaceans.
The latter accounted for 64% of the total by volume
(portunid crabs and scyllarid lobsters were the
most frequently recorded). A few of the groupers
had eaten gastropods and cephalopods.

For the present food-habit study 44 specimens
(210-610 mm SL) were examined, of which 28 were
from Enewetak. The remaining 15 were from
Palmyra, Tutuila, and Rapa (where the largest
specimen was taken). Thirty of the 44 groupers
had empty stomachs. Eight contained crabs
(mainly porcellanids and portunids; one had eaten
the xanthid Carpilius conuexus), three contained
fishes (one identified as Scarus), two had eaten
octopus, and one a spiny lobster, Panulirus.

Epinephelus socialis (Giinther) (Figure 19): This
grouper has numerous small dark brown spots
which tend to coalesce to form irregular longitudi-
nal bands, especially posteriorly. The caudal fin
and soft portions of the dorsal and anal fins have
narrow pale margins and broad blackish submar-
ginal zones. It is found mainly on the outer reef fiat
of the atoll environment, sometimes in surpris-
ingly shallow and often turbulent water. Al-
though fishes living entirely in this habitat would
not be expected to be ciguatoxic, Halstead and
Schall (1958) reported one specimen of this species
as weakly toxic from Maiden Island.

Two specimens, 354 and 360 mm SL, 1.1 and 1.6
kg, from Enewetak were tested. Both proved to be
nontoxic.

The stomach contents of seven specimens from
Enewetak, 235-360 mm SL, and one from Ducie
Atoll, Pitcaim Group (420 mm SL, 2.3 kg) were
examined. Three had eaten crabs (grapsids in two,

219

FISHERY BULLETIN: VOL. 78, NO. 2

Figure 19. — Epinephelus socialis, 222 mm SL, Po- ape, Caroline Islands.

including Percnon, and the xanthid crab Eriphia
sebana was found in the third); one of 330 mm
contained an octopus (60% by volume) and a pre-
juvenile acanthurid fish; one of 354 mm contained
an acanthurid 165 mm SL. The remaining
stomachs were empty.

Epinephelus tauvina (Forsskal) (Figure 20): The
name E. tauvina has often been applied to a huge
grouper for whicli the name E. lanceolatus seems
correct. Though the true E. tauvina can attain
moderately large size (to perhaps 800 mm SL or

more), it is not a giant species. Schultz in Schultz
and collaborators (1953) described this fish as E.
elongatus from the Marshall Islands, Mariana Is-
lands, Phoenix Islands, and Samoa Islands, and
Smith and Smith (1963) named it E. salonotus
from the Seychelles. Katayama (1960) and Ran-
dall (1964) showed that E. to«i;ma, described from
the Red Sea, is the senior synonym. This species
may be confused with other dark-spotted groupers
such as E. merra Bloch and E. hexagonus (Bloch
and Schneider), particularly when it is small. It is
differentiated from them in having 15 instead of

Figure 20. — Epinephelus tauvina, 252 mm SL, Enewetak, Marshall Islands.

220

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

16 soft rays in the dorsal fin, a total of 27-30 gill
rakers, instead of 20-27, and a more elongate body.

Epinephelus tauvina is not very common in the
Marshall Islands. It may be found in both lagoon
and outer reef environments.

Six specimens from Enewetak, 324-434 mm SL,
0.45-2.54 kg, were tested. Four were nontoxic, and
one each was poisonous at the 1 and 2 levels. One
specimen from Bikini, 400 mm SL, was nontoxic,
while a second, 450 mm SL (2.3 kg), gave a mon-
goose test of 3.

Randall and Brock {I960) found food in the
stomachs of 3 of 12 specimens (identified as E.
elongatus) collected in the Society Islands. All had
eaten fishes; in addition, one stomach contained a
crab chela.

Thirty-four specimens, 204-500 mm SL, from
Enewetak, Society Islands, Line Islands, Cook Is-
lands, Rapa, and the Red Sea were examined for
food. Nineteen had empty stomachs, one contained
a crab, and the rest had eaten fishes, of which one
could be identified to species {Adioryx lacteogut-
tatus) and three to family (Pomacentridae,
Holocentridae, and MuUidae).

Plectropomus leopardus (Lacepede) (Figure 21):
This is the largest and most common of four group-
ers of the genus Plectropomus in the Marshall
Islands. The genus is readily distinguished from
other Micronesian serranid genera in having
eight dorsal spines and large canine teeth in the
jaws; also the body is more elongate than most
other groupers. Plectropomus leopardus is reddish
with small dark-edged blue spots and an emargin-
ate caudal fin.

This species is among the worst offenders in
Oceania for causing ciguatera. Halstead (1967)
listed it as poisonous from Jaluit in the Marshall
Islands and in the Tuamotus. He cited 10 papers
that have reported on its toxicity in the Pacific,
among them Randall (1958) who noted it as the
most toxic of the groupers in Tahiti and reported
his own poisoning from the Tuamotus.

Thirty-one specimens were collected at
Enewetak for ciguatoxin content, mainly by
spearing. The fish ranged from 426 to 790 mm SL
and weighed from 1.8 to 11.8 kg. Twelve were
nontoxic, six were poisonous at the 1 level, eight at
2, four at 3, and one (520 mm SL) was a 5. One
specimen (8.2 kg) from Bikini was nontoxic.

Randall and Brock (1960) recorded the food of
seven specimens from the Society Islands: four had
empty stomachs and the rest had eaten fishes.

Thirty-seven specimens 426-790 mm SL were
collected for food-habit study from Enewetak, So-
ciety Islands, and Okinawa. Fifteen had empty
stomachs, and the rest contained fishes. Five had
eaten parrotfishes (one grouper, 702 mm SL, con-
tained a Scarus gibbus 3 13 mm SL). A 643 mm fish
contained two acanthurids, one of which was a
Ctenochaetus striatus 153 mm SL. A 705 mm
grouper had eaten a labrid, Cheilinus undulatus,
270 mm SL. Two others had groupers in their
stomachs, a 659 mm fish contained E. tauvina 267
mm SL, and a 790 mm fish contained a half-
digested Epinephelus sp.

Plectropomus melanoleucus (Lacepede) (Figure
22): This distinctively colored grouper, white with

Figure 2l.— Plectropomus leopardus, 513 mm SL, 3.4 kg, Enewetak, Marshall Islands.

221

FISHERY BULLETIN: VOL. 78, NO. 2

Figure 22. — Plectropomus melanoleucus, 492 mm SL, Enewetak, Marshall Islands.

black saddlelike bars, scattered small blue spots,
and yellow fins has been regarded as a color phase
of P. maculatus (Bloch) by a number of authors
from Boulenger (1895) to Smith and Smith (1963).
Plectropomus melanoleucus, however, is a valid
species. In addition to color, it differs from P.
maculatus (and P. leopardus and truncatus) by
usually having 17 instead of 16 pectoral rays.

This species is rare in Oceania. Only a single
specimen, 506 mm SL, 2.95 kg, was taken at
Enewetak during the ciguatera survey. Its viscera
produced a reaction of 2 when fed to a mongoose.

Its stomach was empty.

Plectropomus truncatus Fowler (Figure 23):
Like P. leopardus, this grouper has dark-edged
blue spots, but the spots are larger in fishes of

about the same size. The best field character to
distinguish this species is its truncate caudal fin.

One specimen (384 mm SL, 1.45 kg) from
Enewetak produced a ciguatoxic reaction of 2; its
stomach was empty.

Hiatt and Strasburg(1960) reported one of three
specimens of this grouper collected at Enewetak
with a holocentrid fish in its stomach.

Variola louti (Forsskal) (Figure 24): This color-
ful grouper is yellowish brown to orange, profusely
spotted with blue or pink (blue from shallow wa-
ter, pink in deeper water), with broad zones of
yellow posteriorly on the median and pectoral fins.
Apart from color, it is readily distinguished by its
deeply concave caudal fin. It is usually found on
outer reefs at depths >15 or 20 m.

Figure 23. — Plectropomus truncatus, 350 mm SL, Enewetak, Marshall Islands.

222

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

Figure 24.— Variola louti, 273 mmSL, Enewetak, Marshall Islands.

Variola louti is well known as a cause of cigua-
tera. In Mauritius it is prohibited from sale in fish
markets. Toxicity there has been reported by
Wheeler in Wheeler and Ommanney (1953).

Nineteen specimens were obtained for testing at
Enewetak. They ranged from 352 to 418 mm SL
and weighed from 1.1 to 2.2 kg. Thirteen were
nontoxic, four gave a mongoose test of 1, and two a
test of 3. Two from Bikini, 292 and 420 mm SL,
were nontoxic.

Randall and Brock (1960) opened seven
stomachs of the species from the Society Islands.
Five were empty and two contained digested
fishes. Hiatt and Strasburg ( 1960) found a juvenile
unicornfish, Naso sp., in the stomach of one of two
specimens from Bikini. Helfrich et al. (1968)
examined the stomach contents of 44 specimens
from the Line Islands. They found fishes, includ-
ing acanthurids, balistids, and muraenids, in 80%
of the stomachs, and crustaceans in 11%.

For the present food-habit study 44 specimens
were examined. These ranged from 180 to 560 mm
SL (largest weighed 5.45 kg). They were caught at
Enewetak, Bikini, Line Islands, Tahiti,
Rarotonga, Pitcairn Group, Rapa, and Tutuila.
Twenty had empty stomachs. One contained a
crab, one a spiny lobster, and the rest had eaten
fishes, of which the following were identified at
least to family: Adioryx sp. ( 120 mm specimen in a
295 mm grouper), Scorpaena sp. ( 28 mm specimen
in a 235 mm grouper), Parupeneus trifasciatus (a
53 mm transforming specimen in a 470 mm
grouper), juvenile Chaetodon sp., Anampses

caeruleopunctatus (identified from scales), Scarus
sordidus ( 140 mm specimen in a 375 mm grouper),
and a pomacentrid.

Lutjanidae (Snappers)

Aprion uirescens Valenciennes (Figure 25): This
elongate snapper has been reported as poisonous
from a number of Pacific localities, including the
leeward Hawaiian Islands (Halstead 1967).
Halstead did not list any Indian Ocean localities.
It may therefore be worthy of note that the author
incurred a mild case of ciguatera from eating a fish
of this species at Mauritius. Also he was informed
that poisoning is known from nearby Reunion.

Aprion uirescens is a roving carnivore of open
water but often found within or near reef areas,
both in atoll lagoons and in outer reef zones. It is
difficult to approach underwater; most of the
specimens were obtained by hook and line, often
while trolling.

Eleven specimens, 435-622 mm SL (1.6-5.2 kg),
from Enewetak were tested. Eight were nontoxic,
one (589 mm) gave a reaction of 1, one (622 mm)
was a 3, and one (620 mm) a 4.

Eight were taken at Bikini ranging from 406 to
685 mm SL (1.8-5.4 kg). All, exept one of 457 mm
SL which produced a mongoose reaction of 1, were
nontoxic.

Ommanney in Wheeler and Ommanney (1953)
reported on the analysis of stomach contents of 80
A. uirescens from the Mauritius-Seychelles region.
Forty-four of these were empty. The stomachs of

223

FISHERY BULLETIN: VOL. 78, NO. 2

Figure 25. — Aprion virescens, 503 mm SL, 2.5 kg, Nuku Hiva, Marquesas Islands.

21 contained fishes; 6 had fishes and macro-
plankton; 5 had only macroplankton; and 4 con-
tained cephalopods. Among the fishes taken from
the stomachs were scarids, ostraciids, siganids, a
bothid, and Caesio coerulaureus.

Talbot (1960) reported on 259 specimens caught
by handline and surface lure on the east African
coast which ranged from 202 to 800 mm SL
(weight to 11.3 kg). He presented a diagram of the
relative abundance of food organisms for this fish
as follows: fishes 49%, plankton 17%, cephalopods
14%, and crustaceans exclusive of plankton
(mainly portunid crabs) 12%. He did not indicate
how many specimens had empty stomachs.

The stomachs of 15 specimens from the Mar-
shall Islands and 1 from Hawaii were examined.
Ten were empty. Four contained fishes; (one prey
fish identified as Scarus sp.); one A. virescens (481
mm SL) had also eaten an octopus (one-third
stomach volume). A 457 mm fish contained a 10
mm calappid crab, and one of 650 mm a
stomatopod.

Lutjanus hohar (Forsskal) (Figure 26): This red
snapper has been implicated more frequently in
ciguatera than any fish of the Indo-Pacific region.
It is probably the species which sickened the crew
of Captain Cook in the New Hebrides in 1774
(Banner 1965). Its toxicity has also been reported
under the junior synonym Lutjanus coatesi Whit-
ley. This species occurs along seaward reefs and in
passes. It is more common around atolls and low
coral islands than high islands (Randall and Brock
1960). It is especially abundant in the Line Is-
lands. Reef fishes became highly toxic there dur-
ing and immediately after World War II; the toxic-

ity declined in the early 1960's (Banner and
Helfrich 1964 ). When the toxicity was high, L. bohar
from these islands was used for the chemical and
pharmacological work on ciguatoxin at the Uni-
versity of Hawaii (replaced by Lycodontis
javanicus from Johnston Island in later years). It
was the species used by Banner et al. (1966) to
demonstrate the long periods of retention of
ciguatoxin in the tissues of poisonous fishes when
removed from the source of the toxin.

The toxicity of 95 specimens from Enewetak
from 430 to 635 mm SL (2.5-7.5 kg) was tested.
Fifty-six were nontoxic; 22 gave a mongoose test of
1; 11 were 2, 5 were 3, and 1 (533 mm) was a 5.

From Bikini 143 specimens which ranged from
330 to 760 mm SL were tested. Of these, 112 were
nontoxic, 15 were 1, 8 were 2, 6 were 3, and 2 gave
a mongoose test of 4.

From the atoll of Rongelap (lat. 11° N, long.
167° E) in the Marshall Islands we obtained 12
specimens of L. bohar which weighed from 3.2 to
9.1 kg. Eight of these were nontoxic, two gave a
reaction of 2, one was a 3, and one a 5.

Hiatt and Strasburg (1960) found fragments of
fish in one of two specimens of L. bohar from
Bikini. Talbot (1960) examined 854 specimens
from the East African coast; 58% had empty
stomachs. Fishes composed 62% of the food mate-
rial, crustaceans 24%, and mollusks 8%. Helfrich
et al. (1968) determined the diet of 2,276 speci-
mens from Palmyra and Christmas Islands in the
Line Islands; 21.4% of these were empty. Fishes
dominated the stomach contents (48.7% by volume
at Palmyra and 65.4% at Christmas), of which
acanthurids were the most common among those
identified. Mollusks represented 19.1% by volume

224

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

Figure 26.— Lutjanus bohar, 520 mm SL, 4.9 kg, Ulithi, Caroline Islands.

of the total food material at Palmyra and 18*7?^ at
Christmas. Crustaceans (principally decapod
megalops) composed 15.4% of the food among
Palmyra fish and 13.3% of Christmas Island
specimens.

The stomachs of 121 adult specimens of L. bohar
from the Marshall Islands, 330-635 mm SL, most
of which were taken by hook and line, were
examined. Eighty-six were empty. Of those with
identifiable food, 76.2% contained fishes (includ-
ing Lycodontis sp., Cephalopholis urodelus, Ar-
chamia sp., Lethrinus variegatus , Scarus sp., and
Ostracion sp.), 10.8% had eaten crabs (including
portunids), 8.7% contained octopus, and 4.3%
shrimps.

Lutjanus fuluus (Schneider) (Figure 27): The
names L. vaigiensis (Quoy and Gaimard) and L.
marginatus (Cuvier) are junior synonyms that
have often been used for this snapper. It is yel-
lowish on the body, the head gray, the caudal fin
reddish black with a narrow white posterior bor-
der; the dorsal fin is reddish and the anal and
pelvic fins yellow. It is a small inshore species,
abundant throughout the Indo-West Pacific. It is
found more often in sheltered than exposed envi-
ronments. Hiyama (1943:48-49, pi. 6, fig. 17) re-
ported that Marshallese natives informed him
that this fish (which he identified as L. flavipes
Valenciennes), rarely causes ciguatera; when it
does, the cases are light. Halstead (1967:98, pi. 68,
fig. 4) listed it among the ciguatoxic fishes
[misidentified as L.janthinuropterus (Bleeker)].

Two specimens from Enewetak, 207 and 217
mm SL, were nontoxic.

Randall (1955a) examined the stomachs of six
specimens taken with rotenone at Tarawa, Gilbert
Islands. One had eaten a small holothurian, one a
brachyuran crab, and two contained fishes that
were probably prior victims of the ichthyocide.
Hiatt and Strasburg (1960) analyzed the stomach
contents of six juveniles from Amo, Marshall Is-
lands; they reported the following food items:
crabs, fishes, amphipods, shrimps, and
stomatopods. Randall and Brock (1960) examined
50 specimens which had food in their stomachs;
54.3% of these contained crustaceans (mainly
crabs) and 42.4% fishes. Helfrich et al. (1968) col-
lected 51 specimens from Palmyra for food-habit
study. The dominant food items were mugilid,
mullid, and pomacentrid fishes; crustaceans made
up the next most frequent organisms of the diet.

For the present study 44 specimens 182-250 mm
SL were collected in the Marshall Islands,
Mariana Islands, and Caroline Islands. Thirty-one
of these had empty stomachs. Of those with food,
68.4% had eaten crustaceans (nearly all crabs,
mainly calappids) and 31.6% fishes.

Lutjanus gibbus (Forsskal) (Figure 28): This
snapper is also reddish like L. bohar, but it does
not attain such large size. The dorsal profile of
adults, beginning with the nape, is highly convex,
which is the basis for the specific name. Schultz in
Schultz and collaborators (1953) stated, "This
species was taken only in moderately deep water.

225

FISHERY BULLETIN: VOL. 78, NO. 2

Figure 27. — Lutjanus fulvus, 215 mm SL, Enewetak, Marshall Islands.

Figure 28. — Lutjanus gibbus, 291 mm SL, Palmyra, Line Islands.

It did not occur over the shallow parts of the reefs."
Talbot (1960), on the other hand, wrote in refer-
ence to L. gibbus in east Africa, "It was only found

226

in shallow water of from 3 to 8 fathoms." Actually,
the species may occur either in the shallows or at
moderate depths, but in the Marshall Islands, at

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

least, it is usually encountered in water of 20 m or
more. Though mainly found on the outside of sea
reefs and in passes, it may also occur in lagoons. It
is often observed in large aggregations.

Thirty-one specimens of L. gibbus from
Enewetak 302-375 mm SL (largest 1.8 kg) were
collected. Twenty-one of these fishes were non-
poisonous; five were rated as 1, two were 2, and
three ranked 3 by the mongoose test.

Thirty-five specimens from Bikini, 279-385 mm
SL, were tested. All but three were nontoxic; the
three toxic fish produced a mongoose reaction of
only 1.

Randall and Brock (1960) collected 23 speci-
mens in the Society Islands of which only 9 had
food in their stomachs (5 of these were juveniles).
The four adults contained fishes, crabs, and un-
identified crustaceans. Hiatt and Strasburg( 1960)
examined 43 specimens (175-260 mm SL) from the
Marshall Islands of which 10 had empty stomachs.
Crustaceans were the main food, especially crabs
(60% contained xanthids and 17% portunids);
Amphineura were found in 13% of the stomachs.
Octopus, Natica,Ptychodera, small holothurians,
polychaetes, sipunculids, and ^sh. Apogon were all
found in 4% of the stomachs. Talbot (1960) re-
ported on the capture of 121 specimens. He wrote,
"Foods eaten were mainly crustaceans, including
crabs and Penaeid prawnis. Small coral fishes were
also occasionally taken." Helfrich et al. (1968)
found food in 36 of 45 stomachs of adults from the

Line Islands; fishes were the main item of diet,
with crustaceans the second most abundant.
[Fishes included unidentified eels, acanthurids,
and Pomacentrus nigricans (= Stegastes nigri-
cans).] Most crustaceans were brachyuran crabs,
but there were also alpheid shrimps and slipper
lobster. Mollusk remains were mainly proso-
branchs, but opisthobranchs and cephalopods
were also found. Sea urchins were the most com-
mon of the miscellaneous invertebrates composing
the rest of the stomach contents.

During the present study the stomachs of 51
specimens from the Marshall Islands, 260-419 mm
SL, were examined. Twenty-seven were empty. Of
those with food, 40% had eaten crabs, 26% fishes
(including Pseudocheilinus sp. and Adioryx mi-
crostomus), 17% echinoids {inclxiding Eucidar is sp.
and Heterocentrotus mamillatus), 12% ophiuroids
(including Ophiocoma erinaceus), 2.1% alpheid
shrimps, 2.1% octopus, and 0.3% gastropods.

Lutjanus monostigmus (Cuvier) (Figure 29):
This species, named from the blackish spot usually
present on its side (on lateral line), is capable of
causing severe cases of ciguatera. Belotte (1955)
gave the case history of an American who was in a
coma 3 days after eating this snapper in Tahiti;
the author also interviewed this man. The sale of
this species in Tahiti, where it is called "taivaiva,"
(Randall 1972) is forbidden. It is found in reef
environments from shallow water to moderate

Figure 29.— Lutjanus monostigmus, 249 mm SL, Florida Island, Solomon Islands.

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FISHERY BULLETIN; VOL. 78, NO. 2

depths, especially where there is deep shelter. Not
infrequently it is encountered in small aggrega-
tions. Adults are wary, hence difficult to spear.

Only three specimens were obtained from
Enewetak, 310-420 mm SL (0.8-1.6 kg), for testing
of toxicity. One was nontoxic, one was 1, and one
a 2.

Five specimens, 400-445 mm SL, were collected
in Bikini. Four were nontoxic; the largest gave a
mongoose reaction of 1.

Randall and Brock (1960) opened 32 stomachs of
adults of this species, of which 18 were empty.
Those with full stomachs all contained fishes,
among them Decapterus pinnulatus, Selar
crumenophthalmus, and Ctenochaetus striatus.
Hiatt and Strasburg ( 1960) found a goatfish in the
stomach of one of three specimens from Enewetak;
the other two were empty. Talbot (1960) collected
18 specimens off east Africa. He reported fish re-
mains (including a mullid and a labrid) in most
stomachs; penaeid prawn remains were also
found. Helfrich et al. (1968) examined 29 speci-
mens from the Line Islands. They found fishes in
92% of the stomachs and crustaceans (stomatopod
larvae and one slipper lobster) in 23%.

For the present food-habit study 41 specimens of
L. monostigmus were examined from the Marshall
Islands, Society Islands, Line Islands, and Samoa
Islands. Twenty-three had empty stomachs. Of
those with food, 92% by volume had eaten fishes
(including the holocentrid Adioryx microstomas,

acanthurids, and a balistid), and 8% crabs (includ-
ing a portunid).

Macolor niger (Forsskal) (Figure 30): Although
not previously reported as poisonous, this lutjanid
fish attains moderate size, is a reef-dweller, and
carnivorous; this would seem to have the potential
for causing ciguatera. A total of 25 adults, 403-445
mm SL (2.3-2.95 kg), were taken, all from
Enewetak, and mainly from explosive stations in
the lagoon. Twenty-three were nontoxic and two
gave a reaction of 1 on the feeding of liver and
viscera to mongooses.

The stomachs of eight adult specimens taken at
9:00 a.m. at Enewetak were examined. All were
empty. The large eyes of this species is suggestive
of nocturnal habits, and the numerous (about 72)
long gill rakers would seem to indicate at least
some feeding on zooplankton (perhaps more im-
portant in smaller individuals than large adults).
Some of the specimens were caught by hook and
line baited with fish. Hiatt and Strasburg (1960)
also reported that this species can be caught on a
baited hook.

Lethrinidae (Emperors)

Lethrinus amboinensis Bleeker (Figure 31): Fol-
lowing Sato (1978), this emperor is identified as
L. amboinensis. It lacks characteristic color mark-
ings, being light brownish to greenish dorsally

Figure 30.— Macolomiger, 378 mm SL, Enewetak, Marshall Islands.

228

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

Figure 31. — Lethrinus amboinensis, 294 mm SL, Enewetak, Marshall Islands.

with small dark brown spots and blotches, shading
to white ventrally. It is somewhat elongate, the
head length greater than the depth; the snout is
moderate, its length in adults 1.8-1.0 in head
length; the maxilla reaches a vertical a little pos-
terior to the anterior nostril. The teeth along the
sides of the jaws are conical.

Twenty-four specimens were taken at
Enewetak and nine at Bikini, the largest 310 mm
SL. All were nontoxic.

Helfrich et al. (1968) determined the food of 14
specimens of L. amboinensis from Palmyra, Line
Islands. Fishes were found in 75% of the stomachs,
mollusks in 25%, and crustaceans in 17%; all
specimens had some sea urchin fragments.

Fish remains were found in one of two stomachs
examined at Bikini.

Lethrinus kallopterus Bleeker (Figure 32): This
Lethrinus is distinctive in having orange fins and
blackish spots over occasional scales; the snout is
short, the maxilla reaching a vertical at anterior
edge of eye. The teeth at the sides of the jaws are
nodular (i.e., neither conical nor well-developed
molars). It was most often seen in the deeper parts
of the atoll lagoons.

A total of 19 specimens were collected at
Enewetak for the testing of toxicity. These ranged
from 337 to 443 mm SL (1.1-2.7 kg). Fourteen were
nontoxic, two produced a reaction of 1, two were 2,
and one (368 mm SL) was a 5.

Two specimens, 330 and 457 mm SL, were pro-
cured from Bikini; neither was toxic.

The stomachs and intestines of 13 specimens,
330-443 mm SL, from the Marshall Islands were
opened. Five of the fish were empty. Four had
eaten only echinoids (including Echinometra
mathaei); one contained mostly echinoids but also
the cowrie Cypraea carneola; another (the largest)
had eaten just the cowrie C. vitella; still another
had a cowrie in its gut (20% by volume of the food
material), and the rest of the food material con-
sisted of crinoids; one specimen contained only a
starfish arm.

Lethrinus miniatus (Forster in Bloch and
Schneider) (Figure 33): This emperor has an espe-
cially long snout (1.6-1.8 in head length of adults).
It is primarily gray in color, but can alter its pat-
tern, like many other Lethrinus, to one of dark
irregular bars and blotches. Often there are two or
three bluish streaks on the snout passing an-
teriorly and diagonally downward from the eye.
The teeth on the sides of the jaws are conical. This
species was seen in both lagoon and outer reef
environments, but mainly in lagoons. It is among
the largest of the emperors, reported to attain
Im.

Of nine adults, 435-530 mm SL (1.8-3.6 kg),
which were caught at Enewetak, six were non-
toxic, and three gave a reaction of 3.

Twelve specimens from Bikini, 381-635 mm SL,
1.4-7.3 kg, were nontoxic.

Eight of 14 specimens from Enewetak and Bi-
kini had food in their stomachs. Three contained
fish remains, one of which (456 mm SL) included a

229

FISHERY BULLETIN: VOL. 78, NO. 2

Figure 32. — Lethrinus kalloptenis, 345 mm SL, Enewetak, Marshall Islands.

Figure 33. — Lethrinus miniatus, 430 mm SL, Enewetak, Marshall Islands.

Lethrinus 115 mm SL; the remaining three had
eaten crustaceans (stomatopod, crab, and alpheid
shrimp).

Lethrinus xanthochilus Klunzinger (Figure 34):
This emperor is one of the more slender species of
Lethrinus (depth 3.1-3.3 in SL). The interorbital

space is nearly flat. The teeth on the sides of the
jaws are conical. The upper lip is orange-yellow,
and there is a red spot at the upper pectoral base. It
is found more in lagoons than exposed reef
habitats; it will venture into shallow water.

Two specimens, 445 and 550 mm SL (smallest
1.7 kg, largest not weighed), were collected at

230

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

Figure 34. — Lethrinus xanthochilus, 395 mm SL, Fanning Island, Line Islands.

^

^^^^.^.M'- .^ ,

\

Figure 35. — Monotaxis grandocuHs, 220 mm SL, Enewetak, Marshall Islands.

Enewetak; two, 305 and 432 mm SL, were taken at
Bikini. All were nontoxic.

The stomach and gut contents of these four
specimens and one of 466 mm from the Society
Islands were examined. One fish contained
crushed echinoids, one the remains of a calappid
crab, one a digested fish, another both crab and
fish remains, and one (the largest) a freshly in-
gested fish (probably from a rotenone station).

Monotaxis grandoculis (Forsskal) (Figure 35): M.
grandocuHs has been classified in the past princi-
pally in the Sparidae or Lutjanidae, but is now
recognized as a lethrinid. It is readily distin-
guished by its large eyes, short blunt snout, and
single row of well-developed molariform teeth
along the side of the jaws. It occurs in a wide
variety of reef habitats. Adults are difficult to ap-
proach underwater. This fish feeds mainly on in-

231

FISHERY BULLETIN: VOL. 78, NO. 2

vertebrates with calcareous or chitinous hard
parts. Although rarely implicated in serious cases
of poisoning, it is capable of being ciguatoxic.
Halstead (1967) listed 11 references attesting to
its toxicity.

Five specimens, 277-362 mm SL (0.73-1.6 kg),
from Enewetak were tested for toxicity. Four were
nontoxic and one gave a reaction of 1 from the
mongoose feeding.

Randall (1955a) reported on the gut contents of
two specimens, 158 and 160 mm SL, from the Gil-
bert Islands; these consisted mainly of crushed
shells of small mollusks and sea urchins. Hiatt
and Strasburg (1960) examined the contents of the
digestive tracts of eight specimens, 195-220 mm
SL, from the Marshall Islands. One fish was
empty. Crushed gastropods (including Atys sp.
and Cerithium sp.) were found in all stomachs,
pelecypods in 71%, crabs in 42%, hermit crabs in
28% , and spatangids and polychaetes each in 14% .
Hobson ( 1974) collected five specimens in Hawaii.
He found the principal prey, in order of importance
in the diet, to be prosobranch gastropods,
ophiuroids, echinoids, opisthobranch gastropods,
and pagurid crabs.

Forty-eight specimens of M. grandoculis, 155-
440 mm SL, were collected from the Marshall Is-
lands, Line Islands, Cook Islands, Society Islands,
Pitcaim, Hawaiian Islands, New Guinea, and the
Red Sea for the study of food habits. Unless fish of

this species are captured during the night or very
early morning hours, their stomachs are nearly
always empty. Occasional feeding by M. grand-
oculis does occur during the day, as indicated by
Hiatt and Strasburg's (1960) observation of its
"blowing" away sand to expose fossorial forms.
Also one specimen taken at 2 p.m. during the au-
thor's survey had the remains of a freshly ingested
crab in its stomach. Five of the fish collected in late
afternoon hours had completely empty digestive
tracts. The remaining fishes contained, on a vol-
ume basis, 39.4% gastropods, 18.9% crabs, 16.8%
pelecypods, 13.9% echinoids (principally
Echinometra and spatangoids such as Clypeaster),
6.1% pagurid crabs, 1.7% ophiuroids, 1.2%
polychaetes, 1.0% unidentified worms, 0.7%
fishes, and 0.3% foraminifera.

Kyphosidae (Sea Chubs)

Kyphosus cinerascens (Forsskal) (Figure 36):
This chub may be distinguished from the other
Kyphosus by the high soft portion of the dorsal fin
(longest dorsal spine contained about 1.8 times in
longest soft ray). It occurs in lagoon or outer reef
areas and is often seen in loose aggregations. It is
associated with hard substratum for its algal food,
generally in the vicinity of crevices or caves with
more than one entrance. Bartsch et al. (1959) re-
ported this species as toxic from Majuro, Marshall
Islands, but their data and the few other records of

Figure 36. — Kyphosus cinerascens, 234 mm SL, Enewetak, Marshall Islands.

232

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

toxicity would seem to indicate that it is only mar-
ginally a cause of ciguatera.

Of two specimens from Enewetak, 356 and 364
mm SL, 1.8 kg, one was nonpoisonous and the
other toxic at level 1.

Hiatt and Strasburg ( 1960) found benthic algae
in the stomachs of three of four specimens
examined in the Marshall Islands. Hobson (1974)
reported algae in three stomachs from Hawaii;
however, K. cinerascens apparently does not
occur in the Hawaiian Islands (though two other
species are present).

Three specimens, 330-364 mm SL, from
Enewetak were opened. The stomach of one was
empty, and the other two contained benthic algae.

Q

The algae of one were identified by Tsuda as the
reds Gelidium pusillum, Champia parvula, and
Leveillea jungermannoids (90%) and the brown
Sphacelaria tribuloides.

Carangidae (Jacks)

Caranx ignobilis (Forsskal) (Figure 37): This
steep-headed jack is the largest species of the
genus. Bagnis et al. (1972) stated that it can attain
a length of 2 m and a weight of 80 kg. It can be
differentiated from other Marshall Islands species

*Roy T. Tsuda, Marine Laboratory, University of Guam, Box
EK, Agana, Guam 96910, pers. commun. 1972.

by the absence of scales on the thorax except for a
small median patch. Like other large carangids, it
is a roving carnivore; it may be encountered any-
where in the atoll environment including water
surprisingly shallow for such a large fish.

The author interviewed a man and wife in
Moorea who were poisoned from eating the liver of
a large individual of this species (estimated 1.5 m)
which overturned their canoe in the long struggle
to catch it. Both were very ill with ciguatera, the
man comatose for several hours.

Five specimens, 573-920 mm FL, 3.6-16.3 kg,
were obtained at Enewetak for the testing of toxic-
ity. Three gave a 0 reaction and two a reaction of 1 .
Two specimens from Bikini, 635 and 1,105 mm FL,
4.5 and 27.3 kg, were nontoxic.

A total of 14 specimens were collected for food-
habit study from the Marshall Islands, Line Is-
lands, Hawaiian Islands, Pitcairn Group, and the
Marquesas. Seven stomachs were empty, and the
rest contained the digested remains of fishes, of
which only one could be identified to species, the
surgeonfish Zebrasoma flauescens. One
stomach-content fish was a scorpaenid, and
another (from a jack of 1,217 mm FL, 37.5 kg) a
scar id.

Caranx lugubris Poey (Figure 38): The black
jack is a circumtropical species with a well-earned
reputation for causing ciguatera. Although the

Figure 31 .—Camnx ignobilis, 378 mm FL, Fanning Island, Line Islands.

233

FISHERY BULLETIN: VOL. 78, NO. 2

(^ r T *¥

Figure SS.—Camnx lugubris, 557 mm FL, 3.1 kg, St. John, U.S. Virgin Islands.

dark color (especially on the scutes) and distinc-
tive configuration generally permit identification,
the fully scaled breast will provide separation
from C. ignobilis, the low number of scutes on
straight portion of lateral line (26-33) from C.
melampygus, and the high gill raker count (18-20
on lower limb) from C. sexfasciatus. This species is
found mainly around oceanic islands and is nearly
always encountered in the clear water of outer reef
environments.

Fifteen specimens were obtained at Enewetak
for testing. These ranged from 488 to 910 mm FL
and weighed from 2.5 to 15.5 kg. Eleven were
nonpoisonous, two gave reactions of 1, one was a 2,
and one a 3. No specimens were collected at Bikini.

Randall (1955a) reported a fish in one of two
specimens collected in the Gilbert Islands and
Randall ( 1967) found fishes in two of six specimens
from the Caribbean Sea.

For the present food-habit study, 10 specimens
were obtained from Enewetak and Henderson Is-
land in the Pitcairn Group. Four had empty
stomachs, and the remaining six contained the
remains of fishes, one of which was a labrid.

Caranx melampygus Cuvier and Valenciennes
(Figure 39): This is the most abundant jack of the
genus in Oceania; it is widespread in the tropical

234

and subtropical Indo-West Pacific and ranges to
the eastern Pacific as well. It is irridescent blue
along the back and median fins in life with a scat-
tering of small blackish spots on the head and body
except ventrally. The chest is completely scaled,
and there are 38-44 scutes in the straight portion
of the lateral line.

Thirty specimens were collected at Enewetak,
417-722 mm FL, 1.4-6.8 kg, for the assay of cigua-
tera. Twenty-four were nontoxic, four gave a reac-
tion of 1, one was a 2, and one a 3.

Six specimens from Bikini, 394-686 mm FL,
1.8-6.6 kg, were nontoxic.

Randall ( 1955a) examined the stomach contents
of four specimens from the Gilbert Islands. Two
contained many small freshly ingested fishes
which were probably the result of a rotenone sta-
tion kill. Of the other two which were speared, one
contained the anthiine fish Mirolabrichthys tuka
(= Anthias pascalus) . Hiatt and Strasburg (1960)
found fish in the stomachs of two from the Mar-
shall Islands, one of which was identified as
Trachurops {— Selar) crumenophthalmus . Hobson
(1974) examined the stomach contents of six
specimens from Hawaii. One contained larval
fishes and mysids, a second had fish and shrimp
remains, and three contained well-digested frag-
ments at least one of which was fish.

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

Figure 39.— Camnx melampygus, 498 mm FL, 1.9 kg, Sanganeb Atoll, Red Sea.

Sixty-one specimens, 298-722 mm FL, from the
Marshall Islands, Hawaiian Islands, Line Islands,
Marcus Island, Solomon Islands, and the Red Sea
were collected for stomach-content study. Seven-
teen stomachs were empty. All the others con-
tained the digested remains of fishes, though one
had, in addition, a squid pen. The following fishes
were identified from the stomach material: eel,
Anthias thompsoni ,Caranx sp. (90 mm FL in a 520
mm C. melampygus), Priacanthus cruentatus,
Cirrhitops fasciatus ,Caesio sp.,Parupeneus sp.,P.
trifasciatus,Pomacentrus pavo, Chromis caerulea,
labrid, Thalassoma purpureum, Ptereleotris mi-
crolepis, Caracanthus unipinnus , Acanthurus tri-
ostegus, acronurus stage of acanthurids (in two
stomachs), and a subadult acanthurid.

Caranx sexfasciatus Quoy and Gaimard (Figure
40): This jack, which ranges from the Red Sea to
eastern Oceania, is closely related to C. hippos of
the Atlantic. It is usually seen in small schools,
but is not common in the Marshall Islands. It is
more elongate than the Caranx spp. discussed
above, and it has a larger eye. The lower-limb gill
raker count is 15-17. The scutes are blackish, there
is a small black spot at the upper end of the gill
opening, and the soft dorsal and anal fins are
tipped with white. The dark bars of the young are
the basis for the specific name.

Only two specimens were caught at Enewetak,
496 and 700 mm FL, 2.3 and 4.6 kg. Both were
nontoxic. No specimens were obtained from
Bikini.

Ommanney in Wheeler and Ommanney (1953)
reported on the stomach contents of specimens
caught during a survey of the Mauritius-
Seychelles region. Eight specimens contained fish
remains, one had squid remains, one had
megalops larvae, and nine were empty. A par-
rotfish and two eels were noted among the stomach
contents.

The stomachs of six specimens of C. sexfasciatus,
385-700 mm FL, from Enewetak and Tahiti were
opened. Five were empty, and one contained
well-digested fish remains. (This jack was speared
at 11:30 a.m.)

Bagnis et al. ( 1972) stated that C. sexfasciatus is
nocturnal. Wheeler and Ommanney (1953) on the
other hand, wrote, "It often takes a lure..."; pre-
sumably he meant one trolled by day.

Scombridae (Tunas)

Gymnosarda unicolor (Riippell) (Figure 41): The
dogtooth tuna is named for its large conical teeth;
it is also unique in having two patches of villiform
teeth on the tongue. It lacks dark stripes or spots
on the body; the second dorsal and anal fins are

235

FISHERY BULLETIN: VOL. 78, NO. 2

Figure 40. — Camnx sexfasciatus, 472 mm FL, 1.8 kg, Enewetak, Marshall Islands.

Figure 41. — Gymnosarda unicolor, 645 mm FL, 3.6 kg, Enewetak, Marshall Islands.

white tipped. A large species, Masuda et al. (1975)
recorded it to a length of 2.4 m. Unlike other large
tunas, in general, it occurs in relatively shallow
coastal water, often around coral reefs, and it read-
ily penetrates the deeper lagoons of atolls.

Thirteen individuals were collected from
Enewetak which ranged from 550 to 1,350 mm FL
(3.2-35.4 kg). Seven caused no symptoms when
liver tissue was fed to mongooses; four produced a
reaction of 1, one was a 2, and one a 3.

Three from Bikini, 737-940 mm FL, 6.4-11.8 kg,
were nontoxic.

Hiatt and Brock (1948, after unpublished data
of J. Marr and O. Smith) stated that the scad,

236

Decapterus sanctaehelenae, was most frequently
encountered in the stomachs of dogtooth tunas in
the Marshall Islands. Schultz in Schultz and col-
laborators (1953) reported that D. muroadsi and
Caesio xanthonotus were regurgitated by Gym-
nosarda nuda ( = G. unicolor) which were caught
at Bikini.

Five of 17 specimens from the Marshall Islands
taken during the survey had empty stomachs. The
others contained fishes, five of which were iden-
tified as: Naso brevirostris, N. vlamingii, Cir-
rhilahrus sp., Caesio sp., Pterocaesio sp. The two
prey specimens of Naso were large adults. The A'^.
vlamingii, taken from the largest G. unicolor,
measured 370 mm SL.

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

Labridae (Wrasses)

Cheilinus undulatus Riippell (Figure 42): The
giant humphead wrasse is one of the largest of
bony fishes. It has been recorded to a length of 2.29
m and a weight of 190.5 kg (Marshall 1964). The
hump on the forehead develops only on larger in-
dividuals. Two dark lines which extend pos-
teriorly from the eye are useful in identifying
juveniles and subadults of this species. It is usu-
ally found on outer reef slopes or in deep channels,
but also occurs in lagoons. It is difficult to ap-
proach underwater. According to Bagnis et al.
(1972) individual fish have a home cave to which
they retreat when threatened and to which they
retire at night. Randall (1958) reported this
species as capable of being moderately to strongly
toxic in Tahiti, where it is called "mara" (Randall
1972). It is one of nine species of fishes which are
banned from sale in the Papeete market (Bagnis
1968).

Seven specimens, 515-995 mm SL, the largest
weighing 34.5 kg, were procured at Enewetak for
testing. The largest gave a reaction of 2 on feeding
to mongooses; the others were 0.

Randall et al. (1978) reported on the food habits
of the giant humphead wrasse based on the
examination of 72 specimens from the Red Sea and
islands of Oceania. The diet is highly varied, the
dominant groups of food organisms being mol-

lusks (gastropods a little more numerous than
pelecypods), crustaceans (especially crabs),
echinoids, and fishes. The hard parts of the inver-
tebrates are crushed to fragments by the powerful
pharyngeal dentition.

Coris aygula Lacepede (Figure 43): This is one of
the two largest species oi Coris (the other an unde-
scribed endemic from Lord Howe Island). The
largest collected, from the Red Sea, measured 465
mm SL and 583 mm TL. Adult males develop a
gibbosity on the forehead similar to that of
Cheilinus undulatus, but these two wrasses could
hardly be confused; the Coris is more elongate
(depth about 3.2 in SL) and has small scales (60-65
lateral line scales for C. aygula, compared with
about 25 for Cheilinus undulatus); also, the lateral
line of Cheilinus is interrupted.

Coris aygula has apparently not been reported
as causing ciguatera but because of its large size
and similar food habits it would seem to be at least
as suspect as C. gaimard which is known to be
poisonous at times. The latter is more colorful,
displaying bright blue spots and a yellow caudal
fin.

Five adults of C. aygula, 329-377 mm SL (0.9-1.9
kg), were obtained from Enewetak for testing. One
of 368 mm SL ( 1 .4 kg) produced a toxic reaction of 1
when its liver and viscera were fed to a mongoose;
the others were nontoxic.

Figure 42.— Cheilinus undulatus, 915 mm SL, 25.8 kg, Enewetak, Marshall Islands.

237

FISHERY BULLETIN: VOL. 78, NO. 2

Al-Hussaini (1947) listed the food of the species
as gastropods {Turbo, Trochus), Dentalium, and
hermit crabs. Hiatt and Strasburg (1960) found
the crushed remains of sand-dwelling pelecypods
and gastropods in a single specimen (identified as
C. angulata) from Enewetak.

Randall, G. J. Vermeij, and H. A. Rehder (man-
uscript in progress) will report in detail on the food
habits of this wrasse. The principal food animals
are gastropods, pelecypods, pagurid crabs,
echinoids, and brachyuran crabs.

Epibulus insidiator (Pallas) (Figure 44): This
unmistakable labrid, popularly known as the
slingjaw wrasse because of its ability to enor-
mously protrude its mouth, occurs from the Red
Sea and east Africa to French Polynesia. Halstead
(1967) listed nine references citing it as
ciguatoxic.

Five specimens from Enewetak, 175-228 mm
SL, 0.34-0.55 kg, were tested for toxicity. None
caused any symptoms in the mongooses.

Hiatt and Strasburg (1960) collected one speci-
men from Enewetak and one from Bikini for food-
habit study; both fish had eaten alpheid shrimps.
They wrote, "This wrasse habitually feeds in
ramose corals by extending its exceedingly pro-
tractile snout into the interstices to capture small
alpheid shrimps and xanthid crabs living there."

For the present food-habit study 16 specimens,
183-240 mm SL, were collected from the Marshall

Figure 43. — Cons aygula, 380 mm SL, Marcus Island.

Islands, Johnston Island, American Samoa, and
the Society Islands. Two had empty stomachs; six
had eaten only fishes and four only crabs. Other
food items were shrimps, unidentified crusta-
ceans, polychaetes, bryozoans, and unidentified
eggs.

Scaridae (Parrotfishes)

Hipposcarus harid (Forsskal) (Figure 45):
Smith (1956) created a new genus, Hipposcarus,
for this species on the basis of the triangular patch
of scales on the cheek with three or four rows
behind, pointed snout, and minute nostrils. Al-
though Schultz (1958, 1969) did not recognize this
genus, it will be considered valid by Nelson and
Randall.

Smith (1959) described a Philippine form of this
species as new, naming it H. schultzi. Schultz
(1969) preferred to regard this form, for which he
gave the range central and western Pacific Ocean,
as a subspecies, Hipposcarus harid longiceps
(Cuvier and Valenciennes).

Halstead (1967) has listed four references re-
porting the occasional toxicity of this parrotfish.

®G. J. Nelson, Department of Ichthyology, American Museum
of Natural History, New York, and the author conferred in Oc-
tober 1977 on the generic limits of the Scaridae. Eventual publi-
cation is planned.

238

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

Figure 44. — Epibulus insidiator, 185 mm SL, Enewetak, Marshall Islands.

Figure 45. — Hipposcarus harid, 282 mm SL, Rangiroa, Tuamotu Archipelago.

Of four specimens, 340-412 mm SL, 1.3-1.8 kg,
obtained at Enewetak, three were nontoxic, and
one produced a reaction of 1.

Reporting on the stomach contents of Ceto-
scarus bicolor, Scarus sordidus, and seven uniden-
tified species of Scarus in the Marshall Islands,
Hiatt and Strasburg (1960) concluded that they
fed mainly on live coral. This is contradictory to

the investigation of scarid food habits by Wood-
Jones (1910), Choat (1966), Randall (1967, 1974),
Rosenblatt and Hobson ( 1969), and Hobson (1974).
Randall (1974), however, presented evidence that
the largest of the parrotfishes, Bolbometopon
muricatus, feed heavily on living coral. Also
Glynn et al. (1972) listed three scarids as coral
predators off the Pacific coast of Panama.

239

FISHERY BULLETIN: VOL. 78, NO. 2

Scarus gibbus Riippell (Figure 46): The name
Scarus microrhinos Bleeker has generally been
used in the Pacific for this species (Schultz 1958),
and it is under this name that its toxicity has been
reported (Halstead 1967). Smith (1959) resur-
rected the name Scams j^t66«s Riippell for the Red
Sea form of this species, though he still recognized
S. microrhinos. Schultz (1969) placed four nomi-
nal species, including S. microrhinos, under the
one name S. gibbus. The large males are readily
distinguished by the near-vertical anterior profile
of the head. Other useful characters for distin-
guishing the species are four median predorsal
scales, three row^s of scales on the cheek, and 16 or
17 pectoral rays.

Of 19 specimens, 326-414 mm SL, 1.05-2.8 kg,
speared from Enewetak, only 1 of 410 mm (2.3 kg)
was slightly toxic (mongoose reaction of 1).

Scarus rubroviolaceus Bleeker (Figure 47): This
parrotfish w^as selected as the type-species of a new
genus, Scarops, by Schultz (1958) principally on
the basis of its having a single enlarged row of
teeth on each upper pharyngeal bone. This genus,
however, was not recognized by Rosenblatt and
Hobson (1969). The primary phase of S. rubro-
violaceus is reddish with small blackish spots
and short streaks on the scales; the terminal male
phase (the nominal Pseudoscarusjordani Jenkins
and Callyodon africanus Smith were based on this
form) is complexly colored, but mainly purplish on
the anterior part of the body and abruptly green

posterior to about the base of the seventh dorsal
spine (this bicolored effect more evident in live
than on freshly dead specimens); the head is
mainly blue-green, shading to orange-yellow on
the opercle, with transverse bands of turquoise
and salmon on the lips and chin. There are gener-
ally 6 median predorsal scales, 3 rows of scales on
the cheek, and 15 pectoral rays.

Like the other species of Scarus, S. rubro-
violaceus is closely tied to coral reefs. It ranges
from east Africa to the tropical eastern Pacific.
Although this species has not been reported as
poisonous, it would seem to have the same poten-
tiality of causing ciguatera as other parrotfishes
which may be toxic.

Three specimens, 355-370 mm SL, 1.4-1.6 kg,
were obtained from Enewetak in order to test for
possible toxicity. None were toxic.

Rosenblatt and Hobson ( 1969) wrote, "All of the
eastern Pacific species of Scarus feed by scraping
algae from the surface of rocks. We did not see

evidence that they bit off pieces of coral " Scarus

rubroviolaceus is one of the four species they
studied. Glynn et al. ( 1972), on the other hand,
included S. rubroviolaceus among the three
scarids they regarded as coral predators from ob-
servations off Panama.

Acanthuridae (Surgeonfishes)

Acanthurus xanthopterus Cuvier and Valen-
ciennes (Figure 48): This is the largest member of

FIGURE 46.— Scarus gibbus, 417 mm SL, 2.8 kg, Tahiti, Society Islands.

240

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

Figure Al.—Scarus rubroviolaceus, 355 mm SL, 1.35 kg, Enewetak, Marshall Islands.

FIGURE 48.— Acanthurus xanthopterus, 400 mm SL, 2.3 kg, Enewetak, Marshall Islands.

the genus Acanthurus. It is one of a complex of
species with a gizzardlike stomach. In the Mar-
shall Islands it could only be confused with A.
mata, also a large species. The outer third of the
pectoral fins of A. xanthopterus are yellowish (fins
uniform brown on A. mata), and there are about 4
lengthwise bands in the dorsal fin (about 8 in the
fin of A. mata); there are fewer gill rakers (16-22
for A. xanthopterus, compared with 21-25 for A.
mata). This species is distributed from east Africa

to the eastern Pacific. It occurs more in lagoons
and bays than exposed outer reef areas, and it
ranges into deeper water than other Acanthurus
in general. Also it ventures farther from the cover
of coral reefs than other species. Schultz in Schultz
and collaborators (1953) used the name Acan-
thurus fuliginosus Lesson for this fish, but there is
no basis for equating it to Lesson's illustration and
description, as explained by Randall (1956). The
junior synonym Teuthis crestonis Jordan and

241

FISHERY BULLETIN: VOL. 78, NO. 2

Starks was created for the species from Mexico.

Two specimens, 423 and 425 mm SL, 2.7 kg,
were obtained from Enewetak for the assay of tox-
icity. Neither were toxic.

Hiatt and Strasburg (1960) examined the
stomachs of four specimens from Enewetak, two of
which were empty. The other two contained short
filaments of algae with much sand, hydroid hy-
drocaulus, and wood splinters (probably from
grazing on pilings). Jones (1968) classified A.
xanthopterus as a grazer on diatoms and detritus
in sand patches. That it will take animal food
when the opportunity arises was aptly shown by
Helfrich and Banner (1963) who used this species
to induce ciguatera toxicity by feeding the poison-
ous flesh of Lutjanus bohar.

Ctenochaetus striatus (Quoy and Gaimard)
(Figure 49): This surgeonfish is much the most
common of the four species of the genus that occur
in the Marshall Islands. It is, in fact, one of the
most abundant reef fishes throughout the Indo-
West Pacific region (though not Hawaii). The
genus is named for its comblike teeth which are
numerous, slender with expanded incurved tips,
and flexible in the jaws. Randall (1955b) has dif-
ferentiated C. striatus from the other species by

having 5-7 denticulations on the expanded distal
tips of the upper teeth, the highest average
number of dorsal and anal soft rays (modally 29
dorsal rays and 26 or 27 anal rays), and a lunate
caudal fin.

Bagnis et al. ( 1968) reported that surgeonfishes
( particularly C. striatus ) are responsible for 65% of
the cases of ciguatera in Tahiti. There are three
reasons for this: 1) the abundance of C. striatus, 2)
its good-eating quality, and 3) the knowledge that
the symptoms will be mild if ciguatera is incurred.

Bagnis (1968) documented the great variation
in the symptoms of ciguatera in French Polynesia.
He noted that digestive and neurologic symptoms
predominated among those patients who had in-
gested surgeonfishes.

Yasumoto et al. (1971) determined that there
are two principal toxins in C. striatus, one of which
is fat soluble and chromatographically identical
with ciguatoxin, and the other is water soluble.
The latter was found only in the liver and gut
contents. In a few specimens from Tahiti a differ-
ent fat-soluble toxin and a different water-soluble
toxin were detected.

In order to determine if more than one toxin is
present in C. striatus in the Marshall Islands, 22
adult specimens were speared on lagoon reefs of

Figure 49. — Ctenochaetus striatus, 94 mm SL, Enewetak, Marshall Islands.

242

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

Enewetak and sent frozen to the Laboratory of
Marine Biochemistry of the University of Tokyo.
The specimens, which weighed from 130 to 230 g
each, were pooled in groups of three (four for one
group). The flesh and the viscera were separated
for each group, and the gut contents of all groups
were pooled. Fat-soluble and water-soluble frac-
tions were prepared and injected intraperitoneally
into mice at doses of 4,000, 2,000, and 1,000 ^g/g-
Two mice were used for each dose. If the mice were
not killed by a dose of 4,000 ;Ltg/g within the obser-
vation period of 48 h, the preparation was re-
garded as nontoxic. If they were killed by a dose of
1,000 iJ-g/g, it was classified as strongly toxic, at
2,000 ixg/g moderately toxic, and at 4,000 /xg/g
weakly toxic. The results were reported in a letter
by the late Yoshiro Hashimoto, then the Director
of the Laboratory. None of the preparations were
strongly toxic. All the preparations from the flesh
were nontoxic. Four of the seven fat-soluble prep-
arations of the viscera were moderately toxic, one
was weakly toxic, and one nontoxic. Five of the
seven water-soluble fractions from the viscera
were weakly toxic and the remaining two non-
toxic. Both the fat-soluble and the water-soluble
preparations of the pooled gut contents were mod-
erately toxic.

The food habits and mode of feeding of C.
strigosus from the Hawaiian Islands were investi-
gated by Randall (1955b); underwater observa-
tions of C. striatus indicate that its feeding is es-
sentially the same. These fishes are detritus
feeders. From a near- vertical position (if the bot-
tom is horizontal) about 15 mm above the sub-
stratum, the fish move abruptly downward with
mouth open. The lips and teeth scrape over the
surface at the same time that suction is initiated.
The soft detrital material and fine inorganic sedi-
ment are ingested. If coarse particles of sand are
picked up, they are forcefully ejected. The stomach
contents of seven adults of C. strigosus from
Hawaii consisted of inorganic sediment (up to 90^
by volume); fragments of red, green, and blue-
green algae; diatoms; and unidentified soft or-
ganic material. In an aquarium experiment C.
strigosus was unable to feed on an intact thallus of
the filamentous alga Polysiphonia sp. When the
same algae was finely fragmented and placed on
the bottom, it was readily consumed.

Baiistidae (Triggerfishes)

Pseudobalistes flavimarginatus (Riippell) (Fig-

ure 50): This is one of three large species of trig-
gerfishes that occur in the Marshall Islands. It
may be distinguished from other balistids by the
following characters collectively: the second dor-
sal and anal fins elevated anteriorly, five or six
rows of spines on the caudal peduncle, no scales on
the cheek (of adults), caudal fin of adults emargin-
ate, and yellowish margins on the median fins.
Woods in Schultz and collaborators (1966) failed
to list this species from the Marshall Islands, but
the color plate in Hiyama ( 1943, pi. 22, fig. 61) and
the study of Hiatt and Strasburg (1960) clearly
indicate its presence there. Hiatt and Strasburg
stated that it is solitary, uncommon, and occurs on
lagoon and interisland reefs in quiet water of
10-30 ft (3.1-9.1 m) deep. Although Hiyama wrote
that this fish was not regarded as poisonous in the
Marshalls, other records (Halstead 1967) dem-
onstrate its capacity for causing ciguatera. It is
one of the nine species of fishes forbidden to be sold
in the fish market in Papeete, Tahiti (Bagnis
1968).

Two specimens, 465 and 535 mm SL, weight not
taken, were collected in Bikini. Neither was
poisonous.

Clark and Gohar (1953) reported pieces of
branched coral (Stylophora) 2-3 cm long in the
stomach of a specimen 440 mm SL from the Red
Sea. Hiatt and Strasburg (1960) examined two
stomachs from the Marshall Islands. They found
the crustacean Lydia annulipes and isopods,
crushed gastropods including Oliva sp., foraminif-
era, and colonial tunicate fragments.

The stomach and gut contents of only two
specimens were obtained for the present study.
One of 254 mm SL from the Red Sea was empty.
The second of 390 mm SL from Tahiti had eaten
Diadema.

Balistoides uiridescens (Bloch and Schneider)
(Figure 51): This is another large triggerfish for
which there have been a few records of toxicity. It
shares the elevated anterior part of the second
dorsal and anal fins and the rows of spines on the
caudal peduncle with P. flavimarginatus, but is
differentiated by having its cheek totally scaled
and its caudal fin rounded to slightly double emar-
ginate as an adult; also the margins of its median
fins are broadly blackish. It ranges from the Red
Sea to eastern Oceania. It occurs in both lagoons
and outer reef slopes. Like other triggerfishes, it
has a favorite hiding place in the reef into which it
wedges itself when threatened.

243

FISHERY BULLETIN: VOL. 78, NO. 2

Figure 50. — Pseudobalistes flavimarginatus , 265 mm SL, Palmyra, Line Islands.

A single specimen, 456 mm SL, 4.5 kg, from
Enewetak was nontoxic.

The stomach and gut contents of four specimens,
278-525 mm SL, from the Society Islands and the
Red Sea were examined. Echinoids, including
Diadema, Echinometra, and spatangoids, were
the main items of diet, but pelecypods, crabs,
polychaete tube worms, gastropods, chitons,
foraminifera, and algae and detritus were also
present.

DISCUSSION AND SUMMARY

As mentioned in introductory remarks, the ini-
tial testing for level of ciguatera at both Enewetak
and Bikini revealed only an occasional toxic fish
among the species responsible for most cases of
this type of poisoning in the Pacific. As expected,
the toxic individuals were invariably adults of
moderate to large size for the species. A decision
was then made to concentrate the fishing effort on
the larger individuals of the species most often
implicated in ciguatera. These dangerous species
are, in general, not common. They are at or near

the peak of the well-known "pyramid of numbers,"
i.e., the reduction in number of individuals one
encounters analyzing the populations in succes-
sive steps up the food chain. Consequently, much
more effort was expended in catching not only
these fishes but just the larger individuals of these
species. Also, it is for this reason that some rela-
tively common species such as Lutjanus fulvus
and Adioryx spinifer are represented by few
individuals in this report and others such as the
smaller species of groupers of the genera Epine-
phelus and Cephalopholis were not collected. In
highly toxic sectors these species can be poisonous,
though even there the incidence is low.

A total of 551 specimens of 48 species were
tested from Enewetak and 256 specimens of 23
species from Bikini. In addition, 12 adult speci-
mens of Lutjanus bohar from Rongelap were tested,
one of which was toxic at the 5 level. The results of
the testing of fishes from Enewetak are sum-
marized in Table 1, and for Bikini in Table 2;
37.3% of the fishes from Enewetak gave a positive
reaction for ciguatoxin, and 19.7% of those from
Bikini.

244

RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

"%

Figure 51. — Balistoides viridescens, 456 mm SL, 4.5 kg, Tetiaroa, Society Islands.

It must be emphasized that liver and viscera of
the suspect fishes were used in the mongoose feed-
ing tests (except for sharks) and not flesh. Because
of the much higher level of ciguatoxin in the inter-
nal organs than in muscle tissue, low-level toxic-
ity (indicated by mongoose reactions of 1 or 2) from
liver and viscera would probably not result in a
detectable level of toxin if flesh from these fishes
had been used in the tests. When the percentage of
toxicity is computed for the reactions 3-5 (it is this
level at which a human eating the flesh of these
species might be expected to fall ill with cigua-
tera), the percentage of toxic fishes drops to 16.2
for Enewetak and 1.4 for Bikini.

When one considers the effort directed almost
entirely to the worst offenders in ciguatera, the
level of toxicity at Enewetak must be regarded as
relatively low and that of Bikini decidedly so. Most
of these fishes are avoided as adults by islanders in
Oceania regardless of the area of capture. There-
fore it is concluded that the returning residents to
Enewetak and Bikini need not fear at this time
any unexpected threat of ciguatera at their atolls.

Only eight species of fishes produced reactions of
4 or 5 in the test animals; that is, severe illness

or death: Lycodontis javanicus, Cephalopholis
argus, Epinephelus hoedtii, E. microdon, Plec-
tropomus leopardus, Aprion virescens, Lutjanus
bohar, and Lethrinus kallopterus. Had more
specimens of Sphyraena barracuda, Caranx ig-
nobilis, and Cheilinus undulatus, particularly of
large size (none of the specimens taken during this
survey approached the maximum size), been col-
lected, then they may be expected to be included in
the above list (in view of their reputations for
causing ciguatera in other areas).

The moray Lycodontis javanicus was clearly the
most toxic of all the species tested, with all indi-
viduals producing a reaction of 2 or more in mon-
gooses and one-third of them the lethal 5.

Randall (1958) analyzed the kinds of fishes
which have caused ciguatera in terms of habitat,
mode of life, and food habits. These species are
shore fishes associated with reefs. Usually they
are bottom-dwelling generally in < 60 m, but they
may be semipelagic open-water forms that range
into the reef habitat to feed. They may be car-
nivorous or they may feed on benthic algae or
detritus. Of the carnivores, those that prey heavily
on reef fishes are the most prone to be poisonous.

245

FISHERY BULLETIN: VOL. 78, NO. 2

whereas those that eat mainly benthic crusta-
ceans the least. Fishes that feed wholly or primar-
ily on plankton are not apt to be toxic. Some mol-
lusk and echinoid feeders may cause severe cases
of ciguatera. The level of toxicity among benthic
herbivores and detritus feeders is consistently

low.

The food-habit studies of this survey support
these generalizations. Seven of the eight most
toxic species are piscivorous. The one other, Leth-
rinus kallopterus, appears to feed mainly on
echinoids and mollusks. No specimens ofLutjanus
fulvus,Epinephelus socialis, and Adioryx spinifer
were found to be toxic (although relatively few
specimens were collected); these feed more on
crustaceans than fishes. Among the herbivores
tested, only two individuals of Scarus and one of
Kyphosus gave a reaction of 1. A water-soluble
toxin as well as ciguatoxin were found in the
detritus-feeding surgeonfish Ctenochaetus
striatus, but in small amounts.

The relatively low level of ciguatoxin in sharks
is surprising. Because they feed heavily on fishes
and are believed to be long-lived, one might expect
them to be as ciguatoxic as the larger moray eels.
The tropical species of sharks are not as widely
eaten as bony fishes. If they were, no doubt more
cases of ciguatera would be attributed to them.
The species of Carcharhinus appear to prey to a
significant degree on pelagic fishes, and when they
do feed on reef-dwelling species, they seem to take
many plankton-feeding forms. This may in part
explain their apparent relatively low level of
ciguatoxin. Still another possibility is that sharks
may not accumulate as much ciguatoxin in their
tissues as bony fishes.

Because ciguatera can be highly localized to cer-
tain reefs or even sectors of reefs, the fish collect-
ing was carried out at many different locations at
the atolls. No one area was detected as having a
notably higher level of toxicity.

Many of the most dangerous ciguatoxic species
are roving predators. Examples are the bar-
racudas, jacks, dogtooth tuna, emperors, and, to a
lesser extent, the snappers. They can be caught at
a different area from which they acquired most of
their toxicity. The strong localization of ciguatera
occurs more where the level of toxicity is high and
the smaller more resident species are poisonous.
Our fishing has not been sufficiently extensive to
demonstrate minor differences in the incidence of
ciguatera with locality.

At Enewetak most of the fishing was un-

dertaken on the southern part of the atoll, par-
ticularly in the vicinity of Enewetak Island, the
largest of the atoll . This island had the largest pop-
ulation of Marshallese people before they were
evacuated from the atoll, and it is expected that
it will have the largest number when all have
been repatriated. Also it is in this area that
most of the long-term disturbances of the marine
environment, such as the dumping of unwanted
material, have taken place. It is fortunate that
ciguatera, though more in evidence at Enewetak
than at Bikini, is not a major problem as might
have been predicted from the impact of western
man on the atoll.

ACKNOWLEDGMENTS

The author and associates acknowledge with
gratitude the support of the U.S. Energy Research
and Development Administration through con-
tract E(26-l)-641 with the University of Hawaii
and Bemice P. Bishop Museum, Honolulu.

The following individuals participated in the
fishing program in the Marshall Islands: Gerald S.
Akiyama, Bruce A. Carlson, the late David Erlen-
kotter. Glen H. Fredholm, James W. Fry, Gregory
Gahagan, Gerald Gulden, Walter C. Gutjahr, Guy
S. Haywood, George MacGuire, Oliver K. McCaus-
land, Rhett M. McNair, Robert F. Meyers, Takeo
Okamura, John E. Randall, Robert P. H. Ruther-
ford, Arnold Y. Suzumoto, and Gordon W. Tribble.
In addition, Phillip B. Lamberson, formerly of the
Mid-Pacific Marine Laboratory, Harry J. Miller
and Russell E. Miller, former resident personnel of
the atoll, assisted in the collecting at Enewetak.

The testing of the toxicity was carried out by
James Murphy and Lambert Yamashita at the
Hawaii Institute of Marine Biology of the Univer-
sity of Hawaii, under the direction of A. H. Ban-
ner, except for the last sampling in May 1978 for
which an initial screening was made by Yoshi-
tsugi Hokama of the Department of Pathology,
University of Hawaii, by radioimmunoassay
(Hokama et al. 1977). The higher reactions were
then confirmed by mongoose feeding at the Ber-
nice P. Bishop Museum by Arnold Y. Suzumoto.

A. H. Banner and Helen A. Randall provided
helpful suggestions and reviewed the manuscript.

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RANDALL: SURVEY OF CIGUATERA AT MARSHALL ISLANDS

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249

CALLINECTES (DECAPODA: PORTUNIDAE) LARVAE IN
THE MIDDLE ATLANTIC BIGHT, 1975-77^

Peter O. Smyth^

ABSTRACT

Distribution of Callinectes larvae in surface (neuston) and subsurface shelf waters in the Middle
Atlantic Bight was determined from quarterly zooplankton collections taken during a 2-year study.
Observations confirmed the presence in offshore waters of a large larval pool from which recruitment
may take place. Larvae were predominantly late zoeae and megalope, with peak abundances in late
summer collections reaching 16,000 per 100 m^ in neuston collections. During summer, crab larvae
were distributed across the shelf with the majority at 10-80 km offshore. Abundances were sig-
nificantly greater in neuston than subsurface zooplankton collections and generally greater in neuston
collections taken at night. Water temperature and distance from shore were factors most closely
correlated with abundance of larvae in the neuston. Megalopae of Callinectes were present at outer
shelf stations in winter and spring and together with megalopae oi Portunus and other forms were of
southern origin. Based on experimentally determined temperature-salinity preferences reported in the
literature for Callinectes larvae, metamorphosis may be delayed in cooler offshore waters, thus
increasing chances of long-range transport.

The community of organisms of the surface layer
(the neuston^ ) has received increasing attention in
terms of samphng problems and possible ecologi-
cal significance. Zaitsev ( 1970 ) described the neus-
ton as consisting chiefly of early developmental
stages of fishes and invertebrates. Berkowitz
(1976) and Morris (1975), however, found oceanic
neuston faunistically impoverished in comparison
with zooplankton of the immediate subsurface.
Few studies of the neuston of shelf and shallow
waters exist; preliminary indications are that the
zooplankton of the surface waters of the continen-
tal shelf are at least quantitatively enriched
(Grant^).

Callinectes , euryhaline members of the predom-
inantly marine Portunidae, spawn along the shore
of open oceans and in mouths of inlets and es-
tuaries. Larval development occurs in shelf wa-

'Contribution No. 952 from the Virginia Institute of Marine
Science. From part of a dissertation to be submitted in partial
fulfillment of requirements for the degree of Doctor of
Philosophy, College of William and Mary.

^Virginia Institute of Marine Science and School of Marine
Science, the College of William and Mary, Gloucester Point, VA
23062.

'Neuston has generally been defined operationally as the
community of organisms sampled by gear specifically designed
to sample the surface layer. The term is used in that sense in this
paper. For a review of numerous terms associated with the sur-
face layers, see Banse (1975).

"Grant, G. C. 1977. Middle Atlantic Bight zooplankton:
seasonal bongo and neuston collections along a transect off
southern New Jersey. Spec. Rep. Appl. Mar. Sci. Ocean Eng.,
Va. Inst. Mar. Sci. 173, 138 p.

Manuscript accepted November 1979.
FISHERY BULLETIN; VOL. 78, NO. 2, 1980.

ters, with probable return inshore by megalopae
andjuveniles (Williams 1965, 1971, 1974; Costlow
1967; Tagatz 1968). Callinectes megalopae have
been reported offshore in shelf waters (Nichols and
Keney 1963; Dudley and Judy 1971); retention in
shelf waters and subsequent transport of
megalopae have been proposed as mechanisms in
dispersal, widespread distribution, and mainte-
nance of genetic continuity in the species (Costlow
1967; Williams 1971, 1974; Cole and Morgan
1978).

Callinectes larvae, at least zoeae, have surface
affinities (Tagatz 1968; Dudley and Judy 1971;
Sandifer 1972), but megalopae have generally
been less numerous in collections than zoeae and
limited to bottom samples (Tagatz 1968; Sandifer
1972; Goy 1976). Williams (1971), however, re-
ported Callinectes megalopae to be active in es-
tuarine surface waters at night.

With the widespread distribution and known
abundance of Callinectes adults and the accepted
migratory sequence of developmental stages
(inshore-offshore-inshore), the reported abun-
dance of late stage larvae is surprisingly low.
Furthermore, the existence in shelf waters of a
Callinectes larval pool from which recruitment to
estuaries may occur is based on relatively few
studies and limited sampling.

This paper reports the identification, distribu-
tion, and abundance oi Callinectes larvae in neus-

251-

FISHERY BULLETIN: VOL. 78, NO. 2

ton and subsurface water column collections from
shelf waters in the Middle Atlantic Bight. My ob-
jectives specifically were to: 1) determine whether
a reservoir of Callinectes larvae, particularly
megalopae, exists in shelf waters; 2) determine
abundance relationships between Callinectes lar-
vae in neuston and water column samples; 3)
examine the role of certain environmental factors
(e.g., temperature, salinity, location) in the dis-
tribution and abundance of these larvae; 4) assess
the role of Callinectes megalopae in larval re-
cruitment and dispersal in view of my findings and
results of laboratory studies of temperature-
salinity tolerances of larvae; and 5) examine in-
teraction of the developmental migratory se-
quence, biogeography, and evolutionary history of
Callinectes.

METHODS

Zooplankton collections were made as part of a
2-yr survey (Table 1) conducted by the Virginia
Institute of Marine Science (VIMS) for the Bureau
of Land Management (1975-77). This study was
designed to provide ecological information prior to
drilling for oil on the Middle Atlantic Bight conti-
nental shelf. In addition to zooplankton studies
the survey included studies of benthic and epiben-
thic communities and the physical, chemical, and
geographical oceanography of the shelf and over-
lying waters.

During the first year, six stations were occupied
seasonally (quarterly) on a transect across the
shelf off Atlantic City, N.J. (Figure 1; Table 2: CI,
Dl, N3, E3, F2, Jl). Zooplankton in the water
column was sampled at night by paired, double
oblique tows with 60 cm diameter, opening-closing
bongo nets (McGowan and Brown^) (505 fim and
202 ixm mesh). Bongo nets were metered (General
Oceanics, Inc. flowmeters^) and were closed during
passage through the surface layer. Neuston was
sampled every 3 h over a 24-h period with a neus-
ton net designed at Woods Hole Oceanographic
Institution. This sampler consisted of two
hydrodynamically-shaped, foam-filled floats con-
nected by an endless fiber glass band (Grant'). The

Table l. — Dates for cruises in the Middle Atlantic Bight, 1975-
77, over which Callinectes larvae were sampled.

*McGowan, J. A., and D. M. Brown. 1966. A new opening-
closing paired zooplankton net. Univ. Calif., Scripps Inst.
Oceanogr. Ref. 66-23, 56 p.

^Reference to trade names dpes not imply endorsement by the
National Marine Fisheries Service, NOAA.

'Grant, G. C. 1979. Middle Atlantic Bight zoo-
plankton. Spec. Rep. Appl. Mar. Sci. Ocean Eng., Va. Inst. Mar.
Sci. 192, 236 p.

252

First year

Second year

Season

Cruise

Date

Cruise

Date

Fall
Winter
spring
Summer

01W
02W
03W
04W

23-30 Oct. 1975
5-16 Feb. 1976
8-16 June 1976
1-9 Sept. 1976

05W
06W
07W
08W

5-28 Nov. 1976'

20Feb.-6 Mar. 1977

18-28 May 1977

19-29 Aug. 1977

'Cruise split into two legs.

\

>

)>r

CI

•

/

.['2000

^^^^\

\

B5>\

f:^

N J

|\

% \

[Iff

^

T

CI \

•

/^ • .-■ E3 t
\ • '■

^

DEL. Js\

\

-.

/

^

M D bi

LI

•

i

■^

\ G)

^•A^ i '^p^ ■■>

i-\

Figure l. — Study area and sampling stations for surface and
subsurface zooplankton in the Middle Atlantic Bight, 1975-77.
Stations LI, L2, L4, L6, B5, A2 were sampled only during the
second year of the study; CI, Dl, N3, E3, F2, Jl were sampled
both years.

mouth of the net was 1.0 m wide, and in calm water
the gear sampled approximately the upper 12 cm
of the water column. However, the net appeared to
sample, on the average, less than the upper 12 cm
due to sea conditions and towing characteristics of
the ship and sampler. Calculated volumes were
based on a 12 cm sample depth and were thus
overestimated, resulting in underestimation of

SMYTH: CALLINECTES LARVAE IN MIDDLE ATLANTIC BIGHT

Table 2. — Station data forzooplankton collections in the Middle
Atlantic Bight, 1975-77.

Location

Distance from

Bottom

Station

Lat. N

Long. W

shore (km)

depth (m)

A2

39°21.8'

72=31.8'

149

131

B5

39^28. 3'

73°02.r

93.6

62.6

CI

39=22.2'

74°14.9'

10.2

16.8

01

3904.7-

73°53,2'

56.5

37.2

N3

38''51.4'

73°44.8'

83.4

44.7

E3

38 41.2'

73°32.5'

112

59.5

F2

38"44.4'

73°09.2'

132

108

J1

38 44.2'

73°00.7'

141

355

L1

37°31.1'

75°18.3'

31.5

22.3

12

3r'20.r

74°58.6'

65.8

41.3

L4

37°08.1'

74°36.8'

105

94.6

L6

3r04.4'

74°33.1'

113

322

larval densities. Tows were of 20-min duration
except when large abundances of neuston required
premature termination of a tow. The net was me-
tered beginning with the June 1976 cruise; before
that cruise, sample volumes were estimated on the
basis of a standard 20-min tow. Tows were made
from an extended boom alongside the ship at
speeds of 1.5-2.5 kn.

During the second year two stations to the north
and a transect to the south of the original transect
were added. On each cruise neuston samples were
taken over 24 h at nine stations (Figure 1; Table 2:
A2, B5, CI, E3, Jl, LI, L2, L4, L6). A single neus-
ton tow was made at stations Dl, N3, and F2 as a
companion to bongo tows. Bongo tows were made
at all 12 stations following the procedure used
during the first year. In addition, replicate tows
were made at stations A2, B5, and E3 (repeated
tows of two bongo nets with paired 202 yum and
505 yum mesh nets). Three such replicate tows
were made at night at each designated station.

Samples were preserved in a 4% solution of
borax-buffered formaldehyde and seawater
(Steedman 1976). In the laboratory, major
taxonomic groups were quantitatively sorted from
whole or split samples (Burrell et al. 1974). Deca-
pods were sorted to species and identified (when
possible ) on the basis of published descriptions and
taxonomic keys.

Megalopae of several taxa, including Cal-
linectes , were reared aboard ship to juveniles. Sev-
eral megalopae were removed from a sample and
tentatively identified or identification characters
noted. Megalopae were placed in plastic tackle
boxes with 505 ixm mesh bottoms and the boxes
were floated in an aquarium filled with seawater
taken in situ. Megalopae were fed Artemia salina
nauplii and bits of fresh fish meat. Megalopae with
the same characteristics as the megalopae used for
rearing were fixed and preserved.

Abundance was expressed as number per 100
m^; for graphical presentation and certain statis-
tical procedures abundance was compressed by the
transformation logio(Z + 1). Most statistical pro-
cedures were based on station means, with eight
neuston collections per station. The distribution of
sample means tends to normality as the sample
size increases (Snedecor and Cochran 1967), and
the logarithmic transformation tends to make var-
iance independent of the mean (Sokal and Rohlf
1969). Based on the i^-max test (Sokal and Rohlf
1969), untransformed abundances within stations
were very heteroscedastic, while log-transformed
abundances at stations with Callinectes larvae in
at least six samples did not have unequal var-
iances at P <0.05. Coefficients of variation for each
station were reduced considerably by the log
transformation, and abundances appeared better
centered about the median based on "box and
whisker" diagrams (Tukey 1977). The assumption
of a multivariate normal distribution could not be
tested for the data set. Significance levels for
mulitvariate data are often difficult to interpret;
therefore, significance levels, where indicated for
parametric procedures, should be taken as a guide.

A larval stage index (LSI) similar to that of
Manzi and Maddox ( 1976) was calculated for sev-
eral larval types. The LSI is a point along the
continuum of development from hatching (first
zoea) to juvenile; the LSI characterizes the stage of
an average individual of a given species in a sam-
ple. It is calculated as a weighted average, i.e.,

LSI =

2 iSi

f=i

where i
n

number of the developmental stage,
number of developmental stages,
first zoeae through adult,
abundance of the ith stage.

The LSI is standardized and constrained in the
interval 0.0-1.0 by the assignment of a stage
number (1> the megalopa) to the adult stage.
Thus, an LSI = 0.67 characterizes animals that
have completed, on the average, about two-thirds
of the developmental sequence from hatching to
first crab. The LSI is, however, a measure of cen-
tral tendency and does not indicate statistical dis-

253

FISHERY BULLETIN: VOL. 78, NO. 2

persion. Based on Costlow and Bookhout ( 1959), n
was set at 10 for eight zoeal stages, a megalopa,
and an adult.

Comparisons between Callinectes abundance in
neuston and bongo (surface vs. subsurface) collec-
tions at each station were made for: 1) maximum
abundance for each gear type; 2) mean abundance
of the consecutive pair of tows with the largest
collective abundance; and 3) mean abundance for
each gear type. Significance of differences for
these means was determined by the Wilcoxon
signed rank test (Wilcoxon 1945), a distribution-
free method (Hollander and Wolfe 1973).

Comparisons between neuston and bongo collec-
tions are comparisons between abundances in a
single "layer" and abundances integrated over the
water column. Therefore, abundances in bongo
collections represent mean abundances in the
water column (excepting the surface) and do not
indicate vertical distribution of the animals.

Diel patterns in neuston abundance during each
cruise were represented by total numbers per 100
m^ for each sampling time interval (3 h) summed
over the stations in a cruise. To weight frequency
as well as abundance during a single cruise, ranks
were assigned to abundance during each time in-
terval (lowest to highest) at each station. The rank
sum of each time interval was calculated as the
sum of the ranks during that time interval over all
stations during a single cruise.

For neuston collections the relationship be-
tween mean abundance per station and environ-
mental factors (temperature, salinity, station
depth, and distance from shore) was examined.
Data were analyzed using subprograms ( multiple)
Regression and Partial Corr (partial correlation)
of the Statistical Package for the Social Sciences
(SPSS, Nie et al. 1975). Relationships between
abundance and factors were examined in terms of
bivariate as well as multivariate distributions.

RESULTS

Identification

Callinectes zoeae were identified and staged on
the basis of Sandifer's ( 1972) key and descriptions
of laboratory -reared zoeae of C. sapidus (Costlow
and Bookhout 1959) and C. similis (Bookhout and
Costlow 1977). Key characters include: 1) relative
length of the antennal exopodite (<'/3 protopodite
length) and the presence of two unequal terminal
setae on the antennal exopodite; 2) the presence of

lateral projections on abdominal somites 2 and 3;
3) the presence of relatively long, sharply pointed
posterolateral spines on abdominal somites 3-5;
and 4) the presence of one dorsal and one lateral
spine in each telson furca. Structure and setation
of mouthparts and appendages were compared
with published descriptions for further confirma-
tion. The above characters effectively separated
Callinectes zoeae from all other zoeal types in my
collections. The planktonic material appeared to
include seven or eight distinct zoeal stages after
allowance for individual variation in certain
structures, setal counts, relative lengths, etc. (e.g.,
the antennal endopodite "bud" denoting stage 5,
which varied from little more than a swelling to a
definite projection).

Identification of Portunidae megalopae was
based on Kurata's (1975) list of familial and sub-
familial (Portuninae) characters, which include
the presence of sternal cornua (paired spines pro-
jecting posteriorly from the fourth sternal seg-
ment beyond the base of the fifth leg) (Figure 2),
and the presence of paddlelike dactyls with long,
hooked setae on the fifth pereopods.

Callinectes and Portunus megalopae were sepa-
rated on the basis of the characters listed by
Bookhout and Costlow (1974), which include the
absence in Callinectes and the presence in Por-
tunus of a ventral spine on the coxa of the second
pereopod ( Figure 2), and carpal spine(s) on the first
pereopod.

My collections included numerous megalopae
attributable to Portunus; all had a coxal spine on
the second pereopod and a carpal spine on the first
pereopod. The basischiopodite hook reported for

Abdominal somife

Portunus

Coxal /
Spine

Sternal cornua

Callinectes

Figure 2. — Lateral profile including the abdomen ofCalUnectes
and Portunus megalopae. Distinguishing characters are indi-
cated. Sizes are not relative.

254

SMYTH: CALLINECTES LARVAE IN MIDDLE ATLANTIC BIGHT

Portunus (Bookhout and Costlow 1974; Kurata
1975) and Callinectes (Costlow and Bookhout
1959; Bookhout and Costlow 1977) was present for
all Callinectes and most, but not all, Portunus
specimens.

The profile of abdominal somites was a more
subjective, yet reliable, criterion for the separa-
tion of Portunus and Callinectes megalopae. In
Portunus the dorsal surface of each somite, par-
ticularly the first, was noticeably raised, creating
a "bumpy" profile; in Callinectes the profile was
noticeably smoother (Figure 2). (See also Book-
hout and Costlow 1974, fig. 11; 1977, fig. 11.) Al-
though identifications were based on numerous
characters, this particular criterion was consis-
tent and reliable.

Carapace lengths in = 418, X = 1.56, SE =
0.004 mm) of Callinectes megalopae (measured
dorsally from the base of the rostrum to the pos-
terior edge of the carapace) were slightly less than
carapace lengths reported for C. sapidus (X = 1.65
mm) but considerably greater than lengths re-
ported for laboratory-reared C. similis (X = 1.30
mm) (Bookhout and Costlow 1977).

I recognized no specific differences among Cal-
linectes megalopae or zoeae; therefore, larvae re-
ferred to as Callinectes may represent more than
one species. Abundance and known distribution of
adults (Williams 1974) indicated that most, if not
all, specimens were C. sapidus. Several small
adult C. similis, however, were taken in neuston
collections at station Cl in late October 1975.

The above characteristics used to separate Cal-
linectes and Portunus megalopae were confirmed
by specimens reared to the juvenile stage. Por-
tunus juveniles were too small ( <10 mm carapace
width) for specific identification. One Callinectes
megalopa developed to a juvenile stage tentatively
identified as C sapidus.

Distribution

Callinectes larvae were collected on six of eight
cruises and were most abundant in late summer
(Figure 3).

Mean abundance in neuston collections (n = 8)
at a single station reached 3,100/100 m^ at L2 in
August 1977; at this station abundance in a single
neuston collection reached a peak of 16,000/100
m^. Abundance generally decreased offshore of the
50 m isobath during the summer-fall cruises (sta-
tion Jl in August 1977 was an exception). During
the second year, with additional stations, larvae
were generally more abundant at stations on the
most southern transect than at more northerly
stations. Peak abundance often coincided with de-
pressed LSI's inshore, evidence that reproductive
activity inshore closely preceded the sampling
periods. Except during the summer, larval popula-
tions consisted almost exclusively of late zoeae
and megalopae, particularly in central and outer
shelf waters. Collections of Callinectes during the
fall of 1975 and winter and spring of 1977 com-
prised only megalopae.

Mean and maximum abundance (Figure 3;
Table 3) was greater in neuston than in bongo
collections except at three stations during summer
1977 (Figure 3). During winter 1977, occurrences
were too few to be tested at the 0.05 confidence
level by the signed rank test. On all other cruises
during which Callinectes larvae occurred, abun-
dance was significantly greater in surface than
subsurface collections (Table 3).

Diel patterns in neuston abundance of Cal-
linectes were not consistent over all cruises (Fig-
ure 4). A dawn peak in abundance was evident in
summer 1976. Dusk peaks appeared in fall 1975
and possibly spring 1977. Total abundance was
greatest during darkness (between sunset and

Table 3. — Comparison of surface and subsurface (neuston vs. bongo) abundance of Callinectes larvae, based on the signed rank test
(Wilcoxon 1945). N denotes greater abundance in neuston, significance level indicated by asterisks (* = 0.05, ** = 0.01); P is the
probability of a rank sum equal or greater under the null hypothesis of equal surface and subsurface abundance; fraction in
parentheses: numerator is the number of occurrences in particular abundance category and denominator is the number of possible
occurrences in abundance category.

Season and

year

of collection

Comparison

Fain 975

Summer 1976

Fall 1976

Winter 1977

Spring 1977

Summer 1977

Maximum neuston vs.

N-P = 0.016

N-P = 0.016

N"P = 0.004

N P = 0.062

N-P = 0.016

N"P = 0.008

maximum bongo

(6/6)

(6/6)

(8/12)

(4/12)

(6/12)

(12/12)

Maximum consecutive

pair of neuston

tows vs.

N-P = 0.016

N'P = 0.016

N"P = 0.008

NP = 0.125

N-P =0.016

N"P= 0.004

bongos, mean

(6/6)

(6/6)

(7/9)

(3/9)

(6/9)

(9/9)

'-euston vs.

N-P = 0.016

N-P =0.016

N" P = 0.008

NP = 0.125

N-P = 0.016

N"P = 00.10

bongos, mean

(6/6)

(6/6)

(7/9)

(3/9)

(6/9)

(9/9)

255

FISHERY BULLETIN: VOL. 78, NO. 2

3 0

2 0-

I 0

30 5

17 A

23-30 OCT 1975

33 6

32 3

32 8

163

16 9

32 8

166

34 7
20 2

I 00
80
60
40
20

* LSI

30.2 Solinily (%.)
19.2 Temperolure(°C)
r-; MAXIMUM ABUNDANCE

•MEAN ABUNDANCE

i

Dl N3 E3 F2

Jl

+
X

o
o

_i

E
O

o
q:

UJ
Q.

</)

q:

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CD

3

5 -28

NOV 1976

2 0-1

1 0-

33 6

10 4

1 1

34 8
124

__iJ

2 0-1

B5

A2

32 4

9 4

34 3 34 I
108 10 3

34 2

110

35.7

14,5

—I 1 ' !■'■ — r-

01 N3 E3 F2

34 4

12 I

("pi

I 00

80

60

.40

.20

I 00

80

,60

.40

■ .20

2.0-1

0-

20

10-

20 FEB - 6 MAR 1977

34,6
6 2

34 9
90

— I —
85

A2

»

*

35 4

35 5

11.4

11 5

,-,

32 7

33 6 34 2 35 4

2 6

1

26 43 97 : ',

1 1 1 M

H 1

• .80

• 60

- .40

■ .20

■I 00

- 80

- 60

- 40

- 20

Jl

Dl N3 E3 F2

J 1

3 On

2 0

I 0

33 2

154

33 9

126

34.8
139

L2 L4

STATION
FALL

34 9
140

i] 'q. ik

L6

p 100
- 80
60
40
,20

2 0-

I 0-

-100

*

»*

- 80

^,60

34 0

34 6

35 7

II 6

35,7
11,8

^- 40
- 20

2 5

4 6

H

',-ff^

' T"

LI

t
L2

L4
STATION
Wl NTER

L6

Figure 3. — Abundance and larval stage indices (LSI) of Callinectes larvae in surface and subsurface collections in

256

SMYTH: CALLINECTES LARVAE IN MIDDLE ATLANTIC BIGHT

20-1

10-

18-

28

MAY 1977

»

33.7

14.7

33.2

15.6

-|

B5

A2

2 0-

10-

32 3

16 0

33.6

174

33.3 33.5 n
171 18.0 U

35 6

19 0

338
17 6

n-

CI

T r— I 1—

Dl N3 E3 F2

Jl

20n

lo-

ss.8
184

32 9 33.3

150 148

35.8

17.6

-4

LI L2

L4 L6

STATION
SPRING

I 00
80
60
.40
.20

I 00

.80

60

40

20

r- I 00

- 80

- 60

- 40

- 20

9 SEPT 1976

31 6
20 6

32 I
21 4

30-1

20

I 0-

32 3
22 3

»*

33 8

216
■» ■»

34 I

« *
21 5

1

34 0
21 8

CI Dl N3 E3 F2 Jl

19-29 AUG 1977

318 33 5

227 23 5

20-1

I 0-

40-

3 0-

2 0

I 0-

Cl

32 0
22 6

Dl N3 E3
31 6
25 0

F2

Jl

349
254

34 6
25 7

LI L2

L4 L6

STATION
SUMMER

the Middle Atlantic Bight, 1975-77. Stations are ordered by increasing depth on a logarithmic scale within each graph.

I 00
80
60
40
20

B5

a2

32 5

32.0

23 7

21,5

* *^ * * *

:**

20-,

' ■•

32 6* *

: ;

; ;

24 3

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p

327 32 2

K

r-

24 1 23.732 2

■ ; ; : 231

10-

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m

i

00

80

60

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_l

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60
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257

FISHERY BULLETIN; VOL. 78, NO. 2

4 0

3.0-

2 0

23-30 OCT 1975

T — r*-i — I — \ — ! — I — I — H — I — r

1-9 SEPT 1976

r 50

40

- 30

20

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C 3.0

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5-28 NOV 1976

fL

~\ 1^ I I I I I I i 1 r

18- 28 MAY 1977

RANK SUM AT TIME INTERVAL
ABUNDANCE AT TIME INTERVAL

20 FEB - 6 MAR 1977

19-29 AUG 1977

- 30

20

13
V)

<

cc

T I — I — I — I — I — I — I — I — T" — r — r

ooooooooooooo
ooooooooooooo

(\J'tiDooOoj^t\l'J"(X)aDO(\|
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r 50

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T — I r^T 1 1 1 1 T 1 — r

ooooooooooooo
ooooooooooooo

OJ^tDCDOOJ'J-CVI'J'lOCDOCM
___ — CJf^c^OOOO — —

TIME OF DAY (EST)

Figure 4. — Die! changes in abundance ofCallinectes Icirvae in neuston collections in the Middle Atlantic Bight, 1975-77. Abundance
(dashed line) for each time interval was averaged over the stations of a cruise. The rank sum for each cruise (solid line) was calculated
by summing over all stations the ranks (lowest to highest) of the abundances at each time interval. (The rank sum weights the
frequency of occurrence at each time interval.)

sunrise) on all cruises except fall 1976, when
abundance was greatest during daylight hours.

258

The rank sum, which weights both abundance and
frequency of occurrence, indicated patterns of

SMYTH: CALUNECTES LARVAE IN MIDDLE ATLANTIC BIGHT

diel change similar to diel patterns of total
abundance — except during fall 1976. As distance
from shore increased and abundance decreased,
however, Callinectes larvae (late zoeae and
megalopae) were generally collected at the surface
only at night. Ten of 15, and 10 of 12 occurrences
(megalopae) during winter and spring 1977 were
at night.

Larvae were taken at salinities ranging from
30.5 to 35.8%o and temperatures from 1 1 .0° to 25.7°
C (surface temperature and salinity); peak abun-
dance occurred in the ranges 31.6-34.9%o and
20.6°-25.7° C. Mean temperature, salinity, and
distance from shore, weighted for abundance, for
all neuston collections of Callinectes larvae were
22.9° C, 31.9%o, and 55.9 km. Plots of temperature
and salinity vs. abundance indicated no clear rela-
tionships among these variables.

For the independent variables — temperature,
salinity, distance from shore, and depth — simple
(bivariate) correlation analysis indicated
strongest correlation between mean neuston
abundance per station and salinity and weakest
correlation of abundance with bottom depth
(Table 4).

Table 4. — Simple correlation matrix for surface abundance of
Callinectes larvae and selected environmental variables.

Table 5. — Partial correlation coefficients for surface abundance
log,(,[X-i-l]) oi Callinectes larvae with selected environmental
variables.

Variable

Abundance
(log,o[X+1])

Temperature
(°C)

Salinity

Distance

from shore

(km)

Temperature

Salinity

Distance

from shore
Bottom depth

0.6260—
-0.7086—

-0.5812"-
-0.4024"

-0.5133"

-0.1695
-0.1218

0.6259"-

0.5621"

0.6261 —

-•p< o.oi,---p<o.ooi.

When considered together, the variables form a
multivariate population. Partial correlation
analysis (Table 5) indicated a very weak relation-
ship between bottom depth and larval abundance
for all second and third, and most first order corre-
lations. Depth was, therefore, deleted from further
analysis. Second order correlations among tem-
perature, salinity, and distance from shore re-
vealed strongest correlation of abundance with
temperature, followed by distance from shore and
salinity.

Based on partial correlation analysis, indepen-
dent variables were entered into a multiple
regression equation in the order temperature,
distance from shore, salinity, and depth. These
variables explained 66.09^^ of the variation in
abundance (Table 6), the maximum possible for

Temperature

Salinity

Distance from shore

Bottom depth

(°C)

(%•)

(km)

(m)

First order correlations:

c'

-0.5787

-0.6182

-0.4214

04331

c

-0.2502

-0.0069

0.6577

-0.5434

c

-0.0606

0.6350

-0.6372

-0.4613

C

Second order correlations:

c

C

-0.3969

-0.1240

c

-0.3051

c

-0.0627

c

-0.4514

-0.5017

c

0.5194

C

c

0.1135

0.4472

c

-0.2732

c

0.6578

-0.5493

c

c

Third order correlations:

c

c

0

0.0378

c

c

-0.3815

c

c

-0.3013

c

c

0.5112

c

c

c

'c indicates variable which is controlled (effects removed).

any linear combination of these variables. Depth
contributed negligibly to explained variance, and
salinity very little (Table 6). The regression equa-
tion containing only the variables temperature
and distance from shore, explaining 62.4% of the
variation in abundance, is

A = 0.1393 + 0.1124r - 0.0115Z)

where A = abundance (logio[Z + 1]),

T = temperature in degrees Celsius,
D = distance from shore in kilometers.

The regression of abundance on temperature and
distance from shore was highly significant (Table
7).

The temperature-distance from shore-
abundance relationship for all cruises is sum-
marized in Figure 5. Summer collections formed a
unique group, distributed across the shelf. Abun-
dance appeared relatively uniform at least to a
distance of 100 km from shore, with a slight in-
crease at the outermost stations. Temperature did
not appear to be a limiting factor for these summer
collections. Relationships are less clear for other
seasons. Fall collections generally decreased in
abundance with decreasing temperature and in-
creasing distance from shore. Winter and spring
collections formed groups which were limited to
the outer shelf.

Cooccurring Decapods

Collections made during periods of peak abun-
dance of Callinectes (in the summer) included

259

FISHERY BULLETIN: VOL. 78, NO. 2

Table 6. — Variation explained by multiple regression of surface abundance (logml^ + 1]) of Callinectes larvae on temperature,
distance from shore, salinity, and depth as estimated by the coefficient of determination (r^). Data were entered in the order indicated
in the Statistical Package for the Social Sciences (Nie et al. 1975) stepwise multiple regression procedure.

Temperature

distance from shore, salinity, depth

Salinity, temperature

distance from shore

depth

Variable

r'

A/-2

Variable

f2

■i/-2

Temperature ("C)
Distance from shore (km)
Salinity (%..)
Bottom depth (m)

03919
0.6243
0.6592
0.6597

0.3919
0.2324
0.0350
0.0005

Salinity
Temperature
Distance from shore
Bottom depth

0.5021
0 5955
06592
0.6597

0.5021
0.0934
0.0637
0.00049

Table 7. — ANOVA table for regression of surface abundance
(logiQ[X + l]) o{ Callinectes larvae on temperature and distance
from shore.

Source of
variation

Degrees of
freedom

Sum of
squares

IVIean
square

Total

Regression

Residual

41 3723161 0908088
2 23.24224 11.62112
39 13.98937

32.39773"

— P'sOOOI.

peak abundances of inshore and estuarine genera
such as Uca (zoeae and megalopae), Emerita
(zoeae), Palaemonetes (zoeae), Upogebia (zoeae),
Libinia (zoeae and megalopae), and Ovalipes
(zoeae and megalopae). Few of the above were
found beyond the inner shelf (Figure 1: CI, Dl,
LI). At offshore stations Callinectes larvae fre-
quently occurred with larvae of shelf forms such as
Cancer, which dominated neuston collections
made in the spring. Megalopae and a few zoeae of
Portunus usually occurred with Callinectes.
Megalopae of Ocypode quadrata were ubiquitous
across the shelf during summer 1977. Megalopae
of Dromidia antillensis and other forms of south-
ern origin often occurred at central and outer shelf
stations.

DISCUSSION

Temperature-salinity tolerances of Callinectes
larvae are available from several laboratory and
field studies. Optimum temperature-salinity
ranges, experimentally determined, for survival
during zoeal development of laboratory-reared C
sapidus were 21-28%o, 19°-29° C (Sandoz and Rog-
ers 1944) and 20-32%o at 25° C (Costlow and
Bookhout 1959). Sandifer (1972) collected C.
sapidus zoeae in Chesapeake Bay in the range
15.7-32.3%o (most at 20-30%o) and 14°-27.9° C (75%
at 25°-26° C). Nichols and Keney (1963) found lar-
vae (zoeae and megalopae) to be most abundant
offshore (Florida-North Carolina) at 27.3°-29.1° C
and least abundant at 14.3°- 16.4° C.

Costlow (1967) reported survival of megalopae
to first crab in temperature-salinity combinations

of 15°-30° C, 5-40%o. Survival was similar at 20°,
25°, and 30° C, 10-40%o (75% survival) and oc-
curred at salinities as low as 5%o at 25°-30° C.
Survival in the lower salinity ranges (5-10%o) in-
creased with increasing temperature to 95% at 30°
C, 10%o. Survival in the upper salinity ranges
(30-35%o) decreased from 95-100% at 25° C to
42-50% at 15° C. At 15° C larvae did not survive
below 20%o, and at 15° C survival was highest at
35%o(50%).

Costlow and Bookhout (1959) found zoeal de-
velopment to require 31-49 days, with no sig-
nificant difference in larval duration at salinities
from 20.1 to 31.1%o (at 25° C). Duration of the
megalopal stage ranged from 5-11 days at 30° C
(5-40%o) to 30-67 days at 15° C (20-40%o) (Costlow
1967). Costlow ( 1967) reported significant interac-
tion between temperature and salinity only at 15°
C. Larval duration at 35%o, 15° C was 37-56 days.
Costlow ( 1967) did not rear larvae at temperatures
<15° C and did not include a regression equation
for extrapolation to lower temperatures.

Based on experimentally determined tolerances
noted above, summer temperatures in the es-
tuaries and inshore waters along most of the mid-
dle Atlantic and southeastern U.S. coast are
sufficiently warm for completion of larval de-
velopment. Metamorphosis of megalopae may
occur during the warmer months at salinities
found from offshore to upper estuaries. Greatest
survival, however, is at higher salinities (30-
40%o), and at 15° C occurs only in the range of
oceanic salinities. Furthermore, at these oceanic
salinities the duration of the megalopal stage in-
creases as temperature decreases. Thus,
megalopal life may be extended in the cooler,
offshore water of the Middle Atlantic Bight, a con-
clusion supported by the presence of Callinectes
megalopae at outer shelf stations (11°-12° C, 35-
36%o).

Results of multivariate analysis of data were
predictable (Figure 5; Tables 5-7). The importance
of temperature (positive correlation) reflected the
seasonal nature of spawning and development (in

260

SMYTH: CALLINECTES LARVAE IN MIDDLE ATLANTIC BIGHT

a: o uj

^ z q: S
< - 0. =)

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261

FISHERY BULLETIN: VOL. 78, NO. 2

summer). The secondary importance of distance
from shore (negative correlation) was reflected in
decreasing abundances with increasing distance
from shore. Because all collections were made well
within the range of optimum salinities for de-
velopment, salinity could have been expected to
contribute little to explained variation in abun-
dance.

Results of multivariate analysis of data em-
phasize that a bivariate approach to multivariate
data can be misleading. Salinity had the highest
simple correlation (-0.7086; Table 4) with abun-
dance. Consequently, in the usual SPSS stepwise
multiple regression procedure (Nie et al. 1975)
salinity would be entered as the first variable in
the analysis. The proportion of variation (r^, Ir'^)
in abundance explained by temperature, distance
from shore, salinity, and depth was quite in con-
trast to proportions of explained variance when
salinity, rather than temperature, was entered
first in the multiple regression equation (Table 6).

The relative importance of temperature, dis-
tance from shore, and salinity was best illustrated
by partial correlation coefficients (Table 5). This
procedure examines correlation between two vari-
ables when the effect of other variables is con-
trolled. I recommend partial correlation as a pre-
liminary step to multiple regression procedures
and as more appropriate than bivariate proce-
dures.

This paper reports for the first time the exis-
tence of a large population ofCallinectes larvae in
offshore shelf waters of the Middle Atlantic Bight.
The presence of an offshore population, necessary
to the accepted model of larval distribution, has
had relatively little documentation. Nichols and
Keney (1963 ) found advanced stages of Callinectes
as far as 64-97 km offshore, with greatest abun-
dance at stations 32 km offshore. Dudley and Judy

( 197 1) reported zoeae, chiefly stage III and earlier,
and a few megalopae at stations 10-13 km
offshore. Tagatz (1968) reported a few megalopae
as far upstream as 40 km in the St. Johns River,
Fla., and Williams (1971) collected megalopae". . .
almost the entire length of the [North Carolina)
estuary."

Abundance reported here (Figure 3) is some-
what less than that previously reported. Sandifer

(1972) and Tagatz (1968) reported maximum lar-
val abundance of 42,000 and 46,100/100 m^, re-
spectively, and Dudley and Judy (1971) reported
maximum abundance of 105,000 100 m^. These
data, however, included few megalopae. Williams

(1971) found considerably greater numbers of
megalopae than did pi evious workers but reported
abundance as numbers per sample (10's-l,000's).

My results confirm the reported affinity of Cal-
linectes larvae, particularly megalopae, for sur-
face layers. Previously Sandifer (1972) reported
that 89.4% of the Callinectes larvae that he col-
lected were from surface samples but reported
only three occurrences of megalopae, all in bottom
samples. Dudley and Judy (1971) found, overall,
more Callinectes larvae in surface (1.0 m) than in
subsurface (8.0 m) collections except at offshore
(10-13 km) stations. They collected advanced
zoeae (their last three stages) only at offshore sta-
tions. Tagatz (1968) collected more zoeae at the
surface than at the bottom, and Williams (1971)
reported Callinectes megalopae to be active at
night in surface waters. The results of these
studies, however, reflect differences in gear types,
mesh sizes, and sampling design; gear specifically
designed to sample surface layers was in no case
employed.

Reasons for the affinity of Callinectes and other
megalopae for the neuston are not readily appar-
ent. Diel increases in abundance in night collec-
tions of neuston may indicate a negative photo-
tropic response or possibly net avoidance in the
daytime. Numerous holoplankters (copepods, etc.)
exhibit the same diel pattern, and the upward
movement of megalopae may be related to feeding
strategies. It is not surprising that of the
megalopae collected in this study, the Portunidae
(swimming crabs) showed the strongest affinity
for the neuston. Megalopae of other crabs, how-
ever, such as Cancer, Ocypode, and Dromidia also
showed strong surface affinities.

Spatial distribution of plankton in shelf waters
is largely determined by circulation patterns.
With cross-shelf flow in the Middle Atlantic Bight
offshore at the surface and onshore at depth
(Bumpus 1973), coastal organisms in the surface
layers would be transported offshore, with the pos-
sibility of return at depth. A coastal boundary
layer, a band of trapped nearshore flow some 10
km wide, has been reported off New Jersey
(Csanady 1976). Coastal boundary layers are as-
sociated with the upwelling of cold water as a
consequence of the offshore movement of surface
waters and subsequent thermocline tilt (Csanady
1976). Most coastal and estuarine larvae in my
collections (species of Uca , Palaemonetes , Libinia,
etc.) were infrequent seaward of station CI and
are evidently retained within this zone. Late stage

262

SMYTH: CALLINECTES LARVAE IN MIDDLE ATLANTIC BIGHT

Callinectes larvae were most abundant outside the
coastal boundary layer in my collections as well as
in those of Nichols and Keney (1963). Callinectes
juveniles or adults were not collected during this
study in extensive benthic sampling (otter and
small biological trawls, dredge and grab
samplers), and small adults were collected only
once in plankton samples (C. similis, n = 5, sta-
tion CI, neuston, October 1975). Thus, this study
presents no evidence for recruitment to inshore
and estuarine populations, either by juveniles or
megalopae; the evidence, however, does not pre-
clude recruitment from the offshore larval popu-
lation.

General longshore drift in the Middle Atlantic
Bight is south westward (Iselin 1955; Harrison et
al. 1967; Bumpus 1973; and others) and may occur
as sporadic events rather than in a continuous
sweep (Ruzecki et al. 1976). Reversals of the
longshore flow, usually confined to a narrow belt
close inshore, may occur from April to September
(Bumpus 1969, 1973). A general constraint, how-
ever, seems to be placed on larval origins, viz.
adult populations are more likely to be re-
plenished by recruitment from larval populations
spawned to the north. Given a mean longshore
drift of 5 crrLS (Bumpus 1973) and a megalopal
duration of 5-67 days (Costlow 1967), a megalopa
has a range of 22-290 km; at inshore tem-
perature-salinity ranges (20--25° C, 30-35%o) a
megalopa might be transported 26-56 km.

Callinectes megalopae collected on the outer
shelf in the winter and spring, as well as some
megalopae found there in the summer and fall,
probably have southern origins. Water masses of
Gulf Stream origin, as meanders and warm-core
eddies, have frequently been observed in the
slope-outer shelf regions (Saunders 1971; see
Wright 1976 for a review). Although large-scale,
long-range transport is not evident, the presence
of Callinectes and Portunus megalopae at station
Jl in the winter indicates either transport from
the south or, less plausibly, delayed metamor-
phosis of megalopae from Middle Atlantic Bight
populations as a result of low winter tempera-
tures. Based on Costlow's (1967) response sur-
faces, a megalopa in Gulf Stream waters would
have a duration of 7-26 days and a range, at 2 kn,
of 600-2,300 km. Thus, some megalopae in the
Middle Atlantic Bight may originate from late
spawning populations to the south. Metamorpho-
sis would be further delayed by depressed temper-
atures of shelf and slope waters. The presence of

definite southern larval forms ie.g.,Dromidia) in
outer shelf collections supports the hypothesis
that at least some of the Callinectes and other
megalopae were produced by southern crab popu-
lations.

The developmental model of Callinectes, i.e.,
larval development in shelf waters and sub-
sequent recruitment to inshore and estuarine
adult populations, reflects the evolutionary his-
tory of the group. Portunids are "reproductively
conservative," migrating to waters of oceanic, or
near oceanic, salinities to release larvae (Norse
1977). Williams (1974) described Callinectes as "a
portunid group evolving at the geographic limits
of the family, specializing in occupation of es-
tuaries, . . . ." In this light, the migratory se-
quence of larval stages is a response to the prob-
lems of an essentially marine group invading the
estuaries. Spawning areas (marine) may repre-
sent a primitive condition, and the spatial se-
quence of stages returns larvae to habitats in
which the adults are successful. It is, as Williams
(1974) described it, a "homeostatic developmental
feature in the life histories of the species" that has
not been carried to an evolutionary conclusion,
that is, retention within the estuary for the entire
life history.

It can be argued that such a model of develop-
ment may in part account for the success and
widespread distribution o{ Callinectes. If, as Norse
(1977) and others have indicated, recruitment oc-
curs through metamorphosis of megalopae rather
than immigration of adults, then such a sequence
would allow dispersal into numerous estuaries yet
assure genetic continuity over broad areas. Such a
role has been suggested by Cole and Morgan
(1978). Furthermore, it would seem more likely
that this is a primitive mechanism retained,
rather than developed, through selection pres-
sures.

The essential features of Callinectes develop-
ment appear to be spawning and hatching in or
near the primitive habitat (along the shore) dur-
ing most of the warmer months, maintenance of a
large larval population in the shelf waters (chiefly
in the surface layers), recruitment from the larval
pool, and exploitation of the estuarine habitat as
adults.

There is, however, a paradox in the biogeog-
raphy of Callinectes and the spatial sequence of
developmental stages. Given the southern
affinities of the genus and general southerly
longshore movement of waters along most of the

263

FISHERY BULLETIN: VOL. 78, NO. 2

U.S. Atlantic shelf, the distribution of CaUinectes
is counter to the direction of immediate larval
transport. Recruitment to adult populations at the
northern limits of CaUinectes is problematical.
Not all larvae can originate from parental stocks
to the north. This may indicate that recruitment
takes place from megalopal populations closer in-
shore than those reported in this study and by
Nichols and Keney (1963), with the coastal boun-
dary layer possibly retaining larvae. The
megalopae collected farther offshore may repre-
sent larval wastage to parental populations (but
not necessarily to the species).

ACKNOWLEDGMENTS

I wish to thank John Olney, Steve Berkowitz,
Cathy Womack, Mike Vecchione, and Roberta
Wallace for assistance in making collections.
Shelia Berry, Pat Crewe, Roberta Wallace, and
JoEllen Sanderson capably sorted the samples. I
thank Jacques van Montfrans, W. A. Van Engel,
George Grant, Morris Roberts, and two anony-
mous reviewers for their critical review of the
manuscript and helpful comments and sugges-
tions. I also thank Shirley Sterling and Ruth Ed-
wards for typing the various drafts. Mary Jo
Shackelford and June Hoagman prepared the final
figures. Final copy of this manuscript was pre-
pared by the VIMS Report Center. This research
was supported in part by contract no. 08550-CT5-
42 and AA550-CT6-62 from the Bureau of Land
Management, U.S. Department of Interior.

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265

AN ANALYSIS OF THE UNITED STATES DEMAND FOR FISH MEAL

D. D. HUPPERT^

ABSTRACT

As fishery management plans are developed under the Fishery Conservation and Management Act of
1976, economic evaluation of management procedures will be necessary. To adequately address the
economics of optimum yield, for instance, research will be required in the traditional economic
subjects of demand, production and costs, industrial organization, and international trade. This paper
addresses the domestic demand for the primary industrial fishery product — fish meal. In developing
the demand model the important points are: 1) choice of empirical variables for inclusion in the
model, 2) determination of appropriate functional form of the demand equation, 3) treatment of the
"simultaneity bias" problem, and 4) choice between a static (or equilibrium) model and a dynamic
model. The paper presents maximum likelihood estimates of both the static and dynamic models.
With either model the price elasticity of demand is high when fish meal price is low, and is low when
price is high.

Analysis of prices and market demand relation-
ships for fish is of increased importance since the
enactment of the U.S. Fishery Conservation and
Management Act of 1976 (FCMA^). The new law
not only establishes a zone of Federal control over
fisheries from 3 to 200 mi offshore, but it also
establishes national standards for fishery man-
agement plans which include economic and social
aspects. A key concept is that of "optimum
yield" — that rate of annual catch "which will
provide the greatest overall benefit to the Nation"
(FCMA, Sec. 3(18)). Economic benefits to the na-
tion accrue primarily through the consumption of
fishery products which are sold in more-or-less
free and competitive markets. Market prices can
be expected to vary in response to changes in the
annual yields permitted under fishery manage-
ment plans. These price impacts, along with
associated changes in real income, cannot be
neglected in the development of appropriate man-
agement methods. The demand analysis present-
ed in this paper will assist in the determination
of optimum yield for fisheries which contribute to
the U.S. fish meal supply.

Fish meal is a primary product of the Atlantic
and Gulf of Mexico menhaden fisheries and the
California anchovy fishery. It also appears as a
byproduct of groundfish and tuna processing. It

is used as a high protein supplement most com-
monly mixed with corn, soybean, or cottonseed
meal; meat byproduct meal; and vitamins and
minerals for feeding to broilers, layers, and tur-
keys. According to J. Vondruska,^ fish meal is
also used in feeds for mink and other fur-bearing
animals, farmed fish, laboratory animals, live-
stock, and household pets. About 80% offish meal
consumed in the United States goes into poultry
feed. A high level of metabolizable energy and
such nutritional elements as riboflavin, panto-
thenic acid, niacin, choline, and several amino
acids are contributed to animal feed by the addi-
tion of fish meal (Karrick 1963). Most of these
constituents are available in high protein vege-
table meals, but fish has a particularly high con-
centration of the amino acids lysine and
methionine.

Because the lysine and methionine are neces-
sary for fast growth in chicks, feed mixers gener-
ally seek to include between 2 and 8% fish meal in
broiler rations. With >8% fish meal, the poultry
tends to pick up a "fishy" flavor. With <2% fish
meal, further substitution of vegetable protein
meals for fish meal will result in slower growth
because the fixed quantity of feed eaten per day
per chick cannot contain the ideal mix of amino
acids. When fish meal is extremely high priced or

'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, La Jolla, CA 92038.

^Public Law 94-265, 94th Congress, 2d Session 13 April
1976, 16 use 1801 et seq. (Suppl. 1977). Hereafter, FCMA.

Manuscript accepted November 1979.
FISHERY BULLETIN: VOL. 78, NO. 2, 1980.

3J. Vondruska. 1979. Postwar production, consumption,
and prices of fish meal. Unpubl. manuscr., 66 p. National
Marine Fisheries Service, 3300 Whitehaven St., N.W.,
Washington, DC 20235.

267

unavailable, the lysine and methionine content of
the feed can be augmented with synthetic pro-
teins. Kolhonen (1974) described the develop-
ment of synthetic methionine and lysine for use
in feed formulas.

Linear programming has been widely adopted
by formula feed manufacturers in the United
States and western Europe (Kolhonen 1974).
Least-cost combinations of feed constituents
needed for adequate nutrition are quickly and ac-
curately computed for any vector of constituent
prices. Thus, the demand for feed ingredients is
expected to exhibit great sensitivity to relative
prices. In a recent examination of demand for ag-
ricultural feed ingredients, Meilke (1974) re-
ported that price elasticities are generally >2 in
absolute value. It is expected that the demand for
fish meal will be elastic also, at least when avail-
able quantities allow the feed formula manufac-
turers to include between 2 and 8% fish meal in
poultry rations. When the supply of fish meal is
low enough to jeopardize the maintenance of at
least 2% fish meal, the demand may become in-
elastic. Thus, one hypothesis to be tested is that
the own price elasticity of demand for fish meal
falls with increasing price and decreasing quan-
tity.

Markets for fish meal in the United States are,
for obvious reasons, concentrated in the poultry-
producing regions — California, Arkansas, and
states in the Deep South. Domestic production of
fish meal occurs mainly in California, the Gulf
Coast States, and the South Atlantic States. In
some years, however, much of the domestic sup-
ply is imported from major foreign producers such
as Peru. Foreign meal is a perfect substitute for
the domestic product, but the supply of foreign
meal has undergone tremendous fluctuations due
to variations in fish stocks (especially the Peru-
vian anchoveta, Engraulis ringens). Domestic
supplies have also been strongly influenced by
uncontrolled variations in domestic stocks (espe-
cially menhaden Brevoortia tyannus and B. pat-
ronus) and by administrative decisions of fishery
management agencies (California's anchovy, £;/i-
graulis mordax, fishery, e.g., see Pacific Fishery
Management Council 1978: 31660-31664). On the
supply side of the domestic market, therefore, the
major fluctuations are not price induced, but are
due to exogeneous factors. On the demand side
the poultry industry experienced a steady expan-
sion starting in the early 1950's and continuing
until about 1970.

FISHERY BULLETIN: VOL. 78, NO. 2

DEVELOPMENT OF DEMAND MODEL

Demand and price analysis has been a cor-
nerstone of applied economic research since the
1930's (Working 1927; Schultz 1938; Wold and
Jureen 1953). Agricultural economists have been
particularly active in developing demand models
for commodities. Research on demand for fish
is of more recent vintage but differs in few im-
portant respects from that for agricultural com-
modities. For an excellent review of the historical
development of demand analysis, see Waugh and
Norton (1969). Among the methodological issues
addressed in applied demand studies are: 1) spec-
ification of the demand model, 2) development of
appropriate functional forms, 3) treatment of
simultaneity bias in market demand and supply
function estimates, and 4) incorporation of
dynamic response mechanisms in the demand
model. These issues are discussed seriatim.

Specification

The specification of a demand model consists of
the choice of dependent and independent vari-
ables. Annual quantity demanded, as measured
by quantity purchased, should be the dependent
variable. Purchased quantities are difficult to ob-
tain, however, while production, import, and ex-
port statistics are well documented. Also, meals
derived from different sources differ in protein
content and sell at different prices. Both the
quantities and the prices must be aggregated
such that they represent a reasonably homoge-
neous commodity. Fish meal quantities (Table 1,
columns 1-6) are converted to a protein equiva-
lent basis by multiplying the quantity of each
type of meal by the prevailing percentage of pro-
tein content. The total available domestic quan-
tity, computed by summation of protein equiva-
lent fish meals and subtraction of exports, is
listed in Table 1, column 7. Similarly, since the
prices of the various fish meal types (Table 2, col-
umns 1-4) are based on protein content, each
price is converted to a protein basis. The aggre-
gate price of fish meal introduced as an indepen-
dent variable in the demand model is the average
price per unit protein for all meal supplied to the
U.S. market (Table 2, column 5). Some specifica-
tion error may enter the model because domestic
supply rather than quantity purchased is used for
the dependent variable, but this problem is un-
avoidable with available information.

268

HUPPERT: ANALYSIS OF UNITED STATES DEMAND FOR FISH MEAL

Table l. — United States fish meal supplies, 1955-76 (thousands
of metric tons). (National Marine Fisheries Service 1975, 1977.)

(1)

(2)

(3)

(4)

(5)

(6)

(7)
Total
supply

Men-

An-

Im-

Ex-

protein

Year

haden

Tuna

chovy

Other'

ports

ports

basis^

Table 2. — Annual average prices for various fish meals and
average price per unit of protein in fish meal in the United
States. (National Marine Fisheries Service 1975.)

1955
1956
1957
1958
1959
1960
1961
1962
1963
1964
1965
1966
1967
1968
1969
1970
1971
1972
1973
1974
1975
1976

172.9
191 1

156.4
143.4
203 1
198 1
2246
217.5
167.1
145.4
159,7
122.5
108-1
129.9
144.7
171.1
200.4
175.6
171.3
185.0
1736
192.9

21.2
23.9

23.3
23.0
23.0
24.0
192
24 1
24.5
19.1
23.0
23.0
23.1
26.1
24.4
24.2
26.6
39.2
39.6
43.7
33.7
36.4

0.0

0.0

00

00

0.0

0.0

0.0

00

0.0

0.0

0.0

4.1

5.1

2-5

10.3

14.7

6.9

10.1

20.0

12.8

25.1

19.9

37.6
44.1
51.3
502
43.1
33 1
28 8
31 5
33.4
39.6
37.3
42.9
46.5
47.4
42 1
232
22,7
238
22.4
23.0
20 9
220

88.9

820

73.7

91.1

120.6

119.4

1976

2289

341.4

398.3

2455

406.2

591.0

775.9

325,1

227,8

256,9

355,6

62 1

62.0

107.4

127.4

na,-'

n.a.

n.a.

n.a.

n.a.

n.a.

n.a.

n.a.

n.a.

n.a.

n.a.

n.a.

n.a.

n.a.

n.a,
43
92
9.5

33.3

50.3

10.7

30.0

195.8
2075
185.3
188.0
238.8
2296
291.0
311.4
355.7
380.4
290.4
378.6
492.9
626.7
343.6
284.9
314.4
373.2
171.4
167.2
215.0
226.7

'Primarily from offal, waste, and scrap from groundfish and herring
^Converted to protein as follows: menhaden, exports, and other meal as-
sumed to be 60°o protein: anchovy and imports assumed to be 65% protein:
tuna meal assumed to be 55% protein. Total supply is production plus imports
minus exports,
^n.a, means data not available.

Year

1955
1956
1957
1958
1959
1960
1961
1962
1963
1964
1965
1966
1967
1968
1969
1970
1971
1972
1973
1974
1975
1976

(1)

Men-
haden

(2)

Tuna

(3)

(4)

Domestic Peruvian
anchovy anchovy

(5)

Average price

per unit protein

in fish meal

Actual' Deflated'

-dollars per metric ton of meal-

123.4
121.7
117.7
125.0
116.2
84.4
106.4
112.6
114.1
119.3
152.9
146.1
123,8
131,8
158,1
167.4
143.3
168.3
433.8
250.5
216.9
314.3

130.7
121.7
114.8
124.8
117,1
86,0
99,7
109.5
106.2
115.8
143.2
134.4
117.6
114.2
132.6
155.4
128.0
141.4
359.6
245.5
206.3
347.8

137.3

117.5
110.7
137.9
156.0
140.4
154.1
3655
270.3
214.8
247.5

121.5
128.2
131.9
86.1
100.0
111.2
109.7
119.7
140.3
141.9
118.1
118.8
142.5
176-4
150.7
162.6
409.8
260.6
226.5
309 9

1.99

1.97

1.95

201

1.95

1.39

1.69

1.81

1.76

1.88

2.30

2.23

1.86

1.88

2.31

272

2.33

259

675

4.15

3.54

4.92

4.34

4.16

4.01

4.19

3.94

2.80

3.40

364

3.58

3.81

4.63

4.33

3.57

3.53

424

4.72

3.92

4.15

9.70

499

388

5.15

' For each meal, price per unit protein equals price per ton divided by percent
protein. Average price computed by weighting the price per unit protein for each
meal by the proportion of U.S. fish meal protein supplied by that meal.

^Deflated by Wholesale Price Index, all commodities (January 1977 = 100).

In addition to the price offish meal, the demand
model should contain independent variables rep-
resenting 1) the prices of close substitute prod-
ucts, 2) prices of complementary products, and
3) the level of production activity that governs
the demand for fish meal. Several high protein
meals (e.g., soybean, cottonseed, meat, and bone
meals) are potential substitutes for fish meal in
poultry rations. Soybean meal is the most com-
mon substitute, and its price is used as an inde-
pendent variable in the demand model. The price
of corn meal (Table 3, column 2) is introduced as a
complementary product price. Demand for fish
meal is expected to increase when the price of a
substitute product increases, and is expected to
decrease when the price of a complementary prod-
uct increases. Finally, the overall production of
poultry products would cause shifts in the level of
demand for fish meal independently of the prices.
The poultry and egg production index (Table 3,
column 3) is adopted as the appropriate measure
of this factor.

In summary, the fish meal demand model is
specified as follows:

1) Quantity demanded, the independent vari-
able, is represented by annual production plus
net imports of protein-equivalent meal.

2) Annual price of fish meal is measured as the
weighted average of the prices per unit protein
for all domestically supplied meals.

Table 3. — Exogenous variables in the fish meal demand model.

Price of

Price of

Poultry and egg

domestic

domestic

production index^

Year

soybean meaP

corn^

(1976 = 100)

dollars per

metric ton

1955

51.6

2.24

58

1956

46.5

2.30

63

1957

42.7

2.06

64

1958

50.8

1.99

68

1959

51.3

1.94

70

1960

48.2

1.84

70

1961

57.3

1.80

75

1962

60.3

18C

75

1963

65.8

2.00

77

1964

62.8

1.99

80

1965

64.9

2.07

83

1966

76.0

2.18

88

1967

694

2.06

92

1968

70.3

1.80

90

1969

67.6

1.96

92

1970

71.8

2.19

97

1971

70.7

2.15

98

1972

95.2

2.10

100

1973

216.3

3.57

97

1974

127.8

5.20

97

1975

112.6

4.71

94

1976

147.5

4.37

100

'Forty-four percent protein. Simple
tional Marine Fisheries Service (1977)

2Price of No. 2 yellow corn, Chicago
PES-294, 1965-77.

3From Schultze et al. (1979).

average price at Decatur, III., from Na-
USDA, ERS, Poultry and Egg Situation,

269

FISHERY BULLETIN: VOL. 78, NO. 2

3) Annual domestic price of corn and annual
domestic price of soybean meal are introduced
as complementary and substitute product
prices.

4) The trend in aggregate demand over time is
accounted for by the aggregate poultry and
egg production in the United States.

All of the variables expressed in dollars are
deflated by the Wholesale Price Index to elimi-
nate spurious correlations caused by the inflation-
ary trend.

Functional Form

Demand studies typically utilize least squares
regression methodology with either a linear or a
log-linear equation. As noted by Chang (1977),
however, there is no a priori reason to choose one
of these forms. Each form imposes some fairly
strict conditions upon the characteristics of the
demand function which may contradict theoreti-
cal considerations or actual experience. Linear
equations imply that the elasticity of demand
with respect to any independent variable is a de-
creasing function of that variable; a log-linear
equation implies constant elasticities. Chang
suggests that the income elasticity of demand for
meat should fall with rising income. A similar
consideration applies to fish meal demand. At low
prices, feed manufacturers would use near
maximum amounts of fish meal allowable and
could easily substitute soybean meal for fish
meal. With relatively high fish meal prices, feed
manufacturers would use a smaller proportion of
fish meal, but as price rises further it would be
increasingly difficult to maintain desired quan-
tities of lysine and methionine by substitution of
soybean meal. Thus it is clearly unwarranted to
rule out increasing price elasticity through a
priori choice of functional form.

The function to be fitted by regression analysis
can be chosen by determining the appropriate
transformation of variables for the linear least
squares procedure. The log-linear transformation
is a special case of a parametric family of trans-
formations introduced by Box and Cox (1964).
The parameter defines the transformation

function is expressed as

r* =

= ix' - l)/\.

(1)

Equation (1) is linear for A = 1, and becomes
logarithmic as \ approaches zero. The demand

270

,* —

6o + ^1 •''^1* + . . . + bf^Xk* + u

(2)

where q is the quantity demanded, thex's are the
independent variables affecting demand, u, is a
stochastic error term, and the 6, and k are
parameters to be determined. The superscript *
indicates that the variable has been transformed
as in Equation (1).

Price elasticity of demand is defined as the ab-
solute value of the ratio of percentage change in
quantity demanded to percentage change in
price. Assuming that the first independent vari-

able is the price, E
tion (2) we get

dq

(t)

E = \bi\(q/x^:

From Equa-

ls)

The elasticity defined in Equation (3) is an in-
creasing function of x^ when A>0, and is a de-
creasing function of x^ when \<0. Thus the esti-
mate of the transformation parameter X provides
a test of whether the price elasticity increases,
decreases, or remains fixed along the demand
curve.

Simultaneity Bias

In economic theory, the supply and demand
curves interact to determine the market price.
Over a period of time, shifts in both supply and
demand factors cause the market price and ob-
served quantities of products to vary. Without
these shifts, only one price and quantity would be
observed, making it impossible to estimate a de-
mand or supply curve. When the demand curve
remains stable, the observed price-quantity pairs
"trace out" the demand curve with, of course,
some stochastic error, and a regression analysis
will result in a demand curve estimate. When the
supply curve remains stable, the observed data
will fall along the supply curve, and a regression
analysis of the price-quantity relationship results
in a supply curve estimate. If shifts in both de-
mand and supply occur, the resulting data will
not unambiguously identify either of these two
curves, and an ordinary least squares regression
will generally result in a set of parameters re-
flecting neither the supply curve nor the demand

HUPPERT: ANALYSIS OF UNITED STATES DEMAND FOR FISH MEAL

curve. In this case the estimated parameters are
said to suffer from simultaneity bias.

The general statistical problems associated
with estimation of individual structural relation-
ships in a simultaneous equation system were
first examined by Haavelmo (1943). Development
of appropriate statistical methods for estimating
simultaneous equation systems has been a major
area of research for econometricians over the last
two decades (Kmenta 1971). In estimating the
demand curve for fish meal, however, direct re-
gression estimates seem appropriate, because
most of the observed variations in annual fish
meal supplies are due to exogeneous shifts rather
than price-induced movements along a stable
supply curve. Production offish meal is subject to
wide fluctuations due to uncontrolled variations
in the fish stocks exploited (Kolhonen 1974). At
the same time, formula feed and poultry indus-
tries have remained relatively stable during the
last 20 yr except for the secular growth accounted
for in the analysis. Under conditions in which the
random shifts in supply are much greater than
the corresponding shifts in demand, the ordinary
least squares procedure results in no significant
simultaneity bias (Rao and Miller 1971).

effect of a price change may be drawn out over
several periods of time. A fairly simple model for
representing a lagged response is the "partial ad-
justment model" originally developed by Nerlove
(1958). Corresponding to any given level of the
independent variable, p, there is an optimal or
desired level of the dependent variable q. For a
demand function with one independent variable,
the level of demand fully adjusted to input prices
by formula manufacturers represents the desired
level offish meal usage:

qf=bp^ +u,

(4)

where the superscript d signifies desired level.

Because purchasers of meal cannot im-
mediately adjust to this desired level of usage, the
demand Equation (4) is not directly observable.
By assuming a simple structure to the adjust-
ment process, however, an estimable equation is
obtained. The partial model assumes that a fixed
percentage of the adjustment to desired level is
made each year. This introduces the difference
equation

Qt -9m = yiqf-qt.i)

(5)

Lagged Response Mechanisms

The use of annual price and quantity data for
estimating the demand function requires that the
response to a change in price occurs rather
rapidly, at least within a period of time much
shorter than a year. Since most domestic formula
feed manufacturers employ professional nutri-
tionists and cost-minimizing computer routines in
calculating formulas, the response to changes in
the vector of prices is probably rapid. If so, each
annual quantity consumed may be assumed to
represent at least approximately an equilibrium
demand response to the set of independent vari-
ables. The assumption of rapid response and
equilibrium approximation, however, has not
been directly verified. In the interests of rigor it is
useful, therefore, to consider alternative assump-
tions.

A lagged response to a change in price may
occur due to rigidities in mixing procedures or
personnel, inventory management problems, or
time lags in renegotiating contracts for supply of
input or sales of products. If any of these factors
results in a sluggish response in the substitution
between fish meal and other protein meals, the

Solving this for q^ and substituting from Equation
(4) yields

q=b yp, ^ (1 - y)(7,^i + yu,.

(6)

The adjustment parameter, y, must be a positive
number <1. Larger values of y imply more rapid
adjustment to changes in the independent vari-
able. The impact of a unit change in p, is distrib-
uted over time in an exponentially decaying fash-
ion with successive annual changes in q being
equal to by, by (1 - y), by [1 - y)^, and so forth.
The ultimate change in q due to a change in p is

Iq =blp lyil

y)J = blp

(7)

where j = lag. The elements in the sequence
under the summation sign are all positive frac-
tions, and sum to one, so that the sequence can be
treated like a probability distribution. Each ele-
ment represents the percentage of the total effect
occuring in year t, and the mean of the distribu-
tion, ( 1 - y)/y, represents the mean lag in the
adjustment process. Distributed lag models like
that in Equation (4) result from other conceptual
models such as models of expectations formation

271

or habit formation. And the exponentially distri-
buted lag is but one of a large class of more com-
plex lag models (Griliches 1967; Kmenta 1971;
Rao and Miller 1971).

Application of the partial adjustment model to
the demand Equation (2) results in the following:

4

Q*t = ^0 + ^a.x* + a,ql^ + u, (8)

where the coefficients a, can be interpreted in
terms of the coefficients of Equation (2) as follows:

at = yb,;i = 1,

. .4

a.

(1- y).

STATISTICAL PROCEDURES

For a given value of the transformation
parameter, k, the coefficients of either the
equilibrium model [Equation (2)] or the partial
Adjustment model [Equation (8)] can be esti-
mated by the ordinary least squares method. Two
statistical issues requiring further development,
however, are the selection of the "best" value for
A, and the test for significance of the lagged ad-
justment parameter. An appropriate procedure
for estimation of K was first suggested by Box and
Cox (1964). The procedure is more clearly
explained in the linear regression context by
Kmenta (1971) and is reviewed by Chang (1977).
For a fixed value of A, the linear regression proce-
dure yields an estimate of the error variance &^.
Box and Cox showed that the maximized log
likelihood is, except for a constant,

^max (^) = -(N/2) log d-2 (A) + (A - 1)S log 9,. (9)

A maximum likelihood estimate of A can, there-
fore, be found by searching through successive
values of A to maximize Equation (9). The use of
this likelihood function implies, of course, that the
error terms conform to full normal theory as-
sumptions, i.e., that the w, are independently
normally distributed with zero mean and con-
stant variance. An approximate 100% (1 - a)
confidence region for A is defined by

■^max *^^) ~ L

(A) < 1/2 x,Ha) (10)

where XiHa) represents the value of the chi-
square distribution with 1 df (Box and Cox 1964).

272

FISHERY BULLETIN: VOL. 78, NO. 2

Serial correlation in the errors of the regression
model raises problems in the interpretation of the
test statistics for the nonlagged variables and the
lagged adjustment parameter, and contradicts
the assumptions of the log likelihood function.
Careful examination of the hypotheses and
statistics regarding the residuals of the regres-
sion equation is clearly necessary. Existence of
serial correlation in the errors of the static de-
mand model can be tested with the Durbin-
Watson statistic. If no serial correlation is appar-
ent in the residuals, then neither the distributed
lag model nor the serial correlation model need be
considered. If serial correlation is present in the
residuals of the static model, then the problem is
to distinguish between the distributed lag model
and the serial correlation model.

Griliches (1967) showed that the serial correla-
tion and lagged adjustment models cannot be dis-
tinguished by a simple ^test on the adjustment
parameter. For example, if errors generated by a
first order Markov process, i.e., e^ = se,_i + Uj,
occur in a regression equation, the coefficients of
the lagged variables may be judged significant
by the usual ^-test even though there is no real
lagged response in the underlying structural
relationship. Similarly, it can be shown that se-
rially correlated residuals will occur if a non-
lagged model is mistakenly fit to data from an
inherently dynamic process.

Although there is no fully satisfactory method
for determining which model is the truth,
Griliches (1967) developed a provisional test.
Briefly, the serial correlation model is

9, =«o +}^^xu +^t

(11a)
(lib)

where s is a positive fraction and u, is a nonse-
rially correlated error term. From Equation
(lla),e,.i =Qt-i -o-Q- S,a,:<;,,.i;sothate^ = s(9m -
Uq - S(a,x„_i) + "r Substituting this into Equation
(11a) yields

% =<1 -s)ao + S(a^A:,, - 6,x,,.,)+ s g^ ^ + u,. (12)

When Equation ( 12) is computed, the serial corre-
lation model implies that a^s = -6, for each i.
Griliches suggested that the first-order serial cor-
relation model be rejected if these four equalities
do not appear to hold. Thus, there are four
h3^otheses of the following form:

HUPPERT: ANALYSIS OF UNITED STATES DEMAND FOR FISH MEAL

Ho:(6, +sa,) = 0. (13)

An approximate sample variance for ib, + sa^) is
computed by the "delta method" described by
Saber (1973). The expression for approximate
variance of a function of a vector of random vari-
ables, G(x), is

v[G(x)] = Zy(x,)(|^y

+ 221: COY (jc
i<J

Mm

dG
dx.

(14)

Assuming that the estimate of (6, + sa^) from the
regression equation is approximately normally
distributed, the following ratio will be approxi-
mately distributed as anF-statistic with 1 and (n
- r) df (where r is the number of regression
parameters estimated):

ib, +sa,)2/v[6, + sa,]^F(l,n-r).

(15)

Since the serial correlation model requires each
of the four hypotheses to hold, a definite rejection
of one or more of the hypotheses may be taken as
evidence against the serial correlation model and
in support of the partial adjustment model. Be-
cause of the lack of rigor in the suggested testing
procedure, however, caution must be exercised in
drawing conclusions.

RESULTS

Ordinary least squares estimates of the static
demand Equation (2) were computed for a range
of values for the transformation parameter A. The
regression coefficients and statistics of most in-
terest are listed in Table 4. A value of \ = -0.55
maximizes the log likelihood function, but the
95% confidence interval for A is 0.2 to -1.4. The
interval includes the logarithmic transformation
(A = 0), but not the linear transformation (A = 1).
The negative value of A, which implies a price
elasticity of demand that decreases as quantity
decreases, conforms to expectations. The signs of
all the coefficients are also consistent with prior
expectations; demand is diminished by increasing
price of fish meal or corn meal, and is increased
by increasing price of soybean meal and by ex-
panding poultry and egg production. Application
of ^-tests to the coefficients of the equation with A
= —0.55 indicates statistical significance with
99% confidence for the coefficients of fish meal
price and corn meal price, and with 90% confidence
for the coefficient of soybean meal price. The poul-
try and egg production index appears to be an
insignificant influence on fish meal demand by the
^-test. But this is insufficient reason for elimi-
nating a theoretically important variable from the
equation.

The squared multiple correlation coefficient, r^
= 0.73, indicates a reasonably "good fit" for a de-
mand equation estimate from time-series data.

Table 4. — Regressions for determining maximum log-likelihood of static demand function. P, = price
offish meal,Pj = price of soybean meal.P^ = price of com feed, Qp = poultry and egg production index.
Superscript * indicates Box-Cox transformation expressed in Equation (1).

Transformation

Coetficient

parameter

(M

Intercept

Pf

Pi

Pc

Op

fl2

D-W

/-max(A)

0.5

44 184

-10.144

9.588

-8.597

0.816

0.695

0.754

-91.21

20.2

12.499

-2.620

2.174

-2.532

0.545

0.714

0.716

-89.70

0.0

6 054

- 1 .064

0.812

-1 125

0.413

0.722

0.704

-88.97

-0.20

3.324

-0.432

0305

-0.501

0.311

0.727

0.705

-88.48

-0.50

1.731

-0.112

0.071

-0.150

0.199

0.730

0.725

-88.14

3-0.55

1 592

-0.089

0.056

-0.123

0 184

0.730

0.731

-88.13

(5.108)

(-2.602)

(1.864)

(-3.489)

(0.976)

-0.60

1.474

-0.071

0044

-0.100

0.171

0.730

0.735

-88.14

-0.70

1.282

-0.455

0027

-0.067

0.146

0.729

0.751

-88.18

-1.0

0 929

-0.012

0.007

-0.020

0.088

0.724

0.801

-88.56

-1.2

0.789

-0.005

0.003

-0.009

0.061

0.719

0.839

-89.02

2-1.4

0,687

-0.002

0,001

-0.004

0.042

0.711

0.879

-89.61

' D-W stands for Durbin-Watson statistic.

^Indicates approximate 90% confidence interval for a.

^Indicates maximum likeiitiood estimate (f-values in parenthesis).

273

FISHERY BULLETIN: VOL. 78, NO. 2

The Durbin-Watson statistic (0.731) is below the
lower critical value (d/ = 0.86 for 21 observations
and 4 parameter estimates), indicating sig-
nificant serial correlation in the errors of the de-
mand model. As suggested above, this serial cor-
relation may be caused by incorrect specification
of a static model when a dynamic adjustment
model would be more appropriate, or it may
reflect true serial correlation in the errors which
may in turn be due to some other source of mis-
specification.

Following the suggestion by Griliches (1967), a
regression equation with lagged dependent and
independent variables was computed (Table 5).
The F-statistics for the four hypotheses as-
sociated with the serial correlation model range
from 0.119 to 6.516. The critical value for each
hypothesis (withP<0.05 and for 1 and 11 df) is
4.84. Clearly, only one of the four hypotheses, the
one associated with the soybean price, can be re-
jected with great confidence. Even this may be
misleading, because the probability of wrongly
rejecting at least one of four hypotheses at the 5%
level is 0.183"*. Due to the provisional nature of
the test procedure and the inconclusiveness of the
result, it is useful to consider both the static and
distributed lag models as plausible representa-
tions.

The distributed lag model [Equation (8)] was
estimated by ordinary least squares for several
values of the transformation parameter A. Re-
gression coefficients and pertinent statistics for
the distributed lag model are listed in Table 6.
The log-likelihood function is greatest for k =

"The probability of type 1 error in a single test is 0.05. If four
tests are made the probability of making at least one type 1 error
is one minus the probability of making no type 1 errors, i.e., 1 -
(0.95)".

Table 5. — Estimates for demand function parameters with all
variables lagged.' Transformation parameter, A, equals -0.55;
and all symbols are as explained in Table 4. R^ = 0.855.

Variable

Estimated
coefficient

SE

F-statistic^

Pfit)

Pfit-n

Ps(f-I)

Pc'C)

Pc(f-I)

Op(f-I)
q-{t-n

0.07521

0.03208

0.01861

0.03258

0.07498

0.0297

0.03765

0.03609

0.2059

0.07897

0.1159

0.04239

1 .3352

0.5497

1 .5422

0.5309

0.5164

0.1979

0.455

6.516

0.119

4.006

'q-(f) = ao + a,P]{t) + b,P){t - ■)) * azP'sU) * b2P■,(t-^) - a^P.d}
+ bjPc{t-n + a,Op{t) + b,0p(f-1) + a5q-(/-l)

^The hypotfiesis to be tested is (b; ^ a, a^) = 0; and the corresponding
F-statistic is F, = {b, + a, as)^/Var(b, + a, a^).

-0.3, and the approximate 95% confidence inter-
val for A is -1.0 to 0.22. As in the earlier nonlag-
ged model, the coefficients of the independent
variables have the appropriate signs. Since the
coefficient of the lagged dependent variable can
be interpreted via Equation (5) as one minus the
rate of adjustment parameter, the partial ad-
justment parameter is 0.503. This implies an av-
erage lag of slightly less than one. As expected,
buyers of fish meal generally adjust to changing
conditions and prices within a year.

DISCUSSION

Both the static demand model and the partial
adjustment model provide reasonable levels of
statistical fit to the historical data series and the
signs and magnitudes of the regression

Table 6. — Regression equations for determining maximum log-likelihood of distributed lag form of
demand function. Pf = price of fish meal, P^ = price of soybean meal, P^ = price of com feed, Q„ =
poultry and egg production index, <7^_i = quantity offish meal, lagged. Superscript* indicates Box- Cox
transformation expressed in Equation (1).

Transformation

parameter

(A)

Intercept

Coefficient

<Ji--[

fl2

Pf

Ps

P6

Op

LmaxW

1.0

297.904

-103.141

105.367

-21.018

0.694

0 468

0.766

-81,133

0.6

40.639

-16.897

13.097

-3,821

0.537

0,485

0.800

-83,953

0.1

4.122

- 1 .792

0.902

-0 482

0.389

0498

0.822

-81.507

0

2.761

-1.147

0.522

-0.323

0,363

0,499

0.824

-81 259

-0.2

1.373

-0.470

0.170

-0.147

0.314

0498

0.825

-81.014

'-0.3

1.030

-0.301

0.098

-0 100

0.291

0,497

0.824

-81.013

(1.396)

(-3.567)

(1,161)

(-0-840)

(1,189)

(2.907)

-0.4

0.809

-0.193

0.056

-0 068

0.268

0.494

0 822

-81.090

-0.5

0,665

-0.124

0.031

-0,047

0.247

0.491

0.819

-81.239

-1.0

0.404

-0.013

0.002

-0.008

0.153

0.458

0.795

-82.853

'Indicates maximum likelihood estimate (f-values in parentheses).

274

HUPPERT: ANALYSIS OF UNITED STATES DEMAND FOR FISH MEAL

coefficients satisfy prior expectations. Because it
yields a significantly higher r^, and because the
test for serial correlation suggested by Griliches
(1967) lends it support, I tend to favor the distrib-
uted lag model. But the evidence is not really
conclusive. For one thing, the "Griliches test"
looks only for first-order serial correlation, and it
will probably fail to give correct guidance when
more complex residual generating processes are
present. Another difficulty is the lower precision
of the regression coefficients in the distributed
lag model. The importance of this depends upon
how the demand function is to be used. In
fisheries management applications the most im-
portant use of the demand model will be for pre-
dicting price effects resulting from changes in
annual production.

To compare the two demand models, the equa-
tions are transformed to give quantity demanded
in natural units (tons offish meal proteins) and
the 1976 values of independent variables other
than fish meal price are inserted. The resulting
relationships between price and quantity are

Table 7. — Demand predictions (q) and price elasticities {E) for
static demand (X = -0.55) and partial adjustment (\ = -0.3)
models.

Price of fish meal
protein (Pf)

Static demand model
4 E

Partial adjustment
model

<5 E

2

852.5

2.49

4,971 .0 6.26

4

295.2

0.95

372.3 2.34

6

215,1

0.64

168.8 1.63

8

182.8

0.50

110.7 1.32

10

165.0

0.42

84.2 1.14

for the dynamic demand model. Quantities pre-
dicted by Equations (15) and (16) and price elas-
ticities of demand for a range of prices are listed
in Table 7. From the Table and Figure 1 it is clear
that the two demand models are grossly simi-
lar. At low supply levels (less than about 250 t),
however, the predicted price responses are
greatly different, as are the quantities demanded
when prices are low (<$4 per unit protein). Thus,
any conclusions reached on the basis of this de-
mand analysis will be sensitive to the specification
of the demand function.

Qt =

-0.00389 + 0.04916

fp —0.55

-0.55

—0.55

(16)

for the static demand model, and

Qt

_, 1

—0.3

-0.03486 + 0.18001

-0.3

-0.3

(17)

Figure l. — Fish meal demand curves
based upon the maximum likelihood es-
timates of the static demand model (X =
-0.55) and the partial adjustment
model (X = -0.3).

100

200 300 400 500 600 700 800

FISH MEAL PROTEIN (1,000 metric tons)

900

1000

275

FISHERY BULLETIN: VOL. 78, NO. 2

Most economic models of fishery management
have ignored the influence of landings on the
price of fish or fishery products. The assumption
of fixed price is a particularly attractive one, be-
cause with fixed prices the harvest quantity is
proportional to the total revenue. Only the rela-
tionship between costs and landings must be
added to the model in order to derive economic
critertia for optimization. When management
programs control landings which are large rela-
tive to the market demand, however, the price is
likely to become a variable rather than a fixed
parameter. The use of demand relationships, such
as the one estimated above, will undoubtedly be-
come important as more control is exercised over
more fisheries in the United States. The means
for incorporating demand analysis into fishery
management models is explained by Anderson
(1973) and Clark (1976, chapter 5). More extensive
use of these complex models which include vari-
able prices will proceed only as fast as the devel-
opment of solid, empirical demand studies.

ACKNOWLEDGMENTS

I wish to thank Jane McMillan for her exten-
sive assistance in compiling data, managing the
computer processing necessary for this paper, and
providing professional and computational assis-
tance during the development of our statistical
results. Also, I thank James Zweifel for his helpful
comments on an earlier draft.

LITERATURE CITED

ANDERSON, L. G.

1973. Optimum economic yield of a fishery given a vari-
able price of output. J. Fish. Res. Board Can. 30:509-518.
BOX, G. E. P., AND D. R. Cox.

1964. An analysis of transformations. J. R. Stat. See,
Ser. B, 26:211-243.

Chang, H. S.

1977. Functional forms and the demand for meat in the
United States. Rev. Econ. Stat. 59:355-359.

Clark, c. w.

1976. Mathematical bioeconomics: the optimal manage-
ment of renewable resources. Wiley, N.Y., 352 p.

GRILICHES, Z.

1967. Distributed lags: a survey. Econometrica 35:16-49.
HAAVELMO, T.

1943. The statistical implications of a system of simul-
taneous equations. Econometrica 11:1-12.
KARRICK, N. L.

1963. Fish meal quality. In M. E. Stansby (editor), In-
dustrial fishery technology, p. 253-259. Reinhold Publ.
Co., N.Y.
Kmenta, J.

1971. Elements of econometrics. MacMillian Publ. Co.,
N.Y., 655 p.
KOLHONEN, J.

1974. Fish meal: International market situation and the
future. Mar. Fish. Rev. 36(3):36-40.
MEILKE, K. D.

1974. Demand for feed ingredients by U.S. formula feed
manufacturers. U.S. Dep. Agric, Agric. Econ. Res.
26:78-89.

National Marine Fisheries Service.

1975. Industrial fishery products, annual summary
1974. U.S. Dep. Commer., NOAA, Natl. Mar. Fish.
Serv., Curr. Fish. Stat. 6702, 8 p.

1977. Industrial fishery products, market review and out-
look. U.S. Dep. Commer., NOAA, Natl. Mar. Fish. Serv.,
Curr. Econ. Anal. 1-29, 27 p.

Nerlove, M.

1958. Distributed lags and demand analysis for agricul-
tural and other commodities. U.S. Dep. Agric, Agric.
Handb. 141, 121 p.

Pacific fishery Management Council.

1978. Northern anchovy fishery management plan. Fed.
Regist. 43(141):31655-31783.

Rao, p., and R. L. Miller.

1971. Applied econometrics. Wadsworth Publ. Co., Bel-
mont, Calif., 235 p.
SCHULTZ, H.

1938. The theory and measurement of demand. Univ.
Chicago Press, Chicago, 817 p.
Shultze, C. L., L. E. Gramley, and W. NORDHAUS.

1979. Annual report of the Council of Economic Advisors.
In Economic report of the president transmitted to the
Congress January 1979, p. 19-306. U.S. Gov. Print. Off.,
Wash., D.C.

Seber, g. a. F.

1973. The estimation of animal abundance and related
parameters. Hafner Press, N.Y., 506 p.

Waugh, F. v., and V. J. Norton.

1969. Some analysis offish prices. Univ. R.I. Agric. Exp.
Stn. Bull. 401, 68 p.

Wold, H., and L. Jureen.

1953. Demand analysis: a study in econometrics. Wiley,
N.Y.,358p.
WORKING, E. J.

1927. What do statistical "demand curves" show? Q. J.
Econ. 41:212-235.

276

DEVELOPMENT AND STRUCTURE OF FINS AND FIN SUPPORTS

IN DOLPHIN FISHES CORYPHAENA HIPPURUS AND

CORYPHAENA EQUISELIS (CORYPHAENIDAE)^

Thomas Potthoff^

ABSTRACT

The development and structure of the fins and fin supports were studied from a cleared and stained size
series of about 400 Coryphaena hippurus and about 400 C. equiselis. Coryphaena hippurus and
C equiselis differ in all aspects of fin ray and fin support development; C . equiselis is always more
advanced than equal-sized C. hippurus during development. The species differ in number of fin rays in
the single dorsal fin. The pterygiophores of the single dorsal fin each develop from a single cartilage in
both species. The cartilage then ossifies to proximal and distal radials. Each fin ray is serially
associated with a distal and proximal radial, and each ray is secondarily associated with the following
(posterior) proximal radial. Exceptions were found at the anteriormost and posteriormost parts of the
dorsal fin. The two species differ only slightly in anal fin ray counts. The pterygiophores of the anal fin
are similar in development and structure to those of the dorsal fin. The species do not differ in caudal fin
ray counts. The caudal fin rays are supported by some of the bones of the caudal complex, which
contains one neural spine, one specialized neural arch, two autogenous haemal spines, one autogenous
parhypural bone, five autogenous hypural bones, two paired uroneural bones, and two epural bones.
During development, hjrpurals one and two and hypurals three and four fuse, forming the dorsal and
ventral hypural plates. The two epurals fuse into one and the two pairs of uroneurals form one pair.
Both species have the same number of pectoral fin rays. In both species, pectoral fin rays are directly
supported by the scapula and four radials, and indirectly by the cleithrum and the coracoid.
The pectoral suspensorium, which consists of seven bones, connects the pectoral bones to the skull.
The posterior process of the coracoid develops as a prominent larval structure that disappears during
development. The pelvic fins of both species have one spinous and five soft rays. These fin rays
are supported on each side by the pelvic basipterygium. The basipterygium develops in similar fashion
to a pterygiophore.

The development and anatomy of the fins and fin
supports for Coryphaena hippurus and C. equi-
selis have not been described. The purpose of this
study was to document the development and
anatomy of the fins and fin supports for the family
Coryphaenidae and to point up differences in
meristic counts and arrangement of fin rays and
supporting bones between the two species of Cory-
phaena using cleared and stained material.

No complete study of the fins and fin supports
for the two Coryphaena species has been done.
Studies on the osteology and meristic counts exist
without use of cleared and stained material.
Jordan and Evermann (1896), Nichols (1909),
Gibbs and Collette (1959), Rothschild (1964),
Miller and Jorgenson (1973), and Shcherbachev
(1973) have published meristic counts for the two

'Contribution No. 80-03M, Southeast Fisheries Center Miami
Laboratory, National Marine Fisheries Service, NOAA.

^Southeast Fisheries Center Miami Laboratory, National
Marine Fisheries Service, NOAA, 75 Virginia Beach Drive,
Miami, FL 33149.

species. Clothier (1950) gave the meristic counts
and an illustration of the head and the vertebral
column for C. hippurus. Potthoff (1971), using
cleared and stained material, studied meristic
counts of C. equiselis. Collette et al. (1969) re-
ported the vertebral numbers of the two species,
and Gregory (1933) depicted the skull of C. hip-
purus and commented on the phylogenetic rela-
tionship of C. hippurus. Starks' (1930) description
of the pectoral girdle of C hippurus was presented
without illustrations.

Many publications deal with the biology (age,
growth, reproduction, food) of Coryphaena spp.,
usually C. hippurus (Schuck 1951; Williams and
Newell 1957; Gibbs and Collette 1959; Kojima
1961, 1963a, b, 1964; Beardsley 1967; Rose and
Hassler 1968, 1974; Shcherbachev 1973; Taka-
hashi and Mori 1973). Others document the distri-
bution of Coryphaena spp., most often that of C.
hippurus (Williams 1953; Morrow 1954; Pew 1957;
Gibbs and Collette 1959; Kojima 1960, 1964; Tibbo
1962; Shcherbachev 1973; Takahashi and Mori

Manuscript accepted November 1979.
FISHERY BULLETIN: VOL. 78, NO. 2, 1980.

277

FISHERY BULLETIN: VOL. 78, NO. 2

1973). Mito (1960) described the eggs and hatched
larvae of C. hippurus, and Gibbs and Collette
(1959) described large larvae and juveniles of both
Coryphaena species. Hassler and Rainville de-
scribed the rearing techniques for C. hippurus
from planktonic eggs and the subsequent growth
to juveniles. Burnett- Herkes (1974) worked on C.
hippurus parasites of the gills and mouth.

METHODS

Size series of 400 specimens of each species were
cleared and stained by the enzyme method of
Taylor (1967). The bones of four adult specimens
(two C. hippurus and two C equiselis) were
prepared by boiling in water and removing the
boiled flesh. Almost all specimens had been caught
in the west Atlantic, Gulf of Mexico, and the
Caribbean. A few specimens were from the mid-
Atlantic, the east Atlantic, and the east Pacific.

For each fin and fin support system, a repre-
sentative size series was chosen for each species
from the cleared and stained material (Table 1).
Thus, the same specimen did not necessarily
contribute to each of the series.

The terms preflexion, flexion, and postflexion
refer to the flexion state of the notochord in the
caudal region during larval development. They
are used to describe and highlight larval stages
based on Ahlstrom et al. (1976).

Only cleared and stained specimens were mea-
sured. Preserved larvae were usually too dis-
torted for accurate measurements, but were easily
straightened and measured after clearing and
staining. Measurements were to the nearest 0.1 of
a millimeter using a calibrated ocular micrometer

^Hassler, W. W., and R. P Rainville. 1975. Techniques for
hatching and rearing dolphin, Coryphaena hippurus, through
larvae and juvenile stages. Univ. N.C., Sea Grant Program
UNC-SG-75-31, 17 p.

Table l. — Number and length range (in millimeters NL or SL)
of cleared and stained specimens of Coryphaena spp. used for
study of individual fins and their support structures.

C. hippurus

C. equiselis

Item

No

Lengtfi

No.

Length

Dorsal fin

211

5.0-172

161

6.5-230

Pteryglophores

216

5.0-176

197

6.5-230,314

Anal fin

212

5.0-172

157

6.5-230

Pterygiophores

216

5.0-176

197

6.5-230,314

Caudal fin

201

5.0-172

138

6.5-230

Caudal complex

47

5.0-172,690

45

6.5-230, 330

Pectoral fin and

supports

123

5.0-172

164

6.5-230

Pelvic fin and

supports

105

6 0-176.449,920

76

7.0-172.315,330

for the smaller specimens (< 20 mm SL) and dial
calipers for the larger ones. Each measurement
was either notochord length ( NL, from the anterior
tip of the upper jaw to the posteriormost tip of the
notochord) for preflexion and early flexion larvae,
or standard length ( SL, from the anterior tip of the
upper jaw to the posteriormost edge of the hypural
bones) for late flexion and postflexion larvae,
juveniles, and adults.

All specimens were examined in 100% glycerin
under a binocular microscope, and illustrations
were drawn with the help of a camera lucida.
Ossification was determined from the uptake of
alizarin. Very light uptake (pink) of alizarin in a
structure was considered as onset of ossification.
Cartilage was determined by the presence of
structure but absence of red stain, and viewed by
carefully manipulating the illumination with the
substage mirror. Specimens from which organic
calcium had leached due to acid Formalin did not
stain and were not used.

The caudal complex terminologies follow Gosline
(1961a, b), Nybelin (1963), and Monod (1968).

Counts of pterygiophores and fin rays include
very small and vestigial structures such as fin
rays that consisted only of a left or right half, or of
two pieces not joined at the center.

RESULTS

Vertebral Column

The development and structure of the vertebral
column was not examined in this study. However,
it was noted that development is similar in all
respects for the two Coryphaena species as it was
reported for Thunnus atlanticus (Potthoff 1975).

Neural and haemal spines developed from car-
tilage before pterygiophores, but were difficult to
count accurately. In small specimens (5.9-6.3 mm
NL) intern eural and interhaemal space numbers
were estimated from myomere counts.

Dorsal Fin

The fully developed dorsal fin of C hippurus
has 58-66 rays (N = 99, x = 61.3, SE = 0.17,
24-172 mm SL) and that of C. equiselis 52-59 rays
(N = 113, 3c = 55.0, SE = 0.15, 18-230 mm SL).
Adult counts for C. hippurus are obtained be-

■* Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

278

POTTHOFF; DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

tween 18 and 24 mm SL and for C. equiselis
between 13 and 18 mm SL (Figure 1). Gibbs and
Collette (1959) reported 46-65 {x = 58.4) dorsal fin
rays for C. hippurus and 48-60 i'x = 52.6) for
C. equiselis. My counts and those of Gibbs and
Collette (1959) differ because Gibbs and Collette
included counts of small specimens (from about 12
mm SL) of both species in their sample and
because C equiselis develops a full complement of
dorsal fin rays at a smaller size than C hippurus
(13-17 mm SL vs. 18-23 mm SL); therefore, more
C. hippurus than C equiselis with incomplete
dorsal fins were counted by Gibbs and Collette,
and inclusion of incomplete dorsal fin ray counts
widened the range of counts and lowered the mean
number of dorsal fin rays. Dorsal fin ray counts
reported by Shcherbachev (1973) (46-67 for C.
hippurus and 48-60 for C equiselis ) are from his
ov^m data and those of Gibbs and Collette. Roth-
schild (1964) reported 54-58 {x = 57.9) for adult

C. equiselis, all from the Pacific Ocean. Here,
count differences probably resulted from the
method of counting (cleared and stained vs.
preserved material) but may also have been due
to population differences.

Dorsal fin rays were first seen in C hippurus at
6 mm SL and were present in all specimens at
8 mm SL (Figure 1). The smallest specimen of
C. equiselis (6.5 mm SL) already had 12 dorsal fin
rays. Development of the dorsal fin rays for both
species started in the dorsal finfold at the posterior
third of the body (Figure 2). This was above the
22d-24th myomere for three C. hippurus with
only 3 or 4 dorsal fin rays. With growth, addition of
dorsal fin rays was in an anterior and posterior
direction for both species, but more fin rays were
added anteriorly (Figure 2). The dorsal fin, despite
the more rapid addition of rays anteriorly, reached
completion posteriorly at a smaller size of the
larvae than anteriorly. This is because more

70

60

t/i

50

■40

CO

U.30

20

10

5 S

99

5 8 3 6

V^.

5 I

'M'W'*

0 0 0 5 0..

C. equiselis^
C. hippurus i

5 6 7 8

9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 >23
LENGTH, mm NL or SL

Figure l. — Number of dorsal fin rays in relation to length in 161 Coryphaena equiselis (6.5-230 mm NL or SL) and 211 C. hippurus
(5.0-172 mm NL or SL). Range (vertical line), mean (horizontal line), and 2 standard errors about the mean (white and black
bars) are indicated. Number of specimens for each length interval is given above the range and is in italics for C. equiselis.

279

FISHERY BULLETIN; VOL. 78, NO 2

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280

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

pterygiophores had to be added from place of
origin anteriorly than posteriorly. Small C. hip-
purus (5 mm NL-11 mm SL) usually had fewer
fin rays compared to equal-sized C equiselis
(Figure 1). Between 12 and 14 mm SL both species
had about equal dorsal fin ray numbers. Spec-
imens of C. hippurus 15 mm SL and longer
usually had more dorsal fin rays than equal-sized
C. equiselis.

The developmental sequence of dorsal fin rays
in Coryphaena spp. is similar to that observed in
Trachurus symmetricus ( Ahlstrom and Ball 1954),
Haemulon plumieri (Saksena and Richards 1975),
and Archosargus rhomboidalis (Houde and Pott-
hoff 1976). It is as though Coryphaena spp. is
developing two dorsal fins in the same pattern of
the above examples, e.g., first the second dorsal fin
followed by the first dorsal. It is of interest to note
that most scombroids do not follow this pattern
and develop the first dorsal fin first (Voss 1954;
Potthoffl975).

Dorsal Fin Pterygiophores

Counts

There was a supporting pterygiophore in both
species of Coryphaena in a jointed series for each
dorsal fin ray, except for the first two or three
anteriormost rays. Each pterygiophore had a
proximal and a distal radial. The distal radial
was located between the bifurcate base of the fin
ray. Proximal and distal radial and fin ray formed
a series, hence, a serial association. Each fin ray
also closely approximated the following posterior
pterygiophore in a secondary association. Thus,
each pterygiophore supported a ray in a serial
association and an immediately anterior ray in a
secondary association. The exceptions were found
at the beginning and the end of the fin. The
anteriormost pterygiophore supported from one to
three rays, but most often two rays (Table 2). Also,
in 2 out of 70 specimens of both species, no rays
were associated with the anteriormost pterygio-
phore, and the pterygiophore was very small and
almost a vestige. The posteriormost ray in the
dorsal fin was a double ray which was serially

Figure 2. — Schematic representation of dorsal and anal.fin and
pterygiophore development in Coryphaena hippurus in relation
to the vertebral column and head. Oval -shaped representation
of pterygiophores are cartilaginous when white and ossifying
when black. Scale represents interneural and interhaemal
spaces and points align with midpoint of vertebral centra.

Table 2. — Number (adult count) of anteriormost dorsal fin rays
without distal radials and number of dorsal fin rays associated
with the anteriormost dorsal fin pterygiophore for 28 Cory-
phaena hippurus (78.8-176 mm SL) and 35 C. equiselis (74.1-172,
314mmSL).

Item

Species

Number of anterior-
most dorsal fin rays

0 12 3

Without distal radials

Associated with the ante-
riormost pterygiophore

C. hippurus
C. equiselis

C. hippurus
C. equiselis

12

1 6

3

1

12 4
25 4
24 1
17 19

associated with the posteriormost pterygiophore.
This was the only ray in the dorsal fin which
lacked a secondary association. Total dorsal fin
ray count in both species was either one less than
the pterygiophore count, equal to the pterygio-
phore count, or one or two greater than the
pterygiophore count. Thus, the two species dif-
fered in their pterygiophore number as they
differed in their fin ray counts.

In larvae, juveniles and small-sized adults of
Coryphaena spp. the proximal radials of the
dorsal fin were inserted in interneural spaces. The
first interneural space was bounded anteriorly by
the head and posteriorly by the first neural spine,
followed posteriorly by the remaining interneural
spaces which were bounded by all other neural
spines (Figure 3).

Fully developed specimens of the two species of
Coryphaena differed by the number of pterygio-
phores that occupied the interneural spaces. The
number of pterygiophores found in the first inter-
neural space separated the species most of the
time, with 10-14 (x = 11.0) for C hippurus and
7-11 ix = 8.0) for C. equiselis (Figures 3, 4). The
species also differed in the number of pterygio-
phores associated with the remainder of the inter-
neural spaces. Although individual variability
within each interneural space was too great to
allow this character to be used to separate the
species, the mean number of pterygiophores in
each interneural space was always greater for
C hippurus.

The species also differed in the number of
interneural spaces that were occupied by the
dorsal fin pterygiophores (Figure 3; Tables 3, 4).
In C. hippurus the dorsal fin pterygiophores
extended to the 26th interneural space and seldom
to the 27th, whereas in C. equiselis they extended
to the 28th and seldom to the 27th or 29th space.
There was some overlap for the two species in this
character, but if the termination of the anal fin
pterygiophores was taken into account, together

281

FISHERY BULLETIN: VOL. 78, NO. 2

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14 15 1 16117 I IB I IVI TO! ^1 1^^ I '•> I^'tl'OI -lo I .</ I .<oi

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Figure 3. — Schematic representation of the relationship of dorsal and anal fin pterygiophores to the vertebral column in adult
Coryphaena hippurus (upper) and C. equiselis (lower). Black numbers, intemeural and interhaemal spaces; white numbers, centra.

14

13

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C. hippurus^

i/\ |10 7 9 4 .

0 ^ lb 11 12 13 14 is 16 17 is 19 20 21 22 23 24 25^28 33 38 43 >43

LENGTH, mm SL

Figure 4. — Number of pterygiophores in the first intemeural space in relation to length in 192 Coryphaena equiselis (8.6-173,
314 mm SL) and 193 C. hippurus (8.6-176 mm SL). For explanation of symbols, see Figure 1.

with the termination of the dorsal fin pterygio-
phores, complete separation for the two species
resulted (Figure 3, Table 3).

282

Dorsal fin pterygiophores had the same pattern
of appearance in both species of Coryphaena as
the dorsal fin rays. Cartilaginous pterygiophores

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

Table 3. — Adult and juvenile position of posteriormost dorsal
and anal fin pterygiophores in their intemeural and inter-
haemal spaces for 193 Coryphaena hippurus (9.0-176 mm SL)
and 186 C. equiselis 18.9-172, 314 mm SL). For numbering of
vertebrae and spaces, see Figure 3,

Intemeural space numbers
Interhaemal space numbers

Species

26

25

26
26

26

27

27
26

27
27

27
28

28
27

C. hippurus
C. equiselis

2

172

3

11

5

2

2

28 28 29 29
28 29 28 29

172

without rays were first seen in the 22d-24th
myomeres at 5.9 mm NL in C. hippurus (Figure 2)
and with some rays in the 18th-27th myomeres at
6.5 mm NL in the smallest available but more
advanced C. equiselis. In both species of Cory-
phaena the pterygiophores appeared shortly be-
fore the fin rays developed. As pterygiophores
were added, anteriorly and posteriorly rays were
lacking for one or two anteriormost and posterior-
most additions (Figure 2).

In both species, the posteriormost intemeural
spaces (numbers 26-28) were occupied with ptery-
giophores between 7 and 8.5 mm SL (Table 4). The
anteriormost intemeural space started to fill with
pterygiophores at 9.3 mm SL in C. equiselis and at
13.1 mm SL in C. hippurus (Figure 4, Table 4).
Adult counts in the anteriormost intemeural
space of 7-11 pterygiophores were obtained for C.
equiselis between 12.3 and 23.2 mm SL and for C.
hippurus of 10-14 pterygiophores between 18.7
and 30.8 mm SL (Figure 4, Table 4).

Ossification of the pterygiophores started in the
same area and proceeded in the same directions as
the cartilaginous development (Figure 2). Ossifi-
cation of pterygiophores occurred first at 8.8 mm
SL in C. equiselis and at 9.7 mm SL in C. hippurus
(Table 4). The posteriormost intemeural space
number 28 of C. equiselis had ossifying pterygio-
phores at 8.9 mm SL, and posteriormost inter-
neural space number 26 of C. hippurus had
ossifying pterygiophores at 10.2 mm SL (Table 4).
Specimens 10.3-11.6 mm SL of C. equiselis, and
16.2-19.2 mm SL specimens of C. hippurus had one
or more ossifying pterygiophores in the first inter-
neural space (Figure 4, Table 5). All dorsal fin
pterygiophores were ossifying in both species at
about 45 mm SL when the count of ossifying
pterygiophores was in the adult range and the
first intemeural space did not have anterior
cartilaginous pterygiophores (Figures 4, 5).

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283

FISHERY BUIXETIN: VOL. 78, NO. 2

Table 5. — Sum ladult count) of anal fin pterygiophores in the
two anteriormost interhaemal spaces, numbers 14 and 15, in
35 Coryphaena hippurus (49.9-176 mm SL) and 32 C. equiselis
(74.1-172, 314 mm SLj. For numbering interhaemal spaces, see
Figure 3.

Number of pterygiophores

Species

4

5

6 7 8

9

10

C. hippurus
C. equiselis

5

20

14 18
6 1

2

1

Morphology' and Development

The pterygiophores in the center area of the
dorsal fin developed first in both species. A ptery-
giophore (proximal and distal radial) appeared as
one elongate piece of cartilage (Figure 6). Ossifica-
tion was first observed at the middle part of the
pterygiophore cartilage (Figure 6) and proceeded
distally and proximally along the cartilage until
only cartilage tips were present at the extremities.
At this point, the sagittal and lateral keels began
to develop (Figure 4). Further development of the
pterygiophore consisted of growth of the keels,
growth of bone around the locus of secondary fin

ray association, and segregation and ossification
of the distal radial. The distal radial developed
from the distal tip of the pterygiophore cartilage
late during ontogeny (Figure 6), and ossified into
two pieces of bone (Figure 7).

The pterygiophores in the posteriormost area of
the dorsal fin developed similarly to those of the
center area. The posteriormost pterygiophore sup-
ported one ray in series. This ray developed from
two rays but was counted as one according to
Hubbs and Lagler (1958). In adults, the base of the
anterior ray fitted closely over the base of the
posterior ray and the base of the posterior ray
articulated with the distal radial of the posterior-
most pterygiophore (Figures 8, 9).

The supports of the anterior portion of the
dorsal fin developed last. In C. equiselis the first
interneural space was almost filled with cartilag-
inous pterygiophores, but in equal-sized C hip-
purus the first interneural space was empty and
the second interneural space had only one carti-
laginous pterygiophore (Figures 10, 11). The ante-
riormost cartilaginous pterygiophores always had

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9
8
7
6
5
4
3
2

C. equiselis^
C. hippurus ^

0 ^ 10 11 12 ]3 14 15 16 17 18 19 20 21 22 23 24 25^8 33 38 43

LENGTH, mm NL or SL

Figure 5.— Number of ossifying pterygiophores in the first interneural space in relation to length in 126 Coryphaena equiselis and

88 C. hippurus. For explanation of symbols see Figure 1.

284

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

Figure 6. — Ontogenetic development of a dorsal fin pterygiophore with its serially associated ray in the
14th intemeural space of Coryphaena equiselis (left lateral view). Pterygiophores drawn in the natural
attitude relative to horizontal body axis. Starting from the left specimen length (millimeters SL) was:
top, 7.6, 9, 9.8, 11.5, 12.2, 14.2; bottom, 17.4, 22.5, 45.4, 31. Symbols: D, distal radial; P, proximal radial;
R, serially associated ray. Stippled, cartilage; darkened, bone.

a ray developing concurrently (Figures 2, 10, 11).
In specimens of both species, which had the full
count of pterygiophores in the first intemeural
space, it was common to have a ray develop in
front of the cartilaginous pterygiophore (Fig-
ure 2). The pterygiophores of the first intemeural
space in large juveniles and adults of both species
were vertical to the body axis near the first neural
spine and slightly anteriorly inclined dorsad near
the head (Figure 12). The anteriormost pterygio-
phore in the adults was either of normal size (not
figured), very small (Figures 12, 13), or just a
vestige (not figured). In a few instances, in both
species, the anteriormost pterygiophore was com-

pletely or partially fused to the second pterygio-
phore. The anteriormost pterygiophore of both
species had either one, two, or three associated
rays (Table 2). For the two species the anterior-
most dorsal fin ray was either normal in size or a
vestige (Figures 12, 13). In both species three types
of first fin ray vestiges were observed: a paired
vestige (Figure 13), a single right vestige, and a
single left vestige.

Distal radials were present between the bases of
each fin ray for almost the entire dorsal fin. Distal
radials were last to ossify from the distal portion of
the pterygiophore cartilage. Only the anterior-
most three fin rays of both species sometimes

285

FISHERY BULLETIN: VOL. 78, NO. 2

1.0 mm
I 1

Figure 7. — Pterygiophore from 14th intemeural space with its secondarily and serially associated rays from a 230 mm SL (Joryphaena
equiselis. Left: anterodorsal view, secondarily associated ray moved to the right of the proximal radial; right: left lateral
view. Symbols: D,, distal radial of secondarily associated ray; D, distal radial of serially associated ray; P, proximal radial;
R,, secondarily associated ray; R, serially associated ray. Stippled, cartilage; darkened, bone.

lacked distal radials. The absence or presence of
distal radials was not related to the number of fin
rays associated with the anteriormost pterygio-
phore (Table 2). The first three or four (anterior-
most) distal radials of both species differed in
structure from the remainder. These radials con-
sisted of one piece of bone (Figure 14) whereas all
other radials were of two pieces (Figures 7, 8).

The dorsal pterygiophores of Coryphaena spp.
differed in several ways from other perciform
fishes. Predorsal bones reported in Apogonidae
(Fraser 1972), Serranidae and Grammistidae
(Kendall 1976), Sparidae (Houde and Potthoff

286

1976), and for all the stromateoid families (Ahl-
strom et al. 1976) were lacking. Also lacking was
the terminal bone in the dorsal fin support series
called a "stay" by Weitzman (1962). Stays have
been reported for such families as Characidae
(Weitzman 1962), Scombridae (Kramer 1960; Pott-
hoff 1975), Sparidae (Houde and Potthoff 1976),
Nomeidae and Centrolophidae (Ahlstrom et al.
1976), and Centropomidae, Kyphosidae, Lutjan-
idae, Percichthyidae, and Scorpidae (Johnson
1978). A stay was observed in the Scombrolabrac-
idae and a double stay in the Gempylidae (Potthoff
et al. 1980).

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

Figure 8. — Posteriormost dorsal fin pterygiophore with its secondarily and serially associated rays from a 230 mm SL Coryphaena
equiselis. Left: anterodorsal view, secondarily associated ray has been moved to the right of the proximal radial; right: left lateral view,
pterygiophore has been tilted 30° from the horizontal toward the vertical. Symbols: Dj, distal radial of secondarily associated ray;
D, distal radial of serially associated double ray; P, proximal radial; Rj, secondarily associated ray; R, serially associated double ray.
Stippled, cartilage; darkened, bone.

1.0 mm

Figure 9, — Anterior and right lateral views of right side of a disarticulated posteriormost double dorsal fin ray with its distal radial
from a 230 mm SL Coryphaena equiselis. a, right half of anterior ray, anterior view; b, right half of posterior ray and right half of its
distal radial, anterior view; c, right half of anterior ray, lateral view; d, right half of posterior ray and right half of its distal radial,
lateral view. Symbol; D, distal radial.

287

FISHERY BULLETIN: VOL. 78, NO. 2

HEAD

Figure lO. — Left lateral view of anteriormost part of the dorsal fin and pterygiophores for a 11 mm SL Coryphaena equiselis, showing
relationship of pterygiophores to head, intemeural spaces, and centra. Symbols: C, first centrum; ENT, second intemeural space;
NS, first neural spine; P, proximal radial. Stippled, cartilage; darkened, bone.

HEAD

0.5 mm

Figure ll. — Left lateral view of anteriormost part of the dorsal fin and pterygiophores for a 11 mm SL Coryphaena
hippurus, showing the relationship of pterygiophores to head, intemeural spaces, and centra. Symbols: C, third
centrum; R, dorsal fin ray. For explanation of other symbols, see Figure 10. Stippled, cartilage; darkened, bone.

288

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

Figure 12. — Left lateral view of four anteriormost dorsal fin pterygiophores with secondarily and serially associated
rays from a 230 mm SL Coryphaena equlselis. Symbols: R, dorsal fin ray; P, proximal radial; D, distal radial.

The proximal and distal radials (except the
anteriormost three or four) of Coryphaena spp.
were similar along the entire fin and were located
between the bifurcate bases of the fin rays. Middle
radials were absent in the posterior portion of the
fin. In most other perciform fishes, distal radials
differ between the first and second dorsal fins. The
first dorsal fin distal radials are anterior to the

bases of the fin spines, and the second dorsal fin
distal radials are between the bifurcate bases
of the fin rays, and middle radials are pres-
ent posteriorly. Anatomically different distal
radials for the first and second dorsal fins and
the presence of middle radials posteriorly have
been reported in the Carangidae (Berry 1969),
Scombridae (Kramer 1960; Potthoff 1974, 1975),

289

FISHERY BULLETIN: VOL. 78, NO. 2

k

0.5 mm

^

Figure 13. — Anteriormost dorsal fin pterygiophore with secondarily associated vestigial ray from a 230 mm SL Coryphaena equiselis.
Left: anterodorsal view, right: left lateral view. Symbols: P, proximal radial; R, vestigial ray.

Sparidae (Houde and Potthoff 1976), Centro-
pomidae, Kyphosidae, Lutjanidae, Percichthy-
idae, and Scorpidae (Johnson 1978), and Gem-
pylidae and Scombrolabracidae (Potthoff et al.
1980).

Anal Fin

The fully developed anal fin of Coryphaena
hippurus has 25-31 rays (N = 147, x = 28, SE =
0.01, 16-172 mm SL) and that of C. equiselis 23-29
(N - 118, X - 26, SE = 0.01, 16-230 mm SL). The
anal fin ray counts, in contrast to the dorsal fin ray
counts, differ only slightly from those reported by
Gibbs and Collette (1959), Rothschild (1964), and
Shcherbachev (1973). Both species have adult anal
fin ray counts at smaller sizes than dorsal fin ray
counts (C. hippurus at 8-11 mm SL, C. equiselis
at 8-9 mm SL).

Anal fin rays v^^ere first seen in some C. hip-
purus at 6 mm NL, just before the onset of dorsal

290

fin ray development and all C. hippurus had anal
rays at 7 mm NL (Figure 15). The smallest
available (6.5 mm NL) C. equiselis had 14 anal
rays. Development of the anal fin of both species
began in the finfold at the approximate center of
the fin, below the 22d or 23d myomere. Addition of
rays was in an anterior and posterior direction for
both species (Figure 2). As in the dorsal fin, the
posterior portion of the anal fin was completed
first and the anteriormost rays developed last.
From 6 mm NL to 9 mm SL, C. hippurus had fewer
anal fin rays than C. equiselis; at 10 and 11 mm SL,
both species had about equal numbers of rays; at
12 mm SL and longer, C. hippurus tended to have
more anal rays than C equiselis (Figure 15).

Appearance and additional sequence of anal fin
rays in Coryphaena spp. are similar to Scomber
Japonicus iPneumatophorus diego) (Kramer 1960),
Thunnus atlanticus (Potthoff 1975), Haemulon
plumieri (Saksena and Richards 1975), and Archo-
sargus rhomboidalis (Houde and Potthoff 1976).

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

Figure 14. — Second anteriormost dorsal fin pterygiophore with
secondarily and serially associated rays from a 230 mm SL
Coryphaena equiselis. Left: anterodorsal view, secondarily asso-
ciated ray has been moved to right of proximal radial; right: left
lateral view, secondarily associated ray has been moved dorsally.
For explanation of symbols, see Figure 7.

1.0 mm

For Trachurus symmetricus, Ahlstrom and Ball
(1954) reported an anterior to posterior anal fin
development.

Anal Fin Pter^giophores

Q)unts

The description for dorsal fin pterygiophores
in the foregoing section may be applied to anal
fin pterygiophores because of the similarities
between the two fins and their supports. Pterygio-
phores of the anal fin are inserted in the in-
terhaemal spaces. The anteriormost (first) in-

terhaemal space is bounded anteriorly by the
stomach, intestine, and anus and posteriorly by
the first haemal spine. The first haemal spine was
of variable length, and in many cases did not reach
the anal fin pterygiophores. The anal fin pterygio-
phores in the two anteriormost interhaemal spaces
were therefore summed (Table 5, Figure 3).

Fully developed specimens of Coryphaena spp.
differed in their numbers and arrangement of anal
fin pterygiophores. The total number of pterygio-
phores closely approximated the anal fin ray
count. For both species the pterygiophore count
was equal to or one to two less than the anal fin ray
count. The sum of the pterygiophores found in the

291

FISHERY BULLETIN: VOL. 78, NO. 2

40

30

20

:}■

w

e. equiselis ^
C. hippurus ^-

165

7 7 "'

„ If -i ** % f

6 7 8 9 10 11 >11

LENGTH, mm NL or SL

Figure 15. — Number of anal fin rays in relation to
length in 159 Coryphaena equiselis (6.5-230 mm NL
or SL) and 210 C. hippurus (5.0-230 mm NL or
SL). For explanation of symbols, see Figure 1.

first two anteriormost interhaemal spaces (14 and
15) separated the species most of the time, with
7-10 (X = 8.0) for C. hippurus and 4-7 (x = 5.0) for
C. equiselis (Table 5). The two species also differed
in the number of pterygiophores found in the
remainder of the interhaemal spaces. Individual
variability, however, was too great for each inter-
haemal space to serve as a separating character.
The mean number of pterygiophores for each
interhaemal space was always greater for C.
hippurus. Coryphaena equiselis had more in-
terhaemal spaces with one pterygiophore and
C. hippurus more with two pterygiophores. In
C. hippurus the anal fin pterygiophores extended
to the 25th, 26th, or 27th interhaemal space, but
most often to the 26th, whereas in C. equiselis
they extended to the 27th, 28th, or 29th inter-
haemal space, but most often to the 28th. There
was some overlap for the two species in this
character, but if the termination of anal and
dorsal fin pterygiophores is considered together,
complete separation for the two species results
(Table 3). The dorsal and anal fin pterygiophores
most often terminated in opposing interneural
and interhaemal spaces (Table 3).

Morphology and Development

Cartilaginous anal fin pterygiophores without
fin rays were first observed in the 18th-24th
myomeres (which approximately correspond to
the 18th-24th interhaemal spaces) in a 5.9 mm NL
C. hippurus (Figure 2, Table 6), but rays were
developing in a 6 mm NL specimen. The smallest
available C. equiselis of 6.5 mm NL had carti-
laginous pterygiophores in myomeres 18-27. Fin

292

rays were developing, but a few anteriormost and
posteriormost pterygiophores lacked rays. Addi-
tion of cartilaginous pterygiophores proceeded in
both species anteriorly and posteriorly (Figure 2,
Table 6). Rays developed after the addition of the
cartilaginous pterygiophores. The posteriormost
interhaemal space number 26 of C. hippurus
had one to three cartilaginous pterygiophores at
7.3-8.3 mm SL (Table 6). The posteriormost inter-
haemal space number 28 of C. equiselis had
cartilaginous pterygiophores at 7 mm SL (Table
6). All specimens of C. hippurus > 9.5 mm SL and
all those of C. equiselis > 8.5 mm SL had some
pterygiophores in their anteriormost interhaemal
space number 14. The size at which adult counts
were reached for the first interhaemal space was
not determined.

Ossification of the cartilaginous pterygiophores
first occurred in the area where the cartilaginous
pterygiophores first appeared and proceeded in
the same direction as cartilage development (Fig-
ure 2). Ossifying anal fin pterygiophores were first
seen at 8.8 mm SL in C. equiselis and at 9.7 mm SL
in C. hippurus in the 16th-19th and 16th-25th
interhaemal spaces (Table 6), and concurrently
with ossifying dorsal fin pterygiophores. The
posteriormost interhaemal space number 28 of
C. equiselis had ossifying pterygiophores at
8.9 mm SL and space number 26 of C. hippurus
had them at 10.2 mm SL (Table 6). All specimens
of C. equiselis > 9.4 mm SL and all specimens of
C. hippurus > 11 mm SL had some ossifying
pterygiophores in the anteriormost interhaemal
space number 14, or rarely space number 15 (Table
6). The anteriormost anal fin pterygiophore was
ossifying in C. equiselis at 14.9-22 mm SL and in

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

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4iricbr^cocnci'-

C. hippurus at 17.2-30 mm SL. The development of
individual anal fin pterygiophores was similar to
that of the dorsal fin pterygiophores.

Each anal fin pterygiophore of both species had
two rays; one ray was in a serial association and
the preceding ray was in a secondary association.
The posteriormost anal ray lacked a secondary
association with a pterygiophore and the anterior-
most anal ray lacked a serial association (Figure
16). Exceptions were common with the anterior-
most pterygiophore and rays. Many specimens of
both species had very small first pterygiophores or
even vestiges. In a few instances in both species
the anteriormost first pterygiophore was com-
pletely or partially fused to the second pterygio-
phore. The normal number of anal rays associated
with the first pterygiophore was two, but for both
species one or three rays also were found. The
anteriormost anal ray was either normal as in
Figure 16, very small, or a vestige. As in the dorsal
fin, the vestige was either single left or right,
or paired.

A distal radial was present between the base of
each fin ray almost for the entire anal fin. It
developed and ossified from the pterygiophore
cartilage. Only the anteriormost anal fin ray
sometimes did not have a distal radial between its
base (Table 7). Only 1 C. hippurus out of 49 had
two anteriormost rays without distal radials.
When the anteriormost ray had a distal radial, it
was either serially or secondarily associated with
the first pterygiophore. When the association was
serial, the anteriormost pterygiophore had only
one ray; when it was secondary, it had two rays. It
is possible that, when the association was sec-
ondary, the distal radial of the first fin ray was in
actuality a vestigial pterygiophore. The specimen
in Figure 16 did not have a distal radial for the
anteriormost ray. The absence or presence of
distal radials for the anteriormost anal fin ray was
not related to the number of fin rays that were

Table 7. — Number (adult count) of anteriormost anal fin rays
without distal radials and number of anal fin rays associated
secondarily and serially with the anteriormost anal fin pterygio-
phore in 49 Coryphaena hippurus (41.0-176 mm SL) and 33
C. equiselis (74.1-172, 314 mm SL).

Number of anterior-
most anal fin rays

Item

Species

0

1

2

3

Without distal

C. hippurus

24

24

1

radials

C. equiselis

10

23

Associated witfi the

C. hippurus

3

40

6

anteriormost anal

C. equiselis

3

29

1

pterygiophore

293

FISHERY BULLETIN: VOL. 78, NO. 2

Figure 16. — Anteriormost anal fin pterygiophore with secondarily and serially associated rays from a 230 mm SL Coryphaena
equiselis. Left: left lateral view; right: anterior view, serially associated ray has been moved to the left of the proximal
radial. » Symbols: D, distal radial of serially associated ray; P, proximal radial; Rj, secondarily associated ray; R, serially
associated ray.

associated with the anteriormost anal pterygio-
phore (Table 7). In both species either one, two, or
three rays were associated with the first pterygio-
phore. In both species the anteriormost distal
radial (which was either between the base of the

first or second anal fin ray) was a single piece of
bone (Figure 16). The second distal radial (which
was either between the base of the second or third
anal fin ray) consisted of two pieces of bone, as
shown for the dorsal pterygiophores in Figures 7

294

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

and 8. The two pieces of the second distal radial
were sometimes partially fused; and in a few rare
the second distal radial was one piece of

cases,

Table 8. — Adult caudal fin ray counts for 117 Coryphaena
hippurus (19.6-172 mm SL) and 97 C. equiselis (19.6-230 mm
SL). Symbols: USCR, upper secondary caudal rays; LSCR,
lower secondary caudal rays; PCR, principal caudal rays.

Number of specimens

Total fin ray count USCR * PCR - LSCR C hippurus C equiselis

37
38
39
39
40
40
41
41
42
43
44
45

10+17-10
10+17*11
10+17+12
11+17+11
11+17+12
12+17+11
11+17+13
12+17+12
12+17+13
13+17+13
13*17+14
14+17*14

0

2

0

10

12

3

0

36

23

26

2

3

1

1

2

0

28

0

6

17

32

8

2

0

bone. All following distal radials of the anal fin
were two pieces of bone in both species. The
posteriormost anal fin ray consisted of two closely
approximated rays with one distal radial.

Caudal Fin

The two species differed little in ray counts on
fully developed caudal fins. Coryphaena hippurus
had 38-45 (x = 41.4) caudal rays and C. equiselis
had 37-44 (x = 41.1) (Table 8). Coryphaena hip-
purus tended to have an equal number of upper
and lower secondary caudal rays whereas C
equiselis tended to have one or two more lower
than upper secondary caudal rays. Adult caudal
ray counts for C. hippurus were obtained between
15.6 and 19.6 mm SL and for C. equiselis between
11.6 and 12.5 mm SL (Tables 9, 10). A procur-

TaBLE 9. — Caudal fin ray development in 201 Coryphaena hippurus (5.0 mm NL-172 mm SL) and 138 C. equiselis (6.5 mm NL-
230 mm SL). Symbols: SCR, secondary caudal rays; PCR, principal caudal rays.

Length
mm NL or SL

5.5
6.5
7.5
8.5
9.5

4.6-

5.6-

6.6-

7.6-

8.6-

96-10.5
10.6-11 5
11,6-12.5
12-6-13.5
13.6-14.5
14.6-15.5
15.6-16.5
16.6-17.5
17.6-18.5
18.6-19.5
>19.5

Coryphaena hippurus

Coryphaena equiselis

Upper

Lower

Total fl
Range

n ray count

N

Upper

Lower

Total fii
Range

1 ray count
X Sx

SCR

PCR

PCR

SCR

SCR

PCR

PCR

SCR

N

0

2-4

2-5

0

4- 9

7.0

1,5

3

—

—

—

—

—

—

—

0

4-8

5-8

0

9-16

11.3

16

4

0

6

6

0

12

—

—

1

0

1-8

2-8

0- 1

3-17

12,9

1,3

10

0

9

8

1- 2

18-19

18.5

0.5

2

0

9

8

1- 2

18-19

18.8

0,2

6

0- 3

9

8

2- 4

19-24

21.2

12

5

0- 3

9

8

2- 4

19-24

19.8

1,1

5

3- 8

9

8

4- 8

24-33

29.0

1.9

4

1- 4

9

8

2- 5

21-26

233

0,7

7

5- 9

9

8

6- 9

28-35

31.0

1.3

5

0- 4

9

8

2- 5

19-26

24.7

1.0

7

7- 9

9

8

8- 9

32-35

33.6

0.4

7

4- 5

9

8

5- 7

26-29

27.7

0.9

3

10-11

9

8

11-12

38-40

38.5

0.5

4

5- 6

9

8

6

28-29

286

0.2

5

11

9

8

12

40

—

—

1

7- 8

9

8

8- 9

32-34

33.3

0.3

6

11

9

8

12

40

—

—

1

7- 9

9

8

8-10

32-36

347

0.6

6

12

9

8

12

41

—

—

1

9-11

9

8

10-12

36-40

37.5

0.7

6

11

9

8

11-13

39-41

40.0

1.0

2

9-11

9

8

9-11

35-39

366

0.7

5

11

9

8

11-13

39-41

40.0

0,6

3

9-11

9

8

9-11

35-39

38.2

0.8

5

11-12

9

8

12-13

40-42

40.5

0.5

4

8-12

9

8

12

37-41

395

0.6

6

11

9

8

12

40

—

—

1

10-14

9

8

11-14

38-45

41.4

0.1

117

10-13

9

8

10-14

37-44

41 1

0.1

97

Table lO. — Length (in millimeters NL or SL) at which parts of the caudal complex first appear in cartilage and then ossify in
41 Coryphaena hippurus (5.0 mm NL-110 mm SL) and 39 C. equiselis (6.5-85 mm SL). "First appearance in cartilage" does not pertaiin
to all specimens of that size but only indicates a first appearance. Symbol: Pu, preural centrum.

Part

Neural spine. PUj
Specialized neu-
ral arch, PUj
Large uroneural
Small uroneural
Epurals
Urostyle
Pu J centrum
PU3 centrum
Haemal spine. PUj
Haemal spine, Pu^
Parhypural
Hypural 1
Hypural 2
Hypural 3
Hypural 4
Hypural 5

Coryphaena hippurus

First appearance
in cartilage

First evidence
of ossification

7.4

7.4

7.4-8.0

6.0

5.0

<5.0

<5.0

<5.0

<5.0

6.0

8.1-9.5

9.5

8.0-

Ossifying in
all specimens

Completely
fused

119

11 9

11.9

10.6

11.9

11,9

11.9

14,6

14.6

80

11.9

9,5

11.9

95

11.9

9,5

11.9

9,5

11.9

9,5

11.9

9.5

11.9

9.5

11.9

95

11.9

95

11.9

11.9

11.9

750-
40.0-

850
47.0

106 0

106.0

Coryphaena equiselis

First appearance
in cartilage

First evidence
of ossification

Ossifying in
all specimens

> 6.5 but 7.6

■6.5 but < 7.6

•6.5but 76

•:^6.5

<6.5
<6.5
<6.5
<6.5
<6.5
65
7.6

7.6

9.5
■6.5but< 7.6
(9.5?) 10.8
10.8
7.6
7.6
7.6
7.6
7.6
7.6
7.6
7.6
7.6
7.6
9.5

8 1

9 5
7.6

10.8
10.8
7.6
9.5
9,5
9.5
9.5
7.6
7,6
7.6
7.6
7.6
9.5

Completely
fused

75.0-800
34.0-39.0

690

69.0

295

FISHERY BULLETIN: VOL. 78, NO. 2

rent spur (Johnson 1975) was not observed in
either species.

The caudal rays first developed in both species
from the midline between hypurals 2 and 3 in
preflexion larvae (Figure 17). Rays were added in
a posterior and anterior direction (Figure 18).
After complete notochord flexure the secondary
caudal rays were added in an anterior direction.
For equal-sized specimens from 6.5 mm NL to 19.5
mm SL, C. hippurus had fewer caudal fin rays
than C. equiselis (Table 9).

Fnfid

I-

0.5 mm

Figure 17. — Caudal complex of Coryphaena hippurus, 5.0 mm
NL. Symbols: Fnfld, finfold; Hs, haemal spine; Hy, hypural;
Nc, notochord; PCR, principal caudal ray; Ph, parhypural.
Stippled, cartilage; darkened, ossifying bones or rays.

Caudal Fin Supports

The caudal fin rays of Coryphaena spp. were
supported by some of the bones of the caudal com-
plex. Three posteriormost centra were involved in
this support. In 2 out of 97 C. equiselis the caudal
fin rays were also supported by a fourth centrum.
This variation was not observed in C. hippurus.

Supporting bones of the caudal complex con-
sisted of three centra (urostyle and preural centra
numbers 2 and 3), one neural spine, one special-
ized neural arch, two autogenous haemal spines,
one autogenous parhypural bone, five autogenous
hypural bones, two paired uroneural bones, and
two epural bones. These parts were seen during

0.5 mm

Figure 18. — Caudal complex of Coryphaena hippurus, 6.0 mm
NL. For explanation of symbols, see Figure 17. Stippled,
cartilage; darkened, ossifying bones or rays.

development, but not all the parts are readily
discerned in the adults due to ontogenetic fusion.

The species did not differ in the anatomy of the
caudal complex, but they differed in the size at
which parts appeared and ossified. The 6.5 mm NL
C. equiselis was at the same stage of caudal
development as a 6.5 mm NL C. hippurus. From
7.6 to 16 mm SL, C. equiselis was more advanced.
Specimens >16 mm SL of both species had the
caudal complex equally ossified for the same
lengths, but epural, uroneural, and hypural fu-
sions occurred at shorter lengths in C. equiselis.

Development of the caudal complex of C. hip-
purus is described here rather than C. equiselis
because small specimens were not available for
C. equiselis. Mostof the illustrations of the caudal
complex are of C. equiselis because they were
drawn before it was apparent that C. equiselis
< 7.6 mm were not available. Because both species
had identical caudal complex anatomy, no draw-
ings of C. hippurus' caudal complex were made for
specimens >7.6 mm SL.

At 5 mm NL, C. hippurus had a straight
notochord. Hypurals 1 to 3, the parhypural, and
the haemal spine of the future preural centrum 2
were present in cartilage and 2+3 principal
caudal rays were counted (Figure 17). At 6 mm
NL, hypural 4 and an additional cartilaginous
haemal spine of the future preural centrum 3 were
present (Figure 18). Notochord flexion in C. hip-

296

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

purus was between 7 mm NL and 7.5 mm SL, and
in C. equiselis between 6.5 mm NL and 7.6 mm SL
(Figure 19). During the flexion stage of some
C. hippurus the neural spine of preural cen-
trum 3, the speciaHzed neural arch of preural
centrum 2, and the two epurals began to develop
from cartilage (Figure 19). Hypural 5 was first
seen in cartilage at 8.1 mm SL. The two paired
uroneurals did not develop from cartilage — in
C. hippurus the larger, more ventrally and ante-

ognized only one epural for adult C. hippurus. In
Coryphaena spp., hypurals 1 and 2 and hypurals 3
and 4 fused to a dorsal and ventral hypural plate
(Figures 20-23, Table 10). During fusion paired
bony ventrolateral and dorsolateral articular pro-
jections formed on the ventral edge of hypural 3
and on the dorsal edge of hypural 2. These
projections became the articulatory surfaces be-
tween the dorsal and ventral hypural plates (Fig-
ures 20-23). The two hypural plates of Cory-

EpS-.— Un

Figure 19. — Supporting bones of the caudal complex of Coryphaena hippurus (right)
7.6 mm SL and C. equiselis (left) 7.6 mm SL. Symbols: Eps, epurals; Hs, haemal spine;
Hy, hypural; "Na", specialized neural arch; Ns, neural spine; Ph, parhypural; Pu, preural
centrum; Un, uroneural; Ur, urostyle. Stippled, cartilage; darkened, ossifying bones;
stippled darkened areas are cartilage just beginning to ossify.

riorly located pair was seen at 8-10.6 mm SL, and
the smaller, more dorsally and posteriorly located
pair was seen at 11.9 mm SL. Development of the
two paired uroneurals occurred at a smaller size in
C. equiselis (Figure 19 left. Table 10). The smaller
uroneural pair gradually fused to the outside of
the larger uroneural pair in both species. This
fusion was completed between 75 and 85 mm SL
for C. hippurus and between 75 and 80 mm SL
for C. equiselis (Table 10). Monod (1968) recog-
nized only one uroneural (stegural) pair in adult
C. hippurus.

Ossification of the cartilage bones in the caudal
complex of C hippurus began with the urostyle at
8 mm SL. Last to ossify at 14.6 mm SL were the two
epurals. The ossification sequence of all hypural
bones is shown in Table 10. The epurals of C.
hippurus developed and fused in the same manner
as those of C. equiselis, although development and
fusion were always at a smaller size for C. equi-
selis (Figures 19-23, Table 10). Monod (1968) rec-

Eps

0.5 mm

FIGURE 20.— Supporting bones of the caudal complex of Cory-
phaena equiselis, 11.0 mm SL. Symbols: Uns, uroneurals. For
explanation of other symbols, see Figure 19. Stippled, articular
cartilage; darkened, bone.

297

FISHERY BULLETIN: VOL. 78, NO. 2

scR

PCR

Figure 21. — Caudal complex of Coryphaena equiselis, 15.9 mm
SL. Symbols: PCR, principal caudal rays; SCR, secondary
caudal rays. Stippled, articular cartilage; darkened, bone.

autogenous (Figures 23, 24). These were two
haemal spines, a parhypural, a ventral and dorsal
hypural plate, hypural 5, a uroneural pair (fused
from two pairs), and an epural (fused from two).
Nonautogenous bones were the specialized neural
arch and one neural spine. The relationship of the
urostyle with the uroneural pair and hypural 5 is
shown in Figure 24. Articular cartilage was pres-
ent on all distal parts of the hypural complex
posterior to preural centrum 4 (Figure 22).

The parhypural and hypurals 1-5 supported the
principal caudal rays. The distribution of principal
caudal rays on the various hypural bones can only
be seen in larvae and smaller juveniles of both
species before hypural fusion (Table 11). There was
no difference in distribution of principal caudal
rays between the two species.

Uns

Hy3&4

Art

Hyi*2

Figure 22. — Supporting bones of the caudal complex of Coryphaena equiselis, 55.5 mm
SL. Symbols: Art, articular projection. For explanation of other symbols, see Figures
19, 20. Stippled, articular cartilage; darkened, bone.

phaena spp. remained autogenous in the adults,
but were closely articulated with the ventroposte-
rior edge of the urostyle.

During development of the hypural complex
bones a small hypurapophysis (Lundberg and
Baskin 1969) was observed on hypural 1 in both
species. It appeared before hypural fusion, but
could not be illustrated in the lateral view. Dis-
articulation of adult caudal skeletons of both
species of Coryphaena revealed the presence of the
hypurapophysis. The hypurapophysis articulated
with the urostyle just dorsad of the parhypur-
apophysis (Nursall 1963).

In the adults of Coryphaena spp., most bones of
the hypural complex were closely articulated, but

298

The anatomy and development of the caudal
complex of Coryphaena spp. had similarities and
dissimilarities with other fish. The hypurapophy-
sis observed in Coryphaena spp. was noted in such
fish as siluriform catfish (Lundberg and Baskin
1969) and adult sea bream, Archosargus rhom-
boidalis (Houde and Potthoff 1976). The hypura-
pophysis was not observed in the blackfin tuna,
Thunnus atlanticus (Potthoff 1975).

In the Coryphaenidae and other percoid fishes
such as Apogonidae (Fraser 1972), A. rhomboi-
dalis (Houde and Potthoff 1976), Carangidae ( Ahl-
strom and Ball 1954; Berry 1969), Haemulon
plumieri (Saksena and Richards 1975), and some
Scombridae (Conrad 1938; Mago Leccia 1958), the

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

Figure 23. — Caudal complex of a Coryphaena equiselis, 230 mm SL. For explanation of symbols,
see Figure 21. Stippled, articular cartilage; darkened, bone.

Table U. — Distribution of principal caudal rays on the hypurals in 136 Coryphaena
hippurus (8.0-53 mm SL) (C. h.) and 75 C. equiselis (7.0-52 mm SL) (C. e.).

Number of principal caudal

rays

1

2

3

4

5

Part

C.h.

C. a

C.h.

C. e.

C.h.

C. e

C.h.

C. e.

C. h. C. e.

Parhypural

51

24

85

51

Hypural 1

52

22

80

51

4 2

Hypural 2

39

32

97

43

Hypural 3

28

27

97

45

11

3

Hypural 4

6

72

36

58 39

Hypural 5

37

16

98

58

1

1

epurals were autogenous. In part of the Scom-
bridae (Fierstine and Walters 1968; Monod 1968;
Patterson 1968; Collette and Chao 1975; Potthoff
1975) the anteriormost epural is secondarily fused
to the specialized neural arch of preural centrum
2. Based on the epurals, Coryphaena spp. is
advanced because epural numbers are reduced
from 3 to 2 and fused to 1 (Patterson 1968;
Fraser 1972).

The haemal spines of preural centrum 2 and 3
were autogenous in Coryphaena spp. This state is
considered basic because advanced percoids have
these spines secondarily fused to the centra ( Fraser
1972). Fusion of these haemal spines occurs in
T. atlanticus (Potthoff 1975), and some apogonids
(Fraser 1972).

The two prezygapophyses of the urostyle (Fig-
ure 24) oi Coryphaena spp. are true prezygapophy-
ses; whereas in T. atlanticus and other Thunnini
and Sardini (Collette and Chao 1975; Potthoff
1975) the prezygapophyses of the urostyle repre-
sent the pair of uroneurals which have fused to the
urostyle during development.

Articular cartilage was present in Coryphaena
spp. on the caudal complex on all parts distally
inclusive of preural centrum 3. No articular car-
tilage was observed anterior to this centrum.
Articular cartilage was observed in scombrids by
Fierstine and Walters (1968), in T. atlanticus
by Potthoff (1975), and in A. rhomboidalis by
Houde and Potthoff (1975). The absence of artic-
ular cartilage in the caudal complex drawings of

299

FISHERY BULLETIN: VOL. 78, NO. 2

5 mm

FIGURE 24.— Urostyle of a Coryphaena equiselis, 330 mm SL,
with disarticulated uroneurals and hypural 5. Dashed lines with
arrows point towards place of articulation. Symbols: AStr,
anterior strut of urostyle; Hy, hypural; Pr, prezygapophysis;
PStr, posterior strut of urostyle; Uns, uroneurals; Ur, urostyle.
The articular cartilage is not shown on hypural 5 because of the
boiling and drying method of preparation.

apogonids (Fraser 1972) is probably an oversight
by the author since he used cleared and stained
material. The lack of articular cartilage in most
of the drawings of caudal complexes by Monod
(1968) can probably be attributed to the method
of skeletal preparation, e.g., boiling and subse-
quent drying.

300

Autogenous dorsal and ventral hypural plates
were observed in adult Coryphaena spp. The
fusion of individual hypural bones was considered
advanced by Fraser (1972). Even more advanced is
the fusion of all hypural bones to one hypural plate
and the fusion of this plate to the urostyle as
in scombrids (Fierstine and Walters 1968; Pott-
hoffl975).

The formation of articulatory projections of
membranous origin during ontogeny at the mid-
line of the caudal complex between the dorsal and
ventral hypural plates was observed in Cory-
phaena spp. (Figures 20-22) as well as in Scom-
brolabrax heterolepis (Potthoff et al. 1980), but
not in T. atlanticus (Potthoff 1975).

Both species of Coryphaena had two pairs of
uroneurals. The smaller posterior pair gradually
moved anteriorly during development and fused
to the outsides of the larger anterior pair, until
only one pair could be recognized in adults. Fraser
(1972) contended that the loss of the posterior
pair of uroneurals constituted an evolutionary
advance. He did not completely rule out fusion,
although he had no evidence for it. There are
fishes such as the scombrids which only develop
one pair of uroneurals (Potthoff 1975). Loss or
fusion of uroneurals can be ascertained through
the examination of developmental series.

Pectoral Fin and Supports

The following description is based upon juve-
niles > 13 mm SL of both Coryphaena species with
adult counts of 19-21 rays. These counts were
obtained between 19 and 13 mm SL in C. equiselis
and between 11 and 13 mm SL in C. hippurus.
Individual differences in counts between the left
and right pectoral fins were lower in both species
of Coryphaena than in four species of Thunnus
(Potthoff 1974). Only 1% of 171 Coryphaena spp.
examined with adult counts >13 mm SL differed
by 2 rays between each side, 18% differed by 1 ray,
and 81% had the same count on both sides. The
pectoral fin rays were directly and indirectly
supported on each side by a number of bones which
composed the pectoral girdle and its suspensorium.
On each side the pectoral girdle consisted of a
scapula (which supported the first fin ray directly),
four radials ( which supported the remainder of the
rays directly), a coracoid, and a cleithrum. The
scapula and coracoid were connected by cartilage.
The suspensorium consisted of seven bones. The
supracleithrum and posttemporal were attached

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

in a row from the outside of the posterior plate
of the cleithrum to the rear of the skull and
postcleithra 1 and 2 extended over the abdominal
area from the inside of the posterior process of
the cleithrum. The supratemporal and two inter-
temporals, which belong with the posttemporal to
the laterosensory canal (Harrington 1955), orig-
inated just anterior to the posttemporal and ended
just short of the supraoccipital crest. Except for
individual variation there was no specific differ-
ence in the shape of bones of the girdle and
suspensorium between the two species. The rela-
tionship of bones of the pectoral girdle, suspen-
sorium, and pelvic basipterygium to each other is
showm in Figure 25.

Formation of the pectoral fin rays started in the
dorsal border of the larval pectoral blade (Figure
26) and continued ventrad (Figure 27). For equal-
sized specimens from 6.5 to 13 mm SL, C. equiselis

PstCI2

Pelv

h

1.0 mm

H

Figure 25. — Lateral external view of left sides of pectoral
girdle and suspensorium from a 20.8 mm SL Coryphaena
hippurus. Symbols: CI, cleithrum; Cor, coracoid; P, posterior
process of the coraco-scapular cartilage; Pelv, pelvic basi-
pterygium; PstCl 1, postcleithrum 1; PstCl 2, postcleithrum 2;
Ft, posttemporal; R, radial; SCI, supracleithrum; St, supra-
temporal (beginning to develop). Stippled, cartilage; dark-
ened, bone.

had more pectoral fin rays than C. hippurus
(Figure 28). Of 86 individuals of both species with
developing fins <13 mm SL, 5% differed by 2 rays
between the left and right sides, 43% differed by 1
ray between the sides, and 52% had the same
count on both sides.

The two species differed in length at which
development of the pectoral girdle occurred but
not in its structure (Table 12). The 6.5 mm NL
C. equiselis had the same pectoral girdle de-
velopment as a 6.5 mm NL C. hippurus. For
individuals of equal length between 7.6 and 18 mm
SL, C. equiselis was more advanced. At lengths
>18 mm SL specimens of both species had the
pectoral girdle equally developed except for the
supratemporal-intertemporal bones which were
first seen at 13 mm SL in C. equiselis and at 18 mm
SL in C. hippurus.

Regarding development of the pectoral girdle in
C. hippurus, the smallest (5 mm NL) specimen
had a simple rod-shaped, bony cleithrum, and a
coraco-scapular cartilage (Figure 26). The car-

I-

0.5 mm

Figure 26. — Lateral external view of left side of pectoral girdle
from a 5.0 mm NL Coryphaena hippurus. Symbols: A, anterior
process of the coraco-scapular cartilage; Bl, blade of the larval
pectoral fin with two fin rays developing dorsally; CI, cleithrum;
D, dorsal process of the coraco-scapular cartilage; P, posterior
process of the coraco-scapular cartilage. Stippled, cartilage;
darkened, bone.

301

FISHERY BULLETIN: VOL. 78, NO. 2

Itnm

-I

Figure 27. — Lateral external view of left side of pectoral girdle
from a 8.1 mm SL Coryphaena hippurus (left) and a 7.9 mm SL
C. equiselis (right). Symbols: ScF, scapular foramen. For
explanation of other symbols, see Figures 25, 26. Stippled,
cartilage; darkened, bone.

tilage consisted of a long dorsal process, a long
posterior process, and a short anterior process.
Houde and Potthoff (1976) found that the anterior
process of the coraco-scapular cartilage formed
after the formation of the dorsal and posterior
processes in labor atory -reared A rcAosar^ws rhom-
boidalis larvae. I believe that both species of
Coryphaena have the same kind of cartilage
development as A. rhomboidalis. At 5.5 mm NL,
C. hippurus first developed the supracleithrum,
and after 6.3 mm NL, it was always present. The
supracleithrum at first was a small rod-shaped
bone, which only gradually acquired its flattened
paddlelike shape. The cleithrum and the coraco-
scapular cartilage did not show any development

between 5 and 7.3 mm NL. The posttemporal first
developed as a small, rod-shaped bone at 6.3 mm
NL. In larvae of 7.4 mm SL the scapular foramen
was first seen in the dorsal process of the coraco-
scapular cartilage, and at 7.6 mm SL the posterior
process of the cleithrum first appeared (Figure
27). Between 7.6 and 8.4 mm SL many develop-
mental changes occurred. In an 8 mm SL specimen
the first dorsalmost radial was seen in cartilage;
the radial was absent in an 8.1 mm SL specimen
(Figure 27), but present again at 8.3 mm SL. The
bony rod-shaped postcleithrum 2 was first seen at
8.3 mm SL. Ossification of the coraco-scapular
cartilage started at 8.1 mm SL in the region of the
future coracoid at the juncture of the dorsal and
anterior processes. The scapula started to ossify
first around the scapular foramen at 9.5 mm SL.
Also at 9.5 mm SL the postcleithrum 1 was first
seen as a tiny speck of bone, but not until 11.9 mm
SL was this structure easy to see. All four radials
were present at 11.9 mm SL; the dorsalmost was
starting to ossify and the following three were
in cartilage. All radials in C. hippurus were
ossifying by 12.3 mm SL (Figure 29). The supra-
temporal was first seen at 18 mm SL as a single
lateral line pore situated anterior to the post-
temporal (Figure 25). Its development was diffi-
cult to trace because the adult bone was very thin,
but distinctive because it was traversed by a
lateral line canal. With increasing size more pores
appeared, some at a distance dorsad for the two
intertemporal and others adjacent to the first
pore for the supratemporal. These pores even-
tually joined to form two tubular canal bones,
the intertemporals and the thin supratemporal.
Further development of the bones in the pectoral
girdle and suspensorium of C. hippurus past
12.3 mm SL (when all component bones are ossi-

TABLE 12. — Development of structures, bones and fin rays of the pelvic and pectoral girdles for the two species of Coryphaena, shown
for lengths (in millimeters NL or SL) at which structures, bones or fin rays first appear in cartilage or ossify. Lengths given signify a
first observance and do not necessarily apply to all specimens of that length or longer.

First evidence of ossification

First appearance

in cartilage

(Stain uptake)

Part

C. hippurus

C. equiselis

C. hippurus

C. equiselis

Cleithrum

_

_

not known

not known

Scapula

not known

not known

9.5

7.0

Scapular foramen

7.4

7.0

—

—

Coracoid

not known

not known

8 1

7,0

Radials 1-4

80-11.9

8.0-89

11,9-12.3

8.8- 9,8

Posttemporal

6.3

not known

Supracleithrum

.

5,5

not known

Postcleithrum 1

9,5

8.9

Postcleithrum 2

_

8,3

7,4

Supratemporal-intertemporals

18.0

13.0

Pectoral fin rays

5,0

not known

Pelvic baslpterygium

7.0

(6.0?) 7.0

87

8.7

Pelvic fin rays

—

—

7.0

7.3

302

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

21
20
19
18
17
16
15
14
13
12
11
lOh

uj 9

(/}

8
7
6
5
4
3
2
1

«

5 12

12

2 11

« 7

4 726 48

t 5 t 9 1 1

1

8

\

0

1

Til

1

C. equiselis -^
C. hippurus ^

8 9 10 11 12

LENGTH, mm NL or SL

13

14

>14

Figure 28. — Number of left pectoral fin rays in relation to length in 164 Coryphaena equiselis (6.5-230 mm NL or SL) and 123

C. hippurus (5-172 mm NL or SL). For explanation of symbols, see Figure 1.

fying, except the supratemporal-intertemporals)
consisted of ossification and growth of the bones,
and the formation of bony shelves on the clei-
thrum, coracoid, posttemporal, and postcleithrum
1 (Figures 29, 30). The supratemporal developed
thin membranous bones around the lateral line
canal tubes. Development also involved loss of
cartilage. The cartilage separating the sc.apula
and coracoid became narrower with increasing
length (Figures 29, 30). The cartilage from the
prominent larval posterior process of the coracoid
completely disappeared by 40 mm SL (Figure 30).

No developmental studies of the pectoral fin and
supports have been done for Coryphaena spp.
Starks (1930) studied the anatomy of the pectoral
girdle in a variety of adult bony fishes including C.
hippurus. The development of the coraco-scapular
cartilage to a scapula and a coracoid bone and
some or total atrophy of the cartilaginous poste-
rior process of the coracoid occurs in most fishes
(Swinnerton 1905; Starks 1930). More recently
Houde and Potthoff (1976) observed the atrophy of
the posterior process in A. rhomboidalis and
Saksena and Richards ( 1975 ) reported the presence

303

FISHERY BULLETIN: VOL. 78, NO, 2

1mm

A

I , _

Figure 29. — Lateral external view of left side of pectoral girdle from a 12.3 mm SL Coryphaena hippurus (left) and a 10.3 mm SL
C. equiselis (right). Symbols: CI, cleithrum; Cor, coracoid; P, posterior process of the coraco-scapular cartilage; PCI, posterior process
of the cleithrum; R, radial; Sc, scapula. Stippled, cartilage; darkened, bone.

of a Y-shaped cartilaginous coracoid (probably
coraco-scapular cartilage) in Haemulon plumieri
larvae. In the Blenniidae, Characidae, and Pho-
lidichthyidae, a small posterior process of the
coracoid was observed in adults (Weitzman 1962;
Springer 1968; Springer and Freihofer 1976). For
the family Gobiesocidae, however, Springer and
Fraser (1976) reported large posterior processes of
the coracoid. Thus, it seems that the posterior
process of the coracoid is present in most fishes,
but that it disappears during development in more
advanced forms. It also appears that this process
remains as a neotenic structure in small fishes.

In more primitive fishes such as the Osteoglos-
sidae (Greenwood and Thomson 1960), Charac-
idae (Weitzman 1962), most stomiatoid families
(Weitzman 1974), and Lile piquitinga (Clupeidae)
(Gomez Gaspar 1976) a mesocoracoid was present.
This bone is absent in the Coryphaenidae.

The presence of intertemporals is considered
primitive because these bones are absent in more
advanced groups, such as scombrids (Collette and
Chao 1975).

Pelvic Fin and Fin Supports

Description is based on large juveniles of both
species > 90 mm SL, two adults of C. equiselis and
two adults of C. hippurus. There were 1,5 rays in
each of the pelvic fins which were located on the
underside of the body below the pectoral fin. All
C hippurus >10.7 mm SL and all C. equiselis
>8.6 mm SL had the full count. Each side of the
pelvic fin was supported by a basipterygium; no
radials were present. The two basipterygia were
closely approximated medially, but not fused (Fig-
ure 31). They were located in the abdominal body
wall and were lying between the ventral portions

304

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

H

Imtn

•\

Figure 30. — Lateral external view of left side of pectoral girdle from a 47.6 mm SL Coryphaena hippurus (left) and a 48 mm SL
C equiselis (right). For explanation of sjrmbols, see Figure 29. Stippled, cartilage; darkened, bone.

of the two cleithra and coracoids (Figure 25). No
fleshy interpelvic processes were present between
the bases of the fins.

The basipterygium is a complex bone. For con-
venience of description, it was divided into three
parts which corresponded to the ontogeny of the
bone: the central part, which was the original
cartilage, the wings (Kishinouye 1923) of mem-
branous bone origin, and the two xiphoid processes
(de Sylva 1955), of which the posterior process was
of cartilage origin and the anterior process of bone

origin. The central part of the basipterygium
carried the four wings along its length (Figures
31-33). Anteriorly the central part was tipped by a
small piece of cartilage. Posteriorly the central
part served the articulation of the fin rays. A thin
layer of articular cartilage was present in adults
on the posteriormost portion of the central part
(Figures 31, 32). Each basipterygium had four
wings, reminiscent of the two sagittal and two
lateral keels of pterygiophores. The wings formed
a dorsal and a ventral "V" shaped groove, and a

305

FISHERY BULLETIN: VOL. 78, NO. 2

^i'l MB' 1 ■! ^

Figure 31. — Pelvic fin and basipterygia from a 449 mm SL Coryphaena hippurus.
Left: ventral external view; right: dorsal internal view. Left pelvic fin has been
removed. Symbols: AX, anterior xiphoid process; CP, central part; EDW, external
dorsolateral wing; EVW, external ventrolateral wing; IW, internal dorsolateral wing;
PX, posterior xiphoid process; VW, ventral wing. Stippled, cartilage; darkened, bone.

lateral "[" shaped channel (Figure 33). Thexiphoid
processes were located internally at the midline
on the basipterygia (Figures 31-33). The anterior
xiphoid process was an anteroventral extension of
the posterior xiphoid process (Figure 32). The
posterior xiphoid process, which pointed in a
posterodorsal direction was attached to the poste-
rior part of the basipterygium by a heavy bony
strut from the central part and anteriorly by the
internal dorsolateral wing (Figures 32, 33). The
two basipterygia were closely approximated at the
edges of the two internal dorsolateral wings and
the internal surfaces of the four xiphoid processes

(Figure 31). The closest approximation was ob-
served on the xiphoid processes at the place where
the anterior and posterior processes were joined
(Figure 32). Here the bone was rough with minute
projections. These projections gave a close fit when
the surfaces were brought together and prevented
the basipterygia from sliding.

No anatomical differences in the development of
the pelvic fin and supports were found between
C. hippurus and C. equiselis. Larval and juvenile
specimens of C. equiselis were more advanced in
pelvic development than equal-sized specimens of
C. hippurus (Table 13; Figures 34, 35). In both

306

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

Figure 32. — Lateral internal view of left basipterygium from a 449 mm SL, ^orypnaena
hippurus. For explanation of symbols, see Figure 31. Stippled, cartilage; darkened, bone.

Figure 33. — Posterior view of left basipterygium after left
pelvic fin had been removed from a 449 mm SL Coryphaena
hippurus. For explanation of symbols, see Figure 31.

species a fin bud developed first on the abdomen
(Table 13). Simultaneously to the fin bud appear-
ance, two cartilaginous basipterygia developed
internally at 7 mm SL in flexion larvae of C
hippurus. In C. equiselis it probably occurred in
flexion larvae betw^een 6 and 7 mm SL, but the
smallest available specimen measured 7 mm SL
(Table 12). The pelvic fin rays developed in the
fin bud after basipterygium formation. Fin ray
appearance was from the outside of the specimen
towards its midline in both species, so that the
first ray to appear was the spinous ray. In C.
hippurus the pelvic fin ray development began at
7-7.5 mm SL and was completed at 10.7 mm SL,
and in C. equiselis it began at 7.3 mm SL and was
completed at 8.6 mm SL.

Each cartilaginous basipterygium in both spe-
cies was cylindrical with its base expanded poste-
riorly near the fin bud (Figure 34). The cartilag-
inous projection of the posterior xiphoid process
developed posteriorly at the inner corner of the
expanded base (Figure 34). Ossification of the
basipterygium cartilage to the central part began
in both species at the center and progressed
anteriorly and posteriorly as the larvae grew
(Figure 34). For C. hippurus it began at 8.7-10.8
mm SL, and for C. equiselis at 8.7 mm SL (Tables
12, 13). After the cartilaginous central part of the
basipterygium had ossified, all structures of mem-
branous origin developed simultaneously; these
were the anterior xiphoid process and the four
wings (Figure 34). All wings developed from
the base in an anterior direction. The posterior
xiphoid process was of cartilage origin and started

307

FISHERY BULLETIN: VOL. 78, NO. 2

0.5 mm

\i

E

io\

EVW

Figure 34. — Development of left basipterygium of Coryphaena spp. Basipterygium of C. hippurus is to left of
letters, that of C. equiselis is to right. Lengths: A, 8.3 and 8.9 mm SL; B, 10.3 and 10.1 mm SL; C, both 11.3 mm SL;
D, 14.1 and 14,2 mm SL; E, 21 and 20.9 mm SL. For explanation of symbols, see Figure 31. Stippled, cartilage;
darkened, bone.

308

POTTHOFF: DEVELOPMENT AND STRUCTURE OF FINS IN CORYPHAENA

5-

= 3

6 10

II

6

\ \

2 3

I

C.equiselis -^
C.hippurus -3-

11

12

LENCTH.mmNLorSL

Figure 35. — Number of pelvic fin rays in relation to length in 15 Coryphaena equiselis
(7.0-12.4 mm SL) and 52 C. hippurus (6.0-12.5 mm NL or SL). For explanation of
symbols, see Figure 1.

Table 13. — Development of pelvic fin and supports in 52 Coryphaena hippurus (6.0 mm NL-12.5 mm SL) (C h.) and 15 C. equiselis
(7.0-12.4 mm SL) (C . e.). Numbers denote number of specimens, dashes denote specimens not available.

5.6- 6.5
6.6- 7.5
7.6- 8 5
8.6- 9.5
96-105
10,6-11.5
11.6-12.5

Fin bud

Fin rays

Baslpterygia

Length
mmNLor SL

Absent Present

Absent Present

Absent

Cartilaginous
C. h. 0. e.

Ossifying

C. h. C. e. C. h. C. e.

C. h. C. e. C. l7. C. e.

C. h. C. e.

C. h. C. e.

0
11

4
10
8
6
3

4
12
0
0
0
0
0

0
5
4
10
8
6
3

4
10
0
0
0
0
0

to ossify shortly after the appearance of the
anterior xiphoid process (Figure 34).

A comparison of pelvic bones of Coryphaena spp.
with those of more primitive fishes revealed the
absence of radials in Coryphaena spp. It is not
known if the radials have been lost, or if they have
fused to the central part and the articular car-
tilage during evolution. In the more primitive
stomiatoid fish families (Weitzman 1974) and in
Lile piquitinga (Gomez Gaspar 1976), radials are
present between the bases of the fin rays.

DISCUSSION

In a tentative classification of the Perciformes,
Greenwood et al. (1966) placed the Coryphaen-
idae to follow the family Carangidae. This place-
ment was arbitrary because Coryphaena spp. is

more advanced than some families that follow in
the placement.

The one continuous dorsal fin of Coryphaena
spp. extends to the head, so that the first inter-
neural space, bounded by the head bones and the
first neural spine, is occupied by pterygiophores
which support the fin rays. Smith and Bailey
( 1961) contended that the dorsal fin of Coryphaena
spp. represents an evolutionary advance and spe-
cialization because of its anterior extension and
the loss or reoccupation by fin rays of the predorsal
bones. In diverse fishes, such as characins, sparids,
carangids, scombrids, and lutjanids, the pterygio-
phores in the posterior parts of the dorsal and anal
fins have three parts. This triserial pterygiophore
structure is considered basic (Eaton 1945; Lindsey
1955; Johnson 1978). Most pterygiophores in Cory-
phaena spp. are biserial, and one or two anterior-
most ones uniserial. Thus, the pterygiophores of

309

FISHERY BULLETIN: VOL. 78, NO. 2

Coryphaena spp. are more advanced or specialized
due to either a loss or fusion of the middle radial.
The loss of the "stay" for the posteriormost dorsal
and anal pterygiophore also represents an ad-
vance. Therefore, based on the dorsal and anal
fin and supports, placement of Coryphaena spp.
should be phylogenetically higher than that given
by Greenwood et al. (1966).

The vertebral number is higher for C. equiselis
than for C. hippurus (Jordan and Evermann 1896;
Collette et al. 1969), yet C. equiselis has fewer
dorsal fin rays than C. hippurus. Coryphaena
equiselis also tends to have fewer anal fin rays
than C. hippurus. Therefore, since fin ray num-
ber is approximately equal to the pterygiophore
number, C. equiselis has fewer dorsal pterygio-
phores arranged in more interneural spaces, and
C. hippurus has more dorsal pterygiophores ar-
ranged in fewer interneural spaces. The situation
is similar for the anal fin. It is noteworthy that the
same number of vertebrae is found in both species
posteriorly to the end of the dorsal and anal
fins (Figure 3). The evolutionary significance of
the relationship between vertebral numbers and
pterygiophore numbers is not understood (Lind-
sey 1955), but may be phylogenetically important.

During development, except for the presence of
two rather than three epurals, Coryphaena spp.
have the basic (unreduced) perciform caudal skel-
eton (Gosline 1961a; Monod 1968; Patterson 1968;
Fraser 1972). Adults of Coryphaena spp., how-
ever, have a more advanced caudal skeleton. The
presence of a single epural and uroneural, as well
as a dorsal and ventral hypural plate, shows
advance over the basic type, although the fused
parts remain autogenous. In the modified and
advanced caudal complex of most Scombridae
these parts may be fused to the centra. For
example, the epural may be fused to the special-
ized neural arch, the uroneurals and hypural
plates may be fused to the urostyle, the parhypural
and the hypural plate may be fused to the urostyle,
and two haemal spines may be fused to preural
centra 2 and 3.

The pectoral skeletons of Coryphaena spp. are of
the basic perciform type. The pectoral supports fit
the description of Greenwood et al. (1966) for the
Acanthopterygii. The presence of supratemporal-
intertemporal bones and two postcleithra in Cory-
phaena spp. characterize them as a basic per-
ciform pectoral support system. Some fishes
may lose some or all supratemporal-intertemporal
bones (Scombridae) and some also may lose

a postcleithrum (Gymnapogon, Apogonidae,
Fraser 1972; Xiphias gladius, author's personal
observation).

The pelvic fin and supports are of the acantho-
pterygian (perciform) type, one bone supporting
an unbranched and five branched rays in a thorac-
ic position. The development and structure of
the pelvic basipterygium is similar to that of a
pterygiophore. The central part and wings of the
basipterygium closely resemble proximal radials
with sagittal and lateral keels.

ACKNOWLEDGMENTS

I wish to thank William J. Richards, Francis
Williams, and Gilbert L. Voss for critical com-
ments on the manuscript. Special thanks are due
to Edward D. Houde for help with statistics and for
a most thorough review of the manuscript. I thank
Elbert H. Ahlstrom for reading the manuscript
and for his comments, especially for those on the
caudal complex.

I thank the persons that supplied me with
specimens: Elbert H. Ahlstrom, Bruce B. Collette,
Edward D. Houde, William J. Richards, C. Richard
Robins, Frederick H. Berry, and George C. Miller.

For tjqjing numerous drafts of the manuscript,
I am grateful to Phyllis Fisher, and for proofread-
ing numerous drafts I thank Teresa Ratajczak and
Kelly Clark. I also thank Grady Reinert, Annalee
Green, and Joaquin Javech for inking the caudal
complex drawings and for labeling all the draw-
ings in the manuscript; Andrew J. Ramsay, Jr. for
the photographic work; Mai M. Brassfield and
Scott Quaas with the clearing and staining of the
study specimens; and Bruce B. Collette and Frank
J. Mather III for providing some original data
on Coryphaena spp.

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312

LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA (CRUSTACEA:

EUPHAUSIACEA) WITH NOTES ON ITS VERTICAL DISTRIBUTION

AND MORPHOLOGICAL DIVERGENCE BETWEEN POPULATIONS

Margaret D. Knight^

ABSTRACT

Larval development of Euphausia eximia includes the following stages: nauplius I-II, metanauplius,
calyptopis I-III, and furcilia I- VI. The larvae are similar to those of congener £. gibboides but differ in
both morphological detail and timing of developmental events.

A comparison of larvae of £. eximia from across the species' range showed significant differences in
morphology between forms from the California Current terminus off Baja California and from the
South Equatorial and Peru Currents. This variation may be evidence of genetic divergence between
populations and perhaps indicates that the oxygen-deficient warm waters of the eastern tropical Pacific
form an effective barrier between reproductive centers of the species. Significant differences in mor-
phology were found as well during a preliminary survey of adults; the southern limit of the northern
form of E. eximia was about latitude 2° north.

The vertical distribution of larval stages in day and night samples from two locations off Baja
California and one in the South Equatorial Current showed development of diurnal vertical migration
in the second half of the furcilia phase after acquisition of the full complement of setose abdominal
pleopods. A "reverse" migration pattern was seen among calyptopes at two stations with the majority of
larvae occurring in the surface stratum during the day and below the surface layer at night; larvae at
the third station were found, both day and night, in the surface stratum until the onset of vertical
migration. Variation in growth rate between areas within the range of each population may be
correlated with relative abundance of food and duration of stay in food-rich surface waters.

Euphausia eximia Hansen is endemic to the east-
ern tropical Pacific, ranging from lat. 32°-34° N to
30° S and with areas of relative abundance in
waters of the California Current terminus off Baja
California and the Gulf of California, in the South
Equatorial Current, and in the Peru Current
(Brinton 1962; Antezana-Jerez 1978). In a recent
study of the horizontal and vertical distribution of
euphausiids along a transect from ca. lat. 23° N,
long. 115° W to lat. 3° S, long. 88° W, Brinton
(1979) observed that E. eximia occurred sparsely
between lat. 11° and 20° N but achieved high den-
sities in the productive zones marginal to the
oxygen-deficient portion of the eastern tropical
Pacific. He noted that "Reproduction, as deter-
mined by presence of larvae, was not observed
between 2° and 20° N; occurrences of juvenile and
adult £. eximia in this zone, therefore, appear due
to meridional advection from the northern (21° to
25° N) and equatorial population centers." This
agreed with earlier observations o{ E. eximia in
these areas (Brinton 1962).

'Scripps Institution of Oceanography, University of Califor-
nia, La Jolla, CA 92093.

Within the genus Euphausia, E. eximia is most
closely related in adult morphology to E.
americana, an Atlantic species, and to E. krohnii,
found in both the Atlantic and Mediterranean
(Mauchline and Fisher 1969). The larvae of E.
krohnii have been described (Frost 1934;
Casanova 1974) but those of E. americana have
not yet been identified. The literature on larval
development within the Euphausiacea has been
reviewed by Gopalakrishnan (1973).

The purpose of this paper is to describe the lar-
val development of £■. eximia in the reproductive
area of the California Current terminus popula-
tion, to note the differences observed in morphol-
ogy of larvae from the South Equatorial-Peru Cur-
rent population and apparent variation within
each population in rate of growth, and to provide
information on the vertical distribution of larval
stages.

METHODS

Larvae ofE. eximia were sorted from preserved
samples of plankton taken in the eastern Pacific
(Figure 1) during Scripps Institution of Oceanog-

Manuscript accepted December 1979.
FISHERY BULLETIN: VOL. 78, NO. 2, 1980.

313

^

FISHERY BULLETIN; VOL. 78, NO. 2

Figure l. — Occurrence of northern
and southern forms of Euphausia
eximia in plankton samples from the
eastern Pacific Ocean; Krill Expedition
station numbers locate samples in
which vertical distribution and growth
of larvae were studied.

0 V\A * larvae

6 (J)^\ Gulf of California

—

10 (A^ \

\rj

—

northern fornn ^""~^-i I

0 K^

Z7^

0

s

0

/ -

0 South Equatorial 21 ® O
Current '^^ , ^

0

c

southern form

-0 \

1604^

PACIFIC OCEAN
1 1 1 1

1520®!
1 1

30'

20'

- 10'

- 0°

10°

20°

120°

110°

100°

90°

80°

raphy Expeditions Krill, Aries, and Muddauber,
and CalCOFI Cruise 5804. They were identified
from an area off western Baja California in which
E. eximia is consistently abundant and where
closely related species {E. mutica and£'. recurva),
whose larvae we have identified, are rarely, if
ever, present (Brinton 1967). At three locations
(Stations 6, 10, and 21) larvae were counted as
well in separate day and night series of tows taken
across eight strata above 500 m on Krill Expedi-
tion (Brinton 1979) to investigate patterns of ver-
tical distribution.

Larvae from each sample were grouped by size,
information from length-frequency histograms,
and degree of morphological differentiation into
developmental stages which, to furcilia IV, were
discrete and assumed to be separated by one molt.
Furcilia V-VI and juvenile I were also presumed to
be one intermolt although individual variation in
growth and morphogenesis made boundaries less
distinct. Altogether 2,210 individuals were mea-

sured and 347 dissected for study of appendages.
Measurements were made with an ocular mi-
crometer; the method was the same as that used in
studies of species of the E. gibboides group
(Knight 1975, 1978). In the comparison of growth
rate between areas within each population larvae
from Stations 1520 and 1604 were treated as one
sample. Larvae were dissected in glycerine and at
least 10 specimens of each stage were examined in
detail . In the description of larval stages, the usual
setation or condition noted is given in parentheses
following the range observed. Drawings were pre-
pared with the drawing attachment of a Wild M20
Microscope.^

The nomenclature used to describe larval mor-
phology was modified from the studies cited above
with respect to the mandible. It appears appro-
priate to refer to the dentate process near incisor

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

314

KNIGHT; LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA

teeth of the right mandible as the lacinia mobilis
(Weigmann-Haass 1977; Hessler^). In species of
Euphausia I have examined in detail (E. gib-
boides, E. sanzoi, E. fallax, E. pacifica), in
Nematoscelis difficilis (Gopalakrishnan 1973),
and Nyctiphanes couchii (Le Roux 1976), the
lacinia mobilis appeared only on the right mandi-
ble; it was found on the left mandible of fi. hanseni
by Weigmann-Haass ( 1977). Leg 1 is referred to as
maxilliped through the furcilia phase.

Adults were sorted from a set of samples (Figure
1) for preliminary exploration of morphological
differences between populations ofE. eximia. The
animals were sexed, measured to the nearest mil-
limeter, and the armature of telson and inner pro-
cess of segment 2 of antennular peduncle were
inspected.

Gravid females o( E. eximia, captured in night-
time plankton tows with aim net from 200 m to
the surface near Santa Catalina Island, were cul-
tured aboard ship using the methods described by
Lasker and Theilacker (1965). Larvae hatched
from eggs spawned by one of the females were held
through calyptopis I to confirm identification of
early larval stages.

RESULTS

Observations of Reared Animals

Two gravid females spawned on the night of
capture; they were 25.7 and 26.6 mm total length
(TL) and shed 154 and 196 eggs. Their ovaries
were blue before spawning and the embryos of the
newly laid eggs were pale blue; the color faded
before hatch. Of 154 eggs allowed to develop, 90%
hatched and, at 17°-19° C room temperature, the
duration of early larval stages was approximately
as follows: 24 h for the egg; 24 h for nauplius I and
II together; 48 h for the metanauplius. The first
calyptopis appeared on the fourth day after spawn.
These stages encounter similar temperatures in
the surface waters off Baja California.

The spent female molted 6 days after spawning
without shedding more eggs; a spermatophore was
not found on the preserved female or her exuvia.
Three other ovigerous females survived capture
and molted twice, with 4 days between molts,
without spav^ming; each shed a spermatophore

with the exuvia during the first molt and the
ovaries remained blue.

Description of Larval Stages

Larval development in the California Current
population (northern form) of^ Euphausia eximia
included the following stages: nauplius I and II;
metanauplius; calyptopis phase, three stages; fur-
cilia phase, six stages. The stage which followed
furcilia VI usually (in 92% of 53 individuals) had
the adult number of spines on the telson (one ter-
minal and two pairs posterolateral) and is referred
to here as juvenile I. The observed furcilia stages
are listed in Table 1 along with the development of
pleopods, telson, and antenna. Measurements of
the calyptopis, furcilia, and juvenile stages are
given in Tables 2 and 3.

Table l. — Development of pleopods, telson spines, and an-
tenna in furcilia I- VI and juvenile I in the northern and south-
em forms of Euphausia eximia; ' = pair nonsetose pleopods, " =
pair setose pleopods.

Pleopod
develop-

Telson spines
Ter- Postero-

Form of

Number of larvae

Northern

Southern

Stage

ment

minal

lateral

antenna

form

form

Furcilia 1

f

7

3

Natatory

151

72

Furcilia II

1"4

7

3

Natatory

132

80

Furcilia III

5"

7

3

Natatory

334

104

6

3

0

9

5

3

1

4

4

3

0

3

3

3

1

5

Furcilia IV

5'

6

3

Juvenile

2

0

5

3

8

0

4

3

16

0

3

3

128

2

2

3
3

85

192

5

57

Furcilia V

5"

3
2

Juvenile

195
0

45

1

FurcihaVI

5"

3
2

Juvenile

40
19

42
25

Juvenile 1

5"

3
2

Juvenile

4
49

0
47

Table 2. — Measurements (millimeters) of metanauplius and
calyptopis I-III in the northern form of Euphausia eximia.

'Robert R. Hessler, Professor of Oceanography, Scripps In-
stitution of Oceanography, Univ. Calif., La Jolla, CA 92037,
pers. commun. July 1978.

stage

Total
length

Carapace
length

Carapace
width

Telson
width

Metanauplius, n

= 123:

Range

0.46-0.51

—

0.33-0.39

—

Mean

0.49

0.35

SD

0.01

0.01

Calyptopis l.n =
Range

127;
0,97-1.09

0.59-0.67

0.36-0.44

0.158-0.186

Mean

1,03

0,62

0.40

0.170

SD

0,02

0.02

0.01

0.006

Calyptopis II, n =
Range

= 140:
1,58-1,76

0.75-0.81

0.40-0.46

0.195-0.242

Mean

1,67

0.78

0.43

0.224

SD

0,04

0.02

0.02

0.008

Calyptopis lll,n
Range

= 140:
2.20-2.55

0.89-0.99

0.50-0.61

0.242-0.279

Mean
SD

2.36
0.06

0.94
0.02

0.56
0.02

0.260
0.009

315

FISHERY BULLETIN: VOL. 78, NO. 2

Although there is variation in timing of events
with respect to stage, the form, setation, and de-

TABLE 3. — Measurements (millimeters) of furcilia I-VI and
juvenile I in the northern form of Euphausia eximia.

Carapace

Stage

Total length

length

Telson width

Furcilia \,n =

151:

Range

2.87-3.19

0.81-0.87

0.232-0.270

Mean

3.02

0.84

0.250

SO

0.07

0.02

0.009

Furcilia II, n =

= 132:

Range

3.41-384

0.89-1.01

0.195-0 232

Mean

3.59

0.94

0.219

SD

0.09

0.02

0.009

Furcilia lll,n

= 183:

Range

384-4.46

0.97-1.13

0.158-0214

Mean

4,13

1.05

0.188

SD

0.12

0.03

0.010

Furcilia IV, n

= 269:

Range

408-497

1.07-1.25

0.149-0.195

Mean

4.60

1.16

0.167

SD

0.15

0.03

0.008

Furcilia V.n =

= 158:

Range

4.52-5.66

1.13-1.39

0.121-0.177

Mean

5.13

1.26

0.153

SD

0.23

0.05

0.008

Furcilia VI, a7

= 58:

Range

5.09-6.06

1.19-1.45

0.112-0.158

Mean

5.55

1.34

0.138

so

0.23

0.06

0.009

Juvenile \,n =

= 53:

Range

5.45-6.79

1.35-1.64

0.112-0.149

Mean

6.15

1.49

0.131

SD

0.32

0.07

0.007

velopment of appendages are very similar in lar-
vae of congeners E. gibboides and E. eximia. The
descriptions with figures of E. gibboides larvae
(Knight 1975) may be consulted for morphology
and development of appendages of E. eximia
which are figured and discussed in detail here only
when necessary to contribute information specific
to.B. eximia. The setations of maxillule, maxilla,
and pleopods in larvae oiE. eximia are given in
Tables 4, 5, and 6.

EGGS. — Perivitelline space relatively small,
50 spawned eggs with the following measure-
ments: Outer diameter, 0.38-0.46 mm; mean, 0.45
mm; SD, 0.02 mm. Perivitelline space, 0.03-0.07
mm; mean, 0.06 mm; SD, 0.01 mm. Eighty-five
eggs from the plankton differed slightly: Outer
diameter, 0.40-0.48 mm; mean, 0.45 mm; SD, 0.01
mm. Perivitelline space, 0.03-0.07 mm; mean, 0.05
mm; SD, 0.01 mm.

NAUPLIUS I AND II.— Body ovoid, as figured
for E. gibboides, with one pair long posterior
spines in nauplius I and a second short outer pair
in nauplius II; both stages with 3 pairs of func-

TABLE 4. — Development of maxillule in the northern form of Euphausia eximia; exopod with 4 setae and endopod with 2

medial and 3 terminal setae in all stages; ( ) = usual condition.

Stage

Endopod

Basal endite setae

Pseudexopod

Segments

Lateral seta

Medial

Proximal

2

0

3

0

2

0

5

0

2

0

6-7(7)

0

2

0

7

0-1(1)

2

0

9

1

1-2

0-1(0)

8-10(9)

1

1

1

8-10(9-10)

1-2(1)

1

1

9-13(10)

1-2

1

1

10-12(10-11)

1-2(2)

Coxal endite setae

Presence Anterior seta

Calyptopis I
Calyptopis II-
Furcilia I
Furcilia II
Furcilia III
Furcilia IV
Furcilia V
Furcilia VI
Juvenile I

7

7

8

8
8-9(8)
8-9(9)
8-9(9)
9-10(9)
9-11(10)

-/ + (+)

+
+

0
0
0
0
0
0
0
0
0-1

Table 5. — Setation of maxilla in the northern form of Euphau-
sia eximia; medial lobe five with 3 setae in all stages; 0 = usual
condition.

Exopod

Endopod

Medial lobes

stage

1

2

3

4

Calyptopis l-lll
Furcilia 1

3
3

8
8

4
4

4
4-5

4
4

Furcilia II

3

8

4

(5)
4-5

4

Furcilia III

3

8

4

(5)
5-6

4-5

Furcilia IV

3

8

4-6

(5)
5-6

(4)
5

Furcilia V

3

8

(4)
4-6

(6)
6-7

5-6

Furcilia VI
Juvenile 1

1-3
(1-2)

2-6
(2-5)

3-4

3-6

(4)

8

8-9

(8)

(5-6)

5-6

(6)

6

(6)
6-7

(6)
6-9

(7)

(5)
5-6

(6)
6-7

(6)

tional appendages — antennule, antenna, and
mandible. Seven hatched nauplius I larvae with
the followdng dimensions: Length, 0.38-0.41 mm;
mean, 0.39 mm; SD, 0.02 mm. Width, 0.25-0.27
mm; mean, 0.26 mm; SD, 0.01 mm.

METANAUPLIUS (FIGURES 2A, 3A).—
Rostral hood of carapace fringed with spines, 3
pairs on anterior margin relatively long, a fourth
anterolateral pair sometimes somewhat longer
than surrounding spines; usually 3 shorter spines
between medial pair of long spines, tiny spines
rarely interspersed; other small spines variable in
number. Dorsal crest high, rounded, with 2 small
spines (frequently broken or bent in preserved

316

KNIGHT: LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA

Table 6. — Setation of pleopods in the northern form of Euphausia eximia; 0 = usual condition.

Pleopod 1

Pleopod 2

Pleopod 3

Pleopoc

14

Pleopod 5

Stage

Exopod

Endopod

Exopod

Endopod

Exopod

Endopod

Exopod

Endopod

Exopod

Endopod

Furcilia 1

0

0

—

—

Furcilia II

6

1

0

0

0

0

0

0

0

0

Furcilia III

6-8(6)

2

6

1

6

1

6

1

6

1

Furcilia IV

7-8(8)

2-4(3-4)

8-9(8)

2-3(2)

8

2-3(2)

7-8(8)

2-3(2)

6-8(7-8)

2

Furcilia V

8-10(9)

4-6(4)

8-10(9)

4-5(4)

8-10(9)

3-5(4)

8-10(9)

4

7-9(8)

3-4(4)

Furcilia VI

9-11(10)

4-6(6)

9-11(10)

4-6(6)

9-11(10)

5-6

9-11(9-10)

4-6(5-6)

8-10(8-9)

4-5(4)

Juvenile 1'

10-13(11)

5-7(6)

11-12(11)

6-7(6)

11-12(11)

6-7(6)

10-12(11)

6-7(6)

9-11(9)

4-6(5)

'In juvenile I, 11, 13, and 7% of pleopods 1,2,and3with 1 seta proximal to appendix interna on endopod in 30 individuals.

specimens). Small pair of papillae on anterior
margin of body beneath carapace; Fraser (1936)
described papillae as frontal sensory organs.

Antennule and antenna functional, mandible
reduced, buds of maxillule, maxilla, and maxil-
liped present.

Abdomen short, posterior margin with 5 pairs of
spines; relatively long third pair articulated with
telson, shorter spines fused. The long spine is
plumose in E. gibboides but appears nearly
smooth (with tiny serrations sometimes visible) in
E. eximia.

CALYPTOPIS I (FIGURES 2B, 3B).— Rostral
hood of carapace fringed with spines curving me-
dially on anterior margin and posteriorly on pos-
terolateral curve of hood; posterior margin of
carapace produced into small dorsal spine; dorsal
crest without spines. Striated body of photophore
visible in developing compound eye, ocular papil-
lae situated medially slightly below anterior mar-
gin of eye.

Mandibles (Figure 4a) with asymmetrical me-
dian armature and with anterolateral process but
without lateral knob seen in species of the E. gib-
boides group (lateral knob is not found in any
stage of £. eximia); anterolateral process, repre-
senting palp (Gurney 1942), decreases in size until
furcilia V.

Maxillule and maxilla functional.

Maxilliped (Figure 5a) with form and setation
as in E. gibboides: coxa with 4 setae on inner
margin and 1 seta on posterior face; basis with 5
setae on inner margin and 1 distal submarginal
seta, 1 marginal seta noticeably stout; endopod
2-segmented, proximal segment with 3 setae, 2
marginal and 1 submarginal, 1 marginal seta
small and stout, distal segment with 4 terminal
setae; exopod with 4 terminal setae and 1 lateral
seta near articulation with basis. In E. gibboides
the stout setae of endopod segment 1 and basis are
nearly equal in length.

Abdomen unsegmented.

Telson (Figure 6a) with 1 pair lateral, 3 pairs
posterolateral, and 6 terminal spines, middle
posterolateral spine slightly longer than other
spines.

CALYPTOPIS II (FIGURES 2C, 3C).—
Carapace with lateral margins of rostral hood
curved ventrally around body so that in dorsal
view marginal spines are visible only on anterior
margin of carapace.

Maxilliped with stout seta of endopod segment 1
and basis now about equal in length, as figured for
calyptopis III (Figure 5b).

Abdomen with 5 segments.

Telson (Figure 6b) with 7 terminal spines, mid-
dle posterolateral spine relatively long, armature
of telson spines as in E. gibboides.

CALPYTOPIS III (FIGURES 2D, 3D).—
Carapace still with marginal spines of rostral hood
visible in dorsal view only on anterior margin
which extends well beyond eyes; lateral margins
with denticle. Pigment sometimes visible in de-
veloping compound eyes; ocular papillae small, set
farther out on eyestalk.

Maxilliped (Figure 5b) endopod with 5 setae on
terminal segment unlike species oiE. gibboides
group which retain 4 setae in this stage, coxa with
6 setae.

Abdomen with 6 segments, sixth segment with
pair of biramous uropods.

FURCILIA I (FIGURES 7A, 8A).— Carapace
wdth rectangular rostral plate fringed with mar-
ginal spines which curve toward small median
spine or denticle; posterior margin with dorsal
spine. Eyes movable, pigmented, with rounded
contour in furcilia stages (Figure 8d) unlike lobed
contour o^ E . gibboides eye.

Bud of leg 2 present.

Abdomen with one pair nonsetose pleopods on
segment 1.

317

FISHERY BULLETIN: VOL. 78, NO. 2

xWUi^

c-d

Figure 2. — Euphausia eximia, northern form, dorsal view: a, metanauplius; b-d, calyptopis I-III.

FURCILIA II (FIGURES 7B, 8B).— Carapace
with narrower rostral plate and larger median
spine, posterior margin without dorsal spine.

Maxilliped endopod with 5 or 6 (5) setae on dis-
tal segment.

318

Leg 2 endopod with 3-5 (4) segments, 1 or 2 (2)
terminal setae, and variable marginal setation;
exopod nonsetose; gill with two lobes; developing
photophore may be visible.

Leg 3 unsegmented, nonsetose, with bud of
exopod and bifid gill bud.

KNIGHT: LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA

c-d, f-g

Figure 3. — Euphausia eximia, lateral view. Northern form: a, metanauplius; b-d, calyp topis I-III. Southern form: e-g, calyp topis I-III.

Buds of legs 4 and 7 sometimes present.

Abdomen with one pair setose pleopods on seg-
ment 1 and 4 pairs nonsetose pleopods on seg-
ments 2-5; photophore on segment 1 pigmented,
photophore of segment 4 sometimes forming.

FURCILIA III (FIGURES 7C, 8C). — Carapace
with rostrum narrower and lengthening.

Antennule with flagella lengthening, often
2-segmented; 1 of 2 aesthetes on outer ramus
bifurcate distally as in E. gihboides furcilia III.

319

FISHERY BULLETIN: VOL. 78, NO. 2

c f

Figure 4. — Euphausia eximia, northern form. Mandible, posterior view: a, calyptopis I; b-e, furcilia III- VI; f, juvenile I.

Maxilliped endopod with 5 or 6 setae on distal
segment.

Leg 2 endopod 5-segmented with more than 2
terminal setae; exopod with 2-4 (3) setae; gill
sometimes with bud of third lobe; photophore pig-
mented.

Leg 3 endopod 5-segmented with 2 terminal
setae and variable marginal setation; exopod with
0 or 1 (0) seta; gill with bud of third lobe.

Leg 4 endopod unsegmented with 0 or 1 (0) ter-
minal seta; exopod nonsetose; gill with two lobes.

Leg 5 rudimentary, sometimes with buds of
exopod and gill.

Leg 7 with bifid gill and developing photophore
visible.

Bud of leg 8 sometimes present.

Abdomen with 5 pairs setose pleopods; photo-
phores pigmented on segments 1 and 4 and form-
ing on segment 2.

Telson (Figure 6f) still usually with 7 terminal
spines and 3 pairs posterolateral spines (2 of 336
larvae varied with 3 and 5 terminal spines); telson
of next instar sometimes visible beneath cuticle,
the following percentages (in parentheses) of ter-
minal spines were observed among 293 furcilia III
larvae: 7(L0), 6(0.3), 5(1.4), 4(2.4), 3(30.4), 2(15.7),
1(48.8). The setation pattern on inner margins of
middle and innermost posterolateral spines differs
from E . gibboides; the middle spine has 3 stronger
spinules separated by small spinules and inner
spine bears several spinules distally.

FURCILIA IV (FIGURES 7D, 9A). — Carapace
with a few small spines on lateral margins of ros-
trum and stronger median spine.

Antennular flagella with 8 or 9 segments, one of
the paired aesthetes on outer ramus no longer
bifurcate.

320

KNIGHT; LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA

0.1 mm

Figure 5. — Euphausia eximia, northern form. Maxilliped, posterior view: a-b,
calyptopis I and III; c-d, furcilia IV-V, setules omitted on a, c, d.

Antenna (Figure 10a) modified from natatory to
juvenile form, scale (exopod) with 11-13 (12) setae,
flagellum (endopod) with 4-6 (4) segments, 2 or 3
(2) peduncular and 2-4 (2) flagellar.

Mandible (Figure 4c) modified with fewer,
somewhat broader incisor teeth and lacinia
mobilis missing or very much reduced; anterolat-
eral process very small.

Maxilliped (Figure 5c) with 5 or 6 (6) setae on
distal segments of lengthening endopod; basis and
coxa with 6-8 (6-7) setae.

Leg 2 exopod with 5 or 6 (5) setae, gill with three
lobes.

Leg 3 endopod with >2 terminal setae, exopod
with 4-6 (5) setae; gill with three lobes, rarely with
bud of fourth lobe.

Leg 4 endopod 5-segmented with 2-5 (2) termi-

nal setae, exopod with 0-4 (0-2) setae; gill with
small third lobe.

Leg 5 endopod usually unsegmented (ca. 3 seg-
ments occasionally seen) with 0-2 (0-1) terminal
setae; exopod nonsetose; gill sometimes with bud
of third lobe.

Leg 6 rudimentary with exopod bud and 2 or 3
gill buds.

Leg 7 with lightly pigmented photophore and
three-lobed gill; leg 8 with three gill lobes.

Abdomen with photophores pigmented on seg-
ments 1,2, and 4, and sometimes forming on seg-
ment 3.

Telson (Figure 6g) with 6-1 terminal spines and
3 pairs posterolateral spines (Table 1), 45% of 431
furcilia IV with 1 and 30% with 3 terminal spines
(frequencies similar to those observed on develop-

321

FISHERY BULLETIN: VOL. 78, NO. 2

ing telson of furcilia IV in premolt furcilia III);
telson of next instar when forming beneath cuticle
with 1 terminal and 3 pairs posterolateral spines.

Inner margin of innermost posterolateral spine
with series of strong spinules and shorter spinules
interspersed. A second pair of lateral spines, or a

Figure 6.—Euphausia eximia, northern form. Telson, dorsal view: a-c, calyptopis I-III; d-e, furcilia I-II; f, furcilia III, 1-premolt to 3
terminal spines, 2-premolt to 1 terminal spine; g, furcilia IV, 1-wath 3 terminal spines, 2-with 1 terminal spine; h-i, furcilia V-VI; j,
juvenile I.

322

KNIGHT: LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA

single additional spine on one side only, was found
on 48^f of 87 larvae examined for this feature.

FURCILIA V (FIGURES 7E, 9B). — Carapace

with or without a few tiny lateral denticles on
rostrum.

Antennule with lateral spine of peduncle seg-
ment 1 slightly longer than or equal to length of

0.5 mm

a-g

Figure 7. — Euphausia eximw, northern form, dorsal view: a-f, furcilia I- VI; g, juvenile I; hl-3, typical development of dorsal lappet on

segment 1 of antennular peduncle in furcilia V-VI and juvenile I

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FISHERY BULLETIN: VOL. 78, NO. 2

segment 2, sometimes small variable rudiment of
dorsal lappet present on segment 1 of peduncle
with margin smooth or extended into 1 or 2 small

knobs (Figure 7h-l); no specimens with flagella
intact.

Antennal scale with 13-16 (14-15) setae and

0. 1 mm

Figure 8.—Euphausia eximia, lateral view. Northern form: a-c, furcilia Mil; d, eye of furcilia II. Southern form: e, carapace of furcilia

I.

324

KNIGHT: LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA

Figure 9. — Euphausia eximia, northern form, lateral view: a-b, fiircilia IV-V; c, juvenile I.

flagellum usually with 12 segments, 3 peduncular
and 7-10 (9) flagellar (Figure 10b).

Mandible (Figure 4d) without remnant of
lacinia mobilis, palp lengthening.

Maxilliped (Figure 5d) with endopod now about
equal in length to knee of leg 2, basis with 7-9 (8),
and coxa with 6-8 (6) setae and usually without
long seta on posterior face.

325

FISHERY BULLETIN: VOL. 78, NO. 2

Figure lO. — Euphausia ecjwia, northern form. Antenna, ventral view: a 1-2, furcilia IV with variation in segmentation of endopod; b,
furcilia V. Maxillule and maxilla, posterior view: c-d, juvenile I. Leg 2 exopod and legs 7-8: e-g, juvenile I (setules omitted in b-e).

Leg 2 exopod with 6 or 7 (6) setae, 1 of 28 appen-
dages examined with additional proximal seta on
inner margin common in furcilia VI and juvenile I
(Figure lOe); gill sometimes with bud of fourth
lobe.

326

Leg 3 exopod with 5-7 (6) setae, 1 of 34 appen-
dages examined with proximal seta as on leg 2
exopod; gill sometimes with bud of fourth lobe.

Leg 4 endopod setose; exopod with 4-6 (5) setae;
gill sometimes with bud of fourth lobe.

KNIGHT: LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA

Leg 5 endopod with 4 or 5 (5) segments and 1-5
(2) terminal setae; exopod with 0-5 (0-2) setae; gill
with bud of third lobe.

Leg 6 endopod unsegmented with 0 or 1 (0) ter-
minal seta; exopod nonsetose and gill with two or
three lobes.

Legs 7 and 8 with more than three gill lobes.

Abdomen with pigmented photophores on seg-
ments 1,2, and 4, photophore on segment 3 some-
times with visible structure and some pigment.

Telson (Figure 6h) with 1 terminal and 3 pairs of
posterolateral spines; telson of next instar when
visible beneath cuticle with only 2 pairs postero-
lateral spines in 38% of 77 larvae; 9T7c of 71 fur-
cilia V with 2 pairs lateral spines.

FURCILIA VI (FIGURE 7F). — Carapace with
smooth lateral margins on well-developed ros-
trum.

Antennule with lateral spine about equal or less
than length of peduncle segment 2, dorsal lappet of
segment 1 with small knob or few spines (Figure
7h-2).

Antennal scale with 15-18 ( 16) setae; flagella no
longer intact in preserved specimens.

Mandibles (Figure 4e) with palp relatively long,
usually unsegmented, sometimes constricted into
2 or 3 weakly defined segments; 1 of 18 furcilia VI
with 1 terminal seta on 2-segmented palp; slender
terminally dentate plate near molar area of each
mandible reduced, sometimes missing on left
mandible.

Maxilliped continues to lengthen to juvenile
form, endopod 5-segmented and setose, exopod
still with 1 proximal and 4 distal setae, coxa with-
out long seta on posterior face.

Leg 2 exopod with 6-8 (6-7) setae, 14 of 17 ap-
pendages examined with additional proximal seta
on inner margin (Figure lOe); gill with four lobes.

Leg 3 exopod with 6-8 (6) setae, 22 of 24 appen-
dages with proximal seta; gill with four lobes.

Leg 4 exopod with 6 or 7 (6) setae, 4 of 21 appen-
dages with proximal seta; gill with four lobes.

Leg 5 endopod 5-segmented and setose; exopod
with 4-6 (5) setae; gill with four lobes.

Leg 6 endopod with 0-5 (0-3) segments and 0-2
(1) terminal setae; exopod with 0-3 (0) setae; gill
with four or more lobes.

Legs 7 and 8 with branching gill lobes, rudiment
of leg 7 sometimes with terminal seta (Figure
lOf).

Abdomen with photophores pigmented on seg-
ments 1-4.

Telson (Figure 6i) with 3 or 2 (in 32% of 59
larvae) pairs of posterolateral spines, developing
telson of next instar when visible beneath cuticle
with 2 pairs posterolateral spines in 18 of 19 lar-
vae; 947c of 52 furcilia VI with 2 pairs of lateral
spines.

JUVENILE I (FIGURES 7G, 90). — Carapace
with lengthening rostrum.

Antennule with lateral spine from slightly less
than to about one-third the length of peduncle
segment 2, lappet with 3-6 spines (Figure 7h-3).

Antennal scale with 16-19 (18) setae.

Mandibles (Figure 4f) with palp usually three-
segmented, sometimes with 1 terminal seta and
0-3 lateral setae on segment 2, median armature
as in furcilia VI.

Maxillule without or with seta on anterior mar-
gin of pseudexopod and maxilla with increasing
numbers of setae on endopod and exopod ( Tables 4,
5; Figure 10 c-d).

Leg 1 (maxilliped) exopod with 4-7 (4) setae.

Leg 2 exopod (Figure lOe) with 6-8 (8) setae, all
with additional proximal seta on inner margin;
gill with four lobes.

Leg 3 exopod with 6-8 (8) setae plus proximal
seta on inner margin; gill with four lobes.

Leg 4 exopod with 6-8 (6-7) setae, 12 of 20 ap-
pendages with proximal seta; gill with four lobes.

Leg 5 exopod with 5-8 (6-7) setae, 3 of 17 appen-
dages with proximal seta; gill with four lobes.

Leg 6 endopod with 4 or 5 (5) segments and 2-4
(2) terminal setae; exopod with 2-6 (2-3) setae; gill
many branched.

Legs 7 and 8 (Figure lOf-g) rudiments each with
terminal seta and ramified gills.

Telson (Figure 6j) usually with 2 pairs postero-
lateral and 2 pairs lateral spines (in 92% and 98%
of 53 larvae).

In E.eximia, as in E . gibboides , the reduction in
number of terminal telson spines appears not to be
a reliable single guide to recognition of develop-
mental stages in furcilia IV-VI but rather only one
of a group of features that characterize these
stages. Furcilia IV of E. eximia, as delimited in
this study, had a variable number of terminal
spines which overlapped with the number of ter-
minal telson spines in furcilia III and V. Furcilia
IV differed from furcilia III, however, in the fol-
lowing features: modification of both antenna and
mandible; segmentation of antennular flagellum;
setation of exopods of legs 2 and 3; setation and
segmentation of leg 4 endopod; and setation of

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FISHERY BULLETIN: VOL. 78, NO. 2

pleopods 2-5. Furcilia IV was separated from fur-
cilia V by the segmentation of antennal flagella,
maxilliped endopod, and leg 5 endopod; and en-
dopod setation of pleopods 2-5, with small overlap
on pleopod 3 only. Grouping of stages by terminal
telson spine number would not be supported by
these characters and if, for instance, all larvae
with 1 terminal and 3 pairs posterolateral telson
spines were grouped together, the range in size
within the stage would become uncomfortably
large, more than twice that of furcilia III and al-
most twice that in furcilia V. Variability in reduc-
tion of posterolateral spines was seen in furcilia VI
and rarely in juvenile I.

The number of telson spines did relate to varia-
tion in size within a stage. For instance, furcilia III
larvae that would molt from 7 to 3 terminal spines
were 0.04 mm smaller on the average than those
that would molt from 7 to 1 terminal spine and in
furcilia IV, larvae with 3 terminal spines were
0.08 mm smaller on the average than those with 1
terminal spine. Variation in morphology within a
stage was assessed in a sample of larvae from one
location, as by midfurcilia phase there was a
noticeable difference in rate of development be-
tween areas within the range of the population. It
may be seen, for example, in a comparison of the
length of larval stages at two locations in the
California Current terminus (Figure 11) that, al-
though they were smaller on the average, furcilia
VI larvae from Station 10 in the mouth of the Gulf
of California were within the size range of juvenile
I of the slower growing larvae from Station 6 off
western Baja California. The patterns of telson
spine reduction in furcilia III-VI and juvenile I at
these two locations, shown in Table 7, exemplify
variation within the stages which appears to
reflect the difference in rate of growth and mor-
phogenesis.

only in all stages (Figure 12, Table 8); northern
form larvae had 2 pairs of lateral telson spines
from furcilia V. Furcilia III was slightly more vari-
able in number of terminal telson spines while
furcilia IV was less variable (Table 1). The
carapace differed also with relatively longer pos-
terodorsal spines from calyptopis I to furcilia I
(Figures 3e-g, 8e) and sometimes with slightly
larger and more persistant marginal spines.

Development of appendages was usually similar
in the two forms. The lateral spine of the anten-
nule was sometimes shorter and the lappet less
developed in southern form furcilia VI and the
setation of maxillule basal endite differed: 20, 62,
and 75% of larvae examined had acquired 2 setae
on the proximal margin of endite in furcilia V, VI,
and juvenile I among northern form larvae while
only 0, 2, and 17% of southern form larvae had a
second seta in these stages.

Southern form larvae were smaller on the aver-
age in the furcilia phase but, as in the California
Current terminus, differences in growth per stage
between areas within the range of the population
were noted. Developmental stages of E. eximia
from the Peru Current (Stations 1520/1604) were
larger on the average than those from the South

Table 7. — Pattern of telson spine reduction in furcilia III-VI
and juvenile I in the northern form of Euphausia eximia at two
locations (Stations 6 and 10) in the California Current terminus.
Values indicate percentage with telson armature in stage.

Terminal + posterolateral telson spines

Stage Stn 7+3 6+3 5+3 4+3 3+3 2+3 1+3 1+2 n

Furcilia 6 100.0 — — — — — — — 280

III 10 97.0 — 15 — 1.5 — — — 68
Furcilia 6 — 0.7 2.9 5.1 36.7 21.1 33.5 — 275

IV 10 — — — — 15.1 190 65.9 — 126
Furcilia e — — — — — — 100.0 — 41

V 10 — — — — — — 100.0 — 97

Furcilia e — — — — — — 92.9 7.1 14

VI 10 — — — — — — 21.4 78.6 14

Juvenile 6 — — — — — — 25.0 750 12

I 10 — — — — — — — 100.0 24

South Pacific Population

Larvae from two areas within the southern
range of E. eximia (Figure 1) were compared with
larvae from the California Current terminus and,
although the populations were generally similar,
discrepancies were discovered. The most con-
spicuous differences proved to be in the armature
of the telson. Among larvae in the South Equato-
rial and Peru Current population (southern form),
the middle posterolateral spine was longer rela-
tive to the other two posterolateral spines and the
majority of larvae had one pair of lateral spines

Table 8. — Number of pairs of lateral telson spines in furcilia
TV- VI, juvenile I, and adult in northern and southern forms of
Euphausia eximia. Values indicate percentage with telson ar-
mature in stage.

Pairs of lateral telson spines

Stage

Form

1

2

3

4

n

Furcilia IV

Northern
Southern

51.7
98.4

48.3
1.6

—

—

87
61

Furcilia V

Northern
Southern

2.8
97.9

97.2
2.1

—

71
48

Furcilia VI

Northern
Southern

5.8
100.0

94.2

—

—

52
67

Juvenile 1

Northern
Southern

1.8
95.0

98.2
5.0

—

—

55
60

Adult

Northern
Southern

56
97.5

85.7
2.5

7.9

0.8

126
121

328

KNIGHT: LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA

6.0

5.0

40

E
E

x:
"&

"o
o

3.0

2.0

1.0 -

ft

fe

^-^-f-i-

Cl

CHI

Fl Fll

stage

FIV

FV

FVI

Jl

Figure 1 1.— Length of developmental stages of northern and southern forms ofEuphausia eximia at four locations: mouth of Gulf of
California, Station 10 (white); west of Baja California, Station 6 (black); Peru Current, Stations 1520/1604 (dots); South Equatorial
Current, Station 21 (diagonal lines); vertical lines indicate range, horizontal lines indicate mean, and rectangles indicate sample
standard deviations.

329

FISHERY BULLETIN: VOL. 78, NO. 2

0.1 mm

FIGURE 12.— Euphausia eximia, southern form. Telson, dorsal view: a-c, calyptopis I-III; d-i, furcilia I- VI.

Equatorial Current (Station 21). The lengths of
larvae from these two locations are compared in
Figure 11 (there were few furcilia V at Station 21
and consequently a small range in total length of
this stage). Proportions of carapace length and

telson width to total length were, on the average,
as in northern form larval stages.

Because of the differences encountered between
northern and southern form larvae, a preliminary
survey of a few adult morphological characters

330

KNIGHT LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA

was carried out on samples of E. eximia from
across the species' range. Variation in number of
pairs of lateral telson spines was found to persist
in the adult (Table 8) and a discrepancy in the
armature of antennular peduncle, described and
photographed by Roger (1967) in equatorial E.
eximia, was found as well. The inner process of
antennular peduncle segment 2 had 1 or 2 spines
in the northern form and 1-5 spines in southern
form adults ( Table 9) and the number of spines was
related to size. Northern form adults <21 mm TL
had 1 spine only; 1 or 2 spines were found only on
the largest animals of 21-27 mm. Southern (ormE.
eximia of 12-18 mm length had 1-4 spines but
animals >18 mm had 2-5 spines; 1 spine was not
seen on the larger adults. Armature of the process
was often asymmetrical.

The differences between populations of E.
eximia in frequency of numbers of lateral spine
pairs on the telson of furcilia V-VI and adult, and
in armature of adult antennular peduncle seg-
ment 2 proved highly significant (P = <0.005) in
chi-square analyses.

Table 9. — Number of spines on inner process of antennular
peduncle segment 2 in adults of the northern and southern forms
ofEuphausia eximia. Values indicate percentage with armature
in form.

Number of spines on inner process,
antennular peciuncle segment 2

Form

12 3 4 5

Number

Northern
Southern

93.2 6.8 — — —
21.2 33.9 33.1 11.0 0 8

117
118

Vertical Distribution

When larvae were sorted for taxonomic study,
they were also counted at three stations in day and
night series of vertical samples taken during Krill
Expedition (Brinton 1979). The data obtained are
presented in Tables 10-12.

At Station 6, west of Baja California in the
California Current (Table 10), the distribution of
eggs corresponded with the nighttime range of
adults indicating that the majority of female E.
eximia had spawned in the surface waters during
the night. The highest concentration of meta-
nauplii was found in the layer below the surface,
reflecting sinkingof eggs prior to hatching( Mauch-
line and Fisher (1969) note that eggs of Thysan-
oessa raschii and Meganyctiphanes norvegica
sank at 5.5-7.5 m/h in water of 33.3% and 15° C).
The majority of calyptopes and early furcilia
stages were in the surface layer during the day,
sinking to strata beneath at night. The pattern
shifted gradually in midfurcilia phase and from
furcilia III, the stage when all pleopods are setose,
the larvae moved deeper in the daytime and
toward the surface at night, and developed stron-
ger migrating capability with increasing size.

The larval population structure and distribu-
tion pattern varied at Station 10 in the mouth of
the Gulf of California (Table 11). No eggs were
found and larvae were most abundant in early
furcilia stages instead of in the metanauplius and
calyptopis phases. The metanauplii were seen at
the surface, and there was no evidence of nightly

Table 10. — Vertical distribution (percentage of stage at depth) of larvae and adults of Euphausia eximia in day and night samples
from the California Current terminus off western Baja California (Station 6) and number/1,000 m^ in each stage.

Eggs

Metanauplius

Calyptopis

Furcilia

Depth (m)

1

II

III

1

II

III

IV

V

VI

Adult

Day;

0-43

97.2

26.2

99,6

99,9

100,0

99.3

95.0

67.7

51.4

40.5

—

—

43-86

2.4

73.6

0,3

—

5.0

16.5

18.0

33.1

60.0

—

86-129

—

0.1

—

—

—

—

—

12.8

14.9

135

—

—

129-172

—

—

—

—

—

—

—

3.0

15.7

10.8

40.0

—

182-275

0.3

(<0.1)

0,1

0.1

—

—

—

—

—

—

—

100.0

275-368

0.1

0.2

—

—

—

—

—

—

—

—

—

—

368-461

—

—

(<0,1)

0.1

—

0.7

—

—

—

—

—

—

461-554

—

—

—

—

—

—

—

—

—

—

—

—

No. 1.000 m3

3,283

10,593

7,510

3,835

991

288

100

436

255

37

5

28

Night:

0-43

88.1

5.7

1.3

1.5

3.8

0.7

0.8

11.1

48.8

50.0

77.8

69.1

43-86

8.4

79.5

70.7

54.5

41.1

52.9

70.7

74.4

51.2

50.0

22.2

15.6

86-129

3.5

14.8

28.0

44.0

55.0

46.4

28.4

14.5

—

—

—

15.3

129-172

—

—

—

—

0.1

0.1

0.1

—

—

—

—

—

182-275

—

—

—

—

—

—

—

—

—

—

—

—

275-368

—

—

—

—

—

—

—

—

—

—

—

—

368-461

—

—

—

—

—

—

—

—

—

—

—

—

461-554

—

—

—

—

—

—

—

—

—

—

—

—

No, 1,000 m^

143

5,402

4,380

2,089

4,018

1,180

874

379

125

18

9

392

331

Table ii.-
from the

FISHERY BULLETIN: VOL. 78, NO. 2

-Vertical distribution (percentage of stage at depth) of larvae and adults of Euphausia eximia in day and night samples
California Current terminus off the mouth of the Gulf of California (Station 10) and number/1,000 m^ in each stage.

Eggs

Metanauplius

Calyptopis

Furcilia

Depth (m)

1

II

III

1

II

III

IV

V

VI

Adult

Day:
0-43
43-136
136-229

—

—

99.7
0.3

998
0.2

99.9
0.1

99.8
0.2

998
0.2

99.3

07

128

790
21 0
14.9

33 2
61 8
135

41 2

45,1

—

229-322
322-415

I

I

—

—

7.8

100.0

No 1,000 m'

—

—

1,021

2.083

3,439

5.522

5,567

1,751

376

382

51

72

Night:
0-43
43-86

—

100.0

100.0

100 0

100.0

99.9
0.1

998
0.2

969

3.1

933
67

100.0

100 0

72.2
27.8

86-129
129-222
222-315
315-408
408-501

—

—

—

—

—

—

—

—

—

=

=

I

—

—

—

—

—

—

—

—

—

—

—

—

No 1,000 m3

—

249

79

1,223

3,464

4.260

4.508

1.651

416

150

11

126

Table 12. — Vertical distribution (percentage of stage at depth) of larvae and adults of Euphausia eximia in day and night samples
from the South Equatorial Current (Station 21) and number/1,000 m^ in each stage.

Eggs

Metanauplius

Calyptopis

Furcili

a

Depth (m)

1

II

III

1

II

III

IV

V

VI

Adulf

Day:

0-37

10.2

—

734

58.5

48.1

303

111

14.1

13,1

28 1

—

—

37-75

41.2

20.6

14,7

31.8

369

486

56.2

45.7

34.0

—

—

—

75-112

27.5

58.8

—

0.4

—

08

7,0

10,5

20.0

—

136

—

112-150

20.8

20 1

119

93

14.7

20.3

257

29.7

31.9

344

9 1

—

150-227

0.1

03

—

—

—

—

—

—

—

—

—

—

227-305

0.2

02

—

—

0,3

—

—

—

0.9

37.5

77.3

36.1

305-382

0.1

—

—

—

—

—

—

—

—

—

—

63.9

382-460

—

—

—

—

—

—

—

—

—

—

—

—

No./I.OOOm^

35,600

2.184

1.734

2,144

1,285

650

844

1.330

429

32

66

391

Night

0-36

21.7

—

25,7

31 9

34.5

35-4

204

6,4

168

—

19.9

45.1

36-72

20 1

—

59,3

62,1

60,1

51.0

49.1

49,1

504

100,0

80 1

39.8

72-108

56.2

98,0

14.1

59

53

13.3

305

43.9

328

—

—

15.1

108-144

0.5

—

—

—

—

03

—

—

—

—

—

—

144-223

1.4

2.0

0.8

0 1

—

__

223-302

(<0.1)

—

—

—

—

—

302-381

(<0.1)

—

—

—

—

—

—

—

—

381-460

—

—

—

—

—

—

—

—

—

—

—

—

No. 1.000 m^

4.478

653

1,605

2.784

2,331

933

407

328

125

25

312

11,388

sinking of calyptopes and early furcilia larvae;
almost the entire population remained in the sur-
face layer until furcilia III. Diurnal vertical mi-
gration again developed in the last half of the
furcilia phase.

The pattern of vertical distribution at Station 21
in the South Equatorial Current (Table 12) had
features in common with the distribution observed
at Station 6 but was less clearly defined. The posi-
tion of the calyptopes reflected a developmental
ascent from the depth at which eggs had hatched;
calyptopis I was more abundant in the surface
layer during the day than at night, and there was
also some evidence of nighttime sinking in calyp-
topis II and III. In the furcilia phase the pattern of
vertical migration was modified in that the larvae
appeared to avoid the surface 0-35 m stratum to

332

some extent. The population structure differed
with calyptopis II being the most abundant larval
stage.

The differences in larval vertical distribution
appeared not to be related to time of sampling; in
the upper 150-200 m, where most of the larvae
were found, the three night samples were taken
between 0000 and 0030 and the day samples in
midaftemoon (1600) at Stations 6 and 21 and
midmorning (0800-0900) at Station 10 (Brinton
1979, figure 3).

DISCUSSION

The species of Euphausia were separated into
groups, characterized by adult armature of
carapace, abdomen, antennule, and petasma, by

KNIGHT: LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA

Brinton (1975). Among species which have two
lateral denticles on the carapace (group lA), E.
eximia is most closely related ioE. krohnii and E.
americana by the conspicuous pectinate dorsal
lappet on the first segment of the antennular
peduncle. The larvae oi E. krohnii have been de-
scribed from the North Atlantic and Mediterra-
nean by Frost (1934) and Casanova (1974) and,
while it is not possible to compare the species in
detail, the development oiE. eximia appears to be
very similar to that of the North Atlantic popula-
tion of E. krohnii. The timing of acquisition of
pigmentation in abdominal photophores may dif-
fer; Frost notes that all are pigmented in furcilia
ni but this condition was not normally seen in E.
eximia until furcilia V. Development of the dis-
tinctive antennular lappet appears to begin at
about the same stage (in furcilia V of £. eximia at
4.5-5.7 mm TL and in 5.9-6.1 mm larvae of North
Atlantic E. krohnii) and with variable form. Ac-
cording to Soulier (1963) the lappet of Mediterra-
nean E. krohnii develops in a fixed pattern, and
>2 spines are not seen until 10 mm TL. There was
greater variability in number of telson spines in
furcilia IV of £. eximia, and one more stage in the
furcilia phase, than noted by Casanova ( 1974) in
E. krohnii from the Mediterranean. Larvae of the
California Current population of £■. eximia were
intermediate in size between the large North At-
lantic larvae of E. krohnii and the smaller
Mediterranean population, while larvae of E.
eximia from the South Equatorial Current tended
to be similar in overall length to Mediterranean E.
krohnii.

Larval forms appear to be very similar within
Euphausia species group lA which, besides E.
eximia, E. krohnii, and E. americana, includes E.
recurva, E. mutica, E. brevis, and E. diomedeae.
Their larvae share the following characters:
spines on anterior margin of carapace in
metanauplius, calyptopis phase, and early furcilia
stages; a posterodorsal spine on carapace in calyp-
topis I-III and furcilia I; telson with middle pos-

terolateral spine relatively long until midfurcilia
phase; and a fixed pattern of pleopod development
which progresses from 1 pair nonsetose to 1 pair
setose plus 4 pair nonsetose, and finally to 5 pairs
setose pleopods. Talbot (1974) noted variation in
number of telson spines developing beneath the
cuticle of furcilia III in E. recurva- mutica of the
Agulhas Current, and Casanova (1974) described
timing of events among larvae ofE. brevis (e.g.,
modification of antenna and mandible, and devel-
opment of legs), which is similar to the pattern
discerned inE. eximia.

Developmental events may vary considerably,
however, between the species groups of
Euphausia. Euphausia eximia (group lA) and E.
gibboides (group IB) differ in several details, some
of which are listed in Table 13, although they
share all the general features of group lA larvae
except pattern of pleopod development. Larvae of
E. gibboides are larger than those ofE. eximia, on
the average, in the metanauplius and calyptopis
phases but they are similar in the furcilia phase
due to a slightly higher rate of growth per stage in
furciliae of E. eximia. The telson is wider in E.
gibboides from calyptopis I through furcilia I, and
the carapace is wider from calyptopis I-III, than in
E. eximia, with no overlap in range of measure-
ments.

The morphological differences observed within

E. eximia, between larvae from the California
Current terminus and the South Equatorial-Peru
Current populations, appear related to the geo-
graphical separation of reproductive centers de-
scribed by Brinton (1979) in his study of the dis-
tributional adaptations of euphausiids to the
oxygen-deficient eastern tropical Pacific. He found
that E. eximia achieved the highest densities
(>500 beneath 1 m^) in the South Equatorial Cur-
rent and across the California Current-eastern
tropical Pacific transition off Baja California, the
productive zones marginal to the low oxygen wat-
ers. The species occurred consistently across a
transect of the eastern tropical Pacific but only

Table 13. — Some differences in leirval development of Euphausia eximia and E. gibboides.

Feature

£ eximia

E. gibboides

Pleopods: pattern of development from furcilia I (' = nonsetose. " = setose)
Telson: dominant pattern of terminal spine reduction from furcilia III to VI
innermost posterolateral spine, inner margin

number of lateral spines
Carapace: stage when anterior median spine develops
Antennule: stage when dorsal lappet develops
Antenna: stage when modified to juvenile form
Mandible: stage when modified to juvenile form
lateral knob in calyptopis phase

V -. 1"4'^5"

r -^ 1"3' -~ 4"V -^ 5"

7 -* 3/1 ^ 1 ^ 1

7-*5 — 3^ 1

With spinules

With distal spinule only

from furcilia III

2 pairs from furcilia V

1 pair

Furcilia 1

Furcilia V-VI

Furcilia V-VI

Juvenile

Furcilia IV

Furcilia V

Furcilia IV

Furcilia VI

Absent

Present

333

FISHERY BULLETIN: VOL. 78, NO. 2

sparsely (<4 under 1 m^) from lat. 11° to 20° N
where the surface temperature exceeded 26° C and
lowest middepth O2 values were <0.05 ml/1
through a stratum of 600 m, and where water of
westerly origin entered with the Equatorial Coun-
tercurrent. Larvae were not observed between lat.
2° and 20° N.

The significant difference in frequency of num-
bers of lateral telson spines on late furciliae of the
California Current and the South Equatorial and
Peru Currents may be evidence of the develop-
ment of reproductive isolation between the two
populations. The larval evidence was corroborated
by a preliminary survey of adult E. eximia which
showed a significant difference between popula-
tions in the armature of both telson and antennu-
lar peduncle. A more thorough examination of
adult morphology is necessary, however, for an
evaluation of the divergence within the species.
The distribution of northern and southern forms
observed (Figure 1) suggests that juveniles and
adults of E. eximia are carried from the species'
reproductive center off Baja California into the
oxygen-deficient warm waters of the eastern trop-
ical Pacific which may form an effective barrier
between the reproductive areas of the two popula-
tions.

Variation in size of larvae at the same stage of
development (Figure 11) between areas sampled
within each population may be related to the
amount of food available among other factors. Le
Roux (1974), investigating the effects of diet and
temperature on the larval development of
Meganyctiphanes noruegica, demonstrated that
rhythm of molt, grov^h, and morphogenesis were
influenced by quality and quantity of food. With
excess food, an elevation in temperature caused an
acceleration in rate of molt but not precocious dif-
ferentiation and reduction of the number of larval
stages; the larvae were found to be a little smaller
in a given stage at the higher temperature due to a
decrease in growth per molt.

The relationship of surface temperature to size
among E. eximia larvae studied was not consis-
tent. Relatively smaller larvae were found at the
higher temperature within the South Equa-
torial-Peru Current population (22° and 16°
C at Stations 21 and 1520/1604) but in cooler wa-
ters of the California Current (18° and 24° C at
Stations 6 and 10). There was a direct correlation
of size with abundance of food, however, among
California Current larvae; the volume of zoo-
plankton biomass was very low at Station 6 but

relatively high at Station 10 (Brinton 1979)
reflecting displacement upward of recently up-
welled waters with high concentrations of nutrients
and probably, with relatively green waters, abun-
dant food for larval forms. The larger size of larvae
from Station 10 may also be related to their posi-
tion in the water column; numbers of calyptopes
and early furcilia at Station 6 sank below the
surface stratum at night while those at Station 10
remained almost entirely day and night in the
food-rich surface layer. Data on biomass and on
larval vertical distribution were not available for
Stations in the Peru Current for comparison with
those in the South Equatorial Current.

Most species of euphausiids studied show indi-
cations of some downward daytime vertical migra-
tion from calyptopis II (Mauchline and Fisher
1969) but at Stations 6 and 21 (Tables 9, 11) the
position of E. eximia calyptopes in day and night
samples appeared to indicate a reverse pattern of
movement. After a presumed developmental as-
cent from the depths at which nauplii hatched
from sinking eggs, the majority of calyptopis I
were found in the surface layer in the daytime and
in deeper strata at night. The pattern continued
through furcilia III at Station 6 and through
calyptopis III, to some extent, at Station 21. As
noted above, most larvae at Station 10 were found
in the surface stratum in both day and night sam-
ples through furcilia II; the lack of nighttime sink-
ing in early stages may be related to the shoaling
of low oxygen water and upwelling conditions ob-
served in the area (Brinton 1979).

The position of calyptopis I in the day-night
series at Stations 6 and 2 1 suggests that the larvae
were drawn to the surface layer by positive photo-
taxis. Sulkin (1973), working with two species of
xanthid brachyurans, showed that, in the absence
of light, the distribution of larvae varied with on-
togeny; the four zoeal and one megalopa stage
assumed a differential vertical distribution due to
forces of gravity and hydrostatic pressure as well
as different sinking rates, with early stages near
the surface. In assessing the influence of light on
depth regulation in the same species, Sulkin
( 1975) suggested that the observed positive photo-
taxis superimposed a diurnal vertical migration
on the basic pattern of differential ontogenetic
vertical distribution. Larvae of E. eximia appear
to show a similar response during the calyptopis
phase with modification of their behavior during
ontogeny as furcilia develop a pattern of vertical
migration similar to that of the adult.

334

KNIGHT: LARVAL DEVELOPMENT OF EUPHAUSIA EXIMIA

ACKNOWLEDGMENTS

I thank E. Brinton for his advice and criticism of
the manuscript, A. Fleminger for dissection of fur-
cilia to confirm morphology of mandibles, and A.
Townsend for helpful discussions of larval mor-
phology. I am also grateful to the Fishery Bulletin
reviewers for their constructive comments. This
work was supported by the Marine Life Research
Program, the Scripps Institution of Oceanog-
raphy's component of the California Cooperative
Oceanic Fisheries Investigations.

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1978. Distribution of euphausiids in the Chile-Peru Cur-
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Brinton, E.

1962. The distribution of Pacific euphausiids. Bull.

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1979. Parameters relating to the distributions of
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1974. Les Euphausiaces de Mediterranee. (Systematique
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Eraser, F. C.

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Frost, w. e.

1934. The occurrence and development of Euphausia
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GOPALAKRISHNAN, K.

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GURNEY, R.

1942. Larvae of decapod crustacea. Ray Soc. Publ. 129,
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Knight, m. D.

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Mar. Sci. 28:255-281.
Lasker, R., and G. H. THEILACKER.

1965. Maintenance of euphausiid shrimps in the labora-
tory. Limnol. Oceanogr. 10:287-288.

LE roux, a.

1974. Observations sur le de'veloppement larvaire de
Meganyctiphanes norvegica (Crustacea: Euphausiacea)
au laboratoire. Mar. Biol. ( Berl.) 26:45-56.

1976. Observations sur les larves de Nyctiphanes couchii
et de Meganyctiphanes norvegica (Crustacea: Euphau-
siacea) re'coltees dans le Golfe du Morbihan. [Engl,
summ.] Cah. Biol. Mar. 17:375-386.

MAUCHLINE, J., AND L. R. FISHER.

1969. The biology of euphausiids. Adv. Mar. Biol. 7, 454 p.
Roger, C.

1967. Note on the distribution of Euphausia eximia and£.
gibboides in the equatorial Pacific. Pac. Sci. 21:429-430.
Soulier, B.

1963. Peches planctoniques, superficielles et profondes, en
Mediterranee Occidentale. IV. Euphausiaces. Rev.
Trav. Inst. Peches Marit. 27:417-440.
SULKIN, S. D.

1973. Depth regulation of crab larvae in the absence of
light. J. Exp. Mar. Biol. Ecol. 13:73-82.

1975. The influence of light in the depth regulation of crab
larvae. Biol. Bull. (Woods Hole) 148:333-343.

Talbot, M.S.

1974. Distribution of euphausiid crustaceans from the
Agulhas Current. Zool. Afr. 9:93-145.

Weigmann-Haass, R.

1977. Die Calyptopis- und Furcilia-Stadien von Euphau-
sia hanseni (Crustacea: Euphausiacea). Helgol. vriss.
Meeresunters. 29:315-327.

335

FEEDING ECOLOGY OF LAGODON RHOMBOIDES
(PISCES: SPARIDAE): VARIATION AND FUNCTIONAL RESPONSES

Allan W. Stoner*

ABSTRACT

Five major ontogenetic stages were found in the diet of pinfish, Lagodon rhomboides, from Apalachee
Bay, Florida, but diet and dietary breadth showed high degrees of variation with space (both local and
geographic), and seasonal variation within size classes was often as dramatic as ontogenetic variation.
Lagodon rhomboides demonstrated planktivory, omnivory, strict camivory, and strict herbivory at
different times, places, and developmental stages.

Ontogenetic pattern in food habits was primarily a fimction of mouth size and changing dentition of
the predator. Until it reaches 35 mm standard length, the pinfish is an obligate carnivore. Spatial and
temporal variation in the food habits of pinfish was a complex function of absolute and relative
abundances of food items in the field. Changes in plant consumption by fish larger than 35 mm standard
length may be due to changing plant abundance or protection of prey species by macrophyte cover at a
given station. Since seagrass biomass and the functional role of a single predator vary over both space
and time, plant-animal and predator-prey relationships change continually; however, the life history
of L. rhomboides is well adapted to seasonal patterns of productivity in food organisms. Multi-
dimensional variation in diets rendered the trophic level concept inoperational. It is concluded that
food webs are static neither in time nor in space and that taxonomic species may not be functional
components in models of energetic pathways and predator-prey relationships.

In recent years, much research effort has been
expended on experiments for testing the role of
predation in seagrass meadows (Young et al. 1976;
Young and Young 1977, 1978; Orth 1977; Nelson
1978; Reise 1978); yet few experimental ecologists
have concerned themselves with variation in the
feeding behavior or functional responses of the
predators involved in their experiments. The prob-
lem is illustrated by empirical data which show
the potential for wide variation in the diets of
fishes with season (Keast and Welsh 1968; Bell et
al. 1978a, b), time of day (Hobson 1974; Hobson
and Chess 1976; Robertson and Howard 1978), age
or size of the animal (Carr and Adams 1973; Hob-
son and Chess 1976; Ross 1978), and with locality
(Feller and Kaczynski 1975; Love and Ebeling
1978). However, very few scientists have
adequately characterized interactions of spatial,
temporal, and ontogenetic variations (Keast 1970,
1979; Nakashima and Leggett 1975). Also, field
studies that have examined relationships between
prey selection by fish and structure of prey as-
semblages are largely limited to fishes that in-
habit structurally simple mud bottom or water

'Department of Biological Science, Florida State University,
Tallahassee, Fla.; present address: Harbor Branch Institution,
hic, R.R. 1, Box 196- A, Fort Pierce, FL 33450.

Manuscript accepted December 1979.
FISHERY BULLETIN: VOL. 78. NO. 2, 1980.

column habitats (Feller and Kaczynski 1975;
Nakashima and Leggett 1975; Repsys et al. 1976;
Stein 1977). To date, only two field studies provide
data on the functional responses of fish to prey
abundance in seagrass habitats. Robertson and
Howard (1978) reported that short-term (diel)
dietary shifts in fishes inhabiting beds oiZostera
muelleri and Heterozostera tasmanica were due to
vertical movements of holoplankton and faculta-
tive zooplankton. Stoner (1979b) showed that the
selectivity of prey by pinfish, Lagodon rhom-
boides, was mediated by standing crop of benthic
macroph)^es. I concluded that increased seagrass
biomass resulted in a higher degree of selectivity
for certain amphipod species by juvenile fish.

The pinfish is the numerically dominant fish on
Thalassia testudinum meadows in the shallow
subtidal areas of the Gulf of Mexico (Hoese and
Jones 1963; Hansen 1969) and onZ. marina beds
along the Atlantic coast of the United States south
of Cape Hatteras, N.C. (Adams 1976). The pinfish
is one of the most important predators on macro-
benthic organisms of seagrass meadows and has
been shown to play a role in the organization of
faunal assemblages (Young et al. 1976; Young and
Young 1978; Nelson 1978). Data have accumu-
lated on the food habits of pinfish; however, most of
the early work reviewed by Caldwell (1957) and

337

FISHERY BULLETIN: VOL. 78, NO. 2

Carr and Adams (1973) is qualitative and based on
small numbers offish with no particular attention
paid to time, space, or fish size. Carr and Adams
provided the best published account of food habits
of pinfish, noting distinct ontogenetic patterns in
the food habits of pinfish and several other fish
species which dwell on seagrass beds near Crystal
River, Fla. The general conclusion has been that
L. rhomboides is a generalist feeder. Because L.
rhomboides is an important mediator of benthic
organization, and because the fish is a generalist-
type feeder, an investigation was undertaken to
test for functional responses of the species to food
abundance in the field. Ontogenetic, spatial (local
and geographic), and temporal (seasonal) varia-
tions in food habits of L. rhomboides were
explained on the basis of predator morphology,
food abundance, and habitat complexity.

METHODS

Based on long-term macrophyte data for the
area (Zimmerman and Livingston 1976a, b), four
collecting stations were chosen from shallow re-
gions offshore from the mouths of the Econfina and
Fenholloway Rivers, in Apalachee Bay, Fla. (Fig-
ure 1). One station was located 2.0 km seaward
from each of the river mouths and a second was
located 4.0 km seaward. Each site was identified
with a permanent marker in a location which was
representative of a broad area. Stations Econfina
10 and 12 were macrophyte-dominated habitats
(primarily T. testudinum and Syringodium

filiforme) with mean annual macrophyte bio-
masses of 214 and 320 g dry w^/m^. The inner
station of the Fenholloway area (station 11) was
characterized by low macrophyte densities (9.3 g
dry wt/m^) and the outer station (Fenholloway 12)
was characterized by macrophyte levels (141 g
dry wt/m^) intermediate between those levels
found at the Econfina stations and those at the
inner Fenholloway station (Livingston^). All sta-
tions were polyhaline with salinities ranging from
approximately 17 to 34%o. The mean water depth
at all stations was between 1.6 and 2.0 m.

Pinfish were collected with a 5 m otter trawl(1.9
cm mesh wing and body, 0.6 cm mesh liner). Seven
2-min tows (2-3 kn) were taken at each station on a
monthly basis. The trawling method for the study
site was examined by Livingston et al.^ All tows
were made at midday since previous work ( Kjelson
et al. 1975; Peters and Kjelson, 1975; Adams,
1976) indicated that pinfish feed primarily during
daylight hours. All fishes were preserved in 10%
Formalin'*-seawater solution, identified to species,
and measured for standard length (SL).

To estimate abundance of prey items in the field,
macrobenthic animals (>0.5 mm) and zoo-
plankton were collected on each of the fish collec-
tion dates. Macrobenthic prey items were collected
with 12 7.6 cm diameter cores and identified to
species (Stoner in press). Zooplankton were col-
lected with horizontal tows of a 0.5 m simple coni-
cal plankton net with 0.202 mm mesh and a T.S.K.
flowmeter. A single tow was made at each station,
on each sampling date, at a speed of 1.5 kn. Tow
time was dependent upon the abundance of plank-
ton but ranged from 2 to 10 min. Each plankton
sample was subsampled with a Folsom plankton
splitter when necessary and a 5 ml Hensen-
Stemple pipette. One one-hundredth of each sam-
ple was counted. Since the importance of plank-
tonic prey items in pinfish food habits was limited
to a small part of the population, animals were
identified only to major taxonomic group (e.g.,
calanoid copepod, crab zoea, polychaete larva, etc.)

Figure l . — Locations of collecting sites for Lagodon rhomboides
and food organisms offshore from the Econfina and Fenholloway
Rivers in Apalachee Bay, Fla.

^R. J. Livingston, Associate Professor, Department of Biologi-
cal Science, Florida State University, Tallahassee, FL 32306,
pers. commun. January 1978.

^Livingston, R. J., K. L. Heck, Jr., and T. A. Hooks.
1972. The ecological impact of pulp ■w\\\ effluent on aquatic
flora and fauna of north Florida: Comparison of a polluted drain-
age system (Fenholloway) with an unpolluted one (Econ-
fina). Unpubl. Rep., 186 p., to the Coastal Coordinating Coun-
cil, Florida.

■• Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

338

STONER: FEEDING ECOLOGY OF LAGODON RHOMBOIDES

and the standing crops of each group were calcu-
lated.

Plants were quantitatively sampled (Livingston
et al. 1976) at the field quadrant from where
macrobenthic animals were collected, on the fish
collection date. Data on the biomass and species
composition of benthic macrophytes at the field
stations were provided by Robert J. Livingston.

Fish, macrophytes, and prey animals were col-
lected monthly from November 1976 to December
1977. All collections for a station were made on the
same date at midday, and all of the stations were
sampled within a 2-4 day period.

For analysis of stomach contents, fish were
placed in 5 mm size classes up to 40 mm SL, 10 mm
size classes from 40 to 100 mm, and 20 mm size
classes for fish >100 mm SL. Food items taken
from the stomachs of up to 25 fish in a size class
were pooled for each sampling date and station
and preserved with lQ9c isopropanol and a dilute
solution of rose bengal stain. The gravimetric
sieve fractionation procedure developed by Carr
and Adams (1972) was used to analyze stomach
contents of pinfish ranging from 11 to 160 mm SL.
Stomach contents were washed through a series of
six sieves of decreasing mesh size (2.0-0.075 mm
mesh) and the frequency of occurrence of each food
type was recorded for each sieve fraction. Because
all of the items in a particular sieve fraction were
of comparable size, the relative proportion of the
stomach contents made up of each food type was
measured directly by counting. After examina-
tion, each sieve fraction was dried overnight at
100° C and the total contribution of each food type
was calculated.

With two exceptions, each food particle was
placed in a mutually exclusive category. General
categories such as amphipod, isopod, harpacticoid
copepod, crab zoea, and mysid were employed. The
categories animal remains (unidentified tissue
stained with rose bengal) and plant remains were
the only food categories that were not mutually
exclusive from other groups. Plants specifically
identified were T. testudinum and S. fili forme. The
general food categories, 40 in number (Table 1),
were used for statistical analyses; however,
whenever an animal or plant could be identified to
a more specific group (e.g., family, genus, species)
this information was recorded.

Cluster analysis, employing the similarity
coefficient, p (Matusita 1955; Van Belle and
Ahmad 1974), and flexible grouping cluster
strategy ((3 = -0.25) was used to describe onto-

Table 1. — List of the general food categories encountered in
the stomachs of pinfish and the codes employed in food habit
histograms.

Code

Food category

Code

Food category

AM

Amphipod

IS

Isopod

BA

Barnacle

IT

Invertebrate tube

Bl

Bivalve

MY

Mysid

BR

Branchiuran

NE

Nematode

BZ

Bryozoan

NM

Nemertean

CC

Calanoid copepod

NU

Nudibranch

CH

Chaetognath

OS

Ostracod

CR

Crab

PL

Polychaete larvae

CU

Cumacean

PM

Plant matter

CZ

Crab zoea

PO

Polychaete

DE

Detritus

SA

Sand

Dl

Diatom

SC

Scallop

FE

Fisti egg

SH

Shrimp

FL

Fish larvae

SL

Spicule

FO

Foraminifera

SP

Shrimp postlarvae

FR

Fish remains

SY

Syringodium filiforme

GA

Gastropod

TA

Tanaid

HC

Harpacticoid copepod

TH

Thalassia testudinum

HY

Hydroid

VL

Veliger larvae

IE

Invertebrate egg

MS

Miscellaneous — used in food habit histograms

for all food Items making

up < 3% of the total mass.

genetic variation in food habits of L. rhomboides.
The appropriateness of the cluster strategy for
dealing with fish diet data was discussed by Sheri-
dan (1978).

Stepwise multiple regression was used in cer-
tain instances to analyze the relationships be-
tween amounts of food items consumed by pinfish
and abundance of food items in the field. Depen-
dent variables included the amount of amphipod,
shrimp, and plant material in stomachs (percent of
contents in dry weight) and independent variables
were amphipod, shrimp, plant, calanoid copepod,
and polychaete abundance values. Maximization
of the coefficient of determination, r^, was the
criterion for selecting the best multiple regression
model. The minimum F value for inclusion of vari-
ables in the regression equations was set at 0.01.

RESULTS

Nearly 5,000 pinfish, representing 61% of all
trawlable ichthyofauna in Apalachee Bay, were
collected at four field sites during a 1-yr sampling
period. The number offish collected at a station,
however, was a direct function of the mean macro-
phyte biomass at the site (r = 0.998, P>0.01).
Most of the fish were collected between April and
October (Figure 2).

The stomach contents of 2,174 pinfish taken
from the four field sites were analyzed. Although
the unvegetated site (Fenholloway 11) produced
only 82 pinfish in routine trawl collections, over
600 stomachs of fish from each of the vegetated

339

T3
(U

•f
u
0)

o
u

1/1
a
-a

o
n

E
o

c
o

"D

o

O)

ni

600

500

<o 400 -

m

t 300

o

z

200 -

100 -

DJFMAMJJ

Month

Figure 2. — Number of Lagodon rhomboides collected in
Apalachee Bay, Fla., from December 1976 to November 1977.
Crosses = Fenholloway 11, triangles = Fenholloway 12, dots =
Econfina 10, circles = Econfina 12.

stations were examined. The relative proportions
of various food items taken by pinfish of different
size classes (for all dates and stations) varied
widely with fish size (Figure 3) and cluster
analysis showed four distinct ontogenetic trophic
groups. The first group was planktivorous and in-
cludes only those fish <16 mm SL. The second
group (16-35 mm) included fish which took har-
pacticoid copepods and amphipods in nearly equal
proportions plus small amounts of shrimp post-
larvae, invertebrate eggs, and other animals. This
group was largely carnivorous. Fish of group three
(36-80 mm) were omnivores, taking about 30% of
their diet in the form of plant material (mostly
microepiphytes) and the rest from the macro-
benthic fauna (mainly amphipods, small shrimp,
and some harpacticoid copepods). Group four ( >80
mm) included mostly adult fish, >1 yr old. At least
one-half of the diet was plant material; however,
stomach contents offish >100 mm SL were <10%
animal matter. A large portion of the plant matter
consumed was seagrass, especially S. filiforme.

Pinfish diet was dependent upon the place of
capture as well as size of the fish (Table 2). Al-
though a large percentage of the stomachs were
empty, the primary food item of pinfish between 1 1
and 15 mm SL was calanoid copepods at Fenhollo-
way 11, Fenholloway 12, and Econfina 12. Fish of
the same size class took a large number of inver-
tebrate eggs at the inner stations, Econfina 10 and
Fenholloway 11. Harpacticoid copepods and

o

x:

>

E

if)
+->

c

0)

c
o
u

..c
u

03

E
o

FISHERY BULLETIN: VOL. 78, NO. 2

0.4

]

0.0 -

0.2 -

0.4 -

- 0.6 -

^ 0.8 -

1.0 -
100 -1
+j 90

>i

t_
"D

O
o

^: 60

7^

11- 16-21-26-31- 36-41-51-61- 71- 81-91-101-121
1 5 20 25 30 35 40 50 60 70 80 90 100120 »

80 -

70 -

50

40 -

30 -

20 -

10 -

0 -^

CC

cc

CC

IE

IE

HC

IE

HC

(^

DE

AM

HC

IE

HC

IE

HC

AM

CC

HC

AM

AM

SP

SA

MS

SA

DE

MS

AM

SP

SH

MY

PO

MS

SP

SH

PM

DE

MS

SP

CC

IE

HC

AM

CC

IE

HC

AM

AM

AM

SP

SH

PO

CZ

PM

MS

SH

PO

PM

MS

SP

SH

PO

PM

SA

DE

SH

AM

AM

PO

SH

PO

Bl

PM

SA

MS

MS

PO

IS

PM

Bl

PC

IS

PM

TH

SA

MS

SA

Bl

PM

TH

SY

SA

PM

Bl

PM

TH

SA

MS

MS

DE

MS

TH

SY

MS

Standard Length (nnnn)

Figure 3. — Ontogenetic changes in diet of Lagodon rhomboides
from Apalachee Bay, Fla. Histograms represent relative propor-
tions of major dietary components (dry weight). Dendogram rep-
resents cluster analysis of diet similarity among size classes.
Codes for the food items are given in Table 1. (See text for
explanation of the cluster strategy.)

amphipods were important food items only at
Econfina 10. The percentage of diet made up by
calanoid copepods was directly related to the mean
calanoid copepod standing crop (number per cubic
meter) at a given station and time (r = 0.804,
P<0.05) (Figure 4). No significant relationships
were found between amphipods consumed by the
small pinfish and abundance of amphipods in the
field; however, amphipods were consumed by post-

340

STONER: FEEDING ECOLOGY OF LAGODON RHOMBOIDES

Table 2. — Composition of stomach contents of Lagodon rhom-
boides at four stations in Apalachee Bay, Fla. Each value is the
mean percentage of the total dry weight of stomach contents for
the fish size class indicated.

^ 100 n

Item

Fen 11

Fen 12 Econ 10 Econ 12

n (% empty)
Calanoid copepods
Invertebrate eggs
Detritus
Harpacticoid
copepods
Amphipods

n (% empty)
Harpacticoid
copepods
Amphipods
Invertebrate eggs
Shrimp postlarvae
Polychaetes
Plant matter
Shrimp

Calanoid copepods
Miscellaneous

n (% empty)
Amphipods
Plant matter
Harpacticoid
copepods
Shrimp postlarvae
Shrimp
Polychaetes
Calanoid copepods
Invertebrate eggs
Bivalves
Miscellaneous

n (% empty)

Plant matter

Polychaetes

Amphipods

Bivalves

Miscellaneous

Total number

% Empty

SL = 11-15mm
23(70.0) 10(70 0)

58.1 91.9

23.9

18.0 8.1

SL = 16-35 mm
14(14.3) 140(5.0)

7.0

30.0

9.5

3.0

3.0

40.0
7.5

40.8
18.3
8.0
6.0
2.8
2.9
5.3

15.9

SL = 36-80 mm
35(8.6) 380(6.6)
56.8 272

16.5 25.3

0.8
0.8
1.3
3.3
3.3
0.8

16.4

5.6
2.8

12.3
5.0
2.9
3.5
3.7

11.7

SL > 80 mm
10(30.0) 85(15.3)

6.0
0.7
6.0
81.3
6.0

82

29.3

63.3

4.9

8.1

10.1

13.6

615

8.4

35(42.8)
17.3
47.7

19.0
16.0

213(1.4)

26.5

38.5
2.7

13.5
1.7
2.5
1.5
1.0

12.1

460(3.0)
27.2
30.0

6.4
4.2
9.7
2.5
2.6
29
0.4
14.1

78(11.5)

84.3

0.1

2.4

0.4

12.8

786

5.2

7.3
7.5
1.0
4.2
0.2
5.2
8.0

408(4.4)
30.1
23.0

6.0
1.4
17.7
5.2
3.6
5.0

8.0

20(15.0)
91.7

2.0

63
691
5.5

larval fish at Econfina stations 10 and 12 only. The
small epifaunal amphipod Gitanopsis tortugae,
one of the few species consumed by small pinfish,
was collected only at these two stations during
these months (see Stoner (1979a) for a detailed
analysis of prey species consumed by L. rhom-
hoides). Because no data are available on abun-
dance of harpacticoid copepods in Apalachee Bay,
the importance of their abundance to food habits of
pinfish remains unknown.

The main components of the diets of pinfish be-
tween 16 and 35 mm were amphipods, harpac-
ticoid copepods, and shrimp postlarvae at the
three vegetated sites; amphipods and calanoid
copepods at Fenholloway 11. Shrimp and shrimp
postlarvae were abundant at the vegetated sta-
tions, but few in number at the unvegetated site
(Table 3). This probably explains the differences in
shrimp consumption. Calanoid copepods were ap-

28(42.8)

79.7

8.8

4.3

E

D
I/)

C

o

(J

2.3
4.9

if)
-o
o

235(2.1)

a

38.3
on 1

a

0

U

80

60 -

40

20

A 2

y = 0.026 X * 13.13
r = 0.804

1 1 1 1

1000 2000 3000 4000

Abundance of Copepods (N/nn^)

Figure 4. — Percentage of stomach contents (dry weight) of post-
larval pinfish composed of calanoid copepods shown as a fimction
of copepod abundance in Apalachee Bay, Fla. Cross = Fenhollo-
way 11, triangle = Fenholloway 12, dots = Econfina 10, circles =
Econfina 12 . Months are indicated by numbers beside the plotted
points.

parently substituted for shrimp at Fenholloway
11, although the copepods were less abundant at
that site than at other stations (Econfina 10 and
12) between April and July (Table 3). Low abun-
dance of harpacticoid copepods may explain their
relatively low contribution to the food habits of
young pinfish at the unvegetated site.

Diets of fish from 36 to 80 mm were similar at
the three vegetated stations and included large
amounts of amphipod, shrimp, and plant material.
At the unvegetated site, amphipods made up ap-
proximately twice the percentage found in fish
from vegetated stations. Because of low shrimp
abundance at the unvegetated site, shrimp con-
tributed little to the diets of fish inhabiting that
site. Amphipods appear to have been substituted
for shrimp.

Fish >80 mm demonstrated wide variability in
the percentage of the stomach contents composed
of plant material, ranging from 6.0% at Fenhollo-
way 11 to 91.7% at Econfina 12. The diet offish
from the unvegetated station was dominated by
the mussel Brachidontes exustus. For adult fish,
the mean percentage of the diet composed of plant
material was a direct function of the mean stand-
ing crop of benthic macrophytes at a given station
(r = 0.952, P<0.05); however, there was wide
temporal variation in the standing crop of benthic
macrophytes at the vegetated sites (Table 3) which
was not followed by proportional changes in plant
consumption at Econfina 10 and Fenholloway 12.

341

FISHERY BULLETIN: VOL. 78, NO. 2

Table 3. — Abundance of prey organisms and biomass of benthic macrophytes' in Apalachee Bay, Fla., from December 1976 to
November 1977. Only epifaunal species commonly consumed by Lagodon rhomboides were included in the abundance of amphipods.

Stn

Prey organisms

Dec.

Jan.

Feb.

Mar.

Apr.

May

June

July

Aug.

Sept.

Oct.

Nov.

F11

Amphipods. no./m'

95

0

38

189

114

0

152

0

0

95

152

151

Shrimp, no./m^

19

0

0

0

0

19

19

38

38

0

19

0

Polychaetes, no./m^

171

246

719

908

1.834

794

284

416

739

701

361

1.287

Copepods, no./m^

2,144

4,423

3,469

946

659

0

327

2,232

4,651

2,583

1.576

1,775

Macrophytes, g dry wt/m=^

—

3

1

6

5

5

8

11

16

10

20

18

F12

Amphipods. no./m'

379

246

152

245

1.209

397

479

246

454

794

730

1,493

Shrimp, no.'m'

57

38

38

0

94

38

190

19

341

133

76

57

Polychaetes. no./m^

1,948

1.194

1,436

1,325

1,722

2,005

1,477

701

965

1.760

607

2.460

Copepods. no./m^

1.973

5,935

4,182

2.202

81

109

411

798

2.730

3.123

1.792

686

Macrophytes, g dry wt/m^

—

110

152

96

197

70

145

165

175

243

117

84

E 10

Amphipods, no./m^

114

76

359

870

1,133

2,910

1.514

416

1,720

567

302

1.846

Shrimp, no., m^

19

0

19

19

19

0

95

189

114

114

208

208

Polychaetes, no./m^

1,154

663

1,079

814

569

2,119

910

758

907

853

625

2.947

Copepods. no./m^

1,020

543

385

803

1,981

7,130

1,069

4,042

3,404

2,898

1.315

1.227

Macrophytes, g dry wt/m^

—

96

164

58

230

246

216

234

279

392

319

126

E 12

Amphipods. no./m^

926

1,191

2,230

1.190

813

1,512

1,000

624

339

435

549

1,343

Shrimp, no./m^

76

19

19

38

76

0

57

57

95

38

76

0

Polychaetes, no./m^

946

1,665

1,304

1,097

890

1,553

1,062

815

797

683

380

1,156

Copepods. no./m^

807

1,147

3.440

1,070

0

527

258

1,387

3,447

2,745

2.136

948

Macrophytes, g dry wt'm^

—

259

237

118

240

319

456

390

374

619

401

104

' Macrophyte data were provided by R. J. Livingston (see text footnote 2).

This point will be discussed later. Polychaetes,
bivalves, amphipods, and other taxa were con-
sumed by adult pinfish where macrophyte cover
was low.

Seventy percent of the postlarval pinfish from
Fenholloway stations were empty and 42.8% of
the fish from Econfina stations had no stomach
contents (Table 2). Empty stomachs in pinfish > 15
mm SL were less common than found in postlarval
fish, but fish collected at the unvegetated site con-
sistently had the highest percentage of empty
stomachs. Between 11.5 and 15.3% of adult fish
taken from vegetated sites had empty stomachs,
but 30% of the adults from Fenholloway 11 were
empty.

Ontogenetic and spatial variations in pinfish
diet were interrelated with changes in diet with
season. Overall diet of the pinfish population at a
given station was highly dependent upon the
length-frequency composition of the population
(Figure 5); therefore, to examine independently
the effect of season on food habits, size was held
constant. Individual size groups, based on the
cluster analysis of feeding ontogeny (Figure 3)
were tested for seasonality in diet. Although the
mean length offish in the 16-35 mm SL size class
increased from 20 to 32 mm between March and
August, an analysis of dietary changes within 5
and 10 mm size classes indicated that the bias was
not serious and that the change in food habits over
time within the larger size group was an accurate
representation of dietary seasonality. Length-fre-

0

Q.
E

40
20

20 -

40
20

20
40
20
40
20
40
20

40
20
40
20
40
20

20

20 h

MB • ^^^^^^^H

N = 92 -

L ^^

30 -

i_

156 -

J -^.

123 -

' M. ..-

258 -

; .L

908 ;

: .*-

1010 -

: ..i

975 -

• • • • • •

686 -

J-

308 -

• • • • •

105 -

— 1 — 1 — 1 — ^^^^' 1

21 1 -
-r 1 1 1 1

Dec
J an

Feb

Mar
Apr

May

J une

July
Aug

Sept
Oct

0 20 40 60 80 100 120 140 160

Standard Length (mnn)

Figure 5. — Length-frequency distributions for Lagodon rhom-
boides collected in Apalachee Bay, Fla., from December 1976
to November 1977. Dots indicate that <3.09c of the sample oc-
curred in the size class.

342

STONER: FEEDING ECOLOGY OF LAGODON RHOMBOIDES

quency changes related to season within the 36-80
mm and adult size groups were minor. Because of
insufficient data for the site, FenhoUoway 11 was
ehminated from analysis of seasonal variation in
pinfish diet.

Data were sufficient for seasonal analysis of diet
in postlarval pinfish only at Econfina 12. Pinfish
<16 mm SL were collected at this site from
January through April. In January and February,
postlarval pinfish consumed primarily calanoid
copepods, plus a small number of invertebrate
eggs. Later, they consumed harpacticoid copepods
and amphipods in large quantities, and no cal-
anoid copepods were taken by postlarvae in April.
The relative abundance of calanoid copepods and
invertebrate eggs in the diet of these fish coin-
cided directly with the absolute abundance of the
plankton ic food items as determined by plankton
tows taken on the day offish collections. Copepods
and invertebrate eggs were most abundant in
January and February, and declined to annual
lows in April (Table 3). Amphipod abundance re-
mained relatively high at Econfina 12 through the
winter and spring with annual minima occurring
in the fall. Because amphipods were most abun-
dant in January and February (Table 3), when
copepod consumption was highest, it would appear
that calanoid copepods are the preferred prey of
postlarval pinfish. Only when calanoid popula-
tions fell to near zero did amphipods become a
major portion of the diet.

Pinfish of the carnivorous feeding group (16-35
mm SL) were collected from March through Au-
gust. In the spring and summer, amphipods and
harpacticoid copepods were the primary dietary
components of these fish (Figure 6). Clearly, how-
ever, amphipods were most important at Econfina
10. Amphipod consumption decreased with time
and by late summer the primary dietary compo-
nents were harpacticoid copepods and small
shrimp. A small amount of plant material was
taken at all three vegetated stations in midwinter.
Invertebrate eggs and other animal foods consis-
tently contributed small amounts to the diets of
pinfish between 16 and 35 mm SL.

Temporal variations in diet of pinfish from 16 to
35 mm were analyzed by stepwise multiple regres-
sion using calanoid copepod, shrimp, amphipod,
and benthic macrophyte abundance (Table 3) as
independent variables. Amphipod consumption
was positively correlated with amphipod abun-
dance (except Econfina 10) and negatively related
to plant, shrimp, and calanoid copepod abundance.

■D

in
■*j
c
t>
+j
c
o
U

sz
(J
CD

E
o

1/1

-r 1 1 T-

3 4 5 6 7 8

(20) (21) (27) (30) (31) (32)

Month

FIGURE 6. — Seasonality in diet of Lagodon rhomboides between
16 and 35 mm SL from three stations (F 12-top, E 10-middle, E
12-bottom) in Apalachee Bay, Fla. (March to August 1977). Diet
is given as the relative proportion of the dry weight of stomach
contents. Codes for the dietary components are given in Table 1.
Numbers in parentheses are the mean lengths of fish.

At least 97.6% of the variation in amphipod con-
sumption was explained by three independent
variables for all three stations. Significant multi-
ple correlation values for temporal variation in
shrimp consumption were obtained for fish from
Econfina 10 and 12 (r^ = 0.986 and 0.999, respec-
tively) (Table 4). Shrimp consumption was posi-
tively correlated with shrimp abundance, plant
biomass, and calanoid copepod abundance. Nega-
tive relationships were found with amphipod
abundance. Harpacticoid intake was positively re-
lated to plant biomass.

Pinfish between 36 and 80 mm SL were avail-
able year-round at vegetated sites and were consid-
ered to be omnivores. Examination of temporal

343

FISHERY BULLETIN: VOL. 78, NO. 2

Table 4. — Pearson correlation coefficients (r) and coefficients of
determination (r^) for p)ercentages of total stomach contents (dry
weight) compMjsed of: amphipods and shrimp in Lagodon rhom-
boides from 16 to 35 mm SL, tested as functions of food abun-
dance. AM = amphipods/m^, CC = calanoid copepods/m^, PM =
grams dry weight benthic macrophytes/m^, and SH = shrimp
and shrimp postlarvae/m^.

Fenholloway 12

Econfina 10

Econfina 1 2

Step

r

r'

Step r r^

Step

r

r^

Amphipods consumed

CC

-0.909

0.826

SH -0.802 0.643-

AM

0.887

0.787-

SH

-0.234

0.995-

AM -0,083 0.994"

SH

-0.716

0.866-

AM

0.482

n.s.

CC -0.388 0.999"

PM

-0.090

0.976-

PM

-0.391

PM -0.692 n.s.
Shrimp consumed

CC

-0.792

n.s.

CC

0789

n.s.

SH 0.872 0.760-

AM

-0.825

0.681-

SH

0318

AM -0066 0.972"

CC

0.231

0.868-

AM

-0.741

CC 0257 0986-

PM

0.662

0.998"

PM

-0.056

PM 0.604 n.s.

SH

0.783

n.s.

'P«0.05; "PsO.OI ; n.s. = not significant.

100

I-

"O

c

(U

c
o
(J

sz
(J

(T5
E

o

-♦-'

2 3 4 5

(51) (52) (761 (48:

6 7 8 9 10 11

(45) (44) (47) (49) (51) (54)

Month

Figure 7. — Seasonality in diet of Lagodon rhomboides between
36 and 80 mm SL from three stations (F 12-top, E 10-middle, E
12-bottom) in Apalachee Bay, Fla. (February to November
1977). Diet is given as the relative proportion of the dry weight of
stomach contents. Codes for the dietary components are given in
Table 1. Numbers in parentheses are the mean lengths offish.

variation in the diet of this ontogenetic group,
however, showed that plant material made up
only a small portion of the diet in winter and early
spring (Figure 7). Amphipod consumption was
highest in March and decreased through the
spring and fall, during which time plant material
became the most important food item. Consump-
tion of shrimp and shrimp postlarvae was low in
the spring but increased to as much as 30% of the
diet in the summer and fall. Consumption of
calanoid copepods by this fish size class was gener-
ally limited to winter. Harpacticoid copepods con-
sistently contributed a small amount to the diet of
these fish but consumption of isopods, crab zoea,
and polychaetes was sporadic.

For fish from 36 to 80 mm, temporal variations
in consumption of amphipods, plant matter, and
shrimp were analyzed with stepwise multiple re-
gression, using abundance of shrimp, amphipods,
polychaetes, and benthic macrophytes as inde-
pendent variables. Pearson correlation coef-
ficients show that consumption of amphipods
was negatively correlated with abundance of
shrimp and macrophytes in the field and positively
related to amphipod abundance (Table 5). The re-
lationships with polychaete abundance were
mixed. Multiple correlation coefficients explained
between 60.8 and 79.4% of the temporal variation
in amphipod consumption using from two to four
independent variables. Consumption of plant
matter by fish from 36 to 80 mm was positively
related to plant biomass and shrimp abundance.

Table 5. — Pearson correlation coefficients (r) and coefficients of
determination (r^) for percentages of total stomach contents (dry
weight) composed of amphipods, plant matter, and shrimp in
Lagodon rhomboides from 36 to 80 mm SL, tested as functions of
food abundance. AM = amphipods/m^, PC = polychaetes/m^,
PM = grams dry weight benthic macrophytes/ m^, and SH =
shrimp and shrimp postlarvae/m^.

Fenholloway 12

Econfina 10

Econfina 12

Step

r

r2

Step r r'

Step

r

r'

Amphipods consumed

SH

-0.561

0.315

SH -0.802 0.643"

AM

0.616

0.380

AM

-0.462

0.500-

PM -0.588 0.746"

SH

-0.126

0 664-

PO

0105

0.608-

PO -0.090 0.758-

PM

-0.574

n.s.

PM

-0.448

0.631-

AM 0.126 0.794-
Plant matter consumed

PO

0.524

SH

0.639

0.408-

PM 0.912 0.831"

PO

-0.714

0,510

AM

0.105

n.s.

SH 0.594 0.912"

SH

0.214

0,652-

PO

-0.257

PO -0.304 0.926"

AM

-0.694

0.786-

PM

0.428

AM 0.022 0.955"
Shrlmp consumed

PM

0.635

n.s.

PO

-0.034

n.s.

PO 0.654 0,428-

PM

0.496

n.s.

AM

0.316

AM 0.013 0.667-

SH

-0.116

PM

-0.218

SH 0.389 0.698-

AM

-0.388

SH

0.024

PM -0.401 0.741-

PO

-0.197

*P«0.05;"P=s0.01;n.s. = not significant.

344

STONER: FEEDING ECOLOGY OF LAGODON RHOMBOIDES

Plant consumption was inversely related to poly-
chaete field density at all three stations and rela-
tionships with amphipod abundance were mixed.
Multiple regression did not provide a satisfactory
model for variation in plant matter consumed at
Fenholloway 12, but plant and food item abun-
dances explained 78.6 and 95.5'7f of the variation
at Econfina 12 and 10. Explanation of temporal
variation in shrimp consumption by multiple re-
gression methods was successful only for fish from
Econfina 10 (r^ = 0.741). Shrimp intake increased
with shrimp abundance in the field and decreased
with plant and polychaete abundances. Other cor-
relations were low. Harpacticoid copepod con-
sumption was positively related to plant biomass
and negatively correlated with amphipod abun-
dance; however, multiple correlation coefficients
were not computed since no data were available on
harpacticoid abundance.

Diet of large pinfish (>80 mm SL) showed little
seasonality at Econfina 10, where plant material
made up at least 809c of the stomach contents on

>>

■D

C
(D

c
o
U

u

E
o

■t->

1 1 1

3 4 5 6

(93) (118) (115) (113) (121) (116) (113) (100) (96)

Month

Figure 8. — Seasonality in diet of Lagodon rhomboides >80 mm
SL from two stations (F 12-top, E 10-bottom) in Apalachee Bay,
Fla. (March to November 1977). Diet is given as the relative
proportion of the dry weight of stomach contents. Codes for the
dietary components are given in Table 1 . Numbers in parenthe-
ses are the mean lengths offish.

all dates. At Fenholloway 12, however, benthic
vegetation was less abundant than at Econfina 10
and major changes in diet occurred with season
(Figure 8). Clearly, large pinfish were carnivorous
during winter and early spring at Fenholloway 12,
but became herbivorous in May. Winter diet in-
cluded polychaetes, bivalves, amphipods, and
isopods. Animal material was unimportant in the
diets of fish taken during the rest of the year.

Temporal variation in the diets of adult fish was
not adequately explained with multiple regres-
sion, as obvious trends in plant consumption did
not follow seasonal patterns in macrophyte abun-
dance. Lack of temporal variation in diet at
Econfina 10 is due to the fact that plants were
readily available at that station when adult
pinfish were present (March through October). On
the other hand, at Fenholloway 12, macrophytes
were patchy in distribution and a high biomass in
April (Table 3) was composed largely of T. tes-
tudinum which was generally not consumed by
pinfish. Abundance of alternative prey organisms,
such as isopods and bivalves, may also explain
earn ivory of adult pinfish at Fenholloway in the
spring.

Breadth of diet in pinfish was examined by cal-
culating Shannon-Weiner diversity indices, H',
and by tabulating the number of food items that
individually contributed >1.0% of the total mass
of stomach contents for each fish size class, sam-
pling date, and station (Table 6, Figure 9). Dietary
diversity of pinfish between 16 and 80 mm was
lowest at the unvegetated site because two food
items, amphipods and calanoid copepods, over-
whelmed the importance of other foods. Low
abundance of alternative prey such as shrimp,
shrimp postlarvae, and benthic macrophytes
probably explain this occurrence. For fish >80

Table 6. — Dietary diversity, H', and number of food types
(individually contributing >1.0'7c of the total mass of stomach
contents) in Lagodon rhomboides from four stations in
Apalachee Bay, Fla. (mean ± SD). Within a fish size group, no
mean values were significantly different (AN OVA and Duncan's
multiple range test, P>0.05).

Size group (mm)

Fen 11

Fen 12

Econ 10

Econ 1 2

Dietary diversity. H'

— — 0.57±0.39 0.54±0.64
0.99r0.50 1.68 = 0.17 1.28 = 0.59 1.45 = 0.13
1.27 = 0.46 1.68 = 0.44 1.64=0.44 1.58=0.25

— 0.92 = 0.44 0.50 = 0.36 0.41=0.22

11-15

16-35

36-80

>80

11-15

16-35

36-80

>80

Number of food types

— — 2.2 = 0.9 2.7 = 2.0
5.0 = 2.8 7.5=2.1 5.5 = 2.3 5.8 = 1.2
6.2 = 1.7 8.6=2.4 8.1=3.0 7.2=1.2

— 6.2 = 2.3 4.4=1.7 4.5=0.7

345

FISHERY BULLETIN: VOL. 78, NO. 2

-♦-•

>

Q

(D

J.U

_

16- 35 mm

-

2.0

-

/*NC^

^

-

1.0

-

(

+
1

^

-

3.0

-

y^^^

36-80 mm

-

2.0

-

• 4

o

^^ <

/v

*%=*4

-

1.0

"

\N

f

N-

■

3.0

-

> 80 mm

-

2.0

-

i

X

-

1.0

-

>

^^^^'Vv^

-

0

— 1 r

i
1 r

r

» VY

I — 1 1 1 1 r-

DJFMAMJ JASON

Month

Figure 9. — Breadth of diet in Lagodon rhomboides from four
sites in Apalachee Bay, Fla., shown as a function of season. Each
value is the Shannon- Weiner index, H', for the food items con-
sumed by fish of three size classes. Crosses = Fenholloway 11,
triangles = Fenholloway 12, dots = Econfina 10, circles =
Econfina 12.

mm, dietary diversity was highest at the sparsely
vegetated station because, in addition to plant
material, mussels, polychaetes, and other animal
prey made an important contribution to the diet.
At the Econfina stations, the diets of adult fish
were dominated by plant material causing low
dietary diversity.

Pinfish between 36 and 80 mm SL showed
greatest breadth in diet; however, some degree of
seasonality in dietary diversity occurred in all fish
>15 mm (Figure 9). In fish between 16 and 35 mm,
peak dietary breadth in June and July corre-
sponded with periods of low amphipod abundance
and a change in food habits to alternative prey
types including shrimp and plant material. Low-
est dietary breadth in fish between 36 and 80 mm
occurred in the late winter and spring when am-
phipods were abundant and macrophyte biomass
was low. Diversity of food items available was
probably lowest at this time. Dietary diversity in
fish >80 mm SL reflected the degree of carnivory
by the fish. At Fenholloway 12 dietary diversity

346

was highest in March and April when various
animal foods were consumed in large quantities.
At Econfina 10, highest diversity occurred in Au-
gust when a large number of animal foods
supplemented a normally herbivorous diet. Dur-
ing late spring and summer months, dietary di-
versity indices at Econfina 10 and Fenholloway 12
converged to similar values as fish at both stations
became largely herbivorous. Very low dietary di-
versities occurred at Econfina 10 in September
and October because over 98% of the diet was
composed of plant material.

DISCUSSION

Pinfish from Apalachee Bay passed through five
major ontogenetic feeding stages, including 1)
planktivory; 2) carnivory on amphipods and har-
pacticoid copepods; 3) omnivory on amphipods,
shrimp, and microepiphytes; 4) omnivory on
epiphytes, amphipods, polychaetes, and isopods;
and 5) herbivory on epiphytes and vascular plant
material (primarily S. filiforme). Darnell (1958)
and Carr and Adams ( 1973) provide the most reli-
able data for comparison with the present study on
food habits of L. rhomboides since each provided
information on ontogenetic variation in the diets
of the fish. Darnell, studying stomachs of pinfish
from Lake Ponchartrain, La., found that the im-
portance of amphipods and other small crusta-
ceans decreased with pinfish length (40-150 mm
SL), while vegetable material became increas-
ingly important in diet with fish size. Except that
Darnell found dipterans to be a common food item
in fish from Lake Ponchartrain, his findings were
similar to mine. Pinfish collected near Crystal
River, Fla., showed five trophic stages (Carr and
Adams 1973); the stages were different from those
reported here (Table 7). Unlike pinfish from
Apalachee Bay, those from Crystal River became
herbivores at an early stage (36-60 mm SL), and
later showed strict carnivory on fish and shrimp
(>80 mm SL). Fishes were rarely found in the
stomachs of pinfish from Apalachee Bay and the
pattern of increasing herbivory with fish length
appeared to hold except at the unvegetated site
where plant material was not available. Because
stomach analyses for both geographical areas cov-
ered a full year, differences between the findings of
the two studies cannot be attributed to artifacts
introduced by seasonal variation in diet. Rather, it
is likely that different abundances of suitable prey
or plant items explain geographical differences in

STONER: FEEDING ECOLOGY OF LAGODON RHOMBOIDES

Table 7. — Trophic ontx)geny of pinfish collected at Crystal River
and Apalachee Bay, Fla. Crystal River data were taken from
Carr and Adams (1973).

Feeding stage

Size of fish
(mm SL)

10-

20

26-

30

36-

60

61-

80

81-

110

11-

15

16-

35

36-

80

81-

120

>

120

Crystal River
1 . Planktivore on copepods

2 Carnivore on shrimp, myslds, and amphipods

3 Herbivore on epiphytes

4. Omnivore on epiphytes, shrimp, and fish

5. Carnivore on shrimp and fish

Apalachee Bay

1 . Planktivore on copepods and Invertebrate eggs

2. Carnivore on amphipods and harpacticoids

3. Omnivore on amphipods. harpacticoids, shrimp,

and epiphytes

4. Omnivore on epiphytes, amphipods, polychaetes.

and Isopods

5. Herbivore on epiphytes and vascular plants

food habits just as food abundance explained local
variations in food habits among stations in
Apalachee Bay. Carr and Adams described their
study site as dominated by Ruppia maritima and
Halodule wrightii. In Apalachee Bay, benthic veg-
etation was dominated by T. testudinum; there-
fore differences in food habits of pinfish between
the two areas, may be due to characteristics of the
habitat other than prey abundances. For example:
1) the wide blades of T. testudinum may provide
better refuge from predation for shrimp and other
crustaceans than that provided by narrow blades
ofi?. maritima and//, wrightii, and/or 2) the plant
material near Crystal River was, in some way,
unsuitable as food for large pinfish. Hansen ( 1969)
also reported that plant material was the domi-
nant food item of pinfish from dense Thalassia and
Ruppia beds in Pensacola Bay, Fla., suggesting
that some characteristic of Thalassia beds pro-
motes herbivory in pinfish. Similar to the present
study, Hansen found that seasonal variation in
plant consumption was related to seasonal avail-
ability of benthic macrophjdes.

Trophic ontogeny in pinfish can be explained in
terms offish morphology. Width and height of the
mouth in the open position was linearally related
to standard length of pinfish and increased body
and mouth size permitted pinfish to capture a
broader range of prey sizes (Stoner 1979a). The
same characteristics undoubtedly explain in-
creases in numbers of prey types associated with
increasing body size in juvenile fish. Increasing
range of prey sizes and types with fish body and
mouth size has been reported by many authors
(e.g., Wong and Ward 1972; Ware 1972, 1973; Ross
1978). Transition to herbivory by pinfish, first as a
microepiphyte nibbler and later to a seagrass
grazer is associated with changes in dentition with

growth. Very fine conical jaw teeth only are found
in fish at 15 mm SL, but conical teeth are replaced
by longer caninelike teeth in fish between 23 and
35 mm. Conical and canine teeth are well adapted
for capturing small animal prey, but chisel-shaped
incisors, which appear in fish >35 mm, provide
pinfish with the dentition required to graze plant
material. Because of its dentition, the pinfish is
probably an obligate carnivore until it reaches
about 35 mm SL (for further discussion and illus-
tration of ontogeny in pinfish dentition, see Cald-
well 1957).

Given the morphological constraints of L.
rhomboides, its reproductive seasonality is par-
ticularly well adapted for exploitation of food re-
sources in seagrass meadows of Apalachee Bay.
Postlarval pinfish entered the seagrass beds in
midwinter at the time of peak abundance of cala-
noid copepods, appropriately small prey or-
ganisms. Winter spawning placed juvenile fish
(16-35 mm) on the seagrass beds in the spring
when the most valuable prey species, amphipods
and harpacticoid copepods, were beginning to re-
produce and reaching maximum abundance
(Stoner^; Thistle^). Optimal prey for larger pinfish
(36-80 mm) probably includes larger organisms
such as shrimp which had peak abundance in the
fall. Reproductive timing and growth placed large
pinfish on the grass beds in the fall. The life his-
tory strategy of L. rhomboides, therefore, appears
to be adapted to seasonal patterns of productivity
and abundance in prey and macrophyte species.
Although pinfish were among the fishes that were
shown to influence the abundance of zooplankton
in the Newport River estuary (Thayer et al. 1974),
it is unlikely that pinfish postlarvae affect the
abundance of calanoid copepods in Apalachee Bay
because of the low number of pinfish postlarvae in
the shallow bay (Brady 1980). However, pinfish
probably do regulate the abundance of certain
amphipod species in the bay (Stoner 1979a, b).

Variation in food habits with space, both on
local and geographic scales, was a function of food
availability and habitat structure. Food habits of
fishes in Apalachee Bay were dramatically differ-
ent at stations separated by distances as little as 2

^Stoner.A. W. 1980. Abundance, reproductive seasonality,
and habitat preferences of amphipod Crustacea in seagrass
meadows of Apalachee Bay, Florida. Manuscript in review.

6D. Thistle, Assistant Professor, Department of Oceanog-
raphy, Florida State University, Tallahassee, FL 32306, pers.
commun. December 1978.

347

FISHERY BULLETIN: VOL. 78. NO. 2

km. At the station where vegetation and epiben-
thic prey organisms were sparse, pinfish took more
food from the water column (e.g., copepods, chae-
tognaths, and polychaete larvae) than at other
stations. Due to the lack of vegetable matter at
this station, pinfish consumed Brachidontes exus-
tus which lives on oyster bars near the unvege-
tated site. A high percentage of empty stomachs at
the unvegetated site indicates that feeding condi-
tions there were poor, especially for postlarval and
adult pinfish. Although selection of food by fish is
confounded by food preferences, the consumption
of food by pinfish appears to reflect local, geo-
graphic, and seasonal abundances of the food or-
ganisms and the morphological limitations of the
consumer.

Temporal variations in the food habits of L.
rhomboides were well explained by abundance of
prey types in the field, but the correlations were
complex. Amphipod, shrimp, and plant consump-
tions were all directly related to the abundance of
these primary food items in the field. Seasonal
relationships between food abundance and con-
sumption by fishes were observed by Lawler
(1965), Repsys et al. (1976), and Hickey (1975).
Diurnal changes in food habits have also been
explained by changes in prey availabilities (Hob-
son and Chess 1976; Robertson and Howard 1978).
Keast's ( 1 970) observation that close correlation of
prey availability with seasonality in food habits
holds for only the most important prey types was
also observed in this study. For example, poly-
chaetes were relatively minor components of
pinfish diets and showed no correlation with sea-
sonal abundance patterns. On a statistical basis,
however, absolute abundance of a food item in
Apalachee Bay explained only part of the varia-
tion in consumption of that item. For example,
although amphipod consumption by juvenile
pinfish was directly related to amphipod abun-
dance in the field, amphipod intake was also in-
versely related to shrimp and plant abundances.
These inverse relationships were often stronger
than the positive relationship with amphipod
abundance. Similarly, shrimp consumption was
negatively correlated with amphipod and plant
abundances, suggesting that the relative abun-
dance of preferred prey items may be as important
as absolute abundance of any one type. The picture
is further clouded by the fact that plant material,
which serves as an important food source for
pinfish >35 mm, is also an obvious component of
the habitat that lends protection to many small

348

prey species (Nelson 1978; Stoner 1979a). Two ex-
planations for the increased plant consumption
with benthic macrophy te biomass are plausible: 1 )
plant material is taken as a simple response to its
abundance, and/or 2) T. testudinum blades pro-
vide amphipods, shrimp, and other animal prey
with protection from fish predation and inhibit the
consumption of these animals; therefore, as blade
density or plant biomass increases, macrophytes
and epiphytes are taken as alternative food. Both
mechanisms are probably influential in the de-
termination of food habits in pinfish; however, the
latter hypothesis is probably the most important
mechanism since cellulase activity is not found in
the alimentary tract of L. rhomboides (Stickney
and Shumway 1974). Densely vegetated seagrass
habitats support greater densities and biomass of
potential prey species than unvegetated or
sparsely vegetated substrates (O'Gower and
Wacasey 1967; Orth 1977; Brook 1978; Stoner in
press), although is is unknown as yet whether
this relationship is due to reduced predation on the
animals or some property inherent in the struc-
ture of the habitat. The problem of omnivory in
pinfish would be an especially fertile area for in-
vestigation in terms of optimal foraging theory,
but a large array of carefully controlled field and
laboratory experiments would be required.

Dietary specialization is generally found to be
correlated with increasing food abundance. This
conclusion is supported by models of predator-prey
relationships (see review by Pyke et al. 1977) and
empirical studies with fishes (Ivlev 1961; Zaret
and Rand 1971; Werner and Hall 1974). On the
basis of seasonal prey abundance patterns and the
diets of pinfish between 16 and 80 mm SL, dietary
specialization did occur with periods of high prey
abundance. For example, at the vegetated stations
amphipods and other macrobenthic organisms
were most abundant between February and May.
Lowest dietary diversities occurred during the
same time period. With adult fish, however, the
characteristic relationship did not seem to hold.
Fenholloway 12 and Econfina 10 showed similar
seasonal trends in abundance of food organisms
yet seasonality of dietary diversity was entirely
different at the two stations. Also, on a spatial
basis, lowest dietary diversity occurred at the site
with extremely low food abundance (Fenholloway
11) for fish between 16 and 80 mm SL. More
generalized diets were found at the vegetated sites
where food was more abundant. The predicted re-
lationship of increasing dietary specialization

STONER: FEEDING ECOLOGY OF LAGODON RHOMBOIDES

with increasing food abundance did not hold in
certain instances because the abundance of
macrobenthic organisms at the study site was
closely related to standing crop of benthic macro-
phytes at the site (Stoner in press). Also, since
seagrasses and epiphytes serve as important di-
etary components of larger pinfish, prediction of
dietary diversity is further complicated.

Data provided in this study further verify the
conclusion that L. rhomboides is a generalist
feeder. Schoener (1969) suggested that generalist
feeding strategy is favored when: 1) food density is
low and there is a premium on the ability of the
animal to take a range of prey, 2) the predator has
a relatively long period to gain energy, and 3 ) prey
densities fluctuate widely. Given the relatively
low abundance of prey species in Apalachee Bay,
the great diversity of potential prey items, and
their high degree of variability with time and
space, the generalist feeding strategy exhibited by
L. rhomboides would be predicted by Schoener's
model.

The detailed analysis of the food habits of L.
rhomboides provided in this study accentuate
difficulties inherent in the description of a trophic
niche. Because of dramatic variation in food habits
and dietary breadth in coastal fishes, serious
methodological problems arise in description of
food habits. In most cases, length-frequency dis-
tributions offish are not constant with time; con-
sequently, when animals are not placed in size
classes or when placed in overly large size classes,
dietary variation may be due to either seasonal
changes in food habits or increasing fish size. The
diet of a group of fish will be a function of the
length-frequency distribution of the population if
variation with size occurs. When food habits are
examined by size and not by season, variation
within a given size class may appear greater than
is actually true at any particular time, and sea-
sonality of diet is completely obscured. Variability
in food habits as a function of space (a common
occurrence) adds still one more dimension to the
problem of describing an animal's food and feeding
habits, but spatial variation is usually ignored.
Keast (1970), in a study of the bioenergetic inter-
relationships of cohabiting freshwater fishes in
Ontario, provided insight into the complex in-
teractions of fish size and season in determining
food habits. One other study (Nakashima and
Leggett 1975), an investigation of responses of
yellow perch to different levels of phytoplankton
and benthic biomass in Lake Memphremagog,

Quebec- Vermont, showed interactions of time and
fish size in diet determination. The dimension of
space was added by comparing the diets of fish
from the northern and southern basins of the lake.
Few studies have described more than one dimen-
sion of an animal's food habits.

Peters (1977) stated that the "Trophodynamic
Concept" (Lindeman 1942) is based upon the
premise that organisms in an ecosystem are
categorized according to their distance along a
food chain from the sun. He pointed out, however,
that the real world is constructed of complex food
webs and organisms do not fall into neat
categories such as "primary consumer" or "sec-
ondary carnivores." This is not a new idea. In
1961, Darnell asserted that "trophic level" is an
inoperational term since: 1 ) animals of a given size
and belonging to a single species take food from
several sources, 2) alternate foods are frequently
utilized as a function of their availabilities, 3) an
ontogenetic progression of food habits is common
in animals, and 4) many animals are dependent
upon detrital material which is itself of a complex
origin and an undefined distance from primary
producers. Regier and Henderson (1973) and
Kercher and Shugart (1975) provided similar
reasoning for the inadequacies of the trophic level
concept. Darnell recommended a spectral ap-
proach to the food habit problem and Kercher and
Shugart defined an "effective trophic position,"
actually a continuous index of trophic position
rather than the conventional discrete level.
Neither solution to the problem addressed all of
Darnell's objections and gave an accurate por-
trayal of the functional role of the organism in its
ecological context. Data provided in this paper
show that, in addition to ontogenetic pattern in
food habits, animals within given size classes take
foods from several sources with the possible excep-
tion of postlarval pinfish which are collected only
in the winter and early spring. Fish of many size
classes consumed significant quantities of cala-
noid copepods which are probably herbivores; har-
pacticoid copepods which may be detritovores,
herbivores, or carnivores; amphipods which show
wide variety in food habits; plus shrimp, inverte-
brate eggs, and many other invertebrate taxa. In
most cases, the prey species themselves cannot
reliably be placed in any one trophic level and,
since individuals of a given species were consumed
at different developmental stages, and prey
species may show trophic ontogeny, the problem of
assigning a trophic level to the predator is further

349

FISHERY BULLETIN: VOL. 78, NO. 2

confounded. Pinfish >35 mm SL nearly always
contained both plant and animal material in their
stomachs. Omnivory, of course, automatically
makes the fish both a "primary" and "secondary
consumer." Darnell's (1961) suggestion that pred-
ators commonly utilize food resources according
to their availabilities was clearly demonstrated in
this paper as it related to other spatial and tem-
poral patterns of food abundance in Apalachee
Bay. Although pinfish do not rely directly on detri-
tal material as a source of nutrition, many of its
prey organisms do (e.g., certain harpacticoid cope-
pods, amphipods, shrimps, and polychaetes). Be-
cause it is difficult to place detritovores in trophic
levels, the predatory fish also falls within no dis-
crete level. On these bases, the trophic level con-
cept is rendered inoperational for relationships
involving the dominant epibenthic fish in
Apalachee Bay. Furthermore, because of migra-
tion of consumers and wide variation in food
habits with season and consumer growth, one may
never assume that food webs, predator-prey rela-
tionships, or the functional role of a predator are
static. The taxonomic species is not, in many cases,
a functional ecological unit. At the very least,
ontogenetic feeding groups should be incorporated
in ecological models. These "trophic units" would
be particularly useful where the true ecological
role of the animal in a model is important. Except
in the most simple food webs, without precise
knowledge of variation in food habits and diet
breadth, models of energetic pathways and
predator-prey relationships and measurement of
niche breadth and overlap will be accurate neither
in theory nor in practice.

Characteristics of prey species which mediate
predation include absolute and relative abun-
dances, conspicuousness, size, palatability, defen-
sive morphology and behavior, spatial distribu-
tion including microhabitat and aggregation, and
nutritional value. All of the above, however, are
limited or mediated by various elements of the
environment including temperature, turbidity,
dissolved oxygen, light, water motion, and struc-
tural aspects of the habitat. Although a great deal
of research has been conducted concerning the im-
portance of predator and prey characteristics,
most of the work has been done in structurally
simple systems, including mud bottom, freshwa-
ter pond, and water column habitats where the
number of food species is relatively low. Data from
this and another paper (Stoner 1979b) show
that seagrass blades and rhizomes provide a very

important structural component in seagrass
meadows which affect both predator and prey
species and their interactions. Since seagrass
biomass, blade densities, and species compositions
vary over both time and space, plant-animal and
predator-prey relationships are in constant flux.
The seagrass habitat, therefore, is an extremely
complex system within which the ecological roles
of predation and habitat structure are ever chang-
ing. The need for further investigation is obvious.

ACKNOWLEDGMENTS

This research was supported by grant number
R-805288010 from the U.S. Environmental Pro-
tection Agency to Robert J. Livingston. I wish to
thank all of those graduate and undergraduate
students who helped with field collections. E. L.
Bousfield, H. Greening, H. Kritzler, F. G. Lewis, S.
L. Santos, P. F. Sheridan, and J. L. Simon provided
assistance with the taxonomy of various benthic
organisms. Aid with computer programming and
statistical procedures was generously provided by
G. C. Woodsum and D. Zahn. L. G. Abele, W. F.
Herrnkind, R. A. Laughlin, K. M. Leber, F. G.
Lewis, R. J. Livingston, R. W. Menzel, R. W.
Yerger, and an anonymous reviewer helped to
point out several inconsistencies in the manu-
script at various stages.

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352

OBSERVATIONS ON A MASS STRANDING OF SPINNER DOLPHIN,
STENELLA LONGIROSTRIS, FROM THE WEST COAST OF FLORIDA

James G. Mead,' Daniel K. Odell,^ Randall S. Wells,'' and Michael D. Scott"

ABSTRACT

The spinner dolphin, Stenella longirostris, while well known in portions of the Pacific Ocean, has rarely
been available for study in the Atlantic. Data from 28 individuals from a mass stranding in Florida
enabled us to make preliminary estimates of mean size and age at sexual and physical maturity,
reproductive seasonality, and sexual dimorphism for this species in the southwest Atlantic. Our
sample most closely resembles the Hawaiian populations described by Perrin, but further work in the
Atlantic is likely to demonstrate other populations differing morphologically from this one.

The spinner dolphin, Stenella longirostris, is
widely distributed in tropical to warm temperate
waters of the world (Perrin 1975), but due to its
predominately pelagic habits, is seldom found
stranded and is not generally taken in coastal
fisheries. As a result, very little is known of its
biology except in the eastern tropical Pacific,
where it is taken in considerable numbers inciden-
tal to purse seining for yellowfin tuna. Perrin et al.
(1977) have recently published investigations on
the eastern population of spinner dolphin from the
Pacific.

The species is apparently common in the Carib-
bean (Caldwell et al. 1971; Erdman et al. 1973;
Taruski and Winn 1976), but there are few rec-
ords, all of them strandings, from the Gulf of
Mexico. Gunter (1954) did not find any evidence
of this species in the Gulf of Mexico. Layne (1965)
reported on a mass stranding of this species from
Dog Island, Fla. (lat 29 48' N, long. 84 38' W),
where 36 animals stranded on September 1961.
Lowery (1974) reported a single adult male from
Fort Walton Beach, Fla. (lat. 30^24 ' N, long. 84°47 '
W). Schmidley and Shane^ reported a 158 cm male
which stranded alive at Sabine Pass Beach, Tex.,
on 16 May 1976, and a pregnant 188 cm female

'Division of Mammals, Smithsonian Institution, Washington,
DC 20560.

^Rosensteil School of Marine and Atmospheric Sciences, Uni-
versity of Miami, Miami, FL 33149.

^Department of Zoology, University of Florida, Gainesville,
Fla.; present address: Center for Coastal Marine Studies, Uni-
versity of California, Santa Cruz, CA 95060.

■•National Fish and Wildlife Laboratory, Gainesville, FL
32601.

=Schmidley, D. F., and S. H. Shane. 1978. A biological as-
sessment of the cetacean fauna of the Texas coast. Final Rep.,
U.S. Marine Mammal Commission Contract MM4AC008, avail-
able Natl. Tech. Inf Serv., Springfield, Va., as PB 281763, 38 p.

Manuscript accepted October 1979.
FISHERY BULLETIN; VOL. 78, NO. 2, 1980.

found on Padre Island, Tex., during March 1975.
Shane ( 1977) reported two additional records from
Padre Island: a 173 cm female which stranded
about January 1976 and a 183 cm male on 4 June
1977. The present study is based on 28 animals
from a single mass stranding on the west coast of
Florida.

At this point it is not possible to determine
whether the occurrences recorded from the west
coast of Florida were derived from a population in
the Gulf of Mexico or were strays from the Carib-
bean. While there is a small fishery for mixed
species of dolphins in the Caribbean (Caldwell et
al. 1971), catches of spinner dolphin are relatively
infrequent and are unlikely to have an apprecia-
ble effect on the population. In contrast, the popu-
lations studied by Perrin and others in the Pacific
are taken in large numbers incidental to purse
seining for yellowfin tuna.

The causes of mass strandings of cetaceans are
still very little understood (see Geraci 1978 for a
recent review of the subject). It is clear that this is
a very complex problem which goes far beyond the
scope of this paper. It is also clear that much of our
lack of understanding is based upon a lack of in-
formation on the species involved. We have felt
that it was also important to include material on
the circumstances of the stranding itself, even
though this is not directly related to the conclu-
sions drawn from examination of the specimens.

CIRCUMSTANCES OF
THE STRANDING

The stranding occurred on the north end of
Casey Key, with most of the dolphins concentrated

353

FISHERY BULLETIN: VOL. 78, NO, 2

at about lat. 27°12'10" N, long. 82°30'30" W (Fig-
ure 1). The animals began coming ashore about
2200 h e.d.t. on the evening of 13 July 1976. At
that time the wind was westerly at 10-15 mi/h,
seas were running about 2 ft, and there was an
extreme low tide at 2211 h. Upon discovering the
animals, local residents attempted to direct them
back to sea or move them to more sheltered areas.

Most observers concurred that there was a great
deal of noise coming from all of the dolphins when
they first came ashore, including much "squealing
and crying," but that this later subsided. The ani-
mals were quite passive on the beach, with the
exception of one large animal that reacted vio-
lently to handling and died during the short trip to
Midnight Pass. Most of the dolphins did not resist
handling and were easily walked to the shallow
sand bar 10-15 m from shore, where they were
pointed seaward, held until they began rhythmic
swimming motions, and then given a push
offshore. This was believed to be successful with
some of the animals, but in many cases they would
turn towards the south with the first wave that
came over the bar and be washed back onto shore.

Eight to 10 animals, one of which was marked
on the dorsal fin with a cattle ear tag, were moved
to the more sheltered waters of Midnight Pass and
released in there. A single small animal (possibly
504457)^ was released in Little Sarasota Bay. The
last live animal to come ashore with the initial
stranding was 504449 which was found at 0130 h
and died while attempts were being made to direct
it back to sea. Estimates of the total number of
animals ranged from 50 to 150, with most of the
observers agreeing on the lower number.

Early morning of 14 July, four large animals
and a calf stranded just north of Turtle Beach on
Siesta Key, about 2 km north of the original
stranding. Three of the large animals were di-
rected back to sea, one died on the beach and was
subsequently lost, and the calf (504459) was
moved to Turtle Lagoon where it died. All of the
live animals were off of the beach by 0800 h.

Later that morning, two live animals were
picked up, one from the northeast end of Casey
Key along the Intracoastal Waterway, and one
from the grass beds just east of Bird Keys. The
animal which had been tagged the night before
(504434) was recovered dead from the latter area.
Both of the live animals were probably from the

GULF

OF
MEXICO

NICE

27 30

27 15

82 30

82 15

®The six digit numbers used to identify the animals are catalog
numbers of the United States National Museum, where the
skeletal remains have been deposited.

Figure l. — Central west coast of Florida localities involved in
the mass stranding of spinner dolphin.

group that had been transported and released at
Midnight Pass. The live animals were held in an
impoundment at the Mote Marine Laboratory on
Siesta Key until they were picked up by Sea World
and transported to holding facilities at Orlando,
Fla., on 15 July. One of these (504456) died the
next day; the other (504455) died 4 days later. A
dead calf (504458) was recovered from the south-
ern tip of Siesta Key, a dead adult (504451) was
picked up on the west side of Bird Keys, and the
accumulation of dead animals at the original
stranding site on Casey Key was recovered and
put on ice at the Mote Marine Laboratory on 14
July.

Late afternoon of 15 July, we received notifica-
tion that a small dolphin had been seen in the
Intracoastal Waterway near marker no. 23 about
6 km south of Midnight Pass. This animal
(504457) was found just after dark swimming
slowly near shore and whistling loudly. It was
picked up alive, but died early the next morning
while being transported to Orlando. This was
probably the calf which had been released in Little
Sarasota Bay on 13 July.

The last animal to be recovered was the decom-
posed carcass of an adult male that was picked up
on 16 July from Casey Key (504460).

An aerial survey was flown in a U.S. Coast
Guard helicopter from 1800 to 2000 h on 14 July
and on the afternoon of 16 July. No animals other
than the dead ones on the beach were seen. The

354

MEAD ET AL.: OBSERVATIONS ON MASS STRANDING OF SPINNER DOLPHIN

stranding received a great deal of publicity from
the news media, and it would be expected that we
would have been notified if any additional animals
had turned up on the coast.

Most of the dolphins bore minor abrasions that
were probably incurred while stranding. Only one
(504448) exhibited any appreciable physical dam-
age. This animal, the largest male of the group,
had two large shark bites on the left flank at about
midlength and a third which completely removed
the left fluke. These bites appeared to have been
inflicted after death.

NECROPSY

One specimen was necropsied late on the even-
ing of 14 July, the others on 15 July. The two
animals which were transported to Sea World
were necropsied on 16 and 20 July by the Sea
World staff. A variety of lesions were observed in
the sample necropsied on 15 July. Most were
parasitic and not serious enough to account for
death. The blubber layer appeared thin, but this
was due at least in part to postmortem changes in
the hot sun and measurements were not taken.

The stomachs of all specimens except the three
calves were empty. Nicholas Hall (Department of
Neuropathology, University of Florida, Gaines-
ville, FL 32601) collected the brains from the ani-
mals necropsied on 15 July for neuropathological
examination. Helminth parasites were collected
and forwarded to Donald Forrester (Laboratory of
Wildlife Disease Research, University of Florida,
Gainesville, FL 32611). Gonad samples were col-
lected and later analyzed at the Smithsonian In-
stitution by Mead. Teeth were taken from all of the
animals except the calves and were sectioned at
about 175 /xm in thickness by Odell using a
Buehler Isomet Low Speed Saw'', and were read for
age determination by Odell and Mead. External
measurements were taken by Wells and Scott
while the animals were still on the beach, and
organ weights were taken during the necropsies.
Copies of all the measurements and necropsy data
are in the Marine Mammal Program files (Divi-
sion of Mammals, Smithsonian Institution,
Washington, DC 20560). Skeleton materials from
the specimens are being studied by William F.
Perrin (Southwest Fisheries Center, NMFS,
NOAA, La Jolla, CA 92038).

REPRODUCTIVE DATA

The female reproductive tracts were removed,
flat diameter of uterine horns measured at their
midlength, ovaries collected and fixed, uterus
opened and examined for fetuses, and mammary
glands checked for gross indications of lactation.
The ovaries were examined for externally visible
corpora, indications of large maturing follicles,
and were weighed. The ovaries were subsequently
sectioned by William F. Perrin, providing
confirmation of the external examination and an
exact count of the corpora albicantia. None of the
animals were visibly pregnant and only one
(504456) was lactating. For practical purposes,
females were considered sexually mature if there
were external indications of at least one corpus on
the ovaries. There was only one individual
(504440) in which there was a discrepancy be-
tween the results of the external ovarian exami-
nation and the sectioning (Table 1). In this case a
large follicle was probably mistaken for a corpus
albicans on external examination.

The smallest sexually mature female was 187
cm long, and the largest immature female was 190
cm long. A 177 cm female showed no indications of
follicular development, while four animals be-
tween 180 and 186 cm showed external indications
of maturing follicles. The diameter of the larger of
the two uterine horns showed a considerable in-
crease (about twofold) at sexual maturity.

The good correspondence between ovarian con-
dition and diameter of the uterine horns indicates
that the latter may be a useful character for defin-
ing sexual maturity, as it is probably the result of
pregnancy.

It seems likely that females begin to mature at
about 180 cm and reach sexual maturity at a
length of about 188 cm and a weight of about 55 kg.
The 188 cm pregnant female reported by Schmid-
ley and Shane (see footnote 5) fits this interpreta-
tion.

Considering only those females in which the
pulp cavity of the tooth was open and for which an
exact count of growth layer groups^ could be made,
there were four sexually immature animals, with
a mean of 8.25 growth layer groups (7, 8, 8, and 10
groups), and three sexually mature animals, with
a mean of 10 groups (7, 11, and 12 groups). Al-

''Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

^Terminology adopted at International Workshop on Deter-
mining Age of Odontocete Cetaceans, 8-19 September 1978,
Southwest Fisheries Center, NMFS, NOAA, La Jolla, Calif.

355

FISHERY BULLETIN: VOL. 78, NO, 2

Table l. — Reproductive data on female spinner dolphin stranded in Florida. Epiphyses: 0 = open; 1 = closed; 2 = fused.
Sexual maturity: 0 = mature; 1 = maturing; 2 ^ mature. Ages are in number of dentinal growth layer groups with +
signifying that the pulp cavity was closed and the age was greater than the number of visible groups. The right and left ovaries
were confused on 504437. However, they are presumed to correspond to the relative diameter of the uterine horns.

Gonad

Uterine

Ovarian

[

USNM

Length
(cm)

Weight
(kg)

Age

Epiphyses

we

ight (g)

diameter (

cm)

corpora

Sexual

number

Right

Lett

Right

Left

Right

Left

maturity

504438

177

49

10

0

0.81

0.76

1.5

1.5

0

0

0

504450

180

54

8

0

0.48

1.47

15

1.5

0

0

1

504449

181

46.1

7

0

0.45

1.36

1.4

1.5

0

0

1

504453

183

47.5

8

0

0.50

1.08

1.5

1.5

0

0

1

504454

186

54

7

0

0.29

1.02

1.2

1.2

0

0

1

504441

187

55.3

8 +

0

1.16

4.29

2.0

2.8

0

4

2

504444

189

53

11 +

0

0.37

1.58

18

1.3

0

0

1

504440

190

56

7

0

0.81

1.85

1.3

1.6

0

0

1

504437

195

61.1

12

0

0.95

6.3 +

1 9

3.0

0

1

2

504433

196

60.3

6 +

1

1.39

1.99

1.9

2.3

0

7

2

504445

197

64

—

0

1.57

2.46

1-6

2.0

0

1

2

504451

201

65.2

11

2

1.22

5.11

29

3.0

0

9

2

504456

204

59

—

—

1.55

4.5

—

—

—

—

2

though sample size is small, it gives a useful pre-
liminary estimate of age at sexual maturity of
7-10 growth layer groups (7-10 yr, seePerrin etal.
1976, 1977 for discussion of alternative growth
layer-age relationships).

Comparable figures were given by Perrin et al.
(1977) for the eastern spinner dolphin from the
Pacific. They found a mean length at sexual
maturity of 165 cm which is appreciably shorter
than the estimate for this sample ( 188 cm). This is
due at least in part to the eastern spinner dolphin
being a relatively smaller animal (mean length of
sexually mature females was 171 cm, whereas it
was 197 cm for this sample). Perrin et al. (1977)
found that mean age at sexual maturity was 5.5
growth layer groups, which may represent a de-
crease in age at sexual maturity as a result of
fishing pressure on the eastern spinner popula-
tion. This also might contribute to the shorter
length at sexual maturity in that population.

As appears to be the case with many delphinids,
there was a marked dominance of the left side of
the reproductive tract (Harrison et al. 1972). In all

of the mature or maturing animals, the left ovary
was decidedly larger than the right, and only one
animal (504441) bore any externally visible cor-
pora on the right ovary. There was a correspond-
ing asymmetry in the size of the uterine horns,
with the left being equal to or larger than the right
in all but one animal (504444), indicating that the
greater number of pregnancies were carried in the
left horn.

The testes were measured, weighed with the
epididymis removed, and a sample taken for his-
tological examination. Sections of testis samples
were cut at 10 /xm, stained with hematoxylin and
eosin, and the diameter of the seminiferous
tubules measured with an ocular micrometer. The
tubules were randomly selected for examination,
but only those approaching a direct rather than an
oblique cross section and free from obvious ar-
tifacts of sectioning or decomposition were chosen
for measurement. The least diameter was mea-
sured and the results given in Table 2 are the
mean of 10 tubules, at a depth of about 1 cm from
the surface of the testis. Tubules were also mea-

TABLE 2. — Reproductive data on male spinner dolphin stranded in Florida. Epiphyses: 0 = open; 1 = closed; 2 = fused. Sperm in
epididymis: 0 = none; 1= present; 2= copious. Testis activity: 0 = no spermatogenesis; 2 = active spermatogenesis. Sexual maturity: 0 =
immature; 1 = maturing; 2 = mature. Ages are in number of dentinal growth layer groups, with + signifying that the pulp cavity was
closed and the age was greater than the number of visible layers.

Gonad

Gonac

i

USNM

Length
(cm)

Weight
(kg)

Age

Epiphyses

wen

3ht (g)

length (cm)

Sperm in
epididymis

Testis
activity

Tubule
diameter

Sexual

number

Right

Left

Right

Left

maturity

504434

188

51

7

0

18

17

11

10

0

0

62

0

504435

189

55.8

7

0

250

220

24

20

0

1

136

1

504455

190

63.6

8 +

320

310

—

—

1

—

—

1

504439

192

65.5

9+

1

730

720

32

30

—

1

244

2

504436

194

65.3

10

0

400

430

23

24

2

1

185

2

504442

195

60

10

—

—

460

27

27

1

1

180

2

504443

197

68

9 +

1

560

550

27

25

1

1

200

2

504447

197

63.8

7+

0

96.5

100

15

16

1

0

80

0

504446

201

75

9+

2

860

870

31

32

2

1

196

2

504452

203

63.6

9 +

—

500

500

27

27

1

1

173

2

504448

208

69 +

8 +

1

980

870

36

35

2

—

—

2

356

MEAD ET AL.: OBSERVATIONS ON MASS STRANDING OF SPINNER DOLPHIN

sured near the surface of the testis and it was
noted that tubule diameter averaged about 10%
less at that level in the mature males. The process
of selection of the tubules for measurement may
have introduced a slight bias in favor of smaller
tubules, as these are possibly less likely to have
been affected by decomposition artifacts. Much of
the variation in tubule diameter within an indi-
vidual slide may have been the result of autolytic
distortion, which would tend to increase the
diameter of the tubules.

There is a sharp increase in the size of the testes
of animals with length of 188 or 189 cm (Table 2),
which apparently is the size range at which mat-
uration of the testes begins. Spermatogenesis was
taking place in the testes of the 189 cm individual,
but the testes weights were still low relative to
those of fully mature animals and no sperm was
present in the epididymis. In the next largest ani-
mal (190 cm), the testes were slightly larger and
sperm was present in the epididymis, indicating
that this animal was functionally sexually ma-
ture. All of the animals above 190 cm had large,
active testes and were sexually mature, with the
exception of a single 203 cm individual (504452),
whose testes were markedly small, though there
was a slight indication of spermatogenesis. The
body weight of this animal was also low for its
length, and it is probable that it was an abnormal
individual.

Although the sample of males was too small to
statistically define sexual maturity, it seems
likely that maturation begins around a body
length of about 190 cm and a weight of about 60 kg,
and maturity is reached at a length of about 192
cm and a weight of about 65 kg. Animals with a
seminiferous tubule diameter of less than about
150 fjLm were immature or maturing, and those
with a diameter in excess of this were sexually
mature. The corresponding figures for testis
weight and length were about 300 g and 24 cm.
The sample of males with the pulp cavity open in
the teeth consists of only four specimens. One of
these did not have well-defined growth layers,
leaving only three usable individuals. These are
an immature animal with 7 growth layer groups
and two mature animals with 10 groups.

Perrin et al. ( 1977) found a mean length at sex-
ual maturity of about 175-180 cm (the middle of
several estimates based on different criteria, and
the estimate which is most comparable with that
applied to the present sample) and a mean age at
sexual maturity of about 10-12 groups in the east-

ern spinner dolphin. As was seen when comparing
the sexual maturity figures for females from the
two populations, the eastern spinner reaches
maturity at a shorter length than our sample from
the Gulf of Mexico. In the case of males, the ages at
attainment of sexual maturity are more similar
and the length difference is probably due to popu-
lation differences in mean size of individuals.

PRODUCTIVE SEASONALITY

Of the six mature females in this sample, one
(504456) was lactating and one had a large corpus
luteum with no visible conceptus. Both of these
had probably given birth recently. None of the six
were pregnant. Six of the seven mature males
were examined for presence of sperm in the
epididymis. Sperm was present in all six and was
judged to be copious in three. Admittedly, this is a
very small sample, but it is indicative of recent
calving and breeding activity.

Perhaps the most convincing evidence for recent
reproductive activity in this sample are the three
calves which were present, with lengths of 90, 91,
and 97 cm. Perrin et al. ( 1977) estimated length at
birth in the eastern spinner to be 75.5 cm. Since
the mean lengths of mature animals and the mean
lengths at attainment of sexual maturity in the
Florida sample are uniformly about 14*7^^ greater
than the corresponding figures for the eastern
spinner dolphin, it is logical to assume, for an
initial approximation, that length at birth would
also be about 14% greater, or about 86 cm. Perrin
et al. ( 1977) estimated the postnatal growth rate
in the first 10 or 11 mo after birth to be 4.77
cm/mo. Again, allowing a difference of 14% for the
larger mean size in the Florida sample, a usable
estimate of the growth rate during this period
would be 5.4 cm/mo. This provides projected ages
for the two smaller calves of about 1 mo old, and for
the larger of about 2 mo, with birth dates of mid-
June and mid-May.

The only other data available for spinner dol-
phins in the Gulf of Mexico are the 8.1 cm fetus
which Layne (1965) found in an animal which
stranded in mid-September and the 61 cm fetus
which Schmidley and Shane (see footnote 5) found
in early March. Using the fetal growth curve for
the eastern spinner (Perrin et al. 1977), and as-
suming that the mean size difference between the
populations would not be significant for small
fetuses, the approximate date of conception for the

357

FISHERY BULLETIN: VOL. 78, NO. 2

8.1 cm fetus would be late June or early July, and
for the 61 cm fetus would be early May.

Thus, although the data are few, there is a con-
vincing consistency indicative of a calving season
for this population in early summer (May-July).

PHYSICAL MATURITY

Physical maturity was judged on the basis of
examination of the epiphyseal suture in one of the
midthoracic vertebrae and noting whether a car-
tilaginous plate was present (open), absent but
with the epiphyseal line still visible (closed), or
absent with all trace of the epiphyseal suture
obliterated (fused). The suture was examined on a
cut surface at least 1 cm deep, and generally on a
median section of a whole centrum. Closure of the
suture takes place last along the periphery of the
epiphyseal plate, and a shallow cut can frequently
be misleading. As can be seen in Table 2, males
reached physical maturity at about the same size
as sexual maturity (with the exception of 504447,
which as noted earlier, was probably an abnormal
individual). Females, however, reached physical
maturity considerably after sexual maturity, at a
length of about 196 cm and a weight of about 61 kg.

EXTERNAL MORPHOLOGY

External measurements were taken in the
manner outlined by Norris (1961), at the time the
animals were picked up from the beach, using a
steel tape graduated in centimeters. Numbers in
parentheses in the text refer to the numbered
measurements as defined in that paper. In the
following discussion, relative dimensions are with
respect to the total length of the individual, and
are expressed as the means of the individual di-
mensions divided by the individual total lengths
(Table 3). Figure 2 shows the long slender rostrum
and a pigmentation pattern characteristic of this
species.

Sexual dimorphism in the external measure-
ments was most apparent in the relative length of
the rostrum (snout to apex of melon (3)). This di-
mension was about 7% larger in females for the
total sample, but was less in the adult and
neonatal samples. Perrin (1975) found the same
sexual difference in the sample of S. longirostris
which he examined from the Pacific.

The other anterior body measurements which
are taken from the tip of the snout show sexual
differences of a lower relative magnitude, due to

358

Table 3. — External measurements on Florida spinner dolphin
expressed as individual dimensions divided by individual total
lengths. For these purposes animals with a total length >195 cm
were considered adult. Numbers in parentheses refer to Norris
(1961) for definitions of the measurement.

Measurement

Sample

N

Mean

SD

Snout to apex of melon (3)

Total males

12

0089

0005

Total females

14

,095

008

Adult Males

9

090

.005

Adult females

4

.093

005

Neonatal males

1

080

—

Neonatal females

2

.081

.005

Snout to genital slit (13)

Adult males

9

652

.020

Adult females

5

706

.023

Girth at anus (23)

Adult males

9

.312

.012

Adult females

5

.281

.022

Fluke width (34)

Total males

12

.233

.017

Total females

15

.216

.017

Adult males

9

235

.019

Adult females

5

222

,016

Neonatal males

1

221

—

Neonatal females

2

.210

,014

Height of dorsal fir

(32)

Total males

12

.102

.009

Total females

15

.095

.006

inclusion of the rostral length as a component of
these dimensions. We should then expect, if no
other factors were active, that all measurements
containing rostral length would be proportion-
ately greater in females, and all those not contain-
ing rostral length would be proportionately
smaller. In this particular sample, however, the
variation is such that these differences are not
apparent in most cases.

The position of the center of the genital slit, as
determined by the measurement from the tip of
the snout to the genital slit (13), differs between
males and females, with the center of the slit being
farther posterior in females. The difference
amounts to a relative increase of about 8% in this
measurement in adult females when compared
with adult males. This particular sexual differ-
ence seems to be true of cetaceans in general.

Girth at the anus (23) relative to total length is
about 11% greater in adult males. This is corre-
lated with development of a postanal keel in adult
males as described by Perrin (1972, 1975).

The relative width of the flukes (34) was 5-8%
greater in males in the adult, total, and neonatal
samples. Although the variation in this character
renders this statistically insignificant in this
sample, the same sort of difference was found by
Perrin (1975) in his Pacific samples, suggesting
that it is a real difference. The relative height of
the dorsal fin (32) was 7% greater in males in the
total sample. Here again, the variation renders
the difference statistically insignificant. There is a
possible indication that the flippers are relatively
larger in females, but the difference is slight

MEAD ET AL.: OBSERVATIONS ON MASS STRANDING OF SPINNER DOLPHIN

Figure 2. — Adult Stenella longirostris stranded at Casey Key, Fla. Above adult male, 195 cm total length (504442); below, head of

adult female, 186 cm total length (504454).

enough that a larger sample would be needed to
demonstrate its validity.

None of the other measurements show any ap-
preciable sexual differences when the differences
in total length and rostral length are taken into
account.

Since the sample is lacking in intermediate-size
animals, there is relatively little that can be said
about growth patterns. It is apparent that the
snout is relatively shorter and the rest of the head
relatively larger in neonatal animals than in
adults. The girths appear to be relatively greater,
the flippers relatively larger, but the flukes and
dorsal fin about the same proportion in the neo-

nates as in the adults. Although the sample of
neonates is too small to have any statistical sig-
nificance, the sexual differences in length of ros-
trum, position of genital slit, width of flukes, and
height of dorsal fin are the same in the neonates as
in the adults.

Although comparable data for samples of S. lon-
girostris from other areas are sparse (Perrin 1975),
this sample appears to be similar to Hawaiian
spinners in total length, rostral length, and girths.
More meaningful comparison to other popula-
tions of S. longirostris will require increased
sample sizes and more sophisticated statistical
procedures.

359

WEIGHTS

The body weights of 11 males (188-208 cm)
ranged from 51 to 75 kg, with a mean of 63.8 kg,
while the body weights of 13 females (177-204 cm)
ranged from 46.1 to 65.2 kg, with a mean of 55.7
kg. Thus, while the sample of males averaged
about 3% longer than the sample of females, they
averaged about 14% heavier. The range of indi-
vidual organ weights and the mean percentages of
total body weight are as follows, with the compa-
rable data for Pacific spinner dolphins given by
Perrin and Roberts (1972) in parentheses; heart
260-440 g, 0.59% (191-272 g, 0.46%); liver 980-
2,200 g, 2.7% (832-997 g, 1.90%); kidneys 350-620
g, 0.78% (289-393 g, 0.65%); brain 500-780 g,
1.02%. The organ weights in the Florida sample,
expressed as mean percentage of body weight, av-
eraged about 25% greater than those given for the
Pacific spinner dolphins. It is possible that some of
this difference is due to weight loss (primarily
blubber and muscle) in the Florida sample induced
by the stress of whatever factors led to their
stranding. As noted earlier, the stomachs of all of
the Florida specimens were empty, and it is likely
that they had not fed for some time. Perrin and
Roberts (1972) noted that in both their samples of
spotted and spinner dolphins, the right kidneys
tended to be larger than the left whereas in our
sample the kidneys were essentially equal (left
was heavier in nine, right was heavier in five, and
both were equal in eight).

ACKNOWLEDGMENTS

The authors particularly wish to acknowledge
the help of Perry Gilbert and the staff of the Mote
Marine Laboratory, who provided facilities and
assistance in the necropsy. We also wish to thank
Edward Asper and the staff of Sea World, Inc.,
Orlando, for data on the two live animals which
were transported to their facilities. Vladimir
Gurevich of the Hubbs-Sea World Research Insti-
tute, San Diego, and J. E. Reynolds of the Univer-
sity of Miami assisted in the necropsies and in the
preparation of skeletal material. William F. Per-
rin, Southwest Fisheries Center, NMFS, NCAA,
La Jolla, kindly read the manuscript and provided
criticism and suggestions.

FISHERY BULLETIN: VOL. 78, NO. 2

LITERATURE CITED

Caldwell, D. K., M. C. Caldwell, W. F. Rathjen, and J. R.

SULLIVAN.

1971. Cetaceans from the Lesser Antillean island of St.
Vincent. Fish. BulL, U.S. 69:303-312.

Erdman, D. S., J. Harms, and M. M. Flores.

1973. Cetacean records from the northeastern Caribbean
region. Cetology 17, 14 p.

GERACI.J. R.

1978. The enigma of marine mammal strandings.
Oceanus21(2):38-47.
GUNTER, G.

1954. Mammals of the Gulf of Mexico. In P. Galtsoff
(editor), Gulf of Mexico, its origin, waters, and marine life,
p. 543-551. U.S. Fish Wildl. Serv., Fish. Bull. 55.

Harrison, R. J., R. L. Brownell, Jr., and R. C. Boice.

1972, Reproduction and gonadal appearances in some
odontocetes. In R. J. Harrison (editor), Functional
anatomy of marine mammals. Vol. 1, p. 361-429. Acad.
Press, N.Y.

layne,j.n.

1965. Observations on marine mammals in Florida wa-
ters. Bull. Fla. State Mus. 9(4):131-181.

LOWERY, G. H.

1974. The mammals of Louisiana and adjacent water.
La. State Univ. Press, Baton Rouge, 565 p.

NORRIS, K. S.

1961 . Standardized methods for measuring and recording
data on the smaller cetaceans. J. Mammal. 42:471-476.

PERRIN, W. F.

1972. Color patterns of spinner porpoises (Stenella cf. S.
longirostris) of the eastern Pacific and Hawaii, with com-
ments on delphinid pigmentation. Fish. Bull., U.S.
70:983-1003.

1975. Variation of spotted and spinner porpoises (genus
Stenella) in the eastern Pacific and Hawaii. Bull.
Scripps Inst. Oceanogr. 21, 206 p.

PERRIN, W. F., J. M. COE, AND J. R. ZWEIFEL.

1976. Growth and reproduction of the spotted porpoise,
Stenella attenuata, in the offshore eastern tropical Pa-
cific. 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 dol-
phin, a geographical form of Stenella longirostris in the
eastern tropical Pacific. Fish. Bull., U.S. 75:725-750.

Perrin, W. F., and E. L. Roberts.

1972. Organ weights of non-captive porpoise {Stenella
spp.). Bull. South. Calif. Acad. Sci. 71:19-32.

Shane, S. H.

1977. The population biology of the Atlantic bottlenose
dolphin, Tursiops truncatus, in the Aransas Pass area of
Texas. M.S. Thesis, Texas A&M Univ., College Station,
239 p.

Taruski, a. G., and H. E. Winn.

1976. Winter sightings of odontocetes in the West Indies.
Cetology 22, 12 p.

360

ANNUAL VARIABILITY OF REEF-FISH ASSEMBLAGES IN
KELP FORESTS OFF SANTA BARBARA, CALIFORNIA

Alfred W. Ebeling/ Ralph J. Larson,^ William S. Alevizon,^ and Richard N. Bray''

ABSTRACT

Assemblages of kelp- bed fishes that live in and about the kelp canopy or over the reef bottom were
censused by movie strips (cinetransects) every September from 1971 to 1974 at rock reefs off Santa
Barbara, southern California. Cinetransects provided an adequate and efficient way to estimate
species composition (order of relative or ranked species abundances), diversity, and numbers offish for
yearly comparisons between canopy and bottom habitats at mainland and Santa Cruz Island study
sites. Canopy assemblages were simpler and more variable than bottom assemblages. They differed
less in composition between sites. Between-site differences in fish assemblages reflected differences in
structural habitat between mainland and island. Variation in species composition was less among
years than between habitats or sites in the sense that site- and habitat-specific composition of
assemblages persisted in the course of significant yearly changes in counts of fish and species per
transect. Despite these changes, "annual variation," as measured by variance of year-to-year log,(,
ratios of numbers of 16 common species, was relatively small. Its size was characteristic of stable
communities in predictable environments. As a group, planktivores, which form dense aggregations in
midwater, fluctuated most in numbers. Perhaps fish responded directly to local changes in water
clarity, temperature, currents, and density of giant kelp. However, coincident changes in fish counts at
mainland and island sites indicated that these local environmental factors, which did not vary
accordingly, were not the only causes of annual variability in fish abundance.

Off southern California, rocky reefs and beds of
giant kelp, Macrocystis pyrifera,h.arhor more than
125 species offish, almost 259c of the Californian
marine total ( Quast 1968b; Feder et al. 1974). Sub-
tidal reef-fish assemblages have been extensively
studied in the warm-temperate San Diegan
Faunal Region to the south of Santa Barbara
(Quast 1968b, c; Hobson and Chess 1976; Lim-
baugh^), and in the cool-temperate Monterey an
Faunal Region to the north (Miller and Geibel
1973; Burge and Schultz'^; Gotshall et al/). Except

'Department of Biological Sciences and Marine Science Insti-
tute, University of California, Santa Barbara, CA 93106.

^Department of Biological Sciences and Marine Science Insti-
tute, University of California, Santa Barbara, Calif.; present
address: MRC Research Center, 533 Stevens Ave., Solana Beach,
CA 92075.

^Department of Biological Sciences and Marine Science Insti-
tute, University of California, Santa Barbara, Calif; present
address: Department of Biological Sciences, Florida Institute of
Technology, Melbourne, FL 32901.

"•Department of Biological Sciences and Marine Science Insti-
tute, University of California, Santa Barbara, Calif.; present
address; Department of Biology, California State University,
Long Beach, CA 90840.

^Limbaugh, C. 1955. Fish life in the kelp beds and the
effects of kelp harvesting. Univ. Calif. Inst. Mar. Resour., IMR
Ref 55-9, 158 p.

^Burge, R. T., and S. A. Schultz. 1973. The marine environ-
ment in the vicinity of Diablo Cove with special reference to
abalones and bony fishes. Calif. Dep. Fish Game Mar. Resour.
Tech. Rep. 19, 433 p.

for scattered observations and species lists
(Hewatt 1946; Quast 1968c; Clarke and Neushul
1967; Neushul et al. 1967; Alevizon 1976), how-
ever, virtually nothing is known of the structure
and annual variability of such fish assemblages off
Santa Barbara, which is at the northern end of the
San Diegan Region as defined by Hubbs (1960).

Ebeling et al. (in press) analyzed Santa Barba-
ran assemblages of kelp-bed fishes sampled from a
variety of habitats and localities along the main-
land coast and across the Santa Barbara Channel
at Santa Cruz Island. The fish community was
assumed to comprise smaller groups of species
that tend to segregate among habitat types.
Photographic observations made throughout 1970
were used to resolve five such "habitat groups." A
group of "kelp-rock species" (e.g., garibaldi, //^'p-
sypops rubicundus, and California sheephead,
Pimelometopon pulchrum) was most abundant in
relatively clear water and dense kelp over high-
relief rocky reef. "Canopy species" (e.g., kelp

■'Gotshall, D. W., L. L. Laurent, E. E. Ebert, F. E. Wendell, and
G. D. Farrens. 1974. Diablo Canyon power plant site ecologi-
cal study annual report July 1, 1973^June 30, 1974 In W. J.
North (editor). Environmental investigations at Diablo Canyon,
1974. Calif. Dep. Fish Game Mar. Resour. Admin. Rep. 74-10,
p. 199-305.

Manuscript accepted October 1979.
FISHERY BULLETIN: VOL. 78, NO. 2, 1980.

361 —

>30

FISHERY BULLETIN: VOL. 78, NO. 2

perch, Brachyistius frenatus, and senorita,
Oxyjulis californica) usually aggregated within
and just below the kelp canopy; "bottom species"
(e.g., gopher rockfish, Setes^es carnatus) rested on
the rocky reef surface far below; while "commuter
species" (e.g., kelp bass, Paralahrax clathratus)
swam about at all depths. "Inner-marginal
species" (e.g., black perch, Embiotocajacksoni) oc-
curred abundantly over mixed rock and sand in-
shore as well as deeper reefs offshore. Members of
different groups tended to mingle in areas of con-
tinuous reef and kelp where habitat types were
close together. The more complex and extensive
island reefs harbored the greatest numbers of
"reef specialists" in the kelp-rock group.

The present study is an analysis of annual var-
iability in species composition, diversity, and
abundance of kelp-bed fishes in the faunistically
transitional (Neushul et al. 1967; Hubbs 1974;
Horn and Allen 1978) Santa Barbara Channel.
There have been few long-term studies of stability
and variability in reef-fish communities (Thomson
and Lehner 1976; Sale 1978). Yet, understanding
the scope and causes of variation in natural com-

munities has both practical and theoretical impor-
tance (Larkin 1978; Wolda 1978). Our primary
purposes, therefore, were to 1) document yearly
changes in kelp-bed fish assemblages, which had
previously impressed us as appearing relatively
uniform in time, and 2) relate observed changes to
environmental variables that we could readily ob-
serve. Secondarily, we assessed the use of under-
water movies to census fishes in a complex envi-
ronment. To these ends, we made annual censuses
of fishes in and about the canopy of giant kelp and
over the bottom in areas of continuous rock reef at
sites off the Santa Barbara mainland and Santa
Cruz Island.

METHODS

Study Sites

Sampling was conducted in areas of rocky reef
and kelp on either side of the Santa Barbara
Channel (Figure 1). Our mainland sampling site
was Naples Reef, an isolated system of rocky out-
crops and ledges located about 1.6 km offshore, 24

PT. CONCEPTION

MONTEREY 266 KM V
SAN DIEGO 342 KM

N

MAINLAND SITE

w-^

f,HTA BARB^^^

'^*N HEL

SAN MIGUEL IS,

ISLAND SITE

*NACAPa

IS.

25 KM

FIGURE 1.— Study sites for yearly sampling of fish assemblages in areas of reef and kelp off Santa Barbara, southern California.
Circled letters identify the mainland site, Naples Reef (NA), and the island site, Fry's Harbor and vicinity (FR).

362

EBELING ET AL.: ANNUAL VARIABILITY OF REEF FISH

km west of Santa Barbara, Calif, (lat. 34°25' N,
long. 119°57' W). Measuring 275 x 80 m (2.2 ha),
the reef surface averaged 8-12 m in depth, though
some crests projected to within 5 m of the surface.
The reef was surrounded by flat sand or cobble
bottom, 16-20 m deep, with smaller rock outcrops.
Above the reef, the kelp canopy usually prolifer-
ated during spring and summer, but thinned dur-
ing late fall and winter.

Island observations were made at a site centered
about Fry's Harbor on the north side of Santa Cruz
Island (Figure 1). The subtidal substrates here
were mostly rocky, with boulder areas, ledges, and
caves interspersed occasionally with sand or flat-
faced rock. The bottom sloped rather steeply to
sand at depths of 15-25 m about 20-50 m from
shore. Most sampling was conducted at depths of
3-15 m. Here, the kelp canopy extended a short
distance seaward over greater depths and shore-
ward to meet steep rock cliffs. In contrast with the
mainland observations, therefore, most island ob-
servations were made within about 10-50 m of the
shore, over an area of rapidly increasing bottom
depth.

We saw anglers and divers at both sites. Yet, we
rarely observed concentrated fishing effort, prob-
ably because of the erratic state of the Santa Bar-
bara partyboat industry during the early 1970's
(Love and Ebeling 1978). Fishermen in small
boats were more frequently seen casting bait and
lures near the surface at Naples Reef than at the
island site. Hence, catches of kelp bass and other
surface predators were probably substantial at
Naples Reef only. Sport divers exploited both sites,
albeit more sporadically than boat fishermen and
seldom during the sampling periods. We suspect
that catches of bottom fishes were not large and
about the same at both sites.

We noted no kelp cutting and harvesting in the
area of either site. About the island site, kelp beds
are limited to a narrow band along the steep shore,
and so are inaccessible and too small for harvest.
Kelp in the mainland area is harvested only in-
shore of Naples Reef, which is left undisturbed.

Cinetransects

We sampled fish and observed habitat charac-

*Ron H. McPeak, Senior Marine Biologist, Kelco Corp., 2145
East Belt St., San Diego, CA 921 13, pers. commun. October 1979.

'Bruce W. W. Harger, General Manager, Neushul Mariculture
Corp., 275 Orange St., Goleta, CA 93017, pers. commun. October
1979.

teristics by means of "cinetransects." These were
2.5-min, Super-8 mm movie films taken at 24
frames/s by scuba divers. The use of 50 ft ( 15.24 m)
film cartridges standardized sampling time, and
allowed rapid changing of film. High-speed color
film yielded good photographs when water visibil-
ity exceeded 3 m. Starting from opportune points
within the kelp-rock habitat, divers swam at rela-
tively constant speeds, and, with the camera held
level or pointed slightly downward (for bottom
transects), steadily panned in about 10° arcs.
Large aggregations of fish were photographed in
one sweep of the camera; thereafter the camera
was not pointed at the aggregation. This proce-
dure allowed rapid and accurate enumeration of
aggregations, and avoided redundant sampling of
fish. During a given transect, a diver would keep to
the same general depth and terrain, so that each
transect could be classified by its habitat charac-
teristics. For each transect, he measured depth of
filming, depth of bottom, underwater visibility,
temperature, and depth of thermocline. Films
were taken in two general habitats: bottom and
kelp canopy. Canopy transects were made at
depths of 2-3 m, just below the mat of floating
fronds. Bottom transects were taken from about a
meter above the bottom, at depths ranging from
about 3 to 15 m. All cinetransects were photo-
graphed during September of the years 1971-74.
This was in the midst of the season of maximum
thermal stratification, when water was predicta-
bly calm and clear (Brown 1974; Love and Ebeling
1978).

Two observers counted and tallied individuals
per species from cinetransects projected at low
speed and stop action. For each film, observers also
scored bottom relief and algal density from 1 (low)
to 5 (high). They often stopped, reversed, and
reran the film to accurately count fish in dense
clusters. When observers disagreed, they re-
counted, and recorded the average of the two
closest values. All species but two were tallied
separately. The sibling rockfishes Sebastes car-
natus andS. chrysomelas, which were identifiable
by color only, were tallied as one, because subtle
color differences were not always discernible in
cinetransects filmed at greater depths or in more
turbid water. Observers did not count small
(young-of-year) juveniles, such as the reddish
growth stage of blue rockfish,S. mystinus. Nor did

'"Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

363

FISHERY BULLETIN: VOL 78. NO. 2

they count island seaperch, Cymatogaster gracilis ,
in 1971-73 samples. Island seaperch were ob-
served only at Santa Cruz Island, sporadically in
dense schools in the kelp canopy. To judge the
effect of ignoring this species in 1971-73, we com-
pared two 1974 samples, one with, the other with-
out counts of island seaperch.

Bottom cinetransects were calibrated for area
covered by estimating their length and width in
the field. We estimated length experimentally by
measuring distances swam during transects at
Naples Reef. On each of five weekly tests, one
diver photographed while a second followed with a
tape measure. On 4 of 5 days, one transect went
upcurrent, the other downcurrent; on the fifth day,
three transects were measured in almost no cur-
rent. Lengths of all 11 transects averaged
47.8 ±2. 78 m (95% confidence interval— CI). We
estimated transect width by counting markers
placed along a surveyed course. A tape measure
marked the midline of a 50 m stretch of reef flat
and rill, and pairs of red floats, anchored 2 m on
either side of the tape at 5 m intervals, delimited a
4 m wide band. Four transects were photographed
along the course, with divers panning the camera
as usual. While viewing the projected films, we
estimated widths of pans by taking 4 m (width of
the marked band) and adding or subtracting esti-
mated distances before or beyond each float seen at
the extremes of the pans. Since widths of 43 pans
averaged 4.41 ±0.288 m (95% CI), the area covered
by an average bottom transect was taken as 47.8 m
(length) times 4.41 m (width) = 211 m^.

Calibration of canopy transects was inherently
less accurate. Photographers swam more circu-
itous routes at more variable speeds in midwater,
where light fluctuated between dim and bright.
The best we could do was roughly measure dis-
tance travelled by a photographer swimming uni-
directionally under the canopy: an average length
of 62.3 m in four trials both with and against the
current. We estimated band width by counting
kelp blades (which averaged 0.5 m long) passed
during sweeps of the camera: counts usually var-
ied from 8 to 10, translating to 4-5 m. Hence, we
assumed band width of canopy transects to equal
that for bottom transects (4.41 m), and estimated
area covered by a canopy transect as 62.3 m
(length) times 4.41 m (width) = 275 m^.

Statistical Analyses
Samples were specific for habitat, site, and year.

For example, one sample was made up of fish
counts from a set of 43 transects filmed in the
canopy habitat at the mainland site during 1974.

Sample species diversity of yearly canopy or bot-
tom samples offish assemblages in mainland and
island sites was measured by information-
theoretical indices (H), combining species "rich-
ness" (total species) and "evenness" (distribution
of individuals among species). We used Pielou's
(1966) method to estimate population diversity
from a set of cinetransects pooled incrementally in
random order. Diversity (Brillouin's//) of succes-
sively larger subsamples (size k) first increases
and then levels off, as the decrease in diversity
from adding more individuals of common species
balances the increase from adding rare species'.
Then increments of diversity per added individual
(hf;) between adjacent subsample estimates_(//^_i
and//^) are independent, and the mean ih) and
variance of /i^'s estimate the corresponding popu-
lation parameters. Species richness (S) was the
species count in a whole sample of size k = n.
Species evenness (J) was the ratio HJlnS, where
H^ is sample diversity and InS (natural log of
species count) is the theoretically maximum value
of H„ if the S species were equally abundant.

We compared species composition between sites
and among years by proportionate similarity and
rank correlation. Similarity (/) in species composi-
tion was measured as: / = 1.0 - [0.5(Si = i |p„ -
Pj^ I )], where p^ is the proportionate abundance of
species i in sample j. Rank correlation (Kendall's
tau) was measured between ranked species arrays
(Johnson and Koo 1975). Clusters of similar sam-
ples were computed from matrices of / by the un-
weighted pair-group method using arithmetic av-
erages (Sneath and Sokal 1973).

Mean counts of individuals and species per
transect were compared between sites and among
years (1971-74) by two-way analysis of variance
(ANOVA) for unequal and disproportionate sub-
class sizes, and by one-way ANOVA for unequal
sample sizes (Nie et al. 1975; Meeter and
Livingston 1978). With variates transformed,
sample distributions tended to normality (as indi-
cated by nonsignificant Kolmogorov-Smirnov
tests of goodness-of-fit) and sample variances
equalized (as indicated by nonsignificant F^ax
tests of largest variance ratios) (Sokal and Rohlf
1969; Meeter and Livingston 1978). A posteriori
contrasts among means were obtained by group-
ing means wdth nonsignificant ranges (Dunnett
1970; Nie et al. 1975).

364

EBELING ET AL.; ANNUAL VARIABILITY OF REEF FISH

Annual variability (AV) in numbers offish per
species was measured as variance in logjo ratios
(logR) of estimated numbers per hectare between
consecutive years. For each species, we estimated
number per hectare by summing mean counts per
bottom and canopy cinetransects after correcting
canopy means for greater area covered per tran-
sect, then multiplying by 47.39, the estimated
number of bottom transects covering 1 ha (which
approximates the average number per year,
44.12). AccordingtoWoldal 1978), logi? = log AT. -
log (iV,-i), where Nj is number of individuals for 1
yr and N, ^ j is that for the preceding year. The
mean log R for an array of species indicates the
average net change in species abundance, and the
variance of the logi?'s ( AV) measures the scope of
change in species abundances. For example, a
mean logi? near zero indicates that about as many
species increased as decreased in abundance be-
tween years, while a relatively low AV shows that
increases and/or decreases were generally small;
i.e., that annual variability was low. To increase
the reliability of R, only species with at least 5
individuals/ha per year were included in the anal-
ysis (Wolda 1978). Although samples covered
more than 2 yr, arrays must appear in calculations
only once (Wolda 1978). Thus, we computed AV's
for an array of 16 log R's for ratios of species
abundances between 1972 and 1971, and for a
similar array between 1974 and 1973 (separately
for mainland and island study sites). Then, we
computed overall AV between the years from the
array of 32 logiJ's: those for 1972-71 plus those for
1974-73.

RESULTS

Yearly sampling yielded 297 and 331 cinetran-
sects from mainland and island study sites, and
recorded 46 fish species in 21 families, although
only 31 species in 11 families were common
enough to be analyzed (Table 1 ).^^ On the average,
about 35 transects were needed to record 90% of 16

"Additional species that were rarely recorded include:
Heterodontus francisci (Heterodontidae), Cephaloscyllium ven-
triosum (Scyliorhinidae), Myliobatis californica
(Myliobatididae), Torpedo californica (Torpedinidae),
Syngnathus spp. (Syngnathidae), Atherinops affinis
(Atherinidael, Cymatogaster gracilis (Embiotocidae —
sporadically common at island, see text), Phanerodon atripes
(Embiotocidae), Caulolatilus princeps (Branchiostegidae), Gib-
bonsia elegans (Clinidae), Coryphopterus nicholsi (Gobiidae),
Scorpaena guttata iScorpaenidaei, Sebastes auriculatus (Scor-
paenidae), P/euronic/zf/iys coenosus (Pleuronectidae), and Mo/a
mola (Molidae).

species that were filmed in the kelp-canopy
habitat (the "canopy assemblage" of fishes), while
50 transects were needed to record 90% of 31
species that were filmed in the reef-bottom habitat
(the "bottom assemblage").

Although our primary objective was to measure
yearly variability, our analysis revealed sig-
nificant differences in species composition, diver-
sity, and abundance offish assemblages between
canopy and bottom habitats, and between main-
land and island study sites. Therefore, we describe
the observed spatial differences as a prelude to the
account of yearly differences.

Spatial Differences

Differences in composition between as-
semblages in canopy and bottom habitats were
obvious and easily demonstrated. For example,
canopy and bottom arrays from all years and both
sites were segregated in the cluster analysis
based on proportionate species abundances (Fig-
ure 2). Canopy samples contained relatively more
planktivores and kelp browsers like black-
smith, Chromis punctipinnis; kelp perch; blue
rockfish; juvenile olive rockfish, S. serranoides;
and sehorita (Table 1). Bottom samples contained
more bottom grazers and ambushers like pile
perch, Damalichthys uacca; black perch; gari-
baldi; California sheephead; gopher rockfish; and
black-and-yellow rockfish, S. chrysomelas.

The canopy assemblage was simpler than the
bottom assemblage in the sense that more indi-
viduals of fewer species occurred in the canopy. All
of our 31 common species were recorded in bottom
cinetransects, but only 16 were filmed in the
canopy (Table 1). Furthermore, while the median
number of individuals (33 — corrected for greater
volume per transect) recorded in canopy transects
significantly exceeded that (24) for bottom trans-
ects, the median species count ( 5) was significantly
less than that (8) in bottom transects (Wilcoxon
tests based on 275 canopy and 353 bottom counts,
P<0.005). These differences were reflected in the
shapes of the abundance-diversity curves for the
two habitats (Figure 3). Those from the canopy
habitats sloped steeply, reflecting the fact that
only a few species were relatively common there,
while those from the bottom habitats had flatter
tops, reflecting a more coequal commonness of
several species.

In general, the composition offish assemblages
differed markedlv between mainland and island

365

FISHERY BULLETIN: VOL. 78, NO. 2

73

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366

EBELING ET AL: ANNUAL VARIABILITY OF REEF FISH

.2

SIMILARITY (1)
0.4 0.6

0.6

1.0

1 ' 1 ■ I '

'

1

■1973

1

-1974

ic-

1974

-1971

p

IC-

1 ^

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MC-

■1972

1973

-1971

MB

-1972

. hjn-

■1973
-1974

MR

1 n

■1971
■1974

_ 1 n

1972
1973

IB-

Figure 2. — Clustering, by year (right number), of canopy (C)
and bottom (B) cinetransect samples of kelp-bed fishes filmed
each September in 1971-74 at mainland (M) and Santa Cruz
Island (I) study sites off Santa Barbara, southern California.

study sites. Samples from within mainland or is-
land sites tended to be more alike than samples
between these sites, particularly for bottom as-
semblages. Samples from within tended to form
secondary subclusters nested in the principal ones
distinguishing canopy and bottom assemblages
(Figure 2), and within-site similarity values
tended to be higher than between-site values (Ta-
ble 2).

As indicated by clusters (Figure 2) and similar-
ity values (Table 2), however, mainland and island
canopy assemblages were more difficult to distin-
guish than bottom assemblages. The mean ratio of
within- to between-site resemblance (/ or tau) was
comparatively large for arrays of canopy species
(Table 2), indicating that canopy assemblages
were only slightly more distinguishable between
sites than among years. This, and the fact that
variances of canopy similarities were relatively
large (Table 2), explained why the clusters of
canopy samples were poorly defined. What few
between-site differences in canopy samples pre-
vailed were due to greater numbers of kelp perch
and juvenile olive rockfish observed in the canopy
habitat of the island site, and of blue rockfish at
the mainland (Table 1). Island canopy samples
contained a few more species than mainland
canopy samples (Table 3, S), and the average
number of species per cinetransect (Table 3) was
significantly greater (Table 4) at the island. (The
significant year-site interaction as indicated in

1000.

CANOPY

MAINLAND

BOTTOM

--I000

-.100

-.30

-10

ISLAND

MAINLAND ISLAND

-_2

SPECIES SEQUENCE (MOST COMMON TO RAREST)

Figure 3. — Abundance-diversity curves for 31 species of kelp-bed fishes from canopy and bottom assemblages in yearly samples filmed
during 1971-74 at mainland and Santa Cruz Island sites off Santa Barbara, southern California.

367

FISHERY BULLETIN: VOL. 78, NO. 2

Table 2. — Comparison of within-site and between-site means ( ±\ standard deviation) of similarity (/) and rank correlation (tau)
between all pairs of species-abundance arrays from yearly cinetransect samples filmed during 1971-74 at mainland and Santa Cruz
Island Study sites ofTSanta Barbara, southern California. Within-site means are of values for all pairs (1971 vs. 1972, 1971 vs. 1973,
. . ., 1973 vs. 1974), both members of which were filmed in canopy or bottom habitats either at the mainland or island site; between-site
means are of values for all such habitat-year pairs, one member of which was from an island sample, the other from a mamland
sample; and mean ratio is the between-site value/mean within-site value (mainland and island). (Figure 2 is a cluster diagram of
yearly samples, computed from all values of/.)

Within sites [n = 6)'

Between
sites (n = 10)

Mean ratio

Mainland

Island

between/within

Habitat

/ Tau

/

Tau

/

Tau

/ Tau

Canopy
Bottom

Mean

0.62 = 0 11 0 58=0.09'

0 68=0 05" 0 67 = 0.06"-

065 0.625

0.61=0.13
075 = 0.06-
0.68

0.59=0.09-
0.80 = 0.03—
0 695

0.50 = 0.17
053 = 009
0.515

0.45 = 0.12
0.49 = 006
0.495

081 0.77
0 74 0 67

0775 072

'Difference of wittiin- and between-site means significant at (f-test) "P 0 05:"P 0.01, ""P 0,001

Table 4 occurred because the relation was re-
versed in 1973 as indicated in Table 3.) Diversity
and evenness (Table 3, h and J) of canopy as-
semblages, however, did not differ significantly
between sites.

However, sporadically abundant endemic is-
land seaperch were not included in these compari-
sons. Adding this species to 1974 counts of the
island-canopy samples increased the fish total
from 1,722 to 3,084 individuals, median fish
counts per transect from 31 to 64 individuals, and
median number of species per transect from^.5 to
6.0. The slight increase in species diversity (A) was

not significant (Table 3). Island seaperch were sel-
dom observed in bottom transects.

In contrast to the canopy assemblages, main-
land and island bottom assemblages were easily
distinguishable. Because between-site re-
semblance was comparatively small for arrays of
bottom species (Table 2), mainland and island
clusters of samples were sharply defined (Figure
2). Island samples contained relatively more
California sheephead, garibaldi, and opaleye,
Girella nigricans, and included rock wrasse,
Halichoeres semicinctus , which were not recorded
from the mainland (Table 1). Mainland-site sam-

TABLE 3. — Yearly abundance and species diversity of canopy and bottom assemblages of kelp-bed fishes m cinetransect samples from
mainland and Santa Cruz Island study sites off Santa Barbara, southern California. Columns include: n, no. of transects in sample;
Geom. X, the antilog of the mean transformed fish count with 95% confidence limits; S, total species in sample; n{h), sample size to
compute /i; /i, the mean of successively pooled transect estimates of diversity per individual (see text); and J, evenness of distribution
of individuals among species in the sample. Contrasts among means that were shown to differ significantly by analysis of variance
(Table 4) were by the Student-Nevraian-Keuls procedure (Sokal and Rohlf 1969:239); means making up homogeneous subsets are
indicated by X's in the same column.

Site

Year

n

Fish counts

Species counts

S

n{h)

/7=95%CI

Habitat

Geon-

, X, 95% CL

Contrasts

x±95%CI

Contrasts

J

Canopy

Mainland

1971

13

11.0-

24,2-53.1

X

X

2.7 = 0.63

X

11

7

1.33 = 0.555

0,54

1972

31

47.4-

70,6 105,0

X

4.7 = 0-57

X

12

19

1 32 = 0,297

0,39

1973

45

322

39 9 49-3

X

50 = 0.42

X

12

27

1,80 = 0,161

0 64

1974

40

16.2

22 5 31 2

X

4.3 = 0.57

X

14

29

1,82 = 0216

052

Unweighted

X

393

4.2

12.2

1,57

0 522

Island

1971

22

30.6

58,8 112,5

X

4.6 = 0.69

X

13

16

1 17 = 0 187

0,40

1972

38

51.0

70,6 97,9

X

6.2 = 0.67

X

13

29

1 63 = 0,137

0,61

1973

46

196

25.4' 32.6

X

3.5 = 0.45

X

14

32

1 70 = 0,301

0 58

1974

40

21.5'

290 393

X

5.7 = 0.63

X

14

27

2 18 = 0 199

0,71

Unweighted

X

46.0

5.0

135

1 67

0,575

1974'

40

303

43. 9-. 63.7

6.3 = 071

15

29

232 = 0,272

0 64

Bottom

Mainland

1971

25

15.7

200 254

X

X

7.3 = 0.82

X X

20

11

2,39 = 0 167

0 75

1972

45

366

42.4 48.9

X

10.1=0.62

X

24

27

2,51=0-130

0 76

1973

55

137

16.2 19.3

X

7.0 = 0.65

X

26

31

2 34 = 0 185

068

1974

43

189

228 274

X

8.2 = 0.83

X

22

33

246 = 0 116

0 77

Unweighted

X

254

8.2

23.0

2242

0 740

Island

1971

37

236

28 6- 34 6

X

87 = 0.65

X X

21

25

2 45 = 0 107

0 77

1972

45

24,1

28 7 34.2

X

95 = 084

X

24

36

260 = 0089

0 82

1973

55

169

19 9 23 5

X

7.8=0,72

X

25

34

2 56 = 0 123

0 78

1974

48

170-

21.3- 26.7

X

X

7,6 = 066

X

22

28

269 = 0 169

0 77

Unweighted

X

246

84

23.0

22 58

0 785

1974'

48

179-

220- 29.2

78 = 0.67

23

30

2,83 = 0,179

0-79

' Including counts of Cymalogasler gracilis
^Difference between unweighted means of

mainland and island values significant at P = 0,05

368

EBELING ET AL.: ANNUAL VARIABILITY OF REEF FISH

Table 4. — Analysis of variance of kelp-bed fish counts (logj^
transformed) and species counts from cinetransects composing
yearly samples filmed during 1971-74 in canopy and bottom
habitats. For the two-way ANOVA's, samples were classified by
sites (Santa Barbara mainland and Santa Cruz Island, southern
California) and years (four sequential Septembers). For the
one-way ANOVA's, samples were classified by years for each site
separately (Mainland and Island subheads).

df

Fish counts

Specie;
MS

3 counts

Source

MS

F

F

Canopy:

Sites. S

1

0.062

-1

17 631

6.17"

Years. Y

3

2.802

16.78—

32629

11.42"*

SY

3

1 079

646—

46.414

16.24"-

Error

267

0.167

2858

Mainland:

Years

3

1.598

8.93—

19.744

8.37"-

Error

125

0.179

2.360

Island:

Years

3

2 282

14.56—

59 298

17 99—

Error

142

0.157

3.296

Bottom:

Sites. S

1

0.001

<1

2.777

<1

Years, Y

3

1 408

19.51 —

106-177

18 07"-

SY

3

0.420

5.83—

19.187

3.26-

Error

345

0.072

5.877

Mainland:

Years

3

1.505

23.48—

88.720

15,99"-

Error

164

0.064

5.547

Island:

Years

3

0.322

4.05"

36.639

5.93—

Error

181

0.080

6.176

•P==0.02; "P = 0.01; — P<0.001.

pies, on the other hand, included relatively more
black perch, pile perch, and rainbow seaperch,
Hypsurus caryi. Whereas one species — the black
perch — usually dominated mainland samples,
several species — the kelp bass; opaleye;
blacksmith; garibaldi; and California sheep-
head — were often equally abundant in island
samples. This more equitable spread of numbers
over several common species resulted in signifi-
cantly greater species diversity ih) by increasing
the evenness component (J) (Table 3), and is
reflected in the flattened tops of dominance-
diversity curves (Figure 3). Neither total species
(Table 3,S) nor mean number of species per tran-
sect (Table 3, species counts) were significantly
larger (Table 4) in island samples.

Mainland and island study sites differed sig-
nificantly in certain characteristics of structural
habitat (Table 5). Scored relief of reef bottom was
significantly greater at the island site, although
scored densities of giant kelp and bottom algae did
not differ significantly between sites. Even though
depth of reef over which bottom transects were
filmed did not differ significantly between sites, it
was more variable at the island site (Table 5) be-
cause the shore there sloped more steeply (Figure
4). Discounting 1973, when water at the island site
was unusually turbid, underwater visibility was
significantly greater by some 2.0 m at the island
site (Table 6). Island water temperatures were
significantly greater, though only slightly so, in
all yearly sampling periods except 1973.

Yearly Differences

Species composition of bottom assemblages at
mainland and island sites was more uniform
(showed greater resemblance among years) than
the corresponding canopy assemblages (Table 2),
although significantly so only for the island site
(^-tests, / between habitats, P<0.05; tau,
P<0.002). Consequently, both measures of yearly
resemblance (/, tau) of bottom-species arrays
within sites were significantly greater than those
between sites (Table 2). Furthermore, among-year
variances of both resemblance measures for main-
land- and island-bottom assemblages were less
than those for both canopy assemblages, though
significantly so only for island measure tau (F-
test, P~0.05). Comparing bottom assemblages
only, the island assemblage was significantly
more uniform (^-tests, / between sites, P~0.05;
tau,P<0.001).

Fish and species counts also reflected the great-
er annual variability of canopy assemblages. We
computed coefficients of variation (CV) —
percentage ratios of standard deviation to

Table 5. — Means of habitat variables measured with each cinetransect for all bottom samples filmed during 1971-74 at mainland
and Santa Cruz Island study sites off Santa Barbara, southern California. Scored from 1 (low) to 5 (high), plant density, other algae
includes all understory forms. Time of day is the 4-yr range of median times at which transects making up yearly samples were filmed.
CV is coefficient of variation and CI, confidence interval. Significance levels are from Mann- Whitney [/-tests of rank differences
between mainland and island values.

••p.
'n =

0.01.

130, excluding unusually low values for 1973 (see Table 6).

No. of
observations (n)

Mean

_. , .. plant density score
Time of Mean —

day (fi) bottom type score Giant kelp Other algae

Bottom depth (m)

Underwater
visibility (m)

Site

x±95%CI CV

J(±95%CI CV

Mainland
Island

168
185

1205-1403 3.89 2.43 3.16
1210-1400 4.43" 2.29 3.29

8.62±0.205 15.4%
8.28 ±0.400 32.8%

6.11 ±0.157 17.4%
'8.11 ±0.439 '34.8%

369

FISHERY BULLETIN: VOL. 78, NO. 2

^r^ ''■"

'^^/XA^^^^y?>Tt^r,-^^ " '

MAINLAND

SLAND

Figure 4. — Offshore profiles (vertically exaggerated) at mainland (Naples ReeD and Santa Cruz Island (Fry's Harbor) study sites off
Santa Barbara, southern California. Off the mainland, broad sand and cobble flats (stippled) separate rocky outcrops (hatched) between
the shore and Naples Reef (highest outcrop), 1.6 km offshore. Off the island, the relatively steep rocky bottom meets sand within only
about 50 m of shore.

Table 6. — Yearly means (±95% confidence interval) of diver
estimated underwater visibility and temperature measured
with each cinetransect in bottom-habitat samples filmed during
1971-74 at mainland and Santa Cruz Island study sites off Santa
Barbara, southern California.

Underwater

Water

Thermocline

Site

Year

n

visibility
(m)

temperature,
surface ("C)

depth
(m)

Mainland

1971

25

5.61 ±0.436

16.51 ±0.309

8.90 ±0.704

1972

45

7.07±0222

18.00±0.081

8,72±0,219

1973

55

6.43±0.317

17.31 ±0.060

8.72±0.326

1974

43

4.97 ±0.347

19.16±0.076

8.78±1.036

Island

1971

37

7.96±0363

19.42±0.063

10.00±0.329

1972

45

8.84±0.991

18.56±0.335

10.45±0.951

1973

55

2.97±0.082

16.63±0.250

Undetected

1974

48

7.56± 1.070

19.56±0.070

•10-11

mean — to compare variability of these different
measures of different magnitudes (Sokal and
Rohlf 1969:62). Averaged among eight yearly
samples (four mainland + four island, sum-
marized in Table 3), CV's for counts per transect of
individuals and species in canopy samples (x =
75.5% and 36.97f ) were significantly greater than
corresponding values (61.1%, 29.0%) for bottom
samples (^tests, P<0.05). Expectedly, therefore,
the CV for species diversity (A) of canopy samples
was also significantly greater (x = 33.8% vs.
13.6%, approximate ^-test, unequal variances,
P<0.05).

Yearly differences in mean fish and species
counts per transect (canopy and bottom) were
highly significant (Table 4). All one-way ANOVA's
revealed such differences (Table 4), and highs and
lows generally coincided between mainland and
island sites (Table 3). For example, counts were
generally high in 1972, low in 1973, and inter-
mediate in 1971 and 1974. Thus, most of the sig-
nificant differences between means were due to a
relatively abrupt decline from high counts in 1972
to low counts in 1973. The 1972 peak was most
pronounced at the mainland site, when 10 of 16
species had greatest abundances, vs. 7 at the is-
land (Table 7). Peaks of five species coincided:
Paralabrax clathratus, D. vacca, E. lateralis, S.
atrovirens, and S. mystinus. The only other coinci-
dent peak abundance was of S. serranoides in
1 973 . Despite the general correspondence between
sites of overall changes in abundance and species
number, however, significant year-site interac-
tions (Table 4) indicated notable exceptions. For
example, 1973 counts of individuals and species
were relatively high in the mainland canopy, but
low in the island canopy (Table 3).

Wolda's (1978) measures of annual variation
revealed overall trends in species abundances

370

EBELING ET AL.: ANNUAL VARIABILITY OF REEF FISH

Table 7. — Annual variation of estimated density (individuals per hectare) of common kelp-bed fish species at mainland and Santa
Cruz Island study sites off Santa Barbara, southern California. Variance \ n, the variance of square roots of yearly densities,
measures yearly variability discounting effects of means; R at bottom of table, the mean of log fl's — the average difference in log^^
density for the species array between two successive years, measures net change in the array; AV, the variance of logic's, measures
the scope of change. Between-year totals yield these statistics for an array of all 32 log R's (See text and Wolda 1978). A dash ( — )
indicates that the number was too small for analysis.

Mainland

Island

Species

1971

1972

1973

1974

Variance \ n

1971

1972

1973

1974

Variance \ n

Paralabrax clalhratus

377

384

171

121

19.3

214

329

301

220

31

Girella nigricans

204

246

53

59

19.2

340

272

128

167

106

Medialuna californiensis

97

132

39

153

8 1

21

19

13

26

0.4

Brachyistius frenatus

—

—

—

—

—

2,161

1.394

299

190

247.9

Damalichthys vacca

103

109

60

62

2.1

47

70

47

39

08

Embiotoca jacksoni

260

512

383

339

7.3

137

117

82

101

1.3

E- lateralis

28

154

35

32

11.6

37

61

48

36

0.7

Hypsurus caryi

27

66

70

231

18.0

—

—

—

—

—

Rhacochilus loxotes

67

43

15

10

5.5

5

30

14

16

18

Chromis punctipinnis

864

1.207

689

657

17.4

1.872

1.420

140

976

1875

Hypsypops rubicundus

—

—

—

—

—

208

273

108

167

66

Oxyjulis calitornica

161

336

280

194

6.6

71

185

143

260

10,4

Pimelometopon pulchrum

25

95

20

14

7.4

213

189

109

113

4,5

Sebastes atrovirens

11

74

15

10

6.7

154

229

124

204

3,3

S. carnatus &

S. chrysomelas

25

17

29

31

0.4

10

23

19

12

0.6

S. mystinus

238

2,379

531

470

217.3

11

472

175

203

572

S. serranoides

11

26

66

29

3.9

85

102

481

145

34,3

Oxylebius pictus

27

38

29

38

0.3

—

—

—

—

—

R Between years

0.29

-0.30

0.00

023

-0.24

006

Between-year total

0.15

0.14

AV Between years

0 12

0.12

0.06

020

0.12

009

Between-year total

0.11

0.15

Mean variance, midwater planktivores

117.3

164 2

Mean variance, all others

8.3

60

(Table 7). In general, mean log i?'s (Table 7, R),
which measure net annual change between
species arrays, differed significantly within
(^tests,P<0.01), but not between (P>0.05) sites.
This further indicated that species abundances
varied concordantly on both sides of the Channel.
For the mainland site, R for 197 1-72 was positive,
indicating net increases in most species between
these years (Table 7) as total fish counts increased
significantly both in canopy and bottom habitats
(Table 3); was negative for 1972-73 as numbers
decreased in both habitats; and was zero for 1973-
74 as a decrease in total canopy numbers offset an
increase in bottom numbers. Net annual changes
at the island site were somewhat less marked (Ta-
ble 7), and numbers offish differed significantly
between 1972 and 1973 only (Table 3). In general,
variances of logo's (Table 7, AV), which measure
the scops of annual differences between species
arrays, did not differ significantly either within or
between sites (F-tests, P>0.1). However, the
within-site differences were more marked, which
is consistent with the concordance of annual
trends of the mainland and island sites.

Much of the yearly variation in fish abundance
was due to fluctuations in species that aggregate
in the kelp canopy, especially midwater plankti-

vores (Table 7). The average among-year variance
of transformed numbers of three abundant plank-
tivores (B. frenatus, Chromis punctipinnis, and S.
mystinus) was relatively large (145.4, n = 5); that
for abundant species whose vertical distributions
are somewhat broader (Paralabrax clathratus, G.
nigricans, S. serranoides, and O. californica) was
substantially less (13.4, n = 8); while that for
abundant demersal species (E. jacksoni, Hyp-
sypops rubicundus, and Pimelometopon pul-
chrum) was smaller still (5.4, n = 5).

Yearly differences were loosely related to
underwater visibility, water temperature, and,
perhaps, to kelp density in the canopy. Water was
relatively clear and warm during September 1972
(Table 6) when counts of individuals and of species
were high. Furthermore, water was turbid and
cool at the island site during 1973 when counts
were low. However, at the mainland site in 1973,
where no such conditions prevailed (Table 6), bot-
tom counts were also low (Table 3). Kelp density
seemed to affect canopy counts at the mainland
site, where lower scores for kelp density in 1974
(Table 5) coincided with lower counts offish in the
canopy (Table 3).

In sum, variation in composition (order of rela-
tive or ranked species abundances) was less

371

nSHERY BULLETIN: VOL. 78, NO. 2

between years than between habitats or sites,
although canopy assemblages maintained less
site-specific integrity than bottom assemblages.
Coincident peak abundances of several species at
both sites in 1972 contributed to significant yearly
differences in fish counts, although significant
year-site interactions revealed exceptions to the
generally concordant annual trends. Fishes that
aggregated in the canopy habitat, especially mid-
water planktivores, probably contributed most to
annual variation measured by between-year log
ratios of numbers per species. Yearly differences
in fish abundances were loosely related to water
clarity and temperature and kelp density, but
correlations were not clear-cut.

DISCUSSION

Sampling

With limited time, personnel, and budget, visu-
al transecting may be the most appropriate
method for sampling fish populations in the com-
plex reef environment, so long as it is understood
that this method always underestimates densities
of small, hidden, and/or cryptic species (Brock
1954; Jones and Chase 1975). Although some in-
vestigators aver that destructive methods ( poison-
ing, dynamiting) provide broader sampling (Ran-
dall 1963; Goldman and Talbot 1976), others
counter that visual methods are more representa-
tive because they record individuals of larger,
stronger species that escape the slaughter (Smith
and Tyler 1973). Hence, a thorough census of cov-
ert and overt species probably requires both
methods (Quast 1968c).

Cinetransecting is analogous to visual transect-
ing. Both methods may miss most covert fish
( Alevizon and Brooks 1975), but record most overt
individuals. For example, the rank order of species
abundances from all mainland-bottom samples
(Table 1) correlated significantly (tau = 0.66,
P<0.001) with that of daytime visual transects
made along a transect line about the reef crest at
this site throughout the year (Ebeling and Bray
1976: table 3). Four of the five top-ranking species
were the same in both studies, even though cine-
transects covered a much broader area.

However, cinetransects have some advantages
over visual transects. They can be made quickly,
as many as 50/ d in the present study. Cinetran-
sects provide permanent records of the fish and
their environment, not only for greater accuracy

in identifying and counting fish, but also for reuse
in related studies (see Alevizon 1975; Bray and
Ebeling 1975; Love and Ebeling 1978 1. Diver pho-
tographers can proceed slowly and steadily, not
diverting their attention from sampling to record
observations or follow a transect line. They do not
need extensive training in quick recognition of
fish species and numbers, so can be replaced by
others if required; if cinetransect samples are
sorted into subsets, each filmed by one or the other
of two different divers, correlations between the
corresponding diver-specific species arrays are
very high. For example, the four habitat-site-
specific samples filmed by two divers in 1973,
when sorted to eight diver-specific subsets, gave
tau rank correlations ranging from 0.71 to 0.'89
(P<0.001).

Within broad limits, furthermore, water visibil-
ity and light levels probably do not appreciably
affect the volume of water sampled by cinetran-
sects filmed along the bottom. At a given focus
distance, the camera lens' depth of field is in-
versely related to the diameter of its aperture. In
bright light, the aperature is small, creating a great-
er zone in which objects are in focus. In the kelp
forest, however, light was generally so dim, even
on clear days, that the aperture was almost always
fully open. Thus, shading probably creates a fairly
constant depth of field. To check this, we estimated
the distance at which objects were first identifiable
on film. Two divers swam along a tape measure
ending in a fishlike target, one filming the target
and nearby fish, the other signaling distance from
target. During the first trial when underwater
visibility (distance at which target was discern-
ible) was 15.2 m, fish were identifiable on film only
when photographed within about 3.5 m of the
camera. During the second when visibility was
only about 4.0 m, fish were still identifiable when
photographed within about 3 m. Hence, the fairly
constant depth of focus of the camera's lens, which
was always set at 2.0 m on the distance scale,
standardized the maximum distance ( about 3.5 m)
at which a photographed fish was identifiable.

Linear regressions of logio-transformed fish
counts on estimated underwater visibility provide
further evidence that visibility had little effect on
values. Mean fish and species counts for the 1973
and 1974 island-bottom samples were similar, so
the two were combined as one large sample in =
103) for regression analysis. Although visibility
varied between 2.1 and 15.2 m, the regression was
nonsignificant ( ANOVA F-test, P = 0.3). Even in

372

EBELING ET AL.: ANNUAL VARIABILITY OF REEF FISH

the canopy habitat, the effect of more variable
light levels is apparently not severe. A similar
regression analysis of pooled 1971-72 island-
canopy samples in = 60) was nonsignificant (P =
0.9), though visibility ranged from 4.6 to 10.7 m.

But while such inferences from camera optics
and counts-visibility relations indicate that esti-
mates of relative abundance obtained from cine-
transects are comparable over a wide range of
sampling conditions, we feel that the calibration of
absolute densities presents difficulties. The pri-
mary problem is that, particularly in the kelp
canopy, our estimates of area or volume sampled
are tenuous. For this reason, we used absolute
densities only for computing Wolda's (1978) mea-
sure of annual variation, which required esti-
mated abundances per species, standardized for
differences in sampling effort among years and
between canopy and bottom habitats. We feel that
this is proper because a systematic error in es-
timating will have little effect on the measure's
value, which is based on yearly ratios of popula-
tion sizes, not on sizes per se.

Also, combining canopy and bottom transects
may miss some fish at middepth. Canopy transects
covered depths between 1 and 4 m, which included
the greatest concentration of fish in the upper
water column. Bottom transects covered depths
between the reef and about 2 m upward, which
included greatest concentrations in the lower col-
umn. Nonetheless, over bottoms averaging 8.5 m
deep, cinetransects generally missed the top meter
as well as midwater between 4 and 6.5 m. Hence,
our fish counts, even of overt midwater species,
probably underestimated true abundances.

Annual Variability

Species composition (order of relative or ranked
species abundances), rather than richness
(number of species), contributed most to differ-
ences between mainland and island fish as-
semblages, which were most marked for the bot-
tom assemblages (see also Ebeling et al. in press).
Yearly mainland and island samples had the same
number of species, although island species diver-
sity was slightly greater because individuals were
more evenly distributed among species. At the
island site, species in a "kelp-rock" habitat group
(Ebeling et al. in press) — tropically derived
species such as Pimelometopon pulchrum and G.
nigricans — were relatively more abundant than
at Naples Reef. We had no indication that fishing

intensity for such species (spear fishing, bottom
angling) differed between the two sites. Nor was
unnatural disturbance by kelp harvesting a fac-
tor. Furthermore, virtually unexploited kelp-rock
species, such as Hypsypops rubicundus , were rela-
tively more abundant at Santa Cruz Island. This
indicates that much of the mainland-island differ-
ence in species composition probably reflected the
observed differences in structure of natural
habitat rather than differences in exploitation.
Likewise, but on a broader scale, insular and con-
tinental shore-fish faunas are distinguished in the
tropical western North Atlantic (Robins 1971;
Gilbert 1972). Whereas turbid waters, muddy-
silty bottoms, and few reefs characterize mainland
habitats, clear water, coral reefs, and more stable
conditions typify island habitats. Consequently,
island fish assemblages contain relatively more
specialized reef species, such as pomacentrids and
labrids, that require the trappings and provisions
of complex surfaces.

We felt that composition and abundance of the
fish assemblages remained fairly constant among
years, considering that they inhabit a presumed
zone of faunal transition (Hubbs 1974; Horn and
Allen 1978). Species composition varied more be-
tween sites and habitats than among years. This
indicates that a particular assemblage persists,
despite significant yearly variation in its fish and
species counts. Yet we had few standards for com-
parison. Sale (1978:85) knew of no evidence that
demonstrated "long-term local stability in reef
fish communities," presumably because long-term
monitoring studies were wanting. With a 7-yr
study of fishes inhabiting a rocky tidal pool in the
northern Gulf of California, however, Thomson
and Lehner (1976) showed that fish abundance,
diversity, and species order were seasonally pre-
dictable and varied little from year to year. In fact,
the fish assemblage was remaikably resilient, re-
covering quickly from unpredictable and devastat-
ing disturbances, such as severe storms, winter
kills, and rotenone poisoning. More general-
ly ,Wolda (1978) emphasized the need for actual
measures of annual variability in tropical and
other animal assemblages to test a plethora of
theoretical speculation.

Our values of Wolda's ( 1978) measure of annual
variation (AV) in arrays of species were in fact
relatively low. AV's for fish assemblages at main-
land and island sites (0.11, 0.15) did not differ
significantly (F-tests of variance ratios) from most
of those (0.06-0.33, averaging 0.15) for arthropods

373

FISHERY BULLETIN; VOL. 78, NO. 2

living in humid, climatically stable and more pre-
dictable areas, but were significantly less than
most values (0.12-0.64, averaging 0.34) for ar-
thropods living in dry, climatically unstable envi-
ronments (Wolda 1978: table 2). Values of AV
(0.17, 0.20) that we calculated from annual sight
transects of reef fishes taken off central California
by Miller and Geibel (1973) and Burge and Schultz
(see footnote 6) exceeded our values, but not sig-
nificantly so. But our AV's were significantly less
than the value (0.55) that we calculated from
Livingston's ( 1976) trawl samples of fish from a
Florida estuary during two successive winters (F-
tests of variance ratios, P<0.01). Thus, annual
variation in species abundances of our fish as-
semblages may be more typical of communities in
relatively stable environments than of those from
highly variable environments.

Climatic and other environmental anomalies
may contribute to annual variation. Peak fish
abundance in 1972 occurred in relatively clear and
warm water, which may stimulate fish to be more
active (Quast 1968a, b, c; Larson 1977), and
perhaps more easily photographed. The summer
and fall of 1972 followed a relatively calm winter
of light rainfall (Harger 1979: append. B), and was
a favorable period for growth of small benthic
algae and associated animals, which are impor-
tant forage for surfperches and other microcarni-
vores. On the other hand, poor visibility may have
caused abrupt decreases in counts of Chromis
punctipinnis at the island site in 1973. An obliga-
tory daytime planktivore (Bray 1978), this species
may seek bottom shelter when water is turbid,
(jlenerally, midwater planktivores were more vari-
able in numbers than other species. Decreased
kelp cover at the mainland site in 1974 probably
drove some fish bottomward, but not necessarily
out of view; an aggregate decrease of eight indi-
viduals per canopy transect of C. punctipinnis,
Paralabrax clathratus, and O. californica accom-
panied a corresponding increase of five per bottom
transect.

However, less obvious factors may be more im-
portant, because other periods of clear and warm
water produced no such peak abundances. Time
lags in responses of fish populations to environ-
mental change preclude simple explanations of
annual variation. Lags between bumper births
and subsequent adult recruitment may cause
populations to overshoot their environmental car-
rying capacities (Hutchinson 1978). Alterna-
tively, fixed spawning seasons coupled with an

unpredictable cycle in food production may limit
recruits independently of the carrying capacity of
the environment for adults (Cushing 1969). From
bottom-trawl catches, Mearns'^ concluded that re-
cruitment of juvenile nearshore fishes occurs over
relatively short periods off southern California
and may vary markedly in success among species
from one year to the next. Larson (1977) found that
counts ofS. carnatus andS. chrysomelas decreased
significantly at several depths in an area near the
island site during 1973-76. This decrease may
have been the result of sparse juvenile settlement
observed in 1974-75.

Migration and predation may play a role, espe-
cially at the mainland site, a semi-isolated
offshore reef; e.g., kelp perch, which are canopy
specialists, occurred sporadically and sparsely
there. Kelp cover has varied considerably over the
years. But even though cover may vary at other
places as well, the distance of this reef from exten-
sive kelp beds inshore may have inhibited kelp-
perch recolonization after periods of canopy loss.
Several natural predators eat reef fishes, but we
do not know if the rate varies from year to year.
During the day, harbor seals and sea lions forage
at both sites. Predatory fish such as kelp bass may
eat relatively more young of species such as
surfperches that do not hide in the reef itself, dur-
ing periods when plant cover is sparse. At night,
larger individuals of such prey fish may be par-
ticularly vulnerable to large Pacific electric ray,
Torpedo californica, which invade the reef then
(Bray and Hixon 1978). Love (1978) concluded
that olive rockfish, which grow slowly and seldom
move between reefs, are decimated chronically by
overfishing. Although kelp bass are equally
exploited, adult replacements apparently move in
to restore a portion of a contiguous population
(Quast 1968d).

It is noteworthy that the constancy or "stability"
in species composition of our fish assemblages was
roughly correlated with species diversity. Canopy
assemblages were relatively simple, with many
individuals distributed unevenly among a few
species. They were less constant in composition
than the bottom assemblages, which were charac-
terized by more species and more even distribution
of individuals among species. Also, the island bot-
tom assemblage, which was the more diverse

'^Meams, A. J. 1977. Abundance of bottom fish off Orange
County. In Coastal water research project, annual report 1977,
p. 133-142. Southern California Coastal Water Research Project,
646 W. Pacific Coast Highway, Long Beach, CA 90806.

374

EBELING ET AL.: ANNUAL VARIABILITY OF REEF FISH

because of greater evenness, maintained a more
constant species composition than the mainland-
bottom assemblage. But there is no good basis,
either theoretical (May 1973) or empirical, for as-
suming that this relation is a causal one. Some
diverse communities of coral-reef fishes are
reportedly not stable at all; in fact, fluctuations in
their species composition may actually increase
their diversity (Sale 1977, 1978; Talbot et al.
1978).

Rather, both constancy and diversity of the as-
semblages are probably determined by the type of
habitat in which they live. Thus, the relatively low
diversity and high temporal instability of the
canopy assemblages probably reflect the simplic-
ity and instability of the canopy habitat. Most fish
meet in the canopy to eat plankton or planktivo-
rous fishes. In this way, the canopy habitat is a
concourse, where animals meet for one purpose
(Elton 1927; Whittaker 1965). Here there are rela-
tively few opportunities for diversifying form and
function, and hence fewer species. Relatively few
environmental factors strongly influence species
distributions, as May (1975) suggested in general
for simply structured communities. Ephemeral
currents, turbidity, temperature, and kelp growth
may influence the distribution of canopy dwellers.
Bray (1978) has showTi that the distribution of
adult blacksmith is strongly affected by food-
bearing currents. Adults have largely indepen-
dent sources of food and shelter: the reef provides
shelter but water currents carry in their
planktonic food. Blacksmith feed in dense aggre-
gations, and since local oceanographic conditions
fluctuate rapidly (Quast 1968a) and plankton oc-
curs in patches (Wiebe 1970), the location of their
optimal area of foraging frequently shifts.

In contrast, our bottom assemblages depend on
more stable commodities like rocks and infaunal
prey, which are not so immediately affected by
factors, like currents, that change rapidly. Many
bottom species are solitary, parochial, or even ter-
ritorial (Clarke 1970; DeMartini 1976; Larson
1977; Hixon 1979). Thus, their local density is not
so likely to change from day to day.

The greater variability of the mainland-bottom
assemblage than that of the island is curious.
Perhaps the relative isolation of the mainland site
may contribute to vagarious settlement offish lar-
vae and other recruitment (Larson 1977). Also, the
mainland site has relatively large areas of reef flat
and a surrounding plain of sand and cobble, creat-
ing more of a "transitional" type of habitat.

Periodic occurrences of such species as the black
croaker, Cheilotrema saturnum, and rainbow
surfperch, which are atypical of continuous high-
relief rocky habitats, lend discontinuity to the
Naples fish assemblage.

ACKNOWLEDGMENTS

We thank Milton Love for help in taking and
viewing cinetransects. Norm Lammer provided
much technical assistance with equipment and
boating operations. We appreciate use of the
UCSB Channel Island Field Station, through the
kindness of Carey Stanton who provided access,
and of the U.S. Navy, Port Hueneme who provided
transport. This work was sponsored by NOAA,
Office of Sea Grant, Department of Commerce,
under grant no. 2-35208-6 and 04-3-158-22 (Pro-
ject R-FA-14); by NSF Sea Grants GH 43 and GH
95; and by NSF grants GA 38588 and OCE76-
23301. Supplementary funding was provided by a
UCSB Faculty Research Grant (No. 369) for com-
puter time and by the Marine Science Institute
through the courtesy of Henry Offen.

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377

CERATIOID ANGLERFISHES OF THE PHILIPPINE ARCHIPELAGO,
WITH DESCRIPTIONS OF FIVE NEW SPECIES ^

Theodore W. Pietsch^ and Jeffrey A. Seigel^

ABSTRACT

Ceratioid anglerfishes of the Philippine Archipelago, an area bounded by the islands of the Philippines
to the north, Malaysia and Sumatra to the west, and New Guinea to the east, represent 10 of the 11
ceratioid families, 22 genera and 42 species, 5 species of which are newly described forms of the genus
Oneirodes (Oneirodidae). The vast bulk of this material has recently been provided by midwater
collections made by the Alpha Helix during the 1975 Southeast Asian Bioluminescence Expedition. All
known records of ceratioids are listed with keys to families, genera, and species represented in the area.
Revised and supplemental diagnostic and descriptive data as well as notes on geographic distribution
are also provided.

Our knowledge of the ceratioid anglerfish fauna of
the Philippine Archipelago, an area bounded by
the islands of the Philippines to the north,
Malaysia and Sumatra to the west, and New
Guinea to the east, has recently been broadly ex-
panded by midwater collections made by the RV
Alpha Helix during the 1975 Southeast Asian
Bioluminescence Expedition. This collecting ef-
fort was the first major ichthyological survey of
this part of the world since the historic cruises of
the United States Fisheries steamer Albatross in
1907-09, and the Danish RV Dana in 1929. The
Ceratioidei are now represented by 10 of the 11
families, 22 genera, and 42 species, 5 species of
which are newly described forms of the genus
Oneirodes (Oneirodidae). All known records of
ceratioids from this area are listed below with
keys to families, genera, and species. Revised and
supplemental diagnostic and descriptive data as
well as notes on geographic distribution are also
provided.

METHODS AND MATERIALS

Standard lengths (SL) are used throughout.
Methods for taking counts and measurements,
and terminology used in describing escal mor-
phology follow Pietsch (1974a, fig. 60). Terminol-
ogy used in describing the various parts of the

'Contribution No. 540 from the College of Fisheries, Univer-
sity of Washington, Seattle, WA 98195.

^College of Fisheries, University of Washington, Seattle, WA
98195.

'Section of Ichthyology, Natural History Museum of Los
Angeles County Los Angeles, CA 90007.

Manuscript approved October 1979.
FISHERY BULLETIN: VOL. 78, NO. 2. 1980.

angling apparatus follows Bradbury (1967). Defi-
nitions of terms used for the different stages of
development follow Bertelsen (1951). Locality
data for Alpha Helix stations that yielded
ceratioid material are listed in Appendix 1. Alpha
Helix collections were made with a rectangular
midwater trawl of 8 m^ mouth area (RMT-8) that
was equipped with an opening and closing device.
This gear is more fully described elsewhere
(Clarke 1969; Baker et al. 1973; Hopkins et al.
1973). All Alpha Helix material was deposited in
the Natural History Museum of Los Angeles
County (LACM). Material from other sources is
catalogued in the following institutions: Austra-
lian Museum, Sydney (AMS), Scripps Institution
of Oceanography, La JoUa (SIO), National
Museum of Natural History, Washington, D.C.
(USNM), and the Zoological Museum, University
of Copenhagen (ZMUC). Specimens are females
unless otherwise stated.

KEY TO FEMALES OF THE FAMILIES OF
SOUTHEAST ASIAN CERATIOIDEI

lA. No distal bulb, illicium tipped with fila-
ments; longest rays of dorsal and anal fin
>60'7c of SL Caulophrynidae

IB. A bulbose light organ on tip of illicum;
longest rays of dorsal and anal fin much
<60% SL 2

2 A. More than 11 dorsal fin rays

Melanocetidae

2B. Less than 11 dorsal fin rays 3

3A. Two or three caruncles on back; cleft of
mouth vertical to very oblique . Ceratiidae

379

FISHERY BULLETIN: VOL. 78, NO. 2

3B. No caruncles on back; cleft of mouth
nearly horizontal 4

4A. A second cephalic ray present immedi-
ately posterior to base of illicium, bearing
a distal luminous gland (withdrawn be-
neath skin in larger specimens, its pres-
ence indicated by a small pore)

Diceratiidae

4B. No second cephalic ray 5

5 A. Upper jaw extending anteriorly far be-
yond lower jaw; esca with 1-3 denticles .
Thaumatichthyidae

5B. Jaws equal anteriorly; esca without den-
ticles 6

6 A. Illicium emerging on tip of snout; length
of head <35% SL; length of caudal pedun-
cle >20% SL; 5 pectoral radials

Gigantactinidae

6B. Illicium emerging behind tip of snout;
length of head >35% SL; length of cau-
dal peduncle <20% SL; 3 or 4 pectoral
radials 7

7 A. Dermal spines or plates present 8

7B. Skin naked 10

8A. Skin with some large, bony plates, each

bearing a median spine

Himantolophidae

SB. Skin with numerous, close set spines . . 9

9A. Teeth present on ceratobranchials 1-4; 4
pectoral radials (but fusing to 3 in spec-
imens greater than about 150 mm SL);
larvae and adolescents up to about 50
mm SL with a short, digitiform, hyoid
barbel Centrophrynidae

9B. Ceratobranchial teeth absent; 3 pectoral

radials; no hyoid barbel

Oneirodidae (Spiniphryne)

lOA. Six branchiostegal rays; more than 4 dor-
sal fin rays; anal fin rays 4-7

Oneirodidae

lOB. Four to five branchiostegal rays; 3 dorsal
fin rays, rarely 2 or 4; anal fin rays
2-4 Linophrynidae

CAULOPHRYNIDAE

Key to Females of Genera and Species of
Southeast Asian Caulophrynidae

lA. Illicium short, less than SL; dorsal fin

rays 14-22; anal fin rays 12-19

Caulophryne pelagica (Brauer)

IB. Illicium long, 268% of SL in a 41 mm SL

specimen; dorsal fin rays 6, anal fin

rays 5 Robia legula Pietsch

(known from only the holotype, 41 mm SL)

Caulophryne Goode and Bean 1896

Caulophryne pelagica (Brauer 1902)

Material— LkCM 36023-1, 13 mm SL, stn 143.

A single individual, representing the sixth
known specimen of C. pelagica , and the first record
of this species from southeast Asian waters, was
collected by the Alpha Helix in 1975. It was in-
cluded in a recent revision of the family (Pietsch
1979).

Caulophryne sp. A

Material— LXCM 36025-1, female 98 mm SL with
parasitic male 12 mm SL, stn 37.

This female and parasitically attached male,
collected from the Banda Sea, cannot be placed
within the material of any of the three recognized
species of Caulophryne (Pietsch 1979). The at-
tached male represents the second example of sex-
ual parasitism in the family Caulophrynidae.

Caulophryne sp. B, Figure 1

Material— LkCM 36112-1, 10 mm SL, stn 183;
LACM 36111-1, 10.5 mm SL, stn 184; LACM
36109-2, 11.5 mm SL, stn 193.

These three small females were sorted out of the
Alpha Helix collections after a recent revision of
the family went to press (Pietsch 1979). They dif-
fer significantly from the material of the three
recognized species of Caulophryne in having an
elongate, distally branched, lateral appendage on
each side of the escal bulb; distal escal filaments,
present in all the described species of the genus,
are absent. Although these most likely represent a
new form, the small size of the specimens and their
poor condition do not warrant description at this
time.

Robia Pietsch 1979
Robia legula Pietsch 1979

Material— LACM 36024-1, 41 mm, stn 81 (holo-
type).

This species is known from a single specimen
collected in the Banda Sea (Pietsch 1979).

380

PIETSCH and SEIGEL: CERATIOID ANGLERFISHES OF THE PfflLIPPINE ARCHIPELAGO

Figure l. — Escae of Caulophryne sp. B, left lateral views: A.
LACM 36112-1, 10 mm SL; B. LACM 36111-1, 10.5 mm SL.

and Van Duzer 1980). This species has a wide geo-
graphic distribution in tropical and subtropical
waters of all three major oceans of the world.

Melanocetus murrayi Giinther 1887

Materia/.— LACM 36114-1, 68 mm SL, stn 66;
LACM 36113-1, 82 mm SL,stn 71; LACM 36115-1,
84 mm SL, stn 102.

Melanocetus murrayi is represented by three
females in the Alpha Helix collections (Pietsch
and Van Duzer 1980). This species has a wide
horizontal distribution in the Atlantic and Pacific
Oceans, but is apparently absent from the Indian
Ocean.

Melanocetus sp.

Ma^ena/.— Males: LACM 36067-2, 13.5 mm SL,
stn 23; LACM 36116-1, 21.5 mm SL, stn 84; LACM
36032-4, 22.5 mm SL, stn 110.

These male specimens could not be satisfactor-
ily identified to species (Pietsch and Van Duzer
1980).

HIMANTOLOPHIDAE

MELANOCETIDAE

Melanocetus Gunther 1864

Key to Females of Species of
Southeast Asian Melanocetus

lA. Anterior margin of vomer nearly straight;
width of pectoral fin lobe 10.7-17.8% SL;

number of lower jaw teeth 32-78

M.johnsoni Gunther

IB. Anterior margin of vomer deeply concave;
width of pectoral fin lobe 6.1-8.99f SL;

number of lower jaw teeth 46-142

M. murrayi Gunther

Melanocetus johnsoni Gunther 1864

Materia/.— LACM 36076-3, 14 mm SL, stn 26;
LACM 36059-3, 15 mm SL, stn 103; LACM
36032-3, 15 mm SL, stn 110; LACM 36076-5, 17
mm SL, stn 26; LACM 36074-2, 18 mm SL, stn 120;
LACM 36033-2, 36 mm SL, stn 88.

Six specimens of M.johnsoni were collected by
the Alpha Helix in 1975, all of which were included
in a recent revision of the Melanocetidae (Pietsch

Himantolophus Reinhardt 1837
Himantolophus sp.

Matena/.— Female: LACM 36038-3, 2(12.5-14 mm
SL), stn 87. Males: LACM 36091-4, 16 mm SL,
stn 142; LACM 36057-4, 19 mm SL, stn 93; LACM
36075-4, 4(19.5-21 mm SL), stn 121; LACM
36074-3, 21 mm SL, stn 120; LACM 36040-3, 27.5
mm SL, stn 27; LACM 36046-8, 2(29.5-33 mm SL),
stn 97; LACM 36124-1, 31 mm SL, stn 112.

Thirteen specimens o^ Himantolophus were col-
lected by the Alpha Helix from the Banda, Coram,
and Halmahera Seas. The genus is cosmopolitan
in all three major oceans of the world (Bertelsen
1951), yet no adult females have been collected in
the immediate area. These males and larval
females could not be identified specifically.

DICERATIIDAE

Key to Genera and Species of
Southeast Asian Diceratiidae

lA. Illicium <50% SL; distance between
insertion of illicium and symphysial car-

381

FISHERY BULLETIN: VOL 78, NO. 2

tilage of upper jaw <159^ SL

Diceratias bispinosus (Giinther)

IB. Illicium >80% SL; distance between in-
sertion of illicium and symphysial carti-
lage of upper jaw >30% SL

Phrynichthys thele Uwate

Diceratias Giinther 1887

Diceratias bispinosus (Giinther 1887)

Material.— LACU 36075-1, 20 mm SL, stn 12L

A single specimen oi Diceratias bispinosus was
collected by the Alpha Helix in the Halmahera
Sea. This species is known only from the Indo-West
Pacific (Uwate 1979).

Phrynichthys Pietschmann 1926

Phrynichthys thele Uwate 1979

Material.— hkCM 36077-1, 32 mm SL, stn 155
(holotype); LACM 36076-1, 22 mm, stn 26 (para-
type).

This species is known only from two specimens
collected from the Ceram and Halmahera Seas,
and described in a recent revision of the Dicer-
atiidae (Uwate 1979).

ONEIRODIDAE

Key to Females of Genera of
Southeast Asian Oneirodidae

lA. Skin covered with numerous, close set
spines Spiniphryne Bertelsen

IB. Skin naked 2

2A. Sphenotic spines present; opercle deeply

notched posteriorly 3

2B. Sphenotic spines absent; opercle only

slightly concave posteriorly

Chaenophryne Regan

3 A. Pectoral fin lobe short and broad, shorter

than longest pectoral fin rays 4

3B. Pectoral fin lobe long and narrow, longer

than longest pectoral fin rays

Chirophryne Regan and Trewavas

4A. Lower jaw with a symphysial spine, ven-
tral margin of dentaries at symphysis
convex; caudal fin rays not internally
pigmented 5

4B. Lower jaw without symphysial spine,
ventral margin of dentaries at symphy-

382

sis concave; caudal fin rays internally

pigmented

Pentherichthys Regan and Trewavas

5A. Illicial apparatus emerging from be-
tween frontal bones 6

5B. Illicial apparatus not emerging from
between frontal bones but between
sphenotic spines or further posterior
Lophodolos Lloyd

6A. Dorsal margin of frontal bones strongly
curved; subopercle short and broad, lower
part nearly circular 7

6B. Dorsal margin of frontal bones nearly
straight; subopercle long and narrow,

lower part strongly oval

Dolopichthys Garman

7A. Caudal fin rays covered with black skin
for some distance beyond fin base; anal
fin rays 5, rarely 4 8

7B. Caudal fin rays not coverd by black skin
except at base; anal fin rays 4, rarely
5 Oneirodes Liitken

8 A. Cleft of mouth extending past eye; length
of escal bulb more than half length of
illicial bone; upper part of subopercle

broad and rounded

. . . Microlophichthys Regan and Trewavas

8B. Cleft of mouth not extending past eye;
escal bulb considerably shorter than half
length of illicial bone; upper part of
subopercle slender and tapering to a
point Danaphyrne Bertelsen

Spiniphryne Bertelsen 1951

Spiniphryne gladisfenae (Beebe 1932)

Materia/.— LACM 36073-2, 18 mm SL, stn 94.

Spiniphryne gladisfenae was previously known
only from the Atlantic Ocean (Bertelsen and
Pietsch 1975): three specimens collected from the
eastern tropical Atlantic, and the holotype from
off Bermuda. A fifth specimen, collected in the
Banda Sea by the Alpha Helix, is the first record
from the Pacific.

Oneirodes Liitken 1871

Key to Females of Species of
Southeast Asian Oneirodes

Oneirodes melanocauda, known only from five
larval specimens is omitted from the following key.

PIETSCH and SEIGEL: CERATIOID ANGLERFISHES OF THE PHILIPPINE ARCHIPELAGO

lA.

IB.

2A.

2B.

Epibranchial of first arch toothed

O. carlsbergi (Regan and Trewavas)

Epibranchial teeth absent 2

Anterior escal appendage without in-
ternal pigment; usually two pairs of
filamentous anterolateral escal append-
ages ( O. schmidti group) . . 3

Anterior escal appendage internally pig-
mented; anterolateral escal appendages,
if present, one or four filamentous pairs

3A. Length of all escal appendages less than

length of escal bulb

O. micronema Grobecker

SB. Length of some escal appendages much
greater than length of escal bulb 4

4A. Anterior escal appendage unbranched,
anterolateral escal appendages absent . .
O. alius Seigel and Pietsch

4B. Anterior escal appendage highly branch-
ed, anterolateral escal appendages pres-
ent .. O. sc/imic?^i (Regan and Trewavas)

5A. Medial escal appendages present 6

5B. Medial escal appendages absent 10

6A. Posterior escal appendage cylindrical in
cross section 7

6B. Posterior escal appendage compressed . . 8

7A. Anterior escal appendage cylindrical in
cross section; posterior escal appendage
as long as or longer than length of escal
bulb O. eschrichtii Liitken

7B. Anterior escal appendage laterally com-
pressed; posterior escal appendage less

than half length of escal bulb

O. sabex n.sp.

8A. Medial escal appendages short and close-
ly set in a tight cluster 9

SB. Medial escal appendages elongate and
widely placed O. thysanema n.sp

9A. Anterior escal appendage elongate and
cylindrical in cross section, with a few
short, distal branches; pectoral fin rays
17 O. pterurus n.sp.

9B. Anterior escal appendage short and lat-
erally compressed, with a membra-
nous scalloped distal margin; pectoral

fin rays 13 or 14

O. cristatus (Regan and Trewavas)

lOA. Anterior escal appendage directed dor-
sally; posterior escal appendage as long
as or longer than length of escal bulb ... 11

lOB. Anterior escal appendage directed antero-
ventrally; posterior escal appendage

much shorter than length of escal bulb
O. plagionema n.sp.

IIA. Posterior escal appendage unbranched,
length two to four times length of escal
bulb . . O. flagellifer (Regan and Trewavas)

IIB. Posterior escal appendage branched,
approximately as long as length of escal
bulb O. schistonema n.sp.

Oneirodes carlsbergi (Regan and Trewavas 1932)

Material.— L ACM 36068-2, 19 mm, stn 25.

Oneirodes carlsbergi is known from the western
tropical Atlantic and Pacific Oceans, and from a
single record in the Indo-West Pacific region at
about lat. 17° N, long. 120° E (Pietsch 1974a, fig.
107). An additional specimen, collected by the
Alpha Helix from the Banda Sea, is the second
known record from this part of the world.

Oneirodes cristatus (Regan and Trewavas
1932), Figure 2

Oneirodes cristatus is known only from the type
material (3 females, 20-165 mm SL) collected by
the Dana in the Banda and Celebes Seas (Pietsch
1974a).

Oneirodes eschrichtii Liitken 1871, Figure 3

Material.— L ACM 36049-1, 10.5 mm SL, stn 194;
LACM 36122-2, 12 mm SL, stn 179; LACM
36121-2, 21 mm SL, stn 178.

Oneirodes eschrichtii has a nearly cosmopolitan

Figure 2. — Esca of Oneirodes cristatus, lectotype, ZMUC
P9286, 165 mm SL, left lateral view.

383

FISHERY BULLETIN: VOL. 78, NO. 2

Figure 3.— Esca of Oneimdes eschrichtii, holotype, ZMUC P64,
153 mm SL, left lateral view.

distribution (Pietsch 1974a, fig. 109). Three
specimens of this species were collected by the
Alpha Helix in southeast Asian waters.

Oneirodes flagellifer (Regan and Trewavas
1932), Figure 4, Table 1

Material.— LP^CM 36118-1, 2(10.5-13.5 mm SL),
stn 180; LACM 36117-1, 11.5 mm SL, stn 173;

Figure 4.— Esca of Oneirodes flagellifer, holotype, ZMUC P9280,
22 mm SL, left lateral view.

LACM 36100-2, 12 mm SL, stn 166; LACM
36112-2, 14 mm SL, stn 183; LACM 36109-3, 15.5
mm SL, stn 193.

Table l . — Measurements and counts of specimens of Oneirodes flagellifer. Measurements expressed as percentage of standard

length.

Item

LACIVl 36118-1

LACM 36117-1

LACM 36100-2

LACM 361 18-1

LACM 361 12-2

LACM 36109-3

Standard length (mm)

10.5

11.5

12

13.5

14

15.5

Length:

Head

—

43.5

41.7

46.1

46.4

45.2

Lower jaw

47.8

45.8

46.1

50.0

48.4

Premaxilla

—

34.8

33.3

37.0

35.7

32.3

lllicium

23.8

21.7

—

22.2

25.0

19.3

Head depth

43.5

41.7

37.0

46.4

45.2

Teeth:

Vomer

4

6

6

6

6

7

Upper jaw

16

19

17

28

42

42

Lower jaw

22

30

28

36

45

48

Dorsal fin rays

—

6

5

5

5

5

Anal fin rays

4

4

4

—

4

4

Pectoral fin rays

—

—

15

15

15

14

384

PIETSCH and SEIGEL: CERATIOID ANGLERFISHES OF THE PHILIPPINE ARCHIPELAGO

Oneirodes flagellifer was previously known
from only three specimens, all collected from the
Indo-West Pacific region: the holotypes of O.
flagellifer and O. thysanophorus (= O. flagellifer)
collected by the Dana in 1929, and an additional
specimen collected by the Galathea in 1951
(Pietsch 1974a, fig. 110). The Alpha Helix has
added six additional females from the Sulu Sea
that compare very well with the previously re-
corded material (Table 1).

Oneirodes melanocauda Bertelsen 1951

Oneirodes melanocauda is known from five lar-
val specimens (easily separated from other
Oneirodes larvae by the presence of pigment on
the tips of the caudal fin rays, Pietsch 1974a) three
of which were collected by the Dana in southeast
Asian waters. No additional material was pro-
vided by the Southeast Asian Bioluminescence
Expedition.

Oneirodes plagtonema n. sp. , Figures 5, 6; Table 2

Material. — A single female, the holotype, LACM
36114-2, 25 mm SL, stn 66.

Diagnosis. — A species of Oneirodes differing from
all previously described species in escal morphol-
ogy: anterior appendage narrow, elongate, and
directed anteroventrally; medial appendages
absent; posterior appendage minute; a pair of
filamentous, branched, anterolateral appendages.

Description. — Escal appendage pattern B (Pietsch
1974a, fig. 60B); esca with anterior appendage
narrow and elongate, with a single, short, distal
filament, directed anteroventrally; medial ap-
pendages absent; terminal papilla unusually
large, rounded, with a distal pigment spot; pos-
terior appendage minute; a filamentous, branched,
anterolateral appendage on each side (Figure 5).

Suboperculum short, upper end rounded with-
out indentation on posterior margin (Figure 6);
length of lower fork of operculum 24.0% of SL;
ratio of lengths of upper and lower forks of oper-
culum 0.53.

Epibranchial teeth absent; teeth present on
pharyngobranchial II.

Counts and measurements in Table 2.

Etymology. — The name plagionema is derived
from the Greek plagios, meaning oblique, and
nema, thread, alluding to the oblique, anteroven-
trally directed anterior escal appendage.

Figure 5. — Esca of Oneirodes plagionema n.sp., holotype,
LACM 36114-2, 25 mm SL, left lateral view.

FIGURE 6. — Opercular bones of Oneirodes plagionema n.sp.,
holotype, LACM 36114-2, 25 mm SL, right lateral view.

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FISHERY BULLETIN: VOL. 78, NO, 2

Table 2. — Measurements and counts of four new species of Oneirodes. Measurements expressed as

percentage of standard length.

O plagionema

0 pterurus

0 schislonema

0, Ihysanema

0 thy sane ma

Holotype

Holotype

Holotype

Paratype

Holotype

LACM

LACM

LACIVI

LACt^

USNIVI

Item

36114-2

36075-3

36036-3

36073-4

207931

Standard length (mm)

24

30

74

13

26.5

Length:

Head

458

46.7

37.2

38.5

45.3

Lower jaw

458

50.0

41.2

42.3

47.2

Premaxilla

31 2

35.0

26.3

26.9

30.2

llllclum

25.0

26.7

28.4

15.4

26.4

Head depth

37.5

46.7

28.4

34.6

43.4

Teeth:

Vomer

5

6

6

4

6

Upper jaw

24

30

42

8

32

Lower jaw

35

39

40

10

30

Dorsal fin rays

5

6

6

5

6

Anal fin rays

4

4

4

4

4

Pectoral fin rays

15

17

14

17

17

Oneirodes pterurus n.sp. , Figures 7, 8; Table 2

Material. — A single female, the holotype, LACM
36075-3, 30 mm SL, stn 121.

Diagnosis. — A species of Oneirodes differing from
all previously described species in escal morphol-
ogy: anterior appendage with a few distal
branches; medial appendage represented by a tuft

A

Figure 7. — Esca of Oneirodes pterurus n.sp., holotype,
LACM 36075-3. 30 mm SL: A. Lefl lateral view. B. Posterior view.

386

PIETSCH and SEIGEL: CERATIOID ANGLERFISHES OF THE PHILIPPINE ARCHIPELAGO

Figure 8. — Opercular bones of
Oneirodes pterurus n.sp.,holotype
LACM 36075-3, 30 mm SL, right
lateral view.

of short filaments; posterior appendage non-
filamentous.

Description. — Escal appendage pattern B (Pietsch
1974a, fig. GOB); esca with anterior appendage ap-
proximately as long as escal bulb, bearing three,
short branches at distal tip; distal end of internal,
pigmented tube of anterior appendage with a cir-
cular, translucent "eye-spot"; medial appendage
represented by a tuft of extremely short filaments;
terminal papilla bulbous, with a distal pigment
spot; posterior appendage nonfilamentous, con-
sisting of a large, compressed wedge of tissue on a
short, narrow base, bearing two or three, short
filaments on each side of anterior surface, and two
winglike projections, one above the other, on pos-
terior margin; anterolateral appendages absent
(Figure?).

Suboperculum unusually long and narrow,
upper end tapering to a point without indentation
on posterior margin (Figure 8); length of lower

fork of operculum 27.3% of SL; ratio of lengths of
upper and lower forks of operculum 0.56.

Epibranchial teeth absent; teeth present on
pharyngobranchial II.

Counts and measurements in Table 2.

Etymology. — The name pterurus is derived from
the Greek pteron, meaning wing, and ura, tail,
alluding to the winglike posterior escal appendage
of this species.

Oneirodes sabex n. sp. , Figures 9, 1 0; Table 3

Oneirodes eschrichtii Pietsch 1974a: 100, 103,
fig. 116B (misidentification).

Material. — Fourteen metamorphosed females,
12-121 mm. Holotype: LACM 36116-3, 46 mm
SL, stn 84. Paratypes: LACM 36087-4, 3( 12-26.5
mm SL), stn 135; LACM 36068-3, 12 mm SL, stn
25; LACM 36028-5, 13 mm SL, stn 141; LACM
36023-3, 13 mm SL, stn 143; LACM 36089-4,
2(15-17 mm SL), stn 137; LACM 36051-3, 15 mm
SL, stn 38; LACM 36088-4, 15.5 mm SL, stn 136;
AMS 1.20315-010, 32.5 mm SL, Kapala, lat. 33°53'
S, long. 152°02' E, Engel Midwater Trawl, 0-900
m, bottom depth 1,800 m, 1330-1990 h, 14 De-
cember 1977; AMS 1.20314-016, 39 mm SL,
Kapala, lat. 33°28' S, long. 152°33' E, Engel Mid-
water Trawl, 0-900 m, bottom depth 4,200 m,
0530-1045 h, 14 December 1977; SIO 70-339, 121
mm SL, lat. 19°35' N, long. 122°57' E, 3 m IKMT
(Isaacs-Kidd Midwater Trawl), 0-1,450 m, 1845-
0225 h, 15-16 September 1970.

Diagnosis. — A species of Oneirodes differing from
all previously described species in escal morphol-
ogy: anterior appendage noncylindrical, com-
pressed, without pigmented, internal tube; medial
appendage present; posterior appendage cylindri-
cal, unbranched.

Description. — Escal appendage pattern B (Pietsch
1974a, fig. 60B); esca with anterior appendage
noncylindrical, strongly compressed and rounded,
darkly pigmented along distal margin in some
specimens; a pair of filamentous medial append-
ages; terminal papilla usually with two distal
pigment spots situated on midline, one just behind
the other; posterior appendage short, stout, and
cylindrical; anterolateral appendages absent
(Figure 9; Pietsch 1974a, fig. 116B).

Suboperculum short, upper end tapering to a

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FISHERY BULLETIN: VOL. 78, NO. 2

Figure 9. — Escae of Oneirodes sabex n.sp., left lateral views: A. Paratype,
LACM 36089-4, 17 mm SL; B. Paratype, LACM 36087-4, 26.5 mm SL; C.
Holotype, LACM 36116-3, 46 mm SL.

1 mw

point without indentation on posterior margin
(Figure 10); length of lower fork of operculum
27.1% of SL; ratio of lengths of upper and lower
forks of operculum 0.48.

Epibranchial teeth absent; teeth present on
pharyngobranchial II.

Counts and measurements in Table 3.

Figure lO. — Subopercula of Oneirodes sabex n.sp., right lateral
views: A. Paratype, LACM 36089-4, 17 mm SL; B. Paratype,
AMS L20315-010, 32 mm SL; C. Holotype, LACM 36116-3, 46
mm SL.

Table 3. — ^Measurements and counts of specimens of Oneirodes sabex n.sp. Measurements expressed as percentage of standard

length.

Paratype

Holotype

Paratype
SIO

LACM

LACM

UVCM

LACM

LACM

U\CM

U\CM

lACM

LACM

Item

36068-3

36028-5

36087-4

36089-4

36051-3

36088-4

36089-4

36087-4

36116-3

70-339

Standard length (mm)

12

13

13

15

15

15.5

17

26.5

45.5

121

Length:

Head

41.7

46.1

38.5

43.3

400

41.9

353

39.5

37.4

35.1

Lower jaw

45.8

42.3

42.3

46.7

43.3

48.4

35.3

45.3

41.8

36.7

Premaxilla

29.2

30.8

30.8

33.3

30.0

32.3

23.5

32.1

27.5

26.0

llllcium

20.8

19.2

19.2

26.7

23.3

29.0

17.6

26.5

18.7

14.4

Head Depth

41.7

38.5

38.5

43.3

400

45.2

35.3

41.5

38.5

34.2

Teeth:

Vomer

4

4

4

8

4

6

4

6

6

6

Upper jaw

5

15

—

22

23

34

25

30

26

42

Lower jaw

5

26

21

30

30

34

25

37

41

50

Dorsal fin rays

6

5

6

6

6

6

6

5

6

6

Anal fin rays

4

4

4

4

4

4

4

4

4

4

Pectoral fin rays

—

16

16

15

15

16

17

15

14

16

388

PIETSCH and SEIGEL: CERATIOID ANGLERFISHES OF THE PHILIPPINE ARCHIPELAGO

Distribution. — Oneirodes sabex is known only
from southeast Asian and eastern Australian
waters: the Alpha Helix material, including the
holotype and 10 paratypes, was collected in the
Banda Sea; the 121 mm SL paratype (SIO 70-339)
is from off Luzon, Philippines; the 32.5 and 39 mm
SL paratypes (AMS L 20315-010, AMS L20314-
016) were collected off Sydney, Australia.

Etymology. — The name sabex is an acronym
formed from the initial letters of the name "South-
east Asian Bioluminescence Expedition" in recog-
nition of the important ichthyological contribu-
tion made by those involved.

Oneirodes schistonema n. sp. , Figures 11, 12; Table 2

Material. — A single female, the holotype, LACM
36036-3, 74 mm, stn 24.

Diagnosis. — A species of Oneirodes differing from
all previously described species in escal morphol-

ogy: anterior appendage branched, unpigmented
internally; medial and anterolateral appendages
absent; posterior appendage branched.

Description. — Escal appendage pattern B (Pietsch
1974a, fig. 60B); esca with a stout, unpigmented,
anterior appendage, less than length of escal bulb,
bearing four, short, distal branches; pigmented
internal tube of anterior appendage absent; me-
dial and anterolateral appendages absent; termi-
nal papilla without distal pigment spot; posterior
appendage as large as anterior appendage, bear-
ing four short branches near distal end (Figure
11).

Upper end of suboperculum long, narrow, and
tapering, left suboperculum deeply indented (Fig-
ure 12); length of lower fork of operculum 25. 3^^ of
SL; ratio of lengths of upper and lower forks of
operculum 0.48.

Epibranchial teeth absent; teeth present on
pharyngobranchial IL

Counts and measurements in Table 2.

Etymology . — The name schistonema is derived
from the Greek schistos, meaning divided, and
nema, thread, alluding to the divided anterior and
posterior escal appendages of this species.

Oneirodes thysanema n. sp. , Figures 13, 14; Table 2

Material. — Two females, 13 and 26.5 mm SL.
Holotype: USNM 207931, 26.5 mm SL; Ocean Acre
cruise 7, stn 13N, Bermuda, lat. 32°18' N, long.
63°30' W, 3 m IKMT, 0-1,500 m, 1430-1730 h, 8

Figure ll. — Esca of Oneirodes schistonema n.sp., holotype,
LACM 36036-3, 74 mm SL, left lateral view.

FIGURE 12. — Subopercle of Oneirodes schistonema n.sp.,
holotype, LACM 36036-3, 74 mm SL: A. Right lateral view; B.
Left lateral view.

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FISHERY BULLETIN: VOL. 78, NO. 2

FIGURE 13.— EscaotOneirodes thysanema n.sp.,USNM 207931,
holotype, 26.5 mm SL, left lateral view.

■S mm

Description. — Escal appendage pattern B (Pietsch
1974a, fig. 60B); esca with a stout, internally pig-
mented, anterior appendage, greater than length
of escal bulb, bearing along posterior margin a
single branched filament proximally, and a series
of unbranched filaments distally; medial append-
ages in three groups, a highly filamentous pair
lying between a similar, but unpaired appendage,
and a series of three, stout papillae situated at the
base of the terminal papilla; terminal papilla un-
usually long, directed posterodorsally; posterior
appendage as long as anterior appendage, highly
compressed, bearing one or two, short, lateral
filaments, and a considerably longer, branched,
filamentous, anterolateral appendage on each
side; distal tip of internal tube of anterior append-
age, and dorsal pigment patch of escal bulb with a
paired circular, translucent "eye spot" (Figure 13).

Suboperculum short and broad, upper end
rounded without indentation on posterior margin
(Figure 14); length of lower fork of operculum
27.7-30.2% of SL; ratio of lengths of upper and
lower forks of operculum 0.48-0.50.

Epibranchial teeth absent; teeth present on
pharyngobranchial II.

Counts and measurements in Table 2.

Etymology. — The name thysanema is derived from
the Greek thysanos, meaning a fringe, and nema,
thread, alluding to the numerous filaments fring-
ing the anterior escal appendage of this species.

Oneirodes alius Seigel and Pietsch 1978,
Figure 15, Table 4

Material.— hkCM 36026-1, 38 mm SL, stn 122
(holotype); LACM 36027-1, 18 mm SL, stn 147
(paratype); LACM 36028-1, 21 mm SL, stn 141

Figure 14. — Subopercula of Oneirodes thysanema n.sp., right
lateral views: A. Paratype, LACM 36093-4, 13 mm SL; B. Holotype,
USNM 207931, 26.5 mm SL.

September 1969.
mm SL, stn 94.

Paratype: LACM 36073-4, 13

Diagnosis. — A species of Oneirodes differing from
all previously described species in escal mor-
phology: anterior appendage with a series of fila-
ments along posterior margin; medial appendages
in three groups; terminal papilla elongate; poste-
rior appendage compressed and branched.

Table 4. — Measurements and counts of specimens of Oneirodes
alius. Measurements expressed as percentage of standard
length.

LACM

LACM

LACM

LACM

Item

36089-2

36091-2

36091-2

36096-2

Standard length (mm)

10

11.5

11.5

12

Length:

Head

45.0

39,1

39.1

37.5

Lower jaw

40.0

43.5

43.5

45.8

Premaxilla

20.0

21.7

26.1

25.0

lllicium

20.0

17.4

17.4

16.7

Head depth

40.0

34.8

34.8

33.3

Teeth:

Vomer

4

4

4

4

Upper jaw

—

—

—

14

Lower |aw

—

—

18

16

Dorsal fin rays

5

5

7

6

Anal fin rays

4

4

4

4

Pectoral fin rays

15

—

15

16

390

PIETSCH and SEIGEL: CERATIOID ANGLERFISHES OF THE PHILIPPINE ARCHIPELAGO

Figure 15. — Esca of Oneirodes alius, holotype,
LACM 36026-1, 38 mm SL, left lateral view.

(paratype); LACM 36089-2, 10 mm SL, stn 137;
LACM 36091-2, 2(11.5 mm SL), stn 142; LACM
36096-2, 12 mm SL, stn 150.

Oneirodes alius, a member of the O. schmidti
group (Pietsch 1974a), was originally described
from three specimens collected by the Alpha Helix
in the Halmahera Sea (Seigel and Pietsch 1978).
After the description went to press, four additional
specimens were sorted out from Alpha Helix sta-
tions made in approximately the same localities as
the type-material. In all respects, these specimens
compare well with the original description.

Oneirodes schmidti (Regan and Trewavas 1932),
Figures 16, 17; Table 5

Material.— LKCM 36031-3, 15.5 mm SL, stn 58;
LACM 36057-3 2(65-92 mm SL), stn 93; LACM
36067-3, 78 mm SL, stn 23.

The 1975 Southeast Asian Bioluminescence
Expedition of the Alpha Helix provided the first
representatives of O. schmidti since the capture of
the holotype by the Dana in 1929. The new mate-
rial compares well with the type-specimen in all
characters, except for some minor differences in
escal morphology. The species is redescribed below
based on the new Alpha Helix material.

Description. — Escal appendage pattern C (Pietsch
1974a, fig. 60C); esca with a large, complex an-
terior appendage consisting of a wide, compressed
base bearing a relatively short, unpaired and
branched filament on posterior margin, two ex-
tremely long, distal filaments ( about 16.3 to 17.3%
of SL) that bifurcate as many as five times, and a
stout, bifurcated, medial filament each branch of
which becomes highly branched distally; a pair of
filamentous, highly branched, medial appendages
less than length of escal bulb; terminal papilla

U

Table 5. — Measurements and counts ofOneirodes schmidti. Mea-
surements expressed as percentage of standard length.

■ -fl^

■■

*

•^

tJ

*-**"'"

LACM

VACU

LACI^I

LACM

i-7

Item

36031-3

36067-3

36057-3

36057-3

Standard length (mm)
Length:

15.5

78

92

65

J

Head

45.2

44.9

46.2

47.7

•W

Lower jaw

51.7

51.3

52.7

52.3

• i^

Premaxilla

38.7

35.9

36.4

40.0

:''W

llllclum

35.5

107.7

91.3

87.7

w

Head depth

38.7

46.1

42.4

46.1

f

Teeth:

,<y

Vomer

4

6

5

5

1 mm

Upper jaw

29

66

67

62

Lower jaw

36

57

56

65

Dorsal fin rays

6

6

5

6

Anal fin rays

4

4

4

4

Pectoral fin rays

16

16

17

16

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FISHERY BULLETIN: VOL. 78. NO. 2

FIGURE 16.— Esca of Oneirodes schmidti, LACM 36057-3, 65 mm SL, left lateral view.

392

PIETSCH and SEIGEL: CERATIOID ANGLERFISHES OF THE PHILIPPINE ARCHIPELAGO

Figure 17. — Subopercula of Oneirodes schmidd, right lateral
views: A. LACM 36057-3, 65 mm SL; B. LACM 36067-3, 78 mm
SL; C. LACM 36057-3, 92 mm SL.

the anterior appendage of the new material; Fig-
ure 16).

Suboperculum long and narrow, upper part ta-
pering without indentation on posterior margin
(Figure 17; Pietsch 1974a:78, fig. 98); length of
lower fork of operculum 26.6-27.7% of SL; ratio of
lengths of upper and lower forks of operculum
0.47-0.51.

Epibranchial teeth absent; teeth present on
pharyngobranchial II.

Counts and measurements in Table 5.

Distribution. — All five known specimens of O.
schmidti, including the holotype, were collected in
the Banda Sea.

with a single, distal streak of pigment; a slender,
unbranched posterior appendage less than length
of escal bulb; a relatively short, filamentous,
branched, anterolateral appendage on each side
(the inner pair of stout, anterolateral appendages
described for the holotype of O. schmidti by
Pietsch 1974a: 78, fig. 99, correspond to the elon-
gate, bifurcated filaments that are associated with

Oneirodes micronema Grobecker 1978, Figure 18.

Materia/.— LACM 36039-3, 89 mm SL, stn 113
(holotype); LACM 36043-3, 17 mm SL, stn 157
(paratype).

This species, a member of the O. schmidti group
(Pietsch 1974a), was recently described by
Grobecker (1978) based on two females collected in
the Banda Sea.

.. 5 inni

Figure 18. — Esca of Oneirodes micronema, holotype, LACM
36039-3, 89 mm SL, left lateral view.

Oneirodes sp. of Oneirodes schmidti Group,
Bertelsen 1951

Material. — LACM 36046-6, metamorphosed
female, 13 mm SK, stn 97 (illicivim length 36. 99^ of
SL).

Oneirodes sp.

Material. — Adolescent and adult males and
females, and metamorphosing stages not identifi-
able to species or species group. Metamorphosed
females representing possible new species: LACM
36087-5, 13 mm SL, stn 135 (illicium 15.4% of SL,
upper jaw teeth 14, lower jaw teeth 21, pectoral fin
rays 15); LACM 36089-5, 14 mm SL, stn 137 (il-
licium 14.3% of SL, upper jaw teeth 15, lower jaw
teeth 20, pectoral fin rays 15; esca like that of
LACM 36087-5); LACM 36115-2, 21 mm SL, stn
102 (illicium 23.8% of SL, upper jaw teeth 27,
lower jaw teeth 38, pectoral fin rays 16). Metamor-
phosing females: LACM 36121-1, 2(7.5-9 mm SL),
stn 178; LACM 36106-2, 8.5 mm SL, stn 187;
LACM 36088-3, 9.5 mm SL, stn 136; LACM
36049-3, 9.5 mm SL, stn 194; LACM 36073-3, 10
mm SL, stn 94; LACM 36087-3, 10 mm SL, stn 135;
LACM 36028-4, 10 mm SL, stn 141; LACM

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FISHERY BULLETIN: VOL. 78, NO. 2

36046-5, 11 mm SL, stn 97; LACM 36027-3, 1 1 mm
SL, stn 147; LACM 36076-4, 11.5 mm SL, stn 26.
Metamorphosed males: LACM 36108-2, 8.5 mm
SL, stn 192; LACM 36087-2, 4(9-10 mm SL), stn
135; LACM 36081-2, 3(9.5 mm SL), stn 127a;
LACM 36104-2, 2(9.5-11.5 mm SL), stn 175;
LACM 36039-5, 2(10-11 mm SL), stn 113; LACM
36024-4, 3(10-12 mm SL), stn 81; LACM 36057-5,
2(10-12 mm SL), stn 93; LACM 36023-4, 4(10-12
mm SL), stn 143; LACM 36028-3, 3(10-13.5 mm
SL), stn 141; LACM 36048-4, 10.5 mm SL, stn 36;
LACM 36073-5, 2(10-5 mm SL), stn 94; LACM
36117-2, 10.5 mm SL, stn 173; LACM 36109-4,
10.5 mm SL, stn 193; LACM 36119-1, 2(10.5-13.5
mm SL), stn 96; LACM 36026-2, 11 mm SL, stn
122; LACM 36090-2, 3(11-12 mm SL), stn 138;
LACM 36027-3, 11 mm SL, stn 147; LACM
36118-2, 11 mm SL, stn 180; LACM 36076-6, 12
mm SL, stn 26; LACM 36095-2, 12 mm SL, stn 149;
LACM 36077-4, 12 mm SL, stn 155; LACM
36122-1, 12 mm SL, stn 179; LACM 36084-2,
2(12-12.5 mm SL), stn 130; LACM 36091-3, 2(12-
12.5 mm SL), stn 142; LACM 36089-3, 6(12-13 mm
SL), stn 137; LACM 36085-2, 3(12-14 mm SL), stn
133; LACM 36120-1, 12.5 mm SL, stn 123; LACM
36041-4, 4(12.5-13 mm SL), stn 39; LACM 36088-
2, 13 mm SL, stn 136; LACM 36024-3, 13 mm SL,
stn 81.

Danaphryne Bertelsen 1951

Danaphryne nigrifilis (Regan and Trewavas 1932)

Danaphryne nigrifilis is known from eight
specimens, one of which (the holotype, 24 mm SL,
ZMUC P92102) was collected by the Dana in the
South China Sea (Bertelsen and Pietsch 1977). No
additional material was provided by the Alpha
Helix.

all respects, these specimens fall within the ob-
served variation of M. microlophus .

Chirophryne Regan and Trewavas

Chirophryne xenolophiis Regan and Trewavas 1932

Chirophryne xenolophus is known from only two
specimens, the holotype ( 1 1 mm SL, ZMUC P9296)
collected by the Dana in the South China Sea, and
a second specimen (22 mm SL, SIO 70-306) from
off Japan at about lat. 32°10' N, long. 136°05' E
(Pietsch 1978).

Dolopichthys Garman 1899
Dolopichthys pullatus Regan and Trewavas 1932

Materia/.— LACM 36116-2, 113 mm SL, stn 84.

Thirty-three metamorphosed females of D. pul-
latus (10-115 mm) have been previously reported
from localities in the Atlantic, the Gulf of Mexico,
and the eastern Pacific and Indian Oceans (Pietsch
1972). The holotype of D. pullatus is the only pre-
vious record from the western Pacific. One ad-
ditional specimen collected by the Alpha Helix
from the Banda Sea constitutes the second record
from the Indo-West Pacific Ocean.

Dolopichthys longicornis Parr 1927

Materia/.— LACM 36046-3, 8.5 mm, stn 97.

Dolopichthys longicornis was previously known
from 18 metamorphosed females (14-159 mm) col-
lected from the Atlantic, Indian, and eastern
Pacific Oceans (Pietsch 1972). The holotype of Z).
mucronatus ( = D. longicornis), collected in the
South China Sea, is the only previous western
Pacific record. An additional specimen was col-
lected by the Alpha Helix in the Banda Sea.

Microlophichthys Regan and Trewavas 1932 Dolopichthys sp.

Microlophichthys microlophus (Regan 1925)

Mater/a/.— LACM 36024-7, male, 17 mm SL, stn
81; LACM 36048-3, female, 22 mm SL, stn 36;
LACM 36047-3, female 29 mm SL, stn 89.

Twenty-three metamorphosed females of this
species (12-99 mm SL) have been previously re-
ported from localities in the Atlantic, Indian, and
Pacific Oceans (Bertelsen and Pietsch 1977). Two
additional females and a male were collected by
the Alpha Helix in the Banda and Ceram Seas. In

394

Material. — LACM 36071-2, metamorphosed male,
12 mm, stn 59.

Chaenophryne Regan 1925

Chaenophryne longiceps Regan 1925

Mater/a/.— LACM 36039-4, metamorphosed male,
10.5 mm, stn 113.

This species has a cosmopolitan distribution in
all three major oceans of the world (Pietsch 1975).

PIETSCH and SEIGEL: CERATIOID ANGLERFISHES OF THE PHILIPPINE ARCHIPELAGO

A single male taken by the Alpha Helix in the
Banda Sea consitutes the second record for this
species in southeast Asian waters.

Chaenophryne draco Beebe 1932

Material.— hACM 36073-6, 17 mm, stn 94; LACM
36123-1, 21.5 mm, stn 80.

Chaenophryne draco has a wide distribution oc-
curring in all three major oceans of the world
(Pietsch 1975). Two metamorphosed females col-
lected by the Alpha Helix in the Banda Sea consti-
tute the first records of this species in southeast
Asian waters.

Chaenophryne sp. of Chaenophryne draco Group

Material. — LACM 36046-7, metamorphosed male,
10 mm, stn 97.

Pentherichthys Regan and Trewavas

Pentherichthys sp.

The genus Pentherichthys is represented in
southeast Asian waters by only two larval speci-
mens (Bertelsen 1951). No additional material
was provided by the Alpha Helix.

terior nostril well separated from eye; operculum
deeply notched posteriorly; suboperculum short
and broad, upper end rounded; inner side of sub-
operculum darkly pigmented; subdermal pigment
continuous over body to posterior margin of caudal
peduncle; pectoral rays on end of a relatively
short, broad lobe; dorsal fin rays 6, anal fin rays 4,
pectoral fin rays 15.

Comments. — These males are similar to
Oneirodes and Microlophichthys in having a
short, rounded suboperculum. They differ from
Oneirodes, however, in having the skin between
the anterior nostrils lightly pigmented, the inner
surface of the suboperculum darkly pigmented,
and the body covered with subdermal pigment to
the base of the caudal fin. On the other hand, they
differ from Microlophichthys in the absence of a
distinct, separate patch of pigment on the caudal
peduncle, and in having four, instead of five anal
fin rays.

THAUMATICHTHYIDAE

Thaumatichthys Smith and Radcliffe 1912

Thaiimatichthys pagidostomns
Smith and Radcliffe 1912

Lophodolos Lloyd 1909

Lophodolos indicus Lloyd 1909

Materia/.— LACM 36116-4, 69 mm, stn 84.

Twenty-two female specimens of this species
were previously recorded from localities in the
eastern Atlantic, and the Indian and Pacific
Oceans between about lat. 4° S and 30° N (Pietsch
1974b). One additional specimen was collected by
the Alpha Helix in the Banda Sea.

Oneirodidae gen. et sp. .-^

Material. — Two metamorphosing males: LACM
36069-3, 11 mm, stn 28; LACM 36039-3, 11.5 mm,
stn 113.

These two metamorphosing males cannot be
reasonably placed within any known oneirodid
genus. Both are very similar in having the follow-
ing characteristics:

Description. — Nostrils opening forward; skin be-
tween anterior nostrils lightly pigmented; pos-

Thaumatichthys pagidostomus is known from
only the holotype (60 mm SL, USNM 72952) col-
lected by the Albatross off Sulawesi (Bertelsen
and Struhsaker 1977).

CENTROPHRYNIDAE

Centrophryne Regan and Trewavas 1932

Centrophryne spinulosa Regan and Trewavas 1932

Centrophryne spinulosa is known from 15
metamorphosed females and 2 metamorphosing
males. The lectotype (39 mm SL female, ZMUC
P92122), collected by the Dana off the northern
coast of New Guinea, is the only record from the
western Pacific (Pietsch 1972).

CERATIIDAE

Key to Females of Genera and
Species of Ceratiidae

lA. Illicium long, much longer than bulb

395

FISHERY BUIXETIN: VOL. 78, NO. 2

of esca; 2 caruncles on back; subopercle

without spine on anterior margin

Ceratias sp.

IB. Illicium short, nearly completely envel-
oped by bulb of esca; 3 caruncles on back;
subopercle with spine on anterior mar-
gin Cryptopsaras couesi Gill

Ceratias Kroyer 1845

Ceratias sp.

Materia/.— L ACM 36046-9, 9 mm, stn 97; LACM
36034-3, 2(10-18 mm), stn 85; LACM 36047-4, 10.5
mm, stn 89; LACM 36073-7, 1 1 mm, stn 94; LACM
36125-1, 12 mm, stn 72; LACM 36032-5, 13 mm,
stn 110; LACM 36074-4 13.5 mm, stn 120; LACM
36076-7, 13.5 mm, stn 26; LACM 36027-4, 15 mm,
stn 147; LACM 36064-2, 16.5 mm, stn 152; LACM
36058-2, 18 mm, stn 99; LACM 36029-2, 23 mm,
stn 162; LACM 36093-2, 25 mm, stn 146.

Fourteen female specimens of the genus
Ceratias were collected by the Alpha Helix from
the Banda, Celebes, Ceram, and Halmahera Seas.
All of these are adolescent females in which the
diagnostic characters of the esca have not as yet
developed. Since there are two, perhaps three
species o^ Ceratias (Bertelsen 1951), specific iden-
tification is impossible at this time.

Cryptopsaras Gill 1883

Cryptopsaras couesi Gill 1883

Materia/.— LACM 36031-4, 8 mm, stn 58; LACM
36090-3, 3(8.5-12.5 mm), stn 138; LACM 36029-3,
2(9.5-10 mm), stn 162; LACM 36042-2, 10 mm, stn
74; LACM 36074-5, 10 mm, stn 120; LACM
36034-4, 10 mm, stn 85; LACM 36100-3, 10 mm,
stn 166; LACM 36109-5, 10 mm, stn 193; LACM
36087-8, 2(10-10.5 mm), stn 135; LACM 36040-4,
3(10-102 mm), stn 27; LACM 36051-4, 11 mm, stn
38; LACM 36028-6, 11 mm, stn 141; LACM
36129-1, 11 mm, stn 181; LACM 36130-1, 11 mm,
stn 186; LACM 36085-4, 2(11-13 mm), stn 133;
LACM 36089-6, 11.5 mm, stn 137; LACM 36063-3,
11.5 mm, stn 140; LACM 36077-5, 2(11.5-12.5
mm), stn 155; LACM 36127-1, 12 mm, stn 167;
LACM 36122-3, 12 mm, stn 179; LACM 36126-1,
12.5 mm, stn 18; LACM 36037-2, 12.5 mm, stn 82;
LACM 36117-3, 12.5 mm, stn 173; LACM 36084-3,
6(12.5-85 mm), stn 130; LACM 36055-2, 13 mm,
stn 79; LACM 36091-5, 13 mm, stn 142; LACM

396

36108-3, 13 mm, stn 192; LACM 36067-4, 14 mm,
stn 23; LACM 36075-5, 14 mm, stn 121; LACM
36064-3, 4(14-19.5 mm), stn 152; LACM 36080-2,
16 mm, stn 126; LACM 36128-1, 19.5 mm, stn 91;
LACM 36073-8, 59 mm, stn 94; LACM 36124-2, 94
mm, stn 112.

Cryptopsaras couesi has a cosmopolitan dis-
tribution in all three major oceans of the world
(Bertelsen 1951). Fifty specimens were collected
by the Alpha Helix from the Banda, Celebes, Hal-
mahera, Sulu, and Timor Seas.

GIGANTACTINIDAE

Gigantactis Brauer 1902

Gigantactis latihoeffeni Brauer 1902

Materia/.— LACM 36031-1, 17 mm, stn 58; LACM
36039-6, 2(24-31 mm), stn 113; LACM 36032-1, 25
mm, stn 110; LACM 36046-10, 26 mm, stn 97;
LACM 36131-1, 32 mm, stn 51; LACM 36034-5, 34
mm, stn 85.

The Alpha Helix collected seven females (six
metamorphosed and one in metamorphosis) of G.
vanhoeffeni, all from the Banda Sea. These have
been incorporated in a forthcoming revision of the
Gigantactindae (Bertelsen et al. in press).

Gigantactis sp. Male Group II, Bertelsen et al. in press

Mater/a/.— LACM 36034-1, 2( 12-12.5 mm), stn 85;
LACM 36033-1, 2(13-14 mm), stn 88; LACM
36032-1, 13.5 mm, stn 110.

Gigantactis sp. Male Group IV,
Bertelsen et al. in press

Materia/.- LACM 36030-1, 16.5 mm, stn 109.

Gigantactinidae gen. et sp. ?

Materia/.— LACM 36024-6, male, 11.5 mm, stn 81.
This male cannot reasonably be placed within
either of the two known gigantactinid genera
(Bertelsen et al. in press).

LINOPHRYNIDAE

Key to Females of Genera and Species of
Southeast Asian Linophrynidae

lA. Skin transparent; hyoid barbel absent;

PIETSCH and SEIGEL: CERATIOID ANGLERFISHES OF THE PHILIPPINE ARCHIPELAGO

jaw teeth small and numerous ACKNOWLEDGMENTS

Edriolychnus schmidti Regan

IB. Skin darkly pigmented; hyoid barbel pres- We thank E. Bertelsen for critically reading the

ent; teeth large and few manuscript and offering valuable suggestions.

Linophryne Collett. . 2 The following people and institutions provided

2A. Distal escal appendages present; barbel material: Bruce H. Robison, Marine Science Insti-

distally divided into about 6 branches . . tute, University of California Santa Barbara;

Linophryne corymbifera Robert J. Lavenberg and Jerry W. Neumann,

Regan and Trewavas LACM; John R. Paxton, AMS; Robert H. Gibbs and
2B. Distal escal appendages absent; barbel Susan Karnella, USNM; and Richard H. Rosen-

unbranched blatt and Jan Pulsifer, SIO. The work was sup-

Linophryne trewavasae Bertelsen ported by National Science Foundation Grants

GB-40700, DEB 76-82279 and DEB 7826540, the
Edriolychnus Regan 1925 National Geographic Society, and PHS Biomedical

Research Support Grant No. RR-07096 adminis-
Edriolychnus schmidti Regan 1925 tered through the Graduate School Research Fund

of the University of Washington.
Edriolychnus schmidti is a relatively common
ceratioid occurring in all three major oceans of the

world (Bertelsen 1951). No additional material, LITERATURE CITED

however, was provided by the Alpha Helix in 1975.

Baker, a. de C, M. R. Clarke, and M. J. Harris.

Lmotfbrrne Coliett 1886 ^^^^' Th^N.I.O. combination net (RMT 1+8) and further

developments of rectangular midwater trawls. J. Mar
Biol. Assoc. U.K. 53:167-184.
Linophryne corymbifera Regan and Trewavas 1932 Beebe, W

1932. Nineteen new species and four post-larval deepsea
Material.— \.KQM 36046-11, female, 42 mm SL fish. ZoologicaiN.Y.) 13:47-107.

with parasitic male, 9.5 mm SL. stn 97. ®^^Tn^f ^;;^' •. . u ^ .• u

. . . . 1951. Ihe ceratioid fishes. Ontogeny, taxonomy, distnbu-

A Single female with parasitic male, represent- tion and biology. Dana Rep., Carlberg Found. 39, 276 p.

ing the first known incidence of sexual parasitism 1978. Notes on linophrynids IV. A new species of deep-sea
in this species, was collected by the AlphaHelix in anglerfish of the genus Lmop/iO'«e and the first record of a

the Banda Sea. The specimen was referred to as parasitic male m Linophryne corymbifera (Pisces,

J- ■ L A u TT J TT • .ir^nt-rs Ceratioldei) . Steenstrupia 5(3):25-32.

Linophryne sp. A by Hansen and Herring ( 1977), bertelsen, E., and T. W. Pietsch.

and recently described and figured by Bertelsen 1975. Results of the research cruises of FRV "Walther

(1978). Herwig" to South America. XXXVIII. Osteology and

relationships of the ceratioid anglerfish genus Spini-

... ^ , ,^_„ phryne (family Oneirodidae). Arch. Fischereiwiss.

Linophryne trewavasae Bertelsen 1978 26(1)1 11

1977. Results of the research cruises of FRV "Walther
Material .—LACM 36116-5, female, 73.5 mm SL Herwig"toSouth America. XLVII. Ceratioid anglerfishes

with parasitic male, 10.7 mm SL, stn 84 ofthefamily Oneirodidae collected by the FRV "Walther

(holotype) Herwig". Arch. Fischereiwiss. 27(31:171-189.

X. , ' , ^1 J -1 J Bertelsen, E., T. w Pietsch, AND R. J. Lavenberg.

Linophryne trewavasae was recently described j„ ^^^^^ Morphology, systematics and distribution of

by Bertelsen (1978) from a single female with an ceratioid anglerfishes of the family Gigantac-

attached male collected by the Alpha Helix in the tinidae. Nat. Hist. Mus. Los Ang. Cty Contrib. Sci.

Banda Sea. The specimen was referred to as Bertelsen, E., and R J. Struhsaker.

Linophryne sp. B by Hansen and Herring (1977). ^^J!' ^" ceratioid fishes of the genus ThaumaUchthys.

° Osteology, relationships, distribution and biol-

ogy Galathea Rep. 14:7-40.
Linophryne sp. male BRADBURY, M. G.

1967. The genera of batfishes (family Ogcocephalidae).
Materia/.— LACM 36088-5, a male, 15 mm SL, stn ^«P^^^ 1967:399-422.

ig/^ BRAUER, A.

,^ . . 1902. Diagnosen von neuen Tiefseefischen, welche von der

This single male specimen could not be iden- Valdivia-Expedition gesammelt sind. Zool. Anz.

tified to species. 25:277-298.

397

FISHERY BULLETIN: VOL. 78, NO. 2

CLARKE, M.R.

1969. A new midwater trawl for sampling discrete depth
horizons. J. Mar. Biol. Assoc. U.K. 49:945-960.
COLLETT, R.

1886. On a new pediculate fish from the sea off Madei-
ra. Proc. Zool. See. Lond. 1886:138-143.

Garman.S.

1899. Reports on an exploration off the west coasts of
Mexico, Central and South America, and off the
Galapagos Islands, in charge of Alexander Agassiz, by the
U.S. Fish Commission Steamer "Albatross" during 1891,
Lieut.-Commander Z. L. Tanner, U.S.N., commanding.
XXVI. The fishes. Mem. Mus. Comp. Zool. Harv. Coll. 24,
431 p.

GILL, T N.

1883. Cryptopsaras couesi. Forest and Stream. Nov. 8,
1883, p. 284.

GooDE, G. B., AND T. H. Bean.

1896. Oceanic ichthyology, a treatise on the deep-sea and
pelagic fishes of the world, based chiefly upon the collec-
tions made by the stetimers Blake, Albatross, and Fish
Hawk in the northwestern Atlantic. U.S. Natl. Mus.
Spec. Bull. 2, 553 p.
GROBECKER, D. B.

1978. A new species of anglerfish. Genus Oneirodes
(Oneirodidae), from the Banda Sea. Copeia 1978:567-
568.
G ij NTHER, A.

1864. On a new genus of pediculate fish from the sea of
Madeira. Proc. Zool. Soc. Lond. 1864:301-303.

1887. Report on the deep-sea fishes collected by H.M.S.
Challenger during the years 1873-1876. Rep. Sci. Res.
Voy H.M.S. Challenger, Zool. 22:1-335.

Hansen, K., and R j. Herring.

1977. Dual bioluminescent systems in the anglerfish
genus Linophryne (Pisces: Ceratioidea). J. Zool. (Lond.)
182:103-124.

Hopkins, t l., r. c. baird, and d. m. milliken.

1973. A messenger-operated closing trawl. Limnol.

Oceanogr. 18:488-490.
KROYER, H.

1845. Ichthyologiske bidrag 10. Ceratias holboel-

li. Naturhist. Tidsskr. l(2):639-649.

Lloyd, R. E.

1909. A description of the deep-sea fish caught by the R. I.
M. S. Ship "Investigator" since the year 1900, with sup-
posed evidence of mutation in Malthopsis. Mem. Indian
Mus. (Calcutta) 2(3):139-180.
LiJTKEN, C. F.

1871. Oneirodes eschrichtii Ltk. en ny grdnlandsk Tud-
sefisk. Overs. K. Dan. Vidensk. Selsk. Forh. 1871:56-74.

Parr, a. E.

1927. Scientific results of the third Oceanographic Ex-

pedition of the "Pawnee" 1927. Bull. Bingham.
Oceanogr. Collect, Yale Univ. 3(1), 34 p.
PIETSCH, T W.

1972. A review of the monotypic deep-sea anglerfish
Family Centrophrynidae: taxonomy, distribution and os-
teology. Copeia 1972:17-47.

1974a. Osteology and relationships of ceratioid
anglerfishes of the fsunily Oneirodidae, with a review of
the genus Oneirodes Liitken. Nat. Hist. Mus. Los Ang.
Cty., Sci. Bull. 18, 113 p.

1974b. Systematics and distribution of ceratioid
anglerfishes of the genus Lophodolos (family
Oneirodidae). Breviora 425:1-19.

1975. Systematics and distribution of ceratioid
anglerfishes of the genus Chaenophryne (family
Oneirodidae). Bull. Mus. Comp. Zool. 147:75-99.

1978. A new genus and species of ceratioid anglerfish from
the North Pacific Ocean with a review of the allied genera
Ctenochirichthys, Chirophryne and Leptacanthichthys.
Nat. Hist. Mus. Los. Ang. Cty, Contrib. Sci. 297, 25 p.

1979. Systematics and distribution of ceratioid
anglerfishes of the family Caulophrynidae with the de-
scription of a new genus and species from the Banda
Sea. Nat. Hist. Mus. Los Ang. Cty, Contrib. Sci. 310:1-
25.

PlETSCH, T. W., AND J. R VAN DUZER.

1980. Systematics and distribution of ceratioid
anglerfishes of the family Melanocetidae wdth the de-
scription of a new species from the eastern North Pacific
Ocean. Fish. Bull., U.S. 78:59-87.

PlETSCHMANN, V.

1926. Ein neuer Tiefseefisch aus der Ordnung der
Pediculati. Anz. Akad. Wiss. Wien 63:88-89.
REGAN, C.T

1925. New ceratioid fishes from the N. Atlantic, the Carib-
bean Sea, and the gulf of Panama, collected by the
'T)ana." Ann. Mag. Nat. Hist, Ser. 8, 8:561-567.

Regan, C. T, and E. Trewavas.

1932. Deep-sea angler-fish (Ceratioidea). Dana Rep.,
Carlsberg Found. 2, 113 p.
REINHARDT, J.

1837. Ichthyologiske bidrag til den grdnlandske fau-
na. Dan. Vidensk. Selsk. Afh. 4(7):83-196.
SEIGEL, J. A., AND T W PIETSCH.

1978. A new species of the ceratioid anglerfish genus
Oneirodes (Pisces: Lophiiformes) from the Indo-West
Pacific. Copeia 1978:11-13.

Smith, H. M., and L. Radcliffe.

1912. Description of a new family of pediculate fishes from
Celebes. Proc. U.S. Natl. Mus. 42:579-581.
UWATE, K. R.

1979. Revision of the anglerfish Diceratiidae with de-
scriptions of two new species. Copeia 1979:129-144.

398

PIETSCH and SEIGEL: CERATIOID ANGLERFISHES OF THE PHILIPPINE ARCHIPELAGO

Appendix Table l. — Alpha Helix stations that yielded Ceratioidei during the Southeast Asian Bioluminescence

Expedition of 1975. Coordinates are for starting position only.

Station

Sea

Latitude

Longitude

Gear depth(m)

Time (h)

Date

18

Timor

8°49.8' S

129=43.0' E

0-550

0900-1400

20 March

23

Banda

4°39.2' S

129=54.1 E

0-2.000

2225-0530

26 March

24

Banda

4=39.1 S

129=53 7' E

0-2.000

0115-0745

28 March

25

Banda

4M6.8S

129=34.4' E

0-1.800

2010-0340

28 March

26

Ceram

2°46.0- S

127=53.7' E

0-1.500

0150-0800

31 March

27

Ceram

2=45.3- S

127=55.1' E

0-2.000

0150-0800

1 April

28

Ceram

3=14.8' S

127=38.0' E

0-100

2035-2205

1 April

36

Banda

4=54.0' S

129=30.5' E

830-1,050

1440-1620

11 April

37

Banda

4=56.3' S

129=25.5' E

0-2,000

1900-0155

11 April

38

Banda

4=40 4' S

129=39.0' E

0-780

0320-0530

12 April

39

Banda

4=45.6' S

129=51.2' E

0-1.000

0950-1435

13 April

51

Banda

4=56.2' S

129=50.0' E

550-815

1545-1655

14 April

58

Banda

4=54.5' S

129=48.4' E

650-810

1200-1400

16 April

59

Banda

4=57.3' S

129=44.0' E

1,100-1,300

1555-1755

16 April

66

Banda

4=54.0' S

129=47.5' E

1 ,500-2,000

1515-1815

17 April

71

Banda

4=55.5' S

129=39.0' E

1,500-2,000

1048-1523

19 April

72

Banda

4=48.5' S

129=58.0' E

0-600

1645-1905

19 April

74

Banda

5=04.0' S

129=54.5' E

720-990

0041-0241

19 April

79

Banda

4=57.5' S

129=51.0' E

0-710

1845-2200

27 April

80

Banda

4=48.7' S

129=47.2' E

0-710

2314-0220

28 April

81

Banda

4°56.5' S

129=59.5' E

1,000-1,500

0416-0616

28 April

82

Banda

5=02.8' S

130=07.0' E

0-690

0745-1050

28 April

84

Banda

5=04.5' S

130=12.0' E

0-1,500

1400-2100

28 April

85

Banda

4=57.5' S

130=11.7' E

0-750

2115-0025

28 April

87

Banda

4=52.0' S

129=50.0' E

0-870

0915-1215

1 May

88

Banda

4=58.0' S

129=43.0' E

1,000-1,500

1450-1650

1 May

89

Banda

5=03.5' S

129=41.0' E

0-960

1820-2112

1 May

91

Banda

4=55.0' S

130=00.0' E

0-600

1030-1250

5 May

93

Banda

5=02.3' S

130=19,5' E

0-760

1650-2013

5 May

94

Banda

5=01.5' S

130=04.6' E

650-1,000

2245-0045

5 May

96

Banda

5=00.0' S

129=54.0' E

0-300

0520-0615

6 May

97

Banda

4=54.0' S

129=42.7' E

0-850

0700-1025

6 May

99

Banda

5=03.0' S

129=52.0' E

0-460

2020-2242

6 May

102

Banda

4=45.0' S

129=19-7' E

0-2,000

0540-1045

7 May

103

Banda

4=49.0' S

129=31.0 E

550-940

1415-1630

7 May

109

Banda

4=33.0' S

129=17.0' E

0-1,100

0030-0445

12 May

110

Banda

4=47.4' S

129=51.8' E

0-1,500

0945-1235

13 May

112

Banda

4=58.0' S

129=59.5' E

650-850

1745-1855

13 May

113

Banda

5=07.5' S

130=08.4' E

650-1,000

2120-2255

13 May

120

tHalmahiera

0=32.0' S

129=08.3' E

450-1,100

1125-1325

16 May

121

Halmahera

0=41 .7' S

128=55.7' E

1,000-1,400

1730-1930

16 May

122

Halmafiera

0=36.3' S

129=03.2' E

575-600

2240-2340

16 May

123

Halmahera

0=29.7' S

129=02.7' E

1,000-1,050

0205-0410

17 May

126

Halmahera

0°22.1' S

129=01.3' E

450-600

1042-1142

17 May

127a

Halmahera

0=04.5' S

128=26.5' E

0-750

1820-2155

17 May

130

Halmahera

0=06.0' S

128=28.7' E

600-790

0724-0933

18 May

133

Halmahera

0=05.7' N

128=24.8' E

0-680

1520-1833

18 May

135

Halmahera

0=06.2' S

128=38.3' E

820-1,000

2306-0106

18 May

136

Halmahera

0=17.4' S

128 47.5' E

1,000-1,250

0446-0646

19 May

137

Halmahera

0=08.9' S

128=40.0' E

0-960

0955-1300

19 May

138

Halmahera

0=05.1 'N

128=29.0' E

750-900

2150-2250

19 May

140

Halmahera

0=00.6' S

128=46.3' E

250-320

0202-0310

20 May

141

Halmahera

0=05.0' S

128=52.7' E

1,000-1,100

0625-0855

20 May

142

Halmahera

0=10.5' S

128=33.3' E

750-1,000

1200-1400

20 May

143

Halmahera

0=14.5' S

128=46.7' E

1,250-1,500

1715-1930

20 May

146

Halmahera

0=36.2' S

129=12.0' E

420-600

0437-0537

21 May

147

Halmahera

0=40.0' S

128=58.5' E

0-1,200

0635-0935

21 May

149

Halmahera

0=22.5' S

128=57.8' E

420-600

1640-1740

21 May

150

Halmahera

0=18.5' S

129=00.8' E

700-1,000

2003-2203

21 May

152

Halmahera

0=13.0' S

129^06.5' E

180-300

0145-0345

22 May

155

Halmahera

0=38,6' S

129=05,6' E

680-850

1210-1400

22 May

157

Banda

4=09.6' S

130=50,0' E

0-840

0215-0615

24 May

162

Celebes

2=37.6' N

124=46,5' E

550-800

0917-1117

1 June

166

Sulu

7=10.7' N

121=25,6' E

660-800

0712-0900

3 June

167

Sulu

7=19.2' N

121=20.1' E

950-1,100

1210-1410

3 June

173

Sulu

8=06.3' N

121=13.2' E

730-810

0645-0845

4 June

175

Sulu

8=28.3' N

121 = 15.0' E

920-1,100

1422-1622

4 June

178

Sulu

8=47 O'N

121=26.0' E

790-910

0200-0330

5 June

179

Sulu

8=58.5' N

121=42.2 E

1 ,500-2,000

0605-1005

5 June

180

Sulu

9=06.0' N

121=51.0' E

710-790

1340-1550

5 June

181

Sulu

9=16.8' N

122=02.2' E

820-950

1905-2105

5 June

183

Sulu

9=24.5' N

122=12.3' E

690-890

0115-0215

6 June

184

Sulu

9=18.0' N

122=10.0' E

480-550

0355-0455

6 June

186

Sulu

9=03.7' N

122=03.6' E

360-640

0936-1036

6 June

187

Sulu

8=53.0' N

122=01,5' E

830-900

1255-1455

6 June

192

Sulu

9=08.0' N

122=02.5' E

800-900

0500-0700

7 June

193

Sulu

9=21.5' N

122=14,7' E

800-1,100

1020-1240

7 June

194

Sulu

9=28.3 N

122=06.8' E

0-1,500

1350-1740

7 June

399

EGGS AND LARVAE OF BUTTER SOLE, ISOPSETTA ISOLEPIS
(PLEURONECTIDAE), OFF OREGON AND WASHINGTON

Sally L. Richardson/ Jean R. Dunn,^ and Nancy Anne Naplin^

ABSTRACT

Development of butter sole, Isopsetta isolepis, is described from egg through benthic juvenile, based on
reared and field-collected specimens.

Isopsetta isolepis eggs are planktonic, spherical, and transparent w^ith a narrow perivitelline space,
homogeneous yolk, and no oil globule. Diameters of 80 reared eggs averaged 0.93 mm (range 0.90-0.99
mm). Using light microscopy, early and middle stage eggs are indistinguishable from those of three
other pleuronectids, English sole, Parophrys vetulus, sand sole, Psettichthys melanostictus , and starry
flounder, Platichthys stellatus, with which they cooccur. Pigment patterns distinguish late stage /.
isolepis eggs from those o{ Psettichthys melanostictus and Platichthys stellatus. Because the late stages
of/, isolepis embryos vary widely in degree and character of pigmentation, they often cannot be reliably
separated from those of Parophrys vetulus.

Larvae are readily distinguished by three bands of melanistic pigment on the tail region of the body
combined with myomere counts (39-42). Transformation from larva to juvenile takes place at about
18-23 mm. Larvae are abundant in nearshore coastal waters off Oregon and Washington in winter and
spring, where they cooccur with larvae of P. vetulus. Recently transformed benthic juveniles of/.
isolepis usually are found offshore rather than in the bay and nearshore habitats occupied by young
juvenile P. vetulus.

This paper presents the first complete description
of development of the butter sole, Isopsetta isolepis
(Lockington), from egg through benthic juvenile.
Larvae of this species are common in the ichthyo-
plankton off Oregon and Washington where they
ranked fifth in overall abundance in April and
May 1967 (Waldron 1972) and third in a coastal
assemblage of larval fishes off Oregon in 1971-72
(Richardson and Pearcy 1977; Richardson'*).

Isopsetta, a monotypic genus of the family
Pleuronectidae, ranges from Ventura, Calif., to
the Bering Sea (Miller and Lea 1972). It is usually
found in coastal waters although it has been re-
ported from the 274-366 m depth zone in western
Alaska (Demory 1971; Miller and Lea 1972; Hart
1973). Adult butter sole ranked 11th and 7th in

'School of Oceanography, Oregon State University, Corvallis,
Greg.; present address: Gulf Coast Research Laboratory, Ocean
Springs, MS 39564.

^Northwest and Alaska Fisheries Center, National Marine
Fisheries Service, NOAA, 2725 Montlake Boulevard East, Seat-
tle, WA 98112.

^Northeast Fisheries Center Sandy Hook Laboratory, Na-
tional Marine Fisheries Service, NOAA, Highlands, NJ 07732.

■•Richardson, S. L. 1977. Larval fishes in ocean waters off
Yaquina Bay, Oregon: abundance, distribution, and seasonal-
ity, January 1971 to August 1972. Oreg. State Univ., Sea
Grant Coll. Prog., Publ. ORESU-T-77-003, 73 p.

biomass of all flatfishes taken during trawl sur-
veys off Oregon in 1971-72 and 1973-74 (Demory
et al.^) and 6th in biomass of all flatfishes off
Washington in both 1975 and 1976 (Barss et al.^).
Because it is a relatively small, <55 cm TL (total
length), slender fish (Miller and Lea 1972; Hart
1973), it is currently of only minor commercial
importance.

Levings ( 1968) briefly described I. isolepis eggs
as single, nonadhesive, transparent, spherical,
without an oil globule, with a mean egg diameter
of 1.013 mm, although he did not illustrate them.
The eggs sank at salinities ss26.61%o but floated at
salinities &28.03%o. Levings concluded that the
eggs were demersal within Skidegate Inlet,
British Columbia, where bottom salinities were
24.96%o. Isopsetta isolepis larvae 4.8, 7.9, 10.0, and
15.5 mm long from Puget Sound were sketched by
Blackburn (1973) but were labeled Lyopsetta
exilis. He also provided short descriptions.

Manuscript accepted December 1979.
FISHERY BULLETIN: VOL. 78, NO 2, 1980.

^Demory, R. L., M. J. Hosie, N. TenEyck, B. O.
Forsberg. 1976. Marine resource surveys on the continental
shelf off Oregon, 1971-74. Oreg. Dep. Fish Wildl., Completion
Rep., June 1976, 49 p.

«Barss, W. H., R. L. Demoiy, N. TenEyck. 1977. Marine
resource surveys on the continental shelf and upper slope off
Washington, 1975-76. Oreg. Dep. Fish Wildl., Completion
Rep., September 1977, 34 p.

401

METHODS

Eggs from ripe fish collected in Bellingham Bay,
Wash., were artificially fertilized on 12 March
1974 and were reared at the Mukilteo field station
of the Northwest and Alaska Fisheries Center
(NWAFC), National Marine Fisheries Service
(NMFS), NOAA, Seattle, Wash. The eggs were
incubated in 0.6 or 1.0 1 glass beakers containing
local Puget Sound seawater maintained at 9°-10°
C. Subsamples of eggs were preserved in Forma-
lin^ in eight time periods, 4, 9, 20, 24, 48, 72, 96,
and 120 h, after fertilization. Subsamples of larvae
were preserved for each of 13 time periods: at
hatching (144 h or 6 d after fertilization) and at
2, 3, 4, 7, 9, 11, 14, 16, 18, 21, 23, and 25 d
after hatching. Although rotifers [Brachionus
plicatilus) were added to the containers at various
levels (4, 8, and 16 rotifers/ml seawater), the lar-
vae did not feed actively and all were dead by 22
April 1974.

Approximately 300 larvae were obtained from
NWAFC collections made off coastal Washington
in 1972. An additional 107 larvae were obtained
from Oregon State University (OSU) ichthyo-
plankton collections taken off the Oregon coast
from 1971 to 1972 (Richardson and Pearcy 1977;
Richardson see footnote 4). Benthic juveniles were
collected in beam trawls off the mouth of the
Columbia River in June and September 1975
(Richardson et al.^).

Counts of meristic structures were made on 209
larvae (3.2-23.6 mm) and 7 juveniles (44-160 mm)
taken from the OSU and NWAFC collections.
Larvae were stained with Alizarin Red S using
Taylor's (1967) enzyme method to determine
sequence of ossification. Some (45) were sub-
sequently restained with Alcian Blue and Alizarin
Red using techniques described by Dingerkus and
Uhler ( 1977). Counts were made of dorsal fin rays,
anal fin rays, caudal fin rays, left and right pec-
toral fin rays, branchiostegal rays, gill rakers, ver-
tebral centra, neural spines, and haemal spines.
Fin rays and vertebrae were counted even if they
were tinted only slightly with alizarin stain. Up-
take and retention of alizarin in ossified structures
may vary depending upon the length of time the

''lieference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

sRichardson, M. D., A. G. Carey, Jr., W. A. Col-
gate. 1977. The effects of dredged material disposal on
benthic assemblages off the mouth of the Columbia River. Fi-
nal Rep., Dep. Army Corps Eng. Contracts DACW 57-75-C-0137
and DACW 57-56-C-0092, Vicksburg, Miss., 411 p.

FISHERY BULLETIN: VOL. 78, NO. 2

specimens have been in preservative. Differential
loss of stain may account for some of the variation
observed in the onset of ossification of certain
structures such as teeth.

Measurements were made using an ocular mi-
crometer in a stereomicroscope. The greatest out-
side diameter and greatest yolk diameter were
recorded for 80 eggs from the reared series, 10 for
each of the eight time periods that eggs were pre-
served from 4 to 120 h after fertilization. Mea-
surements were made on 63 reared larvae, 5
specimens (when available) from each of the 13
time periods after hatching (6 d after fertilization)
that larvae were preserved to 25 d after hatching.
Size range of reared specimens was 2.7-5.3 mm SL
(standard length). Measurements also were made
on 107 larvae from plankton collections including
5 specimens (when available) for each 1.0 mm size
class interval from 2 to 23 mm SL (range 2.9-23.6
mm). Body measurements were made on larvae as
follows:

Standard length - snout tip to notochord tip
until notochord is fully flexed and the poste-
rior margin of the forming hypural elements
is vertical, then to posterior margin of hypur-
als.

Head length - snout tip to cleithrum.

Body depth at pectoral fin base - vertical dis-
tance from dorsal body margin to ventral body
margin, excluding finfold or fins, at the pec-
toral fin base.

Body depth at anus - vertical distance from
dorsal body margin, excluding finfold or fin, to
anus.

Body depth behind anus - vertical distance from
dorsal body margin to ventral body margin,
excluding finfolds or fins, at point im-
mediately behind anus where body depth de-
creases greatly compared to depth at anus.

Body depth at caudal peduncle - before forma-
tion of caudal fin, vertical distance from dor-
sal body margin to ventral body margin,
excluding finfolds or fins, at the posteriormost
myomere; after caudal fin formation, least
depth of caudal peduncle.

Snout length - snout tip to anterior margin of
right eye.

Eye diameter - horizontal distance across right
eyeball.

Snout to anus length - distance along body mid-
line from snout tip to vertical through posteri-
or margin of anus.

402

RICHARDSON ET AL.: EGGS AND LARVAE OF BUTTER SOLE

Upper jaw length - snout tip to posterior margin
of maxillary.

Illustrations of eggs and larvae were made with
the aid of a camera lucida. All specimens had been
preserved in 59c Formalin. Illustrations of the
caudal fin and skeletal structure were made from
cleared and stained specimens.

VERIFICATION OF
IDENTIFICATION

Reared eggs were fertilized from known par-
ents, thus their identity was certain.

A series of larval specimens from plankton col-
lections was linked together by pigment pattern.
The left eye had begun to migrate in the largest
specimens indicating that they were pleuronec-
tids, the only right-eyed flatfishes occurring off
Oregon and Washington. Positive identification
was based on knowledge of early stages of all but
one of the pleuronectids occurring in the area (Ta-
ble 1) and on the following meristic characters for
/. isolepis (Hart 1973; Ahlstrom^; this study):

Table l. — Pleuronectid flatfishes occurring off Oregon and
Washington with references on early developmental stages.

Species

References

Dorsal fin rays
Anal fin rays
Abdominal vertebrae
Total vertebrae
Caudal fin rays
Pectoral fin rays
Pelvic fin rays
Branchiostegal rays
Gill rakers

78-92

58-69

9-11, usually 10

39-42

17-18, usually 18

11-13

6

7

4-6 + 7-8

Additional confirmation was provided by larvae
reared to yolk depletion, which were similar to the
smallest specimens from the plankton samples.

DISTINGUISHING FEATURES

Early and middle stage eggs of/, isolepis are in-
distinguishable from those of English sole, Paro-
phrys vetulus; starry flounder, Platichthys stella-
tus; and sand sole, Psettichthys melanostictus .
Chorions of reared eggs are often noticeably stri-
ated, but this characteristic is not consistent
among reared eggs and is rarely seen in eggs from
the plankton. Thus, chorion sculpturing is not use-
ful for identifying /. isolepis eggs.

Atheresthes stomias
Embassichthys bathybius
Eopsetta lordani

Glyptocephalus zachirus
Hippoglossoides elassodon

HIppoglossus stenolepis

Inopsetta ischyra
Isopsetta isolepis
Lepidopsetta bilineata

Lyposetta exilis
Microstomus pacificus
Parophrys vetulus

Platichthys stellatus

Pleuronichthys coenosus

Pleuronichthys decurrens

Psettichthys melanostictus

Perlseva-Ostroumova (1960. 1961)

Richardson (in press)

Alderdice and Forrester (1971); Ahlstrom (un-
publ. data); Richardson (in press)

Ahlstrom and Moser ( 1 975)

Dekhnik ( 1 959) ; Pertseva-Ostroumova ( 1 961 ) ;
Miller ( 1 969) ; Alderdice and Forrester ( 1 974)
Forrester and Alderdice'

Thompson and Van Cleve (1936): Pertseva-
Ostroumova (1961)

None

Levings ( 1 968) : Blackburn ( 1 973)

Pertseva-Ostroumova (1961); Blackburn
(1973); Richardson (in press)

Blackburn ( 1 973) ; Ahlstrom and Moser ( 1 975)

Hagerman ( 1 952) ; Ahlstrom and Moser ( 1 975)

Budd (1940)2; Orsi (1968); Blackburn (1973);
Ahlstrom and Moser (1975); Misitano (1976)

Orcutt (1950); Yusa (1957); Pertseva-Ostrou-
mova ( 1 961 ) as Pleuronectes stellatus

Budd (1 940) (as P. decurrens); Sumida et al.
(1979)

Budd (1940) (as P coenosus): Sumida et al.
(1979)

H ickman ( 1 959) ; Sommani ( 1 969)

^E. H. Ahlstrom, Senior Scientist, Southwest Fisheries
Center, National Marine Fisheries Service, NOAA, P.O. Box

271, La Jolla, CA 92038, unpubl. data.

'Forrester, C. R., and D. F. Alderdice. 1968. Preliminary observations
on the embryonic development of the flathead sole {Hippoglossoides elasso-
don)^ Fish. Res. Board Can., Tech. Rep. 100, 20 p.

^The 6-3 mm larva is not P. vetulus .

Late stage eggs are readily distinguished from
other northeast Pacific pleuronectids with similar
size eggs by means of pigment. Embryos in late
stage P. melanostictus eggs have scattered yolk-sac
melanophores, and those of Platichthys stellatus
have pigmented finfolds, while /. isolepis embryos
lack pigment in both places. Isopsetta isolepis em-
bryos are most similar to those of Parophrys vet-
ulus. While /. isolepis embryos usually have sev-
eral isolated ventral tail melanophores, their
number is quite variable, ranging from none to
many, whereas P. vetulus embryos have so many
ventral tail melanophores that the pigment ap-
pears almost continuous. The head and anterior
trunk pigment of/, isolepis is more dendritic and
melanophores are less numerous than on P. vet-
ulus. Despite these differences, variation in both
ventral tail and trunk melanophores, especially in
/. isolepis, is so great that late stage eggs of the two
species cannot always be reliably separated.

Most sizes of/, isolepis larvae can be easily dis-
tinguished from other flatfish larvae off Oregon
and Washington by their body form together with
their striking pigment pattern, most notably the
three bands of melanophores on the body posterior
to the abdominal cavity. After notochord flexion
the posteriormost band lines the base of the caudal
fin, but the two other bands remain apparent
through transformation to benthic juvenile. No

403

FISHERY BULLETIN: VOL. 78, NO. 2

other flatfiish larvae of similar form in the area
have three such bands. The only other three-
banded flatfish larva is deepsea sole, Emhas-
sichthys bathybius, but it hatches at about 9 mm,
has over 60 myomeres, and a different elongate
form (Richardson in press). The most similar ap-
pearing banded larval flatfish is the flathead sole,
Hippoglossoides elassodon, which has four pig-
ment bands.

Before the three pigment bands become obvious,
i.e., in larvae <4 mm SL, larvae of/, isolepis are
similar to those of P. vetulus. They usually are
separable by the size and distribution of postanal
ventral midline melanophores. Those of/, isolepis
are small and appear more or less as a double row
when viewed from the ventral surface; those of P.
vetulus are enlarged and stellate and appear as a
single row when viewed ventrally.

Newly transformed /. isolepis juveniles are also
similar to P. vetulus. Before development of adult
characters such as scales on the fins of/, isolepis,
which will easily separate the two, /. isolepis can
usually be distinguished by remnants of the larval
pigment bands on the blind side. The number of
gill rakers on the lower limb (Miller and Lea 1972)
also will separate the two species (7-8 for/, isolepis
and 10-13 for P. vetulus).

DEVELOPMENT OF EGGS

(Figure 1)

Isopsetta isolepis eggs are spherical and trans-
parent, with a narrow perivitelline space, a
homogeneous yolk, and no oil globule. Although
the eggs apparently sink at salinities s;26.61%o
(Levings 1968), they are taken in our plankton
samples, and live eggs floated in the rearing exper-
iments (salinity ~26.9%o). Diameters of 80 reared
eggs averaged 0.93 mm (0.90-0.99 mm), while yolk
diameters averaged 0.76 mm (0.60-0.95 mm).

Embryonic development is typical of most tele-
osts with planktonic eggs. The stages of egg de-
velopment we use correspond to the basic divisions
of embryonic development used by Ahlstrom and
Counts (1955), with detailed subdivisions of each
stage (Naplin and Obenchain in press).

Pigmentation

Pigment first appears during the middle stage of
embryonic development. At this time, distinct
melanophores are scattered unevenly from the
middle of the eyes posteriorly over the trunk. The

Figure l. — isopsetta isolepis eggs, late stage from plankton

collections.

melanophores become more organized into two
dorsolateral lines on the anterior somites, and di-
minish in size and frequency posteriorly. The dor-
solateral lines are the site of melanophore forma-
tion, and pigment is present farther posteriorly as
development continues.

The development of this species is unusual in
that the anteriormost melanophores become in-
creasingly dendritic and so fine that they gradu-
ally become less visible. By the time the embryos
have reached the late stage (tail five-eighths of the
way around the yolk), less head pigment is visible
and the trunk is covered with very small but dis-
tinctly visible dendritic melanophores. Several
distinct ventral melanophores lie at the juncture
of the trunk and the yolk sac, and one or two
isolated spots are on the yolk sac nearby. Most of
the tail pigment is scattered dorsally in no obvious
pattern, and several lateral melanophores are now
in the ventral tail area.

When the tail is three-fourths of the way around
the yolk, the head and trunk generally appear to
be pigmented, although less distinctly than in the
middle stage. Ventral trunk pigment is present,
and some embryos may have one to three yolk-sac
melanophores nearby. Scattered melanophores
appear dorsally on the posterior trunk and on all
surfaces of the tail. More lateral melanophores are
present toward the tail tip.

From the time the tail is seven-eighths of the way
around the yolk through hatching, little change in
the pigment pattern occurs; however, the lateral
tail melanophores have moved to become ventral.
Dorsal and ventral tail pigment melanophores are

404

RICHARDSON ET AL.: EGGS AND LARVAE OF BUTTER SOLE

spread into thin lines between the margin of the
body and finfold. The ventral melanophores are
variable, ranging from no melanophores to many,
and are separated at irregular intervals over the
length of the tail, while the dorsal pigment can
appear almost continuous. Near the tail tip the
dorsal and ventral melanophores align, as in the
early larvae, to form the precursor of the pos-
teriormost band of pigment noted in the larvae.

The reared embryos appear more lightly pig-
mented than wild-caught embryos. In the latter, it
is possible that the marked fading of the head
pigment may not occur until after hatching.

Morphology

Physical development of /. isolepis embryos
progresses as in other fishes. At the time of initial
pigment formation, the blastopore has closed and
the embryonic body is gradually thickening on top
of the yolk sac. During this stage, the eyecups are
forming, but no lens tissue is discernible. About
12 somites have formed, and Kupffer's vesicle is
still visible just anterior to the tail bud.

When the tail is five-eighths of the way around
the yolk, the eyecups are well-formed and lenses
are present. The brain has differentiated into a
forebrain and a larger midbrain. The auditory ves-
icles are forming but are not yet hollow. About 27
somites are present, Kupffer's vesicle is no longer
visible, and the small tail has a definite finfold.

By the time the tail has reached three-fourths of
the way around the yolk, the auditory vesicles are
well-formed and immediately apparent. The em-
bryo now has about 37 somites. Hatching can
occur when the embryo's tail has reached seven-
eighths of the way around the yolk to full circle. At
this point, the embryo has the full complement of
somites or myomeres (39-42) and is morphologi-
cally similar to a newly hatched larva.

DEVELOPMENT OF LARVAE

(Figures 2-5)

Pigmentation

Pigment on newly hatched larvae is scattered
lightly on the head and snout, and appears on the
dorsal, lateral, and ventral body surface above the
abdominal cavity and also in the tail region. No
pattern is obvious. The eyes are unpigmented.

In the head region, the eyes begin to darken by 4
d (about 3.8-4.0 mm) after hatching and are fully

pigmented by 7 d (3.9-4.1 mm) in the reared lar-
vae. Eyes in the smallest plankton specimen (2.9
mm) are pigmented. During early development,
pigment over the head and snout disappears (by
about 4 mm in reared larvae, 2.9 mm in plank-
tonic larvae) except for a few internal melano-
phores above the otic capsule. Pigment appears on
the lower jar and throat region by 4 or 5 mm and
persists through the larval period. By about 6 or 7
mm several melanophores are present at the ven-
tral angle of the preopercle. Later in development,
scattered melanophores are added on the head
(>10 mm) and on the upper jaw ( >14 mm). Addi-
tional pigment is added to the entire head region
on the eyed side during transformation (> 17 mm).

In the abdominal region, melanophores disap-
pear from the dorsal and lateral body surfaces
above the gut cavity by the time larvae are about 4
mm long. Pigment is added again in this region
during the transformation period when larvae are
about 17 mm long. It is added first in two patches
on the dorsal pterygiophores. More melanophores
are then added laterally as well as on the dorsal
pterygiophores, mainly along the myosepta,
obscuring the original patches. A series of internal
melanophores develops dorsal to the notochord
above the abdominal cavity in larvae >10 mm.
Melanophores are added along the ventral margin
of the gut cavity by the time larvae are about 4 mm
long. With development, additional melanophores
extend over the ventral and posterior portions of
the abdominal cavity appearing in a half-moon
shape on most larvae >8 mm long. This pattern
persists until transformation when the increase in
body pigment on the eyed side obscures it.

In the tail region, three characteristic bands of
pigment become obvious in reared larvae 4 d (3.9-
4.1 mm) after hatching and are visible on the 2.9
mm plankton caught larvae. These are located on
the body at positions roughly 50, 67, and 90^^ SL.
In larvae <10 mm, these bands generally extend
from dorsal to ventral body margins. With de-
velopment the middle band becomes the most pro-
nounced of the three. This middle band remains
visible on the eyed side of some newly transformed
benthic juveniles, and remnants of it persist on the
blind side of juveniles as long as 35 mm. After
notochord flexion (>14 mm), the posterior band is
seen as a line of pigment at the base of the caudal
fin. The anterior band becomes less pronounced
and often does not extend above the lateral mid-
line in larvae >14 mm. Along the notochord, a se-
ries of internal melanophores develops dorsal to

405

FISHERY BULLETIN: VOL. 78, NO. 2

2.9nnmSL

— — ■

■ —

_ . I — — -

^

: — ■-■^-

- ^i^n ^

»

^■I^UjlM, JiUU

"~~~

^^__

1/ ^J0-^

4.0 mm SL

4.1 mm SL

Figure 2. — Isopsetta isolepis larvae: 2.9 mm SL (reared, newly hatched, 144 h after fertilization); 4.0
mm SL (reared, 4 d after hatching); 4.1 mm SL (plankton specimen).

it, first in the region of the anterior two pigment
bands in larvae about 6 or 7 mm long. Additional
internal pigment spots then develop along the
notochrod between the three pigment bands and
anterior to them. This line of internal pigment
spots is usually not continuous. It remains visible
until the end of the transformation period. Along
the ventral midline, pigment appears as a charac-
teristic double row (viewed ventrally) of small
melanophores in larvae >4 mm. This double row
remains obvious until the onset of anal fin forma-
tion, about 14 mm, after which these mela-
nophores appear to line the base of the anal fin,
sometimes with one melanophore/fin ray. These
melanophores become indistinct during trans-

406

formation. On the ventrolateral body surface,
melanophores are added just above the ventral
midline row about the time the anal fin begins to
form, around 10 mm. These melanophores even-
tually, by 12 mm, appear in the myosepta in a line
midway between the lateral midline and the ven-
tral margin of the body myomeres. Until the addi-
tion of pigment during transformation this line of
melanophores is visible on the eyed side only, but
is often visible on the blind side of newly trans-
formed benthic juveniles. Along the margin of the
ventral finfold a line of evenly spaced small
melanophores is visible on newly preserved larvae
>4 mm. This is often faded after a long period of
preservation or is missing in plankton collected

RICHARDSON ET AL.: EGGS AND LARVAE OF BUTTER SOLE

6.2 mm SL

9.1 mm SL

13.6 mm SL

Figure 3. — Isopsetta isolepis larvae: 6.2 mm SL, 9.1 mm SL, and 13.6 mm SL.

specimens due to damaged finfolds. It is not visible
on most specimens examined in this study, includ-
ing the series illustrated. This line of mela-
nophores has been seen on a few specimens up
to 7.3 mm long. Additional pigment develops on
the ventral finfold in the vicinity of the three pig-
ment bands in larvae >4 mm and on the dorsal
finfold near the posteriormost pigment band by
the time larvae are 8 mm. This finfold pigment
persists until caudal and anal fin formation. After
the dorsal and anal fins are formed, by the time

larvae are >15 mm, their margins are fringed
with melanophores. However, the fin margins are
often damaged on preserved planktonic specimens
and the pigment fringing is not visible.

With transformation, at >17 mm, pigment is
added to the eyed side in the tail region. Four or
five clusters of melanophores appear along the
dorsal pterygiophores and four along the ventral
pterygiophores. These clusters eventually become
obscured as more pigment is added. Increases in
the number of melanophores along the bases of the

407

FISHERY BULLETIN: VOL. 78, NO. 2

17.1 mm SL

22.1 mm SL

Figure 4. — Isopsetta isolepis larvae: 17.1 mm SL and 22.1 mm SL.

dorsal and anal pterygiophores give the appear-
ance of solid lines of pigment. More melanophores
appear on the body until all larval pigment is
obscured. Additional pigment develops on the dor-
sal, anal, and caudal fins along the fin rays.

Morphology

Newly hatched reared larvae, 144 h after fertili-
zation, range in length from 2.68 to 2.92 mm (X =
2.78 mm, based on 50 specimens). The yolk sac
extends along the anterior third of the body. The

mouth is not yet formed. A moderate finfold ex-
tends from the head around the posterior part of
the body to the anus. The otic capsule is visible on
the head behind the unpigmented eye. The mouth
is formed by 2 d (3.4-3.5 mm) after hatching. The
yolk is nearly gone by 4 d (3.8-4.0 mm) and is no
longer visible by 7 d (3.9-4.1 mm). By 11 d (3.3-4.1
mm) the previously straight gut begins to coil. The
smallest larva identified from plankton collections
is 2.9 mm. It has a formed mouth, no remnant of
yolk, and its gut has begun to coil. The size discrep-
ancy may be an artifact of preservation, or it may

408

RICHARDSON ET AL.: EGGS AND LARVAE OF BUTTER SOLE

21.1 mm SL

Figure 5. — Recently transformed benthic juvenile /sopserta isolepis, 21.1 mm SL.

be due to the different environmental conditions of
the reared and planktonic larvae. With develop-
ment the gut continues to coil and the hindgut,
which is initially directed posteriorly, comes to
rest in an anteriorly directed position, by about 17
mm.

Notochord flexion begins by the time larvae are
about 9 or 10 mm long and the notochord is fully
flexed by about 14 mm. After flexion is complete,
the tip of the urostyle continues to extend beyond
the hypural plate, sometimes until larvae are 17
mm long. When larvae are about 12 or 13 mm long,
near the end of notochord flexion, the left eye be-
gins to migrate to the right side of the head. The
left eye is visible on the ridge of the head, when
viewed from the right side, in some larvae as small
as 15 mm and consistently in specimens >17 mm.
The left eye eventually migrates to the degree that
it is directed upward, the most advanced position
before complete transformation to benthic juve-
nile. This was the most advanced stage of eye mi-
gration of specimens taken in plankton tows and
was observed in some, but not all, specimens >20
mm. The largest specimen collected in the plank-
ton was 23.6 mm, but the most developed plankton
specimen in terms of eye migration and increased
pigmentation was 21.9 mm. The smallest speci-
men collected in a beam trawl was 18.0 mm, but its
eye was on the dorsal ridge of the head directed
upward and it had not completed transformation.

The smallest benthic juvenile, in which the left
eye had crossed over the middorsal ridge and
juvenile pigment had intensified on the eyed side,
was 18.5 mm.

With development (Tables 2, 3), relative head
length increases considerably from mean values of
13-15% SL in preflexion larvae to 25% SL in post-
flexion larvae. Snout to anus length remains es-
sentially constant with respect to standard length
with mean values of 29-32% . Relative body depths
at the pectoral fin base, at the anus, and behind the
anus increase dramatically through the larval
period with mean values nearly doubling in most
cases between preflexion and flexion stages and
doubling again between flexion and postflexion
stages. The greatest rate of increase occurs in the
depth behind the anus. Depth of the caudal pedun-
cle also increases from 3 to 10% relative to stan-
dard length. Relative eye diameter is largest in
preflexion larvae (29-36% HL (head length)) and
decreases in flexion (24% HL) and postflexion (22%
HL) larvae as does the relative length of the upper
jaw (37-25% HL).

Ossification of Meristic Structures

Descriptions, based on cleared and stained
specimens, depict only general trends of develop-
ment because the size at which bones begin to
ossify may vary among specimens and the uptake

409

Table 2.

FISHERY BULLETIN: VOL. 78, NO. 2

-Measurements (millimeters) of plankton caught larvae oflsopsetta isolepis. (Specimens between dashed lines are under-
going notochord flexion.)

Length

Sample

Mean

Snout

Upper

Body depth

Depth

Depth

Caudal

interval

size

length

to

Head

Snout

jaw

Eye

at pectoral

at

behind

peduncle

(mm)

(A/)

(mm)

anus

length

length

length

diameter

fin base

anus

anus

depth

2.9-3.0

2

2.90

0.95

0.45

0.20

0.30

0.20

0,15

0.10

3.1-4.0

'6

3.67

1.07

050

0.10

—

0.20

0.40

030

0.17

0.10

4.1-5.0

24

4.63

1.28

0.55

0.10

—

0.25

0 40

0,35

0.23

0.10

5.1-6.0

35

5.50

1.48

0.68

0.10

0.30

0.28

050

0,46

0.22

0.10

6.1-7.0

"5

6.58

2.04

1.02

0.12

040

0.30

0.72

0,72

0.34

0.12

7.1-8.0

55

7.76

2.20

1.14

0.10

0.43

0.32

1.04

1.00

0.44

0.16

8.1-9.0

6

8.77

2.58

1.32

0.10

0.48

0.38

1.17

1.12

0.50

028

9.1-l6.d

4

2.88

1.48

a20

0.50

0.45

T25

1.23

0.60

0.35

10.1-11.0

6

10.57

3.42

1.95

0.28

0,62

0.48

1.72

1.68

1.25

0.60

11.1-12.0

4

11.25

3.38

1.88

0.20

0.60

0.50

1.78

1.72

1.15

0.55

12.1-13.0

5

12.36

3.70

2.24

0.28

0.76

0.50

2.02

2.14

1.54

0.74

13.1-14.0

5

13.55

4.22

2.74

0.36

0.72

0.62

2,52

3.12

2.08

0.96

14.1-15.o"

5

14.48

4.84

" "3V18

0.50

0.86

0.64

"i'is

3.68

3.00

'""""T34""

15.1-16.0

5

15.38

4.68

3.58

0.54

0.94

0.74

3.74

4,40

3.64

1.48

16.1-17.0

5

16.54

5.64

400

0.60

1.10

0.90

4,64

5.36

4.84

1.68

17.1-18.0

5

17.50

5.88

4.70

0.78

1.12

1.10

560

6,16

6.00

1.86

18.1-19.0

4

18.63

5.85

4.78

0.93

1.28

1.08

643

6.85

6.95

1.88

19.1-20.0

6

19.55

5.92

4.93

0.94

1.20

1.08

6.52

7.00

6.90

2,02

20.1-21 0

6

20.53

5.97

5.12

0.95

1.28

1.10

6.90

7.35

7.50

2.03

21.1-220

4

21.48

6.40

5.93

095

1.60

1.23

768

8.18

8.58

2.23

22.1-23 0

6

22.48

6.27

5.58

0.95

1.22

1.23

7.67

8.33

8.62

2.28

23.1-24.0

4

23.33

6.80

5.68

0.98

1.43

1.25

7.83

8.48

9.03

2.33

W = 2 for snout length.

^N = 3 for snout length.

W = 4 for snout length and 1 for l

ipper jaw length.

*N = 1 for

upper jaw length.

5iV = 4for

upper jaw length.

Table 3. — Body proportions of I sopsetta isolepis larvae. Values given are percentages: mean

in parentheses.

standard deviation, and range

Preflexion larvae

Preflexion larvae

Preflexion larvae

with yolk

without yolk

without yolk

Flexion larvae

Postflexion larvae

Item

(reared)

(reared)

(plankton)

(plankton)

(plankton)

No. measured

20

42

'37

220

50

sl

(2.7-4.0)

(3,4-5,4)

(2,9-9,0)

(10.5-14.2)

(13.5-23.6)

Head length/SL

15.0±2. 7(10.6-19.6)

13.4±0.9(11. 3-15.9)

14.2±2.0(10.2-17.2)

18.3±1.6(15.3-20,7)

24.9±2.1(20.7-29.4)

Snout to anus length/SL

32 4^3.8(28,3-39.3)

28.8± 1.3(26. 7-31.1)

29.2±2. 9(22.9-34, 4)

30.7± 1.8(27. 6-34.0)

31 .0±3. 0(23.2-35.8)

Depth at pectoral fins/SL

5.2±0.8(4.1-6.7)

9.2± 1.0(7.4-1 1.6)

11.4±2.3(8.3-15.2)

16.6±1, 7(12.9-18.5)

31.1+5,0(20.1-38.0)

Depth at anus/SL

9.8 + 1.2(8.2-12.0)

8.9^0.9(6.9-11.1)

10. 3±2. 8(5. 7-15.6)

17.8±3. 7(12.9-28. 9)

34.1^4.4(23.2-40.2)

Depth behind anus/SL

4.3±0.7(2.8-5,9)

3.2±0. 5(2. 5-4.1)

5.1 + 1.3(2.9-7.8)

12.3^2.0(9.0-14.8)

33.4±6. 7(18.8-41.3)

Caudal peduncle depth/SL

—

—

2.6±0.8(1.3-4.1)

6. Oil. 1(4.4-7.4)

9.6 = 2.0(7.6-11.3)

Eye diameter/HL

32.8±2. 6(30.2-38.1)

28.9-3 9(21 6-39.6)

35. 6±9. 1(25.0-50,0)

23.7±2.8( 20.0-29 4)

21.8 = 2 2(17.5-26.2)

Snout length/HL

19.9±6.0(9.4-29.8)

28.1^:4.1(20.8-34,0)

12.5±4.4(6.7-20.0)

13.7±2.8(8. 7-21.0)

16.6 = 3.7(9.4-20.8)

Upper jaw length/HL

—

—

37.1 ±4.9(31.2-50.0)

31.6±5.9(24.0-47.6)

25.2±4.4(17.5-38.5)

'Except W = 29 for snout length and N = 16 for upper jaw length.
^Except N = 19 for snout length.

of stain may be affected by length of preservation.
Terminology of bones generally follows
Richardson and Joseph (1973) and Frame et al.
(1978) except as noted.

Most of the meristic characters of /. isolepis
larvae begin ossifying during notochord flexion
(10-14 mm); only gill rakers and pectoral fin rays
begin to ossify at larger sizes (Table 4; Figure 6).
The following discussion roughly parallels the
sequence of development of meristic characters,
and we note their first appearance as well as the
onset of ossification as indicated by the acceptance
of Alizarin Red stain.

Paired conical teeth may be observed on the
dentary of 5.3 mm larvae, and on the premaxil-

410

laries by 5.8 mm. Teeth continue to increase in
number as the larvae grow. Teeth are consistently
more numerous on the left (ultimately the blind)
side of the head than the right side. The smallest
specimen in which teeth accepted alizarin stain
was 12 mm, possibly an artifact of preservation.
Larval teeth develop in approximately two non-
parallel rows. The outer row consists of conical,
caninelike teeth, and the inner row is composed of
smaller, curved teeth. Most teeth are ossified in 18
mm larvae. By transformation (ca. 20.0 mm), but-
ter sole larvae possess approximately 37 larval
teeth on the left dentary (27 in the outer row; 10
smaller teeth on an inner row) and about 37 large
conical teeth on the left premaxillary arranged in

RICHARDSON ET AL.: EGGS AND LARVAE OF BUTTER SOLE

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two rows. The right dentary contains about 20
teeth (11 large conical teeth in the outer row and 9
smaller teeth in the inner row). The right pre-
maxillary contains nine larger teeth and six small-
er teeth. Teeth continue to increase in number
after transformation. A 44 mm juvenile possessed
about 40 teeth each on the left premaxillary and
left dentary and 14 teeth on the right dentary and
10 teeth on the right premaxillary.

Neural spines ossify during notochord flexion
(Table 4; Figure 6). The first neural spine to ossify
lies just above the first haemal spine in the an-
terior abdominal region, and ossification proceeds
posteriorly and anteriorly. The last two neural
spines to ossify are those on the antepenultimate
and penultimate vertebrae. Ossification is usually
completed at about 16.5 mm. Haemal spines ossify
from anterior to posterior beginning with the first
haemal spine. The last two haemal spines to ossify
are also on the antepenultimate and penultimate
vertebrae.

CHARACTERS

Abdominal ,

Caudal |

Neural Spines ,

Neural Spines '

Pectoral Rays '

1 1 1

Right 1

Pelvic Rays

1 1 1

1 oft 1 1

Ri]ht 1 1

Gill Rakers 1
Upper 1

None ossifiecj

' 1 1

1 . 1 . 1 . 1 . 1 . 1 ,

,1,1.1.1.1.1

10 12 14 16

Standarcj length {in mm)

20

22

24

Figure 6. — Diagrammatic summary of the sequence of os-
sification of principal meristic structures in Isopsetta
isolepis. Dashed vertical lines indicate size range in which
notochord flexion occurs; open bars indicate meristic structure
is undergoing ossification; solid bars indicate meristic structure
is completely ossified.

411

FISHERY BULLETIN: VOL. 78, NO. 2

' In the axial skeleton the first centrum to ossify
(as early as 11 mm) supports the first haemal
spine. Ossification proceeds both anteriorly and
posteriorly, with the urostyle ossifying before the
antepenultimate and penultimate vertebrae. All
centra are ossified by 17 mm.

The first caudal supports to ossify are hypurals^'*
2 and 3 in larvae as small as 12 mm. Hypural 1 is
ossified by 13 mm and hypural 4 at about 15 mm.
The epurals ossify last at about 16 mm. We inter-
pret the caudal complex of/, isolepis to consist of
four hypurals (two below and two above the medial
axis) and two epurals. One is a normal-sized
epural that supports the uppermost caudal ray,
and the other epurallike bone is reduced in size
and supports no rays (Figure 6H). No uroneurals
are present.

Fin rays begin to ossify during notochord flexion
(10-14 mm) in the dorsal, anal, caudal, and pelvic
fins. Ossification is completed in the following or-
der: caudal, dorsal, anal, pelvic, and pectoral fins
(Table 4; Figure 6). Pectoral fin rays were not fully
ossified in the largest stained larva, 22.8 mm.

The anlage of the base of the caudal fin begins to
form by 5.5 mm ( Figure 7 A). Incipient caudal rays
are evident from 5.5 to 8.8 mm. By 10.5 mm (Fig-
ure 7 B) the notochord begins to flex and hypurals
1-3 develop, supporting about eight incipient rays.
At about 12.7 mm the notochord is usually fully
flexed and three hypurals are evident, supporting
10 differentiated but unossified caudal rays ( Figure
7C). By 14.3 mm (Figure 7D), hypurals 1-3 are
ossified and some caudal rays have started ossify-
ing, beginning at the center of the fin and proceed-
ing dorsally and ventrally . The full complement of
18 rays is consistently ossified by 16.4 mm (Figure
7E). By 18.0 mm (Figure 7F) all four hypurals and
both epurals are ossified. By 22.8 mm (Figure 7G)
the caudal fin essentially resembles that of a
juvenile ( Figure 7H) and nearly all elements of the
caudal complex are ossified. The 18 rays, consist-
ing of (from ventral to dorsal) 3 unbranched rays,
12 branched rays, and 3 unbranched rays, are car-
ried on the hypurals as follows: epural 1, 1 ray;
hypural 4, 2 rays; hypural 3, 6 rays; hypural 2, 5
rays; hypural 1, 4 rays.

Incipient dorsal fin rays may be observed in the
proximal portion of the finfold at midbody by 10.5
mm. Ossification of dorsal rays begins at midbody

'"We follow Moser and Ahlstrom's (1970) definition of hypur-
als ". . . all bones of hypaxial origin associated with ural centra
[are defined] as hypurals, including the lowermost bone."

by 11 mm and proceeds anteriorly and posteriorly.
By 17.5 mm the dorsal rays reach their full com-
plement and are completely ossified.

The anal fin develops in a manner analagous to
the dorsal fin and nearly simultaneously. Rays
begin to differentiate at midbody with formation
progressing both anteriorly and posteriorly. Os-
sified rays begin at midbody at about 11 mm and
the full complement may be ossified by 17.5 mm.

Pelvic fin buds may be observed on larvae as
small as 10 mm, although not consistently until
notochord flexion is complete at about 14 mm, and
individual rays may begin ossifying by 11 mm.
The full complement of six rays is ossified by 19
mm.

Pectoral fin buds are visible above the yolk sac
in newly hatched reared larvae. Larval pectoral
fins are present in the smallest stained larvae
examined (3.2 mm). The rays begin to differen-
tiate by 13.5 mm and individual rays begin ossify-
ing as transformation occurs by about 17 mm. The
full complement of pectoral rays was not attained
in the largest larva examined, 22.8 mm, but is
fully developed in a 44 mm juvenile.

Branchiostegal rays begin to accept alizarin
stain at about 9.5 mm. The adult complement of
seven rays may be differentiated, but not ossified,
by 13.6 mm. All rays are ossified by 16 mm.

Gill rakers on the first ceratobranchial begin
forming at about 7 mm. A maximum of six rakers
was formed in the largest stained larva exammed
(22.8 mm). No rakers were formed on the epi-
branchials of this specimen. The adult comple-
ment of four plus seven gill rakers is present on a
44 mm juvenile.

Of the median fin supports, pterygiophores sup-
porting anal and dorsal fin rays begin ossifying at
about 19 mm. These pterygiophores are com-
pletely ossified by 22.8 mm (Figure 8).

Scales form sometime between 22.8 mm (largest
stained larva) and 44 mm (smallest stained
juvenile).

OCCURRENCE

Off Oregon, larvae of/, isolepis are distributed
mainly in the near coastal zone within 18 km of
shore, with abundance peaks at 6-9 km
(Richardson 1973, see footnote 4; Richardson and
Pearcy 1977). Smaller numbers of larvae have
been taken as far as 56 km offshore (Richardson
and Pearcy 1977; Laroche and Richardson 1979),
inside the mouth of Yaquina Bay (Pearcy and

412

RICHARDSON ET AL.: EGGS AND LARVAE OF BUTTER SOLE

hy4

A 5.5nnm

B 10.5mm

C 12.7mm

hy 1

E 16.4mm

F 18.0mm

G 22.8mm

D 14.3mm

H 44.0mm

Figure 7. — Development of the caudal fin oUsopsetta isolepis: 5.5 mm SL, 10.5 mm SL, 12.7 mm SL, 14.3 mm SL, 16.4 mm SL, 18.0
mm SL, 22.8 mm SL, and 44.0 mm SL. Ossified elements are stippled, hy = hypurals; ep = epurals; nc = notochord; APU =
antepenultimate vertebrae; PU = penultimate vertebrae; TV = terminal vertebrae.

413

FISHERY BULLETIN: VOL. 78, NO. 2

..\\ .\\\V '

Figure 8. — Juvenile Isopsetta isolepis, 44 mm SL, showing details of skeletal structure.

Myers 1974), and in the Columbia River (Misitano
1977). A similar coastal distribution is indicated
off Washington with reduced numbers occurring
in Puget Sound (Waldron 1972; Blackburn 1973).
Thus spawning takes place primarily in coastal
areas rather than bays and estuaries.

Larvae occur in the plankton off Oregon mainly
in winter and spring (Waldron 1972; Misitano
1977; Richardson see footnote 4) although in 1971
larvae were taken in every month of the year ex-
cept September, November, and December (Rich-
ardson see footnote 4). In 1972 they were taken in
every month sampled, March through August
(Richardson see footnote 4). In 1971, abundance
peaked in May, and in 1972, smaller abundance
peaks were observed in March and May ( Richard-
son see footnote 4). Spring occurrences of larvae
have been reported off Washington and in Puget
Sound (Waldron 1972; Blackburn 1973).

Monthly length-frequency distributions and
median lengths of larvae collected off Oregon indi-
cate winter-spring spawning (Figure 9). Small
larvae <5 mm were taken January through May
1971, October 1971, and March and April 1972.
Median lengths increased progressively from 2 to
16 mm in January through June 1971 and from 4
to 16 mm in March through June 1972.

Based on available data, /. isolepis apparently
settles to the bottom in coastal areas and rernains
near the coast during the early juvenile period.
Newly transformed juveniles (18-38 mm) have
been collected off the mouth of the Columbia River
in depths of 34-56 m (Table 5). Juveniles in this

Table 5. — Data from beam trawl collections of juvenile Isop-
setta isolepis taken off the mouth of the Columbia River, 1975.

Date

Location
(Lat. N, long. W)

Depth
(m)

Specimens
(no.)

SL of larvae

Median Range
(mm) (mm)

26 June
26 June

14 Sept.

15 Sept.

46°11.5', 124°07.6'
46 09. 5'. 124 06.3'
46 09.5', 124 05.0'
46 09.3'. 12408.0'

37
40
34
56

86

7

5

11

24 18-38
21 18-24

24 22-26

25 20-28

size range have not been reported from bays, es-
tuaries, and nearshore coastal areas where
juvenile Parophrys uetulus have been found (Wes-
trheim 1955; Kendall 1966; Beardsley 1969; Wil-
liam Johnson's data listed in Pearcy and Myers
1974; Peden and Wilson 1976; Laroche and Holton
1979; Cummings and Schwartz^^ Higley and Hol-
toni2; Krygieri3). Although Misitano (1977) re-
ported that both /. isolepis and P. uetulus use the
Columbia River as a nursery area, he was refer-
ring to fish >85 mm long (>95 mm for 7. isolepis).
Thus, smaller I. isolepis juveniles apparently use
offshore coastal areas during their first year of life
as opposed to the bay, estuarine, and near coastal
nursery habitats of P. uetulus.

"Cummings, E., and E. Schwartz. 1971. Fish in Coos Bay,
Oregon, with comments on distribution, temperature, and sa-
linity of the estuary. Oreg. Fish Comm., Res. Div., Coastal
Rivers Invest. Inf. Rep. 70-11, 22 p.

i^Higley, D. L., and R. L. Holton. 1975. Biological baseline
data, Youngs Bay, Oregon, 1974. Final Rep. Alumex Pacific
Aluminum Corp., 1 November 1973 through 30 April
1975. Oreg. State Univ., Sch. Oceanogr. Ref 75-6, 91 p.

'^E. Krygier, Research Assistant, School of Oceanography,
Oregon State University, Corvallis, OR 97331, pers. commun.
June 1978.

414

RICHARDSON ET AL.: EGGS AND LARVAE OF BUTTER SOLE

lOr

H M I I I I M 1 1

80

60

40

20

JAN

TT

FEB

I Ixl I I I

20

0
10

!^ 0
<

Z)

9

> 140
Q

fe '20

ir

LjJ

00 100

I I I I I I I I I I I I I I I I I
MAR

I f lol ui mtTH

loi ui I I'l m n n
ll^lTrfTTi n m 1 1 n 1 1 1

I I I M I I I I
APR

80-

60

40

20

0
20

0
10
0
0

MAY

^

rm

I I I I I M I I I I 1x1 fol I I i I I I I I I 1

I I M I I I I I RxH I I I I ^^'m

OCT

fxl I I I I I I I I I I I I I I I I I I 1 I~

5 10 15 20 25

LENGTH CLASS (mm)

Figure 9. — Length-frequency histograms of Isopsetta isolepis
larvae collected in 70 cm bongo nets off Oregon in 1971 (un-
shaded) and 1972 (shaded). X = median length of larvae in
1971; 0 = median length of larvae in 1972.

The habitat separation of newly transformed
benthic juveniles of /. isolepis and P. vetulus is
interesting since spawning times overlap for the
two species and the larvae are codominants in
coastal waters off Oregon (Richardson and Pearcy
1977). Habitat separation also has been noted in
large OlO mm) larvae; P. vetulus is more abun-
dant in neuston samples relative to plankton sam-
ples than /. isopsetta (Laroche and Richardson
1979). Ratios of relative abundance of P. vetulus to
/. isolepis in plankton samples was 2:1 compared
with 36:1 in neuston samples. Thus the two cooc-
curring species appear to be utilizing different
parts of the water column. Smaller larvae might
be segregated similarly by depth, but we have no
data on vertical distribution to substantiate this
idea. Feeding studies, which may help verify these
habitat differences and provide evidence for re-
source partitioning between these morphologi-
cally similar larvae, remain to be conducted.

ACKNOWLEDGMENTS

We thank Michael D. Richardson (Department
of Navy, NORDA; formerly OSU) for providing
juvenile specimens from beam trawl collections off
the mouth of the Columbia River. Betsy
Washington (OSU) illustrated the larvae and
juvenile; Beverly Vinter (NWAFC) illustrated the
caudal fin and skeleton; Kenneth Waldron
(NWAFC) reared the /. isolepis eggs. Elbert H.
Ahlstrom (Southwest Fisheries Center, Nation-
al Marine Fisheries Service, NOAA, La Jolla,
Calif.) provided unpublished meristic data on /.
isolepis; he also provided stimulating discussions
on osteology of pleuronectids. Earl Krygier (OSU)
provided information on juvenile flatfishes col-
lected in Yaquina Bay and Oregon coastal waters.
Gail Gibbard (formerly OSU) compiled the mor-
phometric data. We thank Beverly Vinter, Ann
Matarese, and Kenneth Waldron for technical as-
sistance.

This work is a result, in part, of research spon-
sored by the Oregon State University Sea Grant
College Program, supported by NOAA Office of
Sea Grant, Department of Commerce, under
Grant No. 04-6-158-44094.

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FISHERY BULLETIN: VOL. 78, NO. 2

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1971. Depth distribution of some small flatfishes off the
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RICHARDSON ET AL.: EGGS AND LARVAE OF BUTTER SOLE

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417

RETENTION OF THI^E TAXA OF POSTLARVAL FISHES IN

AN INTENSIVELY FLUSHED TIDAL ESTUARY,

CAPE FEAR RIVER, NORTH CAROLINA

Michael P. Weinstein,^ Sidney L. Weiss,^ Ronald G. Hodson,^ and Lawrence R. Gerry^

ABSTRACT

Fixed nets were used to sample postlarvae of spot, Leiostomus xanthurus, Atlantic croaker, Mi-
cropogonias undulatus, and flounders, Paralichthys spp., over several 24-hour periods in the Cape Fear
River, near Wilmington, North Carolina. Results of analyses of variance on abundance data collected
at two locations indicate that these taxa exhibit distinct behavioral responses, primarily to photo-
period and tide, which allow them to maintain a selected position in the estuary and avoid being flushed
seaward. The level of response to these variables dictates ultimate residence in at least two primary
nurseries, the river main stem in the vicinity of the salt boundary and the tidal salt marshes. By
migrating to the surface at night, both spot and floimders make apparent use of tides to augment lateral
migration into marshes. Conversely, by tending to remain more bottom oriented at all times, Atlantic
croaker accumulate in greater numbers in deep water at the head of the estuary.

Mechanisms by which larval fishes are recruited
to, and concentrated in, estuaries are poorly un-
derstood. Attempts to elucidate these mechanisms
suffered from the generally high degree of vari-
ability associated with sampling larval fish popula-
tions. Recognizing this, Graham (1972) employed
fixed nets to collect larval Atlantic herring,
Clupea harengus, in the Sheepscot estuary of
Maine. His gear offered the advantage of obtain-
ing synoptic samples over the entire water col-
umn, and because much greater volumes were
filtered, the variability of the data was also re-
duced. Consequently, he was able to infer a
mechanism used by Atlantic herring larvae to
select a specific reach of the estuary, i.e., a behav-
ioral response manifested by interactions between
depth, or location, and tidal direction.

The importance of such interactions has not al-
ways been fully appreciated; e.g., Pearcy and
Richards ( 1962) postulated that larval fish trans-
port in the Mystic estuary occurred mainly in the
lower layer by net nontidal flows. Similarly,
Haven ( 1957) and Sandifer ( 1975) described utili-
zation of net nontidal transport in the lower layers

•Lawler, Matusky & Skelly Engineers, One Blue Hill Plaza,
Pearl River, NY.; present address: Department of Biology, Vir-
ginia Commonwealth University, Richmond, VA 23284.

^Lawler, Matusky & Skelly Engineers, One Blue Hill Plaza,
Pearl River, N.Y.; present address: Sandoz, Inc., East Hanover,
NJ 07936.

'Department of Zoology, North Carolina State University,
Raleigh, NC 28603.

Manuscript accepted November 1979.
nSHERY BULLETIN: VOL. 78, NO. 2, 1980..

for fishes and invertebrates in the Chesapeake
Bay. However, these investigators collected lar-
vae during the daytime only and did not consider
diel migrations which may bring many larvae to
the surface at night (Pacheco and Grant 1968;
Lewis and Wilkens 1971; Williams and Porter
1971). Moreover, certain larval fishes (e.g.,
menhaden ) may also frequent the upper layers to a
considerable extent during the day (Thayer et al.
in press). Thus, it is probable that the retention
mechanism is species-specific and involves several
elements as described by Bousfield (1955): 1) diel
changes in vertical distribution; 2) utilization of
the residual, or nontidal, drift seaward in the
upper layer and landward along the bottom; and 3)
changing behavioral parameters with respect to
tidal direction (e.g., see also Hughes 1969a, b,
1972; Turgeon 1976). Individual species may
utilize one or more of these mechanisms to reach
and stay within a preferred zone of the estuary,
from its mouth (Carriker 1951) to the headwaters
(Haven 1957; Turgeon 1976).

Here we describe distributions of postlarval
fishes in two locations within the Cape Fear River
estuary, near Southport, N.C. Both sampling
areas were situated upriver, in an area believed to
constitute a primary nursery zone for several fish
species. Sampling was stratified by location,
depth, photoperiod, and tidal direction, and an
attempt was made to depict postlarval fish behav-
ior with respect to these strata. A hypothesis is

419

FISHERY BULLETIN: VOL. 78, NO. 2

ATLAMTIC

w^^^^

^

0 12 3 4 5,000

SCALE IN METERS

Figure l —Location of sampling transects
(parallel lines at bouys 32 and 50), Cape
Fear River, N.C.

420

WEINSTEIN ET AL.: RETENTION OF THREE TAXA OF POSTLARVAL FISHES

formulated which relates these behavioral re-
sponses to the maintenance of a preferred position
within the estuary.

STUDY AREA

The Cape Fear River estuary (approximately
lat. 33° N) is relatively narrow, averaging only
1.6-3.6 km in width and extending 45 km from the
general location of the salt boundary at Wil-
mington, N.C., to the river mouth at Baldhead-
Smith Island (Figure 1). A 12 m deep ship channel
with a width of 120-150 m is maintained from
Wilmington to the river entrance, and adjacent
spoil islands are found along its entire length.
Tidal velocities in the Cape Fear are high, averag-
ing 2.1 m/s during ebb near the city of Southport,
N.C. (National Ocean Survey 1977). Recent hy-
drographic and dye studies (Carpenter^) have es-
tablished that a two-layer system occurs in the

estuary between the vicinity of Sunny Point and
Wilmington (Figure 1).

Extensive tidal salt marshes cover about 8,900
ha and form the largest contiguous system of this
type in the State of North Carolina (U.S. Army
Corps of Engineers^). Tidal creeks cover an esti-
mated 648 ha, and shallow open water areas
(shoals) between the channel and salt marshes
contribute an additional 7,285 ha of suitable nur-
sery habitats for the young of fishes and shellfish.

MATERIALS AND METHODS

A modified version of the gear designed by
Graham (1972) was employed in this study (Fig-
ure 2A). Individual 0.5 m plankton nets with
stainless steel cod end buckets were suspended
from aluminum collars (Figure 2B) and bolted
onto orienting vanes attached to a 9.5 mm diam-

••Carpenter, J. H. 1979. Dye tracer and current meter
studies. Cape Fear Estuary 1976", 1977 and 1978. Final report
to the Carolina Power & Light Co., Raleigh, N.C, 339 p.

*U.S. Army Corps of Engineers. 1977. Maintenance of
Wilmington Harbor, North Carolina. Final environmental
statement. U.S. Army Engineers District, Wilmington, N.C,
97 p.

LIGHT

0 5m PLANKTON NET

Figure 2. — A. Sampling apparatus and deployment, the middepth nets were not used on the east and west shoals. B. Detail of the

orienting vane and net mounting. Paired meters were used on all bottom nets.

421

FISHERY BULLETIN. VOL. 78, NO. 2

eter nylon rope. Tidal flows in the Cape Fear es-
tuary were sufficiently high to fully extend these
nets during the sampling period. Lead weights (66
kg) between the anchor and bottom net were used
to fix the depth at which the bottom nets fished,
and a tag line and float attached to the anchor
shaft allowed each rig to be easily retrieved at the
end of the sampling period. Surface nets were
rigged to sample at 1.5 m below the surface, mid-
depth nets at a depth of 6.5 m (in the main chan-
nel), and bottom nets, approximately 1 m above
the substrate. In order to reduce detection by post-
larvae, all nets were dyed deep brown (Rit^ #20,
Cocoa Brown — W. Watson'').

Samples were collected at two locations on three
sets of dates: 14-15 March, 5-6 April, and 11-12
April. A pair of closely spaced transects were
situated near river buoy 50, close to the head of the
estuary, and another pair at river buoy 32, at
Snow's Cut (Figure 1). Two vessels were employed
on each sampling date, and for each transect, three
stations were established across the main channel
from east to west. At slack water the east and west
shoal rigs were set first in 7.6 m of water, and the
channel station nets were anchored last. All nets
at each of the paired transects were set in <40
min. Because the period of slack water continued
for the duration of the setting process, the nets
actually began to fish simultaneously and, except
for the period of retrieval (about 20 min), a nearly
synoptic set of samples was taken across a cross
section of the main channel and shoals. On each
pair of dates four consecutive tides were sampled,
with nets retrieved after 2 h. Limiting the sam-
pling period to 2 h was a necessary precaution in
this study because of the potential for net clogging
in the highly turbid Cape Fear estuary (see below).

It was planned to sample two nighttime and two
daytime tides during each survey but, due to dif-
ferences in the predicted and actual tides, there
was sufficient ambient light to read field data
sheets by the end of the last night set at buoy 50 on
6 April. For this reason, the sample was excluded
from the analyses.

To reduce the potential for clogging, nets were
constructed of 752 /xm mesh material and tapered
to a length of 3 m. Meshes of this size allowed the

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

'W. Watson, Associate, Cape Fear Estuarine Laboratory,
North Carolina State University, Southport, N.C., pers. com-
mun. September 1976.

422

passage of many small plankton as well as fine
detritus, but retained the postlarvae [—7-34 mm
SL (standard length)! of interest. Previous studies
of comparative length frequency in 505 and 760
/xm nets (Copeland et al.^) indicated that postlar-
vae <7 mm (of the species of interest) were un-
common in the Cape Fear estuary, since they were
recruited from well offshore.

In a preliminary experiment in November 1976,
five nets were fished near the bottom, off a tidal
creek bridge, and pulled sequentially every 0.5 h
after an initial fishing period of approximately 1.0
h (Table 1). The flow past each net was monitored
by a TSK^ meter mounted in the center of the
mouth of each net and by a second meter affixed to
the collar support. After more than 3 continuous
hours of fishing at relatively low flows (compared
with the main channel), clogging, as determined
by the difference between the inside and outside
meter readings, did not exceed 28% on the last net
pulled. However, a piece of filamentous algae was
found wrapped around the inner TSK prop and
axle on this net, restricting free movement. Meter
fouling caused by fibrous detritus and algae along
the river bottom created considerable difficulties
in obtaining useful bottom meter readings in the
actual experiments and was deemed a more seri-
ous problem than severe net clogging.

In an attempt to overcome bias due to fouled
meters, all bottom nets were fitted with paired
TSK meters as described above. Based upon the
results of the preliminary study (Table 1), it was
conservatively estimated that an inside meter

^Copeland, B. J., R. G. Hodson, and R. J. Monroe.
1979. Larvae and postlarvae in the Cape Fear River estuary.
North Carolina, during operation of the Brunswick Steam Elec-
tric Plant, 1974-78. Report 79-3 to Carolina Power & Light Co.,
Raleigh, N.C., 214 p.

^Tsurumi Seiki Kosakusho Company.

Table l. — Preliminary net clogging study at Walden Creek,
Cape Fear River. Negative percentage difference indicates that
inside meter reading was largest.

Time

Meter

Volume

% difference

Net

retrieved

Meter

revolutions

(m^)

(Inside/outslde)

1

1235

Inside
Outside

3,053
3,214

97

5

2

1305

Inside
Outside

8,633
8,896

275

3

3

1336

Inside
Outside

6,822
6,357

217

-7

4

1406

Inside
Outside

14,402
15,812

458

9

5

1437

Inside
Outside

12,565
17,410

'400

28

'A piece of filamentous algae was found wrapped around tfie TSK prop and
axle, restricting free movement.

WEINSTEIN ET AL.: RETENTION OF THREE TAXA OF POSTLARVAL FISHES

reading <80% of the outside reading would indi-
cate that the inside meter had fouled. Of the 144
bottom samples collected, 71 had low inside meter
readings and 16 had high inside readings. An ad-
ditional 3 samples were discarded due to gear fail-
ure, leaving a total of 54 samples that could be
used to obtain an estimator for volume.

A strong linear relationship between inside and
outside meter readings (r = 0.996, P<0.01) indi-
cated that an adequate linear predictor could be
obtained:

Y = 0.913 Z

where Y is the inside meter reading and X is the
outside meter reading, both in revolutions. The
standard error of the slope of this line is 0.009, and
the standard error of an individual estimate of the
inner reading is:

SE = V'7.4729 X 10"^ X^ + 1.758337 x 10^ .

The above estimator was used to obtain volumes
for all bottom samples in which the inside meter
reading was <80% of the outside reading. If a net
were actually clogged when we assumed that the
meter was fouled, this procedure would result in
an overestimate of the volume filtered and under-
estimate of the actual density of larvae present.
Thus, differences among strata would be even
larger than depicted in our data.

Upstream and downstream nets at each depth
along the paired transects served as replicates in
the experiments. This survey constituted a facto-
rial design, with site, photoperiod, and tidal direc-
tion as main effects. Nonorthogonal factorial
analyses of variance ( ANOVA) (Searle 1971) were
performed for each taxon, date, and buoy (except
spot and Atlantic croaker at buoy 50 on 14-15
March). Examples of the analytical results are
reproduced in Appendix I to allow the reader to
follow our procedures. A posteriori multiple com-
parison procedures (Bonferroni ^-tests a = 0.05;
O'Neill and Wetherill 1971) were used to examine
station and depth differences and their interac-
tions with photoperiods and tides. Prior to analy-
sis, data were logarithmically transformed [logiQ
(10 + X)] in order to meet the homoscedasticity
requirement of ANOVA.

A partial data analysis was performed for 5
April 1978 at buoy 50, deleting the last night set.
Either daytime or ebb data alone were used, de-
pending on the strata compared. However, data

from all three valid sets were used to obtain an
estimate of sampling variability.

All collections were preserved in 5% buffered
Formalin, and selected taxa were enumerated and
measured for standard length (SL). The latter
measurement was taken from the tip of the snout
to the end of the notochord or hypural plate. Sub-
sampling for lengths was employed when sorted
collections contained >100 individuals of a given
species. Data are presented herein on three taxa:
spot, Leiostomus xanthurus; Atlantic croaker,
Micropogonias undulatus; and flounders of the
genus Paralichthys . Flounders were counted but
not measured in this program.

RESULTS

Since the April sampling dates were near the
end of recruitment for winter-spawned species in
the Cape Fear estuary, the observed pattern of
distribution during this month should reflect the
selection of preferred nursery habitats. On 14-15
March, freshwater flow in the river exceeded 990
m^/s, and the salt boundary was below buoy 50, as
indicated by the absence of measurable salt in the
water column. On these dates, spot were entirely
absent at buoy 50 and only two Atlantic croaker
postlarvae were captured (Figures 3, 4). Floun-
ders, however, were abundant at buoy 50 during
this period. When subsequent sampling indicated
that the salt front was restored to its normal loca-
tion, about 6 km above buoy 50, catches of all taxa
(with one exception) were significantly greater
(P<0.05) upstream (Table 2).

Diel Behavior

Significant differences were only occasionally
detected among stations and were likely
influenced by local patterns of current and larval
transport. For this reason, these comparisons were
not considered further and were omitted from the
ANOVA summary (Table 3). Consistant trends,
however, were evident in several other compari-
sons involving depth, photoperiod, and their in-
teractions. For example, the 24 h mean abundance
across depths for spot and Atlantic croaker, and to
a lesser degree for flounders, was higher (see also
Figures 3, 4) at the bottom on the shoals and at
middepth and below in the channel, with essen-
tially no differences between buoys. Photoperiod,
on the other hand, influenced the catches of floun-
der in a consistent manner. Except for 14-15

423

ro

1000
800
600
400
200
0
200
400
600

O 800

O

O

UJ
<
>

<

q:

UJ
CD

1000

1000

SURFACE

FLOOD , EBB
DAY

BUOY 32

1000

FISHERY BULLETIN: VOL. 78, NO. 2

BOTTOM

IZZl EAST
^ WEST
777^ CHANNEL

NIGHT
FLOOD • EBB

0

1000

'P

'^

o»

BUOY 50

1000

1000

z

FLOOD I EBB

DAY !=' EAST

Wm WEST

PTT, CHANNEL

'^^ MID (6.1m)

EZD CHANNEL

NIGHT
FLOOD EBB

FLOOD I EBB
DAY

14

5

II

14

5

MAR

APR

APR

MAR

APR

APR

14 5 II

MAR APR APR

14 5 II

MAR APR APR

Figure 3. — Abundance of spot, LetostomMsxan^/iizrus, collected on three sampling dates at buoys 32 and 50. Data are stratified to show
mean values for each paired transect with respect to surface-bottom, day-night, and flood-ebb catches. Spot were not captured at buoy 50
on 14-15 March.

424

WTINSTEIN ET AL.: RETENTION OF THREE TAXA OF POSTLARVAL FISHES

BUOY 32

1000

SURFACE

1000
800
600
400-
200
0
200
400-
600
800-

1000

FLOOD EBB
DAY

*TF

CD EAST
^ WEST
^ CHANNEL

c^

NIGHT

flood! ebb

BOTTOM

0

1000

b

CM

FLOOD EBB

1

DAY

CD EAST

^ WEST

PV71 CHANNEL

t^^ MID (6.1m)

en

NIGHT
flood! EBB

CHANNEL

[^

1000

BUOY 50

1000

1000

14 5 II 14 5 ■ II

MAR APR APR MAR APR APR

5 M 14 5 11

APR APR MAR APR APR

Figure 4. — Abundance of Atlantic croaker, Micropogonias undulatus , collected on three
stratified to show mean values for each paired transect with respect to surface- bottom,
croaker were captured at buoy 50 on 14-15 March, these are not shown.

sampling dates at buoys 32 and 50. Data are
day-night, and flood-ebb catches. Only two

425

FISHERY BULLETIN: VOL. 78, NO. 2

Table 2. — Comparison of mean density (number/1,000 m^) at buoy 32 versus buoy
50 for spot, Atlantic croaker, and Pamlichthys spp.

Spot

Atlantic croaker

Paralichthys

spp.

Date

Buoy

Mean

f-value

Buoy

Mean

f-value

Buoy

Mean

(-value

14-15 Mar.

No analysis

conducted

32

50

46,7
147-8

14.76*

5-6 Apr.'

32

50

193.4
302.7

7.85-

32

50

189.4
329.3

11.55-

32
50

17.3
18.0

1.40

11-12 Apr.

32
50

89.1
179.2

8.91-

32

50

52.6
294.9

4. 79'

32

50

2.3
3.9

3.64-

"Significant at a = 0.05; transformed log(10 + X) data utilizing error mean squares from initial
ANOVAs.

'Last nigfit set omitted.

March at buoy 50 and 5-6 April at buoy 32, catches
at night exceeded those taken during daylight
(Table 3). A similar pattern did not emerge for spot
and Atlantic croaker, although night values on
11-12 April at both buoys were significantly
higher. Apparently, net avoidance was negligible
in this study, unlike the findings of Graham
(1972), who limited his sampling for larval Atlan-
tic herring to night hours in the Sheepscot estuary
because of what he described as excessive daytime
net avoidance. High tidal velocities and the turbid
waters of the Cape Fear estuary may have been
partially responsible for this difference. Flounders
were either better able to detect the dyed nets or
perhaps exhibited somewhat different diurnal be-
havior; e.g., a greater tendency to rest on the bot-
tom during the day.

A response to light was further established by
an examination of the photoperiod by depth in-
teractions for the three taxa. During the day, spot
and Atlantic croaker were most abundant at the
bottom and at middepth. Only in the partial data
sets analyzed on 5 April 1978 and for Atlantic
croaker at buoy 32 on this date was this pattern
changed. On this date, depth distributions did not
differ for Atlantic croaker and the surface con-
centration for spot at buoy 50 was not significantly
smaller than the channel middepth value. The
trend for flounders was similar, although not as
distinct as for the other species. At night, all three
taxa moved higher in the water column but to
differing degrees. Whereas flounders and spot
tended to congregate nearer to the surface, most
Atlantic croaker remained lower in the water col-
umn (Table 3).

Of the five significant photoperiod by depth in
teractions involving flounders, a posteriori tests
conducted for night data indicated that surface
concentrations in four instances were sig-

426

nificantly greater than at all other depths. Spot
also tended to accumulate toward the surface, on
the two dates at buoy 32 where a significant in-
teraction was detected, night catches at the sur-
face exceeded those at the bottom; in the main
channel, however, surface and middepth concen-
trations were not significantly different, although
the mean for the former always exceeded that of
bottom values by a substantial margin.

The best indication of a diel movement by At-
lantic croaker occurred in the main channel where
the mean for surface night collections diverged
less from that of other depths (see also Figure 4),
while during the day, the mean for surface collec-
tions was usually significantly lower. No surface
accumulation was detected for Atlantic croakers
on the shoals, on the single date where a sig-
nificant difference was observed, bottom catches
were greater than at the surface.

Response to Tide

Ebb tide catches were generally lower for all
taxa than those of corresponding flood tides (Fig-
ures 3-5). In addition, a shift in catch density from
channel middepth toward the bottom occurred on
ebb, and in several instances bottom concentra-
tions exceeded those of middepth nets for all
species.

The observed difference between ebb and flood
concentrations was always significant for floun-
ders, and on two occasions, for Atlantic croaker.
Tide alone did not seem to exert a major influence
on the concentrations of spot, although a sig-
nificant tidal effect was observed on 14-15 March
1978.

All three taxa displayed a trend towards larger
flood catches on the eastern shoal and in the chan-
nel, while on ebb the western shoal often exhibited

WEINSTEIN ET AL.: RETENTION OF THREE TAX A OF POSTLARVAL FISHES

Table 3. — Analyses of variance summary, for stations (depths), photoperiod and tides. Station as a main
effect is omitted and not all possible interactions are shown. Multiple comparison test results are shown
below individual letter designations.

Buoy 32

Buoy 50

Source

14 March

5 Apnl

11 April

1 4 March

5 April'

1 1 April

Depths^

East west

Spot

B>S

B>S

B>S

—

(B 8)

B>S

Atlantic croaker

B>S

B-S

B>S

—

(B -8)

B>S

Paralichthys spp.

B S

ns3

ns

ns

(ns)

ns

Channel

Spot

MBS

M B

8

MBS

—

(B M

8)

MBS

Atlantic croaker

MBS

M B

8

MBS

—

(ns)~

MBS

Paralichthys spp.

MSB

ns

ns

ns

(ns)

ns

Photoperiod"

Spot

ns

D N

N D

—

(ns)

N D

Atlantic croaker

ns

D N

N>D

—

(ns)

N -D

Paralichthys spp.

N>D

D N

N>D

ns

(N D)

N >D

1 laes^
Spot

F>E

ns

ns

—

(ns)

ns

Atlantic croaker

ns

ns

F>E

—

(F-E)

ns

Paralichthys spp.

F>E

F>E

F.>E

F>E

(F>E)

F>E

Photoperiod x depth

Spot

East/ west

D

B>S

B>S

B>8

—

(ns)

B>8

N

ns

S>B

S>B

—

(ns)

ns

Channel

D

MBS

M B

8

MBS

—

(B M

8)

MBS

N

S M B

8 M

B

8 M B

—

(ns)~

8MB

Atlantic croaker

East, west

D

B 8

B -S

B>8

—

(ns)

B>S

N

B 'S

ns

ns

—

(ns)

ns

Channel

D

MBS

M B

S

MBS

—

(ns)

MBS

N

MBS

ns

MSB

—

(ns)

ns

Paralichthys spp.

East/ west

D

B>S

B S

ns

ns

(ns)

B>S

N

ns

S -B

8>B

ns

(ns)

ns

Channel

D

MBS

M B

S

MBS

ns

(ns)

ns

N

MSB

S M_

B

ns

ns

(ns)

8MB

Tide X station^

Spot

Flood

E W C

E C

W

E C W

—

[ns]

ns

Ebb

ns

W C

E

ns

—

[ns]

W C E

Atlantic croaker

Flood

E C W

E C

W

E C W

—

[ns]

ns

Ebb

ns

C W

J

C E W

—

[C W^

_E]

W C E

Paralichthys spp.

Flood

E C W

E C

w

ns

ns

[ns]

ns

Ebb

ns

ns

ns

ns

[ns]

W E C

Tide X depth

Spot

East/ west

F

ns

ns

ns

—

[ns]

ns

Ebb

B>S

B>S

B>S

—

[ns]

B>S

Channel

F

MSB

M S^

B

MSB

—

[ns]

MSB

Ebb

ns

B M

8

B M 8

—

[B M

8]

B M 8

Atlantic croaker

East/west

F

B >S

ns

ns

—

[ns]

B>S

Ebb

B S

B -8

B>8

—

[ns]

B>S

Channel

F

MBS

M 8

B

MSB

—

[ns]

MSB

Ebb

MBS

B M

S

B M S

—

[ns]

MBS

Paralichthys spp.

East/ west

F

ns

ns

ns

ns

[ns]

ns

Ebb

ns

ns

ns

ns

[ns]

ns

Channel

F

MSB

M 8^

B

ns

ns

[ns]

ns

Ebb

ns

ns

ns

ns

Ins]

ns

'I I — daytime data only from partial data set on 5 April;

^Depths: surface (8), middepth (M). bottom (B).

^ns — no significant difference at a = 0.05 level.

"Photoperiods; day (D). night (N).

^Tides; flood (F),ebb(E),

^Stations: east (E), channel (C), west (W).

-ebb tide data only from partial data set.

427

FISHERY BULLETIN; VOL. 78, NO. 2

SURFACE

14 5 II 14 5

MAR APR APR MAR APR APR

14 5 II 14 5 II

MAR APR APR MAR APR APR

Figure 5. — Abundance of flounders (Paralichthys spp.) collected on three sampling dates at buoys 32 and 50. Data are stratified to
shown mean values for each paired transect with respect to surface-bottom, day-night, and flood-ebb catches.

428

WEINSTEIN ET AL.: RETENTION OF THREE TAXA OF POSTLARVAL FISHES

the largest mean catch. This pattern paralleled
the flow of river water between tides; i.e., water
tended to move upriver on the eastern shoal and
returned on the west. If this phenomenon is real, it
indicates the existence of a large-scale circulation
pattern for postlarval populations.

The tide by depth interaction clearly described
the immediate relationship of these organisms to
tidal flows. Whereas the depth distribution of spot
on flood tides was fairly uniform, bottom and mid-
depth concentrations on ebb often exceeded those
of surface values. Results were not quite as clear
for Atlantic croaker because of their general bot-
tom orientation; nevertheless, a tidal response
was still evident for this species (Figure 4).
Paradoxically, flounder showed little response to
tide (compared with the main effect result), al-
though a pattern similar to that of the other
species is shown in the mean concentrations in
Figure 5.

All of these comparisons are potentially
influenced by diel activity, i.e., by downward mi-
gration during the day. Mean bottom values are
influenced by this effect on both flood and ebb
during daylight hours. One way of isolating the
effect of photoperiod would be to examine the in-
teraction of the three main effects (Table 3).
Unfortunately, this interaction was rarely sig-
nificant. Lack of significance may be a conse-
quence of the use of a logarithmic scale in making

comparisons. Also, the power of tests on this
three-way interaction is considerably less than
that of tests of main effects and of two-way interac-
tions. That diel migration was not entirely respon-
sible for the observed patterns may be seen in the
overall (24 h) differences between flood and ebb.
Since two flood and ebb tides were sampled over
each 24-h period, the effect of diel activity should
be manifested on both tides; i.e., bottom orienta-
tion should occur on flood as well. Table 3 indicates
that this was not the case. Furthermore, a perusal
of the individual strata in Figures 3-5; e.g., an
examination of surface night concentrations
alone, shows that a clear tidal response was exhib-
ited by all three species.

Length-Frequency Distributions

The possibility that buoy 50 was located within
a primary nursery zone was alluded to earlier.
This contention is also supported by length-
frequency data which show that larger (older) fish
tended to accumulate upriver near buoy 50. Un-
fortunately, larger fishes were probably not cap-
tured quantitatively since gear efficiency drops off
rapidly after about 30 mm SL (Copeland et al. see
footnote 8). Hence, only a qualitative picture of
the age composition of a year class is possible.
Nevertheless, distinct size differences occurred
between buoys as indicated in Figures 6 and 7.

10

ro

Q

<

_J

cr

LU
CD

5 01

001

14-15 MAR 78

BUOY 32, n = 2687
BU0Y50,n=0

5-6 APR 78

BUOY 32, n- 2988
BU0Y50,n = 4//3

r

^'

Jl

^\

1

!■

1\

Ti

'1

6 10 14 18 22 26 30 34

LENGTH (mm)

• • BUOY 32, n- 2287

^— -o BUOY 50, n= 3250
1 1 -12 APR 78

6 10 14 18 22 26 30 34

LENGTH (mm)

6 10 14 18 22 26 30 34

LENGTH (mm)

Figure 6. — Length-frequency distribution for spot, Leiostomus xanthurus, on the three collecting dates. This species was entirely

absent from the vicinity of buoy 50 on 14-15 March.

429

FISHERY BULLETIN: VOL. 78. NO. 2

10

fO

O

<

Ixl

DD

5 01

^.001

• • BUOY 32, n= 3659

p— -o BUOY 50, n= 2
14-15 MAR 78

J

• • BUOY 32, n= 2998

^—<^ BUOY 50, n= 4867
5-6 APR 1978

■ /;' \^

■ / ' \ ' '

: / 1 \ \

/ '' '> '' \

10 14 18 22 26 30 34
LENGTH (mm)

6 10 14 18 22 26 30 34

LENGTH (mm)

CD <D

1 1 -12 APR 78

BUOY 32, n= 2017
BUOY 50, n= 4052

Y\, «

10 14 18 22 26 30 34

LENGTH (mm)

Figure 7. — Length-frequency distribution for Atlantic croaker, Micropogonias undulatus, on the three collecting dates. Only two

individuals were captured in the vicinity of buoy 50 on 14-15 March.

Most interestingly, during the high-flow period on
14-15 March 1978, when spot and Atlantic croaker
moved downriver, the larger fish accompanied the
newer recruits to the vicinity of buoy 32. This is
most evident in Figure 7 for Atlantic croaker.
With the return of the salt front above buoy 50 in
April, spot and Atlantic croaker returned up-
stream. For both species in this month, length-
frequency distributions at buoys 32 and 50 were
compared by Pearson chi-square tests. Significant
differences (P<0.05) were found for all compari-
sons, with larger fish predominating upstream.

DISCUSSION

In contemplating the retention of bivalve larvae
within the James River estuary. Wood and Hargis
(1971) stated, "The point at issue is not whether
such retention occurs, but whether evolved pat-
terns of larval behaviour contribute significantly
to the process." Evidence from the present investi-
gation supports the premise that, by displaying
specific behavioral responses, postlarvae of the
three taxa studied were able to reach and stay
within specific portions of the Cape Fear River
estuary. This occurred despite intensive tidal
flows and relatively high exchange ratios in the
system.

Peak recruitment for winter-spawned larvae in
the Cape Fear estuary and many other Atlantic

430

coast estuaries occurs at a time when stratification
and tidal exchange ratios are usually at a yearly
maximum. The exchange ratio may exceed 0.70 in
the Cape Fear estuary and flows above 1,700 m^/s
have been recorded in January and February 1978
(Carpenter see footnote 4). Species recruited from
the ocean also have the peculiar problem of initial
entrance into the estuary and the avoidance of
being washed out on the subsequent tide. By re-
sponding to a combination of hydrographic fea-
tures of the estuary and perhaps to exogenous
variables these species are able to avoid net sea-
ward transport.

Active responses to light and diel migrations in
the water column have been attributed to the lar-
vae of barnacles (Fales 1928; Bassindale 1936;
Bousfield 1955), oysters and other bivalves (Car-
riker 1951; Korringa 1952; Williams and Porter
1971: Wood and Hargis 1971), copepods (Schallek
1943), shrimp (Hughes 1969a, b, 1972; Williams
and Deubler 1968), and fishes (Rogers 1940;
Creutzberg 1961; Pacheco and Grant 1968; Lewis
and Wilkens 1971; Graham 1972; Smith et al.
1978). However, differential avoidance of nets
with respect to depth has also sometimes been
suggested as the cause of diel "migrations" (e.g..
Fore and Baxter 1972). Results of comparative
studies using several kinds of collecting gear, in-
cluding high-speed trawls (Thayer et al. in press),
and the observed absence or low abundance of

WEINSTEIN ET AL.: RETENTION OF THREE TAXA OF POSTLARVAL FISHES

most species (including those studied here) in day-
light entrainment collections at a power plant lo-
cated on the river near Southport (Copeland et al.
see footnote 8) imply that this hypothesis is not
tenable and support the contention that diel mi-
grations actually do take place. If larvae were
similarly stratified in the water column with re-
spect to tide, a result paralleling that of the photo-
period response would be expected. By resting on
the substratum during ebb, or at least by moving
downward in the water column (below the level of
no net motion), larvae would be transported in the
landward direction.

Behavioral responses of spot, Atlantic croaker,
and flounders to photoperiod and tide are sum-
marized in Figure 8. Several important differ-
ences delineate ultimate habitat utilization by
these species. Flounders apparently reacted to
tidal flows by settling to the bottom, as has been
suggested for oysters and shrimps (Carriker 1951;
Hughes 1969a, b, 1972). When the lack of sig-

nificant tide by depth interaction and the presence
of a tidal main effect are considered together, this
hypothesis seems more tenable. To a degree, seek-
ing boundary layers may be a general tidal re-
sponse exhibited by all three species, making
them difBcult to sample on ebb (especially since
the bottom nets were set 1 m above the substrate).
The ability of flounders to effectively penetrate
freshwaters also is enhanced by this behavior.
Tidal flows above the salt boundary are substan-
tial, certainly greater than the ability of flounder
postlarvae to negotiate them directly. Saltatory
movement upriver by "riding out" ebb on the bot-
tom and responding to currents on flood would
then be a primary mechanism for continued up-
stream migration.

Both spot and flounders were also observed to
migrate toward the surface at night; significantly
larger numbers of individuals were captured in
this stratum both in midchannel and on the
shoals, while Atlantic croaker tended to remain

DAY

SPOT - PARALICHTHYS SPR

NIGHT

ATLANTIC CROAKER
DAY NIGHT

SURFACE

• '••••••'••

BOTTOM ♦••»«'.'»•.•«•

• • . ••

OR

• • •

• . • . •

SURFACE

NET NON-TIDAL FLOW
(UPPER LAYER)

A and/or B

BOTTOM

DOWNSTREAM

UPSTREAM NET NON-TIDAL FLOW DOWNSTREAM

(LOWER LAYER)

UPSTREAM

A - TIDAL RESPONSE (MOVEMENT TOWARD BOTTOM ON EBB)

A' - TIDAL RESPONSE (MOVEMENT TOWARD SURFACE ON FLOOD)

B - PHOTOPERIOD RESPONSE (BOTTOM ORIENTATION DURING DAY)

B' - PHOTOPERIOD RESPONSE (SURFACE ORIENTATION AT NIGHT)

Figure 8. — Conceptual model for a larval retention mechanism based on response to photoperiod and tide. Details of the response differ

for the three taxa ( see text).

431

FISHERY BULLETIN: VOL. 78, NO. 2

bottom oriented during this period. In studies of
feeding by postlarval fishes in the Newport River
estuary, N.C., Peters and Kjelson ( 1975) and Kjel-
son et al. (1975) demonstrated that spot were ac-
tively feeding only during the daytime and de-
scribed them as carnivorous sight feeders. If the
nighttime surface orientation observed for floun-
ders and spot is not related to feeding activity,
then to what might it be attributed?

We suggest that active migration into the
marshes is aided by surface movement on flood
tide at night. Since the mouths of many of these
tidal creeks have sills, and since most are shallow
and lack stratification, remaining near the bottom
in the main stem would not aid postlarvae in lat-
eral movements into the marshes. However, by
staying near the surface on night flood tides, large
numbers of individuals would be carried laterally
into the marshes and other shoal areas, perhaps
with the additional advantage of lower predation
pressure.

Once in the marsh or other suitable shallow
area, a tidal response elicited on ebb, i.e., a ten-
dency to seek boundary layers near the bottom or
toward the banks, would allow at least some mem-
bers of the cohort carried into the system on flood
to remain on ebb (Lewis and Mann 1971). This
percentage need not be very high on each tidal
cycle to produce a rapid population accumulation.

Species displaying a greater tendency to remain
in the lower layers over 24 h should not be present
in great numbers in shallow areas. This is pre-
cisely the case for Atlantic croaker. The marshes
in the Cape Fear are not a major nursery zone for
this species, as demonstrated by the nearly com-
plete absence of postlarval Atlantic croaker from
this habitat (Weinstein 1979). A noteworthy
paradox arises when this species is considered
over most of its geographic range. Atlantic croaker
seem to prefer those estuaries with deep channels
and are not taken in large numbers in the shallows
(Welsh and Breder 1923; Wallace 1941; Suttkus
1955; Haven 1957; Nelson 1969; Chao and Musick
1977). It is suspected that in these estuaries, post-
larval Atlantic croaker maintain their general
bottom orientation and do not move laterally to
any great extent; however, in several shallow es-
tuaries along the Gulf of Mexico (Herke 1971;
Parker 1971; Arnoldi et al. 1974; Yakupzack et al.
1977) young Atlantic croaker make extensive use
of the marsh shallows. Thus, in those situations
where deep channels are not predominant fea-
tures of the system, Atlantic croaker will make

use of the marsh shallows. This difference in dis-
tribution in the Gulf States might be further rec-
onciled if temperature is taken into consideration.
Temperature as a potential limiting factor for At-
lantic croaker year class success in most middle
Atlantic coast estuaries has been discussed by
Joseph (1972). Remaining in the warmer waters of
the deep channel during winter might enhance
Atlantic croaker survival. The winters of 1976-77
and 1977-78 along the Atlantic coast have been
colder than usual; greater utilization of shallow
areas by Atlantic croaker might occur in warmer
years.

Others also have observed that the river main
stem at the head of the Cape Fear estuary is a
primary nursery zone for Atlantic croaker and, to
a more limited extent, for spot and flounders
(Copeland et al. see footnote 8). In addition, the
boundaries of this zone for certain species are dic-
tated by freshwater flows and tend to shift with
these flows. Although not captured quantita-
tively, larger spot and Atlantic croaker accumu-
lated upriver in the vicinity of buoy 50 (Figures 6,
7). Although flounders were not measured, a simi-
lar result would be expected for these species.

In summary, we believe the data presented are
consistent with the hypothesis that postlarvae
exhibit behavioral patterns with respect to photo-
period and tide which are instrumental in en-
abling these organisms to: 1) accumulate in up-
stream nurseries by utilizing net nontidal flows in
the lower layer, 2) make strong lateral movements
into the marsh nurseries by migrating to the sur-
face on flood tide at night, and 3) stay in both of
these primary nurseries by dropping lower into or
effectively out of the water column on ebb. The
tidal response may be particularly important in
well-mixed estuaries where upstream drift in the
lower layers is negligible. In fact, it might be the
primary mechanism employed by postlarvae to
penetrate estuaries and reach suitable nursery
habitats.

ACKNOWLEDGMENTS

We are grateful to the biotechnicians of Lawler,
Matusky & Skelly Engineers (LMS) for their con-
scientious efforts in the field and laboratory and to
W. Werth for his assistance in constructing the
sampling gear. We also would like to thank K. L.
Heck, Jr., D. T. Logan, J. P. Lawler, and R. L.
Wyman for their many useful suggestions for im-
proving the manuscript. Appreciation is extended

432

WEINSTEIN ET AL.: RETENTION OF THREE TAXA OF POSTLARVAL FISHES

to S. Moy (statistician) and M. Walters for their
efforts in completing data analyses, and to the
editorial staff of LMS, especially B. Marlowe, B.
Schwartzberg, and M. Barker, for their aid in edit-
ing and typing the manuscript. This study was
funded by the Carolina Power and Light Com-
pany.

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National Ocean Survey.

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Appendix Table l. — Three-way analysis of variance for spot, Leiostomus xanthurus, postlarvae captured at buoy 32, 14-15 March

1978. Catch data are logjg (10 + X) treinsformed.

Source

df

SS

MS

F

Source

df

SS

MS

F

Photoperlod, P

1

0.0551

0,0551

1,50

P ■ S

6

3.2729

0.5455

14.83*

Tide, T

1

0,2218

0,2218

6,03-

T ■ S

6

0,5744

0.9057

2.60-

Sites, S

6

2,6871

0,4479

12,17-

P ■ T ■ S

6

0,3805

0.0634

1.72

P X T

1

1 ,2493

1 ,2493

33,95-

Error

24

0,8831

0,0368

Multiple comparisons (Numbers in parentheses are mean catch for each stratum.)

A. Tides

Flood (100,7) -ebb (68.2)

B. Sites (Bonferroni f-tests; « = 0,05)

1 , Depths: east and west
Bottom (131 ,9) surface (68.3)

2, Depths: channel

Largest: middepth(97,1) bottom (39,3) surface(39,2): smallest

3, Stations

Largest: east( 109.5) west(90.6) channel(58.5): smallest

C. Photoperiod <■ tide (Bonferroni f-tests; « = 0.05)

Largest: flood; night( 120.3) ebb/day( 103.3) flood/day(81-1) ebb./night (27.2): smallest

D. Photoperiod ■ site (bonferroni r-tests; « = 0.05)

1. Photoperiod j< depth: east and west
Day: bottom(178,5)>surface(25,0)
Night: ns'

2. Photoperiod ^ depth; channel

Day: largest: middepth(145.0) bottom(65.9) surface(8.8): smallest
Night; largest: surface(79.5) middepth(49.2; bottom(3.9): smallest

3. Photoperiod » station
Day: ns

Night; largest: west(97.8) east(91.1) channel(44.3): smallest

E. Tide < site (Bonferroni Mests; a = 0.05)

1, Tide ' depth: east and west
Flood: ns

Ebb: bottom(1 12.6) >surface(31 ,3)

2, Tide X depth: channel

Flood; largest: middepth(108,5) surface(58,1) bottom(9,3): smallest

Ebb: ns

3, Tide X station

Flood; largest: east( 158,6) west(110,1) channel(58,6): smallest
Ebb: ns

•Significant at o = 0,05,

'ns — no significant difference(s).

434

WEINSTEIN ET AL.: RETENTION OF THREE TAXA OF POSTLARVAL FISHES

APPENDIX Table 2.

-Three-way analysis of variance for Atlantic croaker, Micropogonias undulatus, postlarvae captured at buoy 32,
14-15 March 1978. Catch data are logjo (10 + X) transformed.

Source

df

SS

MS

F

Source

df

SS

MS

F

Photoperlod, P

1

0.0594

00594

1.46

P X S

6

2.1754

0.3626

8.91-

Tide, T

1

0.1086

0.1086

267

Tx S

6

0.6195

0.1033

2 54-

Sites, S

6

93385

1.5564

38.24-

P X T X S

6

0.5752

0.0959

2.36

P X T

1

0.5152

0.5152

12.66-

Error

24

0.9769

0.0407

Multiple comparisons (Numbers in parentheses are mean catch for each stratum.)
A Photoperiod ■ tide (Bonferroni f-tests: o - 0.05)

Largest: flood night(301 .4) ebb day(249.7) flood day( 266.6) ebb/ night( 143.5): smallest

B. Sites (Bonferroni f-tests; a = 0.05)
1 Depths: east and west

Bottom (31 1.6) -surface (69.5)

2. Depths: channel

Largest: middepth(636.6) bottom(193.2) surface(28.1): smallest

3. Stations: ns'

C. Photoperiod ■ site (Bonferroni f-tests; a = 0.05)

1. Photoperiod ■ depth: east and west
Day: bonom(404.6) •surface(25.7)
Night: bottom(218.5) ■surface( 107.0)

2. Photoperiod ■ depth: channel

Day; largest: middepth(590.9) bottom(288.7) surface(6.3): smallest

Night; largest: middepth(682.2) bonom(65.9) sunace(57.2): smallest

3. Photoperiod > station
Day: ns

Night: ns

D. Tide ■ site (Bonferroni f-tests; a = 0.05)

1. Tide ■ depth: east and west
Flood: bottom(336.3) >surface(1 10.7)
Ebb: bottom(286.8) >sur1ace(38.7)

2. Tide ' depth: channel

Flood; largest: middepth(865.7) bottom(IIO.O) surface(31.6): smallest

Ebb; largest: middeplh(407.4) bottom(304.2) surface(23.6): smallest

3. Tide •' station

Flood; largest: east(336.8) channel(335.8) west(1 10.1)
Ebb: ns

-Significant at « = 0.05.

'ns — no significant difference(s).

435

FISHERY BULLETIN: VOL. 78, NO. 2

Appendix Table 3. — Three-way analysis of variance {or Paralichthys spp. postlarvae captured at buoy 32, 14-15 March 1978. Catch

data are logjg (10 -I- X) transformed.

Source

df

SS

MS

Source

df

SS

MS

Photoperiod, P
Tide, T
Sites, S
P X T

0.3217
2.5208
1 .8388
0.2309

0.3217
2 5208
0.3065
0.2309

12.55*

98.32-

11.95-

9.00-

P X S
T X S
P X T
Error

X S

6

1 7818

0.2970

11.58-

6

1 1400

0 1900

7.41-

6

0.4869

0,0812

3.ir

24

0.6154

0.0256

Multiple comparisons (Numbers in parentheses are mean catch for each stratum.)

A. Photoperiod

Night (50.3) >day (45.7)

B. Tide
Flood(84.7)>ebb(11.1)

C. Sites (Bonferroni (-tests: (* = 0.05)

1. Depths: east and west: bottom (62.3) surface (37.8)

2. Depths: channel

Largest: middepth(89.8) surface(20.3) bottom(14.9): smallest

3. Stations largest: east(79.3) channel(41.6) west(20.8): smallest

D

Photoperiod ■ tide (Bonferroni (-tests: « = 0.05)

Largest: flood/night(87.0) flood./day(82.3) ebb/night (10.5) ebb/day(11.6): smallest

Photoperiod x site (Bonferroni (-tests:
1

0.05)

Photoperiod ^ depth: east and west
Day: bottom(89.0) ~'Surface(3.4)
Night: ns'

2. Photoperiod > depth: channel

Day: largest: middepth(103.4) bottom(19.1) surface(1.9): smallest
Night: largest: middepth(76,1) surface(44.8) bottom(9.2): smallest

3, Photoperiod x station
Day: ns

Night: ns

Tide • site (Bonferroni (-tests: a = 0.05)

1. Tide ■ depth: east and west
Flood: ns

Ebb: ns

2. Tide ■ depth: channel

Flood: largest: middepth(156.4) surface(29.4) bottom(12.4): smallest
Ebb: ns

3. Tide * station

Flood: largest: east(160.3) channel(66.l) west(35.5): smallest
Ebb: ns

"Significant at « = 0.05.

'ns — no significant difference(s).

436

RELATIONSHIPS BETWEEN WAVE DISTURBANCE AND ZONATION

OF BENTHIC INVERTEBRATE COMMUNITIES ALONG A SUBTIDAL

HIGH-ENERGY BEACH IN MONTEREY BAY, CALIFORNIA

John S. Ouver, Peter N. Slattery, Larry W. Hulberg, and James W. Nybakken'

ABSTRACT

Benthic marine invertebrate communities were organized along a gradient of wave-induced substrate
motion on the subtidal high-energy beach in Monterey Bay, California. Two general zones were
distinguished from 6 to 30 m of water. A shallow zone (<14 m) contained sediments that were
commonly disrupted by wave activity and it was primarily occupied by small, mobile, deposit-feeding
peracarid and ostracod crustaceans. Patterns of crustacean morphology and mobility were related to
their depth zonation. Few animals lived in permanent tubes or burrows in the crustacean zone. Wave
disturbance decreased with increasing water depth, while the numbers of sessile and semisessile
species, commensal animals, and suspension or selective- surface-deposit feeders increased. The deeper
zone ( > 14 m) was dominated by polychaete worms living in relatively permanent tubes and burrows. A
variety of descriptive-correlative evidence indicates that community zonation is strongly influenced by
wave- induced bottom disturbance. The evidence includes: 1) a fxjsitive correlation between water
depth and the numbers of tube dwellers, burrow dwellers, and conunensal animals which apparently
cannot establish or maintain papulations in shifting sediments; 2) other depth and thus substrate
disturbance related natural history patterns; 3) a positive correlation between the strength of wave
activity and the width and depth limits of the faunal zones ( i.e., when wave disturbance is more intense,
the crustacean zone ends and the polychaete zone begins in deeper water); 4) a correspondence between
the largest decrease in polychaete population size and the season and location of greatest wave activity
(winter months at the shallowest station); and 5) a marked similarity between community zonation
along a depth-dependent gradient of oscillatory substrate motion (gently sloping sandflats) and the
zonation along a constant depth gradient of creeping substrate motion ( submarine canyon ridge ) . Other
explanations are inconsistent with these biological patterns and, thus, wave disturbance is apparently
the major physical process affecting community zonation.

Sedimentary environments are dynamic and
strongly influenced by water currents and the
physical and biological properties of the sediment.
These animal-sediment relations have become a
major focus of benthic community studies since
the pioneering work of Sanders (1958, 1960) and
Rhoads and Young (1970) and were recently re-
viewed by Rhoads (1974) and Gray (1974). This
previous work was primarily restricted to wave-
protected embayments where deposition and re-
suspension of fine sediments is a major process. In
contrast, the open-coastal environment is com-
monly subjected to oceanic swell which has a
dramatic effect on substrate motion (e.g., Komar
1976). Although sediment scour and motion are
major sedimentary processes affecting the shallow
parts of most continental shelves, little is known

'Moss Landing Marine Laboratories, P.O. Box 223, Moss
Landing, CA 95039.

about their effect on the establishment and
maintenance of soft-bottom communities.

The large areal scale of gradients in wave-in-
duced bottom disturbance and the corresponding
community patterns are difficult to manipulate
experimentally. However, potential relationships
between wave disturbance and community zona-
tion can be explored by a posteriori correlations
and by a priori use of "natural experiments"
(sensu Cody 1974). While communities are often
organized along gradients of environmental vari-
ability ( Whittaker 1962, 1967; Mills 1969; Nichols
1970), the complex interactions between physical
and biological regulatory processes are rarely un-
derstood. The descriptive and experimental
studies in the marine rocky intertidal habitat are
an important exception (e.g., Connell 1961; Day-
ton 1971; Ricketts et al. 1972; Stephenson and
Stephenson 1972; Paine 1974; Lubchenco and
Menge 1978). This study has two primary objec-
tives: to describe the zonation of benthic inverte-

Manuscript accepted November 1979.
fishery BULLETIN: VOL. 78. NO. 2, 1980.

437--

FISHERY BULLETIN: VOL. 78, NO. 2

brates along a subtidal high-energy beach; and to
examine the relationship between community zo-
nation and wave-induced bottom disturbance.
Understanding the role of this predominant
physical process is critical to subsequent studies of
biological phenomena and their interactions with
the physical sedimentary environment.

METHODS

The study area was in central Monterey Bay,
Calif, on the sandflats adjacent to the Monterey
Submarine Canyon and along a ridge in the can-
yon head (Figure 1). The southern sandflat
transect was the main study site (Figures 1, 2).
Stations in 6 (M-1), 9 (M-2), 14 (M-3), 18 (M-4), and
24 m (M-5) of water were sampled at approxi-
mately the same time from June 1971 to June
1974. Three stations (9, 18, 24 m) were sampled

N3 ^•

DEPTH CONTOURS IN METERS

I2I°48'

Figure l.— Southern ( M) and northern (N) sandflat stations and
the canyon transect (A-D) in central Monterey Bay, Calif. N-5
and N-6 were directly east of N-4, 0.5 and 1 km, respectively.

along the northern sandflat from August 1974 to
June 1975 (Figure 1; N stations). The maximum
interval between sampling periods was 3 mo.
Therefore, samples were taken during at least the
four major seasons at each station. The two deep-
est stations along the northern sandflat (N-5, 30
m; N-6, 40 m) were only sampled in May 1975.
Samples were treated separately to document sea-
sonal patterns and were combined over the study
period for each station to examine general zonal
patterns.

A third, but much shorter transect (40 m long)
was located along a flat ridge in the head of the
Monterey Submarine Canyon ( Figure 1 ) . Four sta-
tions were established at 10 m intervals and at a
constant water depth of 14 m. One end of the
transect (station D) was highly disturbed by the
slumping of sediment down an adjacent terrace
wall. No sediment slumping occurred along the
opposite end of the transect (station A) (see En-
vironmental Setting section). The movement of
sediment by slumping was measured by periodic
depth soundings along the terrace wall and by
diver observations and measurements at perma-
nent underwater stations. Divers measured the
distance from the bottom to the tops of the steel
station rods at monthly intervals from May to
November 1972. Periodic visual observations of
station migrations and algal accumulations pro-
ceeded until mid-1974.

All samples and field observations were made by
divers using scuba. Routine samples were taken
with diver-held can corers (length = 17 cm; area =
0.018 m^) and were washed over a 0.5 mm screen
in the laboratory. Eight replicate can cores were
usually taken in a haphazard fashion (Fager 1968)
at each station on each sampling date. The can
corers were 3-lb coffee cans with both ends re-
moved. Animal and sediment loss were prevented
by water-tight snap-on plastic lids. Residues were
fixed in 4% formaldehyde and transferred to 70%
ethanol after sorting. The macrofaunal inverte-
brates were identified to species (i.e., nematodes,
foraminiferans, and copepods were excluded).

A long, diver-operated corer (length = 60 cm;
area = 0.018 m^) was used to document the verti-
cal distribution of organisms within the sediment
at southern sandflat stations in 9, 18, and 30 m of
water during August 1972. To maintain the strata
and minimize animal movement through them,
the corers were held horizontally after sample pro-
curement. Some cores were sectioned immediately
in the boat and others were sectioned within an

438

OLIVER ET AL.: RELATIONSHIPS BETWEEN WAVE DISTURBANCE AND ZONATION

hour at the laboratory. Biomass was calculated
from samples taken with a hydraulic suction
dredge (Brett 1964) in August 1972. Vertical
layers were excavated from a 0.25 m^ cylinder and
collected separately in 1 mm mesh bags. Animals
were weighed after being removed from 709c
ethanol and air-dried for 10 min. These weights
were converted to grams of organic material with
the conversion factors of Lie ( 1968).

Animals swimming near the bottom were sam-
pled with a funnel trap, an inverted funnel ( 20 cm
in diameter) with the spout leading up and into a
holding jar. Legs held the traps within several
centimeters of the bottom. These traps were set
periodically throughout the entire year, primarily
at M-2 (Figure 1; 9 m).

The availability of polychaete larvae was esti-
mated by the settlement of larvae into plastic col-
lecting jars. The jars were wide-mouth gallon con-
tainers (mouth diameter = 10.5 cm; volume = 4.5
1) held vertically in a rack at a height of 1 m from
the bottom. Jars were collected at 14-day intervals
from September 1972 to June 1975 at station M-4
(Figure 1; 18 m). No sediment was placed in the
jars, but a 1 or 2 cm layer of seston accumulated
during each interval. The jars were covered with a
galvanized mesh ( 1 cm square) to prevent the en-
trance offish. The jar contents were washed over a
0.25 mm screen and preserved in 49c formalde-
hyde. Postsettlement polychaetes were identified
to species.

Diver observations of sediment movements and
current patterns were frequent. Direct measure-
ments of wave height and wave period were also
made in the northern bay from September 1971 to
February 1973. They were recorded by the Corps
of Engineers from Santa Cruz Pier approximately
18 km from the study area. Although wave heights
were generally greater in the central bay, the sea-
sonal patterns were similar throughout the bay.

Feeding and burrowing observations were made
in the laboratory and gut contents were examined
under a compound microscope. If an animal con-
tained only sediment, it was called a deposit
feeder. Some deposit feeders also preyed on other
infauna in an aquarium.

ENVIRONMENTAL SETTING

Central Monterey Bay is characterized by
high-energy beaches (sensu Clifton et al. 1971)
that have a relatively gentle seaward slope and a
well-developed winter berm. The most distinct

physiographic feature is the large Monterey Sub-
marine Canyon (Figure 1). Prevailing wind and
wave direction is from the northwest. Wave re-
fraction in relation to bottom topography concen-
trates wave energy on the northern sandflat and
disperses wave energy in the canyon head and
along a portion of the adjacent southern sandflat.
Width of the breaker zone and wave height in-
crease dramatically to the north and south of the
canyon head (Gordon 1974).

Wave-generated bottom currents have primary
control over the sedimentary environment of a
beach. Clifton etal. (1971) gave a detailed descrip-
tion of wave-generated depositional structures in
the high energy-nearshore environment along the
southern coast of Oregon. The same major deposi-
tional structures and zones were present in central
Monterey Bay. The relative position of the near-
shore and offshore is illustrated in Figure 2. The
bulk of the faunal sampling and other field obser-
vations was performed in the offshore area ( Figure
2).

Strong longshore tidal currents can produce lin-
goid and undulatory small ripples (Reineck and
Singh 1973) that trend perpendicular to the rip-
ples produced by oscillating wave-generated cur-
rents. Both types were observed at the stations in
18 m of water and deeper, and often resulted in a
complicated maze of discontinuous ripple crests.
In shallower water, wave-generated currents were
more intense and dominated the depositional
structure. They produced ripple crests in the fine
sand that were more or less continuous and nor-
mal to the direction of wave arrival. During
periods of large winter swell, conditions at the 9 m
station were very similar to those described for the
"outer planner facies" of the nearshore by Clifton
et al. (1971). Here, ripple marks were obliterated
by wave currents and the sediment moved in sheet
flow. Fager (1968) observed similar "miniature
sandstorms" on the sandflats adjacent to the
Scripps Institution of Oceanography in southern
California.

The bottom threshold velocity of sediment
movement is highly dependent on water depth.
Given the narrow range of grain size distributions
among the sandflat stations ( Table 1 ) , the predom-
inant factors controlling the threshold of sediment
movement along the sandflat transects were un-
doubtedly water depth, wave height, and wave
period (Komar 1976). Since unidirectional
longshore currents had a decreasing impact on the
surface sedimentary structures with decreasing

439

NEARSHORE

INNER
OFFSHORE

*

Dendroster

6m

Paraphoxus Sp cf
grandis - h

FISHERY BULLETIN: VOL. 78, NO. 2

OFFSHORE

lOOm

— I

~ rO

M-2

9m

M-4
18 m

i

'tests

Wood ctiips /, ^„,„„,,
fecQlpell

ets <,

,M-5

24mN

•10
M
20

30

P obtusidens

P lucubrans

P epistomus

Pdaboius

\- -

500

Figure 2. — Schematic profile of the beach along the southern transect showing sediment profiles from long cores and the zonation of

paraphoxid amphipods in Monterey Bay, Calif.

Table l. — Characteristics of the surface sediments along southern (M) and northern (N) transects in
Monterey Bay, Calif, (mean ± 95% confidence limits).

Deptti

n

% fine sand

% silt

Coetficient

% organic

Station

(m)

samples

Md (<*)'

(0.250-0.062 mm)

(< 0.062 mm)

sorting^

carbon

M-1

6

6

2.93±0.30

94.4:!: 5.4

1.0±1.3

0.44±0.03

008 = 0.012

M-2

9

11

3.27±0.04

91 .4± 3.6

8.1 ±3.8

0.47±0.04

0.13 = 0.020

M-4

18

7

3.39±0.05

93.3± 1.5

6.2±1.5

0.38 = 0.02

0.10 = 0.050

M-5

24

7

3.53±005

87.6± 2.0

10.8±1.6

0.43 = 0.02

0.18 = 0.020

N-2

9

3

3.04±0.20

96.1 ± 7.0

1.0+0.1

0.42 = 0.20

—

N-3

18

3

3.15=0.03

95.5± 3.6

1.3±1.9

0.42 = 0.03

—

N-4

24

3

3.06±0.10

88.9±14.0

2.0±0.3

0.54=0.30

—

'(A = -log (median diameter).

^Folk and Ward (1957); tiigtier coefficient equals poorer sorting.

water depth, the primary sediment movements
were caused by waves intercepting a shoaling bot-
tom.

An increase in wave height and a decrease in
wave period both cause an increase in the velocity
of sediment movement (Komar 1976). As a result,

winter wave conditions should cause the greatest
sediment motion ( Figure 3 ). Hundreds of dives and
years of qualitative observations of wave activity
indicated a strong gradient in substrate move-
ment with changing depth along the sandflats as
well as considerably greater sediment motion dur-

440

OUVER ET AL.: RELATIONSfflPS BETWEEN WAVE DISTURBANCE AND ZONATION

CO

SI5

. (A)

SlOH

^ r-

PERIOD

71

72

73

en

2-

71

T^^

72

YEARS

73

Figure 3. — Monthly wave periods (A) and heights (B) during
1971-73 at the Santa Cruz pier in northern Monterey Bay, Calif,
(means and ranges).

ing the late fall and winter months. These obser-
vations are consistent with theoretical expecta-
tions (Komar 1976).

Examination of the residue retained by the 0.5
mm mesh screen during the processing of vertical
strata from the long cores revealed additional
characteristics of the depositional environment.
At the 9 m station, strata below 25 cm contained
broken tests and spines of the sand dollar Den-
draster excentricus, broken mollusc shells, and
rounded, olive-green silt stones. The surface
stratum (top 25 cm) was homogenous fine sand
(Figure 2). Similar stratification was observed by
Howard and Reineck (1972) in the upper offshore
of a low-energy beach along Sapelo Island, Ga.
This concentration of shells and tests probably
resulted from physical winnowing or reworking
during severe storms.

Long cores from 18 and 30 m had no shell/test
strata. Instead, there was a concentration of
woody chips of terrigenous, riverine origin and a

VERTICAL STRATA (cm)

05 5-10 10-15 15-20 20-30 30-40

2000

1000

0

1000

2000
50

0
50
50

0
50
50

0
50
50

0
50
50

0
50
50

0
50

Pnonospio
cirnfera
I8m n = 9

E

if)
<

Q
>

Magelona
saccu/ata

I8m n = 9

Magelona
saccu/ata
30 m n = 5

Mediomastus
callforniensis
I8m n = 9

Mediomastus
ca/iforniensis
30m n = 5

Scleroplax
granulata
I8m n=9

Notomastus

tenuis
I8m n=9

Figure 4. — Vertical distribution of invertebrate species living
deep in the sediment in Monterey Bay, Calif, (mean per layer
based on n cores 50 cm long).

high density of large oblong fecal pellets (1 mm
length) below 25-30 cm in the sediment (Figure 2).
The fecal pellets belonged to the deposit-feeding
capitellid polychaete Notomastus tenuis, which
lives deep in the sediment column (Figure 4). Al-
though fecal pellets were produced in situ, the
wood chips had been deposited on the surface and
were either buried by subsequent deposition or by
the biological reworking of the upper sediment
layers. Many large deposit feeders burrowed to a
depth of 20-30 cm (Figures 4, 5, 6). Nevertheless,
this deposit would not persist at the shallower
depths of stronger physical winnowing.

In summary, surface ripple mark patterns, the
composition of deep sediment layers, frequent field
observations, and theoretical predictions indicate
a unidirectional gradient in substrate motion
highly dependent on depth.

441

lOjDOOi

7,500

e

CO

_l
<t

Q

>

Q

— 2,500

5,000

9m

I « 1 1

I ■ ■

■ ■ I
I ■ ■

■ • I

■ ■ ■

■ ■ ■

■ ■ I

R ■ •

■ • I

n=IO

O «0 lO »0 O m

•« fO (VJ -r T V

I I I ■ I '

lO lO i O «o o

to (VJ — ""

18m

FISHERY BULLETIN: VOL. 78. NO. 2

E3 Dendrasterexcentricus
■ Crustacea
Hn Mollusca
□ Vermes

DEPTH (cm)

30m

ioi

-

m

n =

. — 1

5

rmi

Hi

O lo lo lo o in
lO ro cvj — — ■"

o
in

ISS !GO ^

1 1
ro cvj

1

1
o

1

o

1

in
ro

1
in

CVi

in

o

in

o

Figure 5. — Mean number of individuals per square meter per long core layer in n long cores in Monterey Bay, Calif. Vermes are 90%
polychaetes and include enteropneusts, phoronids, oligochaetes, and nemerteans.

30 ID

Q Rare taxo

9m

Molpodto sp

o O o o

« lO - V

I I ' I

o o o o

ro CVJ <^

Amphfuro
ocrystota

18 m

O O o o
lO l»l T V

DEPTH (cm)

Figure 6. — Mean biomass of animals per suction dredge layer in
Monterey Bay, Calif, (except at 30 m, where n = 1). Rare taxa
indicated. See Figure 5 for bar legend.

442

Sediment movements in the canyon head in-
cluded unidirectional dowoi-canyon creeping and
slumping as well as oscillatory movements. Diver
observations and measurements at permanent
bottom stations indicated a general shoaling of
shallow (5-15 m) terrace walls and an accumula-
tion of drift plants (primarily Ulva lobata, Macro-
cystis pyrifera, Zostera marina) during the sum-
mer and early fall. Slumping of terrace walls and
down-canyon flushing of channels were coincident
with the first fall storms and continued through
the winter (see Arnal et al. 1973). The same sea-
sonal cycle of sediment accumulation and flushing
was observed at the heads of the Scripps and La
Jolla Submarine Canyons (Shepard and Dill
1966).

One of the major slumping events occurred at
the shoreward end of the flat canyon ridge. Sedi-
ment creeped down the terrace wall (5-14 m),
across the ridge ( 14 m), and into the deeper canyon
channel (25 m). The slumping was evidenced by a
change in the position of the terrace wall, the
exposure of consolidated mud outcrops on the ter-

OLIVER ET AL.: RELATIONSHIPS BETWEEN WAVE DISTURBANCE ANDZONATION

race after the fall storms, and the down-canyon
movements of station markers along this part of
the ridge. The change in the terrace wall position
was reflected in a 1 or 2 m increase in the depth of a
midwall reference station and in the shifting of the
wall base closer to the permanent stations on the
ridge. The station markers (rods) at station C and
especially D were also moved and slanted in a
down-canyon direction. Furthermore, a large ship
anchor, dropped in slightly deeper water below
station D, moved about 10 m in the same down-
canyon direction (Arnal et al. 1973). In contrast,
the station stakes at stations A and B remained in
a vertical position and did not move. The slumping
of the terrace wall during the fall and winter was
observed in other years and in other parts of the
canyon head as well (Arnal et al. 1973; pers. obs.).

The four ridge stations (A-D) were established
along a gradient of substrate motion. Station D
was nearest to the slump zone and station A was
farthest from the terrace wall, where there was no
evidence of sediment slumping. The animals were
sampled once along the transect in December
1972. Although there were no significant differ-
ences in the median diameter of the sediment and
the sorting coefficients among the four stations
(P>0.1; Kruskal-Walhs test, Conover 1971), the
surface sedimentary structures indicated the per-
sistence of the substrate disturbance gradient
from October to December. During this entire
period, the sandy sediment was well consolidated
and formed parallel ripple marks at stations A and
B, but was poorly consolidated and had no ripple
marks at stations C and especially D (the area of
creeping).

This change in substrate consolidation and rip-
ple mark patterns was not caused by changes in
tidal or oscillatory-wave currents. Tidal and
longshore currents did not vary along the 40 m
transect. Moreover, since oscillatory bottom cur-
rents primarily depend on the grain size, water
depth, wave height, and wave period (Komar
1976), which were all constant along the transect,
the bottom threshold of sediment movement by
these currents did not differ among the ridge sta-
tions. Therefore, the slumping gradient cannot be
quantified in terms of resuspended material or
bottom current velocity. On the other hand, poorly
consolidated sandy sediments characterized all
the slump areas we observed in the canyon head
and were also documented in a large slump near
the Scripps Canyon in southern California (Van-
Blaricom 1978; pers. obs.). These slumping events

are extremely difficult to quantify because they
have never been witnessed (see Shepard and Dill
1966). Nevertheless, the observations and indirect
measurements indicate a unidirectional gradient
of substrate motion related to the distance from
slumping canyon walls and channeling topog-
raphy. Stations A (low movement) and D (high
movement) represent the ends of this gradient.

OFFSHORE ZONATION PATTERNS
ALONG THE SOUTHERN SANDFLAT

The gradational nature of the invertebrate as-
semblages was apparent from the changes in
species abundance along the offshore transect
(Table 2). The crustaceans were the numerically
dominant group at the 6 and 9 m stations (M-1 and
M-2). The density of crustacean species and indi-
viduals was highest at 9 m (Figures 7, 8). Six of the
seven most abundant species at this station were
crustaceans (Table 2). The number of crustaceans
decreased steadily seaward of 9 m. The 14 m sta-
tion was a distinct transition zone between a shal-
low offshore crustacean assemblage and a deeper
polychaete assemblage (Table 2; Figure 7).

The 6 m station was located at the seaward edge
of a large bed of Dendraster excentricus . The width
of the sand dollar bed increased with distance from
the canyon head. It was approximately 40 m at the
southern sandflat transect (Figure 1) and >75 m
wide 2 km to the south. Merrill and Hobson ( 1970)
described a protected open coast/), excentricus bed
which was similar to the local situation.

Crustacean Zone
Crustaceans

The abundant animals of the shallow-water
zone were small, actively burrowing, deposit-
feeding amphipods and ostracods (Table 2). The
amphipods belonged to three typically sand-
dwelling families, Oedicerotidae, Phoxocephali-
dae, and Haustoriidae, and the ostracods to the
Philomedidae. Each family was represented
mainly or exclusively by one genus of several
species and each species was often found within
distinct depth limits.

The genus Eohaustorius contained the only rep-
resentatives of the subfamily Haustoriinae on this
coast (Bousfield 1970). Temporal variations in
Eohaustorius sencillus and E. sawyeri were rela-
tively complementary at the 6 m station and may

443

nSHERY BULLETIN: VOL. 78, NO. 2

Table 2. — Ten most abundant species at each station along southern transect in Monterey Bay, Calif. Data are
number/square meter ± 95% confidence limits and percent frequency of occurrence in n samples in parentheses, x =
species that ranked 11-17 in abundance; B = semipermanent burrow; T = tube dweller.

Crustacean zone

M-3, 14 m

Polychaete zone

M-1, 6 m

M-2. 9 m

M-4, 18 m

M-5, 24 m

Species

n - 108

n = 107

n = 30

n = 141

n = 28

Crustacea:

Euphilomedes longiseta

854±209(81)

397±110 (62)

Eohaustorius sencillus

351 ±105 (60)

1.234 ±165 (100)

333±127 (80)

Paraphoxus lucubrans

298± 72 (68)

E. sawyer!

182± 50(58)

Synchelidium spp.

143± 44(59)

P. obtusidens

66± 21 (31)

Euphilomedes oblonga

1,064 ±204 (87)

513±220 (93)

V

P. daboius

799 ±176 (94)

970 ±209 (100)

402± 61 (91)

X

P epistomus

722±116(98)

320 ± 94 (97)

E carcharodonta

397±116(76)

X

X

Mollusca:

Olivella pycna

309 ±479 (37)

Tellina modesta

55± 17(43)

738 ±182 (93)

132± 61 (63)

722 ±171 (68)

309±121 (93)

Mysella aleutica

386±110(81)

X

Protothaca staminea

X

105± 39(44)

X

Polychaeta:

Prionospio pygmaea T, B

110± 50(19)

X

149± 72 (60)

237 ± 50 (84)

573 ±342 (68)

Scoloplos armiger

105± 33(56)

Armandia bioculata

276 ±133 (32)

Magelona sacculata B

X

237± 72 (61)

303±171 (80)

1,174±231 (94)

628 ±220 (100)

Amaena occidentalis B

X

204 ± 72 (87)

138± 39(57)

276±110 (68)

Mediomastus californiensis

X

182± 66 (80)

331 ± 50(93)

1,053±231 (96)

Northria elegans T

X

116± 44 (67)

242± 28(96)

435 ± 94(100)

Lumbrineris luti B

226 ± 28 (94)

242± 50 (93)

P. cirrifera T, B

193± 99(55)

303 ±132 (89)

Nephtys cornuta

X

325±105 (93)

Edwardsia sp. (Anthozoa) B

X

150± 62 (80)

indicate a well-defined boundary between the two
populations (Figure 9). No Eohaustorius were cap-
tured in funnel traps, indicating that much of the
life history occurs on or within the sediment.

The genus Paraphoxus, in contrast to Eohaus-
torius, has a wide depth distribution in Monterey
Bay (Barnard 1960). Four species occurred along
the subtidal transect in much greater densities
than populations from deeper portions of the bay
(Barnard 1960; Hodgson and Nybakken 1973) and
in more well-defined zones (Figure 2). A fifth
species was the intertidal Paraphoxus sp. cf.
grandis, a new species (Slattery in prep.).

There is an obvious relationship between cer-
tain morphological characteristics and the depth
zonation of Paraphoxus spp. Larger species
reached their peak abundance in shallower water
(Table 3). Paraphoxus sp. cf. grandis and P. ob-
tusidens were giants relative to the other three
species (Table 3). This large size may be an adap-
tation to strong sediment motion (Sameoto 1969;
Fincham 1971). In contrast, P. epistomus and P.
lucubrans were more streamlined and slightly
larger than the deepest species, P. daboius.
Paraphoxus daboius was small and had poorly de-
veloped eyes (Table 3). It lived in the calmest
water (i.e., deepest) and finest sediment and was
the only peracaridean crustacean commonly found

below 5 cm in the long cores. Paraphoxus were
captured by the funnel traps (Table 4).

Euphilomedid ostracods were among the most
abundant crustaceans (Table 2). They occasion-
ally occurred in funnel traps (Table 4). In contrast,
cumaceans were not abundant on the bottom (Ta-
ble 2), but were numerous in funnel traps (Table
4). A number of other rare bottom dwellers were
also abundant in the funnel traps, including the
oedicerotid amphipods Synchelidium shoemakeri,
Synchelidium spp., and Monoculodes spinipes;
other amphipods A^y/us tridens, Tiron biocellata,
and Megaluropus longimerus; and a number of
mysids (Table 4).

No general correlation exists between swim-
ming tendency and species zonation within the
crustacean zone. Although more active Para-
phoxus species were found in shallow water,
nonswimming Eohaustorius spp. lived at the same
depths. Moreover, the cumaceans and oedicerotid
amphipods were active swimmers (Table 4) and
occurred in relatively low numbers throughout
the crustacean zone. On the other hand, there
were distinct morphological patterns suggesting
greater swimming among shallower species
within particular groups (i.e., Paraphoxus and
Euphilomedes species); however, these groups and
others may enter the water column for very differ-

444

OUVER ET AL.: RELATIONSHIPS BETWEEN WAVE DISTURBANCE AND ZONATION

10000

w 7500

\

CO

_J

<

ID
Q5000

>

2500

SOUTHERN TRANSECT

Total

Polychaeta

Crustacea

Mollusca

32

0

I .■••■

M-l M-2 M-3 M-4 M-5

tern) (9m) (14 m) (18 m) (24m)

n«l08 n=l07 n»30 n=l4l n=28

STATION

Figure 7. — Mean number of individuals per square meter and
95% confidence limits of major groups along the southern tran-
sect in Monterey Bay, Calif, (estimates based on n can cores).

24

o
o

o

Q.

8

SOUTHERN TRANSECT
— Total

Polychaeta

Crustacea

Mollusca

•

... %■■

• ■•T

r"'

^ M-l M-2 M-3 M-4 M-5
(6m) (9m) (14m) (18m) (24m)
n=l08 n=l07 n=30 n=l4l n=28

STATION

Figure 8. — Mean number of species per can core (0.018 m^) and
95% confidence limits of major groups along the southern tran-
sect in Monterey Bay, Calif.

ent reasons (e.g., mating, food, substrate move-
ments). Despite these differences, almost all the
crustaceans in the crustacean zone were active,
free-burrowing species and few inhabited tubes.

Other Animal Groups

The polychaetes were much less abundant than
crustaceans in the crustacean zone (Table 2; Fig-
ure 7). Scoloplos armiger, Chaetozone setosa,
Nephtys caecoides, and Dispio uncinata were the
most characteristic species at the shallowest sta-
tion (M-l). Prionospio pygmaea and Magelona
sacculata maintained highly ephemeral popula-
tions near the surf zone (see Seasonal Patterns).
The uncommon onuphid Onuphus eremita was
only encountered at 6 m (M-l). In general, the
more frequent members of the polychaete as-

1500

YEARS

Figure 9. — Complementary temporal variations of Eohaus-
torius sencillus and E. sawyeri at M-l (6 m) in Monterey Bay,
Calif.

445

FISHERY BULLETIN: VOL. 78, NO. 2

Table 3. — Gradation of adult morphological characters in the five species of paraphoxid amphipods in Monterey

Bay, Calif.

Paraphoxus sp.

P.

P.

P.

P.

Character

cf. grandis

obtusidens

lucubrans

epistomus

daboius

Depth of dispersion center

Intertidal

<6m

36 m

9m

14m

Mean size (mm) mature females (±SD)

15±2.5

12±2.2

4.5±0.8

3.7±0.4

2.8±0,2

Ratio of eye diameter to body length

1:35

1:39

1:17

1:33

1:56

Ratio of inner' to outer ramus of uropod III

1:1.09

1:1.04

1:1.1

1:1.5

1:4.2

Number of individuals measured

10

10

20

20

20

'Higher ratio indicates more foliose uropod used in swimming.

Table 4. — Abundance of crustaceans caught in funnel traps at
station M-2 (9 m) in Monterey Bay, Calif. (410 trap days).

No.

No.

Species

trapped

Species

trapped

Amphipods:

Cumaceans:

Synchelidium shoemakeri

160

Diastylopsis tenuis

57

Paraphoxus daboius

79

Lamprops carinata

35

Atylus tridens

66

Hemilamprops californica

27

Tiron biocellata

40

Mesolamprops bodegensis

25

Monoculodes spinipes

40

Cyclaspsis spp.

9

P. epistomus

11

Anchicolorous

Megaluropus longimerus

1

occidentalis

4

Ostracods:

IVIysids:

Euphilomedes

Neomysis kadiakensis

550

carcharodonta

12

Acanthomysis spp.

250

E. longiseta

7

Others

50

E. oblonga

5

semblage at M-1 were mobile deposit feeders. The
most abundant polychaetes at M-2 (9 m) were
species that maintained larger populations in
deeper water. The one exception, Armandia bre-
vis, had a low frequency of occurrence (Table 2),
was highly opportunistic, and primarily lived in
more protected areas (Oliver 1979).

Polychaete Zone

The polychaete zone (Table 2) was characterized
by animals that require a more stable substratum
to establish and maintain burrows and tubes.
Most of the polychaetes living exclusively in the
shallow crustacean zone did not have permanent
tubes or burrows (Table 2). This was true of all the
crustaceans. The gradual change in ripple mark
and vertical sedimentary structure discussed pre-
viously reflected this increase in substrate stabil-
ity. There were several other distinct visual
changes between the two zones. The most con-
spicuous were the increase in burrow openings
and tube fragments and the density of large
siphons of the goeduck, Panopea generosa, which
was first encountered in the transition area (14 m).

Polychaetes

The polychaetes Magelona sacculata and Noth-
ria elegans were abundant at the deeper stations
(Table 2). The onuphid N. elegans lived in a verti-

cal tube constructed of clean sand. Laboratory ob-
servations and gut contents indicated that N. ele-
gans was a surface-deposit feeder, scavenger, and
predator. Magelona sacculata lived in a burrow
and was a surface-deposit and suspension feeder.
The gut contents of 25 M. sacculata were mainly
amorphous organic matter with very little sand.

Many other polychaetes were generally more
abundant in deeper water. These included the
spionids Prionospio cirrifera and P. pygmaea and
the large terebellid Amaeana occidentalis (Table
2). Amaeana occidentalis constructed a burrow
with a mucus-impregnated wall and was capable
of extensive burrowing activity in the laboratory.
The mouth v/as often positioned a centimeter or
more below the substrate surface with the tenta-
cles extended through the sediment and into the
overlying water. The gut contents of A. occiden-
talis and Prionospio spp. were similar to those of
M. sacculata. Apparently, they scrape fine mate-
rial from the sediment-water interface and catch
suspended particles.

In general, a higher proportion of animals was
found in lower vertical sediment strata from the
polychaete zone (> 14 m depth) compared with the
crustacean zone (Figures 5,6). This was expected
due to the greater number of tube- and burrow-
dwelling inhabitants. Coincident with this in-
crease was an increase in known or suspected
commensal or symbiont animals. These included
the pinnotherid crabs Scleroplax granulata (Fig-
ure 4) and Pinnixa franciscana and several species
of polynoid polychaetes. Although Day (1967) de-
scribed the paraonid polychaetes as shallow sur-
face burrowers, almost half of the individuals of
the three local species (Aricidea suecica, Aedicira
pacifica, and Paraonides platybranchia) were
found below 10 cm in the sediment (9 individuals
in 0-10 cm and 7 in 10-20 cm).

Several rather small species also burrowed deep
into the sediment. The capitellid polychaete
Mediomastus californiensis was generally <1 cm
long after preservation and was found throughout
the sediment column (Figure 4). Additionally, the

446

OLIVER ET AL.: RELATIONSfflPS BETWEEN WAVE DISTURBANCE AND ZONATION

small (< 1 cm long) Prionospio cirri fera was found
as deep as 30-40 cm in the sediment (Figure 4). It
was the most abundant polychaete from the long
cores at the 18 m station (Figure 4) and yet ranked
only seventh in abundance, when the top 10 cm of
the sediment was considered separately. Spionids
have ciliated feeding palps and dorsal gill fila-
ments. They generally live in mucus-lined bur-
rows or sand tubes and feed on, or just above, the
bottom surface (Hartman 1941 ). Perhaps P. cirrif-
era inhabits the burrows of thalassinid shrimps in
a manner similar to the phoronid worm Phoronis
pallida. In Bodega Bay, Calif., P. pallida is found
deep in the sediment in association with Upogebia
pugettensis (Thompson 1972). The lower portion of
the phoronid tube is constructed of relatively
coarse sand and the distal end is composed of fine
black sediment where the tube passes through the
burrow wall of U. pugettensis . The tube is oriented
normal to the shrimp burrow such that the
lophophore can be extended into the burrow for
feeding and respiration (Zimmer^). Coinciden-
tally, the highest concentration of P. cirrifera per
vertical stratum (175) was found deep (30-40 cm)
in the only core that contained a large thalassinid,
Callianassa sp.

It is important to note that these vertical pat-
terns were not artifacts resulting from migration
down the core or from physical disturbance. Corers
were oriented horizontally while out of water and
quickly cut by extruding the core from the corer
bottom. Moreover, animals that were known to
live very near to the sediment-water interface
were not displaced (e.g., small bivalves, crusta-
ceans, and Nephtys cornuta).

Other Animal Groups

Although the density of crustaceans was very
low in the polychaete zone (Figure 7), the number
of tube-dwelling forms was greater (e.g., Am-
pelisca and Photis species). Variations in the
number of individuals and species of bivalve mol-
luscs (Figures 7, 8) were due to periodical heavy
settlement along the entire transect. Juvenile
mortality was almost complete and very few
specimens were observed that were larger than a
few millimeters. The same observation was made
by Muss (1973) in the 0resund in Denmark. The

most abundant local bivalves were Tellina mod-
esta and Mysella aleutica (Table 2). The distribu-
tion of T. modesta was correlated with the percent-
age of silt in shallow- water sediments by Barnard
(1963). Large individuals were observed in the
northern bay and in Moss Landing Harbor, where
the fine sediment fraction was greater than that
along the transects. There were also high numbers
of small (1 mm) juvenile bivalves present in the
surface strata of the long cores (Figure 5); how-
ever, most of the biomass of molluscs in the lower,
hydraulically dredged strata was due to a few
large individuals of Solen sicarius and Macoma
spp. (Figure 6).

Ophiuroid communities are generally found at
depths ranging from 45 to 90 m in southern
California (Barnard and Ziesenhenne 1961).
Large individuals of Amphiura acrystata were
found deep in the substrate at the 24 m station.
The animal's oral disc was usually 10-15 cm below
the surface and its arms extended through the
sediment into the water column. All observed in-
dividuals appeared to be suspension feeding. The
density of A. acrystata was <llm^ at the 24 m
station, but increased to 1 or 2lvciP- south of the
study area.

NORTHERN SANDFLAT

The northern sandflat received larger waves
and the bottom surge was consistently greater
than that along the southern sandflat. The
theoretical difference in relative wave energy
reaching both beaches was estimated from a de-
tailed wave refraction diagram.^ Assuming wave
arrival from the northwest and wave period of 14 s,
the total energy reaching the southern transect is
only three-quarters of that arriving at a compara-
ble segment of the northern beach. The southern
stations also had finer sediment compared with
the same northern depths (Table 1). During winter
storms, wave heights in the northern area were
often more than a meter higher than those at the
southern study site. These differences only oc-
curred close to the canyon in the vicinity of the
sampling transects and were corroborated by
hundreds of scuba diving observations of substrate
motion and wave swell on the two sandflats.

If the primary control of the offshore zonation
pattern is due to wave-induced substrate motion,

^R. Zimmer, Professor, Biology Department, University of
Southern California, Los Angeles, CA 90007, pers. commun.
June 1973.

^U.S. Army Corps of Engineers wave refraction diagrams 14-
51-1, 1948.

447

FISHERY BULLETIN: VOL. 78, NO. 2

then faunal zones should be shifted into deeper
waters by an increase in wave activity. The differ-
ence in wave energy arriving at the two sides of
the canyon allows a partial test of this hypothesis.
As predicted, the animal zones described on the
southern sandflat were wider and shifted toward
deeper water on the northern sandflat (Figures 7,
10). Density of crustaceans was highest in 18 m of
water, the transition zone was wider, and poly-
chaetes did not increase in number until 30 m
(Figure 10). Nevertheless, the shape of the curves
in Figures 7 and 10, and thus the gross zonal
patterns, were remarkably similar. The abundant
species were the same on both sides of the canyon,
but the rank orders of abundance were not identi-
cal (Oliver 1979). Abundance of the numerically
dominant crustaceans and the total number of
crustaceans was significantly higher along the
northern transect (Figures 7, 10). Presumably,
this increase was related to the extension of the
crustacean zone into deeper water.

12500

10000

CM

E
\

00 7500

_J
<
Z)
Q

>5000
Q

2500

NORTHERN TRANSECT

— Polychaeta

Crustacea

Mollusca

0

r

I"

..J.

N-2 N-3 fsr-4 N-5 N-6
(9 m) (18 m) (24m) (30m) (40m)
n=l4 n=24 n=22 n=4 n=8

STATION

Figure lO. — Mean number of individuals per square meter and
95% confidence limits of major groups along northern transect in
Monterey Bay, Calif. N-5 and N-6 were only visited once.

The predicted effect of increased wave activity
on the infaunal zonation was also observed on the
zonation of the sand dollar bed. During moderate
to heavy sea states, the outer edge of the bed was in
6 m on the southern and in 9 m of water on the
northern sandflat. In addition, the bed was more
than 30 m wider along the northern transect.
Therefore, the greater width and seaward depth
limits of the sand dollar bed were also associated
with stronger wave swell.

CANYON RIDGE TRANSECT

Faunal changes along the canyon ridge transect
provide further evidence for the relationship be-
tween benthic community zonation and substrate
motions. The ridge stations (A through D)
traversed a substrate movement or disturbance
gradient at a constant water depth of 14 m. There-
fore, a number of other environmental factors that
changed with water depth along the sandflats did
not vary along the ridge transect. These included
light, temperature, resuspension and settlement
of food particles, and the zonation of predatory
demersal fish (see Discussion). On the other hand,
there was a distinct gradient of substrate move-
ment along the sandflats as well as along the can-
yon ridge. The type of sediment movement, how-
ever, was rather different. The primary substrate
movements along the sandflats were caused by
wave-generated, oscillating bottom currents,
which became greater with decreasing water
depth. Water depth was constant along the ridge.
This substrate disturbance gradient was caused
by a unidirectional (down-canyon) creeping of sed-
iment which was greater at stations located
nearer to the terrace walls and channels (i.e., sta-
tions D and C) (see Environmental Setting).

Despite these differences, benthic community
zonation was similar along the sandflat and can-
yon ridge transects. The similarity is partially
illustrated by the abundance of polychaetes and
crustaceans (Figure 11). The most striking paral-
lels, however, were in the distributions of indi-
vidual species (Oliver 1979). Species that were
highly characteristic of the shallowest sandflat
stations (e.g., Scoloplos armiger, Dispio uncinata,
Onuphus eremita, Olivella pycna, Euphilomedes
longiseta) were found at stations D and C along the
ridge (zone of sediment slumping). Species that
were most abundant at intermediate sandflat
depths were found at intermediate ridge stations,
C and B (e.g., juvenile Dendraster excentricus,

448

OUVER ET AL.: RELATIONSHIPS BETWEEN WAVE DISTURBANCE AND ZONATION

3000

2000

1000

A — A Sand Flat 1971-75
o — o Sand Flat Dec. 1972
n--n Canyon Dec. 1972

A 4500

CRUSTACEA

3000 r

M-l

M-2 M-3

M-4

6m

9m I4m

18m

D

C B

STATION

A

Figure ll. — Variations in abundance of crustaceans and
polychaetes along the canyon ridge ( A-D) and sandflat transects
(M) in December 1972, and along the sandflat from 1971 to 1975
in Monterey Bay, Calif.

Eohaustorius sencillus, Euphilomedes car-
charodonta) . Finally, several polychaetes (Noth-
ria elegans, Amaeana occidentalis , Lumbrineris
luti, Magelona spp.) that were common in deeper
water were most abundant at ridge stations B and
especially A (farthest from sediment slumping).

There were only a few statistically significant
correlations between the abundance of individual
species along the sandflat and canyon transects
(P<0.05). Since the correlations involved four
pairs of stations, there were just 2 degrees of
freedom in determining the significance of a
product-moment correlation coefficient (Snedecor
and Cochran 1967). With 2 degrees of freedom, a
significant (P<0.05) coefficient must be at least r
= 0.95. However, there were more positive corre-
lation coefficients computed for the individual

species than expected by chance alone. Eighteen of
the most abundant 23 species (those inhabiting
both transects at >l/core) had positive co-
efficients. Assuming no correlation between the
two transects (i.e., independence), the probability
of 18 positive correlation coefficients is 0.019 (sign
test, Snedecor and Cochran 1967 ). The probability
is less when only the species with relatively dis-
tinct zonation patterns are considered (P<0.01).
The average correlation coefficient among these
species is 0.54±0.12 (95% CL). Therefore, al-
though few individual species showed a statisti-
cally significant correlation in abundance along
the sandflat and canyon transects, there was a
significant trend in positive correlation when the
abundant species were considered together.

In summary, benthic community zonation along
the gently sloping sandflats (6-18 m) was similar
to the zonation along a constant depth transect on
the canyon ridge (14 m). This similarity was ob-
served despite differences in substrate distur-
bance (oscillating vs. unidirectional creeping) and
transect lengths (almost 1 km vs. 40 m).

SEASONAL PATTERNS

Seasonal changes in polychaete abundance
were more regular than those of the crustaceans
(Figures 12, 13). The lowest polychaete abundance
generally occurred in the late fall and the winter
(Figure 12). The most dramatic population de-

8000

2 6000
\

_i

3 4000 -
9

>

Q

M-4(l8m)

M^/Wli^ ,^,.

2000 - ft ' ; \ 4 i t , ,-<}>M-2(9nn)

M-I(6m)

YEARS

Figure 12. — Temporal variations in number of polychaete indi-
viduals at three depths along the southern sandflat in Monterey
Bay, Calif, (means and 95^ confidence limits).

449

FISHERY BULLETIN: VOL. 78, NO. 2

10,000 -I

w 5,000

<

Q
>

O

M-2(9nn)

IVl-l(6m)

YEARS

Figure 13. — Temporal variations in number of crustacean indi-
viduals along the southern transect in Monterey Bay, Calif,
(means and 95% confidence limits).

creases, to zero in some cases, were at the shal-
lowest station (Figure 12; M-1, 6 m). Because of
the shallow water depth, wave-induced substrate
motions were most severe at this station (see En-
vironmental Setting). Furthermore, seasonal sub-
strate movements were greatest during the late
fall and winter, when wave heights were large and
wave periods short (Figure 3). Therefore, the low-
est polychaete numbers were found during that
time (late fall and winter) and at the water depth
(6 m) corresponding to the greatest substrate
motions.

Many environmental factors had a general
seasonal trend similar to wave activity. Water
temperature, river runoff, and phytoplankton
standing stocks also had marked winter-summer
variations in Monterey Bay (Oliver et al.'*). How-
ever, wave-induced sediment motion was one of
the only seasonal factors that changed with water
depth and was, thus, coincident with the depth and
seasonal changes in polychaete abundance. The
depth-dependent changes in resuspended particu-
late material are treated in the discussion.

Prionospio pygmaea, Armandia brevis, and
Magelona sacculata settled into the crustacean
zone (M-1 and M-2), but rarely survived to adult
size. Their frequency of occurrence at the shal-

"Oliver, J. S., P. N. Slattery, L. W. Hulberg, and J. W. Nybak-
ken. 1977. Patterns of benthic succession after dredging and
dredge material disposal in Monterey Bay, California. U.S.
Army Corps Eng. Waterways Exp. Stn., Tech. Rep. 0-77-27,
186 p.

lower stations was much lower than it was in
deeper water (Table 2). Moreover, the low popula-
tion abundance during the winter was not simply
a result of seasonal changes in larval availability.
Although some polychaete species appeared to
have a relatively seasonal pattern of larval avail-
ability (e.g., M. sacculata), the larvae of other
species (e.g., N. elegans and P. cirrifera) were
present throughout the year (Figure 14).

The seasonal peaks in polychaete abundance in
deeper water (M-4, 18 m) were largely due to the

40-

20-

Nothria elegans

M\A

^c-N.

kAA

r^\ \/

72

73

74

75

<

en

Ll)
CD

60-

Magelona sacculata

20-

10-

.. A. h 1

J

20-

10

72 73 74

Prionospio pygmaea

75

73 74

YEARS

Figure 14. — Abundant sandflat polychaetes collected in larval
settling jars at the 18 m station (M-4) in Monterey Bay, Calif.

450

OLIVER ET AL.: RELATIONSHIPS BETWEEN WAVE DISTURBANCE AND ZONATION

settlement of M. sacculata. The correlation of the
abundance of M. sacculata with the total number
of polychaetes at M-4 was highly significant (r =
0.71; P<0.001). Magelona sacculata generally ac-
counted for about one-quarter of the polychaete
numbers at M-4. As a result, polychaete abun-
dance patterns in deeper water were dominated by
seasonal changes in larval availability (Figure 14)
and recruitment, and were not clearly related to
substrate motions. This correlation between the
abundance of M. sacculata and the total
polychaete numbers decreased in shallower water
(M-2, 9 m: r = 0.34, P>0.1; M-1, 6 m: r = 0.39,
P>0.1).

In summary, seasonal abundance patterns were
probably affected by a number of environmental
factors including seasonal reproductive cycles and
substrate motions. The recruitment or survival of
polychaetes was lowest at the time of year and
water depth of maximum substrate motions.
Hence, the zonation of polychaetes in the crusta-
cean zone was apparently influenced by seasonal
changes in wave-induced substrate movements.
On the other hand, seasonal variations in crusta-
cean abundance and in deeper living polychaete
populations could not be related to sediment mo-
tion in a simple manner.

DISCUSSION

The general zonation of benthic invertebrate
communities observed in central Monterey Bay is
common along much of the temperate open coast of
western North America. Carey (1965, 1972), Lie
(1969), and Lie and Kisker ( 1970) observed a high
abundance of crustaceans at their shallowest
sampling stations and the numerical dominance of
polychaetes in deeper areas off Oregon and
Washington. Barnard (1963) and VanBlaricom
(1978) found the same two zones in southern
California and Hodgson and Nybakken ( 1973) de-
scribed a comparable pattern in the northern part
of Monterey Bay. A similar change from a crusta-
cean- to a polychaete-dominated assemblage was
also related to wave exposure by Masse (1972)
in the Mediterranean. On the other hand. Day
et al. (1971) and Field (1971) did not find a rich
crustacean fauna in the "turbulent" zone they
described in 3-20 m on the continental shelves
of North Carolina and False Bay, South Africa,
respectively.

The composition of the fauna along the sandflats
was similar to that found at comparable depths in

southern California, but the animal density in
Monterey Bay was almost a power of 10 greater
(compare Table 2 with Barnard 1963). This dispar-
ity was greatest in the crustacean zone. The differ-
ences are probably related to different sampling
methods: diver corers contrasted to the orange-
peel grab used in the earlier studies.

None of the previous studies provide convincing
evidence for a relationship between community
zonation and wave-induced substrate motions. Al-
though the evidence from the present study is de-
scriptive and correlative, it is consistent with
many observations. The general hypothesis is that
wave-induced sediment movement has a strong
influence on community zonation along the sub-
tidal high-energy beach.

Some of the strongest evidence supporting this
hypothesis comes from the natural history pat-
terns of the fauna. There was a significant positive
correlation (r = 0.92,P<0.05) between the water
depth of a station and the numbers of tube build-
ers, burrow dwellers, and commensal animals. A
similar trend emerges when the animals are
grouped into mobile and sedentary forms (Figure
15). Apparently, biogenic structures were difficult
or impossible to establish and maintain in areas of
more intense physical sediment movement. Al-
though wave disturbance might destroy burrows
and tubes and dislodge their inhabitants, some
adults were tolerant of heavy sediment accumula-
tions and capable of vertical substrate migrations
(e.g., Nothria elegans). The zonation of poly-
chaetes may be largely determined by the habitat
selection of settling larvae (Oliver 1979).

100 -I

CO

Mobile

>

? 50-

1-

U

^ 25-

UJ

Q.

Sedentary

•

M-l M-2 M-3 M-4 M-5

6m 9m 14m 18m 24m

STATIONS

Figure 15. — Variations in animal motility patterns along
southern sandflat in Monterey Bay, Calif, (percentage of total
individuals).

451

FISHERY BULLETIN: VOL. 78, NO. 2

Other natural history patterns also support the
relationship between community zonation and
substrate motion. In particular, the small
peracarid and ostracod crustaceans seem well
suited for life in the shifting substrate of the crus-
tacean zone. Their durable chitonous exoskeleton
and general activity probably ensure a greater
survival relative to many soft-bodied and more
sessile forms. Furthermore, their brooding habit
and the parturition of large, armoured juveniles
undoubtedly increased recruitment success.
While no general pattern of crustacean mobility
characterized a particular depth, almost all the
crustaceans were active burrowers and few main-
tained a permanent tube or burrow. The lack of
dependence on such structures is probably impor-
tant to the persistence of these large, shallow-
water populations. In addition, the most fre-
quently occurring polychaetes in the crustacean
zone were also active burrowers that did not live in
permanent tubes or burrows.

Variations in zonal patterns along the two
sandflats also support the wave-disturbance
hypothesis. Wave activity and therefore bottom
disturbance were greater along the northern
sandflat, where faunal zones were wider and
shifted into deeper water. At least one seasonal
change in zonation was coincident with an in-
crease in wave activity. The season (late fall and
winter) and location (shallowest station, M-1, 6 m)
of the greatest wave-induced bottom currents
were characterized by the lowest recruitment and
survival of polychaetes.

The last source of evidence supporting the
hypothesis involves the canyon. While the gra-
dient of substrate motion along the sandflat was
caused by waves intercepting a shoaling bottom,
the gradient of substrate motion along the
canyon ridge transect was caused by unidirec-
tional sediment slumping at a constant depth. De-
spite these very different types of sediment move-
ment gradients, changes in community zonation
along the canyon ridge and sandflat transects
were similar. This result negates the importance
of several other ecological factors that vary with
water depth along the sandflat, but were held con-
stant by the canyon contrast. These include light,
temperature, the deposition and resuspension of
fine food particles, and the zonation of bottom fish.

The deposition and resuspension of fine parti-
cles, which might be used as food, depend upon
bottom currents. The strongest bottom currents
were caused by wave swell (see Environmental

Setting). These oscillatory bottom currents are
highly dependent upon water depth and other fac-
tors that did not vary along the canyon ridge
transect. Thus, while there were probably sig-
nificant variations in the availability of suspended
particles to the different sandflat stations (i.e.,
their fauna), deposition and resuspension were
apparently uniform along the canyon transect.

Demersal flatfish have a zonation that coincides
with the zonation of bottom invertebrates. Many
species of fish become more abundant with in-
creasing water depth and are more common in the
polychaete zone (Table 5). The only species that
was numerous in <20 m was the speckled
sanddab, Citharichthys stigmaeus. Its peak abun-
dance, however, was in 14-18 m and decreased
markedly in shallower depths (Ford 1965;
Kukowski 1973). Since these flatfish are major
predators of sand-bottom invertebrates and they
primarily feed by sight (Ford 1965; VanBlaricom
1978; Hulberg and Oliver 1979), active, surface-
dwelling crustaceans might be particularly sus-
ceptible prey. If this is true, the depth-related in-
crease in bottom feeding fish might account for the
correlated decrease in the shallow-water crusta-
ceans. The changes in community zonation along
the canyon ridge do not support this idea. Large
and highly mobile flatfish can easily patrol the
entire length of a 40 m transect.

In summary, trends in the natural history of the
animals, changes in zonal patterns along the
southern and northern sandflats, seasonal pat-
terns of polychaete recruitment and survival in
the shallows, and the similarity between the can-
yon and sandflat transects support the contention
that community zonation is influenced by changes
in wave-induced bottom disturbance. Alternate
explanations concerning changes in physical
sedimentary parameters (Table 1), the avail-
ability of suspended food, and the zonation of large
flatfish are not consistent with as many observa-
tions. One potentially important alternate
hypothesis could not be evaluated here. This is the
effect of active crustaceans on the settlement and

Table 5. — Total number of species and individuals of fish and
abundance of the three most common demersal flatfish in otter
trawls taken in Monterey Bay, Calif, (from Kukowski 1973).

Item

15 m

36 m

No. species'

7.7

13.8

No. individuals

239

359

Citharichthys stigmaeus

33

12

C. sordidus

14

120

Parofjhrys vetulus

10

33

'Mean number caught per 10-min tow with 20 tows at each depth.

452

OLI\TER ET AL.: RELATIONSHIPS BETWEEN WAVE DISTURBANCE AND ZONATION

early survival of polychaete larvae in the crusta-
cean zone.

The most disruptive wave disturbances were
caused by the mass accretion and erosion of the
substrate by heavy storm swells. The local
sedimentary structures indicated that severe
scouring occurred at a water depth of at least 10 m
and numerous diving observations revealed sig-
nificant sediment movement at the deepest study
stations. These periodic and catastrophic distur-
bances are probably more important in maintain-
ing the zonal patterns than the average wave ac-
tivity of the region. In either case, wave-induced
substrate motion undoubtedly prevents the estab-
lishment and restricts the activities of many ani-
mals and directly or indirectly controls commun-
ity zonation.

ACKNOWLEDGMENTS

We are grateful to P. Dayton, K. Fauchald, R.
Hessler, J. Thompson, and G. VanBlaricom for
reading and criticizing an earlier manuscript.
This study could not have been completed without
the contributions of our friends and colleagues at
Moss Landing Marine Laboratories, including R.
Christensen, T. Ekhart, R. Fricks, C. Hannan, R.
Keegan, L. McMasters, D. Mitchell, E. O'Connor,
S. Pace, and many others. Changes in canyon to-
pography were measured by the enthusiastic S.
Pace and W. Head. The work was partially sup-
ported by the Corps of Engineers in San Francisco
(DACW 07-72-C-0060), in Virginia (DACW 72-
72-C-0016). and in Vicksburg (DACW 39-74-C-
0151). We are indebted to T. Wakeman,R. Yancey,
and R. Engler for that support. The comments of
two anonymous reviewers were also very helpful.

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454

DAILY TIME OF SPAWNING OF 12 FISHES IN
THE PECONIC BAYS, NEW YORK

Steven P. Ferraro^

ABSTRACT

Diel spawning periodicity occurs throughout the spawning season in 11 of 12 fishes studied in the
Peconic Bays, New York. The bay anchovy, An c/ioa mitchilli; Atlantic menhaden, Brevoortia tyrannus;
northern and striped seaiohins, Prionotus carolinus andP evolans; hogchoker, Trinectes maculatus;
weakfish, Cynoscion regalis; windowpane flounder, Scophthalmus aquosus; and butterfish, Peprilus
triacanthus, spawn primarily in the evening or at night. The tautog, Tautoga onitis, and cunner,
Tautogolabrus adspersus , begin spawning in the afternoon and spawning continues into the night.
Scup, S^enotomus c^T^sops, spawns in the morning, and Atlantic mackerel, Scomfcerscomferus, spawns
throughout the day.

The prevalence of nocturnal spawners in the Peconic Bays is inconsistent with predictions of
hypotheses attributing diel spawning periodicity to reproductive isolation and visual constraints.
Some possible causes of diel spawning periodicity are reproductive synchronism between the sexes,
deleterious effects of sunlight on embryogenesis, and parent or embryo predator avoidance.

In his review, Woodhead ( 1966) cited several refer-
ences indicating that spawning occurs only in the
evening or at night in some clupeids, gadids,
pleuronectids, exocoetids, and mullets, and only
during daylight hours in some gobies, blennies,
and pomacentrids. Woodhead concluded: "There is
relatively little direct information describing the
spawning behaviour of marine fish, but such as is
available suggests that spawning is restricted to a
particular part of the day." Recent research gener-
ally supports that conclusion.

Simpson (1971) determined the time of day of
spawning of four marine fishes from the occur-
rence of recently spawned eggs in plankton collec-
tions. His results showed spawning occurs in
plaice, Pleuronectes platessa, between 1800 and
0700 h; sprat, Sprattus sprattus, between 2200
and 0600 h; pilchard, Sardina pilchardus , be-
tween 2000 and 0200 h; and throughout the day in
dab, Limanda limanda, but most intensely be-
tween 2400 and 1200 h. Wicklund (1970) observed
that natural spawning of small (total length <125
mm) cunner, Tautogolabrus adspersus, was re-
stricted to between 1200 and 1700 h. A sevenfold
difference in numbers offish eggs in night vs. day
plankton collections prompted Hobson and Chess
( 1978) to suggest that many reef fishes primarily
spawn at night. Ten anchovy species in the Gulf of

Panama have daily spawning periods lasting
about 3 h, and all spawn between about 1700 and
0430 h (Simpson 1959).

Accumulating evidence indicates that diel
spawning periodicity is a common phenomenon in
marine fishes. In this paper further information is
presented on daily spawning times of 12 marine
fishes from 10 families.

METHODS

From midspring to late fall 1972, 1973, and 1974
plankton collections were taken usually at 9-13
locations in the Peconic Bay area. Long Island,
N.Y. (Figure 1). In 1972 and 1973 samples were
taken on two consecutive days at intervals of 5-11
days. In 1974 samples were collected at monthly
intervals. All collections were made during day-
light hours from 0600 to 1735 h e.s.t. At least three
vertical plankton-haul samples were taken from
the bottom (or to a maximum depth of 12 m) to the
surface at each location with a No. 3 (0.333 mm
mesh) conical plankton net with a mouth area of
0.5 m^. The plankton samples were killed and pre-
served in 4% sea water Formalin^ and stored in 1 1
glass jars. Surface water temperature and solar
time of day (hours since sunrise; time of sunrise

'Department of Ecology and Evolution, State University of
New York at Stony Brook, Stony Brook, NY 11794.

^Reference to trade names does not imply endorsement by the
State University of New York at Stony Brook, Stony Brook,
N.Y., or the National Marine Fisheries Service, NOAA.

Manuscript accepted October 1979.
FISHERY BULLETIN: VOL. 78, NO. 2, 1980.

455

FISHERY BULLETIN: VOL. 78, NO. 2

Figure l. — Location of study site and 13 sampling stations in the Peconic Bays, Long Island, N.Y.

from National Ocean Survey 1971, 1972, 1973) of
each collection were recorded. Since Peconic Bay
waters are well mixed (Hardy 1976), the surface
water temperatures were adequate indicators of
temperatures of the water column and the natural
incubation temperatures of recently spawned fish
eggs (see Discussion section).

Over the 3-yr period more than 2,600 samples
were collected and processed. Plankton samples
were split into manageable subsamples and their
entire contents were viewed under a stereo-
microscope. Fish eggs were separated, identified to
species, staged (Table 1), and counted. Devel-
opmental stages in Table 1 are approximately
equal in duration when fish embryos are reared at
constant temperatures (Ferraro 1980). References
used for fish egg identification included: Kuntz
(1915), Kuntz and Radcliffe (1917), Hildebrand
and Cable (1930, 1934), Merriman and Sclar
(1952), Wheatland (1956), Richards (1959), Man-
sueti and Hardy (1967), Williams (1967), Austin
(1973), Berrien (1975), and Colton and Marak^.

Estimates of time of day of spawning for each
species in a sample were determined by estimat-
ing the mean age of fish eggs <24 h old using
embryo age prediction equations for Atlantic
menhaden, Breuoortia tyrannus, in Ferraro
(1980), below:

logioB = -0.193 + 17.193ri + 34.090 T^

-461.276 7-3 (1)

stage

Table l. — Fish embryo stages of development.

Description

1 Fertilized eggs prior to cell division to 8-cell stage

2 Eight-cell stage to completion of blastodisc formation

3 Blastodisc formation to germ nng V2 way around egg

4 Germ ring Vz way around egg to just prior to blastopore closure

5 Blastopore closure to tail bud beginning to separate from ttie

yolk

6 Tail bud free of yolk to caudal '/e of body free of the yolk

7 Caudal Vs of body free of yolk to caudal 'Ath of body free of

yolk

8 Caudal 'Ath of body free of yolk to fin fold moderately wide and

tail portion of embryo rotated out of embryonic axis and tail
approaching head

9 Tip of tail approaching head to hatching

and,

where B =

T =

S =

A =

A =B (S -1)

(2)

development time (hours) per

stage of development
temperature (in degrees Celsius)
stage of development (Table 1)
mean age (in hours)

and subtracting these values from the time the
samples were collected in the field. (Field data on
differences in development stages of embryos from
consecutive day classes indicated that the B.
tyrannus embryo age equations introduced little
or no error when estimating embryo ages of <24 h
of most of the species in this study (see Results).)

RESULTS

3Colton,J.B.,Jr.,andR.R.Marak. 1969. Guide to identify-
ing the common planktonic fish eggs and larvae of Continental
Shelf waters. Cape Sable to Block Island. Bur. Commer. Fish.
Lab., Woods Hole, Mass., Lab. Ref No. 69-9, 43 p.

Discrete day classes offish eggs of most species
were identified in the field samples. Fish eggs were
present in samples at distinct morphological
stages of development while other morphological

456

FERRARO: DAILY TIME OF SPAWNING

stages were completely absent. Spring spawners
typically had polymodal embryonic stage fre-
quency distributions with one or more embryonic
stages absent between adjacent modes. As water
in the Peconic Bays warmed, the number of modes
in the embryo stage frequency distribution de-
creased such that by midsummer the distribution
was unimodal. Also, as water temperature in-
creased the most recently spawned eggs of most
fishes were found at consistently later stages of
development.

Indirect evidence from field data indicated that
embryonic development rates of most species in
this study were similar. Tests of differences be-
tween modes of embryo development stages repre-
senting two consecutive day classes from field
samples at 17° C by a posteriori sums of squares
simultaneous testing procedure 'Sokal and Rohlf
1969) indicated no significant difference (P>0.05)
in embryonic growi:h per day of 5. tyrannus; bay
anchovy, Anchoa mitchilli; tautog, Tautoga onitis;
Tautogolabrus adspersus; and searobins,
Prionotus spp. Also, age differences between day
classes offish embryos in field samples at tempera-
tures between 15.0° and 17.5° C were calculated
using the B. tyrannus embryo age prediction
Equations ( 1) and (2). The results (Table 2) showed
that the B. tyrannus equations gave good predic-
tions of the expected age difference between em-
bryo day classes for most of the species in this
study.

With the exceptions of scup, Stenotomus
chrysops; Atlantic mackerel, Scomber scombrus;
and to a lesser extent Tautoga onitis and
Tautogolabrus adspersus very few early -cleavage
stage eggs were collected in our daytime sampling
program.

Table 2. — Mean age differences (x, in hours) of fish embryos
representing two consecutive day classes in field samples at
temperatures' between 15.0° and 17.5° C determined by devel-
opment stage differences between day classes and embryo age
prediction equations for Brevoortia tyrannus. The expected age
difference is 24 h.

Species

Number of samples

tSE

Brevoortia tyrannus

124

Anchoa mitchilli

53

Stenotomus chrysops

20

Cynoscion regalis

15

Tautoga onitis

101

Tautogolabrus adspersus

53

Peprilus triacanthus

4

Prionotus spp.

64

Scophthalmus aquosus

7

25.6:

21.8:
20.5i
25.4:
24.9:
23. 6i
24.2 =
22.0:
22.0:

0.40
0.31
0.48
1.21
0.43
0.77
1.57
0.39
3.16

Mean daily spawning times of fishes were calcu-
lated from hourly time of spawning frequency dis-
tributions of sample estimates of spawning time
(Table 3). The 1974 data were used to compute
estimated spawning times of Stenotomus
chrysops; weakfish, Cynoscion regalis; window-
pane flounder, Scophthalmus aquosus; and but-
terfish, Peprilus triacanthus, and only 1973 data
were used to compute the spawning time of the
hogchoker, Trinectes maculatus. Time of spawning
estimates were similar for species where data were
available for 2 yr. Histograms of relative fre-
quency distributions of sample estimates of
spavining time are presented for 1973 data on An-
choa mitchilli; Brevoortia tyrannus; Tautoga
onitis; Tautogolabrus adspersus; northern and
striped searobins, Prionotus carolinus and P. evo-
lans (note: the searobins are considered together
because their embryos can not be reliably distin-
guished); and Trinectes maculatus in Figure 2. In
summary, the results show that A. mitchilli, B.
tyrannus, P. carolinus , P. evolans, T. maculatus , C.
regalis, S. aquosus, and Peprilus triacanthus
spawn primarily in the evening or at night;
Tautoga onitis and Tautogolabrus adspersus
spawn in the afternoon and at night; and
Stenotomus chrysops spawns in the morning.

There was no evidence of diel spawning
periodicity by Atlantic mackerel. Typically, all de-
velopmental stages (Table 1) were present in sam-
ples containing Atlantic mackerel eggs. The only
general trend in the Atlantic mackerel egg data
was a decrease in numbers of later developmental
stages, presumably due to dispersion or egg mor-
tality.

Table 3. — Mean daily spawning times [DST, in hours after
sunrise) of fishes calculated from hourly frequency distributions
of sample estimates of spawning time. Estimated ages of fish
eggs <24 h old in field samples were subtracted from their time of
collection to obtain sample estimates of spawning time.

Species

Year

DSr=SE

'Range of temperatures cfiosen were temperatures at whiicfi at least two fish
embryo day classes would be present.

Brevoortia tyrannus

Anchoa mitchilli

Stenotomus chrysops
Cynoscion regalis
Tautoga onitis

Tautogolabrus adspersus

Peprilus triacanthus
Prionotus spp.

Scophthalmus aquosus
Trinectes maculatus

1972

198

16.36-0.175

1973

370

17.84-0.168

1972

455

16.09-0.103

1973

693

16.78-0.078

1974

32

5.28 ±0.276

1974

74

17.45±0.407

1972

160

15.52±0.200

1973

447

17.62±0.126

1972

101

15.40±0.343

1973

322

15.98^0.215

1974

22

18.55^0.881

1972

174

19.19 = 0.307

1973

330

19.15 = 0.197

1974

38

16.68±0.607

1973

132

16.55±0.110

457

o

z

LiJ

ID
O
LU

LU
>

LlI

day

<#

30-,

25

20

15

5-

Anchoa mitchilli 1973

N= 693

TOS± SE= 16 8± 08

"prrn^ I n^ I — 1 — I — I — I T^ I

0.5 3.5 6.5 9 5 12 5 15 5 18.5 215

Trt-n

B

day

<!

► "

' s

ht

20^

15-

Brevoort
N=370

la tvrannu^

1973

■^^-1

10-

TOS± SE

= I7.8±.l 7

^

5 -

— 1 . — ,

r

'■r-f rT-

r-r T T 1 I

II 1

1

I

I

1

1

1

1

1 I

0.5 3.5 6.5 9.5 12.5 15.5 18.5 21.5

day<*

20

15-

Tauloga oni lis 1973

N=447
TOS^SE - 17.6±.13

nipht

X ]

Tn — I — I — I — I — I — r r I ' I I I

0,5 3,5 6,5 9,5 12,5 15,5 18.5 21.5

TIME OF SPAWNING

( HOURS AFTER SUNRISE )

z

LU

13
O
LlJ
CC
U.

UJ
>

LjJ

D

FISHERY BULLETIN: VOL. 78, NO. 2

day Q^ n I g h I

20-1

laulugoldbrus adspersus 197-

'^i N=322 r

10

TO^tSE- I6.0±. 22

I ' I ' I ' I ' I I r r I ' I ' r I I

0,5 3.5 6,5 9,5 12.5 15.5 18.5 21.5

^

dav

25

20-

15-

10

<♦

5-

Pr ionotub spp. 1973

N- 330
fOS±SE= 19. I ±.20

11111111111 — I — 111

0,5 3 5 6,5 9.5 12 5 15 5 18 5 215

35

30-

25

20

15

<$

day \Jvnight

5 -

Trinectes maculatus 1973

N= 132

TOS±SE= 16.6 ±.i I

T 1 1 1 1 1 1 1 1 1 1 1 I I I

n

1

I r I — I — r—r

05 3,5 e.5 95 125 155 18,5 21 5

TIME OF SPAWNING

( HOURS AFTER SUNRISE )

Figure 2. — Relative frequency distributions of estimated spawning times (TOS) of (A) Anchoa mitchilli, ( B) Brevoortia tyrannus, (C)
Tautoga onitis, (D) Tautogolabrus adspersus, (E) Prionotus spp., and (F) Trinectes maculatus, determined by subtracting estimated
mean ages offish eggs <24 h old from their time of collection in 1973 samples. Mean day length during spawning seasons is indicated.

DISCUSSION

Direct observation of fish spawning at sea is
rare, and aquarium observations may not be
characteristic of natural spaw^ning or may be dif-
ficult or impractical to implement for logistic
reasons. Since embryogenesis begins at spawning
in most marine teleosts, the time of day spawning
occurs can be determined indirectly from the age
of embryos captured at sea. Several investigators,
including Ahlstrom (1943), Gamulin and Hure

(1956), and Simpson (1971), collected plankton
samples throughout the day and determined
spawning times of fishes from the occurrence of
recently spawned eggs. Under certain cir-
cumstances (when field temperatures are fairly
constant and there is little translocation of eggs)
and with knowledge of embryonic development
rates, however, spawning times can be back calcu-
lated by subtracting age offish embryos from their
time of collection. The method of estimating
spawTiing time of fishes in this paper utilizes field

458

FERRARO; DAILY TIME OF SPAWNING

data commonly obtained in ichthyoplankton re-
search and does not require a continuous field
sampling program.

Factors influencing the accuracy of estimated
spawning times of fishes in this paper are intra-
specific and interspecific differences in develop-
ment rates offish embryos and temperature effects
on embryo stage (Table 1) duration. Intraspecific
differences in development rates are likely to intro-
duce only small and unbiased error in spawning
time estimates since incubation times from which
age estimates are made are short (<24 h) and
mean stages of development of all embryos of a
species (<24 h old) in a sample are used in the
embryo age calculation. Interspecific differences
in development rates of most species in this study
are also probably small ( see Results). A maximum
standard deviation of 2.3 h can be expected in
spawning time estimates due to the influence of
temperature on embryo stage duration because
most fish eggs were collected in water tempera-
tures above 15° C (Ferraro 1980). Surface water
temperatures at the time of field collection were
probably adequate indicators of natural incuba-
tion temperatures of recently spawned eggs since
there is little, if any, vertical thermal stratification
in the Peconic Bays and surface water tempera-
ture at a particular location generally fluctuates
by <1° C during a tidal cycle (Hardy 1976).

Based on the occurrence of recently spawned
eggs in plankton collections at Beaufort, N.C.,
Kuntz (1915) and Hildebrand and Cable (1930)
concluded that A. mitchilli spawned between 1800
and 2100 h ( 13-16 h after sunrise), and Hildebrand
and Cable (1938) concluded that Trinectes
maculatus spawned between 1800 and 2000 h
(13.5-15.5 h after sunrise). Those observations
coincide with the onset of spawning estimated for
A. mitchilli and T. maculatus in this paper. Reint-
jes' (1968) conclusion that B. tyrannus spawns at
night, Welsh and Breder's (1924) conclusion that
C. regalis spawns in the evening and at night, and
Sette's (1943) calculations showing Scomber
scombrus spawns throughout the day were con-
firmed in this research. Wicklund's (1970) obser-
vations on the spawning of cunner overlap but
have a much shorter duration than that indicated
for cunner in Figure 2D. Wicklund (1970) only
observed spawning by small (total length <125
mm) cunners between 1200 and 1700 h (7-12 h
after sunrise); he never observed larger cunners
spawning although they were present and de-
fended territories in his study area. 011a and

Samet (1977) noted that tautog in laboratory
aquaria spawned almost exclusively between 1330
and 1600 h (7.5-10 h after sunrise). Their experi-
mental fish, however, had been exposed to un-
natural photoperiod and temperatures and
spawned about 2 mo earlier than tautog normally
spawn in nature. Recently spawned eggs in
plankton collections indicated that some tautog
spawn in the afternoon (8-10 h after sunrise) in the
Peconic Bays, but the bulk of tautog spawning
appears to take place later in the evening and at
night.

A systematic division of fishes in the Peconic
Bays and a summary of their spawning times is
presented in Table 4. Only Atlantic mackerel
showed no indication of diel spawning periodicity,
and only scup spawned exclusively during day-
light hours. The remaining species spawned
primarily during the evening or at night. Nothing
exceptional is known about the adult habits or
embryos of Atlantic mackerel or scup to suggest
why their spawning times are different from the
other species. There appears to be no connection
between bathymetric distributions of embryos of
some of the species (Williams 1968) and spawning
time. There was no evidence of constancy in
spawning time above the family level. Solar
spawning times of most species, though, were con-
sistent throughout the spawning season and in
samples collected at different locations, indicating
seasonal and local differences in ecologic factors
(e.g., temperature, salinity, water depth, tide) had
no effect on daily spawning time.

The tendency of marine teleosts with planktonic
eggs to spawn in the evening or at night is evident
in a listing (Table 5) of some species known or
suspected of diel spawning periodicity. There is

Table 4. — Systematic division and summary of spawning times
(hours after sunrise) of fishes in the Peconic Bays, N.Y. Spawn-
ing is indicated by + .

Species

Spawn

ing time

Taxa

0-6 6-12

12-18

18-24

Clupeltormes:

Clupeidae

Brevoortia tyrannus

+

+

Engraulidae

Anchoa mitchilli

+

+

Perclformes:

Sparldae

Stenotomus chrysops

+

Sciaenidae

Cynoscion regalis

+

+

Labrldae

Tautoga onitis

+

+

-1-

Tautogolabrus adspersus

+

+

-1-

Scombrldae

Scomber scombrus

+ +

+

+

Stromateidae

Peprilus triacanthus

+

+

Triglidae

Prionotus carolinus

+

+

Pnonotus evolans

-1-

+

Pleuronectiformes:

Bothidae

Scophthalmus aquosus

-1-

+

Soleidae

Trinectes maculatus

^

459

FISHERY BULLETIN: VOL. 78, NO. 2

Table 5. — Some marine teleosts which spawn plank. tonic eggs and are known or suspected of spawn-
ing only at particular times of the day.

Family and species

Spawning

1 time

Reference

Ophichthidae;

Pisodonophis cruentifer

Night

Naplin and Obenchain (1980)

Clupeidae:

Etrumeus teres

Night

Houde (1977)

Sardinella melanosticta

Night

Kamiya(1925)

Sardinops sagax

Evening

Ahlstrom (1943)

Sardinia pilchardus

Evening and

night

Gamulin and Hure (1956): Simpson (1971)

Sprattus sprattus

Night

Simpson (1971)

Engraulidae:

Anchoa hepsetus

Evening and

night

Hildebrand and Cable (1930)

A. mitchilli

Evening and

night

Kuntz (1915); Hildebrand and Cable (1930)

Cetengraulis mysticetus

Night

Simpson (1959)

Engraulis euryslole

Evening

Kuntz and Radcliffe (1917)

E mordax

Night

Bolin(1936)

Engraulis spp.

Evening

Delsman(1929)

Stolephorus purpureas

Night

Yamashita(1951)

Stolephorus spp.

Night

Delsman(1931)

Antennanidae:

Histrio histrio

Afternoon and evening

Walters (pers. commun. in Breder and Rosen 1966)

Gadidae;

Enchelyopus cimbrius

Morning

Battle (1930)

Gadus morhua

Evening and

night

Brawn (1961), Breder and Rosen (1966)

Merluccius merluccius

Morning

Storrow(1913)

Pomatomidae:

Pomatomus saltatrix

Evening

Norcrossetal. (1974)

Carangidae:

Caranx kurra

Night

Delsman (1926)

C. macrosoma

Night

Delsman (1926)

C. crumenophthalmus

Night

Delsman ( 1 926)

Pomadasyidae:

Orthopristis chrysoptera

Evening

Hildebrand and Cable (1930)

Sciaenidae:

Bairdiella chrysura

Evening

Kuntz (1915)

Cynoscion nebulosus

Night

Tabb(1966)

C. regalis

Evening and

night

Welsh and Breder (1924)

Labndae.

Tautoga onitis

Afternoon

Ollaand Samet(1977)

Tautogolabrus adspersus

Afternoon

Wicklund (1970)

Scaridae:

Scarus croicensis

Afternoon

Colin (1978)

Sparisoma rubripinne

Afternoon

Randall and Randall (1963)

Mugilldae:

Mugil cephalus

Night

Arnold and Thompson (1958)

M. curema

Night

Anderson (1957)

Scombridae:

Scomber japonicus

Night

Kamiya(1925)

Scomberomorus maculatus

Evening and

night

Ryder (1882): Rathbun (1894); Smith (1907)

Pleuronectidae:

Hippoglossus hippoglossus

Night

Nordgard (1929)

Pleuronectes plalessa

Night

Forster (1953); Simpson (1971)

Pelotretis flavilatus

Night

Thomson and Anderton (1921)

Colistium nudipinnis

Night

Thomson and Anderton (1921)

C. guntherl

Night

Thomson and Anderton (1921)

Peltorhamphus novaezeelandiae

Night

Thomson and Anderton (1921)

Rhombosolea plebeia

Night

Thomson and Anderton (1921)

R. tapirina

Night

Thomson and Anderton (1921)

Soleidae:

Trinectes maculatus

Evening

Hildebrand and Cable (1938)

diel and lunar spawning periodicity in some coral
reef fishes (e.g., Lobel 1978; Johannes 1978; May
et al.l979). References cited in Breder and Rosen
(1966) indicate that at least 70 freshwater and
marine teleosts with demersal or attached eggs
may spawn or oviposit at particular times of the
day. Even though many of the data are only
suggestive, there are indications that diel spawn-
ing periodicity may be a common and widespread
phenomenon among fishes.

Diel spawning periodicity in fishes may be due

to physiological constraints or may be adaptive.
Woodhead ( 1966) and Blaxter ( 1965, 1970) pointed
out that light may restrict spawning to a particu-
lar time of day, especially in species where vision is
important in sexual displays, courtship, and pair-
ing. Woodhead (1966) noted, however, that species
which require daylight for courtship might still
spawn or oviposit at other times of the day. Obvi-
ously, nocturnal spawners are not light limited. If
adaptive, the value of reproductive periodicity
may be found in the synchronization of reproduc-

460

FERRARO: DAILY TIME OF SPAWNING

tion with the biotic or abiotic environment
(Nikolsky 1963; Aschoff 1964; Schwassman 1969).
The annual spawning cycle of fishes which may be
timed to coincide with the annual production cy-
cle, or a period of low predation, etc. (Nikolsky
1963; Gushing 1969; Hoar 1969), may be the
coarse adjustment, and diel spawning time the
fine tuning adjustment to temporally changing
environmental conditions.

Spawning periodicity may be important in syn-
chronizing reproduction between the sexes (As-
choff 1964; Marshall 1967). The precise daily tim-
ing of reproduction may be particularly important
in species which engage in mass spawnings. An
extreme example are the lancelets (e.g., Bran-
chiostoma lanceolatum) which, according to Bre-
der and Rosen ( 1966), release eggs and sperm into
the water at sunset for chance fertilization. Tem-
porally synchronizing spawning in pairing species
presumably is more efficient and may optimize the
number of receptive encounters.

Marshall (1967) suggested diel spawning
periodicity might serve to increase reproductive
isolation between related and morphologically
similar species. Reproductive isolation may be im-
portant in a species-rich habitat such as a coral
reef, but many temperate water marine fishes ap-
parently spawn at or about the same time, i.e., in
the evening and at night (Tables 4, 5).

Diel spawning periodicity could be an adaptive
behavior of fishes to avoid high incident solar
radiation during a very sensitive period of em-
bryonic development. Bell and Hoar (1950) and
Eisler (1958, 1961) demonstrated the lethal and
deleterious effects of light on salmonid embryos,
especially during early embryogenesis; and Mari-
naro and Bernard (1966) demonstrated lethal ef-
fects of light, particularly ultraviolet light, on
some marine planktonic fish embryos. Perlmutter
(1961) and Breder (1962) believed that some
characteristics offish eggs (e.g., transparency, oil
droplets, melanophores) were physiological
adaptations to minimize deleterious effects of
lighten fish embryos, and Perlmutter (1961) listed
several spawming behaviors of fishes which he
thought were adaptions to avoid or minimize ex-
posure of embryos to light. If light is especially
harmful to recently fertilized fish eggs, nocturnal
spawning could be an adaptive behavior to avoid
light during early embryonic development. How-
ever, an explanation is then necessary for why
light is not a factor for diurnal spawners such as
Atlantic mackerel and scup.

Nikolsky (1963) suggested that some fishes
spawn at times of day when spawning adults or
their eggs will be least susceptible to predation.
The "exhausted" condition of some fishes that have
recently spawned (Brawn 1961; Breder and Rosen
1966) and evidence of increased vulnerability of
some spawning fishes to trawling (Mohr, in Blax-
ter 1965) tend to support the idea that spawning
time may be an adaption to minimize losses due to
predation on the parents. Visual predators, pre-
dators with diurnal feeding patterns, or predators
which undergo diurnal vertical migrations (e.g.,
ctenophores; Hirota 1974) could subject
planktonic fish embryos to different levels of pre-
dation over a diurnal cycle. Synchronizing daily
spawning time to coincide with a period of low fish
embryo predation minimizes fish embryo mortal-
ity due to predation. If a fish embryo predator had
a diurnal predation cycle of 12 h high and 12 h low
predation. Figure 3 shows that a fish spawning at
the beginning of a low predation period ensures
50% or more of the embryo incubation time of its
progeny will be spent at the low predation level.
Qualitatively the results would be the same if
changes in predation were gradual and periods of
high and low predation were of different dura-
tions. Figure 3 also shows that if predation cycles
cause diel spawning periodicity, selection for diel
spawning periodicity is potentially greater when
embryo incubation times are short.

PREDAT I ON

100

X 50

0 24 48 72 96 120 144 168

INCUBATION TIME (h)

FIGURE 3.— Relationship between percentage of time spent at
low predation when spawning occurs at the beginning of a period
of low predation and total incubation time of embryos, assuming
12 h alternating periods of low (L) and high (H) predation.

461

FISHERY BULLETIN: VOL. 78, NO. 2

The physiological or adaptive cause(s) of diel
spawning periodicity in fishes may become clear
as data on its occurrence accumulates or by exper-
iments. Effects of natural maximum solar radia-
tion at the sea surface on different development
stages of marine planktonic fish embryos should
be studied experimentally. Field studies on fish
embryo mortality at different times of day, and
studies on feeding patterns of major fish embryo
predators and adult fish predators during the
spawning season could help elucidate or eliminate
some of the factors suspected of causing diel
spawning periodicity. If correct, one of the implicit
consequences of the diurnal predation cycle
hypothesis is that diel spawning periodicity
should be more common in fishes with short em-
bryo incubation times (Figure 3), and this predic-
tion should be tested. Additional data on diel
spawning periodicity in fishes and studies such as
those listed above should ultimately provide im-
portant insights into fish physiology, reproductive
biology, and ecology.

ACKNOWLEDGMENTS

I thank Kathy Schweyer and William Medeiros
for assisting in the laboratory and field work, and
Frederick G. Roberts of the Marine Sciences Re-
search Center, State University of New York at
Stony Brook, for providing research vessels. I also
thank John L. McHugh, Marine Sciences Research
Center, State University of New York at Stony
Brook, and George Boehlert, Virginia Institute of
Marine Science, for reviewing an earlier draft of
the manuscript, and Fishery Bulletin reviewers
for their criticism of the manuscript. Special
thanks to George C. Williams, State University of
New York at Stony Brook, for reviewing the man-
uscript and for assistance and support throughout
the research.

Research for this paper was financially sup-
ported in part by NOAA, Sea Grant Project
2-35281 to G. C. Williams, and by Grant-In-Aid
and University Awards from the State University
of New York at Stony Brook Research Foundation,
and 1977 and 1978 summer Biomedical Research
Grants to the author.

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464

AN IMPROVED METHOD TO ANALYZE TRIMETHYLAMINE IN
FISH AND THE INTERFERENCE OF AMMONIA AND DIMETHYLAMINE

Fern A. Bullard and Jeff Collins*

ABSTRACT

The trimethylamine content of most marine fish, especially the gadoid species, is internationally
accepted as an index of spoilage. However, ammonia, dimethylamine, and other amines also contribute
to the trimethylamine value. Variations in the conditions of the three current methods used to analyze
for trimethylamine content were studied in detail to determine the best condition to extract
trimethylamine and to reduce the extraction of ammonia, dimethylamine, and other amines.
Formaldehyde does not inhibit the interference from ammonia but the interference is negligible even
in advanced spoilage. Formaldehyde inhibits the interference from dimethylamine to some extent if
KOH is used as the base but increases the interference in the KjCOg method. The extraction of di- and
trimethylamine are highly dependent upon the base used and the temperature of extraction. A new
method of extracting at - 15° C using 45% KOH was developed that essentially eliminates interference
from ammonia, dimethylamine, and other amines. To directly compare the methods, the trimethyl-
amine content of a sample of spoiled walleye pollock, Theragra chalcogramma , flesh was determined
by the three currently used methods and the cold method of extraction. All methods gave similar
standard deviations but the K2CO3 method gave higher values than the KOH methods and the cold
method gave the lowest value. Various levels of trimethylamine and dimethylamine simulating
different qualities of fish and frozen storage times were added to samples of Pacific cod, Gadus
macrocephalus, Q.esh.. The cold method consistently extracts more accurate amounts of trimethylamine
with less interference from dimethylamine than any of the other extraction methods.

The trimethylamine (TMAl content of most ma-
rine fish, especially the gadoid species, is accepted
internationally as an index of spoilage. Dyer's
1959 method of analysis for TMA, except for the
concentration of formaldehyde (FA), has been
adopted by the Association of Official Analytical
Chemists (Horwitz 1975). Trimethylamine is pro-
duced by the reduction of trimethylamine oxide by
microorganisms (Poller and Linneweh 1926).
Ammonia, dimethylamine (DMA), and other vol-
atile bases are also formed when fish spoil and to
some extent interfere with the measurement of
TMA. In advanced spoilage, some of the higher
aliphatic amines are formed by decarboxylation of
amino acids and may cause interference (Dyer
1945).

A number of investigators studied the TMA
method to improve the accuracy and reduce the
effects of ammonia, DMA, and other amines. Dyer
(1945) adapted the method of determining amines
to fish and used 0.02% picric acid in dry toluene
instead of chloroform (Richter 1938; Richter et al.
1941). Dyer and Mounsey (1945) used a trichloro-

'Northwest and Alaska Fisheries Center Kodiak Investiga-
tions-Utilization, National Marine Fisheries Service, NOAA,
PO. Box 1638, Kodiak, AK 99615.

acetic acid (TCA) extract of fresh cod instead of the
unstable press juice or weighed samples. Hashi-
moto and Okaichi ( 1957) claimed that variation of
temperature caused serious errors in the determi-
nation of TMA, and recommended a 30° C extrac-
tion with 257r KOH rather than 50% K-^COa and
room temperature. Tozawa et al. ( 1971 ) confirmed
these findings and showed that 25% KOH reduced
the interference caused by DMA and claimed the
formation of a compound from FA and DMA which
was not extracted in the presence of hydroxide
ions. Murray and Gibson (1972) found that 45%
KOH extracted more TMA and gave more linear
and reproducible results than if extracted with
25% KOH or 50% K^COg.

The three current methods of analysis for TMA
employ 25% KOH, 45% KOH, or 50% K2CO3 to
release TMA for extraction into the toluene layer
and result in different absorbancies for the picrate
color with DMA and TMA. In general, the use of
K2CO3 results in a higher extraction of DMA and a
lower extraction of TMA than if KOH were used.
Ideally, the best method to measure TMA content
should result in complete extraction of TMA and
zero extraction of ammonia (NH3), DMA, and
other amines so that these components will not
contribute to the TMA value. A new method was

Manuscript accepted December 1979.
FISHERY BULLETIN; VOL. 78, NO. 2, 1980.

465

developed from information obtained from a de-
tailed study of how temperature, type and concen-
tration of base, and the presence (or not) of FA
affect the extraction and subsequent absorbancies
of the picrate color of NH3, DMA, and TMA.

EXPERIMENTAL

Purification Procedures

Trimethylamine hydrochloride (TMA ■ HCl) and
dimethylamine hydrochloride (DMA HCl) were
crystallized twice from hot 2-propanol and dried
under high vacuum overnight. Reagent grade and
previously used toluene was purified by shaking
and partitioning with concentrated sulfuric acid
in a separatory funnel followed by water, sodium
hydroxide, and water; filtering through anhydrous
sodium sulfate (NA2SO4); and distilling at 110° C.
Reagent grade Formalin^ (37% FA) was shaken
with magnesium carbonate, filtered, and diluted
1:9 with water Hexamethylenetetramine (HMTA)
from Pfaltz and Bauer was crystallized twice from
hot 2-propanol or from hot, dry toluene and dried
overnight under high vacuum. N N N'N'-
tetramethylmethanediamine (TMMD) from
Pfaltz and Bauer was distilled using a column
packed with glass helices. The first 25 ml fraction
(72°-81° C) was discarded, the next 25 ml fraction
(81° C) was used for analysis, and the final 25 ml
distillate was discarded. Reagent grade ammoni-
um chloride (NH4CI) was crystallized twice from
hot water and dried under high vacuum overnight.

Extraction Procedure for Fish Flesh

Procedures cited in the literature for the extrac-
tion of fish have used a specific amount of flesh
plus water or TCA followed by shaking or blend-
ing and filtration. These methods assume a speci-
fic moisture content of the fiesh, a total volume,
and a complete extraction or uniform dispersion
of TMA in the extract, e.g., 100 g flesh at
SO^f moisture plus 300 ml TCA solution would
give a 1/95 aliquot for a 4 ml sample. To improve
accuracy of the method, we used an exhaustive
extraction-filtration procedure and dilution to a
volume. Details of the procedure are given in the
Recommended Procedures section.

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

FISHERY BULLETIN: VOL. 78, NO. 2

Methods of Analyses for TMA

Unless otherwise indicated, the three common-
ly used methods of analyses for TMA were modi-
fied slightly to fit our equipment and to reflect
recent advances in the methods. The methods of
Dyer (1945), Tozawa et al. (1971), and Murray and
Gibson (1972) were used as follows: a 4 ml sample
of a standard solution in 57f TCA or a 5% TCA
extract of fish flesh was added to a 25 x 150 mm
screw top test tube, followed by the addition of 10
ml toluene, 1 ml of 3.79?^ FA solution, and left to
stand 5 min before the addition of 3 ml of base
(25% KOH, 45% KOH, or 50% K2CO3). The tube
was tightly sealed using a gasket of a double layer
of 1 mil polyethylene film under the cap and
shaken for 15 min at room temperature on a
Burrell wrist action shaker modified by building-
up the platform 20.3 cm with Styrofoam. After
standing several minutes, about 7 ml of the
toluene layer were removed and dried with 0.5 g
anhydrous NagSO^. After drying, 5 ml were added
to 5 ml of 0.02% picric acid in dry toluene and the
absorbance was determined at 415 nm on a
Gilford modified Beckman D.U. spectrophotome-
ter. A fourth method will be referred to as the "cold
method" of extraction and uses 45% KOH (Murray
and Gibson 1972) but the extraction is done at -15°
C. The details of this method are given in the
section on Recommended Procedures.

Standard Curves

Since four distinctly different methods were
used to analyze for TMA content, complete blank
determinations and standard curves were made
for each method. The equations for the regression
lines (standard curves) of absorbance on concen-
tration of TMA (micrograms TMA- N/milliliter)
for each of the methods were as follows:

25% KOH, room temperature Y = O.OllX - 0.007 (1)

45% KOH, room temperature Y = G.OSTX - 0.001 (2)

50% K2CO3, room temperature Y = 0.067X - 0.012 (3)

45% KOH, cold ( - 15° C) Y = 0.082X - 0.007 (4)

where Y = absorbance and X = micrograms TMA-
N/milliliter.

The trimethylamine values in milligrams TMA-
N/100 g flesh were calculated from these equa-
tions and from the total volume (250 ml) of 5%
TCA extract, weight of extracted fish flesh (75 g), 4
ml of sample extract per tube, and a dilution factor

466

BULLARD and COLLINS: IMPROVED METHOD TO ANALYZE TRIMETHYLAMINE

(K), if present (e.g., for the cold method use
Equation (4)):

(A + 0.007)(250 ml)( lOOHK) .,, .
= milligrams

(0.082X75 g fleshH 1,000 ^g/mg) TMA-N/100 g flesh. (5)

RESULTS AND DISCUSSION

In the following sections, the influence of the
presence of FA (or not), the type and concentration
of base used, and temperature of extraction were
determined separately on each component in the
reaction and extraction mixture; i.e., 1) NHg and
HMTA, 2) DMA and TMMD, and 3) TMA. The four
methods were directly compared for precision by
replicate analyses of a composite sample of minced
fish flesh. Finally, accuracy (recovery of TMA and
the interference of DMA) was determined for the
four methods by direct addition of known quan-
tities of TMA and DMA.

Reaction of Ammonia

Sprung (1940) reported that FA reacts with NH3
to form HMTA. Under vacuum distillation condi-
tions at 30° C, the addition of FA to solutions of
NH4CI and NaaCOs rendered the NH3 nonvolatile
but in the absence of FA, NH3 was volatile (Benoit
and Norris 1942). Dyer (1945) claimed that the
addition of 1 or 2 ml of 49c FA did not affect the
recovery of TMA, and was sufficient to eliminate
the interference of NH3 up to 10-20 times over the
usual concentration of trimethylamine nitrogen.
Dyer, however, did not directly study the influ-
ence of FA on the development of the picric acid
color in the presence of NH3 . Researchers studying
the TMA method have followed the prior proce-
dures and used FA to tie up NH3 in the TMA test.

Standard solutions of NH4CI in 5% TCA were
prepared and used in the three TMA methods. To
simulate various stages of spoilage the concentra-
tion ranged from 6.6 to 66 /xg N/ml; i.e., 2.2-22.0
mg N/100 g flesh. The absorbancies from the
NH^^Cl solutions with and without FA (Table 1,
columns 1-6) were low and of questionable signifi-
cance except if 45% KOH was used. The absorban-
cies seemed to increase with concentration of
NH4CI and were about the same whether FA were
present or not if 50% K2CO3 and 25% KOH were
used. Even at the higher concentrations, the
absorbancies were low and would contribute little
to the TMA value. When 45% KOH was used, the
absorbancies were much higher than the absor-
bancies with the other bases and were not affected
by FA except at the higher concentrations. Accord-
ingly, FA and NH3 did not react under these
conditions and NH3 could contribute to the TMA
value. To determine if FA would react with NH3 at
elevated temperatures, the same standard solu-
tions in 5% TCA were treated as before but were
preheated in the presence of FA at 60° C for 30
min, cooled to room temperature, and 45% KOH
added and extracted in the usual way. The absor-
bancies of the preheated samples were reduced
significantly — see columns 5 and 7 in Table 1. The
low absorbancies indicated that FA reacted with
NH4CI when heated and there was no interference
through 26.4 (xg N/ml sample. The color develop-
ment in the samples containing 33.0 /xg N/ml and
more could be caused by: 1) residual NHg through
an incomplete reaction with FA, 2) NH3 through a
reverse reaction of the product which is assumed
to be HMTA, by the law of mass action or chemical
equilibrium, and 3) a partial extraction of HMTA
by toluene and subsequent reaction with picric
acid.

Table 1. — Ammonium chloride or hexamethylenetetramine (HMTA): the absorbancies of picrates in
the trimethylamine test as affected by the addition of standard solutions of ammonium chloride or
hexamethylenetetramine. Samples (columns 1-10) were extracted at room temperature for 15 min
(except 9 and 10 which were extracted at -15° C for 60 s by hand), with formaldehyde ( +) and without
formaldehyde (0).

NH4CI

NH4CI

NH4CI

NH4CI

NH4CI;HMTA

NH4CI

or

50%

K2CO3

25%

KOH

45%

KOH

45%

KOH

45%

KOH

HMTA

1

2

3

4

5

6

7'

8

9

10

(MgN/ml)

+

0

+

0

+

0

+

0

+

0

6.6

0.008

0.000

0.001

0.001

0.008

0.005

0.000

0.012

0.003

0.004

13.2

.012

.000

001

.005

.024

.015

.000

.012

.013

.006

16.5

.012

.000

.001

.011

.029

.018

.000

.023

.016

.008

26.4

.016

.004

.010

.011

.027

.028

.000

.027

.017

.008

33.0

.004

008

.000

.014

.042

.049

.023

.032

.019

.016

52.8

.012

.019

.010

.027

066

.095

.019

.042

.022

.034

66.0

.020

.027

oil

.039

.072

.119

.044

.045

.024

.043

'After addition of FA. samples were heated at 60' C for 30 min to allow FA and NH3 to react. Samples were then cooled, base
added, and extracted at room temperature.

467

FISHERY BULLETIN: VOL. 78, NO. 2

To determine if HMTA would react with picric
acid, purified HMTA in dry toluene was added to
the picric acid reagent. A strong color developed
which indicated that HMTA reacted with picric
acid. To determine if HMTA would be extracted
under the standard conditions of the TMA test
using 45% KOH, standard solutions of HMTA
were prepared and used in the same manner as
NH^Cl solutions. The absorbancies for the HMTA
samples (Table 1, column 8) were similar to the
absorbancies of the samples represented by col-
umns 5 and 7 of Table 1. Further, the absorbancies
for HMTA samples were not 0 as would be expect-
ed from the literature and indicated that either
HMTA was extracted by toluene and reacted with
picric acid or a partial reverse reaction occurred
and NH3 was extracted and reacted with picric
acid. Whether the picrate color was caused by NH3
or by HMTA, FA did not eliminate the interfer-
ence of NHj when 45% KOH was used. Formalde-
hyde gave some protection, however, if the reac-
tion mixture was heated at 60° C for 30 min prior
to the addition of 45% KOH.

Since NH.j or HMTA was extracted by toluene
at room temperature and reacted with picric acid,
NH3 was extracted at a low temperature to see if
the interference could be reduced. The same stan-
dard solutions of NH4CI were treated as before but
were extracted by the cold method. The data given
in columns 9 and 10 of Table 1 showed that the
absorbancies were at the same general level as the
preheated samples and the presence of FA had
little effect on absorbance. We conclude that 45%
KOH was less effective in releasing NHg at -15° C
than at room temperature (Table 1, compare col-
umns 5 with 9, 6 with 10) or NH3 was less
extractable by toluene at -15° C. Although other
researchers have used FA to eliminate the inter-
ference of NH3, our data showed that FA does not
tie up NH3 under the usual conditions in the
analysis for TMA. On practical grounds, the

Table 2. — Dimethylamine hydrochloride: the absorbancies of
picrates in the trimethylamine test as affected by the three bases
used and temperature of extraction. Samples were extracted for
60 s with vigorous hand shaking using 4 ml 15.9 fxg DMA-N/ml,
with formaldehyde ( +) and without formaldehyde (0).

25% KOH

45% KOH

50% K2CO3

Temperature

3 of

1

2

3

4

5

6

extraction (°C)

+

0

+

0

+

0

-15

0.015

0.067

0.015

0.605

0.119

0.000

0

.016

.130

.031

.657

.200

.000

6

.024

.208

.053

.721

.251

.007

22

,062

.310

.157

.774

.327

.037

30

.079

.371

.361

.967

.453

.088

contribution of NK, to the TMA value would be
quite low because the bases (except 45% KOH)
released only a small amount of NH3 or NH3 was
only slightly extracted by toluene. Even in ad-
vanced spoilage such as 22 mg NH.j-N/100 g flesh
(66 ixg N/ml), the contribution of NH3 to the TMA
value would be equivalent to 0.45 mg TMA-N/100
g flesh if extracted at room temperature with 45%
KOH but only 0.10 mg TMA-N/100 g flesh if
determined by the cold method.

Reaction of DMA

Several researchers have found that DMA and
TMA are not completely extracted by toluene
under conditions used in the TMA test unless
replicate extractions are made (Castell et al.
1974). Further, different bases resulted in differ-
ent extractabilities of DMA. Accordingly, we de-
termined the absorbancies of the picrate color
using a standard solution of DMA (15.9 /xg DMA-
N/ml; i.e., 5.3 mg DMA-N/100 g flesh) under
various conditions of the TMA test; temperature,
base (KjCOg and KOH), replicate extraction, and
presence or absence of FA.

A standard solution of DMAHCl in 5% TCA
was extracted with and without FA by the usual
methods but the temperature of extraction was
varied (-15° C to +30° C) and the tubes were
vigorously shaken by hand for 60 s. The extraction
of DMA was strongly influenced by the base and
by temperature (Table 2). In the absence of FA, the
differences in reactivity of the bases in releasing
DMA from the hydrochloride salt are shown in
columns 2, 4, and 6 (Table 2). At -15° C, 45% KOH
released about half of the DMA present, 25% KOH
released l/20th, and K2CO3 was unreactive and
did not release DMA. The bases were more reac-
tive at higher temperatures than at lower temper-
atures but had the same order of reactivity. The
date also showed that, if released from the salt,
DMA was extracted by toluene even at low tem-
peratures. When FA was present however, a
different order of release was evident (Table 2,
columns 1, 3, and 5) and showed that FA reacted
with DMA to give a product having different
reactivity with the bases. The order of release (or
extractability) for the product was different than
for DMA, i.e., high absorbance with K2CO3, in-
termediate with 45% KOH, and low with 25%
KOH. Considerable amounts of the product were
extracted in the presence of FA at all tempera-
tures in the carbonate system and would result in

468

BULLARD and COLLINS: IMPROVED METHOD TO ANALYZE TRIMETHYLAMINE

a contribution by DMA of 1.69 mg N/100 g flesh to
the TMA value at 22° C. In frozen flesh of gadoid
fish, the DMA content might be high relative to
TMA and would result in a substantial error in the
TMA value unless determined at low tempera-
tures with KOH where DMA would contribute 0.1
mg N or less.

We next studied the effects of the three bases
and the presence or absence of FA on the total
extractability of DMA. Similar extractions were
performed by Castell et al. (1974) but these au-
thors only considered the carbonate system with
FA present. The same DMA solutions (15.9 /xg
DMA-N/ml) with or without FA were extracted as
before but at room temperature for 15 min, i.e., 4
ml DMA solution, 10 ml toluene, 1 ml FA (or not),
and 3 ml base. After removing about 7 ml toluene
for drying and reacting with picric acid, the
remainder of the toluene layer was carefully
aspirated off, 10 ml toluene added, and reextract-
ed. This process was repeated for a total of six
extractions. In the absence of FA, DMA was
released rapidly from the salt by 45% KOH, about
half as fast by 25% KOH, and slowly by 50%
K2CO3 (Table 3). If FA were present however,
many extractions would be required to extract all
of the DMA which, in agreement with Sprung
(1940), showed that FA reacted with DMA to give
TMMD. The data further showed that TMMD was
relatively soluble in toluene but the extractabili-
ties were different because each base had a differ-
ent rate of reaction with TMMD, i.e., a rapid
release of TMMD with K2CO3 and slow with 25%
KOH. The possibility of each base having a
different salting-out effect was eliminated when
equal absorbancies were obtained if the same
extractions were made with the addition of 0.5 g
KCl (data not given).

The data also showed that in the carbonate
method TMMD was released to the toluene phase

more rapidly than DMA and explains the known
interference of DMA in the presence of FA by the
Dyer (1945) method. Formaldehyde might best be
left out in the 50% K2CO3 method. The lower
picrate color absorbancies in the KOH systems
with FA present might also be explained by the
law of mass action (equilibrium) as was done in
the section on NH3. In the equilibrium (FA + DMA
^TMMD) the concentrations of FA, DMA, and
TMMD in the aqueous phase are dependent on the
type and concentration of base. The products (FA
and DMA) of the hydrolysis of TMMD would be
formed at a rate dependent upon these same
variables and DMA would be rapidly removed
from the aqueous phase in the KOH systems
because of the rapid extraction of DMA by toluene.
Since the absorbancies in the KOH systems were
relatively low in the presence of FA, the concen-
tration of DMA from the hydrolysis of TMMD
must have been low. In the carbonate system
however, DMA from TMMD was slowly released
from the aqueous phase into the toluene layer.
Apparently a low concentration of DMA existed in
the equilibrium formed in the carbonate sy.stem
and favored the extraction of TMMD by toluene. It
is likely that both TMMD and DMA were extract-
ed by toluene at rates that depend on the base and
temperature used.

To further study the extraction of TMMD, the
same multiple extractions described for DMA
were made using purified TMMD in 5% TCA but
at a slightly lower concentration 115.0 /xg TMMD-
N/ml). The absorbancies of the TMMD-picrates
(Table 4) were nearly the same as the absorban-
cies of the DMA-picrates (Table 3). The similarity
of data between DMA and TMMD inferred again
that FA and DMA react to give TMMD. The
addition of FA forced the reaction toward TMMD
where the type and concentration of base con-

TaBLE 3. — Dimethylamine hydrochloride: the absorbancies of
picrates in multiple extractions in the trimethylamine test as
affected by the three bases used. Samples were extracted for 15
min at room temperature using 4 ml 15.9 ng DMA-N/ml, with
formaldehyde ( + ) and without formaldehyde (0).

Table 4.— N N N'N'-tetramethylmethanediamine: the ab-
sorbancies of picrates in multiple extractions in the trimethyl-
amine test as affected by the three bases used. Samples were
extracted for 15 min at room temperature using 4 ml 15.0 /ig
TMMD-N/ml, with formaldehyde 1+) and without formalde-
hyde (0).

25%

KOH

45%

KOH

50% K2CO3

25% KOH

45% KOH

50% K2C03

Extraction

1

2

3

4

5

6

Extraction

1

2

3

4

5

6

number

+

0

+

0

+

0

number

+

0

+

0

+

0

1

0.064

0.416

0.184

1.022

0.498

0.03

1

0.051

0.308

0.193

0.882

0.417

0.041

2

.042

.175

.160

.204

.273

.02

2

.038

.198

.160

.180

.277

041

3

.049

.125

.149

.017

.195

.01

3

.046

.123

.142

.028

.185

.044

4

.040

.057

.114

.000

114

.02

4

.036

067

.122

.002

.126

.048

5

.049

.036

.117

.000

.074

.02

5

.039

.031

.090

.000

.081

.028

6

.049

.015

.092

000

.051

.02

6

.046

.022.

.073

.000

.059

.025

469

FISHERY BULLETIN: VOL. 78, NO. 2

trolled the degree of retention of TMMD in the
aqueous phase or its release to the toluene phase.
The use of 1 ml 3.7% FA and 4 ml 15.9 fxg DMA-
N/ml results in a large excess of FA, about 500
times over that required (1 FA to 2 DMA). Conse-
quently, in the absence of added FA where only
the stoichiometric amount of FA was present from
TMMD, an equilibrium was established in the
KOH systems that favored the formation of DMA
and its rapid extraction by toluene. A different
equilibrium was formed in the K2CO3 system that
favored the release of TMMD and extraction by
toluene.

Extraction of TMA

The extraction of TMA under various conditions
of base, temperature, and FA was examined. A
standard solution of TMA ■ HCl in 5% TCA was
prepared (15.9 AAgTMA-N/ml, i.e., 5.3 mg TMA-N/
100 g). This concentration was chosen as it is near
the point of unacceptable quality for fish. In the
carbonate method (Table 5), the extraction of
TMA was highly dependent upon temperature
and would result in a lack of precision unless the
temperature was controlled as suggested by Hashi-
moto and Okaichi (1957). Absorbancies were not
as dependent upon temperature in the 25% KOH
method as with K2CO3 and were nearly indepen-
dent of temperature with 45% KOH. The slightly
lower absorbancies with FA present than if not
present might be caused by an impurity of DMA or
an interference from FA even though FA would
not be expected to react with a tertiary amine. As
stated in the section on DMA, FA might best be
left out in the carbonate method, i.e., only 10% less
TMA was extracted than was extracted in the 45%
KOH method.

To determine the conditions for maximum ex-
tractions of TMA, the same multiple extractions

Table 5. — Trimethylamine hydrochloride: the absorbancies of
picrates in the trimethylamine test as affected by the three bases
used and temperature of extraction. Samples were extracted for
60 s with vigorous hand shaking using 4 ml of 15.9 /xg TMA-N/ml,
with formaldehyde ( + ) and without formaldehyde (0).

Table 6. — Trimethylamine hydrochloride: the absorbancies of
picrates in multiple extractions in the trimethylamine test as
affected by the three bases used. Samples were extracted for 15
min at room temperature using 4 ml 15.9 /ng TMA-N/ml, with
formaldehyde ( +) and without formaldehyde (0).

25% KOH

45%

KOH

50% K2CO3

Temperature of
extraction (°C)

1
+

2

0

3

+

4
0

5

+

6
0

-17

0.685

0.854

1.312

1.402

0.286

0.682

0

.921

1.099

1.366

1.412

.630

1.027

6

1.050

1.138

1.378

1.391

.722

1.095

21

1.136

1.235

1.373

1.350

1.013

1.218

30

1.198

1.269

1.408

1.420

1.150

1.303

25%

KOH

45%

KOH

50% K2C03

Extraction

1

2

3

4

5

6

number

+

0

+

0

+

0

1

1.113

1.223

1.384

1.403

0987

1.245

2

.233

.159

.050

.033

.282

.130

3

.044

.020

.000

.001

.079

.009

4

.003

.005

.000

.000

.016

.003

were done as with DMA. In the 45% KOH test
(Table 6), 97% of the TMA was removed in the first
extraction and the remainder was removed in the
second extraction. The first, second, and third
extractions removed 80, 17, and 3% with 25% KOH
and removed 72, 21, and 6% with 50% K2CO3.
Standard curves are assumed to compensate for
constant experimental errors such as slightly less
than 100% extraction of TMA, but the reliability of
the data would be questionable with the low
recoveries reported here for 25% KOH and 50%
K2CO3. Neither do standard curves compensate
for variable errors such as the observed strong
dependence on temperature of the extraction of
TMA in the 25% KOH and 50% K2CO3 methods
(Table 5).

Comparative Analyses Using Fish Flesh

Walleye pollock, Theragra chalcogramma, were
held in slush-ice for 9 d and filleted. Twelve
separate TCA extractions were made on a compos-
ite sample of the ground flesh. Each extract was
analyzed in duplicate by each of the three TMA
methods and the cold method. Portions of the
extracts were neutralized and analyzed for DMA
by Dowden's 1938 method, modified slightly by
increasing the time of extraction to 15 min on the
modified mechanical shaker.

All methods (Table 7) resulted in similar stan-
dard deviations but the TMA values were higher
in the K2CO3 method than in the KOH methods
and the cold method of extraction gave the lowest
value. The absorbancy data at 22° C of Table 2 can
be used to approximate the degree of contribution
of DMA to the TMA values in Table 7. The flesh
contained 2.25 mg DMA-N/100 g (6.75 /^g/ml)
and would contribute different amounts to the
TMA value according to the method of analysis
employed. The data of Table 2 for K2CO3 (0.327 A
at 22° C using 15.9 ^ig DMA-N/ml) are equivalent

470

BULLARD and COLLINS: IMPROVED METHOD TO ANALYZE TRIMETHYLAMINE

Table 7.— Trimethylamine content in mg TMA-N/100 g flesh
from 9-d-old walleye pollock using four methods of analysis.

Extract
number

Room temperature extraction

-15° C extraction

25% KOH

45% KOH

50°/o K2CO3

45% KOH

1

9.52

984

10.42

9.18

2

9.73

9,76

10,27

9.14

3

9.55

9.78

1018

9.08

4

9.66

10.01

10.28

8.84

5

9.53

992

10 34

8.84

6

9.69

10.07

10.25

9.10

7

9.51

9.93

10,39

9.28

8

9.56

9.78

10,28

8.97

9

9.49

982

10,22

9.18

10

965

9.79

10,21

8.91

11

9.65

9.75

10,22

9.11

12

9.55

982

10,39

9.11

Mean

9.59

9.85

10,29

9.06

SO

.08

.10

.08

.14

to 0.139 A for 6.75 ^g DMA-N/ml by a simple ratio,
i.e., 0.327A/(15.9 ixg DMA-N/ml):X/(6.75 /xg
DMA-N/ml). An equivalent TM A value was calcu-
lated to be 0.75 mg TMA-N/100 g flesh from Equa-
tions (3) and (5). If corrected for DMA, the TMA
value from Table 71X2003) would be 10.29 - 0.75
= 9.54 mg TMA-N/100 g flesh. Similar calcula-
tions for the 25 and 45'7f KOH methods gave cor-
rected values of 9.45 and 9.59 mg TMA-N/100 g
flesh. The small contribution of DMA at -15°C
(0.015 A ) would be 0.05 mg TMA-N/100 g flesh and
give a corrected value of 9.01 for the cold method.
The TMA values obtained by the three methods of
analysis were in good agreement if corrected for
DMA. The cold method of extraction gave slightly
lower and more accurate values than the other
methods. Cold extraction reduced the release and
extractability of numerous other interfering sub-
stances discussed by Dyer (1945).

Extraction of Fish Flesh with
Added TMA and DMA

To determine the recovery of TMA and the
interference of DMA, varying amounts of both
were added to blended flesh of Pacific cod, Gadus
macrocephalus , extracted with TCA in the usual
way and analyzed for TMA content by four meth-
ods. The sample of flesh contained 3.25 mg DMA-
N/100 g by Dowden's method (1938). The amount
of amine added, the resulting TMA value, and the
percentage of the theoretical value (recovery) by
each method of analysis are given in Table 8. The
TMA values of cod flesh with added TMA (3, 6, 9,
and 12 mg) resulted in similar recoveries of TMA
by all methods. If 5, 15, 30, and 50 mg DMA were
added to the blended flesh, however, the TMA
values were unacceptably high by the 50*7^ K2CO3,
25^/c KOH, and 45% KOH methods. The cold
method gave acceptable values although the addi-
tion of 50 mg DMA-N increased the TMA value
from 1.59 to 2.12, i.e., 133% of theory If the same
quantities of DMA were added plus a small
amount of TMA (3 mg), only the cold method gave
acceptable TMA values. The other methods were
strongly influenced by the presence of DMA.
However, if larger amounts of TMA were added
(12 mg), along with DMA, the influence of DMA
was reduced considerably and the 25% KOH and
cold methods gave acceptable results.

All methods gave about equal recovery of added
TMA provided the DMA content was low. Tri-
methylamine values by the three published meth-
ods were strongly influenced by the relative

Table 8. — Trimethylamine values In mg TMA-N/100 g flesh of Pacific cod as affected by different methods of
analysis when varying amounts of the TMA- HCl and DMA- HCl salts were added to the flesh before extracting
with TCA.

Levels of TMA
and DMA added

Sample, as is

SmgTMA

6 mg TMA

9mgTMA

12mgTMA

5 mg DMA

1 5 mg DMA

30 mg DMA

50 mg DMA

3mgTMA
3 mg TMA +
3mgTMA
3 mgTMA +

12mgTMA
12mgTMA
12mgTMA +
12mgTMA

5 mg DMA
15mg DMA
30 mg DMA
50 mg DMA

5 mg DMA
15mgDMA
30 mg DMA
50 mg DMA

25%

KOH

45%

KOH

50%

K2CO3

Cold method

TMA-N

Recovery

TMA-N

Recovery

TMA-N

Recovery

TMA-N

Recovery

(mg)

(%)

(mg)

(%)

(mg)

(%)

(mg)

(%)

1.65

1.94

2.36

1.59

4.81

103

5.17

105

4.89

91

4.81

105

7.34

96

8.28

104

739

88

8.12

107

11.62

109

10.71

98

11.39

100

11.32

107

13.94

102

15.23

109

17.04

119

14.90

110

2.00

121

2.83

146

3.79

161

1.72

108

2.47

150

4.24

219

6.32

268

1.77

111

3.18

193

5.89

304

10.16

431

1.89

119

3,83

232

8.09

417

14.46

613

2.12

133

5.21

112

6.14

124

6.84

128

4.60

100

5.70

123

7.59

154

9.25

173

4.81

105

6.35

137

9.74

197

11.87

221

4.97

108

7.78

167

13.10

265

16.35

305

4.98

108

14.48

106

16.42

118

19.39

135

15.24

112

14.88

109

16.71

120

1983

138

15.34

113

14.93

109

17.90

128

21.17

147

15.16

112

15.79

116

19.72

141

24.27

169

15.19

112

471

FISHERY BULLETIN: VOL. 78, NO. 2

amounts of TMA and DMA in the sample. Only
the cold method gave TMA values that were
nearly independent of the DMA content of all
levels of DMA and TMA. If methods other than the
cold method are used to analyze for TMA, the
history of the fish and sample storage should be
known or the DMA content should be determined
separately.

RECOMMENDED PROCEDURES

Extraction Procedure for Fish Flesh

Blend a thoroughly mixed composite sample of
fish flesh (75 g) with 90 ml of 8.27^ (weight/volume)
TCA for 5 min at high speed in a Vertis blender.
Pour contents of blender jar into a 150 ml medium
porosity sintered glass funnel and filter under
vacuum. To prevent foaming and plugging of
filter, clamp off the suction line after filtering
starts and briefly open when required. Reextract
residue with 70 ml of 59^ TCA for 2 min and filter
into the same filter flask and rinse with 5% TCA
from a wash bottle. Quantitatively transfer the
combined filtrates and washings to a 250 ml
volumetric flask and dilute to the mark with 59c
TCA. The extract (4 ml) is used in the TMA
analysis without dilution but, if required, 4 ml of a
diluted extract is used rather than smaller vol-
umes of extract.

Cold Method of Analysis for TMA

Add 4 ml samples of standard solutions of
TMAHCl in 5% TCA or 57c TCA extracts, 10 ml
toluene, and 1 ml of 3.77f FA to 25 x 150 mm screw
top test tubes. Allow to stand for 5 min then place
tubes in an ice- water bath in an effort to avoid the
possible yellow color caused by the addition of
concentrated KOH (Castell et al. 1974). When
completely chilled, add 3 ml 45*^ KOH and tightly
seal tubes, invert twice, and place in a mixture of
salt and precooled saturated brine-ice at -15° C.
Use a pump or stirring motor to maintain constant
temperature by circulating the brine through the
salt, brine-ice mixture. After 2 min, remove the
test tubes and shake vigorously by hand for 15 s
and replace in the cold bath for 2 min. Repeat this
procedure three times for a total of 60 s of vigorous
hand shaking. After settling ( almost immediately),
transfer about 7 ml of the toluene layer to clean
dry 18 x 150 mm test tubes and dry with about 0.5
g anhydrous Na2S04 by swirling (Vortex Mixer).

After drying, remove 5 ml and add to 5 ml of 0.02%
picric acid in dry toluene. Determine the absor-
bance at 415 nm using 1 cm standard silica cells
and a Gilford modified Beckman D.U. spectro-
photometer. Determine the blank in the same
manner but use 4 ml TCA. Calculate the TMA
content in mg TMA-N/100 g from the absorbance
and Equations (4) and (5).

SUMMARY

Although NH.j, DMA, and other amines contrib-
ute to the TMA value, the TMA content of some
marine fish, especially gadoid species, is accepted
internationally as an index of spoilage. Variations
in the conditions of the three methods used to
analyze for TMA were studied to determine the
best condition to extract TMA and to reduce the
extraction of HN3, DMA, and other amines. We
found that NHg was not tied up by FA as suggested
in the literature but has little affect on the TMA
value of fish even in advanced spoilage. The
amount of DMA extracted was strongly dependent
on the temperature of extraction, the base used,
and the presence or absence of FA. Formaldehyde
and DMA reacted to form a compound that was
rapidly extracted by 507c KaCOy and very slowly
by 25% KOH. If DMA and TMMD were extracted,
the absorbancies were nearly the same which
infers that the compound formed from FA and
DMA was TMMD. The amount of TMA extracted
was strongly dependent on the temperature of
extraction when 25% KOH or 50% K2CO3 was
used as the base but nearly independent when
45% KOH was used. A cold method of extraction
(45% KOH and -15° C) was developed that essen-
tially eliminated the contribution of DMA to the
TMA value. Trimethylamine was determined in
spoiled fish flesh by the cold method and the three
other methods. Standard deviations were similar
for all four methods. The KgCO^ method gave the
highest value and the cold method gave the lowest
value. If varying amounts of TMA and DMA were
added to Pacific cod flesh and analyzed by the
three published TMA methods, the recovery of
TMA and interference from DMA was strongly
influenced by the relative amounts of TMA and
DMA present. Relative to the other methods, the
cold method gave TMA values that were indepen-
dent of the presence of DMA or the relative
amounts of DMA and TMA. We recommend that
the cold method be used because it extracts most of
the TMA (97%), gives good recovery of added

472

BULLARD and COLLINS: IMPROVED METHOD TO ANALYZE TRI METHYL AMINE

TMA, is nearly independent of DMA content, and
is not affected by other amines or NHg.

LITERATURE CITED

BENOIT, G. J., JR., AND E. R. NORRIS.

1942. Effect of formaldehyde on the volatilizations of am-
monia, mono-, di-, and trimethylamines. Ind. Eng.
Chem., Anal. Ed, 14:823-825.

Castell, C. H., B. Smith, and W J. Dyer.

1974. Simultaneous measurements of trimethylamine and
dimethylamine in fish, and their use for estimating qual-
ity of frozen-stored gadoid fillets. J. Fish. Res. Board
Can. 31:383-389.
DOWDEN.H.C.

1938. The determination of small amounts of dimethyl-
amine in biological fluids. Biochem. J. 32:455-459.

Dyer, W J.

1945. Amines in fish muscle I. Colorimetric determination

of trimethylamine as the picrate salt. J. Fish. Res. Board

Can. 6:351-358.
1959. Report on trimethylamine in fish. J. Assoc. Off.

Agric. Chem. 42:292-294.
DYER, W. J., AND Y. A. MOUNSEY.

1945. Amines in fish muscle II. Development of

trimethylamine and other amines. J. Fish. Res. Board

Can. 6:359-367.
HASHIMOTO, Y, AND T. OKAICHI.

1957. On the determination of trimethylamine and

trimethylamine oxide. A modification of the Dyer
method. Bull. Jpn. Soc. Sci. Fish. 23:269-272.

H0RWITZ,W (editor).

1975. Official methods of analysis of the Association of
Official Analytical Chemists. 12th ed. Assoc. Off.
Anal. Chem., Wash., D.C., 1094 p.

MURRAY, C. K., AND D. M. GlB-SON.

1972. An investigation of the method of determining
trimethylamine in fish muscle extracts by the formation
of its picrate salt-Part I. J. Food Technol. 7:35-46.

POLLER, K., AND W LINNEWEH.

1926. Uber das Vorkommen von Trimethylamin-oxyd in
Clupea harengus. (The occurrence of trimethylamine
oxide in Clupea harengus.) Ber. Dtsch. Chem. Ges.
59:1362-1365.
RICHTER, D.

1938. Elimination of amines in man. Biochem. J.
32:1763-1769.
RiCHTER, D., M. H. LEE, AND D. HILL.

1941. The rate of removal of amines from the
blood. Biochem. J. 35:1225-1230.

Sprung, M. M.

1940. A summary of the reactions of aldehydes with

amines. Chem. Rev 26:297-338.
TOZAWA, H., K. ENOKIHARA, AND K. AMANO.

1971. Proposed modification of Dyer's method for

trimethylamine determination in cod fish. In Rudolf

Kreuzer (editor), Fish inspection and quality control, p.

187-190.

473

PERCENTAGE OF STARVING NORTHERN ANCHOVY,

ENGRAULIS MORDAX, LARVAE IN THE SEA AS

ESTIMATED BY HISTOLOGICAL METHODS

Charles P. O'Connelli

ABSTRACT

The proportion of starving larvae of northern anchovy, Engraulis mordax, was estimated for the
Southern California Bight in March 1977 from histological examination of larvae for 64 1 m net tow
samples. The number of larvae in the tows varied from 0 to about 400. Approximately 6 per tow were
sectioned and examined with the light microscope. Twenty-six specimens were identified as emaciated
from anomalies of the trunk musculature and digestive tract. Some of the emaciated larvae occurred as
isolated cases at widely scattered locations, but most were from a few nearshore tows, indicating
"patches" of starving larvae. Temperature and plankton volume data indicate that the patches were
associated with fluctuating environmental conditions. The samples indicate that about 8% of northern
anchovy larvae in the Southern California Bight were starving.

One of the goals in investigations of pelagic
fish stocks is that of predicting how large year
classes will be at the time they are recruited to the
fishery. One of the primary approaches to this
problem has been the estimation of larval mortal-
ity rates based on abundance estimates from egg
and larval surveys. While such surveys will prob-
ably continue to be the most reliable source of
information on abundance at early ages, the high
costs and time delays in processing samples are
reasons for seeking alternative approaches
(Hunter 1976b). Recently, Lasker (1975, in press)
has developed a promising index based on avail-
ability of food in concentrations suitable for survi-
val of early feeding stages of the northern anchovy,
Engraulis mordax.

This study reports another approach that could
provide an independent prediction of year class
strength for the northern anchovy; namely, esti-
mation by histological methods of the proportion
of larvae in the sea showing symptoms of starva-
tion. Since level of mortality in a population is
likely to be some function of the proportion of
larvae observed to be starving, the proportion, if
based on adequate sampling, could be an indicator
of ultimate year class success.

Condition factor (Blaxter 1971), chemical indi-
ces (Ehrlich 1974), morphometric analyses (Shel-
bourne 1957; Nakai et al. 1969; Ehrlich et al. 1976;

Theilacker 1978), and histological analyses
(Umeda and Ochiai 1975; O'Connell 1976;
Theilacker 1978) have all been used with some
success to chai'acterize the starving condition in
larvae of various marine species, in most cases
under controlled laboratory conditions. The his-
tological approach differs from the others in that
the criteria of starvation are based on qualitative
changes in the character of cells and tissues, not on
quantitative measurements. Histological criteria
developed earlier for northern anchovy larvae
starved in the laboratory (O'Connell 1976) were
the principal guidelines for evaluating the condi-
tion of ocean-caught larvae in this study.

METHODS

In March 1977, 64 net tows were taken over a
12-d period from the NOAA ship David Starr Jor-
dan to obtain northern anchovy larvae for his-
tological study. Almost half of the tows were taken
between 2 and 10 mi (3.7-18.5 km) from the coast,
most were near Newport Beach, Calif., where
northern anchovy eggs and larvae were abundant,
but some were much farther offshore. A surface
temperature was taken by bucket thermometer at
each net tow station.

Net tows were taken with aim plankton net on
which the cod end was a cylindrical Plexiglas^

'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.

Manuscript accepted October 1979.
FISHERY BULLETIN: VOL. 78, NO. 2, 1980.

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

475

FISHERY BULLETIN: VOL. 78, NO. 2

bucket (length 30.5 cm, diameter 10 cm) that could
be removed quickly. Tows were of short duration
to minimize the time larvae would be under stress
during capture. The net was let out at a fast steady
rate to a depth of 20 m, and then retrieved at a
moderate rate. The mean tow time was 3 min (SD
= 40 s).

The net drained rapidly as it was hauled out of
the water, leaving the cod end cylinder filled with
water containing a light to moderate amount of
plankton. The contents of the cylinder were im-
mediately poured into a small sieve made of 0.505
Nitex mesh netting, and the sieve was then sus-
pended in Bouin's fluid to fix the concentrated
plankton. The total elapsed time from start of tow,
when the plankton net first entered the sea sur-
face, to submergence in Bouin's averaged 5 min, 8
s (SD = 1 min, 9 s). After the initial fixation, about
10 or 15 min, the sample was transferred from the
sieve to ajar of fresh Bouin's, and this was replaced
by 709c ethyl alcohol 2 or 3 d later.

In carrying out the above procedure the inside of
the plankton net was not washed down after re-
trieval until the cod end containing the sample
had been removed. After the cod end was removed,
the inside of the net was hosed down thoroughly in
preparation for the next tow.

Subsequent to the cruise, all northern anchovy
and other fish larvae were sorted out of the sam-
ples and counted. From those tows containing only
a few northern anchovy larvae, all were set aside
for sectioning. From those tows containing many
larvae, about half a dozen were chosen for section-
ing. The number was approximately doubled for a
few samples of special interest, e.g., offshore
banks. Specimens were picked at random by put-
ting all northern anchovy larvae from a given tow
in a shallow, wide-mouth container and re-
peatedly dipping with a vial as the contents were
swirling slowly. During this procedure small
specimens with obvious yolk sacs were rejected
because they represented nonfeeding larvae not
yet vulnerable to starvation.

The total number of larvae selected for section-
ing was 318. Standard length was measured with
an ocular micrometer, then each specimen was
imbedded in paraffin, sectioned serially as close to
the sagittal plane as feasible, and stained in Har-
ris' hematoxylin and eosin-phloxine B. Prior to
microscope examination the mounted specimens
were put in random order with their identities
concealed.

Histological criteria similar to those diagnostic

for laboratory starved larvae were readily estab-
lished for ocean-caught larvae by preliminary
examination of a few dozen (unidentified) speci-
mens, after which all ocean-caught larvae were
classified as to condition. Under Results, the his-
tological indications of condition are described
first, and then the classification of larvae is
examined in relation to other variables, i.e., stan-
dard length, geographical distribution, tempera-
ture, and plankton volume.

RESULTS

Histological Characteristics of Condition

O'Connell (1976) found the most noticeable ef-
fects of artificial starvation of northern anchovy
larvae just beyond yolk absorption (3-5 mm) to be
cellular dissociation with loss of zymogen in the
pancreas, separation and hyalinization of trunk
muscle fibers, and shrinkage of the notochord. In
the ocean-caught material examined in the pres-
ent study, specimens ranging from 2.5 to 10 mm
showed anomalies in the trunk musculature and
notochord, and occasionally also in the pancreas,
that closely resembled the effects of starvation in
the laboratory material. These larvae almost al-
ways showed, in addition, certain irregularities in
the histology of the foregut and the midgut that
were more striking than effects seen in the diges-
tive tracts of artificially starved larvae.

Trunk Musculature

The trunk musculature in the majority of larvae
showed good integrity and texture, forming a
compact, solid sheet over the lateral surfaces of the
notochord, with evident intermuscular matrix tis-
sue and only occasional small separations (Figure
1). The notochord in such larvae generally had a
smooth profile and was rarely separated from the
musculature. In some specimens, however, the
muscle fibers were noticeably separated from each
other throughout, indicating an anomalous condi-
tion. In the more extreme cases (Figure 2) the
fibers were widely separated with degraded fibril
clarity, and matrix tissue was greatly reduced. In
such specimens the notochord was also irregular
in profile, imparting a "lumpy" shape to the trunk
of the animal as a whole.

Degraded musculature, of course, might be the
result of some process other than starvation. One
possibility is capture myopathy, which has been

476

O'CONNELL; PERCENTAGE OF STARVING NORTHERN ANCHOVY LARVAE

6 3gv«,^„^_^^_^

Figures 1-6. — Histx)logical comparisons of healthy (left) and emaciated (right) nort;hem anchovy larvae. All sections are approximately
sagittal. 1) The trunk musculature, cut tangential to the body surface, forms a solid sheet. The foregut mucosa is composed of imiform
cuboidal cells. 6.1 mm SL; 250 x . 2> The trunk musculature, cut tangentially, shows widely separated fibers. 8.5 nmi SL; 250 x . 3)The
foregut mucosa is composed of uniform thick cuboidal cells. 7.0 mm SL; 630 x . 4) The foregut is irregular and the cells of the mucosa are
diminished in size. 6.1 mm SL; 630 x. 5) The mucosa of the midgut shows good integrity and organization, and the lumen contains
moderate food residue. 6.3 mm SL; 250 x. 6) The midgut is filled with disassociated cellular debris and the mucosa is fragmentary.
Separated trunk muscle fibers are also visible. 8.5 mm SL; 250 x . Symbols: Fg, foregut; K, kidney; L, liver; M, trunk muscle; Mg, midgut;
N, notochord; R, food residue; T, transverse muscle coat of digestive tract; U, mucosa.

reported for a number of ungulates, primates, and
birds (Harthoorn 1977) and in the swordfish,
Xiphias gladius (Tibbo et al. 1961). The outstand-
ing symptom is degeneration of skeletal muscle,

presumably from acidemia from overexertion dur-
ing intense flight and struggle in capture. Though
the possibility cannot be entirely dismissed, cap-
ture myopathy seems an unlikely cause of the

477

FISHERY BULLETIN: VOL. 78, NO. 2

II

12

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v..

•:;\^^=^'''a^S?^3»&"*'> '*''''**^

N

Figures 7-12. — Histological comparisons of healthy (left) and emaciated (right) northern anchovy larvae. — Continued. 7) The trunk
muscles cut in cross section above and below the notochord are compact. The foregut and midgut have mucosa of good thickness and
integrity. 5.5 mm SL; 100 x . 8) Trunk muscles are separated and uneven, the midgut is filled with disassociated cellular material, and the
pancreas is severely disassociated. 5.5 mm SL; 100 x. 9) Portions of the midgut, the pancresis, and the trunk musculature below the
notochord all show good integrity. 5.0 mm SL; 250 x. 10) Enlargement of Figure 8 for comparison of pancreas to that in Figure 9.
250 X . 11) The foregut is regular and the trunk muscles are compact. The foregut is not yet expanded, and the midgut is not visible in the
section. The remnant of the yolk sac, primarily periblast tissue, is prominent. 2;5 mm SL; 250 x . 12) The midgut is a solid mass of necrotic
debris. The notochord and trunk muscles are collapsed and irregular. The kidney is necrotic. 2.2 mm SL; 250 x . Symbols: Fg, foregut; K,
kidney; L, liver; M, trimk muscle; Mg, midgut; N, notochord; P, pancreas; S, spinal cord; U, mucosa; Y, yolk.

muscle deterioration observed in the northern an-
chovy larva. It is essentially a phenomenon of
protracted struggle in large animals. In the case of

478

the northern anchovy larvae, time and physical
manipulation were minimized in capture.

Depletion of tissues arising from starvation

/

O'CONNELL: PERCENTAGE OF STARVING NORTHERN ANCHOVY LARVAE

seems a more likely cause of muscle deterioration.
Love (1974), in summarizing depletion in (adult)
fishes, states that ". . . when fish are starved the
lipid reserves . . . decrease to a certain point
beyond which the muscle protein is mobilized. As
the protein decreases, the water increases, and
this change is mainly brought about by shrinkage
of the cells and a corresponding increase in the
fluid between them." In conjunction with these
findings it had been shown that extracellular
spaces appeared in the musculature of Atlantic
cod, Gadus morhua (Love et al. 1968), and Ameri-
can plaice, Hippoglossoides platessoides (Tem-
pleman and Andrews 1956). Deterioration of the
musculature was a prominent effect following ar-
tificial starvation of early postyolk-sac northern
anchovy larvae ( O'Connell 1976) and of jack mack-
erel, Trachurus symmetricus, larvae (Theilacker
1978). Deterioration of musculature during starva-
tion has also been observed in larval herring,
Clupea harengus, and plaice, Pleuronectes platessa
(Ehrlich et al. 1976).

Digestive Tract

In most larvae the long foregut was straight with
a uniform lumen and a smooth surfaced mucosa of
cuboidal or thick squamous cells (Figure 3; see also
Figures 1 and 7). The foregut was considered
anomalous if the profile was noticeably irregular in
sagittal view. The mucosa usually also showed some
variation in cell thickness and shape. In the more
extreme cases the mucosa cells tended to be re-
duced to little more than the nucleus (Figure 4),
and the lumen sometimes contained a few
sloughed cells.

The midgut varied greatly in appearance, de-
pending on the degree of longitudinal folding and
transverse ridge development and on the plane of
a particular section. Nevertheless, in most speci-
mens a substantial lumen, sometimes containing
food, and a simple mucosa of low columnar cells
could be traced (Figures 5, 7, 9). Although the
infranuclear portions of the cells were often nar-
rowed and slightly separated, the supranuclear
portions were always well joined.

The midgut was judged anomalous when little
or no lumen could be traced, or when the traceable
lumen contained a considerable bulk of loose nu-
clei and necrotic cellular debris, and the mucosa
proper was fragmenting (Figures 6, 8, 10). In the
worst case the midgut was a homogeneous mass of
necrotic debris enclosed in only a basement mem-

brane, with no trace of either lumen or mucosa
(Figure 12). This specimen, which happened to be
the smallest examined, also showed a severely
collapsed notochord and degenerate musculature.
The degree of organ development, including fully
pigmented eyes, indicated that it had shrunken.
Healthy specimens of comparable size, which still
had unpigmented eyes, showed good notochord
and musculature, and often a sizable remnant of
the yolk sac (Figure 11). Shrinkage has been
shown in laboratory starved larvae of both the
Atlantic herring (Blaxter and Hempel 1963) and
the northern anchovy (O'Connell 1976; O'Connell
and Raymond 1970).

Whereas the muscle and foregut anomalies are
at least logically acceptable as consequences of
inadequate nourishment, interpretation of the
midgut anomaly is problematical. In artificially
starved northern anchovy larvae the midgut
showed thinning and increased separation of cells,
and the loss of some cells (O'Connell 1976), but not
strong contraction followed by general fragmenta-
tion and necrosis of the mucosa as seen in some of
the ocean-caught specimens. It may be, of course,
that the symptoms were different because the
laboratory and ocean situations were different.
Laboratory animals were starved without ever
having an opportunity to feed, whereas the
oceanic larvae showing symptoms undoubtedly
did have the opportunity to feed. Most in fact had
processed food through the digestive tract, as indi-
cated by the presence of supranuclear inclusion
bodies in the mucosa cells of the hindgut, though
the hindgut and the inclusion bodies were some-
times in a state of disintegration. Such inclusion
bodies were never found in laboratory specimens
deprived of food from time of hatching (O'Connell
1976).

Contraction and congestion resembling that
seen in the midguts of the emaciated northern
anchovy larvae from the ocean have been de-
scribed for some other fishes, but they can be
symptomatic of disease as well as of starvation.
Clupea harengus larvae of 9-13 mm, for example,
are vulnerable to a nematode that grows in the
body cavity and deforms the gut, often resulting in
occlusion of the lumen that blocks food intake
and/or defecation (Margolis 1970). There are other
nematodes whose larvae attack the gut walls of
certain fishes, causing inflammatory and de-
generative changes, including localized necrosis
and infiltration of abundant lymphocytes (Mar-
golis 1970). There are also protozoans, such as

479

FISHERY BULLETIN: VOL. 78, NO. 2

Nosema anomala, which invade the intestinal
wall of the young of the threespine stickleback,
Gasterosteus aculeatus , and generate hyper-
trophied cells filled with its vegetative and repro-
ductive stages (Lorn 1970). Certain viral diseases
produce degenerative changes that include necro-

sis and sloughing of intestinal epithelium
( Yasutake 1975). On the other hand, starvation of
immature salmon cause, among other things,
marked atrophy of the stomach with degeneration
of the epithelium, which ". . . could presumably be
used for nourishment" (Love 1974). Starvation of

Table l. — Numbers of northern anchovy larvae and other data by net tow for March 1977, off southern California. Number
emaciated and standard length pertain only to sectioned larvae. See Figures 13 and 14 for tow locations.

Tow

Date

Hour

Temperature
(°C)

Plankton
volume (ml)

Number of Larvae

In tow

Sectioned

Mean standard
length

Number emaciated
Severe Moderate Incipient

1

2

3

4

5

6

7

8

9

10

11

12

M3
14
15
16
17

M8
19
20
21
22
23
24

'25
26
27
28
29

'30
31
32
33
34

'35
36
37
38
39
40

'41
42
43

'44
45

'46
47
48
49
50
51
52
53
54
55
56
57

'58
59
60
61
62
63
64

17

1530

13.2

1750

13.8

2210

13.5

18

0825

14.2

1035

14.5

1440

14.7

1910

14.7

2340

14.8

19

0350

13.7

1010

15.2

1215

15.6

1550

15.5

1600

2215

14,6

20

0005

13.4

0735

13.6

1155

14.0

1205

2045

15.0

21

0005

14.9

2045

14.2

22

1920

14.2

2255

13.6

23

0945
0955

14.6

1110

14.7

2045

14.1

2315

13.4

24

1020
1030

14.7

1440

13.7

1915

14.8

25

0120

13.8

1550

13.1

1555

2310

13.4

26

0140

13.1

0345

12.7

0550

123

0730

12.8

0740

0927

12.7

1300

144

1325

1620

14.1

1630

1745

14.5

2030

14.2

2205

14.2

2345

14.3

27

0120

13.8

0240

13.2

0410

13.2

0645

14.2

1340

14.5

1450

14.6

1600

14.5

1610

1839

14.1

2115

14.0

2330

13.8

28

0145

14.4

0415

15.2

0640

15.2

1

5

4

2

2

3

3

2

3

4

3

1

8

11

4

4

10

3

7

4

21

7

32

6

10

3

12

7

14

8

7

11

35

14

5

6

38

10

33

17

29

106

4

21

1

12

7

13
21
15
19
29
42
7

10

20

7

30

27

17

12

15

5

2

0

9

33

9

9

14

68

47

54

7

2

32

2200

43

24

59

20

15

70

65

2400

16

2350

40

54

5

180

56

62

67

8

2200

2300

97

22

122

2250

19

4

0

0

1

1

1

0

1

0

2

2

3

2

16

35

0

0

0

0

0

5

3

1

11

42

22

6

7
5
5
6
6
6
6
7
2
6
6
6
10
6
7
6
6
7
6
6
7
6
6
5
6
5
6
7
6
6
6
7
6
7
6
6
4

2
2

3

2

16

15

4
3

1

7
14
15

4.6
4.0
5.0
4.9
6.4
5.4
4.7
4.5
4.9
39
5.1
5.2
4.7
6.7
4.7
5.5
4.2
5.5
6.5
5.0
5.7
6.0
4.2
4.4
44
4.9
5.4
5.3
5.3
5.4
4.7
4.9
4.8
5.7
6.9
7.1
6.6
12.5

8.0

5.9

12.2

8.5

10.6

9.3

7.2

8.2

12.3

11.0

9.8
12.8
11.7
9.4
7.1
6.9

'Taken at same location as precedi
^Number estimated from count of a

ng tow at almost twice the depth,
substantial fraction.

480

OCONNELL: PERCENTAGE OF STARVING NORTHERN ANCHOVY LARVAE

mummichog, Fundulus heteroclitus, up to 8 days
resulted in a decrease in the quantity of lipid drop-
lets in cells of the digestive tract and contraction of
the intestine such that the lumen was small, some-
times scarcely traceable (Ciullo 1975). While these
considerations suggest that disease could be the
cause of the midgut anomaly present in certain of
the ocean-caught northern anchovy larvae, starva-
tion is the more tenable explanation because there
was no evidence of parasites or pathogens in the
hematoxylin- and eosin-stained specimens, and
other anomalies in these specimens were consistent
with demonstrated effects of starvation.

Other Organs

Deterioration was sometimes evident in other
organs, particularly in the specimens with the
most severe anomalies in the musculature and
digestive tract. The pancreas and liver, for exam-
ple, showed good integrity in most larvae (Figures
1, 9), but some showed an unusual degree of dis-
sociation in these organs (Figures 8, 10), and in a
few, both organs had undergone considerable
lysis. The kidney ducts were intact in all speci-
mens, but in a few the cells of the ducts were
unusually thin, or necrotic (Figure 12). In several
the mantle layer of the brain showed poor integ-
rity, perhaps from a reduction of neuroglia.

Classification of Larvae

During the course of microscope examination,
each larva was designated healthy, incipient
emaciation, moderate emaciation, or severe
emaciation. The three classes pertaining to larvae
with anomalies are not rigorous, but they imply
the following: incipient, slight looseness of the
trunk muscles; moderate, obvious separation of
the trunk muscle fibers, some irregularity of the
notochord and possibly the foregut, strong contrac-
tion of the midgut, and sometimes a high incidence
of hypertrophic cells in the midgut mucosa; and
severe, obvious separation and hyalinization, and
sometimes disarray, of the muscle fibers, notable
irregularity in the profile of the notochord and
foregut, depletion of foregut muscosa cells, and
fragmentation of midgut mucosa, with a central
core of dissociated and necrotic cellular debris. Of
the 318 larvae sectioned, 26 were classified as se-
verely or moderately emaciated, and another 11
were classified as incipient. These are listed by net
tow in Table 1 along with the raw data for all tows.

The larvae classified as incipient are included with
the healthy rather than with the emaciated or
"starving" group in the sections that follow.

Relation of Emaciated Larvae to
Other Variables

Standard Length

Emaciated larvae were all < 10 mm SL and were
distributed almost proportionately over the range
2-10 mm SL (Table 2). Larvae classified incipient
were similarly distributed. In the lowest size
category, 2.1-4.0 mm SL, only half of the 46 larvae
examined had exhausted their yolk and become
vulnerable to starvation. The emaciated individu-
als were part of this contingent. The absence of
emaciated larvae in the categories above 10 mm
SL may be a chance result of the relatively fewer
numbers of larger larvae present in the tows, but
there may also be some actual reduction in starva-
tion effects at this size because of increasing lipid
reserves with growth (Love 1974).

Table 2. — Standard length distribution of the northern an-
chovy larvae sectioned and examined and of those classified as
emaciated or incipient.

Standard

Number

Number

Number

length

examined

emaciated

Incipient

2.1- 4.0

46

6

3

4.1- 6.0

137

8

3

6.1- 8.0

60

8

3

8.1-10.0

30

4

1

10.1-12.0

26

1

12.1-14.0

14

14.1-16.0

3

16.1-20.0

3

Geographical Distribution

More than half of the tows were spread over a
large offshore area where abundance of northern
anchovy larvae was generally low (Figure 13,
Table 1) and where samples from six tows each
contained a single emaciated larva. The remain-
der of the tows occurred in an area of a few
hundred square miles off Newport Beach where
larval abundance was high (Figure 14, Table 1)
and where samples from four tows each contained
several emaciated larvae. The fact that these four
samples showed a high proportion of emaciated
larvae, while others from nearby tows showed only
healthy larvae, indicates that there was a conta-
gious or patchy distribution of such larvae off
Nevqjort Beach.

481

FISHERY BULLETIN: VOL. 78, NO. 2

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483

FISHERY BULLETIN: VOL. 78, NO. 2

The impression of "patches" of larvae in poor
condition indicated by the histological samples
from the Newport Beach area was further
strengthened by subsequent examination of the
unsectioned larvae remaining from all net tows.
Figure 15 shows a random portion of tow 23, which
contained over 300 larvae and produced only
healthy larvae in the histological sampling. The
specimens are full-bodied with good symmetry
and are straight, or at worst gently curved. Figure
16 shows a random portion of tow 9, which pro-
duced a high proportion of emaciated larvae in the
histological sampling. Several of these larvae
have angular body bends, trunks and digestive
tracts that are lumpy and sinuous, and heads often
misshapen with loose or missing eyes. They also
appeared to be less intensely colored by the fixing
solution than the others. When viewed in toto, this
and the other three tow collections of larvae that
produced histologically poor samples were readily
distinguishable from all others.

The emaciated larvae consititute a percentage
of the number of larvae examined, but the mag-
nitude of this percentage depends on the portion of

the total samples that are considered (Table 3).
The four tows with a high incidence of emaciation,
considered by themselves, indicate 60%
emaciated larvae within local patches. This drops
sharply to 12% when coverage is expanded to a few
dozen tows in approximately 200 mi^ off Newport
Beach, and to 10% when an additional 10 tows,
rather widely scattered over the San Pedro Channel
area are included (inshore set). By comparison, the
pooled offshore samples (offshore set) which repre-
sent perhaps 6,000 mi^, indicate 5% emaciated, and
samples pooled for the entire cruise show an inter-
mediate value of 8% emaciated.

Day and night subsets of the inshore and
offshore sets show differences in both the available
population and the percentage of emaciated lar-
vae. The lower daytime catches imply that the
population was less available during this period,
probably because much of it migrated below the 20
m depth of the tows during the day and probably
also because larvae have some success in visually
avoiding the net during the day. As a simple
binomial function, the 15% emaciated larvae for
the inshore night group is significantly higher

Figure 15. — A random portion of the northern anchovy larvae from tow 23, in which the larvae show generally good body form.

484

O'CONNELL: PERCENTAGE OF STARVING NORTHERN ANCHOVY LARVAE

Figure 16.— a random portion of the northern anchovy larvae from tow 9, in which the larvae show generally irregular body form.

TABLE 3.-

—Percentage of emaciat

ed northern

anchovy larvae

for different sa

imple arrays.

Sample arrays

Number

of

tows

Larvae/
tow

Number
of larvae
examined

Number

of larvae

emaciated

Percent
emaciated

95%

confidence

limits

Samples vi^itti fiigti incidence
of emaciation

4

37.5

30

18

60.0

±17.5

200 mi2 coastal area
includes above

27

77.1

165

20

12.1

It 5.0

Insfiore set (tows 1-37):
Day (0600-1800 h)
Nigtit (1800-0600 h)
Pooled

20
17
37

36.6

134.0

81.3

111
109
220

4
17

21

3.6

15.6

9.6

± 3.5
± 6.8
± 3.9

Offsfiore set (tows 38-64):
Day (0600-1800 h)
Night (1800-0600 h)
Pooled

14
13
27

1.9

11.2

6.3

19
79
98

1
4
5

5.3
5.1
5.1

±10.0
± 4.8
± 4.4

Total cruise pooled

64

50.0

318

26

8.2

± 3.0

than the other three subset percentages, but the
obvious contagious nature of the distribution of
these larvae casts doubt on the value of such tests.
It is probably safer here to choose a lower percent-
age, such as the 8% for the entire cruise pooled, as
representative, and assume that the observed sub-
set differences are nothing more than sampling
variation.

Surface Temperature

The tows with a high incidence of emaciated
larvae were not associated with a given level of
temperature, but it appears that they were located
in an area of variable temperature (Figure 14).
The 13° and 15° C tongues of water may have been
basically persistent water masses, as Methot and

485

FISHERY BULLETIN: VOL. 78. NO. 2

Kramer (1979) suggested, but the irregularity of
the isotherms defining these tongues off Newport
Beach implies local shifting of temperatures.
Comparison of time as well as temperature differ-
ences along and adjacent to the cruise track for 20
March indicates, in fact, that notable temperature
differences between closely located tows were
probably more a matter of change over time than
of static gradients between locations. Tows 15 and
20 are of particular interest because they both had
a high incidence of emaciated larvae and were
close together, but differed in temperature by 1.5°
C. However, tow 20 was taken 24 h later than tow
15, and the thermograph record showed that the
higher temperature applied to tow 15, as well as to
the tow 19 and tow 20 positions, at the later time.
Such short-term temperature shifts indicate that
there was water mass instability or movement in
the area.

Plankton Volume

Plankton volume averaged appreciably lower
for the four tows with a high proportion of
emaciated larvae than for either the inshore or the
offshore set of tows (Table 4). The average number
of larvae was also relatively low in these four tows,
being about half the average for all tows off New-
port Beach, or in the San Pedro Channel area
(inshore set). Number of larvae and plankton vol-
ume, in fact, tend to be associated for the inshore
set (Figure 17), and while the four tows with high
incidence of emaciated larvae do not show the low-
est values, they are among the tows with low val-
ues.

Plankton volume did not relate to temperature
in the inshore area, but there were some interest-
ing changes with time (Figure 18). From 17 March
to midnight of 20 March all volumes were 11 ml or
less. This includes the four tows with a high inci-
dence of emaciated larvae, one of which (tow 20)

Table 4. — Mean plankton displacement volume (milliliters) for
different sample arrays in the study of northern anchovy larvae
off southern California.

Plankton

Item

No. of
tows

Larvae/
tow

Volume/
tow

SD

Samples with high inci-

dence of emaciation

4

37.5

38

200 mi2 coastal area

includes above

27

77.1

8.3

Inshore set includes

above

37

81.3

8.7

Offshore set

27

6.3

19.7

Total cruise

64

50.0

13.3

0.5

9.3

9.0
20 1

15.6

was the last taken in this time period. Twenty-four
hours later tow 21, the first tow with a markedly
higher volume (21 ml), was taken at a nearby
position (Figure 14). Three more tows of progres-
sively higher volume were taken during night
hours over the next few days, but there were also
several tows with lower volumes (3-14 ml) taken
during this period, some at night. This pattern
indicates that there was a striking change in the
plankton regime off Newport Beach starting on 2 1
March, with volume tending to be higher, espe-
cially at night, than it had been during the preced-

<
>

<

U.

o

CO

3

300 -

200

10 20 30

PLANKTON VOLUME (ml)

40

Figure 17. — The regression of number of anchovy larvae on dis-
placement volume of plankton (larvae excluded) for the inshore
tows, 1-37. The solid circles indicate the four tows with a high
incidence of emaciated larvae.

40

30

2
3

O

>

o

I-

z
<

a.

20

10

o
o o

oo 9

CD O

% •% •

—I — I — I — I — I I I — 1 — I — f— 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

06 13 18 \0€ 12 IB \ 06 12 18 \ 06 12 18 \ 06 12 W \ 06 12 18 \ 06 12 '8 \06 12 W \ 06 12 18 \ 06

17 18 19 20 21 22 23 24 25 26

DATE a MOUff OF TOW

Figure 18. — Displacement volume of plankton on date (March
1977) and hour of tow. Dots indicate the four tows with a high
incidence of emaciated larvae. Dates are in bold type and located
at midnight points on the hour scale.

486

O'CONNELL: PERCENTAGE OF STARVING NORTHERN ANCHOVY LARVAE

ing few days, when the tows with a high incidence
of emaciated larvae were taken.

DISCUSSION

The most significant result of this study is that
northern anchovy larvae showing symptoms in-
dicative of starvation were indeed found in the
ocean and were thus identified on the basis of their
individual appearance. The emaciated condition
of these larvae is very similar to that induced in
laboratory animals by total food deprivation
(O'Connell 1976), which implies that cir-
cumstances of insufficient food were responsible
for their occurrence in the ocean, especially where
samples contained many such larvae, as off New-
port Beach. Other causes are possible, and one of
the most obvious is discharge from sewage outfalls
in the area. However, the discharges are now dif-
fused rapidly and in general appear to be harmless
and perhaps even beneficial to nearby young and
adult fish (Southern California Coastal Water Re-
search Project^).

Zones of insufficient food might well have
existed in the Newport Beach area at the time of
the survey. The variations in both temperature
and plankton volume, which were clearly dynamic
in nature, indicate that there was appreciable
water mass movement or instability, and such
conditions can alter plankton abundance. Lasker
(1975, in press) found, for example, that phyto-
plankton blooms believed to be advantageous for
first feeding anchovy larvae were variously dissi-
pated and suppressed as the water column became
unstable in turbulent weather and sea conditions.
In the present study the time sequence of plankton
volume change off Newport Beach shows the pos-
sibility that water with relatively low plankton
levels and "patches" of emaciated larvae was
being replaced by water with greater plankton
abundance, in which larvae were also more abun-
dant and generally healthy.

Although the occurrence of zones of insufficient
food is a reasonable hypothesis in regard to the
"patches" of emaciated larvae off New^jort Beach,
it is not a plausible explanation for some of the
other samples, where occasional emaciated indi-
viduals occurred among abundant healthy larvae.

^Southern California Coastal Water Research Pro-
ject. 1978. The effects of the ocean disposal of municipal
waste. Summary Report of the Commission of the Coastal
Water Research Project, June 1978, 27 p. Filed at 1500 East
Imperial Highway, El Segundo, CA 90245.

It can only be surmised that in any location, and
despite generally good conditions, there will be
some instances of starvation through detrimental
combinations of genetic constitution, accident, and
chance failure to capture food.

If circumstances of poor food availability are
produced by water mass activity, as suggested
above for the Newport Beach area, they are likely
to be more or less transient phenomena, which
raises the question of short-term susceptibility of
northern anchovy larvae. Immediately after yolk
absorption, northern anchovy larvae will survive
only a day or two without food (Lasker et al. 1970),
and they will show visible effects before dying
(O'Connell 1976). Protein components are quickly
affected because early postyolk-sac fish larvae have
negligible lipid reserves (Ehrlich 1974), though
such reserves obviously increase with growth and
become a buffer against insufficient food (Love
1974). Even so, northern anchovy larvae of rela-
tively large size, 35 mm SL, survived only 2 wk, on
the average, after feeding was stopped, and during
this period the average lipid content of living larvae
was declining while mortality in the population
was rising, with smaller individuals dying sooner
than larger ones (Hunter 1976a). Since larvae
examined in the present survey were appreciably
smaller than the above, thus having lower lipid
reserves, the signs of emaciation could have re-
sulted from relatively few days of insufficient food.

Most of the larvae showing histological signs of
emaciation in this study also showed signs of pre-
vious feeding, not by the presence of food residue,
but rather by remnants of eosinophilic inclusion
bodies in the hindgut mucosa cells. The starvation
and previous feeding indications are not incom-
patible. Laboratory feeding studies have shown
that growth, lipid content, and survival all decline
quickly under limited or discontinued feeding
(O'Connell and Raymond 1970; Hunter 1976a),
and it is probable that histological signs of deterio-
ration would also appear quickly, especially in early
larval stages.

If, as proposed by Hjort (1914, 1926), the level of
mortality suffered by the early feeding stages of
fish populations is a decisive component of the
prerecruitment mortality, some measure of that
mortality should be a useful indicator of ultimate
year class success. The proportion of larvae ob-
served to be starving may be one such useful indi-
cator: It is directly visible, and it may reflect a
substantial part of total daily mortality. Zweifel
and Smith (in press) have estimated average daily

487

FISHERY BULLETIN: VOL. 78, NO. 2

population abundance of larval anchovies by
length and region for the 1967 through 1975
California Cooperative Oceanic Fisheries Investi-
gations net tow data, and length dependent mor-
tality rates were calculated from the abundance
estimates. For larvae of 7.5 mm SL, which approx-
imates the median length of those showing
symptoms of starvation in the present study, the
estimated average daily mortality rate in the San
Pedro Channel area was 21%. If it is assumed that
all larvae showing symptoms will die directly or
indirectly from starvation, the observed 8% with
symptoms in the March 1977 survey could indicate
a net daily mortality from starvation of 8%, which
is 409c of the average total daily mortality for this
length group. If starvation tends to contribute this
substantially to total mortality, variations in the
proportion of larvae observed to be starving may
relate reasonably well to the magnitude of ongoing
total mortality and consequently to recruitment
from the year class.

How well the proportion of starving larvae from
a given sampling in 1 yr will predict the eventual
recruitment of that year class will only be evident
from correlation of the two variables for at least a
few years. As for 1977, with a northern anchovy
"starvation ratio" of 8%, there were indications
that recruitment would be good. The winter and
early spring were relatively mild, a condition con-
ducive to development of high density patches of
larval food organisms, particularly from di-
noflagellate blooms (Lasker in press). Growth rate
of northern anchovy larvae was also shown to be
above average in the San Pedro Channel area for
March 1977 (Methot and Kramer 1979). The above
average growth rate may have been valid for much
of the population developing in the region without
applying to the patches of emaciated larvae, which
were taken at different locations than the grovd;h
samples. Estimates from recent catch data indi-
cate that the 1977 year class is of moderate size, as
compared with the large 1976 and 1978 year clas-
ses and the small 1974 and 1975 year classes (J. S.
Sunada^). Thus, to the extent that 8% starving
larvae is a reliable estimate of that parameter for
1977 and to the extent that the parameter is as-
sociated with recruitment, both higher and lower
occurrences of starving larvae are likely pos-
sibilities from future surveys.

''J. S. Sunada, Assistant Biologist, Marine Resources Region,
California Department of Fish and Game, 350 Golden Shore,
Long Beach, CA 90802, pers. commun. May 1979.

Reliability of the estimate of starving larvae is
probably reasonably good for 1977 in that tows
were most concentrated in a region of high abun-
dance, but reliability in future sampling efforts
could probably be improved by more diligent
stratification in respect to population distribution.
In addition to sampling at more than one point in
time, an effective strategy might be to expand
sampling in several areas that show high abun-
dance, particularly of larvae under 10 mm SL,
along a preplanned survey track. Expanding sam-
pling in this way would likely result in a quantity
of samples that would be formidable if analysis is
entirely dependent on histological or physiological
parameters. The distinctive appearance of the
aggregated larvae from those few tows of the pres-
ent survey that contained predominantly
emaciated larvae, however, suggests that histologi-
cal analysis can be greatly reduced.

Assuming that starvation of any consequence
will occur in patches, a stereomicroscope scan of
the total aggregation of larvae from each tow
should suffice for the identification and enumera-
tion of such patches, with histological processing
reserved for selected verification. Undoubtedly
some of the starving larvae that occur as scattered
single cases would be missed under such a proce-
dure, but this should have little effect on the over-
all estimate.

ACKNOWLEDGMENT

I would like to acknowledge the very able assis-
tance of Pedro Paloma, who sorted and measured
all the samples and prepared all the slides.

LITERATURE CITED

Blaxter, J. H. S.

1971. Feeding and condition of Clyde herring lar-
vae. Rapp. P.-V. Reun. Cons. Int. Explor. Mer 160:128-
136.

Blaxter, J. H. S., and G. Hemple.

1963. Influence of egg size on herring larvae (Clupea
harengus L.). J. Cons. 28:211-240.
CIULLO, R. H.

1975. Intestinal histology of Fundulus heteroclitus with
observations on the effects of starvation. In W. E. Ribe-
lin and G. Migaki (editors). The pathology of fishes, p.
733-767. Univ. Wis. Press, Madison.

EHRLICH, K. F.

1974. Chemical changes during growth and starvation of
herring larvae. In J. H. S. Blaxter (editor). The early life
history offish, p. 301-323. Springer- Verlag, Berl.

EHRLICH, K. F., J. H. S. BLAXTER, AND R. PEMBERTON.

1976. Morphological and histological changes during the

488

O'CONNELL: PERCENTAGE OF STARVING NORTHERN ANCHOVY LARVAE

growth and starvation of herring and plaice larvae. Mar.
Biol. (Berl.) 35:105-118.

Harthoorn, a. M.

1977. Problems relating to capture. Anim. Regul. Stud.
1:23-46
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.

1926. Fluctuations in the year classes of important food
fishes. J. Cons. 1:5-38.
HUNTER, J. R.

1976a. Culture and growth of northern anchovy, En-
graulis mordax, larvae. Fish Bull., U.S. 74:81-88.

1976b. Report of a colloquium on larval fish mortality
studies and their relation to fishery research, January
1975. U.S. Dep. Commer., NOAA Tech. Rep. NMFS
Circ. 395, 5 p.
Lasker, R.

1975. Field criteria for survival of anchovy larvae: the
relation between inshore chlorophyll maximum layers
and successful first feeding. Fish. Bull. , U.S. 73:453-462.

In press. Factors contributing to variable recruitment of
the northern anchovy (Engraulis mordax) in the Califor-
nia Current: contrasting years, 1975 through 1978. In
K. Sherman and R. Lasker (editors), Symposium on the
early life history offish. Woods Hole, April 1979. Rapp.
P.-V. Reun. Cons. Int. Explor. Mer.

Lasker, R., H. M. Feder, G. H. Theilacker, and R. C. May.

1970. Feeding, growth, and survival oi Engraulis mordax
larvae reared in the laboratory. Mar. Biol. (Berl.)
5:345-353.
LOM,J.

1970. Protozoacausingdiseases in marine fishes. /nS.F.
Snieszko (editor), A symposium on diseases of fishes and
shellfishes, p. 101-123, Am. Fish. Soc, Spec. Publ. 5.
LOVE, R. M.

1974. The chemical biology of fishes. Acad. Press, Lond.,
547 p.

Lox'E, R. M., I. Robertson, and I. Strachan.

1968. Studies on the North Sea cod. VI. Effects of starva-
tion. 4. Sodium and potassium. J. Sci. Food Agric.
19:415-422.

Margolis, L.

1970. Nematode diseases of marine fishes. In S. F.
Snieszko (editor), A symposium of diseases of fishes and
shellfishes, p. 190-208. Am. Fish. Soc, Spec. Publ. 5.
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 con-
dition. [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
condition in early post yolk sac larvae of the northern
anchovy, Engraulis mordax Girard. J. Exp. Mar. Biol.
Ecol. 25:285-312.

O'CONNELL, C. R, and L. P RAYMOND.

1970. The effect of food density on survival and growth of
early post yolk-sac larvae of the northern anchovy (En-
graulis mordax Girard) in the laboratory. J. Exp.
Mar. Biol. Ecol. 5:187-197.

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.

Templeman, W., and G. L. Andrews.

1956. Jellied condition in the American plaice Hippoglos-
soides platessoides (Fabricus). J. Fish. Res. Board Can.
13:147-182.

Theilacker, G. H.

1978. Effect of starvation on the histological and mor-
phological characteristics of jack mackerel, Trachurus
symmetricus, larvae. Fish. Bull., U.S. 76:403-414.

TiBBo, S. N., L. R. Day, and W. F. Doucet.

1961. The swordfish iXiphias gladius L.), its life-history
and economic importance in the northwest Atlan-
tic. Fish. Res. Board Can., Bull. 130, 47 p.

UMEDA, S., AND A. OCHIAl.

1975. On the histological structure and function of diges-
tive organs of the fed and starved larvae of the yellovrtail,
Seriola quinqueradiata. [In Jpn., Engl, summ.] Jpn. J.
Ichthyol. 21:213-219.

Yasutake, W. T.

1975. Fish viral diseases: clinical, histopathological and
comparative aspects. In W. E. Ribelin and G. Migaki
(editors). The pathology of fishes, p. 247-271. Univ. Wis.
Press, Madison.

ZWEIFEL, J. R., AND P. E. SMITH.

In press. A time series of anchovy embryonic and larval
mortality estimates with confidence limits on the esti-
mates of abundance of all sizes and on the mortality
rate. In K. Sherman and R. Lasker (editors). Sym-
posium on the early life history offish. Woods Hole, April
1979. Rapp. P.-V. Reun. Cons. Int. Explor. Mer.

489

TRANSPORTATION OF CHINOOK SALMON, ONCORHYNCHUS
TSHAWYTSCHA, AND STEELHEAD, SALMO GAIRDNERI, SMOLTS IN
THE COLUMBIA RIVER AND EFFECTS ON ADULT RETURNS

Wesley J. Ebel^

ABSTRACT

Chinook salmon, Oncorhynchus tshawytscha , and steelhead, Salmo gairdneri, were captured at Little
Goose Dam in the Snake River during their seaward migration and transported 400 km downstream to
the lower Columbia River below Bonneville Dam. Their survival was increased from 1.1 to 15 times as
compared with control fish which passed by seven mainstem low-level dams and reservoirs. Variations in
survival were mainly dependent on species and environmental conditions in the river during the period
fish were transported.

The homing ability of the adult fish was not significantly diminished; less than 0.2% of strays occurred
among adult returns from groups transported. Transportation did not affect ocean age or size of returning
adult steelhead, but ocean age of returning adult chinook salmon may have been affected. Steelhead
returned to Little Goose Dam at a substantially higher rate (1.4-2. 7% I than chinook salmon (0.1-0.8%)
from groups transported. The timing of adult returns of both species to Little Goose Dam was not related
to the time of capture and downstream release of smolts.

Salmonid populations of the Snake River and its
Idaho tributaries have declined rapidly in recent
years to the point that the very survival of some
stocks is threatened. The total run (i.e., catch plus
escapement) of chinook salmon, Oncorhynchus
tshawytscha, attributable to the Snake River
dropped from 120,000 adults in 1972 to 50,000 in
1974 (Raymond 1979). Similarly, the total run of
steelhead, Salmo gairdneri, an anadromous form
of rainbow trout, declined from 100,000 adults in
1972 to below 20,000 in 1974. The downward trend
of the anadromous salmonid populations has been
ascribed to losses of juvenile migrants at the series
of eight dams (Figure 1) and associated reservoirs
in the Snake and Columbia Rivers through which
the smolts must pass on their way to the sea
(Raymond 1979).

With the goal of protecting the migrants from
the hazards of dams, a system for transporting
smolts around the dams was investigated by the
National Marine Fisheries Service. The juvenile
migrants were collected from the Snake River at
Little Goose Dam (the uppermost dam — Figure
1), transported around the entire series of dams,
and released below Bonneville Dam (the lower-

'Northwest and Alaska Fisheries Center, National Marine
Fisheries Service, NOAA, 2725 Montlake Blvd. E., Seattle, WA
98112.

most dam) on the Columbia River. The effects of
such transportation on the survival and catch of
the fish and on the ability of the adults to "home"
to their natal streams must be known if fishery
agencies are to evaluate the transportation sys-
tem as a practical means of protecting Snake River
salmonid runs. The main objectives of the research
at Little Goose Dam were: to determine the effect
of transportation on homing and survival of
juvenile chinook salmon and steelhead collected at
Little Goose Dam and released at two locations
downstream from Bonneville Dam and to compare
these results with an earlier study done at Ice
Harbor Dam (Ebel et al. 1973) where fish were

Little Goose
Lower n, _

Monumental ^\L*-Central

Manuscript accepted December 1979.
FISHERY BULLETIN: VOL. 78, NO. 2.

Figure l.— Transportation routes and release location of exper-
imental chinook salmon and steelhead collected and marked at
Little Goose Dam, 1971-73.

491

1980.

FISHERY BULLETIN: VOL. 78, NO. 2

transported a shorter distance. Secondary objec-
tives were: to determine any relation between tim-
ing of downstream juvenile migrants and timing
of subsequent adult returns and to determine
whether size and ocean age of adults (transported
as smolts) were affected by the collection and
transport process. The results of the experiments
described in this report are also compared with the
preliminary results of the current experiment at
Lower Granite Dam.

BACKGROUND

The changes in abundance and the causes of
changes in abundance of individual salmonid
populations in the Columbia River drainage have
been summarized by Chaney and Perry (1976).
Raymond^ analyzed the trends in abundance of
Snake River runs in detail and clearly showed that
the major causes of the decline of the Snake River
stocks are due to the losses of juveniles during
their seaward migration. These losses are caused
by injury or death occuring when the fish attempt
to pass the eight dams and reservoirs placed in
their migratory path. These dams now inundate
over 630 km of the migratory route. The main
causes of the juvenile losses have been attributed
to: passage through turbines (Bell et al. ; Long,
Krcma, and Ossiander ; Long, Ossiander, Ruehle,
and Mathews^); supersaturation of river water
with atmospheric gas (Ebel and Raymond 1976);
delay in migration (Raymond 1968, 1969); and
increased predation (Chaney and Perry 1976).

^Raymond, H. L. 1975. Snake River runs of salmon and
steelhead trout: trends in abundance of adults and downstream
survival of juveniles. Unpubl. manuscr., 11 p. Northwest and
Alaska Fisheries Center, Natl. Mar. Fish. Serv., NOAA, 2725
Montlake Boulevard East, Seattle, WA 98112.

3Bell, M. C, A. C. DeLacy, G. J. Paulik, and R. A. Win-
nor. 1967. A compendium on the success of passage of small
fish through turbines. Northwest and Alaska Fisheries Center,
Natl. Mar. Fish. Serv., NOAA, 2725 Montlake Boulevard East,
Seattle, WA 98112. (Contract DA-35-026-CIVENG-66-16, Re-
port to U.S. Army Corps of Engineers, Portland, Oreg.)

*Long, C. W., R. F. Krcma, and F. J. Ossiander. 1968. Re-
search on fingerling mortality in Kaplan turbines —
1968. Unpubl. manuscr., 7 p. Northwest and Alaska Fisheries
Center, Natl. Mar. Fish. Serv., NOAA, 2725 Montlake
Boulevard East, Seattle, WA 98112.

*Long, C. W., F. J. Ossiander, T. E. Ruehle, and G. M. Mat-
thews. 1975. Final report on survival of coho salmon fingerlings
passing through operating turbines with and without perforated
bulkheads and of steelhead trout fingerlings passing through
spillways with and without a flow deflector. Northwest and
Alaska Fisheries Center, Natl. Mar. Fish. Serv., NOAA, 2725
Montlake Boulevard East, Seattle, WA 98112. (Contract
DACW68-74C-0113, Report to U.S. Army Corps of Engineers,
Portland, Oreg.)

492

The National Marine Fisheries Service (NMFS)
has been conducting transportation experiments
since 1965 in an attempt to find ways of reducing
these losses. The first study where natually mi-
grating juveniles were collected and transported
was conducted by Ebel et al. (1973). This study
showed that the homing ability of adult spring and
summer chinook salmon and steelhead captured
during their seaward migration as juveniles and
then transported downstream (from Ice Harbor
Dam to below Bonneville Dam) was not di-
minished. Data based on returning adults indi-
cated that survival rate of adult fish that had been
transported as juveniles increased 1.5-3 times the
survival rate of those not transported, depending
on environmental conditions in the river during
the time of transport. Studies conducted prior to
this study with hatchery stocks of salmonids
showed that the majority of the adult fish that had
been transported as juveniles returned to the re-
lease site, not to the parent location (Snyder 1928;
Ellis and Noble 1960). Obviously, juvenile salmo-
nids captured during their seaward migration
and then transported differed in their responses
from fish transported directly from hatcheries.
The wild and hatchery stocks captured in the ex-
periment conducted by Ebel et al. (1973) were
smolting and had traversed several hundred
kilometers before capture. These may be the main
factors causing the different response (homing
ability was not diminished) obtained in the exper-
iment done in 1973.

Previous experiments (Hasler and Wisby 1951;
Groves et al. 1968; Scholz et al. 1973) on
mechanisms used by fish for homing indicated
that the experience prior to and during the time
that a juvenile salmon migrates is important in
enabling the fish to receive visual and olfactory
cues necessary for homing as an adult.

Only a portion of the migration route was elimi-
nated by transporting the fish from Ice Harbor
Dam to The Dalles and Bonneville Dams. Elimi-
nation of this portion of the migratory route appar-
ently did not seriously affect the ability of either
the chinook salmon or steelhead to home. How-
ever, the length of the migration route or amount
of homing cues that can be eliminated and still
achieve satisfactory homing is unknown.

The success of the experiment by Ebel et al.
(1973) at Ice Harbor Dam encouraged the NMFS
to begin a similar experiment at Little Goose Dam
in 1971. As this dam is approximately 130 km
upstream from Ice Harbor Dam, an additional 130

EBEL: TRANSPORTATION OF CHINOOK SALMON AND STEELHEAD SMOLTS

km of the migratory route would be eliminated,
and the fish would be intercepted during their
juvenile migratory life stage about 2-3 wk earlier
than they were at Ice Harbor Dam. The results
achieved at this site could be quite different from
those obtained at Ice Harbor Dam. To facilitate the
collection offish, an orifice bypass system, juvenile
fish diversion screens, and raceways for collection
of juvenile fish were built into Little Goose Dam
during its construction. This system provided sub-
stantial numbers of fish for the experiment, but
there was the possibility that these fish might be
injured or stressed during the diversion and collec-
tion process.

Table l. — Number of transported and nontransported (control)
juvenile chinook salmon and steelhead that were marked and
released from Little Goose Dam, 1971-73.

Control fish

Transported

fish'

Species and

Dalton Point

Bonneville Dam

release year

No. released^

No. released^

Nc

) released^

Chinook salmon:

1971

20.673

30,637

35.252

1972

32.836

51,499

54,906

1973

88.170

57,758

83,606

Steelhead:

1971

33,243

35.967

44,939

1972

32.488

22.831

27,326

1973

42.461

26,650

36,802

'Transported fish were released in the Columbia River at two sites down-
stream from Bonneville Dam: 2 km downstream on the Washington (side re-
ferred to in the table as Bonneville Dam) and 1 7 km downstream on the Oregon
side at Dalton Point.

^Release totals adjusted for initial tag loss.

METHODS

Experimental Design

During the downstream migrations in 1971,
1972, and 1973 juvenile chinook salmon and
steelhead were randomly selected from the race-
ways at Little Goose Dam and divided into three
groups — one control and two transported groups.
The adipose fin was removed from all experimen-
tal fish and each group was selectively marked
with a thermal brand and magnetized wire tags.
Thermal brands were changed every 5 d among all
treatment groups except for the first 10-d marking
period. During this period, marking continued for
10 d before a change was made. Codes for mag-
netized wire tags were changed yearly for each
treatment group. The control group was released
at Central Ferry, about 10 km upstream from Lit-
tle Goose Dam; the transported groups were
hauled in tank trucks to two locations downstream
from Bonneville Dam (Figure 1). One release site
was at Dalton Point, 17 km downstream from
Bonneville on the Oregon side of the river; the
other was at the Washington State boat launching
site, about 2 km downstream from Bonneville
Dam. Each year the goal was to mark at least
50,000 chinook salmon and 25,000 steelhead for
each group. This goal was exceeded every year
(Table 1) except for all groups ofchinook salmon in
1971 and the control group ofchinook salmon in
1972.

Collection and Marking of Fish and
Fish Hauling Procedures

Juvenile chinook salmon and steelhead were
collected at Little Goose Dam, using a fingerling

collection and bypass system (Smith and Farr
1974). The system consisted of: 1) screens in the
turbine intakes which diverted fish into the
gatewells of each turbine intake; 2) a gatewell
orifice and piping system which transported fish
from the gatewells to a grader and counter; and 3)
a fish grader and counter which sorted fish by size
and electronically counted fish entering five race-
ways. When desired, fish could be diverted directly
to the river — thus bypassing the grader, counter,
and raceways.

Fingerling chinook salmon and steelhead were
pumped with a 5 -in Paco model fish pump into the
marking building where they were anesthetized
and sorted. Previously marked fish were returned
to the river in the tailrace of the turbine discharge.
Samples of at least 100 chinook salmon and
steelhead were examined each day for percentage
descaling to provide an index offish condition. Any
fish with >10'^ of the scales missing was consid-
ered descaled. Each of the remaining fish was
cold-branded with liquid nitrogen (Park and Ebel
1974), had the adipose fin excised, and had a
magnetic wire tag ( Jefferts et al. 1963) inserted in
the snout. Before passing into a transport truck,
the fish went through a magnetic field and detec-
tion coil; an untagged fish was automatically re-
jected and returned to the marker for retagging.
Initial tag loss was measured by examining sam-
ples of juveniles 48-72 h after tagging; subsequent
tag loss was determined by examining returns of
adult control and test fish at Rapid River Hatchery
near Riggins, Idaho, and Dworshak National Fish
Hatchery at Ahsahka, Idaho. A branded fish with
an adipose fin clip that did not also have a coded

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

493

FISHERY BULLETIN: VOL. 78, NO. 2

wire tag was considered a fish that had lost its tag
after marking. Steelhead and chinook salmon
were kept in separate compartments in the tank
truck whenever both species were hauled simul-
taneously. All fish were transported in a truck of
18,900 1 (5,000 gal) capacity (Smith and Ebel 1973)
that was equipped with aeration, refrigeration,
and filtration systems. Load densities were gov-
erned by the size of the daily catch and were usu-
ally <0.12 kg/1 (1 lb/gal) except during periods
when unmarked fish were hauled. Maximum load
density was kept <0.18 kg/1 (1.5 lbs/gal) of water.
Water chemistry measurements were taken
from the truck at the time of release for every load
transported. Concentrations of ammonia, nitro-
gen, dissolved oxygen, carbon dioxide, pH, and
total alkalinity were recorded for possible correla-
tions with delayed mortality information. All re-
leases were made at dusk. Records of mortality
were kept during marking and at time of release; a
sample of 50-100 fish was taken from each trans-
ported load and held for 48 h at Bonneville Dam to
provide an indication of delayed mortality. This
procedure was repeated during downstream mi-
grations in 1971, 1972, and 1973.

Evaluation of Returning Adults

The effect of transportation on the survival and
homing of adult fish was evaluated by comparing
returns of transported and nontransported fish to
the sport, commercial, and Indian fisheries in the
lower Columbia River; to Little Goose Dam on the
lower Snake River; to Rapid River Hatchery,
Pahsimeroi Hatchery near Salmon, Idaho, and
Dworshak Hatchery; and to the spawning grounds
throughout the Snake River drainage.

All adult fish migrating upstream at Little
Goose Dam must ascend one ladder located on the
south side of the dam. An adult tag detection and
fish separating device that intercepted tagged
salmon and steelhead and diverted them into a
holding pen was installed in this ladder in 1972
(Ebel 1974). Tagged fish from our study were read-
ily identified by the missing adipose fin. All fish
were anesthetized and further examined for
brands. If the brand was recognizable, the origin of
the fish could be determined without having to
extract the magnetic tag from the snout.

Fish with recognizable brands were then
weighed and measured, dart-tagged or jaw-tagged
(Slatick 1976), and released to provide further in-
formation in the event of recapture upstream and

to identify fish that fell back over the dam and
ascended the ladder a second time. If a fish was
known to be tagged but had a brand that was
indistinguishable, it was held until maturity in
holding tanks at the dam and artificially spawned.
The tag was then extracted after spawning, and
the test or control group was determined from the
color code. Data obtained from these fish were
combined with those obtained from reading
brands.

The Columbia River gillnet fishery below Bon-
neville Dam, the Indian fishery above the dam,
and the sport fishery (primarily below the dam)
provided samples of chinook salmon throughout
the spring run. The samples yielded information
concerning the returns to the lower river of
marked fish originating primarily in Idaho. Clo-
sure of the summer fishery on chinook salmon
during all 3 yr and the spring fishery in 1974 and
1975 prevented sampling of this segment of the
run in the lower river. The sport and commercial
fisheries of the lower Columbia River and the sport
fishery above Little Goose Dam provided samples
of steelhead.

Surveys of spawning grounds were conducted
with the cooperation of the Washington Depart-
ment of Fisheries, Fish Commission of Oregon,
and the Idaho Department of Fish and Game. Most
of the surveys were in the Snake River drainage of
Idaho, but hatcheries and spawning grounds of
spring and summer chinook salmon in the upper
Columbia River were also checked for strays.

The G statistic. Student's ^-test, and analysis of
variance were used for analysis of most return
data.

RESULTS

Factors Influencing Assessment of Data

Tag loss, tag detector efficiency, transport mor-
tality, and delayed mortality were factors that
influenced the assessment of the experimental
data. Comparisons of tests and control releases
could be biased if a differential effect among any of
these factors occurred between test and control
releases and was not considered in the analysis.
For example, if tag loss was greater in control
releases than in test releases, percentage return
would be biased in favor of the test release if the
data were not adjusted for this loss.

During the 3 yr of this study, average annual
initial tag loss ranged from 0.45% in 1973 to 10.4%

494

EBEL: TRANSPORTATION OF CHINOOK SALMON AND STEELHEAD SMOLTS

in 1972; average tag loss for the 3 yr of marking
was 3.79c. Release totals were adjusted for initial
tag loss. Additional tag loss (occurring after initial
tag loss), based on examination of 884 marked
adult steelhead at Dworshak National Fish
Hatchery and 154 marked adult chinook salmon
at Rapid River Fish Hatchery, was nill (<0.1%)
and did not affect data analysis.

About 4-8^^ of the juvenile chinook salmon and
4-109^ (Park et al."^) of the juvenile steelhead re-
leased as controls were recaptured and released at
Little Goose Dam. No attempt was made to adjust
the data for a small bias that might have occurred
from this procedure. It was assumed that survival
of this portion of the controls that were handled
and released after passing through the collection
system was the same or greater than survival of
the majority of the control fish that had to pass
either through the turbines or over the spillway.

The primary recovery site for evaluation of tag
returns was at Little Goose Dam where an au-
tomatic tag detector and fish trap were installed
(Ebel 1974). The efficiency of the detector and trap
was based on a comparison of known recovery of
fish with magnetized wire tags at Little Goose
Dam and subsequent recovery of these and other
marked fish at Rapid River and Dworshak Hatch-
eries. For example, 54 fish were identified at Rapid
River Hatchery in 1975 from treatment groups
that had passed Little Goose Dam. Of these, 50 had
jaw tags indicating they had been captured and
identified at Little Goose Dam; 4 did not have jaw
tags indicating these fish had passed the dam
without being trapped or identified. The trap ef-
ficiency for chinook salmon in 1975 was therefore
50/54 or 0.92. Thus, a factor of 1.08 was used to
expand recoveries of .2- and .3-age^ chinook salm-
on captured and identified at Little Goose Dam
in 1975 from experimental releases in 1972 and
1973. Similar calculations were made for each
year of recovery of chinook salmon during 1972-76
in computing estimated percentage return for a
particular treatment group. The same procedure
was used to estimate trap efficiency for steelhead

'Park, D. L., J. R. Smith, E. Slatick, G. Matthews, L. R.
Basham, and G. A. Swan. 1978. Evaluation offish protective
facilities at Little Goose and Lower Granite Dams and review of
mass transportation activities, 1977. Northwest and Alaska
Fisheries Center, Natl. Mar. Fish. Serv., NOAA, 2725 Montlake
Boulevard East, Seattle, WA 98112. (Contract DACW68-77-
0043, Report to U.S. Army Corps of Engineers, Portland, Oreg.)

*Age designations follow the formulas of Koo ( 1962). The
number of winters at sea is shown by an Arabic numeral pre-
ceded by a dot.

with data obtained from recoveries at Dworshak
Hatchery. The efficiency of recovery varied among
years from 43 to 90^^ during the spring and sum-
mer when tagged chinook salmon were recovered.
One source of variation was due to periodic shut-
downs of the detector and trap for special studies of
passage of adult fish. The efficiency remained con-
stant (72'7f ) during the fall of each year when most
adult steelhead were recovered. An examination
of the timing of test and control fish returning to
Little Goose Dam indicated there was no sig-
nificant difference. Thus, variations in efficiency
did not affect comparisons of recoveries of test and
control fish because all experimental groups
passed the detector throughout the recovery
period, and both test and control groups were sub-
jected to the same variations in recovery ef-
ficiency. Total estimates of adult returns were ad-
justed for detector efficiency for a given period of
recovery.

The use of the above method of estimating total
percentage return for treatment groups assumes:
loss of jaw tags from fish identified at Little Goose
Dam was nil and jaw-tagged fish survived at the
same rate as fish not jaw tagged. The first assump-
tion is valid, I believe, because examination of
several hundred fish at both Dworshak and Rapid
River Hatcheries each year of recovery did not
reveal any evidence of lost tags. Data from recent
radio tracking studies (see Monan and Liscom^)
suggest that the second assumption is also valid.
In these studies, adult chinook salmon were ob-
tained from the fish ladder with a similar trap and
handled in an identical manner before tagging,
and mortality of tagged fish was nil.

Transport mortality was defined as the mortal-
ity which occurred as a result of handling, mark-
ing, and hauling; delayed mortality was consid-
ered mortality that occurred in samples held at
Bonneville Dam immediately after hauling.
Transport mortality of both species was <l9c of
the total number of smolts handled (Table 2). De-
layed mortality (Table 3) was considerably more,
ranging from 10to229J^ for chinook salmon and 1.0
to 4.5% for steelhead. Transport and delayed mor-
tality obviously reduced the total number of

''Monan, G. E., and K. L. Liscom. 1974. Radio-tracking of
spring chinook salmon to determine effect of spillway deflectors
on passage at Lower Monumental Dam, 1973. Northwest and
Alaska Fisheries Center, Natl. Mar. Fish. Serv., NOAA, 2725
Montlake Boulevard East, Seattle, WA 98112. (Contract
DACW57-73-F-0534, Final Report to U.S. Army Corps of En-
gineers, Portland, Oreg.)

495

FISHERY BULLETIN: VOL. 78, NO, 2

Table 2. — Mean mortality of juvenile chinook salmon and steel -
head during transport from Little Goose Dam to release loca-
tions downstream from Bonneville Dam, 1971-73.

Percentage mortality

Species

1971

1972

1973

Chinook salmon
Steelhead

0.87
0.16

0.57
0.51

0.70
0.51

Table 3. — Mean delayed mortality of samples of juvenile
chinook salmon and steelhead taken from marked groups
transported from Little Goose to below Bonneville Dam. Fish
were held from 48 to 72 h after transport.

Percentage mortality

Species

1971

1972

1973

Chinook salmon
Steelhead

22.8
1.0

10.0
1.4

17.2
4.5

transported smolts released and correspondingly
reduced adult returns from transported groups.
Control groups may have been less affected be-
cause of the shorter transport time (1 h vs. 6 h).
However, the assessment of benefits or losses ob-
tained from transport of salmonid smolts must
include this mortality. Release totals were there-
fore not adjusted for either transport or delayed
mortality. It was noted that over 90% of the dead
fish in the delayed mortality group had obvious
signs of descaling or injury.

Measurements of descaling (fish with >10% of
the body area descaled) of chinook salmon smolts
that were recorded during the marking process
varied from 0 to as high as 50% of the individuals
observed. The average annual descaling rate was
16.6% in 1972 and 19.6% in 1973. Incomplete
records of descaling measurements made it impos-
sible to determine the average rate of 1971. De-
scaling of steelhead was substantially less than
descaling of chinook salmon; the overall average
for 1972 and 1973 was <1%. It was determined
from other studies being conducted that most of
the descaling was caused by experimental diver-
sion screens being tested in the turbine intakes
(Ebel et aU°).

There was a relation between descaling rate and
delayed mortality. Steelhead were less descaled
than chinook salmon and had much less delayed

'"Ebel, W. J., R. F. Krcma, and H. L. Raymond.
1973. Evaluation of fish protective facilities at Little Goose
Dam and review of other studies relating to protection of other
salmonids in the Columbia and Snake River, 1973. 62 p.
Northwest and Alaska Fisheries Center, Natl. Mar Fish. Serv,
NOAA, 2725 Montlake Boulevard East, Seattle, WA 98112.
(Contract DACW68-71-0093, Progress Rep. to U.S. Army Corps
of Engineers, Portland, Oreg.)

mortality than chinook salmon. It appears that if
the injury that occurred during diversion and
handling could be eliminated, survival of trans-
ported chinook salmon could be substantially im-
proved.

Returns of Adult Experimental Fish
to Little Goose Dam

A comparison of ratios of transport and control
percentage returns of adults to Little Goose Dam
from releases of chinook salmon and steelhead for
the 3 yr of this study (Figure 2) indicated that
survival of both species was substantially in-
creased in 1973 by transporting the fish to the
Dalton Point and Bonneville Dam release sites;

The percentage increase in survival varied from
year to year and, I believe, was dependent primar-

16

14

r CHINOOK SALMON

1971 1972

'' □ Control
/ 5)5 Transport

0

n

n a

1973

n

o

Q.

N= 52 266

Ratio=1.6:1

16 r steelhead

1971

14

V

6 -

n

0

N= 199 811

Ratio=1,7;1

25 89

Ratio=l.l;l

1972

nJ.

20 502

Ratio=15.4:l

1973

^

n

I

132 664

Ratio=3.25;l

61 1225
Ratio=13.4:1

Figure 2. — Comparison of ratios of adult percentage return to
Little Goose Dam from control and transported juvenile chinook
salmon and steelhead. (Returns from Dalton Point and Bonne-
ville Dam releases combined.) Percentage return of controls was
set at unity for each year and species; the increase (transport
percentage return -^ control percentage return) is shown by
darkened bar.

496

EBEL: TRANSPORTATION OF CHINOOK SALMON AND STEELHEAD SMOLTS

ily on river conditions. During years when survi-
val of natural migrants (hatchery and wild stocks
migrating naturally) was low, there was corres-
pondingly low survival of control releases and
greatest benefit from transportation. For exam-
ple, in 1973, natural migrant survival estimates
(Raymond 1979, see footnote 2) indicated an all-
time low survival rate for both juvenile chinook
salmon and steelhead migrants; in contrast,
transport-control ratios were highest — 15.4:1 for
chinook salmon and 13.4:1 for steelhead (Figure
2). Raymond (1979) compared survival estimates
of control releases from this study and other ear-
lier studies (Ebel et al. 1973; Slatick et al. 1975)
with survival estimates of naturally migrating
smolts and found a high correlation (r = 0.95 for
chinook salmon; 0.92 for steelhead) between sur-
vival of controls from transportation studies and
his estimates of survival of natural migrants for
the years 1968 to 1975. These data indicated there
were close relationships between survival of re-
leases of control fish marked for the transportation
studies and hatchery and wild stocks migrating
naturally. Raymond also correlated low survival
with adverse river conditions; thus benefits from
transportation would be highest when river condi-
tions are the most adverse.

Statistical analysis of the return percentages
(Table 4) was done by analysis of variance. A test

of normality (Shapiro and Wilk 1965) of the per-
centage return data showed that the data were
normally distributed (P 0.05); thus, transforma-
tion of percentage figures was not necessary.
Analysis of variance of the return percentages in-
dicated that the differences between "treatments"
(test and control releases) were significant at the
IVc level (Table 5). Interactions of the treatment x
species were significant at the d^c level, indicating
that the effects of treatment varied between
chinook salmon and steelhead. For example, the
mean transport/control ratio for returning
chinook salmon in 1972 was 1.1:1, whereas the
mean ratio for steelhead was 3.25: 1 . An analysis of
the test of treatment effects — to compare the two
downstream releases (both transported) and the
control vs. the transported groups (Table 5) —
clearly showed that there were no differences be-
tween recoveries from the Dalton Point and Bon-
neville Dam release sites and that the differences
shown between test and control groups (Figure 2)
were highly significant (P<0.01). Since interac-
tions of the treatment x species were significant
(P<0.05), I also analyzed the chinook salmon and
steelhead percentages separately (Table 6). These
analyses confirmed that differences shown be-
tween test and control groups were significant
(P<0.05) for both steelhead and chinook salmon
and that there were no differences between re-

TabLE 4. — Releases and recaptures of experimental fish.

Species, release
site, and year

Number

Ocean age'

(no.)

Adult returns (%)

Transport/ control

released

.1

.2

.3

Total

Observed

Estimated^

ratio^

Chinook salmon'*:

Control:

1971

20,673

5

28

19

52

0.252

0470

1972

32,836

4

12

9

25

0.076

0,106

1973

88.170

2

11

7

20

0.023

0026

Transport:

Dalton Point: '

1971

30,637

9

70

40

119

0.388

0.760

1.6:1

1972

51.499

4

20

20

44

0.085

0.114

1.1:1

1973

57.758

35

130

76

241

0417

0.730

28.1:1

Bonneville Dam:

1971

35.252

11

83

53

147

0.417

0.785

1.7:1

1972

54.906

5

28

12

45

0.082

0.110

1.0:1

1973

83.606

34

142

85

261

0.312

0.438

12.2:1

Steelhead:

Control:

1971

33,243

75

121

3

199

0.599

0.833

1972

32,488

75

57

—

132

0.406

0.564

1973

42,461

20

41

—

61

0.144

0.199

Transport:

Dalton Point:

1971

35.967

124

237

6

367

1.020

1.418

1.7:1

1972

22.831

187

130

1

318

1.393

1.936

3.6:1

1973

26.650

276

276

5

517

1.940

2.698

13.5:1

Bonneville Dam:

1971

44,939

166

287

11

464

1.033

1.436

1.7:1

1972

27,326

202

139

5

346

1 266

1.750

3.1:1

1973

36,802

352

353

3

708

1.924

2.673

13.4:1

'Age designation follows the formulas of Koo (1962). The number of years at sea is shown by an Arabic numeral preceded by a dot.
^Return percentage adjusted according to tag detector and trap efficiency.

^Transport,' control ratios determined by dividing estimated percentage return of controls into estimated return of transported fish.
•• Adult returns of spring and summer chinook salmon combined.

497

FISHERY BULLETIN: VOL. 78, NO. 2

Table 5. — Analysis of variance of comparative percentage returns of adult chinook salmon and
steelhead to Little Goose Dam for transported and nontransported (control) juveniles, 1971-73.

Pooled residual

Residual

Source

df

SS

MS

iF)

(F)

Treatments (test and control returns)

2

3053

1 526253

8924"

12 717"

Years (1971-73)

2

0398

0 198794

1 162

1 657

Species (Chinook and steelhead)

1

5520

5520057

32276--

46005"

Treatment ■ years

4

0 890077

0 223

—

1 858

Treatment ■ species

2

1 356179

0.678

3.965

5650-

Years • species

2

0 698503

0349

2.042

2.908

Residual

4

0.478141

0.120

—

—

Pooled residual

8

1 368218

0 171

—

—

Total

17

13 762118

Partition of treatment SS (above), comparing

adult Chinook salmon

and steelhead returns for control vs

transport and

Dalton Point vs. Bonneville Dam

Control vs transport

1

3.035

3.035

17 743"

Bonneville vs Dalton Point

1

0018

0.018

0.105

•P 0.05; "P 0.01.

Table 6. — Analysis of variance of comparative percentage
returns of adult chinook salmon and steelhead to Little Goose
Dam for transported and nontransported (control) juveniles,
1971-73 (returns analyzed by species).

Source

Chinook salmon return data
df SS

MS

Treatments

2

0.179

0.089

270

(test and control returns)

Years (1971-73)

2

0.473

0.237

7.14-

Error

4

0.132

0.033

Total

8

0 7849

Partition of treatment sum of squares (above) comparing adult chinook salmon
returns for control vs. transport and Dalton Point vs. Bonneville Dam.

Control vs. transport
Bonneville vs. Dalton Point

1 1 .604
1 0.014

1.604
0.014

48.45"
0.4342NS

Source

Steelhead return data
df SS

MS

Treatments

2

4.230

2.115

6.845

(test and control returns)

Years (1971-73)

2

0 623

0.311

1.006

Error

4

1.236

0309

Total

8

6.089

Partition of treatment sum of squares (above) comparing adult steelhead re-
turns for control vs. transport and Dalton Point vs.Bonneville Dam.

Control vs. transport
Bonneville vs. Dalton Point

4.223

0.062

4.223

0.062

iseer*

0.020NS

• = P'-0.05; " = P' 0.01; NS = nonsignificance.

coveries from the Dalton Point and Bonneville
Dam release sites for either chinook salmon or
steelhead.

Percentage Adult Returns of
Transported Releases

Analysis of the transport/control ratio provides
the best insight as to the possible benefits from the
transportation system, but total percentage re-
turn obtained from the groups transported must
also be examined to accurately assess the effec-
tiveness of the system as it operated. If both trans-
port and control groups were excessively stressed
during the diversion, collection, marking, and
transport operations, then percentage returns
would have been abnormally low even though

transport/ control ratios were favorable. I, there-
fore, compared percentage returns of the transport
groups with percentage returns of production re-
leases achieved at Dworshak and Rapid River
Hatcheries and with estimated percentage re-
turns of steelhead and chinook salmon to Little
Goose Dam.

Returns from production releases of juvenile
steelhead at Dworshak Hatchery (Olson^^) were
0.25% in 1971, 0.20% in 1972, and 0.052% in 1973.
Corresponding estimated percentage returns of
steelhead from those transported from Little
Goose Dam in 1971, 1972, and 1973 (returns from
Dalton Point and Bonneville Dam releases com-
bined) were 1.4, 1.8, and 2.7%, respectively. Al-
though the sport fishery for steelhead above Little
Goose Dam in 1973 would have reduced the per-
centage returns to Dworshak for releases in 1971,
the estimated catch of 2,459 (Petit^'^) when added
to the total hatchery returns, resulted in a return
percentage of<0. 50 for the 1971 release. The sport
fishery was closed from 1974 to 1976; thus returns
from releases in 1972 and 1973 at Dworshak
Hatchery were not affected.

I also compared percentage adult returns of
steelhead with the estimated percentage adult re-
turns from populations of natural migrants pass-
ing Little Goose Dam in 1971, 1972, and 1973 by
Raymond (1979, see footnote 2). His estimates of
percentage returns were based on counts of adults
passing the dam and estimates of populations of
smolts (both hatchery and wild) passing Little
Goose Dam for a given year. His estimates of per-
centage adult returns of steelhead to Little Goose

"Wayne Olson, Hatchery Manager, Dworshak National Fish
Hatchery, Ahsahka, Idaho, pers commun. 1973-76.

'^Steven Petit, Senior Fisheries Research Biologist, Idaho
Fish and Game Dep., Lewiston, Idaho, pers. commun. June 1974.

498

EBEL: TRANSPORTATION OF CHINOOK SALMON AND STEELHEAD SMOLTS

Dam for 1971, 1972, and 1973 were 0.8, 0.4, and
0.2%, respectively. These estimates did not in-
clude fish that were transported. A substantial
increase in survival of transported steelhead is
indicated by both analysis of test/control ratios
and comparisons of percentage returns of adults
from transported groups with percentage returns
of adults to Dworshak Hatchery and Little Goose
Dam.

Percentage returns from production releases of
juvenile chinook salmon to Rapid River Hatchery
(Parrish^^) in 1971, 1972, and 1973 were 0.59,
0.12, and 0.15%, respectively. The corresponding
percentage returns from juvenile chinook salmon
transported from Little Goose Dam were 0.77,
0.11, and 0.52%, respectively. Estimated adult re-
turns (Raymond 1979, see footnote 2) of the mix-
ture of wild and hatchery populations of juvenile
chinook salmon passing Little Goose Dam in 1971,
1972, and 1973 were 1.3, 0.6, and 0.4%, respec-
tively. While some benefit can be shown when
percentage return data from transported groups
are compared with only the Rapid River Hatchery
returns for 1971 and 1973, only those transported
in 1973 showed a benefit when returns were com-
pared with estimated percentage returns of adults
from mixed wild and hatchery smolts passing Lit-
tle Goose Dam.

When the combined returns of spring and sum-
mer chinook salmon were divided into seasonal
races (Table 7) and compared for the 3 yr of this
study, the benefits or losses from transportation
were defined by time. Transport/ control ratios in-
dicated that spring chinook salmon received great-
er benefit from transportation in 1971 and 1973
than summer chinook salmon. Summer chinook
salmon appeared to receive more benefit than
spring chinook salmon in 1972, but returns from
all chinook salmon releases were low in 1972.

Several factors could be responsible for the dif-
ferential in transport/control ratios between
spring and summer chinook salmon among the

years. Probably the most important factor was the
timing of seaward migration of the two races of
salmon. The race migrating downstream during
the most favorable river conditions would receive
the least benefit from transport in any particular
year.

Timing of Adult Returns of Chinook Salmon

Analysis of data on timing of adult returns in
comparison with timing of the juvenile seaward
migration (Table 8) indicated that the timing of
adult returns of chinook salmon to Little Goose
Dam was independent of timing of juvenile sea-
ward migration (G = 0.518, 0.516, and 0.293: df =
1,P<0.05 for 1971, 1972, and 1973, respectively).
This is in contrast to what Ebel et al. ( 1973) found
in adult chinook salmon returning from groups
marked at Ice Harbor Dam in 1968. In this study
most of the chinook salmon marked early in the
spring migration returned early as spring chinook
salmon, and most of those marked late returned
later as summer chinook salmon. Perhaps inter-
cepting the fish 130 km farther upstream elimi-
nated the relation indicated from the earlier
study. It is also possible that races of chinook salm-
on that exhibited this behavior in 1968 were
absent or very low in numbers during 1971-73.

Table 8. — G-statistic test of relationship between timing of
adult returns of chinook salmon to timing of juvenile seaward
migration at Little Goose Dam, 1971-73.

migration
Period'

Adult returns

Juvenile
Year

Spring^
(no.)

Summer
(no.)

3 Total
(no.)

G

Signif-
icance''

1971

Early
Late

73
120

25
33

98
153

Total

193

58

251

0.518

NS

1972

Early
Late

22

14

23
10

45
24

Total

36

33

69

0.516

NS

1973

Early
Late

149
122

86
63

235
185

Total

271

149

420

0.293

NS

'^Evan Parrish, Hatchery Manager, Idaho Fish and Game
Dep., Rapid River Hatchery, Riggins, Idaho, pers commim.
1973-76.

'Early = marked as juveniles from beginning of migration to 5 May. Late
= marked as juveniles after 5 May.

^Prior to 15 June.

Mfter 14 June.

"P >0.05. df = 1 ; NS (nonsignificance) indicates timing of adult returns is
independent of timing of seaward migration.

Table 7. — A comparison of adult returns to Little Goose Dam of transported and nontransported (control) spring and summer
chinook salmon smolts, 1971-73. Percentage values indicate adult returns from transported group.

1971

1972

1973

Seasonal
race of

Control

Transport
No,

Ratio

transport

control

Control Transport

Ratio

transport

control

Control

Transport
No. %

Ratio
transport;

Chinook

No,

No. % No.

No,

control

Spring
Summer

37 0.179
15 0 073

200 0303
66 0 100

1.70:1
1.37:1

18 0.055 65 0.061
5 0009 24 0022

1,1:1
2,4:1

10 0.011
10 0.011

329 0232
161 0114

21.2:1
10.4:1

499

Size and Years-in-Ocean of Adult
Experimental Fish

Since transported fish (chinook salmon and
steelhead) had the opportunity to enter the ocean
more than 1 mo earlier than control fish that mi-
grated naturally, the size and ocean age of return-
ing adults were examined to determine whether a
difference existed. The average weights of chinook
salmon and steelhead released as controls were
compared with the average weights of transported
groups returning at the same ocean age. A paired
comparison ^test using the data from Table 9
showed no significant differences in average
weights for chinook salmon and steelhead
(chinook salmon: t = 0.315, P>0. 5; steelhead: t =
0.297,P>0.5df =8).

The ratio of age .3 to age .2 chinook salmon and
the ratio of age .2 to age .1 steelhead were com-
pared (Table 10) between transported and control
groups. These comparisons indicated whether
transporting affected the time that fish spent in
the ocean before their return to Little Goose Dam.
An analysis of variance of the ratios for the 3 yr of
the study (Table 1 1 ) showed that the differences in
ocean age between transported and control

Table 9. — Average weights (kilograms) of returning chinook
salmon and steelhead to Little Goose Dam from control (C) and
transported (T) releases of smolts, 1971-73.

2-yr-

in-

3-yr-

in-

Species and

Jacks

ocean
C

fish

T

ocean
C

fish

year of release

C

T

T

Chinook salmon:

1971

1.66

1.40

5.06

4.74

8.22

9.20

1972

1.41

1.39

4.19

4.28

10.08

9.27

1973

1.86

1.51

4.40

4.46

7.77

9.02

Steelhead:

1971

2.42

2.37

5.80

5.16

6.19

5.75

1972

2.39

2.53

4.38

4.24

4.44

4.84

1973

2.32

2.25

4.47

4.73

3.74

4.70

Table lO. — Comparison of transport and control age ratios on
adults returning to Little Goose Dam, 1971-73. Chinook salmon
age .3/. 2 and steelhead age .1/.2 were used to determine ratios.

Control

Transported

Ocean

age' (no.)

Ocean

age' (no.)

Year

.2

.3

Ratio

.2

.3

Ratio

Chinook salmon:

1971

28

19

0.68

153

93

0.61

1972

12

9

0.75

48

32

0.67

1973

11

7

0.64

272

161

0.59

.1

.2

1

2

Steelhead:

1971

75

121

1.61

290

524

1 81

1972

75

57

0.76

389

269

0,69

1973

21

41

1.95

628

629

1.00

FISHERY BULLETIN: VOL. 78, NO, 2

Table ll. — Analysis of variance of ratios of ocean age .3 to .2'
chinook salmon and age .2 to .1 steelhead adults returning to
Little Goose Dam from transported and control releases.

Species

Source

df

ss

MS

F

Chinook
salmon

Treatments (trans-
port and controls)
Years (1971-73)
Error

1
2
2

0.00657
000931
0.00394

0.00657
0 00465
0.000197

23.6-
33.3*

Total

5

0.016274

steel-
head

Treatments (trans-
port and controls)
Years (1971-73)
Error

1
2
2

0.114
1.058
0.359

0.114
0.529
0.180

0633NS
2.94NS

Total

5

1.532

'Age designation follows the formulas of Koo (1962). The number of years at
sea is shown by an Arabic numeral preceded by a dot.

*P'0.05.

'Age designation follows the formulas of Koo (1962), The number of winters
at sea is shown by an Arabic numeral preceded by a dot

steelhead were not significant (P<0.05). A sig-
nificant (P<0.05) difference in ocean age between
control and transported chinook salmon did occur
with a slightly higher ratio of .3/.2-age chinook
salmon indicated among control returns. By these
analyses, the transportation of smolts to locations
downstream from Bonneville Dam was not shown
to influence either the age or size of returning
adult steelhead but may have influenced age of
returning adult chinook salmon.

Recovery of Marked Chinook Salmon in
the Commercial and Sport Fisheries

The experimental plan to evaluate recoveries of
adult chinook salmon in the commercial, Indian,
and sport fisheries required sampling of these
fisheries each year from 1973 to 1975. However,
the spring chinook salmon run began a rapid de-
cline in 1973, which forced the commercial fishery
to close in 1974 and 1975. As a consequence,
sufficient data on chinook salmon were obtained
only in 1973 for comparison of transported and
control recoveries. A test fishery was conducted in
1974 and 1975, but only 18 salmon were recovered
from the experimental releases during these
years — too few to make comparisons of recoveries.
Sixty-one salmon (Table 12) were recovered in
1973 from the 1971 experimental releases. The
combined transport/control ratio of these re-
coveries, computed after adjusting the number of
juveniles released, indicated that chinook salmon
transported as juveniles were captured at 2.86
times the rate of control fish. This is a substan-
tially higher test/control ratio than the 1.6:1 com-
puted for returns to Little Goose Dam, indicating
that transported groups were captured at a higher
rate in the fishery than at Little Goose Dam. This

500

EBEL: TRANSPORTATION OF CHINOOK SALMON AND STEELHEAD SMOLTS

Table 12. — Comparison between transported and nontransport-
ed (control) chinook salmon of 1971 that were captured during
1973 as adults in the commercial, Indian, and sport fisheries in
the lower Columbia River. (Numbers observed, not estimated.)

Transported
Dalton Point Bonneville Dam

Control

Recaptures

Item

No.

Recaptures

No. %

Recaptures

No.

Upstream from
Bonneville Dam
(Indian fishery)

Downstream from
Bonneville Dam
(commercial and
sport fisheries)

Total

14

9
23

0.046

0.029
0.075

14

18
32

0.040

0.051
0.091

0.019

0.010
0.029

Combined recoveries
(Dalton Point and Bonneville Dam)'

0,083

0.029

'Transport/control ratio = 2.86:1.

suggests that perhaps the adult fish from trans-
ported stocks were spending a longer time in the
lower river, thus allowing a greater catch of these
groups.

Recovery of Marked Steelhead in the
Indian and Sport Fisheries

The Indian fishery of the lower Columbia River
in 1973 and 1974 was not sampled because of clo-
sures during most of the season. However, in 1975
a substantial fishery was in progress. Sampling of
this fishery yielded 39 marked steelhead from
1973 experimental releases. Thirty-eight of these
were from transported groups; only one fish of a
control group was recovered. The ratio of transport
to control was 30:1, again indicating a higher
catch rate of transported steelhead in 1973 than
was recorded at Little Goose Dam where the
transport/ control ratio was 13.4:1.

Table 13. — Recoveries of adult steelhead from the sport fishery
upstream from Little Goose Dam. Juveniles were released, 1971-
73, as controls at Central Ferry; transported groups were re-
leased at Dalton Point and Bonneville Dam.

Control

Transported groups

No. Percentage
of fish return

Transport/

Year
released

No.
of fish

Percentage
return

control
ratio'

1971
1972
1973
Total

50

24

0

74

0.150
0.074

149
63
24

236

0.184
0.126
0.037

1.2;1
1.7:1

'Transport/ control ratios computed from the combined recoveries of the
Bonneville Dam and Dalton Point releases.

The sport fishery upstream from Little Goose
Dam in the Snake River was intensive in 1972 and
1973 but was closed for a portion of 1974. Sam-
pling of this fishery yielded 310 marked steelhead
(Table 13) from experimental releases in 1971-73.
The transport/control ratio estimated from these
recoveries indicated a benefit from transport, but
the benefit was about half that indicated
downstream at Little Goose Dam from releases in
1971 and 1972. The benefit was substantial in all
recovery locations from releases in 1973.

Returns of Adult Experimental Fish to
Hatcheries and Spawning Grounds

Spawning ground surveys and examination of
adult fish in Idaho hatcheries provided further
information concerning transport/ control ratios of
chinook salmon and steelhead at their "home" des-
tination.

Adult chinook salmon returns were examined at
Rapid River Hatchery; steelhead returns were
examined at Dworshak National Fish Hatchery
and at the Pahsimeroi Hatchery (Table 14). Ex-

Table 14. — Returns of adult chinook salmon and steelhead to hatcheries of the upper Snake River drainage, 1971-73.

Release site and
experimental group'

Released 1971

Released 1 972

Released 1973

Species and

hatchery of

origin

Recoveries

Transport/

control

ratio

1

=lecoveries

Transport/

control

ratio

Recoveries

Transport/
control

No

%

No.

%

No.

%

ratio

Chinook salmon
Rapid River

Bonneville Dam (T)
Dalton Point (T)

33
25

0.094
0.082

4.95:1
332:1

5

7

0.009
0.014

—

24
42

0.029
0.073

14.5:1
365:1

Total

58

0.088

4.63:1

12

0.011

—

66

0.047

235:1

Central Ferry (C)

4

0019

0

0

—

2

0.002

Steelhead
Dworshak

Bonneville Dam (T)
Dalton Point (T)

96
49

0214
0.136

1.37:1
0.87:1

26

17

0095
0.074

3 80:1
3.00:1

104

114

0.283
0.428

13.5:1
20.4:1

Total

145

0 179

0.87:1

43

0.086

344:1

218

0.344

16.4:1

Central Ferry (C)

52

0.156

8

0026

9

0.021

Pahsimeroi

Bonneville Dam (T)
Dalton Point (T)

8

5

0.018
0014

11
9

0.040
0.039

333:1
3.25:1

18
18

0.049
0.068

24.5:1
34.0:1

Total

13

0016

—

20

0 040

3.33:1

36

0057

280:1

Central Ferry (C)

0

4

0.012

1

0002

'T = transported group; C = control.

501

FISHERY BULLETIN: VOL. 78. NO. 2

cept for steelhead returns to Dworshak Hatchery
from releases in 1971, transport/control ratios
computed from these data indicated that the ben-
efits from transportation were greater than those
indicated from returns to Little Goose Dam.

This was particularly evident in returns of
chinook salmon and steelhead from releases in
1973. At Little Goose Dam the combined
transport/control ratio was 15.4:1 for chinook
salmon and 13.4:1 for steelhead; the ratios at the
hatcheries were 23.5:1 for chinook salmon (Rapid
River Hatchery) and 16.4:1 (Dworshak) and 28:1
(Pahsimeroi) for steelhead. One possible reason
for the difference might be a differential in benefit
which favored hatchery stocks. Because returns to
Little Goose Dam were a mixture of hatchery and
wild stocks, the proportion of each stock in a sam-
ple could alter the transport/control ratio.

Spawning ground surveys for adult chinook
salmon were conducted in 1972, 1973, 1975, and
1976. No surveys were made in 1974 because of the
small number of marked fish available for recov-
ery. The location of streams surveyed was identi-
cal to that described by Ebel et al. ( 1973). Fourteen
marked fish were recovered during the 4 yr of
surveys. Of these, 12 were identified as having
been released as transports and 2 as controls. Al-
though the recoveries of adults on the spawning
grounds were very low, recoveries at Rapid River
Hatchery were substantial (Table 14). The fact
that 12 adult fish, transported as juveniles from
Little Goose Dam, were recovered on the spawning
grounds indicates that transported wild stocks as
well as hatchery stocks continued their upstream
migration after leaving Little Goose Dam.

Straying of Experimental Groups

The chinook spawning grounds of the Okanogan
and Methow Rivers and other spring chinook
hatcheries in the Columbia River drainage were
checked to determine if adult returns from release
groups had "strayed" to spawning locations other
than their parent stream or hatchery. No strays
were indicated in checks of hatcheries and spawn-
ing areas in the Columbia River above the mouth
of the Snake River, but a few strays (16 chinook
salmon and 3 steelhead) were recovered at Pelton
Dam on the Deschutes River in Oregon. Of the 16
chinook salmon recovered, 10 were from groups
transported as juveniles, 2 from controls, and the
remaining 4 could not be positively identified as to
release group because tag codes were lost. The

502

three steelhead recovered were also from groups
transported. These recoveries indicate that the
homing behavior of a portion of the chinook salm-
on transported as juveniles may have been ad-
versely affected. However, the proportion of the
transported groups affected to this degree must
have been small; 857 chinook salmon and 2,720
steelhead were identified at Little Goose Dam
from the same release groups. The homing be-
havior of these fish obviously was not damaged.
Additional data are needed to quantify the degree
of straying that occurs from transporting
steelhead and chinook salmon from Little Goose
Dam.

DISCUSSION

Comparison of Results With Other Studies

The results of this study are similar to an earlier
study done by Ebel et al. (1973) in which survival
was definitely increased by transporting the fish
downstream as juveniles. Percentage returns of
adults to Little Goose Dam from transported fish
were greater than that from control fish for the
Dalton Point as well as the Bonneville Dam re-
lease sites for all 3 yr. However, the estimated per-
centage returns of chinook salmon were much
lower than those reported by Ebel et al. (1973)
when fish were collected and transported from Ice
Harbor Dam in 1968. Estimated returns of adult
chinook salmon, transported as juveniles from Ice
Harbor Dam, ranged from 4.3 to 9.0%; whereas,
returns of adult chinook salmon, transported as
juveniles from Little Goose Dam in this study,
ranged from 0.11 to 0.78% — substantially lower
than achieved at Ice Harbor Dam.

There are several factors which could have
caused the lower percentage returns from Little
Goose Dam: 1 ) some homing ability may have been
lost because the fish were intercepted and trans-
ported from a location about 130 km farther up-
stream; 2) the fish collected at Ice Harbor Dam
may have been more hardy individuals because
they migrated a greater distance, which would
have allowed more of the weaker individuals to be
eliminated from the populations; 3) the stocks col-
lected at Ice Harbor Dam in 1968 were primarily
wild stocks and thus hardier — more able to stand
the stress of handling, marking, and hauling; or 4)
the general condition of the fish at the time of
marking may have been better because the collec-
tion, handling, and hauling system used at Ice

EBEL: TRANSPORTATION OF CHINOOK SALMON AND STEELHEAD SMOLTS

Harbor Dam could have resulted in less stress
than that at Little Goose Dam. Further examina-
tion of the data, however, implies that the condi-
tion of the fish (factor 4) may have been the main
factor. Estimated adult returns of chinook salmon
to Ice Harbor Dam from fish transported in 1969
and 1970 (Slatick et al. 1975) were much lower
(0.113-0.581^ ) than recorded from experimental
groups released in 1968. The authors attributed
the lower returns to stress caused by the place-
ment of two new dams (Lower Monumental and
Little Goose) in the migratory path of the juveniles
and from stress caused by the use of a fish pump in
the handling operation. The descaling and delayed
mortality percentages in the study at Little Goose
Dam indicated that stress in the collection, han-
dling, and hauling procedures was a factor.

Steelhead were not affected in the same manner
as chinook salmon in either this study or the ear-
lier studies at Ice Harbor Dam. In both studies
steelhead returned at a substantially higher rate
than chinook salmon. Estimated percentage re-
turns to Little Goose Dam of steelhead that had
been transported as juveniles ranged from 1.4 to
2.6%; returns from releases at Ice Harbor Dam in
1969 and 1970 ranged from 0.6 to 1.6%. Since
steelhead smolts are larger than chinook salmon
smolts, they may have been able to withstand the
rigors of collection, handling, and marking; the
very low delayed mortality percentages, shown in
this study for steelhead, support this reasoning.

Effect of Transportation on Homing

The transport/control ratios provide informa-
tion on the effect of transportation on homing. For
example, if no differential mortality occurred be-
tween groups, a steadily decreasing ratio of
transport/control numbers from the commercial
and sport fisheries below Bonneville Dam to the
spawning ground would indicate a loss of homing
ability or straying.

During the 3 yr of study , this type of comparison
could only be made from 1971 releases of juvenile
chinook salmon because the lower river commer-
cial fishery was closed after 1973. A comparison of
recovery ratios of adult fish from these releases
showed that the transport to control ratios were
2.86, 1.65, and 3.95:1 in the commercial fishery at
Little Goose Dam and the spawning grounds,

**Retum to the hatcheries included in computation of
transport/control ratio.

respectively. Although there was a variation in
the ratios from the lower river to the spawning
grounds, these ratios indicated that ability of
transported chinook salmon to home to either
their parent stream or Rapid River Hatchery was
not seriously damaged by transporting the fish
around the seven dams and reservoirs between
Little Goose and Bonneville Dams.

The ratios also imply that hatchery stocks were
benefited to a greater degree than wild stocks.
When returns to the spawning grounds were sepa-
rated from returns to Rapid River Hatchery and
separate transport/control ratios were computed,
the ratio for wild stocks became 1.5:1 and hatchery
stocks, 4.6:1. However, more data are needed re-
garding this aspect ( only six fish were recovered on
the spawning grounds from releases in 1973) be-
fore conclusions can be made on the differential
effect that transportation might have on hatchery
and wild stocks of chinook salmon. A comparison
between the ratio in the commercial fishery (2.8:1)
and at Little Goose Dam (1.6:1) also indicates that
transported chinook salmon may have been af-
fected differently from controls — if one assumes
that no differential mortality occurred between
control and transported fish as they moved upriver
and that wild and hatchery stocks were captured
at the same rate in the fishery as they were at
Little Goose Dam. Returning adults transported
as smolts may have been slightly disoriented or
remained for a longer period in the lower river,
thus permitting the fishery to take a dispropor-
tionate number of transported fish.

Ebel et al. (1973) found no difference in
transport/control ratios from the commercial
fishery to the spawning grounds when data from
releases at Ice Harbor Dam in 1968 were analyzed.

Disproportionate straying of adults from groups
transported as juveniles would also be an indica-
tion that homing behavior had been affected by
the transportation. No straying of either chinook
salmon or steelhead was observed in the earlier
study at Ice Harbor Dam. On the basis of re-
coveries of marked chinook salmon in the Des-
chutes River, some straying of chinook salmon
that had been transported as juveniles occurred in
this study. This instance of straying and the varia-
tions of transport/control ratios from the fishery to
Little Goose Dam indicate that the migratory
route lost by collecting the juveniles 130 km up-
stream at Little Goose Dam may be of some impor-
tance in determining homing behavior. A current

503

FISHERY BULLETIN: VOL. 78. NO. 2

study (Park^^) being conducted at Lower Granite
Dam (about 200 km upstream from Ice Harbor
Dam) by NMFS should provide further informa-
tion on this subject. Preliminary data obtained
from adult steelhead and chinook salmon return-
ing to Lower Granite Dam show that transport/
control ratios (2.5-2.7:1) obtained from experi-
ments in 1975 and 1976 are similar to those ob-
tained at Little Goose Dam. Insufficient data art
available at this writing to determine variations
in ratios from the lower river to the estuary or to
determine degree of straying.

SUMMARY AND CONCLUSIONS

The main objectives of the research at Little
Goose Dam were to determine the effect of trans-
portation on homing and survival of juvenile
chinook salmon and steelhead collected at Little
Goose Dam and released downstream and to com-
pare these results with an earlier study done at Ice
Harbor Dam where fish were transported a shorter
distance. The data clearly show that homing abil-
ity was not seriously diminished in either chinook
salmon or steelhead, and that survival of both
species was increased by transporting the fish to
release locations downstream from Bonneville
Dam.

A comparison of the results of this study with an
earlier study done by Ebel et al. (1973) and by
Slatick et al. ( 1975) at Ice Harbor Dam indicates
that the effect of collecting the fish about 130 km
farther upstream did not seriously diminish their
homing ability in comparison with homing ability
obtained in the experiment at Ice Harbor Dam.
The increases in survival of transported fish noted
in the study at Little Goose Dam were also similar
to those noted at Ice Harbor Dam, but estimated
percentage return of chinook salmon was substan-
tially lower than that achieved at Ice Harbor Dam.
Observations made throughout the study indi-
cated that chinook salmon returns might be in-
creased by reducing injury or stress during diver-
sion, collection, and handling process.

The main conclusions bearing on the effect of
transporting juveniles from Little Goose Dam to
release locations downstream from Bonneville
Dam were:

1) Analysis of transport/control ratios obtained

"Donn L. Park, Northwest and Alaska Fisheries Center, Natl .
Mar. Fish. Serv., NOAA, 2725 Montlake Boulevard East, Seat-
tle, WA 98112, pers. commun. December 1977.

from returning adults indicated that returns from
naturally migrating juvenile chinook salmon and
steelhead that were transported from Little Goose
Dam to release locations downstream from Bon-
neville Dam were increased from 1.1 to 15 times in
the fishery and to Little Goose Dam.

2) A significant (P<0.01) difference in benefit
from transportation was noted between chinook
salmon and steelhead; the greatest return and,
hence, the greatest benefit occurred with
steelhead.

3) Homing of adult fish that had been collected
as juveniles at Little Goose Dam and transported
several hundred kilometers downstream to Bon-
neville Dam apparently was not seriously di-
minished although a small portion (P<0.02%)of
the transported adult chinook salmon was known
to have strayed.

4) There was no significant (P <0.05) difference
in adult returns from two release sites tested (Dal-
ton Point and Bonneville Dam) of either steelhead
or chinook salmon.

5) Timing of migration of juvenile migrants
was not related to timing of adult returns to Little
Goose Dam.

6) Neither size nor ocean age of adult steelhead
transported experimentally as juveniles was sig-
nificantly (P<0.05) different from controls. Thus
transporting the fish did not appear to affect either
size or age of returning adult steelhead.

7) Although size of adult chinook salmon
transported as juveniles was not significantly
(P<0.05) different from controls, ocean age was.
Transportation, therefore, may have influenced
ocean age of returning adult chinook salmon.

ACKNOWLEDGMENTS

I thank Donn Park and Emil Slatick of the
Northwest and Alaska Fisheries Center, NMFS,
NOAA, for their help in carrying out the opera-
tions involved in collecting, marking, and hauling
of the thousands of fish involved in this experi-
ment and for their help in compiling the data for
analysis. I also wish to thank all of the personnel
of the Idaho Department of Fish and Game, Oregon
Department of Fish and Wildlife, Washington De-
partment of Fisheries, and the U.S. Fish and
Wildlife Service for their cooperation in obtaining
adult recoveries. I particularly wish to thank
Frank Ossiander, Northwest and Alaska
Fisheries Center, NMFS, NOAA, for his advice
regarding statistical analysis; Craig MacPhee,

504

EBEL: TRANSPORTATION OF CHINOOK SALMON AND STEELHEAD SMOLTS

University of Idaho, for his help and advice in
preparing this manuscript; and, of course, the
U.S. Army Corps of Engineers for their coopera-
tion in providing the facihties and majority of the
funding required to do this research. The review of
this paper by D. O. Everson, K. E. Hungerford, and
R. G. White of the University of Idaho is also ap-
preciated.

LITERATURE CITED

CHANEY, E., AND L. E. PERRY.

1976. Columbia Basin salmon and steelhead analysis
sxmimary report, September 1, 1976. Pac. Northwest
Reg. Comm., Vancouver, Wash., 74 p.
EBEL, W. J.

1974. Marking fishes and invertebrates. III. Coded wire
tags useful in automatic recovery of chinook salmon and
steelhead trout. Mar. Fish. Rev, 36(7): 10-13.

EBEL, W. J., D. L. Park, and R. C. Johnsen.

1973. Effects of transportation on survival and homing of
Snake River chinook salmon and steelhead trout. Fish.
Bull., U.S. 71:549-563.

EBEL. W. J., AND H. L. Raymond.

1976. Effect of atmospheric gas supersaturation on salmon
and steelhead trout of the Snake and Columbia Rivers.
Mar. Fish. Rev. 38(7): 1-14.

Ellis, C. H., and R. E. Noble.

[1961.] Barging and hauling experiments with fall
chinook salmon on the Klickitat River to test effects on
survivals. 1960 Annu. Rep. Wash. Dep. Fish., p. 57-71.
Groves, a. B., G. B. Coluns, and P. S. Trefethen.

1968. Roles of olfaction and vision in choice of spawning
site by homing adult chinook salmon (Oncorhynchus
tshawytscha). J. Fish. Res. Board Can. 25:867-876.
HaSLER, a. D., and W. J. WISBY.

1951. Discrimination of stream odors by fishes and its rela-
tion to parent stream behavior. Am. Nat. 85:223-238.

Jefferts, k. b., p. K. Bergman, and H. F. Fiscus.

1963. A coded wire identification system for macro-
organisms. Nature (Lond.) 198:460-462.

KOO, T. S. Y.

1962. Age designation in salmon. In T. S. Y. Koo (editor).

Studies of Alaska red salmon, p. 37-48. Univ. Wash. Publ.

Fish., New Ser. 1.
Park, D. L., and W. J. Ebel.

1 974 . Marking fishes and invertebrates. II. Brand size emd
configuration in relation to long-term retention on
steelhead trout and chinook salmon. Mar. Fish. Rev.
36(7):7-9.

Raymond, H. L.

1968. Migration rates of yearling chinook salmon in rela-
tion to flows and impoundments in the Columbia and
Snake Rivers. Trans. Am. Fish. Soc. 97:356-359.

1969. Effect of John Day Reservoir on the migration rate of
juvenile chinook salmon in the Columbia River. Trans.
Am. Fish. Soc. 98:513-514.

1979. Effects of dams and impoundments on migrations of

juvenile chinook salmon and steelhead from the Snake

River, 1966 to 1975. Trans. Am. Fish. Soc. 108:505-529.

Scholz, a. T., J. C. Cooper, D. M. Madison, R. M. Horrall,

A. D. HASLER, a. E. DIZON, and R. J. POFF.

1973. Olfactory imprinting in coho salmon: behavioral and
electrophysiological evidence. Proc. 16 Conf. Great
Lakes Res., p. 143-153.
Shapiro, S. S., and M. B. Wilk.

1965. An analysis of variance test for normality (complete
samples). Biometrika 52:591-611.
Slatick, E.

1976. Comparative retention of dart and jaw tags on
chinook salmon and steelhead trout during their spawn-
ing migration. Mar. Fish. Rev. 38(7);24-26.

Slatick, E., D. L. Park, and W. J. Ebel.

1975. Further studies regarding effects of transportation
on survival and homing of Snake River chinook salmon
and steelhead trout. Fish. Bull., U.S. 73:925-931.

Smith, J. R., and W. J. Ebel.

1973. Aircraft-refueling trailer modified to haul salmon
and trout. Mar. Fish. Rev. 35(8):37-40.
Smith, J. R., and W. E. Farr.

1975. Bypass and collection system for protection of
juvenile salmon and trout at Little Goose Dam. Mar.
Fish. Rev. 37(2):31-35.
Snyder, J. O.

1928. Salmon investigations. Calif. Fish. Game 14:
25-29.

505

IS OVULATION IN DOLPHINS, STENELLA LONGIROSTRIS
AND STENELLA ATTENUATA, ALWAYS COPULATION-INDUCED?

K. Benirschke, ^' ^ Mary L. Johnson. ^ and Rolf J. Benirschke'"^

ABSTRACT

This study of 58 nonpregnant uteri and ovaries of the spinner dolphin, Stenella longirostris , and the
spotted dolphin, S. attenuata, was undertaken to ascertain whether ovulation is copulation-induced
(reflex) or occurs spontaneously. Control specimens of immature, pregnant, and lactating females were
examined also and were used to define the normal reproductive events in uteri and ovaries of these
species. No differences were found between the two species. In about one half of the specimens we found
active corpora lutea of recent origin and in another 15^f of S. attenuata and 29'7c of S. longirostris,
corpora had fibrous centers but were hormonally active. No embryos were found and the endometrial
changes were such that early but unobserved pregnancies could be excluded. In 35% of the specimens
from S. attenuata the macroscopic diagnosis of corpus luteum was erroneous, while this was true of 21%
in S. longirostris. The corpora were degenerating and more resembled early corpora albicantia his-
tologically. In two of these specimens, endometritis was found and the endometrial histology gave
evidence of abortion in three. These findings are evidence that these Stenella species may sometimes
ovulate spontaneously and that macroscopic classification of corpora lutea in the past may frequently
have been erroneous.

The reproductive physiology of the spotted dol-
phin, Stenella attenuata, and spinner dolphin, S.
longirostris, has not been fully elucidated. In par-
ticular, it is presently unknown whether these
dolphins ovulate spontaneously or on reflex after
copulation. Some reasons to believe the latter
have been presented for Tursiops truncatus (Har-
rison 1977) and the same is implied for other
Cetacea. The finding of corpora lutea almost ex-
clusively in pregnant animals is the basis for this
assumption, and the purpose of this study is to
examine the genital tracts of 58 nonpregnant
animals with corpora lutea in detail in an attempt
to resolve this question. In a detailed study of
spotted dolphin, Perrin et al. (1976) found that of
242 females with corpora lutea, 229 (95%) were
pregnant. In a similar study of spinner dolphins,
Perrin et al. (1977) found that 2.8% of 536 adult
females contained corpora lutea whose presence
could not be explained by pregnancy, lactation, or
abortion.

The distribution of species with and without
reflex ovulation has been reviewed by Jochle
(1973). A surprisingly large number of species is

listed as having exclusively or predominantly
reflex ovulation, including Cetacea. Only pri-
mates, mouse and rat are cited as exceptions; how-
ever, modern studies suggest this to be an incom-
plete list. In several papers on Camelidae, reflex
ovulation is well supported by experimental
studies and by observations from abatoirs. Al-
though camels and their South American rela-
tives must be accepted as being reflex ovulators,
the carefully controlled study by England et al.
(1969) showed that "occasional spontaneous ovu-
lation occurred during the height of the breeding
season" in the llama. Lama glama.

In an attempt to gain additional information on
the reproductive physiology of S. longirostris and
S. attenuata, we examined the reproductive tracts
of animals recorded to possess corpora lutea while
not pregnant. Special attention was paid to ascer-
taining any reasons for the existence of these cor-
pora lutea, such as early undetected pregnancy
and an attempt was made to correlate the ovarian
status with endometrial changes.

MATERIALS AND METHODS

'Research Department, San Diego Zoo, P.O. Box 551, San
Diego, CA 92112.
^University of California, San Diego, La Jolla, CA 92093.
3San Diego Chargers, P.O. Box 20666, San Diego, CA 92121.

Manuscript accepted October 1979.
FISHERY BULLETIN: VOL. 78. NO. 2, 1980.

Reproductive tracts of female S. longirostris and
S. attenuata were collected at sea by observers
during commercial tuna fishing operations in the
southeastern Pacific Ocean (Perrin et al. 1976,

507'

FISHERY BULLETIN: VOL. 78, NO 2

1977). The organs were preserved in 10% Forma-
lin'' (Mallinkrodt) solution and stored at the
Southwest Fisheries Center (SWFC), National
Marine Fisheries Service, NOAA, La Jolla, Calif.
At the time of capture, a variety of observations
were recorded, including identified pregnancy,
size of the fetus, and lactation. These data, dates
and location of capture as well as related pertinent
information, are recorded in logs at SWFC. Here
also the ovaries were sliced at 1 mm intervals, and
observations such as the presence of corpora lutea,
corpora albicantia, and ovarian size were recorded
and correlated with capture information. Those
apparently gravid uteri whose ovaries had a cor-
pus luteum were dissected further and, occasion-
ally, small fetuses were identified by SWFC staff.
In addition, the present authors carefully dissect-
ed three intact uteri of the 1977 catches where
ovaries contained corpora lutea but in which
pregnancy had not been recorded.

For the purpose of the present study the repro-
ductive tracts of 53 nonpregnant dolphins, cap-
tured in 1976, and whose ovaries were recorded to
contain corpora lutea, were examined in detail. A
few specimens of 1975 and 1977 were also studied
and are included, bringing the figure to 58 genital
tracts. The tabulation of the reproductive condi-
tion of these tracts is showm in Table 1.

These specimens represent the majority of re-
productive tracts recorded to possess unexplained
corpora lutea in 1976. There were 67 in all but not
all of the specimens were in suitable condition for
inclusion in this study. Thus, several were too
severely autolyzed for proper evaluation; in
others, either the complete ovaries or uteri could
not be located in the specimen collection.

■•Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

Table l. — Reproductive tracts of Steneila spp. studied because
corpora lutea were found in the absence of pregnancy or lacta-
tion.

Species

1975

1976

1977

Stenella longirostris
S attenuate

38

15

In an effort to better understand the macro-
scopic and histologic features of dolphins with
known reproductive events, it was desirable to
select suitable control material from the same
stored collection. Six groups of specimens were
selected for this purpose and consisted of the fol-
lowing specimens: Group I, 3 tracts of immature S.
longirostris; Group II, 6 tracts of mature female S.
longirostris having no corpus luteum and, there-
fore, termed "resting"; Group III, 12 tracts of S.
longirostris with early pregnancy, the embryos
measuring from 1 to 53 mm long (1-5 g with
placenta); Group IV, 6 tracts of later pregnant
dolphins (AS. longirostris and 2 S. attenuata) with
fetal sizes ranging from 300 to 725 mm; Group V,
11 tracts of lactating, nonpregnant females (10 S.
longirostris and 1 S. attenuata); Group VI, the
experimental group, 58 tracts of nonpregnant
females possessing a corpus luteum (38 S. lon-
girostris and 20 S. attenuata; Table 1); for a total of
96 female genital tracts.

The gross examination of genital tracts by us
ascertained the following standard information:
Weight; length and width of uterine horns and
cervices; thickness of uterine walls at standard
locations. Histologic sections, stained with
hematoxylin and eosin, were prepared from stan-
dard locations of tubes, uterine horns, lower
uterine segments, and ovaries (Figure 1). Mea-
surements of uterine mucosa and muscularis were
made at low power microscopic examination with
the aid of a calibrated ocular micrometer. At his-
tologic examination the uterine findings (glands,
secretion, mitoses, edema, hyalinization, inflam-
mation) were compared with the ovarian activity.
Relevant photomicrographs were made with a
Zeiss Axiomat.

RESULTS
Controls
Group I, Immature Females

These three S. longirostris measured from 164 to
176 cm body length (Table 2) and possessed neither

Table 2.-

—Group I:

Immature controls, Stenella longirostris captured

on 20 February 1976.

Speci-

Dolphin
length
(cm)

Uterus
weight

(g)

Left horn of uterus

Right horn of uterus

men

no.

Length
(cm)

Endometrial Endometrial
fold (mm) valley (mm)

Myometrium
(mm)

Length
(cm)

Endometrial Endometrial
fold (mm) valley (mm)

Myometrium
(mm)

1
2
3

176
168
164

47
44
22

10
9
9

Average

1.49 0.60
1.34 0.39
1.10 0.60
1.31 0.53

0.54
0.60
0.42

0.52

9
9

7

209 075
1.07 0,36
1.07 0.36

1.41 0.59

060
0.62
0-54

0.58

508

BENIRSCHKE ET AL.: OVULATION IN DOLPHINS

MEASUREMENT IN CM
SECTION

Figure l. — Diagram of dolphin uterus. Arrows indicate mea-
surements taken in Stenella spp. and squares denote location of
histologic sections.

corpora lutea nor corpora albicantia. Because of
their size it was assumed that they were at the
verge of maturity. As shown in Figure 2, uterine
horns were of equal size, there were no stretch
marks and the endometrium was flat. Numerous
Graafian foHicles of varying stages of development
were present in both ovaries, but there was no
evidence of ovulation. The endometrium was thin
and composed of tubular glands possessing neither
secretion nor mitoses; the stroma was devoid of
inflammation and edema or hyalinization (Figure
3). The fallopian tubes were small and empty. In
all subsequent specimens, slides of fallopian tubes
were examined. No relevant changes were ob-
served and they are therefore not described
further. Also, sections of the lower uterine seg-
ment were found to make no contribution in the
assessment of reproductive state and are not in-
cluded in this analysis.

Group II, Mature Females

These six S. longirostris measured from 173 to
186 cm in length and were adjudged to be mature

Figure 2.— Immature uterus oi Stenella longirostris (no. 1, Table 2). Note the flat folds of endometrium, equal-sized horns, and lack of

serosal stretch marks (center)

509

FISHERY BULLETIN: VOL. 78, NO. 2

■'■5>.„

* • '*

.; '^

Arm- ^v / '"C**'" '-^^ '"'

yy

^^^

Figure 3. — Endometrium of immature Stenella longirostris (no. 3, Table 2). Tubular glands, little folding, thin endometrium, no

secretion or mitoses (hematoxylin and eosin x 60).

because of their size and the presence of at least
one corpus albicans. They were not lactating nor
did they possess a corpus luteum. The appropriate
measurements are set forth in Table 3. In general,
the horns were asymmetrical but not so markedly
as those of lactating females (Group V), with the
exception of specimen no. 4 (Table 3). The wrin-
kled serosa and congestion of endometrium of this
animal's left horn indicated recent pregnancy
(Figure 4). All but one female of this group had
"stretch marks" which we assumed to be an indi-
cation of previous pregnancy. Microscopic study of
the corpora albicantia in this group allowed some
correlation with the endometrial findings. Thus,
the apparently most recently delivered uterus

(Figure 4) had a still cellular corpus albicans (Fig-
ure 5) and, inflammatory cells, hemosiderin mac-
rophages and stromal hyalinization were observed
in the congested endometrium (Figure 6). In the
others, judged to have had past pregnancies, the
corpus albicans was less cellular, more hyalinized
and shrunken. The endometrium did not appear to
be stimulated, had thin epithelium, no mitoses but
scattered macrophages were in the process of re-
moving debris. Apparently later still, Graafian
follicle development commences, uterine horns
are of nearly equal size and endometrial glandular
redevelopment occurs with mitoses, glandular
convolutions, occasional epithelial vacuoles, and
stromal edema (Figure 7).

Table 3. — Group II: Mature controls, Stenella longirostris, for 1976.

Speci-

Month of

Dolphin
length

Uterus
weight

Left horn of uterus

Right 1

lorn of uterus

men

Length

Endometrial

Endometrial

Myometrium

Length

Endometrial

Endometrial

Myometrium

no.

capture

(cm)

(g)

(cm)

fold (mm)

valley (mm)

(mm)

(cm)

fold (mm)

valley (mm)

(mm)

1

February

186

108

13

1-79

0.75

1.49

10

1,94

0.66

1.49

2

February

181

123

17

2.70

0.75

1.04

15

2.24

0.90

0.90

3

February

179

136

13

1.79

0.66

1.19

11

1.19

0.75

1.64

4

February

178

152

17

2.99

0.90

2.39

8

4.78

0.90

1.94

5

July

175

98

16

1.64

0.30

0.90

18

1.49

0.60

1.49

6

June

173

110

23

4.18

0.90

1,49

18

3.58

1.04

1.49

Average

2.52

0.71

1.42

254

0.81

1.49

510

BENIRSCHKE ET AL.: OVULATION IN DOLPHINS

<•'. ♦:>,

^.:^^^i0m^^^

)^f^.

Figure 4. — Mature animal's uterus, presumably recently delivered (no. 4, Table 3). Note larger left horn with congestion and serosal

stretch marks.

' / >

^«v

^N>

V».

^>1..

^.

-*<*/

Tv*.

. * '•---

Figure 5. — Corpus albicans of animal in Figure 4. At right is former follicular cavity, replaced by young fibroblastic tissue. Dark cells
in central (former luteal) band of corpus albicans suggest recent conversion of corpus luteum to corpus albicans (hematoxylin and eosin
X 120).

511

FISHERY BULLETIN: VOL. 78, NO. 2

■«>.

' V '^ if-

■,:n

(X

r \4f

V

.4

•» I

Figure 6. — Endometrium of animal in Figures 4 and 5, surface at right. Infiltration of stroma with macrophages; sparse glands;
hyalinization of stroma and larger vessel walls at H (hematoxylin and eosin x 120).

Group III, Early Pregnancy

There were 12 S. longirostris in this group
measuring from 166 to 188 cm in length (Table 4).
With the exception of the first specimen listed, the
left uterine horn was the larger. In this excep-
tional animal, the corpus luteum was also on the
right and no corpus albicans was found in the left
side. Uterine size and weight did not correlate well
with embryonic size (1-53 mm) or weight (1-5 g).
The embryos had been removed previously and
their placentas had apparently not yet implanted.

The larger (pregnant) horn had a congested en-
dometrium and distended lumen (Figure 8).

This is an important control group for the ex-
perimental Group VI whose uteri were empty de-
spite the presence of a corpus luteum. Thus, it is
noteworthy that even in small embryos (Figure 9)
the placental membranes are of appreciable size
and they grow rapidly (Figure 10) so that they are
not easily overlooked in dissections. Early limb
bud development could be recognized in embryos
sized 5 mm or more.

Table 4.— Group III:

Early pregnant control

s, Stenella longirostris. All from February

1976 except

no. 1 1 captured in May

1976.

Speci- Dolphin

Uterus
weight

Left horn of uterus

Right horn of uterus

Fetus

men length

Length

Endometrial

Endometrial

l\/1yometrium

Length

Endometrial

Endometrial

Myometrium

Length

Weight

(g)

no. (cm)

(g)

(cm)

fold (mm)

valley (mm)

(mm)

(cm)

fold (mm)

valley (mm)

(mm)

(mm)

1 176

140

10

6.87

1.49

1.49

15

5.37

1.49

1.49

1

1

2 172

171

20

—

—

—

12

5.67

1 19

1.49

2

1

3 178

145

15

5.07

0.90

1.49

12

4.03

1.04

1.94

2

1

4 181

208

28

2.69

1.19

0.96

20

2.69

090

0.78

5

1

5 188

163

20

2.83

0.75

0.04

15

299

0,75

1.04

5

2

6 172

192

19

5.97

1 19

1.04

12

6,87

1.79

1.49

5

2

7 166

204

17

6.87

0.75

0.90

11

7.46

1.34

0.75

5

2

8 176

212

25

5.37

1.49

1.04

15

388

0.60

1.19

5

2

9 167

227

19

6.87

1.19

1.94

13

—

2.39

1.49

5

2

10 184

229

28

2.09

0.36

1.04

15

3.58

0.90

1.19

5

2

11 180

144

17

4.78

1.19

1.04

13

2.99

1.19

1.19

8

2

12 180

187

23

1.04

0.35

0.90

16

2.09

0.30

0.90

53

5

Average

4.68

0.99

1.17

4.33

1.16

1.25

512

BENIRSCHKE ET AL.: OVULATION IN DOLPHINS

Figure 7. — Endometrium undergoing eariy stimulation, presumably after past pregnancy (no. 3, Table 3). Glands are more numerous
and coiled. They contain occasional epithelial secretory vacuoles and mitoses. Focal edema (E) of stroma commences (hematoxylin and
eosin x 60).

Figure 8. — Early pregnant uterus with distended left horn and hyperemia of endometrium (no. 4, Table 4).

513

FISHERY BULLETIN: VOL. 78, NO. 2

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mmmmmmmm

■MM!

2

«■*■*■■'■▼■■▼

! I

Figure 9. — Smallest (2 mm) normal embryo at arrow with long, filmy placental membranes (no. 3, Table 4).

Figure lO. — Five mm embryo (arrow) with huge placental membranes (no. 9, Table 4).

The cells of the corpus luteum of all of these
animals were well supported, and the central
fibrin clot was invaded by vessels and fibroblasts
in all but one animal (no. 3, Table 4; Figure 9).
This was also the smallest embryo other than that
of the aberrant right specimen (no. 1, Table 4). Its

514

corpus luteum is showoi in Figure 11 and is readily
distinguishable from the small luteal mass found
in the experimental group.

The endometrium had characteristic changes
that should allow the histologic diagnosis of early
pregnancy. First, the tips of endometrial folds be-

BENTRSCHKE ET AL.: OVULATION IN DOLPHINS

f .

J'

V ' "'

*

*>

'^ --- •.

e.

Figure ll. — Portion of active corpus luteum of earliest pregnancy with cavity at bottom right and ovarian stroma (S) at top left (no. 3,

Table 4; hematoxylin and eosin x 100).

come edematous (Figure 12). At this stage the
glands are empty and crowded in the basal por-
tions. Their epithelium lacked mitoses. With ad-
vancing pregnancy the edema diminished while
secretion accumulated in glands. Most charac-
teristic, however, is the development of a rich
capillary network with congestion, most notably
in the superficial strata (Figure 13). Despite the
presence of significant chronic endometritis in two
cases, normally developing early embryos were
found.

Group IV, Late Pregnancy

We selected four S. longirostris and two S. at-
tenuata between 165 and 199 cm in length and

embryos of 300-725 mm in length (the S. attenuata
fetuses were lost at sea) for this comparison (Table
5). All implantations were in the larger left horn
but a portion of the membranes traversed into the
right horn. The large single corpus luteum of these
six specimens was present in the left ovary.

The superficial endometrium was extremely ar-
borized with distended glands into which the villi
of the epitheliochorial placenta penetrated, form-
ing an intimately interdigitating connection (Fig-
ure 14). The basal endometrium was edematous
and glands contained secretion. With advancing
gestation the villous arborization increased. The
corpus luteum had characteristic appearance
(Figure 15). Among the plump, eosinophilic luteal
cells streamers of fibrocytes gave the first appear-

Table 5. — Group IV: Late pregnant controls. Specimen no. 1-4 Stenella longirostris, captured October 1978; no. 5-6 S. attenuata,

captured July 1976.

Speci-
men
no.

Dolphin

length

(cm)

Weight of

placenta

and uterus (g)

Left uterine horn

Right

uterine horn

Fetus

Length
(cm)

Endometrial
fold (mm)

Endometrial
valley (mm)

r^yometnum
(mm)

Length
(cm)

Endometrial
fold (mm)

Endometrial
valley (mm)

Myometrium
(mm)

length
(mm)

1

197

617

—

0.60

—

—

—

0.75

300

2

182

703

42

—

—

—

21

—

—

—

429

3

165

700

60

2.69

0.60

0.75

26

5.97

1.49

1.19

557

4

168

982

64

1.79

0.60

0.60

20

—

—

—

725

5

—

730

—

—

—

1.79

12

—

—

0.75

—

6

—

965

—

—

—

2.08

21

—

—

0.60

—

515

FISHERY BULLETIN: VOL. 78, NO. 2

.* .;'<» O

oo

'\-<e0'

6

CO o^> ^

0

,^ CO o'^^ **

Figure 12. — Endometrium of eariiest pregnancy ( Figures 9, 11; no. 3, Table 4). Uterine lumen (L) at right. Note the marked edema
in superficial stroma, congestion (C) and compact arrangement of secretory glands at left (hematoxylin and eosin x 50).

»V"*''

j:^'

.^ ^VV

h

Figure 13. — Typical capillary distension (arrows) and neovascularization of endometrial stroma immediately beneath surface
endometrial epithelium in early pregnancy (no. 9, Table 4; hematoxylin and eosin x 300).

516

BENIRSCHKE ET AL.: OVULATION IN DOLPHINS

^

%^::i^^-^..'pi^'^

*%;>-- _ >,

i-^

Figure 14. — Placental attachment with basal endometrial glands (G) at left and interdigitating villi (V) within distended glandular

Ixmiina (no. 2, Table 5; hematoxylin and eosin x 80).

i* !' ' >l W ►'• '^

Figure 15. — Corpus luteum of uterus shown in Figure 14, the organized cavity is at bottom right. Note well-supported dark luteal cells

with fibrocytes in between (hematoxylin and eosin x 150).

517

ance of degeneration. This connective tissue be-
came less apparent with advancing pregnancy.

Group V, Lactating Females

Six specimens were selected measuring from
167 to 182 cm iS. longirostris) and one 202 cm (S.
attenuata). They had been identified as lactating
during dissection at sea. It is a heterogeneous
group as judged by uterine size, endometrial his-
tology, and the appearance of the corpora albican-
tia (Table 6). Some animals must have delivered
very recently as evidenced by the marked dispar-
ity of uterine horn size, hyperemia, and the recent
degenerative changes in the corpus luteum, while
others had more equal horns and well-advanced
corpora albicantia. No active corpora lutea were
present while at least one corpus albicans was
found in all specimens. Some corpora albicantia
had chronic inflammatory cell infiltration and
four ovaries had Graafian follicles maturing at
various stages. Stretch marks were present on the
uterine serosa and the endometrium had typical
involutional changes histologically. Beneath the
surface epithelium there was a thin zone of
hyalinization in most specimens, while recently
delivered animals had prominent, congested ves-
sels in myometrium and endometrium. Some of
these had hyalinized walls also. In a majority of
endometria a mild chronic inflammatory infiltrate
was present; one had acute pyometritis. No
mitoses or edema was present, the endometria ap-
peared "resting." Hemosiderin-laden mac-
rophages in endometrium or lower uterine seg-
ment were present in three, presumably due to
interstitial hemorrhage at recent delivery. Such
deposits were found in only one other female (Con-
trol Group II) whom we suspect to have delivered
recently but who was not recorded as lactating.

FISHERY BULLETIN: VOL. 78, NO. 2

Experimental Groups

Group VI, Nonpregnant Animals
With Corpus Luteum

The 58 animals of this group were not detected
to be pregnant at sea but had a corpus luteum
present in one of their ovaries. The group is di-
vided into three subgroups made up of specimens
with corpora lutea at different stages of develop-
ment or involution.

GROUP Via.— These 28 animals (19 S. lon-
girostris; 9 S. attenuata) measured 163-191 cm in
length, and the group was of special importance
because the corpora lutea were judged to be the
youngest. For this reason, an early pregnancy
could have been overlooked. Two intact uteri were
dissected meticulously, including the fallopian
tubes. Neither embryos nor placentas were iden-
tified in any of the 28 specimens. From the dates of
capture (Table 7) it will be noted that most (17)
were captured in February, as is also true of early
pregnant animals (Table 4). These figures must be
interpreted with caution, however, because of dif-
ferent catch sizes on various cruises. The macro-
scopic findings were not uniform in that uterine
weight varied between 90 and 467 g, the horn sizes
varied considerably and endometrium was as
often congested or mucus-covered as not. Only
once was the corpus luteum found in the right
ovary.

The histologic appearance of the endometrium
correlated neatly with the corpus luteum devel-
opment and grouping was undertaken accord-
ingly. Those specimens whose corpus luteum had a
central fibrin-filled cavity were placed into Group
Via; those whose cavity was replaced by fibrous
tissue were adjudged to have ovulated earlier and

Table 6. — Group V: Lactating controls. Specimen no. 1-10 Stenella longirostris; no. 11 S. attenuata.

Left uterine horn

Right

uterine horn

Graaf-

Cor-

Speci-

Month and

Dolphin

Uterus

Endometrial

Endometrial

t^yome-

Endometrial

Endometrial

Myome-

ian

pus

men

year of

length

weight

Length

fold

valley

trlum

Length

fold

valley

trium

folli-

albi-

no.

capture

(cm)

(g)

(cm)

(mm)

(mm)

(mm)

(cm)

(mm)

(mm)

(mm)

cle

cans

1

Feb. 1976

171

113

14

2.24

0.21

1.64

8

—

0.60

0.90

no

-1-

2

Feb. 1976

182

112

13

2.29

0.57

2.54

9

2.99

0,66

1,04

+

-h

3

Feb, 1976

171

73

11

1.73

0.24

1.64

9

1.19

0.39

1,94

+

-H

4

June 1976

171

65

12

1.34

0.30

2.99

11

1.79

0.30

2,09

no

-F

5

June 1976

167

126

20

3.88

0.60

1,04

13

3.58

1.64

1.34

-1-

-1-

6

Feb. 1976

174

74

15

1.79

0.60

1.49

8

2.24

0.75

0.90

no

-1-

7

Feb. 1976

175

109

17

2.99

0.24

1.79

8

299

0.66

0.90

no

-1-

8

Feb. 1976

174

198

21

7.91

0.90

2.09

13

6.87

1.13

1.19

no

■V

9

Feb. 1976

173

112

12

4.78

1.04

1.04

10

2.09

0.45

1.06

no

■¥

10

June 1976

173

60

13

1.49

0.75

2.09

12

1.19

0.60

0.75

-1-

■1-

11

Sept. 1977

202

550

—

1.64

0.75

2.09

—

1.64

0.60

1.34

no

^-

S. longirostris —

- Average

3.04

0.56

1.84

2.77

0.72

1.21

518

BENIRSCHKE ET AL.: OVULATION IN DOLPfflNS
Table 7. — Group via: Experimental group with early corpora lutea. Specimen no. 1-19 Stenella longirostris; no. 20-28 S. attenuata.

Speci-
men

Month and
year of

Dolphin
length

Uterus

Left horn of uterus

Right horn of uterus

weight

Length

Endometrial

Endometrial

Myometrium

Length

Endometrial

Endometrial

Myometrium

no.

capture
Feb 1976

(cm)
184

(g)

120

(cm)

fold (mm)

valley (mm)

(mm)

(cm)

fold (mm)

valley (mm)

(mm)

1

15

5.37

1 72

1.04

19

2.69

1.04

0.75

2

Apr 1976

182

132

14

4.78

1 49

060

14

5.67

1.19

0.75

3

Feb 1976

171

—

26

418

1.49

1 34

16

4 48

1.34

0.60

4

Feb. 1976

176

—

16

4.48

1 94

1 49

14

4.02

1.49

1.34

5

Feb 1976

173

—

16

2.84

1.19

0,45

18

—

—

0.75

6

Feb 1976

149

90

15

3.13

0,90

096

15

4.18

1 19

1.04

7

Feb 1976

180

119

25

6.56

0,75

1,34

13

4.18

1.04

1.04

8

Feb 1976

180

166

20

2.53

0.75

1.04

14

4 18

1 79

0.90

9

Feb 1976

184

217

25

4.48

1.49

1.19

20

3.28

1.40

0.90

10

Feb 1976

183

224

18

8.66

1.19

1.34

15

5,97

0.75

1.04

11

Feb. 1976

181

167

16

4.48

1 19

1,94

14

597

1.04

0.90

12

Feb. 1976

188

180

18

8.35

060

1,79

12

4.78

1.19

090

13

Aug, 1976

163

127

16

8.96

090

0,90

12

448

1.49

1 19

14

Feb 1976

168

158

21

3.58

1.19

269

13

5,07

1.79

1.64

15

Feb. 1976

177

118

20

3.13

090

1.49

14

4,18

0.60

096

16

Feb. 1976

167

111

17

3.28

209

1,04

15

3,58

1.79

0.75

17

Feb 1976

176

—

22

4,78

096

1.34

14

3,58

0.75

1.04

18

Feb 1976

171

—

14

4,18

1,64

1.19

11

328

1.49

1.04

19

Aug 1976

167

165

22

5.97

2.99

1.49

21

388

1 64

0.90

S

longirostns -

— Average

4.93

1.33

1,29

4,30

1.28

077

20

Oct. 1976

174

190

29

388

060

1,49

18

3.28

0.84

209

21

Feb 1976

189

192

23

298

0,60

1.49

19

2.38

1 19

1,49

22

Aug, 1976

176

390

35

7.46

1,49

1.64

15

—

1,19

1,49

23

Oct, 1975

191

156

25

4.93

1.04

1.34

14

3.58

1.04

1 34

24

Aug 1976

174

333

26

7.16

1.79

1.94

16

2.99

0.75

1.19

25

May 1976

185

467

27

6.57

1,19

239

17

4.48

0.90

1 64

26

Apr, 1976

180

154

18

418

1,19

090

20

3.28

1,79

1 04

27

June 1977

185

190

12

269

0.90

1 19

17

1.79

0.30

075

28

June 1977

186

220

13

284

0.90

0.90

12

239

0.45

1 49

S, attenuata

— Average

4.74

1.01

1.48

302

0.94

1.39

placed into Group VIb. Because of the potential
insight these specimens give into the dynamics of
ovarian/endometrial relationships, these speci-
mens are described in more detail.

When the Graafian follicle has recently rup-
tured, stromal vessels infiltrate the granulosa
layer (Figure 16). The follicular lumen is filled
with serous fluid and fibrin but rarely contains
blood as in many other species. The corresponding
endometrial stroma is edematous, the glands are
tubular, lack secretory vacuoles and contain
mitoses (Figure 17). When the corpus luteum is
better established, the central cavity is more pro-
nounced, capillaries have penetrated the
granulosa layer, and, in contrast to its cells in
specimens from early pregnancy (Figure 11), they
possess less cytoplasm, being less plump (Figure
18). It should again be noted that the cavities
rarely contain red blood cells. The endometrial
glands at this stage are more crowded, have more
coiling, and still possess mitoses, but the earliest
appearance of epithelial cytoplasmic vacuoles oc-
curs (Figure 19). The vacuolization appears to
commence under the endometrial surface and
penetrates slowly throughout the entire thickness
of the endometrium (Figure 20). At the same time,
fibroblastic infiltration of the corpus luteum cav-
ity has taken place and the luteinized cell wall has

folded remarkably. Very few mitoses were found
in superficial endometrial cells at this stage and in
the final stages before the central corpus luteum
cavity has been completely filled in by fibrous tis-
sue, the endometrial stromal edema disappears, to
be replaced by coiled secretory glands (Figure 21).
No mitoses exist, nor is secretion exuded into the
glandular lumina. Such corpora lutea are ex-
pected to be associated with early pregnancy par-
ticularly because of the conspicuous size of
granulosa luteal cells. Since no embryonic sacs
were found, it is then also not surprising that the
endometrium possesses different histologic fea-
tures from those whose comparable corpora lutea
were associated with early pregnancy (Figures
11-13). Perhaps this climaxes endometrial de-
velopment before regression of corpus luteum
occurs.

One of these specimens from an October catch
(no. 20, Table 6) had a fresh corpus luteum with
fibrin-filled cavity and unusual endometrium. The
stroma beneath the surface epithelium had the
typical hyalinization of the post partum state, yet,
early secretory endometrium was found in deeper
layers (Figure 22). Moreover, hemosiderin pig-
ment was found. It would appear that this was the
first and infertile ovulation after a recently past
pregnancy which is further supported by the

519

FISHERY BULLETIN; VOL. 78, NO. 2

■■■<

•

v..<M^^^

I

•%r

■'♦*',.

- W«*-"

OS

Figure 16.— Very fresh corpus luteum with focal hemorrhages (left), luteinized granulosa cells (LG) infiltrated by capillaries (arrows)
sprouting from the ovarian stroma (OS) (no. 18, Table 7; hematoxylin and eosin x 400).

**4

-^i^'-i\ F-

^

.-*»

M m..

* 1

•?k-. '^

/

%

*<! » **^

« •

/

f?/^'

Figure 17. — Endometrium of specimen in Figure 16 with glandular mitosis at arrow. Note stromal edema (hematoxylin and

eosin x 400).

520

BENIRSCHKE ET AL.: OVULATION IN DOLPHINS

Figure 18. — Young corpus luteum in nonpregnant animal. Note central cavity (top) is filled with fibrin and granulosa layer is
penetrated by capillaries (black). Size of granulosa lutein cells is much smaller than in Figure 11, an early pregnant specimen (no. 3,
Table 7; hematoxylin and eosin x 100).

. I WS1i i^^ /!■<' ' •?#.>. . : , Ci

•t#'. ,♦ >>

f

Figure 19. — Endometrium of same specimen as Figure 18 to show increased glandular coiling and earliest appearance of light

cytoplasmic vacuoles in dark epithelial cells (hematoxylin and eosin x 100).

521

FISHERY BULLETIN: VOL. 78, NO. 2

•- «

>* '

\h^

'^^^ V

>*•"

X

Figure 20

. — Endometrium of nonpregnant Stenella longirostris with well-established corpus lutei
endometrial glands as well as stromal edema (no. 10, Table 7; hematoxylin and

eosin x 100).

» *

Figure 21. — Final stages of secretory change in endometrium of nonpregnant Stenella longirostris with advanced corpus luteum.
Crowding of secretory glands occurs in stroma that has now lost its edema. No secretion in lumen. Endometrial cavity at right (no. 16,

A. .^.^ivij i,i. — i iiicii ouigcs ui secretory cnange in enaomeinum wi iiunj^icgnam- .jic><.cini ^^.i-gi.. i^oi.. lo ..»v.. ia^,«..w^- ^v-., .

Crowding of secretory glands occurs in stroma that has now lost its edema. No secretion in lumen. Endometrial cavity at right (
Table 7; hematoxylin and eosin x 100).

522

BENIRSCHKE ET AL.; OVULATION IN DOLPHINS

??•!£?:•'• vS? ?

I

Figure 22. — Endometrium of presumably delivered Stenella attenuata whose ovary had a fresh corpus luteum. Endometrial cavity top
left, hyalinized stroma (HyS) beneath surface epithelium and secretory glands (SG) beneath this layer (no. 20, Table 7; hematoxylin and
eosin x 100).

marked discrepancy of the uterine horns (29 cm
left; 18 cm right).

GROUP VIb.— These 15 animals (US. lon-
girostris; 4 S. attenuata) were found to be non-
pregnant but had well-established corpora lutea
with completely organized cavities, the luteal cells
appeared well supported (Table 8). Their lengths

varied from 169 to 198 cm and uterine weights
were between 110 and 580 g. One of these speci-
mens had not been opened, was carefully dissected
by us, and found to be nonpregnant. Again, most
(12) were from February catches, many uteri had
stretch marks from former pregnancy, and in two
ovaries the corpus luteum was found on the right.
The secretory endometrium of almost all these

Table 8. — Group VIb: Experimental group with well-supported corpora lutea. Specimen no. 1-11 Stenella longirostris; no. 12-15

S. attenuata.

Speci-
men

Month and

Dolphin
length

Uterus

Left uterine horn

Right uterine horn

year of

weight

Length

Endometrial

Endometrial

IVIyometrium

Length

Endometrial

Endometrial

Myometrium

no.

capture

(cm)

(g)

(cm)

fold (mm)

valley (mm)

(mm)

(cm)

fold (mm)

valley (mm)

(mm)

1

Feb 1976

191

281

21

5.97

1.19

0.66

18

5.07

1.64

0.60

2

Feb. 1976

169

—

17

2.23

1.64

0.90

14

1.94

1.19

0.84

3

Feb. 1976

180

—

19

4.18

1.04

0.75

13

3.28

1.04

0.75

4

Feb. 1976

184

142

18

7.16

0.84

1.49

16

6.57

1.49

1.79

5

Feb. 1976

180

149

22

5.67

0.90

1.19

16

4.33

1.04

1.19

6

May 1976

178

268

24

448

1.04

1.94

19

2.84

0.75

1.34

7

Feb. 1976

180

194

20

3.58

1.34

1.34

16

3.73

1.94

0.90

8

Feb. 1976

178

227

21

4.18

0.75

1.19

13

3.28

1.19

1.04

9

Feb. 1976

181

148

16

3.58

1.19

1.34

11

328

1.19

1.19

10

Feb. 1976

170

117

18

448

1.04

1.04

15

3.88

1.04

1.49

11

Feb. 1976

181

166

21

1.79

0.90

1.19

12

2.99

1.04

1.04

S

. longirostris ■

— Average

4.30

108

1.18

3.74

1.23

1.11

12

Feb. 1976

193

250

24

5.67

2.09

1.34

23

2.84

1.19

0.90

13

Feb. 1976

184

110

11

3.28

0.90

1.04

10

4.18

0.90

0.84

14

June 1977

185

240

22

2.39

1.19

1,79

17

1.79

0.60

1.88

15

Nov. 1975

198

580

37

5.67

1.49

2,09

21

6.87

1.49

2.39

S. attenuata ■

— Average

4.25

1.42

1.57

3.92

1.05

1.50

523

FISHERY BULLETIN: VOL. 78, NO. 2

specimens showed great similarity with those
shown in Figures 20 and 21. The amount of edema
varied slightly and so did the glandular vacuoliza-
tion. No secretion was found within the glands
although frequently there was thick mucus cover-
ing the endometrial surface on gross examination.
The luteal cells were supported, not degenerated
but less plump than in early pregnancy. The only
difference was the complete fibrosis of the central
cavity, probably insufficient findings for a mean-
ingful separation of some specimens from the pre-
vious group Via. Of course, no capillary prolifera-
tion of the superficial endometrium, so typical of
pregnancy was evident.

One specimen is probably misclassified (no. 15,
Table 8). Not only is this the largest uterus (580 g)

with pronounced stretch marks (Figure 23) but
also it exhibits a differing histologic appearance of
the endometrium (Figure 24). This shows acute
endometritis in a mucosa which otherwise had all
of the characteristics of pregnancy. The corpus
luteum was well supported with large plump cells.
In all likelihood this S. attenuata had very re-
cently delivered. This is from a November catch
and it is impossible to determine whether this
represented a full-term pregnancy since Perrin et
al. (1976) showed that calving does occur in this
species in the winter, although less commonly. It
may well be that this inflammatory exudate in the
superficial endometrial regions represents the
normal immediately post partum event. This
would explain the persistence of an active corpus

Figure 23.— uterus of recently Ae\\\eredStenella attenuata, no. 15, Table 8. Note stretch marks of left horn,

congestion and disparate size of horns.

524

BENIRSCHKE ET AL.: OVULATION IN DOLPHINS

"i

^

p

o

<

o

o

«

(

Figure 24. — Endometrium of uterus in Figure
23. The marked stromal edema ( E) and distended
glands (G) of basal endometrium are tj^pical of
late pregnancy. The superficial endometrium is
infiltrated by polymorphonuclear leukocytes that
exude into the glandular limiina (arrow). No sur-
face stromal hyalinization has yet taken place.
The former interdigitation of placental villi with
surface endometrium can be imagined from the
irregularities the surface presents (hematoxylin
andeosin x 100).

luteum, presumably destined to involute shortly.

GROUP Vic— This composes 15 animals (8 S.
longirostris; 7 S. a^^enuato) measuring 162-193 cm
whose features are listed in Table 9. These non-
pregnant dolphins possessed histologically re-
gressing corpora lutea. Eight animals in fact had
corpora albicantia and were probably misclas-
sified by the gross observations because the corpus
luteum in each case was recently involuted, had
still some vascularization and microscopic in-
flammation. Similarly, the endometria in these
specimens usually had inflammation and hyalini-

zation and were most likely recently delivered.
This is further supported by the disparity in
uterine horns. These animals were not listed as
lactating either because this feature had been
overlooked or perhaps the calves had died or were
aborted. This material does not allow this dif-
ferentiation.

Six of the remaining seven animals had corpora
lutea with histologic signs of early degeneration.
Two had late secretory endometrium and this
would likely to have involuted upon further re-
gression of the corpus luteum since pregnancy did
not occur. Two animals had marked chronic en-

525

FISHERY BULLETIN: VOL. 78, NO. 2

Table 9.— Group Vic: Experimental group with degenerating corpora lutea. Specimen no. 1-8 Stenella longirostris; no. 9-15 S.

attenuata.

Speci-
men

Month and
year of

Dolphin
length

Uterus
weight

Lett horn of uterus

Right horn of uterus

Length

Endometrial

Endometrial

Myometrium

Length

Endometrial

Endometrial

Myometrium

no.

capture

(cm)

(g)

(cm)

fold (mm)

valley (mm)

(mm)

(cm)

fold (mm)

valley (mm)

(mm)

1

Sept 1976

162

250

32

5.22

1.19

2.24

15

3.88

1.19

1.64

2

Feb 1976

175

252

25

10.14

2.09

1.19

12

—

—

1.04

3

May 1976

183

273

25

4.93

1.04

1.19

15

3.88

1.19

1.04

4

Feb, 1976

179

—

23

4.78

0.90

1,19

14

4.48

1,94

1 34

5

Feb 1976

185

—

21

2.09

090

090

16

1,19

1,04

0,75

6

Feb. 1976

186

—

22

2.24

0.75

0,90

16

1,04

0,45

0 90

7

Feb. 1976

186

291

25

5.37

1.19

1.34

14

3,58

0,90

1 04

8

Mar. 1976

189

197

17

5.37

1.19

1.64

13

3.28

1,04

1,04

S. longirostris

— Average

5.02

1.16

1,32

3.05

1,11

1,10

9

Aug, 1976

172

145

—

1.64

0.45

0.90

—

2.09

0,60

0,60

10

Feb 1976

180

122

18

5.79

1.34

1.64

15

6.57

1 19

1 04

11

Feb, 1976

185

—

23

3.13

0.90

1.34

18

2.39

0,60

1,04

12

May 1976

191

205

18

4.18

0.75

1.79

18

2.39

0-60

1 79

13

June 1976

193

375

22

8.80

1.94

2.09

15

6.42

1,79

1,79

14

Aug, 1976

179

356

30

6.57

1.04

1.79

16

5.07

0,75

0.90

15

Apr 1976

185

305

25

4.18

090

1.49

13

3.28

0-90

1 64_

S. atter^uata ■

— Average

4.90

1.05

1.60

4.03

092

1 26'

dometritis. Two others had marked endometrial
stromal edema in addition to having horns of dif-
ferent lengths. The possibility of abortion exists in
these animals but this cannot be proven. Finally,
one animal of this heterogeneous group (no. 12,
Table 9) had equal uterine horns ( 18 cm) and pos-
sessed corpora albicantia in addition to a de-
generating right-sided corpus luteum. The
endometrium with hyalinization and capillary
development suggested recent pregnancy but be-
cause of the size of the uterus (205 g) it appears
likely that a recent right-sided pregnancy had
ended in abortion.

DISCUSSION

Although conclusive proof is lacking, the results
support the notion that dolphins may ovulate
spontaneously, at least at times. Control material
of different reproductive phases (96 specimens) of
the two species of dolphin investigated, the east-
ern spinner dolphin, S. longirostris , and the spot-
ted dolphin, S. attenuata, provided a life history of
the macroscopic and microscopic events in the
uteri and ovaries of these species for the first time.
The principal findings were the following: In three
immature animals neither corpora lutea nor cor-
pora albicantia were present in the ovaries but
Graafian follicles were forming. The endometrium
had tubular glands. Six mature animals without
corpus luteum all were found to have one or more
corpus albicans, the horns were disparate in size,
five had stretch marks as an excellent sign of
former pregnancy, in most the inactive endome-
trium possessed inflammatory cells, hyalinization,

had hemosiderin macrophages as indications of
former pregnancy. Eleven of twelve early preg-
nant animals with embryonic sizes of 1-53 mm
had the pregnancy in the left horn; one in the right
on which side the corpus luteum was also located.
The endometrium of the earliest pregnancy had
characteristic changes that should allow preg-
nancy diagnosis even if the embryo is overlooked
or lost. Six late pregnant specimens had their cor-
pus luteum in the left ovary, typical epitheliocho-
rial implantation and again characteristic en-
dometrial histology. Eleven lactating females
were studied, none of which had a corpus luteum,
but all possessed at least one corpus albicans
which was in various stages of degeneration. The
endometrium showed typical regressive changes
with hyalinization, chronic inflammation, and
hemosiderin. These features will also allow
categorization of uteri from females with un-
known reproductive state in future studies. Of the
58 animals with macroscopically diagnosed cor-
pora lutea and no detectable pregnancy, only 43 in
fact had an active corpus luteum, the remaining
15 specimens had corpora albicantia in various
stages of regression. Three corpora lutea were on
the right, the remaining 40 were on the left, con-
firming the usual finding of Cetacea that the left
side predominates in reproduction. When a corre-
lation was sought between the development of the
corpus luteum and endometrial changes a well-
delineated cycle of proliferation and edema to se-
cretory stages emerged. No changes indicative of
early pregnancy were seen and three intact uteri
contained no embryos. Thus, clearly, ovulation
does occur without pregnancy ensuing. In three

526

BENIRSCHKE ET AL.: OVULATION IN DOLPHINS

specimens the findings are consistent with abor-
tion, two had marked endometritis. These latter
findings are summarized in Table 10.

Table lO. — Group VI: Summary of experimental, nonpregnant
animals; 38 Stenella longirostris, 20 S. attenuata.

S longirostris:

19 (50°o) Fresh corpus luteum

1 1 (29%) Well-established corpus luteum

8 (21%) Degenerating corpus luteum — wrong gross diagnosis (2 en-

dometritis; 2 unimplanted abortion?)
S. attenuata:

9 (45%) Fresh corpus luteum

3 (15%) Well-established corpus luteum
1 ( 5%) Misclasslfied. recently delivered

7 (35%) Degenerating corpus luteum — wrong gross diagnosis ( 1 recent
abortion?)

The findings of Perrin et al. (1976, 1977) indi-
cate that over 90^7^ of female genital tracts of S.
longirostris and S. attenuata contain a corpus
luteum because of their pregnancy. The possibility
that abortions of implanted pregnancies occur fre-
quently can be ruled out from the histologic ap-
pearance of the endometria in the majority of the
specimens from the experimental group. Early
embryonic death remains a possibility although
no evidence can be adduced for this. The present
study provides strong evidence that spontaneous
ovulation may occur in these species, at least that
the presence of a corpus luteum is not indicative of
pregnancy. Moreover, recent and as yet unpub-
lished results from our laboratory I J. Sawyer)
have identified hormonally the occurrence of
spontaneous ovulation in a Delphinus delphis
female that was kept in isolation. Evidence for
regression of corpora lutea in nonfertile cycles was
also found in our experimental group. It is possible
then that either ovulation is induced in a majority
of cycles or that a majority of dolphins become
pregnant when ovulating. In either case, it is not
likely that a count of corpora albicantia in dolphin
ovaries accurately reflects the number of past preg-
nancies. We were unable to differentiate with
certainty between the histologic appearance of a
corpus luteum of early pregnancy and one from
nonpregnant animals and cannot accept the al-
leged feasibility of the diagnosis of pregnancy
from the histology of only a corpus luteum. The
endometrial histology is a better guide. Whereas
accessory corpora lutea have been found in other
odontocetes ( Brodie 1 972 ), no such structures were
encountered in the genital tracts of these two
Stenella species.

It would be useful to know from aquaria with
accurate historical information and pathologic
study at death whether older females that have
been kept in isolation since youth possess corpora
albicantia. Inasmuch as the question of artificial
insemination of exhibited animals has been raised
in the past (Hill and Gilmartin 1977) it can be
concluded that it would appear feasible without
the need of superovulation.

From a practical standpoint it is suggested that
the following points be considered in future
studies. First, it would have been helpful to have
had a histologic sample of mammary gland and
vagina in all specimens to enhance histologic cor-
relations. Moreover, inasmuch as the hormonal
cycle of D. delphis is now being defined by modern
endocrine techniques undertaken by sequential
sampling of captive specimens it may be useful for
future studies to save, for endocrine analysis, an
aliquot of frozen serum. Potentially, such a study
would clarify the status of equivocal corpora lutea.
At the same time storage of fetal serum would
allow insight into the fetal endocrine behavior
which is known to differ so markedly between
species. Perhaps such comparative studies will ul-
timately give additional insight into the
phylogenetic descendency of Cetacea.

This study extends the sparse literature that
exists on the morphology of the female reproduc-
tive organs. In general, the endometrial cycle is
similar to that illustrated schematically for sev-
eral whales (Slijper 1966) and for Globiocephala
melaena (Harrison 1949). In this latter species
Harrison (1949) also described the small superfi-
cial anastomosing vessels beneath the uterine
epithelium and, in three recently ovulated speci-
mens, he was unable to identify products of con-
ception. In a later contribution, Harrison et al.
(1969) suggested that while ovulation in Tursiops
truncatus appears to be of a reflex nature, that of
S. graffmani and Lagenorhynchus obliquidens
may be spontaneous as in G. melaena. Our own
findings cited above suggest, however, that in D.
delphis spontaneous ovulation occurs and one
wonders whether this then may not be the rule in
Cetacea. A resolution can come only from lon-
gitudinal endocrine studies of isolated females
from different species. Finally, as was the case in
most other studies of the morphology of Cetacean
reproductive organs, we observed no significant
pathologic features in these specimens other than
the endometritis described and occasional
parametrial parasitic granulomata. ^

527

ACKNOWLEDGMENTS

The encouragement and constructive criticism
of W. F. Perrin is warmly acknowledged. The
study was performed under contract NAS07-
35234. The original slides, additional data, photo-
graphs, negatives, and an expanded manuscript
are on file at the Southwest Fisheries Center, La
Jolla Laboratory, National Marine Fisheries Ser-
vice, NOAA, La Jolla, Calif

LITERATURE CITED

Brodie, p. F.

1972. Significance of accessory corpora lutea in odonto-
cetes with reference to Delphinapterus leucas. J. Mam-
mal. 53:614-616.

England, B. G., W. C. Foote, D. H. Matthews, A. G. Car-

DOZO, AND S. RIERA.

1969. Ovulation and corpus luteum function in the llama
(Lama glama). J. Endocrinol. 45:505-513.

Harrison, R. J.

1949. Observations on the female reproductive organs of
the ca'aing whale, Globiocephala melaena Traill. J.
Anat. 83:238-253.

1977. Ovarian appearance and histology in Tursiops trun-
catus. In S. H. Ridgway and K. Benirschke (editors).

FISHERY BULLETIN: VOL. 78, NO. 2

Breeding dolphins, present status, suggestions for the fu-
ture, p. 195-204. U.S. Mar. Mammal Comm. Rep. MMC
76-07; available U.S. Dep. Commer., Natl. Tech. Inf. Serv.
as PB 273-73.
HARRISON, R. J., R. C. BOICE, AND R. L. BROWNELL.

1969. Reproduction in wild and captive dolphins. Nature
(Lond.) 222:1143-1147,

Hill, H. G., and W. G. Gilmartin.

1977. Collection and storage of semen from dolphins. In
S. H. Ridgway and K. Benirschke (editors), Breeding dol-
phins, present status, suggestions for the future, p. 205-
210. U.S. Mar. Mammal Comm. Rep. MMC 76-07; avail-
able U.S. Dep. Commer., Natl. Tech. Inf. Serv. as PB
273-73.
JOCHLE, W.

1973. Coitus-induced ovulation. Contraception 7:523-
564.

Perrin, W. F., J. M. Coe, and J. R. Zweifel.

1976. Growth and reproduction of the spotted porpoige,
Stenella attenuate , 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 dol-
phin, a geographical form o{ Stenella longirostris in the
eastern tropical Pacific. Fish. Bull., U.S. 75:725-750.

SLIJPER, E. J.

1966. Functional morphology of the reproductive system
in Cetacea. In K. S. Norris (editor). Whales, dolphins,
and porpoises, p. 277-318. Univ. Calif. Press, Berkeley
and Los Ang.

528

NOTES

A LARGE, OPENING-CLOSING MIDWATER

TRAVC L FOR SAMPLING OCEANIC NEKTON,

AND COMPARISON OF CATCHES WITH

AN ISAACS-KIDD MIDWATER TRAWL

Avoidance of nets by agile micronekton and nek-
ton is one of the major problems with small mid-
water trawls routinely used for oceanic sampling
by oceanographers and marine biologists (e.g.,
Harrisson 1967; Pearcy 1975; Roper 1977). A major
advantage of small trawls is that they can be
equipped with opening-closing devices so that
samples can be ascribed to discrete depths. This
capability is especially important for sampling
deep water where densities of animals are low. An
opening-closing rectangular midwater trawl with
a mouth area of about 25 m^ is the largest
opening-closing net described (Baker et al. 1973).
Another important advantage of small nets is that
they can be used from most oceanographic vessels.

Large, commercial-size midwater trawls used to
sample oceanic micronekton (Berry and Perkins
1966; Harrisson 1967; Taylor 1968; Clarke 1973,
1974; Krefft 1974; Roper 1977) are usually not
evaded as successfully by nektonic animals. Big
nets which filter large volumes of water have the
added advantage of catching enough animals to
characterize species and size composition from
sparsely populated waters. However, these large
nets lack opening-closing capability, and most
oceanographic research vessels are unable to
handle large nets, otter doors, and bridles ( Pearcy
1975).

This paper describes a 50 m"^ pelagic trawl es-
pecially designed for use with an opening-closing
cod end, attempts to evaluate its performance, and
compares its catches of mesopelagic fishes and
cephalopods with those from a 5.4 m^ Isaacs-Kidd
midwater trawl.

Midwater Trawl Description and Operation

The midwater or pelagic trawl was designed by
G. Loverich, Nor'Eastern Trawl Systems, Inc.,^
Bainbridge Island, Wash., for sampling meso-

' Reference to trade names or commercial firms does not imply
endorsement by the National Marine Fisheries Service, NOAA.

FISHERY BULLETIN: VOL. 78, NO, 2, 1980.

pelagic fishes and cephalopods in conjunction with
a 1 m^ five-net opening-closing device which is
attached to the cod end of the trawl (Figure 1). The
body of the trawl is lined throughout with 19 mm
(% in) stretch mesh. The net is 42 m long and was
constructed with a gradual taper from mouth to
cod end in order to provide a large netting area for
filtration in order to reduce the water velocity
through the meshes, stagnation and hang-up of
animals on the netting, and extrusion of animals
through the netting. The wings of the trawl are
made of large mesh ( 292 mm). It was assumed that
micronekton (fishes, squids, and shrimps up to 200
mm in length) escape or pass through this large
mesh rather than lead into the trawl body, giving
an effective diameter of the net for micronekton
equivalent to the small mesh body of the trawl.
Unfortunately data do not exist to evaluate herd-
ing or leading of oceanic micronekton by the wings
of trawls.

The trawl has six seams with four identical
panels for the top and bottom (wing, body, and
intermediate) two identical side (wing, body, and
intermediate) panels, and four cod end panels
( Figure 2). The meshes were hung at 29. 3"^^ in both
directions to allow formation of square openings
and laced to make six seamlines. Two riblines are
located along the middle of the side panels and
extend to the opening-closing device.

A 1 m2 Multiple Plankton Sampler (MPS) with
five separate nets, each 4.6 m long (see Pearcy et
al. 1977 for details), was used as an opening-
closing cod end device on the trawl. The levers for
release of the five nets of the sampler are actuated
by a modular timer which employed a crystal oscil-
lator and a binary series of counters for selection of
release times (Evans 1975). The timer is mounted
on the MPS, started as the trawl is launched, and
is set to give the trawl time to stabilize at a
selected towing depth before net 1 is released
(usually 30-60 min). Thus the first net fishes
obliquely from the surface to the fishing depth of
net 2. The four remaining nets (nets 2-5) all fish
the same amount of time on a given tow (usually
40 min), either at the same depth (horizontal
series) or at different depths (vertically stratified
series).

The footrope and headrope are each 28.6 m of 16

529

Figure l. — Sketch of the pelagic trawl in operation.

mm poly-Dacron rope. The wings are of #60
thread, the body of #3 thread, the intermediate of
#4 thread, and the cod end of #6 thread. Nineteen
25.4 cm (diameter) aluminum floats (good to 1,000
m) are attached to the headrope. Galvanized chain
is attached to the footrope and one 23 kg lead ball
is attached to the tip of each of the bottom wings.
The bridles to the bottom wings are 55 m long;
bridles to the upper wing are 36 m long, and the
middle bridle is 47 m long (Figure 1).

The trawl was designed to be towed with 1.5-1.8
X 2.4-2.7 m (5 x 8 ft or 6 x 9 ft) otter doors. A scale
model of the trawl was first constructed and tested
in a tank to test its design and performance.

Observations were made on the trawl by divers
during trials in Puget Sound using 1.8 x 2.7 m
doors and towing speeds of 1.0 to 1.6 m/s at depths
of about 12 m. The towing characteristics of the net
were observed and the number of floats needed to
provide neutral buoyancy to the cod end opening-
closing device was determined by trial. At a tow-
ing speed of 1.6 m/s the vertical opening of the
mouth was measured to be about 8 m and the body
of the trawl was observed to be nearly circular and
about 8 m in diameter, providing an estimate of
about 50 m^ for the cross-sectional area of the fine
mesh netting of the trawl body.

The depth that each net fished was determined
from the depth-modulated signal from an acous-
tical pinger mounted on the headrope of the trawl,
a hydrophone towed from the vessel, and a graphic
recorder. An EG&G pinger was used initially but
was replaced with an Institute of Oceanographic
Sciences (lOS) 0-683 m (0-100 atmospheres pres-
sure) acoustical net monitoring system (Baker et
al. 1973) with an overall accuracy of 0.1% of the full
depth range.

Methods

A timer-actuated ejection device was used as a
method to provide some information on the flush-
ing rate through the body of the trawl. This device,
similar to the one described by Pearcy et al. (1977),
has a modular timer (Evans 1975) to release the
contents of two 1.3 1 chambers. It was hung from
the headrope inside the trawl mouth and its con-
tents were ejected against the 19 mm mesh. Pre-
served juvenile salmon (10-20 cm total length)
were released into the net at intervals of 5, 10, 15,
or 25 min before closure of net 1 and opening of net
2.

The pelagic trawl-MPS combination was used
on three chartered trawlers off Oregon. All vessels
had net reels and used double-warp towing. A
boom was used to launch and recover the MPS
during 1975 and 1976 cruises. The vessel chartered
in 1977 had a stern ramp, which greatly facilitated
use of the pelagic trawl. Twelve tows were made in
1975 to test the monitoring equipment and to
evaluate flushing of the net. Eight tows were made
in 1976 and 10 in 1977. All tows were 110-130 km
off the central Oregon coast; 18 of these tows pro-
vided the data for comparison of pelagic trawls and
Isaacs-Kidd midwater trawls (IKMT's) (Table 1).

Tows were also made with a 5.4 m^ IKMT with
10 mm stretch mesh and a 1 m^ MPS opening-
closing device (Pearcy et al. 1977) at 1.5-2.0 m/s at
a similar location and within 10 days after each of
three cruises that used the pelagic trawl (Table 1).
Volume of water entering the IKMT was moni-
tored with a modified TSK flowmeter on all tows.
One of the purposes of these IKMT tows was to
enable comparisons of the catches by the two dif-
ferent types of nets.

530

6 6m

COD END

74

13.4m

00 I

INTERMEDIATE

226

226

226

226

10.8m

BODY

419

453

WINGS

Figure 2. — Net plans for the pelagic trawl. Numbers on the net panels indicate number of meshes along the margins.

Collections were preserved in 109c Formalin at
sea. In several instances large catches (>35 1) of
the pelagic trawl were subsampled, but at least 14
1 of the catch of each of the nets for discrete depths
were preserved. Fishes and cephalopods were
identified and measured [standard length (SL) of
fishes and dorsal mantle length ( DML ) of squids].

Table l. — Summary of pelagic trawl (PT) and Isaacs-Kidd
midwater trawl ( IKMT) tows made on the three "paired" cruises
off Oregon.

Net

Dates

Vessel

No
Tows

Depth
(m)

Time

1975:

PT
IKMT

23 Sept
12-16 Sept,
1976:

Betty-A
Yaquina

1
5

340-360
334-362

Day
Day

PT
IKMT

19-22 July
8-13 July
1977:

Pacific Raider
Wecoma

8
11

0-500
0-465

Day-night
Day-night

PT
IKMT

30 July-2 Aug
8-10 Aug

Excalibur
Wecoma

9
5

185-365
187-350

Day-night
Day-night

Results
Flushing of the Pelagic Trawl

In Puget Sound, divers observed that dead salm-
on smolts released in the mouth of the trawl were
never stuck against the netting in the forward
part of the trawl where the meshes were taut from
water pressure. Occasionally fish stalled against
the mesh in the aft section of net where netting
was less rigid, but these fish were easily dislodged
and tumbled toward the cod end. Because live
fishes usually swim away from the netting when
inside a trawl, it seems unlikely that live, active
fish would be pinned against the netting (G.
Loverich^). Obviously, dead, preserved fish do not

^G. Loverich, Nor'Eastem Trawl Systems, Inc., Bainbridge
Island, WA 98110, pers. commun. January 1979.

531

behave like live ones, but they do provide some
information on flow characteristics through the
net and how easily objects are pinned against the
mesh.

The results of the release of preserved salmon
smolts into the mouth of the pelagic trawl on two
cruises in the open ocean are shown in Table 2.
Ninety-seven percent of the fish released in the
mouth were recovered in cod end nets 1 and 2
within 5-25 min after release: 827c were recovered
in net 1. These data indicate an average residence
timeofpreservedfishof <10min in the body of the
trawl.

If live animals were delayed by 10-120 min in
passing through the net into the cod end, then the
number of animals found in different cod end nets
may vary, with largest numbers in latter nets and
fewest in the first or second net as found by Foxton
(1970) and Donaldson (1975) in other cod end
opening-closing devices. Coefficients of concor-
dance, W, (Tate and Clelland 1957) were not sig-
nificant (P>0.2) for rank order of abundance of
fishes (12 tows), squids (10 tows), and Steno-
brachius leucopsarus, the most common fish (10
tows) for nets 2-5 that sampled equal time inter-
vals and also caught at least 10 of each of these
three types of animals. Similar nonparametric
tests of the rank order of abundance of 15 common
species were not significant for nets 2-5 of nine
tows with same net, where each net fished 2 h
(Willis 1979). This lack of correlation of catch with
net number provides no evidence for delay or stag-
nation of animals in the net over time periods of 10
min to 6 h. Characteristic species compositions or
size-frequency distributions from specific depths
(Willis and Pearcy^) also indicate that cod end
catches are predominantly from the depths fished.

Entanglement or hang-up of fishes and
cephalopods in the meshes of the trawl appeared to
be restricted to a few types. Fishes such as the
stomiatoid, Tactostoma macropus, were oc-
casionally found hanging on the meshes of the
trawl body by their teeth. Soft-bodied cephalopods,
such as Chiroteuthis calyx and Vampyroteuthis in-
fernalis, were sometimes entangled in the mesh.
The number of animals hung on the net after a tow
was always a small fraction of those in the cod
ends. These entangled animals that are retained
in the net from one tow are probably washed-down

Table 2. — Results of release of preserved salmon from the ejec-
tion device in front of the pelagic trawl. All tows were horizontal
at 2.5-3.0 kn. ND means no data.

Minutes thiat
ejection de-
vice was set
to go off
before clo-
sure of net 1

Interval

between

closure of

nets 2-5

(min)

No. of fish

in net:

No recov-
ered/no

Vessel

1

2

3

4

5

used

Betty-A

10
10

15
15

35
35

0
0

0

0

(')
0

V)

ND
ND

10

15

30

3

0

0

0

ND

25

20

36

0

0

0

0

ND

Pacific Raider

5

40

30

24

1

4

2

61/65

10

40

20

234

22

20

27

43/60

10

40

33

25

0

0

0

58/60

15

40

49

1

0

0

2

52,59

Percent recovered in eacfi net

82

15

1

1

1

'Net failed to close

2Cod end of trawl was twisted. This trawl was excluded from percentage
calculations.

into the first net of the next trawl. Since this first
net is the one that fishes obliquely from the sur-
face to the selected depth of sampling, it is not
usually used in studying vertical distribution of
animals.

Pelagic Trawi-IKMT Comparisons

The 17 pelagic trawls caught almost twice as
many species of fishes, and about the same number
of cephalopod species as the 16 IKMT's during the
two major cruises in 1976 and 1977. These differ-
ences are mainly due to the large volumes of water
filtered by the pelagic trawl and consequently the
large number of individuals captured.

One of the most significant differences between
the catches was the presence of some fish species in
the pelagic trawl and their complete absence in
the IKMT catches (number caught-vessel, where
PR = Pacific Raider and EX = Excalibur):
Aphanophus carbo (3-PR), Merluccius productus
(3-PR), Idiacanthus antrostomus (23-PR), Aristo-
stomias scintillans (24-PR, 6-EX), Macrouridae
id-PR), Lestidium ringens (37 -EX), Nansenia Can-
dida (22-EX), Symbolophorus californiensis (5-
EX). In over 2,000 (2, 2.5, and 3 m mouth opening)
IKMT tows made off Oregon since 1961, we have
never before captured Aphanophus carbo or M.
productus in oceanic waters. These fishes were
large (436-570 mm) and presumably always avoid
IKMT's.

Length- Frequency Comparisons

^Willis, J. M., and W. G. Pearcy. Spatial and temporal varia-
tion in the population size structure of three lanternfishes (Myc-
tophidae) off Oregon. Unpubl. manuscr.

532

Significant differences [P<0.5, Kolmogorov-
Smirov (K-S) two sample comparisons (Tate and
Clelland 1957)] were found in the size-frequency

distributions of four common species ( where n >50
for fishes for each of the two nets, and n>20 for
squid) for: Stenobranchius leucopsarus in two of
the three comparisons, Z)/ap/ii/s theta in one of two
comparisons, and Tarletonbeania crenularis in two
of two comparisons. In all instances where length
distributions differed, the pelagic trawl caught an
appreciably higher percentage of large animals.
Even though the one K-S test for the squid
Gonatus pyros was not significant (because of
small numbers caught in the IKMT), IB^c of num-
bers of this squid from the pelagic trawl were >35
mm DML and no animals >35 mm were caught in
the IKMT.

Length-frequency distributions for S. leucop-
sarus and T. crenularis from both trawls (Figure 3)
show that large lanternfishes are clearly un-
dersampled by the IKMT. The modes composed of
fishes >45 mm, which are prominent in pelagic
trawl catches, are absent in IKMT catches.

Another notable example of differences between
catches of large fish in these collections were cap-
tures of Tactostoma macropus. Few large indi-
viduals ( >250 mm) have been collected in IKMT
tows off Oregon. Three tows with the pelagic trawl
at depths of 470-1,070 m in 1978, however, cap-
tured many large fish. Twenty-nine percent of the
T. macropus caught in these pelagic trawl collec-
tions were >250 mm, compared with only 8.2^c in
252 IKMT tows to 500 m depth or deeper during
previous years.

Effective Cross-Sectional Area of the Pelagic Trawl

The cross-sectional area of the pelagic trawl was
indirectly estimated from the catches of four
species of lanternfishes caught in both the pelagic
trawl and IKMT on the three "paired" cruises (Ta-
ble 1) to see how it compared with the divers' esti-
mates of 50 m^. The following equation was used:

A =

CoD

where A = area in square meters,

Cj = number of fish caught by pelagic

trawl,
V = volume filtered by the IKMT, in cubic

meters,
Cg = number of fish caught by the IKMT,
D = distance trawled by the pelagic trawl

in meters.

The volume of water filtered by the IKMT was

cr

UJ
CD

3

600

400

200

0
200

100

I I I I I I

I I I I I I

Stenobrachius
leucopsarus

+"-1— f

Tarletonbeania
crenularis

40 60

LENGTH (mm)

80

100

Figure 3. — Length-frequency distribution for Stenobrachius
leucopsarus and Tarletonbeania crenularis in pelagic trawl and
IKMT collections, July 1976, 0-500 m.

calculated from a flowmeter mounted in the MPS
and monitored aboard ship via electrical cable (see
Pearcy et al. 1977). Distances trawled by the
pelagic trawl were calculated from ship speed
(based on Loran readings) and the duration of the
tow. In each comparison, tows and nets selected
fished similar depths at the same time of day. The
mouth area estimated in this way varied from 19 to
3,161 m^ with a median value between 48 and 62
m2 (Table 3). The smallest area (19 m^), for D.
theta, can be largely explained by the retention of
small fish (10-15 mm) in the IKMT but not by the
slightly larger mesh of the pelagic trawl. This is
the only obvious example of differences in size-
frequency distributions that can be explained by
escapement of small fish. The large values of
mouth area may result from different population
densities of two species at the times of sampling
during the 1977 cruises.

The present study indicates that large nets
usually catch more individuals, and usually, but
not always, more species and larger animals than
small IKMT-type nets. Detailed quantitative com-
parisons are needed with nets of known cross-
sectional areas, with similar mesh size, at the
same depths and locations (Roper 1977). Large
nets will never replace the smaller IKMT's and
rectangular midwater trawls because of the
specialized equipment needed to launch and re-

533

Table 3. — Estimates of the effective mouth size of the pelagic trawl (PD based on estimated distance trawled
(speed X time), the catches of four lantemfishes, and the catches of four lantemfishes and volumes for IKMT's
on "paired" cruises.

Stenobrachius

Diaphus

Tarletonbeania

Protomyctophum

Item

leucopsarus

theta

crenularis

thompsoni

1975—1 PT. 5 IKMT, 340-350 m, day:

Distance trawled by PT - 23.718 m

Vol. filtered by IKMT = 435.210 m^

No. caught in PT

2,121

216

146

218

No. caught in IKMT

816

212

61

123

Effective mouth area, m^

48

19

44

32

1976—8 PT 11 IKMT 0-350 m. day/night:

Distance trawled by PT ^ 148,425 m

Vol. filtered by IKMT -= 1,525,860 m^

No. caught in PT

4.306

1,663

1.007

183

No. caught in IKMT

718

644

167

60

Effective mouth area, m^

62

27

62

31

1977—2 PT, 3 IKMT, 290-325 m, day/night:

Distance trawled by PT = 18,931 m

Vol. filtered by IKMT = 630,385 m^

No. caught in PT

2,658

149

388

192

No. caught in IKMT

28

4

2

100

Effective mouth area, m^

3,161

1.240

646

64

cover large nets from oceanographic vessels. We
need to compare catches of different-sized trawls,
however, in order to evaluate biases and to learn
what portions of the plankton-micronekton-
nekton spectrum are effectively sampled by dif-
ferent nets.

Acknowledgments

This research was supported by the Office of
Naval Research through Contract N00017-76-C-
0067 under Project NR083-102. I am grateful to
M. Willis, D. Stein, and R. Mesecar for comments
on the manuscript, to J. Fisher, F. Evans, and
D. Stein for invaluable help at sea, and to
G. Loverich for design and evaluation of the
pelagic trawl.

References

Baker, A. de C, M. R. Clarke, and M. J. Harris.

1973. The N.I.O. combination net (RMT 1 + 8) and further
developments of rectangular midwater trawls. J. Mar
Biol. Assoc. U.K. 53:167-184.
BERRY, F. H., AND H. C. PERKINS.

1966. Survey of pelagic fishes of the California Current
area. U.S. Fish Wildl. Serv, Fish. Bull. 65:625-682.
CLARKE, T. A.

1973. Some aspects of the ecology of lantemfishes (Myc-
tophidae) in the Pacific Ocean near Hawaii. Fish. Bull.,
U.S. 71:401-434.

1974. Some aspects of the ecology of stomiatoid fishes in
the Pacific Ocean near Hawaii. Fish. Bull., U.S. 72:337-
351.

Donaldson, H. A.

1975. Vertical distribution and feeding of sergestid
shrimps (Decapoda: Natantia) collected near Bermu-
da. Mar. Biol. (Berl.) 31:37-50.

EVANS, F.

1975. Universal modular timer Exposure 3:8-11.
FO.XTON, P

1970. The vertical distribution of pelagic decapods (Crus-
tacea: Natantia) collected on the SOND cruise 1965. J.
Mar. Biol. Assoc. U.K. 50:939-960.
Harrisson, C. M. H.

1967. On methods for sampling mesopelagic fishes.
Symp. Zool. See. Lond. 19:71-126.

Krefft, G.

1974. Investigations on midwater fish in the Atlantic
Ocean. Ber. dtsch. wiss. Komm. Meeresforsch., Neue
Folge, 23:226-254.

Pearcy, W. G. (editor).

1975. Workshop on problems of assessing populations of
nekton. Off. Nav Res. Rep. ACR 211, 30 p.

Pearcy, W. G., E. E. Krygier, R. mesecar, and F Ramsey.

1977. Vertical distribution and migration of oceanic
micronekton off Oregon. Deep-Sea Res. 24:223-245.

Pearcy, W. G., and R. M. Laurs.

1966. Vertical migration and distribution of mesopelagic
fishes off Oregon. Deep-Sea Res. 13:153-165.
ROPER, C. F E.

1977. Comparative captures of pelagic cephalopods by
midwater trawls. Symp. Zool. Soc. Lond. 38:61-87.

Tate, M. W., and R. C. Clelland.

1957. Nonparametic and shortcut statistics in the social,
biological , and medical sciences. Interstate Printers and
Publishers, Inc., Danville, 111., 171 p.

Taylor, F H. C.

1968. The relationship of midwater trawl catches to sound
scattering layers off the coast of northern British Colum-
bia. J. Fish. Res. Board Can. 25:457-472.

Willis, J. M.

1979. Vertical distribution and migration of fishes from the
lower mesopelagic zone off Oregon. M.S. Thesis, Oregon
State Univ., Corvallis, 52 p.

WILLIAM G. Pearcy

School of Oceanography
Oregon State University
Corvallis, OR 97331

534

PASSIVE BEHAVIOR BY THE SPOTTED

DOLPHIN, STENELLA ATTENUATA, IN

TUNA PURSE SEINE NETS

The purse seining method of catching yellowfin
tuna, Thunnus albacares, in association with
schools of dolphins in the eastern tropical Pacific
has been described by Perrin ( 1969). The primary
target species, in order of importance, are the spot-
ted dolphin, Stenella attenuata, and the spinner
dolphin, S. longirostris , with occasional net sets
made on schools of the common dolphin, De/p/imws
delphis. Schools of these dolphins ranging in size
from 50 to several thousand are herded with
speedboats and encircled with a purse seine net
that is from 900 to 1,400 m long and as much as
130 m deep. After the dolphins are encircled, the
bottom of the net is pursed, entrapping the mam-
mals and any tuna that are associated with the
school. Presently, neither the mechanisms nor the
function of the close association of the yellowfin
tuna with these schools of dolphins in the eastern
tropical Pacific are clearly understood.

Studies of the behavior of dolphins while captive
in a purse seine net were pursued during the char-
tered cruise of the commercial seiner MV
Elizabeth C. J., in October 1976 (Norris et alM.
Prior to this cruise, however, beginning in 1973, an
intensive effort was made to develop net modifica-
tions and fishing techniques that would decrease
the incidental killing of the mammals. Much of
this effort was based upon general, to date unpub-
lished, observations of captured dolphins and tuna
made by National Marine Fisheries Service
(NMFS) observers and technologists. One of the
behavioral patterns of the spotted dolphin first
noted by NMFS divers in 1973 and then recognized
for its contribution to incidental mortality in 1975
is termed here "passive" behavior.

In the fall of 1975, NMFS chartered the purse
seiner MY Bold Contender to carry on fishing gear
dynamics research aimed at reducing incidental
dolphin mortality. Part of this research included
the evaluation of the use of a two-man inflatable
raft as a dolphin rescue platform during and after
the release procedure known as the "backdown"
(Perrin 1969; Coe and Sousa 1972). A face mask
and snorkel were worn by the person in the rescue

'Norris, K. S., W. E. Stuntz, and W. Rogers. 1978. The be-
havior of porpoises and tuna in the eastern tropical Pacific
yellowfin tuna fishery - preliminary studies. Available U.S. Dep.
Commer, Natl. Tech. Inf. Serv., Springfield, Va., as PB-283970,
86 p.

nSHERY BULLETIN: VOL. 78, NO. 2, 1980.

raft to enable him to: 1) signal when tuna were
approaching the release area during backdown, 2)
keep track of sharks, particularly the oceanic
whitetip shark, Carcharinus longimanus, both in-
side and outside of the net, 3) locate and release
any stray dolphins and, 4) observe the dynamics of
the net modification being tested during the
cruise. Notes on the behavior of the captured dol-
phins during backdown were recorded after each
of the 25 net sets in which the rescue raft was used.
The underwater passive behavior of spotted dol-
phins was first noted in the eighth net set of the
cruise and in 14 subsequent sets.

The passive behavior manifests itself in possibly
two forms during the backdown release procedure.
The first, which has been described as "rafting" by
Norris et al. (see footnote 1 ), consists of groups of
5-50 or more spotted dolphins hanging tail-down
at or near the surface and showing no overt reac-
tions to their surroundings. This type of passive
behavior can be seen from the deck of the seiner
and is generally displayed from the time the net is
pursed through the backdown (about V2 h). There
is a steady increase in the number of rafting ani-
mals until backdown begins and then an apparent
sharp decrease as backdown proceeds. The de-
crease in rafting may be due to the crowding and
confusion during that period. Rafting behavior
simplifies the effective release of these animals by
backdown, because the net is actually pulled out
from under the "raft" of dolphins as it remains
relatively stationary in the water. Observations
during the Elizabeth C. J. cruise showed that in
every school of captured spotted dolphins some
portion exhibited this behavior.

Dolphins in the captured school that are not in
rafts during backdown are either actively swim-
ming, usually in the horizontal plane directly
away from the advancing wall of the net, or dis-
play the second manifestation of passive behavior.
Prior to backdown, rafting dolphins are occasion-
ally observed to sink tail first to depths up to 5 m
before they swim awkwardly back to the surface,
breathe, and sink again. During backdown, how-
ever, there are occasionally relatively large num-
bers of animals that sink to lie on the webbing
(Figure 1) and many more that show signs of the
sinking behavior and drop out of the rafts.

During backdowns on iheElizabeth C. J. cruise,
from 3 to an estimated 75 spotted dolphins and, in
one set, 2 bottlenose dolphins, Tursiops truncatus,
were observed lying on the webbing in the bottom
of the backdown channel. These animals, which

535

Figure l . — Photograph taken during backdown of a tuna purse seiner showing three passive dolphins in the foreground. Note that the
middle animal is resting on its dorsal fin. The four animals that are hanging flukes downward in the water are displaying the sinking
behavior associated with rafting. (Photo courtesy of the Cooperative Dedicated Vessel Research Program, 1978.)

were making no apparent attempt to surface, were
at depths that varied from 2 or 3 m to as much as 12
to 15 m. At first glance, the animals appeared to be
struggling feebly, perhaps against the current
being produced as the seine was pulled through
the water during backdown. Their movements
were weak and lacked the grace that long observa-
tion leads one to expect in dolphins. The majority
of animals lying on the net in this manner were
oriented with their heads toward the release area
of the net (i.e., in the direction of the current),
whereas the rafting and active animals were nor-
mally oriented away from the release area (i.e.,
heading into the current). After about 3-5 min, the
passive dolphins began to rise singly or in two's
and three's to breathe and were either backed out
of the net or hand-released if the backdown proce-
dure had already been terminated. No animals
were seen returning to rest on the bottom of the
net after surfacing.

Prior to promulgation and adoption of a federal
regulation requiring use of a rescuer in a raft
using a mask and snorkel, which resulted from the
chartered cruise of the Bold Contender, this pas-
sive behavior probably was an important con-
tributor to dolphin mortality in purse seines.

When viewed from the deck of a speedboat tending
the corkline in the dolphin-release area during
backdown, these animals appeared to be dead if
they were noticed at all, and as a result the release
efforts were often prematurely terminated. Dol-
phins not released during the backdown have a
high probability of being killed ( Coe and DeBeer^).

The reasons for passive behavior in purse
seine-caught spotted dolphins are not understood.
The behavior has only rarely been observed in
spinner dolphins in the tuna fishery. A similar
behavior pattern has been described for two newly
captured Hawaiian spinner dolphins during es-
cape behavior experiments designed to delineate
the dimensions of a dolphin release gate for
possible use in purse seine nets (Perrin and
Hunter 1972).

Animal trainers and biologists have noted what
appears as similar behavior in individual captive
dolphins of several species. Caldwell et al. (1966)
reported prolonged inverted "resting or sleeping

2Coe,J.M.,andJ.DeBeer 1977. Results of the 1976 twenty
vessel test of two fine mesh systems to reduce incidental porpoise
mortality in tuna purse seining. Unpubl. manuscr., 75 p.
Southwest Fisheries Center, PO. Box 271, La Jolla, CA 92038.

536

on the bottom of the tank" by a juvenile male
Bontu, Inia geoffrensis. The occurrence of this be-
havior in /. geoffrensis and that observed in a
juvenile male Atlantic bottlenose dolphin was fre-
quent and apparently spontaneous tCaldwelF).
Pryor* and Norris et al. (footnote 1) have noted
instances where the passive-type behavior was
presumably induced in training situations where
Tursiops spp. were being "worked hard." These
animals would go to the bottom of the tank, emit a
quantity of air and might remain at the bottom for
several minutes. Norris et al. hypothesized that
this behavior may be similar to the "dearoused
state" described by Delius (1970) for terrestrial
animals, the most widely known example of which
is the feigning of death by the Virginia opposum,
Didelphis marsupialis . The major criticism (Nor-
ris et al.) of the dearousal hypothesis in the pres-
ent situation would seem to concern the
evolutionary value of such a response to a pelagic
air breathing animal that would tend to sink to-
ward the bottom in very deep water. One argu-
ment (Norris et al.) is that the situation which
elicits dearousal (purse seining) has been a factor
for only about 15-20 yr, and it is therefore not
necessary to hypothesize an adaptive value for the
behavior. To accept this hypothesis it would have
to be assumed that the capability for dearousal has
evolved in response to other circumstances.

A second hypothesis to explain this behavior
relates to the effects of chase and capture on the
physiology of the dolphins. Possibly indicative is
the awkwardness of the swimming movements
displayed by the animals while "passive." Hart-
hoorn (1973) described the effects of chase and
capture on large African mammals. Long chases
using motor-driven vehicles result in a typical
condition termed "capture myopathy." Capture
myopathy is very common in the animals captured
for zoos and often causes a delayed mortality.
Symptoms include stiffness and awkward move-
ments. The method of capturing dolphin schools
involves a chase by speedboats that lasts up to 1.5
h and averages between 20 and 30 min. A chase of
that duration is capable of causing myopathies in
large terrestrial mammals which can be detected
by measuring changes in blood serum enzyme

^David K. Caldwell, Director, Biocommunication and Marine
Mammal Research Facility, University of Florida, Route 1, Box
121, St. Augustine. FL 32084, pars, commun. October 1979.

••Karen Pryor, former head animal trainer, Sea Life Park,
Hawaii; present address: 28 East 10th Street, New York, NY
10003, pers. commun. November 1976.

levels (Harthoorn). A recent paper by Colgrove
( 1978) documents a suspected case of myopathy in
a dolphin, Tursiops gilli = T. truncatus. This case
of myopathy appears to have been induced by the
stress of transporting the animal. Investigation of
blood chemistry of passive dolphins may allow de-
termination of whether capture myopathy does
occur as a result of chase and capture during the
tuna seining operation.

Acknowledgments

We thank Jack Hailman, Kenneth Norris, and
William Rogers for reviewing versions of this
manuscript. The photograph was taken by
Thomas Shay of the National Marine Fisheries
Service during the Cooperative Dedicated Vessel
Research Program cosponsored by the United
States Tuna Foundation, the National Marine
Fisheries Service, and the Marine Mammal Com-
mission.

Literature Cited

Caldwell, M. C, D. K. Caldwell, and W. E. Evans.

1966. Sounds and behavior of captive Amazon freshwater
dolphins, /nia geoffrensis. Los. Ang. Cty. Mus., Contrib.
Sci. 108, 24 p.
COE, J., AND G. SOUSA.

1972. Removing porpoise from a tuna purse seine. Mar.
Fish. Rev 34(11-12):15-19.

COLGROVE, G. S.

1978. Suspected transportation-associated myopathy in a
dolphin. J. Am. Vet. Med. Assoc. 173:1121-1123.
DELIUS, J. D.

1970. Irrelevant behavior, information processing and
arousal homeostasis. Psychol. Forsch. 33:165-188.

Harthoorn, a. M.

1973. Physiology and therapy of capture myopathy 2d
Annu. Rep. Transvaal Nat. Conserv. Div., Pretoria, Afr.,
p. 1-191.

PERRIN, W. F

1969. Using porpoise to catch tuna. World Fishing
18(6):42-45.
PERRIN, W. E, AND J. R. HUNTER.

1972. Escape behavior of the Hawaiian spinner porpoise
(Stenella cf. S. longirostris). Fish. Bull., U.S. 70:49-60.

James M. Coe
Warren E. Stuntz

Southwest Fisheries Center La Jolla Laboratory
National Marine Fisheries Service, NOAA
P.O. Box 271
La Jolla, CA 92038

537

EFFECTS OF LARGE PREDATORS ON

THE FIELD CULTURE OF THE HARD CLAM,

MERCENARIA MERCENARIA^

Individuals in the clam industry have used fences
to keep the cownose ray, Rhinoptera bonasus, out
of planted areas (Lewis^; Burton ). Tiller et al.
(1952) indicated losses due to skates in planted
holding areas and stated that "One man reported
the loss of 600 bushels of small clams in two nights

during 1948 " Merriner and Smith'* stated

that cownose ray predation is a serious problem on
oyster and clam grounds in Chesapeake Bay. From
these observations it is clear that such large pred-
ators could be a significant deterrent to the culture
of clams from Delaware Bay southward along the
Atlantic coast.

The present study continues a program de-
signed to evaluate methods of protecting areas
seeded with young Mercenaria mercenaria. The
initial portion of the study outlined the interactive
effects of pens, gravel, current baffles and crab
traps on the first year's growth and survival
(Kraeuter and Castagna 1977). The results of the
second year study on the interactive effects of
these manipulations are recorded below. The data
indicate effectiveness of efforts to prevent preda-
tion on clams surviving the first year's plantings.

of metal framed current baffles and crushed gran-
ite gravel. Current baffles 0.6 m high were con-
structed to decrease the scouring effects of cur-
rents. Since average tidal amplitudes are 1.2 m,
the baffles did not prevent entrance offish or crabs
into the plots. Each baffle was about 1.5 m long
and 12 baffles were set in an array forming four
squares (Figure 1). Clam seed (about 2 mm) was
planted in all sites at 3,000/m2.

Clams were sampled in each site with a 7.4 cm
diameter corer. A 0.6 m^ grid was placed over each
treatment and 10 random samples were removed
in July 1977. This is a continuation of the previous
year's sampling. For final sampling (October-
November 1977), all sites were harvested using a
suction sampler with an attached mesh bag. Four
quadrats corresponding to the squares formed by
placing current baffles in squares were sampled as
discrete units (Figure 1). Where no baffles were
utilized for the treatment, squares were marked
by stakes and sampled as though the baffles had
been present. All clams removed from the plots
were brought to the laboratory, counted, and the
percent commercial size (1 in (25.4 mm) thick New
York legal limit) was determined. The data
(counts) were transformed by logj^ and compared
by a factorial analysis of variance design
(ANOVA).

Methods

Results and Discussion

Details of the experimental design were pre-
sented in the previous paper (Kraeuter and Cas-
tagna 1977) and are briefly discussed below.

Four contiguous intertidal sites were marked by
pushing stakes into the muddy substrate and two
of the four sites were enclosed by 10 mm mesh
plastic net 2.3 m high stretched around the 38 m
circumference. The two remaining sites were left
open (Figure 1 ). Crab traps were placed within one
of the penned and one of the unpenned (no net)
sites to assess the predatory effects of the blue
crab, Callinectes sapidus. In addition, within each
site, areas to be seeded were marked and desig-
nated to be treated with or without combinations

'Contribution No. 924 from Virginia Institute of Marine
Science.

^J. H. Lewis, seafood shipper and packer, Saxis, VA 23427,
pers. commun. Nov. 1976.

^L. L. Burton, seafood shipper and packer, Burton's Seafood,
Chincoteague, VA 23336, pers. commun. Sept. 1976.

"Merriner, J. V, and J. W. Smith. 1979. Gear feasibility
study for the cownose ray, Rhinoptera bonasus. Va. Inst. Mar.
Sci., Spec. Rep. Appl. Mar. Sci. Ocean Eng. 227, 27 p.

Results from the first year sampling (through
September 1976) indicated that baffles and gravel
in combination were superior to any other ti'eat-
ment. Plots were sited in an area where preda-
ceous echinoderms were not present, and although
pens were not effective in preventing crab preda-
tion, no discernable damage could be attributed to
other predators (Kraeuter and Castagna 1977).

The statistical summaries (Table 1) are a con-
tinuation of the table presented by Kraeuter and
Castagna (1977), and, as in that paper, it is impor-
tant to emphasize that the sampling results from
one period to the next were not independent. The
final data represent the cumulative effects of all
environmental and biotic interactions on clams
planted in fall 1975.

The July 1977 results mirrored those of earlier
sampling periods (Kraeuter and Castagna 1977)
with the exception that the pen x trap and pen x
baffle X trap interactions were significant at the
0.05 level. This was due, in part, to the higher level
of predation in the penned area without traps (18

538

FISHERY BULLETIN: VOL. 78, NO. 2. 1980.

Baffle, NoGravel

Figure l. — Diagram of one site of the experimental design indicating the presence of each plot and the net for protection of juvenile
Mercenaria mercenaria . Included in one site with a net would be a crab trap (not illustrated). The net was pushed into the substrate.

Table l. — ANOVA table for survival of hard clam, Mercenaria mercenaria, juveniles
with tests of pens, baffles, gravel, and traps and their interactions. Identical SS in the
July data were caused by clams being absent in all sites with no baffle and no gravel.

July

1977

October-November 1977

Source of variation

df

SS

MS

F

df

SS

MS

F

Total

159

791

63

54.64

Pens (P)

02

002

4.31

4.31

114.31"*

Baffles (B)

1.44

1.44

63.17—

32.17

32.17

853.37—

Gravel (G)

1,56

1.56

68.27—

10.21

10.21

270.89—

Traps (T)

-01

.01

.39

.39

10.43"

P xB

.05

.05

1.16

1.16

30.64*-*

P X G

.03

.03

2.76

276

73.30"*

P X T

.09

.09

4.08-

.94

.94

24.90—

B X G

1.12

1.12

49.02—

07

.07

B X T

.00

.00

.01

.01

G X T

.001

.001

.42

.42

11. 12**

P X B X G

08

.08

.04

.04

P X B X T

.09

.09

4.05*

.001

.001

P X G X T

07

.07

.01

.01

B X G X T

.004

.004

.17

.17

4.61*

P X B X G X T

.07

.07

.16

.16

4.20*

Residual

144

329

.02

48

1.81

0.04

*"P<0.001, "P<0.01, •P<0.05.

clams sampled vs. 31 clams sampled in penned
areas with traps), and, in part, to predation at the
no pen no trap site, 23 clams sampled vs. 15 clams
at the no pen plus trap site. These data indicate
that trapping is essential in penned areas, but that

when pens are absent crab trapping is of no
benefit.

Within 2 wk following the July sampling, in-
spection of the sites revealed that clams 1.5-4.0 cm
high had been crushed. These shell fragments

539

were the result of large predators. The shells were
clean and some were mixed within the surface
layer on the bottom. In addition, the predators had
created pits 50 cm in diameter and 6-10 cm deep in
the aggregate and substrate which had been cover-
ing the clams.

To eliminate effects of losses due to predation
during the first year's study and concentrate on
the effects due to these predators, we have utilized
the estimate of the mean number of clams from the
July 1977 samples as 100% of those present for
further predation. The estimated numbers of
clams in each experimental plot for July 1977 are
given in Table 2, and the number of clams remain-
ing for the corresponding treatments from the Oc-
tober to November 1977 sampling are given in the
same table. Several important aspects not evident
from the ANOVA table are apparent. A combina-
tion of baffles, gravel, pens, and traps was essen-
tial for high survival. Pens were significant only
because of the predation between July and Oc-
tober. The percentage survival between these two
sampling periods seemed to indicate that gravel
somehow negatively interacted with the baffles
(compare percent survival B + G and B + NG,
Table 2) when pens were absent. This was not the
case, but resulted from heavy predation in the
baffle + gravel sites with no pens. Since there were
more clams in these areas in July, the percent
survival was lower, but total survival was better
than in the baffle + no gravel sites (Table 2). The
higher survival in the baffled sites was due to the
protection the baffles offered the clams when the
predators entered the area. Almost all clams found
in these areas were close to, or beneath, the cross
rods supporting the bottom of the baffle. This same
shadow effect was the cause of the nonsignificant

Table 2. — Total number of clams estimated from mean number
per sample (July 1977), total counts (October- November 1977),
and the percent mortality between the sampling dates. — = not
calculated because of 0 estimate in July. P = pens,T = traps, G =
gravel, B = baffle. The prefix N = absence; NP = no pen, etc.

Month or period

Item

B + G NB + G B + NG NBNG

July 1977

Oct.-Nov. 1977

% survival
July to Oct.-Nov.

P + T

6.670

230

230

0

P + NT

4.140

0

0

0

NP + T

2,760

460

230

0

NPNT

4,830

230

230

0

P +T

6,723

174

352

2

P + NT

3,228

23

126

2

NP + T

257

17

75

2

NPNT

248

13

148

5

P + T

101

76

153

—

P + NT

78

—

—

—

NP + T

9

4

33

NPNT

5

6

65

baffle + gravel interaction in the October-
November ANOVA table. If more clams had been
present in the B + NG sites, the clams would have
been in the center of the plot and thus vulnerable
to predation.

The impact of predation to the mariculture of
clams can be seen by comparing survival inside
and outside the penned sites (Table 2). Estimated
survival inside a penned area was always more
than 76%, and the average survival for both
penned sites was 94% from July to October-
November. Average survival for the same period in
the unpenned sites was 8.75%. The greatest survi-
val in the unpenned areas was 65% but, as ex-
plained above, was due to protection provided by
baffle frames. These data indicate that at least
85-90% of the observed losses in the unpenned
sites were due to predation. The importance of
these data is amplified when the size of the clams
is considered.

The average size of clams in July 1977 was 3.2
cm and by October was 3.9 cm (hinge to lip). The
percentage marketable clams (1 in (25.4 mm)
thick) was the same for both the penned and un-
penned sites (58.5 and 58.6%) in October. This
indicates no size selection of clams, but that clams
of all sizes were consumed. The loss of such large
clams represents 2 yr of work and a product of
market size.

Flounders, known to prey on young Mercenaria
mercenaria and to selectively eat the neck of adult
clams, have been eliminated as potential pred-
ators because they are not capable of crushing the
shell of 3 cm high hard clams. Of the seven species
of fish capable of forming pits and crushing the
shell of 3 cm size hard clams (Table 3), only two are
known to be common away from the inlets and
near the planted areas (Richards and Castagna
1970; Musick 1972). These two species, Z)asya^/s
centroura andRhinoptera bonasus, are prime sus-
pects for causing the destruction in our unpro-
tected plots. The former cannot be eliminated be-

TABLE 3. — Potential fish predators on 3 cm hard clams in Vir-
ginia. Information from Richards and Castagna ( 1970) and
Musick (1972).

Scientific name

Common name

Dasyatis americana
D. centroura
D. sayi

Myliobatis freminvillei
Aetobatus narinari
Rhinoptera bonasus
Pogonias cromis

Souttiern stingray
Roughtall stingray
Bluntnose stingray
Bullnose ray
Spotted eagle ray
Cownose ray
Black drum

540

cause of its large size and overall abundance
within the area and the latter because of its school-
ing behavior. Schools of i?. bonasus often destroy
large areas of eelgrass and other habitats in
search of clams, their primary food (Orth 1975,
1977). Burton (footnote 3) used hog wire fencing to
keep schools of cownose rays from his beds of in-
ventoried and replanted market size Mercenaria.
Because of the suddenness of the disappearance
(<2 wk) and the presence of crushed clam shell in
this and other plantings, we believe the most
likely predator was a school of/?, bonasus.

Our data indicate that losses, due to such preda-
tion, would be unpredictable, but it would be
financially devastating to the clam grower. The
use of a fence or some other device to protect the
clams is essential for successful field culture in
areas where large predators occur. These fences
can be removed during the winter to prevent ice
damage, but along the Virginia coast they should
be kept in place and maintained at all times from
late March to early November.

Literature Cited

KRAEUTER, J. N., AND M. CASTAGNA.

1977. An analysis of gravel, pens, crab traps, and current
baffles as protection for juvenile hard clams (Mercenaria
mercenaria). Proc. 8th Annu. Meet. World Mariculture
Soc, p. 581-592.

MUSICK, J. A.

1972. Fishes of Chesapeake Bay and the adjacent coastal
plain. In M. L. Wass i compiler), A check list of the biota
of lower Chesapeake Bay, p. 175-212. Va. Inst. Mar Sci.
Spec. Sci. Rep. 65.

Orth, r. j.

1975. Destruction of eelgrass, Zosfera marina, by the cow-
nose ray, Rhinoptera bonasus, in the Chesapeake
Bay Chesapeake Sci. 16:205-208.

1977. The importance of sediment stability in seagrass
communities. In B. C. Coull (editor), Ecology of marine
benthos, p. 281-300. Belle W. Baruch Lib. Mar Sci. 6.
Univ. S.C. Press, Columbia.
RICH.ARDS, C. E., AND M. CAST.^GNA.

1970. Marine fishes of Virginia's Eastern Shore (inlet and
marsh, seaside waters). Chesapeake Sci. 11:235-248.

Tiller, R. e., J. B. Glude, and L. D. Stringer.

1952. Hard-clam fishery of the Atlantic coast. Commer
Fish. Rev 14(10:1-25.

JOHN N. KRAEUTER

Michael Castagna

Virginia Insititute of Marine Science and
School of Marine Science
College of William and Mary
Wachapreague, VA 23480

A DIRECT METHOD FOR

ESTIMATING NORTHERN ANCHOVY,

ENGRAULIS MORDAX, SPAWNING BIOMASS

Two methods exist for estimating spawning bio-
mass, the total weight of mature fish, from abun-
dance of spawning products. The first, or direct,
method (Saville 1963) consists of dividing an
estimate of egg production by the product of batch
fecundity and the proportion of females in the
mature stock. Saville safely assumed spawning
frequency to be unity. The second method is
indirect (Murphy 1966; Smith 1972) and utilizes
information from two different species. Smith
illustrated the second method, using information
on the Pacific sardine, Sardinops caerulea, and
northern anchovy, Engraulis mordax. Sardine
spawner biomass is estimated from landings data
and cohort analysis; anchovy spawner biomass is
estimated by multiplying the estimated sardine
spawner biomass by the product of the anchovy-to-
sardine ratio of larval abundance and the sardine-
to-anchovy ratios of fecundity, and spawning
frequency. Computation was facilitated by assum-
ing the unknown spawning frequencies to be
equal, making the ratio of spawning frequencies
unity. Up to the present only the second method
has been used for the northern anchovy. This
paper presents estimates derived from the first.

Computation of spawning biomass is simplified
for the direct method when spawning occurs but
once and for the indirect method when both
species spawn with equal frequency. Difficulties
arise when spawning is continuous and when it
cannot be safely assumed that all mature fish
spawn with the same frequency. This is the case
with the northern anchovy. Spawning products
are present all year, with a maximum abundance
occurring in the late winter and early spring and
a minimum during late summer and early fall.
Abundance of and seasonal pattern of spawning
products give no clue as to the number of spawn-
ings by size and age, or even to the average
number of spawnings.

Under the following conditions spawning fre-
quency can be estimated from examining the
spawming condition of females: 1) females can be
examined for a characteristic that indicates when
spawning takes place; 2) the length of tim.e such
a characteristic remains detectable can be esti-
mated; 3) the spavming rate remains relatively
constant over the sampling interval.

The spawning fraction, or frequency, is the

FISHERY BULLETIN: VOL. 78. NO. 2. 1980.

541

fraction of females displaying the characteristic
divided by the length of the time interval the
characteristic remains detectable. Say, from a
sample of 10 females, 2 display a characteristic
which lasts for 1 day and which indicates that
spawning will take place in approximately 1 wk.
The daily spawning fraction 1 wk hence will be 1/5.
Given this method for estimating spawning
fraction the following relationship holds:

P - Siabc)

(1)

where P = production in eggs,

a = batch fecundity in (eggs)/(unit
weight),

b = fraction spawning (weight of spawn-
ing females)/(weight of all mature
females),

c = (weight of females)/! weight of spawn-
ing stock),

S = spawning biomass.

Spawning biomass can be estimated directly:

S = P{abc)~\ (2)

Hunter and Goldberg (1979) examined female
northern anchovies for characteristics that would
indicate a recent spawning. They found that
following spawning follicles of the northern an-
chovy go through a sequence of identifiable de-
generative stages. The first two stages, which
Hunter and Goldberg referred to as day 0 and day
1, have durations of 1 day. Stage identification is
subject to error. Day-0 follicles can be misiden-
tified as day 1; day-1 follicles can be misidentified
as day 2 and beyond. The most easily identified
stage is day 1. If the spawning fraction, 6, is based
on day-1 follicles an adjustment factor, say d, is
required in Equation (2):

P(ab'c)^d

(3)

where 6', replacing b, is the observed fraction.

The adjustment factor is computed by using
information on the fraction of day-0 follicles mis-
classified as day 1, say do, and the fraction of
day-1 follicles correctly classified, say d^.

d = (c?o + di)
Yarid) = VarCffo) + Var(di).

Estimates based on Hunter and Goldberg's (1979,
542

table 1) blind classification study for d^ and d^
are 5/21 and 16/19 respectively; hence

d = 1.080
Var(d) = 0.016.

From examination of 195 females taken by mid-
water trawl during the time interval 15-27 Feb-
ruary 1978, Hunter and Goldberg estimated the
observed daily spawning fraction and its variance:

b' = 0.159

Var(6'

4.561 X 10

Based on the total female weight of nonspawners
the estimated batch fecundity and variance ai-e
from Hunter and Goldberg (1979, table 6)

a = 396 eggs/g (or 3.96 x 10^ eggs/t)
Var(a) = 886.

For the time period 18 February-17 March 1978,
Zweifel^ estimated daily egg production. From 177
plankton samples, northern anchovy eggs and
larvae were staged from time of spawning. Esti-
mated total numbers at stage were regressed on
time. The ordinate intercept, number at time zero,
is the estimated egg production:

2.321 X lO'-'eggs/d

26

Var(P) = 1.825 x 10

If the female to male sex ratio in numbers were
1:1 and if the two sexes had equal growth rates in
terms of weight then c could be assumed to be 0.5.
However, because of conflicting and insufficient
evidence neither of these two hypotheses can be
supported. Klingbeil ( 1978) demonstrated that the
distribution of northern anchovy sexes is hetero-
geneous over space and time and that estimates of
sex ratio are dependent on the sampling gear. From
the purse seine fishery Klingbeil estimated that
the ratio of numbers of females to males varies
between 1.14:1 and 2.02:1 for 1969-76. From 9yr of
midwater trawl data Klingbeil estimated that the
sex ratio is 1.03:1. Since midwater trawl surveys
cover a wider geographic area and size range of
anchovies, they probably provide an estimate
closer to that of the true population sex ratio.
However, since neither midwater trawl surveys

'James Zweifel, Southwest Fisheries Center La Jolla Lab-
oratory, NMFS, NOAA, P.O. Box 271, La Jolla, CA 92038,
pers. commun.

nor purse seines are designed to estimate sex ratio
it can only be stated that the anchovy sex ratio has
not been adequately estimated.

Collins (1969) showed that females are greater
in length and weight at age than males. However,
since Collins' estimates are based on combined
data from three fishing seasons and, since female
weights are known to fluctuate within season due
to spawning activity, the precision with which the
data can be used for estimation purposes is open
to speculation.

For the present purpose of estimating c the sex
ratio of the number of females to males plus
females as estimated from the February 1978
midwater trawl survey (Hunter and Goldberg
1979) will be used. Reexamining original data
used by Hunter and Goldberg (1979, table 5) the
ratio estimate is

c
Var(c)

0.550
0.001.

This assumes, of course, an equal weight at age.

In the future, the best estimate of c is likely to be
the ratio of the actual sampled weights of males
and females; these were not available for the

proximations. P may not be constant for as long a
time interval as assumed here. Observed b' was
found to be consistent for time of day, weight of
fish, and geographic location. This may not prove
to be the case under more intensive sampling.
Another problem in estimating the spawning
fraction is in determining female sexual maturity.
This problem may be particularly acute for recent-
ly spawned young females where microscopic
analysis is necessary to separate the recently
spawned from the sexually immature. Misclassi-
fying recently spawned as immature would tend to
inflate the estimated b.

By the delta method (Seber 1973), the variance
of Sis

[

Var(S) = {ab'cV^ d^VariP) + P^Varid)

+ {PdY

r Var(a

) Var(6') Var(c)

+

b'-

+

&

]]

.(4)

Dividing Equation (4) by the square of Equation
(3) and then taking the square root we have the
coefficient of variation (CV) of spawning biomass

CV(S) = J[CY{P)f + [Cy{a)f + [CV(6)]' + [CV(c)]' + [CV{d)f, (5)

February 1978 survey. This would, of course,
require the assumption that the sex ratio can
differ from 1:1, that the weight distribution of the
two sexes can change with time, and that a sample
estimate is a better estimate than any hypothe-
sized or long-term average value.
Using the following estimates

P = 2.321 X lO'-'eggs/d

eggs/t

a = 3.96 X 10
b' = 0.159

8

c
d

0.550
1.080

the estimated S is approximately 0.72 million t.
This is reasonably close to the estimate by the
Smith procedure (Stauffer and Parker^) of 1.17 t.
At this time caution should be exercised in inter-
preting the general range described by these two
estimates. The parameters of Smith's procedure
have not been formally estimated. The parameter
estimates of this new method are only first ap-

=^StaufTer, G. S., and K. R. Parker. 1978. Estimate of the
spawning biomass of the northern anchovy central subpopula-
tion for the 1978-79 fishing season. U.S. Dep. Commer., NOAA,
NMFS/SWFC Adm. Rep. LJ-78-9, 10 p.

which is the component vector of the coefficients of
variation of the estimated parameters, right side
of Equation (3). Since possible covariance terms
are neglected, Equation (5) may be somewhat
oversimplified. However, Equation (5) allows a
first approximation to delegating the relative
impact of the precision of the individual param-
eter estimates. The squared coefficients of varia-
tion are as follows:

[CV(P)]^ = 0.339
[CYia)f = 0.005
[CV(6)]=' = 0.018

[cy(c)v

[CY{d)f

0.003
0.013.

ThusCV(S) = 0.614. P contributes approximately
8 times more to the coefficient of variation of the
spawner biomass estimate than all other param-
eters combined. In the future, additional effort
will be allocated to estimating production.

The utility of the direct method, Equation (2),
lies in the fact that all the parameters can be
estimated. The same samples used for estimating
b' can be used to estimate a and c. This can be
done with 2 wk of midwater trawling. It is hoped

543

that precise estimation of production can be done
within 30 d by sampling for eggs; this goal seems
attainable for the northern anchovy. Utilization of
the method for other species seems feasible.

Literature Cited

COLLINS, R. A.

1969. Size and age composition of northern anchovies
^Engraulis mordax) in the California anchovy reduction
fishery for the 1965-66, 1966-67, and 1967-68 seasons. In
the northern anchovy (Engraulis mordax) and its fishery
1965-1968, p. 56-74. Calif. Dep. Fish Game,Fish Bull. 147.

Hunter, J. R., and S. R. Goldberg.

1980. Spawning incidence and batch fecundity in north-
em anchovy, Engraulis mordax. Fish. Bull., U.S. 77:
641-652.

Klingbeil, r. a.

1978. Sex ratios of the northern anchovy, Engraulis
mordax, off southern California. Calif. Fish Game
64:200-209.

Murphy, G. I.

1966. Population biology of the Pacific sardine ( Sardinops
caerulea). Proc Calif. Acad. Sci., Ser 4, 34:1-84.

Saville, a.

1964. Estimation of the abundance of a fish stock from egg
and larval surveys. In J. A. Gullsmd (editor). On the
measurement of abundance of fish stocks, p. 164-170.
Rapp. P-V. Reun. Cons. Perm. Int. Explor Mer 155.
SebeR, G. a. E

1973. The estimation of animal abundance and related
parameters. Hafner Press, N.Y., 506 p.
SMITH, P E.

1972. The increase in spawning biomass of northern
anchovy, Engraulis mordax. Fish. Bull., U.S. 70:
849-874.

Keith Parker

Southwest Fisheries Center La Jolla Laboratory
National Marine Fisheries Service, NOAA
P.O. Box 271
La Jolla, CA 92038

FOOD OF THE HARBOR SEAL,

PHOCA VITULINA RICHARDSI,

IN THE GULF OF ALASKA

The harbor seal, Phoca vitulina richardsi (Shaugh-
nessy and Fay 1977), is the most abundant and
widespread coastal pinniped in the Gulf of Alaska.
Harbor seals occupy virtually all nearshore hab-
itats, and individuals occasionally occur as far as
100 km offshore (Spalding 1964; Wahl 1977; Fiscus
et al. ). Despite their abundance and ecological

'Fiscus, C. H., H. W. Braham, R. W. Mercer, R. D. Everitt,
B. D. Krogman, P D. McGuire, C. E. Peterson, R. M. Sonntag,

importance, little information is available on
their diet in Alaskan waters. In the most extensive
food study published to date, Imler and Sarber
( 1947) examined stomachs of 99 seals from south-
eastern Alaska and 67 from the Copper River
Delta. Wilke (1957) presented information on the
food of seven harbor seals collected from Amchitka
Island in the western Aleutian Islands. Kenyon
(1965) reported on the stomach contents of 11
harbor seals taken in the same location. Bishop
(1967) commented on stomach contents of two
seals from Aialik Bay and two from Tugidak
Island. Virtually no information has been avail-
able on the food of harbor seals from the Gulf
of Alaska.

The study area (Figure 1) included coastal Gulf
of Alaska from Yakutat Bay to Sanak Island. The
portion of Cook Inlet north of Kachemak and
Kamishak Bays was not included. The study area
was divided into seven subareas for data analysis:
northeastern Gulf of Alaska, Copper River Delta,
Prince William Sound, Kenai coast, Lower Cook
Inlet, Kodiak, and Alaska Peninsula.

Selection of Valdez as terminus of the trans-
Alaskan oil pipeline and planned outer conti-
nental shelf oil and gas lease sales were the
principal motivating factors for conducting this
research. Production and transport of crude oil
appeared to have the potential for significant
alteration of the marine biota (Evans and Rice
1974) thus influencing the abundance and com-
position of harbor seal prey species. Established
commercial fisheries for salmon, Oncorhynchus
spp.; Pacific herring, Clupea h. harengus; halibut,
Hippoglossus stenolepis; king crab, Paralithodes
camtschatica; snow crab, Chionoecetes bairdi; Dun-
geness crab. Cancer magister; and shrimp, Pan-
dalus spp., occur over the area, and pinnipeds are
sometimes considered to be significant compet-
itors with these fisheries. Data are needed to
establish the possible impact of harbor seals on
these commercially exploited species. Plans for
developing fisheries are required by Federal laws
(Public Law 94-265, Fishery Conservation and
Management Act of 1976, and Public Law 92-522,
Marine Mammal Protection Act of 1972) to utilize
an integrated ecosystem approach to management

and D. E. Withrow. 1976. Seasonal distribution and relative
abundance of marine mammals in the Gulf of Alaska. In
Environmental assessment of the Alaskan Continental Shelf.
Vol. 1. Principal investigators reports for October- December
1976, p. 19-264. Environmental Research Laboratories, NOAA,
Boulder, Colo.

544

FISHERY BULLETIN: VOL. 78, NO. 2, 1980.

164°

160°

Figure i.

156° 152° 148°

-Geographic subdivisions of Gulf of Alaska study area.

144°

considering marine mammal populations as well
as fishery resources.

Methods

A total of 548 harbor seals were collected by rifle
throughout the Gulf of Alaska from 1973 through
1978 (Table 1). Reasonably complete seasonal
coverage was obtained for Prince William Sound
and the Kodiak area. Stomach contents were
removed in the field, wrapped in muslin, and
preserved in 10% Formalin.^ In the laboratory the
volumes and number of occurrences (number of

Reference to trade names does not imply endorsement by
the National Marine Fisheries Service, NOAA.

Table l. — Geographic and seasonal distribution of harbor seals
collected in the Gulf of Alaska.

Number of seals

Area

Jan-

Mar.

Apr.-
June

July-
Sept.

Oct-
Dec.

Northeastern Gulf of Alaska

Copper River Delta

Prince William Sound

Kenai coast

Lower Cook Inlet

Kodiak

Alaska Peninsula

62
43

4

22
18
24
14
37
106
20

27
26

38
3

9

39
3

53

stomachs in which a prey species was found) were
determined for prey species. Because digestion
was often advanced, skeletal materials, partic-
ularly fish otoliths and cephalopod mandibles
(beaks), were the primary criteria for identifica-
tion (Fitch and Brownell 1968; Pinkas et al. 1971).

Otoliths and other skeletal components from
fish were tentatively identified to the lowest
taxonomic level possible by comparison with ref-
erence materials. Otolith identifications were ver-
ified by John E. Fitch, California Department of
Fish and Game, Long Beach. Cephalopod beaks
were classified as either squid or octopus with the
aid of Pinkas et al. (1971), and squid beaks were
identified to family by Clifford H. Fiscus, National
Marine Fisheries Service, NOAA, Seattle, Wash.
Decapod crustaceans were identified by Kathryn
J. Frost and Lloyd F. Lowry, Alaska Department
of Fish and Game, Fairbanks.

In order to integrate data on both frequency of
occurrence and prey volumes into a single ranking
of prey utilization I used a modified form of the
Index of Relative Importance (IRI)^ devised by

^Original Index of Relative Importance as derived by Pinkas
et al. (19711 was calculated by summing the numerical and
volumetric percentage values and multiplying by the frequency
of occurrence jjercentage value.

545

Pinkas et al. (1971). The numerical component
of their formula was deleted because of the dis-
parity in size of harbor seal prey items. The
modified IRI was calculated as percentage of
occurrences multiplied by percentage of volume.

Results

Food was present in 269 of the 548 stomachs.
Fishes composed 74.5*^, cephalopods 21.5%, and
decapod crustaceans 4.0% of the occurrences
(Table 2). A minimum of 27 species of fish were
identified belonging to 13 families. Cephalopods
included both octopus and squids of the family
Gonatidae. Decapod crustaceans were primarily
shrimps with one occurrence of a crab. The five
top-ranked prey of harbor seals in the Gulf of
Alaska were walleye pollock, octopus, capelin,
eulachon, and Pacific herring (Table 3).

Regarding prey utilization by area of collection
(Table 4), sample sizes were small and collections
did not span all seasons (Table 1). Either walleye
pollock or octopus was the top-ranked food in all

Table 2. — Stomach contents of 269 harbor seals collected in
the Gulf of Alaska, all areas and seasons combined. [% under
Occurrences = Percentage of occurrences and 95% confidence
limits.]

Table 2.— Continued.

Occurrences

Volume

Occurrences

Volume

Prey

No.

ml

Cephalopocia:
Octopus sp., octopus
Gonatidae. squids
Decapoda:
Stirimps
Crabs
Rajidae:

Raja spp.. skates
Clupeldae:

Clupea h. harengus. Pacific
herring
Salmonidae:

Oncorhynchus spp.. salmon
Osmeridae:
Mallotus villosus. capelin
Thaleichthys pacificus,

eulachon
Hypomesus pretiosus,

surf smelt
Unidentified Osmeridae,
smelts
Gadidae:
Eleginus gracilis, saffron cod
Gadus macrocephalus .

Pacific cod
Microgradus proximus.

Pacific tomcod
Theragra chalcogramma .
walleye pollock
Zoarcldae:

Lycodes spp.. eelpouts
Scorpaenidae:

Sebastes spp., rockfishes
Hexagram midae:
Hexagrammos spp.,
greenlings

97

77
20
18
17

1

29

9
67
40

22

4

1

134

5

28

7

94

6

4

21,5=3.9
17.1±3.5
4.4r2.0
4.0±1,9
3.8=1.9
0.2 = 0.5

0.7 = 0.9

6.4 = 2.4

2.0=1.4
14.9±3,4

8.8 = 2.7

4.9 = 2.1
0.9= 1.0

0.2 = 0.5

29.7 = 4.3

1.1 = 1.1

6.2 = 2.3

1.6=0.7

20.8 = 3.9
1.3=1.2
0.9=1.0

0.4 = 0.7

20,433

18,753

1,680

3,800

3,400

400

2,780

6,560

4,477
23,034
10,687

1 1 ,837

460

50

26,603

395

3,240

1,030

21,938

60

810

400

20.0
18.3
1.6
3.7
3.3
0.4

2.7

6.4

4.4
22.5
104

11.6

04

■ 0.1

26.0

0.4

3.2

1.0

21.4

0 1

0.8

0,4

Prey

No.

%

ml

%

Cottidae:

Dasycottus setiger.

spinyhead sculpin
Enophrys bison, buffalo

sculpin
Myoxocephalus spp.,

sculpins
Unidentified Cottidae,

sculpins
Trichodontidae:

Trichodon tnchodon. Pacific

sand fish
Bathymastendae:
Bathymaster signatus.

searcher
Ammodytidae;
Ammodytes hexapterus.

Pacific sand lance
Pleuronectidae:
Atheresthes stomias .

arrowtooth flounder
Eopsettajordani. petrale sole
Glyptocephalus zachirus .

Rex sole
Hippoglossoides elassodon .

flathead sole
Lepidopsetta bilineata . rock

sole
Limanda aspera. yellowfin

sole
Lyopsetta exilis. slender sole
Parophrys vetulus. English

sole
Unidentified Pleuronectidae
Unidentified fish remains

Totals

10 22=1.5

2 0,4 = 0.7

1 0.2 = 0.5

2 0.4 = 0.7
5 1.1 = 1.1

10

19
23

3

1

1

5

1

6
2

2

2
17

2.2=1.5
07=09

4.2 = 2.0

5.3 = 22

0.7=09
0.2=0.5

0.2 = 0.5

1.1 = 1.1

0.2=0.5

1.3=1.2
0-4=0.7

0.4 = 0.7
0.4 = 0-7
3.8=1.9

451 100.0

1.912 1.9

240 0.2

1 ,430 1 .4

242 02

3,025 3.0

40 0.1

463 0.5

2,615 2.6

150 0.1

130 0.1

1,650 1.6

65 0.1

620 0.6

5,320 5.2

102.332 100.1

Table 3. — Rankings by modified Index of Relative Importance
(IRI, see text footnote 3) of major prey of harbor seals collected
in the Gulf of Alaska. Only those prey with IRI 3= 2 are included.

Rank

Prey

Modified
IRI

Occur-
rences

Volume

Co)

1

Walleye pollock

2

Octopus

3

Capelin

4

Eulachon

5

Pacific herring

6

Pacific cod

7.5

Flatfishes

7.5

Shrimps

9

Salmon

10

Squids

11

Pacific sandfish

12

Sculpins

14

Skates

14

Pacific sand lance

14

Pacific tomcod

445

313

92

57

41

20

13

13

9

7

7

4

2

2

2

20.8
17.1
8.8
4.9
6.4
6.2
5.1
3.8
2.0
4.4
2.2
2.2
0.7
4.2
1.6

21.4

18.3

10.4

11.6

6.4

3.2

26

3.3

4.4

1.6

3.0

1.9

2.7

0.5

1.0

marine areas and eulachon was dominant in the
estuarian and freshwater habitats of the Copper
River Delta. Walleye pollock was the top-ranked
item in the eastern areas: northeastern Gulf of
Alaska, Prince William Sound, and the Kenai
coast. In the western areas: Lower Cook Inlet,
Kodiak, and the Alaska Peninsula, octopus had
the highest ranking. In Lower Cook Inlet, octopus
and shrimps made up over 60% of both total

546

Table 4. — Major prey of harbor seals from seven geographic
areas in the Gulf of Alaska. Prey ranked in order of modified
Index of Relative Importance (IRI, see text footnote 3). Only prey
with IRI ^2 are included. [Occurrences = Percentage of
occurrences ± 95% confidence limits.]

Area and prey

IRI

Occurrences

Volume

(%)

Northeastern Gulf of Alaska (stomachs with contents 17: occurrences 39;

volume 2,420 ml)
Walleye pollock 640 28.2±15.4 22.7

Surf smelt 196 10.3±10.8 19.0

Capelm 143 23.1 ±14.5 6.2

Shrimps 131 2.6± 6.3 50.4

Copper River Delta (stomachs with contents 14; occurrences 15; volume

8.115 ml)
Eulachon 8,826 93.3 ±17.4 94.6

Salmon 36 6.7±17.4 5.4

Prince William Sound (stomachs with contents 83; occurrences 122; volume

28,290 ml)

Walleye pollock
Pacific herring
Squids
Octopus
Salmon
Capelin
Pacific tomcod
Pacific cod
Saffron cod
Eulachon

1,375

166

77

75

33

16

5

4

3

3

29. 5±

14.8±

13. 1±

13.9±

3.3±

4.1 ±

1.6±

4.9 ±

2.5±

1.6±

8.5
6.7
6.4
6.6
3.6
3.9
2.7
4.2
3.2
2.7

46.6
11.2
5.9
5.4
10.0
3.8
3.3
0.9
1.3
1.9

Kenai coast (stomachs with contents 30; occurrences 52; volume 7,225 ml)

Walleye pollock
Pacific herring
Pacific sandfish
Capelin
Pacific tomcod

1,503

247

44

19

4

40.4±14.3

11. 5±
7.7±
5.8 ±
3.8±

9.6
8.2
7.3

6.2

Lower Cook Inlet (stomachs with contents 17; occurrences 23;

5.412 ml)

Octopus 1.697 39.1 ±23.4

Eulachon 532 17.4 ±18.6

Shrimps 501 21, 7± 20.0

Capelin 17 8.7±14.4

Kodiak Island (stomachs with contents 102; occurrences

42.685 ml)

192;

Octopus

Capelin

Walleye pollock

Flatfishes

Pacific cod

Pacific sand lance

Pacific herring

Shrimps

Salmon

Sculpins

Eulachon

631

323

70

63

55

9

9

8

6

3

2

21.4 =

10. 9±

12.0±

10.9±

8.3±

8.3±

2.1 ±

3.6±

2.1 ±

4.2±

0.5±

6.1
4.7
4.9
4.7
4.2
4.2
2.3
2.9
2.3
3.1
1.3

37.2

21.5

5.7

3.3

1.0
volume

43.4

30.6

23.1

1.9

volume

29.5
21.3
5.8
5.8
6.6
1.1
4.2
2.2
2.9
0.7
4.6

Alaska Peninsula (stomachs with contents 6; occurrences 9; volumes 8,185 ml)
Octopus 929 33.3±41.8 27.9

Walleye pollock 824 22.2±37.5 37.1

Pacific sandfish 342 11.1 ±29.7 30.8

Pacific cod 40 22. 2± 37.5 1.8

Sculpins 26 11.1 ±29.7 2.3

occurrences and volumes which was nearly twice
the percentages in other areas.

Chi-square analyses of prey occurrences for
Kodiak Island and Prince William Sound indi-
cated that in Prince William Sound more walleye
pollock (P<0.01) were eaten than in Kodiak
(Table 5). In Kodiak there was higher utilization
(P< 0.05) of capelin than in Prince William Sound.
Octopus and Pacific cod were not utilized at
significantly different rates {P> 0.05). While sam-
ples were inadequate for statistical testing, it
appeared that more squids and Pacific herring and

Table 5. — Comparison of occurrences of principal prey (N^4)
of harbor seals collected in Prince William Sound and the
Kodiak Island area. Statistical comparisons were made by
chi-square analysis. [% = Percentage ± 95% confidence limits;
— = Inadequate sample for statistical testing.]

Kodiak

Prince William Sound

Prey

No.

%

No.

%

>0.05

< 0.05
>0.10
<0.01

Octopus 41 21.4 + 6.1 17 13.9±6.5

Squids 2 1.0±1.7 16 13.1±6.4

Shrimps 7 3.6±2.9 1 0.8±2.0

Pacific herring 4 2 1 ±2 3 18 14.8±6.7

Salmon 4 2.1 ±2.3 4 3.3±3.6

Capelin 21 10.9 ±4.7 5 4.1 ±3 9

Pacific cod 16 8.3±4.2 6 4.9±4.2

Walleye pollock • 23 12.0±4.9 36 29.5±8.5

Sculpins 8 4.2±3.1 0 0.0

Pacific sand lance 16 8.3±4.2 0 0.0

Flatfishes 21 10.9±4.7 1 0.8±2.0

Total occurrences 1 92 1 22

fewer Pacific sand lances, flatfishes, and sculpins
were eaten in Prince William Sound than in
Kodiak.

Salmon were found in the diet of harbor seals
from both Prince William Sound and the Kodiak
Island area only during the summer (Table 6). In
the Kodiak area, feeding on Pacific sand lance
appeared to be greatest in the fall while use of
capelin seemed to peak in the spring. Use of
Pacific herring by harbor seals appeared greatest
in the spring in Prince William Sound.

Prey items were found in the stomachs of 13
harbor seal pups 2.5-11 mo of age and included
shrimps, capelin, Pacific tomcod, walleye pollock,
and Pacific sand lance. All items were <15 cm
total length.

Discussion

The high ranking of walleye pollock in the
harbor seal diet may have been a direct function of
its abundance. Pereyra and Ronholf* found that
walleye pollock was the dominant fish species in
the Gulf of Alaska, composing 459c by weight of
total fish stocks. Octopus, the second-ranked prey,
appears to be an important food of harbor seals
throughout the eastern North Pacific as nearly all
food studies have found them to be a major
component of the diet (Scheffer and Sperry 1931;
Imler and Sarber 1947; Fisher 1952; Wilke 1957;
Spalding 1964; Kenyon 1965; Bishop 1967). Five
of the six, top-ranked prey were off-bottom, school-
ing fishes. Use of this type of prey may minimize

"Pereyra, W. T, and L. L. Ronholt. 1976. Baseline studies
of demersal resources of the northern Gulf of Alaska shelf
and slope. U.S. Dep. Commer., NOAA Processed Rep. NMFS
NWFC, 281 p.

547

Table 6. — Seasonal occurrences of principal prey (N^4) of harbor seals from the Kodiak
Island area and Prince William Sound. [No. = Occurrences of prey; % = Percentage and
95% confidence limits.]

Jan .-Mar.

Apr.- June

July-Sept.

Oct.- Dec.

Area and prey

No.

%

No.

%

No.

%

No.

%

Kodiak Island area:

Octopus

0

0.0

24

25.8± 94

6

15 0+12.3

9

15.8±10.3

Salmon

0

0.0

0

0.0

4

10 0± 10.5

0

0.0

Capelin

0

0.0

14

15.1± 7.8

3

7.5± 9.4

3

5.3± 6.7

Pacific cod

0

0.0

8

8.6± 6.2

3

7.5± 9.4

4

7.0± 7.5

Walleye pollock

0

00

15

16.1 ± 8.0

3

7.5± 9.4

6

10.5:= 8.8

Pacific sand lance

0

0.0

0

0.0

3

7.5± 9.4

12

21.1±11.5

Total occurrences

2

93

40

57

Prince William Sound:

Octopus

9

15.8±

10.3

2

15.4±21.6

2

14.3±20.1

5

13.2±12.1

Squids

8

14.0±

9.9

0

0.0

3

21 4-23.5

5

13.2±12.1

Herring

8

14.0±

9.9

5

38 5^29.2

2

14.3±20.1

2

5.3± 8.4

Salmon

0

0.0

0

0.0

4

28.6±25.9

0

0.0

Capelin

4

7.0 ±

7.5

0

00

1

7.1 ±14.7

0

0.0

Walleye pollock

15

26. 3i

12.3

4

30.8-27.7

1

7.1±14.7

15

39.5-16,9

Total occurrences

57

13

14

38

foraging effort and conserve energy compared
with selection of more solitary species (Smith and
Gaskin 1974).

The major differences in prey utilization be-
tween Prince William Sound and Kodiak are not
readily explainable. However, water depths and
topography for the two areas are considerably dif-
ferent (U.S. Department of Commerce^). Kodiak
waters have considerable shallow shelf area, par-
ticularly east and south of the Island, and Prince
William Sound generally has a rocky, precipitous
coast and deep waters reaching 740 m. These
features may influence prey composition, abun-
dance, and availability to harbor seals.

Differential utilization of certain prey by season
appeared to be explained by availability in most
instances. Salmon occurred in stomachs of seals
from both Kodiak and Prince William Sound only
during the summer. In both areas salmon are only
available in quantity in nearshore waters during
this period. The apparent increases during spring
in utilization of herring in Prince William Sound
and capelin in the Kodiak area probably reflected
nearshore distribution associated with spawning
in these species (Hart 1973; Jangaard 1974). In the
Kodiak area. Pacific sand lance were utilized to
a greater extent during fall. No reason is known
for this.

Six of the 10, top-ranked prey; walleye pollock,
Pacific herring. Pacific cod, flatfishes, shrimps,
and salmon are either currently harvested com-
mercially or may be harvested in the near future
(North Pacific Fishery Management Council^). Of

particular interest is the possibility of increased
harvests of walleye pollock which was the top-
ranked prey of harbor seals accounting for about
21% of both total occurrences and volumes of food
items. Sergeant (1976) believed that fisheries
could compete with natural predators and cause
their populations to stabilize at levels well below
those existing prior to the fishery.

Harbor seals are present on the Copper River
Delta from May through September. The results of
this study and those of Imler and Sarber (1947)
indicated that eulachon was the dominant prey
from late May to mid-July. Nothing is known
about feeding during late summer and fall when
eulachon are not present.

Although specialized feeding on shrimps by
newly weaned harbor seal pups was reported by
Havinga (1933), Fisher (1952), and Bigg (1973),
small fishes were the primary food of young seals
<1 yr old collected during this study.

During this study several sampling problems
and prey identification biases became apparent.
Distinct geographic and seasonal variations in
prey utilization were found to occur and because of
this it was difficult to determine if a completely
representative sample was obtained. Also, our
sampling was restricted to nearshore waters. If a
significant amount of feeding took place offshore
and availability and composition of potential prey
was different there, the results of this study would
not be totally representative. In addition, the
probability of detecting and identifying various

^U.S. Department of Commerce, NOAA, Nautical Charts
No. 8556 and 16700.

"North Pacific Fishery Management Council. 1978. Fish-
ery management plan for the Gulf of Alaska groundfish fishery
during 1978. Unpubl. manuscr, 220 p. North Pacific Fishery
Management Council, PO, Box 3136 DT, Anchorage, AK 99510.

548

prey in the stomachs was not equal. Cephalopod
beaks are not always passed through the intes-
tinal tract and may remain in the stomach for
several days before they are regurgitated (Pitcher
unpubl. data). This increases the probability of
detection thereby exaggerating estimates of their
utilization.

Acknowledgments

This study was supported in part by the Bureau
of Land Management through an interagency
agreement with the National Oceanic and Atmo-
spheric Administration, under which a multiyear
program responding to needs of petroleum devel-
opment of the Alaska continental shelf is managed
by the Outer Continental Shelf Environmental
Assessment Program office. Support was also
provided by the Marine Mammal Commission and
the Alaska Department of Fish and Game. I
am grateful to R. Aulabaugh, D. Calkins, D.
McAllister, and K. Schneider for field assistance.
Thanks are due to D. Calkins, F. Fay, K. Frost,
L. Lowry, D. McKnight, and K. Schneider who
reviewed drafts of this paper.

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KENNETH W. Pitcher

Alaska Department of Fish and Game
333 Raspberry Road
Anchorage, AK 99502

PRODUCTION AND GROWTH OF SUBYEARLING

COHO SALMON, ONCORHYSCHUS KISLTCH,

CHINOOK SALMON, OSCORHYSCHUS

TSHAVC^TSCHA, AND STEELHEAD,

SALMO GAIRDNERI, IN ORWELL BROOK,

TRIBUTARY OF SALMON RIVER, NEW YORK

Decline of lake trout, Salvelinus namaycush, and
burbot. Lota lota, populations in the Great Lakes
from 1930 to 1950 created a void of a large offshore
piscivore in these waters. Smith (1968) attributed
the decline to overexploitation by the commerical
fishery and predation by the sea lamprey, Pet-
romyzon marinus. The decline was followed by
proliferation of the alewife, Alosa pseudoharen-
gus, in Lakes Ontario, Huron, and Michigan

fishery BULLETIN: VOL. 78, NO. 2, 1980.

549

(Berst and Spangler 1973; Christie 1973; Wells
and McLain 1973). As a result the State of Michi-
gan in 1966 undertook a program to establish coho
salmon, Oncorhynchus kisutch, in Lakes Michi-
gan and Superior in hopes of creating a valuable
sport fishery based on alewife as the major forage
species (Tody and TannerV). The success of the
Michigan program provided an incentive to other
states and provinces bordering the Great Lakes to
undertake similar programs.

New York State began its salmonid program for
Lake Ontario in 1968 w^hen 41,000 coho salmon
were planted in the Salmon River. The following
year 70,000 chinook salmon, O. tshawytscha, were
planted in the Little Salmon River (Parsons 1973).
Stocking of steelhead, Salmo gairdneri, com-
menced in 1974 (Parker^). Stockings of coho salm-
on and steelhead have continued annually since
their inception. Chinook salmon plantings were
stopped after releases in the spring of 1976 be-
cause contaminant levels in their flesh generally
exceeded action levels for Mirex^ and PCB's when
these fish first became available to anglers as pre-
cocious jacks on their maiden spawning run at
1.8-2.7 kg (New York State Department of En-
vironmental Conservation^). However, chinook
salmon stocking was resumed in 1979.

From its inception, Michigan's salmonid pro-
gram has given high priority to natural reproduc-
tion as a supplement to hatchery production (Tody
and Tanner footnote 1). Subsequent studies have
focused on the extent of natural reproduction in
Michigan (Stauffer^) and other ecological aspects
of spawning activity (Taube^). Reproductive suc-
cess of Pacific salmonids has been examined in
Minnesota (Hassinger et al. 1974) and Wisconsin

•Tody, W.H., and H. A. Tanner. 1966. Coho salmon for the
Great Lakes. Mich. Cons. Dep. Fish. Manage. Rep. 1, 38 p. Fish
Division, Michigan Department of Natural Resources, Mason
Building, Lansing, MI 48926.

^C. E. Parker, Chief, Bureau of Fisheries, New York State
Department of Environmental Conservation, 50 Wolf Road, Al-
bany, NY 12233, pars, commun. October 1979.

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

"New York State Department of Environmental Conserva-
tion. 1977. Monthly report on toxic substances impacting on
fish and wildlife. Rep. 1, April 20, 1977.

^Stauffer, T. M. 1977. Numbers of juvenile salmonids
produced in five Lake Superior tributaries and the effect of
juvenile coho salmon on their numbers and growth, 1967-
1974. Mich. Dep. Nat. Resour, Fish. Res. Rep. 1846, 29 p. Insti-
tute for Fisheries Research, Museums Annex Building, Ann
Arbor, MI 48109.

^Taube, C. M. 1975. Abundance, growth, biomass, and in-
terrelationship of trout and coho salmon in the Platte
River. Mich. Dep. Nat. Resour., Fish. Res. Rep. 1830, 82 p.
Institute for Fisheries Research, Museums Annex Building, Ann
Arbor, MI 48109.

(Avery''). Canadian studies on Great Lakes
tributaries have mainly focused on steelhead re-
production (Alexander and MacCrimmon 1974).

In New York, chinook salmon begin their spawn-
ing run from Lake Ontario in late August and
early September ( Jolliff^). Chinook salmon redds
are present as early as mid-September in the
Salmon River in Oswego County. Although most
chinook salmon spawning occurs in the Salmon
River, smaller tributaries are also utilized. Spawn-
ing in smaller tributaries usually does not begin
until late September with the peak occurring in
mid-October. The selection of larger tributaries
such as the Salmon River for spawning is charac-
teristic of chinook salmon in their native range
(Stein et al. 1972; Scott and Grossman 1973). Coho
salmon run somewhat later than chinook salmon,
usually beginning in late September and peaking
in late October to early November. Limited coho
salmon spasming activity occurs in the Salmon
River, possibly because of the large size of the
substrate materials. Adult steelhead are present
in the Salmon River throughout the fall and into
early summer. Steelhead can be found in the
smaller tributaries from March through June
with most spawning activity occurring in April
and May. Stream residence time for juvenile salm-
onids in the Salmon River system is <1 yr for
chinook salmon, up to 1 yr for coho salmon, and up
to 2 yr for steelhead (Johnson 1978).

Prior to 1977 the reproductive success of Pacific
salmonids was unknown in New York tributaries
of Lake Ontario. In 1977, five streams in the Salm-
on River system were examined for evidence of
successful spawning of coho salmon, chinook
salmon, and steelhead (Johnson 1978). Initial evi-
dence indicated substantial reproduction of coho
salmon and steelhead in some of the streams. The
purpose of this study was to quantify reproductive
success of Pacific salmonids in one tributary of the
Salmon River.

Methods

Orwell Brook was selected as it contained high
densities of coho and chinook salmon and
steelhead juveniles. Orwell Brook flows for ap-

■^ Avery, E. L. 1974. Reproduction and recruitment of anad-
romous salmonids in Wisconsin tributaries of Lake
Michigan. Dingell-Johnson final Rep., Proj. F-33-R, Study 108,
Wis. Dep. Nat. Resour., 32 p.

*T. Jolliff, Associate Aquatic Biologist, Bureau of Fisheries,
New York State Department of Environmental Conservation,
Cape Vincent, NY 13618, pers. commun.

550

proximately 14.5 km before entering the Salmon
River, 17 km from Lake Ontario (Figure 1). About
6(y7c of Orwell Brook is considered adequate for
successful salmonid reproduction with suitable
substrate generally consisting of gravel ( 1-2 cm in
diameter) and pebbles (3-6 cm in diameter). The
maximum summer water temperature recorded
during 1977 and 1978 was 21° C. Mean monthly
stream discharge from June to October 1978 was
0.26 m^/s. Salmonids, cyprinids, and catostomids,
in order of abundance are the principal compo-
nents of the Orwell Brook fish fauna.

A single 100 m station was established on Or-
well Brook 3 km above the Salmon River. This
section was generally characteristic of the lower
portion of Orwell Brook. Sections of the stream
were visually examined weekly from early May to
mid-June in 1978 in order to estimate the approx-
imate time of peak emergence of salmon fry. Peak

emergence, as used in this study, occurred when
the densities of coho and chinook salmon and
steelhead were highest in Orwell Brook. Collec-
tions of juvenile salmonids were made monthly
from May to October with a 3 m minnow seine.
Supplemental observations on salmon emergence
were also made in May 1979. Monthly population
estimates derived using the Chapman mark-
recapture index (Ricker 1975) and average
monthly weights of juvenile salmonids were plot-
ted with the area beneath the curve providing an
estimate of total production (Chapman 1968). A
logarithmic plot assuming an exponential decline
in monthly densities was used to determine the
population size at peak emergence for coho and
chinook salmon. This method, based on the as-
sumption that natural mortality is greatest just
after emergence and then gradually diminishes,
has previously been employed to estimate the

Figure l . — The study area near the south-
eastern shore of Lake Ontario in central
New York.

551

population size at peak emergence in salmonid
populations (Hunt 1966; O'Connor and Power
1976). Total production of each species was divided
by the smallest stream area within the 100 m
section that was recorded during the study in
order to give an estimate of production per unit
area.

Results and Discussion

Recently emerged coho and chinook salmon
were first observed in Orwell Brook in 1978 on
May 13. In 1979, coho salmon were first observed
on May 9th and chinook salmon on May 10. Peak
emergence of both species occurred during early
June 1978. Steelhead began emerging during
mid-June and peaked in early to mid-July.

Population estimates were initiated in mid-
June about 2 wk after peak salmon emergence. At
this time both salmon species were abundant in
the main stream and steelhead had started to
emerge. Estimates of population size at peak
emergence were 718 coho salmon and 189 chinook
salmon fry/lOO m in the section (Table 1). Densi-
ties of fry (number per square meter) at this time
were 1.30 and 0.34 for coho and chinook salmon
(Table 1). The initial estimate of steelhead in June
was 103 fry/lOO m or 0.20 fry/m^ of stream bottom.
However, the highest densities of steelhead fry
were not recorded until August (Table 1).

Total production of subyearling coho salmon
from 1 June to 30 October 1978 was 1,248 g. This
was substantially greater than production of
chinook salmon, 282 g and steelhead, 404 g (17
June-10 October) (Figure 2). Production per
square meter was 2.7, 0.6, and 0.9 g for coho and
chinook salmon and steelhead. Combined total
production of the three species was 4.2 g/m"' for the
period of study.

Production of subyearling coho salmon in Or-
well Brook during 1978 was intermediate between

Table l. — Estimated monthly numbers (with 95% confidence
limits) and densities (number per square meter) of subyearling
coho salmon, chinook salmon, and steelhead in 100 m study area
of Orwell Brook, Oswego County, N.Y., during 1978.

Streann
area (m^)

Coho salmon
Number Density

Chinook salmon

Steelhead

Date

Number Density

Number Density

1 June

553

'718

1.30

M89 0.34

— —

17 June

521

500±101

1.04

139 ±43 .27

103±41 0.20

16 July

483

428 = 184

.89

121 ±50 .25

212±72 44

12 Aug.

469

118±64

.25

51 ±29 .11

262 ±84 ,56

10 Sept.

476

104 ±62

.22

36±25 .08

199 ±58 .42

10 Oct.

495

68 ±23

.14

31 ±16 .06

138±34 .28

800 ■

COHO

^

700 .

\

1 June

bOO ■

\

UJ

Q-
>•
u.

500 .
■400 .

17

June \.

\ 16 July

C

300 '

\

o
z

2 00 «

\

100 ,

12 Aug. ^...,..,,^^^10 Sept.

^\ 10 Oct

1

2 3 4 5 6
MEAN WEIGHT (g)

o
c

ad

UJ

o.

C

z

o
o

LU

c

>-

O

d

250 1

200

150

TOO

50

300
250
200
150
100
50 4

CHINOOK

10 Sept.

10 Oct.

1 2 3

MEAN WEIGHT (R)

STEELHEAD

17 June

'Logarithmic extrapolation.

0.5 1,0 1.5 2.0 2.5

MEAN WEIGHT (g)

Figure 2. — Production curves of subyearling coho and chinook
salmon in Orwell Brook, Oswego County, N.Y., 1 June-10 October
1978, and steelhead 17 June-10 October 1978.

552

that observed in Oregon, 5.6 g/m^ (Chapman 1965)
and Michigan, 0-1.9 g/m^ (Stauffer^) during a
similar time interval. Production of coho salmon
in the 100 m section of Orwell Brook from 1 June to
15 October 1977 was 5.9 g/m^ (Johnson 1978). Al-
though the 1978 production estimate for coho
salmon represents a 549c decrease from 1977, the
variation in production between years is within
the range reported by Chapman (1965) for coho
salmon in Oregon coastal streams.

No information on chinook salmon production is
available for the Great Lakes region; however,
production of chinook salmon in Orwell Brook was
intermediate to that recorded in the Lemhi River
and Big Springs Creek, Idaho (Goodnight and
Bjornn 1971). Production of steelhead is less
than recorded in Michigan (Hannuksela^°) and
intermediate between the two Idaho streams
(Goodnight and Bjornn 1971).

From emergence in May until the termination
of sampling in November, subyearling coho salmon
were larger than either subyearling chinook
salmon or steelhead (Table 2). However, since
chinook salmon characteristically leave their
natal streams earlier than coho salmon, larger
chinook salmon smolts may be migrating early.
The growth rate (total length in millimeters per
day) of coho and chinook salmon and steelhead
was greatest during the first 2 mo following
emergence (Table 2). Growth during this 2 mo
period was 0.44, 0.47, and 0.39 mm/d for coho and
chinook salmon and steelhead (Table 2). High ini-
tial growth rates of subyearling coho salmon and
steelhead have previously been reported by
Chapman (1965) and Stauffer (footnote 9). For the
entire period (175 d for salmon, 145 d for
steelhead) the growth rates of chinook salmon and
steelhead were identical, 0.27 mm/d, with coho
salmon being only slightly slower, 0.26 mm/d. In
Michigan, growth rates of subyearling coho salm-
on and steelhead from June to November were
0.29 and 0.26 mm/d (Stauffer footnote 9). However,
although these estimates are similar to those ob-

TabLE 2. — Number examined, mean total length (millimeters)
(with 95% confidence limits), and daily growth increments
(mm/d) of subyearling coho salmon, chinook salmon, and
steelhead from Orwell Brook, May-November 1978.

Coho salmon

Chinook salmon

Steelhead

^Stauffer, T. M. 1975. Population characteristics and
summer-to-autumn survival of juvenile rainbow trout and coho
salmon in two Lake Superior tributaries, 1969-1972. Mich.
Dep. Nat. Resour, Fish. Res. Rep. 1825, 21 p. Institute for
Fisheries Research, Museums Annex Building, Ann Arbor, MI
48109.

'"Hannuksela, P R. 1973. Food interrelationships of the
mottled sculpin, Cottus bairdi, and juveniles of the rainbow
trout, Salmo gairdneri, in a tributary of Lake Superior. Mich.
Dep. Nat. Resour., Fish. Res. Rep. 1801, 21 p. Institute for Fish-
eries Research, Museums Annex Building, Ann Arbor, MI
48109.

Date No. TL mm/d No. TL mm/d No. TL mm/d

18 May 10 45.1 ±4.4 10 36.7±3.9

0.65 0.34

17June 20 63.6-5.7 20 46.7-1.9 10 297±1.8

0.26 0.61 0.52

16 July 40 711 ±2.8 40 64.5±20 30 44.9±1.6

0.13 0.06 0.24

12Aug. 30 74.7±2.5 20 66.0±3.0 25 51.5±1.7

0.27 0.11 0.19

lOSept. 20 82.4±4.9 20 69.2±3.0 30 570±3.2

0.05 0.22 0.16

lOOct. 20 83.9±49 10 75.7±3.4 25 61.7±3.8

022 0.28 0.26

9 Nov. 10 90.4±5.2 10 84.0±4.3 10 69.5±4.1

tained in Orwell Brook, both coho salmon and
steelhead are initially larger in June in Orwell
Brook and this size differential (especially for coho
salmon) is retained throughout the fall. There is
no available information on chinook salmon
growth in the Great Lakes region; however,
growth in New York is slower than reported in
Washington (Becker 1973).

Acknowledgments

I wish to thank E. M. Zebisch for assistance in
the field and J. D. Sheppard and E. W. Radle for
reviewing preliminary drafts of the manuscript.
The comments and suggestions of two anonymous
reviewers substantially contributed to the content
of the final manuscript.

Literature Cited

ALEXANDER, D. R., AND H. R. MACCRIMMON.

1974. Production and movement of juvenile rainbow trout
(Salmo gairdneri) in a headwater of Bothwell's Creek,
Georgian Bay, Canada. J. Fish. Res. Board Can.
31:117-121.

Becker, C. D.

1973. Food and growth parameters of juvenile chinook

salmon, Oncorhynchus tshawytscha, in central Columbia

River. Fish. Bull., 'U.S. 71:387-400.
Berst, a. H., and G. R. SPANGLER.

1973. Lake Huron: The ecology of the fish community and

man's effects on it. Great Lakes Fish. Comm. Tech. Rep.

21, 41 p.

Chapman, D. W.

1965. Net production of juvenile coho salmon in three Ore-
gon streams. Trans. Am. Fish. Soc. 94:40-52.

1968. Production. In W. E. Ricker (editor). Methods for
assessment offish production in fresh waters, p. 182-196.
Blackwell Sci. Publ., Oxf., Engl.
Christie, W. J.

1973. A review of the changes in the fish species composi-

553

tion of Lake Ontario. Great Lakes Fish. Comm. Tech.
Rep. 23, 65 p.

Goodnight, w. h., and T. C. Bjornn.

1971. Fish production in two Idaho streams. Trans. Am.
Fish. Soc. 100:769-780.
Hassinger, R. L., J. G. Hale, and D. E. Woods.

1974. Steelhead of the Minnesota north shore. Minn.

Dap. Nat. Resour, Tech. Bull. 11, 38 p.
HUNT, R. L.

1966. Production and angler harvest of wild brook trout in

Lawrence Creek, Wisconsin. Wis. Conserv. Dep. Tech.

Bull. 35, 52 p.

JOHNSON, J. H.

1978. Natural reproduction and juvenile ecology of Pacific
salmon and steelhead trout in tributaries of the Salmon
River, New York. M.S. Thesis, State Univ New York,
Syracuse, 133 p.

O'CONNER, J. F, AND G. POWER.

1976. Production by brook trout iSalvelinus fontinalis) in
four streams in the Matamek watershed, Quebec. J.
Fish. Res. Board Can. 33:6-18.

Parsons, J. W.

1973. History of salmon in the Great Lakes, 1850-
1950. U.S. Bur Sport Fish. Wildl. Tech. Pap. 68, 80 p.

RICKER, W. E.

1975. Computation and interpretation of biological statis-
tics offish populations. Fish. Res. Board Can., Bull. 191,
382 p.

Scott, W. B., and E. J. Grossman.

1973. Freshwater fishes of Canada. Fish. Res. Board
Can., Bull. 184, 966 p.

Smith, S. H.

1968. Species succession and fishery exploitation in the
Great Lakes. J. Fish. Res. Board Can. 25:667-693.

Stein, R. a., R E. Reimers, and J. D. Hall.

1972. Social interaction between juvenile coho (Oncorhyn-
chus kisutch) and fall chinook salmon (O. tshawytscha) in
Sixes River, Oregon. J. Fish. Res. Board Can. 29:1737-
1748.

Wells, L., and A. L. McLain.

1973. Lake Michigan: Man's effects on native fish stocks
and other biota. Great Lakes Fish. Comm. Tech. Rep. 20,
55 p.

James H. Johnson

New York State Department of Environmental Conservation
50 Wolf Road
Albany, NY 12233

554

ERRATA

Fishery Bulletin, Vol. 77, No. 4

Caillouet, Charles W., Frank J. Patella, and William B. Jackson, "Trends toward decreasing size of brown
shrimp, Penaeus aztecus, and white shrimp, Penaeus setiferus, in reported annual catches from Texas and
Louisiana," p. 985-989.

1) Page 987, left colum, last line, correct line to read:
InF, = ln(a) + bC, + e

2) Page 989, Table 3, first line, under Brown shrimp, Texas coast, 1961-1976, correct line to read:
0.00141* (adding asterisk)

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Contents-continued

O'CONNELL, CHARLES P. Percentage of starving northern anchovy, Engraulis
mordax, larvae in the sea as estimated by histological methods 475

EBEL, WESLEY J. Transportation of chinook salmon, Oncorhynchus tshawytscha,
and stee\\ieaid,Salmo gairdneri, smolts in the Columbia River and effects on adult
returns 491

BENIRSCHKE, K., MARY L. JOHNSON, and ROLF J. BENIRSCHKE. Is ovula-
tion in dolphins, Stenella longirostris and Stenella attenuata, always copulation-
induced? 507

Notes

PEARCY, WILLIAM G. A large, opening-closing midwater trawl for sampling
oceanic nekton, and comparison of catches with an Isaacs-Kidd midwater trawl . . 529

COE, JAMES M., and WARREN E. STUNTZ. Passive behavior by the spotted
dolphin, Stenella attenuata, in tuna purse seine nets 535

KRAEUTER, JOHN N., and MICHAEL CASTAGNA. Effects of large predators on
the field culture of the hard clam, Mercenaria mercenaria 538

PARKER, KEITH. A direct method for estimating northern anchovy, Engraulis
mordax, spawning biomass 541

PITCHER, KENNETH W Food of the harbor seal, Phoca uitulina richardsi, in the
Gulf of Alaska 544

JOHNSON, JAMES H. Production and growth of subyearling coho salmon, On-
corhynchus kisutch, chinook salmon, Oncorhynchus tshawytscha, and steelhead,
Salmo gairdneri, in Orwell Brook, tributary of Salmon River, New York 549

* GPO 696-404

..^T '%

Fishery Bulletin

'^'-^TESO^^

Marine BiolCvOical Laboratory j
\lBZb 1981

Woods Mole, Mass.

Vol. 78, No. 3

July 1980

HANKIN, DAVID G. A multistage recruitment process in laboratory fish popula-
tions: implications for models offish population dynamics 555

CHENG, LANNA, and ERIC SHULENBERGER. Distribution and abundance of
Halobates species (Insecta: Heteroptera) in the eastern tropical Pacific 579

SHANE, SUSAN H. Occurrence, movements, and distribution of bottlenose dol-
phin, Tursiops truncatus, in southern Texas 593

LAROCHE, JOANNE LYCZKOWSKI, and SALLY L. RICHARDSON. Reproduc-
tion of northern anchovy, Engraulis mordax, off Oregon and Washington 603

CLARKE, THOMAS A. Diets of fourteen species of vertically migrating meso-
pelagic fishes in Hawaiian waters 619

RICE, STANLEY D., and JACK E. BAILEY Survival, size, and emergence of pink
salmon, Oncorhynchus gorbuscha, alevins after short- and long-term exposures to
ammonia 641

BAILEY, JACK E., STANLEY D. RICE, JEROME J. PELLA, and SIDNEY G.
TAYLOR. Effects of seeding density of pink salmon, Oncorhynchus gorbuscha,
eggs on water chemistry, fry characteristics, and fry survival in gravel incubators 649

LENARZ, WILLIAM H., and PETER B. ADAMS. Some statistical considerations of
the design of trawl surveys for rockfish (Scorpaenidae) 659

RICE, D. W, JR., F. L. HARRISON, and A. JEARLD, JR. Effects of copper on early
life history stages of northern anchovy, Engraulis mordax 675

THEILACKER, GAIL H. Changes in body measurements of larval northern an-
chovy, Engraulis mordax, and other fishes due to handling and preservation 685

MORGAN, STEVEN G. Aspects of larval ecology of Squilla empusa (Crustacea,
Stomatopoda) in Chesapeake Bay 693

POWELL, ALLYN B., and HERBERT R. GORDY Egg and larval development of the
spot, Leiostomus xanthurus (Sciaenidae) 701

CRESSEY, ROGER, and HILLARY BOYLE CRESSEY. Bomolochid copepods
parasitic on the eyes of Indo-West Pacific clupeid fishes 715

HOWELL, W HUNTING. Temperature effects on growth and yolk utilization in
yellowtail flounder, Limanda ferruginea, yolk-sac larvae 731

BISHOI^ JAMES M., JAMES G. GOSSELINK, and JAMES H. STONE. Oxygen
consumption and hemolymph osmolality of brov^n shrimp, Penaeus aztecus 741

HORN, MICHAEL H. Diel and seasonal variation in abundance and diversity of
shallow-water fish populations in Morrow Bay, California 759

(Continued on back cover)

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U.S. DEPARTMENT OF COMMERCE

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NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION

Richard A. Frank, Administrator

Terry L. Leitzell, Assistant Administrator for Fisheries

NATIONAL MARINE FISHERIES SERVICE

Fishery Bulletin

The Fishery Bulletin carries original research reports and technical notes on investigations in fishery science, engfineering, and
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Dr. Jay C. Quast

Scientific Editor, Fishery Bulletin

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Auke Bay Laboratory

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P.O. Box 155, Auke Bay, AK 99821

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National Marine Fisheries Service National Marine Fisheries Service

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Dr. Edward D. Houde Dr. Jerome J. Pella

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Management and Budget through 31 March 1982.

Fishery Bulletin

CONTENTS

Vol. 78, No. 3 July 1980

HANKIN, DAVID G. A multistage recruitment process in laboratory fish popula-
tions: implications for models offish population dynamics 555

CHENG, LANNA, and ERIC SHULENBERGER. Distribution and abundance of
Halobates species (Insecta: Heteroptera) in the eastern tropical Pacific 579

SHANE, SUSAN H. Occurrence, movements, and distribution of bottlenose dol-
phin, Tursiops truncatus, in southern Texas 593

LAROCHE, JOANNE LYCZKOWSKI, and SALLY L. RICHARDSON. Reproduc-
tion of northern anchovy, Engraulis mordax, off Oregon and Washington 603

CLARKE, THOMAS A. Diets of fourteen species of vertically migrating meso-
pelagic fishes in Hawaiian waters 619

RICE, STANLEY D., and JACK E. BAILEY Survival, size, and emergence of pink
salmon, Oncorhynchus gorbuscha, alevins after short- and long-term exposures to
ammonia 641

BAILEY, JACK E., STANLEY D. RICE, JEROME J. PELL A, and SIDNEY G.
TAYLOR. Effects of seeding density of pink salmon, Oncorhynchus gorbuscha,
eggs on water chemistry, fry characteristics, and fry survival in gravel incubators 649

LENARZ, WILLIAM H., and PETER B. ADAMS. Some statistical considerations of
the design of trawl surveys for rockfish (Scorpaenidae) 659

RICE, D. W, JR., R L. HARRISON, and A. JEARLD, JR. Effects of copper on early
life history stages of northern anchovy, Engraulis mordax 675

THEILACKER, GAIL H. Changes in body measurements of larval northern an-
chovy, Engraulis mordax, and other fishes due to handling and preservation 685

MORGAN, STEVEN G. Aspects of larval ecology of Squilla empusa (Crustacea,
Stomatopoda) in Chesapeake Bay 693

POWELL, ALLYNB., and HERBERT R. GORDY Egg and larval development of the
spot, Leiostomus xanthurus (Sciaenidae) 701

CRESSEY, ROGER, and HILLARY BOYLE CRESSEY Bomolochid copepods
parasitic on the eyes of Indo-West Pacific clupeid fishes 715

HOWELL, W HUNTING. Temperature effects on growth and yolk utilization in
yellowtail flounder, Limanda ferruginea, yolk-sac larvae 731

BISHOP JAMES M., JAMES G. GOSSELINK, and JAMES H. STONE. Oxygen
consumption and hemol3anph osmolality of browTi shrimp, Penaeus aztecus 741

HORN, MICHAEL H. Diel and seasonal variation in abundance and diversity of
shallow-water fish populations in Morrow Bay, California 759

(Continued on next page)

Seattle, Washington
1980

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Contents-continued

FOGARTY, MICHAEL J., DAVID V D. BORDEN, and HOWARD J. RUSSELL.

Movements of tagged American lobster, Homarus americanus, off Rhode Island . . . 771
RENSEL, JOHN E., and EARL E PRENTICE. Factors controlling growth and survi-
val of cultured spot prawn, Pandalus platyceros , in Puget Sound, Washington 781

Notes

THEILACKER, GAIL H. Rearing container size affects morphology and nutritional
condition of larval jack mackerel, Trachurus symmetricus 789

CARNEY, ROBERT S., and ANDREW G. CAREY JR. Effectiveness of metering
wheels for measurement of area sampled by beam trawls 791

PITCHER, KENNETH W Stomach contents and feces as indicators of harbor seal,
Phoca uitulina, foods in the Gulf of Alaska 797

CHRISTENSEN, DARRYL J., and WALTER J. CLIFFORD. The 1978 spring recre-
ational catch of Atlantic mackerel, Scomber scombrus, off the Middle Atlantic region 799

BEARDSLEY, GRANT L. Size and possible origin of sailfish, Istiophorus platypterus,
from the eastern Atlantic Ocean 805

RICE, STANLEY D., and JACK E. BAILEY Ammonia concentrations in pink

salmon, Oncorhynchus gorbuscha, redds of Sashin Creek, southeastern Alaska . . . 809

HUNTER, JOHN R., and CAROL A. KIMBRELL. Egg cannibalism in the northern
anchovy, Engraulis mordax 811

QUINN, THOMAS P, BRUCE S. MILLER, and R. CRAIG WINGERT Depth dis-
tribution and seasonal and diel movements of ratfish, Hydrolagus colliei, in Puget
Sound, Washington 816

PEARSON, WALTER H., PETER C. SUGARMAN, DANA L. WOODRUFF, J. W
BLAYLOCK, and BORI L. OLLA. Detection of petroleum hydrocarbons by the
Dungeness crab, Cancer magister 821

Notices
NOAA Technical Reports NMFS published during the first 6 months of 1980 827

Vol. 78, No. 2 was published on 17 November 1980.

The National Marine Fisheries Service (NMFS) does not approve, rec-
ommend or endorse 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 pro-
motion which would indicate or imply that NMFS approves, recommends
or endorses any proprietary product or proprietary material mentioned
herein, or which has as its purpose an intent to cause directly or indirectly
the advertised product to be used or purchased because of this NMFS
publication.

A MULTISTAGE RECRUITMENT PROCESS IN

LABORATORY FISH POPULATIONS: IMPLICATIONS FOR

MODELS OF FISH POPULATION DYNAMICS'

David G. Hankin^

ABSTRACT

Laboratory studies have been previously used to examine fundamental aspects of fish population
dynamics and may be explicitly structured to examine the stock-recruitment relation. Previous studies
have shown that cycling of population numbers occurs in refuge-free environments, but provision of
refuge areas allows maintenance of stable population numbers. Results of these studies may be
adequately explained by simple stock-recruitment theory.

Laboratory experiments described here show that manipulation of refuge habitat quality can
profoundly influence interactions among population components. Complex interactions among fry,
juveniles, and adults created erratic pulses in numerical population growth. Numerical population
dynamics could not be adequately explained by simple stock-recruitment theory.

Based on experimental observations, a multistage adult-juvenile stock-recruitment relation was
developed and was found, through statistical analyses, to adequately describe observed numerical
dynamics. The biological plausibility of complex multistage recruitment processes argues that
expectations for empirical support of simple stock-recruitment theory may be unreasonable and
inappropriate. The simple theory may often not be biologically appropriate and more complex models of
numerical population dynamics may be required for biological realism and for meaningful data
analysis. Whether collection of data necessary to allow use of such complex recruitment models is
economically feasible and, if so, whether more complex models may prove of practical use for
management of fish populations is at present unclear.

One poorly understood population process is the
so-called stock-recruitment relation (Ricker 1954)
describing the dependency of input of new indi-
viduals, Rf, on the density of adult parents some
time previous, St-T- Although the theoretical
basis of the stock-recruitment relation is well
established ( Ricker 1954; Beverton and Holt 1957)
and recent study in theoretical ecology (May 1975;
Oster 1975) has emphasized the impressive variety
of population behaviors suggested by simple dis-
crete-time models of the form /?; = St-r ■ GiSt-r),
remarkably little empirical support for the theory
exists. In part this reflects severe restrictions in
data collection. In temperate populations, for
example, only one observation of recruitment may
be obtained annually and this observation is
normally related not only to parent stock but also
to fluctuating environmental conditions and mor-
tality (from birth to recruitment) which may

Based on a dissertation submitted in partial fulfillment of
the requirements for the degree of Doctor of Philosophy, Depart-
ment of Natural Resources, Cornell University.

Department of Natural Resources, Cornell University,
Ithaca, N.Y.; present address: Department of Fisheries, Hum-
boldt State University, Areata, CA 95521.

strongly influence the ultimate size of a recruited
year class or cohort. The data collection process
is exceedingly slow, and exogenous factors may
confound the dependency of recruitment on parent
stock.

Further, the theory itself is simplistic. Chief
limitations are the requirements that feedback be
exerted at only one point in time and that the
responsible population component consists solely
of adults. Alternative feedback control mechan-
isms could involve either juveniles or the adult
stock at more than one point in time. For example,
in largemouth bass, Micropterus salmoides, adults
are in contact with developing larvae for only a
short period of time during which adult-related
density-dependent mortality might occur. Adults
leave inshore nesting and nursery areas shortly
after spawning, but yearling bass, produced by the
adult stock a year previous, remain in inshore
areas where they may prey extensively on younger
juveniles (Ricker 1954). In Dungeness crab, Can-
cer magister, and other cannibalistic species, re-
cruitment may depend not only on parent stock
but also on adult densities when juveniles first
enter the adult population and are extremely

Manuscript accepted: February 1980.
FISHERY BULLETIN: VOL. 78, NO. 3, 1980.

555

FISHERY BULLETIN: VOL. 78, NO. 3

vulnerable (Butler 1961; Gotshall 1978). The be-
havior of mathematical models describing such
multiple adult feedback mechanisms, termed
"multistage" recruitment processes, has been re-
cently investigated by McKelvey et al. (in press).
Collection of data suitable for analysis of these
more complex models would seem to pose difficul-
ties far in excess of those required for the simple
models. In such cases experimental laboratory
studies may be more effective and more effi-
cient than "field" investigations for providing
insight into the fundamental problem of stock and
recruitment.

Laboratory studies of stock and recruitment
have many advantages over similar studies of
natural wild populations. Strict environmental
control (of food supply, temperature, dissolved
oxygen, photoperiod, habitat dimension and
type), elimination of sampling error through com-
plete enumeration, and opportunity for unique
behavioral observations in an aquatic environ-
ment are the most obvious. Less obvious but
perhaps more significant advantages include the
investigator's unrestricted manipulative control
over population size and age structure, so that
the chief modes of regulation are likely to be
endogenous population mechanisms, causally den-
sity-dependent, and the opportunity for replica-
tion in quantity.

From the perspective of statistical analysis, the
influence of exogenous, density-independent fac-
tors is reduced, observations may be collected over
as wide a range of population states as desired,
and (through replication) the inherent variability
of the dynamic population processes themselves
may be examined (Royama 1977).

Among fishes the study of laboratory popula-
tions has centered on a single species, the guppy,
Poecilia reticulata. The characteristics of small
size, rapid maturity, frequent and repeated repro-
duction, and a relatively short life span render the
guppy an ideal subject for laboratory study of the
stock-recruitment relation. Basic information has
been gathered regarding reproduction (Felin 1935;
Purser 1938; Turner 1937; Rosenthal 1952). fecun-
dity (Felin 1935; Hester 1964), and growth (von
Bertalanffy 1938), and there have been many,
often long-term, studies of population behavior
(Breder and Coates 1932; Shoemaker 1944; Silli-
man 1948, 1968; Silliman and Outsell 1958; Laak-
so 1959; Warren 1973; Yamagishi 1976). While the
focus of these studies has not been the stock-
recruitment relation per se, it is often possible to

interpret observed population dynamics in part as
a reflection of an overcompensatory function re-
lating numerical population addition to densities
of adult fish.

The guppy is a viviparous member of the family
Poeciliidae and exhibits strong sexual dimorph-
ism. The maximum weight for mature males is
perhaps 0.2-0.4 g as compared with a maximum
weight for females of perhaps 1-2 g. Sexual matu-
rity is normally reached by both males and females
at 12-16 wk at weights of 0.1-0.15 and 0.2-0.3 g.
Average longevity under laboratory conditions
might be 12-18 mo. Young are produced in discrete
broods, ranging in size from 2 or 3 to 50, at roughly
monthly intervals at 25° C. Brood size depends on
female size and, as a result, the appropriate
measure of adult reproductive potential is not the
number of adults but, since fecundity is nearly
proportional to female weight, the total adult
female biomass. Males mate freely and indiscrim-
inantly with available females, and sperm from a
single mating may remain viable and produce
successive broods for periods up to 6 mo (Winge
1937). Females are clearly the overwhelmingly
important component of the adult stock.

At birth fry weigh 7-8 mg and, immediately
after ejection by females, are extremely vulner-
able to predation by adults. Cannibalism has been
regarded as the primary feedback mechanism
controlling population size (Breder and Coates
1932; Laakso 1959). Recent experiments have
suggested that cannibalism is chiefly a function of
contacts between individuals rather than of re-
sponses to limitations in food supply (Silliman
1968; Warren 1973).

Laboratory environments for guppy population
study have differed significantly in two respects:
food supply and provision of refuge areas. Food has
been delivered at either fixed and limiting or
"to excess" ration levels, and refuge areas have
only rarely been provided. These studies have
shown that total population biomass is strongly
influenced by food supply (Silliman 1968), but
numerical densities and dynamics are strongly
affected by refuge area provision and only slightly
influenced by food supply.

Cycles of abundance have been observed in all
long-term studies where refuge areas have been
absent (Breder and Coates 1932; Shoemaker 1944;
Laakso 1959). Characteristics of abundance cycles
(begun with small numbers of adults) include
initial increases in numbers, reduction of such
increases to near zero as adult predator density

556

HANKIN: A MULTISTAGE RECRUITMENT PROCESS

becomes large, shift to an adult-dominated age
structure, and reappearance of young individuals
when adult density declines through mortality to
levels at which fry survival once more occurs. In
those few instances in which refuge habitats have
been provided (Silliman 1948, 1968; Silliman and
Outsell 1958), the results have demonstrated that
roughly stable populations, of greater numerical
size, with finely graded age (or size) structure,
may be maintained for apparently indefinite peri-
ods. Presumably, the stability of these popula-
tions reflects the decreased period of time during
which fry are vulnerable to cannibalism.

In previous guppy population studies the weight
of the mature female stock has not been recorded
and hence it is impossible to attempt an adequate
quantitative examination of stock-recruitment
relations which may have been responsible for
observed dynamics (e.g., Gulland 1962 based on
previous studies). The experiments described on
the following pages were specifically designed
to allow quantitative assessment of the stock-
recruitment relation. Refuge areas were provided
and fry successfully entering these areas were
considered as rough equals of recruited fish.
Although females do not release broods synchro-
nously (broods are delivered continuously with
respect to the entire population), data were col-
lected at discrete biweekly intervals. Net numeri-
cal change in a sampling interval could thus be
related to adult reproductive potential and adult
predator density at the beginning of an interval in
a fashion analogous to that which might be
attempted in analysis of the simple discrete-time
models. A simple difference in refuge design (as
compared with Silliman's earlier work) involving
spacing between glass rods in a refuge fence,
however, created unexpected patterns of numeri-
cal increase. These patterns were not anticipated
and could not be explained on the basis of simple
stock-recruitment theory. Analysis ultimately
showed the presence of a complex mechanism
involving both adult and immature population
components, an adult-juvenile stock-recruitment
relation.

METHODS AND MATERIALS

Experiments were performed in a 3 m x 3.7 m
room insulated on three walls, including two out-
side walls, from floor to ceiling. A small electric
floor heater maintained room temperature at
approximately 22° C, about 3° C above ambient

winter temperature supplied by a propane heating
unit in an adjoining room. An air-conditioner in
the same adjoining room prevented summer tem-
peratures from exceeding 26° C. Experimental
aquaria were located along the three insulated
walls.

Experimental Environments

Twelve aquaria, of dimensions 31 cm x 62 cm x
41 cm, each holding about 80 1 of water, served as
experimental units. Each aquarium was equipped
with a 75 W thermostat-controlled aquarium
heater, about 1 cm deep layer of 3-5 mm gravel, a
large inside-type charcoal -glass wool filter, a full
hood reflector with two 15 W showcase bulbs, a
thermometer, and a refuge area (Figure 1). Refuge
areas were enclosed by a fence consisting of two
sheets of solid glass rods, 3 mm in diameter,
spaced (initially) 5 mm apart on centers, fitted in
Plexiglas^ frames glued at right angles. The

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

-heater

41

cm

crn inside
filter

Figure l. — Schematic of the experimental environments for
guppies and southern platyfish.

557

FISHERY BULLETIN: VOL. 78. NO. 3

fences partitioned off corners of aquaria, roughly
15 cm X 15 cm of aquaria bottoms, extended from
aquaria bottoms to aquaria frames above the
water level, and reserved about one-eighth of the
total volume as refuge and nursery areas for fry. A
2 cm high Plexiglas frame surrounded both sides
of a refuge fence base, preventing gravel from
interfering with fence manipulation and allowing
easy removal and replacement of the fence at
population enumerations.

Light was provided for 12 h per day and was
regulated by electric timers. To ensure standard-
ized lighting conditions in all aquaria, the two 62
cm sides of an aquarium were covered with opaque
polyethylene sheeting; of the two remaining sides,
one abutted the wall and the other was left clear
for observations of population behavior. Tempera-
tures were maintained at approximately 25.5° C
with a maximum recorded range in all aquaria
over a 58-wk period of roughly 24°-28° C. Tem-
peratures were monitored and recorded every
2 d. Air for filter units was supplied by small
air pumps.

At weekly intervals filter units were cleaned,
charcoal and glass wool replaced, and about 16 1 of
aquarium water and detritus were siphoned from
each aquarium bottom and replaced with aged
aerated water. A diatomaceous earth power filter
was used weekly for 60-90 min periods per aquar-
ium and helped maintain water quality.

Routine Experimental Manipulations

Feeding

Populations were fed accurately weighed
amounts of food twice daily. Morning feedings
consisted of dried food only (Tetramin brand
Conditioning Food). Evening feedings consisted
of thawed, rinsed, and drained adult brine shrimp,
Artemia salina, and newly hatched Artemia
nauplii. Nauplii were suspended in freshwater
and pipetted directly into the refuge areas while
dried food and adult brine shrimp were delivered
to the main aquarium volume outside the refuge
area.

Since no technical assistance was available to
daily siphon uneaten food from aquaria, it was not
possible to maintain a steady fixed ration level
throughout the experimental period. Instead, ra-
tions of dried food and of adult brine shrimp were
increased in increment steps as populations grew,
maintaining a relatively constant ratio of food

supply to population biomass during initial stages
of population growth. Food supply became fixed u
when populations had achieved about SO'^ of the '
apparent maximum biomass supported at the
final fixed ration level. The increment steps pre-
vented deterioration of water quality through
decomposition of uneaten food and allowed for
subsequent analysis of changes in population
biomass as related to food supply. Exact ration
levels and corresponding dates appear in the
section on experimental design.

Marking

At triweekly intervals a fluorochrome, DCAF
(2,4 bis (N,N' di/carboxymethyl/aminomethyl)
fluorescein), was incorporated into the adult
brine shrimp ration component. The DCAF-laden
shrimp was fed twice daily for 3-d periods at ration
levels corresponding to the normal adult brine
shrimp feeding for the period. Dried food was not
fed during marking intervals. Marking trials had
indicated that circular fluorescent rings corre-
sponding to time of injestion of DCAF were
produced on the growing margin of guppy scales.
Repeated marks could be produced by repeated
administration at intervals exceeding 1 wk. Mark-
ing was designed to allow assessment of age
structure at conclusion of the experiments from
analysis of fluorescent marks on scales removed
from fish. Scales were removed from samples of
fish from all populations at week 36 and at week
58. Details of marking procedures may be found in
Hankin (1978a).

Data Collection

At biweekly intervals complete enumeration of
populations was performed. In early weeks (0-14)
enumeration was staggered by 1 wk so that four
populations and eight populations were enumer-
ated on alternate weekends. In later weeks ( 14-58)
all populations were enumerated in a 2-d interval
at biweekly intervals.

All fish were removed from individual aquaria
during enumerations and separated by size cate-
gories. Glass rod-Plexiglas grading devices, simi-
lar in design to refuge fences, were used to
separate fish on the basis of "diameter" (or more
correctly, maximum breadth). During weeks 0-36
six size categories were monitored, and two addi-
tional categories were included during weeks
36-58. A description of the size structure classifi-

558

HANKIN: A MULTISTAGE RECRUITMENT PROCESS

cation achieved by the grading process and size
category designations are contained in Table 1.
These size category designations will be adopted
throughout the paper for brevity.

After separation into size categories, numbers
of males and females in each size category were
recorded, and weights of males and females in size
categories Ag, A7, Ag (weeks 0-36) and A55, Ag,
A7, Ag (weeks 36-58) were obtained separately.
Weights of fry were not obtained due to dangers of
handling mortality. Weights of remaining size
categories were obtained without separation by
sex as these groups contained nearly all immature
fish. To determine weights, fish were placed in a
small nylon net, blotted on paper towels until no
further moisture was observed (about 1 min), and
then transferred to a previously weighed plastic
beaker containing about 40 ml of water. Weights
of fish were determined as the difference between
the previous weight and the weight obtained after
addition of fish. Total population biomass was
determined as the sum of all weight measure-
ments for a given population but did not include
weight of fry. An Ainsworth Model ION analytical
balance, accurate to three decimal places, was
used for all weighings. Handling mortality was
negligible. In 58 wk only five mortalities, all fish
<2 mm in "diameter," were recorded as a direct
result of biweekly manipulations at enumeration.
Approximately 38,000 fish were handled during
these enumerations.

All fish were also examined for external symp-
toms of disease at biweekly enumerations. Disease
diagnosis and/or confirmation was performed at

Table 1. — Size-group classifications of guppies at enumerations
during weeks 0-36 ( Phase I) and weeks 36-58 ( Phase II). Grader
spacing is measured from center to center.

Grader

Fish

Size-group

spacing

diameter

Weeks

designation

(mm)

range (mm)

Description

0-36

Fry

4

<1

Newly born fry

J.

4

1-2

All immature

Js

5

2-3

Immature males and females,
mature males

Ae

6

3-4

Largest mature males, small
mature females

A,

7

4-5

Large mature females

As

8

>5

Largest mature females

36-58

Fry

4

<1

Newly born fry

J40

4

1-1.5

All immature

J. 5

4.5

1.5-2

All immature

J5.0

5.0

2-25

Immature females, maturing
males

A5.5

5.5

2.5-3

Maturing females, mature
males

As

6

3-4

Largest mature males, small
mature females

A7

7

4-5

Large mature females

As

8

>5

Largest mature females

irregular intervals by Louis Leibovitz, Cornell
University Veterinary School. Fish with obvious
external disease symptoms (consistently diag-
nosed as chronic piscine tuberculosis) but other-
wise apparently healthy were treated by a 20-min
bath in Formalin (1:4,000). Severely afflicted fish
near death were removed from populations and
counted as mortalities. Numbers, weights, and
sexes of fish showing symptoms and/or treated
were recorded for each population at enumeration.
Aquaria were examined daily for mortalities.
Date of death, size category estimate, and sex were
recorded for each observed mortality.

At termination (week 58) a sample of 41 gravid
females ranging from 21 to 39 mm was selected
from the populations. Each female was dissected
and the number of embryos counted. Data col-
lected was used to establish an overall relation
between fecundity and female size for the experi-
mental populations.

Experimental Design

The initial intent of population experiments
was to examine dynamics of mixed species popula-
tions (guppies, P. reticulata, and southern platy-
fish, "platy," Xiphophorous maculatus) from the
perspective of stock-recruitment theory. Due to
excessive mortality among the southern platyfish
and an apparent inability of their fry to success-
fully compete with guppy fry, the southern platy-
fish were removed from all populations at week 8
and experimental goals became limited to analy-
sis of single species populations based on simple
stock-recruitment theory. Numerical population
growth of single species populations, however,
was not anticipated on the basis of the sim-
ple theory. Numerical population growth often
occurred as a series of discrete pulses of increase,
followed by periods of roughly static population
numbers. Behavioral observations and analyses of
collected population data through week 36 indi-
cated that the pulsing quality of numerical growth
was probably caused by juvenile-fry interactions
within refuge areas. Based on this hypothesis,
experimental populations were manipulated and
exposed to different treatments at week 36. Treat-
ment consisted of alteration of original refuge
area habitat quality and population growth under
these new conditions was monitored through week
58 to test the juvenile-fry interaction hypothesis.

The experiments have been separated into two
distinct phases based on the above-described ex-

559

perimental path. Weeks 0-36, which included
original mixed species populations and subse-
quent unexpected behavior of single species pop-
ulations, may be regarded as exploratory in nature
and have been designated Phase I. The test of the
juvenile-fry interaction hypothesis, during weeks
36-58, may be considered confirmatory in nature
and has been designated Phase II. The logic of the
experimental path is depicted in Figure 2. Experi-
mental observations collected during Phase I were
indeed responsible for the development of the
juvenile-fry hypothesis tested during Phase II.

EXPERIMENTAL PATH

1. Mixed species stock- recruitment

relations , .

(platy mortality)

2. Single species stock -recruitment
analysis

( juvenlle-f ry Interaction?)

WEEKS DESIGNATION

0-8

PHASE I

8-36

3. Test of juvenile-fry
Interaction hypottiesis

Retention of

long-term

controls

36- 58

PHASE II

Figure 2. — The experimental design for guppy and southern
platyfish (platy) populations.

Phase I (Weeks 0-36)

WEEKS 0-8. — Twelve experimental aquaria
were grouped into three blocks of four aquaria
each and each block was assumed to have equal
position effect (Figure 3). Blocks A and C con-
tained replicate groups of four mixed species
populations each. Block B had replicate single
species guppy populations (aquaria 5 and 6) and
platy populations (aquaria 7 and 8). A gold strain
of guppies was used to allow visual separation of

•BLOCK A

timer

6

FISHERY BULLETIN: VOL. 78, NO. 3
BLOCK B y-BLOCK C'

4 5 6

8 9

10
11
12

timer

♦

yk

mttmmitiiMmim

I [♦heater

•♦balance

FIGURE 3. — Schematic of the laboratory facility showing block-
ing of experimental aquaria for guppy and southern platyfish
populations.

guppy and platy fry at birth, otherwise difficult
with wild-type strains. Weights, sex, and numbers
of each species initially stocked in aquaria are
listed in Table 2. Estimated age of both guppies
and platies at stocking was 14-18 wk.

All populations were fed rations containing
approximately equal proportions of the food items
with the exception of Artemia nauplii. All popula-
tions received a fixed daily ration of Artemia
nauplii, 0.2 g. Total rations were increased in
stepwise increments to keep the daily wet weight
equivalent of rations at from 25 to 359c of total
population biomass. Since growth of guppies ap-
peared more rapid in mixed species populations,
single species population rations were increased
in rapid increments at the end of week 6. Food
rations supplied to populations during the first 8
wk are in Table 3. At the end of week 8 all platies
were removed from mixed species populations and

Table 2. — Stocking of guppies and southern platyfish at initiation of experiments, 5 June

1975. Weights (grams) in parentheses.

Tank
number

Guppies

Southern platyfish

Block

Female

Male

Total

Female

Male

Total

totals

A
A
A
A

1
2
3
4

5(2.540)
5(2.452)
5(2.548)
5(2.574)

4(0.581)
4(0.599)
4(0.590)
4(0.664)

9(3,121)
9(3.051)
9(3,138)
9(3.238)

4(3,488)
4(3,668)
4(3,788)
4(3.455)

4(2.188)
4(2.359)
4(1.861)
4(2.155)

8(5,676)
8(6.027)
8(5.649)
8(5.610)

17(8.797)
17(9.078)
17(8.787)
17(8.848)

B
B
B
B

5
6

7
8

5(2,639)
5(2.746)

4(0.655)
4(0.677)

9(3.294)
9(3.423)

4(4,038)
4(4,176)

4(2.568)
4(2.511)

8(6.606)
8(6.687)

9(3.294)
9(3.423)
8(6.606)
8(6.687)

C

C
C

C

9

10
11
12

5(2.521)
5(2.355)
5(2.288)
5(2.290)

4(0.654)
4(0.542)
4(0605)
4(0.675)

9(3.175)
9(2.897)
9(2.893)
9(2.965)

4(3.550)
4(3.553)
4(3,470)
4(3,762)

4(2.152)
4(2.198)
4(2,161)
4(2,230)

8(5.702)
8(5.751)
8(5.631)
8(5.992)

17(8.877)
17(8.648)
17(8.524)
17(8.957)

560

HANKIN: A MULTISTAGE RECRUITMENT PROCESS

Table 3. — Schedule of daily rations fed to guppy and southern
platyfish populations during weeks 0-8. Total is expressed as a
wet weight equivalent.

Dry

Artemia

Artemia

Dates

food

adults

nauplii

Total

(1975) Weeks

(g)

(g)

(g)

(g)

Mixed-species populations (populat

ions 1-4,

9-12)

2 June- 6 July 0-4

0.2

1.0

0.2

3.2

7 July - 3 Aug. 4-8

0.15

1.25

0.2

2.95

Single species populations

Guppies (populations 5, 6)

2 June-21 June 0-2

0.08

0.4

0.08

1.28

22 June- 6 July 2-4

0.08

0.4

0.2

1.4

7 July -20 July 4-6

0.06

0.6

0.2

1.4

21 July -22 July —

0.08

08

0.2

1.8

23 July - 3 Aug. 6-8

0.10

1.0

0.2

2.2

Southern platyfish (populations 7

8)

2 June-21 June 0-2

0.15

0.75

0.15

2.4

22 June- 6 July 2-4

0.15

0.75

0.2

2.45

7 July - 3 Aug. 4-8

0.10

1.0

0.2

2.2

To determine, multiply dry food ration by 10 and add all food types.

rations were reduced to equal ration levels in
original single species guppy populations.

WEEKS 8-36. — Neither guppy population bio-
mass nor numbers at week 8 differed significantly
between original single species populations and
mixed species populations so the 10 remaining
populations were considered replicates during
weeks 8-36. To eventually achieve population age
structure which would be finely graded and to
achieve equality in numbers of original females in
all aquaria, the original females were gradually
"phased out" by removal of one adult female from
each population at weeks 11, 13, 15, and 17.
Original females were easily separated from re-
cently matured female progeny by their larger
size and were removed by selecting the smallest
female first, in each population, to least affect
population biomass. Food rations were increased
in stepwise increments through week 22 after
which time rations were fixed. A slight departure
occurred during weeks 28-29 when dried food only
was fed twice daily (Table 4).

Table 4. — Schedule of daily rations fed to guppy popula-
tions during weeks 8-36. Total is expressed as a wet weight
equivalent.'

Dry

Artemia

Artemia

Dates

food

adults

nauplii

Total

(1975-76)

Weeks

(g)

(9)

(g)

(g)

3 Aug. -19 Aug.

8-10

0.10

1.0

0.20

2.2

20 Aug -17 Sept.

10-14

0.13

1.3

0.20

2.8

17Sept.-28 0ct.

14-20

0.15

1.5

0.20

3.2

29 Oct. -12 Nov

20-22

0.18

1.8

0.20

3.8

13 Nov. -21 Dec.

22-28

0.20

2.0

0.20

4.2

22 Dec -30 Dec.

28-29

^0.40

—

—

4.0

31 Dec -15 Feb.

29-36

0.20

2.0

0.20

4.2

jTo determine, multiply dry food by 10 and add all ration types.
0.20 g fed twice daily. Three morning feedings were missed during
this period.

Phase II (Weeks ^6-58)

Three populations (5, 6, and 12) from the original
10 were selected at random to be long-term con-
trols. Of the remaining seven populations, two
pairs (1 and 2, 4 and 10) were mixed and divided to
give three approximately comparable populations
(for each mixed pair) of reduced numerical size
and biomass. The remaining three populations
were simply reduced in size to similar levels.
Numbers of individuals in reduced populations
ranged from 74 to 81, of which 42-49 were adults in
size categories > A55 (the largest adult male and
smallest adult female size category, see Table 1).
Total reduced population biomass ranged from 12
to 14 g, slightly less than one-half of apparent
maximum population biomass.

The nine reduced populations produced in the
above manner were assigned to three groups of
three each for treatment. Treatment consisted of
replacing original 5.0 mm spacing (on centers)
refuge fences with refuge fences of 4.5, 5.0, or 5.5
mm spacing. Each group contained two popula-
tions of mixed population origin and one which
had been reduced from a larger single population.
Refuge areas were assigned to populations with
the restriction that each of the three populations
produced from a mixed pair must be assigned a
different refuge fence spacing. A summary of
manipulations at week 36 is presented in Table 5.
Daily rations for Phase II are presented in Table 6.

RESULTS
Phase I
Weeks 0-8

The attempt to examine stock-recruitment rela-
tions in mixed species populations failed due to
high platy mortality in certain aquaria and an
apparent inability of platy fry to successfully
compete with guppy fry for food. Relative competi-
tive ability of platy and guppy fry was reflected in
contrasting mean weights of platy juveniles in
mixed and single species populations at the end of
week 8. Mean weights of platy juveniles, all born
during the first 2 wk of the experiments, were
0.0144 g in a mixed species population and 0.1037
g in a single species population at week 8. Guppy
juveniles, also presumably born within the first 2
wk, had reached a mean weight of 0.0979 g by
week 8 in the same mixed species population.

561

FISHERY BULLETIN: VOL. 78, NO. 3

Table 5. — Manipulations of guppy populations at the end of
Phase I (week 36» for test of refuge fence spacing treatment
effect during Phase II (weeks 36-58).

Tank Refuge

number assignment (mm) Origin

1 5.0 No. 1 and 2, mixed and reduced'

2 5.5 No. 1 and 2. mixed and reduced'

3 5.0 No. 3, reduced

4 4.5 No 4 and 10, mixed and reduced^

5 5.0 — "Long-term control"

6 5.0 — "Long-term control"

7 4.5 No, 1 and 2, mixed and reduced'

8 5.5 No. 4 and 10. mixed and reduced

9 4.5 No. 9, reduced

10 5.0 No. 4 and 1 0. mixed and reduced'

11 5.5 No. 11, reduced

12 5.0 — "Long-term control'

'Pluseightfry from tank no. 3.

Plus five fry and four A5 5 (an adult male size category, refer to Table 1)
males from tank no. 11.

Table 6. — Schedule of daily rations fed to treated guppy pop-
ulations during Phase II (weeks 36-58). Total is expressed as a
wet weight equivalent.

Dates

(1976)

Dry
food
Weeks (g)

Anemia
adults

(g)

Artemia
nauplii

(g)

Total

(g)

17 Feb. -28 Feb.

1 (Vlar.-15Mar.

16IVIar,-18 Apr.

36-38
38-40
40-58

0,15
0,18
0,20

1,5
1,8
2,0

0.20
0.20
0.20

3.2
3.8

4.2

'To determine, multiply dry food by 10 and add all ration types.

Since both mixed and single species populations
were fed at equal ration levels relative to total
population biomass, it seems reasonable to infer a
strong competitive advantage to guppy fry in
securing food.

In contrast, the presence of platies apparently
had little effect on guppy populations in mixed
populations. Tests (Student's t) for differences in
mean guppy population numbers and biomass
between single species and mixed species popula-
tions at week 8 failed to reject, at the a = 0.05
level, null hypotheses of equality in population
numbers or biomass. After removal of platies, all
guppy populations were treated as (equivalent)
replicates.

Weeks 8-.^6

The 10 replicate guppy populations through
week 36 showed a striking contrast between
growth in numbers and growth in biomass. Bio-
mass steadily increased in all populations and
weights attained at each sampling period were
nearly equal in all populations. Populations
seemed near a common maximum supportable
biomass by week 36. In contrast, numerical growth
was highly variable and often occurred as discrete
pulses of increase. Total population numbers

always varied greatly among populations and
there was no indication of a common approach to
an asymptotic or stable numerical population size
(Table 7).

BIOMASS DYNAMICS. — In general, biomass
growth in all guppy populations was typified
by steady, nearly uniform, biweekly increments
through the first 28 wk and by declining incre-
ments during weeks 28-36. Removals of individual
females at weeks 11, 13, 15, and 17 and restriction
of rations to dried food only during weeks 28-29
were clearly reflected in depressed biomass incre-
ments during these intervals of disturbance (Fig-
ure 4). At week 36 mean population biomass was
28.906 g and ranged from 26.291 to 30.717 g.

Using data for weeks 18-28 and 30-36 (periods
during which neither removals nor atypical feed-
ings occurred, and beyond the time when platies
were also present in certain populations), maxi-
mum supportable biomass for each population was
estimated by assuming a logistic biomass growth
model. Application of the logistic model presumed
that biomass growth was limited by the final fixed
ration level reached at week 22. Maximum bio-

T
O

T
A

L

B
I

O
M
A
S
S

g

r
a
m
s

12 18

WEEKS

Figure 4. — Mean population biomass of guppies during Phase
I. Removals of individual females at weeks 11, 13, 15, and
17 and restriction of ration to dried food only during weeks 28-29
are indicated by arrows. Vertical lines represent standard
deviations.

562

HANKIN; A MULTISTAGE RECRUITMENT PROCESS

Table 7. — Total population numbers and, in parentheses, total biomass in grams for single species tguppy) populations at week

of enumeration during Phase I, weeks 0-36.

Populatior

1 number

Mean
numbers

Mean
biomass

Week

1

2

3

4

5

6

9

10

11

12

(SD)

(SD)

0

9

9

9

9

9

9

9

9

9

9

9

3.120

(3.121)

(3.051)

(3.145)

(3.238)

(3.294)

(3.423)

(3.175)

(2.897)

(2893)

(2.965)

(0)

(0.173)

1

9

(3.955)

34
(3.548)

21.5
(17.7)

3.752
(0.288)

2

29

43

37

31

38

39

40

12

33.6

3.930

(3.903)

(4.025)

(4.176)

(4.599)

(4.074)

(4.162)

(3.009)

(3.495)

(9.9)

(0.483)

3

38
(4.685)

33

(4.921)

35.5
(3.5)

4 803
(0.167)

4

53

57

39

50

35

64

32

28

44.8

5.436

(5.798)

(5.985)

(4.935)

(6.059)

(5.332)

(5.995)

(4.642)

(4.740)

(13.0)

(0.599)

5

43
(5.713)

63
(5.443)

53.0
(14.1)

5573
(0 191)

6

72

75

39

58

48

61

33

34

52.5

6 860

(7.379)

(7.968)

(5.466)

(8.027)

(6.871)

(7.552)

(5.835)

(5.778)

(16.5)

(1.035)

7

41
(6.682)

61
(7.392)

51.0
(14.1)

7.037
(0.502)

8

91

97

38

69

47

59

33

54

61.0

8.558

(9.355)

(8.372)

(8.216)

(9.073)

(8.373)

(9.458)

(7.711)

(7.902)

(23.3)

(0.659)

9

39
(8.582)

61
(8.494)

50.0
(15.6)

8.538
(0.062)

10

108

93

39

83

48

60

32

78

67.6

10.173

(10.853)

(9.965)

(9.423)

(10.785)

(10.228)

(11.335)

(9.519)

(9.273)

(27.1)

(0.756)

11

40
(10.241)

63
(10.638)

51.5
(16.3)

10.440
(0281)

12

136

103

38

89

46

58

62

76

76.0

11.205

(12.087)

(12.058)

(10.235)

(11.686)

(10.734)

(11.483)

(10.420)

(10.929)

(32.4)

(0-724)

13

38

(10.047)

59
(10.964)

48.5
(14.8)

10.506
(0.648)

14

158

100

61

88

36

58

46

66

85

100

79.8

11.416

(12.881)

(12.391)

(10.233)

(12.440)

(10.002)

(10.808)

(11.403)

(12.509)

(10.482)

(11.009)

(35.1)

(1 062)

16

181

106

77

85

36

66

43

74

89

105

862

12.137

(13.762)

(13.253)

(10.794)

(12.989)

(9.934)

(12.419)

(11.908)

(12.552)

( 1 1 .447)

(12.309)

(40.5)

(1.158)

18

190

113

92

83

40

92

51

67

84

104

91.6

12 623

(13.729)

(14.552)

(11.042)

(13.697)

(10.488)

(12.365)

(12.302)

(13.176)

(12.113)

(12.768)

(41.3)

(1.243)

20

190

112

98

81

64

111

82

78

86

103

100.5

15.230

(16.169)

(17.282)

(13.555)

(15.687)

(12.710)

(15.075)

(14.826)

(15.518)

(15.801)

(15.681)

(35.0)

(1.302)

22

192

112

100

78

73

107

95

92

87

101

103.7

18.097

(19.709)

(19.688)

(16.151)

(18.502)

(15.989)

(18.555)

(17.354)

(18.571)

(17.545)

(18.906)

(33.3)

(1.311)

24

189

113

98

95

76

104

98

97

85

103

105.8

20.187

(21,837)

(21.562)

(19.618)

(20.220)

(18.037)

(19.898)

(18.828)

(19.827)

(20-674)

(21.365)

(31.0)

(1.213)

26

191

112

99

127

75

102

96

125

85

102

111.4

22.528

(24.391)

(24.144)

(21.276)

(22.687)

(20.760)

(23.289)

(21.388)

(21,479)

(22.149)

(23.714)

(32.2)

(1.305)

28

200

111

95

149

75

102

103

130

85

104

115.4

24519

(25.953)

(25.886)

(22.705)

(24.824)

(23.305)

(25.171)

(23.810)

(23.890)

(24.361)

(25.284)

(36.4)

(1.091)

30

197

112

107

142

83

102

101

139

138

132

125.3

25.133

(26.558)

(26.465)

(23.624)

(25.584)

(23.857)

(26.295)

(24.607)

(23.947)

(24.526)

(25,865)

(32.1)

(1.148)

32

194

110

128

151

91

168

101

135

152

160

139.0

27.350

(28.909)

(28.641)

(26.355)

(27.953)

(26.093)

(27.654)

(26.418)

(25.377)

(27.452)

(28.679)

(32.2)

(1.232)

34

191

118

162

143

98

171

98

149

178

173

148.1

28395

(29.614)

(29.580)

(28.085)

(29.099)

(27.548)

(29.842)

(27.327)

(27.104)

(26.150)

(29.599)

(33.4)

(1.316)

36

186

114

178

156

112

197

119

144

186

169

156.1

28.906

(29.580)

(30.158)

(28.363)

(30.004)

(28.258)

(30.717)

(27.470)

(27.560)

(26.291)

(30.656)

(32.2)

(1.527)

mass for each population was estimated from the
slope and intercept of a regression of the reciprocal
of population biomass at week t + 2 against the
reciprocal of biomass at week t as: maximum
biomass — Sj^ax = '1 ~ slope )/intercept. Esti-
mates of maximum biomass ranged from 27.8 to
37.6 g (Table 8) with a mean estimate of 31.8 g.

The nearly uniform changes in total biomass
throughout Phase I, despite widely divergent
numerical growth patterns, implied that growth
was strongly density-dependent. Density-depen-
dence of growth was seen most dramatically in
the mean weights of large adult females. Mean
weights of adult females in size categories A^ and

Ag were inversely related to mean population
numbers during weeks 0-36 (Figure 5).

NUMERICAL DYNAMICS. — WTiile the guppy
populations appeared to approach a common maxi-
mum supportable biomass, no such commonality
was evident in total population numbers. Numeri-
cally, populations grew in erratic and independent
fashion with no clear indications of asymptotic
behavior. Numerical growth was steadily positive
\s\ only a single population (population 1). In all
other populations patterns of numerical increase
were unanticipated and often consisted of discrete
pulses of increase, followed by periods of static

563

FISHERY BULLETIN: VOL. 78, NO. 3

Table 8. — Logistic growth method estimates of maximum bio-
mass (finiax in grams ( for Phase I guppy populations. Esti-
mates exclude weight of fry and are based on data collected
for weeks 18-28, and 30-36.

200

Population
number

Population
number

1

0.992

32.7

6

0.980

32.4

2

.997

33.4

9

994

30.9

3

993

32.0

10

.991

29 9

4

.995

37.6

11

.972

27.8

5

.993

30.6

12

.987

31,1

'Correlation coefficient for regression of 1/biomasSf + 2 against 1/biomasSf .

M
E
A
N

F
E
M
A
L
E

W

E

I

G

H

T

g"

r
a
m
s

1.1

1.0

0.9

0.8

0.7

0.6

0.5^

I II III-

50 75 100

MEAN TOTAL

125 150

NUMBERS

Figure 5. — Density-dependence of guppy growth illustrated by
plot of mean female weight (in size categories A 7 -i- A g ) at week
36 against mean total numbers during weeks 0-36.

population numbers, followed by further pulses of
increase (Figure 6). No position effect was detected
when mean total numbers in blocks A and C were
compared by Student's t test.

The patterns of numerical increase exhibited by
these populations were in striking contrast with
the control (unexploited) populations maintained
by Silliman and Outsell (1958). Behavioral obser-
vations and examination of size structure data
collected during Phase I indicated that the pres-
ence of juveniles in the J4 size category somehow
inhibited survival of newly born fry, presumably
through some juvenile-fry interaction within the
refuge area. Plots of estimated numbers of fry
surviving to enumeration during a biweekly in-
terval, corrected for observed mortalities ( = ad-

is 24

WEEKS

Figure 6. — Pulsing behavior of numerical population growth
illustrated by guppy populations 3 (solid line) and 11 (dots).

justed population increment), and numbers of J4
juveniles present at the beginning of the interval,
against time showed distinct offset peaks of abun-
dance in many populations. The relations could be
further improved by introducing a 2-wk time lag
and plotting the number of J4 juveniles at t — 2 wk
and the adjusted population increment from t to
t + 2 wk against time (Figure 7). The time lag
improvement implied that only larger juveniles
within the J4 size category were responsible for
inhibition of fry survival. Small J4 juveniles at
t — 2 wk would have become large J4 juveniles
(roughly equal to the J45 size category monitored
during Phase II) at time t.

Strong and statistically significant (P<0.05)
negative correlations between biweekly adjusted
population increments and the natural logarithm
of J4 juveniles (-1-1) present 2 wk before the begin-
ning of a sampling interval were found in 8 of 10
populations (Table 9). These negative correlations
between numerical population growth and juve-
nile densities detected at several levels of adult
stock density showed that numerical population
growth, and thus the recruitment process, in these
populations could not be a simple function of adult
stock alone. Likely, interactions between newly

564

HANKIN: A MULTISTAGE RECRUITMENT PROCESS

A
D
J
U
S
T
E
D

P
0
P
U
L
A
T
I

0
N

1
N

c

R

E
M
E
N

T

Figure 7. — Adjusted population increment (in t, t + 2) and
number of J^ guppy juveniles (at t - 2) plotted against week
(at t + 2) in population 3. The plot incorporates a 2-wk time
lag. Solid line is adjusted population increment. Dots show
juvenile densities.

born fry and immature juveniles had created a
complicated population growth process involving
both immature and adult population components
as had been briefly mentioned by Ricker (1954).

A tentative conceptual model of numerical pop-
ulation dynamics was proposed and is depicted in
Figure 8. Survival of newly born fry in a given
experimental interval can be viewed as a two-step
process. Fry born must first elude adult predators
outside the refuge area. Fry which successfully
elude adults and enter the refuge area are faced by
predation, competition, or harrassment by large
J4 juveniles present in the refuge area. Pulses of
numerical increase can easily be created if such a
process occurs. Following the initial entrance of
fry into the refuge area, growth of fry occurs. Once
fry grow to the juvenile size at which interaction
with newly born fry occurs, fry survival is inhib-
ited so long as juveniles are smaller than the J5
size category. Once reaching the J5 size category,
juveniles are transferred to the main aquarium
environment at enumeration. The refuge area is
once more free of juveniles, and fry successfully
eluding adult predators and entering the refuge
area are once more expected to survive.

Since the above explanation for the pulsing
quality of numerical growth seen in many popula-
tions seemed a plausible hypothesis, alteration of
the refuge fence design (by either increasing or
decreasing spacing between glass rods) would
likely increase or decrease the intensity and
duration of juvenile-fry interactions within refuge
areas. This hypothesis was examined in Phase II.

Table 9. — Linear correlation coefficients (r) between adjusted
population increment (AP/^_ , + 2) and natural logarithm of
juvenile numbers [ln(e/4^_2 "'' ^^^ in Phase I guppy populations.

Population number

Population number

1

-0.5166-

6

- 0.7704-

2

-.5919-

9

- .6042-

3

-.5215-

10

- .0487

4

- .7300-

11

- .6047-

5

-.6158-

12

- .3600

•PsO.05.

Adult
Predators
at t

Adult
Females

at t

Fry Born
in t,t+2

• • •Refuge Fence* • •

• r

Fry in
Refuge Area

Growth to
J4

Juveniles

Predators
at t

Growth to

Size Category

• 'Refuge Fence*

Figure 8. — Diagram depicting the hypothesized numerical
dynamics model for guppy populations. Solid lines and arrows
indicate path from birth to survival as adult. Small dots and
arrows depict paths leading to death through cannibalism by
adults or juveniles.

OTHER OBSERVATIONS. — Additional data
collected during Phase I included examination of
guppy scales for fluorescent marks and records of
disease incidence. Examination of scales removed
from fish at week 36 was disappointing. No scales
showed more than five to seven marks while the
maximum expected number of marks was nine. It
is possible that at the final ration level individual
fish did not receive sufficient food intake to
produce detectable marks. Further research into
the matter was not pursued, but marking was
continued during Phase II so that experimental
manipulations would remain constant. All guppy
disease problems were chronic in nature, minor,
and were consistently diagnosed as piscine tuber-

565

FISHERY BULLETIN: VOL. 78, NO. 3

culosis. At no time did deaths due to disease
approach epidemic levels in any population. Fre-
quency of disease symptoms, deaths attributable
to disease, etc., for each population may be found
in Hankin (1978b).

Phase II (Weeks 36-58)

Long-Term Controls: Populations 5, 6, and 12

Total population biomass of control guppy popu-
lations during weeks 36-58 confirmed the earlier
speculation that populations were near their max-
imum biomass by week 36. Net changes in total
biomass from week 36 to week 58 were +0.5, + 0.1,
and +0.9 g in populations 5, 6, and 12. Minor
asynchronous fluctuations in biomass occurred
throughout Phase II in all control populations.
Logistic-based estimates of maximum supportable
biomass made at week 36 were 30.6, 32.4, and
31.1 g and agreed remarkably well with actual
biomass levels at termination, 28.3, 30.7, and
30.7 g.

Control populations showed no signs of conver-
gence in total population numbers nor of parallel
fluctuations. Although total numbers in the three
control populations differed greatly, total num-
bers and weights of reproductive females (size
categories Ag-Ag) were similar. In populations
5, 6, and 12 there were 37, 36, and 42 such females
at termination with corresponding total weights
of 20.6, 17.6, and 20.0 g. Since fecundity is roughly
proportional to female weight, the three popula-
tions had nearly equal reproductive potentials in
spite of large differences in total numbers. Adult
females accounted for from 57 to 72% of total
population biomass. No uniformity in numerical
or biomass densities was noted for adult males.

Treated Populations

BIOMASS DYNAMICS.— Total population bio-
mass increased in all treated guppy populations
during Phase II (Figure 9). At termination, mean
population weights of the three treatment groups
were not found significantly different in pairwise
comparisons (Student's t tests). Since greatest
differences in mean biomass among treatment
groups occurred at week 58, there were probably
no statistically significant differences in mean
biomass throughout Phase II. Alteration of refuge
fence spacing had no apparent effect on population
biomass growth.

30

4.5

mm

group

•

5.0

mm

group

B

25

5.5

mm

group

*

0

M
A

20

«

i

«

_^_^

15

*i

9
r

I;

m

s

10

36

40

44 48

WEEKS

52

56

Figure 9. — Mean total biomass in treatment groups of guppies
during Phase II.

Mean total weights of mature females (size
categories Ag-Ag) differed significantly among
treatment groups (Student's t tests). The mean
percentage of total population biomass accounted
for by adult females was consistently higher in
the 5.5 mm group (71%) than in the 4.5 mm
group (56%).

NUMERICAL DYNAMICS. — Although bio-
mass growth was roughly equal for all treated
guppy populations, treatment groups diverged
rapidly in total numbers (Figure 10). Smallest
population numbers were maintained in the
5.5 mm group, intermediate but highly variable
numbers in the 5.0 mm group, and largest num-
bers in the 4.5 mm group. At termination mean
total numbers in the 4.5, 5.0, and 5.5 mm treat-
ment groups were 249, 160, and 128. Mean net
additions during Phase II, in the same order, were
172, 86, and 47.

M
E
A
N

N
U
M
B

E
R
S

JUU

4.5 mm

group

•

•

•

240

5.0 mm
5.5 mm

group
group

*

•

•

•

•

•

180

•

D

D

n

a

a

D

•

D

D

#

■X-

*

120

n

*

*

*

•X-

*

■X-

*

•

^ *

60

36

40

44 48

WEEKS

52

56

Figure 10. — Mean total numbers in treatment groups of guppies
during Phase II.

566

HANKIN: A MULTISTAGE RECRUITMENT PROCESS

Alteration of refuge fence spacing during Phase
II was believed to have influenced both the inten-
sity and duration of juvenile-fry interactions.
Behavioral observations of a 5.0 mm refuge popu-
lation provided a partial explanation of mecha-
nisms involved. A female was observed delivering
four fry and the subsequent immediate fate of the
fry was followed. Two of the fry were pursued and
consumed by two different adult females. Two
other fry successfully entered a refuge area after
vigorous pursuit by several males and females,
including the female giving birth. Once w'ithin the
refuge area the fry were chased and nipped by
larger juveniles. Although the juvenile chase
shortly ceased and the fry settled to the aquar-
ium bottom apparently uninjured, alternative
outcomes seemed possible. Fry could have been
chased outside the refuge area where they would
once more be vulnerable to adult predation or the
juvenile contact could have resulted in death and
perhaps cannibalism. The observations indicated
that survival of newly born fry was determined in
an extremely short period of time. From release to
death or apparent survival in the refuge area
never occupied more than perhaps 2 min. Since
guppy fry are capable of rapid swimming within
minutes after birth, it is unlikely that juvenile
pursuit within the refuge area would be successful
except during the first few minutes after birth.

The intensity and duration of juvenile-fry inter-
actions, reflected in patterns and magnitude of
numerical population growth among treatment
groups, was measured and characterized (in pa-
rentheses see Table 10) in several ways:

1) by the number of biweekly intervals in
which adjusted population increments were
«0(#PI«0);

2) by the length in biweekly intervals of the
longest period without a positive population
increment (Long. 0 PI);

3) by the median adjusted population incre-
ment (Med. PI);

4) by the median population numbers (Med. N);

5) by the total number of data observations
with zero individuals per any size category
(#0/CAT);and

6) by the mean percentage of population num-
bers in size categories ^ J5.0 (% adult).

Measures 1) and 2) were designed to evaluate the
prominence of pulsing. Intervals between succes-
sive pulses of increase should be greatest when

Table 10. — Comparison of measures of numerical population
growth for treated guppy populations during Phase II. See text
for explanation of column entries.

Treatment

Long.

group

#PI«0

OPI

Med. PI

Med.N

#0;CAT

% adult

4.5 mm:

4

1

1

9

192

0

52

7

1

1

22

236

0

41

9

1

1

9

178

0

53

Mean

1

1

13.3

202

0

48.7

5.0 mm;

1

2

2

21

196

0

47

3

4

1

8

146

0

64

10

4

2

1

83

6

87

Mean

3.3

1.7

10

141.7

2

66

5.5 mm:

2

4

2

1

99

4

81

8

6

2

0

122

5

73

11

5

4

0

79

12

73

Mean

5

2-7

03

100

7

75-7

longest periods of juvenile presence occur within
refuge areas. The 5.5 mm group should exhibit
strong pulsing behavior while the 4.5 mm group
should show little if any pulsing (Silliman and
Outsell 1958). Measures 3) and 4) were designed to
evaluate effects of juvenile-fry interactions on
population numbers. Although the duration of
juvenile-fry interactions might not be reflected in
total population size at any given time, it should
be reflected in median population numbers and in
median population increments during the experi-
mental period. Measures 5) and 6) were designed
to evaluate size structure smoothness and relative
dominance by adults. The characteristic patterns
of growth produced under different refuge envi-
ronments should be reflected in the age structure
of treated populations and, although less distinct-
ly, in the size structure. The 4.5 mm group should
have a finely graded size structure with juveniles
nearly always present, while the 5.5 mm group
should have a fluctuating size structure perhaps
including distinct "size classes" corresponding to
separate pulses of increase.

Comparison of these measures compiled for all
treated populations showed clear separation for
each measure between 4.5 mm and 5.5 mm groups.
In no case was the 5.0 mm group clearly separated
from the other groups, although means of all
measures for the 5.0 mm group fell between means
for 4.5 mm and 5.5 mm groups. Orders of means
were in the directions expected on the basis of the
juvenile-fry interaction hypothesis (Table 10).

The above comparisons do not, however, allow a
"test" for differences in numerical population
growth patterns among treatment groups, in part
because the several measures are not independent
of one another. Rather, comparison of these quan-

567

FISHERY BULLETIN: VOL. 78, NO. 3

titative measures allows qualitative separation of
treatment group behavior, illustrates the high
variability in behavior within the 5.0 mm refuge
fence group, and shows that measures of numeri-
cal dynamics generally conform to anticipated
differences.

The larger variability in population behavior
among the 5.0 mm treatment group was witnessed
earlier among the original 10 replicate popula-
tions equipped with 5.0 mm refuge fence. Laakso
(1959) speculated that the tendency toward canni-
balism increased with age of guppies and it may be
that at the J45 stage such tendencies are first
beginning to be expressed. The exact age or size at
which they become fully expressed may be highly
variable. An alternative possibility here would
certainly include possible imperfections in refuge
fence construction which might have allowed J50
fish, which clearly exhibited antagonistic behav-
iors toward fry, to remain within 5.0 mm refuge
areas beyond the size at which they should have
been excluded.

(LENGTH) X 10

Figure 11 — Number of embryos plotted against the cube of
female guppy length (stEtndard length in millimeters). Regres-
sion line is forced through the origin.

SURVIVAL RATES. — Since the juvenile-fry
interactions often created pulses of numerical
increase in the guppy populations, there were
frequent intervals in which there were no new
individuals entering populations. Survival rates
for most populations during Phase I and Phase II
were estimated by comparing the numbers of fish
present at the beginning of such an interval to
numbers present at the beginning of the next
biweekly interval during which new numerical
growth was recorded. Survival rates for the 4.5
mm group and for certain 5.0 mm populations
during Phase II could not be estimated due to the
continuous nature of numerical increase. Esti-
mates of survival rates for intervals > 2 wk were
converted to biweekly estimates assuming con-
stant biweekly survival over the longer period.
Mean biweekly survival rate estimates ranged
from 0.972 to 0.995 during Phase I and from 0.953
to 0.984 during Phase II, averaging 0.984 and
0.970. These biweekly rates indicate roughly 50%
annual survival, a reasonable figure for laboratory
populations of guppies.

FECUNDITY. — Dissection of a wide size range
of gravid guppy females at termination showed
that numbers of embryos were linearly related
to the cube of female length. Variability in
embryo counts appeared to increase with female
size (Figure 11). A linear regression of num-

bers of embryos against the cube of female length
was forced through the origin and could be ex-
pressed as:

E = 5.328 (L^ X 10""*)

where E = number of embryos

L = standard length in millimeters.

The regression was forced through the origin to
ease manipulation of the fecundity relation in
further analyses and, over the majority of the size
range, did not differ appreciably from a regression
with intercept. The empirical relation obtained
was similar to earlier results of Felin (1935) and
Laakso (1959).

A mean condition factor {K in the formula
weight = /C • L^) for gravid and nongravid fe-
males in A5 5 and larger size categories at weeks
36 and 58 was applied to the above relation to
obtain an expression relating embryo counts to
female weight in grams: E = 22.347 ■ female
weight. In the following analyses the fecundity
relation was assumed to have held constant
throughout the 58- wk experimental period.

ANALYSIS: NUMERICAL DYNAMICS

Behavior of the treated guppy populations dur-
ing Phase II generally supported the hypothesis of

568

HANKIN: A MULTISTAGE RECRUITMENT PROCESS

juvenile-fry interactions and the proposed concep-
tual model. However, analysis to this point has
implicitly assumed a constant input of newly born
fry into the refuge areas, modified downward by
the presence of interacting juveniles. Since fry
were produced by reproductive females whose
numbers and weights increased greatly as pop-
ulations grew, a complete analysis must clearly
include a description of the female reproduc-
tive component. Additionally, the influence of
adult predators outside the refuge area must be
considered. In this section I develop a mathe-
matical model of the dynamics of numerical pop-
ulation change and subject this model to statis-
tical analyses.

Development of a Mathematical Model

Population reproductive potential increases
with the weight and number of adult guppy
females. The total reproductive potential, i.e., the
maximum possible number of fry born in a given
interval, in a population at the beginning of an
interval can be computed from the fecundity
relation and the total female weight as: reproduc-
tive potential = 22.347 • S t' total weight fe-

males per size category. Total reproductive poten-
tial is not realized in any given interval since only
some (variable) fraction of females will actually
deliver broods. In order to obtain estimates of
biweekly fry production, the probability that a
female will deliver a brood during a 14-d experi-
mental interval is needed.

The calculation of this probability requires:
1) the expected length of an interbrood interval
(time from the last brood when the next brood is
delivered), 2) an estimate of the gestation period
or minimum time between broods, and 3) a fre-
quency distribution for the interbrood interval. In
guppies the interbrood interval is roughly 31 d
(Breder and Coates 1932; Winge 1937; Rosenthal
1952), gestation period has been estimated at from
21 to 25 d (Winge 1937; Rosenthal 1952), and a
rough frequency distribution may be constructed
from the preceding studies. Using "renewal pro-
cess" theory (Drake 1967), the probability that the
waiting time Y until the next brood of an individ-
ual female is delivered will be ^14 d (length of a
sampling interval ), when there is no knowledge of
her exact stage in the brood cycle (as was the case
for these populations), is denoted by P(y^l4 d).
Letting T = interbrood interval, and s be a fixed

but random point in the brood cycle, then T =
s + y; that is, the total length of the interbrood
interval (T) is equal to the time since the last
brood is) plus the waiting time (y) until the next
brood is delivered. Using a cumulative density
function for the interbrood interval (T), which
may be constructed from previous studies, one
has (using standard notation):

Then fyiy)

PiT^t) = Frit).

^[1 - P(T^y)]
EiT)

J4

, [1 - P[T^y)]
and P(y^l4) = J ^^^^ -" dy

14

= IIE(T)- / [1 - FT(y)]dy (1)

where EiT) denotes expected value.

The probability of an interbrood interval of ^14 d
is 0 (gestation period estimates are at least 21 d)
so Equation (1) may be reduced to: P(y«14) =
lAIEiT) = 14/31 = 0.452.

This probability may be applied to the esti-
mated reproductive potential to obtain an esti-
mate of the expected number of births in a 2-wk
interval as: expected number of births t, t+2 =
0.452 • reproductive potential f Comparison of
adjusted population increments (API) with ex-
pected number of births (EB) allows estimation
of survival rates (S) for fry born in a given
interval as:

St, t+2 - APIt,t+2lEBt^t+2-

Survival of newly born fry through a 2-wk
interval depends on both predation by adults
outside the refuge area and juvenile-fry inter-
actions within the refuge area. Survival within
the refuge area is conditioned upon the event
"successful refuge entry," so one has:

P(surviveto^+ 2) = P(A andS) = P(A) • P(B| A)

where P(A)

P(B\A)

P( "successful refuge entry")
P( survive within refuge area

given A has a successful

outcome).

569

FISHERY BULLETIN: VOL. 78. NO. 3

Events A and B are related to densities of adults
and juveniles, respectively, during a 2-wk interval.
By examination of only those sampling inter-
vals for which the (initial) juvenile ( J4.5) density
equals 0, one may separate the relation between
adult density and fry survival from the compli-
cating juvenile-fry interaction. For such intervals,
neglecting natural mortality, survival within the
refuge area should be approximately 1. That is,
when J45 density = 0: Pi A and B) = PiA) =
/"(adult density only). Biweekly fry survival rates
were estimated as described above and plotted
against numerical densities of fish in size cate-
gories J5.0 through A 8 in 5.0 mm populations
from Phase I and from long-term control popula-
tions during Phase II revealing a decreasing trend
in survival rates with increasing predator density
(Figure 12). Beyond 100 adults, estimated survival
was close to zero. The trend appeared roughly
exponential (one explanation is based on random
encounters between predators and prey, see Ricker
1954), so a negative exponential model was used
for further analysis:

PiA) = exp[Si • (adult density)]; Bi<0.

Since adults were always present when juve-
niles were present in refuge areas, it was not
possible to separate the effects of the juvenile-fry
interaction from adult predation. By analogy,
I also used the negative exponential model to
describe the relation between juvenile numbers
and refuge area fry survival rates, i.e.:

P{B\A) = exp[B2 • (J4 5 density)]; 5 2 ^0.

E
S
T
I

M
A
T
E
D

F
R
Y

S

U
R
V
I

V
A
L

R
A

T
E

1.6

•

1.2

•

0.8

\j

0.4

•
•

•
•

••

• •

•
•

•
•

U..-

•

20

40
ADULT

60 80

PREDATORS

100

120

The full model appropriate for all sampling in-
tervals is then:

P(survive to ^ + 2 given born in ^, / + 2)

= S = API/EB = exp(BiX, + ^2^2)

where X^ = number of adults in size categories
t/s 0 and above at time t
X2 = number of J45 juveniles at t.

Statistical Analysis

Two techniques were used to fit the collected
guppy population data to the proposed model
developed above. Both techniques were based
on the same assumed model although the model
was expressed in different forms according to
analysis technique:

St,t+2 ^ ■^h,t + ilEBt,t+-2

= exp(fiiXi^ + B2^2;K and (2)

APIt^t+2 = EBt,t+2 • exp(SiXi^ + B^X^f). (3)

Multiple regi'essions, forced through the origin,
were fit to a transformation of Equation (2)
(adding 1 unit to API to avoid undefined natural
logarithms)'*:

ln[(AP/^, ^+2 + l)IEBt,t+2^ = B^Xif + B^X^r

Alternative estimates of Sj and B2, the "coeffi-
cients of predation" for adults and juveniles, were
obtained by nonlinear least-squares regressions
based on a Taylor series linearization of Equation
(3) (Draper and Smith 1966). In this case one
minimizes:

liAPIt,t+2- AFIt,t+2)^ - l[APIt,t+2

- EBt,t+2 ■ exp(5iXi^ + ^2^2^)]^

to obtain the iterative solutions for B^ and B2-
Iteration was continued for these estimates until
the last estimate agreed with the previous esti-
mate to six decimal places. All population data
series were subjected to analysis by the same
model. Note that the dependent variable for the

Figure 12. — Relation between estimated guppy fry survival
rates (&t.t + 2' ^^^ number of adult guppy predators (number
3= J5 g at t) when no J4 5 juveniles were present at t. Line is
drawn by eye. Squares represent multiple observations.

^ While an interaction term of the form X^X^ might seem a
logical addition to the above model, analyses failed to indicate
that such an interaction was significantly involved in deter-
mining numerical dynamics of the populations.

570

HANKIN: A MULTISTAGE RECRUITMENT PROCESS

multiple linear regressions is the natural loga-
rithm of estimated survival rates, while for the
nonlinear regressions it is actual observed popula-
tion increments.

If the model were correct one would expect that
statistical analyses should give:

1) estimates of the B^ coefficient similar in
all populations,

2) estimates of the B2 coefficients which are:

a) close to 0 in the 4.5 mm populations,

b) some negative number in the 5.0 mm
populations,

c) some negative number larger in absolute
value than in b) for 5.5 mm populations.

No juvenile interactions would be expected in the
4.5 mm treatment group and J5 0 individuals
contributing to predation in the 5.5 mm popula-
tions, but not included in X2 , would be expected
to increase the 82 coefficient. Numbers of J4 5
individuals present at the beginning of intervals
during Phase I were estimated from total numbers
and weights recorded for the combined J4 cate-

gory monitored during Phase I (see Hankin 1978b
for details).

Results of multiple regression analyses of orig-
inal and long-term 5.0 mm populations appear in
Table 11 and of treated populations during Phase
II in Table 12. Squared multiple correlation coeffi-
cients (r^), when both adults and juveniles were
included in regressions, ranged from 0.8003 to
0.9272 in Phase I populations indicating that
about 80 to 907c of the uncorrected sums of squares
of the natural logarithms of estimated fry survival
rates could be explained by regression on adult
and juvenile densities. Estimates of adult preda-
tion coefficients were similar for all populations,
and estimates of juvenile predation coefficients
differed in the expected order among treatment
groups. Differences among juvenile predation co-
efficients were less striking than had been antici-
pated. Mean estimates of B2 for 4.5, 5.0, and 5.5
mm treatment groups were -0.0280, -0.1009,
and -0.1249.

Alternative estimates of 5i and B2, obtained
by minimizing the squared deviations between
actual and predicted biweekly adjusted popula-

Table 11. — Estimates of predation coefficients (Bj, fij' ^nd squared multiple correlation
coefficients (r ) for Phase I guppy populations. Based on multiple regression analysis of the
hypothesized model: ln[lAP/ + 1)/EB] = B^Xi + B^X^. See text for explanation of model
parameters.

Population
number

Adu

Its and juvenll(

3S

Adults

only

Juveniles

only

Weeks

(mm)

e,

e.

r'

e,

r^

e,

r=

1

0-36

5.0

-0.0471

+ 0.0055

0.9186

-0.0449

0.9185

-0.1029

0.8423

2

0-36

5.0

- .0426

- .0031

9272

- .0429

.9272

-.1568

.3370

3

0-36

5.0

- .0202

-.1457

.8116

-.0397

.6298

-2146

.7223

4

0-36

5.0

- .0322

- .0994

9044

-.0448

.8406

- 2292

.6910

5

0-58

5.0

-.0316

-.1485

8691

-.0512

.8099

- .3084

7661

6

0-58

5.0

-.0221

- . 1 1 70

.9111

-.0416

.8580

- 2207

.8576

9

0-36

5.0

- .0472

-.0771

.8324

- .0589

.8080

- .2530

6090

10

0-36

5.0

-.0317

-.1033

.8774

- .0480

.7954

- .2094

.7129

11

0-36

5.0

- .0335

-.1131

.8003

- .0456

.6664

-.1943

.5352

12

0-58

5.0

- .0257

- .0963

8489

- .0347

.8140

- .2637

.6762

Table 12. — Estimates of predation coefficients (Bj, B^) and squared multiple correlation
coefficients (r ) for treated guppy populations during Phase II. Based on multiple regression
analysis of the hypothesized model: ln([AP/ -1- l]IEB) = B,Xi -t- B^X^- See text for explana-
tion of model parameters.

Adults and juveni

les

Adults

only

Juveniles only

Population
number Weeks

Fence
(mm)

s,

e.

2

r

8,

r'

^2

r'

4 36-58

4.5

-0.0155

-0.0665

0.9005

-0.0328

0.8850

-0.1225

0.8888

7 36-58

4.5

-.0176

- .0253

.8529

- 0250

.8385

- .0755

.7852

9 36-58

4.5

- .0303

+ .0079

.8867

- .0288

.8864

-.1340

.8047

Means: 4.5 mm group

-.0211

- .0280

8800

- .0289

.8700

-.1107

.8262

1 36-58

5.0

- .0068

-.1228

.8744

- 0282

.8567

-.1608

.8727

3 36-58

5.0

- .0276

- .0682

.9211

- .0375

.9078

- .2258

.8352

10 36-58

5.0

- .0492

-.1117

.9501

- .0538

.9437

-.7307

.5749

Means: 5 0 mm group

- .0270

-.1009

.9152

- .0398

.9027

- .3724

.7609

2 36-58

5.5

- .0392

-.1433

9599

-.0518

.9532

- .2274

.9078

8 36-58

5.5

- .0430

-.0417

.9550

- .0486

.9536

-.1732

.8999

11 36-58

55

- .0450

-.1896

.9114

- .0589

.8617

-.3131

.8057

Means: 5.5 mm group

- .0424

- 1249

.9421

- .0531

.9228

- .2546

.8711

571

FISHERY BULLETIN: VOL. 78, NO. 3

tion increments, were strikingly different among
treatment groups. Mean estimates of B2 in 4.5
mm and 5.0 mm treatment groups were -0.0024
and - 0.0857. Estimates for the three 5.5 mm pop-
ulations were -0.0494, -0.1523, and "- . Large"
(fails to converge to finite negative number),
again indicating strong interaction by juveniles
(Table 13). However, alternative fits of actual
population increases against adult and juvenile
densities could account for an average of only 59%
of the variation in the uncorrected sums of squares
of the adjusted population increment variable.
Still, given initial population states at the begin-
ning of intervals, the patterns of predicted incre-
ments exhibited pronounced pulses and generally
behaved well relative to actual population his-
tories (Figure 13).

Table 13. — Estimates of predation coefficients (Bj and fij'
and squared multiple correlation coefficients (r ) for all treated
guppy populations for specified intervals. Based on iterative
Taylor Series approximation analysis of the hypothesized model;
API = EB X exp(B,X, + B2X2). Estimates which fail to
converge ( — .Large) are not included in means.

Population

Refuge

number Weeks

(mm)

s,

B^

/•'

1 0-36

5.0

-0,0258

-0.0224

0.8286

2 0-36

5.0

- .0340

-0137

7364

3 0-36

5.0

-.0172

-.1972

.5295

4 0-36

5.0

- .0223

-.1290

.7867

5 0-58

5.0

- .0636

-.4198

.4000

6 0-58

5.0

-.0184

-.1354

,4997

9 0-36

5.0

- .0509

-.0640

,2900

10 0-36

5.0

- .0346

- 0585

.6453

11 0-36

5.0

-.0195

(-.Large)

.7671

12 0-58

5.0

- .0204

-.1137

.4270

Means: Phase 1 and long-term

controls — 5.0 mm

- .0307

-.1282

.5461

4 36-58

4.5

- .0267

-.0025

.6519

7 36-58

4.5

-.0181

- ,0088

.8022

9 36-58

4.5

- .0284

+ .0041

.7512

Means: 4 5 mm group

- .0244

- .0024

,7351

1 36-58

5.0

-.0120

-.0717

8459

3 36-58

5.0

- .0286

- ,0367

,7236

10 36-58

5.0

- .0484

-,1487

.4371

Means: 5.0 mm group

- .0297

- .0857

6689

2 36-58

5.5

- 0367

-.1523

,5103

8 36-58

5.5

- .0355

-.0494

.5890

11 36-58

5.5

- .0246

(-.Large)

.6060

Means: 5.5 mm group

- .0323

-.1009

.5684

DISCUSSION

In no earlier population experiments with
guppies have detailed analyses of numerical pop-
ulation growth been attempted. Analyses em-
ployed in this study were designed with two
purposes in mind. Comparisons of numerical
dynamics measures, while perhaps unsatisfying
to those demanding rigorous statistical tests or
parameter estimates, allowed qualitative distinc-
tions to be drawn among treatment groups and

S
U

M

O 160

F

P
0
P

u

L

A

T

I

O

N

I

N
C

R

E
M
E
N
T
S

120

80

40

0 6 12 18 24 30 36

WEEKS

Figure 13. — Sum of observed (solid line) and predicted (dots)
population increments for guppy population 4 during Phase I.

showed clear differences in the patterns and
variability of numerical population growth. Least-
squares regression techniques, while shedding no
light on the qualitative features of numerical
increase, allowed evaluation of the fit of the
hypothesized numerical dynamics model to col-
lected experimental data and also allowed esti-
mation of adult and juvenile stock predation
coefficients. That multiple regression analysis
failed to indicate as striking differences in ju-
venile predation coefficients among treatment
groups as did nonlinear least-squares regression
illustrates a strong relation between analysis
technique and analysis result. Clearly, parameter
estimates based on linear fits of a survival equa-
tion are not comparable with those obtained by
minimizing squared deviations between observed
and predicted population increments, although
the underlying numerical dynamics model and
experimental data used are identical for both
analyses. In the absence of detailed data specify-
ing the true error component of the underlying
model it is unclear which regression technique is
appropriate. Regardless of such technical issues,
all analyses support the hypothesis that altera-
tion of refuge habitat quality may significantly
change biological interactions among components
of a population. This finding is compatible with
earlier studies and also unifies the "conflicting"
results of previous studies with and without ref-
uge areas.

572

HANKIN: A MULTISTAGE RECRUITMENT PROCESS

Analyses of these experimental populations
show that there are two distinctly different com-
ponents of experimental population growth and
that these two components should be separated in
mathematical treatments of population dynamics.
Numerical growth in experimental populations is
an extremely variable population phenomenon,
only weakly predictable through convential mod-
els and statistical techniques. Total biomass
growth is a relatively invariant population pro-
cess, highly predictable, and nearly immediately
responsive to slight disturbances in food supply.
From a modeling perspective, these considera-
tions imply that population biomass growth might
be adequately described by a simple deterministic
model, such as logistic growth, while description
of numerical growth may require more complex
and perhaps stochastic models.

Description of numerical dynamics is, of course,
the province of stock-recruitment theory. Neglect-
ing the issue of the extreme variability in numeri-
cal behavior of these populations for the moment,
these experiments reveal at least two likely bio-
logical complications which may render simple
stock-recruitment theory of limited practical ap-
plication. The observed strong juvenile-fry inter-
action shows that recruitment may depend not
only on parent adult stock but also on juvenile
stock, perhaps at different times and in different
places. Simple stock-recruitment theory clearly
requires modification to account for such inter-
actions. Also, density-dependence of growth may
further compound the complexity of the recruit-
ment process. While numerical change within
sampling intervals may be adequately, although
imperfectly, described by the model developed,
eventual recruits, say in terms of adult females,
are evidently not a simple fraction of numerical
increase some fixed number of weeks previous.
Models of recruitment in fish populations have not
explicitly dealt with complications that might be
introduced by the density-dependence of year-
class growth, dependence that may occur after a
year class has been established.

The probable general effects of a strong juvenile-
fry interaction may be examined by making a few
simplifying assumptions (none of which are more
than only approximately met by guppies) and then
to recast the experimental numerical dynamics
model as a more general relation similar in form to
the simple stock-recruitment model first proposed
by Ricker (1954). These assumptions are: 1) The
expected number of births is proportional to the

number of reproductive females rather than to the
biomass of females. 2) The number of reproductive
females is proportional to the total number of
adult predators. 3) The correlation between size
and age is perfect and growth rates of individuals
are density independent. Then, letting A = num-
ber of adult predators, J = number of interacting
juveniles, and a, b^ , 6-2 = constants, the experi-
mental numerical dynamics model,

API - EB exp(BiXi + B^X^),

may be reexpressed as (using assumptions 1)
and 2)):

API = aA exp(6i A + b^J)

and if recruits are a constant fraction of numerical
increase in a given period (using assumption 3) ):

R = a' A exp(6iA + bzJ)

where a' = constant

R — "recruitment."

Three dimensions are required for visualization
of a hypothetical stock-recuitment relation incor-
porating a juvenile-fry interaction. To examine
such a relation, experimental estimates of b^
(-0.031) and of 62 (-0.160) were taken from the
mean nonlinear estimates for 5.0 mm refuge fence
populations. Based on ratios of expected number of
births to numbers of adult predators, a rough
estimate for a' was obtained (= 2) by assuming
that recruitment was determined at the end of a
sampling period. A plot of the adult-juvenile stock-
recruitment relation thus produced is given in
Figure 14.

There is a pronounced flattening of the recruit-
ment surface with increasing juvenile density. At
high juvenile density (15 on the graph), recruit-
ment is low, nearly constant, and is essentially
independent of adult stock. If such interactions
occur within populations of fish simple plots of
recruitment against adult stock would reveal
little trend at high juvenile densities. At low
juvenile densities, however, recruitment appears
strongly related to adult stock in the classic dome-
shaped manner. At low levels of adult stock
recruitment may fluctuate considerably, indepen-
dent of adult stock, as a response to high or low
juvenile densities. In general the more intense the
inhibition of fry survival rates by juveniles, the

573

FISHERY BULLETIN; VOL. 78, NO. 3

Figure 14. — Visualization of proposed
adult-juvenile stock-recruitment model.
See text for explanation.

^e/v,^'o

-2,0 py

more extreme would be the expected fluctuations
in recruitment at the same adult stock densities.
Variability in recruitment would be increased
with a decrease in adult stock, as would be caused
by fishing.

If, instead of juveniles of the same species,
juveniles (or perhaps adults) of another species
interact with fry (or larvae) in a similar manner,
one may begin to imagine the complexity of
possible "true" recruitment mechanisms in fish
populations. Standard simple stock-recruitment
relations may require more dependence of recruit-
ment on adult stock alone than is justified. In-
traspecific or interspecific interactions of the
type observed in these experimental populations
clearly create complex recruitment processes, in-
capable of even approximate description on the
basis of adult stock alone. If recruitment theory is
to be of practical significance in the management
of fish populations, it seems that the numerical
dynamics of given populations will have to be
examined as unique biological phenomena, per-
haps only rarely susceptible to standardized
mathematical descriptions such as the Ricker
stock-recruitment model.

One may, of course, deny the relevance of the
above conclusions, derived from single species
laboratory populations maintained under fixed
food supply, for the modeling of natural popula-
tions. In particular, it may be questioned whether
the extreme variability in numerical population
growth observed in experimental populations does
in fact also occur in natural populations. And it

may also be questioned whether natural popula-
tions actually exhibit such extreme response of
individual growth rates to variations in popula-
tion density. Several aspects of guppy life history
and empirical observations from natural popula-
tions together argue that experimental variation
in numerical population growth indeed has clear
parallels in natural populations. The second issue,
that concerning density dependence of growth, is
less easily resolved.

The extreme variability in numerical popula-
tion growth observed in these experimental pop-
ulations arises primarily from small population
size. This variation is inherent and depends on the
guppy reproductive cycle. Since all statistical
analyses were based on expectations of events,
and since in small populations the discrepancy
between actual outcomes of events and their
expectations may be large, statistical analysis and
prediction of numerical growth patterns were
inherently weak. For example, fry survival rate
estimates were based on the expected number of
births in a 2-wk interval rather than on actual
births which were unknown. At initiation of
populations only five adult females were present.
The initial "biweekly" sampling interval was 16 d
so the probability of an individual female deliver-
ing a brood within the first interval was 16/31 =
0.516. Since broods of females are delivered in-
dependently of one another, one may reasonably
assume that the number of broods delivered in the
first interval among five adult females was bi-
nomially distributed with parameters n ( = 5) and

574

HANKIN: A MULTISTAGE RECRUITMENT PROCESS

p ( = 0.516). The mean of this distribution, n p,
is the expected number of broods delivered in the
first period, or: 5 x 0.516 = 2.58 broods.

Further, taking the mean initial weight of adult
females to be 0.5 g, the fecundity relation predicts
an expected brood size of 11.14 fry and a possible
range of from 5 to perhaps 20/brood. Thus, the
expected number of births iEB) is: 2.58 broods
X 11.14 births/brood = 28.73 births = npu
where: u = expected outcome of a success (i.e.,
expected number per brood). But the range of
possible values for the random variable "number
of births in a biweekly interval" was from 0
(0 broods x 5 births/brood) to 100 (5 broods x
20 births/brood) births. Assuming that perhaps
70% of the fry born in the first interval survived,
since adult predator densities were very low, the
collected statistic API could have had a range
from 0 to about 70. Hence the estimated fry
survival rates could have had a range of from
0 (APLEB = 0/28.73), had no broods been de-
livered, to as high as 2.44 (70/28.73), if all five
females delivered broods. Estimated fry survival
rates at adult densities of eight or nine during the
first 4 wk reflected this possible variation in
actual numbers of broods delivered and number
of births per brood and ranged from 0 to 1.38.
Thus large variation among estimated fry sur-
vival rates at low adult densities is possible and
unavoidable if the actual number of births is
unknown.

In natural populations fluctuations in year-
class strength, the natural analog to numerical
experimental population increase, due to varia-
tion in early life survival, often range over two
orders of magnitude (Forney 1976). While the
primary causes behind such variations (often at
the same or similar stock densities) seem to be
usually environmental, unlike experimental pop-
ulations under controlled conditions, this varia-
tion seems at least equal to that observed in these
experiments. Guppy reproductive features, includ-
ing small brood size, very high but variable fry
survival, and high variability in timing of brood
delivery, are replaced in most natiu-al fish popula-
tions by high fecundity and extremely low and
variable early life survival. Thus, although under-
lying causes differ markedly, observed fluctua-
tions in numerical population growth of natural
populations at least equal those observed in ex-
perimental populations.

The striking density dependence of growth ob-
served in these populations may, however, repre-

sent an exaggeration of probable levels of growth
response to density that may exist in natural
populations. Many natural populations are prob-
ably not directly limited by their food supply, but
rather by competing species, suitable habitat for
all life stages, and/or harvest by man. Natural
population biomass may in general fall below that
which the underlying food supply could in theory
support. Also, variation in food supply would
make field observations of density-dependent
growth less striking. Finally, empirical observa-
tions suggest that such intense growth depression
with high population density is rarely a feature of
commercial fish populations. Rather, observations
of extreme stunting of fish size have been collected
from simple single species populations in many
respects analogous to the experimental popula-
tions. Stunting among high density pond and
small lake populations of yellow perch, Perca
flauescens, and eastern brook trout, Saluelinus
fontinalis , is well known. Although extreme den-
sity dependence of growth does occur in natural
populations, it seems unlikely for most exploited
populations, especially when population biomass
has been reduced to perhaps one-half of unex-
ploited levels.

SUMMARY

The ultimate interest in laboratory study of the
stock-recruitment process is to gain insight into
this fundamental problem and to apply such
insight to the study and modeling of natural
populations. These experiments illustrate that
the stock-recruitment process may involve more
than a single adult stock -related feedback control
and that more complex mechanisms may involve
interactions among several stock components.
While mathematical models of more complex
stock-recruitment processes may be constructed,
that such complex analytic models may be use-
fully applied in practice is far from clear. Two
serious application problems exist and these prob-
lems seem inherent to analysis of stock-recruit-
ment relations for any temperate species. The
time frame and economic expense necessary to
collect data suitable for statistical analysis of
possible complex stock-recruitment models and
the probably inherent variability of the recruit-
ment process argue that if, indeed, such complex
models are to be of practical use, major rethinking
of analysis and data collection approaches is
required.

Data collection during these experimental stud-

575

FISHERY BULLETIN: VOL. 78, NO. 3

ies, which allowed eventual crude prediction of
numerical population behavior, might be roughly
analogous to the following field data collection:
1) Collecting data on at least adult stock, young-of-
year, and yearling densities from 10 fish popula-
tions of the same species in similar environments
for 18 yr each. 2) Restructuring refuge area
habitats for six of the similar populations, perhaps
by removing or increasing weed cover, dramat-
ically reducing the size of all populations, and
collecting appropriate data for an additional 11 yr.
Few fishery investigators have the opportunity
to carry out such an "experiment" in a field
context. Instead, a single population may be
studied, under fortunate circumstances, for per-
haps one or two decades. Analogous replication is
impossible. Since the investigator is (usually) not
allowed to actively manipulate population age or
size structure, but must instead maintain a pas-
sive observer role, data collected in a decade might
cover only a small range of juvenile and/or adult
stock sizes. Recruited year classes, exposed to
perhaps violent fluctuations in environmental
factors influencing early life survival, might rare-
ly give any indications of a dependency of recruit-
ment on adult or juvenile densities in previous
years.

Faced with such constraints on data collection,
there seem possible several constructive alterna-
tive responses. The general passive approach may
be neither appropriate nor effective, and active
(experimental) manipulation of populations, forc-
ing collection of data not otherwise obtainable,
may be required. This approach has been advo-
cated by Walters and Hilborn (1976) although it
clearly calls for major rethinking of the fishery
biologist's role. Second, it is possible that year-
class strength and adult and other stock compo-
nents during past years may be estimated through
data extraction techniques based on simple gross
population measures, e.g., from total biomass
harvested from commercial species (Walter and
Hoagman 1975). Thus, rather than bemoaning the
slow pace at which future observations may be
gathered, one may consider past fishery data as an
untapped reservoir of information suitable for
analysis of the dynamics of recruitment. Statis-
tical evaluation of relations among such extracted
estimates does, however, raise serious analytic
and philosophic issues. Finally, comparative study
of year-class fluctuations among related species
and fisheries holds far more promise for revealing
biological mechanisms underlying recruitment

than is indicated by published literature (Regier
1978).

Since there may be constructive responses to
data collection problems, the probably inherent
high variability of the stock-recruitment process
causes the author greater concern. Although the
impact of specific environmental factors may oc-
casionally be separated from possible internal
biological controls (Nelson et al. 1977) and allow
reduction of unexplained variation in year-class
strength, it seems unlikely that a single environ-
mental variable regularly exerts significant im-
pact on year-class strength. Thus, while apparent
variation in year-class strength may be reduced
under fortunate circumstances, either by account-
ing for environmental impacts or by considering
all relevant stock components, it seems unlikely
that collected data will ever fall neatly along some
theoretical curve or surface. In general, expecta-
tions for statistical measures of goodness of fit for
stock-recruitment relations are probably grossly
unrealistic and poor fits should be expected. How
one ought to evaluate empirical stock-recruitment
fits, when the appropriate standard for compari-
son is probably not "100*7^ of variation" or a
correlation of 1, is not clear, although attention
has already focused on optimal use of unreliable
stock-recruitment parameter estimates (Walters
1975). The danger of presuming independence of
recruitment and population stock components,
however, seems far more severe than are errors of
estimation and generally unsatisfying statistical
analyses.

It is hoped that the results of these experiments
and the demonstration of a complex multistage
recruitment process will stimulate renewed inter-
est in study of the possible biological determinants
of recruitment. That simple stock-recruitment
theory may often be biologically inappropriate
seems clear But whether more complex and more
biologically realistic models of recruitment pro-
cesses, with their further demands for data collec-
tion, will prove of practical use seems far from
clear. In the author's view, at present, a wide gulf
separates stock-recruitment theory from practice.
More careful consideration of the practical use of
this body of theory and more realistic expectations
from its use are required if the theory is to achieve
its proper role in fishery management.

ACKNOWLEDGMENTS

My deep appreciation is given to the many

576

HANKIN: A MULTISTAGE RECRUITMENT PROCESS

Cornell faculty and staff who contributed to this
research. Louis Leibovitz performed needed path-
ological examinations of fish and the Levine
Laboratory for Avian and Aquatic Animal Medi-
cine allowed access to their fluorescence micro-
scope. Alfred Eipper, former Leader, New York
Cooperative Fishery Research Unit, purchased
and loaned the analytical balance which enabled
accurate measurements of weight. Douglas Rob-
son, Biometrics Unit, and William Youngs, Nat-
ural Resources, provided invaluable criticism,
encouragement, and moral support throughout
the research. Edward Raney, President, Ichthyo-
logical Associates, is thanked for his support of the
graduate program in Natural Resources and Harry
Everhart, Chairman, for considering me worthy of
this support. Thanks are also extended to James
Zweifel, Southwest Fisheries Center La JoUa
Laboratory, National Marine Fisheries Service,
NOAA, for his perceptive review of an earlier
draft, and the final paper contents reflect his
significant contributions.

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578

DISTRIBUTION AND ABUNDANCE OF HALOBATES SPECIES
(INSECTA: HETEROPTERA) IN THE EASTERN TROPICAL PACIFIC

Lanna Chenqi and Eric Shulenberger^

ABSTRACT

Halobates specimens were sorted from 1,649 surface neuston samples collected from the eastern
tropical Pacific Ocean. At least one specimen was captured in each of 498 samples. Only 34 samples
contained more than one species of Halobates. Four species, H. micans, H. sobrinus, H. sericeus, and//.
splendens, were found in the eastern tropical Pacific area. The abundance estimates (lower bounds)
range from 400 to 10,000 per km^. Detailed zoogeographical distributions of the four species are
presented. Halobates micans is a warmwater cosmopolite found between lat. 20° N and 20° S; H. sericeus
appears to be confined to the central watermasses of the North and South Pacific and does not occur in the
zonal equatorial currents; H. sobrinus, the most abundant of the four, is confined to the equatorial
upwelling regions off the west coast of Central America; and//, splendens, the rarest species, appears to
be associated with the central South Pacific watermass or the South American west coast current
system. Although there is considerable overlap in the absolute geographical ranges of the three more
abundant species, the regions in which they are abundant are almost entirely separate. Whether this is
due to biological or physical processes is unknown.

Five species of the genus Halobates Eschscholtz
(Insecta, Heteroptera: Gerridae), popularly called
marine "water striders" or "sea skaters," are
the only known insects whose normal habitat is
the high seas. These pelagic insect plankters oc-
cupy an unique, truly two-dimensional environ-
ment. They are not known to penetrate below or
rise above the surface (no winged forms are known
for any Halobates species; Cheng and Fernando
1969). Halobates spp. spend their entire life cycle
at the air-sea interface, and may therefore provide
us with an unique opportunity to use them as
biological tools for investigating air-sea and sur-
face phenomena.

The peculiar habitat of oceanic Halobates spp.
precludes their capture (except accidentally) by
standard zooplankton or water-sampling equip-
ment, and presents interesting questions of
zoogeography and in the evolution of species. The
occasional oceanic Halobates specimens found in
conventional plankton samples made with sub-
merged nets have shown that the five oceanic
species are widely distributed on a scale of ocean-
basin magnitude (Herring 1961; Savilov 1967;
Scheltema 1968; Cheng 1973a, 1974). Although
the ranges of distribution of the Pacific //a /o6ates

'Scripps Listitution of Oceanography, University of California,
La Jolla,CA 92093.

^San Diego Natural History Museum, PO. Box 1390, San
Diego, CA 92112.

Manuscript accepted February 1980.
FISHERY BULLETIN: VOL .78, NO. 3. 1980

spp. have been broadly defined by Savilov ( 1967),
there have been few data for these insects from the
southeastern Pacific; furthermore, no detailed
quantitative study has hitherto been made on the
sea skaters in the Pacific Ocean. An unique series
of surface samples collected during the EAS-
TROPAC survey enabled us to carry out an exten-
sive study ofHalobates spp. in the eastern tropical
Pacific Ocean. We present here a detailed descrip-
tion of mesoscale (several hundreds of kilometers)
zoogeographic patterns of four Halobates spp. in
the area, as well as information on abundance,
cooccurrence of species, and temperature effects
on occurrence of species.

Various aspects of the biology of Halobates spp.
are described in the literature. The taxonomy of
the genus is reasonably well understood (Herring
1961). All 42 species described are to some extent
associated with saltwater — mostly brackish
waters or nearshore marine habitats. Some are
confined to island groups or nearshore lagoons,
estuaries, or bays (Cheng 1973a; Andersen and
Polhemus 1976). Only five Halobates species (H.
micans Eschscholtz, H. sericeus Eschscholtz, H.
sobrinus White, H. splendens Witlaczil, and H.
germanus White) are truly high-seas animals.
Special adaptations of pelagic Halobates to its
peculiar habitat include: 1) an ability to lay eggs
on flotsam (Cheng 1974); 2) a cuticle with a mi-
crohair layer which traps air and prevents the

579^^

FISHERY BULLETIN; VOL. 78, NO. 3

insects from being wetted by rain, spray, waves,
and accidental submergence (Cheng 1973b; An-
dersen 1977); 3) a highly UV-absorbent cuticle,
presumably to prevent chromosomal damage
(Cheng et al. 1978); and 4) an ability to store
relatively large amounts of food as triglycerides
which their brackish-water and freshwater rela-
tives are not known to possess (Lee and Cheng
1974). To date, attempts to rear pelagic Halobates
in the laboratory have failed. Our knowledge of
these insects is thus based upon analyses of pre-
served samples and on short-term observations or
experiments carried out at sea. The present data
are from an extensive set of neuston samples taken
during the EASTROPAC investigations, which al-
lows us to examine some aspects of species dis-
tribution and cooccurrence in relatively fine spa-
tial detail.

METHODS

Present samples were collected during the
EASTROPAC project, which surveyed the eastern
Pacific between lat. 20° N and 20° S from the west
coast of the American continents to about long.
120° W. There were seven cruises between January
1967 and April 1968, each of about 2-mo duration.
Figure 1 presents areas surveyed for most of these
cruises; some cruise tracks were complex, and
areas surveyed and cruise length differed from
cruise to cruise: details of cruise tracks are avail-
able (Fishery-Oceanography Center,^ and figures
10-70 TC in Love 1972 [EASTROPAC Atlas, Vol.
1]). The results of some of the biological, chemical,
physical, and meteorological measurements have
been published in several EASTROPAC Atlases
(Love 1970-75) and elsewhere (Ahlstrom 1971,
1972; Tsuchiya 1974).

The neuston nets used to collect our samples
filter only the top few centimeters of water, but
may occasionally skip out of the water ("porpois-
ing"; see Cheng 1975a). Moreover, to some extent,
Halobates is able to detect and avoid such a net
both visually (Cheng 1973c; Cheng and Enright
1973) and by receiving tactile warnings of its ap-
proach (Wilcox 1972). Consequently, the samples
yield at best only semiquantitative data on Halo-
bates and other pleustonic organisms (Cheng
1975a).

All the samples were replicates; a 505 (xm mesh
net with a circular mouth 1 m in diameter was
towed half submerged at about 3 kn (= 1.5 m/s) for
20 min. Optimally, such a tow sweeps a path 1 m
wide and 1,800 m long. Abundance of Halobates
spp. is treated as number of individuals caught per
standard tow; such a tow covers an area of about
1 ,800 m^. However, our use of 1 ,800 m^ as the "area
per tow" is conservative, because both porpoising
and variable depth of submergence will decrease
the actual area covered. Possible avoidance by
Halobates makes our abundance estimates even
more conservative. Samples were preserved in
70% ethanol. Of 1,649 surface samples, 498 con-
tained at least one Halobates individual. A total of
3,236 individuals were identified to species
(Cheng 1975b). For each sample, we recorded the
number of adults and nymphs; nymphs were iden-
tified to developmental stage and final instar
nymphs and adults were sexed. Detailed informa-
tion on the cruise series, the total number of sur-
face tows made during each cruise, and the
number of positive tows (i.e., containing Halo-
bates) are presented in Table 1.

Table l. — EASTROPAC cruise series, number of surface tows
made, and number of tows containing //a/o6a<es spp. (1967-68).

Cruise

No. surface tows

Series

With

number

Inclusive dates

Total

Halobates spp.

11

24 Jan- 6 Mar.

120

67

12

7 Feb -24 Mar.

118

41

13

20 Jan.-31 Mar.

141

42

14

'^ 21Jan.-10Apr.

98

25

20

\ 10 Apr.-31 May.

128

52

30

■"^ 14 June- 2 Aug.

127

26 ■

47

31 July-29Sept.

156

24

45

3Aug.-25Sept.

85

32

50

16 Oct.- 3 Dec.

120

36

OP'

13 Nov.- 2 Dec.

49

9

60

18 Dec- 5 Feb.

124

31

76

19 Feb.- 5 Apr.

101

40

77

20 Jan, -28 Apr.

157

39

75

15 Feb -15 Apr.

125

34

^Fishery-Oceanography Center. 1966-69. EASTROPAC In-
formation Paper no. 1-11 (available from National Marine
Fisheries Center, PO. Box 271, La Jolla, CA 92038).

' First digit of cruise number denotes the series, except for Oceanographer
which IS a "ship of opportunity" used in series 50.

RESULTS AND DISCUSSION
Species Distributions

Worldwide distributions of oceanic Halobates
spp. have been presented by Herring (1961),
Savilov (1967), and Cheng (1973a, 1974). Updated
worldwide distributions of the four oceanic species
which occur in the EASTROPAC area are shown in
Figure 2. The general distribution of Halobates
spp. resembles known large-scale plankton dis-

580

CHENG and SHULENBERGER: DISTRIBUTION AND ABUNDANCE OF HALOBATES

130* 120* no* _L00*

30*

20*

10*

10*

20'

ROCKA/VAY-13

130*

120*

110*

100*

90'

80"

70*

Figure l. — General cruise tracks for the EASTROPAC Investigation showing basic station positions and areas covered during each
cruise. Detailed data given in Table 1; exact station positions differ slightly from cruise to cruise.

tribution patterns, e.g., the eastern tropical
Pacific, transition zone, central watermass,
warmwater cosmopolite, and equatorial distri-
butional patterns found by McGowan (1971, 1974),
Reid et al. (1978), and Brinton ( 1979). These pat-
terns seem to parallel the general surface circula-
tion of central gyres, equatorial zonal flows, and
eastern-boundary upwelling areas at the Equator
(Sverdrup et al. 1942). NoHalobates spp. is known
to occur regularly at high latitudes.

Halobates micans is clearly a cosmopolitan trop-
ical species occurring in all the world's equatorial
current regions (Figure 2). Specimens occur at

latitudes higher than about 40° (lat. 55° S, long.
45° W and lat. 52° N, long. 36° W in Figure 2a) only
where poleward extensions of strong warm sur-
face currents are known (e.g., Gulf Stream and
Kuroshio).

The North and South Pacific central gyres and
the South Atlantic central gyre do not appear to
contain H. micans in contrast to the North Atlan-
tic central gyre (Figure 2). The central North At-
lantic is more heavily sampled than any of the
other three gyres; however, there are hydrogaphic
reasons to believe that the results are valid, inde-
pendent of sampling density The Gulf Stream

581

I80«

FISHERY BULLETIN: VOL. 78, NO. 3
0°

Halobates micans <i

Figure 2. — Worldwide distributions o^Halobates species: A.H.
micans, B.H. sobrinus, C.H. sericeus, and D.H. splendens. Each
circle represents a position where at least one specimen has been
collected. (Data from Herring 1961; Savilov 1967; Scheltema
1968; Cheng 1974; and Cheng this study).

582

CHENG and SHULENBERGER: DISTRIBUTION AND ABUNDANCE OF HALOBATES

produces cold core "rings" of water which migrate
into the central North Atlantic watermass (Fu-
glister 1972; Lai and Richardson^'). These rings (as
opposed to the "cold core" within the ring) are bits
of the warm Gulf Stream. They are numerous,
physically large, temporally persistant, and are
known to carry with them large populations of

■•Lai, D. Y, and P. L. Richardson. 1977. Distribution and
movement of cyclonic Gulf Stream Rings. Tech. Rep. Ref. No.
77-1, Graduate School of Oceanography, Univ. Rhode Island,
Kingston, R.I.

organisms. Such populations may persist for
months or years ( Ortner et al. 1978). Other species
which occur primarily in the Atlantic equatorial
current system show distributions very like H.
micans, presumably as the result of occasional
captures of specimens carried by cold-core rings
(Nafpaktitis et al. 1977).

Cold core rings are also produced by the
Kuroshio Current ( Hori 1970; Kawai 1972 ). When
sufficient samples become available, H. micans
will probably show a distribution in the western
half of the North Pacific central watermass very

30°

130'

20°

10°

10°

20'

•2

!•
•I
•3
•2

•I

•25

I*
»2

8*

il8

•I
•I

•3

•I
•3

•I
•3

•2

•I

120°

100°

■x:

90°

7^

80°

70'

•I

2#2

•1,3

M.I%2XI
.,•53

12^2

!•'
I,I,7,3«L-I,I

i,5,3j;g

5,f>53
l'32,4

2%l,ll

•1,1

•3

Hal abates micans

2,'»^-^-l,i
2,1,1* ■3,1,8

^••1.2
2/1.10

H,2
!•■

• 1,8

*3
•2

•I
•I

30°

20°

0°

10°

20°

130°

120°

110°

100°

90°

80°

70°

Figure ^.—Halobates micans distribution in the EASTROR\C area, showing number of insects caught per tow. When insects were
caught in more than one tow at each station the numbers are separated by a comma. Small dots represent negative stations, large dots
are positive stations.

583

FISHERY BULLETIN. VOL. 78, NO. 3

much like that seen in the western North Atlantic.
This is because the general circulation patterns of
the North Atlantic and the North Pacific are simi-
lar, and the scattered records in the western mid-
latitudes in the North Atlantic are probably a re-
sult of the Gulf Stream.

In the eastern tropical Pacific, H. micans does
not often occur south of lat. 10° S or north of lat. 20°
N (Figure 3). The southern border of its distribu-
tion is well defined by the EASTROPAC sampling
program. The northern border could be an artifact
of that sampling program, since distributions of
both samples and the species approximately coin-

cide. However, many negative EASTROPAC sam-
ples were taken north of the edge of the species
distribution (Figure 3), a large number of Califor-
nia Current samples have also been negative for
the species (Cheng unpubl. data), and other sam-
pling programs have shown the same feature
(Figure 2). These combine to convince us that the
northern border shown in Figure 3 is not artificial.
Halobates sobrinus seems to be confined to the
equatorial upwelling regions off the west coast of
Central America, with some northward extension
along the Mexican coast (Figure 2). Although both
the North and South Equatorial Currents could

30'

130°

120°

100° 90°

20'

10°

10°

20'

Halobates sobrinus

130°

120° 110° 100° 90°

Figure 4. — Halobates sobrinus distribution, as in Figure 3.

70°

584

CHENG and SHULENBERGER: DISTRIBUTION AND ABUNDANCE OF HALOBATES

carry the species westward (Sverdrup et al. 1942),
its range shows no such effect (Figures 2, 4). More
samples from the central equatorial Pacific are
needed to confirm the apparent abrupt termina-
tion of the species' range at about long. 112° W. In
the EASTROPAC area,//, sobrinus does not occur
west of about long. 112° W or south of lat. 5° S
(Figure 4). While the ranges of//, sobrinus and//.
micans overlap somewhat, their regions of high
population density (defined as samples with ^10
individuals) overlap very little (Figure 5).

Halobates sericeus is clearly confined to the
central watermasses of the North and South

Pacific. The three records of this species on the
Equator (at long. 82° W, 119° W, and 129° W; Figure
2) appear likely to be misidentifications (data from
Herring 1961). However, present data also include
one individual which lies well outside the appar-
ent range of the species (Figure 6; at long. 100° W,
lat. 16° N) and we have reconfirmed the identifica-
tion of this specimen. Since these insects are usu-
ally <4 mm long, individuals may be carried long
distances by the wind. This could explain such
isolated captures. Halobates sericeus does not
occur in the upwelling areas of the eastern tropical
Pacific, nor in the zonal equatorial currents (Fig-

FlGURE 5.— Areas of high population densities of three Halobates species in the EASTROPAC area. "High" is defined as occurrence of

A^^IO individuals in at least one sample (area per sampe =1,800 m^).

585

30"

130°

120°

FISHERY BULLETIN: VOL. 78, NO, 3

80° 70°

20"

10°

10°

20°

•5

•3

•3

•19

•I

•II

•18

•20

•7

•7
•2
•7
7^^9-

•6.6

2«|

•6

I.I
2

)

•4

•1.4

•2

it'^

10.

• •i-7«^ie

Halobates sericeus

130°

120° 110° 100° 90°

Figure 6. — Halobates sericeus distribution, as in Figure 3,

80°

70°

ure 6). It occurs completely outside the range of//.
sobrinus (Figures 4, 5) and shows only very small
overlap with//, micans (Figures 3, 5).

Halobates splendens , rarest of the four EAS-
TROPAC species, has not been found north of
about lat. 8° N (Figure 7 ). The captures reported in
the Chile Current (Figure 2) indicate that this
species may be primarily associated with the cen-
tral South Pacific watermass or the South Amer-
ican coastal current System. Sampling in this
region is insufficient at present to permit better
definition of its range.

The distributions oi Halobates spp. appear to be

controlled by two major influences: 1) the patterns
agree with broad, general surface-circulation pat-
terns, and 2) species' regions of high abundance
generally tend not to overlap. We do not know
whether the nonoverlap is due to competitive ef-
fects or to physiological adaptations by each
species to a particular environmental regime.

Abundance

Two important difficulties in deriving quantita-
tive estimates of Halobates spp. abundance are: 1)
most neuston nets (including ours) tend to skip out

586

CHENG and SHULENBERGER: DISTRIBUTION AND ABUNDANCE OF HALOBATES

130° 120° 110° 100°

110° 100° 90°

Figure 7. — Halobates splendens distribution, as in Figure 3.

of the water in anything except calm weather,
making estimation of area sampled or volume fil-
tered difficult; and 2) these insects are known to
avoid nets but the extent of avoidance is unknown
(Cheng 1973c; Cheng and Enright 1973). However,
the samples used in this study resulted from repli-
cate tows and may therefore be reasonably com-
pared with one another and used to set lower
limits on abundance.

Our data showed that in//. micans,H. sobrinus,
and H. splendens numbers of adults are about
twice that of nymphs (Table 2). This may be a
result of several factors: 1) nymphs might avoid

the net more actively than adults (unlikely); 2)
nymphs are smaller than adults and may wash
through the meshes of the net more easily (possi-
ble); 3) nymphs might have been missed in sorting
(unlikely; samples have been rechecked); and 4)
aspects of their natural history might produce
such a distribution (e.g., heavy predation on
nymphs plus long life-span of adults). Data do not
exist to test hypotheses 1) and 4). We can offer no
explanation for the differences between H.
sericeus and the other three species.

Since//, micans and//, sobrinus accounted for
almost 909c of total individuals caught (65.6 and

587

FISHERY BULLETIN: VOL. 78. NO. 3

Table 2.

-Numbers of Halobates spp. caught in the EASTROPAC area. Roman num-
erals = nymphal instar number.

Species

Individuals

Adults

Nymphs

Numbers

per

ife stage

Adults

1

II

III

IV

V

6

9

H

micans

754

490

264

22

15

45

83

99

204

286

H

sobnnus

2,156

1,388

768

63

75

179

178

273

693

695

H

senceus

285

126

159

19

20

34

31

55

55

71

H.

splendens

77

50

27

0

5

6

8

8

20

30

23.3'^, respectively), we will confine further dis-
cussions of abundance to these two species.

In an attempt to determine if H. micans and H.
sobrinus are randomly distributed on the ocean
surface, curves of "number per tow" vs. "number of
tows with that number of insects" were compared
with Poisson probability density functions. Such
tests are appropriate for these data (Sokal and
Rohlf 1969) but difficult to perform because of un-
certainty as to how many "zero" catches should be
included in the divisor when calculating a mean
catch-per-tow Maximum likelihood estimates of
the means for truncated Poisson distributions ( i.e.,
lacking a zero class) were therefore calculated for
both species (Cohen 1960), and the frequency dis-
tributions of Figure 8 were compared with the
calculated (expected) Poisson distribution. Chi-
square tests of expected vs. observed were very
highly significant for both species (P<<0.001),
leading to the rejection of the null hypothesis that
observed distribution cannot be told from a Pois-
son. We therefore conclude that both H. micans
and H. sobrinus are nonrandomly distributed

across the ocean surface in the regions where they
occur.

The coefficient of disperson is^/x, Sokal and
Rohlf 1969) for H. sobrinus is —46.0 and for H.
micans is =5.8. We thus conclude that both species
are very strongly clumped ("patchy"),//, sobrinus
more so than H. micans. The numbers per sam-
ple also vary widely, e.g., from 0 to 179 for H.
sobrinus. It is not known what environmental fac-
tors cause one location to provide higher catches
than another. Assuming optimum sampling condi-
tions (perfect net performance, etc.), the highest
population densities calculatable for each of the
four species are presented in Table 3. These are
lower limits because of probable net avoidance

Table 3. — Highest estimates of population density for Halo-
bates spp. in the EASTROPAC area.

Maximum

observed population

Species

Max

mum no.

/sample

(no./km2)

H. micans

39

2x103

H sobnnus

179

1x10»

H- senceus

20

1x103

H. splendens

7

4x102

Figure 8. — Frequency distribution of
Halobates micans and H. sobrinus in
positive samples. The number of insects
caught per tow is plotted against the
number of tows containing that many
insects. "Zero catches" are excluded (see
text).

H micans

8 12 16 20 24 28 32 36 40
INDIVIDUALS /SAMPLE

H sobrinus

r«-^V-f

20 24

28 32 36 40 44 48 52
INDIVIDUALS /SAMPLE

56 60 70 80 100 140 ISO

588

CHENG and SHULENBERGER: DISTRIBUTION AND ABUNDANCE OF HALOBATES

behavior (Cheng 1973c; Cheng and Enright 1973).
Actual maximum densities are probably consider-
ably higher.

Cooccurrence

The incidence of cooccurrence of two or more
Halobates spp. in our samples was low. Out of 498
positive samples, only 33 contained two species
(Table 4); 1 sample had three species. This con-
firms the impression given by distributional maps
(Figures 2-7) that the various species seldom occur
together. Separation of distribution holds, even for
species with overlapping ranges (H. micans andH.
sobrinus). In those samples in which these two
species cooccur, there is no correlation of abun-
dance (Figure 9). This indicates that local varia-
tions in abundance of these two species are not
merely responses to vectorial ( i.e., physical) forces.
If vectorial forcing were the case, then the two
species should be abundant in the same samples
and be positively correlated when they cooccur.

The mean number of individuals per positive
tow (pooled for all cruises and by cruise) is much
higher in//, sobrinus than in//, micans, although
the percentage of positive tows is similar for both
species (Table 5). However, the highest frequency
of capture (i.e., percentage of positive tows) for//.
sobrinus occurred in the same series as the lowest
frequency for H. micans (Figure 10). This may
represent some temporal partitioning of re-
sources, but is undoubtedly partly a function of the
species' nonoverlapping centers of high abundance

Table 4. — Cooccurrences of Halobates spp. in 498 positive
EASTROPAC samples (at least one specimen of each species per
sample).

40 r-

Species

H. micans H. sobrinus H. sericeus H. splendens

H. micans
H. sobrinus
H. senceus
H. splendens

28

<0

10 I*

0

• •

» •

1

J

10 20 30

No. /-/. mi cons

Figure 9. — Abundance ofHalobates micans andH. sobrinus in
samples in which the species cooccurred. Abundance of the two
species is not correlated (Olmstead and Turkeys' comer test for
associativity, P>0. 05).

(Figure 5), differences in cruise tracks, and differ-
ences in times of the year (Figure 1).

Temperature Effects

Temperature of surface waters appears to be
important in the distribution of Halobates spp.
Figure 11 shows the number of individuals per
positive sample plotted against surface water
temperature for both March and August 1967.
Abundance was very low in samples taken at <24°
C and >28° C. The optimal temperature band ap-
pears to be quite narrow. The shape of these curves
is not an artifact of the number of samples ob-
tained at each temperature: the data have been
standardized to a per tow basis and there were
many tows taken at each temperature.

Table 5. — Occurrence ofHalobates micans andH. sobrinus by EASTROPAC cruise series.

H micans

H. sobrinus

Cruise

No. positive

Total no.

Mean no.

No. positive

Total no.

Mean no.

series

tows

insects

insects/tow

tows

insects

insects/tow

10

76

387

5.1

50

568

11.4

20

23

43

1.9

28

436

15.6

30

8

10

1.3

17

65

3.8

40

17

61

3.6

30

446

14.9

50

20

45

2.3

18

192

10.7

60

22

50

2.3

5

20

4.0

70

52

196

3.8

29

382

13.2

Totals

218

792

3.6

177

2.109

11.9

Positive tows. %

13.2

10.7

589

FISHERY BULLETIN: VOL. 78. NO. 3

^

-5 fU

• 30

Q

^^ 60

—

^

• 40

• 20

a>50

-

c

'c

P 40

k-

• 50

c

o

^30

-

•10

<D

•70

g-zo

-

o

• 60

(f)

H- 10

-

o

^

1 1 1

I 1 1

1

0 10 20 30 40 50 60 70
% of Samples Containing H. micans

FIGURE 10. — Percentage of samples containing Ha/o6a?es mi-
cans and//, sohrinus compared by cruise series (Table 1). Series
numbers are shown beside each point. Note inverse relationship.

CONCLUSIONS

Four pelagic species of Halobates — H. micans,
H. sericeus, H. sobrinus, and//, splendens — are
found in the eastern tropical Pacific area. Within
the EASTROPAC area, the ranges of the four species

agree well with dominant oceanic zones or do-
mains; e.g., tropical-equatorial, central water-
mass, and coastal upwelling. The worldwide dis-
tributions of the four species in the Pacific Ocean
have also been found to agree with recognized
oceanic domains (Herring 1961; Savilov 1967) al-
though at present data are still insufficient to
clearly define some boundaries, especially in the
southern tropical Pacific. Although species may
cooccur in the EASTROPAC area, geographical
regions of high abundance for H. micans, H. so-
brinus, and H. sericeus show little overlap. Our
estimates for maximum abundance (lower
bounds) for the two more abundant species, H.
micans andH. sobrinus, are 400-10, OOO/km^. This
is likely to be conservative because they can avoid
nets and because the neuston net used in our study
did not sample in an ideal manner. We found Halo-
bates to be most abundant in 24°-28° C waters. The
two abundant species showed very patchy dis-
tributions. Present temporal and spatial cov-
erages are insufficient to allow us to define possi-
ble seasonal variations in population density or
structure.

It seems clear that the distributions of Halobates
spp., inhabiting a strictly two-dimensional world,
are governed by the same oceanic processes which
shape the distributions of other marine species
that inhabit a three-dimensional world. /^

A. Series 10 (March 1967)

1-120

oi 4— I

Q.

E

co ^
~\

|2H

I'

oH-

NO. SAMPLES

16

22 24

TEMPERATURE °C

FIGURE 11. — Number of Halobates
specimens (data for all four species
combined) per positive sample vs. sea-
surface temperatures. A. Series 10,
March 1967. B. Series 40, August 1967.
(Exact dates and area covered given in
Table 1 and Figure 1.)

B Series 40 (August 1967)

NO. SAMPLES

MEAN NQ INDIVIDUALS/SAMPLE

20 22

TEMPERATURE °C

590

CHENG and SHULENBERGER: DISTRIBUTION AND ABUNDANCE OF HALOBATES

ACKNOWLEDGMENTS

This work was partially supported by the U.S.
Office of Naval Research (Codes 461, 482, 484;
contracts N00014-78-C-0697, N00014-79-C-0200,
and N00014-75-C-0152) and by the National Sci-
ence Foundation (grant OCE76-19786).

LITERATURE CITED

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1971. Kinds and abundance of fish larvae in the eastern
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- ANDERSEN, N. M.

1977. Fine structure of the body hair layers and morphol-
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ANDERSEN, N. M., AND J. T. POLHEMUS.

1976. Water-striders (Hemiptera: Gerridae, Veliidae,
etc.). In L. Cheng (editor). Marine insects, p. 187-224.
North-Holland Publishing Co., Amsterdam.

BRINTON, E.

1979. Parameters relating to the distributions of
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Cheng, L.

1973a. Halobates. Oceanogr. Mar. Biol. Annu. Rev.

11:223-235.
1973b. Marine and freshwater skaters: differences in sur-
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— 1973c. Can//a/o6ates dodge nets? I: By daylight? Limnol.

Oceanogr. 18:663-665.
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1975b. Insecta Hemiptera: Heteroptera, Gerridae, Genus
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1978. UV absorption by gerrid cuticles. Limnol.
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Cheng, L., and J. T. Enright.

1973. Can Halobates dodge nets? II. By moonlight? Lim-
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Cheng, L., and C. H. Fern.ando.

1969. A taxonomic study of the Malayan Gerridae
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Cohen, A. C, JR.

1960. Estimating the parameter in a conditional Poisson
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FUGLISTER, F C.

1972. Cyclonic rings formed by the Gulf Stream, 1965-
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1961. The genus Halobates (Hemiptera: Gerridae). Pac.

Insects 3:223-305.
HORI, S.

1970. Horizontal flow in the Kuroshio Extension area. In
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of the Kuroshio and adjacent regions, p. 61-64. Tokyo.

KAWAI,H.

1972. Hydrography of the Kuroshio Extension. In H.
Stommel and K. Yoshida (editors), Kuroshio: Physical as-
pects of the Japan Current, p. 235-352. Univ. Wash. Press,
Seattle.
" LEE, R. F, AND L. Cheng.

1974. A comparative study of the lipids of water-striders
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1970-75. EASTROPAC Atlases. 10 vol. U.S. Dep. Com-
mer., NOAA, Natl. Mar Fish. Serv., Circ. 330.
McGOWAN, J. A.

1971. Oceanic biogeography of the Pacific. In B. M. Fun-
nell and W. R. Riedel (editors). The micropaleontology of
the oceans, p. 3-74. Camb. Univ. Press, Lond.

1974. The nature of oceanic ecosystems. In C. B. Miller
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State Univ. Press.

NAFPAKTiTis, B. G., R. H. Backus, J. E. Craddock, R. L.
Haedrich, B. H. Robison, and C. Karnella.

1977. Family Myctophidae. In R. H. Gibbs, Jr. (editor-in-
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13-265. Sears Found. Mar Res., Yale Univ Mem. 1.

Ortner, P B., P H. wiebe, L. H.\ury, and S. Boyd.

1978. Variability in zooplankton biomass distribution in the
northern Sargasso Sea: the contribution of Gulf Stream
cold core rings. Fish. Bull., U.S. 76:323-334.
REID, J. L., E. BRINTON, A. FLEMINGER, E. L. VENRICK, AND J.
A. MCGOWAN.

1978. Ocean circulation and marine life. In H. Chamock
and Sir George Deacon (editors). Advances in oceanog-
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Savilov, a. I.

1967. Oceanic insects of the genus Halobates (Hemiptera,
Gerridae) in the Pacific. Oceanology 7:252-261.

SCHELTEMA, R. S.

1968. Ocean insects. Oceanus 14(3):9-12.
SOKAL, R. R., AND F J. ROHLF.

1969. Biometn,'. The principles and practice of statistics in
biological research. W. H. Freeman, San Franc, 776 p.

SVERDRUP, H. U., M. w. Johnson, and R. H. Fleming.

1942. The oceans. Their physics, chemistry and general
biology Prentice Hall, N.Y, 1087 p.
Tsuchiya, M.

1974. Variation of the surface geostrophic flow in the east-
ern intertropical Pacific Ocean. Fish. Bull., U.S.
72:1075-1086.
WILCOX, R. S.

1972. Communication by surface waves. Mating behavior
of a water strider (Gerridae). J. Comp. Physiol. 80:255-
266.

591

OCCURRENCE, MOVEMENTS, AND DISTRIBUTION OF
BOTTLENOSE DOLPHIN, TURSIOPS TRUNCATUS, IN SOUTHERN TEXAS

Susan H. Shane*

ABSTRACT

Boat and land observations of free- ranging bottlenose dolphins, Tursiops truncatus, near Port Aransas,
Texas, provided data on seasonal occurrence, daily movements, and individual distribution patterns.
Censuses revealed that the winter population in the study area was twice the size of the summer
population. Individual dolphins were variously identified as summer residents, winter residents, or
year-round residents in the study area. There was a significant relationship between dolphin move-
ments and tide in some sections of the study area. Dolphins consistently moved against the ebb tide and
sometimes against the flood tide in these sections. Time of day was significantly related to dolphin
movements in a few sections of the study area. Part or all of the study area was included in the home
ranges of several individually recognizable dolphins.

Only three long-term studies of free-ranging At-
lantic bottlenose dolphins, Tursiops truncatus,
have been conducted (Wiirsig and Wiirsig 1977,
1979; Hogan^; Irvine et al.^). Bottlenose dolphins
in Texas have been studied only opportunistically
by Gunter (1942, 1943, 1951). Lack of detailed in-
formation on free-ranging T. truncatus provided
an incentive for a 1-yr study of bottlenose dolphins
in southern Texas. This paper presents data on
seasonal occurrence, daily movements, and indi-
vidual distribution patterns of dolphins in the
study area.

METHODS

The study area was located near Port Aransas,
Texas, (lat. 27°50'15" N; long. 97°02'45" W) and
included seven sections (Figure 1). Aransas Pass is
the shipping outlet into the Gulf of Mexico for the
Port of Corpus Christi. The next open pass through
which dolphins could enter or leave the Gulf is
Cedar Bayou, a natural pass, located 37 km to the
northeast. Sections 1, 2, and 6 are dredged to a

'Department of Wildlife and Fisheries Sciences, Texas A&M
University, College Station, TX 77843; present address: National
Fish and Wildlife Laboratory, 412 N.E. 16th Avenue, Gainesville,
FL 32601.

''Hogan, T. 1975. Untitled draft of M.S. thesis. Unpubl.
manuscr, 42 p. Univ. Rhode Island, Kingston.

^Irvine, A. B., M. D. Scott, R. S. Wells, J. H. Kaufmann, and W.
E. Evans. 1979. A study of the activities and movements of
the Atlantic bottlenosed dolphin, Tursiops truncatus, including
an evaluation of tagging techniques. Available National Tech-
nical Information Service, 5285 Port Royal Road, Springfield, VA
22151 as PB-298 042.

depth of 14 m and are all used by large tankers and
a variety of other boats. Sections 3 and 7 are
dredged to a depth of 5 m and are used by commer-
cial and sport fishing boats, barges, and pleasure
boats. Sections 4 and 5 average 2-3 m deep and are
frequented only by small fishing boats. The entire
study area covers approximately 34 km^.

Between 1 June 1976 and 31 May 1977, I spent
1,065 h observing dolphins, either from a 4 m Bos-
ton Whaler'* or from land. Opportunistic observa-
tions were made from June through December
1977. Uniquely marked dorsal fins (Wiirsig and
Wiirsig 1977) were used to identify 21 individual
dolphins, and these individuals provided informa-
tion on distribution and seasonal movements.

I defined the seasons as follows: 1) summer,
June- August; 2) fall, September- November; 3)
winter, December-February; 4) spring, March-
May. Initially, air and water temperatures from
the U.S. Coast Guard Station at Port Aransas
were used, but after 1 December 1976 I collected
these data at the beginning of each day in a harbor
off Aransas Pass. Mean air and water tempera-
tures were 28.2° and 28.4° C for summer 1976, 18.7°
and 18.8° C for fall 1976, 1L2° and 1L4° C for winter
1976-77, and 22.5° and 22.7° C for spring 1977.

Zigzag censuses, conducted an average of four
times (range = 0-9) per month in each section of
the study area, were used to estimate population
size. A zigzag census was conducted by piloting the

•'Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

Manuscript accepted January 1980.
FISHERY BULLETIN: VOL. 78. NO. 3, 1980.

593

FISHERY BULLETIN: VOL. 78, NO. 3

Figure l. — Bottlenose dolphin study area near Port Aransas, Texas. Circled numbers designate the seven sections of the study area:
1) Aransas Pass, 2) the Confluence, 3) Lydia Ann Channel, 4) Corpus Christi Bayou, 5) Morris and Cummings Cut, 6) Corpus Christi
Channel, and 7) Aransas Channel. The boundaries of the study area are the ends of the jetties at the southeast end of section 1, the
mouth of Aransas Bay to the northeast, the mouth of Corpus Christi Bay to the southwest, and the islands along the northwest border of
sections 4 and 5. The zigzag line drawn through section 3 shows the path followed while conducting zigzag censuses of dolphins. Similar
paths were followed while censusing dolphins in the other sections.

boat at slow speed back and forth through a sec-
tion and counting all dolphins sighted (Figure 1).
A total of 335 zigzag censuses was conducted dur-
ing 201 h during the 1-yr study. The average time
per census was 23.9 min for Aransas Pass, 11.0 min
for the Confluence, 55.7 min for Lydia Ann Chan-
nel, 28.3 min for Corpus Christi Bayou, 63.5 min
for Morris and Cummings Cut, 52.6 min for Cor-
pus Christi Channel, and 25.6 min for Aransas
Channel.

Data on direction of dolphin movement, tidal
state, and time of day were used to identify daily
movement patterns. The terms used to describe

direction of movement in sections 1, 3, and 6 are
"up" for movement toward the bays and "down" for
movement toward the Gulf of Mexico. Time of day
is divided into three periods: early (0700-0900 h),
midday (1000-1300 h), and late (1400-1900 h). Very
few observations were made from 2000 to 0600 h,
so this time period is not considered. The chi-
square test was used to determine whether there
was a significant relationship between dolphin
movements and tide and time of day. When a rela-
tionship was found to be significant (P<0.01), the
strength of the relationship was measured by
Cramer's V (Nie et al. 1970).

594

SHANE: OCCURRENCE AND DISTRIBUTION OF BOTTLENOSE DOLPHIN

RESULTS

Seasonal Occurrence

Seasonal occurrence patterns were derived from
seasonal variation in dolphin numbers and from
observations of individual dolphins. The monthly
mean number of dolphins in the study area varied
from a low of 48 in October (range = 8-104) (the
September low is inaccurate because no zigzag
censuses were conducted in some sections) to a
high of 164 in January (range = 65-281) (Figure
2). Dolphin abundance declined from summer to
fall, rose in the winter, and declined again in the
spring. Boat and land observations from August
through December 1977 showed the same pattern
as the previous fall and early winter: dolphin
numbers declined noticeably in early fall and then
increased to higher than summer numbers in
November and December.

Sightings of identifiable dolphins confirmed a
seasonal occurrence in the study area. Sixteen of
the 19 recognizable dolphins in the study area
were seen on 5 or more days and were identified by
the fifth month of the study. The other three dol-

280-

240

200

160

o
a

° 120

o

Z

80

40

1

■J-

J J A S O N D
Month

F M A M

Figure 2. — Mean number of Atlantic bottlenose dolphins
counted in the study area near Port Aransas, Texas, for each
month from June 1976 through May 1977. Ranges are indicated
by the vertical lines. The September count is unreliable because
an insufficient number of censuses were conducted that month.

phins were seen on <5 d or were not identified
until the eighth month of the study. Three patterns
of seasonal occurrence in the study area were
demonstrated by the 16 dolphins (Table 1). Four
individuals (Thick Fin, Jagger, Notched Fin, and
Short Triangle) were predominantly spring and
summer residents: over 6(¥7c of the days each was
seen in the study area occurred during spring and
summer and <409c occurred during fall and
winter. Five individuals (Lumpy, Cloud, Bent Fin,
Twin, and Tiki) were predominantly fall and
winter residents: over 60% of the days each was
seen in the study area occurred during fall and
winter and <40'7f occurred during spring and
summer. The remaining seven dolphins spent ap-
proximately the same amount of time in the study
area during spring and summer as during fall and
winter.

My observations from June through December
1977 confirmed the seasonal occurrence pattern of
some dolpins established during the 1-yr study.
Lumpy, a fall and winter resident who had been
seen only between 20 November 1976 and 2 Feb-
ruary 1977, was seen again on 1 and 3 December
1977. Bent Fin, a fall and winter resident who was
seen regularly from October 1976 through Feb-
ruary 1977 and then only on 3 d through November
1977, was again sighted in the study area on 5 and
8 December 1977. I saw Thick Fin (spring and
summer resident) in the study area frequently
from June 1977 to 8 September 1977 but never
after that through December 1977, when I left the

Table l. — Seasonal occurrence of 16 bottlenose dolphins in the
Port Aransas, Texas, area. Percentage of days each dolphin was
seen during each season and each spring and summer (Sp/S)
period and fall and winter (F/W) period are given. Individual
dolphin occurrence patterns suggested the spring-summer and
fall-winter links. Dashes indicate that the dolphin was not iden-
tified until after that season.

Total days
sighted

Percentage of total days

Dolphin

Sp

S

F

W

Sp/S

F/W

Thick Fin

70

36

46

17

1

82

18

Jagger

5

20

60

20

0

80

20

Notched Fin

9

0

67

22

11

67

33

Short Triangle

86

31

35

29

5

66

34

Lumpy

10

0

—

30

70

0

100

Cloud

23

9

13

22

57

22

79

Bent Fin

38

5

18

24

53

23

77

Twin

13

31

—

15

54

31

69

Tiki

28

29

7

18

46

36

64

Nicky

8

25

25

0

50

50

50

Trigger

18

50

—

28

22

50

50

Chopper

46

24

24

22

30

48

52

Teaser

27

48

—

19

33

52

48

Raggedy Ann

33

33

12

12

42

45

54

V-TIp

9

44

11

33

11

55

44

Snaggle Tooth

21

33

24

24

19

57

43

595

FISHERY BULLETIN: VOL. 78, NO. 3

area. Poff ^ reported that Thick Fin remained pre-
dominantly a spring and summer resident and
Bent Fin primarily a fall and winter resident in
the study area through midsummer 1979.

Daily Movements

Field observations indicated that tide and time
of day influenced the movement patterns of dol-
phins in some sections of the study area. Most
apparent was the tendency of dolphins in the lower
sections of the study area ( 1, 3, and 6 on Figure 1) to
move up against an ebb tide. The most apparent
time of day effect occurred in Morris and Cum-
mings Cut (section 5) where dolphins moved
northward early in the day, all directions at mid-
day, and southward late in the day.

The chi-square test showed that tide and direc-
tion of movement were significantly related
(P<0.0001) in the lower section of the study area
(sections 1, 3, and 6 combined) at three separate
periods of the day (early, midday, late) and at all
times of day combined. At all time periods most
dolphins moved up during ebb tide. During flood
tide most dolphins moved down, although many

moved across the channel or randomly. The associ-
ation between tide and direction of movement was
strongest early (V - 0.513) and weakest at midday
(V — 0.297) with intermediate values late (V =
0.410) and at all times combined (V = 0.407). Di-
rection of movement and tide were significantly
related in four of the six sections of the study area
considered (Table 2).

The relationship between direction of move-
ment and time of day also proved significant in
four out of six sections under some conditions (Ta-
ble 3). The observations on dolphin movements in
Morris and Cummings Cut were quantitatively
confirmed, and the association between direction
of movement and time of day was stronger in that
section than in any other section (see Cramer's V
values in Table 3).

The frequency of sightings of groups of dolphins
was calculated for all of the conditions presented
in Tables 2 and 3. In all cases where the relation-
ship between the variables was significant (chi-
square P<0.01), the group sighting data con-
formed with the individual sighting data.

Individual Distribution Patterns

*M. Poff, Research Assistant, University of Texas, Marine Sci-
ence Institute, Port Aransas, TX 78373, pers. commun. July
1979. (Deceased.)

Sightings of each recognizable individual were
confined to a specific portion of the study area
rather than distributed randomly throughout the

Table 2. — Relationship between direction of movement and tide proved significant (chi-square P<0.01) in
four sections of the Port Aransas, Texas, study area at certain times of day. Numbers in the table represent
frequency of individual dolphin sightings. Cramer's V indicates strength of the relationship between the
two variables, and each V is comparable with every other V.

Tidal stages at selected times of day

Early

Midday

Late

All times

Section

Ebb

Flood

Ebb

Flood

Ebb

Flood

Ebb

Flood

Aransas Pass (1) direction:

Up

613

54

347

56

182

83

1,165

194

Down

65

200

179

80

35

74

283

357

Across/ random

126

153

92

31

27

43

245

227

Chi-square

459.06

28.53

50.73

422.07

Cramer s V

0.616

0.191

0.338

0.413

Corpus Christi Channel (6) direction:

Up

513

77

205

186

296

153

1,035

416

Down

86

202

70

360

33

227

192

789

Across/random

305

226

191

348

123

228

632

802

Chi-square

291.02

119.36

203.15

642.81

Cramer's V

0.454

0.296

0.438

0.408

Lydia Ann Channel (3) direction:

Up

329

57

380

93

20

21

729

171

Down

13

47

59

48

5

27

77

126

Across/random

114

58

178

44

6

25

298

127

Chi-square

115.43

33.05

11.749

154.59

Cramer's V

0.432

0.203

0.336

0.318

Morris and Cummings Cut (5) direction:

North

30

28

Not

12

9

149

153

South

0

16

significant

0

99

165

250

Across/random

33

0

0

10

146

112

Chi-square

M7.183

'68.620

18.90

Cramer's V

'0.664

'0.727

0.139

' Insufficient data in a given case made the chi-square test potentially invalid.

596

SHANE: OCCURRENCE AND DISTRIBUTION OF BOTTLENOSE DOLPHIN

Table 3. — Relationship between direction of dolphin movement and time of day was significant (chi-
squareP<0.01) in four sections of the Port Aransas, Texas, study area during a few tidal stages. Numbers
in the table represent frequency of individual dolphin sightings. Cramer's V indicates the strength of
the relationship between the two variables, and each V is comparable with every other V.

Time of day

at selected tida

1 stages

Ebb

Flood

All tides

Section

Early

Midday

Late

Early

Midday

Late

Early

Midday

Late

Aransas Pass (1) direction:

Up

613

347

182

54

56

83

740

501

390

Down

65

179

35

200

80

74

398

386

175

Across/ random

126

92

27

153

31

43

385

165

148

Chi-square

116.78

73.97

62.41

Cramer's V

0187

0.219

0.097

Corpus Christi Channel (6) direction:

Up

513

205

296

77

186

153

775

567

648

Down

86

70

33

202

360

227

506

724

310

Across/random

305

191

123

226

348

228

781

763

501

Chl-square

46.74

18.029

145.71

Cramer's V

0.113

0.067

0.114

Lydia Ann Channel (3) direction:

Up

329

380

20

57

93

21

494

750

72

Down

13

59

5

47

48

27

125

190

60

Across/random

114

178

6

58

44

25

260

425

90

Chl-square

'27.335

14.717

49 50

Cramer's V

'0.111

0.132

0.100

Morns and Cummlngs

Cut (5) direction

North

30

107

12

28

116

9

330

857

54

South

0

165

0

16

135

99

85

684

537

Across/ random

33

113

0

0

102

10

182

1.038

165

Chl-square

'69.059

104.46

737 32

Cramer s V

'0.274

0.318

0.306

' Insufficient data in a given case made chl-square test potentially invalid.

study area. Thick Fin and Raggedy Ann used
separate but adjacent portions of the study area
(Figure 3). Teaser used a portion of the study area
which included most of Thick Fin's portion and all
of Raggedy Ann's portion (Figure 3).

The portions of the study area used by Thick Fin
and Raggedy Ann were designated Region A and
Region B. Region A encompassed Aransas Pass,
the Confluence, Lydia Ann Channel, and Corpus
Christi Channel. Five dolphins, including Thick
Fin, were sighted 80% or more of the time in this
region (Table 4). Region B covered Morris and
Cummings Cut, and three dolphins, including
Raggedy Ann, were seen SS'Ji or more of the time
there (Table 4). These three Region B dolphins
consistently traveled in a large group of usually 20
or more dolphins which moved into and out of the
study area through Corpus Christi Bay. Two dol-
phins. Teaser and Cloud, were observed often in
both Regions A and B, and their sightings covered
20 km2 and 25 km^.

In addition to the 19 identifiable dolphins in the
study area, two recognizable individuals, South-
paw and Half Fin, were sighted only in the Gulf of
Mexico. Other dolphins with unique dorsal fins
were seen in the gulf whenever observations were
made there. These T. truncatus from the Gulf of
Mexico were sometimes seen within meters of

Aransas Pass, but they entered the study area
only rarely and briefly.

As discussed earlier, many dolphins inhabited
the study area on a seasonal basis. Observations of
some individuals indicated their possible locations
when they left the study area. On 22 February
1977 I saw Short Triangle traveling up Aransas
Pass toward the bays at 11:07 a.m. and traveling
down the Pass to the Gulf at 12:35 p.m. Although I
made continuous observations for the remainder
of the day from the shoreline of the Pass, I did not
resight Short Triangle. On 18 October 1976 I saw
Thick Fin entering the Gulf of Mexico; after that
and until mid-March 1977,1 saw Thick Fin only on
18 November 1976 and 25 January 1977. On 29
June 1979, Gruber^ sighted Thick Fin 50 m off the
Port O'Connor, Texas, jetties in the Gulf of Mexico,
100 km northeast of Port Aransas. I was able to
confirm the sighting from photographs taken by
Gruber. Port Aransas ferry operators, familiar
with Thick Fin, reported to Gruber that they had
seen Thick Fin on 24 June and again on 22 July.
Bent Fin entered and left the study area through

^J. Gruber, graduate student. Department of Wildlife and
Fishery Sciences, Texas A&M University, College Station, TX
77843, pers. commun. July 1979.

597

FISHERY BULLETIN: VOL. 78, NO. 3

Figure 3. — Distribution of sightings of three bottlenose dolphins (Thick Fin, Raggedy Ann, and Teaser) near Port Aransas, Texas,
during 1976-77 . The map is a diagram (not drawn to scale) of the study area shown in Figure 1, and the circled numbers identify the same
seven sections of the study area given in Figure 1.

Table 4. — Sightings of individual bottlenose dolphins in in-
shore waters near Port Aransas, Texas. Only dolphins sighted 25
or more times from June 1976 through May 1977 are included.
Region A includes Aransas Pass (1), the Confluence (2), Lydia
Ann Channel (3), and Corpus Christi Channel (6) (total area, 11
km^). Region B includes Morris and Cummings Cut (5) (total
area, 14 km^).

Individual
(total no.
sightings)

No. sightings

in
Region A (%)

No. sightings

in
Region B (%)

No, sightings

outside Regions

A and 6

Thick Fin (140)
Short Triangle (142)
Snaggle Tooth (28)
Bent Fin (64)
Tngger (25)

140 (100%)

139 (98%)

26 (93%)

57 (89%)

20 (80%)

0
0

1 (4%)
3 (5%)
1 (4%)

0

3 (2%)
1 (4%)

4 (6%)
4 (16%)

Raggedy Ann (36)
Tiki (33)
Chopper (52)

2 (6%)
4 (12%)

3 (6%)

32 (89%)
29 (88%)
47 (90%)

2 (6%)

0

2 (4%)

Teaser (28)
Cloud (33)

13 (46%)
21 (64%)

15(54%)
8 (24%)

0

4 (12%)

the northeast boundary where Lydia Ann Chan-
nel joins Aransas Bay.

DISCUSSION

Seasonal Occurrence

Contrary to Gunter (1942), the present study
provides evidence for seasonal variation in abun-
dance of T. truncatus in Texas. As Figure 2 shows,
the winter population in the study area was about
twice the size of the summer population. The popu-
lation increased or declined during the fall and
spring as dolphins moved into or out of the study
area. Irvine et al. (footnote 3) noted fewer dolphins
in their study area in central west Florida during
the winter than during the summer. They also
observed seasonal changes in the distribution of
bottlenose dolphins in that area. Seasonal migra-
tions have been hypothesized for T. truncatus on
the Atlantic coast (True 1890), and Caldwell and
Caldwell (1972) noted variations in abundance of

598

SHANE; OCCURRENCE AND DISTRIBUTION OF BOTTLENOSE DOLPHIN

T. truncatus in northeastern Florida on a seasonal
basis. Wiirsig (1978) found no evidence for a sea-
sonal migration of T. truncatus in Argentina.

The belief that the seasonal variation in abun-
dance of bottlenose dolphins in the study area was
an annual occurrence and not a result of the un-
usually cold winter of 1976-77 was supported by
my 1977 fall and winter observations. Later obser-
vations on the seasonal presence of Thick Fin and
Bent Fin in the study area by Poff (footnote 5)
further substantiated the first year's data.

Bottlenose dolphins in the Port Aransas area
responded to seasonal changes by emigrating out
of the study area for the winter, immigrating into
the study area for the winter or by remaining
year-round residents. Hogan (footnote 2) and True
(1890) reported the first and third patterns for T.
truncatus in the Atlantic.

The three responses to seasonal changes exhib-
ited by dolphins in the study area prohibit a simple
explanation of seasonal occurrence patterns. Two
factors cited as affecting cetacean distribution are
water temperature (Gaskin 1968) and food avail-
ability (Mercer 1975). Water temperature in the
study area changed from a winter mean of 11.4° C
to a summer mean of 28.4° C, and this change
could have had a direct or indirect effect upon
dolphin movements. Food is available to dolphins
both in the study area and in the Gulf of Mexico
during the winter: most fish species emigrate from
the bays to the Gulf for the winter, but a few
species spend the winter in the bays ( Gunter 1945).
Three of the latter species — striped mullet, Mugil
cephalus; sand trout, Cynoscion arenarius; and
black drum, Pogonias cromis — have been found in
the stomachs of bottlenose dolphins ( Gunter 1942).
Other fish species wintering in the bays near Port
Aransas were killed by cold spells during the win-
ters of 1940 and 1951 (Gunter 1941; Gunter and
Hildebrand 1951). Of these, spot, Leiostomus
xanthurus; croaker, Micropogon undulatus;
sheepshead, Archosargus probatocephalus; spot-
ted trout, C. nebulosus; pinfish, Lagodon rhom-
boides; and ribbonfish, Trichiurus lepturus, are
eaten by T. truncatus (Gunter 1942; Kemp'). If
water temperature and food availability influence
the seasonal occurrence of dolphins in the study
area, individual dolphins or social groups may
have different temperature or food preferences.

Daily Movements

Dolphins generally move against the tide in the
lower sections of the study area, although they
moved against the ebb tide more consistently than
they moved against the flood tide (Table 2). In all
other studies where cetacean movements and tides
were correlated, cetaceans moved with tidal cur-
rents (Irvine and Wells 1972; Norris et al. 1977;
Irvine et al. footnote 3; Wiirsig^). Tide was sig-
nificantly related to dolphin movements in only
one case in the upper section of the study area, and
the strength of the relationship there was weak ( V
= 0.139). In two other cases where tide and direc-
tion were significantly related in the upper section
of the study area, insufficient data made the chi-
square results potentially invalid. This lack of
tidal effect for the upper bays agrees with the
observation that gray whales moved with tidal
currents in channels but ignored tidal flow in bays
(Norris et al. 1977).

Dolphins consistently moved against the ebb
tide in Aransas Pass where the strongest ebb tides
were slightly stronger (2.5 km/h) than the
strongest flood tides (2.4 km/h) (Smith 1979) and
where there was a net outflow averaging 0.3 km/h
(Smith 1978). Dolphins showed little or no consis-
tency in their tide-related movements in Morris
and Cummings Cut where inflow and outflow
should be approximately equal in strength and net
effect (Smith 1978). The tidal data indicate that
dolphins respond to the dominant tidal currents in
this area by moving against them, and that their
movements are less affected by tide in areas where
tidal effects are diluted such as in the upper bays.

Two explanations for the movement of dolphins
against tidal flow seem possible. First, the coun-
tercurrent movement may represent a method of
feeding. Dolphins may catch fish more easily when
the fish are swimming with or being carried by the
current. The possible increase in feeding efficiency
might outweigh the energy expenditure required
to move against a strong current. There is evi-
dence that more fish move through Aransas Pass
during ebb tides than during fiood tides: "The dif-
ference in catch [of fishes in Aransas Pass] be-
tween flood tide collections and ebb tide collections
was tremendous. Few specimens were collected
during flood tide, although the tide trap was low-

'Kemp, R. J. 1949. Report on stomach analysis-
Delphininae. Annual Report of the Marine Laboratory of the
Texas Game, Fish and Oyster Commission for the fiscal year
1948-1949. Unpubl. manuscr., p. 111-112, 126-127.

^Wiirsig, B. 1976. Radio tracking of dusky porpoises
(Lagenorhynchus obscurus) in the south Atlantic, a preliminary
analysis. In FAO-ACMRR Scientific Consultation on Marine
Mammals, Bergen, Norway, p. 1-21.

599

FISHERY BULLETIN: VOL. 78, NO. 3

ered for almost as many flood tide collections as
ebb tide." (Copeland 1965). Thus, dolphins may
have developed a special technique for taking ad-
vantage of the concentration of food which appar-
ently occurs in Aransas Pass during ebb tide. A
second possibility is that dolphins which maintain
a stationary position against a strong tidal cur-
rent, as dolphins were frequently observed to do,
were resting. Resting captive dolphins reportedly
face against the current in the tank and use slow
beats of the fluke to maintain position (McBride
and Hebb 1948).

The relationship between time of day and dol-
phin movements was stronger in Morris and
Cummings Cut than in the lower sections of the
study area (Table 3). The observation that most
dolphins moved northward early, all directions at
midday, and southward late in the day was sub-
stantiated statistically (Table 3). The higher
Cramer's V" values for the time of day-direction
relationship as compared with the tide-direction
relationship indicated that time of day influenced
direction of movement more than tide did in Mor-
ris and Cummings Cut.

The agreement between individual and group
movement data in the present study showed that
group size was not a significant variable. In con-
trast, Irvine et al. (footnote 3) found that more
dolphins moved with the tide than against it, be-
cause group sizes were larger for dolphins moving
with the current. They found approximately the
same number of groups moving against the tide as
with it.

In summary, dolphin movements were signifi-
cantly related to tide and time of day in some
sections of the study area. The relationship with
tide was strongest in Aransas Pass where tidal
effects were most pronounced and resulted in a net
outflow. The relationship with time was strongest
in Morris and Cummings Cut where tidal effects
were diluted.

Individual Distribution Patterns

The concentration of sightings of individual
dolphins in portions of the study area (Figure 3,
Table 4) indicated that some individuals included
parts of the study area in their home ranges (as
defined by Burt 1943). Caldwell (1955) provided
the first evidence for T. truncatus having a home
range. Later, Caldwell and Caldwell (1972) pro-
posed a dumbbell-shaped home range for T. trun-
catus which included two home ranges connected

by a traveling range. At least two interpretations
of my data are possible: each dolphin had one home
range that extended outside of the study area, and
some dolphins used different portions of their
home ranges on a seasonal basis; or each dolphin
had two or more home ranges connected by travel-
ing ranges, and one home range partially or com-
pletely coincided with the study area and was used
seasonally. Irvine and Wells (1972) and Saayman
et al. (1973) indicated that the bottlenose dolphins
which they studied exhibited localized move-
ments, but did not specify home ranges. Wells et al.
(in press) defined a home range of 85 km^ for the
dolphin herd which they studied, and they stated
that it was inhabited year-round by at least some
of the dolphins.

Eight of the 10 dolphins whose distributions
were considered in Table 4 apparently recognized
a boundary between Regions A and B. The bound-
ary might have been a physical feature (e.g., deep
channels versus large, shallow bays), or it might
have been a social barrier separating social
groups. Two dolphins. Teaser and Cloud, passed
over the apparent boundary between Regions A
and B on a regular basis. Segregation according to
sex in the two regions is unlikely because Short
Triangle, Raggedy Ann, and Teaser were females
and used Region A, Region B, and Regions A and
B, respectively.

Southpaw and Half Fin and the other dolphins
with unique dorsal fins that were observed only in
the Gulf of Mexico may be part of a population of
T. truncatus that is socially or otherwise segre-
gated from inshore T. truncatus. The existence of
offshore T. truncatus has been discussed (Mitchell
1975; Odell et al.^). However, it is not known
whether offshore and inshore T. truncatus are
reproductively isolated and, if they are, why
this is so.

The February 1977 sightings of Short Triangle
and the October 1976 sighting of Thick Fin indi-
cated that they may have spent the winter in the
Gulf of Mexico or in other bay systems reached by
traveling through the gulf. The June and July
1979 sightings of Thick Fin at Port Aransas and
Port O'Connor showed that T. truncatus does move
long distances in fairly short periods of time. Wiir-
sig and Wiirsig (1977) documented a round-trip
movement of 600 km for T. truncatus, but this

>'Odell, D. K., D. B. Siniff, and G. H. Waring (edi-
tors). 1975. Final report: Tursiops truncatus assessment
workshop. Rosenstiel School of Marine and Atmospheric Sci-
ences, University of Miami, Miami, Fla., 141 p.

600

SHANE: OCCURRENCE AND DISTRIBUTION OF BOTTLENOSE DOLPHIN

movement occurred over a 15-mo period. The ob-
servations of Bent Fin entering and leaving the
study area indicated that he may have inhabited
the bays north of the study area during the spring
and summer.

ACKNOWLEDGMENTS

I am grateful to Pat Parker and Oswald Roels of
the University of Texas, Marine Science Institute,
Port Aransas Marine Laboratory, for providing
the research boat, gas, oil, and maintenance. Di-
rect financial support was received from the
Marine Mammal Commission, the Rob and Bessie
Welder Wildlife Foundation, and the Graduate
College of Texas A&M University. Thanks go to
Blair Irvine, Bernd Wiirsig, Michael Scott, Galen
Rathbun, David Schmidly, and an anonymous
Fishery Bulletin reviewer for exhaustively critiqu-
ing several versions of the manuscript. Howard
Kochman provided invaluable assistance with the
statistical and computer analyses.

LITERATURE CITED

Burt, W. H.

1943. Territoriality and home range concepts as applied to
mammals. J. Mammal. 24:346-352.

Caldwell, D. K.

1955. Evidence of home range of an Atlantic bottlenose
dolphin. J. Mammal. 36:304-305.
CALDWELL, D. K., AND M. C. CALDWELL.

1972. The world of the bottlenosed dolphin. J. B. Lippin-
cott Co., Phila., 157 p.
COPELAND, B. J.

1965. Fauna of the Aransas Pass Inlet, Texas. I. Emigra-
tion as shown by tide trap collections. Publ. hist. Mar.
Sci. Univ. Tex. 10:9-21.
Gaskin, D. E.

1968. Distribution of Delphinidae (Cetacea) in relation to
sea surface temperatures off eastern and southern New
Zealand. N.Z. J. Mar. Freshwater Res. 2:527-534.
GUNTER.G.

1941. Death of fishes due to cold on the Texas coast, Jan-
uary, 1940. Ecology 22:203-208.

1942. Contributions to the natural history of the bottle-
nose dolphin, Ti/rsiopsirw«ca^ws( Montague), on the Texas
coast, with particular reference to food habits. J. Mam-
mal. 23:267-276.

1943. Letter to the editor. J. Mammal. 24:521.

1945. Studies on marine fishes of Texas. Publ. Inst. Mar.

Sci. Univ. Tex. 1:1-190.
1951. Consumption of shrimp by the bottle-nosed dol-
phin. J. Mammal. 32:465-466.
GUNTER, G., AND H. H. HiLDEBRAND.

1951. Destruction of fishes and other organisms on the

South Texas coast by the cold wave of January 28-Feb-
ruary 3, 1951. Ecology 32:731-736.
Irvine, B., and R. S. Wells.

1972. Results of attempts to tag Atlantic bottlenosed dol-
phins (Tlirsiops truncatus). Cetology 13:1-5.

mcbride, a. e, and D. O. hebb.

1948. Behavior of the captive bottle-nose dolphin, Tlirsiops
truncatus. J. Comp. Physiol. Psychol. 41:111-123.

Mercer, M. C.

1975. Modified Leslie-DeLury population models of the
long-finned pilot whale iGlobicephala melaena) and an-
nual production of the short-finned squid (///ex illece-
brosus) based upon their interaction at Newfoundland.
J. Fish. Res. Board Can. 32:1145-1154.

Mitchell, E. (editor)

1975. Review of biology and fisheries for smaller ceta-
ceans. Report and papers from a meeting of the Sub-
committee on Smaller Cetaceans, International Whaling
Commission, in Montreal, April 1-11, 1974. J. Fish. Res.
Board Can. 32:889-983.

NiE, N. H., C. H. HULL, J. G. JENKINS, K. STEINBRENNER, AND
D. H. BENT.
1970. Statistical package for the social sciences.
McGraw-Hill, N.Y., 675 p.

NoRRis, K. S., R. M. Goodman, B. Villa-Ramirez, and L.

HOBBS.

1977. Behavior of California gray whale, Eschrichtius
robustus. in southern Baja California, Mexico. Fish.
Bull., U.S. 75:159-172.

Saayman, G. S., C. K. Tayler, and D. Bower.

1973. Diurnal activity cycles in captive and free-ranging
Indian Ocean bottlenose dolphins (Tursiops aduncus
Ehrenburg). Behaviour 44:212-233.

Smith, N. E

1978. Long-period, estuarine-shelf exchanges in response
to meteorological forcing. In J. C. J. Nihoul (editor).
Hydrodynamics of estuaries and Qords, p. 147-159. Pro-
ceedings of the 9th International Liege Colloquium on
Ocean Hydrodynamics, (Elsevier Oceanogr. Ser. 23).
Elsevier Sci. Publ. Co., Amsterdam.

1979. Tidal dynamics of low-frequency exchanges in the
Aransas Pass, Texas. Estuaries 2:218-227.

TRUE, E W.

1890. Observations on the life history of the bottlenose
porpoise. Proc. U.S. Natl. Mus. 13:197-203.
WELLS, R. S., A. B. Irvine, and M. D. Scott.

In press. The social ecology of inshore odontocetes. In L.
M. Herman (editor), The behavior of dolphins. Wiley-
Interscience, N.Y.
WURSIG, B.

1978. Occurrence and group organization of Atlantic
bottlenose porpoises {Tursiops truncatus) in an Argentine
Bay Biol. Bull. (Woods Hole) 154:348-359.

WURSIG, B., AND M. WURSIG.

1977. The photographic determination of group size, com-
position, and stability of coastal porpoises (Tursiops trun-
catus). Science (Wash., D.C.) 198:755-756.

1979. Behavior and ecology of the bottlenose dolphin , Tur-
siops truncatus, in the South Atlantic. Fish. Bull., U.S.
77:399-412.

601

REPRODUCTION OF NORTHERN ANCHOVY, ENGRAULIS MORDAX,

OFF OREGON AND WASHINGTON

Joanne Lyczkowski Laroche and Sally L. Richardson'

ABSTRACT

Mean relative fecundity of 21 anchovies from the northern subpopulation off Oregon and Washington
was 826 ±49 oocytes per g ovary-free body weight, or 720 ±40 oocytes per g total body weight. These
estimates are higher than those for the central subpopulation and may represent a racial difference
between the two subpopulations. Sexual maturity is not reached in most anchovies off Oregon and
Washington until the third summer (age II). The smallest anchovies found in spawning condition were
104 mm (male) and 107 mm (female) standard length. Overall male and female ratio of anchovies before
and after spawning was about 1:1, but males outnumbered females 2.6;1 in regions of active spawning.
Degeneration and apparent reduced growth among yolked oocytes prior to and after release of one
batch of oocytes may limit the number of anchovy spawnings per season off Oregon and Washington.

Ovarian maturation is described from direct observations of whole oocytes including both normally
developing and degenerating oocytes and from oocyte size-frequency distributions.

Sexually mature and immature anchovies off Oregon and Washington are segregated during the
summer spawning season with mature fish occurring offshore beyond the continental shelf and
immature fish occurring in nearshore coastal waters, bays, and estuaries. In winter and spring
anchovies of all sizes occur together in nearshore coastal waters.

The northern anchovy, Engraulis mordax Girard,
occurs along the west coast of North America from
Cape San Lucas, Baja California, to the Queen
Charlotte Islands, British Columbia (Miller and
Lea 1972; Hart 1973). Within this range three sub-
populations (northern, central, and southern)
have been defined based on meristic characters
(McHugh 1951) and blood serum proteins (Vroo-
man and Paloma^). The central subpopulation, in-
habiting the general region between San Fran-
cisco, Calif., and Punta Baja, Calif., currently
supports major fisheries and has been extensively
studied (see most recent review, Huppert et al.^).
The northern subpopulation, inhabiting the re-
gion north of San Francisco to British Columbia,
supports only minor seasonal bait fisheries (Hup-
pert et al. footnote 3) and has been little studied
(Richardson in press).

In 1975 we initiated a study to assess the size of
the stock of E. mordax occurring off Oregon and
Washington by egg and larva survey Knowledge of

'School of Oceanography, Oregon State University, Corvallis,
Oreg.; present address: Gulf Coast Research Laboratory, East
Beach Drive, Ocean Springs, MS 39564.

^Vrooman, A. M.. and R A. Paloma. 1975. Subpopulations
of northern anchovy, Engraulis mordax mordax. Southwest
Fish. Cent., NMFS, NOAA, Adm. Rep. LJ-75-62, 10 p.

^Huppert, D., H. Prey A. MacCall, G. Stauffer, and O. Mathi-
sen. 1977. First draft — Anchovy fishery management
plan. 119 p. + append. Pacific Fishery Management Council,
526 S.W Mill St., Portland, OR 97201.

individual fecundity (the number of eggs matured
as a group and spawned at one time) is essential
for this method of stock assessment. Three previ-
ous estimates of northern anchovy fecundity, one
for the northern subpopulation off British Colum-
bia (Pike 1951) and two for the central subpopula-
tion (MacGregor 1968; Hunter and Goldberg 1980)
differed widely in methods and results. Pike's es-
timate of fecundity based on counts of all oocytes
>0.20 mm was 1,369 oocytes/g total body weight.
MacGregor 's estimate based on counts of only the
most advanced, nonhydrated, yolked oocytes
(^0.50 mm) was 574 oocytes/total body weight,
and Hunter and Goldberg's estimate based on
counts of ripe, hydra ted oocytes was 389/g ovary-
free body weight.

This study was prompted by the discrepancy
between estimates of northern anchovy fecundity
in the northern and central subpopulations and
the general lack of information on other aspects of
northern anchovy reproduction off the Oregon-
Washington coast. Our primary objective was to
determine anchovy fecundity in the northern sub-
population. Additional objectives were to examine
length and age at sexual maturity, sex ratio,
spawning frequency, ovarian maturation, sea-
sonal gonadal condition, and patterns in geo-
graphic distribution related to the reproductive
cycle.

Manuscript accepted January 1980.
FISHERY BULLETIN: VOL. 78. NO. 3, 1980.

603

FISHERY BULLETIN: VOL. 78, NO. 3

METHODS

All collections of juvenile and adult northern
anchovies used in this study were made off the
Oregon-Washington coast, 1975-77 (Table 1, Fig-
ure 1). Because no commercial anchovy fishery
exists in this region our sampling for northern
anchovies was exploratory in nature and re-
stricted by available vessel and gear facilities,
most of which were not specifically designed for
efficient capture of pelagic schooling fishes. In the
field, fish were either frozen in plastic bags or
preserved in 10% Formalin.'* In the laboratory, fro-
zen fish (=1,400) were thawed, blotted on paper
towels to remove excess moisture, measured (to
nearest millimeter standard length, SL), and
weighed (to nearest 0.1 g). Fish were slit open and
sex and stage of gonadal development were re-
corded. Both otoliths were removed and placed in a

''Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

scale envelope for later age determination. Pre-
served fish ( =700) were soaked in freshwater, blot-
ted on paper towels, measured, and weighed. The
paired gonads were then removed and stored in 5%
Formalin. These were later weighed (wet weight)
to the nearest 0.1 mg on a Mettler electronic bal-
ance.

General gonadal condition was determined
using the criteria of Lagler (1956). Northern an-
chovies taken in March, May, and October before
and after the spawning season were classified as
immature or mature, depending on whether eggs
or milt were grossly apparent. Fish taken in July
during the spawning season were classified as
either immature (no eggs or milt grossly visible),
ripe ( gonads firm, eggs and milt distinctly visible),
or spent (gonads flaccid, often dark in color). Spent
female anchovies were further characterized by
the absence of oocytes in the posteriormost region
of each ovary. No attempt was made to distinguish
the spent condition in males or stages of recovery
after spawning in either sex. A gonadal index (GI)

Table l. — Collection data for juvenile and adult northern anchovies, Engraulis mordax, off Oregon and Washington, 1975-77. ((Jear
abbreviations: ST — shrimp trawl, MST — modified shrimp trawl, IKMT — Isaacs-Kidd midwater trawl, OT — otter trawl, MOT — mod-
ified otter trawl, MCPT — modified Cobb pelagic trawl.)

Sampling effort

Date

Gear

No. tows

Tow duration (mm)

Sampling location

Results

28 April 1 975

10 m MOT

2

13 May

5 & 8 m ST

8

25-29 May

1.8 m IKMT
7mOT

32

30 May

5 & 8 m ST

8

21-25 July

1.8 m IKMT
7mOT

53

15 Aug.

5 m ST
Gill net

8
2 sets

3-8 Oct.

1.8 m IKMT
7mOT

72

7-16 Mar. 1976 12.5m MST

25-27 May

1.8 m IKMT

7mOT

9-11July

Dipnet

19-22 July

1.8 m IKMT

18-26 July 1977 40 m MCPT

52

53

36

11

14

5

5-40

5

10-20

5
=30

10-15

30

10-15

10-20

30

Columbia River moutti just inside
north jetty and near buoy 1

Off Columbia River mouth, buoys
1 and 2

Off Columbia River mouth, light-
ship to North Head, between
lat. 46°22' and 46°10' N and
long. 124°22' and 124° 09' W,
20-91 m

Off Columbia River mouth,
buoys 1 and 2

Off Columbia River mouth, lightship
to North Head, inside 91 m contour

Columbia River mouth, just inside south
jetty and off Gearhart, Oreg. (3.7
km south of mouth)

Columbia River mouth, inside river along
north shore to Tongue Pt. (3.7 km from
mouth) and offshore between lightship
and North Head inside 91 m contour

Columbia River to Coos Bay, Oreg
=91-183 m, on commercial shrimp
grounds

Oft Columbia River mouth, 20-91 m

= 120-140 km off Newport, Oreg.

Between Columbia River and Tillamook
Bay, 120-157 km offshore

Off Oregon- Washington coast between lat
47' and 43'" N and long 124°38' and
126° 32.8' W from= 18.5 to 175-1- km
offshore, trawl depth usually 15-20 m

0 anchovies

=500 anchovies, 95% juveniles,

<100 mm SL
Thousands of anchovies, 50-170

mm SL, most captured in OT

on or near bottom in daytime

at lat. 46° 16.6' N, long. 124°10.9' W,

33-35 m
=200 anchovies, mostly juveniles,

52-123 mm SL
=700 anchovies, mostly juveniles, 70-90 mm

SL, in small schools near surface at night

(few mature fish and none in spawning

condition)
2 anchovies, <100 mm SL

Thousands of anchovies, only juveniles
(60-90 mm SL) in nver near surface, botfl
juveniles and small adults (102-126 mm
SL) offshore near bottom and in midwater

Thousands of anchovies, =70-140 mm SL —
most abundant between Astoria Canyon
and Tillamook Bay

Thousands of anchovies, =50-170 mm SL,
most in midwater, greatest catches in
24-27 m

31 adult anchovies, 104-134 mm SL, most in
spawning condition (only caught at night)

14 adult anchovies, 108-134 mm SL, most
in spawning condition, small schools of fish
observed near surface around ship

=640 adult anchovies, 105-147 mm
SL, many in spawning condition, taken only
at four stations north of lat. 45°41 ' N
between 65 and 1 20 km offshore

604

LAROCHE and RICHARDSON: REPRODUCTION OF NORTHERN ANCHOVY

48° —

46'

44'

42° —

40'

126"

124°

122°

Figure l. — General region of the northeastern Pacific where
EngrauUs mordax from the northern subpopulation have been
collected.

was calculated for preserved fish by dividing total
gonad w^eight by body weight (before gonad re-
moval) and multiplying the resultant value by
100.

Oocytes from preserved ovaries were measured
to the nearest 0.02 mm at 50 x magnification with
an ocular micrometer in a dissecting microscope.
Oocyte diameter was measured until oocytes be-
came elliptical in shape, then length (longest di-
mension) was measured. Measurements were
made of approximately 200 oocytes/ maturing fish
(with oocytes S20.14 mm) and 100 oocytes/
immature fish (with oocytes ^0.14 mm). Fish were
then grouped into 10 stages of ovarian develop-
ment, depending on the modal length of the
largest and most advanced group of oocytes in the
ovary (Clark 1934) (Table 2). The size intervals
used to define these ovarian stages were arbitrar-
ily chosen and do not necessarily represent actual
physiological stages of maturation. Composite
oocyte size-frequency distributions based on all
anchovies in each stage of ovarian development
were derived from the mean number of oocytes in
each 0.02 mm size class.

Table 2. — Ten stages of ovarian development in Engraulis
mordax based on modal length of the most advemced oocytes and
the length interval containing the mode.

Stage of Location of mode

ovarian of advanced

development oocytes (mm)

Stage of

ovarian

development

Location of mode
of advanced
oocytes (mm)

1

<0.20

6

0.60-0.68

2

0.20-0.28

7

0.70-0.78

3

0.30-0 38

8

0.80-0.88

4

0.40-0.48

9

0.90-0.98

5

0.50-0.58

10

>1.00

Fecundity estimates were based on counts of
only the largest and most advanced oocytes ( vary-
ing with stage of ovarian development) in three,
wet weighed subsamples from the central region of
the left, preserved ovary. Chi-square tests of inde-
pendence indicated no significant difference
(P>0.05) in oocyte size-frequency distribution
among three different regions, anterior, central,
and posterior, within the left ovary or between the
central regions of either ovary. Each subsample,
consisting of a clump of oocytes, was lifted from the
ovary with a forceps and weighed to the nearest 0.1
mg. Subsample weights ranged from 10 to 50 mg.
Oocyte counts were made under a dissecting mi-
croscope after the subsample had been teased
apart in water. Each subsample yielded an esti-
mate of fecundity expressed as total number of
advanced oocytes contained in the ovaries,
number of advanced oocytes per gram total body
weight, and number of advanced ooctyes per gram
ovary-free body weight. The mean of these sub-
samples provided the fecundity estimate for each

605

FISHERY BULLETIN: VOL. 78, NO. 3

of 21 northern anchovies. Functional (geometric
mean) regressions (Ricker 1973) were used to
examine relationships between total fecundity
and body weight (grams), standard length (mil-
limeters), and ovary weight (grams). These re-
gression equations can also be used for prediction
of fecundity from body weight and standard
length. The standard error of each (geometric
mean) regression coefficient was obtained by tak-
ing the square root of the variance as calculated
from Ricker (1973). Ricker also gave procedures to
transform functional parameters to predictive if
this is desired.

Photomicrographs of oocytes in various stages of
development were taken at magnifications of 12.5,
21, or 25 X through a dissecting microscope using
transmitted light.

RESULTS

Length and Age at Sexual Maturity

Estimates of the size when northern anchovies
reach sexual maturity were determined from ob-
servations of gonads from frozen fish collected in
May (991 fish) and July (263 fish) 1975. Estimates
of age were based on counts of annuli, the interface
between an inner hyaline and outer opaque zone,
on otoliths (Collins and Spratt 1969; Spratt 1975)
but only data on ages I and II fish are reported
here. Otoliths of anchovies collected in May and
July with either a hyaline margin but no com-
pleted annulus or an annulus at the margin were
considered to be age I. Northern anchovies from
May and July with one completed annulus on their
otoliths and a hyaline margin were considered to
be age II.

All fish, <85 mm SL, taken in May (376) were
immature. Both mature and immature fish were

found within the size range 85-128 mm SL. Of 79
fish between 85 and 100 mm SL, 69% were imma-
ture and 31% were mature. Of 205 fish between 101
and 120 mm SL, only 5% were immature and 95%
were mature. Only 3 out of 147 fish between 120
and 128 mm were immature and all fish >128 mm
SL were mature.

Of 183 age I fish taken in May and measuring
55-99 mm SL (x = 75 mm SL) only 5 males, 84-96
mm SL, appeared to be mature. Yet of 263 age I
fish measuring 56-94 mm SL ix = 76 mm SL),
collected in July during the spawning season,
none were mature. Possibly gametes begin to de-
velop in adolescent northern anchovies early in
the season but then do not reach the final stages of
maturation required for spawning. Hickling
(1930, 1935) reported this phenomenon in adoles-
cent hake, Merluccius merluccius, from the North
Atlantic. Of 14 age II northern anchovies from
May (sex was not recorded), 7 were immature and
7 were mature. The smallest northern anchovies
observed in spawning condition in July were 104
mm SL (male) and 107 mm SL (female). Ages are
not available for these fish. This evidence indi-
cates attainment of sexual maturity in some
northern anchovies by age II.

Gonadal Condition

General gonadal development was measured in
both immature and mature northern anchovies by
mean monthly gonadal indices (Table 3). Mean
GFs of immature males between 86 and 100 mm SL
and females between 96 and 100 mm SL increased
between March and May indicating some gonadal
growth and differentiation. By July GI's in these
size groups were lower than in May indicating no
further gonadal development had occurred. Mean
GI's of mature fish, >101 mm SL, increased from

Table 3. — Mean gonadal indices (GI) by month for male (M) and female (F) Engraulis mordax in different size (standard length)

intervals (N = no. offish).

Item

81-85

mm

86-90

mm

91

■95 mm

96-100

mm

101-

110 mm

111-

120 mm

121-

130 mm

■131

mm

Month

M

F

M

F

M

F

M

F

M

F

M

F

M

F

M

F

March

N

3

3

10

8

5

12

8

4

14

25

27

28

9

19

1

4

May

GI
N

0.22
9

1.12
9

025
4

099

7

0.20
9

1.08
6

0.36
5

1.20
2

0.48
23

1.18
9

0.68
20

1.24
6

1.22
10

1.55
9

0.64
16

1.70
36

June
July

GI

N

GI
N

032

0.45

0.77

0.57

1 52

1.07

3.06

3.60

5.10

3.57

5.43

2.68
"1

5.21

4.21

7.21

5.30
1

1 1

4

9

3

4

8

3

2

7

4

26

4.77
15

38

23

13

5.64
21

October

GI
N

0,08
4

032
10

009
4

039
2

0.11

1

0.43
3

0.59

0.55
1

7.75
4

10 92

7.53
3

1077

820
1

11.66

885

10.62

GI

0.07

0.52

0.05

0.50

0.04

0.40

0.43

0.11

0 18

0.14

606

.AROCHE and RICHARDSON: REPRODUCTION OF NORTHERN ANCHOVY

March through July. October GFs were the lowest
values observed in mature fish. Only in May were
the GI values of males higher than those of
females. The highest mean GFs were observed in
July, approximately midway through the spawn-
ing season, mid-June to mid- August, (Richardson
1973, footnote 5; Richardson and Pearcy 1977). The
highest, 22.90 (female) and 15.39 (male), and low-
est, 1.55 ( female ), individual values of the GI found
in July indicated the presence of both running ripe
and spent fish, respectively.

Sex Ratio

The male to female ratio of mature and imma-
ture northern anchovies before spawning in May;
immature, nonspawning, fish in July; and mostly
immature fish in October did not deviate signifi-
cantly from 1:1 (P>0.05; chi-square test for good-
ness of fit) (Table 4). The sex ratio of 506 northern
anchovies taken in March was 1.2:1 which, al-
though close to 1:1, was significantly different
iP<0.05). The overall male to female ratio of ma-
ture fish caught during active spawning in July at
four different locations was 2.6:1. Values for each
catch were 2:1 (167 fish), 8.3:1 (278 fish), 1:1 (186
fish), and 5.7:1 (40 fish). The sex ratios in those
catches where males outnumbered females all de-
viated significantly from 1:1 (P<0.005) and may be
related to anchovy spawning behavior. In the
three catches where males greatly outnumbered
females, the percent of ripe females with hydrated
oocytes which were either actively spawning or
about to spawn ranged from 33 to 46*;^ . In the catch
with a 1:1 sex ratio, only 2% of the females were
ripe with ovaries full of hydrated oocytes.

Ovarian Maturation

Oocyte Morphology

The smallest oocytes visible at 50 x magnifica-
tion were roughly spherical but by 0.20 mm were
becoming elliptical in shape (Figure 2a). Most oo-
cytes <0.38 mm lacked yolk and were transparent.
Vitellogenesis became evident only in oocytes
>0.38 mm. As yolk production continued, oocytes
became more opaque and by 0.50 mm the nucleus

Table 4. — Male to female ratios of northern anchovies collected
in March, May, July, and October off Oregon and Washington.

Month

N

Male

: female ratio

Size

range (mm SL)

March

506

1.2:1

72-140

May

163

0.9:1

53-162

July:

Nonspawning

247

1.2:1

56-94

Spawning

646

2.6:1

104-147

October

115

0.7:1

58-126

^Richardson, S. L. 1977. Abundance, distribution and sea-
sonality of larval fishes collected 2 to 11 km of Yaquina Bay,
Oregon from January 1971-August 1972 — a data sum-
mary Oreg, State Univ Sea Grant Coll. Prog. Publ, ORESU-
T-77-003, 73 p.

was obscured. Most oocytes >0.50 mm were com-
pletely opaque, and oocytes between 0.50 and 0.68
appeared dark in transmitted light (Figure 2b).
Oocytes between 0.70 and 0.90 mm often appeared
less dense and dark than smaller yolked oocytes. A
general lightening occurred first at the poles and
then throughout the oocyte. These oocytes were
grainy in appearance because globules of yolk had
replaced the single amorphous yolk mass of small-
er oocytes. The yolk of hydrated oocytes, ranging
in size from 0.90 to 1.42 mm, was segmented (Fig-
ure 2c). Hydration, the accumulation of fluids of
lower specific gravity than seawater in ooc3^es,
results in greatly increased volumes and is the
final stage of oocyte maturation in many marine
fishes ([Fulton 1898] in Leary et al. 1975; Smith
1957 ). The largest oocytes ( 1.10-1.42 mm) in Figure
2c had been ovulated, i.e., released from their folli-
cles, and were lying loose in the ovary. The
shadowy areas among the opaque oocytes to the
left of the transparent ones in this figure are
empty follicles. These structures were dispersed
throughout the ovary and were visible without the
aid of histological techniques. They appeared as
thin, flattened mats of tissue about the size and
shape of ripe oocytes with a thinner, oval region in
the center.

In addition to normally developing oocytes, de-
generating or atretic oocytes were found in some
anchovy ovaries collected before, during, and after
the spawning season. Atresia has been observed in
both immature oocytes undergoing vitellogenesis
and mature oocytes remaining in the ovary after
spawning in many teleosts (Wallace 1903; Matth-
ews 1938; Hoar 1955; Vladykov 1956; Beach 1959;
Barr 1968). Degenerating oocytes of all sizes inE.
mordax most frequently appeared as opaque, ir-
regularly shaped, masses dispersed among the
normal yolked and yolkless oocytes (Figure 3a).
Another type of abnormal and presumably de-
generating oocyte was found primarily in fish with
ripe oocytes. These medium-sized, 0.36-0.54 mm,
oocytes were in early stages of vitellogenesis and
had irregularly shaped nuclei which frequently
appeared partially collapsed (Figure 3b). Within

607

FISHERY BULLETIN: VOL. 78, NO. 3

KZT^

Figure 2. — Photomicrographs of normally developing, ovarian oocytes from Engraulis mordax. a. Yolkless oocytes, ranging from 0.14
to 0.28 mm length, from a northern anchovy captured in March ( x25). b. Yolked (opaque) and yolkless (transparent) oocytes from a
northern anchovy captured in June ( xl2.5). c. Ovulated oocytes (right) and empty follicles (arrows left) from a northern anchovy
captured in July ( xl2.5).

608

LAROCHE and RICHARDSON: REPRODUCTION OF NORTHERN ANCHOVY

iS

■i"\ i» • jjw

Figure 3. — Photomicrographs of degenerating ovarian oocytes from Engraulis mordax. a. Degenerating oocytes (arrows) from a
northern anchovy captured in July ( x25). b. Degenerating oocytes with abnormal nuclei (arrows) from a ripe northern anchovy
captured in July ( x25). c. Degenerating oocytes (arrows) from a northern anchovy captured in May ( x25). d. Degenerating ripe oocytes
(arrows) from a northern anchovy captured in July (xl2.5).

more mature, degenerating oocytes the yolk ap-
peared mottled and often the outline of the oocyte
was irregular (Figure 3c). Ripe, ovulated oocytes
that were degenerating differed from normal ones
primarily in the appearance of the yolk. Instead of
the honeycomblike, segmented yolk of normal
oocytes, yolk in degenerating, ripe oocytes was
either a solid opaque mass, or was dispersed into

individual globules that looked like oil droplets
(Figure 3d).

Oocyte Size-Frequency Distributions

Oocyte growth was traced through the compos-
ite size-frequency curves of 51 northern anchovies,
representing nine stages of ovarian development,

609

FISHERY BULLETIN. VOL. 78, NO. 3

to

o
o
o

o

UJ
CD

3

that were arranged in increasing order of matur-
ity (Figure 4). Only fish taken in March and May
before the spawning season were used for the
curves of stages 1-8, although fish in these stages
were taken in other months. Stage 10 fish, charac-
terized by the presence of hydrated oocytes, were
taken only in July. Few oocytes in the 0.90-0.98
mm size range were seen and no stage 9 fish were
found. This apparent break in size distribution
was caused by rapid hydration of oocytes during
final maturation to ripe oocytes >0.90 mm. The
increase in oocyte size during hydration is illus-
trated by the comparison of oocyte size distribu-
tions in stage 10 fish before and after ovulation
(the release of oocytes from their follicles just prior
to spawning) (Figure 5).

The most mature group of oocytes first began to
form a distinct mode in stage 4 ovaries. Secondary
modes of early yolked oocytes also appeared in
stage 4 and were present in stages 5 through 10 but
one of these groups never separated from the yolk-
less oocytes to form a distinct intermediate mode.
These same groups of early yolked oocytes, espe-
cially the mode between 0.45 and 0.50 mm, were in
essentially the same position in the oocyte size
distributions of spent and ovulated stage 10 fish
(Figure 5).

At least two stages of oocyte maturation prior to
hydration were indicated by two modes in the
size-frequency distributions of all completely
opaque oocytes in weighed subsamples from two

1 o^o ooooooooooo
o^o'C o' d d o d d — ■ — — ■ — '
OOCYTE LENGTH (mm)

o o

ii4

16
8

-

''K>

A

A/

^

STAGE 10
unovulated

A

K

July
N't

-

K]:6

H
t3 8

o
o

f

%

^

\

STAGE 10
unovulated

\

^

July

-

Li. U

O 16

3 r^

-

V

/

V

A-

STAGE 10
ovulated

^^

July

1

16
8
0

-

1 1 1

1

1

^

SPENT

SI 1 1 1

1 1 "

July
N-3

0<3- O

C\J

OO o

o
o

o

o

o
in
o

o o o o

ID ^- 00 (T>

o O o o

o o
o -

o o

O O
^ IT)

OOCYTE LENGTH (mm)

Figure 4. — Composite oocyte size-frequency curves represent-
ing nine stages of ovarian development in Engraulis mordax. (N
= no. offish.)

Figure 5. — Composite oocyte size-frequency curves from north-
em anchovies in ovarian stage 10, before and after ovulation, and
in spent condition. (A^ = no. offish.)

610

LAROCHE and RICHARDSON: REPRODUCTION OF NORTHERN ANCHOVY

mature northern anchovies (130 and 141 mm SL)
captured in July (Figure 6). Four maturation

CO

UJ

I-
>-

o
o

50 -
45 -
40 -
35-
30 -
25 -
20

15

10

5

0

UJ

m

-ih

40

35

30

25

20
15
10 -
5 -
oIa-

STAGE 7

\<

'm

I30mm SL
24 July 1975
N=486

!»
^

m",

iK

'\:M;.ik^:MA.X>'\X<:

..i >y '.-J

ji

•3J

STAGE 8

v\

•i>

'.vT tV

■-^m.-

w%

141 mm SL
24 July 1975
N=4I7

^

ro

O

d

00 U3

^ IT)

d d

CD

d

CJ

o

CO

d

(D
00

d

OOCYTE LENGTH (mm)

Figure 6. — Size-frequency histograms of all completely opaque
oocytes in weighed subsamples from two northern anchovies, one
in ovarian stage 7 and one in ovarian stage 8. (N = total number
of oocytes measured.)

stages among yolked oocytes were found in E.
japonicus after inspection of histological prepara-
tions, a more precise method, which were found to
coincide with stages of ovarian development based
on oocyte size composition (Usami 1963). At 50 x
magnification the general appearance of oocytes
from the two mature, northern anchovies was the
same but inspection of the size distributions indi-
cated two groups. In the 130 mm fish, two modes of
oocytes were apparent but not distinctly separate.
But in the 141 mm fish, after additional growth the
mode of larger oocytes became distinct and were
probably ready to undergo hydration and ovula-
tion subsequent to spawning.

Fecundity

Estimates of fecundity were made on only the
ripest northern anchovies, ovarian stages 6-10,
captured in July during the spawning season
when recruitment of yolked oocytes to the most
advanced mode was nearly complete (Table 5).
Fish in stages 6-8 used for fecundity determina-
tions had not spawned recently as evidenced by
the absence of empty follicles or degenerating ripe
oocytes in their ovaries. Oocytes in stage 10 fish
had not been ovulated yet; therefore, none had
been lost because of spawning or handling during
capture.

The mean total fecundity of 21 northern an-
chovies was 16, 826± 1,563 oocytes, and mean rela-
tive fecundity was 720 ±40 oocytes/g total body
weight or 826±49 oocytes/g ovary-free body

Table 5. — Data for 21 female northern anchovies, Engraulis mordax, collected off the Oregon-Washington coast in July
1975-77 used to estimate fecundity. Gonadal index (1) and relative fecundity (1) were calculated using body weight + ovary
weight. Gonadal index (2) and relative fecundity (2) were calculated using ovary-free body weight.

Collection
year

Standard
length

(mm)

Body
weight

(g)

Ovary

weight

(9)

Gonadal

index

(1)

Gonadal

index

(2)

Ovarian
stage

Total
fecundity

Relative

fecundity

(1)

Relative

fecundity

(2)

Size range of

advanced oocytes

(mm)

1975

130

23,83

1.1733

4.92

5.18

7

10,409

437

459

=0.56-0.78

141

28.60

2.1407

7.48

8.09

8

14,561

510

550

0.68-0.90

1976

110

16.07

0.9072

5.65

5.98

6

9.514

592

628

0.58-0.70

129

24.24

1.8615

7.68

8.32

7

20,766

857

928

0.60-0.76

1977

115

17.86

3.2030

17.93

21.85

10

12.426

696

848

1.13-1.40

117

16.33

1.5167

929

10.24

7-8

17,039

1,044

1,151

0.63-0.83

117

21.11

48348

2290

29.70

10

17,712

839

1,088

1.08-1.33

118

15.47

0.8538

5.52

5.84

7

8.694

562

595

0.63-0.78

120

20.29

1.0179

5.02

5.28

7-8

12,294

606

638

0.65-0.83

120

18.57

2.8745

15.48

18.30

10

10,922

588

696

1.18-1.38

120

20.22

2.5489

12.61

14.43

10

8,673

429

491

1.13-1.38

120

17.77

3.3445

18.82

23.18

10

13.813

777

957

0.95-1.25

124

22.68

3.6194

15.96

18.99

10

15,089

665

792

1.03-1.23

124

21.60

3.3617

15.56

18.43

10

13,369

630

733

1.02-1.22

127

23.63

1.7524

7.42

8.01

7-8

19,451

823

889

0.68-0.85

127

23.44

4.7776

20.38

25.60

10

19,623

837

1,052

1.03-1.28

128

23.57

1 .0465

4.44

4.65

6-7

14,157

601

629

0.60-0.78

133

29.90

5.9563

2084

24.88

10

22,012

736

919

1.05-1.31

139

3037

2.2317

7.35

7.93

7

28,235

929

1,003

063-0.75

140

31.37

6.2765

20.01

25.02

10

29.035

926

1,157

0 92-1.18

147

34 53

3.2000

9.27

10.21

7-8

35.561

1,030

1.135

0.68-0.85

611

FISHERY BULLETIN: VOL. 78, NO. 3

weight (Table 6). These two expressions of relative
fecundity were calculated to allow comparisons
with results of previous studies and to illustrate
how each method might bias fecundity estimates.
Mean relative fecundity based on total body
weight of fish in ovarian stages 6-8 and 10 was
similar. But mean relative fecundity based on
ovary-free body weight in these two groups dif-
fered by nearly 100 oocytes. Because oocyte hydra-
tion substantially increases ovary weight in ripe
fish, the best (least biased) estimate of mean rela-
tive fecundity, when individual estimates are
based on fish captured both prior to and after oo-
cyte hydration, is ooctyes per unit ovary-free body
weight. Yet either expression of relative fecundity
can be biased if there are changes in somatic
weight associated with the reproductive cycle or
changes in condition, i.e., the length-weight rela-
tionship from year-to-year or among geographical
regions (Bagenal 1967).

Linear and exponential (based on logjo trans-
formed variates) expressions yielded similar fits to
the relationship between fecundity (TF) and total
body weight (W) and between TF and standard
length (SL) with r values ranging from 0.73 to 0.82
(Table 7). The linear equations describing the re-
lationship between TF and ovary weight (OVW)
also yielded high r values, 0.92 for stages 6-8 fish

Table 6. — Mean fecundity (± SE) oiEngraulis mordax collected
off the Oregon-Washington coast. Tbtal fecundity = number of
advanced oocytes in ovaries; relative fecundity = (1) number
advanced oocytes per gram total body weight (ovary weight
included) and (2) number advanced oocytes per gram ovary-free
body weight.

Classification

Ovarian

stages 6-8

(11 fish)

Ovarian
stage 1 0
(10 fish)

Ovarian
stages 6- 1 0

(21 fish)

Total fecundity
Relative fecundity (1)
Relative fecundity (2)

17,335±2,525
726 ±65
782 ±75

16.267 ±1,881
712±43
873 ±63

16,826 ±1,563
720 ±40
826±49

Table 7. — Functional (geometric mean) regression equations,
sample size (N), standard error of the regression coefficient (SE),
and correlation coefficient (r) for the relationship between total
fecundity {TF) and total body weight (IV), standard length iSL),
and ovary weight ( OVW) in Engraulis mordax collected off the
Oregon-Washington coast.

Equations

SE

Ovarian stages 6-10:

TF= -13,889.91 + 1,339.57W
LogioTF =1.91-1- l.69logiolV

TF = -76,286.31 -i- 738.99 SL
Logio TF = -6.80 + 5.23 logio SL
Ovarian stages 6-8:

TF = -1,181.63 + 11,506.73 OVW
Ovarian stage 10:

TF = -2,654.20 + 4,637.89 OVW

21

1 76.54

0.82

21

0.24

0.77

21

108.56

0.77

21

0.82

0.73

11

1,534.23

0.92

10

433.83

0.96

and 0.96 for stage 10 fish. The apparent difference
between the slopes of these two equations,
11,506.73 for stages 6-8 and 4,637.89 for stage 10,
can be explained by the substantial increase in
ovary weight in stage 10 fish caused by oocyte
hydration, and not by an actual decrease in
number of oocytes in these fish. Fecundity would
be underestimated if an equation relating TF to
OVW in fish with hydrated oocytes was used to
predict fecundity. The relationship between TF
and OVW, if based on fish captured both prior to
and after oocyte hydration, would yield a low cor-
relation coefficient (r).

Spawning Frequency

The number of times a female anchovy in the
northern subpopulation spawns during the year
could not be determined directly with available
data. Oocyte observations, however, provided
some information pertinent to the question of
spawning frequency in these fish.

Degenerating, immature, yolked oocytes (those
with abnormal-looking nuclei) were found in ripe
northern anchovies during the spawning season.
Although relative numbers of these oocytes were
not determined, their presence suggests that oo-
cytes in early stages of vitellogenesis in July may
eventually degenerate and be absorbed. Higham
and Nicholson (1964) also found disintegrating in-
termediate and maturing oocytes in the ovaries of
recently spent Atlantic menhaden, Breuoortia
tyrannus, indicating perhaps that this species may
also absorb immature, yolked oocytes after spawn-
ing.

The presence of a distinct, intermediate mode of
oocytes, indicating simultaneous maturation of a
new batch of oocytes while a group of advanced
oocytes is still in the ovary, is considered to be
strong evidence of multiple spawning (Clark 1929;
MacGregor 1976). In the oocyte size distributions
of mature northern anchovies an intermediate
mode of yolked oocytes never became distinctly
separate from the smaller, yolkless oocytes (Figure
5). There was some indication of continued growth
among intermediate-sized, yolked oocytes (0.56-
0.66 mm) in five stage 10 fish (both unovulated and
ovulated) before spawning. Yet oocytes in this size
range were absent in three spent fish (Figure 5).
The mode of intermediate-sized, yolked oocytes at
0.50 mm in these spent fish was in essentially the
same position as in stage 10 (ovulated) fish, indi-
cating little additional oocyte growth for some un-

612

LAROCHE and RICHARDSON: REPRODUCTION OF NORTHERN ANCHOVY

determined period of time after spawning (Figure
5). Similarly shaped oocyte size distributions were
used as indirect evidence of a single seasonal
spawning in the Hawaiian anchovy, Stolephorus
purpureas (Leary et al. 1975), the anchoveta,
Cetengraulis mysticetus (Howard and Landa
1958), and the Pacific and jack mackerels, Scomber
japonicus and Trachurus symmetricus (Mac-
Gregor 1976).

A secondary batch of oocytes, numerically equal
to the group of hydrated oocytes about to be
spawned was not found in stage 10 fish. The
number of intermediate-sized, 0.46-0.62 mm,
yolked oocytes, the next most advanced oocytes in
ovaries of all stage 10 fish, was 427 oocytes/g
ovary -free body weight (mean of three subsam-
ples) in a 154 mm SL, stage 10 anchovy. This value,
expressed as an estimate of relative fecundity, was
about one-half the value of mean relative fecun-
dity often stage 10 fish (Table 6) and lay outside
the range of all 21 individual fecundity estimates
(Table 5).

DISCUSSION

Length and Age at First Maturity

Published reports of size and age at first matur-
ity of anchovies in the central subpopulation are
somewhat conflicting. Clark and Phillips (1952)
found that only 30% of the fish in the size range
100-120 mm SL (ages I and II) were mature and
only 50% in the size range 120-139 mm SL (ages II
and III) were mature. Yet Huppert et al. (footnote
3) reported a recent study that found all northern
anchovies older than 24 mo, —120 mm SL, to be
mature.

Sexual maturity is also attained in nothern an-
chovies of the northern subpopulation at the end of
the second year. Pike (1951) found that 96% of the
northern anchovies in the size range 105-109 mm
SL (age II fish), from commercial catches, were
mature while only 14% of the fish ranging from 100
to 104 mm SL (<2 yr old) were mature. Northern
anchovies off Oregon similarly do not attain sex-
ual maturity until after the second year (i.e., in the
third summer). The smallest northern anchovies
taken in this study in spawning condition were 104
mm SL (male) and 107 mm SL (female). Size at
maturity seems to be somewhat smaller in the
northern subpopulation, possibly reflecting dif-
ferences in growth rates between the two subpopu-
lations.

Sex Ratio

It appears that the overall sex ratio in both the
central and northern subpopulations is —1:1.
Klingbeil (1978) reported that the overall male to
female ratio of northern anchovies from sea sur-
vey samples off California combined for the years
1966-75 was 0.97:1. Monthly sex ratios in commer-
cial catches from February to August off British
Columbia were approximately 1:1 with females
slightly outnumbering males (0.77:1 the lowest
ratio) (Pike 1951). The male to female ratio of both
mature and immature anchovies off Oregon before
the spawning season (May) and immature fish
during and after the spawning (July and October)
was also about 1:1.

Yet samples from both central and northern
subpopulations were found with unexpectedly
higher numbers of either males or females.
Klingbeil (1978) suggested that adult northern
anchovies may often be segregated by sex. al-
though no seasonal trends could be discerned in
their data. Hunter and Goldberg (1980) found that
in trawl collections of northern anchovies off
California dominated by males, 40% of the females
had spawned on the night of capture. But in female
dominated collections only about 10% of the
females had spawned the night of capture. They
suggested that changing sex ratios in northern
anchovy schools may be associated with reproduc-
tive behavior. The overall male to female ratio of
mature fish caught in July in areas of active
spawning off Oregon and Washington was 2.6:1,
with sex ratios in individual catches ranging from
1:1 to 8:1. The highest male to female ratios were
also associated with catches containing high
numbers of ripe females which were or soon would
be spawning. The percent of these ripe females in
male dominated schools off Oregon and Washing-
ton ranged from 33 to 40% and was similar to the
percent of most recently spawned females in male
dominated schools off California (Hunter and
Goldberg 1980). Pike ( 1951) found that the relative
number of male anchovies increased as the spawn-
ing season approached and in July males slightly
outnumbered females. But by August, at the end
of the spawning season, the male to female ratio
was 0.71:1.

Fecundity

The only previous estimate of northern anchovy
fecundity in the northern subpopulation.

613

1,369 ±148 ooc5^es/g total body weight in =4)
(Pike 1951), differs from our estimate of 720±40
oocytes/g total body weight in = 21). Our estimate
is more accurate than Pike's because it is based on
counts of only the most advanced oocytes in ripe or
nearly ripe fish. Pike's fecundity estimate was
based on the assumption that northern anchovies
spawn three equal batches of oocytes per year and
was calculated by dividing the total number of
oocytes >0.20 mm by three. His assumption of
spawning frequency, based on the number of
modal peaks in oocyte size-frequency distribu-
tions, is still unproven and could lead to erroneous
fecundity estimates depending on the actual
number of spawnings per fish.

Northern anchovies in the northern subpopula-
tion off Oregon and Washington apparently have a
greater fecundity (based on ovary-free body
weight), 826 in = 21), than those in the central
subpopulation off California, based on estimates
by MacGregor (1968) and Hunter and Goldberg
(1980), 606 (n = 19) and 389 (« = 23), respectively.
An analysis of variance (single classification) in-
dicated the presence of a highly significant
(P<0.01) added variance component between in-
dividual relative fecundity estimates (based on
ovary-free body weight) of our fish and those
examined by MacGregor (1968). Hunter and
Goldberg's mean value, which is more directly
comparable than MacGregor 's with our estimate
because it was similarly based on ripe fish with
hydrated oocytes, was even lower than Mac-
Gregor's, although statistical comparisons were
not possible (individual fecundity values were not
listed). The difference between the two California
estimates may have been due primarily to differ-
ences in the stage of ovarian maturation of the fish
used for fecundity determinations. Difficulty in
distinguishing the most mature oocytes from less
mature ones before hydration could have caused
the higher estimate obtained by MacGregor who
used only fish with unhydrated oocytes.

The higher fecundity of northern anchovies off
Oregon and Washington may represent a true ra-
cial difference between fish in the northern and
central subpopulations. Racial differences in
fecundity have been demonstrated in many
species of fish with probable causes being either
environmental or genetic factors (Bagenal 1957,
1967). Bagenal (1966) speculated that geographic
differences in plaice fecundity were caused by dif-
ferences in food availability and population den-
sity

FISHERY BULLETIN: VOL. 78, NO. 3

Spawning Frequency

Fish, such as the northern anchovy, with asyn-
chronous oocyte development have the potential to
spawn more than once during the season (de Vla-
ming 1974). Yet the actual number of times a
female northern anchovy spawns during a year
has not been conclusively documented in any of
the subpopulations. Pike (1951) estimated that
northern anchovies in the northern subpopulation
off British Columbia spawn three times during the
3-mo spawning season. MacGregor (1968)
suggested that at least some fish in the central
subpopulation spawn more than once during the
spawning season, which may include all 12 mo of
the year. Hunter and Goldberg (1980) estimated
the spawning frequency of northern anchovies in
the central subpopulation to be once every 6-7 d
during months of peak spawning.

Pike's (1951) conclusion was based solely on the
presence of multiple modes in oocyte size distribu-
tions and ambiguous data on changes in the ratio
of immature to advanced oocytes during the
spawning season. These data alone cannot be used
to determine spawning frequency in fishes. Mac-
Gregor (1968) concluded that spawning later in
the year represented repeat spawning by some
northern anchovies because early in the spawning
season all mature females had well-developed
eggs or were recently spent. Christiansen and
Cousseau (1971), using histological techniques,
found that some female M. merluccius had the
physiological ability to recover more rapidly after
spawning than the rest of the population and that
these fish spawned a second time later in the sea-
son off Argentina. It seems likely, therefore, that
anchovies in the central subpopulation spawn
more than once during the protracted spavvming
season. But the number of spawnings per year may
be variable because environmental conditions
such as temperature and food supply, which are
known to influence reproductive cycling in fishes,
can vary from year to year (Bagenal 1966, 1969; de
Vlaming 1971, 1974; Hodder 1972', Tyler and Dunn
1976). Recently, Brewer (1978) suggested that food
availability may limit both the number of eggs
spawned and the number of spawnings per year by
northern anchovies in San Pedro Bay, Calif.

Hunter and Goldberg's (1980) estimate of
spawning frequency was based on the mean per-
cent incidence of northern anchovies with 1-d-old
ovarian follicles in trawl samples taken during a
2-wk period in February. Their determination of

614

LAROCHE and RICHARDSON: REPRODUCTION OF NORTHERN ANCHOVY

spawning frequency depended on the, as yet, un-
proven assumption that all mature females in the
central subpopulation spawn during 1 mo of the
peak spawning period. Even if this assumption is
correct the dependence of this method on obtain-
ing samples which accurately reflect the propor-
tion of spawning and nonspawning females in the
population poses another problem. Spawning fre-
quency will be overestimated if nonspawning
females are not as susceptible as spawning fish to
capture by sampling gear because of differences in
spatial distribution or behavior of the two groups.
Our oocyte observations alone, without data on
rates of oocj^e maturation and degeneration, did
not yield an estimate of northern anchovy spawn-
ing frequency in the northern subpopulation. But
our findings indicated that oocyte degeneration
and apparent reduced growth among
intermediate-sized, yolked oocytes prior to and
after release of one batch of oocytes may limit the
number of subsequent spawnings. In addition, the
actual length of the spawning season off Oregon
and Washington is only 2 mo, although water
temperatures favorable for northern anchovy
spawning (13°-17.5° C at 10 m depth, Baxter 1967)
are present in this region for 5-6 mo. This discrep-
ancy supports our interpretation of the oocyte ob-
servations by indicating that environmental fac-
tors may not be suitable for complete maturation
of all yolked oocytes present in northern anchovy
ovaries in the northern subpopulation. Only data
from laboratory experiments designed to deter-
mine rates of oocyte maturation (and degenera-
tion) under varying environmental conditions,
such as photoperiod, temperature, and food supply,
will provide a definitive answer to the question of
how many times northern anchovies spawn per
year.

Seasonal Distribution Associated
with Reproduction

A distinct geographic segregation of mature and
immature northern anchovies and hence an in-
ferred spawning migration during the summer-
time spawning season occurs in the northern sub-
population off Washington, Oregon, and northern
California but apparently not around British Co-
lumbia. Evidence for this resulted from a sum-
mary of data from a number of sources including
data and cruise reports (Table 8), Tillman,^ and
personal observations from our own sampling ef-
forts (Table 1, Figure 1). These seasonal patterns in

the northern subpopulation, described here for the
first time, were evident even though the data were
obtained with various types of sampling gear and
unequal sampling effort.

In winter, January through March, both mature
and immature northern anchovies of all sizes
( =50-180 mm) occur in nearshore coastal areas off
British Columbia, Washington, and Oregon. Small
schools were seen in British Columbia coastal
waters. Concentrations were found off Washing-
ton between Cape Flattery and Destruction Island
(over 31-313 m depths) and between Grays Harbor
and the Columbia River (42-101 m depths). Off
Oregon, northern anchovies were taken between
the Columbia River and Coos Bay (91-183 m
depths) with largest numbers occurring between
the Columbia River and Tillamook Bay. Fish off
Washington and Oregon were observed or cap-
tured near the bottom or in midwater in coastal
areas, but were not commonly taken in bays and
estuaries. Small catches offish were taken in the
Strait of Juan de Fuca but none were taken in
Puget Sound, Wash.; Yaquina Bay, Oreg; or Hum-
boldt Bay, Calif. A few rare occurrences ( 50-70 mm
FL) have been reported from Tillamook Bay, Oreg.

In spring, April through mid-June, northern
anchovies still occur in nearshore coastal waters.
Fish, 80-160 mm SL, were taken in the seine
fishery of the 1940's in British Columbia coastal
waters. Although no schools were observed off the
northern Washington coast, northern anchovies,
50-170 mm SL, were consistently taken near the
bottom or in midwater in the vicinity of the Co-
lumbia River mouth (20-91 m depth). Northern
anchovies, mostly <100 mm, were collected in the
spring in Tillamook Bay, Yaquina Bay, and Coos
Bay, Oreg. (sizes not given). Northern anchovies of
all sizes entered Humboldt Bay in April and re-
mained there into June and July.

In summer, mid-June through September, both
mature and immature anchovies (up to 160 mm
SL) occur in nearshore coastal waters of British
Columbia where they supported a major seine
fishery in the 1940's. Although few ripe or spent
adults were taken, spawning is reported to occur
in bays and inlets around southern British Co-
lumbia in summer. Off Washington and Oregon,
sexually mature and immature northern an-
chovies are geographically separated. Adult fish

^M. F. Tillman, Northwest and Alaska Fisheries Center
Marine Mammal Division, NMFS, NOAA, 7600 Sand Point Way
NE, Seattle, WA 98115, pers. commun. April 1975.

615

FISHERY BULLETIN: VOL. 78, NO. 3

Table 8. — Summary of additional studies in which juvenile and adult Engraulis mordax from the northern subpopulation were

collected.

General area

Dates

Principal gear

Sampling effort

Reference

British Columbia, bays and inlets

1940-50; mostly Feb.-Sepl.

Commercial purse seine

40 random samples

Pike (1951)

1947 and June-July

1948

Britisti Columbia, Saanicti Inlet

23Apr.-21 July 1968

6 m surface trawl

= weekly.

1 1 6 tows

Barraclough et al.'

British Columbia, Strait of

4-6 July 1967

6 m surface trawl

24 tows

Robinson^

Georgia

Puget Sound, Strait of Juan de

10-28 Jan. 1966

Standard Cobb pelagic trawl

1 9 tows

BCF exploratory cruise no. 75,

Fuca, Washington coast from

and 2 3 scale Cobb pelagic

RV John N. Cobb^

Mukkaw Bay to Columbia River

trawl (echosounder used to

(1 5-220 fm)

locate fish schools)

Washington coast between Cape

6 Apr.-4 May 1966

Standard Cobb pelagic trawl and

6 tows

BCF exploratory cruise no. 77,

Flattery and Columbia River

2/3 scale Cobb pelagic trawl

RV John W Cobb^

(10-140 fm)

(echosounder used to locate

Washington coast between Cape 8-18 Nov 1 966

Flattery and Destruction

Island (20-100fm) and

between Grays Harbor and

Columbia River (10-50 fm)
Washington-Oregon coast

between Cape Flattery and

Yaquina Bay

18 Nov- 16 Dec. 1966 and
3 Jan -8 Apr. 1967

Washington-Oregon coast
between Cape Flattery and
HecetaHead (15-100 fm)

Tillamook Bay, Oreg.

Yaquina Bay, Oreg.

Coos Bay, Oreg.

Humboldt Bay, Calif.

1 5 IVIay-2 June 1967

May 1974-May 1976
July 1964-Sept. 1967
June-Sept. 1970

Apr. 1974-Oct. 1976

fish schools)
2/3 scale Cobb pelagic trawl
(echosounder used to locate
fish schools)

Standard Cobb pelagic trawl,
2/3 scale Cobb pelagic
trawl, and 2 experimental
anchovy trawls (echosounder
used to locate fish schools)
BCF Universal trawl (echo-
sounder used to locate fish
schools)
6 m try net; 46 m beach seine
6 m otter trawl (plus other gear)
61 m beach seine; 30 m bag

seine (plus other gear)
Echosounder — to determine
distribution of anchovy
schools; 200 m lampara bait
seine 66.7 x 6.7 m purse
seine (plus other gear)

2 tows

71 tows (most tows made
in Jan-Apr.)

7 tows

-biweekly, then monthly

^monthly

Not specified

Weekly echosounder
surveys plus 45 net
hauls

BCF exploratory cruise no. 82,
RV John N. Cobb^

BCF gear research cruise
no. 8, MV Baron^

BCF exploratory cruise no. 87,
RV John N. Cobb^

Forsberg et a!.-'
Beardsley (1969)
Cummings and Schwartz^

Waldvogel(1977)

'Barraclough, W. E, D. G. Robinson, and J. D. Fulton. 1968. Data record — Number, size composition, weight, and food of larval and juvenile fish caught with a
two-boat surface trawl in Saanich Inlet April 23-July 21, 1968. Fish. Res. Board Can., Manuscr. Rep. Ser. 1004, 305 p.

2Robinson, D. G. 1969. Data record — Number, size composition, weight and food of larval and juvenile fish caught with a two-boat surface trawl in the Strait of
Georgia July 4-6, 1967. Fish. Res. Board Can., Manuscr, Rep Ser. 1012, 71 p.

^Information from cruise reports. Northwest and Alaska Fisheries Center, NMFS, NOAA, 2725 Montlake Blvd. East, Seattle, WA 98112.

■•Forsberg, B. O, J. A, Johnson, and S. M. Klug. 1977. Identification, distribution, and notes on food habits of fish and shellfish in Tillamook Bay Oregon. Oreg.
Dep. Fish Wildl. Res. Sec, Fed. Aid Prog, Rep. Fish. 1977, 117 p.

^Cummings, E., and E. Schwartz. 1971. Fish in Coos Bay, Oregon, with comments on distribution, temperature, and salinity of the estuary Oreg. Dep. Fish
Wildl., Coastal rivers invest— -Inf. Rep. 70-11, 22 p.

in spawning condition were found offshore with
main concentrations between lat. 43° and 47° N
and -65-157 km offshore. They occurred in small
schools near the surface at night and deeper in the
water column during daylight. Immature fish
(mostly <100 mm SL) remained in nearshore
coastal areas or in bays. They were taken in Grays
Harbor, Wash., around the Columbia River mouth,
in Tillamook Bay, Yaquina Bay, and Coos Bay,
where they were observed feeding at the surface
during daylight. In Humboldt Bay, mature fish left
in June and July leaving only immature fish in the
bay through the summer. Adults presumably
moved offshore to spawn, although it is not known
whether they moved north off Oregon and Wash-
ington or elsewhere. Adults returned to the bay
around mid-September in spent condition.

In fall, October through December, northern an-
chovies are no longer abundant around British
Columbia. The fishery of the 1940's was generally
not in operation that season. Off Washington and

Oregon, adults eventually return to coastal waters
from offshore spawning areas although few adults
were collected in the fall. Fall catches occurred
mainly off the Columbia River mouth (13-61 m
depth) and Grays Harbor (35-37 m depth). Imma-
ture fish appeared to leave the bays and estuaries
and returned to nearshore coastal waters. Young
fish were seen in the Columbia River in October,
feeding at the surface. No anchovies were collected
in Tillamook Bay, Yaquina Bay, or Coos Bay.
Juveniles and adults left Humboldt Bay in late
October- November.

A pronounced and well-defined onshore-offshore
segregation of mature and immature fish and in-
ferred offshore spawning migration during the
spawning period as observed in the northern sub-
population off Washington, Oregon, and northern
California has not been documented for northern
anchovies in the central or southern subpopula-
tions. Baxter (1967) stated that off California
northern anchovies apparently move offshore in

616

LAROCHE and RICHARDSON: REPRODUCTION OF NORTHERN ANCHOVY

fall and winter, during the peak spawning period,
and return inshore in spring. Huppert et al. (foot-
note 3) indicated similar movements but provided
little additional information. Brewer 11978)
suggested that mature northern anchovies in the
vicinity of San Pedro Bay move to deeper, cooler
waters offshore to spawn. The distinct geographic
segregation of mature and immature northern an-
chovies in the northern subpopulation which oc-
curs because of an offshore migration of spawning
fish may represent an additional racial difference
among the three northern anchovy subpopula-
tions in the northeast Pacific.

ACKNOWLEDGMENTS

Wayne A. Laroche took the photomicrographs of
oocytes. Jerome D. Spratt and John S. Sunada of
the California Department of Fish and Game
checked our otolith readings and provided useful
advice concerning interpretation of northern an-
chovy age data. Percy L. Donaghay gave us many
helpful ideas for data analyses and Rae Deane
Leatham generously provided assistance with all
computer work. David L. Stein rendered a careful
review of the manuscript. John R. Hunter, Na-
tional Marine Fisheries Service (NMFS), La Jolla,
read an earlier version of the manuscript and
suggested useful ways to improve it. The following
individuals helped us during this study by provid-
ing information on the location of northern an-
chovies at sea or collected and saved fish for us: P.
Killian, W. Nichols, and G. Muhlberg of the Clat-
sop Community College, Astoria, Oreg.; M. Hosie,
G. Hettman, J. Lukas, and B. Forsberg of the Ore-
gon Department of Fish and Wildlife; T. Durkin,
NMFS, Hammond, Oreg.; W Pearcy, D. Stein, and
E. Krygier of the Oregon State University, Corval-
lis, Oreg.

This work is a result of research sponsored by
the Oregon State University Sea Grant College
Program, supported by NOAA Office of Sea Grant,
Department of Commerce, under Grant No. 04-6-
158-44094.

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618

DIETS OF FOURTEEN SPECIES OF VERTICALLY
MIGRATING MESOPELAGIC FISHES IN HAWAIIAN WATERS

Thomas A. Clarke ^

ABSTRACT

Fishes and zooplankton were sampled at four depths (70, 90, 110, 170 m) at night in the upper layers
near Hawaii. Diets of the fishes were determined from stomach contents and preferences estimated by
comparison with prey densities at the appropriate depth. Generally, the fishes fed on relatively large,
pigmented or opaque crustaceans; other taxa and very small or translucent prey were rarely eaten.
There were, however, differences in diet and preference between species; these were frequently corre-
lated with morphological features, especially lens size and gill raker spacing. One group of four fishes
which were very similar in both diet and morphology were separated by depth distribution and size.
Comparison with other studies indicates that tropical species are perhaps more specialized and
ecologically separated in diet than their counterparts in high latitudes.

Vertically migrating mesopelagic fishes are im-
portant components of oceanic ecosytems. In the
tropical open ocean, abundance of larvae
(Ahlstrom 1969) and estimates of biomass (Clarke
1973; Maynard et al. 1975) indicate that they are
the dominant group of micronekton and greatly
exceed the abundance of epipelagic forms. Stand-
ing crops are even higher in oceanic situations at
higher latitudes (Frost and McCrone 1979) and
coastal upwelling areas (Pearcy and Laurs 1966).
Tropical oceanic faunas are much more diverse. At
high latitudes and in quasi-neritic situations, one
to three species typically make up the great major-
ity of the standing crop (Pearcy and Laurs 1966;
Zahuranec and Pugh 1971; Baird et al. 1975; Frost
and McCrone 1979), while in the tropical open
ocean the abundances of the dozens of cooccurring
species are more evenly distributed (Clarke 1973,
1974).

The diets of these fishes are of interest both to
assess their impact on lower trophic levels in
oceanic ecosystems and to determine the degree to
which cooccurring species are specialized with re-
spect to their feeding habits; however, previous
studies do not allow serious consideration of these
aspects. Few have presented extensive data on
more than one to three species. For the most part,
prey have not been identified adequately enough
to seriously discuss preference or dietary overlap,
and there has been no consideration of bias due to

'University of Hawaii, Department of Oceanography and
Hawaii Institute of Marine Biology, PO. Box 1346, Kaneohe, HI
96744.

Manuscript accepted January 1980.
FISHERY BULLETIN: VOL! 78, NO. 3, 1980.

differing rates of digestibility and, therefore, abil-
ity to identify different prey types (Gannon 1976).
Few studies have compared stomach contents of
fishes with appropriate samples of the prey avail-
able; those that have done so have simply com-
pared percentages of different prey types and have
not considered biases or errors inherent in the
samples taken for prey abundance.

This paper considers diets of 14 species of verti-
cally migrating mesopelagic fishes based on data
from collections taken near Hawaii in the central
North Pacific Ocean. All species are primarily zoo-
planktivorous and are known (Clarke 1978) or
suspected to feed principally in the upper 250 m at
night. The diets of each species are compared with
densities of zooplankton at each of the depths
sampled. While problems in feeding studies men-
tioned above have by no means been completely
eliminated, the methodology recognizes and at
least qualitatively attempts to account for major
sources of error. The results allow consideration of
biases of the fishes as "samplers" of the potentially
available prey and of dietary overlap between
species or sizes cooccurring at the same depths in
the water column.

METHODS

Field Collections

All specimens for this study were collected ca. 20
km off the coast of Oahu, Hawaii, (ca. lat. 21°10'-
30 ' N, long. 158°10 '-30 ' W) over bottom depths of
2,000-4,000 m. The depth ranges, vertical migra-

619 ^^

FISHERY BULLETIN: VOL. 78, NO. 3

tions, and other aspects of the ecology of the
species considered have been reported for the same
Study area (Clarke 1973; Clarke and Wagner 1976)
and other studies there summarized by Maynard
etal. (1975).

Fishes were collected with a 3 m (lO-ft) Isaacs-
Kidd mid water trawl. To minimize the probability
of fishes' feeding while in the net, the terminal
section of the net was of ca. 3 mm knotless nylon
mesh instead of the commonly used, finer
plankton netting.

The trawl was launched and towed at ca. 2 m/s
and the ship was slowed to ca. 1 m/s for retrieval.
Total time for descent to and ascent from towing
depth was 12-20 min. The trawl was towed at the
desired depth for ca. 2 h. Zooplankton were sam-
pled with 70 cm diameter, opening-closing bongo
nets of 505 /xm mesh. Ship's speed of ca. 1 m/s was
maintained for the entire tow; the nets were open
at the desired depth for 30-33 min. Time-depth
recorders attached to the nets indicated that the
depths of the "horizontal" (2 h) portions of the
trawl tows and the open part of the bongo net tows
were within 5 m of each other and of the desired
depth for each set of samples. All collections were
preserved in ca. 5% formaldehyde in seawater so-
lution immediately after the nets were on deck.

Four different depths (70, 90, 110, 170 m) were
sampled (Table 1). In September 1973, two plank-
ton tows followed by two trawl tows were made on

Table l. — Sampling information for trawl and plankton collec-
tions at four different depths off Oahu, Hawaii. D -(- R = total
time for descent and retrieval of trawl.

Trawl

Plankton net

Deptti
(m)

Time at
Date depth'

D -1- R
(min)

Date

Time open
at depth'

70

24-25 Sept. 1973 2158-2400
25 Sept. 1973 0045-0245

13
12

24 Sept. 1973
24 Sept. 1973

2010-2040
2101-2131

90

11-12 Nov. 1974 2300-0100

18

14 Nov. 1974

2353-0023

110

26 Sept 1973 0007-0207
26 Sept. 1973 0237-0437

13
15

25 Sept 1973
25 Sept. 1973

2202-2235
2256-2328

170

26-27 Sept. 1973 2318-0118
27 Sept. 1973 0150-0350

15
20

26 Sept. 1973

1953-2030

'Hawaii standarcj time.

the same night at each of three depths ( 70, 110, and
170 m). For the 170 m collections the bongo nets
failed to open and close properly on one of the tows.
A single trawl sample from 90 m was taken in
November 1974, and a single plankton sample
taken at the same depth two nights later. All tows
were taken between last light at dusk and first
light at dawn and within 2 d of new moon. Thus

ambient light was essentially constant for all
samples taken at a given depth, and there were
probably no between-sample differences in verti-
cal distribution of either the fishes or their prey at
a given depth. Consequently, except for possible
captures in transit to and from towing depth (see
below), the fishes captured at a given depth were
assumed to have been feeding on the same prey
population sampled by the appropriate plankton
tows.

Laboratory Procedures

All nonlarval fishes from the trawls were iden-
tified and standard length (SL) measured to the
nearest millimeter. The fishes from each depth
were grouped by species and arbitrary size classes:
16-25 mm, 26-35 mm, 36-45 mm, 45-60 mm, and
>61 mm. Certain species or size classes from each
depth were eliminated from consideration be-
cause, based on previous evidence of depth-size
distributions (Clarke 1973; Clarke and Wagner
1976), they were almost certainly taken in transit
to and from towing depth. Among the size classes
that were considered, a few possibly, included
specimens that were captured above towing depth
and thus were not exposed to the same array of
prey as sampled by the plankton nets; these
groups are noted specifically in subsequent sec-
tions.

For each specimen examined, standard length
was recorded and the stomach (anterior end of the
esophagus to the pyloric constriction) removed.
Prey items with bodies intact were noted sepa-
rately and measured to the nearest 0.1 mm with an
ocular micrometer. For the commonly occurring
crustacean prey, the following measurements
were used: copepods — prosome length, ostracods
— maximum carapace length, malacostracans —
the distance from the anteriormost point exclu-
sive of the antennae to the base of the telson. (The
telson of malacostracans was too frequently sepa-
rated to routinely include it in the length.) The
dimensions measured for other intact prey were
standard length for fishes, maximum diameter for
nearly spherical items such as gastropod veligers,
and total length for all others. Most intact
copepods and euphausiids could be indentified to
genus and most copepodite VI stages of the former
and juveniles and adults of the latter to species.
Ostracods were almost all Conchoecia spp., but
were not identified further. Other prey types were
identified only to major taxa. Identifiable frag-

620

CLARKE: DIETS OF FOURTEEN SPECIES OF MESOPELAGIC FISHES

ments of digested prey among the remainder of the
stomach contents were also recorded.

Prey items in the mouth were discarded, but
items in the esophagus were included with the
stomach contents. The bodies of items in the
esophagus were compressed and the appendages
were flattened against the body. Such items could
conceivably have been eaten in the trawl, but sev-
eral lines of evidence indicate that this is an un-
important source of error. Hopkins and Baird
(1975) reported no evidence of net feeding even
when a fine mesh cod end (which would presuma-
bly accumulate more zooplankton and restrict
water flow) was used. Only a few of the species
considered here had items in the esophagus at all
frequently, and in all cases such items were the
same or very similar to items frequently found
among digested or partially digested matter in the
stomach. Thus if there was significant net feeding,
only some species did so and apparently selected
prey from that in the cod end similar to their
normal habits.

The species-size groups for which data are pre-
sented here are those from which a reasonable
number of intact prey were recorded. If sufficient
numbers of specimens were available, I examined
specimens until about 100 intact items were re-
corded. For other groups, I examined all the fish
collected, but eliminated from consideration those
for which too few prey items were recorded either
because of low numbers of specimens or low inci-
dence of prey in the stomach.

Zooplankton from the bongo net samples were
identified and counted from aliquots taken with a
plankton splitter. Euphausiids and most adult
copepods were identified to species — the former
from between all and one-eighth of the sample and
the latter from one-sixteenth to one-thirtysecond.
Most immature copepods were identified to genus.
Ostracods and amphipods from one-sixteenth to
one-thirtysecond of the sample were counted and
measured to the nearest 0.1 mm. Other taxa were
counted from all to one-eighth of the sample.
Flowmeters on the plankton nets gave suspect
readings; consequently, volumes sampled by each
tow were calculated from the duration of the open
part of the tow and estimated speed (1 m/s). The
densities (per cubic meter) of the different prey
types were calculated from the volumes and ad-
justed counts.

The apparent search volume per fish ( ASV) was
used as an index of relative preference for the
different prey types. For each type of prey noted

from the stomachs of each category of fish, the
ratio of the total number of intact items to the
density of that type was divided by the number of
fish with intact items in the stomach. Fish
examined but with no intact prey items in the
stomach were eliminated because they provided
no information on preference, they included fish
that had not fed at all as well as those with vari-
able amounts of digested material in the stomach,
and finally their proportion of the total fish
examined varied between categories. Thus the
ASV's as calculated here apply to fish that had fed
recently before capture and take no account of
between-category differences in feeding success.

The ASV is the minimum volume the average
fish of each category had to search to capture the
observed number of a given prey type. The actual
volume searched is larger to the extent that the
fish are not 100% effective in detecting, capturing,
and ingesting prey. If the fish were equally effec-
tive in detecting, capturing, and ingesting all
types of prey, the ASV's would be equal. For a given
category offish, differences in ASV's between prey
types indicate the degree to which the fish were
"biased samplers" of the available prey and thus
measure relative preference in the broadest sense,
i.e., without specifying which aspects of predation
were biased.

The ASV is similar to the index of preference
recently derived by Chesson (1978); the relation-
ship between the two indices is:

V,

OCi =

where for type i out of m prey types, V", is the ASV
and a^ is Chesson's index. Unlike ASV « has no
dimensions and is normalized. Assuming that
predation does not substantially alter prey densi-
ties, i.e., that the number of prey eaten is low
relative to the total available, both indices are
equivalently related to the probability of a given
type of prey being eaten:

^ipi

a^n,.

Pi '-

— —

I

m

m

2 V^.P/e

2 otjnj

fe = l

y = i

where P, is the probability of prey type i being
eaten, andp^ and n, are the density and number of

621

FISHERY BULLETIN: VOL. 78. NO. 3

prey type i available. Like a, the ASV is unaffec-
ted by negative or positive preference for other
types of prey. As pointed out by Chesson (1978),
most other indices of preference, including that of
Ivlev (1961), are so affected and their biological
meaning is not clear.

Preference could be affected by many charac-
teristics of the prey, only one of which could
be considered in this study. Other things being
equal, large or more visible prey types could be
detected at greater distances (Zaret and Kerfoot
1975; O'Brien et al. 1976) and thus have higher
ASV's than small or translucent types. Con-
sequently, in addition to measuring size of prey, I
examined several samples of living zooplankton
from the study area and noted, for as many prey
types as possible, whether they were opaque or
translucent in life and the presence of any pig-
ment.

Ability to escape once detected and attacked
would decrease ASV Prey with bioluminescent
organs could either be more readily detected than
those without or conceivably use them to decrease
probability of detection or capture. Aggregation or
patchiness of prey could also affect ASV either
way depending upon patch size, predator capacity,
and the search behavior of the predator. Unfortu-
nately, none of these behavioral aspects of preda-
tion could be investigated.

For each of the fish species considered here, I
examined four morphological features which
could affect preference. Relevant measurements
were made to the nearest 0.1 mm with either an
ocular micrometer or vernier calipers on at least
five specimens spanning the size range of each
species considered. The length of the premaxillary
was taken as a measure of gape; the diameter of
the lens, as a measure of visual ability; and the
average space between gill rakers on the lower
branch of the first arch, as a measure of minimum
particle size that could be retained. These were
expressed as linear functions of standard length
determined by least squares regression. The filter-
ing area of the gill rakers, which could not be
directly calculated without knowledge of the angle
at which the arch is held during feeding, was as-
sumed proportional to the product of the length of
the raker-bearing segments of the first arch and
the length of the gill raker at the joint between the
upper and lower branches. This product or "area"
was expressed as a power function of standard
length determined by linear squares regression on
the logarithms.

Aside from being affected by characteristics of
the fishes and their prey, ASV's could have been
biased by problems in the methodology. Any feed-
ing in the net (considered above) would tend to
increase ASV for large prey retained there and
also blur any differences in visibility or escape
behavior. Differential rates of digestion and disin-
tegration of prey would bias stomach content data
toward more resistant and more easily recogniza-
ble prey (Gannon 1976). Counting only intact and
measurable prey eliminated bias due to differ-
ential ease of identification. For example, if all
identifiable parts had been counted, the data
would have been heavily biased toward
Pleuromamma spp. whose spots or "buttons" can
be recognized even after the items have completely
disintegrated and passed into the intestine, while
certain other prey which cannot be identified posi-
tively if only one or two features are missing would
have been underrepresented. Even among the
crustaceans, the rate at which the prey disinte-
grates probably varies; Corel ova (1975) indicated
that some small cyclopoid copepods remain intact
even in the intestine of myctophids. Other types of
prey are probably digested much faster than crus-
taceans. To at least qualitatively correct for the
latter bias, I counted all recognizable remains of
chaetognaths, heteropods, other gastropods,
siphonophores, and tunicates as "intact" for calcu-
lation of ASV's.

The densities of small zooplankton were un-
derestimated due to escapement through the 505
^im mesh of the plankton nets used. Counts of
ostracods and certain copepods from an available
plankton tow from the study area with 333 /xm
mesh on one frame and 505 /um on the other indi-
cated that — assuming that the 333 /itm sampled
the small prey accurately — prey >1 mm long were
adequately retained by the 505 ^tm net. These
included most of the prey eaten by the fishes. Two
types of frequently eaten prey, large (0.6-0.8 mm)
Oncaea spp. and ostracods <1.0 mm were un-
derestimated by factors of roughly 4 and 5, respec-
tively, in the 505 /u,m sample, and their ASV's are
overestimated by the same factors. There were
insufficient numbers of other small prey types in
the 333/505 sample to provide even roughly reli-
able estimates of error.

Any avoidance of the bongo nets by prey would
result in erroneously high estimates of ASV No
studies have documented the extent of error due to
avoidance by different prey types, but it can prob-
ably be assumed to be negligible for the great

622

CLARKE: DIETS OF FOURTEEN SPECIES OF MESOPELAGIC FISHES

majority of prey types eaten by the fishes consid-
ered here. Certain types, e.g., large (>10 mm)
euphausiids, shrimps, or fish larvae, must cer-
tainly be able to avoid the bongo nets; con-
sequently, high ASV's associated with such types
must be considered as doubtful.

Uncertainty associated with the estimated
densities from the plankton tows probably limits
interpretation more than any other factor. Since
only one or two pairs of zooplankton samples were
available from each depth, the sampling error as-
sociated with estimated densities cannot be
specified. Overall, the between tow, between net,
and between aliquot differences in counts of abun-
dant types indicated that the densities and there-
fore the ASV's are probably accurate to within a
factor of 0.5-2 X of the values given. Thus small
differences in ASV's cannot be considered real.
Absurdly high values of ASV frequently resulted
for prey types that were very rare or absent in the
plankton samples. Such types were frequently
large forms that may have been "rare" because of
net avoidance, and even for those that were truly
rare, the potential sampling error was probably
large due to insufficient volumes sampled. Con-
sequently, after inspection of the data, all values
>1.0 m^ were lumped together.

RESULTS

A total of 14 species of fishes comprising 51 size-
depth-species categories (Table 2) yielded suffi-
cient data to merit presentation and discussion.
Although most prey items were identified to genus
or species and all were measured to the nearest 0.1
mm, certain prey were grouped by higher taxa or
size ranges for presentation of prey densities (Ta-
ble 3) and to avoid dealing with low numbers in
calculations of ASV's.

In the individual species accounts below, an at-
tempt is made to summarize the major points in
the tabulated data. For these purposes and sub-
sequently throughout the paper, "microzooplank-
ton" are operationally defined as those prey types
too small ( <1.0 mm) to have been accurately sam-
pled by the plankton tows and thus those whose
ASV's are overestimated. The remaining prey
types or "macrozooplankton" are considered by
species or as small (1.0-1.5 mm), medium (1.5-3.0
mm), or large (^3.0 mm). For each category of
fishes considered, the number of macrozooplank-
ton prey types and their frequencies in the diet are

grouped by ASV values in 0.1 m'' increments be-
tween 0 and 1.0 m^ (Table 2).

LampanyctNs steinhecki (Table 4)

The data for L. steinhecki are the most extensive
of all species considered. Large numbers of at least
two size classes were taken at each of the four
depths sampled, and, in spite of the rather low
numbers of prey per fish, the numbers identified
for most categories were relatively high. The 18-25
mm fish from 90 and 110 m and 36-45 mm fish from
170 m may have included some individuals caught
in transit above the towing depth.

Microplankton were of minor importance in the
diets of all but the smallest size groups considered.
Small macrozooplankton were eaten infrequently
and had low ASV's for all sizes of fish. The most
frequently taken prey were euphausiids and
medium to large copepods. The ASV's for these and
other large prey were usually relatively high.
Candacia longimana was most consistent in this
respect. The ASV's for Pleuromamma xiphias at
90 m were markedly lower than at the other
depths as were those for Euphausia spp. at 70 m.
Neither of these exceptions appeared to result
from differences in importance in the diet.
Pleuromamma xiphias was extremely abundant
at 90 m (Table 3), and this, combined with the
lower numbers of prey per fish at this depth,
caused most of the reduction in ASV Euphausia
spp. were extremely abundant at 70 m (Table 3);
most were E. tenera, a species eaten infrequently.
As a coni^equence of these and similar differences
between depths, there was no clear trend or consis-
tency to the distribution of ASV's of the different
prey types. Most types and most items had low
ASV's at 90 m, ASV's were more nearly evenly
distributed at 70 and 110 m, and the majority of
prey had high ASV's at 170 m (Table 2).

Lampanyctus nohilis (Table 5)

Lam.panyctus nobilis was taken from three
depths; with the possible exception of the smallest
size group from 110 m, the data were unlikely to
have been seriously affected by catches in transit
to and from towing depth.

The diet of L. nohilis was generally similar to
that of L. steinhecki but with a greater frequency
of large prey. Microzooplankton were hardly eaten
(Table 2), and ASV's for the few types of small
macrozooplankton were very low. The most fre-

623

FISHERY BULLETIN: VOL. 78, NO. 3

Table 2. — Number of identified prey items, percentage of prey items <1.0 mm long, and distribution of types and percentages of prey
items as a fimction of apparent search volume (see textl for each species, depth, and size category offish examined. Given under each
interval of apparent search volume are the number of types of macrozooplankton prey and, in parentheses, the percentage of total prey
items whose apparent search volumes were in that interval.

Species,

No

Apparent searcti voiume (m^)

depth,

prey items

standard lengtti

(% < 1.0 mm)

0-0.10

0.11-0.20 0.21-0.30 0.31-0.40 0.41-0.50 0.51-0.60 0.61-0.70 0.71-0.80 0.81-0.90

0.91-1.0

>1.0

Lampanyclus steinbecki:

70 m:

26-35 mm

44(14)

3(20)

3(14)

1(5)

1(2)

1(23)

—

2(9)

—

—

1(9)

2(5)

36-45 mm

33

3(24)

1(3)

3(9)

1(3)

—

2(30)

—

—

—

1(9)

3(21)

46-52 mm

16

—

1(37)

—

1(6)

—

—

1(6)

1(37)

—

1(13)

—

90 m:

1&-25mm

17(35)

3(24)

2(18)

—

2(18)

—

—

1(6)

—

—

—

—

26-35 mm

37(14)

9(35)

3(19)

1(11)

2(14)

1(8)

—

—

—

—

—

—

36-45 mm

99 (6)

15(48)

3(14)

—

1(12)

1(6)

—

—

—

—

1(13)

—

46-51 mm

11 (9)

1(9)

2(27)

2(18)

—

—

1(9)

—

1(9)

—

—

1(18)

110m:

19-25 mm

17

1(12)

3(24)

—

3(35)

1(6)

1(24)

—

—

—

—

—

26-35 mm

47(21)

6(17)

—

2(11)

1(21)

—

1(11)

1(11)

—

—

1(6)

1(2)

36-45 mm

133 (4)

4(5)

4(8)

1(4)

1(4)

1(7)

—

1(2)

1(34)

2(26)

—

2(7)

45-50 mm

69 (3)

6(12)

2(9)

2(3)

3(16)

2(51)

—

—

—

—

—

3(7)

170 m:

36-45 mm

40 (7)

2(5)

—

—

—

—

—

—

—

1(7)

—

8(80)

46-54 mm

89 (1)

5(8)

3(10)

—

—

1(3)

—

—

—

—

—

10(77)

L. nobilis :

70 m:

36-45 mm

56 (4)

5(32)

6(18)

1(2)

—

1(4)

1(23)

1(2)

—

—

—

4(16)

47-57 mm

18

2(33)

2(11)

1(17)

—

—

—

—

—

1(6)

—

2(33)

64-78 mm

9

—

1(56)

1(11)

—

—

—

—

—

—

—

3(33)

90 m:

36-45 mm

45 (9)

4(22)

4(18)

2(7)

2(9)

1(13)

—

—

—

—

—

3(22)

46-60 mm

33

9(39)

1(6)

2(12)

—

1(6)

—

2(21)

—

—

—

4(15)

110m:

37-45 mm

32

1(6)

3(9)

1(6)

2(25)

—

—

1(9)

1(16)

—

—

4(28)

47-60 mm

28

1(4)

3(1)

—

—

—

— -

1(11)

1(36)

—

—

3(39)

62-75 mm

61

2(3)

2(5)

1(3)

—

1(7)

—

—

1(30)

—

1(2)

7(51)

76-86 mm

25

—

—

2(28)

—

—

2(20)

—

—

—

—

6(52)

Triphoturus nigrescens :

70 m;

19-25 mm

108(44)

7(17)

1(2)

5(8)

1(13)

3(8)

—

1(3)

1(1)

1(2)

—

1(2)

26-37 mm

98(14)

12(31)

5(9)

3(4)

1(3)

4(6)

—

1(26)

1(5)

—

—

2(2)

Notolychnus valdiviae :

90 m:

16-24 mm

51(51)

13(37)

1(2)

—

—

—

—

—

1(10)

—

—

—

110m:

19-24 mm

136(57)

14(15)

3(15)

2(9)

1(1)

1(2)

—

—

—

—

—

—

170m:

20-23 mm

89(25)

5(11)

2(2)

1(4)

3(8)

—

—

—

—

1(11)

—

5(38)

Ceratoscopelus warmingi:

70 m:

46-69 mm

56(18)

6(21)

4(11)

2(4)

—

—

2(7)

1(2)

1(4)

—

—

7(34)

90 m:

38-45 mm

32(37)

4(22)

1(3)

3(16)

1(3)

—

—

1(6)

—

1(9)

—

1(3)

46-62 mm

153(20)

15(25)

5(18)

2(3)

2(4)

2(9)

2(3)

—

1(8)

—

1(5)

3(8)

110m:

48-68 mm

53 (8)

1(4)

1(2)

3(9)

—

1(6)

—

—

—

—

1(13)

10(58)

Bolinichthys longipes-

70 m:

17-26 mm

77(86)

3(4)

1(1)

—

3(6)

1(3)

—

—

—

—

—

—

90 m:

27-35 mm

125(86)

10(12)

2(2)

1(1)

—

—

—

—

—

—

—

—

36-47 mm

166(83)

12(10)

3(5)

1(1)

—

—

—

—

—

—

—

2(1)

110m:

26-35 mm

236(88)

9(7)

2(2)

—

—

1(3)

—

—

—

—

—

—

36-49 mm

317(76)

8(3)

3(4)

1(1)

—

—

—

1(3)

—

—

1(5)

1(8)

Diogenichthys atlanticus:

70 m:

17-21 mm

40(77)

4(10)

2(5)

—

1(3)

1(5)

—

—

—

—

—

—

Benthosema suborbitale :

70 m:

18-25 mm

28(54)

4(14)

1(4)

1(4)

2(7)

—

—

2(11)

1(4)

—

—

1(4)

26-30 mm

69(42)

9(19)

4(13)

1(16)

1(4)

—

1(3)

—

—

—

—

1(3)

110m:

26-32 mm

47(45)

4(13)

3(15)

2(23)

—

1(2)

—

—

—

—

1(2)

—

Diaphus schmidti :

70 m;

31-35 mm

154(30)

1(5)

7(8)

—

2(10)

2(4)

1(1)

1(1)

—

—

—

10(42)

36-40 mm

120(39)

4(7)

5(8)

6(7)

2(18)

1(4)

1(1)

—

—

2(2)

1(2)

5(11)

90 m;

27-35 mm

180(49)

9(11)

4(4)

3(6)

—

2(5)

—

3(14)

—

—

1(1)

5(9)

36-41 mm

78(46)

5(15)

6(9)

4(14)

1(8)

—

—

1(4)

1(1)

—

—

2(3)

D. perspicillatus.

70 m:

46-56 mm

418(33)

4(2)

2(3)

2(2)

—

2(3)

—

2(8)

—

2(2)

1(5)

16(41)

D. fragilis

90 m:

34-44 mm

29(52)

2(7)

3(24)

2(7)

1(3)

—

—

—

—

1(3)

—

1(3)

D trachops-.

170 m:

36-50 mm

29(10)

—

2(10)

—

2(10)

1(3)

—

—

—

—

1(3)

7(62)

Melamphi

3es danae :

70 m:

17-22 mm

54(22)

4(15)

5(22)

—

—

1(2)

2(18)

—

—

—

—

4(22)

90 m;

19-22 mm

31(23)

1(3)

2(26)

1(16)

—

1(16)

—

—

—

—

—

2(16)

110m;

19-22 mm

34 (9)

—

1(6)

3(12)

—

—

—

—

—

1(21)

1(3)

7(50)

Bregmaceros japonicus ;

70 m:

38-51 mm

41 (2)

5(24)

1(5)

—

—

2(15)

2(39)

—

—

1(12)

—

1(2)

quent prey were euphausiids and P. xiphias; ex-
cept at 70 m and 90 m, respectively, ASV's for these
forms were relatively high. Generally ASV's of
other large prey were also high.

Although there were no major between-depth
differences in diet composition, ASV's were gener-
ally higher for fish from 110 m than for those from
70 and 90 m (Table 2). Among the fish from 110 m,

624

CLARKE: DIETS OF FOURTEEN SPECIES OF MESOPELAGIC FISHES

Table 3. — Density estimates of prey types at each of the four depths sampled. A " + " indicates presence, but with estimated density
<0.005 m"3. Undetermined subadult copepodite stages of copepods are designated by "C" and specific stages by "C" plus the
appropriate Roman numeral; otherwise, copepods are all adults (CVI). Prey types <1.0 mm long, whose densities are probably
underestimated due to mesh escapement, are starred.

Prey type

Density (m-^)

Prey type

Density (m"^)

70 m

90m

110m

170 m

70 m

90m

110m

170 m

Euphausiids:

1,98

0,57

082

0.02

Euphausia spp.

640

030

052

0.01

0.62

0,42

0.23

0.05

Stylocheiron spp.

0.26

0 24

0.17

1.08

0,05

003

0 13

005

Nematoscelis spp.

0.02

0.01

007

1.17

092

2 43

272

062

Thysanopoda aequalis

0.03

0.24

0.04

+

0.98

046

0,04

—

Thysanopoda spp.

0.01

—

0.02

+

0.08

002

—

—

Nematobrachion sexspinosus

—

-¥

+

+

0.12

0.36

001

—

Euphausild larvae

0.44

0.24

0.11

0.07

0.06

0.02

002

0.01

0.09

—

0,04

0.01

1.26

1.11

2,45

0.47

Ostracods:

0.60

0 19

223

0.80

■< 1.0mm

0.50

0.46

0.11

0.37

0.45

038

1 00

0.01

1.0-1.4 mm

1.40

1.67

0.60

1.18

—

0.35

0,15

0.17

1.5-1.9 mm

0.89

1.04

036

0.97

0.35

0.96

0,58

0,25

2.0-2.9 mm

0.09

0.19

0.04

0.09

0.28

0.96

1,02

0.22

» 3.0 mm

—

0.05

0.01

—

0.27

0.59

0.55

0.08

0.16

0,19

0,58

001

Amphipods:

0.09

0,16

0,04

—

1.0-1,9 mm

0.49

035

0.13

0.07

0.11

0.68

0.92

0.39

2.0-2.9 mm

0.15

0.09

0.09

0.17

0.17

1.37

0.30

0.28

» 3.0 mm

0,03

0.03

0.07

0.12

0.08

0.03

+

—

0.74

0 38

0.81

0.06

Carideans:

0.45

0.32

0.23

0.35

juveniles and adults

+

+

4-

4-

1.68

3.49

5.97

1.17

larvae

0.50

0.07

0.08

0.07

0.49

0.41

003

—

0,21

0,15

0.22

0.04

Penaeideans:

023

0.36

0.35

0.14

juveniles and adults

0.02

0.03

0.02

0.01

1 29

5.01

1.42

0.43

larvae

003

0.05

0.01

—

0.93

0.65

0.67

0.82

0.34

063

0.49

0.09

3.87

0.38

0.81

1.82

Mysids

0.02

0.03

0.01

+

2.57

2.37

5.34

1.42

Brachyuran zoeae

0.69

+

0.02

-1-

0.72

0.65

0.68

0.72

Brachyuran megalopae

0.03

0.05

0.01

0.07

0.09

0.02

—

—

Anomuran larvae

0.02

—

0.01

0.03

0.74

0.35

0.31

0.99

Ottier crustacean larvae

—

+

+

+

0.84

061

0,79

0.17

Chaetognaths

2.97

3.32

1.08

0.15

0.01

—

0.08

0.14

Larvaceans

0.14

0.76

0.17

—

0.16

0.24

0.29

3.38

Other tunicates

0.29

1.37

0.16

-t-

0.24

0.24

0.44

0.05

Siphonophores

0.71

1.26

0.12

0.01

0.34

0,93

0,51

0.41

Polychaetes

0.07

0.20

0.04

0.03

1.23

1 84

0.44

—

Heteropods

0.39

0.07

-♦-

-1-

0.01

—

—

—

•Gastropod larvae + pteropods < 1 .0 mm

2.82

0.21

0.17

0.03

0.38

022

0.44

0.01

■Pelecypod larvae

0.12

0.02

0.01

—

0.13

—

—

0.07

Ottier invertebrate larvae

0.11

—

0.27

—

0.81

080

051

0.07

Miscellaneous

0.01

—

0.01

+

0.54

053

0.60

1.00

Fisti eggs

0.04

0.09

0.06

0.01

0.04

—

0.01

0.22

Fish larvae

0.21

0.14

008

0.04

2 89

1,11

1.38

0.49

0.15

092

0.27

008

Copepods:

Neocalanus spp. Oil, Gill

Neocalanus spp. CIV, CV

Neocalanus spp

Calanus tenuicornis

Nannocalanus minor

Undinula vulgaris

U. darwini

Eucalanus spp
'Acrocalanus spp
'Clausocalanus spp.
■Pseudocalanidae

Euaetideus acutus

Chiridius + Gaetanus spp.

Aetideidae — C <2.0 mm

Aetideidae— C 2,0-3,0 mm

Aetidedae— CV, CVI >3.0 mm

Euchaeta media

Euchaeta spp

Euchaeta spp C s2 0 mm

Euchaeta spp, C >2,0 mm

Scolecithrix danae
'Scolecithrix bradyi
'Scolecithicella spp. < 1.0

Scolecithicella spp. 3 1.0

Lophothrix spp CV CVI

ScottocaJanus spp, CV, CVI

Unident, Scolecithriodae./Phaennidae

Pleuromamma xiphias

P. xiphias CV

P abdominalis

P. abdominalis C

P. gracilis

P gracilis CV

Centropages spp,

Lucicutia sp,,

Heterorhabdus papilliger

Heterorhabdus spp.

Augaptilidae

Candacia longimana

Candacia spp, CV. CVI

Paracandacia spp, CV CVI

Pontellidae
'Acartia spp

Unident. calanoids

'Oithona spp.
'Oncaea spp. >0.6 mm

'Oncaea spp sO.e mm

Corycaeus spp.

Other cyclopoids

there was a trend for higher ASV's in the larger
fish; about half the prey taken by the two largest
size groups had ASV's of 1.0 m^ or more.

Triphoturus nigrescens (Table 6)

A large fraction of the diet of the smaller T.
nigrescens were microzooplankton — mostly Oncaea
spp. The most frequent prey among the macrozoo-
plankton was P. xiphias; it and several other
medium to large prey types had moderately high
ASV's. Few prey had high ASV's and those with
low ASV's included all sizes. If the ASV for Oncaea
spp. is reduced by a factor of 4 to roughly correct

for undersampling, it is still equal to or greater
than those for the medium to large macrozoo-
plankton. This indicates that preference for On-
caea by small T. nigrescens is similar to that for
several larger prey types.

The microzooplankton were a small fraction of
the diet of the larger T. nigrescens, and the cor-
rected ASV for Oncaea spp. is relatively low.
Pleuromamma xiphias was the most frequent prey
species and had one of the higher ASV's. Most of
the other prey were medium to large types, and
some of these had moderate to high ASV's. The
largest fraction of both items and prey types, how-
ever, had low ASV's (Table 2). These included both

625

FISHERY BULLETIN: VOL. 78, NO. 3

Table 4. — Stomach contents oiLampanyctus steinbecki: number offish examined, number with intact prey, total number of prey, and
number of each prey type for each depth and size category. The apparent search volume (see text) for each prey type is given in
parentheses after the number eaten. Rarely eaten prey types ("Other prey") are given by depth and size categories below the main
body of the table. Copepodite stages of copepods are designated as in Table 3.

Depth

70 m

90

m

110

m

170

m

Standard length, mm

26-35

36-45

46-52

18-25

26-35

36-45

46-51

19-25

26-35

36-45

46-50

36-45

46-54

No, examined

23

14

7

18

38

103

12

15

22

50

45

20

53

No. with intact prey

18

11

6

8

25

55

7

12

19

42

41

16

35

No. of intact prey

45

33

16

18

39

101

11

18

47

134

69

40

93

Prey type

Nc

) (Apparent search volume, m^)

Calanus tenuicornis

—

—

—

1(0.05)

1(0.02)

3(0.02)

—

—

2(0.04)

—

—

—

1(0.05)

Gaetanus spp.

—

—

—

—

—

1(0.10)

—

—

—

—

—

—

3(0.49)

AetideldaeC <2.0mm

—

1(0.26)

—

—

—

1(0.02)

—

—

—

—

—

—

1(0.11)

Aetideidae C 2.0-3.0 mm

1(0.20)

1(0.33)

—

—

3(0.12)

3(0.06)

—

—

1(0.05)

3(0.07)

2(0.05)

3(0.86) 11(1.44)

Aetideidae CV, CVI >3.0 mm

3(0.61)

3(0.99)

—

— -

4(0.27)

6(0.19)

1(0.24)

—

3(0.29)

5(0.22)

9(0.40)

4(27.7)

10(3.49)

Euchaeta media

1(0.35)

—

—

1(0.66)

—

—

1(0.76)

—

—

1(0.04)

1(0.04)

1(6.94)

—

Euchaeta spp. C >2.0 mm

—

-—

—

—

—

2(0.01)

—

—

—

—

1(0.08)

—

—

Scolecithricella si.Omm

3(0.10)

—

—

—

—

1(0)

—

—

1(0)

2(0)

—

—

—

Scottocalanus spp. CV, CVI

—

—

—

—

—

—

—

—

—

1(0.11)

—

—

2(1.54)

Pleuromamma xiphias

10(0,43)

8(0.56)

6(0.77)

2(0.05)

3(0.02)

18(0.07)

—

2(0.12)

10(0.37) 45(0.75) 26(0.45)

10(1.45) 23(1.54)

P. xiphias CV

—

1(0.10)

—

2(0.39)

1(0.06)

6(0.17)

—

1(0.12)

1(0.08)

3(0.11)

—

—

— ,

P abdominalis

1(0.16)

2(0.54)

2(0.98)

—

3(0,19)

12(0.35)

1(0.23)

2(0.33)

2(0.21)

9(0.44)

4(0.20)

8(5.56)

12(3.a0)

P. abdominalis C

1(0.01)

—

—

—

—

—

—

—

—

—

—

1(0.07)

1(0,02)

P gracilis

—

—

—

1(0.05)

1(0.02)

3(0.02)

2(0.12)

2(0.03)

2(0.02)

—

1(0)

—

—

Lucicutia spp.

—

—

—

1(0,36)

1(0.12)

—

—

—

—

—

—

—

—

Heterorhabdus papilliger

—

—

—

1(0.20)

—

—

—

—

—

1(0.03)

—

—

—

Candacia longimana

4(0,93) 5(1.89)

1(0.69)

—

3(0.50)

13(0.99)

2(1.19)

2(0.38)

5(0.61) 15(0.82)

2(0.11)

2(2.41)

5(2.74)

Candacia spp. CV CVI

—

1(0.26)

—

—

1(0.04)

3(0.06)

—

2(0.33)

—

4(0.19)

2(0.10)

—

—

Paracandacia spp. CV, CVI

4(0.18)

—

—

2(0.14)

3(0.06)

5(0.05)

—

1(0,19)

—

3(0.16)

—

—

—

Unident, calanoid

1

—

—

1

2

2

—

1

—

1

—

—

4

Oncaea spp. >0.6 mm

3(0.31)

—

—

6(1.41)

4(0.30)

6(0.21)

1(0.27)

—

8(0.70)

5(0.20)

1(0.04)

3(0.19)

1(0.03)

Corycaeus spp.

—

—

—

—

1(0.04)

1(0.02)

—

—

—

—

—

—

1(0.06)

Euphausia spp.

5(0.04)

6(0.09)

6(0.16)

—

3(0.40)

2(0.12)

—

4(0.64)

5(0.51) 19(0.87)

9(0.42)

—

2(7.14)

Stylocheiron spp.

—

—

—

—

2(0.31)

6(0.45)

—

1(0.49)

3(0.92)

8(1.11)

—

—

7(0.19)

Nematoscelis spp.

—

—

—

—

—

—

—

—

—

—

1(0.38)

—

3(0.07)

Thysanopoda aequalis

—

—

—

—

—

—

1(0.60)

—

—

—

2(1.32)

3(46.9)

2(14.3)

Euphausiid larva

2(0.26)

1(0,21)

1(0.38)

—

1(0.17)

—

—

—

—

3(0.66)

1(0.22)

—

—

Ostracod • 1 .0 mm

1(0.11)

—

—

—

—

—

—

—

2(0.92)

—

—

—

—

Ostracod 1.0-1.4 mm

—

—

—

—

1(0.02)

3(0.04)

1(0.09)

—

1(0.09)

—

1(0.04)

1(0.05)

1(0.02)

Ostracod 1.5-1.9 mm

—

1(0.10)

—

—

1(0.04)

2(0.03)

1(0.14)

—

—

5(0.33)

—

—

—

Ostracod 2 0-2.9 mm

—

—

—

—

—

1(0.10)

—

—

1(1.22)

—

—

—

—

Amphipod 1.0-1.9 mm

—

1(0,18)

—

—

—

—

—

—

—

—

—

—

—

Amphipod 2.0-2.9 mm

—

—

—

—

—

—

—

—

—

—

1(0.27)

3(1.10)

1(0.17)

Amphipod 33.0 mm

1(1.6)

—

—

—

—

—

—

—

—

—

—

—

—

Penaeidean larva

—

1(3,0)

—

—

—

—

—

—

—

—

—

—

1(x)

other prey: 70 m: 26-35 mm-

36-45 mm-

90 m: 36-45 mm-

110 m: 36-45 mm-

46-50 mm-

170 m: 36-45 mm -

46-54 mm-

-2 Clausocalanus spp. (0.09), 1 Neocalanus spp. (1.2), 1 Scolecithrix danae (0.69)

-1 mysid (4.5)

-1 Euaetideus acutus (0.05)

-1 Thysanopoda sp. (1.4)

-2 megalopae (5.4), 1 Undinula darwini (1.73), 1 cyclopoid (0.09), 1 fish larva (0.31)

-1 Penaeidean adult (8.94)

-1 Nematobrachion sexspinosus (9.51)

TABLE 5.-

— Stomach contents of Lampanyctus nobilis. Format ;

as in Table 4.

Depth

70 m

No

90 m

110 m

Standard length, mm
No. examined
No. with intact prey
No. of intact prey

Prey type

36-45
28
19
56

47-57

11

8

18

64-78
8
5
9

36-45 46-60
35 30
22 19
45 33

(Apparent search volume

37-45
18
12
32

. m^)

45-60 62-75
13 23
10 16
28 61

76-86
17
13
25

Aetideidae 2.0-3.0 mm
Aetideidae >3.0 mm
Euchaeta media
Pleuromamma xiphias
P xiphias CV
P abdominalis
P. gracilis

Candacia longimana
Candacia spp. CV, CVI
Paracandacia spp. CV, CVI
Oncaea spp. >0.6 mm
Corycaeus spp.
Euphausia spp.
Stylocheiron spp.
Thysanopoda aequalis
Thysanopoda spp.

1(0.19) — —

1(0.19) — —

- - 1(1.25)

13(0.53) 3(0.29) —

1(0.15) — —

3(0.06) 1(0.05) —

2(0.47) 5(2.60) —

1(0.04) — —

2(0.19) — —

2(0.04) — —

11(0.09) 5(0.09) 5(0.16)

5(0.20) — —

2(3.60) 1(4.30) —

1(5.80) — 1(22.2)

2(0.15)
1(0.24)
2(0.02)
1(0.07)
6(0.43)
4(0.08)
1(0.19)
4(0.20)
3(0.07)
2(0.17)

8(1.21)
2(0.38)
1(0.09)

1(0,05)
3(0.27)

2(0.02)
1(0.08)
2(0.17)
3(0.07)
2(0.44)

2(0.06)

1(0.05)
4(0.70)
3(0.66)
1(0.22)

1(x) 1(x)

— — 2(0.12) —
2(0.31) 1(0.18) 4(0.46) 2(0.28)

— 1(0.17) - -
6(0.35) 10(0.71) 18(0.79) 5(0.27)
2(0.25) 1(0.15) — —
1(0.17) — 2(0.25) —
2(0.03) 1(0.02) — —
1(0.19) 3(0.69) — —
1(0.17) _ _ _

— — 1(0.14) —

— — 1(0.04) —
5(0.80) 6(1.15) 12(1.44) 4(0.59)
4(1.95) 4(2.34) 3(1.09) 5(2.25)
3(6.75) — 5(8.44) 1(2.1)
1(4,9) — 4(14.7) 2(9.1)

626

CLARKE: DIETS OF FOURTEEN SPECIES OF MESOPELAGIC FISHES

Table 5.— Continued.

Depth

Standard length, mm
Prey type

70 m

90 m

110m

36-45 47-57 64-78

36-45 46-60 37-45

No. (Apparent search volume, m')

45-60 62-75 76-86

Euphausiid larva 1(0.12)

Ostracod ■ 1 .0 mm —

Ostracod 1 ,0-1 .4 mm —
Ostracod 1 .5-1.9 mm

Ostracod 2 0-2.9 mm —

Amphipod 1.0-1.9 mm 1(0.11)

Amphipod 2.0-2.9 mm 5(1.75)

Amphipod s3.0 mm —

Penaeldean juvenile -i- adult —

Other prey: 70 m: 36-45 mm

1(0,14) 1(0.22)

1(0.83)

2(0.38)
2(0.20)

2(0.26)

1(0.03)
1(0.05)

3(0.70)

2(3.60)
1(0.60)

— 2(3.00)

— — 2(1.76) 2(2.20)

— — 1(3.5) 1(4.2) 4(10.4) —

1 Scolecithrix danae (0,65), 1 Scottocalanus spp. (0,25),

1 Neocalanus spp, (1,14)
1 Lucicutia spp. (0.07)
47-57 mm — 1 Nannocalanus minor (0.12)
64-78 mm — 1 mysid (10.09)
90 m: 36-45 mm— 1 Eucalanus spp. (2.30)

46-60 mm — 1 Heterorhabdus spp. {-^). 1 Aetideidae C s2,0 mm (0,05), 1 megalopa (1,05)
110 m: 62-75 mm — 1 Euchaeta spp. (1.6), 1 Pleuromamma abdominalis C (0.09), 1 Nematoscelis spp
76-86 mm— 1 Carldean juvenile (19.2)

(0.96)

Table 6. — Stomach contents oi Triphotorus nigrescens and Notolychnus valdiuiae.

Format as in Table 4.

Species
Depth

Standard length, mm
No, examined
No, with intact prey
No, of intact prey

Prey type

T. nigrescens
70 m

19-25 26-37

32 29

30 28

108 99

No, (Apparent search volume, m^)

90 m

16-24
59
28
52

N. valdiviae
110m

19-24

77

62

138

170 m

20-23
88
55
92

Calanus tenuicornis —

Nannocalanus minor 2(0,07)

Undinula vulgaris 2(0,83)

Undinula darwini 1(0,28)

Clausocalanus spp. —

Gaetanus spp. —

Aetideidae C < 2.0 mm —

Aetideidae C 2.0-3.0 mm 2(0.24)

Aetideidae CV, CVI >3,0 mm 2(0,24)

Euchaeta media 1(0,21)

Scolecithrix danae 1 (0,42)

Scolecithncella spp. < 1.0 mm 2(0.15)

Scolecithricella spp. s=1.0 mm 1(0.02)

Scottocalanus spp. CV, CVI —

Pleuromamma xiphias 14(0,36)

P xiphias CV —

P abdominalis 5(0,49)

P abdominalis C —

P gracilis 6(0.08)

Lucicutia spp. —

Heterorhabdus spp. —

Candacia longimana 3(0.42)

Candacia spp. CV, CVI —

Paracandacia spp. CV, CVI 2(0,05)

Unident, calanoid —

Oncaea spp. >0.6 mm 43(2.65)

Corycaeus spp. 2(0.02)

Euphausia spp 4(0,02)

Euphausiid larva 3(0,23)

Ostracod < 1.0 mm 3(0,20)

Ostracod 1 ,0-1.4 mm —

Ostracod 1.5-1.9 mm 1(0.04)

Amphipod 1.0-1.9 mm 2(0.14)

Amphipod 2.0-2.9 mm 3(0.67)

Amphipod 33.0 mm 2(2.22)

Other prey;

T. nigrescens — 70 m

1(0.04)
1(0.45)
1(0.30)

1(0.13)
2(0.26)
2(0.45)
1(0.45)
2(0.16)
2(0.04)
1(0.17)
25(0.69)
1(0,04)
3(0.31)
2(0.02)
6(0.08)
1(0.05)

5(0.74)

4(0.12)

1
12(0.79)

1(0.01)
12(0.07)

2(0.16)

1(0.02)
1(0.04)
1(0.07)
1(0.24)
1(1.19)

1(0.01)

1(0.10)
2(0.07)
1(0.04)
1(0.06)
1(0.19)

3(0.02)

1(0.06)

2(0.03)
1(0.10)

5(0.74)
1(0.04)

1
22(1,48)

4(0.31)
3(0,06)
1(0,03)
1(0,10)

2(0,01)

1(0.01)

2(0,03)

2(0.06)
1(0.03)

1(0)

14(0.16)
4(0.10)
9(0.30)

2(0.01)
1(0.05)
2(0.40)
3(0.11)
1(0.03)
3(0.11)
2
74(1.99)

1(0.03)
3(0.45)
2(0.28)

1(0.10)
3(0.23)

1(0.03)

1(0.04)
4(0.42)
4(0.29)
10(0.83)
2(0.44)
1(2.00)

2(0.03)
1(0.49)
25(1.10)
4(0.09)
1(0.20)
2(0.20)

1(0.02)
1(0.13)
5(1.75)

2(^)
3

21(0.38)

19-25 mm
26-37 mm

N. valdiviae

-110m:

— 170m:

19-25 mm

20-23 mm

— 1 Neocalanus spp. (0.72)

— 1 megalopa (1.38), 1 Stylocheiron spp, (0,14)

1 Euaetideus acutus (0 08), 2 Euchaeta spp, C
>2,0 mm (0.42)

— 1 Scolecithrix bradyi (0.02), 1 Pleuromamma
gracilis CV (0,02), 1 Heterorhabdus papilliger (0,02),
1 Stylocheiron spp, (0.09)

— 1 zoea (-t)

627

FISHERY BULLETIN: VOL. 78, NO. 3

small to medium copepods and euphausiids, the
latter of which were taken frequently.

Notolychnus valdiviae (Table 6)

Notolychnus valdiviae occurs throughout the
depth range covered by the three deepest samples
as evidenced by the high numbers of specimens
available from each depth. With such large
catches, it is unlikely that data from the deeper
samples were seriously affected by catches in
transit to and from towing depth.

Microzooplankton made up over half the diet at
90 and 110 m and about one-fourth at 170 m (Table
2). These were almost all Oncaea. If the ASV's are
roughly corrected for undersampling, they are
still relatively high at 90 and 110 m.

Most of the remaining prey were medium to
large copepods; P. xiphias, P. abdominalis , C. lon-
gimana, and aetideids were important at one or
more depths. Euphausiids were rarely taken.
ASV's for items from 90 and 110 m were mostly
rather low (Table 2). At 170 m ASV's for a large
fraction of items and prey types were high (> 0.80
m^) mainly due to high values for P. xiphias, C.
longimana, and 2-3 mm aetideids. This plus the
lower proportion of microzooplankton in the diet
at 170 m indicates increased preference for larger
prey

Ceratoscopelus warmingi (Table 7)

Ceratoscopelus warmingi took a wide variety of
sizes and taxa of prey. Small fractions of the diets
of the large fish were microzooplankton — mostly
Oncaea spp., but including several species of small
calanoids, ostracods, and gastropod veligers. On-
caea and small ostracods made up over a third of
the diet of the small fish from 90 m (Table 2). If the
ASV's for Oncaea are decreased by a factor of 4 to
roughly correct for undersampling, preference
equivalent to that for larger prey is indicated.
ASV's for other microzooplankton were very low.
All sizes of calanoids and small to medium os-
tracods were taken, but ASV's were usually low.

Many prey items were large and most of these
had high ASV's, resulting in large fractions of the
prey from large fish at 70 and 110 m having high
ASV's (Table 2). Euphausiids, decapods and their
larvae, large amphipods, and ostracods were
taken frequently, but fish, siphonophores,
heteropods, and polychaetes (all >5 mm) were also

Table 7. — Stomach contents of Ceratoscopelus warmingi. For-
mat as in Table 4.

Depth

70 m

90

m

110m

Standard length, mm

46-69

38-45

46-62

46-68

No examined

23

16

90

25

No. with intact prey

12

12

61

14

No, of intact prey

57

34

179

55

Prey type

No

(Apparent search volume.

m^)

Nannocalanus minor

1(0.08)

1(0.18)

—

—

AetideldaeC 2.0-3.0 mm

1(0.30)

—

1(0.02)

—

AetldeidaeCV, CVI >3.0 mm

1(0.30)

2(0.28)

3(0.08)

2(0.26)

Pleuromamma xiphias

2(0.13)

3(0.05)

9(0.03)

2(0.10)

P abdominalis

—

2(0.27)

6(0.16)

3(0.43)

P. abdominalis C

1(0.02)

1(0.22)

1(0.04)

—

P gracilis

2(0.06)

2(0.07)

1(0.01)

—

Lucicutia spp.

1(0.11)

—

4(0.09)

1(0.23)

Paracandacia spp. CV, CVI

—

—

1(0.01)

1(0.16)

Unident. calanoid

—

2

—

2

Oncaea spp. >0.6 mm

7(1.08)

10(1.57) 20(0.62)

4(0.48)

Corycaeus spp.

—

1(0.07)

2(0.03)

Euphausia spp.

6(0.08)

3(0.83)

8(0.44)

7(0.96)

Stylocheiron spp.

—

—

4(0.27)

7(2,90)

Thysanopoda aequalis

3(8.60)

2(0.69)

6(0.41)

6(11.6)

Euphausiid larva

3(0.58)

1(0.35)

3(0.20)

2(1.3)

Ostracod <1.0 mm

3(0.09)

2(0.36)

3(0.11)

—

Ostracod 1.0-1 4 mm

1(0.06)

—

12(0.12)

2(0.24)

Ostracod 1.5-1 9 mm

2(0.18)

1(0.08)

9(0.72)

—

Ostracod ^2.0 mm

5(4.50)

—

5(0.34)

3(4.30)

Amphipod 1 .0-1.9 mm

—

—

5(0.05)

—

Amphipod 2.0-2.9 mm

—

—

3(0.53)

—

Amphipod 2=3. 0 mm

6(14.2)

1(2.40)

4( 1 .90)

—

Penaeidean juvenile -t- adult

—

—

1(0.55)

2(5.90)

Mysid

1(4.20)

—

—

2(20.4)

Polychaete

—

—

1(0.08)

2(1.70)

Siphonophore

1(0.12)

—

5(0.06)

—

Fish larva

2(0.79)

—

8(0.94)

4(3.60)

Cyclothone spp.

1(»)

—

26(x)

—

Other prey:

70 m — 1 Undinula darwini (0.69). 1 Heterorhabdus papilliger (0.10),
— 1 Augaptilidae (0.52), 1 megalopa (3.20), 2 stomatopod larvae
— (x), 1 Ctenophore (»).
90 m — 46-62 mm — 1 Calanus tenuicornis (0.01), 2 Clausocalanus spp.
(0.03), 1 Pseudocalanidae (0.55), 1 Ischnocalanus sp. {^),
1 Aetideidae C <2.0 mm (0.02), 1 Euchaeta media (0.09),
1 Scolecithrix bradyi (0.04), 2 Candacia longimana (0.14),
5 Candacia spp. CV, CVI (0.09), 1 Caridean larva (0.23),
1 Penaeidean larva (0.33), 2 Anomuran larvae (x), 1 Chaetognath
(0), 6 Heteropods (1.14), 2 Gastropods (0.16).
110 m — 2 Nematoscelis spp. (2.20) , 1 Nematobrachion sexspinosus (23.8).

present. Items listed as "fish" (Table 7) were all
epipelagic larvae or juveniles, but C. warmingi
also frequently eats Cyclothone, which it en-
counters only during the day. Results of studies of
feeding chronology (Clarke 1978) indicate that
Ceratoscopelus warmingi takes such large items
both day and night. While it is possible that the
other large items mentioned above could have
been taken at depths other than those sampled
and thus that the high ASV's are artifacts, these
items do cooccur with C warmingi at the depths
sampled and those recorded were relatively fresh
and intact in stomachs offish collected in the latter
half of the night. {Cyclothone were, however,
eliminated for calculations in Table 2.) Even al-
lowing for the probability that ASV's of some of the
largest prey types were overestimated due to
avoidance of the plankton nets (see Methods sec-

628

CLARKE: DIETS OF FOURTEEN SPECIES OF MESOPELAGIC FISHES

tion), the high ASV's observed probably indicate a
real preference for large prey.

A 48 mm Ceratoscopelus warmingi female from
90 m had no lenses in the eyes. The outer eye cover
was intact and the space normally occupied by the
lens was filled with gelatinous material similar to
the humor in the rest of the eye. Thus the lenses
were not missing due to damage during capture or
even a recent injury. This fish had not only man-
aged to reach adult size, but had three fresh
copepods and remains of others and a euphausiid
in the stomach.

Bolinichthys longipes (Table 8)

Trematode parasites were frequently present in
the stomachs of B. longipes : The large fish from 110
m averaged over six parasites/stomach (Table 8).
Parasite load and frequency was much lower in the
small fish from 70 m. It was not possible, due to

insufficient numbers, to rigorously compare
stomach contents of fish with and without para-
sites from any given depth-size group; however,
while some of the unparasitized fish had more
intact prey than most parasitized specimens, there
were no obvious differences in prey type or fre-
quency. Thus the parasites did not appear to bias
the diet directly or by effectively increasing diges-
tion rate and causing more resistant prey types to
appear as intact in disproportionate frequencies.
Microzooplankton, 90% of which were Oncaea
spp., made up the great majority of food items in
all groups (Table 2). A large fraction of the Oncaea
spp. eaten were very small (^0.6 mm); such sizes
were rarely eaten by most of the other fishes con-
sidered. The ASV's for these small forms were ab-
surdly high; data from very fine mesh plankton
nets would be needed to estimate preference. If the
ASV's for the large Oncaea are reduced by a factor
of 4 (see Methods section), the values are still quite

Table 8. — Stomach contents of Bolinichthys longipes and Diogenichthys atlanticus. Format as in Table 4.
Also given are incidence and number per fish of trematode parasites in B. longipes.

Species

8. longipes

D. atlanticus

Depth

70 m

90m

110m

70 m

Standard length, mm

17-26

27-35

36-47

26-35

36-49

17-21

No examined

11

25

35

38

35

9

No. with Intact prey

11

25

35

38

35

6

No. of Intact prey

78

127

168

238

323

43

No. with trematodes

3

19

35

36

32

—

Average (range) no. fish

0.36(0-2)

1 .84(0-6)

3.48(1

-9)

2.74(0-8) 6.03(0-12)

—

Prey type

No.

(Apparent search voli

J me, m^)

Calanus tenuiformis
Acrocalanus spp.
Clausocalanus spp.
Euaetideus acutus
Aetldeldae CV, CVI >3.0 mm
Scolecittirix bradyi
Scolecithricella spp. <1.0 mm
Scolecithricella spp. sl.O mm
Pleuromamma xiphias
P. abdominalis
P gracilis
Lucicutia spp.
Heterortiabdus papilliger
Candacia longimana
Candacia spp CV, CVI
Paracandacia spp. CV, CVI
Unident. caianoid
Oittiona spp.
Oncaea spp. >0.6 mm
Oncaea spp. sO.6 mm
Corycaeus spp.
Microsetella spp.
Euptjausia spp.
Euphausiid larva
Ostracod <- 1 .0 mm
Ostracod 1 .0-1.4 mm
Ostracod 1 .5-1.9 mm
Amphipod 1 .0-1 .9 mm
Chaetognath
Gastropod larva

Other prey: B longipes

1(0.07)

1(0.33)
1(0.12)

1(0.07)

1(0.38)

1(0.07)
1

17(2.86)
42(95)

1(0.03)

2(-)

2(0.42)
1(0.18)

3(0.31)
1(0.18)

1(0.03)

2(0.03)

1(0.10)
1(0.07)
2(0.21)
1(0.12)

1(0.01)
1(0.06)
2(0.03)

1(0.17)
1(0.04)
2(0.04)

2
1(0,05)

45(3.40)

52(x)
2(0.07)

1(=c)

5(0.44)
1(0.11)

1(0.01)

2(0.15)
1(0.05)

2(0.15)
1(0.09)

2(0.01)

1(0.01)

1(0.08)

1(0.05)

2(0.24)

2(0.06)

5(0.15)

2

1(0.04)

86(4.64)

42(x)
1(0,03)

1(x)

3(0.19)
2(0.03)
2(0.05)
1(0.08)

1(0.14)

2(0,06)

1(0)

4(0,07)

2(0,11)

4(0,02)

1(0,08)

1(0.03)

2(0.12)

8(0.41)

1(0,06)

2

125(5,48)
78(205)

2(x)

2(0.09)
1(0.07)

1(0.01)

1(0.01)
2(0.06)
1(0.05)
4(0.14)

10(0.20)
2(0.11)
2(0.01)

10(0.66)
26(1.46)
15(0.97)
6

150(7.14)

84(240)

2(0.04)

1(0.05)
1(0.27)
2(0.50)
1(0.05)
1(0.08)

1(0.02) —

70 m: 17-26 mm— 1 Pontella sp. (x)
90 m: 26-35 mm— 2 Aetldeldae C -; 2,0 mm (0,08), 1 Euctiaeta media (0,21)
36-47 mm— 2 Loptiottirix spp, (0,14), 1 Gaetanus sp. (0.08).
1 Pareuctiaeta sp (^), 1 zoea (9.50)
110 m: 26-35—1 Amphipod <1.0 mm (^)
36-49—1 Stylocheiron sp. (0.17)

3(5.40)

2(0.45)
1(0.10)

1(0.06)
2(0.45)

1(0.14)
3

11(3.40)
11(45.8)

4(x)
1(0.03)

1(0.18)
1(0,33)
1(0.05)

629

FISHERY BULLETIN: VOL. 78, NO. 3

high, indicating a real preference for Oncaea. Ex-
cept for three prey types not taken by the plankton
tows, the ASV's for other microzooplankton are
low even without any adjustment for undersam-
pling.

Except for the large fish from 110 m, macrozoo-
plankton were taken very infrequently and mostly
had low ASV's. The large fish from 110 m had eaten
Pleuromamma and candaciids frequently, and this
was the only group from which euphausiids were
recorded. The data indicate some preference for
candaciids. ASV's for these copepods were high for
the large fish from 110 m and sometimes fairly
high in other groups.

Diogenichthys atlanticus (Table 8)

About three-fourths of the items eaten by D.
atlanticus were microzooplankton — mostly On-
caea spp. The ASV for the grossly undersampled
small Oncaea is meaningless, but if ASV's for the
other microzooplankton are reduced by a factor of
4, there is reasonable indication of preference for
the large Oncaea spp. and Acrocalanus spp. Most
of the macrozooplankton were small to medium
copepods, and ASV's of most types were low.

Benthosema suhorhitale (Table 9)

Benthosema suhorhitale usually does not occur
as deep as 110 m, but the number collected at that
depth was considerably larger than that expected
from catches in transit. Thus the data are probably
not seriously affected by fish caught at shallower
depths. The sample from 90 m, which was taken at
a different time of the year, had too few B. suhor-
hitale to merit analysis.

Microzooplankton were important fractions of
the diet of B. suhorhitale; they made up over half
the items from the small fish and slightly less for
the larger ones. Almost all were Oncaea spp. —
mostly the larger forms. Macrozooplankton were
mostly medium to large copepods, but also in-
cluded euphausiids and large amphipods. Such
prey, especially P. xiphias and candaciids, were
eaten more frequently by the large fish from both
depths. ASV's for most macrozooplankton prey
types were 0.40 m^ or less. If the ASV's for the
large Oncaea spp. are reduced by a factor of 4, they
are commensurate with those of the macrozoo-
plankton.

630

Table 9. — Stomach contents of Benthosema suhorhitale. For-
mat as in Table 4.

Depth

70

m

110 m

Standard length, mm

18-25

26-30

26-32

No. examined

20

48

38

No. with Intact prey

11

32

26

No. of intact prey

29

69

47

Prey type

No. (Apparent search volume, m^)

Nannocalanus minor

—

—

1(0.98)

Undinula darwini

1(0.75)

2(0.52)

—

Clausocalanus spp.

1(0.07)

—

1(0.02)

Aetideidae C 2.0-3.0 mm

—

—

3(0.12)

Aetideidae CV, CVI >3.0 mm

1(0.33)

1(0.11)

2(0.14)

Euchaeta media

—

1(0.20)

—

Scolecittirix danae

1(1.14)

—

—

Pleuromamma xiphias

1(0.07)

11(0,27)

8(0.22)

P. xiphias CV

1(0.10)

1(0.03)

—

P abdominalis

1(0.27)

2(0.18)

2(0.15)

P gracilis

1(0.04)

2(0.02)

3(0.02)

Heterorhabdus papilliger

1(0.11)

—

—

Candacia longimana

1(0.38)

3(0.39)

—

Candacia spp. CV, CVI

—

1(0.09)

1(0.08)

Paracandacia spp. CV, CVI

—

5(0.13)

3(0.26)

Unident. calanold

1

—

—

Oncaea spp. >0.6 mm

10(1.68)

21(1,22)

19(1.22)

Oncaea spp. s;0.6 mm

4(9.09)

8(6.25)

1(3.85)

Corycaeus spp.

—

2(0.02)

1(0.03)

Euphausia spp.

—

3(0.01)

1(0.07)

Thysanopoda aequalis

—

2(2.20)

—

Euphausiid larva

3(0.63)

1(0.07)

—

Ostracod 1.5-1.9 mm

1(0.10)

1(0.03)

—

Amphipod 1 .0-1.9 mm

—

1(0.06)

—

Amphlpod 2.0-2.9 mm

—

—

1(0.42)

Zoea

—

1(0.04)

—

Diaphus schmidti (Table 10)

The numbers of prey per fish and diversity of
prey were relatively high for D. schmidti; several
small copepods and noncrustacean prey that were
either rare or absent in the diets of other species
were taken relatively frequently.

Microzooplankton made up SO-SO^f of the items
(Table 2); half to two-thirds of these were Oncaea.
If ASV's for Oncaea are roughly corrected, they
are still quite high. ASV's for other types of micro-
zooplankton were variable.

Although the composition of macrozooplankton
prey was generally similar for all groups, there
were some differences between sizes or depths.
Pleuromamma and Euphausia spp. were eaten
more frequently at 70 m than at 90 m. Overall,
Corycaeus spp. were the most frequently eaten
prey, but at both depths, frequency and ASV's were
higher for the small fish. About half the prey of the
small fish from 70 m had high ASV's. These were
mostly Corycaeus spp., but also included several
medium to large prey types. Among the large fish
from 70 m, a few types of large prey had high
ASV's, but most prey from both these and both
groups from 90 m had low ASV's. The generally
higher ASV's associated with the small fish from
70 m appear to have resulted mostly from higher

CLARKE: DIETS OF FOURTEEN SPECIES OF MESOPELAGIC FISHES

Table lO. — Stomach contents of four Diaphus species. Format as in Table 4.

Species

D. schmidti

D. perspicillatus

D. fragiiis

D trachops

Depth

70

m

90

m

70 m
46-56

90 m
34-44

170 m

Standard length, mm

31-35

36-40

27-35

36-41

36-50

No examined

12

15

30

21

20

6

15

No with Intact Items

11

14

30

19

17

5

12

No. of Intact Items

162

124

188

81

457

29

32

Prey type

No. (Apparent search volume, m^)

Neocalanus spp.

2(3.90)

—

—

—

2(2.60)

—

—

Calanus tenuicornis

—

—

2(0.03)

—

—

1(0.08)

—

Nannocalanus minor

2(0.18)

2(0.14)

3(0.22)

—

8(0.48)

—

—

Undinula vulgaris

1(1.10)

1(0.89)

—

—

6(0.44)

—

—

U. darwini

5(3.80)

2(1.20)

1(0.09)

—

4(2.00)

—

—

Acrocalanus spp.

—

1(0.76)

l(-)

—

2(1.30)

1(x)

—

Clausocalanus spp.

1(0.07)

—

2(0.06)

1(0.05)

—

—

Gaetanus + Chiridius spp.

—

—

—

1(0.15)

—

—

7(3.30)

Aetldeidae C -20 mm

—

—

—

—

—

1(0.21)

4(1.30)

Aetideldae C 2.0-3.0 mm

—

—

3(0.10)

—

—

1(0.21)

1(0.38)

Aetldeidae CV, CVI ^3.0 mm

—

1(0.26)

—

1(0.09)

9( 1 .90)

—

2(2.00)

Euchaeta media

1(0.57)

—

—

—

5(1.80)

—

—

Scolecithrix danae

2(2.30)

1(0.89)

-—

—

—

—

—

Scottocalanus spp. CV. CVI

—

—

—

—

1(2.80)

—

2(4.50)

Pleuromamma xiphias

2(0.14)

6(0.33)

4(0.03)

5(0.05)

29(1.30)

5(0.20)

1(0.19)

P. xiphias CV

2(0.20)

—

—

—

1(0.06)

—

—

P abdominalis

6(1.60)

7(1.50)

2(0.11)

3(0.25)

23(4.00)

1(0.32)

1(0.93)

P abdominalis C

—

1(0.02)

—

1(0.14)

3(0.05)

—

—

P gracilis

10(0.35)

4(0.14)

3(0.04)

3(0.07)

51(1.16)

1(0.08)

—

Centropages spp.

—

—

1(1.70)

—

2(1.40)

—

—

Lucicutia spp

4(0.49)

5(0.48)

5(0.48)

1(0.15)

18(1.40)

—

2(0.17)

Heterorhabdus papilliger

1(0.11)

1(0.09)

—

—

—

—

1(0.47)

Candacia longimana

—

1(0.30)

1(0.14)

—

5( 1 .20)

1(0.83)

—

Candacia spp. CV, CVI

—

1(0.21)

3(0.11)

2(0.11)

1(0.17)

—

—

Paracandacia spp. CV, CVI

2(0.15)

2(0.11)

1(0.06)

2(0.06)

20(0.96)

1(0.11)

—

Acartia spp.

1(0.24)

1(0.19)

1(0.15)

—

2(0.31)

1(0.90)

—

Unident. calanold

8

4

8

3

38

—

3

Oithona spp.

—

—

1(0.04)

—

1(0.07)

—

—

Oncaea spp. '0.6 mm

32(5.39)

35(4.63)

46(2.89)

24(2.38)

121(13.20)

9(3.39)

2(0.17)

Corycaeus spp.

40(1.25)

16(0.39)

23(0.69)

6(0.28)

34(0.69)

—

2(0.34)

Other cyclopoids

1(0.61)

2(0.95)

1(0.04)

—

2(0.78)

—

—

Euphausia spp.

7(0.10)

5(0.06)

4(0.44)

1(0.17)

13(0.12)

—

—

Stylocheiron spp.

2(0.69)

1(0.27)

—

1(0.22)

4(0.09)

—

—

Thysanopoda aequalis

—

—

—

1(0.22)

—

—

1(20.80)

Euphausiid larva

2(0.42)

—

11(1.50)

3(0.66)

6(0.81)

—

—

Ostracod - 1 .0 mm

5(0.91)

4(0.57)

10(0.72)

3(0.34)

2(0.24)

4(1.70)

1(0.22)

Ostracod 10-14 mm

5(0.33)

2(0.10)

3(0.06)

1(0.03)

6(0.25)

1(0.12)

—

Ostracod 1.5-1.9 mm

2(0.20)

3(0.24)

7(0.22)

6(0.31)

4(0.26)

—

—

Amphipod 1 .0-1.9 mm

—

1(0.14)

1(0.09)

1(0.15)

—

—

—

Amphipod 2.0-2.9 mm

—

2(0.95)

3(1.07)

—

—

—

—

Amphipod 33.0 mm

—

1(2.0)

—

—

1(1.70)

—

—

Caridean larva

1(0.18)

2(0.29)

—

1(0.75)

16(1.90)

—

—

Penaeldean larva

—

—

1(0.67)

—

—

1(4.00)

—

Zoea

—

—

1(11.1)

—

—

—

1(~x)

Megalopa

3(10.50)

—

1(0.67)

—

1(2.30)

—

—

Chaetognath

—

—

2(0.02)

—

2(0.04)

—

—

Larvacean

2(1.30)

1(0.52)

—

—

—

—

—

Gastropod larva

4(0.13)

3(0.08)

11(1.70)

1(0.25)

3(0.06)

—

—

Pelecypod larva

3(2.30)

—

14(20.30)

6(13.70)

2(0.98)

—

—

Other prey: O. schmidti — 70 m: 31-35 mm — 1 Eucalanus sp. (1 .60), 2 isopods (^)

36-40 mm — 1 Neocalanus CV (0.1 1). 1 Unident. Harpactacoid (y-), 1 Thysanopoda sp. (7.90),
2 pteropods >1 0 mm (x)
90 m: 27-35 mm — 1 Scolecithrix bradyi (0.09). 1 Calocalanus sp. (^-). 2 heteropods (0.95),
1 Penaeldean juvenile,' adult (1.10), 1 polychaete (0.17), 1 fish larva (0.24)
36-41 mm — 1 Ischnocalanus sp. (-.'-), 1 amphipod 1.0 mm (x), i ostracod >3.0 mm (1.10)
D. perspicillatus — 3 Euchaeta rimana (^.). 1 Euchaeta sp. (0.63). 1 Scolecithricella sp. <1.0 mm

(0.13), 1 Nematoscelis sp. (2.70), 1 Caridean juvenlle/adult (0.84),
1 polychaete larva (x), 1 insect (■.=)
D. trachops — 1 Siphonophore (11.90)

numbers of prey per fish rather than from any
obvious differences in diet composition or relative
preference.

Diaphus perspicillatus (Table 10)

The number of prey per fish for D. perspicillatus
was the highest of any species included and, possi-

bly because of this, so was the diversity of prey.
Almost a third of the prey were microzooplankton
(Table 2) — the great majority of these, Oncaea
spp. The AS V for Oncaea , if corrected, is still high,
as were the ASV's for about half the macrozoo-
plankton prey types. The most frequent macrozoo-
plankton were small copepods: P. gracilis,
Lucicutia, Paracandacia; but several medium to

631

FISHERY BULLETIN: VOL. 78, NO. 3

large prey: Pleuromamma xiphias, P. ah-
dominalis, and large aetideids, were eaten fre-
quently. Several small to medium copepods, the
most frequent of which was Corycaeus, had inter-
mediate ASV's (0.41-0.70 m^). Very few prey had
low ASV's; half of these were ostracods and
euphausiids.

Diaphus fragilis (Table 10)

Few D. fragilis were available, and number of
prey items was low. The data are most similar to
those for D. schmidti. Microzooplankton ac-
counted for about one-half the diet. The corrected
ASV for Oncaea spp., the dominant microzoo-
plankton, and those of most macrozooplankton
were low. Only two prey types — each taken only
once — had ASV's over 0.40 m^.

Diaphus trachops (Table 10)

Data for D. trachops are few, but indicate that its
diet is quite different from those of the other

Table ll. — Stomach contents of Melamphaes danae and Breg-
maceros japonicus . Format as in Table 4.

Species

M. danae

B.

japonicus

Depth

70 m

90 m

110m

70 m

Standard length, mm

17-22

19-22

19-22

38-51

No. examined

26

15

10

23

No. with intact prey

18

10

8

18

No of intact prey

54

32

34

41

Prey type

No.

(Apparent search volume

, m3)

Neocalanus spp.

3(3.60)

—

1(0.96)

—

Calanus lenuicornis

—

—

1(0.05)

—

Nannocalanus minor

2(0.11)

—

3(9.60)

1(0.06)

Undinula darwini

1(0.46)

—

1(8.90)

—

Clausocalanus spp.

—

—

1(0.05)

—

Aetideidae C 2.0-3.0 mm

—

1(0.10)

—

—

Aetideidae CV, CVI > 3.0 mm

1(0.20)

—

1(0.23)

—

Euchaeta rimana

3(^)

—

2(x)

1(^)

Scolecithricella spp. < 1 .0 mm

—

1(0.31)

—

—

Pleuromamma xiphias

—

—

—

12(0.52)

P. xipliias CV

—

—

—

2(0.12)

P abdominalis

—

—

—

5(0.82)

P. gracilis

—

—

—

1(0.02)

Heterorhabdus papilliger

—

—

—

1(0,07)

Candacia longimana

—

—

—

2(0.46)

Paracandacia spp.

1(0.04)

—

1(0.29)

—

Unident. calanoid

—

1

—

—

Oncaea spp. >0.6 mm

—

1(0.19)

—

—

Oncaea spp. sO.6 mm

—

—

—

1(1.38)

Corycaeus spp.

4(0.07)

5(0.45)

2(0.18)

—

Euphausia spp.

1(0.01)

—

1(0.24)

2(0.02)

Euphausiid larva

4(0.51)

4(1.67)

6(6.95)

4(0.51)

Ostracod <1.0 mm

4(0.44)

3(0.65)

1(1.10)

—

Ostracod 1.0-1.4 mm

2(0.08)

5(0.30)

—

—

Ostracod 1.5-1.9 mm

2(0.12)

2(0.19)

—

—

Amphipod 1 .0-1.9 mm

5(0.57)

—

—

—

Amphipod 2.0-2.9 mm

5(1.85)

—

2(2.70)

—

Caridean larva

1(0.11)

—

2(3.20)

4(0.44)

Penaeidean larva

1(1.80)

—

—

—

Mysid

—

—

1(17.90)

—

Chaetognath

6(0.11)

6(0.18)

7(0.81)

5(0-09)

Heteropod

—

1(1.43)

—

—

Gastropod larva

8(0.16)

2(0,95)

1(0.72)

—

Diaphus spp. in that few microzooplankton were
eaten. Most prey items were medium to large
forms and had high ASV's.

Melamphaes danae (Table 11)

Microzooplankton made up minor fractions of
the diet of M. danae; most were either small os-
tracods or gastropods. Among the other prey only
chaetognaths and euphausiid larvae were consis-
tently important. At 70 and 90 m, 22 and 26% of
the prey had high ASV's; most other types had low
values (Table 2). At 110 m, the great majority of
prey types and items had high ASV's. For most
prey types, the ASV's at different depths were
either consistently high (euphausiid larvae,
A^eocaZa^Ms, amphipods) or low (ostracods), but the
value for chaetognaths at 110 m was much higher
than shallower,

Bregmaceros japonicus (Table 11)

Bregmaceros japonicus ate few microzooplank-
ton; small macrozooplankton were also taken in-
frequently and usually with low ASV Most prey
were medium to large and, except for chaeto-
gnaths and Euphausia spp., ASV's were moderate
to high.

DISCUSSION

The fishes considered here clearly showed pref-
erence in a broad sense, i.e., some abundant zoo-
plankton were rarely or never taken, and the
ASV's of types regularly eaten were variable.
Though there were exceptions, these fishes gener-
ally grazed on relatively large, visible crustaceans.
Other taxa were rarely taken and then usually
with low ASV's. Most other taxa in the plankton
were either translucent forms, e.g., chaetognaths
and tunicates, or quite small, e.g., gastropod
veligers. Among the crustacean microzooplank-
ton, the densely pigmented and relatively
opaque Oncaea spp. were the only types that were
taken regularly and had high ASV's. Some appar-
ently less visible forms such as Clausocalanus and
small Scolecithricella spp. were abundant in the
plankton samples (in spite of mesh escapement),
but rarely eaten, and the undoubtedly more
numerous smaller types which mostly passed
through the plankton net mesh were absent from
almost all the fishes' diets. Among the crustacean
macrozooplankton, several translucent or weakly

632

CLARKE; DIETS OF FOURTEEN SPECIES OF MESOPELAGIC FISHES

pigmented types, e.g., Calanus tenuicornis and
Neocalanus and Pleuromamma spp. copepodites,
were abundant but mostly ignored by the fishes.

Difference between species' diets were often cor-
related with differences in one or more of the mor-
phological features examined (Figures 1-4). The

0

15 20 25 30 35 40 45 50 55 60 65 70 75 80

STANDARD LENGTH (mm)

Figure l. — Relationships between standard length and premaxillary length for 14 species of mesopelagic fishes designated by initials
of genus and species names. Lines for Lampanyctus nobilis, Triphoturus nigrescens, Notolychnus valdiviae, Benthosema suborbitale,
Diogenichthys atlanticus, Diaphus schmidti , D.perspicillatus, D. fragilis, D. trachops , and Bregmacerosjaponicus and ( dashed lines) for
Lampanyctus steinbecki, Ceratoscopelus warmingi. and Bolinichthys longipes are drawn from equations determined by least squares
regression on measurements from five or more specimens of each species over the size ranges plotted; coefficients of determination (r*)
exceeded 0.80 for all. Melamphaes danae (r^ = 0.48) is represented by the area enclosed by points from five specimens.

633

34
32-

3.0-
2.8-
26-
24-

FISHERY BULLETIN: VOL. 78. NO. 3

r

E

22

E

2.0

cr

LU

H

1.8

LU

^

<

1.6

Q

(D

1.4

LU

_l

1.2

1.0

0.8

0.6

04

0.2-

0.0

20 25 30 35 40 45 50 55 60 65 70 75 80

STANDARD LENGTH (mm)

Figure 2. — Relationships between standard length and lens diameter for 14 species of mesopelagic fishes designated by initials of
genus and species names. Lines for Lampanyctus steinbecki, L. nobilis, Ceratoscopelus warmingi, Benthosema suborbitale,
Diogenichthys atlanticus .Bolinichthys longipes ,Dixiphus schmidti ,D . perspicillatus ,D . trachops,Melamphaesdanae, and Bregmaceros
japonicus and dashed lines for Triphoturus nigrescens and D. fragilis are drawn from equations determined by least squares regression
on measurements from five or more specimens of each species over the size ranges plotted; coefficients of determination (r^) exceeded
0.80 for all except Diogenichthys atlanticus (r^ = 0.62). Notolychnus valdiviae ir^ = 0.23) is represented by the area enclosed by points
from five specimens.

634

CLARKE: DIETS OF FOURTEEN SPECIES OF MESOPELAGIC FISHES

14

20 25 30 35 40 45 50 55 60 65 70 75 80

STANDARD LENGTH (mm)

Figure 3. — Relationships between standard length and average space between gill rakers on the lower branch of the first gill arch for
12 species of mesopelagic fishes designated by initials of genus and species names. Lines for Lampanyctus nobilis, Triphoturus
nigrescens, Ceratoscopelus warmingi, Benthosema suborbitale, Bolinichthys longipes, Diaphus schmidti,D. perspicillatus, D. fragilis,D.
trachops, and Melamphaes danae and dashed line for Lampanyctus steinbecki are drawn from equations determined by least squares
regression on measurements from five or more specimens of each species over the size ranges plotted; coefficients of determination (r^)
exceeded 0.80 for all except M. danae ( r^ = 0.78). The equation for Diogenichthys atlanticus (r* = 0.60) was almost identical vdth that for
M. danae and was omitted for clarity. Notolychnus valdiviae ( r^ = 0.04) is represented by the area enclosed by points from five specimens.

most similar species were Lampanyctus steinbecki,
L. nobilis, T. nigrescens, and Notolychnus val-
diviae. All ate relatively large and opaque or pig-
mented prey. Both within and between species, the
sizes of the most frequent and most preferred prey
were roughly correlated with standard length, i.e.,

the large L. nobilis favored euphausiids and large
copepods, while A^. valdiviae and the small L.
steinbecki and T. nigrescens preferred some types
as small as Oncaea. All four species had relatively
small eyes and relatively large gill raker gaps, and
three had relatively low gill raker "areas." The gill

635

100

FISHERY BULLETIN: VOL. 78, NO. 3

1 r

70 80 90 100

STANDARD LENGTH (mm)

Figure 4. — Relationships (on logarithmic scales) between standard length and gill raker "area" (see text) for 10 species of mesopelagic
fishes designated by initials of genus and species names. Lines for Lampanyctus steinbecki, L. nobilis, Triphoturus nigrescens,
Ceratoscopelus warmingi, Benthosema suborbitale, Diaphus perspicillatus, and D. trachops are drawn from equations determined by
least squares linear regression on the logarithms of the data from five or more specimens of each species over the size ranges plotted;
coefficients of determination (r^) exceeded 0.89 for all shown and also for Bolinichthys longipes. D. schmidti, and D. fragilis whose
relationships were so similar to those of one or more species illustrated that they were omitted for clarity. Notolychnus valdiviae (r^ =
0.26, dashed lines) and Diogenichthys atlanticus (r^ = 0.09) emd Melamphaes danae ir^ = 0.23) are represented by the areas enclosed by
points from five specimens each.

rakers of all four were thin, cylindrical in cross
section, and covered with short rasplike teeth;
while those of the other species were flattened
usually with sawlike teeth on the leading edge.
Thus these species seem best adapted for detecting
the more visible prey and for retaining only rela-
tively large items.

Ceratoscopelus warmingi and D. perspicillatus
had the largest lenses of any species and sizes
considered. For both species the ASV's of many
types of prey were high, indicating that they are
capable of searching greater volumes than species
with smaller lenses. Ceratoscopelus warmingi,
however, preferred relatively large prey while D.
perspicillatus showed high ASV's for small as well
as large types. Consonant with these differences
in diet, C warmingi had a relatively larger gape

and less closely spaced gill rakers than did D.
perspicillatus.

Diogenichthys atlanticus, Benthosema subor-
bitale, Bolinichthys longipes, and Diaphus
trachops also had relatively large lenses; if
Diogenichthys atlanticus or Benthosema subor-
bitale grew as large as C. warmingi or Diaphus
perspicillatus, their lenses would be larger. The
first three species' diets included high fractions of
microzooplankton. Diogenichthys atlanticus,
which had the largest relative lens size and small-
est gape, had eaten the widest variety of micro-
zooplankton including many forms probably less
visible than the Oncaea spp., which dominated the
microzooplankton eaten by B. suborbitale and
Bolinichthys longipes. Bolinichthys longipes,
which was the only species which ate the small

636

CLARKE; DIETS OF FOURTEEN SPECIES OF MESOPELAGIC FISHES

Oncaea spp. (^0.6 mm) frequently and had the
lowest fractions of macrozooplankton, had much
finer gill rakers and somewhat larger lenses than
similar-sized Benthosema suborbitale, which took
a wider variety of sizes. Diaphus trachops, in con-
trast to the other three, ate mostly large prey.
ASV's of most of its prey were also much higher
than those of the other species. Its gape was the
largest of all species examined, consonant with
large prey size, but its relatively finely spaced gill
rakers and high raker area indicate it is equip-
ped to retain small prey as well. Diaphus trachops
was the only species caught only at 170 m where
zooplankton densities and particularly microzoo-
plankton were much lower. While the large lenses
of the other three species seem related to increased
ability to detect small prey, D. trachops' seem re-
lated to detection of relatively large, less dense
prey from greater distances. Lower light levels in
its depth range would also favor large lenses.

Diaphus schmidti andD. fragilis were similar to
each other other and intermediate to other myc-
tophids in all four features. Diet of D. schmidti was
generally similar to that of D. perspicillatus, i.e.,
very general, but it differed in that high ASV's
were not associated with many types of small
copepods preferred by D. perspicillatus. This is
consonant with D. perspicillatus' much finer gill
rakers and larger lenses. Although data are few,
the diet ofD. fragilis seems most similar to that of
D. schmidti. Diaphus fragilis is uncommon near
Hawaii but very abundant in more productive
waters near the Equator (Hartmann and Clarke
1975). It is also larger than D. schmidti. Ebeling
(1962) has suggested that "dwarf" species of
melamphaids are adapted to the less productive
central water masses. The above indicates that
similarly the larger of two otherwise similar myc-
tophids is less successful in the central water
mass.

Bregmaceros japonicus was the most distinct
morphologically of all species considered. It had no
gill rakers and the smallest lenses and gape of all
species. Though it ate chaetognaths fairly fre-
quently, the ASV's indicated that it prefers large
crustaceans. Apparently the small mouth of this
species does not inhibit it from ingesting large
prey, and in spite of its small lenses, it is able to
detect and capture at least a fraction of the trans-
lucent chaetognaths encountered.

Diet of M. danae was quite distinct from that of
the others. The most frequent and preferred items
included large and small forms and taxa other

than crustaceans — many of which were rarely
eaten by other fishes. Also, certain prey such as
Pleuromamma and Oncaea spp., which appeared
in diets of almost all other fishes, were absent or
nearly so from that of M. danae. Not a great deal
can be gleaned from its morphological features; in
spite of its small mouth and lens, M. danae is
obviously capable of ingesting fairly large items
and detecting small or translucent prey, but there
is no clear indication of why certain prey types
were not eaten.

Among the myctophids, differences in lens size
and gill raker space were most obviously and fre-
quently correlated with differences in diet and
preference. These indicate that ability to visually
detect and to retain prey in the mouth are impor-
tant factors affecting frequency and preference.
The general lack of correlation of dietary features
with differences in gill raker area indicates
these fish are probably not simply filtering. Mor-
phological relationships within the myctophids,
however, do not seem to extend to the sole repre-
sentatives of the other two families considered
here. Bregmaceros japonicus and M. danae appear
basically different; whether their morphological
features are in any way related to diet must await
data on other species of these families.

Aside from the correlations of lens size with diet
and lack thereof for gill raker area, the prefer-
ences observed and absolute values of ASV's also
indicate that these fishes feed in a particulate,
visually oriented mode (O'Connell 1972) as op-
posed to filtering. That the fishes are selective
precludes simple filtration unless it is assumed
that the differences between diet and available
prey are due entirely to differential escape
capabilities of the prey, and the general absence of
small or translucent prey from the diets implicates
vision. In many cases, the ASV's, which are mini-
mal estimates of the volume searched, seem too
high to have resulted from filtering alone. Even
assuming that the area filtered is as large as the
square of the premaxillary and that the fish swam
at 2.5 body lengths/s (Ware 1978) for 5 h, a 50 mm
D. trachops, C. warmingi, D. perspicillatus, or L.
steinbecki would search only 0.25-0.32 m-' (de-
pending on premaxillary length). Yet ASV's were
as high as 1.0 m^ for several prey of these species.
To search 1.0 m^ visually would require that the
fish detect prey within only about 12 mm. Simi-
larly, a 20 mm Diogenichthys atlanticus could at
best filter only about 0.008 m^, while ASV's of at
least five times this were associated with several of

637

FISHERY BULLETIN: VOL. 78, NO. 3

its prey. Even the smaller and therefore slower D.
atlanticus would have to detect prey only within
about 19 mm to search 1.0 m^ in the same time.

Comparison of my results with those of other
studies is limited to generalizations due to differ-
ent methodologies. In most other studies, prey
items have been identified only to major taxa, bias
due to differential digestion has not been consid-
ered, and diets have not been compared with ap-
propriate estimates of available prey densities.

Legand and Rivaton (1969) gave diets of nine
comparable species from the tropical Indian
Ocean. As near Hawaii, crustaceans dominated
the diets, and except for higher proportions of
amphipods and lower proportions of ostracods,
the diets of the myctophids were similar to those
of congeners from Hawaii. Ceratoscopelus
"townsendi" (which is probably really C. war-
mingi) had a wide variety of prey and with the two
Lampanyctus spp. had the highest frequency of
euphausiids. The diet of Benthosema simile, the
only species for which copepod genera were given,
was quite similar to that of B. suborbitale. Breg-
maceros macclellandi , unlike B. Japonicus from
Hawaii, had eaten no chaetognaths. Merrett and
Roe's (1974) data on three myctophid species from
the subtropical Atlantic also indicate that crusta-
ceans were the most important prey. Diets of the
individual species appear generally similar to
those of the most closely related species considered
from Hawaii.

Gorelova (1978) found that migratory crusta-
ceans dominated the diets of both C. warmingi and
Bolinichthys longipes in the western equatorial
Pacific. The diet of small C warmingi was domi-
nated by copepods, and most items were <4 mm
long, but specimens of sizes comparable to those
examined in my study (40-90 mm total length)
had eaten a wider variety of prey, over 50% of
which (by weight) were >4 mm. The dominant
euphausiids were the large Thysanopoda and
Nematobrachion spp. The diet of all sizes of B.
longipes was dominated by copepods, and the
euphausiids eaten were mostly the smaller
Euphausia and Stylocheiron spp. Oncaea spp.
were much less important than near Hawaii.
Among the large copepods, however, candaciids
were the dominant type in both areas. Gorelova
(1977) noted that Lampanyctus and Triphoturus
(species not given) in the equatorial Pacific eat
euphausiids almost exclusively.

Baird et al. (1975) showed that Diaphus
taaningi in the Cariaco Trench, like two Hawaiian

Diaphus spp., ate a wide variety of prey, but in
contrast to all other species considered here or
elsewhere, the diet was heavily dominated by
Oikopleura. Since Oikopleura is probably ren-
dered unrecognizable in the stomach faster than
most of the other prey types, its importance in the
diet is probably even greater than Baird et al.'s
data indicate. Its frequency in the plankton from
the cod end of the trawl was much lower than in
the diet; however, it was probably under-
represented relative to larger forms in such a sam-
ple. Whether the dominance of Oikopleura reflects
a real preference or simply very high densities at
the depths where the fish were feeding cannot be
determined.

Tyler and Percy (1975) investigated three
species of myctophids from off Oregon. The diets of
all three were heavily dominated by euphausiids,
mostly E. pacifica which was the most abundant
species in the area, and medium to large copepods,
the most frequently identified of which were
Calanus and Metridia spp. There was little indica-
tion of differences between fish species. Gjosaeter
(1973) showed similar results for another high
latitude myctophid, Benthosema glaciale; in this
case Thysanoessa spp. were the dominant
euphausiids.

The results of most studies generally agree that,
with the obvious exception of D. taaningi, verti-
cally migrating fishes feed primarily upon rela-
tively large, probably more visible crustacean
zooplankton; however, the data for some species
considered here and by Gorelova (1978) indicate
that small juveniles graze the microzooplankton
more heavily than sizes considered by most
studies. In contrast to the neustonic myctophids,
e.g., Centrobranchus and certain Myctophum spp.,
which feed primarily on shallow-living zooplank-
ton (Gorelova 1977), the principal prey of the
species considered here and by most other studies
undertake substantial diel vertical migrations
themselves (Brinton 1967; Roe 1972) — some al-
most as extensive as those of the fishes — and are
not present in the epipelagic by day.

Though the diets of the 14 species considered
here show some general similarities, differences
in frequency of and preference for different prey
types indicate that most species are at least some-
what specialized. The discussion of diet and mor-
phology above points out unique features for most
species. Lampanyctus steinbecki, L. nobilis,
Triphoturus nigrescens, and Notolychnus val-
diviae were the only species which were very simi-

638

CLARKE: DIETS OF FOURTEEN SPECIES OF MESOPELAGIC FISHES

lar to each other, but quite distinct from the others.
Differences in size and depth distribution at night
probably reduce diet overlap among these species.
Triphoturus nigrescens and L. nobilis occur shal-
lower than do N. valdiviae and L. steinbecki, and
within each pair, one species is considerably larger
than the other. Other multispecies studies in the
tropical or subtropical open ocean also indicate
some degree of specialization among cooccurring
species.

In contrast, Tyler and Pearcy's (1975) results
indicate that high latitude species have little or no
separation or specialization in diet. Confirmation
and further documentation of the apparent differ-
ence are certainly merited. If true, it could indi-
cate that tropical species are less likely to be com-
peting against each other for food or that species in
the highly productive waters off Oregon are not
food limited. The apparent difference in degree of
dietary specialization also has obvious implica-
tions relevant to differences in diversity — both of
the fish faunas and of their prey — between tropi-
cal and temperate oceanic communities.

ACKNOWLEDGMENTS

This research was supported by NSF GA-38423
and the Hawaii Institute of Marine Biology, Uni-
versity of Hawaii. I thank the officers and crew of
the research vessels Teritu and Moana Wave; the
staff of Ship Operations, Hawaii Institute of Geo-
physics; and the many people who participated on
the cruises for their assistance and cooperation.
Patricia J. Wagner capably assisted in the early
phases of the work. Euphausiids and decapods
were identified by K. Gopalakrishnan.

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Baird, r. c, T. l. Hopkins, and d. F. Wilson.

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BRINTON, E.

1967. Vertical migration and avoidance capability of
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1978. Diel feeding patterns of 16 species of mesopelagic
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ebeling, a. W

1962. Melamphaidae. L Systematics and zoogeography of
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Frost, B. W, and L. E. McCrone.

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Gannon, J. E.

1976. The effects of differential digestion rates of zoo-
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G.JOSAETER, J.

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GORELOVA, T A.

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Hartmann, A. R., AND T A. Clarke.

1975. The distribution of myctophid fishes across the Cen-
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IVLEV, V S.

1961. Experimental ecology of the feeding of fishes. Yale
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O'CONNELL, C.R

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Ware, D. M.

1978. Bioenergetics of pelagic fish: Theoretical change in
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640

SURVIVAL, SIZE, AND EMERGENCE OF PINK SALMON,

ONCORHYNCHUS GORBUSCHA, ALEVINS AFTER
SHORT- AND LONG-TERM EXPOSURES TO AMMONIA

Stanley D. Rice and Jack E. Bailey^

ABSTRACT

Eggs and alevins of pink salmon, Oncorhynchus gorbuscha , were exposed to ammonia in a series of stat-
ic and flow-through experiments to determine what levels of ammonia would decrease survival. Short-
term acute toxicity tests (96 hours) were conducted at several stages in development to determine
which of the early life stages were most sensitive to ammonia. Long-term tests (up to 61 days! with
lower ammonia concentrations were conducted to determine effects on survival and size of fry at emer-
gence. The possibility of ammonia stimulating emergence of immature fry was tested at various stages
of development.

Pink salmon alevins were most sensitive at the completion of yolk absorption, when the 96-hour
median tolerance limit was 83 parts per billion of un-ionized ammonia. Concentrations as low as 1.2
parts per billion reduced fry length in the 61-day exposures. Only levels above 10 parts per billion of
ammonia stimulated early emergence of immature fry.

The concentrations of ammonia causing any of the deleterious effects observed are greater than con-
centrations observed in the hatcherv or the natural environment.

Ammonia is a natural waste product of protein
catabolism and can be toxic to aquatic organisms
under certain conditions. Ammonia exists in the
water in two forms, un-ionized NHg and ionized
NH^^; the NHg is much more toxic than NH4^
(European Inland Fisheries Advisory Commission
1970). The percentage of ammonia in the more
toxic form, NHg, is influenced primarily by pH of
the water and by factors that influence pH, e.g.,
temperature, carbon dioxide, and bicarbonate al-
kalinity (European Inland Fisheries Advisory
Commission 1970).

Much information is available on the toxicity of
ammonia to fishes, including juvenile and adult
salmonids; but it is surprising that little informa-
tion exists on the toxicity of ammonia to fertilized
eggs and larvae of teleosts, especially because
these life stages are often assumed to be relatively
sensitive. In acute toxicity studies, trout eggs and
alevins^ are much more tolerant to ammonia than
fry ( Penaz 1965; Rice and Stokes 1975). Long-term

'Northwest and Alaska Fisheries Center Auke Bay Labora-
tory, National Marine Fisheries Service, NOAA, PO. Box 155,
Auke Bay AK 99821.

^After hatching, alevins (salmon larvae) reside in the spawn-
ing gravels for several months while consuming their large
yolks. Salmon alevins that have no externally visible yolk ("but-
toned up") become fry when they inflate their swim bladder and
become free-swdmming; this occurs immediately after volitional
emergence from natural redds and gravel incubators.

Manuscript accepted January 1980.
FISHERY BULLETI.N: VOL 78. NO. 3, 1980.

studies of larval and juvenile forms exposed to
ammonia are virtually nonexistent; but in one
long-term study Burkhalter and Kaya (1977) con-
tinuously exposed rainbow trout, Salmo
gairdneri, eggs and alevins to ammonia until the
end of yolk absorption (about 67 d). They found
retardation of growth at the lowest concentrations
tested and other adverse effects at higher concen-
trations.

Toxicity of NHg to the early life stages of salmon
in the northern latitudes would not be a problem
because low temperature and pH cause most of the
ammonia (99-1-%) in the water to be in the less
toxic form, NH^*. However, salmon eggs and ale-
vins in subarctic latitudes have a long devel-
opmental life history in an intragravel stream en-
vironment (up to 8 mo) where intragravel
waterflow can be reduced for several months dur-
ing the winter because of low temperatures. The
low waterflow may not be sufficient to prevent a
buildup of excreted ammonia in the water layer
immediately adjacent to the developing egg or ale-
vin. Ammonia levels may rise during these periods
of low flow to concentrations that are deleterious
to survival, health, and/or growth of the develop-
ing salmon.

Our study had three specific objectives: 1) to
determine the sensitivities (judged by survival) of
early life stages of pink salmon, Oncorhynchus

641

FISHERY BULLETIN; VOL. 78, NO. 3

gorbuscha, to short-term, high concentrations of
NH3; 2) to determine the size of emergent fry after
long-term exposure of alevins to low concentra-
tions of NH3; and 3) to determine whether early
emergence of immature salmon fry can be caused
by short-term sublethal concentrations of NH3.
The short-term tests with high concentrations of
NH3 identified the more sensitive life stages and
provided information on concentrations that were
lethal. The sublethal tests identified NH3 concen-
trations that caused decreases in the size of emer-
gent fry or caused early emergence of immature
fry. Identification of factors that cause smaller fry
at emergence is important because smaller fry are
less capable of surviving in the environment.
Laboratory and field studies by Bams (1967) and
Parker (1971) have shown that smaller salmon fry
have less swimming endurance and are selectively
preyed upon by larger predators.

Our ultimate objective was to compare the con-
centrations of NH3 that are harmful to pink salm-
on in the laboratory with concentrations of NH3
that are harmful in hatchery incubators (Bailey et
al. 1980) and in natural spawning redds (Rice and
Bailey 1980). To compare the studies of Bailey et
al. and Rice and Bailey with our study, our tests
were conducted with pink salmon eggs, alevins,
and fry exposed to NHg at temperatures <4.8° C
and pH's <6.5 — conditions that are typical for
freshwater streams in boggy rain forests of the
colder northern latitudes.

MATERIALS AND METHODS

The pink salmon eggs were fertilized in Sep-
tember at Lovers Cove Creek, southern Baranof
Island, southeastern Alaska, and incubated to the
eyed stage in Heath^ incubators at Auke Bay, near
Juneau, Alaska. Some eyed eggs were taken from
the Heath incubators and placed in upwelling in-
cubator cups or in 15.2 cm diameter pipe in-
cubators (Rice and Moles'*) for long-term expo-
sures or emergence stimulation tests. The rest of
the eggs were left in the Heath incubators for
short-term bioassays.

We measured concentrations of total ammonia

(NH3 -I- NH4 ^ ) by an automated method that mea-
sured the intensity of indophenol blue formed
after the reaction of ammonia with alkaline phenol
hypochlorite (U.S. Environmental Protection
Agency 1974). Total ammonia concentrations
were analyzed the same day water samples were
taken. The concentrations reported in this study
are for the toxic, un-ionized NH3. Total ammonia
was measured and the concentration of NHg de-
termined by using the temperature-pH correction
tables of Emerson et al. (1975).

Our experimental approach involved three
types of experiments: 1) to determine the sensitiv-
ity (survival) of each early life stage to NH3, we
exposed eyed eggs, alevins, and fry to short-term,
high concentrations of NH3 ( >50ppb);2) to deter-
mine the effect of long-term exposures of NH3 on
size of fry at emergence (end of yolk absorption),
we exposed alevins at different stages of develop-
ment to low concentrations of NH3 ( <3 ppb) for up
to 61 d; and 3) to determine whether NH3 would
cause emergence of immature fry, we exposed ale-
vins to high concentrations of NH3 (30-150 ppb)
for 24 h and counted voluntary out-migrants from
the incubators.

The senstivities of different life stages to short-
term, high concentrations of NH3 were tested with
96-h bioassays conducted according to the stan-
dard procedures of Doudoroff et al. (1951). Eggs,
alevins, and fry were exposed to static solutions of
ammonium sulfate in freshwater at pH of 6.3-6.5
and 3.7°-4.8° C. Twenty-five animals were placed
in each 18 1 test container; resulting ratios of tis-
sue to test solution were <0.3 g/1. The test solu-
tions were aerated and the tests were conducted in
the dark. Median tolerance limits (TLm's) and as-
sociated 95% confidence levels were calculated by
a computerized probit analysis program based on
the method discussed by Finney (1971).

To test the effect of long-term exposures to NHg
on size of fry at emergence, ammonium sulfate
was introduced into the water which flowed
through incubator cups containing the developing
alevins. Twenty-five eyed eggs were placed in each
upwelling incubator cup (Bailey^), and exposures
to NH3 began at selected times after hatching. The
NH3 was introduced by dripping small quantities
of concentrated ammonium sulfate solutions into

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

"Rice, S. D., and D. A. Moles. 1977. Apparatus for incuba-
ting salmonid eggs and alevins in a variety of controlled envi-
ronments for laboratory studies. Unpubl. manuscr. Northwest
and Alaska Fisheries Center Auke Bay Laboratory, NMFS,
NOAA, Auke Bay, AK 99821.

^Bailey, J. E. 1964. Incubation of pink salmon eggs in a
simulated intertidal environment. In Proceedings 15th An-
nual Northwest Fish Culture Conference, p. 79-89. Oregon Agri-
cultural Experiment Station, Corvallis, OR 97330.

642

RICE and BAILEY: SURVIVAL, SIZE, AND EMERGENCE OF PINK SALMON

the incoming water line to each cup. Flow rates of
both water and ammonium sulfate were kept con-
stant by using supplies with a constant head. We
measured flow rates daily and concentrations of
total ammonia in each cup twice each week.

In the long-term tests, three groups of alevins
(A, B, and C) were exposed to ammonium sulfate
solutions for three different lengths of time. Group
A was exposed for the 21 d preceding the comple-
tion of yolk absorption (time of normal emergence
and migration). Group B was exposed for 40 d,
with the exposure ending 21 d before yolk absorp-
tion. Group C was exposed for 61 d before yolk
absorption. In each group, subgroups of alevins
were exposed to concentrations of NH^ ranging
from 0 (control) to 4 ppb.

At the end of the long-term exposures when
control fry had absorbed all visible yolk, 50 fry
from each NH3 exposure were sampled and pre-
served in d^c Formalin. Size was determined after
6 wk when tissue hydration adjustments were sta-
ble. After blotting the fry with a damp paper towel,
fork lengths were measured to the nearest mil-
limeter and weights to the nearest milligram.
Mean Kjj developmental indices (Bams 1970) were
1.99 for the controls and 1.96-2.07 for the groups
exposed to NH3; therefore, fry were at similar de-
velopmental stages and the size of fry from the
various groups could be compared directly with
the size of controls. Data are reported as means
±95% confidence intervals.

In another experiment, the possible stimulation
of early emergence of immature fry was tested by
exposing alevins in gravel incubators to a single
exposure of NHg for 24 h at various times during
development. Concentrated ammonium sulfate
solutions were pumped into the intake lines of
small experimental gravel incubators (Rice and
Moles footnote 4) at rates sufficient to produce
desired concentrations of NH3. Alevins or fry were
trapped if they voluntarily emerged during the
exposure. The numbers of fry and stage of devel-
opment were noted daily. Pink salmon were judged
to have emerged early when they emerged before
control fry and were judged to have emerged pre-
maturely if yolk sacs were visible externally. Pipe
incubators with a volume of 5 1 and a water flow of
450 ml/min were seeded in November with 300
eyed eggs each. Each week after hatching, several
incubators were exposed to four different concen-
trations of NHg for 24 h. Each incubator received
only one 24-h treatment and different sets of in-
cubators were used for the NH3 exposures that

were performed every week during the 2 mo prior
to emergence of controls. All NH3 concentrations
were measured analytically by the method previ-
ously described.

SENSITIVITY OF DIFFERENT
LIFE STAGES TO AMMONIA

Late alevins near emergence were the most sen-
sitive of all life stages tested to short-term, acute
concentrations of NH3 (Figure 1). Eyed eggs ex-

T 1 r

24JAN 14 FEB 13 MAR

DATE OF ACUTE BIOASSAY

10 APR

Figure l.— 96-h median tolerance limits (TLm's) and ±95%
confidence limits of pink salmon alevins and fry exposed during
short-term, acute experiments to un-ionized ammonia (NH3).
Eggs were also tested, but no mortalities were observed at the
highest concentration (1,500 ppb NH^).

posed for 96 h to toxicants in December were not
harmed by concentrations > 1,500 ppb and ap-
peared to hatch normally. Late alevins (tested
13-17 March) had the lowest 96-h TLm measured,
83 ppb of NH3. The fry (tested on 10-14 April) had
been feeding for 2 wk and appeared to have
slightly greater tolerance to NH3 than the alevins
tested just prior to emergence, but the differences
between the tests were not statistically signifi-
cant. Greater sensitivity just prior to emergence is
consistent with similar observations of trout eggs
and alevins exposed to ammonia (Penaz 1965; Rice
and Stokes 1975). Studies with other toxicants
have identified eggs to be much more tolerant than
alevins (Wurtz-Arlet 1959; Garrison 1968; Rice et
al. 1975).

643

EFFECT OF LONG-TERM AMMONIA

EXPOSURES ON SIZE OF

FRY AT EMERGENCE

Lengthy exposure of alevins to NH, resulted in
fry that were smaller than control fry at
emergence (Figure 2). Although the three test
groups of alevins (groups A, B, and C) were ex-
posed to NH3 for different time periods (21, 40, and
61 d), they were all sampled when the control
groups had completed yolk absorption. The high-
est exposure concentration of NH3 (4 ppb) caused
significant decreases in weight (P<0.05) of ex-
posed fry in all three exposure groups. At exposure
concentrations <4 ppb, the groups held for 40 d
and 61 d (B and C) were similar in response: both
were significantly smaller in length and weight
after exposure to 2.4 ppb NH3; after exposure to 1.2
ppb there was no significant difference. Effects
were consistently more adverse for group C, the
group receiving the longest exposures. The statis-
tically significant decrease in weight (P<0.05) of
one observation of group A exposed to 0.2 ppb of
NHg appeared to be an aberrant observation.

EFFECT OF AMMONIA ON
EARLY EMERGENCE

Short-term (24 h) exposures to low concentra-
tions of NHg (<25 ppb) did not stimulate early
emergence during or immediately after the expo-
sures; emergence patterns were the same as those
of unexposed fry. At higher concentrations (30-50
ppb) of NHg, early emergence of the alevins (up to
11%) occurred within 24 h of exposures, but little
residual effect was observed later when 50%
emerged at approximately the same date as unex-
posed alevins (Figure 3). Some early emergence of
the alevins (up to 12%) occurred at high concen-
trations of 100-150 ppb NH3, but massive early
emergence was not observed even though these
concentrations were above the 96-h TLm's for ale-
vins or fry during the period 15 February to 10
April (Figure 1). Although the high concentra-
tions were probably stressful, mortalities never
exceeded 4%. In all cases, when early emergence
was stimulated, it occurred within 24 h of the
beginning of exposure. In response to the acute
exposures to NH3, the alevins that emerged early
had visible amounts of yolk, indicating they were
not ready for normal emergence. The alevins that
did not emerge during or immediately after NH3
exposures stayed in the incubators almost as long

644

FISHERY BULLETIN: VOL. 78, NO. 3

as the unexposed alevins and emerged without
any visible yolk.

IMPLICATIONS OF
AMMONIA EXPOSURE STUDIES

Ammonia exposures resulting in immature or
small fry would be detrimental to the survival of
pink salmon fry because these small fish are easily
preyed upon (Bams 1967; Parker 1971). We did
observe some early emergence of immature fry
during or immediately after short-term exposures
to NHg, but only at the high concentrations that
aproached highly toxic levels. These high concen-
trations are not likely to be encountered in natural
or hatchery environments, but if they were en-
countered, the immature alevins that emerged
with visible yolk would have difficulty swimming
and avoiding predators.

We do not know the effect of long-term expo-
sures to low concentration of NHg on time of volun-
tary emergence, but these tests do produce emer-
gent fry with decreased weight and length.
Exposed emergent fry have increased metabolic
rate and, therefore, increased demand on yolk re-
serves and less yolk reserve available for incorpo-
ration into developing tissues. Adult trout exposed
to NH3 have increased metabolic rates, and NHg
probably has the same toxic action in fishes that it
has in mammals — impairment of cerebral energy
metabolism (Smart 1978).

The lowest concentration of NH3 that caused fry
to be significantly smaller in length and weight at
emergence was 2.4 ppb (61- and 40-d exposures)
(Figure 2). This concentration is about one-
twentieth of the concentration (50 ppb) that
caused retardation of growth in rainbow trout fry
that had been exposed continuously for about 67 d
from the beginning of the egg stage (Burkhalter
and Kaya 1977). Pink salmon alevins exposed to
NH3 for 61 d at 4° C in our study were more sensi-
tive (as judged by effects on size) than the faster
developing rainbow trout eggs and alevins ex-
posed for about 67 d at 12° C. In the trout study
(Burkhalter and Kaya 1977), 25 d of the 67-d expo-
sure were during the egg stage, a stage that is
relatively tolerant compared with the alevin
stage.

The highest concentrations of NH3 in the dis-
charge water of a hatchery incubator with an ab-
normally high density of pink salmon alevins
(Bailey et al. 1980) was 0.14 ppb, and the highest
concentration from intragravel water of a stream

RICE and BAILEY: SURVIVAL, SIZE, AND EMERGENCE OF PINK SALMON

1

0.0

T 1 1 1 r

02 .04 .2 .4 1.2 2.4

CONCENTRATION OF UN-IONIZED AMMONIA IN PPB

Figure 2.— Length (upper) and weight (lower) of migrant pink salmon fry at emergence resulting from groups of alevins exposed to
various concentrations of un-ionized ammonia (NH3) for three lengths of long-term exposure. For each mean, n = 50 fry, bars indicate
95% confidence limits. Group A— exposed for 21 d just prior to migration; group B— exposed for 40 d, ending 21 d prior to migration;
group C — exposed for 61 d continuously until migration. Asterisks indicate significant differences in length or weight (P<0.05)
between those fry that had been exposed and control fry.

645

FISHERY BULLETIN: VOL. 78, NO. 3

100

16 22 28
FEB

1 1 r-

12 18 24 30
MAR

-i 1 r-

12 18 24
APR

30

Figure 3 . — Daily cumulative percent of emergence of pink salmon fry that did not receive exposure to ammonia (controls) or received a
single 24-h exposure to ammonia sometime prior to normal emergence. The dates when the 24-h exposures began are indicated by
arrows and exposure concentrations. Three ranges of un-ionized ammonia concentrations were used: 1) <25 ppb (not shown) which
resulted in <1% immediate emergence. The date of 50% emergence was within ±3 d of 50% control emergence, 2) 30-60 ppb of
un-ionized ammonia (upper), 3) 90-150 ppb of un-ionized ammonia (lower). Asterisk indicates the lack of initial emergence (<1%) in
response to ammonia exposures ( same pattern as controls).

646

RICE and BAILEY: SURVIVAL, SIZE. AND EMERGENCE OF PINK SALMON

with known densities of pink salmon alevins (Rice
and Bailey 1980) was 0.096 ppb. Both of these
"real life" extremes of NH3 were much less than
the concentrations we found to cause early
emergence of immature fry and acute toxicity. The
concentrations that caused small size after
lengthy exposure in this study were about 10
times greater than the maximum concentrations
found in hatchery incubator effluents and intra-
gravel water from salmon redds (Bailey et al.
1980; Rice and Bailey 1980). Thus, exposure to
naturally occurring ammonia is not a likely prob-
lem for salmon eggs and alevins in Alaska under
natural or hatchery conditions where tempera-
tures are low and waters are acidic — conditions
that cause the percentage of NH3 to be very low
(<0.1^f).

If pink salmon are reared at higher tempera-
tures and alkalinities, the potential for adverse
effects from NH3 is increased because of the shift
in the equilibrium toward NH3. At 5° C and pH of
7.5, 0.394'^ of the total ammonia is NH3; in con-
trast, at 5° C and pH of 6.5, 0.0395^^ is NH3 ( Emer-
son et al. 1975). Therefore, if the pH of Auke Creek
and Sashin Creek were 7.5 rather than 6.5, ap-
proximately 10 times more NH3 might have been
observed. The level of total ammonia would have
been the same, but the percentage of NH3 would
have been much greater. Assuming no losses from
aeration or other factors, the percentage of NH3
would be about 100 times greater at a pH of 8.5
than at a pH of 6.5. It is possible that high densi-
ties of alevins in hatcheries or stream gravels
could produce unhealthy concentrations of NH3 if
the pH is alkaline. From our exeriments, we con-
clude that concentrations of NH3 >0.50 ppb should
be avoided. Because our results were generated at
relatively low temperature and pH, extrapolation
of our data to extreme situations of temperature
>10° C or pH >7.8 is inappropriate.

ACKNOWLEDGMENTS

Sidney G. Taylor aided in the 61-d tests and the
length-weight analysis. Charlotte Misch con-
ducted the tests on early emergence.

LITERATURE CITED

Bailey, J. E., S. D. Rice, J. J. Pella, and S. G. T.wlor.

1980. Effects of seeding density of pink salmon, Oncorhyn-
chus gorbuscha , eggs on water chemistry, fry characteris-
tics, and fry survival in gravel incubators. Fish. Bull.,
U.S. 78:649-658.

Bams, R. A.

1967. Differences in performance of naturally and artifi-
cially propagated sockeye salmon migrant fry, as mea-
sured with swimming and predation tests. J. Fish. Res.
Board Can. 24:1117-1153.

1970. Evaluation of a revised hatchery method tested on
pink and chum salmon fry. J. Fish. Res. Board Can.
27:1429-1452.
BURKHALTER, D. E., AND C. M. KAYA.

1977. Effects of prolonged exposure to ammonia on fer-
tilized eggs and sac fry of rainbow trout ^Salmo
gairdneri). Trans. Am. Fish. Soc. 106:470-475.

doudoroff, p, b. g. anderson, g. e. burdick, r s.
Galtsoff, W. b. Hart, R. Patrick, E. R. Strong, E. W.
surber, and w. m. van horn.

1951. Bio-assay methods for the evaluation of acute toxicity
of industrial wastes to fish. Sewage Ind. Wastes
23:1380-1397.

Emerson, K., R. C. Russo, R. E. Lund, and R. V. Thurston.

1975. Aqueous ammonia equilibrium calculations: effect
of pH and temperature. J. Fish. Res. Board Can.
32:2379-2383.

European Inland Fisheries Advisory Commission.

1970. Water quality criteria for European freshwater fish.
Report on ammonia and inland fisheries. FAQ, EIFAC
I Eur Inland Fish. Advis. Comm.) Tech. Pap. 11, 12 p.

Finney, d. j.

1971. Probit analysis, 3d ed. Camb. Univ Press, Lond.,
333 p.

Garrison, R. L.

1968. The toxicity of pro-noxfish to salmonid eggs and
fry. Prog. Fish-Cult. 30:35-38.
Parker, R. R.

1971. Size selective predation among juvenile salmonid
fishes in a British Columbia inlet. J. Fish. Res. Board
Can. 28:1503-1510.

Penaz, M.

1 965 . Influence of ammonia on eggs and spawns of stream
trout Salmo trutta M. Fario. Zool. Listy, Folia Zool.
14:47-53. [Translated by and available from Foreign
Fisheries (Translations), U.S. Dep. Commer. Wash.. D.C.I

Rice, S. D., and J. E. Bailey.

1980. Ammonia concentrations in pink salmon, On-
corhynchus gorbuscha, redds of Sashin Creek, southeast-
em Alaska. Fish. Bull., U.S. 78:809-811.

RICE, S. D., D. a. Moles, and J. W. Short.

1975. The effect of Prudhoe Bay crude oil on survival and
growth of eggs, alevins, and fry of pink salmon, On-
corhynchus gorbuscha. In Proceedings of 1975 Confer-
ence on Prevention and Control of Oil Pollution, p. 503-
507. Am. Pet. Inst., Environ. Prot. Agency, and U.S. Coast
Guard, Wash., D.C.
RICE, S. D., AND R. M. Stokes.

1975. Acute toxicity of ammonia to several developmental
stages of rainbow trout, Salmo gairdneri. Fish. Bull.,
U.S. 73:207-211.

Smart, G. R.

1978. Investigations of the toxic mechanisms of ammonia
to fish — gas exchange in rainbow trout i Salmo gairdneri)
exposed to acutely lethal concentrations. J. Fish. Biol.
12:93-104.

U. S. Environmental Protection Agency.

1974. Methods for chemical analysis of water and wastes.
U.S. Environ. Prot. Agency, EPA-625/6-74-003, 298 p.

647

FISHERY BULLETIN: VOL. 78, NO. 3

WURTZ-ARLET, J.

1959. Toxicite des detergents anioniques vis-a-vis des
alevins de Truite commune [The toxicity of anionic deter-
gents towards the alevins of common trout]. [In. Fr]
BulL Fr Piscic. 32:41-45.

648

EFFECTS OF SEEDING DENSITY OF PINK SALMON,
ONCORHYNCHUS GORBUSCHA, EGGS ON WATER CHEMISTRY, FRY
CHARACTERISTICS, AND FRY SURVIVAL IN GRAVEL INCUBATORS

Jack E. Bailey, Stanley D. Rice, Jerome J. Pella, and Sidney G. Taylor'

ABSTRACT

We determined the effects of seeding density of pink salmon eggs in gravel incubators on water
chemistry and on size, stage of development, and time of emergence of fry. Sixty days after fertilization,
eyed eggs were placed in eight identical test incubators at five different densities ( 0 to 25,600 eggs per
incubator). Test incubators had upwelling water ( apparent velocity, 53 cm per hour); 0.015 m^ of gravel
(size, 3-32 mm); and an average incubation temperature of 4.5° C (range, 3.5°-10.0° C). Total ammonia
(NH3 + NH4*) production and oxygen consumption rates per alevin generally increased throughout
incubation. Maximum total ammonia production at any density was about 8 x lO"* mg/h per alevin.
Maximum oxygen consumption was 0.028 mg/h per alevin. The rate of ammonia production and
oxygen consumption per alevin increased with increased seeding density until the reduced oxygen
concentration limited metabolism. Indications of stress — reduction in size of fry and early
emergence— were evident only at the higher seeding densities, 12,800 and 25,600 eggs per 0.015 m^,
and were either absent or unimportant at the lower seeding densities, 1,600 and 6,400 eggs per 0.015
m^. Un-ionized ammonia ( NH3 ) concentrations did not reach lethal levels. The stress at higher seeding
densities, 12,800 and 25,600 eggs per 0.015 m^, was probably caused by depletion of oxygen to
concentrations below 6 mg/1. Sublethal ammonia concentrations and low dissolved oxygen concentra-
tions were probably synergistic.

Gravel incubators with upwelling water are being
tested at hatcheries in the Pacific Northwest for
production of fry from eggs of pink salmon, On-
corhynchus gorbuscha, chum salmon, O. keta, and
sockeye salmon, O. nerka. To operate most
economically, these incubators must be stocked
with optimum numbers of eggs and be supplied
with a flow of water consistent with production of
good quality fry. Frugal use of water is important
to hatcheries in Alaska where long, cold winters
limit free-flowing water. However, densities of
eggs that are too high for water flows result in
oxygen depletion or ammonia buildup — stressing
conditions that produce undersized fry or early
emerging alevins. Both undersized fry and early
emerging alevins are believed to survive poorly if
released unfed (Bams and Simpson 1977).

Acute ammonia toxicity may not be a significant
problem in Alaska where waters typically have
low temperature and low pH. Ammonia equili-
brates in water to form dissolved, un-ionized NH3

and ionized NH.

(NH3 is more toxic than NH4

),

and low temperature and low pH shift the equilib-

'Northwest and Alaska Fisheries Center Auke Bay Labora-
tory, National Marine Fisheries Sevice, NOAA, PO. Box 155,
Auke Bay AK 99821.

Manuscript accepted January 1980.
FISHERY BULLETIN: VOL. 78, NO. 3, 1980.

rium toward NH^^ (Emerson et al. 1975). At lower
temperatures, however, salmon incubation times
are longer than at higher temperatures so that
increased cumulative exposure to NH3 could have
adverse effects.

In this paper we describe effects of seeding den-
sities of pink salmon eggs in gravel incubators on
1 ) oxygen consumption, 2 ) ammonia production, 3 )
physical characteristics of fry, 4) survival of fry,
and 5) time of volitional emergence. The produc-
tion limits of the gravel incubators are also de-
fined.

METHODS

Experimental gravel incubators were seeded
with different densities of eggs. Temperature, pH,
dissolved oxygen, and total ammonia (NH3 and
NH4 + ) concentrations were measured in water en-
tering and leaving the incubators. Rates of oxygen
consumption and ammonia production per egg or
alevin were estimated during incubation. We mon-
itored numbers and size of fry and time of
emergence of fry to identify stressful conditions.
Chemical data were compared with biological data
to determine maximum seeding densities for the
gravel incubators and to define limits of oxygen

64£

FISHERY BULLETIN: VOL. 78, NO. 3

and ammonia concentrations that do not produce
stressful conditions.

On 16 September 1971, pink salmon eggs were
collected from spawners in Sashin Creek on
Baranof Island, southeastern Alaska. The eggs
were immediately fertilized, water hardened, and
placed in Heath^ trays. On 4 November, we trans-
ported the eyed eggs from Sashin Creek to Auke
Creek near Juneau, Alaska, and on 16 November,
the eggs were placed in eight gravel incubators at
five seeding densities— 0, 1,600, 6,400, 12,800,
and 25,600 eggs /incubator (Table 1).

Each incubator (inside measurements, 30 cm x
30 cm X 30 cm, Bailey and Heard 1973) contained
0.015 m^ of gravel. A 25 mm layer of bird's-eye
gravel (particle size, 2-4 mm) covered the sides and
bottom. The remainder of the gravel was larger
(particle size, 13-32 mm). We installed airtight
covers on the incubators to prevent exchange of
gases between atmosphere and water. Water was
introduced into each incubator from the bottom in
an upwelling flow of 0.8 1/min (apparent velocity,
53 cm/h).

Numbers of eggs were estimated by displace-
ment (Burrows 1951). Precision of the seeding
densities, given by ±2 times their estimated stan-
dard error (Table 1), was based on appropriate
expansion of variation in egg counts from ten 100
ml samples. In previous studies of incubation at
this hatchery (Bailey and Taylor 1974), the eggs
hatched in late December or early January, 100-
120 d after fertilization; and the fry emerged in
April, 205-225 d after fertilization. In this study,
we expected the eggs to hatch and the fry to
emerge at similar times.

Oxygen and total ammonia concentrations were
measured weekly between 3 December 1971 and
11 April 1972. Dissolved oxygen concentrations
were measured with the Winkler method to the
nearest 0.01 mg/1. Total ammonia (NHg -I- NH4^)
in the water was measured with an autoanalyzer
using a procedure modified from that of the U.S.

Environmental Protection Agency (1974). Our
modification used a larger capacity heating bath
and measured total ammonia to within 0.004 ppb.
If temperature and pH are known, the amount of
NH3 can be calculated from tables by Emerson et
al. ( 1975). When calculating periodic estimates of
oxygen uptake and total ammonia production per
individual, we corrected for the number of fry that
had left the incubator. We assumed the number of
alevins in the incubator equaled the final total of
alevins emerging from the incubator less the
number of alevins already emerged. Tempera-
tures of incubator effluents were measured daily
to the nearest 0. 1° C , and pH was measured twice a
week with a standardized Corning model 112 pH
meter. Confidence intervals were calculated for
each estimate and displayed graphically. These
confidence intervals were computed under the as-
sumptions of normality of variation and
homogeneous variance, the latter holding both
among incubators and over observation times.

The fry were sampled and counted daily (Feb-
ruary through April 1972) as they voluntarily
emerged from incubators. Samples of fry were pre-
served in 5% Formalin for 6 wk. Later we selected
three samples of 50 fry from the daily samples of
each incubator to represent the days when
cumulative fry emergence was 25'7f , 50^7^ , and 75%
of the total emergent fry for each incubator. Fry in
these selected samples were measured to the
nearest millimeter (fork length) and weighed to
the nearest milligram after they were blotted with
a damp paper towel. Developmental index iK^)
was computed to determine efficiency of yolk con-
version [Kj) = 10( weight, milligrams)' '/(length,
millimeters). Bams 1972]. The /C^ index was com-
puted for unfed fry at the time of emergence. A
high K,-i indicates a large amount of unabsorbed
yolk, whereas a small Kd indicates a small
amount of yolk and a more developed fry. The sam-
ple of fry at 25% emergence from the incubator
seeded with 25,600 eggs was lost.

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

Table 1. — Survival of pink salmon from eyed egg to migrant fry
in gravel incubators seeded with indicated number of eggs

(±2SE).

Eyed eggs
per incubator

Survival
(%)

Eyed eggs
per incubator

Survival

1.600 ± 76
6,400 ±302
6,400 ± 302

100
94
92

6,400 ± 302
1 2,800 ± 604
25,600 ± 1 .209

92

100

50

TEMPERATURE, pH, AND

TOTAL AMMONIA IN

INCUBATOR EFFLUENT

Temperature of the water source decreased as
the experiment proceeded. Temperature was
about 8° C when the eggs were fertilized 16 Sep-
tember 1971 (day 0, Figure 1), remained above 7° C
until 14 October (day 28), and then gradually
dropped to 3.6° C (range, 3.5°-3.8° C) by 16

650

BAILEY ET AL.: EFFECTS OF SEEDING DENSITY OF PINK SALMON

lOl

FiGLTRE 1. — Incubation temperature of pink
salmon eggs from fertilization, 16 September
1971 (day 0) until termination of the experi-
ment, 28 April 1972 (day 2251 after fry emerged
from the incubators. Horizontal bars show
when eggs hatched and fry emerged from the
incubator seeded with 1,600 eggs.

FRY
EMERGED

wimiiin

_l I 1—1 L-l_

I ■ ■ ■

_l l__l i__l I 1-

75 100 125 150

DAYS AFTER FERTILIZATION

175

200

November (day 61). It remained near 3.6° C from
16 November 1971 until termination of the exper-
iment on 28 April 1972 (day 225). The daily tem-
perature variation was <0.2° C.

During the incubation period, pH of the hatch-
ery water supply changed little (pH, 6.13-6.39).
Effluents of incubators with eggs had a pH from
6.08 to 6.36. Effluent from the incubator with the
highest density of eggs (average pH, 6.19) was
more acidic than the hatchery supply (average pH,
6.27).

Concentrations of total ammonia in effluents
were higher in seeded incubators than in control
incubators and generally increased with more
eggs (Figure 2). Concentrations of total ammonia

ECCS HATCHED ^2,

mmmmmA

FRY EMERGED

100 125 150

DAYS AFTER FERTILIZATION

Figure 2. — Concentrations of total ammonia in hatchery water
supply ( 0 eggs) and in effluents from incubators seeded with in-
dicated numbers of pink salmon eggs. Horizontal bars show when
eggs hatched and fry emerged in the incubator seeded with 1,600
eggs. Peak total ammonia concentration for each seeding density
is indicated numerically.

in the effluent from control incubators and in the
water supply were nearly identical (maximum
concentration about 0.011 mg/1). During the
study, maximum concentrations of total ammonia
in seeded incubators ranged from 0.03 mg/1 for the
incubator seeded with 1,600 eggs (March) to 0.32
mg/1 for the incubator seeded with 25,600 eggs
(January).

The rate of total ammonia production per indi-
vidual was periodically measured in all of the in-
cubators. As development progressed from the
eyed-egg stage to the emerging fry stage, rate of
total ammonia production per individual in-
creased. For example, in the three incubators
seeded with 6,400 eggs (Figure 3), the mean of
total ammonia production 3 wk before hatching
(89 d after fertilization) was <2 x 10 "* mg/h per
egg. By hatching (110 d after fertilization), the
mean of total ammonia production increased to
nearly 4 x 10"^ mg/h per egg. At emergence, ap-
proximately 14 wk after hatching (208 d after fer-
tilization), the mean of total ammonia production
was almost 6 x 10 ■* mg/h per alevin.

The rate of total ammonia production per egg or
alevin increased with seeding density (Figure 4).
The rates of total ammonia production per indi-
vidual were meaningless for the incubator with
25,600 eggs (not shown in Figure 4) because many
of the eggs and alevins had died and were decom-
posing and because many of the alevins had
emerged 30-60 days early. At the other three seed-
ing densities (1,600, 6,400, and 12,800 eggs), the
rates of total ammonia production were higher at
higher seeding densities, and the regression of av-
erage rates of total ammonia production per indi-

651

FISHERY BULLETIN: VOL 78, NO. 3

o

o

S 5.00

I- 3.00

U

ECCS
HATCHED

125 150 175

DAYS AFTER FERTILIZATION

FRY

EMERGED

1///////M

L

Figure 3. — ^Total ammonia production per individual pink salm-
on egg or alevin in the three gravel incubators seeded with 6,400
eggs. Ninety-five percent confidence limits for the periodic means
were calculated using the error mean square from a one-way
ANOVA for sampling periods. Horizontal bars show when eggs
hatched and fry emerged.

z
>

LU
<

o

o
u

01 5

z
o

V-

u

D
O
O

a:

z
o

<

5i

DAYS AFTER
FERTILIZATION

r

ECCS-

1600

SEEDING DENSITY,

6100
ECCS PER INCUBATOR

12,800

Figure 4. — ^The effect of seeding density on individual ammonia-
production rates during development of eggs to emerging alevins.
Total ammonia was measured in incubator effluents cmd was cor-
rected for emergence from the incubators. Eggs hatched 100-120
days after fertilization, and alevins from 1,600-egg density
emerged about 203-220 days after fertilization.

vidual egg or alevin in the incubators on their
seeding densities was significant (P<0.01). The
average rate of total ammonia production in each

652

incubator was the mean of 22 periodic rates mea-
sured as the eggs developed into emergent fry.

DISSOLVED OXYGEN

Dissolved oxygen concentration in the supply
water declined gradually from 9.16 mg/1 (70%
saturation) on 14 December 1971 (day 89), about 2
wk before the eggs hatched, to 8.08 mg/1 (62%
saturation) on 11 April 1972 (day 208, Figure 5).
This decline was normal because the lake source is
usually covered with ice in winter.

Generally, as the eggs developed into fry, dis-
solved oxygen concentrations in the seeded in-
cubators decreased more in incubators seeded
with more eggs (Figure 5), except in the incubator
with 25,600 eggs. In the incubator seeded with
25,600 eggs, massive early emergence of fry left
fewer alevins in the incubator than in the in-
cubator initially seeded with 12,800 eggs. After
the early emergence in the incubator initially
seeded with 25,600 eggs, the effluent of the in-
cubator with 12,800 eggs had the lowest dissolved
oxygen concentration of the study — 3.8 mg/1 dis-
solved oxygen (29% saturated) on 7 March (day
173).

Generally, oxygen consumption per egg or ale-
vin increased steadily during development. At 7-d
intervals during incubation, we estimated oxygen
consumption rates in each of the three incubators
seeded with 6,400 eggs (Figure 6) and averaged
these rates. The average rate of oxygen consump-
tion about 2 wk before hatching was about 0.003

9 6

y 5

o

"<! 3

25.600

ECCS
HATCHED

FRY
EMERGED

— I —
100

125 150 175

DAYS AFTER FERTILIZATION

—I —
200

Figure 5. — Dissolved oxygen concentration in hatchery water
supply (0 eggs) and in effluents from incubators seeded with indi-
cated numbers of pink salmon eggs, December 1971-April 1972.
Horizontal bars show when eggs hatched and fry emerged in the
incubator seeded with 1 ,600 eggs.

BAILEY ET AL.: EFFECTS OF SEEDING DENSITY OF PINK SALMON

S .010

13

1/1

z
o
o

IM

}I

tJ

l^i

n

Hi

ECCS HATCHED

mminiwin

L.

FRY EMERGED

vmiirnm
_i I

75 too 125 ISO 175

DAYS AFTER FERTILIZATION

Figure 6. — Oxygen consumption per individual pink salmon egg
or alevin in three gravel incubators seeded with 6,400 eggs. Ninety-
five percent confidence limits for the periodic means were calcu-
lated using the error mean square from a one-way ANOVA for
sampling periods. Horizontal bars show when eggs hatched and
fry emerged.

mg/h per egg; by hatching, oxygen consumption
increased to about 0.010 mg/h per alevin. The
transient peak of oxygen consumption at the end
of hatching is probably associated with increases
in metabolism due to increases in activity during
the hatching process and activity of alevins as
they redistribute themselves within the incubator.
These transient increases during hatching would
have been more significant if the large numbers of
eggs in the incubators had hatched synchronously
over a day rather than over a 2-wk period. By the
time of emergence, oxygen consumption had in-
creased to a mean of 0.027 mg/h per alevin in the
incubators seeded with 6,400 eggs. In the in-
cubators seeded with other densities of eggs, oxy-
gen consumption per individual also increased as
eggs developed into alevins. The increase in oxy-
gen consumption by eggs and alevins during
development was in response to growth and
not in response to increased temperature. Tem-
perature remained nearly constant (about 3.6° C)
from 2 wk before hatching until all alevins
emerged.

Densities of alevins in the incubators influenced
the individual oxygen consumption rates (Figure
7 ). Before hatching, the oxygen consumption rates
per egg (days 89 and 96 1 were about the same in
incubators of different densities. After hatching
and to the time approaching emergence (days 117,
152, and 173, Figure 7), oxygen demand by indi-
vidual alevins increased with increased seeding
density (excluding the incubator with 25,600
eggs). The incubator seeded with 25,600 eggs (not

0.01

-DAYS AFTER FERTILIZATION

r 96 ,;

]_ 89 *

1,600 6.U00

SEEDING DENSITY, EGGS PER INCUBATOR

12,800

Figure 7. — The effect of seeding density on individual oxygen
consumption rates during development of eggs to emerging
alevins. Oxygen measurements were taken from incubator
effluents and corrected for emergence to milligrams/ alevin per
hour. Eggs hatched 100-120 days after fertilization, and alevins
from the 1,600-egg density emerged about 203-220 days after
fertilization.

shown in Figure 7) contained a large number of
dead eggs and alevins, which were decomposing.
As emergence approached (days 201 and 208),
oxygen consumption per alevin did not tend to
increase with alevin density.

The increased production of ammonia and con-
sumption of oxygen by alevins with increased
seeding densities indicate increased metabolic
rates caused by more frequent stimulation and
interaction of neighboring alevins.

QUANTITY AND QUALITY OF
FRY PRODUCED

Egg-to-Fry Survival and Time of Emergence

Survival from eyed eggs to fry in the incubator
seeded with 25,600 eggs (50%) was markedly
lower than survival in all other incubators ( ^92% ,
Table 1). Survival was almost 100% in the in-
cubator seeded with 12,800 eggs; the incubator
seeded with 12,800 eggs produced almost as many
live fry as the incubator seeded with 25,600 eggs.
Survival in the incubators seeded with 1,600 eggs
and 6,400 eggs ranged from 92% to 100%.

Alevins emerged markedly earlier from in-
cubators seeded with >6,400 eggs (Figure 8). If the

653

FISHERY BULLETIN: VOL. 78, NO. 3

time of50% emergence in the incubator with 1,600
eggs is used as a standard, 50% of the fry in in-
cubators seeded with 6,400 eggs emerged on the
sameday (15 April, day 212); 50% of the fry in the
incubator seeded with 12,800 eggs emerged 7 d
early (8 April, day 205); and 50% of the fry in the
incubator seeded with 25,600 eggs emerged 82 d
early (24 January, day 130).

150 175

DAYS AFTER FERTILIZATION

225

FIGLTRE 8. — Effect of seeding density on daily cumulative per-
centages of emergence of pink salmon fry from gravel incubators,
December 1971- April 1972. Horizontal bars show when eggs
hatched and fry emerged from incubator seeded with 1 ,600 eggs.
Number beside each line is the number of eggs seeded in each
incubator.

Size of Fry and Stage of Development

In the incubators with seeding densities above
6,400 eggs, fry emerged earlier and were shorter,
lighter, and less developed (higher Kq ) than fry in
incubators with lower seeding densities.

During the time we monitored emergence, ale-
vins emerging from the incubator seeded with
25,600 eggs were substantially smaller than ale-
vins emerging from the other incubators. At 50%
emergence, the alevins in the incubators seeded
with 25,600 eggs were in an earlier stage of devel-
opment (higher A'q) (Figures 9-11) than alevins in
other incubators.

Analysis of variance of average lengths of fry at
the three lower seeding levels — 1,600, 6,400, and
12,800 eggs — indicated significant and changing
differences (P<0.001), i.e., interaction, in fry
length among seeding densities and sampling
times (Table 2, Figure 9). At the first sampling time
(about 25% emergence), fry emerging from the
incubator seeded with 12,800 eggs were substan-

25 50 75

SAMPLING TIME (PERCENTAGE EMERGENCE)

Figure 9. — Average length of pink salmon fry that emerged
from gravel incubators seeded with indicated numbers of eggs.
Samples of 50 fry were taken from each incubator when 25%,
50%, and 75% of emergence from that incubator had occurred.
Bars represent 95% confidence limits. The sample for 25%
emergence at the 25,600 density was lost.

Table 2. — Analysis of variance of average lengths of pink salm-
on fry, with variation among seeding levels within sampling
times partitioned out.

Source

df

ss

MS

F

A Sampling times

2

0.18437

0.09218

—

B Seeding levels

2

0.63706

0.31863

—

Levels in time 1

2

1.21253

060626

78.33—

Levels in time 2

2

0.17941

0.08970

11.59"

Levels in time 3

2

0.04821

0.02410

3.11ns

A X B Interaction

4

0.80309

0,20077

25.93—

Wltliin

6

0.04641

0.00774

Total

14

1 .67093

•••p-iO.001.

••p<o.oi.

ns = not significant.

tially smaller than fry emerging from incubators
seeded with 1,600 and 6,400 eggs. At the second
sampling (about 50% emergence), fry emerging
from the incubator seeded with 12,800 eggs were
still smaller than fry emerging from incubators
seeded with < 12,800 eggs, but the difference was
not as large as at the first sampling. By the third
sampling (about 75% emergence), differences
were not statistically significant (P>0.05).

Analysis of variance of average weights of the
same fry from the three lower seeding densities
detected differences among seeding densities (Ta-

654

BAILEY ET AL.: EFFECTS OF SEEDING DENSITY OF PINK SALMON

260

250 -

210

5 230

>
a:

220

200

1,600
6,«00

12,800

1

25,600

25 50 75

SAMPLING TIME (PERCENTAGE EMERGENCE)

Figure 10. — Average weight of pink salmon fry that emerged
from gravel incubators seeded with indicated numbers of eggs.
Samples of 50 fry were taken from each incubator when 25%,
50% , and 75% of emergence from that incubator had occurred.
Bars represent 95% confidence limits. The sample for 25% emer-
gence at the 25,600 density was lost.

ble 3, P<0.01). Differences in weights were par-
ticularly evident at first sampling I about 259^
emergence. Figure 10), although no change in
these differences in average weight with time was
detectable, i.e., interaction was not significant
(P>0.05). Mean weight of fry in the incubator
seeded with 12,800 eggs was considerably less
than the mean weight of fry in the incubators
seeded with 1,600 or 6,400 eggs.

Analysis of variance of average developmental
index of these fry from incubators seeded with
1,600, 6,400, and 12,800 eggs determined that dif-
ferences among incubators varied with time, i.e.,
interaction is significant (Table 4,P = 0.05). At the
first sampling time, fry from the incubator seeded
with 12,800 eggs had a substantially larger mean
developmental index (were less developed) than
fry from incubators seeded with fewer eggs. Yolk
was still visible through the transparent abdomi-
nal sutures of fry in the incubator seeded with
12,800 eggs. At the second and third sampling
times, developmental indices did not vary sig-
nificantly among these lower densities (P>0.05,
Figure 11). However, early-emerging alevins from
the incubator seeded with 25,600 eggs were

Table 3. — Analysis of variance of average weights of pink

salmon fry.

Source

df

ss

MS

F

A Times

B Seeding levels

A X B Interactions

Within

Total

2

2

4

6

14

65836

150 0017

19.4129

39.7934

275.0440

32918

75 00085
4.853225
663223

11.308"
0.7317ns

•■p<o.oi.

ns = not significant.

Table 4. — Analysis of variance of average developmental index
of pink salmon fry with variation among seeding levels within
sampling times partitioned out.

Source

df

ss

MS

A Sampling times 2 0 00108893 0.000544465 —

B Seeding levels 2 0,00028737 0.000143685 —

Levels in time 1 2 0.00165333 0 000826665 8.24-

Levels in time 2 2 0 00013653 0 000068265 0.68ns

Levels in time 3 2 0.00031413 0.000157065 1.57ns

A X B Interaction 4 0 00181662 0 000454155 4.53-

Within 6 0.00060201 0 000100335

Total 14 000379493

•P<0.05.

ns = not significant.

clearly less developed at the second sampling than
early-emerging alevins in the other incubators
(Figure 11). (The first sample from the incubator
seeded with 25,600 eggs was lost.)

WATER QUALITY AND FRY

PRODUCTION IN RELATION TO

SEEDING DENSITY

The maximum concentration of total ammonia
(0.32 mg/1) detected during the experiment oc-
curred shortly after hatching in the effluent from
the incubator seeded with 25,600 eggs. Even in
combination with the highest pH encountered
during our study (6.4), this total ammonia con-
centration is equivalent to only 0.092 /Ltg/l NHg
(0.092 ppb). Concentrations of NHg 13 times
greater (1.2 ppb) inhibit grovvi;h of emergent fry
after 60-d exposures in their late alevin stages,
and concentrations 100 times greater stimulate
early emergence of alevins (Rice and Bailey
1980a). Concentrations of NH3«0.4 ppb have no
discernible effect on either size or emergence of
the alevins in late stages. Ammonia concentra-
tions in this experiment were not stressing even
though alevins nearing emergence are more sensi-
tive to NH3 than earlier alevin stages (Rice and
Stokes 1975; Rice and Bailey 1980a).

Similarly, Rice and Bailey (1980b) did not find
toxic concentrations of ammonia in samples of in-
tragravel water taken in late March from a
streambed where alevin densities were much

655

FISHERY BULLETIN; VOL. 78. NO. 3

2.10

2.08

2.06 -

2.M -

z

Q

2.02

Q

Z

<

I-

uj 2.00 -

1.98 -

1.96

I ,9i( -

25 50 75

SAMPLING TIME (PERCENTAGE EMERGENCE)

Figure ll. — Average developmental indices (Bams 1972) of
pink salmon fry that emerged from gravel incubators seeded
with indicated numbers of eggs. Samples of 50 fry were taken
from each incubator when 25% , 50% , and 75% of emergence from
that incubator had occurred. Bars represent 95% confidence
limits. The sample for 25% emergence at the 25,600 density was
lost.

lower than the highest densities in our experimen-
tal incubators. Densities of pink salmon alevins in
the stream sampled ranged from 0 to 352
alevins/0.1 m^ (mean, 21 alevins/0.1 m^), and the
highest concentration of NHg was 0.1 ppb. For
comparison, the alevin densities in our experi-
ment were >1,700 alevins/0.1 m^.

Oxygen consumption rates per individual in-
creased with time. The highest rate observed
(0.028 mg/h per alevin) occurred near the end of
incubation when 25% of the fry had emerged from
the incubators seeded with 1,600 and 6,400 eggs.
Further increases in rate of oxygen consumption
per alevin might have occurred before emergence
was complete, but this potential for stress was
eliminated because fry left the incubators.

The respiration rates of salmon eggs and alevins
are oxygen dependent (Fry 1957); consequently,

low dissolved oxygen concentrations in the water
will limit normal metabolic rates. Our data
suggest that oxygen concentrations below about 6
mg/1 may decrease the normal metabolism of pink
salmon alevins, although survival to emergence
may not be noticeably affected. Alevins in the
incubator seeded with 12,800 eggs were probably
stressed and began to emerge early, about 60 d
earlier than alevins in lower density incubators
(Figure 8), when oxygen concentrations decreased
to about 5 mg/1 (Figure 5). Just prior to peak
emergence (201 and 208 d after fertilization), ale-
vins in the incubators seeded with 6,400 and
12,800 eggs probably had their oxygen consump-
tion limited because oxygen concentrations had
decreased to <6 mg/1 at a time when their demand
was greatest. If oxygen concentrations were not
limiting, oxygen consumption rates (Figure 7)
would have been greater than the rates for alevins
in the 1,600-egg incubator as in the earlier mea-
surements.

Although ammonia (NH3) alone did not in-
crease to concentrations that decreased size at
emergence or reduced survival, it may have acted
synergistically with relatively low oxygen concen-
trations to create stressful conditions in our study.
In earlier studies, survival time offish exposed to
ammonia (NHg) was reduced at adequate but low
oxygen levels (Wuhrmann 1952; Downing and
Merkens 1955).

Stressful conditions associated with low dis-
solved oxygen concentrations alone, or in combi-
nation with ammonia, probably not only reduced
survival and caused premature emergence of fry
but may have also reduced the ability of alevins to
use yolk for growth. In incubation studies at simi-
lar temperatures, the developmental indices de-
creased and lengths increased just before
emergence of pink salmon fry (Bams 1972; Bailey
and Taylor 1974). A decrease of 0.01 in /C^ corre-
sponds to about 0.2 mm increase in length (Bams
1972; Bailey and Taylor 1974). In our study, the
developmental index decreased to about 1.96 at
emergence in the incubator seeded with 1 ,600 eggs
(Figure 11). The fry in the incubator seeded with
25,600 eggs were 28.44 mm, mean length, at 50%
emergence and had a mean developmental index
of 2.07. If these fry had remained in the incubator
until their developmental index decreased to 1.96,
they would have been only 30.64 mm long, 1.52
mm shorter than the fry emerging from the in-
cubator seeded with 1,600 eggs.

Survival from egg to fry exceeded 90% in in-

656

BAILEY ET AL.: EFFECTS OF SEEDING DENSITY OF PINK SALMON

cubators seeded with < 25,600 eggs, but survival
was only 5(y/( in the incubator seeded with 25,600
eggs. We attribute this poor survival to crowding,
possibly low dissolved oxygen concentrations, or
the combined effects of these and elevated NH^
concentrations. Ammonia, as a single factor, is
unlikely to reach levels harmful to pink salmon
alevins in gravel incubators supplied with slightly
acidic water, as the water in Auke Creek. However,
if the pH were 7.75 rather than 6.4, then the high-
est concentration of total ammonia, 0.32 mg 1,
would be equivalent to 2.1 ppb of NHg and would
reduce survival.

Much remains to be learned before we can define
combinations of seeding density and water flow for
efficient production of healthy, unfed fry. Seeding
densities of 1,200-1,800 eggs/0.015 m^ of gravel
and an apparent water velocity of 70-300 cm^/h
per cm^ can be used (Bams 1972; Bailey et al.
1976). Bams and Simpson (1977) suggested that
1,965 eggs/0.015 m^ with a water velocity of 200
cm/'h is safe. In our study, increasing seeding den-
sity from 1,600 eggs 0.015 m=^ to 6,400 eggs/0.015
m^ at a water flow of 53 cm /h apparently increased
swimming activity of the alevins and also in-
creased oxygen consumption and ammonia pro-
duction. However, the average length, weight, de-
velopmental index, emergence time, and survival
of these alevins were not importantly affected.

Under our experimental conditions, a seeding
density of 6,400 eggs /0. 015 m^ appears to be ac-
ceptable, although perhaps a nearly maximum
seeding density. Our test incubators were operated
at a water flow of only 0.81/ min ( apparent velocity,
53 cm^/h per cm^). If an apparent water velocity of
200 cm^/h per cm^ were used as recommended by
Bams and Simpson (1977), acceptable seeding
densities might be higher.

SUMMARY

Pink salmon eggs were seeded in gravel in-
cubators at four different densities (from 1,600 to
25,600 eggs/0.015 m^ of gravel) and incubated
until fry voluntarily emerged. Dissolved oxygen
and total ammonia concentrations of the in-
cubator effluent were monitored periodically, and
the emerged fry were counted, sampled, and mea-
sured. The rate of total ammonia production per
egg or alevin increased with time after seeding at
all densities. At seeding densities of 6,400 eggs/
0.015 m^ the rate of total ammonia production
increased from 2 x 10 "* mgh per egg 3 wk before

hatching, to 4 x 10^ mg/h per alevin at hatching,
to 6 X 10"* mg/h per alevin at emergence. The rate
of total ammonia production per individual also
increased with seeding density. Because of low pH
and low temperature, NHg concentrations did not
reach toxic or lethal concentrations in any in-
cubator; however, NH3 concentrations would have
become toxic in the incubator seeded with the most
eggs (25,600 eggs/0.015 m"^) shortly after hatch-
ing if the pH had been 7.75 rather than 6.4.

Rate of oxygen consumption per egg or alevin
increased during incubation. In the incubator
seeded with 6,400 eggs/ 0.0 15 m^, it increased from
0.003 mg/h per egg 3 wk before hatching, to 0.007
mg/h per egg at hatching, to 0.028 mg/h per ale-
vin at emergence. Probably because of increased
interaction between adjacent alevins, rates of
oxygen consumption per hour per alevin in-
creased, until emergence, with increased seeding
density. In incubators seeded with >6,400 eggs/
0.015 m^, dissolved oxygen concentrations
dropped to stressful levels (<6 mg/1) that limited
metabolism. At seeding densities >6,400 eggs/
0.015 m^, stressful conditions caused early
emergence of premature fry and reduced the abil-
ity of alevins to convert yolk for growth. Addition-
ally, survival was reduced at 25,600 eggs '0.015
m^. At an apparent water velocity of 53 cm^/ h per
cm^, a seeding density of 6,400 eggs appeared to be
marginally acceptable for the production of
healthy pink salmon fry.

ACKNOWLEDGMENTS

The pH determinations were made by James
Knull, oceanographer at the Auke Bay Labora-
tory. We wish to thank Don Alderdice, Envi-
ronment Canada, for his helpful review of this
manuscript.

LITERATURE CITED

Bailey, J. E., and W. R. Heard.

1973. An improved incubator for salmonids and results of
preliminary tests of its use. U.S. Dep. Commer,
NOAA Tech. Memo. NMFS ABFL-1, 7 p.

Bailey, J. E., J. J. Pella, and S. G. T.'XYLOR.

1976. Production of fry and adults of the 1972 brood of pink
salmon, Oncorhynchus gorbuscha, from gravel incuba-
tors and natural spawning at Auke Creek, Alaska. Fish.
Bull., U.S. 74:961-971.
BAILEY, J. E., AND S. G. TA\T0R.

1974. Salmon fry production in a gravel incubator hatch-
ery, Auke Creek, Alaska. 1971-72. U.S. Dep. Commer,
NOAA Tech. Memo. NMFS ABFL-3, 13 p.

657

FISHERY BULLETIN: VOL. 78, NO. 3

Bams, R. A.

1972. A quantitative evaluation of survival to the adult
stage and other characteristics of pink salmon iOnco-
rhynchus gorbuscha) produced by a revised hatchery
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Fish. Res. Board Can. 29:1151-1167.

Bams, R. A., and K. S. Simpson.

1977. Substrate incubators workshop - 1976. Report on
current state-of-the-art. Environ. Can., Fish. Mar. Serv.,
Tech. Rep. 689, 68 p.
BURROWS, R. E.

1951. A method for enumeration of salmon and trout eggs
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the toxicity of un-ionized ammonia to rainbow trout (Salmo
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Emerson, K., R. C. russo, R. E. lund, and R. V. Thurston.

1975. Aqueous ammonia equilibrium calculations: effect of
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Fry, f e. j.

1957. Theaquaticrespiration offish, /n M.E.Brown (editor).
The physiology of fishes. Vol. I, p. 1-63. Acad. Press, N.Y.

RICE, S. D., AND J. E. Bailey.

1980a. Survival, size, and emergence of pink salmon, Onco-
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WUHRMANN, K,

1952, Sur quelques principes de la toxicologie du poisson.

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658

SOME STATISTICAL CONSIDERATIONS OF THE DESIGN OF
TRAWL SURVEYS FOR ROCKFISH (SCORPAENIDAE)

William H. Lenarz and Peter B. Adams*

ABSTRACT

This study is in two parts. The first part reviews statistical theory for choosing among random,
stratified random, and systematic sample survey schemes when strata are of equal size and receive
equal sampling effort. The theory is applied to data collected during a pilot trawl survey for rockfish in
Queen Charlotte Sound, British Columbia, and a full scale survey along the coasts of Washington,
Oregon, and California. The results indicate that on a scale of about 80 km, a systematic survey scheme
provides more precise estimates than the other schemes. However, the differences in precision are
slight and probably should not outweigh other factors such as logistical constraints in the design of
trawl surveys. The second part of the study reviews statistical theory for sampling from negative
binomial distributions. Results of the Queen Charlotte Sound pilot survey indicate that except for fish
with very low densities, numerous tows of short distances are relatively more precise than fewer tows of
longer distances for trawl surveys for rockfish.

The Fisheries Conservation and Management Act
of 1976 requires the development of fishery man-
agement plans for each marine fishery under
jurisdiction of the United States. The requirement
emphasizes the need to assess the status of U.S.
fisheries. Estimates of stock abundance are essen-
tial for fishery assessment, and trawl surveys
often are used to estimate absolute or relative
stock abundance where suitable data from a
fishery itself are lacking.

Very little data are available from the com-
plex fisheries for rockfish (genus Sebastes) of the
Pacific coast of North America. The fisheries
are complex because many species and types of
gear are involved. Often landing statistics do
not specify species, and catches are seldom suf-
ficiently sampled for age, length, and sex com-
position. Catch per effort data also are not
reported by species and are difficult to interpret
because of temporal changes in fishing power and
target species.

Because of this lack of needed data, the North-
west and Alaska Fisheries Center of the National
Marine Fisheries Service initiated a large scale
trawl survey of rockfish stocks from southern
California to the Aleutian Islands. The first stage
of the 4-yr survey was to conduct pilot surveys in
the Monterey Bay area, Calif., and Queen Char-

Southwest Fisheries Center Tiburon Laboratory, National
Marine Fisheries Service, NOAA, 3150 Paradise Drive, Tiburon,
CA 94920.

lotte Sound, British Columbia, during 1976. The
overall goal of the pilot surveys was to provide
information for design of the full scale survey.
Gunderson and Nelson describe the pilot survey
and present preliminary results of the effort. A
full scale survey was conducted in 1977 off the
coasts of Washington, Oregon, and California.
Design of the 1977 survey was partly based on
results of the pilot surveys. Gunderson and Sam-
ple (1980) discussed the 1977 survey.

While trawl surveys have proven to be a useful
tool for assessing fish stocks, problems still remain
in their design and analysis. This paper presents
analyses of results of the Queen Charlotte Sound
pilot survey and 1977 survey. The analyses were
aimed at answering three questions: 1) Should the
full scale survey design be based on a random,
stratified random, or systematic scheme? 2) Do
results of the 1977 survey indicate that aspects of
the design based on the pilot survey were correct?
3) What are the trade offs in precision between
distance trawled and number of tows? Ancillary to
question one are the questions: 1) Are there
significant benefits to be gained by choosing one
or a combination of the three sampling schemes?
2) Are there significant biases in estimates of

Manuscript accepted December 1979.
FISHERY BULLETIN: VOL. 78, NO. 3, 1980.

^Gunderson, D. R., and M. O. Nelson. 1977. Preliminary
report on an experimental rockfish survey conducted off
Monterey, California and in Queen Charlotte Sound, British
Columbia during August-September, 1976. Prepared for Feb-
ruary 15-16, 1977 Interagency Rockfish Survey Coordinating
Committee Meeting, Northwest and Alaska Fisheries Center,
Seattle, Wash., 82 p.

659

FISHERY BULLETIN: VOL. 78, NO. 3

either means or variances using one or a combina-
tion of the three sampling schemes?

While our analyses are limited to data from
the Queen Charlotte Sound pilot survey and the
1977 survey, the questions repeatedly arise in
discussions of trawl surveys and thus are of
general interest.

COMPARISONS OF RANDOM,

STRATIFIED RANDOM, AND

SYSTEMATIC SAMPLING

Methodology

Chapter 8 of Cochran ( 1964) discusses systemat-
ic sampling and presents methodology for choosing
among random, stratified random, and systematic
(every /jth) sampling. Similar discussions are
found in other sampling texts such as Hansen et
al. (1953) and Sukhatme and Sukhatme (1970).
The methodology used in comparing the three
sampling techniques assumes equal sampling
effort in each strata. If prior information indicated
that variance differs considerably among strata,
the optimal stratified random sampling scheme
would not be equal allocation of sampling effort
among strata. Unfortunately as shown by Abram-
son (1968), it can be difficult to obtain meaningful
information on within strata variance for trawl
surveys even if previous surveys have been made
in the area. The methodology also only considers
regularly spaced strata of uniform size. While
prior knowledge (catch records) made it possible to
design strata of unequal size on a large scale
basis, knowledge is insufficient to do so on the
scale considered in the analysis. The multispecies
aspects of the survey made it particularly difficult
to devise an optimal stratified random scheme.

In this section we use Cochran's notation. How-
ever, instead of examining components of variance
for choosing among the three types of sampling as
Cochran did, we calculated the variances for each
type of sampling. Using the notation of Cochran,
let a population of k possible systematic samples
be represented by

Member Systematic sample number
1 ... i ... k

1 jii ■■■ Jh •■■ yk\

n

yij

yin

yu

yin

ykj

ykn

where yij is the 7 th member of the jth systematic
sample.

If the yifs are arranged as they actually occur
for a population of two systematic samples {k = 2)
with four (n = 4) members they appear as follows:

Unit 12 3 4 5 6 7 8

Variable y^ 3^21 y 12 3' 22 >'i3 3' 23 3'i4 >'24-

In a systematic survey a number (i) is chosen
between 1 and k and then n members that are k
units apart are sampled. Under a scheme of
drawing one systematic sample, either units 1, 3,
5, and 7 or 2, 4, 6, and 8 would be observed. Under a
stratified random scheme one unit out of each of
four strata (units 1 and 2, 3 and 4, 5 and 6, and
7 and 8 ) would be chosen at random for observa-
tion. Under the corresponding random scheme
any four of the eight units would be chosen at
random to be observed. The example population
contains 2 possible systematic samples, 16 pos-
sible stratified random samples, and 70 possible
random samples. While more than 20'7f of the
possible random samples match with a stratified
random sample, <3% match with a systematic
sample. A systematic sample is much more struc-
tured or constrained than the other schemes.
Population variances of the means of random,
stratified random, and systematic sampling are
calculated as follows:

(1)

where V (yran) = variance of the mean calcu-
lated from random sampling

(yran),
N=kXn,

ran

k

n

2

2;

1=1

j=l

fe

n

2

2

(=1

7=1

{y,j'yYIN-\,

y, 1^^

660

LENARZ and ADAMS: SOME STATISTICAL CONSIDERATIONS OF TRAWL SURVEYS

(2)

V {yst ) - — }v~ ^st/"

where V (5'st) = variance of the mean calcu-
lated from stratified random
sampling (J St),

o,,* —

1

77 \2

^^ = ht^) ,?i ,fi ^y^j ~ y.j ^

yj = '^ yijlk,and
1=1

S' (Jsvs)

sys'

1 2 (y. - yy

(6)

where S^ (3' sys) - estimate of V (>'sys),

>', = S yJk, and
1=1

v(ysys) = T s iy,-y)

r,\2

k

(3)

i-i

where V (^-gys)

yt. =

variance of the mean calcu-
lated from systematic sam-
pling (^sys) ,

S yijin.

7=1

If k systematic samples are taken from a popula-
tion that is sufficiently large to ignore the finite
population correction factor then the variance
estimates become:

S' (Xan) = S'ln (4)

where S^ (jran) = estimate of V (>'ran)>

sL = 2 s {y,j-y)' link-1),

1=1 ;=1

k n

y= 2 2 yulkn,
j=i j=i

s' (yst) - si. In

where S^ (ysO = estimate of V (yst),

(5)

n k

"st

;^(^^ A ll ^^^>"^.P'

Results of Pilot Survey

In the case of the Queen Charlotte survey, two
random starting points were chosen and then tows
were made along four transects for each of the two
systematic samples. The transects within a sys-
tematic sample were approximately 16.1 km
(10 mi) apart and bottom topography dictated
some deviations from the desired transects. Be-
cause preferred depths differ among species of
rockfish (e.g., Sebastes alutus is relatively scarce
in shallow waters, while S. proriger is relatively
scarce in deep waters), attempts were made to dis-
tribute sampling effort among 18.3 m (10-fathom)
depth intervals within the depth range of concern,
91.4 m (50 fathoms) and 292 m (160 fathoms).
Examination of the data indicated that, to obtain
reasonable sample sizes, observations should be
divided into only three depth intervals: 91-145 m
(79 fathoms), 146-181 m (80-99 fathoms), and
>181m.

The Queen Charlotte data were organized in
two ways to examine the relative precision of the
three sample schemes. We first arranged tows at
depths >181 m into a hypothetical population of
four systematic samples for each species. While
the original sample design called for two system-
atic samples, the two random starting points
resulted in all transects being about 8.1 km (5 mi)
apart. Each systematic sample contains two mem-
bers. Furthermore, each hypothetical population
is composed of x is = the average catch (kilograms)
per 1.8 km (nautical mile) of species s of all tows
taken >181 m in transect i of the Queen Charlotte
survey. Under the preceding definition the hypo-
thetical population of systematic samples of spe-
cies s is

661

FISHERY BULLETIN: VOL. 78, NO. 3

Member Systematic sample

12 3 4

1 .Vll^-^lS >'21=-^2S ^31=^38 3'41--^4S

2 ^12 = -^58 ^22= -^68 >'32=-^7S 3'42 = -^8S •

In this case k — 4 and n = 2. The yifs are averages
of 1-5 tows (Table 1). The resulting estimates of
variance apply only to these hypothetical popula-
tions and particular mixture of tows per average
iyij). It was not possible to construct similar
hypothetical populations for the other depth inter-
vals because of missing cells.

Values of V (yran), V {ysO, and V (j^gys) for the
first hypothetical populations are shown in Table
2. Comparison of the precision of the three sam-
pling methods indicates that systematic sampling
would be the most precise (has lowest variance)
scheme for 8 of the 15 species. Ties occurred for the
other seven species. Assuming that each species
represents an independent observation, the sign
test indicated that systematic sampling gave

Table l. — Number of tows taken during the Queen Charlotte
survey by stratum, systematic sample, member, and group of
hypothetical populations.

First group of hypothetical populations
Systematic sample

Member

1 2

3

4

1
2

1 1

2 2

1
4

2
5

Second group of hypothetical populations
Systematic sample

Depth (m)

Member 1

2

91-145

146-181

>181

Table 2. — Variances of means of catch (per 1.8 km towed) from
the first hypothetical populations of Queen Charlotte rockfish.
Calculations are made under random, stratified random, and
systematic sampling schemes.

Variance

Population

Random

Stratified random

Systematic

Setiastes alutus

6,595.069

5,791.227

3,312.254

S. flavidus

0.188

0.188

0 188

S. pinniger

0.003

0.003

0.003

S. paucispinis

0 766

0.734

0 620

S. brevispinis

6.601

6.431

6.273

S. elongatus

0.002

0.002

0.002

S. proriger

0.002

0.002

0 002

S. babcocki

225.734

238.282

191 356

S. crameri

0.107

0.083

0.060

S zacentrus

73.723

74.613

71.624

S. diploproa

0.344

0.329

0.329

S. entomelas

0.117

0.117

0.117

S. reedi

74.625

74.625

74.625

S. aleutianus

0.246

0.266

0.163

S helvomaculatus

0.056

0.057

0.054

better results than stratified random sampling
and random sampling at the 1% level of sig-
nificance, and that stratified random sampling
did not give significantly better results than
random sampling.

Because of the uneven distribution of tows per
transect, we organized the data in another fashion
to determine if the relative precision of the three
sampling schemes is affected by organization of
the data.

We next grouped the data into three depth
intervals: 91-145 m, 146-181 m, and >181 m. In
order to avoid missing cells it was necessary to
create hypothetical populations of only two sys-
tematic samples with two members. We did so as
follows: X is^ = the average of catch (kilograrhs)
per 1.8 km of species s in depth interval d of all
tows in transects i and i + 1. The hypothetical
population of systematic samples of species s from
depth interval d is

Member
(stratum)

1
2

Systematic sample
1 2

J'li ~ -^ 1 and 2, s. d ^21 ~ ^ 3 and 4, s, d
yi2 — X ^ and 6. s, d J'22 ~ X ^ and 8, s, d •

In this case k = 2 and n = 2. The yifs are
averages of 1 to 9 tows (Table 1). The values
of V (^ranK V (^stK ^^d V (jgyg) are shown in
Tables.

The results indicate that systematic sampling
produces more precise estimates of rockfish densi-
ties than either random or stratified random
sampling. However, the sign test revealed that
systematic sampling is not significantly better
than stratified random sampling and only better
than random sampling at the 5% level of sig-
nificance. Stratified random sampling was not
significantly better than random sampling. While
systematic sampling appears to be the most pre-
cise of the three survey design schemes, there
were many cases in which two or more of the
schemes would be equally precise. In many other
cases little precision would be lost if either strati-
fied random or random designs were chosen.

Results of 1977 Survey

The 1977 survey design included both stratified
random and systematic sampling strategies. The
coast was stratified into three types of areas: high
density sampling, low density sampling, and no

662

LENARZ and ADAMS: SOME STATISTICAL CONSIDERATIONS OF TRAWL SURVEYS

Table 3. — Variances of means of catch (per 1.8 km towed) from
second hypothetical populations of Queen Charlotte rockfish.
Calculations are made under random, stratified random, and
systematic sampling schemes.

Variance

Population

Depth
interval (m)

Stratified
Random random Systematic

Se5as(es alutus
S. alutus
S. alutus
S. flavidus
S. flavidus
S. flavidus
S. pinniger
S. pinniger
S. pinniger
S. pa uc is pin is
S. paucispinis
S. paucispinis
S. brevispinis
S. brevispinis
S. brevispinis
S. elongatus
S. elongatus
S. elongatus
S. proriger
S. proriger
S. proriger
S. babcocki
S. babcocki
S. babcocki
S crameri
S. crameri
S. crameri
S. zacentrus
S. zacentrus
S. zacentrus
S diploproa
S. diploproa
S diploproa
S entomelas
S. entomelas
S. entomelas
S. reedi
S. reedi
S. reedi
S. aleutianus
S^ aleutianus
S. aleutianus
S. helvomaculatus
S helvomaculatus
S. helvomaculatus

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

91-145

146-181

>181

82.313
2.745.670
1,892.520
8.442
0.259
0063
257.220
0.507
0.001
2.657
1.560
0.260
60.440
8.703
2.328
0.129
0.327
0.001
1,019.197
5.152
0.002
2.090
3.241
49.730
0.001
0.057
0.061
0.006
0.220
29.261
0.000
0.000
0.165
0.006
0.609
0.048
0.000
0,302
30.710
0 000
0.002
0.087
0.000
0.001
0.022

59.446
3,803.277
1,270.058

12.750
0.193
0.063
234.198
0.759
0.001
3.987
0.287
0.197

19,718

13.020
2.194
0.100
0.317
0.001
686814
5.560
0.002
1.584
0,339

50,671
0,001
0051
0,037
0006
0.217

30.641
0.000
0 000
0.162
0.006
0.724
0.048
0 000
0.302

30.710
0.000
0.002
0.057
0.000
0.001
0.024

55.285

1,125.770

2,502.014

0.102

0.160

0.063

228.577

0.400

0.001

1.503

0.402

0.121

13.783

1 1 .262
3.464
0.102
0,345
0.001
657.281
6.494
0.002
1.169
0.339

24.671
0.001
0.029
0.074
0.006
0.217

30.641
0.000
0.000
0.162
0.006
0.378
0.048
0.000
0.302

30.710
0.000
0.002
0.018
0.000
0.001
0.020

sampling. Areas in which historical fisheries data
indicated high abundances of important rockfish
species were assigned high density sampling. In
these areas, transects were set at 8.1 km (5-mi)
intervals. The typical high density area used in
the study was about 81 km ( 50 mi) long. Transects
in other areas were set at 16.1 km (10-mi) intervals
unless bottom topography precluded sampling.
Each transect was divided into four 91 m (50-
fathom) depth strata between 91 and 457 m
(250 fathoms). Sampled depths were then chosen
at random within each depth stratum of a tran-
sect. The number of samples within a depth
stratum was proportional to the bottom area of
that stratum.

The survey design was based on several factors.
The large scale stratification along the coast was
an attempt to make sampling proportional to
expected densities of important rockfish. This
was done with the knowledge that there often are
positive correlations among means and variances
of fish densities. Depths were randomly chosen
because it was known that often within an area
densities of many species of rockfish sometimes
only occur over a narrow depth interval. Thus,
unless depths were chosen at random, bias could
occur. Sampling was proportional to bottom area,
because bottom area is used to convert fish densi-
ties to abundance estimates. Systematic transects
were taken to ensure adequate aerial coverage for
one intended use of the data, because of logistics
and the results of the pilot survey.

Four high density areas had sufficient sampling
effort to be included in the study. Eight or more
adjacent transects were sampled in one or more
depth strata in each chosen area. Area 1 was
between lat. 34°33' and 35°19' N, area 2: lat.
35°19' and 35°59' N, area 3: lat. 39°7' and
39°53' N, and area 4: lat. 44°59' and 45°50' N.
If more than one sample was taken from a depth
stratum of a transect, one sample was chosen at
random for the study. As in the case of the first
Queen Charlotte hypothetical populations, pop-
ulations of four or five systematic samples of two
members each were created from the data. The
results again indicated that systematic samples
were slightly more precise than either random or
stratified random (Table 4). The sign test indi-
cated that systematic sampling was more precise
than random at the 1% level of significance and
stratified random at the 107c level. Stratified
random sampling was not significantly less pre-
cise than random.

The data were also arranged into two systematic
samples with four or five members each. System-
atic sampling was more precise than random at
the 1% level of significance, but was not signifi-
cantly more precise than stratified random (Table
5). Stratified random sampling was not signifi-
cantly less precise than random sampling.

Discussion

The results of this study indicate that on a scale
of about 80 km along the coast systematic sam-
pling for rockfish is slightly more precise than
random sampling or a stratified random scheme
with regularly spaced strata of equal size and

663

FISHERY BULLETIN: VOL. 78. NO. .!

Table 4. — Variances of means of catch (per 1.8 km towed) from hypothetical populations of rockfish that
were constructed from 1977 survey data. Calculations are made under random, stratified random, and system-
atic sampling schemes. Hypothetical populations are composed of either four or five systematic samples
with two members.

Systematic samples

Area

Depthi interval (m)

Variance

Population

Random

Stratified random

Systematic

Sebastes alulus

4

4

183-273

6,276924

6.232073

5.426781

S alutus

4

4

366-457

46 552

49621

51.403

S flavidus

4

2

91-182

0090

0.102

0.074

S pinniger

4

1

91-182

8420

6.604

6.604

S pinniger

4

2

91-182

0.185

0.215

0 422

S- paucispinis

4

1

91-182

9,630 529

9,888812

8.989353

S paucispinis

4

2

91-182

34452

39381

27.818

S paucispinis

5

2

183-273

24.181

23.665

30.904

S paucispinis

5

3

91-182

37 490

42 176

81 772

S brevispinis

4

4

183-273

2.185

2.290

1.421

S. elongatus

4

1

91-182

3.651

3 930

3.039

S elongatus

4

2

183-273

0060

0.054

0054

S elongatus

5

3

91-182

3.062

2 994

2 994

S. elongatus

4

4

183-273

63 100

66 665

93.148

S babcocki

4

2

183-273

3974

3434

3.434

S babcocki

4

2

274-365

4 998

5.820

8 106

S. babcocki

4

3

366-457

0789

0469

0469

S babcocki

4

4

183-273

7.761

6.086

6 125

S babcocki

4

4

366-457

90.164

85.971

85 971

S. cramen

4

2

274-365

32481

27 882

26 134

S crameri

5

2

366-457

3.516

3200

3.200

S. crameri

4

4

183-273

1.903.722

1,948.233

1,741.187

S crameri

4

4

366-457

0230

0.251

0.110

S. zacentrus

4

4

183-273

15.078

12.492

12.492

S diploproa

4

2

183-273

1,255 342

1,389 344

1,317.551

S diploproa

4

2

274-365

2.861 498

3,304.897

5.275483

S. diploproa

5

2

366-457

2.727.360

1,979 702

948.597

S diploproa

4

3

366-457

159.021

68670

91.114

S diploproa

4

4

183-273

683.478

700.234

779467

S. diploproa

4

4

366-457

1 827

1 966

1.216

S. entomelas

4

1

91-182

467.709

468.780

476280

S. entomelas

4

2

91-182

1.012

1.001

0.981

S. entomelas

4

2

183-273

3.050

3.103

2.633

S entomelas

5

3

91-182

0 376

0423

0846

S entomelas

4

4

183-273

3.002

3.057

2.129

S. aleutianus

4

4

366-457

589997

688030

399 129

S goodei

4

1

91-182

119.235

119.105

121.329

S goodei

4

2

91-182

4,439.160

4,391.472

4.226895

S. goodei

4

2

183-273

416.868

468696

301.373

S. goodei

5

3

91-182

258 380

221.057

220.347

S jordani

4

1

91-182

467.621

406.738

399.790

S jordani

4

2

91-182

26.765.442

27.254.716

25.958.703

S jordani

4

2

183-273

7256

8.158

5.457

S. jordani

5

3

91-182

0.575

0.570

0 570

S. saxicola

4

1

91-182

11.033.375

8.981.548

8.450.645

S saxicola

4

2

91-182

145.957

162.133

120 545

S saxicola

4

2

183-273

11,177.436

11,261.334

11.301.092

S. saxicola

4

2

274-365

0.244

0.235

0.235

S. saxicola

5

2

366-457

0.104

0.066

0.057

S. saxicola

5

3

91-182

3,402868

3,070.065

3,068507

S. saxicola

4

3

366-457

3.106

3.304

2.843

S saxicola

4

4

183-273

4.630

4,187

3.308

S. rufus

4

2

183-273

10.247

11.501

10.092

S rufus

4

2

274-365

6 588

6.561

7.374

S. rufus

5

2

366-457

0.513

0.566

0.870

S aurora

4

2

274-365

6.835

7.591

6.215

S aurora

5

2

366-457

22452

24.477

20.423

S. aurora

4

3

366-457

54.214

45.845

45.465

S aurora

4

4

366-457

0.507

0.511

0.782

S. melanostomus

4

2

274-365

0.566

0.148

0.148

S melanostomus

5

2

366-457

22.167

20.848

24547

Average

1,398.584

1,369.394

1,314.689

observations. It was also noted that our present
state of knowledge precludes more optimally de-
signed stratified random schemes on the scale
considered. It appears that the decision to space

664

transects of the 1977 survey in a systematic
fashion was correct. While the data do indicate
that systematic sampling is more precise than
stratified random, the differences are slight and

LENARZ and ADAMS: SOME STATISTICAL CONSIDERATIONS OF TRAWT SURVEYS

Table 5. — Variances of means of catch (per L8 km towed) from hypothetical papulations of rockfish that were
constructed from 1977 survey data. Calculations are made under random, stratified random, and systematic
sampling schemes. Hypothetical populations are composed of two systematic samples with four or five members.

Variance

Population

Members

Area

Depth interval (m)

Random

Stratified random

Systematic

Sebastes alutus
S alutus
S flavidus
S pinniger
S pinniger
S paucispinis
S paucispinis
S paucispinis
S paucispinis
S brevispinis
S elongatus
S elongatus
S. elongatus
S elongatus
S babcocki
S babcocki
S babcocki
S babcocki
S babcocki
S. crameri
S. crameri
S. crameri
S. crameri
S zacentrus
S diploproa
S diploproa
S diploproa
S- diploproa
S diploproa
S diploproa
S entomelas
S. entomelas
S entomelas
S entomelas
S entomelas
S aleutianus
S goodei

goodei
. goodei
- goodei
'. jordani
. jordani

fordani
S jordani
S saxicola
S saxicola
S saxicola
S saxicola
S saxicola
S- saxicola
S saxicola
S saxicola
S. rufus
S rufus
S rufus
S aurora
S. aurora
S aurora
S aurora
S melanostomus
S. melanostomus

Average

S
S.
S
S,
S
S

4
4
4
4
4
4
4
5
5
4
4
4
5
4
4
4
4
4
4
4
5
4
4
4
4
4
5
4
4
4
4
4
4
5
4
4
4
4
4
5
4
4
4
5
4
4
4
4
5
5
4
4
4
4
5
4
5
4
4
4
5

4
4
2
1
2
1
2
2
3
4
1
2
3
4
2
2
3
4
4
2
2
4
4
4
2
2
2
3
4
4
1
2
2
3
4
4
1
2
2
3
1
2
2
3
1
2
2
2
2
3
3
4
2
2
2
2
2
3
4
2
2

183-273

366-457

91-182

91-182

91-182

91-182

91-182

183-273

91-182

183-273

91-182

183-273

91-182

183-273

183-273

274-365

366-457

183-273

366-457

274-365

366-457

183-273

366-457

183-273

183-273

274-365

366-457

366-457

183-273

366-457

91-182

91-182

183-273

91-182

183-273

366-457

91-182

91-182

183-273

91-182

91-182

91-182

183-273

91-182

91-182

91-182

183-273

274-365

366-457

91-182

366-457

183-273

183-273

274-365

366-457

274-365

366-457

366-457

366-457

274-365

366-457

1,569 231

15.517

0.030

2,807

0,062

3.210,176

1 1 ,484

6,045

9,373

0,546

1,217

0,015

0 766

15,775

0,994

1,666

0,263

30,055

1,940

10,827

0.879

475,931

0,077

3,770

313,836

953 833

681,840

53 007

170,870

0609

155,903

0,337

0,763

0,094

0,751

196 666

39,745

1.479,720

104,217

64 595

155,874

8,921,814

1,814

0,144

3.677^92

48652

2,794,359

0081

0,026

850,717

1,035

1,158

2 562

2,196

0 128

2,278

5,613

18,071

0 169

0 189

5,542

427,483

1,576 140

5 162

0,034

3,261

0 072

3.203,033

13 142

5,266

10,639

0,226

1,436

0,016

0,656

17,090

1,102

0,909

0,197

31,103

0,551

12414

0372

378,362

0 107

0,485

243015

869,422

375,130

25279

178,211

0,803

156 260

0,402

0,275

0,106

0,849

199 264

38 155

1,367,750

127,159

72,201

163,576

9,116,721

2,179

0,137

335847

55,079

3.362,293

0,069

0,007

916,415

1,101

1.285

1.899

2.447

0.144

2.502

2,157

12,091

0045

0,008

4 153

375349

3.193.380

3.195

0.063

6.439

0.141

2.889.063

24.503

3.534

1.145

0.336

2.441

0.026

0.656

1 1 .696

0.130

0.063

0.002

38.440

1.000

2.403

0.372

426423

0.035

0.281

367,489

1 .065.206

53 290

0,191

122,324

0,090

158 760

0.856

0.723

0.000

0,250

398,003

35,106

1,531 744

335,989

140 660

85794

7,983,423

0 004

0 137

431 081

106,864

3,068,052

0.069

0.000

388,878

0,640

2.789

2.161

3.331

0.000

0.902

1.988

14.440

0.051

0.004

3.686

375,586

probably should not outweigh other factors such
as logistical constraints in the design of trawl
surveys.

The sign test used to test the significance of
differences among sample designs assumed that
values for each species were independent. To

examine this assumption we calculated correla-
tion coefficients for each species pair in each
combination of depth and area. Only samples
containing at least one occurrence of each species
of a pair were included. The average of the
absolute value of the correlation coefficient is

665

FISHERY BULLETIN: VOL. 78. NO. 3

0.324. This indicates that the assumption of in-
dependence is reasonable.

Even though our results indicate that system-
atic sampling is slightly more precise for the type
of survey studied, the consequence of using a
systematic design when another design may be
more appropriate should be considered.

We first examine the effects of using a system-
atic design when in actuality the data are ran-
domly distributed. Under these conditions the
expected value of S ^st of Equation (5) is equal to
the expected value of S^sys of Equation (6) and is
related to the expected value of S^ran of Equa-
tion (4) as follows:

E (S'J

nk-1
nk —n

E (S;a„)

Thus, random sampling will produce the lowest
variance and if total sampling effort ink) is
constant, the variance of systematic and stratified
random sampling will decrease relative to random
sampling as n decreases. All three design strate-
gies will result in unbiased estimates of the mean.
If there is a linear trend in the data such as
shown below

Transect 12 3 4 5 6 7 8
Value 1 1.5 2 2.5 3 3.5 4 4.5,

then as Cochran (1964:217) showed, stratified
random sampling is the same or more precise than
systematic sampling, which is the same or more
precise than random. The discrepancies increase
as 77 increases.

If there are cycles in the data with a periodicity
equal to or a multiple of spacing of transects
such as

Transect 12 3 4 5 6 7 8
Value 12 12 12 12,

then systematic sampling is less precise than
stratified random sampling, which is less pre-
cise than random sampling. The discrepancies
increase as n increases. In addition, a single
systematic sample would result in a biased esti-
mate of the mean.

Systematic sampling is equal to or more precise
than stratified random sampling which is equal to
or more precise than random sampling if a popula-

tion in which a plot of correlations between pairs
of transects against distance between transects is
concave upward and greater than or equal to 0
(Cochran 1964). Since systematic sampling was
the most precise in this study, bias due to periodic-
ity in the data should not be a problem.

Often in practice, investigators use a systematic
sampling scheme with only one sample and cal-
culate the variance as if the scheme is random. If

V (j'sys' is <V (jranK as it appears to be for
rockfishes, the resulting confidence limits would
be conservative. The choice between precision and
estimation of V (5'sys) would depend on the objec-
tives of the survey and the difference between
V(jran) and V (5'sys). If V(ysys) is <V(5'ran) and
total number of transects is constant, increasiiig
the number of systematic samples {k) in order to
estimate V (^sys) causes the sampling scheme to
become more like a random scheme and results in
a corresponding increase in V (5'sys* relative to

V (3' ran) (compare average variances shown in
Tables 4 and 5).

A review by Cochran (1964) of a small number of
surveys of terrestrial populations also indicated
that systematic sampling is more precise than
stratified random. Although Cochran did not state
so, it also appeared that systematic sampling
would be more precise than random sampling.

Two studies were found in the literature on
marine populations. Venrick (1978) found that on
the average systematic samples of chlorophyll in
the water column produced estimates of total
chlorophyll that were closer to the true value than
stratified random samples, but was not able to
compare precision of estimates for a given water
column because only one systematic sample was
taken from each column. She expressed a pref-
erence for stratified random sampling, because
there tended to be more temporal correlations of
deviations of the estimated values from the true
values for the systematic samples than for the
stratified random samples. The deviations were
usually < 5% and the temporal correlations prob-
ably could have been eliminated if the starting
points of the systematic samples were observed at
random instead of being fixed at the surface as
was done in her study. Fiedler (1978) examined
the relative precision of random, systematic, and
stratified systematic transect surveys of northern
anchovy, Engraulis mordax, school groups. He
found that random sampling was the least precise
of the three schemes. He also found that stratified

666

l.ENARZ and ADAMS: SOME STATISTICAL CONSIDERATIONS OF TRAWL SURVEYS

systematic sampling was more precise than sys-
tematic sampling when school groups were dis-
tributed in a highly nonrandom way. Systematic
sampling was more precise than stratified sys-
tematic sampling when sampling density was
high. In other cases there were no significant
differences between systematic and stratified sys-
tematic sampling.

Fiedler based allocations of sampling effort
among strata on results of previous sampling. His
results, in conjunction with those of Abramson
(1968) and Venrick (1978), indicate the difficulty
of determining optimum allocation of sampling
effort among strata in the marine environment.
The frustration of scientists who have attempted
to do so is aptly stated by Venrick: "Study A
demonstrated the dependence of the success of a
sampling design upon the interaction of that
design with the structure of the population being
sampled; thus, it would seem that intelligent
application of knowledge about the sampled popu-
lation should improve the design. It was, there-
fore, disconcerting to find that RSS every 20 m,
RSS-1, consistently performed as successfully as
did RSS-3 which was designed by a presumably
experienced worker (the author) with total knowl-
edge about the population to be sampled."

We hope that improved knowledge on the dis-
tributions of populations will eventually result in
more efficient allocation of effort among strata of
systematic or random sampling schemes in the
marine environment. However, we point out that
fishermen still have their failures in attempting
to restrict their sampling effort to times and areas
of high fish catches in spite of years of experience,
sophisticated fish finding equipment — presum-
ably flexible sampling plans — and at times recent
information from their colleagues.

EXAMINATION OF TRADE OFFS

BETWEEN TOW LENGTH AND

NUMBER OF TOWS

The distance trawled is an important factor to
consider in the design of trawl surveys. Considera-
tions include distance needed to obtain sufficient
specimens for biological samples; time required to
set and retrieve a trawl, to cover the distance, and
to move between trawl locations; and the relation-
ship among precision, tow length, and number
of tows.

In this section we first use a negative binomial
model with varying element size to estimate the

relationship among precision and tow length and
number of tows. We next use this relationship and
time factors to illustrate the relationship between
logistically feasible tow lengths and precision.

Animals in nature are rarely randomly distrib-
uted. They usually show some degree of aggrega-
tion or contagion. When these populations are
sampled, they lead to distributions which are
markedly skewed and have a large proportion of
zero elements. The negative binomial distribution
is often assumed for such populations because of
practical performance (Laubscher 1961; Pielou
1969) and theoretical basis (Taylor 1953; Patil and
Stiteler 1974). The distribution can be used to
provide an estimate of the relationship between
sample element size and precision.

The negative binomial distribution often is used
to describe observed distributions in both general
ecological research (Pielou 1969; Poole 1974) and
fisheries research (Taylor 1953; Moyle and Lound
1960; Lambou 1963; Roessler 1965; Clark 1974).
The distribution is characterized by two param-
eters, m the mean number of units per sampling
element, and k, an "index of aggregation" (Waters
1959). The value of k varies inversely with the
degree of aggregation of the population. The
variance of a mean drawn from a population which
follows a negative binomial distribution (Vnb) is
a function of the mean ( m ) and k ,

Xib = '^ ^ ^'Z^-

As the degree of aggregation increases, k ap-
proaches 0 and when the empty elements are
ignored, this distribution approaches Fisher's log-
arithmic series. As the degree of aggregation
decreases, k will approach infinity and the dis-
tribution converges to the Poisson.

The negative binomial can be derived from five
or more different models, which may be mutually
contradictory (Anscombe 1950; Bliss and Fisher
1953). A commonly used procedure to derive the
distribution is to assume that it arises from a
cluster of objects in space where the clusters follow
a Poisson distribution and the number of animals
in a cluster are distributed according to Fisher's
logarithmic series. Taylor (1953) derived a form of
the negative binomial as a probability model
specifically to describe the relative abundance of
fish species in trawl catches.

The data used for this analysis come from the
pilot survey made in Queen Charlotte Sound.
Since the negative binomial distribution is a

667

FISHERY BULLETIN: VOL. 78. NO. 3

discrete function, catches are measured in num-
bers of fish instead of weight as in the preceding
section.

Fitting data from a systematically designed
survey to the negative binomial distribution is a
common practice (Moyle and Lound 1960; Taft
1960; Roessler 1965; Clark 1974). Hairston et al.
(1971) made one of the few studies of sampling
design for measuring spatial pattern. They found
that estimates based on a grid (systematic) pat-
tern were superior to those made from sampling at
random. The grid pattern correctly reflected the
spatial patterns of 17 of 22 species, while random
sampling with the same number of samples cor-
rectly reflected only 12 of 22 species.

The standard negative binomial model requires
a constant element size. This leads to two prob-
lems. The first is that comparisons can only be
made at one sampling element size. The second
problem is the negative binomial model cannot be
fit to data with variation in sample element size.

To specifically deal with these problems, Bissell
(1970, 1972) derived a negative binomial model
that can be used when sample element size is
variable and/or to predict the distribution of
events for element sizes which differ from those
on which the observations were based. The prob-
ability of observing Xi events on the i element
which has a size of wi is

Table 6. — Estimates of mean densities (d) (in numbers per
kilometer), k, standard errors, with chi-square goodness of
fit tests for trawl catches made in all depths in the Queen
Charlotte survey.

Mean

Chi-square

Species

density

SE(d)

k

SE(/()

probability

Sebastes alutus

75.368

18 466

0.334

0.055

N.S.

S. Ilavidus

0648

0028

2.608

0.803

PeOOl

S. pinniger

1.564

0287

0 398

0.071

N.S.

S paucispinis

0 508

0,072

2.546

0814

N.S.

S brevispinis

2.446

0426

0 528

0.098

N.S.

S elongatus

0.519

0.070

3.393

1.253

PsJO.OI

S. proriger

30.402

9.612

0 198

0.031

Peo.05

S. babcocki

1-723

0,273

0 665

0.131

P«0.01

S crameri

0.509

0.070

3.233

1 008

PsO.OI

S. zacentrus

4.973

1.428

0.274

0.044

PsO.01

S. diploproa

0.623

0.102

1.157

0.292

PsO.OI

S entomelas

0.119

0028

6.289

1.004

N.S.

S. reedi

1.867

0.412

0-390

0.069

PsO.01

S. aleutianus

0.205

0-037

6-550

1.215

N.S.

S. helvomaculatus

0.301

0.048

4.424

1.078

PsO.01

then compared with the observed value using a
chi-square test. Values of k from trawls in all
depths ranged from 0.2 to 0.6 for the most abun-
dant species. The low values of k indicate that the
more abundant species are highly aggregated.
The estimates for k are close to the value of k
(0.27) that we estimated for S. marinus, an abun-
dant species of rockfish, from Georges Bank from
data in the paper by Taylor (1953).

We next divided the trawls into three depth
intervals: 91-145 m, 146-181 m, and >181 m.

Estimates of mean densities, k, and goodness of
fit tests by depth strata are presented in Table 7.

P{x.lWi) = {klimw^ + k)}" {mw-limw, + k)}^i n {(A- +7 - 1)/;] (7)

where m = mean value of jc, for element size of
unit size
k = parameter representing the degree
of aggregation (Note that k in this
section has a different meaning than
in the section on sampling schemes)
Wi = element size (distance towed).

Iterative maximum likelihood solutions (Bissell
1972) gave estimates of values of m, k, and their
standard errors relative to the average distance
towed. The values were converted to densities id)
with units of numbers per kilometer. Estimates of
d, k, and chi-square goodness of fit tests are given
in Table 6. These tests were made by calculating
the probability of a given number of fish occurring
in a trawl of a given length from the probability
density function given by Bissell (1972). This
probability was cumulated over all trawls and

The chi-square tests show that the data combined
over all depths are not well represented by the
negative binomial model. However, when the data
are divided up by depth strata, the agreement is
quite good. When the data from low density and
high density depth strata are combined, the result-
ing frequency distribution has too many zero
elements and too many high abundance elements.
This results in the high chi-square values from
trawls at all depths. In comparing the results in
Tables 6 and 7, it is obvious that depth stratifica-
tion is important. The differences between densi-
ties of species among depth strata were tested at
the 10% level of significance. Of 43 possible
comparisons, 27 (or 63%) were significantly
different. This can be tested against what would
have occurred randomly as a binomial proportion
(Hollander and Wolfe 1973). The proportion is
significantly different than random {z = 6.77,

668

LENARZ and ADAMS: SOME STATISTICAL CONSIDERATIONS OF TRAWL SURVEYS

Table 7. — Estimates of mean densities id) (in numbers per kilometer), k, standard errors, with chi-square
goodness of fit tests for trawl catches by depth strata in the Queen Charlotte survey.

Species

Depth strata (m)

Mean density

SE(cf)

k

SE(k)

Chi-square probability

Sebastes alutus

91-145

7.119

3.098

0,290

0080

N.S.

S alutus

146-181

90816

37.533

0,419

0 132

N.S.

S. alutus

>181

131.914

36.838

0,693

0 197

N.S.

S flavidus

91-145

1.160

0.253

1 660

0.817

N.S.

S flavidus

146-181

0,724

0,200

2037

1 030

N.S.

S. flavidus

>181

0051

0.003

4 900

1 231

(')

S pinniger

91-145

5,200

2.084

0,322

0.090

N.S.

S. pinniger

146-181

0.465

0.136

2.155

1.063

V)

S. pinniger

>181

0,018

0.017

{')

—

—

S paucispinis

91-145

1,051

0308

0870

0.323

N.S.

S paucispinis

146-181

0.262

0.088

2.494

0944

N.S.

S. paucispinis

>181

0,196

0.064

3.580

1 077

N.S.

S brevispinis

91-145

4,401

1.435

0.531

0.160

N.S.

S. brevispinis

146-181

3.027

0.993

0.652

0.232

N.S.

S. brevispinis

>181

1.145

0 354

0.679

0.231

P«0.05

S elongatus

91-145

0426

0.106

2.623

1.130

N.S.

S. elongatus

146-181

1.023

0.326

0 857

0353

N.S.

S elongatus

-181

0.193

0.062

4.535

1 334

N.S.

S- prong er

91-145

81.620

64.163

0.090

0.022

N.S.

S. proriger

146-181

4.701

1.901

0,440

0.146

N.S.

S. proriger

>181

0053

0.031

5.968

1.537

(')

S. babcocki

91-145

0,220

0.068

3.108

0.956

N.S.

S babcocki

146-181

1,426

0.446

1.274

0.627

N.S.

S. babcocki

>181

4.526

1.395

0 600

0.170

N.S.

S. crameri

91-145

0,017

0.016

{')

—

—

S. crameri

146-181

0,916

0.280

1.042

0.476

PssO.OI

S crameri

>181

0,673

0.146

2 549

1 168

N.S.

S zacentrus

91-145

0.118

0,047

4.040

1.098

N.S.

S. zacentrus

146-181

1.065

0,363

0.622

0239

N.S.

S zacentrus

>181

12.991

6 382

0229

0.061

N.S.

S diploproa

91-145

0.000

S diploproa

146-181

0.000

S. diploproa

>181

1 563

0,504

0.496

0.154

PsOOl

S. entomelas

91-145

0.034

0,024

4.442

1 087

V)

S^ entomelas

146-181

0202

0,073

3.306

1.105

P«0.05

S. entomelas

>181

0,142

0,053

4.451

1.241

N.S.

S. reedi

91-145

0,000

S. reedi

146-181

0.066

0.039

4.124

1 177

n

S reedi

>181

5.445

2.332

0.302

0 084

P^O.OI

S. aleutianus

91-145

0.000

.

S. aleutianus

146-181

0087

0,040

{')

—

—

S. aleutianus

>181

0.517

0,125

2.379

1.035

N.S.

S helvomaculatus

91-145

0.000

S. tielvomaculatus

146-181

0.022

0.022

3.277

0.908

N.S

S. helvomaculatus

>181

0.844

0227

1 098

0.457

PsO.01

Insufficient nonzero elements to perform chi-square test.
^Randomly distributed, fc -*^.

P<0.01). Although the rockfish species tended to
be aggregated, the group covers a wide range of
spatial patterns.

In sampling from a negative binomial distribu-
tion, the precision of a density estimate for any
given population depends both on the properties of
the population, its density id) and degree of
aggregation ik), and on the characteristics of
sampling, sample size (n) and the sample ele-
ment size (S) (tow length). By modifying the
sample characteristics, one can modify the preci-
sion of estimates.

Taylor (1953) showed in his Appendix E that
reducing sample element size ( length of the trawl )
was the optimal sampling strategy under the
condition that the total sampling area remained
constant. That is, if A = area of strata (which is
constant over all strata, i.e., Aj = A 2 = A3 ...),

a = area of the sampling element, and n = the
number of samples taken in each stratum, then
the value (a/A )n is fixed. Therefore, by reducing
the length of tow, there must be a corresponding
increase in the number of tows. However, in the
body of his paper, Taylor implies that it would be
advantageous to reduce sample element size even
with a constant number of samples. His argument
is based on the relationship between the mean and
variance for a negative binomial population ( Vnb^ )

Y

nb-i

m + m' Ik.

The argument is that as m is reduced by some
factor 176, then Vnbg would only be

V.

nbf

mlb + {mlbf Ik.

669

FISHERY BULLETIN: VOL. 78, NO. 3

While this argument is correct, it does not mean
that the estimate of total numbers of fish over the
entire strata is more precise with decreasing
sample element size. The effect of reducing sample
element size on the variance of the estimate of the
total number of fish in a stratum under the condi-
tion of a fixed sample size is considered below.
Using the definitions of A, a, n from above,
then A^ = total possible number of samples in a
stratum where the sample element size equals a
(i.e.,N — A/a). The variance of the total number of
fish in a stratum from n samples of the standard
element size ( V^^ ) is

V,

iVr

V,

nbi

or

V, =

a^n

m +

m'

(Cochran 1964). The variance (V^g^ ^^ the total
number of fish in a stratum for the sample ele-
ment size reduced by 1/6 is

V, =— Y

nbf

~A

2

n

mm

\

1^6^ \m , m^ A" T , m^l

The difference in variance between the different
sample element sizes is

relative increase =

1

i-f

The purpose of many surveys is to produce total
biomass estimates. These total biomass estimates
are made by expanding a density estimate (usual-
ly in the form of a catch per unit effort measure)
(Gunderson and Sample 1980) by the total area
(Cochran 1964). Since measurement of the area
involved can be made with relatively little error
compared with the density estimate, we ignore
error in area measurements in the following
discussion. The precision of an estimate will vary
inversely to its standard error. An index of preci-
sion (Pj) is:

Pr

dISE.

(9)

This index is the inverse of the coefficient of
variation and is used here because it varies
directly rather than inversely with precision. The
density of a population is equal to the mean of the
negative binomial distribution divided by the
sample element size (S):

d = mlS

(10)

Vd = v,^

V,

^- 6m + — 2- m+-—

a-n L k J a^n L kJ

where m — the mean of a number of tows of sam-
ple element size ( S ) ,
S = a constant sample element size with
no variance.

The variance of m is

2

an

[m(6-l)].

(8)

Although there is actually an increase in overall
variance by reducing sample element size with a
constant sample size, it will be relatively small
compared with the overall variance when m is
large in value and/or k small:

V,, = {m + m^lk)ln.

(11)

Therefore the variance of the density estimate is

Vj = {m + m^ lk)lnS''

(12)

and from Equation (10)

670

LENARZ and ADAMS: SOME STATISTICAL CONSIDERATIONS OF TRAWL SURVEYS

or

Vj = {dS+(dSflk)lnS'

V- = A + Jl
"^ nS nK

(13)
(14)

The standard error of the density is

SEa = (^^-)V2

\nS nK)

(15)
(16)

and the index of precision is

Pj = id)l{dlnS + d^- /nkf'
= illdnS + llnky'^\

(17)

From Equation (17), the precision of a density
estimate will decrease as the degree of aggrega-
tion increases (i.e., k -> 0). For the case when
k >> d, then the index approaches idnS)'' and
a unit increase in sample size and sample elemen_t
size are of equal importance. In the case of d
approximately equal to k then sample element
size has almost no effect on precision. When d >>
k, which is often the case for species that support
a commercial fishery, the index simplifies to

Pa

ink)

1/2

(18)

In these cases, only sample size will affect
precision.

More specific evaluation of sampling negative
binomial populations can be made by considering
the estimates of k for three rockfish species and
Equation (17). Since the limiting factor in these
surveys is usually ship time and not cost in a direct
sense, the evaluation is in terms of the most
efficient use of a ship day. The first two species
were the two target species in the Queen Charlotte
Sound survey: S. alutus, a high density, highly
aggregated species, and S. flavidus, a low density,
highly aggregated species. The third species was
S. aleutianus, a low density more randomly dis-
tributed species in Queen Charlotte Sound.

The sampling plan in Queen Charlotte Sound
was to perform trawls of 0.5 h on the bottom which
covered an average of 2.80 km. The average
number of trawls per working day was 4.3. The
average working day was 13 h long. Assuming 0.5
h on the bottom per trawl and 4.3 trawls/d, then
the average nontrawling time per haul is 2.05 h.
The minimum nontrawling time per haul was 1.07
h. The current sampling plan calls for an average
of about 5 trawls/d. Using the above times, four
possible alternative strategies are: 1) 3 trawls/d
with gear at depth for 2.1 h, 2) 4 trawls/d with gear
at depth for 1.2 h, 3) 5 trawls/d with gear at depth
for 0.5 h, or 4) 6 trawls/d with gear at depth for
0.3 h.

Using the four strategies, values for precision of
estimate of density were calculated for S. alutus,
S. flavidus, and S. aleutianus and are showm in
Figures 1, 2, and 3. The results of this analysis
follow directly from the result of the general
analysis. When the density to k ratio increases
above a critical level, precision is for all practical
purposes unaffected by changes in density. For the
more randomly distributed species (S. aleutianus)
the critical ratio occurs at higher density. For
more aggregated species (S. alutus, S. flavidus)
sample size (n) is not as effective in increasing
Pj in an absolute sense as in the less aggregated
species. Also, since sample size and sample ele-
ment size are inversely related and precision
increases with increased sample size except at
very low density, sample element size has little
effect on precision for these species except at very
low density Even for the less aggregated species,
sample element size has little effect on precision
except at low densities.

For a fixed amount of sampling effort, the
precision of an estimate from a negative binomial
population is a result_of the interaction of popula-
tion factors, density ( d ) and degree of aggregation
ik); and sampling factors, sample size in) and
sample element size (S). Analysis of the results of
the Queen Charlotte Sound survey shows that
rockfish species have a wide range of possible
combinations of population factors. The analysis
of sampling strategies showed that the same
sampling plan could have been used for all three
species with no significant loss in precision. This is
due to the highly aggregated nature of rockfish
species. However, for other less aggregated species,
such as flatfishes, there would have been a greater
difference among sampling schemes. This empha-
sizes the importance of picking target species on

671

FISHERY BULLETIN: VOL. 78, NO. 3

□

l/l
M
LJ
Ul

Ct:

Q.

LL

□

X

UJ

Q

Figure l. — Comparison of precision-density
curves of four different sampling strategies for
Sebastes alutus: 1) Three trawls/d with gear
at depth for 2.1 h, 2) four trawls/d with gear at
depth for 1.2 h, 3) five trawls/d with gear at
depth for 0.5 h, and 4) six trawls/d with gear at
depth for 0.3 h.

2.0

1 .8

1 .5

1 .3

1 .0

.a

.5 ,

0 .OJ

° SOnPLING STRQTEGY 1

I SanPLlNO STRQTEGV 2

° SPnPLINO STRQTEGV 3

^ SOHPLING STRQTEGY 4

-♦ — ♦ — •—

-• — ♦ — ♦—

-♦ — ♦ — o .

-e — e — e — e — b — b — e — o — g — e — & — e — e — e — e — b — e — o — e — e — e — o — < \

0.0 20.0 40.0 60.0 BO.O 100.0

DENSITY I NUMBERS/Kn . 1

120.0

5 .0

2:
□

I— I

LJ

a.

□

X

UJ
Q

Figure 2. — Comparison of precision-density
curves of four different sampling strategies for
Sebastes fJavidus: 1) Three trawls/d with gear
at depth for 2.1 h, 2) four trawls/d with gear at
depth for 1.2 h, 3) five trawls/d with gear at
depth for 0.5 h, and 4) six trawls/d with gear at
depth for 0,3 h.

4 .0

3.S

3 .0

2 .5

2 .0

1 .5

1 .0

0.0

° SQnPLING STRPTEGY 1

' SOMPLING STROTEGY 2

o SOnPLING STRQTEGY 3

^ SPHPLING STRQTEGY 4

0.0 20.0 40.0 60.0 BO.O 100.0

DENSITY I NUMBERS/KM . )

120.0

672

LENARZ and ADAMS: SOME STATISTICAL CONSIDERATIONS OF TRAWL SURVEYS

a

LO
1-4

l_)

LlI

a

Q.
Ll.

a

o

2:

B.O

7 .0

6.0

5 .0

4 .0

° St>nPLlNG sreoTEGv 1

' SOnPLlNO STROTEOV 2

0 SOriPLlNG STBOTEOV 3

^ SOnPLING STROTEGV 4

Figure 3. — Comparison of precision-density
curves of four different sampling strategies
for Sebastes aleutianus: ll Three trawls/d
with gear at depth for 2.1 h, 2) four trawls/d
with gear at depth for 1.2 h, 3) five trawls/d
with gear at depth for 0.5 h, and 4) six trawls/d
with gear at depth for 0.3 h.

20 .0

40.0 60 .0 BO .0 iOO .0

DENSITY ( NUnBEPS ^Kh . I

120.0

which to focus sampling strategies. For rockfish,
these are likely to be high density, highly aggre-
gated species. Generally, in sampling strategies
for these species, the effects of sample element size
would be unimportant. Increases in sample size
would be much more important in terms of in-
creased precision; however, increases in sample
size would have to be fairly large to make a
significant difference.

ACKNOWLEDGMENTS

We owe considerable thanks to Candis Cooper-
rider of the Tiburon Laboratory for writing com-
puter programs for the study. Reviews by N.
Abramson (Southwest Fisheries Center Tiburon
Laboratory), T. Foin (University of California at
Davis), D. Gunderson (University of Washington),
D. Kimura (Washington Department of Fisheries,
Seattle), J. Zweifel (Southwest Fisheries Center
La Jolla Laboratory), and two anonymous referees
resulted in a number of useful suggestions.

LITERATURE CITED

ABRAMSON, N. J.

1968. A probability sea survey plan for estimating rela-

tive abundance of ocean shrimp. Calif Fish Game 54:
257-269.

ANSCOMBE, F J.

1950. Sampling theory of the negative binomial and log-
arithmic series distributions. Biometrika 37:358-382.

BISSELL, A. F

1970. Analysis of data based on incident counts. The
Statistician 19:215-247.

1972. A negative binomial model with varying element
sizes. Biometrika 59:435-441.
BLISS, C. I., AND R. A. FISHER.

1953. Fitting the negative binomial distribution to bio-
logical data and note on the efficient fitting of the
negative binomial. Biometrics 9:176-200.

Clark, S. H.

1974. A study of variation in trawl data collected in
Everglades National Park, Florida. Trans. Am. Fish.
Soc. 103:777-785.

Cochran, W. G.

1964. Sampling techniques. 2d ed. Wiley, N.Y., 413 p.

Fiedler, p. C.

1978. The precision of simulated transect surveys of north-
em anchovy, Engraulis mordax, school groups. Fish.
Bull., U.S. 76:679-685.

Gunderson, D. R., and T. M. Sample.

1980. Distribution and abundance of rockfish off Wash-
ington, Oregon and California during 1977. Mar. Fish.
Rev 42(3-4):2-16.

Hairston, N. G., R. W. Hill, and U. Ritte.

1971. The interpretation of aggregation patterns. In G.P.
Patil, E. C. Pielou. and W E. Waters (editors), Statistical
ecology Vol. 1. Spatial patterns and statistical distribu-
tions, p. 337-353. Pa. State Univ. Press, Univ Park, Pa.

673

Hansen, M. H., W. N. Hurwitz, and W. G. Madow.

1953. Sample survey methods and theory. Vol. 1. Methods
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Hollander, M., and D. A. Wolfe.

1973. Nonparametric statistical methods. Wiley, N.Y.,
503 p.

LAMBOU, V w

1963. Application of distribution pattern of fishes in Lake
Bistineau to design of sampling programs. Prog. Fish-
Cult. 25:79-87.
LAUBSCHER, N. F.

1961. On stabilizing the binomial and negative binomial
variances. J. Am. Stat. Assoc. 56:143-150.
MOYLE, J. B., AND R. LOUND.

1960. Confidence limits associated with means and me-
dians of series of net catches. Trans. Am. Fish. Soc.
89:53-58.
Patil, G. P, and W. M. STITELER.

1974. Concepts of aggregation and their quantification:
a critical review with some results and applications. Res.
Popul. Ecol. 15:238-254.

PlELOU, E. C.

1969. An introduction to mathematical ecology. Wiley-
Interscience, N.Y, 286 p.

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POOLE, R. W.

1974. An introduction to quantitative ecology. McGraw-
Hill, San Francisco, 532 p.
ROESSLER, M.

1965. An analysis of the variability of fish populations
taken by otter trawl in Biscayne Bay, Florida. Trans.
Am. Fish. Soc. 94:311-318.

SUKHATME, P v., AND B. V. SUKHATME.

1970. Sampling theory of surveys with applications. 2d
ed. Iowa State Univ. Press, Ames, 452 p.
TAFT, B. a.

1960. A statistical study of the estimation of abundance
of sardine (Sardinops caerulea) eggs. Limnol. Oceanogr.
5:245-264.

Taylor, C.C.

1953. Nature of variability in trawl catches. U.S. Fish
Wildl. Serv, Fish. Bull. 54:145-166.

Venrick, E. L.

1978. Systematic sampling in a planktonic ecosystem.
Fish. Bull., U.S. 76:617-627.
WATERS, W. E.

1959. A quantitative measure of aggregation in insects.
J. Econ. Entomol. 52:1180-1184.

674

EFFECTS OF COPPER ON EARLY LIFE HISTORY STAGES OF
NORTHERN ANCHOVY, ENGRAVLIS MORDAX

D. W. Rice, Jr.,' F. L. Harrison,* and A. Jearld, Jr.^

ABSTRACT

The sensitivity to copper of embryonic and larval stages of the Northern anchovy, Engraulis mordax,
was determined using a flow-through bioassay system. Northern anchovy embryos were exposed
continuously from 8 to 10 hours after fertilization until hatching, and the larvae were exposed within 12
hours after hatching until yolk-sac absorption. During the testing both total copper concentrations and
the percent copper in labile forms were determined. From the cumulative mortality versus measured
copper exposure data, a series of median lethal concentrations (LCso* were determined. These LC50
values were used to construct comparative toxicity curves.

The northern anchovy life stage most sensitive to copper was the embryonic stage. For northern
anchovy embryos the 12-hour LC50 was 200 /xg Cu/1, and the estimated incipient lethal concentrations
(ILCjq) was 190 /u,g Cu/l; a sensitive period of embryonic development was noted prior to closure of the
blastopore. The 12 hours, 24 hours, and ILC^^ for northern anchovy larvae were 460, 400, and 370 /xg
Cul.

Copper is one of the wastes commonly discharged
into coastal waters that has been shown to be toxic
to marine fishes (Becker and Thatcher 1973; Lewis
and Whitfield"^). Increased copper concentrations
in coastal marine waters have resulted from the
release of municipal wastewater (Schafer^), power
plant effluents (Young et al.^), and marine an-
tifouling paints (Young and Alexander*^). In pol-
luted waters, concentrations have been recorded
as high as 16,800 )ng Cu/1 in municipal waste ef-
fluents ( Schafer footnote 4 ) and 1,800 fxg Cu/1 dur-
ing start up of a power plant (Martin et al. 1977).
One important factor in the toxic effect of copper
on marine fishes is the life history stage when the
exposure occurs. Few studies have examined the

'Environmental Sciences Division, Lawrence Livermore
Laboratory, University of California, Livermore, CA 94550.

^Northeast Fisheries Center Woods Hole Laboratory, National
Marine Fisheries Service, NOAA, Woods Hole, MA 02543.

3Lewis, A. G., and EH. Whitfield. 1974. The biological im-
portance of copper in the sea, a literature review. International
Copper Research Association, Proj. No. 223, Final Rep., 132 p.

■'Schafer, H. A. 1977. Characteristics of municipal waste-
water discharges, 1976. Coastal Water Research Project, An-
nual Report, 1977, 253 p. Southern California Coastal Water
Research Project, 1500 East Imperial Highway, El Segundo, CA
90245.

5Young,D.R.,Tsu-Kai Jan, and M.D.Moore. 1977. Metals
in power plant cooling water discharges. Coastal Water Re-
search Project, Annual Report, 1977, 253 p. Southern California
Coastal Water Research Project, 1500 East Imperial Highway, El
Segundo, CA 90245.

^Young,D.R.. and G.V.Alexander 1977. Metals in mussels
from harbors and outfall areas. Coastal Water Research Proj-
ect, Annual Report, 1977, 253 p. Southern California Coastal
Water Research Project, 1500 East Imperial Highway, El
Segundo, CA 90245.

comparative sensitivities of the major life stages of
marine fishes: embryo, larva, and adult. The spot,
Leiostomus xanthurus, was found to be more sensi-
tive to copper in the embryonic stage than in the
larval stage (Engel et al. 1976). The incipient le-
thal concentration (ILC50 — that concentration
that kills 507c of a population during an exposure
sufficiently long that acute lethal action has
ceased [Sprague 1969]) for Pacific herring, Clupea
harengus pallasi , embryos exposed to copper was
found to be approximately 30 times lower than the
ILC50 for Pacific herring larvae ( Rice and Harri-
son 1978) and 7 times lower than the ILC50 for
Pacific herring adults (Harrison and Rice'^).
Natural mortalities that occur during the early
life stages have been suggested to be a major factor
in reducing the size of a given year class of fish
(May 1974; Cushing 1975; Vaughan and Saila
1976). Pollutants that have an impact on the sur-
vival of fish embryos or larvae might further re-
duce the size of a given year class offish.

In addition to the life stage, the chemical form of
copper to which fishes are exposed may play an
important role in the toxic response (Lee 1973;
Neff and Anderson 1977; Chapman and
McCrady^). Copper in seawater can exist in many

Manuscript accepted February 1980.
FISHERY BULLETIN; VOL. 78, NO. 3, 1980.

■'Harrison, F L., and D. W Rice, Jr. In prep. Toxic response
and copper body burdens of adult Pacific herring, Clupea haren-
gus pallasi, and northern anchovy, Engraulis mordax, exposed to
increased copper concentrations.

«Chapman,G.A.,andJ.K.McCrady. 1977. Copper toxicity:
a question of form. Recent advances in fish toxicology, a sym-

675

FISHERY BULLETIN: VOL. 78, NO. 3

forms. We will use the terminology proposed by
Batley and Florence (1976*. According to these
authors, labile copper, as defined by experimental
conditions, includes ionic, as well as some dissoci-
able, complexed forms; bound copper is that frac-
tion of the total copper which is not labile and
includes soluble copper-organic complexes, copper
bound to high molecular weight organic mate-
rials, and copper occluded in or adsorbed onto
highly dispersed colloids. Although current cop-
per emission standards are defined in terms of the
total copper concentration in the water i Anony-
mous 1972. 1976 1 complexation of copper has been
shown to reduce its toxicity to marine organisms
(Lewis et al. 1972, 1973: Davey et al. 1973: Sunda
and Guillard 1976: Harrison et al.^V Ionic copper
has been suggested as the form most toxic to
freshwater fishes iPagenkopf et al. 1974*. During
our testing of the early life stages of the northern
ancho\y. we determined both total copper concen-
trations and the percent copper in the labile forms.
Northern anchovy. Engraulis mordax, is a
pelagic, filter-feeding fish that spawns in upwell-
ing waters along the Pacific coast of the United
States and Mexico i Ahlstrom 1960 1. During recent
years, the northern ancho\y catch has been the
third largest commercial catch on the Pacific coast
(McAllister 1976: Pinkas 1977 '. Having conducted
earlier tests on the sensitivity to copper of Pacific
herring during its early life stages i Rice and Har-
rison 1978), we set two objectives for the present
study: to conduct similar tests on the northern
ancho\y and to compare the sensitivities of these
two species offish during their early life histories.
We continuously exposed northern anchoNy em-
bryos and larvae to copper over a range of concen-
trations and then constructed comparative toxic-
ity curves.

METHODS

Northern anchovy embryos were collected in
San Francisco Bay. Calif., between the Tiburon
Peninsula and Angel Island. Collections and tests
were carried out over a period of 2 \t. Collections
were made with a 0.5 m. 505 iim mesh, nylon
plankton net. towed for 2 min just below the sur-

posium. U.S. En\-iron. Prot. Agencv EcoL Res. Ser. ER^ 600 3-
77-085. July 1977. 204 p.

^Harrison. F. L., J. P. Knezovich. and J. S. Tucker.
1979. Sensiti\'ity of Crassostiva gigas embryos to different
chemical forms of copi)er. Univ. Calif.. Lawrence Livermore
Lab., LiN-ermore. UCRL 52725; XLTIEG CR-1088.

face of the water. Collections from each tow were
placed into a plastic bag half full of seawater: the
bag was inflated with air and then held in an
insulated ice chest containing seawater from the
collection site. Water temperature at the collection
site was between 17" and 18.5' C: upon arrival at
La\\Tence Livermore Laboratory the temperature
of the water in the ice chest was always <19" C.

The water for the bioassay system was obtained
from the University of California Marine Station
at Bodega Bay. Calif. This water is pumped from
the ocean off the open coast in an area that re-
ceives little anthropogenic input. The water con-
tains low levels of trace metals, dissolved organics,
and particulate material. The collected seawater
was stored in a 40.000 1 underground tank and
passed through a filter with 1.0 /xm openings prior
to experimental use.

Two embr\-o tests were conducted during 1976
(test I: 7 July 1976: test II: 23 July 1976' and one
embryo test during 1977 (test III: 27 June 1977).
All larval tests were conducted during 1977 (test I:
6 June 1977: test II: 13 June 1977).

All transfers of embryos or lar\'ae were carried
out with a large-bore, polished glass pipette. Dur-
ing embryo tests, healthy embryos estimated to be
8-10 h old ( stages IV- V, Ahlstrom 1943 ) were placed
either directly into exposure chambers containing
seawater with known concentrations of copper or
allowed to hatch in control seawater. Larvae used
during larvae tests hatched within the 12-h period
preceding the test: hatched larvae were placed
directly into exposure chambers containing sea-
water with known concentrations of copper. Ap-
proximately 50 embryos or 30 larvae were used in
each exposure chamber.

Anchovy embryos and larvae were exposed to
copper in 500 ml clear glass, flow-through, expo-
sure chambers (Figure 1) which, in turn, were im-
mersed in a water bath (mean temperature:
16.8'' =1.0" C'. Seawater containing a known con-
centration of copper, as copper chloride, was
pumped into each chamber from a 19 1 plastic jug
at a rate of 5 ml min. About 5 h were required to
replace 95'~f of the water in the exposure chamber:
the mixture of seawater and copper in the 19 1
plastic jugs was prepared daily.

The height of the water in the exposure cham-
bers was maintained by a constant-level, outflow
siphon. The mouth of the siphon, located at the
base of the exposure chamber, was covered with
nylon netting 1 265 ^tm pore size^ to prevent the loss

676

RICE ET AL EFFECTS OF COPPER OX NORTHERN ANCHOVY
-Air

Premixed
seawater V'
and copper ^ >

-Clear plastic cover

Glass

exposure
chamber
(500 ml)

Water bath

Figure l. — Diagram of the exposure chamber and flow-through
bioassay s>-stem used to erpwse northern andio\">' embrj-os and
larvae to copper

of organisms from the chamber. The bottom outlet
from each exposure chamber was fitted with a
valve that could be closed to allow removal of the
chamber from the water bath. This was important
because during each observation the exposure
chambers were removed and illuminated from the
side. In this manner both live and dead organism^
could be examined. Observations were made ever>
2-4 h during the copper exposures. During embryo
exposures, a gentle stream of bubbles was deliv-
ered to the bottom of the exposure chamber: dur-
ing larval exposures, no aeration was used. Over-
head illumination was provided by the fluorescent
lighting in the laboratory and followed the regular
ambient photoperiod. The number of embryos or
larvae exposed during each test is giN^en in Tables 1
and 2.

Exposures continued until li all animals died,
or 2 1 in the case of the embryos, until hatching was
complete, or 3) in the case of the larvae, until the

Table l. — Samples mortality data used to calculate LC50 values for northern anchovy embr>-os exposed to different copp>er
concentrations. Chi-square tests used the null h\-pothesis that the relationship berw-een dose and response followed the logit model.

Measured exposure concentration (/ig

Cul =

SDi

^LCso

Chi- square

Exposure

92

116

171

177

190

197

242

272

285

531

55J

589

ti^T>e !^'

Corrtrol'

= 8

= 14

=31

= 30

=12

=41

= 46

=22

= 19

= 66

=39

=28

(M-gCuH

value^

df

ortion dead*-

2

0-00

0.04

0.02

0.00

0.02

0.03

0.16

0.21

0.03

0.27

0.77

0.93

0.85

409=22

29.14"

11

4

.00

.04

.03

.01

.14

.24

.32

.44

.29

.61

.96

.93

.94

292=16

38.82—

11

6

.00

.14

.03

.08

.14

.47

.44

.63

.51

.86

.98

.96

.98

235=10

40.67—

11

8

.00

.21

.09

.12

.25

.59

.49

.72

.64

.88

.98

1.00

1.00

213= 8

29.24"

11

12

.00

.25

.09

.15

.27

.62

.62

.76

.75

.95

1.00

199= 8

40.06"-

9

18

.00

.27

.09

.17

.31

.67

.65

.80

.78

.98

1.00

193= 7

40.65—

9

25

.00

-27

.09

17

38

.67

.69

.84

.85

.98

1.00

186= 6

40.49—

9

32

.00

-27

09

-~

35

e-

70

84

.88

.96

1.00

185= 9

41.88—

9

No. organisms

exposed

260

28

90

94

124

34

161

•12

66

96

126

29

104

■ Labie copper = 1.3 (SD = 0.1) ;ig Cu/I.
' =95°o confidence Bmrt-
2"P«0.01: — P«0.001.
'Corrected for control mortaSty.

Table 2. — Samples mortality data used to calculate LC50 values for northern anchoN-y larvae exposed to
different copper concentrations. Chi-square tests used the null hj-pothesis that the relationship between
dose and response followed the logit model.

Exix3Su-e

Measured

exposure concentration (^g Cu

1 = SD)

^LCs:

Ch.- square

ii"-.e "

Control'

277=6

289=29

427 = -

531=42

'724

(MgCui)

vaiue-

df

_

4

0-00

0.14

0.02 0.42 0.49

0.76

523=58

7J20

4

8

.00

.15

.18

.49

.53

-84

485=54

4.02

4

12

.00

.16

.16

.50

.65

.87

457=46

2.61

4

20

.00

.07

.30

.59

.79

1-00

412=34

7.35

4

26

.00

.06

.30

.71

.85

1.00

391 =31

7.61

4

32

.00

.06

.41

.75

.87

1.00

375=31

11-15-

4

40

.00

.11

.41

.73

.87

1.00

374=32

8-86

4

46

.00

.01

.51

.79

.87

1.00

372=30

27-28—

4

No. organisms

exposed

74

71

33

Ci

60

26

" labie copper = 1.3 (SD = 0.1) /ig Cu I.
^Single measixemerrt
^=95°-o confidence Umit
*'PsO-05:— P«0-001-
^Corrected for control mortaSty.

677

FISHERY BULLETIN: VOL. 78, NO. 3

yolk sac was absorbed. The criterion for embryo
mortality was the appearance of opacity of the
embryo, and the criterion for larval mortality was
failure to respond to a prod with a polished glass
rod. Cumulative mortality with time, percentage
hatching, and the stage of development at mortal-
ity were taken to be indices of the toxic effect of
copper.

Total copper concentrations were measured
every other day during all tests. Labile copper
concentrations were measured every other day
during embryonic test III and larval tests I and II.
Total copper in samples containing >200 ixg Cu/1
was determined by direct aspiration of seawater
into the flame of a Model 303 Perkin Elmeri"
atomic absorption spectrophotometer (AAS) with
a deuterium background corrector; total copper in
samples containing <200 and >10 ^ig Cu/1 was
determined by direct injection of a sample aliquot
into an HGA 2100 model graphite furnace after 1:1
dilution of the sample with ultrapure 2 N HNO3.
Labile copper, defined operationally as that frac-
tion passing through a 0.45 ^tm filter and retained
by NHj-Chelex resin, was determined by the
method of Riley and Taylor (1968). Eluants from
the columns were analyzed directly in the flame or
in the graphite furnace of the AAS.

The mean total copper concentrations measured
during each test are given in Tables 1 and 2. The
percentage of the total copper in the labile form for
all concentrations averaged 96% (SD = ±2.60).
The mean pH of the exposure seawater for all tests
was 8.06 (SD = ±0.05).

The primary measure of toxicity for this study
was the copper concentration resulting in 50%
mortality over a given time (median lethal con-
centration, LCgp). This toxicity measure was de-
termined by performing weighted least squares
estimates and maximum likelihood estimates for
the parameters cc and f3 in the logit model:

Pix)

g^ + fix

1 + e X + /iv

The linear transform of the logistic function is
logit P = lnP(x)/l-P(x) = oc + /3x; thus if logit P
is plotted against x, the points should fall on a
straight line with cc as the intercept and /3 as the
slope (Berkson 1953). The weighted least squares

estimates for « and (i were found first and then
used as the initial estimates for the maximum
likelihood estimates (Koshiver and Moore 1979).

In our calculation of LC5o,P(x) is the proportion
responding at dose x. Our method followed that
outlined by the American Public Health Associa-
tion (1976) except that the logit analysis was used
in place of a probit analysis. For each observation
time, an estimated LC50 value was determined.
The series of LC50 values obtained were used to
construct a toxicity curve that was used to esti-
mate the incipient lethal concentration (lethal
threshold concentration, ILCg^; Sprague 1969).

RESULTS

Northern anchovy embryos continuously ex-
posed to copper showed high mortality during the
first 8-10 h of exposure (Table 1). After 10 h, the
mortality rate was relatively constant until hatch-
ing (Figures 2-4). The embryos took two different
forms at mortality. The first form (Type I) was
observed predominantly during the initial 8-10 h
of exposure and accounted for varying proportions
of the total mortality, depending on the copper
exposure concentration (Table 3). These embryos
appeared to have had epiboly disrupted; the yolk
was naked and a deformed opaque mass of proto-
plasm was found at the animal pole. The second
form (Type II) appeared similar to normally devel-
oping embryos (the embryo encircling the yolk
sac), except for an opacity of the embryo. In em-

100 -

10

20 30 40

Time — h

50

'"Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA, or the University of
California.

Figure 2. — Percentage cumulative mortality of northern an-
chovy embryos continuously exposed to copper during test I:
numbers next to curves are the exposure concentrations in ju.g
Cu/1.

678

RICE ET AL.: EFFECTS OF COPPER ON NORTHERN ANCHOVY

I

>

o

E

>

3
E

o

Figure 3. — Percentage cumulative mortality of northern an-
chovy embryos continuously exposed to copper during test II:
numbers next to curves are the exposure concentrations in /xg
Cu/1.

100

^ 80

I

>

^ 60

o
E

>

£
o

40

20

AJL

r

1

1
"■^

272

-■

- IbGA

m^M''^

-

/

A

_^

-

- /

190

\L

92

D

V

^ o-

T^

Control

-O

10

20

Time

30

h

40

50

Figure 4. — Percentage cumulative mortality of northern an-
chovy embryos continuously exposed to copper during test III:
numbers next to curves are the exposure concentrations in /xg
Cu/1.

Table 3. — Types of mortality and the percentage hatching of
northern anchovy embryos exposed to different concentrations of
copper.

Mean Cu
tratlon

concen-

(mq/I)

Tests
pooled

Embryos showing type
of mortality (%)

Hatching
(%)

Type 1

' Type l|2

Control

1, III

3

4

93

92

III

4

32

64

177

II

34

20

46

194

II. Ill

63

17

20

257

II. Ill

60

35

5

548

II. Ill

96

2

2

bryos with either type of mortality the chorion was
clear at the time the embryos were removed from
the exposure chambers. However, during prelimi-
nary testing, we noted that the chorion became
opaque when dead embryos were allowed to re-
main in copper concentrations as low as 100 /u.g
Cu/1 for a period of time. Embryo mortalities of
both types were found at the bottom of the expo-
sure chambers whereas normal embryos were
found at or near the surface of the water, except
just before hatching when they tended to sink. The
estimated mean hatching time from the start of
copper exposure was 32, 33, and 37 h for embryo
tests I, II, and III, indicating that in each test the
embryos were exposed during similar devel-
opmental periods. Hatching success was high for
controls and decreased with increases in copper
exposure concentration.

Larval control mortalities were high, but fol-
lowed the general pattern for larvae not fed during
yolk-sac absorption (O'Connell and Raymond
1970; Lasker et al. 1970). Northern anchovy larvae
continuously exposed to concentrations <200 /xg
Cu/1 consistently showed better survival than did
the controls (Table 3) (Figures 5, 6). Though he
offered no explanation, Benoit (1975) found
bluegill, Lepomis macrochirus, larval survival
greater at 12 /xg Cu/1 than in the controls. It is
possible that low levels of copper exposure in-
creased survival of both the northern anchovy and
bluegill larvae by inhibiting harmful microbial
populations. The period of yolk absorption was
estimated to be between 24 and 30 h from the start

100

o

E

OJ

>

E

3

u

'Epiboly disrupted, the yolk naked and a deformed opaque mass of proto-
plasm at the animal pole.
^Dead after epiboly, embryo appears normally developed.

100

Figure 5. — Percentage cumulative mortality of northern an-
chovy larvae continuously exposed to copper during test I: num-
bers next to curves are the exposure concentrations in fig Cu/1.

679

FISHERY BULLETIN: VOL. 78, NO. 3

100

I

o
E

E
o

20

40 60

Time — h

100

Figure 6. — Percentage cumulative mortality of northern an-
chovy larvae continuously exposed to copper during test II: num-
bers next to curves are the exposure concentrations in /ng Cu/1.

of larval exposure. During exposures >200 fxg
Cu/1, synergism between copper toxicity and star-
vation may have played a role in the mortality and
the shape of the 277 and 289 /xg Cu/1 mortality
curves (Figures 5, 6) may show this effect.

No obvious abnormalities were noted in the dead
larvae. Before death, larvae tended to sink to the
bottom of the exposure chambers and often exhib-
ited head shaking movements and whip
movements in which head and tail met.

Examples of the cumulative mortality data used
to calculate LCg^ values and to generate the toxic-

ity curves (Figure 7) are given in Tables 1 and 3.
Chi-square values for embryo cumulative mortal-
ity curves at every observation time were signifi-
cant. This variation from the logit model may pos-
sibly be due to changes in copper sensitivity as the
embryos developed. Chi-square values for larval
cumulative mortality curves at different observa-
tion times indicate a better fit to the logit model.
The embryonic and larval toxicity curves reflect
several developmental changes in sensitivity
(Figure 7). A slight increase in copper sensitivity
can be seen in the embryos during hatching. When
we estimated the embryo ILC^q, we considered
only mortalities before hatching. For embryos, the
estimated ILC50 was found to be 190 /xg Cu/1, and
was reached approximately 24 h after the start, of
copper exposure. The sudden increase in mortality
of the larvae at about 40 h probably was the result
of starvation. Only mortalities before this time
were considered in the larval estimated I LC^^ . The
ILC50 for the northern anchovy larvae was found
to be higher than for embryos: 370 /xg Cu/1 copper,
and was reached about 32 h after the start of
copper exposure. The estimated 24-h LC50 was 398
/xgCu/1.

DISCUSSION

We found the embryonic stage of the northern
anchovy to be more sensitive to copper than the
larval stage. This is in keeping with the majority

200

100

>

1-1

"to

50

■t-'

^

0

E

^

0

Ln

0

10

■M

O)

E

B

i-

J J Period of
J_ f yolk sac
absorption

1
100

Figure 7.— Toxicity curves fornothem
anchovy embryos and larvae con-
tinuously exposed to copper.

200

500

800

jug Cu/C

680

RICE ET AL.: EFFECTS OF COPPER ON NORTHERN ANCHOVY

of previous studies examining the sensitivity to
copper of marine fishes' early life history stages
(Engleet al. 1976; Blaxter 1977; Rice and Harrison
1978). In contrast, studies examining the copper
sensitivity of various life stages of freshwater
fishes revealed that the larval stages are the most
sensitive to copper ( Hazel and Meith 1970; McKim
and Benoit 1971; Gardner and LaRoche 1973; Be-
noit 1975; McKim et al. 1978; 0'Rear>M. This dif-
ference in comparative sensitivity between em-
bryos and larvae of freshwater and marine fishes
suggests that caution should be exercised in apply-
ing the extensive results of toxicity tests on fresh-
water fishes to marine fishes.

The adult northern anchovy and Pacific herring
are similar in form and in behavior, but their re-
productive strategies are quite different. The
northern anchovy spawns pelagic eggs into
offshore waters; the 1.0 x 0.5 mm diameter egg is
covered by an elliptical, transparent chorion.
Northern anchovy eggs hatch in about 48 h at 17°
or 18° C into fragile, unpigmented larvae, 2.5-3.0
mm long (Ahlstrom 1956). The Pacific herring
spawns demersal, adhesive eggs on shallow inter-
tidal substrates; the 1.3-1.6 mm diameter egg is
covered by a thick, three-layered, chorion (Blaxter
and Holliday 1963). Herring eggs hatch in 7-9 d at
14° C into pigmented larvae 5.0-6.0 mm long ( Al-
derdice and Velsen 1971). Comparisons of the sen-
sitivities of the early life stages of these two fish
may prove useful for predicting the impact of cop-
per on broad groups of fishes. For comparisons
between the copper sensitivity of northern an-
chovy and Pacific herring embryos and larvae, the
data on herring sensitivity are taken from our
earlier study (Rice and Harrison 1978).

It might be expected that the fragile northern
anchovy embryo would be more sensitive to copper
than the larger, tougher Pacific herring embryo; in
fact, however, the opposite appears to be the case.
The ILC50 for northern anchovy embryos was ap-
proximately six times higher than that for Pacific
herring embryos. The results of Engel and Sunda
(1979) showed a similar pattern; relatively tough
benthic spawned eggs of the silverside, Menidia
menidia, were found to be more sensitive to copper
than the more fragile pelagic eggs of the spot.

The differences in sensitivity seen in the two
embryos may be the result of differences in the
chorionic structure and the developmental period
during copper exposure. The chorion of Atlantic
herring, C. h. harengus (Rosenthal and Sperling
1974), and another demersal adhesive egg, the
Baltic garpike, Belone belone (Dethlefsen et al.
1975), have been shown to concentrate cadmium.
The chorion of the Pacific herring may be the site
of mechanisms to accumulate metals, mechanisms
that may be reduced or lacking in the northern
anchovy. Changes in sensitivity during develop-
ment were seen in both the northern anchovy and
Pacific herring embryos. The high percentage of
northern anchovy mortalities during epiboly indi-
cates that this period of development might be
more sensitive to copper than the later devel-
opmental periods. Increased copper sensitivity
during this period also was found for winter floun-
der, Pseudopleuronectes americanus, (Cardin^^).
The sensitive period for the Pacific herring embryo
appeared to be about 96 h after fertilization, well
beyond epiboly.

Differences in sensitivity were also seen be-
tween the two larvae. The fragile northern an-
chovy larvae were about three times more sensi-
tive to copper than the Pacific herring larvae.

Both northern anchovy and Pacific herring lar-
vae displayed spasms before death at the higher
copper concentrations to which they were exposed.
Such spasms during copper poisoning have been
suggested to be similar to those seen in Wilson's
Disease (Baker 1969).

ACKNOWLEDGMENTS

The authors thank Revelle Davis, John Dawson,
and Rose Carrillo for their assistance in the collec-
tion, handling, and observation of the test or-
ganisms.

This work was supported by the U.S. Nuclear
Regulatory Commission under a Memorandum of
Understanding with the U.S. Department of
Energy.

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O'CONNELL, C. P, AND L. R RAYMOND.

1970. The effect of food density on survival and growt;h of
early post yolk-sac larvae on the northern anchovy {En-
graulis mordax Girard) in the laboratory. J. Exp. Mar
Biol. Ecol. 5:187-197.
PAGENKOPF, G. K., R. C. RUSSO, AND R. V. THURSTON.

1974. Effect of complexation on toxicity of copper to fishes.
J. Fish. Res. Board Can. 31:462-465.
PINKAS, L.

1977. California marine fish landings for 1975. Calif Dep.
Fish Game, Fish Bull. 168, 55 p.

RICE, D. W, Jr., AND F. L. Harrison.

1978. Copper sensitivity of Pacific herring, Clupea haren-

682

RICE ET AL.: EFFECTS OF COPPER ON NORTHERN ANCHOVY

gus pallasi. during its early life history. Fish. Bull., U.S.
76:347-356.

Riley, J. R, and D. Taylor.

1968. Chelating resins for the concentration of trace
elements from sea water and their analytical use in con-
junction with atomic absorption spectrophotometry. Anal.
Chim. Acta 40:479-485.

Rosenthal, H., and K.-R. Sperling.

1974. Effects of cadmium on development and survival of
herring eggs. In J. H. S. Blaxter (editor). The early life
history offish, p. 383-396. Springer- Verlag, N.Y.

Spr.acue, J. B.

1969. Measurement of pollutant toxicity to fish. I. Bioassay
methods for acute toxicity. Water Res. 3:793-821.

Sunda, W., and R. R. L. Guili.ard.

1976. The relationship between cupric ion activity and the
toxicity of copper to phytoplankton. J. Mar Res. 34:511-
529.

Vaughan, D. S., and S. B. Saila.

1976. A method for determining mortality rates using the
Leslie matrix. Trans. Am. Fish. Soc. 105:380-383.

683

CHANGES IN BODY MEASUREMENTS OF LARVAL

NORTHERN ANCHOVY, ENGRAULIS MORDAX, AND OTHER FISHES

DUE TO HANDLING AND PRESERVATION

Gail H. Theilacker*

ABSTRACT

The relation between northern anchovy length and body parts was compared for live and laboratory-
preserved larvae as well as larvae treated in a net to simulate field collection conditions. Larvae were
damaged by net abrasion, and those netted before preservation shrank more than those that were
laboratory preserved (that is, larvae pipetted directly into preservative). Shrinkage of net-treated
individuals decreased with age and increased with handling time, but shrinkage of laboratory-
preserved larvae was constant for the size class studied. The results show that morphological differ-
ences reported for laboratorv'-reared and sea-caught larvae of the same length may result from the
method of handling larvae prior to preservation.

To describe life stages of larval fish, field and
laboratory studies rely on length measurements of
preserved sea-collected and preserved labora-
tory-collected larvae. Sea-collected larvae incur
mechanical damage, abrasion from the collecting
net and from other plankters, while the net is
being towed and washed down (Ahlstrom 1976).
When damaged, delicate larvae shrink. This ini-
tial shrinkage usually occurs before death, and
this shrinkage is compounded by preservative
shrinkage (Blaxter 1971). Conversely, laboratory
handling of larvae prior to preservation is less
damaging than net abrasion. In the laboratory,
individual larvae are usually transferred by
pipette or beaker to preservative, and they die and
shrink in the preservative.

Laboratory-reared fish larvae differ morpholog-
ically from sea-caught larvae. Body depth of wild
herring, Clupea harengus, larvae was smaller
than that of starved laboratory-reared larvae of
the same preserved length (Blaxter 1971). Ryland
(1966) observed that sea-sampled larval plaice,
Pleuronectes platessa, were smaller than labora-
tory larvae at a comparable stage and suggested
that a factor for shrinkage was needed to equate
field with laboratory measurements. I have
noticed a similar discrepancy in preserved length
of sea-collected yolk-sac larvae and laboratory-
hatched and preserved yolk-sac larvae of the jack
mackerel, Trachurus symmetricus (Theilacker

'Southwest Fisheries Center La Jolla Laboratory, National
Marine Fisheries Service, NOAA, P.O. Box 271, La Jolla, CA
92038.

Manuscript accepted January 1980.
FISHERY BULLETIN: VOL' 78. NO. .3. 1980.

unpubl. data). These morphological differences
may be the result of the method of handling
(laboratory capture or net capture) prior to pres-
ervation. Since it is necessary to compare animals
at the same developmental stage to relate labora-
tory larval fish studies to the field, there is a need to
intercalibrate field (preserved) and laboratory
(live and preserved) larval fish measurements.

METHODS

Adult northern anchovy, Engraulis mordax,
maintained in the Southwest Fisheries Center's
aquarium, were spawned by hormone injection
(Leong 1971). I reared the anchovy larvae at 15.5°
C on cultured food organisms {Gymnodinium
splendens; rotifers, Brachionus plicatilis; and
copepods, Tisbe furcata) in 100 1 tanks using
methods described by Lasker et al. (1970),
Theilacker and McMaster (1971), and Hunter
(1976).

I considered several factors that could affect
shrinkage of larval fish: 1) size, 2) type of fixative,
3) treatment of larvae before fixation (net or
laboratory capture), and 4) duration of net reten-
tion. Larval fish measurements fit into four treat-
ment categories (Figure 1): 1) live, 2) laboratory
pipetted and preserved, 3) net treated, and 4)
preserved after net treatment (equivalent to
"field-collected" larvae). Five body measurements
(in millimeters) were taken: standard length (SL),
tip of upper jaw to perpendicular at end of
notochord; head length, tip of upper jaw to clei-
thrum; body depth at the pectoral (not measured

685

FISHERY BULLETIN; VOL, 78, NO. 3

Live
SL, HL, BD, ED

Laboratory
Preserved
Formalin
Alcohol

Net Treatment

minutes:

_^ Preserved

Formalin
Alcohol

("Field Collected'

Figure L — Experimental design. Four measurements of larval
northern anchovy were taken to estimate shrinkage during han-
dling treatments: standard length, SL; head length, HL; body
depth at the anus. BD; and eye diameter, ED.

for northern anchovy ); body depth at the anus; and
eye diameter. I kept track of individual larvae
during all treatments and determined body part
shrinkage on an individual basis. The same larva
could be measured as many as six times; e.g., a
"field-collected" larva was measured live, after
four time intervals in the net, and again after
preservation. However, not all net-treated larvae
were measured for four time intervals. I used sev-
eral preservatives: Bouin's fixative, usually used
for histological studies; 57^ buffered Formalin-
(2.2% formaldehyde), the standard ichthyoplank-
ton-survey preservative (Ahlstrom 1976; Smith
and Richardson 1977); and SOVc ethyl alcohol, pre-
servative for otoliths (Methot and Kramer 1979).
In treatments (2) and (4), larvae were kept in pre-
servative for 4-5 wk before remeasuring.

As an example of laboratory handling proce-
dures, I have included results from ongoing
studies on morphology of jack mackerel and
Pacific barracuda, Sphyraeria argentea, larvae.
Eggs of jack mackerel and Pacific barracuda were
collected 30-50 km off the coast of southern
California in June and July 1977, and rearing
procedures were the same as for northern anchovy.
Laboratory handling in this study consisted of
pipetting live larvae 1) onto a slide for measure-
ment and 2) into preservative. Time spent han-
dling was an important factor affecting shrinkage.
Larvae shrink during the measuring process. In
this study, all live and laboratory shrinkage mea-

surements include about a 30 s handling time.
Some scientists measure laboratory-reared larvae
only after preservation; these larvae are probably
handled -30 s.

In his paper on the quality of field-collected fish
larvae, Ahlstrom (1976) noted several conditions
that damaged specimens: fast net speeds, high
temperatures, and increased time in the net. Dur-
ing standard ichthyoplankton surveys, larvae in
the nets could be damaged by abrasion for up to 20
min before preservation, the net is towed for 20
min, ascending 15 min, and then the collected
sample is washed down into the cod end and pre-
served (Ahlstrom 1976; Smith and Richardson
1977). Considering these variables, I designed a
net treatment to simulate shipboard procedures.
For the treatment, seawater was circulated over a
single larva in a submerged net container. (Small
larvae, 4-7 mm, were treated in groups of 10.) To
obtain conservative results, the water tempera-
ture was cool, 13° C, and the net-treatment time
varied: 5, 10, 15, and 20 min. The net-treatment
time included the pipetting and measuring as well
as the time in the net. After net treatment, larvae
were preserved; I equate these net-treated and
preserved larvae with field-collected larvae (Fig-
ure 1).

RESULTS

Live Body Parts

Head length, body depth, and eye diameter were
examined as functions of standard length for live
northern anchovy larvae (Figure 2, Table 1). On a
double logarithmic scale (Figure 2) both head
length and body depth relationships show curva-
ture, but the eye diameter relation appears to be
nearly linear. According to Zweifel,^ the simple
allometric body part relationships used for
juvenile and adult fish are not adequate for de-
scribing body part relationships of larval fish, ex-
cept for very limited ranges of size or age. There-
fore, I assumed that the larval body proportions (y)
change continuously during growth, varying ac-
cording to a nonlinear allometric growth model,

Iny = a - bic-lnx)''.

''Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

^Zweiful, J. T. Equations of growth and allometry in larval
and adult fish. Unpubl. manuscr Southwest Fisheries Center La
JoUa Laboratory, National Marine Fisheries Service, NOAA,
RO. Box 27L La Jolla, CA 92038.

686

THEILACKER: CHANGES IN BODY MEASUREMENTS OF LARVAL NORTHERN ANCHOVY

4.0
3.0

2.0 -

1.0 -

0.1

0.9

0.8
0.7

0.6
0.5

-^0.4

E

— 0.3

0.2

/

-

HEAD LENGTH

J

/"

—

'^

#

-

/

BODY DEPTH

—

/

1 1

0.1

3 4 5 6 7 89 10 15 20

EYE DIAMETER

J I I I I

2 3 4 5 6 7 8 910 15 20

LIVE STANDARD LENGTH (mm)

Figure 2. — Head length, body depth, and eye diameter as func-
tions of standard length in live northern anchovy larvae. Non-
linear models for live head length and body depth with standard
lengths and linear model for eye diameter with standard length
are described in the text; estimated parameters are in Table 1.
Dots are means of 10 larvae. Circles represent individual fish.

obtained by eliminating time it) from two Gom-
pertz equations

y ^ yo exp(Ao [l -exp( -at)]/a) and
X = Xoexp(Bo[l~exp(-/30]//3)

Table L — Estimated parameters for nonlinear and linear mod-
els relating live body part measurements (y) with standard
length (x I of northern anchovy larvae.

y

n

a

b

c

d

Head length'
Body depth'
Eyediameter^

86
38
44

4.120

2 922

-3.021

2.456
3.699
0.976

4.189
3.241

0,607
0.389

'Iny = a - £i (c -
2|ny = a + b Inx.

In

x)d.

(Zweifel footnote 3). a corresponds to the natural
logarithm of the asymptotic size of 3'; c represents
the natural logarithm of the asymptotic size of a:
(standard length); and d is the ratio of the decay
parameters a and /3 in the individual Gompertz
growth curves. The parameter b has no simple
biological interpretation except when the decay
parameters are equal id = 1); in this case the
equation is reduced to a simple allometric growth
model. The model was fit to the observed head
length and body depth measurements using Mar-
quardt's algorithm for fitting nonlinear models
(Conway et al. 1970). The equations (Table 1) gave
a good fit to the data (Figure 2). The relation be-
tween eye diameter and all treatments is discus-
sed in the section on Eye Diameter.

Laboratory Shrinkage

For northern anchovy larvae preserved in For-
malin, the ratio of preserved to preceding live size
for standard length (Figure 3), head length, and
body depth did not increase with length; i.e.,
shrinkage did not decrease with age. The ratio
averaged 0.92 for standard length after shrinkage
in Formalin, and this relation also held for shrink-
age in standard length of northern anchovy, jack
mackerel, and Pacific barracuda larvae preserved
in Bouin's fixative (Table 2). Shrinkage of other
body parts differed among species, but the mea-
surements were not made on all three species in

(.50

0-75 -

0-50

2,50

7.50 125 17.5 22.5 27.5
LIVE STANDARD LENGTH (mm)

Figure 3. — Ratio of subsequent laboratory -preserved standard
length to live standard length in northern anchovy preserved in
Formalin. Dots are means of two or three larvae. Circles repre-
sent individual fish.

687

FISHERY BULLETIN: VOL. 78. NO. 3

Table 2. — Shrinkage of laboratory-preserved northern anchovy, jack mackerel, and Pacific barracuda. Ratio is laboratory-preserved
size divided by previous live size (1.00 = no shrinkage). Standard length; head length; eye diameter; body depth at the pectoral, BD-1;
and body depth at the anus, BD-2. Measurements in millimeters.

Standard length

Head length

Eye diameter

BD-1

BD-2

Species Fixative No. Range Ratio SD No. Range Ratio SD Range Ratio SD Range Ratio SD Range Ratio SO

Northern
anchovy

Jack

mackerel
Pacific
barracuda

Formalin 61 3.9 -21.6 0.92 0.03 23 0 58-2.41 0 91 0.07 0 17-0.61 1.05 0.08
Alcohol 26 3.7 -19.0 1.00 04 — — — — — — —

Bouins' 224 3.8 -15.7 92 .00 — — — — — — —

_ _ 014-082 0.90 0.10

Bouins 45 325-3.90 92 03 43 0.74-0.97 .82

Bouins 54 3.75-5.23 .92 .02 56 1.00-1.63 .79

.04 0.26-0,33 90 .06 0.48-0 67 0.75 0 05 0 20-0.26 .75 .05
.05 0.30-0.48 .82 .04 0.58-0.96 .75 .04 0.24-0,41 .77 .05

'R Paloma. Fishery Biologist, National Marine Fisheries Service. La Jolla. Calif. Unpubl. data.

the same preservative. Jack mackerel and Pacific
barracuda, deeper bodied than northern anchovy
at the same length, were preserved in Bouin's fixa-
tive, and northern anchovy were preserved in
Formalin. Head length, eye diameter, and body
depth shrank more in jack mackerel and Pacific
barracuda larvae than in northern anchovy larvae
(Table 2). Eye diameter of northern anchovy in-
creased in size after Formalin preservation; the
increase was significant (P = 0.058; paired ^-test)
but small (0.0145±0.0031 mm).

Alcohol preservation did not cause a change in
northern anchovy standard length (Figure 4,
Table 2); smaller body parts were not mea-
sured because alcohol distorted the larvae and
they were extremely difficult to remeasure after
preservation.

• 25

1.00

:k

•

o

o°

§0^°°°

o

o°

0.75

1 i

1 1

1 1 1

6 8 10 12 14 16 18

LIVE STANOaRD LENGTH Imm)

Figure 4. — Ratio of subsequent laboratory-preserved standard
length to live standard length in northern anchovy preserved in
alcohol . Dots are means of 10 larvae. Circles represent individual

fish.

Net-Treatment Shrinkage

Shrinkage of net-treated larval northern an-
chovy varied with handling time and fish size (Ta-

TABLE 3. — Shrinkage in standard length (millimeter) of northern anchovy larvae after net handling for four time intervals (X2). Ratio
(R) = mean net standard length (X,) divided by mean live standard length (L). Ratio of 1.00 = no shrinkage.

n

Mean size

Ratio

n

Mean size

Ratio

Live size

Live

5 min net

Observed

Estimated'

Live

10 min net

Observed

Estimated'

4.00- 5.99

3

4.27

3.46

0.81

0.84

8

4.40

3.55

0.81

0.81

6.00- 7.99

3

7.57

6.87

0.91

0,90

9

7.17

5.99

0.84

085

8.00- 9.99

5

9.02

8.16

0.90

0.92

11

8.87

7.71

0,87

0.87

10.00-11.99

9

10.98

10.21

0.93

0.94

21

11.11

9.85

0.89

089

12.00-13.99

6

12.63

12.12

0.96

0.95

29

12.90

11.58

0.90

0.90

14.00-15.99

6

14.60

13.83

0.95

0.96

18

14.85

13.45

0.91

092

16.00-17.99

2

16.70

15.80

095

0.97

11

16.65

15.22

0.91

0.93

18 00-19.99

4

19.20

18.73

098

0.98

11

18.93

17.71

0.94

0.94

20.00-21 99

3

21.10

20.67

0 98

099

7

20.80

19.71

0.95

0.95

22.00-23.99

—

—

—

—

—

2

22.75

21,50

0.95

0.96

24.00-25.99

1

24.70

24.50

0.99

0.99

2

24,85

24,10

0.97

0.97

26.00-27.99

1

2670

26.00

0.97

0.99

1

26.70

25,50

0.96

097

n

Mean size

Ratio

n

Mean size

Ratio

Live size

Live

15 min net

Observed

Estimated'

Live

20 min net

Observed

Estimated'

4.00- 5.99

2

4.22

3.41

0,81

0.80

_

6.00- 7.99

2

7.35

6.20

0.84

0.83

1

7.50

650

0.87

0.82

8.00- 9.99

4

8.96

7.55

0.84

0.84

—

—

—

—

—

10.00-11.99

5

11.44

9.84

086

0.86

3

11.73

10,30

088

0.85

12.00-13.99

4

12.85

11.29

0.88

0.88

1

13.70

11.50

084

0.86

14.00-1599

7

14.57

12.73

0.87

0.89

6

14.60

12.55

0.86

0.87

16.00-17.99

4

16.57

14.53

0.88

0.90

2

16.70

14.30

0.86

0.88

18.00-19.99

5

19.22

17.72

0.92

0.92

5

19,22

17.22

0.90

0.90

20.00-21.99

3

21.10

19.67

0.93

0.93

3

21.10

19.37

0.92

0.91

22.00-23.99

1

23 50

21.40

0.91

0.94

1

23 50

21.40

0.91

0.92

24 00-2599

1

2470

23.40

0.95

0.94

1

25.00

23.80

0.95

0.93

26.00-27.99

1

26,70

24.60

092

0.95

—

—

—

—

—

'Estimated ratio = In X, -in L; Equation (4), see text and Table 4.

688

THEILACKER: CHANGES IN BODY MEASUREMENTS OK I.AKVAI. NOKTHERN ANCHOVY

ble 3). In larvae 6 mm SL or less, maximum
shrinkage (19^r) occurred after 5-10 min treat-
ment in the net; larvae were usually dead at the
end of the treatment. Older larvae shrank
throughout the 20-min period and were often alive
at the end. For example, 18-22 mm larvae were 2*^
smaller after 5 min and S-W/e smaller after 20 min
in the net. Further net treatment of larger larvae
caused an additional 1-2*^ shrinkage. Figure 5

t-O

0-9
0.8

;•

•

■■ '-, .■'- ■ ■ &»=

o

"o ""■

0

C..7

•

0.6

Ci

I i . I 1 . i. — 1 —

i

,

■O.C '2 0 14-0 16 0
LIVE ST4NDAHD LENGTH (mml

Figure 5. — Ten-minute net-treated shrinkage of standard
length as a function of size for northern anchovy larvae. Dots are
means of 10 larvae. Circles represent individual fish.

shows that measurable shrinkage decreases for
older, larger larvae, and that the ratio (R ) of the
size of net-treated iX^ ) to live (L ) size larvae rises
rapidly from about 0.7-0.8 at 4 mm SL to 0.9 by
11-12 mm SL. Although shrinkage appears nearly
constant for larvae from 12 to 22 mm (Figure 5), I
measured few older, larger larvae. Conceptually,
shrinkage is probably related to the degi'ee of os-
sification; ossification of northern anchovy verte-
brae begins at 14 mm SL and is complete at trans-
formation, about 35 mm (E. H. Ahlstrom"*). At
transformation, shrinkage should be negligible or
zero, and the ratio should approach an asymptote
of one. To characterize this relationship, I used the
equation

R ^exp[{-f,)exp(-f^X,)].

(1)

Equation ( 1) may be transformed so that the dou-
ble logarithm of i? is a linear function of size, X^,
i.e.

ln[-ln(i?)] = In/; -f.^X^.

(2)

For standard length measurements, the parame-
ters of Equation (2) were estimated for each of the
four net-treatment periods as shown below:

"•E. H. Ahlstrom, Senior Scientist, Southwest Fisheries Center
La Jolla Laboratory, National Marine Fisheries Service. NOAA,
RO. Box 271, La Jolla, CA 92038, pers. commun. December 1978.

Net-treatment time = t

/nf,

^^2

5

-1.3436

0.1209

10

-1.2708

0.0752

15

-1.2479

0.0509

20

-1.3759

0.0430

The logarithm of/!, is linear with net-treatment
time, i.e.

4 = s,t^^.

(3)

while/*! shows no trend. Combining these two rela-
tionships, i.e., R with size (Equation (D) and f.2
with time (Equation (3)), and inverting the equa-
tion to solve for live size in terms of treated larvae,
the resultant relationship is

InL = InXj +Pj exp(-P2XjX/')

(4)

X, is

where L is live size, Pj =fi,P.2 ^fiSi'P^ ^ S-z
treated size, and X.^ is time it) in minutes. Equa-
tion (4) was then fit directly using a nonlinear
fitting procedure (Conway et al. 1970 ) to obtain the
final parameter estimates. The same procedure for
estimating parameters and fitting equations was
followed for shrinkage of head length and body
depth. All equations gave a good fit to the observed
data (Figure 6, Table 3); estimates of the parame-

30
20

10

E
_E

LlJ

>

ro

0.1

STANDARD
LENGTH

HEAD
LENGTH

BODY
^ DEPTH

I I I I I I I I I

I I I 1 1 I i_

0.1 1.0 10 20 30

10 MINUTE NET TREATMENT (mm)

Figure 6. — Fit of models (Equation (4)) describing net-
treatment shrinkage of larval northern anchovy body parts.
Estimates of parameters for models are given in Table 4. Models
predict live size from net-treated size.

689

FISHERY BULLETIN: VOL. 78, NO. 3

Table 4. — Estimated parameters for models that predict live
northern anchovy body part size (L) from net-treated size (X,).

Model'

P3

Standard length
Head length
Body depth

0.289

0.177
0.413

0.434

3858

29.746

-0,680
-0605
-0620

'Equation (4), see text.

ters for the standard length, head length, and body
depth models are given in Table 4. These equations
can be used to estimate live size of each body part
from measurements of northern anchovy larvae
after net capture.

Preservation Shrinkage
(After Net Treatment)

After larvae shrank during net treatment, addi-
tional shrinkage caused by Formalin was nearly a
constant proportion of length (Figure 7). The ratio
of preserved length to net-treated length (Figure
7) may decrease slightly (i.e., shrinkage may in-
crease) with increasing fish size, but this slight
decrease has no practical significance for length
calibration of larvae taken in routine plankton
samples. Because ossification begins at 14 mm SL,
I expect large fish would shrink less, not more,
than small fish. The overall mean ratio (preserved
size/size after each timed-net treatment) of 104
standard length measurements was 0.9668±
0.0020; percent shrinkage of the other body parts
was the same as standard length shrinkage. I rec-
ommend using 39c shrinkage for all body parts in
Formalin after net treatment. Preservation in al-
cohol after net treatment did not cause further
shrinkage (only standard length measured).

To adjust the shrinkage models (Table 4) to pre-
dict live size from net-treated and Formalin-
preserved size (equivalent to field-collected lar-
vae), the preserved size is multiplied by 1.03. No

6 0 8.0 10.0 12.0 14.0 16.0

NET TREATED STANDARD LENGTH (mm)

Figure 7. — Size specific shrinkage of northern anchovy larvae
preserved in Formalin after 10-min net treatment. Dots are
means of 10 larvae. Circles represent individual fish.

adjustments are needed for alcohol-preserved
samples.

The difference in shrinkage between
laboratory-preserved larvae and net-treated and
preserved larvae of the same initial live size de-
creased with age. For example, 3 mm larvae that
were net treated and preserved in Formalin
shrank IB'A more in standard length than 3 mm
larvae that were laboratory preserved in Forma-
lin, but shrinkage of 20 mm larvae was the same
for both treatments (Table 5). Shrinkage of

Table 5. — Comparison of standard length for live (L),
laboratory-preserved and net-treated northern anchovy larvae
(X^). Numbers in parentheses are preserved length divided by
live length (ratio of 1.00 = no shrinkage).

Estimated prese

ved size (mm)

Live size

(mm)

Laboratory'

Net-treated^

Alcohol

Formalin

Alcohol

Formalin

3

3 (1.00)

2.76(0.92)

2.38(0.79)

2.31 (0.77)

5

5(1.00)

4.59(0.92)

4.10(0,82)

3 98(0.80)

10

10(1 00)

9.18(0.92)

8.77 (0.88)

8.51 (0.85)

15

15(1.00)

13.78 (0.92)

13.81 (0.92)

13.40(0.89)

20

20(1.00)

18.37 (0.92)

18.99(0.95)

18.42 (0.92)

25

24.21 (0.97)

23.48 (0.94)

30

29.40 (0.98)

28.52 (0.95)

35

34.56(0.99)

33,52 (0.96)

40

39.68(0.99)

38.49 (0.96)

45

44.77 (0.99)

43.43 (0.97)

50

49.84(1.00)

48.34 (0.97)

'Includes 30 s handling time; no shrinkage in alcohol and 8% shrinkage in
Formalin (see text).

^Estimated preserved size calculated from Equation (4) for 10 mm net treat-
ment: size adjusted for 3% additional shrinkage in Formalin (see text and
Table 4).

laboratory-preserved larvae in Formalin probably
decreases to something <8% (Table 5) as the skele-
ton develops and ossification occurs. Formalin pres-
ervation of 90 mm and larger salmon, Oncoryn-
chus spp., smolts caused 3-49^^ shrinkage in length
(Parker 1963). Laboratory shrinkage of northern
anchovy after transformation may be similar;
thus, shrinkage of net-collected and preserved
northern anchovy >35 mm (Table 5) should be
similar to shrinkage of laboratory-preserved fish
>35 mm.

Eye Diameter

Netting live larvae for 10 min caused the eye
diameter to shrink an average of 0.0443 ±0.0069
mm, and Formalin preservation after net treat-
ment caused an increase in eye diameter that av-
eraged 0.0177 ±0.0046 mm. The increase in eye
diameter after preservation was similar to the in-
crease after preservation noted for eye diameter of
laboratory-preserved larvae. The ^tests for paired
data (n=23) showed that in all cases the differ-

690

THEILACKER: CHANGES IN BODY MEASUREMENTS OF LARVAL NORTHERN ANCHOVY

ences between treatments (live, net treated, and
preserved) were significant (P<0.01). Even though
these differences were significant, the small
changes in eye diameter size caused by net treat-
ing and preserving probably are not important for
calibration of size of field-collected larvae. Thus
eye diameter should be a useful parameter for
estimating average live standard length of field-
collected larvae (Table 1).

DISCUSSION AND CONCLUSION

The causes of antemortem shrinkage offish lar-
vae are not completely understood. Before death,
appearance of the body changes from translucent
to opaque. This phenomenon is an indicator of
ensuing death of larvae in rearing experiments.
Autolysis, digestion of tissues by their own en-
zymes, is occurring during this antemortem
period (Theilacker 1978 ), and the enzymatic action
on proteins may cause denaturation, thus the color
change and shrinkage. Shrinkage also may be
caused by an osmoregulatory problem. An inabil-
ity to osmoregulate may develop from loss of
mucus by abrasion after contact with a surface.
The internal osmolar concentration of another
clupeoid larva, Pacific sardine, Sardmops sagax, is
0.24 M and that of seawater 0.56 M (Lasker and
Theilacker 1962). If a larva were unable to os-
moregulate, this difference in osmolarity would
cause it to lose fluid and shrink.

The amount of shrinkage that occurred before
larvae were killed in a preservative was depen-
dent on larval fish size and the extent of "han-
dling" (measuring and netting). The elapsed time
of surface contact was the main determinant of
final length. This was especially noticeable while
measuring small, 3-7 mm larvae. As larvae in-
creased in size and ossification progressed, net-
treatment shrinkage decreased.

Preserving larvae after handling caused addi-
tional shrinkage that was a constant proportion of
size. Laboratory-preserved shrinkage in Formalin
included a 30 s handling time; shrinkage in For-
malin was constant at 8'7c and independent of size.
Preserving larvae that had been retained in a net
caused an additional 37^ shrinkage; the additional
shrinkage was nearly a constant proportion of
size.

Farris' (1963) results on shrinkage of labora-
tory-preserved, 3-6 mm yolk-sac Pacific sardine
larvae agree with my results. He found Formalin
shrinkage of standard length ranged between 7

and 11'%^, similar to the 8*7^ shrinkage for
laboratory-preserved northern anchovy in my
study. Rosenthal et al. (1978) reported a I67c
shrinkage of newly hatched, 2 mm larvae of the
sea bream, Chrysophrys major. The larvae were
anesthesized with MS-222 and measured with a
projector prior to preservation in Formalin. It ap-
pears that handling of the sea bream was minimal;
however, MS-222 has been reported to interfere
with osmoregulation (Parker 1963), and an inabil-
ity to osmoregulate would cause a greater shrink-
age. Blaxter (1971) reported on a net-shrinkage
experiment that was similar to my study. After his
net treatment, mean live size of 22 herring larvae
(10.77 mm) decreased by 17'7f ; Formalin fixation
caused an additional 3-5*%^ shrinkage for a total of
20-22^f . He noted the larvae were dead after net-
ting, but the elapsed time is unknown. In this
study, the netted 11 mm northern anchovy were
usually dead after 20 min, and the total shrinkage
of the 20-min treated 11 mm northern anchovy
was about 18*%^, similar to Blaxter 's experiment.

If the larvae to be measured are badly damaged
or partially digested, the models generated in this
study, which describe live body proportions and
shrinkage, could be used to estimate average fish
length from size of head or eye. Packard and
Wainwright (1974) found that eye diameter of
young herring (up to 100 mm) was a useful refer-
ence parameter for estimating both size and
weight. Because eye diameter of northern anchovy
changed little during netting and preservation,
eye diameter may be a useful parameter for es-
timating average live size of field-collected larvae.
However, use of eye diameter to estimate live stan-
dard length assumes that the relation between eye
diameter and standard length is the same for
laboratory-reared and field-collected larvae. Bal-
bontin et al. ( 1973) and Blaxter ( 1976) have shown
that morphological differences exist between
reared and wild fish of the same length, thus the
assumption, that the body forms of reared and wild
northern anchovy larvae are similar, may be in-
valid. However, as I have shown in this study, the
method of handling larvae prior to preservation
causes shrinkage differences that could be inter-
preted as morphological differences.

The most important use of the shrinkage models
is to predict live size, and thus age, of sea-collected
northern anchovy larvae so that results from
laboratory larval fish studies can be related to the
sea. Use of the standard length shrinkage model
(Table 4) should give the best estimate of live size

691

FISHERY BULLETIN: VOL. 78, NO. 3

for field collected larvae. The standard length
model can probably be applied to shrinkage of all
clupeidlike larvae if the patterns of calcification
are similar

FORTRAN computer programs for the non-
linear models are available at the Southwest
Fisheries Center La Jolla Laboratory.

ACKNOWLEDGMENTS

I especially wish to thank James Zweifel for his
consultation, encouragement, and assistance in
developing these models. Thanks also to Joe
Caruso for his interest in the study and patient
assistance with the computer programs, Jack
Metoyer for assisting with the tedious task of
measuring larvae, Kathleen Coleman for helping
me by typing the draft and the tables, and Lor-
raine Prescott for typing the final draft. John
Hunter, Reuben Lasker, and two anonymous re-
viewers read the manuscript and offered many
helpful suggestions.

LITERATURE CITED

Ahlstrom, E. H.

1976. Maintenance of quality in fish eggs and larvae col-
lected during plankton hauls. In H.F.Steedman( editor),
Zooplankton fixation and preservation, p. 313-318.
Monogr. Oceanogr. Methodol. 4.
Balbontin, F., S. S. desilva, and K. F. EHRLICH.

1973. A comparative study of anatomical and chemical
characteristics of reared and wild herring. Aquaculture
2:217-240.
Blaxter, J. H. S.

1971. Feeding and condition of Clyde herring lar-
vae. Rapp. P.-V. Reun. Cons. Int. Explor Mer 160:128-
136.

1976. Reared and wild fish — how do they compare? Proc.
10th Eur Symp. Mar Biol. 1:11-26.

Conway, G. R., N. R. Glass, and J. C. Wilcox.

1970. Fitting nonlinear models to biological data by Mar-

quardt's algorithm. Ecology 51:503-507.

farris, d. a.

1963. Shrinkage of sardine (Sardinops caerulae) larvae
upon preservation in buffered formalin. Copeia
1963:185-186.

Hunter, J. R.

1976. Culture and growth of northern anchovy, Engraulis
mordax, larvae. Fish. Bull., U.S. 74:81-88.

Lasker, R., H. M. Feder, G. H. Theil.acker, and R. C. May.

1970. Feeding, growth and survival of Engraulis mordax
larvae reared in the laboratory. Mar Biol. ( Berl.) 5:345-
353.

Lasker, R., and G. H. Theilacker.

1962. Oxygen consumption and osmoregulation by single
Pacific sardine eggs and larvae, {Sardinops caerulea
Girard). J. Cons. 27:25-33.

LEONG, R.

1971. Induced spawning of the northern anchovy, En-
graulis mordax Girard. Fish. Bull., U.S. 69:357-360.

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.

Packard, A., and A. W. Wainwright.

1974. Brain growfth of young herring and trout. /nJ.H.S.
Blaxter (editor), The early life history offish, p. 499-507.
Springer- Verlag, N.Y.

Parker, R. R.

1963. Effects of formalin on length and weight of
fishes. J. Fish. Res. Board Can. 20:1441-1455.

Rosenthal, H., D. Kuhlmann, and O. Fukuhara.

1978. Shrinkage of newly hatched larvae of the red sea
bream (Chrysophrys major Temminck and Schlegel) pre-
served in Formalin. Arch. Fischereiwiss. 29:59-63.
RYLAND, J. S.

1966. Observations on the development of larvae of the
plaice. Pleuronectes platessa L., in aquaria. J. Cons.
30:177-195.

Smith, R E., and S. L. Richardson.

1977. Standard techniques for pelagic fish egg and larva
surveys. FAO Fish. Tech. Pap. 197,

Theilacker, G. H.

1978. Effect of starvation on the histological and mor-
phological characteristics of jack mackerel, Trachurus
symmetricus, larvae. Fish. Bull., U.S. 76:403-414.

Theilacker, G. H., and m. f. mcMaster.

1971. Mass culture of the rotifer Brachionus plicatilis and
its evaluation as a food for larval anchovies. Mar Biol.
(Berl.) 10:183-188.

692

ASPECTS OF LARVAL ECOLOGY OF SQUILLA EMPUSA
(CRUSTACEA, STOMATOPODA) IN CHESAPEAKE BAY

Steven G. Morgan'

ABSTRACT

Larvae ofSquilla empusa were collected from the plankton and were laboratory-reared in 16 combina-
tions of temperature and salinity to determine their tolerances. Larvae survived longer and molted
more frequently when reared at 25%o and 20° or 25° C, which corresponds to the natural conditions of
Chesapeake Bay when the larvae were collected.

A 2-yr planktonic survey conducted in the lower region of the bay by the Virginia Institute of Marine
Sciences was compared with a survey made at the bay mouth in 1976. The seasonal occurrence of
Squilla empusa larvae extended from the last week of July until the first week of October with a peak
abundance occurring about the first week of September The peak abundance in the lower region of the
bay was 0.37 larva/m^ in 1971 and 0.59 larva/m^ in 1972. Four of the nine stages were not captured.
Collections taken at the bay mouth in 1976 with a % m net captured all stages and the peak abundance
was determined to be 0.27 larva/m^. The larvae were more abundant in the higher salinity waters of the
channel areas and eastern portion of lower Chesapeake Bay. A large-mouth plankton net with rela-
tively coarse mesh should be towed at night to ensure the collection of all larval stages since the larger
larvae are apparently able to avoid small nets.

The Order Stomatopoda is a small group of primi-
tive, specialized crustaceans which reside primar-
ily in shallow tropical marine waters. Of the 350
species (Caldwell and Dingle 1976) only a few ex-
tend into temperate waters, Squilla empusa
among them. This mantis shrimp, which attains a
length of 20 cm, is found from Massachusetts to
northern South America and is quite abundant
throughout its range, including Chesapeake Bay
(Brooks 1878; Cowles 1930; Wass 1972).

Stomatopod larvae are often found in great
swarms, particularly in tropical waters where
adults are most abundant. The planktonic larval
stages compose a substantial portion of the neritic
plankton and constitute a considerable part of the
diet of reef fishes, jacks, scads, herrings, snappers,
and commercially important pelagic fishes such as
tunas and mackerel (Sunier 1917; Fish 1925;
Reintjes and King 1953; Randall 1967; Dragovich
1970).

Squilla empusa larvae are large crustacean lar-
vae, attaining 17.5 mm long. The larvae undergo
nine pelagic stages before settling to the bottom as
postlarvae (Morgan and Provenzano 1979). Brooks
(1878) found stomatopod larvae he assumed were

'Institute of Oceanography, Old Dominion University, Norfolk,
Va.; present address: Duke University Marine Laboratory, Pivers
Island, Beaufort, NC 28516.

those of S. empusa present in Chesapeake Bay
from early July to the middle of August in the
greatest abundance, but he discontinued the study
before the larvae had completed their metamor-
phosis. No other data on larvae of this species have
been added to the literature since.

Due to the paucity of ecological information on
the larvae of this prevalent crustacean, an inves-
tigation was undertaken to determine their sea-
sonal occurrence, distribution, and abundance in
Chesapeake Bay. The abundance and duration of
the larvae as part of the plankton may be impor-
tant factors in the ecology of the bay, since the
larvae not only serve as food for a variety of or-
ganisms, including commercially important
fishes, but are also rapacious predators them-
selves, thriving on other members of the
planktonic community.

In recent years the effects of temperature and
salinity on the larval development of decapod
crustaceans have been studied, but no studies
have been made on the temperature and salinity
tolerance for the larvae of any species within the
Order Stomatopoda. Temperature and salinity are
critical factors affecting the survival of marine
and estuarine organisms, especially during the
sensitive developmental stages upon which the
success of the species relies. Thus, a qualitative
determination of the temperature and salinity tol-

Manuscript accepted February 1980.
FISHERY BULLETIN: VOL. 78, NO.

3. 1980.

693

FISHERY BULLETIN: VOL. 78, NO. 3

erance of S. empusa is presented and a compari-
son of the laboratory result with the observed dis-
tributions is made.

METHODS

Research Applied to
National Needs (RANN) Survey

The sampling area extended from lat. 37°40' N,
just north of the Rappahannock River, to the bay
mouth, an area covering 1,300 km of the lower
Chesapeake Bay (Figure 1). The survey area was
divided into eight subareas designated A through
H. A, D, and G were situated in the western por-
tion and B, F, and H in the eastern section of the
bay. These divisions were based on salinity differ-
ences in the bay, while areas C and E were sepa-
rated because they represented channel areas.

Figure l.— Subareas (A-H) of RANN survey, August 1971 to
July 1973, in lower Chesapeake Bay, Va.

The study area, consisting of 688 stations set 1.8
km apart, was sampled from August 1971 to July
1973. Three to five stations were randomly
selected from each subarea to be sampled each
month.

The plankton samples collected during the
RANN survey were taken with a bongo sampler,
having a mouth diameter of 18.7 cm (8 in) and
equipped with 202 /xm mesh nets. Stepped oblique
tows were taken for varying lengths of time at
each station, depending on station depth. A sub-
mersible pump was used at depth intervals of 2 m
to gather hydrographic data. The temperature and
salinities taken at each interval from each station
were then averaged. All tows were taken during
daylight. The stomatopod larvae were sorted from
the general catch by the Virginia Institute of
Marine Science staff and staged by the author.

Cape Henry Survey

Using the Old Dominion University RV Lin-
wood Holton , larval specimens of S. empusa were
collected weekly at Cape Henry where a popula-
tion of adults exists. By using a V2 m plankton net
(153 /xm mesh), 10 min stepped oblique tows were
accomplished as the ship circled the collection site
at idle speed. The volume of water filtered through
the net was calculated from the duration of the tow
and the area of the net because the flowmeters
employed yielded wildly erratic readings. The
volume of water filtered for a 10-min tow was cal-
culated to be 47.6 m^. Surface and bottom water
temperatures and salinities were recorded for
each tow, using an inductive salinometer with a
45.7 m cable.

Upon collection each plankton sample was
placed in a 1.9 1 (y2-gal) jar and filled with seawa-
ter. Samples containing large amounts of biomass
were split into two such jars to facilitate the survi-
val of the stomatopod larvae until they could be
separated from the sample. As many larvae as
possible were extracted from the samples aboard
the ship and the task was completed in the
laboratory. These larvae were placed in 1.9 1 jars
filled with seawater and were grouped according
to size so that cannibalism would be minimal. The
jars were aerated until the samples reached the
laboratory, whereupon the larvae were placed in
compartmentalized plastic trays, one per com-
partment. Each compartment measured 4.5 x 5 x
4 cm. Medium used for rearing the larvae was

694

MORGAN: ASPECTS OF LARVAL ECOLOGY Of SQUILLA EMPUSA

made from Instant Ocean Synthetic Sea Salts^
(Aquarium Systems, Inc., Eastlake, Ohio) and
tapwater.

Larvae representing all nine developmental
stages of S. empusa were reared in 16 combina-
tions of temperature and salinity, each having a
similar composition of larval stages. The experi-
mental temperatures used were 10°, 15°, 20°, and
25° C, and salinities were 10, 15, 25, and 35%o,
chosen because they represent the range of condi-
tions the larvae might be expected to encounter in
the lower Chesapeake Bay. The salinities of 20 and
30%o were omitted from the experimental regime
because insufficient numbers of larvae were ob-
tained to determine their tolerances to all inter-
mediate salinities as well as to the more extreme
salinities. Thirty-six larvae were subjected to each
temperature-salinity combination. Because the
larvae were not hatched in the laboratory under
the temperature-salinity combination at which
they would be reared, some larvae were subjected
to changes as great as 5° C and 10%o per day until
the experimental value was attained. No light
cycle was used in the experiment, the larvae being
maintained in total darkness except for 10-min
periods when the larvae were given fresh food and
water.

Each larva was reared in 25 ml of water and
given freshwater and approximately 30 Artemia
salina nauplii/ml daily. Great increases in size
from the first to the last stage necessitated ad-
justments in food size and quantity. At about the
fifth stage of development food was switched from
A. salina nauplii to decapod zoeae or A. salina
larvae grown on a yeast or algal culture. While
changing the culture medium, observations were
recorded on the progress of each larva regarding
the frequency of molting, duration of larval devel-
opment, survival, and the stage of development.

Percent survival and molting frequency are
often used as measures of success of larvae under
different temperature-salinity regimes, but were
not meaningful in this experiment because the
larvae were captured at different stages of devel-
opment and different places in the molt cycle.
Therefore, the length of survival and number of
molts were used as the standards of success. The
temperature and salinity combinations which
promoted the greatest number of molts and the

longest periods of survival among the larvae were
considered to be most conducive to the larval de-
velopment of S. empusa, because the larvae were
not only surviving best but were also maturing
fastest. The mean number of ecdyses and days of
survival were calculated for each larva and then
collective means were figured for each
temperature-salinity combination. In this way a
general indication of success of populations under
varying temperature and salinity conditions could
be determined.

RESULTS

Seasonal Occurrence

The RANN survey extended from 16 August
1971 until 25 July 1973. and S. empusa larvae were
found in the Chesapeake Bay only from late July
to mid-September or late October (Figure 2). Dur-
ing these months in 1971 the RANN study sampled
on 16-19 August, 21-23 September, and 26-29 Oc-
tober, while in 1972 samples were taken on 24-27
July, 15, 17, 18, 21 August, 12-14 September, and 16,
18, 24 October. In 1973, sampling was conducted on
23-25 July.

The monthly sampling program used by the
RANN program left the larval occurrence of S.
empusa somewhat unclear In both years of the
survey, larvae were found on the first day of sam-
pling in July, 24 July 1972 and 23 July 1973; since
a month elapsed between the June and July sam-
plings, however, the earliest appearance of the

ASONDJ FMAMJ JASON DJ FMAM,
1971 1972 1973

A SON

1976

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

Figure 2. — Lar\'al abundance ofSquilla empusa collected from
the lower Chesapeake Bay from August 1971 to July 1973 and
from June to November 1976.

695

FISHERY BULLETIN: VOL. 78, NO. 3

larvae could have gone undetected. The same
problem occurred in defining the time of disap-
pearance, for larvae were abundant on 14 Sep-
tember 1971 and 1972 but the next sampling was
not conducted until 26 October 1971 and 16 Oc-
tober 1972. Only one Stage I larva was found in
October 1971.

The Cape Henry data helped to determine more
closely the planktonic duration of the larvae since
a weekly sampling program was followed when
weather permitted. In agreement with the RANN
survey, the first larvae appeared in late July. Lar-
vae were present on 28 July but none were found
on 20 July. Larvae were found until 6 October;
none were collected on 13 October. From the
RANN and Cape Henry surveys it is apparent that
the planktonic occurrence of S. empusa extends
from the last week of July until the first week of
October, a period of almost 11 wk or about 2V2 mo.

Only Stages I-IV and IX were collected by the
RANN survey (Figure 3). Bearing this in mind,
the RANN data showed the month of maximum
abundance to be August, with 0.37 larva/m^ col-
lected in 1971 and 0.59 larva/m^ in 1972; Sep-

tember, July, and October trailed in order of de-
creasing abundance (Figure 2). The Cape Henry
data, on the other hand, showed a peak abundance
in September with 0.27 larva/m^ in 1976 followed
by August, July, and October

All nine stages were collected during the Cape
Henry sampling program (Figure 4). In July, when
the larvae first began to appear. Stages I and II
were the only stages collected in abundance and
they were more numerous than in any following
month. Several specimens of Stages V and VIII
were also captured. All larval stages were present
in August with younger larvae generally being
predominant over older larvae. By early Sep-
tember the larvae had reached their peak abun-
dance. Although some of the younger larval stages
had begun to decline, they were still predominant.
The latest larval stages, VIII and IX, were becom-
ing increasingly abundant until October when
only Stage IX larvae were obtained.

The abundance of larvae caught from each sub-
area during the RANN survey indicates that lar-
vae were more prevalent in the eastern and chan-
nel areas of the bay than in the western portion

CO

<
>

<

'A S O N
1971

J J A S O N
1972

J J
1973

Figure 3. — Abundance of larval stages (I-IX) ofSquiUa empusa
collected from the lower Chesapeake Bay from August 1971 to
July 1973. Larval stages described in Morgan and Provenzano
(1979).

FIGURE 4.— Abundance of larval stages (I-EX) and postlarva
(PL) of Squilla empusa collected at Cape Henry, lower
Chesapeake Bay, from June to October 1976. Larval stages de-
scribed in Morgan and Provenzano (1979).

696

MORGAN: ASPECTS OF LARVAL ECOLOGY OF SQUILLA EMPUSA

Table l. — Larval abundance ofSquilla empusa with mean temperatures and salinities for each
subarea (Figure 1) of the lower Chesapeake Bay for August and September 1971 and 1972.

Lower

Middle

Upper

West

Ctiannel

East

West

Ctiannel

East

West

East

A

B

0

D

E

F

G

H

1971:

Larvae/m'

0.13

0.36

0.19

0.12

0.28

0.28

0.05

0.47

Mean salinity

24.8

25.5

26.0

201

22.4

22.9

17.7

20.8

Mean temperature.

0

24.5

24.3

23.7

255

25.1

24.4

24.9

247

1972:

Larvae/m^

0.43

0.44

0.41

0.04

0.70

0.89

0.02

0.08

Mean salinity

20.5

21.0

23.0

17.3

19.4

19.4

15.3

15.8

Mean temperature,

C

23.4

234

23.1

24.3

23.9

23.5

24.2

23.9

1971 and 1972:

Larvae m^

0.30

0.40

033

0.08

0.49

0.75

0.03

0.28

Mean salinity

22.7

23.2

245

18.7

20.9

21.1

16.5

18.3

Mean temperature.

'C

23.9

23.9

23.4

24.9

245

240

24.6

24.3

(Table 1). Larvae were also more abundant in the
lower regions of the sampling area than in the
upper (subareas G and H).

Squilla empusa larvae occur in the Chesapeake
Bay when the mean temperatures are the highest
of the year. The first larvae were encountered in
July for both 1972 and 1973 when mean tempera-
tures were 25.2° and 24.5° C. The larvae were most
abundant in August when the mean temperatures
were 24.9° and 24.2° C in 1971 and 1972. The mean
temperatures declined in September along with
the abundance of larvae until larvae were rarely
found or not found in October when temperatures
were 19.7° and 19.4° C in 1971 and 1972. The mean
salinity during the seasonal occurrence of the lar-
vae in 1971 and 1973 fluctuated between 21.5 and
23.1%o, while in 1972 it was much lower as a result
of Tropical Storm Agnes. In July 1972 the mean
salinity was 16.5%© and it increased to 21.2%o in
October when larvae no longer occurred in the
plankton.

Temperature and Salinity Tolerance

Although none of the 576 larvae reared at the 16
different temperature and salinity combinations
was reared through the entire pelagic develop-
ment to metamorphosis, larvae survived well and
molted frequently at 2 of the test combinations. At
20° C-25%0 and 25° C-25%o, A19c of the larvae
molted three or more times, 24*7^ underwent at
least five ecdyses, and 3% molted seven times over
a 6-wk period. Metamorphosis to postlarva oc-
curred 34 times and was not a problem in the
rearing process.

In general, larvae fared best at higher tempera-
tures and salinities (20°, 25° C, 25, 35%o) and
were least successful at the lower temperatures
and salinities (10°, 15° C, 10, 15%o). Excluding lar-

vae reared at 10° C, the longest survival and
greatest number of molts occurred at salinities of
25%o followed by 35, 15, and 10%o in order of de-
creasing length of survival and number of molts
(Figures 5, 6). Length of survival at 25°, 20°, and
15° C was similar but at 25° and 20° C the mean
number of molts was much higher. At 10° C larvae

>
<

<
>

>

DC

CO

<

24

1

23

- 10%o 15%o 25%o

35%o

22

-

21

-

-|

20

-

19

-

18

-

17

-

—

16

-

1

15

-

14

-

13
12

-

1 1

! 1

10

9

8

7

6

5

r-

4

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— !

3

2

1

n

10152025 10152025 10152025 10152025
TEMPERATURE (°C)

Figure 5. — Average survival, in days, for all larval stages of
Squilla empusa, grouped by 16 temperature-salinity combina-
tions according to salinity.

697

FISHERY BULLETIN: VOL. 78, NO. 3

10 15 20 25 10 15 20 25 10 15 20 25 10 15 20 25
TEMPERATURE (°C)

Figure 6. — Average number of ecdyses for all larval stages of
Squilla empusa grouped by 16 temperature-salinity combina-
tions according to salinity.

molted rarely and did not survive long at the lower
salinities. At higher salinities molting occurred
slightly more often and larvae at 10° C-35%o were
able to endure the longest of any of the combina-
tions. Some of these larvae persisted for as long as
47 d, but usually without molting. Since these
larvae did not appear to feed and moved only
slightly, the low temperature only seemed to delay
their deaths.

DISCUSSION

The information provided by the RANN survey
only loosely delimited the seasonal occurrence of
S. empusa larvae in Chesapeake Bay because of
infrequent sampling. A weekly sampling program
would have been beyond the scope of the investiga-
tion considering that the purpose of the RANN
study was to survey the entire zooplankton com-
munity of the lower Chesapeake Bay over a 2-yr
period. Supplemental data taken at Cape Henry
combined with the RANN data indicate that the
seasonal occurrence of S. empusa larvae extends
from late July to early October, a period of about
11 wk. Observations made by Brooks (1878) con-
cerning the planktonic duration of S. empusa lar-
vae are in agreement with the current study, but
the time of occurrence was slightly earlier in the
previous study. Larvae were present in the
plankton from early July through August when
Brooks discontinued the study. Eleven weeks is a

fairly short planktonic duration for stomatopod
larvae. The temperate species Oratosquilla
oratoria, common in Japan, has a 5-mo duration
(Senta 1967), and Pterygosquilla armata
schizodontia was discovered to remain in the
plankton for up to 9 mo (Pyne 1972).

Although Brooks (1878) found the .S. empusa
larvae in great abundance, sometimes collecting
200 or 300 in a single evening from the mouth of
the James River, both the RANN data and the
Cape Henry data showed that the larvae were
never abundant. Because only five of the nine lar-
val stages were collected during the RANN survey
the abundance values are inordinately low. Ap-
parently, the larger larvae are able to avoid the
small bongo plankton nets. Great quantities of
Stage I larvae were captured throughout the lar-
val season but far fewer numbers of Stage II were
caught and fewer still Stage III larvae were caught
and so on until Stages V-VIII were not collected at
all. The large decreases seem to be too great to be
accounted for by mortality alone.

It is possible that the large, quick-moving (pers.
obs.) stomatopod larvae could avoid the small
mouth of the net which was easily detectable since
sampling was conducted during daylight
(Fleminger and Clutter 1965; McGowan and
Fraundorf 1966; Murphy and Clutter 1972). Olney
(1978) also used data collected during the RANN
survey and found evidence of avoidance in other
large, agile zooplankters, particularly mysids and
fish larvae. A Vi m net and night sampling were
used during the Cape Henry survey and the elu-
sive stages missed by the bongo sampler were cap-
tured. Although all nine stages were collected,
peak abundance was still slightly lower than the
RANN values. The lower value may have resulted
from the use of a smaller mesh net, from not
employing a flowmeter to obtain better filtration
estimates, or from yearly fluctuations in the popu-
lation; but, the abundance figures determined by
the RANN and Cape Henry surveys are low for
an organism that has been considered to be abun-
dant in Chesapeake Bay (Brooks 1878; Cowles
1930; Wass 1972).

The RANN data showed the month of maximum
abundance to be August, but the Cape Henry data
demonstrated a peak abundance in early Sep-
tember. Again, this discrepancy may be attributed
to normal yearly variation, but it probably re-
sulted from the RANN program having sampled
only the younger element of the population.

698

MORGAN: ASPECTS OF LARVAL ECOLOGY OF SQUILLA EMPUSA

Larvae reared in the laboratory survived
longest and molted the greatest number of times
at 20° C-25%0 and 25° C-25%o which corresponds to
the temperatures and salinities found in the bay
where the larvae were most abundant. The mean
temperature of the bay from July through Sep-
tember, the season of larval occurrence of S. em-
pusa, ranged from 19.7 ° to 25.2° C while the mean
salinity was recorded from 21.5 to 23.1%o in 1971
and 1973.

The greater abundance of larvae in the eastern
and channel subareas of the bay is likely a result of
the higher salinities. In Chesapeake Bay
salinities are higher on the eastern side than on
the western side due to the earth's rotation
(Coriolis force) and the differences are enhanced
by the larger inflow of freshwater from rivers on
the western side (Pritchard 1952). The lower
salinities of the upper reaches of the sampling
area are also probably responsible for the lesser
larval abundances in subareas G and H.

In 1972, Tropical Storm Agnes produced the
most extensive flooding and greatest freshwater
runoff in Chesapeake Bay in many decades, if not
centuries, causing the distribution and abundance
of most estuarine organisms to be seriously dis-
rupted (Andrews 1973). The mean salinity of the
lower Chesapeake was reduced to 16.5%o in July
only to increase to 19.4%o in October. Although the
larvae were more abundant in 1972 than in 1971,
the reduced salinity resulted in a distribution
compressed into the more southern subareas
where the salinity was greater. Few larvae were
captured in subareas D, G, and H where salinities
ranged from 15.3 to 17.3%o, which would be ex-
pected considering the poor development of larvae
reared at 15%o during the temperature and salin-
ity experiment. Grant et al. (1976) found other
zooplankters in the lower Chesapeake Bay to be as
abundant in 1972 as in 1971 and their distributions
were also compressed in 1972.

Of the S. empusa larvae reared at the most
favorable temperature and salinity combinations
for survival and growth, 3% of the larvae were
reared through eight of the nine larval stages in 6
wk, indicating that the length of the pelagic larval
development would be slightly longer than 6 wk.
However, the appearance of the postlarvae in the
bay 1 mo after the initial appearance of the larvae
indicates a substantially briefer period of larval
development, provided that all larvae originated
within the bay. The development of the larvae
reared in the laboratory may have been extended

as a result of dietary insufficiencies and an overall
more stressful environment. Furthermore, the
few specimens of stages V and VIII collected early
in the 1976 larval season may have drifted into the
bay from more southerly populations where eggs
may have hatched earlier and been transported by
currents into Chesapeake Bay. Nevertheless, since
all larval stages and the postlarva were collected
in Chesapeake Bay throughout their seasonal oc-
currence, it appears that the populations of S.
empusa in the bay is self-sustaining. In addition,
the temperature and salinity tolerances of the
larvae correspond to those of the adults, which
may occur in salinities as low as 16%o, but are most
abundant in waters >25%o (Cowles 1930; Gunter
1950; Parker 1956; Lee and McFarland 1962).

ACKNOWLEDGMENTS

I am indebted to George C. Grant of the Virginia
Institute of Marine Science who made available
plankton samples collected during the RANN sur-
vey of the lower Chesapeake Bay. He also kindly
provided the map of the survey area and com-
mented on the manuscript.

Thanks are also due Anthony J. Provenzano, Jr.
for his guidance during the investigation and his
comments on the manuscript.

This work was supported in part by the National
Science Foundation Grant DEB-76-11716.

LITERATURE CITED

Andrews, J. D.

1973. Effects of Tropical Storm Agnes on epifaunal inver-
tebrates in Virginia estuaries. Chesapeake Sci. 14:223-
234.
BROOKS, W. K.

1878. The larval stages of Squilla empusa Say. Johns
Hopkins Univ, Chesapeake Zool. Lab. Sci. Res. 1878:143-
170.
Caldwell, R. L., and H. Dingle.

1976. Stomatopods. Sci. Am. 234(l):80-89.
COWLES, R. P.

1930. A biological study of the offshore waters of
Chesapeake Bay Bull. U.S. Bur. Fish. 46:276-381.
DRAGOVICH, A.

1970. The food of skipjack and yellowfin tunas in the Atlan-
tic Ocean. U.S. Fish Wildl. Serv., Fish. Bull. 68:445-460.

Fish, C. J.

1925. Seasonal distribution of the plankton of the Woods
Hole region. Bull. U.S. Bur. Fish. 41:91-179.
FLEMINGER, A„ and R. I. CLUTTER.

1965. Avoidance of towed nets by zooplankton. Limnol.
Oceanogr. 10:96-104.

Grant, G. C, B. B. Bryan, F Jacobs, and J. E. Olney.

1976. Effects of Tropical Storm Agnes on zooplankton in

699

the lower Chesapeake Bay. In The effects of Tropical
Storm Agnes on the Chesapeake Bay Estuarine System, p.
425-442. Chesapeake Research Consortium, Inc. CRC
Publ. 54.
GUNTER, G.

1950. Seasonal population changes and distributions as
related to salinity, of certain invertebrates of the Texas
coast, including the commercial shrimp. Publ. Inst. Mar.
Sci., Univ. Tex. 1(2):7-51.

Lee, B. D., and W. N. McFarland.

1962. Osmotic and ionic concentrations in the mantis
shrimp Squilla empusa Say. Publ. Inst. Mar. Sci., Univ.
Tex. 8:126-142.

MCGOWAN, J. A., AND V. J. FRAUNDORF.

1966. The relationships between size of net used and esti-
mates of zooplankton diversity. Limnol. Oceanogr.
11:456-469.

Morgan, S. G., and a. J. Provenzano, jr.

1979. Development of pelagic larvae and postlarva of
S^wiV/a empusa (Crustacea, Stomatopoda). Fish. Bull.,
U.S. 77:61-90.

Murphy, G. I., and R. I. Clutter.

1972. Sampling anchovy larvae with a plankton purse

seine. Fish. Bull., U.S. 70:789-798.
OLNEY, J. E.

1978. Planktonic fish eggs and larvae of the lower

Chesapeake Bay. M.A. Thesis, Coll. William and Mary,

Williamsburg, Va., 123 p.

fishery bulletin: vol. 78, no. 3
Parker, R. H.

1956. Macro-invertebrate assemblages as indicators of
sedimentary environments in East Mississippi Delta re-
gion. Am. Assoc. Pet. Geol. Bull. 40:295-376.
PRITCHARD, D. W.

1952. Salinity distribution and circulation in the
Chesapeake Bay estuarine system. J. Mar Res. 11:106-
123.

PYNE, R. R.

1972. Larval development and behaviour of the mantis
shrimp Squilla armata Milne Edwards (Crustacea:
Stomatopoda). J. R. Soc. N.Z. 2:121-146.

Randall, J. E.

1967. Food habits of reef fishes of the West Indies. Stud.
Trop. Oceanogr. (Miami) 5:665-847.
REINTJES, J. W, AND J. E. KING.

1953. Food of yellowfin tuna in the central Pacific. U.S.
Fish Wildl. Serv., Fish. Bull. 54:91-110.

SENTA, T.

1967. Seasonal abundance and diurnal migration of alima
larvae of Squilla oratoria in the Seto Inland Sea. [In
Jpn., Engl, summ.] Bull. Jpn. Soc. Sci. Fish. 33:508-512.
SUNIER, A.

1917. The Stomatopoda of the collection "Visscherij-
station" at Batavia. Contrib. Faune Indes Neerl.
l(4):62-75.
WASS, M. L. (compiler).

1972. A check list of the biota of lower Chesapeake
Bay Va. Inst. Mar. Sci., Spec. Sci. Rep. 65, 290 p.

700

EGG AND LARVAL DEVELOPMENT OF THE SPOT,
LEIOSTOMUS XANTHURUS (SCIAENIDAE)'

Allyn B. Powell and Herbert R. Gordy^

ABSTRACT

The egg and larval development of the spot, Leiostomus xanthurus, was described mainly from
laboratory-reared specimens. Egg diameters averaged 0.80 mm and ranged from 0.72 to 0.87 mm. The
number of oil globules varied, but coalesced during development. Oil globule diameters of eggs with one
globule averaged 0.21 mm and ranged from 0.18 to 0.28 mm. Newly hatched larvae measured 1.6-1.7
mm standard length, had a single oil globule located at the posterior margin of the yolk sac, and were
inconspicuously pigmented. Late yolk-sac larvae developed a characteristic pigment pattern of a single
row of melanophores along the ventral midline that persisted throughout the larval period. An
important pigment pattern — embedded pigment at the anterior of the gut — was first observed in clear
and stained late flexion larvae (2.9 mm standard length). Vertebrae and anal fin pterygiophore counts
were considered useful in separating spot from other sciaenids. Vertebral counts (25) were established
by 4.6 mm standard length, and precaudal (lOi and caudal (15) vertebrae were recognized at 5.1 mm
standard length. Anal fin pterygiophores which numbered two fewer than the number of anal fin
elements were established at 6.3 mm standard length.

The spot, Leiostomus xanthurus (Lacepede), is a
commercially important sciaenid found along the
Northwest Atlantic and Gulf of Mexico coasts from
Massachusetts Bay to the Bay of Campeche
(Johnson 1978). Spot spawns in offshore waters
during late fall and early winter, throughout its
range (Hildebrand and Cable 1930; Nelson 1969).
The larvae are transported towards shore and into
estuaries which serve as nursery areas (Fahay
1975; Chao and Musick 1977).

The eggs and yolk-sac larvae of spot have not
been described. Pearson (1929) briefly described
larvae ranging from 7 to 15 mm. Hildebrand and
Cable ( 1930 ) described larvae in greater detail and
attempted to distinguish spot larvae from mor-
phologically similar larvae of Atlantic croaker,
Micropogonias undulatus (the generic name
change from Micropogon follows Chao 1978). Hil-
debrand and Cable (1934) summarized early life
history data for 13 species of sciaenids, including
spot, but the keys they prepared were limited since
the early developmental stages for many species
were unknown. Lippson and Moran (1974) and
Johnson (1978) summarized early life history

'Contribution No. 80-27B of the Southeast Fisheries Center
Beaufort Laboratory, National Marine Fisheries Service,
NOAA.

^Southeast Fisheries Center Beaufort Laboratory, National
Marine Fisheries Service, NOAA, Beaufort, NC 28516.

Manuscript accepted FebruaQf 1980.
FISHERY BULLETIN: VOL. 78, NO. 3, 1980.

studies on sciaenids and included previously un-
published illustrations useful in separating spot
and croaker larvae. Fruge and Truesdale (1978)
and Powles and Stender (1978) described devel-
opmental stages of spot larvae from the Gulf of
Mexico and the South Atlantic Bight. Fruge and
Truesdale provided comparative data useful for
separating larvae of spot from larvae of Atlantic
croaker, while Powles and Stender emphasized
characters useful in separating early sciaenid lar-
vae.

In this paper we describe the life history of spot
from egg to juvenile, using the dynamic approach
of Ahlstrom and Ball (1954). Our objective is to
provide descriptive information useful in identifi-
cation and classification, as patterns of larval
development and larval anatomical features may
provide keys to possible relations among groups
( Aprieto 1974). Furthermore, studies of variations
of these patterns and features could provide keys
to how environmental factors may affect larval
development.

METHODS

Spot used for spawning were collected from a
commercial long-haul seine in Back Sound off
Harkers Island, N.C., during their spawning mi-
gration to the ocean. Eggs were obtained from fish
using an induced spawning technique developed

701

FISHERY BULLETIN: VOL. 78. NO. 3

by Hettler et al.^ This technique allows for a vol-
untary release of ova by females injected with
human chorionic gonadotropin (HCG) and sperm
by uninjected males. The quality of eggs produced
by this technique is far superior to injecting HCG
and manually removing and mixing gametes. The
rotifer Brachionus plicatilis, cultured in the
laboratory, was used as food for spot larvae till
they were approximately 30 d old. Zooplankton
captured from the field and predominated by
copepod nauplii and copepodites were sporadically
included in their diets during this period. Newly
hatched Artemia nauplii were used as food for
larvae older than about 30 d. Eggs and larvae were
maintained at temperatures and salinities of ca.
20° C and ca. 30-35%o. Some advanced larvae and
juveniles were collected with a modified neuston
net (Hettler 1979) near Beaufort, N.C.

Two developmental series of larvae were used.
Specimens in the first series were used for compil-
ing morphometric data, describing pigment pat-
terns and illustrating larval stages. Those in the
second series were cleared with trypsin, stained
with a combination of alcian blue and alizarin red
according to Dingerkus and Uhler (1977), and
Taylor and Van Dyke"* and used for meristic
studies. Egg stages follow those described by
Ahlstrom and Ball (1954). The embryonic period
was divided into three stages: early (fertilization
to blastopore closure), middle (from blastopore clo-
sure until the tail twists out of the plane of the
embryonic axis), and late (from tail twisting to
hatching). Larval stages followed those described
by Ahlstrom et al. (1976). The larval period was
separated into the preflexion, flexion, and postflex-
ion stages associated with the development of the
caudal fin; the stages occurring before, during,
and after the upward fiexion of the notochord tip.
We also included a yolk-sac stage, which we be-
lieved should be treated separately.

Pterygiophore nomenclature followed Houde
and Potthoff (1976). Nominal, full complement
counts were taken from Johnson (1978), although
we obtained pectoral ray counts directly from 15
specimens (University of North Carolina; UNC

^'Hettler, W. F., A. B. Powell, and L. C. Clements.
1978. Laboratory induced spawning of spot, Leiostomus
xanthurus (Lacepedel. Annual Report of the Beaufort
Laboratory to the U.S. Department of Energy, p. 351-356.

••Taylor, W. R., and G, C. Van Dyke. 1978. Staining and
clearing small vertebraes for bone and cartilage study. Unpubl.
manuscr., 19 p. National Museum of Natural History, Washing-
ton, DC 20560.

563). Measurements from eggs and larvae pre-
served in 5% buffered Formalin^ are identified as
follows:

Standard length (SL) — in preflexion and flex-
ion larvae, the horizontal distance from the tip of
the snout to the tip of the notochord. In postflexion
larvae, from the tip of the snout to the base of the
hypural plate.

Preanus length — horizontal distance from the
tip of the snout to the posterior part of the anus.

Head length — horizontal distance from the tip
of the snout to the posterior margin of the otic
capsules in yolk-sac larvae and the horizontal dis-
tance from the tip of the snout to the opercular
margin in other larvae and juveniles.

Snout length — horizontal distance from the tip
of the snout to the anterior margin of the pig-
mented region of the eye.

Eye diameter — maximum horizontal width of
the pigmented eye.

Body depth — the vertical depth of the body
measured at the pectoral fin base exclusive of the
finfold.

RESULTS

Embryonic Development

General

Spot eggs are pelagic. The chorion was trans-
parent and unsculptured. The yolk was imseg-
mented, unpigmented, and the perivitelline space
narrow in live eggs. Oil globules were yellow. We
have obtained batches of eggs with almost all
single oil globules, almost all multiple oil
globules, or a gradient between these conditions.
Batches of eggs with single oil globules occurred
most commonly. When oil globules were multiple,
they were grouped together and not scattered
throughout the yolk. The maximum number of oil
globules observed was 12. Oil globules coalesced
during egg development and it appeared that only
one oil globule was present on newly hatched lar-
vae. Egg diameter averaged 0.80 mm and ranged
from 0.72 to 0.87 mm (N = 265). Oil globules, from
eggs with one oil globule, averaged 0.21 mm in
diameter and ranged from 0.18 to 0.28 mm (A'' =
86). The eggs hatched in about 48 h at 20° C.

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

702

POWELL and GORDY: EGG AND LARVAL DEVELOPMENT OF THE SPOT

Early Stage Eggs

Pigment was never observed on the embryo or
oil globule of early stage eggs. By the end of the
early stage, when the blastopore was reduced to a
small opening, optical vesicles were discernible,
there were no visible myomeres, and the oil
globule was situated adjacent to the blastopore,
slightly posterior to the tail.

Middle Stage Eggs

Pigment first appeared on the embryo and oil
globule during the middle stage (Figure lA).
Melanophores, which were mainly punctate, were
scattered on the dorsal and lateral surface. Pig-
ment was sparse or missing from the snout and on
the posterior one-fourth of the body and was never
present near the notochord tip. Melanophores ap-

peared to be most dense in an area about one-third
the body length from the snout. At the end of the
middle stage, dendritic melanophores were more
common and the pigment pattern was transitional
from that illustrated for middle and late stage
embryos (Figure 1). Also at this stage melano-
phores were relatively more dense on the dorsal
surface of the head just posterior to the eyes and
appeared to migrate laterally to form, eventually,
a longitudinal row of dorsolateral melanophores.
Initially, melanophores occurred on the posterior
surface of the oil globule, but by the end of the
middle stage they were located on the anterodor-
sal surface.

Late Stage Eggs

The embryos of late stage eggs developed a
characteristic pigment pattern ( Figure IB) similar

Figure l. — Eggs of Leiostomus xanthurus: A, middle stage; left, the anterior part of embryo, right, the
posterior part of embryo; B, late stage: left, the anterior part of embryo, right, the posterior part of embryo.

703

FISHERY BULLETIN: VOL. 78, NO. 3

to that of Atlantic mackerel, Scomber scombrus
(Berrien 1975). Melanophores on late stage eggs
were relatively more dendritic than on earlier
stage eggs. A row of dorsolateral melanophores on
each side of the body extended from the posterior
edge of the eyes posteriad. At about midbody,
melanophores scattered over the dorsal surface
disrupted this row of dorsolateral melanophores.
Additional melanophores, which formed a trans-
verse row across the head just posterior to the eyes
were commonly observed. In the head region, an-
terior to the eyes and on the posterior portion of
the body, melanophores were sparse. They were
never observed on the posterior portion of the body
near the notochord tip. Melanophores on the sur-
face of the oil globule were located anteriorly.

Larval Development
Body Proportions

Newly hatched larvae measured 1.6-1.7 mm SL.
A single oil globule was situated near the posterior
margin of the yolk sac. The anterior portion of the
body was arched over the yolk sac, but
straightened out at ca. 2.0 mm SL (Figure 2). The
yolk sac and oil globule were absorbed within 5 d
at 20° C.

Most body proportions changed gradually dur-
ing ontogeny except during very early develop-
ment, when abrupt changes were observed. At this
time, the head length, preanus length, body depth,
and snout length became proportionately greater
(Figures 3-5). On the other hand, the eye diameter,
relative to the head length, became propor-
tionately smaller with increasing body length
(Figure 5A).

The most striking change in body shape was the
development of the robust head which charac-
terizes sciaenid larvae (Lippson and Moran 1974).
This change, as revealed by an increase in the
head length to body length ratio, occurred during
the transition from the yolk sac to the preflexion
stage, a time when little increase in body length
occurred (Figure 3B).

Body proportions of larvae collected from the
South Atlantic Bight (Powles and Stender 1978)
and our laboratory-reared larvae are in good
agreement, except that laboratory-reared larvae
may be slightly more robust, especially those >7.0
mm SL. Fourteen percent of our laboratory-reared
larvae (>7.0 mm SL) and 60% of our laboratory-
reared juveniles ( >14.4 mm SL) had body depths
greater than the maximum (29.3%) reported by
Powles and Stender (1978).

B

Figure 2. — Newly hatched Leiostomus xanthurus: A, dorsal view; B, lateral view.

704

POWELL and GORDY: EGG AND LARVAL DEVELOPMENT OF THE SPOT

o

z

UJ

a
cc

<
o

z
<
I-
co

o

LU

o
cc

lU

40

30

20

10

0

60
50
40
30
20
10

A. Body depth

'x^\ •V-:

^\

.r

• s

X

1

X

J 1 I L

B. . Preanus length
o Head length

. . • ••

« * • • • •

<to o

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STANDARD LENGTH (mm)

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32

Figure 3. — Body proportions of Leiostomus xanthurus relative to the standard length: A, body depth; B, preanus length and head

length.

Fin Development (Table 1)

Rayed fins initiated development in the follow-
ing sequence: caudal, anal, second dorsal, first
dorsal and pectoral, and pelvic. The adult com-
plement of spines and rays was attained in the
following sequence: principal caudal rays (9 upper
+ 8 lower), anal (II, 12-13), second dorsal (I, 29-35),
first dorsal (IX-XI) and pelvic (1,5), secondary
caudal rays (6-8 upper and lower), and pectoral
(20-22).

A thickened area of tissue on the ventral side of
the notochord was the first indication of caudal fin
development (Figure 6). The rays began to form at
the middle of the fin and developed dorsally and
ventrally simultaneously. Principal caudal rays
developed rapidly. They were first visible at 4.6
mm SL and by 65.3 mm SL the adult complement
(9 upper -t- 8 lower), which is shared by all sci-

aenids, was reached. On the other hand, secondary
caudal rays were slow to form. All specimens
5=14.4 mm SL had a complete caudal fin.

Dorsal fin rays started to form near the middle
of the fin, between the 8th and 17th vertebrae, then
developed anteriorly and posteriorly simultane-
ously. Soft rays were first observed at 6.7 mm SL. A
full complement of second dorsal fin spines and
soft rays was attained at 8.8 mm SL. A full com-
plement of first dorsal fin spines was attained at
9.0 mm SL, and although the second dorsal on that
particular larvae had a ray count within the adult
range, the last soft ray was not formed. All speci-
mens ^10.8 mm SL had a complete dorsal fin. All
our specimens had a first dorsal fin of 10 spines.

Anal fin rays started to form near the middle of
the fin, between the 11th and 15th vertebrae, and
then developed rapidly anteriorly and posteriorly.
Soft rays were first observed at 6.3 mm SL and

705

FISHERY BULLETIN: VOL. 78, NO. 3

o

z

lU

o

<
o

z
<
I-
co

liJ
o
cc

LU
0.

15

10

5

0

A. Eye diameter

• •

• •

•
•
•

• •

•

•

1 . 1 ■ 1 1 1

1 1

1 1 1

. 1

■ »

B. Snout length

15

-

10
5

.i^X, >:•>••« :s.-.-

. •••

•

•

•

0

I 1 i -1 — 1 — 1 — 1^

1

1 1

. 1 .

_1

' 1

0 4 8 12 16 20 24 28 32

STANDARD LENGTH (mm)

Figure 4. — Body proportions o( Leiostomus xanthurus relative to the standard length: A, eye diameter; B, snout length.

I
I-

(D

Z
UJ

_l

Q

<

m

I

11.
O

UJ

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Q.

A. Eye diameter

40
30
20

^'5 •

•

*

•

•

•

10

-

--

1 1 1 1 1 1 1 1

' 1

1 1 1

1

■

1_

I

40

30

20

10

B. Snout length

-•• • <••

i

• /

•• \

J L

X

J I L

J.

J L

±

J I l_L

28

J.

1

32

8 12 16 20 24

STANDARD LENGTH (mm)

Figure 5. — Body proportions of Leiostomus xanthurus relative to the head length: A, eye diameter; B, snout length.

706

POWELL and GORDY: EGG AND LARVAL DEVELOPMENT OF THE SPOT

Table l. — Meristic data from cleared and stained larval and juvenile Leiostomus xanthurus. Standard lengths suffixed with W

indicate wild-caught specimens. All others are laboratory reared.

Dorsal Anal

Pelvic

Lett pec-

Principal

Secondary

Brancfiios-

Gill rakers (left first arch)

Standard

Epi-

Cerato-

Hypo-

length (mm)

fin

in

fin

toral fin'

caudal rays^

caudal rays^

tegal rays

branchlal

branchial

branchial

23
2.7
3.0

—

—

—

LF
LF
LF

—

—

—

—

—

—

—

—

—

—

3,7

—

—

—

LF

—

—

3

—

—

—

4.4

—

—

—

LF

—

—

5

—

—

—

46

—

—

—

LF

3 + 3

—

6

—

—

—

4,7

—

—

—

LF

—

—

6

—

—

—

5.1

—

—

Bud

LF

7 + 7

—

6

—

4

—

5.5

—

—

Bud

LF

7 + 7

—

6

—

4

—

5,5

—

—

Bud

LF

6+6

—

7

—

6

—

5.7

—

—

Bud

LF

8+7

—

6

—

6

—

63

—

6

Bud

LF

9+8

0+1

7

2

8

—

6.7

18

10

Bud

LF

9+8

1+1

7

1

8

—

68

14

7

Bud

LF

9+8

1+1

7

—

7

—

6.9

20

1,10

Bud

LF

9+8

1+2

7

2

8

—

7.9

23

1,11

Bud

LF

9+8

2 + 1

7

1

8

—

8.0

VIII, 1,23

1.13

Bud

4

9+8

2^2

7

1

9

—

8.2

IX, 1,26

1.12

1,3

7

9+8

2-2

7

3

11

—

8.4

IX, 1,27

1,12

1,3

7

9+8

3^3

7

2

10

—

8.8

VIII, 1,29

1,12

1.1

5

9+8

2 + 2

7

2

9

—

8.9

VIII, 1,28

1,12

1,2

5

9+8

3 + 2

7

2

9

—

9.0

X,l,29

1,13

1.5

10

9+8

3 + 3

7

1?)

(^)

C)

9.5

IX, 1,30

1,12

Bud

5

9+8

2 + 2

7

2

9

—

9.7

IX, 1.31

1,13

1,3

9

9+8

3-3

7

3

10

—

10.0

IX, 1.31

1.12

1,4

10

9+8

3 + 2

7

3

10

—

10.8W

X,l,31

1,12

1,5

14

9+8

4 + 4

7

5

12

—

12.9

X,l,31

1,13

1,5

15

9+8

5*5

7

5

13

—

14.4

X,l,30

1,12

1,5

18

9 + 8

6+6

7

6

13

1

14.4

X,l,30

1,13

1,5

20

9+8

7 + 7

7

7

13

3

15.0

X,l,30

1,13

1,5

19

9+8

6 + 6

7

6

13

1

16.0

X,l,30

1,12

1,5

22

9+8

8 + 8

7

8

13

4

16.6W

X,l,31

1,12

1,5

20

9+8

7 + 7

7

8

13

2

17. 7W

X,l,29

1,12

1,5

21

9+8

7+6

7

9

13

3

18. 5W

X.I, 31

1,12

1,5

21

9+8

7+7

7

7

13

4

19. 1W

X,l,31

1,12

1,5

21

9+8

8+7

7

9

13

4

19. 6W

X,l,29

1,12

1,5

21

9+8

7 + 7

7

9

13

4

20. 1W

X,l,30

1,13

1,5

20

9+8

7+7

7

9

13

4

21, 5W

X,l,31

1,12

1,5

22

9+8

7+7

7

8

13

5

48.0W

X.1.32

1,12

1,5

22

9+8

8 + 7

7

12

13

8

' LF designates larval fin.
^ Upper - lower.
^Damaged.

spines at 6.9 mm SL. All specimens &8.2 mm SL
had a completely developed anal fin.

The pelvic fin appeared as a bud at 5.1 mm SL.
All specimens 2=10.8 mm SL had a completely de-
veloped pelvic fin. The fin formula 1,5 is typical
among sciaenids.

The pectoral, the last fin to develop a full com-
plement of rays, persisted as a rayless blade for a
relatively long period. Rays began to appear at 8.0
mm SL at the dorsal position of the blade and then
developed ventrally. All specimens ^16.0 mm SL
had a complete pectoral fin.

Fin development, relative to body length of lar-
vae, collected from the South Atlantic Bight
(Powles and Stender 1978) was similar to fin de-
velopment of laboratory-reared larvae, but spot
larvae collected from the Gulf of Mexico (Fruge
and Truesdale 1978) began and completed fin de-
velopment at a much smaller size (Table 2). Rate of
fin development could be influenced by tempera-

TabLE 2. — The size (mm SL) when fins and associated struc-
tures begin and complete development for laboratory-reared spot
(this study), spot collected from the South Atlantic Bight ( Powles
and Stender 1978) and spot collected from the Gulf of Mexico
(Fruge and Truesdale 1978).

Fin or associated
structure

Begins formation

Powles Fruge

and and

Stender Truesdale This

(1978) (1978) study

Completes formation

Powles

and

Stender

(1978)

Fruge
and
Truesdale This
(1978) study

Notochord flexion
Caudal fin:

Principal rays

Secondary rays
Anal fin

pterygiophores
Anal fin
Dorsal fin:

Pterygiophores

Second

First
Pelvic fin bud
Pelvic fin
Pectoral fin

4.4

4.5
6.2

4.4
7.2

4.4
7.2
7.2
5.2

8.0
10.7

4-5

3
5

5

7

5-6

6

7

3.8

4.6
63

5.5
6.3

5.1
6.7
8.0
5.1
8.2
8.0

4.7

7.2

15.5

6.2

9.3

9.3

14.1

10.7
16.8

4-5

5
>10.7

8
9

7-9
>10.7

5.3

6.3
14.4

6.3
8.2

7.3

8.8

10.8

10.8
16.0

ture. Size at hatching, at least, has been show^n to
be influenced by incubation temperature (Laur-
ence and Rogers 1976).

707

FISHERY BULLETIN: VOL. 78, NO. 3

Figure 6. — Developmental stages oi Leiostomus xanthurus: A, 2.4 mm SL late yolk-sac larva; B, 2.6 mm SL pre-
flexion larva; C, 4.1 mm SL early-flexion larva; D, 5.2 mm SL postflexion larva; E, 8.0 mm SL postflexion larva.

708

POWELL and GORDY: EGG AND LARVAL DEVELOPMENT OF THE SPOT
Pter>'giophore Development and Arrangements

Fully developed spot had three predorsal bones
which did not support spines (Figure 7): One such
bone was located between the skull and first
neural spine, one between the first and second
neural spines, and one between the second and
third neural spines. They began to develop at 5.7
mm SL, anteroposteriorly, and the full comple-
ment was recognizable at 8.2 mm SL (Figure 8).

There were two fewer pterygiophores than dor-
sal fin elements (spines and soft rays) on fully
developed spot. The anteriormost pterygiophore
was associated with three spines (Figure 7). It was
secondarily associated with the first two spines
and serially associated with the third spine. All
other pterygiophores were serially associated with
one dorsal fin element and secondarily associated
with a preceding element.

Dorsal fin pterygiophores were first apparent at
5.1 mm SL between neural spines 9 through 14 and
development proceeded anteriorly and posteriorly
simultaneously (Figure 8). The adult complement
was achieved at 8.2 mm SL.

Although there was a variable number of dorsal
pterygiophores between neural spines (Table 3), a
nearly consistent pattern was observed (Figure 7).
The formula^

P/P/P+1/2/ 1/2/ 1/2/2/

12 3 4 5 6 7 6 9 10 1112 1314 1516 17 1819202122232425

— r — I r — I — 1 T 1 — 1 1 — r-

I I r r"

I I I r

rrrrrrrrr.

^ ^ T ^ VVrVrVrrVrVVVV--^

nrvnTrTTTTTT

5.1 mm SL

, .rrrrr^rc

'mms<;^,-^^,m^

.^,

rr/:r/:rrr/;r/^r/-r/^rmr

5.5 mm SL

T W'V \ \ \ \ \\ \ \ \\ '■! '" \ '" 'V 'V

\^:^:i;i^\.

5.7 mm SL

VN^JL^NiNiNiNi*

6.7 mm SL

' ' ' ' 'v 'v 'v -V\ \\ \ \\ \ \ \ \ \\ \ \\ \\ \\ \ \ ' ■"

OXnTTTTT

8.0 mm SL

^ N.N.V\^.NwN^^wV\. >8.2 mm SL

FIGURE 8. — Schematic representation of the development of
predorsal bones (unshaded), and dorsal and anal fin
pterygiophores ( darkened) in Leiostomus xanthurus.

*Each P represents a predorsal bone, each slant a neural spine
and the numerals indicate the number of pterygiophores be-
tween neural spines.

Pdl

Nsl

FIGURE 7. — Arrangement of predorsal bones, and the first 11
dorsal fin pterygiophores in relation to neural spines for Leio-
stomus xanthurus (19.6 mm SL). Spine Sll is the first spine of the
second dorsal fin. Ps3, represents the pterygiophore in serial
association with the third dorsal spine; Pr2, the pterygiophore in
serial association with the second ray of the second dorsal fin; SI,
the first spine on the first dorsal fin: Rl, the first ray on the second
dorsal fin; Nsl, the neural spine on the first centrum; and Pd, the
predorsal bones.

Table 3. — Frequencies of dorsal fin pterygiophores between
neural spines in 23 Leiostomus xanthurus (8.2-48.0 mm SL).

Neural

spine

number

No of pterygiophores
between neural spines

0 12 3 4

Neural

spine

number

No. of pterygiophores
between neural spines

0 12 3 4

2-3

23

—

12-13

—

—

19

4 —

3-4

—

1

22

— —

13-14

—

—

17

6 —

4-5

—

22

1

— —

14-15

—

—

10

13 —

5-6

—

1

22

— —

15-16

—

—

15

8 —

6-7

21

2

— —

16-17

—

—

11

12 —

7-8

23

— —

17-18

—

—

9

14 —

8-9

—

23

— —

18-19

—

—

2

21 —

9-10

—

1

20

2 —

19-20

—

1

—

16 6

10-11

—

—

21

2 —

20-21

11

9

2

— 1

11-12

—

—

13

10 —

occurred in 87% of our 23 specimens. We also ob-
served that in 96% of those specimens the an-
teriormost pterygiophore between neural spines 7
and 8 was serially associated with the last spine of
the first dorsal fin (Figure 7).

Fully developed spot had two fewer pterygio-
phores than anal fin elements. Like the dorsal fin,
the anteriormost anal fin pterygiophore was as-

709

FISHERY BULLETIN: VOL. 78. NO. 3

sociated with three elements (Figure 9). It was
secondarily associated with the first two spines
and serially associated with the first ray. All other
pterygiophores were serially associated with one
anal fin ray and secondarily associated with a pre-
ceding ray. In the largest specimen (48.0 mm SL) a
stay was associated with the last anal fin
pterygiophore.

The number of anal fin pterygiophores between
haemal spines was highly variable. The first
pterygiophore, however, always occurred, singly,
between the last precaudal vertebra (number 10)
and the first caudal vertebra (number 11) (Table 4).

Anal fin pterygiophores were first observed at
5.5 mm SL (Figure 8). Development began be-
tween haemal spines 3 and 4 and proceeded an-
teriorly and posteriorly simultaneously. Develop-
ment was rapid. The adult complement was
reached at 6.3 mm SL.

Table 4. — Frequencies of anal fin pterygiophores between
haemal spines in 30 Leiostomus xanthurus (5.7-40.8 mm SL).

Figure 9. — Arrangement of the first four anal fin pterygio-
phores in relation to haemal spines for Leiostomus xanthurus
(19.6 mm SL). Prl, pterygiophore in serial association with the
first anal fin ray; Hsll, the first haemal spine on the 11th cen-
trum; S, anal spine; R, anal ray.

Other Structures

Centra were not fully differentiated until ca. 9
mm SL, but the adult complement of vertebrae
(25, including urostyle) was determined from lar-
vae as small as 4.6 mm SL by counting combina-
tions of neural spines and myosepta (Figure 10 A).
Precaudal vertebrae (10) were differentiated from
caudal vertebrae (15) in larvae as small as 5.1 mm
SL (Figure lOB). The first caudal vertebra was
easily identified as its haemal spine was approxi-
mately three times longer than the preceding
parapophysis.

Haemal

spine

number

No of pterygiophores
between tiaemal spines

0 12 3

Haemal

spine

number

10-11 — 30 — — 14-15

11-12 19 10 1 — 15-16

12-13 — 9 21 — 16-17

13-14 — 1 29 — 17-18

No of pterygioptiores
between haemal spines

0 1

2 3

— 1
9 14

28 1
28 2
22 8

7 —

One important adult characteristic of the genus
Leiostomus is an entire preopercular margin. Spot
larvae and early juveniles, however, exhibited
preopercular, subopercular, and interopercular
spines (Figure 11). Preopercular spines formed
first (4.4 mm SL). They occurred in two rows, one of
weak lateral spines and one of stouter marginal
spines. Preopercular spines increased during on-
togeny, but juveniles eventually lost these spines.
Interopercular and subopercular spines are less
important characters for larval identification be-
cause they formed during the late larval period
(Figure 11). They also were lost during the early
juvenile stage.

Branchiostegal rays appeared early in develop-
ment and attained the adult complement (7),
shared by all sciaenids, at 6.3 mm SL (Table 1).

Spot have a high number of gill rakers among
sciaenids ( 29-36, Chao and Musick 1977), but since
the adult complement was not attained until a
large size was reached (Table 1), total gill raker
counts were not considered to be a good diagnostic
character. The full complement of gill rakers on
the ceratobranchial, however, was obtained at ca.
13 mm SL.

Pigmentation

Newly hatched larvae were inconspicuously
pigmented (Figure 2). An ill-defined row of faint
melanophores on the anterior portion of the body
extended from the anterodorsal surface of the
head to the ventrolateral surface of the trunk.
Posterior to the anus on the dorsal midline, there
were about two to five faint punctate melano-
phores. Faint melanophores occurred on the an-
terodorsal surface of the oil globule.

Shortly after hatching (ca. 1 d), a characteristic
pattern began to form on the body. Initially, on
almost all larvae, there was a faint dorsal and
ventral melanophore opposite each other, located
about midbody. In addition, there were other faint
melanophores which, initially, occurred mainly on
the dorsal midline. With larval growth, there were

710

POWELL and GORDY: EGG AND LARVAL DEVELOPMENT OF THE SPOT

4.6 mm SL

B

5.1 mm SL

Figure lO. — Parts of axial skeleton used in counting: (A) total vertebrae (only myosepta useful in counting vertebrae are shown) and
(B) precaudal and caudal vertebrae in Leiostomus xanthurus early larvae. Ns, neural spine; Hs, haemal spine; My3, myosepta
associated with the third neural spine; Ph, parhypural; Hy, hypural bone; Eps, epurals; Nc, notochord.

fewer dorsal melanophores and more ventral
melanophores. Finally, at the late yolk-sac stage
(Figure 6A) a characteristic body pigment pattern
was established (i.e., a single row of melanophores
along the ventral midline) that persisted through-
out the larval period.

Distinguishing characteristics of postyolk-sac
spot larvae have been reported (Fruge and Trues-
dale 1978; Powles and Stender 1978), but the size
or stage when spot larvae acquire these charac-
teristics has generally been unknown. After yolk-
sac absorption, there were five characteristic pig-

mented areas that developed in the region of the
head and abdomen (Figure 6B-E)

1. Embedded melanophores over the air bladder
and hindgut. They were observed on the
youngest preflexion larvae (2.3 mm SL).

2. A triangle on the ventral side of the abdomen
composed of a well-defined melanophore just
anterior to the anus and a faint melanophore at
each future pelvic fin base, although one was
lacking at times (see Lippson and Moran 1974
for illustration), This pattern was occasionally

711

LU

z

Q.
CO

CC
Hi
CQ

Z

41-
2

4-
2

4-
2

• • • • • •

•• • • •

J L

4-

2-

0 - ••••

• • • • • •

•••»'

• • • • ••

• • • • • •

— ••• •

J.

J.

J.

FISHERY BULLETIN: VOL. 78. NO. 3

— r—A/ — I

Subopercular
Spines

^

Interopercular
Spines

^

Preopercular

Spines
(marginal)

^

Preopercular
Spines
(lateral)

5 10 15 20 25

STANDARD LENGTH (mm)

^r

50

Figure ll. — Frequency of preopercular, interopercular, and subopercular spines in Leiostomus

xanthurus.

observed on preflexion larvae and on almost all
older larvae.

3. A well-defined melanophore at the cleithral
s5Tnphysis on the ventral side of the abdomen.
This melanophore first appeared on flexion lar-
vae (3.8 mm SL).

4. A melanophore at the lower jaw angle first ap-
peared on preflexion larvae (2.6 mm SL).

5. Embedded pigment at the anterior of the gut
between the left and right cleithrum first be-
came apparent on flexion larvae (4.0 mm SL),
but were seen on cleared and stained late pre-
flexion larvae (2.9 mm SL).

Two other characteristic pigment patterns were
observed on the body: 1) a faint melanophore at
the base of the caudal fin first appeared on most
early flexion larvae (Figure 6C); then additional
melanophores were added (Figure 6D) which
eventually outlined the base of the caudal fin (Fig-

ure 6E), and 2) imbedded melanophores on the
perineural sheath appeared at ca. 6-7 mm SL
(Figure 6E).

Distinguishing Spot from Other Sciaenids

The eggs and larvae of most sciaenids are not
likely to occur with spot eggs and larvae since the
spawning seasons and localities of these sciaenids
and spot do not overlap (Guest and Gunter 1958;
Johnson 1978; Powles and Stender 1978). Spot,
which spawns in continental shelf waters during
the winter, share this spawning locality with
Cynoscion nothus, Equetus spp., Larimus fas-
ciatus, and Micropogonias undulatus. Of these
sciaenids, only the Atlantic croaker appears to
share the same spawning season with spot (the
spawming season oi Equetus spp. is unknown ). The
eggs and early preflexion larvae of Atlantic
croaker have not been described and, therefore,

712

POWELL and GORDY: EGG AND LARVAL DEVELOPMENT OF THE SPOT

cannot presently be separated from spot, but dis-
tinguishing characteristics useful in separating
older larvae are well documented (Fruge and
Truesdale 1978; Powles and Stender 1978). During
late fall and early spring, eggs and early larvae of
L. fasciatus and C. nothus could occur with those of
spot (Berrien et al. 1978; Powles and Stender
1978). The eggs of both these species are unde-
scribed, whereas their larvae bear no resemblance
to spot larvae (Powles and Stender 1978).

Meristic characters are useful in separating
spot larvae from those of other sciaenids (Table 5).
Flexion and older stage spot can be separated from
C. nothus, which may be the only species o^Cynos-
cion whose eggs and early larvae occur with spot,
by total vertebrae counts. Cynoscion nothus has
27, rarely 26 vertebrae (high for sciaenids); spot
has 25. Beginning at ca. 5 mm SL, spot can be
separated from all members of the genus Cynos-
cion inhabiting the western North Atlantic by the
number of precaudal vertebrae. Cynoscion spp.
have more precaudal vertebrae (13-15) than spot
(10).

The arrangement of predorsal bones and
pterygiophores can be important in determining
phylogenetic relationships (Kendall 1976) and in
distinguishing between closely related species
(Potthoff 1974; Berrien 1978; Butler 1979).

Table 5. — Meristic characters useful for separating spot larvae
from other sciaenids. Check ( ^ ) indicates nonoverlapping counts,
dash ( — ) indicates overlapping counts. Meristics were obtained
from cleared and stained specimens.

Meristic character and (in parenttiesi

IS)

the

size (mm SL) at which spot attained

the full complement

in this study

Precaudal

Anal fin'

Dorsal fin^

Total

+ caudal

pteryg-

pteryg-

vertebrae

vertebrae

iophores

iophores

Species

(4.6)

(5.1)

(6.3)

(7.3)

Bairdiella

chrysoura

—

—

y/

y/

Cynoscion

arenarius

—

y

y

C nebulosus

—

y

—

—

C. nothus

y

y

y

—

C. regalis

—

y

—

—

Larimus

fasciatus

—

—

y

—

Menticirrhus

americanus

—

—

y

y

M. littoralis

—

—

y

y

M. saxatilis

—

—

y

y

Micropogonias

undulatus

—

—

y

—

Pogonias

cromis

y

y

y

y

Sciaenops

ocellata

—

—

y

y

Stellifer

lanceolatus

—

—

/

/

'The full complement of anal fin spines and rays was attained at 8.2 mm SL.
^The full complement of dorsal fin spines and rays was attained at 10.8 mm
SL

Pterygiophores are important larval meristic
characters, since their full complement is attained
before accompanying spines and rays are formed.
Since spot have high anal fin ray counts among
sciaenids, then anal fin pterygiophore counts
would be of utmost importance in separating spot
larvae from other sciaenid larvae (Table 5i.

ACKNOWLEDGMENTS

We are most grateful to Howard Powles (Envi-
ronment Canada, Quebec, Canada) and William
R. Nicholson, Southeast Fisheries Center
Beaufort Laboratory, National Marine Fisheries
Service, NOAA, who reviewed an earlier draft of
this manuscript and offered valuable comments
and criticism, and to William Hettler (Southeast
Fisheries Center Beaufort Laboratory, National
Marine Fisheries Service, NOAA) for his valuable
contributions to our larval fish rearing program.
This research was supported by an interagency
agreement between the National Marine
Fisheries Service and the Department of Energy.

LITERATURE CITED

AHLSTROM, E. H., AND O. P. BALL.

1954. Description of eggs and larvae of jack mackerel
iTrachurus symmetricus) and description and abundance
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AHLSTROM, E. H., J. L. BUTLER. AND B. Y. SUMIDA.

1976. Pelagic stromateoid fishes (Pisces, Perciformes) of
the Eastern Pacific: kinds, distributions, and early life
histories and observations on five of these from the
Northwest Atlantic. Bull. Mar. Sci. 26:285-402.

APRIETO, V. L.

1974. Early development of five carangid fishes of the Gulf
of Mexico and the south Atlantic coast of the United
States. Fish. Bull.. U.S. 72:415-443.

BERRIEN, P. L.

1975. A description of Atlantic mackerel. Scomber scom-
brus, eggs and early larvae. Fish. Bull., U.S. 73:186-192.

1978. Eggs and larvae of Scomber scombrus and Scomber
japonicus in continental shelf waters between Mas-
sachusetts and Florida. Fish. Bull., U.S. 76:95-115.

berrien, p l., m. p f.\h.ay, a. w. kendall, jr., and w. g.
Smith.

1978. Ichthyoplankton from the KV Dolphin survey of Con-
tinental Shelf waters between Martha's Vineyard, Mas-
sachusetts and Cape Lookout, North Carolina, 1965-
1966. U.S. Natl. Mar. Fish. Serv., Northeast Fish. Cent.,
Sandy Hook Lab., Tech. Ser Rep. 15, 152 p.

BUTLER, J. L.

1979. The nomeid genus Cubiceps (Pisces) with a descrip-
tion of a new species. Bull. Mar Sci. 29:226-241.

CHAD, L.N.

1978. A basis for classifying western Atlantic Sciaenidae

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(Teleostei: Perciformes). U.S. Dep. Commer, NOAA
Tech. Rep. NMFS Circ. 415, 64 p.
Chad, L. N., and J. A. Musick.

1977. Life history, feeding habits, and functional morphol-
ogy of juvenile sciaenid fishes in the York River estuary,
Virginia. Fish. Bull., U.S. 75:657-702.
DINGERKUS, G., AND L. D. UHLER.

1977. Enzyme clearing of alcian blue stained whole small
vertebrates for demonstration of cartilage. Stain
Technol. 52:229-232.

FAHAY, M. p.

1975. An annotated list of larval and juvenile fishes cap-
tured with surface- towed meter net in the South Atlantic
Bight during four RV Dolphin cruises between May 1967
and February 1968. U.S. Dep. Commer, NOAA Tech.
Rep. NMFS SSRF-685, 39 p.

FRUGE, D. J., AND E M. TRUESDALE.

1978. Comparative larval development oi Micropogon un-
dulatus and Leiostomus xanthurus (Pisces: Sciaenidae)
from the northern Gulf of Mexico. Copeia 1978:643-
648.

Guest, W. C, and G. Gunter.

1958. The seatrout or weakfishes (genus Cynoscion) of the
Gulf of Mexico. Gulf States Mar. Fish. Comm., Tech.
Summ. 1, 40 p.
HETTLER, W. F.

1979. Modified neuston net for collecting live larval and
juvenile fish. Prog. Fish-Cult. 41:32-33.

HILDEBRAND, S. F, AND L. E. CABLE.

1930. Development and life history of fourteen teleostean
fishes at Beaufort, N.C. Bull. U.S. Bur Fish. 46:383-
488.
1934. Reproduction and development of whitings or king-
fishes, drums, spot, croEiker, and weakfishes or sea trouts,
family Sciaenidae, of the Atlantic coast of the United
States. Bull. U.S. Bur. Fish. 48:40-117.

HOUDE, E. D., AND T. POTTHOFF.

1976. Egg and larval development of the sea bream Ar-
chosargus rhomboidalis (Linnaeus): Pisces, Sparidae.
Bull. Mar Sci. 26:506-529.
JOHNSON, G. D.

1978. Development of fishes of the Mid-Atlantic Bight, vol.
4. U.S. Fish. Wildl. Serv., Biol. Serv Program, Wash.,
D.C.,314p.
KENDALL, A. W., Jr.

1976. Predorsal and associated bones in serranid and
grammistid fishes. Bull. Mar Sci. 26:585-592.

Laurence, G. C, and C. a. Rogers.

1976. Effects of temperature and salinity on comparative
embryo development and mortality of Atlantic cod (Gacfus
morhua L.) and haddock (Melanogrammus aeglefinus
(L.)). J. Cons. 36:220-228.
LIPPSON, A. J., AND R. L. MORAN.

1974. Manual for identification of early developmental
stages of fishes of the Potomac River Estuary. Md. Dep.
Nat. Resour, Baltimore, 282 p.
Nelson, W. r.

1969. Studies on tlie croaker, Micropogon undulatus Lin-
naeus, and the spot, Leiostomus xanthurus Lacepede, in
Mobile Bay, Alabama. J. Mar. Sci. (Ala.) 1:4-92.

Pearson, J. C.

1929. Natural history and conservation of redfish and
other commercial sciaenids on the Texas coast. Bull.
U.S. Bur. Fish. 44:129-214.
POTTHOFF, T

1974. Osteological development and variation in young
tunas, genus Thunnus (Pisces, Scombridae), from the At-
lantic Ocean. Fish. Bull., U.S. 72:563-588.
POWLES, H., AND B. W. STENDER.

1978. Taxonomic data on the early life history stages of
Sciaenidae of the South Atlantic Bight of the United
States. S.C. Mar Resour. Cent. Tech. Rep. 31, 64 p.

714

BOMOLOCHID COPEPODS PARASITIC ON THE EYES OF
INDO-WEST PACIFIC CLUPEID FISHES

Roger Cressey and Hillary Boyle Cressey'

ABSTRACT

Three genera of bomolochid copepods (Pumiliopes, Pumiliopsis,Pseudorbitacolax) parasitic on the eyes
of Indo-West Pacific clupeid fishes are redefined. Pseudorbitacolax fimbriatus new species is described,
Pseudorbitacolax varunae i Bennet) is redescribed, Orbitacolax nudus Cressey and Boyle is transferred
to the genns Pseudorbitacolax, Pumiliopsis emarginatus Cressey and Boyle is placed in synonymy with
Pumlliopsis sardinellae (Bennet), and Pumiliopes capitulatus Cressey and Boyle is placed in synonymy
with Pumiliopes jonesi (Bennet). Included also is a key to the genera of bomolochid copepods parasitic
on the eyes of Indo-West Pacific clupeids and scanning electron micrographs of three species.

In 1973 we described five new bomolochid copepods
collected from the eyes of Indo-West Pacific clupeid
fishes housed in the Smithsonian (USNM) collec-
tions. Since then we have collected more copepods
(including one new species) from clupeids in the
collections of the Museum of Comparative Zoology
at Harvard University (MCZ) and the British
Museum (Natural History) (BM).

Examination of these additional collections
(Table 1) enabled us to redescribe the three genera
of bomolochids (Pumiliopes, Pumiliopsis,
Pseudorbitacolax) parasitic on the eyes of Indo-
West Pacific clupeid hosts, to transfer Orbitacolax
nudus Cressey and Boyle to the genus Pseudor-
bitacolax Pillai, and to place Pumiliopsis emar-
ginatus Cressey and Boyle in synonymy with
Pumiliopsis sardinellae (Bennet), and to place
Pumiliopes capitulatus Cressey and Boyle in

'Department of Invertebrate Zoology, Smithsonian Institu-
tion, Washington, DC 20560.

Table l. — Indo-West Pacific clupeids and the copepods parasitic
on their eyes.

Host

Parasite

Anodontostoma chacunda

Pseudorbitacolax varunae

Clupanodon punctatus

Pumiliopes jonesi

Herklotsichthys displonotus

P. /ones!

H. punctatus

Pseudorbitacolax nudus

Sardinella albetla

Pumiliopsis sardinellae

S. bulan

P. sardinellae

S. fimbriata

Pumiliopes squamosus

Pumiliopsis sardinellae

Pseudorbitacolax fimbriatus

S. lussieui

Pumiliopes squamosus

Pumiliopsis sardinellae

S sirm

P plautus

S zunasi

Pumiliopes squamosus

Manuscript accepted December 1979.
fishery BULLETIN: VOL. 78, NO. 3, 1980.

synonymy with Pumiliopes jonesi (Bennet). This
paper also includes scanning electron micro-
graphs of some species and a summary of the re-
sults of our later collections.

Key to the Genera of

Female Bomolochids Parasitic on

the Eyes of Indo-West Pacific

Clupeid Fishes

la. Legs 2-4 exopods 2 -segmented 2

lb. Legs 2-4 exopods 3-segmented

Pseudorbitacolax

2a. Legs 2-4 exopod last segment with

barbed or serrate spine Pumiliopsis

2b. Legs 2-4 exopod last segment with smooth,

clawlike spine Pumiliopes

Pseudorbitacolax Pillai 1971

Diagnosis. — Bomolochidae. Female: Body dor-
soventrally flattened. Rostrum rounded or
bilobed. Abdomen 2- or indistinctly 3-segmented.
Caudal rami each with one long, five short setae.
First antenna with no modified setae. Last seg-
ment of second antenna with few to many hook-
lets, four hooked spines, and two setae terminally.
Maxilliped claw with no outer accessory process.
Legs 1-4 biramous. Leg 1 flattened, rami
2-segmented. Rami of legs 2-4 3-segmented, last
segment of exopods each with apical barbed or
serrate spine. Second endopod segment of leg 2
with two inner setae. Second endopod segment of
legs 3 and 4 each with one inner seta.

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FISHERY BULLETIN: VOL. 78, NO. 3

Male. — Rostrum slightly produced, broader than
long. Thoracic segments each slightly narrower
than preceding segment. Genital segment longer
than broad. Abdomen 2 -segmented. Caudal rami
each with one very long and five shorter setae.
First antenna extending beyond margins of
cephalothorax, with numerous long slender setae.
Second segment of maxilliped ornamented on
inner surface with numerous small, knoblike
spinules, one long seta, and a row of short
spinules; terminal segment in focm of a claw
armed with stout teeth along entire inner margin
apposing second segment. Legs 1-4 biramous, rami
3-segmented except endopod of leg 4 2-segmented.
Leg 1 endopod flattened. Second endopod segment
of legs 2 and 3 each with two inner setae.

Type-species . — Pseudorbitacolax varunae (Bennet
1966).

Remarks. — In placing two more species in this
genus we have been able to modify Pillai's (1971)
original generic diagnosis, especially with regard
to the size and shape of the rostrum and the first
maxilla. As with. Pumiliopsis, the structure of the
rostrum is a specific rather than a generic charac-
ter. The three setae of the first maxilla are of vari-
able lengths rather than all small as stated by
Pillai.

Our diagnosis of the male is based on a single,
damaged specimen of Pseudorbitacolax fimbriatus
and, as such, must be considered tentative until
additional material is collected.

Pseudorbitacolax fimhriatus
new species (Figures 1-17)

Material examined. — Two collections containing 3
916 (holotype 9 USNM 173021, allotype 6 USNM
173022, two paratype 9 USNM 173023) from the
eyes of two SardineUa fimbriata (BM 1972.9.5.22,
BM 1972.9.5.25) from New Guinea.

Female. — Body form as in Figure 1. Total length
3.66 mm, greatest width 1.60 mm (measured at
widest part of cephalothorax). Cephalothorax
length 1.42 mm and with lateral marginal mem-
branes. Rostrum (Figure 2) with bilobed tip, each
lobe gently rounded, with two dorsal hooks near
base; rostrum length 236 ^tm, width at base 206
jLtm. Genital segment (see Figure 1) wider than
long (389 X 601 yitm) with a greatly rounded pro-
cess at each outer distal corner. Abdomen

2-segmented: first segment wider than long (118 x
224 yum) without ornamentation; second segment
wider than long (94 x 200 ^tm) with two ventral
patches of scalelike spinules arranged in uneven
longitudinal rows (see Figures 3 and 4). Caudal
rami (Figure 3) longer than wide (82 x 53 yum);
each ramus with a patch of scalelike spinules
in rows (Figure 4) and six setae (longest seta
289 yum).

First antenna (Figure 5) 5-segmented: basal two
segments with 9 naked and 15 plumose setae; lat-
ter with broad, flattened plumosities ( Figure 6 ); an
aesthete present on each of last two segments.
Second antenna (Figure 7) with several rows of
minute spinules on third segment, four hooked
spines, and two setae distally. Labrum with two
large patches of scalelike spinules. Mandible,
paragnath, first maxilla, and second maxilla as in
Figure 8. Labium represented as a small, rounded,
hairy lobe posterior to mouth. Base of maxilliped
(Figure 9) posterior to oral area, armed with four
setae and a strongly curved hook without an acces-
sory process.

Legs 1-4 biramous, rami of legs 2-4 3-seg-
mented. Leg 1 (Figure 10) interpodal plate with
two patches of scalelike spinules; coxopod with
broad inner seta; basipod with two patches of
scalelike spinules; exopod first segment with outer
spine, second segment with two naked and seven
plumose setae; endopod first segment with outer
patch of scalelike spinules and inner plumose seta,
second segment with outer patch of scalelike
spinules and six plumose setae; outer edges of en-
dopod heavily hirsute. Basipod of leg 2 (Figure 11)
with large ventral patch of scalelike spinules and a
short dorsal seta; first segment of exopod with
patch of scalelike spinules (Figure 11a) covering
most of segment and one spine on outer distal
corner, second segment with outer spine and outer
patch of minute pointed spinules (Figure lib),
third segment with two outer spines, one barbed
terminal spine and three inner setae, outer por-
tion of segment with two distinct patches of
spinules similar to those on second segment; first
segment of endopod with minute, barely percepti-
ble inner seta and a large patch of scalelike
spinules, outer edge of segment fringed with short,
blunt hairs, second segment with two inner setae
and outer patch of scalelike spinules, outer edge of
segment fringed with short hairs, third segment
with two inner setae, one terminal spine and outer
to terminal patch of scalelike spinules. Basipod of
leg 3 (Figure 12) with dorsal seta, exopod and first

716

CRESSEY and CRESSEY: BOMOLOCfflD COPEPODS PARASITIC ON EYES OF CLUPEIDS

Figures 1-6. — Pseudorbitacolax fimbriatus. new species, female: 1. dorsal; 2, rostrum, ventral: 3, last abdominal segment and caudal

rami, ventral; 4, same, enlarged; 5, first antenna; 6, first antenna seta.

717

FISHERY BULLETIN: VOL. 78, NO. 3

Figures 7-10. — Pseudorbitacolaxfimbriatus, new species, female (continued): 7, second antenna; 8, mandible, paragnath, first maxilla,

second maxilla, labium; 9, maxilliped; 10, leg. 1.

718

CRESSEY and CRESSEY: BOMOLOCHID COPEPODS PARASITIC ON EYES OF CLUPEIDS

Figures 11-14. — Pseudorbitacolax fimbriatus, new species, female (continued): 11, leg 2, a, scalelike spinules on endopod and first
exopod segment, b, pointed spinules on exopod second and third segments; 12, leg 3; 13, leg 4; 14, leg 5.

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FISHERY BULLETIN; VOL. 78, NO. 3

segment of endopod similar to leg 2; second seg-
ment of endopod similar to leg 2 but with only one
inner seta, third segment with two inner to termi-
nal setae and one minute outer seta, outer portion
of segment with scalelike spinules. Leg 4 (Figure
13) basipod, exopod, endopod first and second seg-
ments similar to leg 3 except first segment of en-
dopod with short but well-developed inner seta;
third segment of endopod with three setae (middle
longest). Basal segment of leg 5 (Figure 14) with
dorsal seta, terminal segment with minute
spinules on outer proximal portion and four setae
as indicated in the figure. Area of leg 6 obscured by
egg sacs and not seen (usually present on
bomolochids as three setae on genital segment).

Male. — Body form as in Figure 15. Total length
1.14 mm, greatest width 0.44 mm (measured at
widest part of cephalothorax). Cephalothorax
more or less rounded (length 0.41 mm) with broad
rostrum. Genital segment longer than wide (247 x
177 (xm) indistinctly separate from segment bear-
ing leg 5. Abdomen 2-segmented: first segment
slightly longer than wide (65 x 59 /xm); second
segment (59 x 88 ^tm) with two patches of
scalelike spinules as in Figure 16. Caudal rami
(Figure 16) longer than wide (50 x 35 /um), each
with a single row of scalelike spinules and six
setae (longest seta 531 ixm).

Maxilliped (Figure 17) 4-segmented: second
segment with several uneven rows of small knob-
like processes, one seta, and an inner row of uni-
form spinules, proximal half of outer edge fringed
with long hairs; last segment in form of claw with
single small, toothlike process near proximal
inner corner, inner edge serrate along entire
length.

The single specimen examined was not dissect-
ed; therefore, detailed inspection of remaining
appendages was not possible. The following de-
scription is based on gross examination of the
specimen. First antenna 5-segmented with sev-
eral long graceful setae and an aesthete on each of
last two segments. Second antenna similar to
female except spinules on third segment propor-
tionately larger. Oral appendages similar to
female. Legs 1-5 similar to Pumiliopsis sardinel-
lae male with the following exceptions. Leg 2 en-
dopod third segment with at least three setae. Leg
3 endopod third segment of Pseudorbitacolax fim-
briatus damaged and examination not possible.

Etymology. — The specific name, fimbriatus, refers
720

to the specific name of the host fish iSardinella
fimbriata) from which this copepod was collected.

Remarks. — The female of this species can be sepa-
rated from P. uarunae and P. nudus on the basis of
the size and shape of the rostrum; in P. fimbriatus
it is slightly longer than broad, and in the other
two species it is broader than long. The genital
segment of P. fimbriatus has two prominent
rounded processes that are lacking in P . varunae
and P. nudus. Also, the maxilliped hook of P. fim-
briatus is much more strongly curved than in
either of the other two species.

Pseudorbitacolax varunae
(Bennet 1966) (Figures 18-29)

Syn: Bomolochus varunae Bennet 1966:295.

Material examined. — All copepods were collected
from the orbit of the host fish, Anodontostoma
chacunda: 8 9 from Manila, Philippine Islands; 4 9
from Kerala, India; 4 9 from Madras, India; 2 9
from Java; 8 9 from Sandakan Bay, Borneo.

Female. — Body form as in Figure 18. Total length
2.01 mm, greatest width 1.07 mm (measured at
widest part of cephalothorax); cephalothorax
length 0.88 mm. Rostrum (see Figure 21) wider
than long ( 106 x 601 ixm.) with no dorsal or ventral
hooks. Genital segment (Figure 19) wider than
long (147 X 253 fxm). Abdomen (see Figure 19)
3 -segmented, segmentation incomplete between
second and third segments; segments measure
(length X width) 88 xl53/>tm,53 x 153/xm,and76
X 141 fxra; third segment (Figure 20) with two
ventral patches of scalelike spinules. Caudal rami
(Figure 20) longer than wide (118 x 47 jxm), each
ramus with ventral patch of scalelike spinules and
six setae; longest seta 165 yum.

First antenna (Figure 21) 7-segmented with an
aesthete on each of the last two segments; plumose
setae similar to those of P. fimbriatus . Second an-
tenna (Figure 22) with 2 or 3 rows of conspicuous
hooked spinules on third segment, four hooked
spines and two setae distally. Mandible, parag-
nath, first maxilla, and second maxilla as in Fig-
ure 23; labrum with two large patches of scalelike
spinules. Maxilliped (Figure 24) hook only
slightly curved, with small, inner, toothlike pro-
jection.

Legs 1-4 biramous, rami of legs 2-4
3-segmented. Interpodal plate of leg 1 (Figure 25)

CRESSEY and CRESSEY: BOMOLOCHID COPEPODS PARASITIC ON EYES OF CLUPEIDS

Figures 15-19. — P seudorbitacolax fimbriatus, new species, male: 15, dorsal; 16, last abdominal segment and caudal rami, ventral; 17,
maxilliped. P seudorbitacolax varunae ( Bennet), female: 18, dorsal; 19, genital segment and abdomen, dorsal.

721

FISHERY BULLETIN: VOL. 78, NO. 3

jLo (jJf isf

Figures 20-25. — Pseudorbitacolax varunae (Bennet), female (continued): 20, last abdominal segment and caudal rami, ventral; 21,
first antenna and rostrum, ventral; 22, second antenna; 23, mandible, paragnath, first maxilla, second maxilla; 24, maxilliped; 25, leg 1.

722

CRESSEY and CRESSE Y: BOMOLOCHID COPEPODS PARASITIC ON EYES OF CLUPEIDS

Figures 26-29.— Pseudorbitacolax varunae (Bennet), female (continued): 26. leg 2; 27, leg 3; 28, leg 4; 29, leg 5.

723

FISHERY BULLETIN: VOL. 78, NO. 3

with two patches of scalelike spinules; coxopod
with broad, inner plumose seta and outer
sclerotized spine; basipod with several rows of
small, scalelike spinules above insertion of en-
dopod; exopod 2 -segmented, first segment with
outer, stout, flagellated spine, second segment
with three outer setiform spines and six terminal
to inner plumose setae; endopod 2-segmented, first
segment with inner seta, second segment with six
inner to terminal setae. Basipod of leg 2 (Figure
26) with ventral patch of scalelike spinules and
dorsal seta; first segment of exopod with large
patch of scalelike spinules along outer half of seg-
ment and setiform spine on outer distal corner;
second segment with 1 or 2 rows of stout spinules
along outer edge and one outer spine, third seg-
ment with row of stout spinules along outer edge,
two outer spines, one barbed terminal spine, and
three inner setae; first segment of endopod with
scalelike spinules along outer edge and short
inner seta, second segment with scalelike spinules
along outer edge and two inner setae, third seg-
ment small, with three setae (innermost longest).
Leg 3 (Figure 27) similar to leg 2 with following
exceptions: basipod lacks ventral patch of
scalelike spinules; second segment of endopod
with only one seta; outermost seta on endopod
third segment reduced to a setule. Leg 4 (Figure
28) similar to leg 3 except middle seta of endopod
third segment longest (about three times longer
than innermost). Leg 5 (Figure 29) basal segment
with dorsal seta; free segment slightly inflated
with one outer seta and three terminal setae (mid-
dle seta longest); no surface ornamentation vis-
ible. Leg 6 represented by three setae at area of
egg sac attachment (see Figure 19); setae reach to
about middle of first abdominal segment. Egg sacs
flattened in most specimens. (The egg sacs of
ovigerous females of bomolochids parasitic in the
orbit of their hosts are typically flattened. The egg
sacs of a few specimens of this new species were
more rounded.)

Male. — Unknown.

Remarks. — Our description of this species is in
general agreement with Pillai's (1971) redescrip-
tion with the following exceptions on specific
points. We found the segmentation between the
second and third abdominal segments less distinct
than did Pillai. Pillai failed to mention the or-
namentation on the ventral surface of the last
abdominal segment and caudal rami. We found the

first antenna to have one more segment than did
Pillai. The last segment of the second antenna has
four hooked spines and two setae rather than "5
claws and one stiff seta" as stated by Pillai. The
maxilliped hook has a small but noticeable inner
tooth. The basipod of leg 2 has a patch of scales not
present on the basipods of legs 3 and 4. While these
points are relatively minor, they aid in defining
the species.

P seudorbitacolax nudus
(Cressey and Boyle 1973) (Figures 30-35)

Syn: Orbitacolax nudus Cressey and Boyle
1973:6.

Originally reported from Herklotsichthys
punctatus from the Philippines. Additional collec-
tions of 4 9 from the same host species and locality
(BM 1933.3. n:15-16, BM 1933.3.11:17-18).

Our redescription oi P seudorbitacolax enabled
us to reassign Orbitacolax nudus to this genus.

Figure 30 (SEM photo) reveals the presence of
ridges on the surface of the dorsal cephalic hooks.
Figure 32 shows the surface of the tip of the second
maxilla to be covered with closely packed spinules.
Figure 34 shows the spinules on the exopod of leg 2
to be somewhat blunted. The spinules on the ter-
minal spines of legs 2-4 are hooklike (Figure 35)
and similar to those commonly found on the second
antenna.

Pumiliopsis Pillai 1967

Diagnosis. — Bomolochidae. Female: Body
dorsoventrally fiattened. Rostrum bilobed. Dorsal
cephalic hooks present; ventral rostral hooks may
or may not be present. Thoracic segments nar-
rower than cephalothorax. Abdomen elongate,
segmentation indistinct. Caudal rami each with
one long, five short setae. First antenna with no
modified setae. Second antenna typical of family,
terminal segment with several rows of booklets,
four hooked spines, and two setae. First maxilla
with three setae, middle seta more than twice the
length of other two. Maxilliped hook with no outer
accessory process, inner process may be present.
Legs 1-4 biramous, rami 2-segmented, except en-
dopod of leg 4 3-segmented. Leg 1 rami flattened.
Last exopod segment of legs 2-4 with barbed spine.

Male. — Rostrum slightly produced. Thoracic
segments each narrower than preceding segment.

724

CRESSEY and CRESSEY: BOMOLOCHID COPEPODS PARASITIC ON EYES OF CLUPEIDS

Figures 30-35.— Pseudorbitacolax nudus (Cressey and Boyle), female: 30, dorsal cephalic hook (xl,475); 31, tip of mandible,
paragnath, labium ( x2,150); 32, tip of second maxilla ( x5,000); 33, leg 2 basipod, exopod first segment ( xl.OOO); 34, leg 2 exopod first
segment, outer distal comer ( x5,000); 35, leg 3 exopod third segment spine ( x5,000).

725

FISHERY BULLETIN: VOL. 78, NO. 3

Genital segment longer than broad. Abdomen
2-segmented. Caudal rami each with one very
long and five short setae. First antenna extending
beyond margin of cephalothorax, segments with
numerous long, slender setae. Maxilliped second
segment with numerous teethlike spines and
large triangular process, last segment clawlike
with very fine teeth at tip only. Legs 1-4 biramous,
rami 3-segmented except endopod of leg 4
2-segmented. Leg 1 endopod flattened. Second en-
dopod segment of legs 2 and 3 each with two inner
setae.

Type-species. — Pumiliopsis sardinellae (Bennet
1964).

Remarks. — Pillai (1967) included in his generic
diagnosis "rostrum triangular, longer than broad."
While this is a prominent feature of the type-
species, P. sardinellae, the shape of the rostrum of
P. plautus is quite different. In other respects,
however, P. plautus agrees with Pillai's descrip-
tion of Pumiliopsis. Furthermore, Pseudor-
bitacolax fimbriatus new species has a rostrum
similar in shape to Pumiliopsis sardinellae; on the
basis of several other characters, however, the two
cannot be considered members of the same genus.
We therefore consider the shape and relative size
of the rostrum to be specific rather than generic
characters.

Pumiliopsis sardinellae
(Bennet 1964) (Figures 36-42)

Syn: Pumiliopsis emarginatus Cressey and
Boyle 1973:4

Bennet originally described this copepod from
the eye of Sardinella albella from Mandapam,
South India. In 1973 we reported it from S. per-
forata (= S. bulan) from the Philippines. Since
then we have collected the following: 12 9 from S.
albella (BM 1962.3.26:96-98, BM 1963.5.6:6-7, BM
1966.11.16:28-33, BM 1966.11.16:52-54) from
Mombasa, Aden, and Zanzibar; 17 9 1 d from S.
bulan (BM 68.6.9:6, BM 1966.11.16:56-70, MCZ
17632, MCZ 30372, MCZ 30811, MCZ 32182) from
Sarawak, Nosy Be, Batavia, Penang, Java, and the
Philippine Islands; 24 9 2 d from S. fimbriata (BM
84.5.15:27-28, BM 1965.7.5:11-13, BM 1965.7.5:15-
16, BM 1966.1.28:20, BM 1966.2.28:10-11, BM
1966.11.20:2, BM 1970.4.24:1-20) from Sri Lanka,
Thailand, Hong Kong, and Formosa; 4 9 from S.

jussieui (BM 1973.4.5:8-9) from Thailand. All ad-
ditional collections were from the eye of the host.

Since our description of P. emarginatus in 1973
we collected additional material from S. albella,
Bonnet's type host for P. sardinellae . This, along
with the minor differences noted between the two
copepods (segmentation of abdomen, setation of
leg 3 endopod of female, segmentation of legs 1-4 of
male) have led us to conclude that P. emarginatus
is synonymous with P. sardinellae. The differ-
ences noted could be due to the age or condition of
the specimens examined.

Scanning electron micrographs of the female of
this species reveals features not easily seen with
the light microscope. The rostrum (Figure 36) has
a ventral groove with a cluster of pores near each
outer basal margin. The cephalic "horns" (Figures
37-39) appear to be grooved ventrally. Figures 40
and 42 show the nature of the scales on the labrum
and leg 1.

Pumiliopsis plautus Cressey and
Boyle 1973 (Figures 43-46)

Syn: Pumiliopsis spathepedes Bennet 1975:156.

Originally described from Sardinella sirm and
S. leiogaster {= S. sirm) from the Philippines.
Bennet (1975) reported collecting 50 females from
the eyes of S. sirm from Tuticorin, India. We col-
lected an additional 6 9 from the same host (BM
1962.3.26:119-122, BM 1963.5.6:5, BM 1964.12.14:
180-185) from Zanzibar and Aden.

Bonnet's (1975) description of P. spathepedes is
essentially in agreement with that of P. plautus
(1973) with the following differences. Bennet did
not observe a paragnath; however, one is present.
He also failed to observe the tooth on the inner
margin of the maxilliped hook ( this process may be
difficult to detect with the specimen lying flat).
The rami of leg 1 are both 2-segmented rather than
3 as stated by Bennet, and he apparently mistook
the coxopod with its seta for the first endopod seg-
ment; the terminal exopod segment has three
spines and six setae rather than one spine and six
setae. The basipods and exopods of legs 2-4 are all
similar: the basipods each have one dorsal seta and
two ventral patches of spinules; the second seg-
ment of the exopods each have three stout outer
spines, one apical barbed spine, and two terminal
setae. The second endopod segment of leg 2 has two
small outer spinules and five terminal to inner
setae rather than the armature reported by Ben-

726

CRESSEY and CRESSEY: BOMOLOCHID COPEPODS PARASITIC ON EYES OF CLUPEIDS

Figures 36-41.— PumUiopsis sardinellae (Bennet), female: 36, rostrum, ventral (x500); 37, rostrum and dorsal cephalic hooks,
head-on view ( x260); 38, rostrum and dorsal cephalic hooks, head-on view ( x260); 39, dorsal cephalic hook, lateral view ( x500); 40,
scales on labrum ( xlO,OOOl; 41, maxilliped ( x400).

727

FISHERY BULLETIN: VOL. 78, NO. 3

yil

Figures 42-46. — PumiUopsis sardinellae (Bennet), female (continued): 42, scales on basipod of leg 1 ( x3,500). Pitmiliopsis plautus
Cressey and Boyle, female: 43, second antenna ( x 1,900); 44, booklets on second antenna ( x7,000); 45, maxilliped ( x500); 46, leg 4
endopod hairs ( x 10 ,000).

728

CRESSEY and CRESSEY: BOMOLOCHID COPEPODS PARASITIC ON EYES OF CLUPEIDS

net. The first endopod segment of leg 3 does have a
very short inner spinule. The last endopod seg-
ment of leg 4 has a small outer seta in addition to
the two mentioned by Bennet. Leg 5 has a total of
four setae on the terminal segment, one on the
midouter margin and one subterminally in addi-
tion to the two terminal setae Bennet noted.

The scanning electron micrographs of the
female indicate the hooklike nature of the or-
namentation on the second antenna (Figures 43,
44) and the bifurcate tips on the lateral hairs on
the endopod of leg 4 (Figure 46).

Pumiliopes Shen 1957

Diagnosis: — Bomolochidae. Female: Body dor-
soventrally flattened. Rostrum only slightly pro-
duced, rounded, broader than long. Thoracic seg-
ments bearing legs 2-5 free, each segment slightly
narrower than preceding one. Genital segment
wider than last thoracic segment. Abdomen
3-segmented, segmentation may be indistinct.
Caudal rami each with one long and five short
setae. Neither dorsal cephalic nor ventral rostral
hooks present. First antenna with no modified
setae. Second antenna 3-segmented, last segment
subdivided; subterminal portion with 1 or 2 rows of
booklets and one stout claw, terminal portion with
three hooked spines and two setae. First maxilla
with no or three short setae. Second segment of
second maxilla produced posteriorly. Maxilliped
hook with no accessory processes. Legs 1-4 bi-
ramous. rami 2 -segmented except leg 4 endopod
3-segmented. Leg 1 rami flattened. Last segment
of exopod of legs 2-4 with smooth, stout, clawlike
spine.

Male. — Unknown.

Type-species. — Pumiliopes opisthopteri Shen 1957.

Remarks. — In Shen's (1957) description of P. opis-
thopteri he reported no setae on the first maxilla,
and based on that report we have included it in the
generic diagnosis. This condition, however, is
unique in bomolochids; therefore, we consider
Shen's description of the first maxilla to be tenta-
tive until additional material of this species can be
examined.

Pumiliopes opisthopteri Shen 1957
Originally described from the "left eye" ofOpis-

thopterus tardoore from Yin-ku Bay, Hainan Is-
land, China. This copepod has not been reported
since and we did not recover specimens in our
examination of 24 specimens of the original host
species (including specimens from China).

Pumiliopes jonesi (Bennet 1967)

Syn: Bomolochus jonesi Bennet 1967:132.

Pumiliopes capitulatus Cressey and Boyle
1973:1.

Bennet originally described this copepod as
Bomolochus Jonesi from a collection of over 200
specimens collected from under the adipose eyelids
of Rastrelliger kanagurta (Scombridae) from
Calicut, India. In 1973 we collected the same
species of copepod, which we reported as P.
capitulatus, from the orbit of Clupanodon
punctatus (a clupeid). Our additional collections
from clupeids include 1 9 from C. punctatus (BM
93.4:21-28) from Hae-yoe Chi Kiang and 3 9 from
Herklotsichthys displonotus (BM 1967.11.13:1-9)
from Singapore.

We also recovered 35 females from the orbits of
the following scombrid fishes (all USNM collec-
tions): 17 from R . kanagurta from the Red Sea, Sri
Lanka, Madras, India, Philippine Islands, and
Java; 2 from R. faughni from the Philippine Is-
lands; 13 from Scomber japonic us from the Gulf of
Guinea, Mauritania, and Zanzibar; 3 from S. aus-
tralasicus from the Philippine Islands. We have
reported these scombrid collections in more detail
in a paper describing the parasitic copepods of
scombrid fishes (Cressey and Cressey 1980).

Due to the larger numbers of P. jonesi collected
from scombrids rather than clupeids, we consider
scombrids to be the preferred hosts of this copepod.

A comparison of Bonnet's (1967) description of
Bomolochus jonesi and our (Cressey and Boyle
1973) specimens and description of Pumiliopes
capitulatus indicates that they are the same
species and that Bonnet's species clearly belongs
in the genus Pumiliopes. We note the following
differences in details of the two descriptions.

Bennet found only four setae on each caudal
ramus; there are actually six, five apical (one long)
and one lateral. Bennet reported the first antenna
to be 6-segmented while we reported it to be
5-segmented, with the second segment relatively
long; the exact segmentation of this appendage is
often difficult to determine, but we agree on its
general ornamentation. The second antenna has

729

FISHERY BULLETIN: VOL. 78, NO. 3

one stout claw, three hooked spines, and two setae
rather than five digitate claws as reported by Ben-
net. Bennet, like Shen in describing P. opistho-
pteri, reported no setae on the first maxilla; there
are, however, three short setae present which may
be difficult to detect in some specimens. The sec-
ond segment of the second maxilla is produced
posteriorly, a character not apparent from Ben-
net's figure. The exopod second segment of leg 1
has six plumose setae and three small spinules
rather than seven plumose setae; the endopod sec-
ond segment has six rather than four plumose
setae. Bennet stated that the basipods of legs 2-4
are 2-segmented, these 2 segments are actually
the coxopod and the basipod; the basipod of leg 2
has a patch of scalelike spinules near the insertion
of the endopod. The second exopod segment of legs
2-4 each have small patches of spinules and weak
outer spines in addition to the apical clawiike
spine noted by Bennet. The "hairs" present on the
outer endopod margins of legs 2-4, as noted by
Bennet, are actually flattened, scalelike spinules.
The free segment of leg 5 is 1-segmented, not
2-segmented, and has one lateral and three termi-
nal setae. Leg 6 consists of three rather than two
setae on the genital segment.

Putniliopes sqtiamosns Cressey
and Boyle 1973

Originally described from Sardinella zunasi
from Nagasaki, Japan. Additional collections
include 4 9 from S. fimbriata (BM 1965.7.5:1-10)
from Hong Kong; 3 9 from S. fimbriata

(BM 1966.11.16:57-70) from Nosy Be, Madagascar;
13 9 from S. zunasi (BM 1905.6.6:13-22, BM
1971.2.8:151-153) from Japan; 2 9 from S.jussieui
(MCZ 30806) from Batavia. All copepods collected
from the orbit of the host fish.

LITERATURE CITED

Bennet, P S.

1964. On Bomolochus sardinellae sp. nov. (Copepoda, Cy-
clopoida) parasitic on Sardinella albella. J. Mar. Biol.
Assoc. India 6:84-88.

1966. Bomolochus varunae, a new species of parasitic
copepod from Anodontostoma chacunda (Hamilton
Buchanan). J. Mar Biol. Assoc. India 8:295-301.

1967. On Bomolochus jonesi sp. nov. parasitic on the eye of
the Indian mackerel Rastrelliger kanagurta. J. Mar.
Biol. Assoc. India 9:132-136.

1975. Pumiliopsis spathepedes sp. nov., a cyclopoid copepod
parasitic on the eye of Sardinella sirm. J. Mar. Biol.
Assoc. India 16:156-160.

Cressey, R. E, and H. Boyle.

1973. Five new bomolochid copepods parasitic on Indo-

Pacific clupeid fishes. Smithson. Contrib. Zool. 161:1-25.
CRESSEY, R. E, AND H. B. CRESSEY.

1980. The parasitic copepods of mackerel and tuna-like

fishes (Scombridae) of the world. Smithson. Contrib.

Zool. 311:1-186.
PILLAI, N. K.

1967. Redescription oiBomolochus sardinellae Bennet and

its transfer to Pumiliopsis gen. nov. (Copepodai. Crus-

taceana 12:249-256.
1971. On the transfer of Bomolochus varunae Bennet to

Pseudorbitacolax gen. nov. (Copepoda: Bomolochidaei. J.

Zoo). Soc. India 23:13-19.
SHEN, C.

1957. Parasitic copepods from fishes of China, Part I: Cy-

clopoida (1). Acta Zool. Sin. 9(41:297-327.

730

TEMPERATURE EFFECTS ON GROWTH AND YOLK UTILIZATION IN
YELLOWTAIL FLOUNDER, LIMANDA FERRUGINEA, YOLK-SAC LARVAE

W. HuNTTiNG Howell'

ABSTRACT

Embryos and yolk-sac larvae of yellowtail flounder, Limanda ferruginea , were incubated at 4°, 8°, 10°,
and 12° C. Embryos incubated at 8° and 10°C produced significantly larger yolk-sac larvae at hatching
than those incubated at 4° and 12° C. Yolk utilization rate was positively correlated with temperature.
Growth in length was fastest at 12° C. At yolk-sac absorption there was no significant difference in size
among larvae incubated at 8°, 10°, or 12° C. Efficiency of yolk utilization prior to hatching was 86.2,
76.8, 73.5, and 45.9^r for 12°, 10°, 8°, and 4° C. Overall yolk utilization efficiency from fertilization to
yolk-sac absorption was highest at 12° C (47.17( ), intermediate at 8° and 10° C (43.8 and 42.2% ), and
lowest at 4 ° C ( 29. 8^^ i . Efficiency decreased during the course of development at all four temperatures.

Based on the experimental results, it appears that sea temperatures between 8° and 12° C would have
little, if any, differential effect on larval size at yolk-sac absorption and therefore ability to survive. It
also appears that 4° C may be at or near the lower thermal limit for successful reproduction of southern
New England yellowtail flounder

The yellowtail flounder, Limanda ferruginea, is an
important commercial species in both the New
England and Canadian otter trawl fisheries. Yel-
lowtail flounder range from the Gulf of St. Law-
rence south to lower Chesapeake Bay (Bigelow
and Schroeder 1953). Royce et al. (1959) and Lux
( 1963) found that there are five relatively distinct
stocks within this range with little migration oc-
curring between them: Georges Bank, Cape Cod,
Nova Scotian, Newfoundland, and southern New
England.

Over the past 35 yr, landings from the southern
New England ground have fluctuated widely
(Royce et al. 1959; Lux 1964, 1969; Sissenwine
1974), with a sharp decline observed in the late
1940's not accompanied by the usual symptoms of
overfishing, i.e., a decline in average size, in-
creased percentage of young fish, or increased
growth rate. Royce et al., (1959) suggested the
decline was caused by a warming trend inducing a
temporary northeastward shift of the population
center away from the southern New England
grounds. Sissenwine (1974) demonstrated a sig-
nificant inverse relationship between water tem-
perature and equilibrium catch and recruitment.

The correlation between temperature and yel-
lowtail flounder abundance is an indication that
temperature may be causing fluctuations in the
fishery. This research was designed to investigate

'Department of Zoology, University of Rhode Island, Kingston.
K.I.; present address: Department of Zoologv, University of New-
Hampshire, Durham, NH 03824.

Manuscript accepted February 1980.
FISHERY BULLETIN: VOL. '78. NO. 3, 1980.

the effect of temperature on growth rate, size at
hatching and yolk-sac absorption, and yolk utili-
zation rate and efficiency. Most fisheries biologists
agree that early life history stages of fishes are the
most vulnerable due to their small size, poor
swimming ability, and susceptibility to rapid en-
vironmental changes (May 1974a). Because of
this, the total set of environmental parameters in
which these young fishes develop will largely de-
termine their collective success or failure, and
consequently their year-class strength. During
larval development, the time when the larva
changes from its endogenous source of food (yolk)
to exogenous feeding is a "critical period" in the
organism's life history (Hjort 1926; Marr 1956;
Toetz 1966; May 1974a). Particularly important to
successful initiation of exogenous feeding is the
size and condition of the larva (Blaxter and Hem-
pel 1963; Braum 1967). To a large extent size and
condition will depend on the efficiency with which
the organism is able to convert its yolk to larval
tissue. Any environmental variable that affects
conversion efficiency could affect larval size, and
consequently larval ability to begin feeding.
Taken over the entire population of larvae, year-
class strength could be significantly affected by
such environmental influences.

One such variable affecting yolk utilization
efficiency is temperature (e.g., May 1974b). Be-
cause temperature has been suggested as the
dominant environmental variable affecting yel-
lowtail flounder abundance and because other in-

731

FISHERY BULLETIN: VOL. 78. NO. 3

vestigators have found that temperature can
affect yolk utilization efficiency and thereby sub-
sequent size and feeding ability, the current
study examines the hypothesis that temperature
affects yolk utilization efficiency and size of yel-
lowtail flounder larvae.

METHODS

Adult yellowtail flounder were collected south-
east of Block Island, R.I., on 28 March 1979
aboard a commercial fishing vessel. They were
placed in a 680 1 tank periodically supplied with
running seawater and transported to the labora-
tory where they were held, four to a tank, in 286 1
aquaria supplied with a continuous flow of filtered
seawater.

To induce ripening, both sexes were anes-
thetized with tricaine methanesulfonate (MS-
222^) at a concentration of 1:20,000 g and injected
intramuscularly with 2.0 mg of carp pituitary dis-
solved in marine fish Ringer's solution per kilo-
gram of fish wet weight following Smigielski
(1979). Daily injections continued until spawning
occurred. Two females of 34.4 and 42.0 cm TL
(total length) were anesthetized and their eggs
manually stripped into a glass bowl containing
0.45 /Ltm filtered, ultraviolet-treated seawater
(34.0%o salinity, 10.5° C). The eggs were fertilized
with milt stripped from two anesthetized males
(34.5 and 33.0 cm TL). The fertilized eggs were
divided volumetrically among four 6 1 black plas-
tic pans containing seawater identical to that in
which fertilization had occurred. Twenty-five
lU/ml penicillin and 0.02 mg/ml streptomycin
were added to each pan as an antibiotic. These
pans were placed in temperature-regulating circu-
lation baths, gently aerated, and allowed to
equilibrate slowly to the test temperatures. The
four test temperatures chosen (4°, 8°, 10°, and 12°
C) were maintained at 4.5±0.6°, 8.7±0.6°,
10.3±0.5°, and 12.2±0.6° C (mean ± 1 SD). The
temperatures chosen encompass the range over
which most eggs and larvae of yellowtail flounder
have been collected in nature (Royce et al. 1959;
Colton 1972; Smith et al. 1975). Dissolved oxygen
and salinity ranged from 7.6 to 8.1 mg/1 and 33.0
to 34.0%o. Photoperiod was 12D:12L throughout
the experiment.

Measurements of egg and yolk diameters of a

random sample of unfertilized eggs ( n = 100) were
made by ocular micrometer, and egg and yolk vol-
umes calculated.

Prior to weighing, fresh unfertilized eggs were
rinsed in three changes of isotonic 0.99f (weight/
volume) ammonium formate to remove residual
saltwater. Mean dry weight and ash-free dry
weight of 390 eggs were determined to the nearest
1.0 ^tg, using a Perkin-Elmer electrobalance fol-
lowing the method of Laurence ( 1973). To deter-
mine the mean dry weight and ash-free dry weight
of yolk per egg it was necessary to subtract mean
dry and ash-free dry weight of the egg capsule
(zona radiata) from the two values. Twenty-six
capsules were removed from embryos just prior to
hatching and dry weights and ash-free dry
weights were determined by the method previ-
ously cited. Mean capsule weights were subtracted
from the mean values of dry weight and ash-free
dry weight of unfertilized eggs. The difference was
taken as the mean dry and ash-free dry weight of
yolk per egg. As both mean yolk weight and mean
yolk volume were known, it was possible to calcu-
late the dry weight and ash-free dry weight of yolk
for any given volume.

Random samples of 25 yolk-sac larvae were re-
moved from each temperature treatment begin-
ning 2 h after hatching, and continuing at 24-h
intervals until the experiments were terminated.
Yolk-sac measurements were made with an ocular
micrometer. The volume of the elliptical yolk sac
( V^g in cubic millimeters) was calculated from the
formula for a spheroid:

V.

ys

(77/6)L//2

(1)

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

where L is the length (millimeters) and H the
height (millimeters) of the yolk sac (Blaxter and
Hempel 1963 ). At each sampling period the length
from tip of snout to tip of notochord was measured
to the nearest 0.01 mm for each of the larvae sam-
pled using an ocular micrometer. The fish then
were rinsed in ammonium formate, and mean dry
weights and ash-free dry weights determined as
previously described.

Because of inherent variability in micromea-
surements, data were smoothed using linear re-
gression to relate ash-free dry weights of yolk-sac
larvae and yolk-sac volumes to numbers of hours
posthatch at all four temperatures. Ash-free dry
weights of yolk-sac larvae and yolk-sac volumes
were predicted using regression equations for each
24-h time interval and temperature. Predicted

732

HOWELL: TEMPERATURE EFFECTS ON YELLOWTAIL FLOUNDER

yolk-sac volume (cubic millimeters) then was mul-
tiplied by the calculated ash-free dry weight of a
cubic millimeter of yolk to yield the ash-free dry
weight of the yolk within the yolk sac. This value
was subtracted from the predicted ash-free dry
weight of the yolk-sac larvae to give the ash-free
dry weight of the larval tissue alone. The validity
of using the same ash-free dry weight (and caloric
value) of yolk throughout the yolk-sac stage has
been demonstrated by Lasker ( 1962).

Temperature effects on yolk utilization rate
were determined using analysis of covariance to
compare the slopes of the regression lines. The
relationship between larval notochord length and
hours posthatch was nonlinear. Growth curves,
linearized by logarithmic (natural) transforma-
tion of the time axis (hours posthatch), were com-
pared by analysis of covariance. Notochord
lengths, ash-free dry weights of yolk-sac larvae,
and yolk-sac volumes at time of hatching and
yolk-sac absorption for the four different tempera-
tures were compared using analysis of variance.
Where significant differences were found, the
Student-Newman-Keuls (SNK) test was used to
locate individual treatment differences.

Caloric values of yolk and larval tissue were
determined by wet oxidation following Maciolek
(1962). Ten samples of unfertilized ova were used
to determine the caloric content of yolk. Caloric
content of larval tissue was determined from
finely ground samples of larvae after total yolk
absorption. Three samples each were done from

Table l. — Summary of size, ash-free dry weight (AFDW), and
caloric value of unfertilized yellowtail flounder eggs.

n

Mean

SD

Egg diameter, mm

100

07566

00079

Yolk diameter, mm

100

.7324

.0126

Egg volume, mm^

100

2268

0071

Yolk volume, mm^

100

2059

.0105

Total AFDW, mg

390

.0127

0009

Egg capsule AFDW,

mg

26

0006

0001

'Yolk AFDW, mg

—

.0121

—

Cal g AFDW ot yolk

3

4,268.3

155.48

'AFDW, mg, per mm

3 yolk

—

.059

—

larvae reared at 8° and 12° C. No calorimetry was
attempted at 4° and 10° C since insufficient num-
bers of larvae were available at yolk-sac absorp-
tion.

Yolk utilization efficiency, expressed as a per-
centage, is defined as the ash-free dry weight of the
larva minus its yolk (or its caloric equivalent) at
time t, divided by the ash-free dry weight of yolk
(or its caloric equivalent) that had been used from
fertilization to time t. Details of this method are
described elsewhere (Toetz 1966; Laurence 1969).
Because variability was high in ash-free dry
weight measurements, it was not possible to calcu-
late meaningful daily efficiencies. Thus efficien-
cies were calculated at ony two points in time — at
hatching and at yolk-sac absorption. Efficiencies
also were calculated using ash-free dry weights of
larvae minus their yolk sacs and ash-free dry
weights of yolk utilized, as predicted by linear
regressions. These values were used to examine
trends in efficiency over time.

RESULTS

Data on size, ash-free dry weight, and caloric
value of unfertilized eggs from the females used in
this study are given in Table 1. The mean egg
diameter (0.75 mm) is slightly smaller than the
mean diameters of 0.9 and 0.88 mm reported by
Bigelow and Schroeder (1953) and Colton and
Marak.3

Incubation temperature affected both the
length and weight of yolk-sac larvae at time of
hatching, but not at yolk-sac absorption (Table 2).
At hatching, notochord length was significantly
longer in larvae incubated at 8° and 10° C than in
those incubated at 12° and 4° C (ANOVA, SNK,
P<0.05). Among the four temperatures, no sig-
nificant differences ( ANOVA, P>0.05) were found
between ash-free dry weights of entire yolk-sac

'Since the mean was derived by subtraction, no sample size or standard
deviation are given.

^Colton.J. B. Jr.andR. R. Marak. 1969. Guide for identify-
ing the common planktonic fish eggs and larvae of Continental
Shelf waters. Cape Sable to Block Island. U.S. Bur. Commer.
Fish., Biol. Lab., Woods Hole, Mass., Lab. Ref 69-9, 43 p.

Table 2. — Mean ± standard deviation of lengths, ash-free dry weights, and yolk-sac volume of yellowtail flounder reared at
four temperatures. Values connected by vertical lines are not significantly different (ANOVA. SNK,P>0.05).

At yolk-sac absorption

Tempera-
ture (" C)

Sample
size

Notochord length
(mm) at hatching

At hatching

Yolk-sac
volume (mm^)

4

25

2.117 = 0.213

0.1155 = 0.016

12

50

2.096±0.126

.1213 = 0020

8

25

2.494 = 0.138

0958 = 0012

10

35

2419 = 0.215

.0978 = 0.014

Ash-free dry weight of
yolk-sac larvae (mg)

0.0086 = 0.001
,0116=0 002
.0100 = 0.002
.0119 = 0.002

Ash-free dry weight of
yolk-sac larvae (mg)

0.0040 = 0.001
.0043=0.001
0042 = 0.001

Notochord
length (mm)

3.458=0,218
3.542 = 0,189
3,406=0.190

733

FISHERY BULLETIN: VOL. 78, NO. 3

larvae compared at hatching. Yolk-sac volumes,
however, differed significantly. Larvae reared at
12° and 4° C had significantly larger yolk volumes
than those reared at 8° and 10° C (ANOVA, SNK,
P<0.05). Larval tissue weight is taken as the dif-
ference between ash-free dry weight of the entire
yolk-sac larva and ash-free dry weight of yolk.
Since total ash-free dry weight was not signifi-
cantly different between the four temperatures, it
follows that the ash-free dry weight of the larval
tissue alone must be significantly greater in those
larvae reared at 8° and 10° C. This coincides with
the difference seen in length. At yolk-sac absorp-
tion there were no significant differences either in
length or ash-free dry weight of yolk-sac larvae
(ANOVA, P>0.05) for the three temperatures
where these variables were measured.

Notochord length increased with time after hatch-
ing (Table 3). Analysis of covariance revealed
that larvae incubated at 12° C grew significantly
faster than those at the other temperatures

(P<0.05). Larvae at 4° C grew at an interme-
diate rate that was significantly different (P<0. 05)
from fish in other treatments. No significant
difference (P>0.05) in growth rate was evident
between 8° and 10° C larvae. Fish in both of
these treatments exhibited the slowest growth
rates (P<0.05). Regression coefficients of ash-free
dry-weight of yolk-sac larvae and yolk-sac vol-
umes vs. hours posthatch were significantly
different (P<0.001) from zero (Table 3).

Ash-free dry weight of the larva minus its yolk
sac at a particular temperature and time was cal-
culated as the difference between the predicted
total ash-free dry weight and the predicted ash-
free dry weight of the yolk (Tables 4-7). Predicted
values indicate that embryo weight increases
linearly with time at all temperatures except 8° C
(Table 5) where it remains constant.

Temperature effects on yolk utilization rate
were examined by comparing the regression coef-
ficients of the four equations for decrease in yolk-

TabLE 3. — Predictive linear equations (Y = a + bX) derived from least squares linear fits of the yellowtail
flounder data. All equations are based on measurements taken every 24 h between hatching and yolk-sac
absorption. AFDW = ash-free dry weight, and In = natural logarithm.

Variables Y vs X and temperature (° C)

Sample
size

95% confidence
limit for a

95% confidence
limit for ti

Notoctiord lengtfi (mm) vs. In hours posttiatcti:

4

308

1 .6446

0- 1 1 92

0.27799

0 02564

0.81

8

228

2.2737

.0919

.21710

.02147

.85

10

195

2.2464

.0997

.20723

.02563

.83

12

225

1 .8852

,0660

.30749

-01681

.95

AFDW yolk-sac larvae (mg) vs. fiours postfiatch:

4

58

.0092

.0008

-.000021

.000005

.79

8

39

0103

.0009

-000035

000008

,86

10

28

.0106

.0016

■000046

.000016

.81

12

36

.0114

.0011

-000047

.000010

88

Yolk-sac volume (mm^) vs. hours posthatch:

4

308

.1139

.0028

-000432

000017

.95

8

203

0840

.0036

- 000584

000036

.94

10

170

.0931

.0034

-000822

000050

.95

12

200

.1068

.0054

-000899

.000067

.92

Table 4.-

—Predicted values of yo

Ik-sac larval

weight, yo

Ik-sac volume and

wei

and calculated efficiencies at 4° C. AFDW = ash-free dry weight.

Hours
posthatch

Yolk-sac larvae
(mg AFDW)

Yolk-sac volume
(mm^)

Yolk'
(mg AFDW)

Larval tissue^
(mgAFDW)

Yolk utilized^
(mg AFDW)

Efficiency*

2 0.0092

0.1131

0-0067

0.0025

0,0054

46.3

24 .0087

,1035

.0061

.0026

,0060

43.3

48 .0082

,0932

.0055

0027

,0066

40.9

72 .0077

.0828

.0049

0028

,0072

38.9

96 .0072

0724

.0043

0029

,0078

37.2

120 .0067

0620

.0037

.0030

,0084

35.7

144 .0061

.0516

.0030

.0031

,0090

34.4

168 .0056

.0413

.0024

.0032

,0097

33.0

192 .0051

.0309

,0018

0033

,0103

32,0

216 .0046

.0205

.0012

,0034

.0109

31-2

240 .0041

.0101

0006

0035

0115

30-4

264 .0036

0

0

,0036

0121

298

288 .0031

0

0

,0031

0121

25,6

'Yolk-sac volume times 0 059,

^Yolk-sac larvae minus yolk.

^0.0121 minus yolk

"Larval tissue divided by yolk utilized

times 100.

734

HOWELL: TEMPERATURE EFFECTS ON YELLOWTAIL FLOUNDER

Table 5. — Predicted values of yolk-sac larval weight, yolk-sac volume, weight, and caloric value, larval tissue weight
and caloric value, and calculated efficiencies at 8° C. AFDW = ash-free dry weight.

Hours
posthatcfi

Yolk-sac

larvae

(mgAFDW)

Yolk-sac
volume
(mm^)

Yolk'
(mg AFDW)

Larval

tissue^

(mg AFDW)

Yolk

utilized^

(mg AFDW)

Effi-
cienc/"

Caloric value
of yolk
utilized^

Caloric value
of larval
tissue*

Caloric
efficiency'

2

00102

0.0828

0.0049

0.0053

0.0072

73.6

0,0307

00167

544

24

.0094

.0670

.0040

0054

.0081

66.7

.0346

.0170

49.1

48

.0086

.0559

.0033

0053

.0088

60.2

.0376

.0167

44.4

72

.0078

.0419

.0025

0053

0096

55.2

.0410

.0167

40,7

96

.0069

.0279

.0016

0053

.0105

50.5

.0448

.0167

37.3

120

.0061

.0138

0008

0053

0113

46.9

.0482

0167

34.6

144

.0053

0

0

0053

0121

43.8

.0516

.0167

32 4

'Yolk-sac volume times 0,059.

^Yolk-sac larvae minus yolk

^0.0121 minus yolk

■•Larval tissue divided by yolk utilized times 1(X),

^Yolk utilized times 4,2683.

^Larval tissue times 3.6959.

'Caloric value of larval tissue divided by caloric value of yolk utilized times 100.

Table 6. — Predicted values of yolk-sac larval weight, yolk-sac volume and weight, larval tissue weight,
and calculated efficiencies at 10° C. AFDW = ash-free dr>' weight.

Hours
postfiatch

Yolk-sac larvae
(mgAFDW)

Yolk-sac volume
(mm^)

Yolk'
(mgAFDW)

Larval tissue^
(mg AFDW)

Yolk utilized^
(mg AFDW)

Efficiency^

2

0.0105

0.0915

0,0054

0.0051

0,0067

76,1

24

.0095

0734

.0043

.0052

.0078

67.0

48

.0084

0537

.0032

.0052

0089

584

72

.0073

.0339

.0020

OOS."?

,0101

52.5

96

.0062

,0142

.0008

.0054

0113

47.8

120

.0051

0

0

,0051

-0121

42.2

'Yolk-sac volume times 0,059,

'Yolk-sac larvae minus yolk,

^0 0121 minus yolk,

*' Larval tissue divided by yolk utilized times 100,

Table 7. — Predicted values of yolk-sac larval weight, yolk-sac volume, weight, and caloric value, larval tissue weight and
caloric value, and calculated efficiencies at 12° C. AFDW = ash-free dry weight.

Yolk-sac

Yolk-sac

Larval

Yolk

Calonc value

Caloric value

Hours

larvae

volume

Yolk'

tissue^

utilized^

Effi-

of yolk

of larval

Caloric

postfiatch

(mg AFDW)

(mm^)

(mg AFDW)

(mg AFDW)

(mg AFDW)

ciency"

utilized^

tissue^

efficiency'

2

0.0113

0 1050

0,0062

0,0051

0,0059

86-4

0-0252

00188

74,6

24

,0102

,0852

-0050

,0052

,0071

73.2

.0303

.0192

63.4

48

,0091

,0636

,0038

,0053

0083

63.9

.0354

.0196

55.4

72

0080

,0420

,0025

-0055

.0096

573

.0410

.0203

49.5

96

-0069

,0204

,0012

,0057

,0109

52,3

.0465

,0211

45.4

120

,0057

0

0

.0057

,0121

47-1

.0516

0211

409

'Yolk-sac volume times 0059,

^Yolk-sac larvae minus yolk,

^0,0121 minus yolk,

■■Larval tissue divided by yolk utilized 100 times,

^Yolk utilized times 4,2683,

^Larval tissue times 3,6959,

'Caloric value of larval tissue divided by caloric value of yolk utilized times 100.

sac volume (Table 3). Analysis of covariance
showed that the rate of decrease was related di-
rectly to temperature. All coefficients were sig-
nificantly different (P<0.05) with yolk utilization
being fastest at 12° C, followed by 10°, 8°, and
finally 4° C.

Efficiency was estimated as ash-free dry weight
of yolk converted into ash-free dry weight of larval
tissue at all four temperatures. Overall efficiency
was considered as the calculated efficiency at time
of yolk-sac absorption. Values were lowest at 4° C
(29.89'f) intermediate at 8° and 10° C (43.8 and
42. 27^), and highest at 12° C (47.1%) (Tables 4-7).

Efficiency in terms of calories of yolk converted
into calories of larval tissue was calculatecd at 8°
and 12° C (Tables 5 and 7). Estimates were ob-
tained by dividing the caloric value of larval tissue
at time t by the estimated caloric value of yolk
utilized to time t. Calories per milligram ash-free
dry weight of larval tissue at yolk-sac absorption
were 3.152±0.37 at 8° C and 3.696±0.23 at 12° C.
Analysis of variance indicated the two values were
not different (P>0.10). Efficiencies based on
caloric conversions were lower than those based on
ash-free dry weight. Larvae reared at 12° C still
ranked highest in overall efficiency (40.9%) with

735

FISHERY BULLETIN: VOL. 78, NO. 3

larvae at 8° C showing a somewhat lower overall
efficiency (32.4^7.).

Efficiencies calculated at hatching reflect the
efficiency with which yolk was converted to larval
tissue during embryological development. These
values were consistently higher than overall
efficiencies (Tables 4-7) and were similar in rank-
ing. Based upon ash-free dry weight conversions,
larvae at 12° C were most efficient (86.2%), fol-
lowed by those at 10° C (76.8%), at 8° C (73.5%),
and, last, at 4° C (45.9%). As for overall efficien-
cies, caloric efficiencies at hatching were lower
than those calculated on an ash-free dry weight
basis: 74.7% at 12° C and 54.3% at 8° C.

A decrease in efficiency with continuing devel-
opment was noted at all four temperatures (Tables
4-7).

DISCUSSION

Mean diameter of eggs used in this study were
slightly smaller than mean sizes reported by other
investigators (Bigelow and Schroeder 1953; Col-
ton and Marak footnote 3). Many variables can
effect egg diameter. Laurence (1969) and Alder-
dice and Forrester (1974) have demonstrated a
relationship between egg diameter and parental
size. Egg diameter has also been related to incuba-
tion temperature and salinity, as well as time from
fertilization (Alderdice and Forrester 1974; Al-
derdice et al. 1979). In addition, Blaxter and Hem-
pel (1963) found differences in egg diameter be-
tween stocks of herring. If any of these variables
affect egg size in yellowtail flounder, it appears
likely that the results found here may not be com-
parable with reported values.

Larvae incubated at the intermediate tempera-
tures (8° and 10° C) were significantly larger at
hatching than those incubated at the extremes (4°
and 12° C). This conflicts with data of Smigielski^
who found that mean length at hatching was inde-
pendent of temperature over a 6°-14° C range. One
reason for the different findings may be the time at
which measurements were taken. Since hatching
occurs over a period of about 12-36 h, depending on
the temperature, and since growth is rapid, the
mean size estimated will depend on the time mea-
surements were taken. Furthermore, Alderdice
and Forrester (1974) and Alderdice and Velsen
(1971) have shown that larval size at hatching can

••Alphonse Smigielski, Fisheries Biologist, National Marine
Fisheries Service, NOAA, Narragansett, RI 02882, pers. commun.
November 1979.

be different among fish in the same treatment
depending on hatching time.

The implications of larval size at hatching may
not be great relative to size at yolk-sac absorption.
Upon hatching there is no need for larvae to feed
actively due to their endogenous yolk supply. Be-
cause larger size confers an advantage in swim-
ming ability, which in turn affects feeding ability
(Hunter 1972), it follows that the size attained at
yolk-sac absorption, when the larvae change to
exogenous feeding, is more critical than the size at
hatching. Analysis of growth rates from hatching
to yolk-sac absorption indicate that larvae at 12° C
grew significantly faster than those at other tem-
peratures. Because of this, 12° C larvae attained a
size equal to that of 8° and 10° C larvae by yolk-sac
absorption. Because of the similarity in size' of
larvae reared at these three temperatures, it is
presumed that they would be equally successful in
capturing prey. Although no data were available
for 4° C larvae at yolk-sac absorption, their small-
er size at hatching, combined with their low con-
version efficiency, should result in their being sig-
nificantly smaller at yolk-sac absorption. The
added fact that all larvae in the 4° C treatment
died shortly before yolk-sac absorption makes it
probable that 4° C is at, or near, the lower tempera-
ture limit for successful reproduction in the south-
ern New England yellowtail flounder stock.

Yolk utilization rate, measured by decrease in
yolk-sac volume over time, also was affected sig-
nificantly by temperature; the higher the temper-
ature, the more rapidly yolk was used. This is to
be expected since rate of yolk (food) consumption,
is one measure of the rate of physiological func-
tions (metabolism and growth) which are tem-
perature-dependent in most ectotherms (Brett
1970). A number of previous studies have shown
similar results (e.g., Blaxter 1956; Ryland and
Nichols 1967; Fluchter and Pandian 1968).

Calculated efficiencies indicate the number of
calories incorporated, or the amount of yolk con-
verted into larval tissue in a particular time inter-
val. The remaining calories, or weight, are lost
through the metabolic processes of yolk transfor-
mation, maintenance, activity, and excretion. In-
cubation temperatures in this study were observed
to affect both rate of growth and rate of yolk utili-
zation. Since the calculated efficiency will depend
on the relationship between these two rates, a
change in either rate, relative to the other, will be
reflected in a change in efficiency. Because tem-
perature affects both these rates, it is not surpris-

736

HOWELL: TEMPERATURE EFFECTS ON YELLOWTAIL FLOUNDER

ing that several investigators have found a rela-
tionship between incubation temperature and
yolk utilization efficiency. Laurence (1973) found
that overall efficiencies for tautog, Tautoga onitis,
were 36.3, 25.5, and 25.89c for 16°, 19°, and 22° C.
Ryland and Nichols (1967) found that for plaice,
Pleiironectes platessa, efficiencies were roughly
35-407r at lower temperatures (2.5°-5.0° C)
and 43-579^ at higher temperatures (6.5°-8.5° C).
Working with the Atlantic salmon, Salmo salar,
Hayes and Pelluet ( 1945) found that efficiency was
low (429f ) at temperatures of 0°-5° C, and in-
creased linearly with increasing temperature to
607^ at 16° C.

The overall efficiencies in this study, based upon
ash-free dry weights, were 43.8, 42.2, and 47.1%
for 8°, 10°, and 12° C. The similarity of these values
is an indication that within this temperature
range, mechanisms are available whereby the in-
creased metabolic demands of the larval tissue,
caused by the higher temperatures, are balanced
by an increased transfer of energy from the yolk
for the building of tissues. The fact that increasing
growth rate with temperature is accompanied by
an increased rate of yolk utilization lends support
to this hypothesis. Blaxter and Hempel ( 1966) also
point out that overall efficiencies can be similar at
different temperatures if the interrelationship be-
tween rate of rise in metabolic requirements and
reduction in development time are balanced over a
temperature range. Wood (1932) reported that
yolk utilization efficiency in trout was indepen-
dent of temperature between 7° and 12° C. Marr
(1966), however, after recalculating the data, con-
cluded that efficiency was actually higher at 10° C.
Johns and Howell (1980) found that efficiencies
were similar in summer flounder, Paralichthys
dentatus, larvae at 16° and 21° C. They noted that
the ratio of yolk needed for metabolism to yolk
converted to tissue remained constant at the two
temperatures, causing efficiencies to be similar.
Although none of the investigations on yolk utili-
zation efficiency demonstrates temperature inde-
pendence, several of the studies show, over a par-
ticular section of the temperature range tested,
that efficiencies are quite similar. These include
work on S. salar (Hayes and Pelluet 1945), Clupea
harengus (Blaxter and Hempel 1966), and T. onitis
(Laurence 1973).

Larvae incubated at 4° C did not survive to
yolk-sac absorption; however, 288 h after hatch-
ing, when approximately 2% of the yolk remained,
the calculated efficiency was 25.6%. This low

value indicates that the energy within the yolk
was being largely used for metabolic demands
other than growth of larval tissue. The relatively
low efficiency of yolk conversion at 4° C adds
further support to the conclusion that 4° C is a
suboptimal temperature for this stock of yellow-
tail flounder.

A reduction in efficiency as development pro-
ceeded was noted at all four temperatures. Blaxter
and Hempel ( 1966) noted such a decrease in her-
ring larvae and concluded that the reduction was
due to the relatively higher metabolic demands of
heavier larvae. Although no metabolic mea-
surements were made in this study, it is suspected
that the explanation offered by Blaxter and Hem-
pel ( 1966) applies to these results.

The hypothesis that a deficit in food energy can
be caused by yolk exhaustion prior to initiation of
exogenous feeding has received considerable at-
tention. Such a deficit has been demonstrated by
Lasker (1962) for the Pacific sardine, Sardinops
caerulea. Laurence (1969, 1973) working with
largemouth bass, Micropterus salmoides, and
tautog found that no such deficit occurred in
either species. Yellowtail flounder larvae reared at
8°, 10°, and 12° C in this study, as well as those
reared by Smigielski ( 1979), all possessed darkly
pigmented eyes, a functional mouth and jaw- ap-
paratus, and a completely formed gut at yolk-sac
absorption. These morphological traits strongly
indicate that larvae were able to begin feeding at
this time. Smigielski (1979) further noted that
yellowtail flounder larvae were capable of surviv-
ing for several days without food after the yolk
reserves were depleted. The larva's apparent ca-
pacity to feed at yolk-sac absorption, and its ability
to survive temporarily without exogenous food
make it unlikely that an energy deficit signifi-
cantly effects survival. This observation, com-
bined with the fact that larvae reared at 8°, 10°,
and 12° C were equal in size at yolk-sac absorption,
thus conferring equal feeding and predator avoid-
ance abilities, is an indication that larvae grow-
ing at these temperatures would have equal sur-
vival potential.

Results of this study indicate that yellowtail
flounder eggs and yolk-sac larvae are euryther-
mal. Smith et al. (1978), studying diel vertical
migrations of yellowtail flounder larvae, found
that those less than about 4 mm long migrated
only short distances, and thus experienced little
temperature change. Larger larvae, however, were
subjected to as much as a 10° C change (from 5° to

737

FISHERY BULLETIN: VOL. 78, NO. 3

15° C) during the course of their migration, and
Smith et al. concluded that yellowtail flounder
larvae were "physiologically adapted to wide
ranges in temperature." Even though larger
yellowtail flounder larvae are apparently rather
eurythermal, the fact that their zone of tolerance
can be exceeded in nature is demonstrated by the
observation of Colton (1959). Colton found many
dead yellowtail flounder larvae across a 16 km ( 10-
mi) transect in which the temperature rose from 8"'
to 20° C in <24 h. This observation does not,
however, refute eurythermality in this species
since the temperature changes were so extensive
and abrupt.

These experimental results indicate that tem-
peratures between 8° and 12° C have little direct
effect on survival of yellowtail flounder larvae.
This, combined with the observations of Smith et
al. (1978) indicate that early stages of yellowtail
flounder are eurythermal. Because of this, it
seems doubtful if temperature causes the observed
fluctuations through direct physiological means.
Obviously abrupt thermal changes such as those
observed by Colton (1959) could cause mass mor-
tality and therefore poor recruitment of a year
class. Perhaps it is through such a mechanism that
temperature affects abundance. It is also possible
that temperatures tested in this study were not
high enough to demonstrate a clear relationship
between a high temperature and some physio-
logical response that would affect the larva's
ability to survive.

ACKNOWLEDGMENTS

I am grateful to Tom Dykstra and the crew of the
FV Freisland for their considerable help with col-
lection of specimens. Al Smigielski, Mike Johns,
and Gary Davis provided valuable discussions. I
am also indebted to Saul B. Saila, William H.
Krueger, H. Perry Jeffries, and the two anony-
mous reviewers who critically reviewed the manu-
script and offered many helpful suggestions.

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LUX, F. E.

1963. Identification of New England yellowtail flounder
groups, U,S. Fish Wildl, Serv,, Fish, Bull, 63:1-10.

1964. Landings, fishing effort, and apparent abundance in

738

HOWELL: TEMPERATURE EFFECTS ON YELLOWTAIL FLOUNDER

the yellowtail flounder fishery. Int. Comm. Northwest
Atl. Fish., Res. Bull 1:5-21.
1969. Landings per unit effort, age composition, and total
mortality of yellowtail flounder, Limanda ferruginea,
(Storer), off New England. Int. Comm. Northwest Atl.
Fish., Res. Bull. 6:47-52.

MACIOLEK, J. A.

1962. Limnological organic analyses by quantitative di-
chromate oxidation. U.S. Fish Wildl. Serv., Bur Sport
Fish Wildl., Res. Rep. 60, 61 p.

MARR, D. h. a.

1956. The 'critical period' in the early life history of

marine fishes. J. Cons. 21:160-170.
1966. Influence of temperature on the efficiency of growth

of salmonid embryos. Nature (Lond.) 212:957-959.

MAY, R. C.

1974a. Larval mortality in marine fishes and the critical
period concept. In J. H. S. Blaxterl editor). The early life
history offish, p. 3-19. Springer-Verlag, N.Y.

1974b. Effects of temperature and salinity on yolk utiliza-
tion in Bairdiella icistia (Jordan and Gilbert) (Pisces:Sci-
aenidae). J. Exp. Mar. Biol. Ecol. 16:213-225.
ROYCE, W. F, R. J. BULLER, AND E. O. PREMETZ.

1959. Decline of the yellowtail flounder Limanda ferrugi-
nea off New England. U.S. Fish Wildl. Serv., Fish. Bull.
59:169-267.

RYLAND, J. S., AND J. H. NICHOLS.

1967. Effect of temperature on the efficiency of growth of
plaice prolarvae. Nature (Lond.) 214:529-530.
SISSENWINE.M. P.

1974. Variability in recruitment and equilibrium catch of
the Southern New England yellowtail flounder fishery. J.
Cons. 36:15-26.

Smigielski, a. S.

1979. Induced spawning and larval rearing of the yellow-
tail flounder, Limanda ferruginea. Fish. Bull., U.S.
76:931-936.

Smith, W. G., J. D. Sibunka, and A. Wells.

1975. Seasonal distributions of larval flatfishes (Pleuro-
nectiformes) on the continental shelf betwen Cape Cod,
Massachusetts, and Cape Lookout, North Carolina, 1965-
66. U.S. Dep. Commer., NOAA Tech. Rep. NMFS SSRF-
691, 68 p.

1978. Diel movements of larval yellowtail flounder Li-
manda ferruginea, determined from discrete depth sam-
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TOETZ, D. W.

1966. The changes from endogenous to exogenous sources
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tion offish embryos (Salmofario). J. Exp. Biol. 9:271-276.

739

OXYGEN CONSUMPTION AND HEMOLYMPH OSMOLALITY OF
BROWN SHRIMP, PENAEUS AZTECUS

James M. Bishop, > James G. Gosselink,^ and James H. Stone^

ABSTRACT

Oxygen consumption and (or) osmoregulation of brown shrimp was measured under conditions appli-
cable to their natural environment or culture. Shrimp were acclimated to test salinity and temperature
a minimum of 1 week prior to any test and to the respirometer chamber for 1 hour prior to recording
data. Time of day, effects of white-light illumination, and crowding were not found to influence
significantly their mass ( m) specific oxygen consumption rate (mg O2 ■ g wet m • h ); however,
disturbedshrimpconsumedoxygennearly four times faster than shrimp at rest (0.56 vs. 0.13 mg02 ■ g
wet m ~ ' • h ~ ' ). The effects of size (3.7 and 6.7 g shrimp), salinity (10, 20, and 30% ), and temperature
(18°, 23°, 28°, 33° C) on shrimp hemolymph concentrations and oxygen consumption rates showed
that hemolymph osmolalities increased significantly with salinity and that oxygen consumption
rates increased significantly with temperature. Mean hemolymph concentrations in 10, 20, and 30%o
salinity were 616, 696, and 774 milliosmoles, but differences among oxygen consumption rates in
these salinities were negligible, supporting the hypothesis that relatively little energy is required
for osmoregulation by euryhaline species. Mean hemolymph concentrations were significantly higher
for 3.7 g shrimp (796 milliosmoles) than for 6.7 g shrimp (753 milliosmoles) only 30?. salinity, indi-
cating that the larger shrimp may be better hypoosmoregulators. At 18° C, oxygen consumption
rates averaged 0.29 mg O2 • g wet m ' • h ' and increased significantly at each test temperature
to 0.55 mg O2 ■ g wet m ' • h ~' at 33° C. Indirect calorimetry calculations showed that juvenile
shrimp (~5.2 g) in 10-30% salinity and 23°-28° C respired a daily equivalent approximating 3.4% of
their energy content, that is, 105 calories.

Shrimp comprise the basis for the nation's most
valuable seafood industry (Roedel 1973). Demand
has surpassed domestic production, and in 1975
the United States imported about 37% of its an-
nual consumption (National Marine Fisheries
Service 1978). Demand and high pound value have
made shrimp an attractive species for culture
( Rose et al. 1975 ). Although slirimp iPenaeus spp. )
culture is biologically possible, no operations have
been economically successful in the United States.
Reasons for this, in part, are that in spite of years
of study, many basic aspects of shrimp behavior,
biology, and physiology remain unknown. Fun-
damental to intensive husbandry of any animal is
knowledge of its energy budget, i.e., its consump-
tion and utilization of energy under specified con-
ditions.

Energy budgets are usually depicted as flow
schemes and diagrammatically trace energy de-
rived from food to expenditures in various

^Marine Resources Research Institute, South Carolina
Wildlife and Marine Resources Department, P.O. Box 12559,
Charieston, SC 29412.

^Center for Wetland Resources, Louisiana State University,
Baton Rouge, LA 70803.

Manuscript accepted March 1980.

FISHERY BULLETIN: VOL. 78, NO. 3, 1980.

physiological processes (see Brody 1945; Harris
1966; Crampton and Harris 1969; Brett 1970). The
amount of energy channelled through an or-
ganism and the compartmentalization of that
energy depends upon environmental and
physiological variables such as season, tempera-
ture, photoperiod, salinity, sex, size, age, food,
crowding, stage of molt cycle, etc. (Zeuthen 1947;
Waterman 1960; Prosser and Brown 1961;
Crampton and Harris 1969; Brett 1970). Because
metabolic demands of maintenance and feeding
activity must be satisfied before growth can occur,
knowledge of these demands under various condi-
tions may be used advantageously to control or
manipulate food conversion (Brett 1970). Most as-
similated energy is expended in basal metabolism
and maintenance (Brody 1945).

Internal respiration or intermediary metabo-
lism is the sum of enzymatic reactions in which
energy is made available for biological work (Pros-
ser and Brown 1961), and the best measure of
metabolism is caloric output (Fry 1957). Obtain-
ing the caloric output for an experimental or-
ganism requires the determination of its oxygen
consumption, carbon dioxide production, nitrogen
excretion, and the caloric content of excreta (Fry

741

1957). This difficult task has seldom been carried
out completely and usually oxygen consumption
alone is used to measure metabolism (Fry 1957).

To date, few researchers have studied any por-
tion of the energy budget of penaeid shrimp. The
most complete attempt was that of Qasim and
Easterson (1974), who ascertained energy in-
gested, assimilated, and egested by Metapenaeus
monoceros . Condrey et al. ( 1972) tested conversion
efficiencies of selected diets of P. aztecus and P.
setiferus, and Nose (1964) obtained protein digest-
ibility for P. Japonicus. Finally, assimilation
efficiencies of P. aztecus feeding naturally were
determined by Jones (1973).

A number of investigators have studied penaeid
oxygen consumption ( Rao 1958; Egusa 1961; Kader
1962; Subrahmanyam 1962, 1976; Zein-Eldin and
Klima 1965; Weerasinghe and Arudpragasam 1967;
Steed and Copeland 1967; Kutty 1969; Ikeda 1970;
Kutty et al. 1971; Venkataramiah et al. 1975, see
footnote 3; Green et al. 1976; Venkataramiah et
al. ). Subrahmanyam (1962) has shown that one
shrimp. P. indicus, is an oxygen conformer and
that its oxygen-consumption rate depends upon
the partial pressure of oxygen, even at saturation
levels. Thus, as the ambient oxygen concentration
in a closed chamber decreases from respiration,
the shrimp's respiratory rate will also decrease.
Because all previous investigators, except Egusa
(1961), Subrahmanyam (1976), and Ven-
kataramiah et al. (footnote 4) used static situa-
tions to measure oxygen consumption of shrimp,
their results may not be representative of res-
piratory rates in natural or culture conditions.

Shrimp of the genus Penaeus in the Gulf of
Mexico exhibit a complex life cycle that includes a
distinct migration between deep offshore waters
and shallow estuarine waters. Shrimp enter es-
tuaries as postlarvae and may grow from an initial
size of 12 mm to lengths >100 mm before returning
offshore (Williams 1965; Perez Farfante 1969). In
estuaries, shrimp experience daily and seasonal
changes in salinity and temperatui-e and, prior to

^Venkataramiah, A., G. J. Lakshmi, and G. Gun-
ter. 1974. Studies on the effects of salinity and temperature
on the commercial shrimp, Penaeus aztecus Ives, with special
regard to survival limits, growth, oxygen consumption, and ionic
regulation. U.S. Army Engineer WES, Vicksburg, Miss., Con-
tract No. DACW 39-71-C-008, 134 p.

•'Venkataramiah, A., G. J. Lakshmi, R Biesiot, J. D. Valleau,
and G. Gunter. 1977. Studies on the time course of salinity
and temperature adaptation in the commercial brown shrimp
Penaeus aztecus Ives. U.S. Army Engineer WES, Vicksburg,
Miss., Contract No. DACW 39-73-C-0115, 370 p.

FISHERY BULLETIN: VOL. 78, NO. 3

emigration, are one of the most abundant and im-
portant macroinvertebrates. In this paper we re-
port the effects of selected environmental factors
influencing the shrimp's metabolic rate and (or)
osmoregulation. We also estimate energy budgets
for animals under typical environmental condi-
tions. Experimental conditions were selected to be
applicable to the shrimp's natural environment,
i.e., typical estuarine salinities and temperatures
(St. Amant et al. 1966), or to provide knowledge
relevant to their intensive culture.

METHODS

Experimental Procedure

Brown shrimp, Penaeus aztecus Ives, were cap-,
tured in a 4.9 m otter trawl in Airplane Lake,
Jefferson Parish, La., between 1 September 1973
and 30 June 1974 (from November 1973 to January
1974, some pink shrimp, P. duorarum, may have
been included among the test animals). After cap-
ture shrimp were selected for size and transported
to Louisiana State University (LSU) in Baton
Rouge. One of two size classes, 3.7 ±0.6 g (73-82
mm total length, TL) and 6.7 ±0.9 g (90-100 mm
TL), of shrimp were used in all tests. The 3.7 g
shrimp are typical of estuarine shrimp popula-
tions (St. Amant et al. 1966), and 6.7 g shrimp are
frequently among the size range emigrating from
estuaries (Parker 1970).

In the laboratory, shrimp were placed in
polyethylene holding tanks and acclimated to test
salinity and temperature combinations for a min-
imum of 1 wk(Sick etal. 1973) prior to any experi-
ment. Acclimation and test temperatures were
maintained to within ±1.5° C. Salinity was main-
tained to within ±1.5%o (refractometer readings)
with artificial sea salt. Photoperiod was kept at 12
h light, 12 h dark ( 12:12 LD); the photophase began
at 0630 and ended at 1830 h central standard time
(c.s.t.). Shrimp were starved 24 h before testing
but otherwise fed daily an excess amount of an
extruded pellet ( EST 21-5/72A).5 Uneaten food was
removed daily. Chopped fresh shrimp or Tetra
Werke's TetraMin*^ was occasionally included in
the diet.

^Obtained from S. P Meyers, Professor, Department of Food
Science and Technologv, Louisiana State University, Baton
Rouge, LA 70803.

^Reference to trade names does not imply endorsement of that
product by the National Marine Fisheries Service, NOAA.

742

BISHOF ET AL. OXYGEN CONSUMPTION OF BROWN SHRIMP

A closed, continuously flowing, differential res-
pirometer was used to measure the oxygen con-
sumption rates. Its basic design was modified from
the apparatus employed by Keys (1930) and con-
sisted of a test chamber positioned between two
oxygen polarographs through which a known vol-
ume of water flowed from a supply to a catchment
reservoir (Bishop 1976). Hourly flow rates varied
between 1.934 and 2.519 1 depending on salinity-
temperature combinations.

Prior to a test, polarograph readings were
checked for identical response, shrimp were placed
in the chamber, the chamber voided of air and
sealed, and the water switched to flow through the
test chamber. At the end of a test, water flow was
again shunted past the chamber, and probe read-
ings were rechecked to ensure similar readings.
Probes were read to the nearest 0.05 ppm. If probe
drift occurred and exceeded 0.15 ppm the test was
discontinued and disregarded. If drift occurred,
but was <0.15 ppm, it was assumed to have oc-
curred at a constant rate, and data were corrected
accordingly. After a test the shrimp were mea-
sured, sexed, and weighed individually. Except for
diurnal experiments, all tests lasted 2 h. Mean live
mass (m ) of test shrimp is used to denote the size
class of shrimp being discussed. Hourly rates of
oxygen consumption are expressed on a per
gram live mass basis, i.e., mg O^ -g wet m~' h'K
Statistical designs and arrangements were from
Cochran and Cox (1957) and Steel and Torrie
(1960), and significant differences were tested at a
= 0.05 or 0.01.

Experiments

Diurnal Effects

Light; Reduced-Light Effects

Four 6.7 g shrimp were individually tested
while exposed to laboratory light ( 193 Im m"^ ). Test
salinity and temperature were 20%o and 25° C, and
tests lasted 2 h. An inverted, bottomless, opaque
plastic bucket was placed over the test chamber to
preclude visual disturbances. The next day each
shrimp was again tested in the same sequence, but
the light was reduced ( <10 Im m") by placing an
intact plastic bucket over the test chamber. Two
days of similar tests were repeated with three dif-
ferent 6.7 g shrimp except that the shrimp were
first tested in reduced light. An ANOVA in a cross-
over design was computed on the average oxygen
consumption rates of the last two 15-min periods.

Disturbance Effects

Four 6.7 g shrimp were tested singly for oxygen
consumption after disturbance. Test salinity and
temperature were 20%o and 25° C, and ambient
oxygen concentration was 7.4 ppm. Shrimp were
placed in the test chamber, and the chamber was
shaken by hand for approximately 5 min. The
highest oxygen consumption rate during the fol-
lowing 15 min was considered to approach that for
active shrimp.

The lowest oxygen consumption rate of shrimp
from four randomly selected diurnal experiments
was obtained to estimate standard respiration.
Because both disturbance and diurnal tests were
conducted at the same salinity and temperature,
oxygen consumption differences between these
two test conditions should result primarily from
increased metabolic activity. We used f-tests com-
paring two sample means to test for significant
differences between the shrimp's resting and ac-
tive oxygen consumption rates.

Five 6.7 g shrimp were tested individually for 24
h under a 12:12 LD photoperiod. Test salinity and
temperature was 20%o and 25° C, respectively.
Shrimp were allowed to acclimate to the test
chamber during the first 1.5 h. Except for the ini-
tial 1.5 h and 1 h following each probe check, oxy-
gen consumption data were averaged for each
15-min period and grouped into eight 3-h intervals
(0630-0930, 0930-1230, ..., 0330-0630 h). An
analysis of variance (ANOVA) employing a ran-
domized block design was computed on the aver-
age oxygen consumption for each shrimp (block)
during the eight 3-h intervals (treatments).

Crowding Effects

The effects of crowding on the oxygen consump-
tion of 3.7 and 6.7 g shrimp were investigated.
Area of the test-chamber floor was 103.9 cm^, and
chamber volume was 240 ml. Shrimp were tested
at 20%o S (salinity ) and 25° C. Light was reduced to
<10 Im m~2 during the tests by placing an in-
verted, opaque plastic bucket over the test
chamber. Eight replicates were obtained for 3.7 g
shrimp tested in groups of one and two, and a ^-test
involving two sample means was employed to test
for significant differences. Eight replicates of 6.7 g

743

FISHERY BULLETIN: VOL. 78, NO. 3

shrimp in groups of one, two, and three, and four
replicates of 6.7 g shrimp in groups of four were
also tested. An ANOVA in a completely ran-
domized design was computed for the average oxy-
gen consumption of the last two 15-min periods of
each test.

Size, Salinity, and Temperature Effects

The influence of salinity and temperature was
tested on the oxygen consumption and osmoregu-
lation of two sizes of P. aztecus. Three test
salinities (10, 20, 30%o) and four temperatures ( 18°,
23°, 28°, 33° C) were selected to represent ranges
that shrimp may experience in estuaries.

Shrimp were caught and maintained in
salinities approximating 20%o; after acclimation
to room temperature (23°-25° C) in the laboratory,
shrimp of each size class were distributed equally
among tanks of 10, 20, and 30%o S. Transferred
shrimp experienced no difficulties adjusting to a
10%o S change at 23°-25° C. Ambient laboratory
temperature was lowered to 18° C and maintained
for a week. After oxygen consumption or hemo-
lymph data were obtained from acclimated
shrimp, ambient temperature was gradually
raised for the next test and the procedure re-
peated. Four to five days appeared to be necessary
to raise the temperature from 28° to 33° C; shrimp
mortality increased with faster acclimation rates.

Shrimp were tested in pairs because two shrimp
of the smaller size were necessary to cause approx-
imately a 1 ppm oxygen concentration dif-
ference between the probes at the tested flow
rates. A 1 ppm difference minimized percent-
age error caused by translating data from the
strip-chart recorder and permitted enough flow
through the test chamber to avoid oxygen deple-
tion and excreta buildup. An inverted plastic
bucket was placed over the chamber during tests
to preclude visual disturbances and to reduce light
(<10 1mm-2).

Each of the 24 treatment combinations (2 sizes
X 3 salinities x 4 temperatures) was replicated
seven or eight times, and each test lasted 2 h.
Acclimated shrimp were selected completely at
random without replacement for each test. There-
fore the oxygen consumption of a minimum of
seven pairs of different shrimp was obtained for
each treatment combination. To allow shrimp
time to acclimate to the test chamber, data ob-
tained during the first hour were disregarded.
Data collected during the second hour were divid-

ed into four 15-min periods and the average oxygen
consumption for each period was calculated. An
ANOVA employing a split plot in a completely
randomized design with a 2 x 3 x 4 factorial
arrangement as the whole plots and period as the
subfactor was computed on the data. The effects of
the treatments (size, salinity, temperature), the
periods, and the interactions on the oxygen con-
sumption rates were evaluated. If a significant
difference was found, then orthogonal compari-
sons (Snedecor and Cochran 1967) were made to
explain more specifically the differences among
the treatments, periods, and their interactions.
Data plotted in the graphs are the average oxygen
consumption during the last Va h (the third and
fourth periods) only.

Shrimp for the osmoregulation studies were
caught between 20 March and 20 April 1974 at
Airplane Lake. After shrimp were acclimated in
the laboratory, hemolymph samples were obtained
by puncturing the dorsal arthroidal membrane
(just anterior to the first abdominal segment) and
bleeding no less than 0.2 ml directly into cuvettes.
Cuvettes were sealed with Parafilm to prevent
evaporation. The least amount of hemolymph
necessary for accurate osmolality determination
was 0.2 ml and was obtained from each 6.7 g
shrimp; however, two 3.7 g shrimp were needed to
collect the minimum volume. Osmolality was
measured within 1.5 h with an Osmette. Five sam-
ples were tested for each treatment combination
except for the following instances: 6.7 g shrimp at
18° C and 10%o S— three samples; 3.7 g shrimp at
33° C and 10, 20, 30%o S— four samples; and 6.7 g
shrimp at 18° and 28° C and 30%o S— four samples.
Hemolymph was not centrifuged, and little diffi-
culty was experienced in obtaining repeatable
readings with the Osmette.

Data were analyzed by an ANOVA employing a
2x3x4 factorial arrangement in a completely
randomized design, and orthogonal comparisons
were made on treatment combinations with sig-
nificant differences. Correlations between
hemolymph concentration and oxygen consump-
tion data at corresponding size, salinity, and
temperature combinations were made.

RESULTS

Diurnal Effects

Mean oxygen consumption rates ranged from
0.18 to 0.30 mgOag wet m~^ h"^ among the eight

744

BISHOP ET AL : OXYGEN CONSUMPTION OF BROWN SHRIMP

3-h periods (Table 1), but were not found to be
significantly different. The mean oxygen con-
sumption rates for individual shrimp during the
24-h test varied from 0.20 to 0.38 mg O2 g wet
h~' and were significantly different (Table 1).

m

Table 1. — Mean diurnal oxygen consumption rates (mg Oz-g
wet m"' • h' ) of five Penaeus aztecus: m = mass.

Size (g) of

ndividu

al test shrim

P

Mean O2

consumption

per period'

Time

6,1

7.3

6.3

5.9

6.7

0630-0930

018

0.38

0.49

0.17

0.25

0.29

0930-1230

.48

.14

.39

.18

.13

.26

1230-1530

.32

.16

.41

.22

.14

25

1530-1830

.18

.18

.26

.12

.16

18

1830-2130

.37

.21

.30

.32

.25

.29

2130-0030

.34

.18

.34

.23

.29

.28

0030-0330

.32

.15

.40

.28

.28

29

0330-0630

.33

.20

.41

28

.28

,30

Mean O2 con-

sumption

per 24 h^

.32

.20

38

23

22

.27

' Differences among time periods not significant
^Differences among shrimp fiigtily significant (P- 0 01)

Light; Reduced Light Effects

Mean oxygen consumption rates and standard
error for seven shrimp tested in light compared
with reduced light were 0.25±0.09 and 0.17±0.09
mg O2 ■ g wet m ~^ ■ h~^ and were not found to differ
significantly.

Disturbance Effects

The mean oxygen consumption rate of 6.7 g
shrimp after disturbance was 0.56±0.05 mg O2 -g
wet m~^ h"^ and 4.3 times higher than that
(0.13 ±0.01 mg Oag wet m-^-h'^) for resting
shrimp. This difference was highly significant.

Crowding Effects

Mean oxygen consumption rates and standard
error for 3.7 g f! aztecus tested singly and in pairs
were 0.50±0.06 and 0.41±0.05 mg Oag wet
m~' -h"'. These differences were not found to be
significant. One or two 3.7 g shrimp in the test
chamber resulted in an average of 0.035 or 0.071 g
of shrimp cm"^ of chamber floor and 0.015 or 0.031
g of shrimp cm""^ of chamber volume.

Mean oxygen consumption rates and standard
error of 6.7 gP. aztecus tested singly and in groups
of two, three, and four were 0.30±0.04, 0.37 ±0.02,
0.35±0.03, and 0.29±0.02 mg O2 g wet m"^ h'^
respectively. These differences were not statisti-
cally significant. One, two, three, or four 6.7 g

shrimp in the test chamber represented 0.064,
0.126, 0.188, or 0.247 g of shrimp cm-^ and 0.028,
0.054, 0.081, or 0.107 g of shrimp cm~', respec-
tively.

Size, SaHnity, and Temperature Effects

In the factorial test, size and temperature were
the only significant main effects, but salinity-size
and salinity-temperature effects were significant
interactions. (Figure 1, Table 2). The smaller

aztecus

O)

E

IS

23 28

TEMPERATURE ("C)

Figure 1. — Mean oxygen consumption rate of 3.7 and 6.7 g
Penaeus aztecus vs. temperature at salinities of 10, 20, and 30%o.

shrimp consumed more oxygen per unit mass (0.44
mg O2 ■ g wet m -1 • h-i ) than did the larger shrimp
(0.40 mg O2 g wet m~^ h-i), but this difference
was confined to salinities of 20%o as shown by the
salinity-size interaction (Figure 1, Tables 2, 3). In
20%o S, the 3.7 g shrimp consumed an average of
0.46 mgOj g wetm-i h-^ and the 6.7 g shrimp
consumed about 0.34 mg O2 g wet m ~J h"!.

745

FISHERY BULLETIN: VOL. 78, NO. 3

Table 2. — Analysis of variance of the effects of size, salinity,
temperature, and period on the mean oxygen consumption rates
ofPenaeus aztecus.

Table 4.-

-Mean oxygen consumption rates of Penaeus aztecus
for each test temperature; m = mass.

Source of variation

df

Mean square'

Size

1

0.3089-

Salinity

2

.0333

Sallnlty-size

2

.3922"

10%o:3.7 vs. 6.7 g shrimp

.0554

20%o:3.7 vs. 6.7 g shrimp

.9458--

30%o:3.7 vs. 6.7 g shrimp

.0480

Temperature

3

25200--

18°. 23° vs. 28°, 33° C

66970--

18° vs. 23° C

.3254-

28° vs. 33° C

.4532-

Temperature-size

3

.0172

Salinity-temperature^

6

.2744"

10%o:T|

4. 2317"

Tc

.0100

.0583

20%.:T|

1.6643"

:Tq

.1327

Tc

.0133

30%.:T|

1.7817"

:Tq

.1393

;Tc

1.0509"

SIze-salinity-temperature

6

.0636

Error (a)

161

.0597

Period:

3

.0838"

Periods 1. 2 vs. periods 3, 4

1

.2024"

Period 1 vs. period 2

1

.0266"

Period 3 vs. period 4

1

.0132"

Size period

3

.0023

Salinity period

6

.0005

Size-salinity period

6

.0001

Temperature period

9

.0048

Size-temperature period

9

.0019

Salinity-temperature period

18

.0031

Size-salinity-temperature period

18

.0007

Error (b)

481

.0017

'• = P<0.05;"P<0.01.

^Subscripts: I = linear; q = quadratic; c = cubic.

Table 3. — Mean oxygen consumption rates ofPenaeus aztecus
for the salinity-size interactions; m = mass.

mg O2

S(%.)

Size (g)

n

g wet m ■ h

SE

10

3.7

127

0.411

0.022

10

6.7

120

.442

.022

20

3.7

127

.465

.022

20

6.7

116

.338

.023

30

3-7

124

.436

.022

30

6.7

124

,408

.022

The average oxygen consumption rate increased
significantly with increasing temperature, from
0.29 mg 02-g wet m^i h'' at 18° C to 0.55 mg
Oag wet m-i-h-i at 33° C (Table 4). At each
salinity oxygen consumption increased linearly
with temperature, except at 30%o, where oxygen
consumption peaked at 28° C and decreased signi-
ficantly at 33° C (Figure 1, Table 2).

Oxygen consumption rates differed significant-
ly among periods (Table 2). Rates during the first
15-min period averaged 0.44 mg O2 g wet m'^ h"^
and decreased to an average of 0.40 mg O2 -g wet
m~i h"^ during the fourth 15-min period (Table
5). Significant differences of oxygen consumption

mg02

T(°C)

n

g wetm h

SE

18

187

0.293

0.018

23

184

.352

,018

28

183

.479

.018

33

184

.549

018

Table 5. — Mean oxygen consumption rate of Penaeus aztecus
during four consecutive 15-min periods after 1 h acclimation in
respirometer chamber; m = mass.

od

n

mg O2

15-min per

g wet m h

SE

First
Second
Third
Fourth

184
184
186
184

0.443
.426
.407
.395

0,003
,003
.003
.003

rates among period interactions were not found
(Table 2).

When hemolymph osmolality was analyzed for
shrimp acclimated to the same conditions as previ-
ously described, size and salinity were significant
main effects; and salinity-size, temperature-size,
and salinity-temperature effects were signifi-
cant interactions (Figure 2, Table 6). The mean
hemolymph osmolality of 3.7 g shrimp was sig-
nificantly higher than that of 6.7 g shrimp (Tables
6, 7), but this difference was found only in combi-
nations that included 30%o S or 33° C. In 30%o S the
smaller shrimp's hemolymph osmolality averaged
over all temperatures was 796 mOsm (millios-
moles) compared with 753 for the larger shrimp.
At 33° C the same comparison averaged over all
salinities was 734 and 678 mOsm (Figure 2).

The mean hemolymph osmolality increased
with increasing salinity (616, 696, and 774 mOsm
at 10, 20, and 30%o, respectively; Table 7). At each
salinity, the effect of increasing temperature on
the shrimp's hemolymph osmolality was tested.
Significant linear responses were obtained at 10
and 30%o (Table 6, Figure 3). Significant correla-
tions were not found between hemolymph osmolal-
ity and oxygen consumption rates.

DISCUSSION

Sources of Variability

Many complicating variables must be consid-
ered in attempting to obtain the standard
metabolism of penaeid shrimp. Physiological
rhythms, stage of the molt cycle, and lunar phases

746

BISHOP ET AL.: OXYGEN CONSUMPTION OF BROWN SHRIMP

« ^2.7 g ?. aztecus

» «6.7 g P^. aztecus

900 r

Line of Isotonicity

J 1 1 1 I

yuu

T^23 'C

/

800

-

/ .•

700

y

600

••■■'

/

500

1 1

/ 1 1

1 1 1

600 800

1000

200 400

600

800 1000

900

<

z

a:

Z 800

700

600

500

T=28 C

900

800

700

600

500

200

400

600

800

1000

200

400

600

800

1000

EXTERNAL MEDIUM (mOsm)
Figure 2.— Mean hemolymph osmolality (mOsm) of 3.7 and 6.7 gPenaeus aztecus vs. temperatures at 18°, 23°, 28°, and 33° C.

may complicate the ideal of testing uniform sub-
jects under similar conditions. In addition, the ef-
fects of spontaneous activity often mask any dif-
ferences of metabolism resulting from the effects
of osmoregulation, size, temperature, etc. In the
present study, attempts to eliminate molt-stage
differences were made by testing a minimum of
seven pairs of shrimp. Because integumental
changes occur at least 70% of the time between

successive molts for decapods (Passano 1960), the
testing of only intermolt, acclimated animals
would have been nearly impossible. Most of the
shrimp tested, however, should have been in a
stage other than immediate premolt, and newly
molted shrimp were not tested. Therefore it is as-
sumed that most of the test animals were at a molt
stage that affected the total oxygen consumption
relatively little.

747

FISHERY BULLETIN: VOL. 78, NO. 3

Table 6. — Analysis of variance of the effects of size, salinity,
and temperature on the osmolality of Penaeus aztecus
hemolymph.

Source of variation

df

Mean square'

Size

1

9,343-

Salinity

2

231,198*-

10, 20vs, 30%..

332,414"

lOvs. 20%«

121,516"

Salinity-size

2

5,836-

10%«;3.7 vs. 6.7 g shrimp

4,076

20%«;3 7vs. 6.7 g shrimp

624

30%«:3.7vs. 6.7 g shrimp

16,781"

Temperature

3

2,734

Temperature-size

3

4,899-

18' C: 3 7 vs. 6.7 g shrimp

447

23° C: 3.7 vs. 6.7 g shrimp

367

28° C: 3.7 vs. 6.7 g shrimp

4,136

33° C: 3.7 vs. 6.7 g shrimp

20,449"

Salinity-temperature^

6

5.597"

10%«:T|

8,959-

:Tq

231

Ic

3,110

20V:T|

12

:Tq

1,523

:Tc

12

30%«:T|

23,623"

:Tq

2,368

:T?

1,065

Size-sail nity-temperature

6

2,061

Error (a)

89

1,231

'- = P<0.05;-- =P<0.01
^Subscripts: I = linear; q = quadratic; c

cubic.

Table 7. — Mean hemolymph osmolality of Penaeus aztecus in
relation to size and salinity of acclimation water.

Hemolymph

Osmolality of external

Variable

n

(mOsm)

SE

medl

um (mOsm)

Size, g:

37

56

703

47

606

6.7

57

688

4.6

584

Salinity, %«:

10

37

616

5.8

310

20

39

696

5.6

590

30

37

774

5,8

886

850

800

S 750

o

E

S 700

>-
— I

o

5

LU

X 650

600

550

S=10%o

23 28

TEMPERATURE (X]

33

Figure 3. — Mean hemolymph osmolality ofPenaeus aztecus vs.
temperature at salinities of 10, 20, and 30%o.

Although no significant time-of-day differences
were found (Table 1), efforts were made to test
equal numbers of shrimp in the morning and af-
ternoon at each treatment combination. Evidence
indicates that shrimp are influenced by lunar cy-
cles (Wheeler 1937; Racek 1959; Aaron and Msby
1964; Wickham 1967; Hughes 1972; Bishop and
Herrnkind 1976), but in the present studies, we
assumed that lunar influences on the oxygen con-
sumption were negligible because of acclimation
periods. Subrahmanyam (1976) obtained results
indicating the presence of an oxygen consumption
rhythm in pink shrimp that coincided with the
tidal cycle, but this rhythm waned after the
shrimp were maintained for a week in captivity.

Because of the absence of standardized
techniques for measuring routine oxygen con-
sumption of poikilotherms, many of the previous
studies on the oxygen consumption of penaeid
shrimp are of limited usefulness. Frequently per-
tinent circumstances relating to acclimation time
and (or) test conditions were not reported (Sub-
rahmanyam 1962; Zein-Eldin and Klima 1965;
Weerasinghe and Arudpragasam 1967; Steed and
Copeland 1967), and closed chambers were used in
most published studies. Consequently, test ani-
mals could not acclimate to test chamber condi-
tions and probably exhibited increased activity.

In our studies, the shrimp's activity was
minimized by several methods: first, the test ani-
mals were acclimated to a specific test salinity-
temperature combination for at least a week prior
to testing; second, the shrimp were allowed to ac-
climate to the test chamber for an hour before data
were collected; and third, an inverted opaque plas-
tic bucket was placed over the test chamber to
reduce the light and to prevent disturbances from
human activity in the laboratory.

Reducing the light to the test chamber reduced
the mean oxygen consumption (0.25 vs. 0.17 mg
02g wet m~' h"') although the effect was not
statistically significant. The hour acclimation
prior to taking data was not enough time to allow
the shrimp to adjust to the test chamber because
the oxygen consumption rate for each 15-min
period continued to decline throughout the second
hour (Tables 2, 5). Although the average oxygen
consumption rate decreased significantly during
each subsequent 15-min period of the second hour
of testing, the overall rate change was small, an
11% decrease between the first and last period. The
rate change was consistent across all treatments
and unrelated to the treatment effects because no

748

BISHOP ET AL.: OXYGEN CONSUMPTION OF BROWN SHRIMP

significant differences were found among any of
the period interactions (Table 2 ); thus the effects of
size, salinity, and temperature are independent of
acclimation time. The average oxygen consump-
tion data for each treatment combination in Table
3 and Figure 1 are slightly higher than would be
expected for shrimp completely acclimated to the
test chamber, however. Egusa ( 1961) found that the
oxygen consumption rate ofP.japonicus stabilized
after about 3 h. Acclimation time to test conditions
may have been reduced if fine-grained substrate
had been included in the test chamber. Penaeid
shrimp exhibit arrhythmic activity when they
cannot bury in substrate (Racek 1959; Moller and
Jones 1975).

Because shrimp may be both oxygen conformers
and regulators, crowding could profoundly influ-
ence their oxygen consumption by increasing the
extent of activity. We found no significant oxygen
consumption rate differences between one and two
3.7 gP. aztecus or among one, two, three, and four
6.7 gP. aztecus when compared on a per gram wet
mass basis, and believe that testing two shrimp
simultaneously did not appreciably affect their
oxygen consumption rates. Subrahmanyam ( 1976)
noticed no differences in activity when testing
pink shrimp singly or in pairs.

Salinity Effects on
Oxygen Consumption and Osmoregulation

The influence of salinity on the life habits of
penaeid shrimp has received considerable atten-
tion (Panikkar 1951, 1968; Gunter and Hildebrand
1954; Zein-Eldin 1963; Gunter et al. 1964; Parker
1970). Panikkar (1951) suggested that high salin-
ity may be necessary for ovarian development, but
its importance still remains unknown. Life cycles
of the three penaeid shrimp important commer-
cially in the Gulf are similar (Williams 1965), but
juvenile white shrimp, P. setiferus, are reported to
prefer salinities <10%o; juvenile brown shrimp,
salinities between 10 and 20%©; and juvenile pink
shrimp, salinities >18%o (Gunter et al. 1964).
Adaptation to low salinities is highly developed in
young penaeids, and juveniles are more widely
distributed in estuaries than are adults. Thus, os-
moregulatory capabilities may influence emigra-
tion of subadults from estuaries (Panikkar 1968).
Zein-Eldin (1963) obtained good growth and sur-
vival for postlarval P. aztecus at 2, 5, 10, 25, and
40%o, and concluded that salinity per se may not
directly affect growth during the estuarine por-

tion of their life cycle. These postlarvae were
grown only to sizes <0.2 g (Zein-Eldin 1963 ), so the
effects of low salinity on growth rate during a
substantial portion of their life cycle remains un-
investigated.

Brown shrimp were hyperosmotic regulators in
10 and 20%o S and hypoosmotic regulators in 30%o
S. Depending on salinity and temperature,
hemolymph osmolality was maintained at con-
centrations approximating 600-900 mOsm (Fig-
ure 2). These results agree with those of Williams
(1960) and McFarland and Lee (1963). Thus P. az-
tecus cannot be considered a perfect regulator, but
it differs substantially from nonregulators.
Panikkar (1968) considered homoiosmotic regula-
tion to be one of the most advanced capabilities of
marine invertebrates.

Oxygen consumption would be expected to in-
crease for osmoregulators as the osmotic differ-
ence between the shrimp's hemolymph and its en-
vironment increased because metabolism would
increase to maintain a constant hemolymph con-
centration. Energy expenditure for osmoregula-
tion depends on the species and is related to tem-
perature as well as other variables (see reviews
by Kinne 1964, 1966, 1967).

There is conflicting evidence as to whether im-
portant energy expenditures are necessary to
maintain homoiosmotic hemolymph (Schwabe
1933; Lofts 1956; Rao 1958; Dehnel 1960). In our
tests hemolymph osmolalities of P. aztecus were
significantly affected by salinity, but the energy
expenditures for osmoregulation after acclimation
were small in relation to total metabolic rate.
Other studies on euryhaline decapods show that
salinity does not have pronounced effects on oxy-
gen consumption if the experimental animals are
acclimated to the test salinities and if test
salinities are not too extreme (Lofts 1956; Rao
1958; Kader 1962; Kutty et al. 1971).

Venkataramiah et al. (footnote 4) acclimated
brown shrimp to 15%o S at 25° C and measured
oxygen consumption rates after salinity was
changed to 2, 5, 10, 15, 25, and 36%o. Metabolic
rates increased initially, but generally tended to-
ward that of acclimation conditions after a day
unless deviations from acclimation salinity were
substantial, i.e., 2, 5, and 36%o. Salinity changes in
the respirometer were made over a 1-h period,
however, and may have been too rapid and (or)
extreme for the shrimp's capacity to adjust. Ven-
kataramiah et al. (footnote 4) found that blood
hemolymph required 6 h to achieve osmotic stabil-

749

ity when shrimp were transferred from 15 to 2 or
36%o S; osmotic stability was achieved in 2 h after
transfer from 15 to 5, 10, 15, or 25%o S.

Highest catch rates for brown shrimp were de-
termined by Copeland and Bechtel (1974) to occur
in salinities from <4 to >35%o. This lower limit is
slightly less than the range of salinities (5-8%o)
suggested by Khlebovich (1968) at which ion ratios
change from typically freshwater to marine.
Therefore it appears that if juvenile or subadult
shrimp were acclimated to salinities that are typi-
cally marine (8-35%o), oxygen consumption rates
will not reflect any significant increased energy

FISHERY BULLETIN: VOL. 78. NO. .3

demands necessary for osmoregulation. Table 8
summarizes oxygen consumption rates of penaeid
shrimp that have been acclimated to and tested at
various salinity-temperature combinations.
Routine and standard rates vary from 0.14 to 0.75
mg O2 g wet m~^ h"^.

Shrimp Size Effects on
Oxygen Consumption and Osmoregulation

The effects of size on an animal's oxygen con-
sumption are apparent for individuals ranging
from 1 to 1,000 g (Zeuthen 1947). Generally a large

Table 8. — Oxygen consumption of penaeid shrimps; some data converted to allow uniform reporting. Temperature (T) in degrees
Celsius, salinity (S) in parts p)er thousand, and mass (m) of live shrimp in grams. Genera Metapenaeus and Penaeus abbreviated as M.
and P.

Acclimation

Test

Size

(g)

Metabolic
state

mg O2

Species

T

s

Days

T

S

g wet m ■ h

Source

M. monoceros^

29

35

>3

29

30

0.53

Routine''

1.34

Kader (1962)

31

33

V/2

31

33

2-6

Routine

.75

Rao (1958)

31

20

V/2

31

17

2-6

Routine

.75

Rao (1958)

P. aztecus

—

—

Several

—

—

4-7

Routine^

.39

Zein-Eldin and Klima (1965)

—

32

V2

—

32

—

Routine''

.3

Steed and Copeland (1967)

18

10

>7

18

10

3.7

Routine

.22

Bistiop (1974)

18

20

>7

18

20

3.7

Routine

.35

Bistiop(1974)

18

30

>7

18

30

3.7

Routine

.38

Bishop (1974)

23

10

>7

23

10

3.7

Routine

.40

Bishop (1974)

23

20

>7

23

20

3,7

Routine

.40

Bishop (1974)

23

30

>7

23

30

3.7

Routine

,30

Bishop (1974)

28

10

>7

28

10

3,7

Routine

.44

Bishop (1974)

28

20

>7

28

20

3.7

Routine

.49

Bishop (1974)

28

30

>7

28

30

3.7

Routine

.59

Bishop (1974)

33

10

>7

33

10

3.7

Routine

.59

Bishop (1974)

33

20

>7

33

20

3.7

Routine

.62

Bishop (1974)

33

30

>7

33

30

3.7

Routine

.49

Bishop (1974)

18

10

>7

18

10

6.7

Routine

.28

Bishop (1974)

18

20

>7

18

20

6.7

Routine

.27

Bishop (1974)

18

30

>7

18

30

6.7

Routine

.26

Bishop (1974)

23

10

>7

23

10

6.7

Routine

.37

Bishop (1974)

23

20

>7

23

20

6,7

Routine

.31

Bishop (1974)

23

30

>7

23

30

6.7

Routine

.35

Bishop (1974)

28

10

>7

28

10

6.7

Routine

.47

Bishop (1974)

28

20

>7

28

20

6.7

Routine

.33

Bishop (1974)

28

30

>7

28

30

67

Routine

.57

Bishop (1974)

33

10

>7

33

10

6.7

Routine

.64

Bishop (1974)

33

20

>7

33

20

6.7

Routine

.45

Bishop (1974)

33

30

>7

33

30

67

Routine

.48

Bishop (1974)

18

15

7

18

15

-6

Standard

12

Venkataramiah et al. (text footnote 4)

25

15

7

25

15

~6

Standard

.18

Venkataramiah et al. (text footnote 4)

32

15

7

32

15

--6

Standard

.38

Venkataramiah et al. (text footnote 4)

P du or arum

—

32

Vz

—

32

—

Routine

.14

Steed & Copeland (1967)

25

20

25

20

0.44

Standard

.59

Subrahmanyam (1976)

25

20

25

20

0.44

Active

1.19

Subrahmanyam (1976)

25

20

25

20

0.52

Standard

.76

Subrahmanyam (1976)

25

20

25

20

0.52

Active

1.54

Subrahmanyam (1976)

25

20

25

20

1.68

Standard

26

Subrahmanyam (1976)

25

20

25

20

1.68

Active

.47

Subrahmanyam (1976)

25

20

25

20

3.65

Standard

.47

Subrahmanyam (1976)

25

20

25

20

365

Active

.57

Subrahmanyam (1976)

25

20

25

20

9.66

standard

.18

Subrahmanyam (1976)

25

20

25

20

9.66

Active

.26

Subrahmanyam (1976)

25

20

25

20

11.0

standard

.26

Subrahmanyam (1976)

25

20

25

20

110

Active

.30

Subrahmanyam (1976)

P. indicus

28

15

—

28

15

2.4-3.7

Routine

.57

Subrahmanyam (1962)

28

15

—

28

15

5.1-7.8

Routine

.36

Subrahmanyam (1962)

30

36

14

30

36

2 7

Routine

.7

Kutty (1969)

28

21

5

28

21

0.1

Routine

.9

Kutty etal.(1971)

P japonicus

23

28

7-14

23

28

2.4-3.7

standard

.18

Egusa (1961)

23

28

7-14

23

28

4.6-6.2

standard

.15

Egusa (1961)

P semisulcatus

30

36

14

30

36

17.3

Routine

.35

Kutty (1969)

P setiferus

25

22

14

25

25

0.04

Routine?

1.60

Green et al. (1976)

'Tested at 63% oxygen saturation.

750

BISHOP ET AL.: OXYGEN CONSUMPTION OF BROWN SHRIMP

individual consumes more oxygen than a smaller
one, but its rate of oxygen consumption per unit
mass is less (Mill 1972). In our study this generali-
zation was found for shrimp only at 20%o S. Al-
though it is not known why this difference was
evident at only one salinity, it should be noted that
among the six salinity-size treatment combina-
tions, the lowest as well as the highest metabolic
rates occurred at 20%o S (Figure 4). It is possible
that the 3.7 g shrimp were more active than
"routine" in the test chamber and that the 6.7 g
shrimp were less active than "routine." Tests for
both sizes at each temperature were conducted
within a few days of each other, and we believe that
the time element was not responsible for the ob-
served difference. Each salinity-size combination
is the average of approximately 30 tests, and the
possibility of obtaining the results by chance is
small. The data in Table 8 indicate decreasing
metabolic rate (per unit mass) with increasing
size, although extreme variability exists.

0.50

0.45

u>

E

0.40

0.35

0.30

• 3.7 g P. gztecus

• 6.7 g £. gztecus

10

20

SALINITY (%o)

30

Figure 4. — Mean oxygen consumption rate (average for all test
temperatures) of 3.7 and 6.7 gPenaeus aztecus at salinities of 10,
20, and 30%o.

As shrimp increase in size in the estuary, they
move to higher, more stable salinities (Weymouth
et al. 1933; Gunter 1945, 1950; Williams 1960;
Bishop and Shealy'^). This movement may be, in

'Bishop, J. M., and M.H.Shealy.Jr 1977. Biological obser-
vations on commercial penaeid shrimps caught by bottom trawl
in South Carolina estuaries, February 1973 - January
1975. S.C. Wildl. Mar. Resour. Dep., Mar Res. Div., Tech. Rep.
25, 97 p.

part, a response to a decrease in osmoregulatory
ability with increasing size. Only two sizes of
shrimp were tested, and both sizes were obtained
from the same locality ( often from the same trawl
tow). Thus osmoregulation differences would not
be anticipated to be large. The larger shrimp ap-
pear to be better regulators in hyperosmotic salin-
ity and at high temperatures. The slopes of the
hemolymph data over test salinities at 33° C for
the 3.7 and 6.7 g shrimp were 0.47 and 0.33, indi-
cating that the larger shrimp maintained
homoiosmoticity to a better degree than did the
smaller shrimp at a temperature approaching an
environmental extreme (Figure 2).

Some of our test conditions and those of Wil-
liams (1960) are nearly identical, and hemolymph
data from shrimp acclimated to similar conditions
are comparable. Hemolymph data from both 3.7
and 6.7 g shrimp were averaged to be compatible
with Williams' (1960) juvenile P. aztecus (42-100
mm TL). At 28° C and 10, 20, and 30%o S, we
obtained average hemolymph osmolalities of 619,
689, and 785 mOsm, respectively, whereas Wil-
liams obtained values approximating 657, 804,
and 825 mOsm. Williams' values are somewhat
higher than ours, but physiological differences in
populations, analytical techniques, or acclimation
history of test animals could be responsible.

Because small shrimp (3.7 g) may encounter
highly variable salinities, they may be capable of
tolerating relatively variable hemolymph os-
molalities and their osmoregulatory processes
may not be as capable of homoiosmoregulation as
those of larger shrimp. This implies that varying
salinities would be more expensive energetically
for larger shrimp and partially responsible for
their offshore movement prior to maturity.

Temperature Effects on
Oxygen Consumption and Osmoregulation

Metabolic rate of most poikilotherms is related
to temperature (Prosser 1973). The lowest test
temperature that we used (18° C) approached as
closely as our facilities permitted the 16° C at
which P. aztecus is reported to exhibit little growth
(St. Amant et al. 1966). The highest test tempera-
ture approaches the shrimp's lethal limit (Zein-
Eldin and Griffith 1969) and is seldom experienced
in Louisiana estuaries. The oxygen consumption
rates of shrimp increased linearly as temperature
increased, and rates for both sizes increased in a
similar manner (Figure 1).

751

FISHERY BULLETIN. VOL. 78. NO. 3

The Qio's [oxygen consumption at (T + 10)
° C/oxygen consumption at T° C] are presented in
Table 9. Although there are minor differences at
different temperature ranges, the average Q,,j's
are nearly equal and very close to the average 1.7
obtained by Scholander et al. (1953) for P.
brasiliensis tested at 25° and 30° C. Wolvekamp
and Waterman (1960) stated that generally Q^,
values increase as the temperature decreases, but
an increase was not obvious in this study.

Table 9. — Qio's for two sizes of Penaeus aztecus; oxygen con-
sumption data averaged over all test salinities.

Table lO. — Calculation of oxygen available to Penaeus aztecus
and consumed at 20 and 30%o salinity (S) and 33° C; m = mass.

Size (g)

Temperature ( C)

Q,n

3.7
3.7

6.7

6,7

Mean

Mean

18-28
23-33

18-28
23-33

18-28
23-33

1-59
1 63

1.71
1.63
1.65
1.63

Temperature effects at tested salinities were not
uniform. In 10 and 20%o S, oxygen consumption
increased significantly as temperature increased
(Figure 1, Table 2), but in 30%o S, oxygen consump-
tion peaked at 28° C and decreased at 33° C. This
reduction indicates a possible detrimental effect
on P. aztecus when both salinity and temperature
are high. The osmoregulatory abilities of P. az-
tecus are reduced at 33° C (Figures 2, 3), and salin-
ity effects appear to become increasingly impor-
tant. Other studies have also indicated reduced
responses of P. aztecus tested at high tempera-
tures. Survival of juveniles (10-50 mm TL) was
<80% at temperatures >28° C at 25%o S (Zein-
Eldin and Aldrich 1965; Zein-Eldin and Griffith
1969). Rates of growth ( mass) of postlarvae in salin-
ities >25%o were less at 32° C than at 25° C (Zein-
Eldin and Aldrich 1965). Brown shrimp acclimat-
ed to 32° C were more sensitive to temperature
change than those acclimated to 18° or 25° C and
showed reduced osmoregulatory abilities in salin-
ities <10%o ( Venkataramiah et al. footnote 4).

The possibility exists that oxygen consumption
rates at 33° C and 30%o S are a reflection of reduced
dissolved O2 concentration. That is, at 33° C, oxy-
gen is less soluble in 30%o S than in 10 or 20%o S,
and the shrimp's oxygen consumption may be pro-
portional to the oxygen concentration. To test this
hypothesis, the difference between the average
oxygen consumption in 20 and 30%o S at 33° C was
calculated and compared with the difference be-
tween the oxygen available in the test chamber at
20 and 30%o at 33° C (Table 10). The decrease of

O2 available (mg h " ' ) at 20%. S

15.62

O2 available (mg h ') at 30%«S

14.06

Difference (mg Oj h"')

1.56

Average Oj consumption mg ■ g wet m ' h ~ ' for sfinmp

at 20%oS

0.54

Average mass (g) of stirimp

5.10

Average 0^ consumption (mg h~') per sfirimp

275

Average Oj consumption mgg wetm^' h~' for sfirimp

at 30%o S

0.49

Average mass (g) of shrimp

547

Average O2 consumption (mg fi^') per sfirimp

2.68

O2 consumption difference between 20 and 30%o S

(mgOjfi-')

0.07

total oxygen consumption between 20 and 30%o
was <0.1 mg h~' and is not of similar magnitude to
the oxygen-available difference of 1.56 mg h~' ; the
differences indicate that P. aztecus is an oxygen
regulator. Also the saturated oxygen concentra-
tion at 30%o S and 33° C is well above the stress
level of 2 ppm obtained by Egusa (1961) for P.
japonicus. Therefore the decrease in dissolved
oxygen resulting from the increased salinity does
not appear to be responsible for the reduced rate of
oxygen consumption of brown shrimp in 30%o S
and 33° C.

As temperature increased to 33° C, hemolymph
osmolality tended toward that of the external
medium for shrimp tested in 10 and 30%o S ( Figure
3). Williams (1960) found the osmoregulatory
abilities of P. aztecus were significantly less at 8.8°
C than at 28° C. Thus it appears that as tempera-
ture approaches environmental extremes, os-
moregulatory abilities are impaired, and shrimp
tend toward osmoconformity. Penaeus aztecus was
able to maintain homoiosmoticity at 20%o over the
tested temperatures (Figure 3), indicating that at
high temperatures ( 33° C ) and a moderate salinity,
osmoregulatory processes are not adversely af-
fected.

Energy Considerations

The metabolic energy expenditure of shrimp can
be calculated from knowledge of their oxygen con-
sumption rates and their metabolic substrate (in-
direct calorimetry). Because shrimp are omnivo-
rous (Williams 1955; Mistakidis 1957; Eldred et
al. 1961; Perez Farfante 1969; Moriarty 1977), a
combination of carbohydrate, lipid, and protein as
the shrimp's metabolic substrate should give a
reasonable estimate of the oxygen-consumption/
energy-expenditure relationship. At standard
conditions, combustion of 1 g of carbohydrate,
lipid, or protein with 1 1 of oxygen yields 5,007,

752

BISHOP ET AI,.: OXYGEN CONSUMPTION OF BROWN SHRIMP

4,686, or 4,500 cal, respectively (Giese 1968). The
caloric value of each of these sources varies <67(
from the mean. Therefore, for every milligram of
oxygen consumed, about 3.31 cal will be liberated.
A 6.7 gP. aztecus utilizes 0.87 and 3.75 mg 0^ h'^ at
rest and during activity at 25° C, which translates
to 2.88 and 12.41 cal h"V (The caloric expenditure
during activity is calculated from the maximum
oxygen consumption over a 15-min period.) Other
average energy expenditures of P. aztecus at
selected conditions are presented in Table 11.

T.\BLE 11. — Mean rates of oxygen consumption and energy ex-
penditures ofPenaeus aztecus at each test temperature averaged
over all test salinities; m = mass.

Temperature CC)

mg O2

calories

Size (g)

g welm h

g wet m h

3.7

18

032

1 06

3.7

23

0.36

1.19

37

28

0.51

1.69

3.7

33

0.57

1 89

6.7

18

0.27

089

67

23

0.34

1 13

6.7

28

0.45

1.49

67

33

0.53

1.75

Q

About 80% of a penaeid shrimp's mass is water,
so the dry mass of a 3.7 and a 6.7 g shrimp ap-
proaches 0.74 and 1.34 g, respectively. A gram of
dried whole Metapenaeus monoceros yields 3,066
cal upon combustion (Qasim and Easterson 1974);
thus the energy content of a 3.7 g P. aztecus is
about 2,269 cal and that of a 6.7 g shrimp, about
4,108.

If a 6.7 g shrimp maintains a resting state for 24
h at 25° C, then a minimum of 69 cal will be
utilized just for maintenance. This is about 1.7'7f of
its total caloric content or 0.11 g wet mass equiva-
lent. Therefore, a 6.7 g shrimp must daily assimi-
late a minimum of 1.7*7^ of its body wet mass of
equal caloric value food to maintain itself at rest.
If a maximum state of activity were continued for
24 h (oxygen consumption = 0.56 mg Og g wet
m"'h"', then approximately 298 cal would be
expended. This is more than 7.27c of the 6.7 g
shrimp's total caloric content. Shrimp obviously do
not maintain a continuous state of maximum ac-
tivity, and their mean daily energy expenditure is
probably 3-4% of body caloric content.

Oxygen consumption averaged over all test
salinities and at 23° and 28° C during the fourth
15-min test period was 0.40 and 0.37 mg O2 g wet

*H. C. Loesch, marine biologist, 1232 Dahlia St., Baton Rouge,
LA 70808, unpubl. data 13 November 1974.

m'h' for 3.7 and 6.7 g shrimp (Bishop 1974).
These two shrimp sizes and water temperatures
are characteristic of Barataria Bay, La. during
May (St. Amant et al. 1966), and an average oxy-
gen consumption rate of 0.38 mg Ogg wet
m~ih~i should be a conservative estimate of
routine oxygen consumption for inshore shrimp
during this time period. Because P. aztecus buries
itself in the substrate during the day (Williams
1965), we calculated daily caloric expenditures
based on a routine state of metabolism for 12 h and
a resting state for 12 h. Using the average value of
0.38 mg O^g wet m~*h~^ for routine oxygen
consumption and 0.13 mg Og -g wet m~' h"! for
standard metabolism for 5.2 g P. aztecus (average
of 3.7 and 6.7 g shrimp), a daily caloric expendi-
ture of 105 cal is obtained. This is about 3.3% of a
5.2 g shrimp's caloric content and supports the
assumption of a 3-4% expenditure of their body
wet mass per 24 h.

St. Amant et al. ( 1966) estimated that P. aztecus
grew an average of 1 mm d ' while in the es-
tuaries, which represents a daily gain in wet mass
of 0.18 g (Fontaine and Neal 1971) or 110 cal in
potential energy.

Because shrimp feed on a variety of materials in
the estuary (Williams 1955; Dall 1968; George
1974), assimilation rates probably vary widely de-
pending on the food ingested and its chemical
composition. Assimilation efficiency calculated on
a mass basis may differ from that based on
calories, and a range of efficiencies would be ex-
pected in natural conditions. As assimilation effi-
ciency decreases, maintenance energy increases,
but the point of diminishing returns is not known.
Condrey et al. (1972) determined from laboratory
experiments that shrimp of the genus Penaeus
assimilated 33-74% of the ingested food mass, and
Jones (1973) reported 25-40% assimilation rates
from shrimp feeding naturally in Airplane Lake.
Using extremes of these percentages and assum-
ing that assimilation rates for mass and calories
are similar and ihaXP. aztecus is primarily a detri-
tal consumer in Louisiana estuaries, first order
approximations are possible for daily ingestion
rates (Table 12).

Assimilation (A ) of food energy must equal the
sum of that for respiration {R), stored energy
(growth G), and excretion iE) (see Table 12). As-
similated food is derived from food ingested (/). If
the energy assimilation efficiency (A// x 100) is
assumed to be 34% , a 5.2 g shrimp must consume
about 638 cal d" at observed growth rates [G +

753

FISHERY BULLETIN: VOL. 78, NO. 3

R +E =A; 110 + 105 + 2 =217cald"';/ = A/0.34
= 638 cal d~'J. This is equivalent to 1.10 g wet
Spartina alterniflora detritus [assuming 3,760
cal/dry g (Gosselink and Kirby 1974) and SAA%
water'*], or about 20. 07^^ of the shrimp's body mass
per day. Daily growth rates of brown shrimp have
been reported as rapid as 3.3 mm (Ringo 1965).
This is more than three times the rate used for our
calculations and would substantially increase the
amount of ingested food and consequently the per-
cent of food mass intake relative to body mass.

Table 12. — Daily calorie values for energy ingested (/) and that
utilized for growth (G), respiration (R), and excretion iE) based
on assimilation rates of 25 £ind 1A% for a 5.2 g (live mass) Penaeus
aztecus.

Assimilation efficiency (°o)

/

25

74

110
110

105
105

868
293

'Calculated from Nelson et al. (1977) and Brafield and Solomon (1972).

Qasim and Easterson (1974) obtained caloric as-
similation efficiencies as high as 96.84% for M.
monoceros , but they fed shrimp small particle de-
tritus, which they settled from estuarine waters.
This detritus was composed of a substrate of "fine
silt and sand" (Qasim and Sankaranarayanan
1972), and its caloric value was nearly an order of
magnitude less than that of S. alterniflora detritus
(Gosselink and Kirby 1974). The low caloric de-
tritus used in Qasim and Easterson's experiments
may be responsible for the high assimilation
efficiencies (assimilation calculated on ingested
mass would probably be less efficient). We believe
that the wide range of assimilation efficiencies
used in our calculations are representative of most
wild shrimp even if efficiencies for ingested mass
and calories differ considerably. Also, diets of
shrimp are not readily ascertained and more re-
fined estimates may not be practical. Shrimp
grown in intensive culture situations and fed a
prepared diet, however, exist in relatively stable
conditions; energy budgets for these shrimp could
be more accurately determined and used to reduce
feeding costs and possibly to increase production.

The wide tolerance of P. aztecus to temperature
and salinity allows it to make maximum use of
estuaries. Although we obtained evidence indi-
ciating that larger shrimp can regulate hypoos-
motically to a better degree than smaller shrimp,
smaller shrimp can readily grow and survive Gulf

^Unpublished data of senior author

754

salinities (Hoese 1960; Zein-Eldin 1963). Thus dur-
ing years when shrimp populations are unusually
dense in estuaries, shrimp can emigrate from the
estuaries to Gulf waters at a size less than that of
shrimp during average population years. This
may reduce competition for space and food in the
nursery areas (Parker 1970) and result in greater
estuarine shrimp production. The suitability of
estuaries as nursery grounds for shrimp results
from several important circumstances including
food abundance (Zein-Eldin 1963; Copeland and
Bechtel 1974), protection (Hoese 1960), cover (Wil-
liams 1955; Giles and Zamora 1973), substrate
(Williams 1958), absence of competition between
juveniles and adults, and to a lesser degree, the
shrimp's osmoregulatory abilities.

ACKNOWLEDGMENTS

We thank P. E. Schilling for his consultation on
experimental design and analyses of data; J. D.
Woodring for use of his osmometer; N.J. Gazaway
and L. H. Hodges for typing; C. J. Poche for draft-
ing; D. E. Wohlschlag and anonymous reviewers
for editorial comments; and W B. Stickle, R. D.
Adams, and E. M. Bishop for assisting in various
ways. N. L. Mickelberry supported and encour-
aged the senior author throughout this study; her
efforts are particularly appreciated. This research
was submitted by the senior author in partial
fulfillment of the requirements for the degree of
Doctor of Philosophy at Louisiana State Univer-
sity. This report is the result of research supported
by the Louisiana Sea Grant Program, a part of the
National Sea Grant Program maintained by the
National Oceanic and Atmospheric Administra-
tion, U.S. Department of Commerce.

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757

DIEL AND SEASONAL VARIATION IN ABUNDANCE AND DIVERSITY OF
SHALLOW- WATER FISH POPULATIONS IN MORRO BAY, CALIFORNIA

Michael H. Horn'

ABSTRACT

More than 11,000 fishes weighing over 197 kg and representing 21 species were caught in bag seine
hauls taken at quarterly periods (November 1974. May and August 1975, February 1976) in the
southeastern section of Morro Bay. During each sampling period, nine seine hauls were completed, one
at each 3-hour interval over a 24-hour cycle. Atherinops affinis, Cymatogaster aggregata , andLeptocot-
tus armatus accounted for 82''"f of the individuals collected, and A. affinis, C. aggregata, and Mustelus
californicus constituted 84*7^ of the biomass obtained. Larger numbers of individuals and greater
biomass were collected in night hauls, but nearly equal numbers of species were captured during the
day and night. The largest number of species and individuals and greatest biomass were obtained in
May, a period of high reproductive activity, whereas the smallest values of these three parameters were
recorded in August. Diversity (H') for numbers peaked in May (1.56) but reached a maximum for
biomass in November ( 1.91). Lowest diversity for both numbers (0.86) and biomass (0.79) was recorded
in February. Total diversity was 1.63 for numbers and 1.59 for biomass. Wide ranging similarity values
(PS) between consecutive sampling periods for numbers (24-64%) and biomass (2 1-76%) demonstrated
the marked seasonality of the shallow-water fish populations of the bay and primarily reflected the
fluctuations in numbers or biomass of the four most abundant species (above).

The pattern of total diversity and seasonal similarity for Morro Bay fishes was consistent with a
recent model that utilizes diversity and similarity indices together as measures of environmental
quality. Analysis of data from three other localities indicated that the model has the potential for
application in a variety of temperate bay-estuarine habitats.

Morro Bay (Figure 1), an estuary located on the
central California coast (lat. 35°20' N), is one of
the largest and least altered coastal wetlands in
California and a critically important aquatic
habitat. It supports abundant invertebrate
populations and is an integral part of the Pacific
flyway for migratory, water-associated birds
(Gerdes et al. 1974). The bay is the site of rookeries
for two species of herons, and the two endangered
bird species, California least tern and peregrine
falcon, utilize the resources of the bay. Steelhead
occur in the tributary streams and a sizeable sport
fishery exists in the bay. Although more than 60
species of fishes are known to occur in Morro Bay
(Fierstine et al. 1973), little is known of the
dynamics and organization of the fish com-
munities. This lack of information provided the
impetus for the present study.

The main purpose of the study was to assess in
terms of abundance, diversity, and species compo-
sition, the diel (24 h) and seasonal variation of the
fish community occurring in the shallow waters of

'Department of Biology, California State University, Ful-
lerton, CA 92634.

the bay. In addition, the investigation was de-
signed to provide a preliminary test in Morro Bay
of the relationship proposed by Haedrich (1975)
that indices of diversity (measuring species
richness and equitability ) and similarity (measur-
ing seasonal composition and succession) as com-
munity parameters can be used together as indi-
cators of environmental quality of temperate bays
and estuaries. Based on trawl collections of fishes
in nine Massachusetts estuaries and embayments,
Haedrich (1975) showed that in habitats of low
annual (or total) diversity little seasonal change is
reflected in high similarity from season to season
whereas in locations of high annual diversity
lower similarity indicates a greater degree of sea-
sonal change. Low diversities characterized areas
of high pollution and higher diversities those of
lesser pollution. Because of the reportedly low
levels of environmental stress (including human-
induced pollution) in Morro Bay (Gerdes et al.
1974), the expected outcome of the present study
was that total diversity would be relatively high
and similarity between seasons relatively low or
show a wide range of values. Comparisons of total
diversity and seasonal similarity were made be-
tween Morro Bay samples and bag seine collec-

Manuscript accepted December 1979.
FISHERY BULLETIN: VOL. 78, NO. 3, 1980.

759

FISHERY BULLETIN: VOL. 78, NO. 3

MORRO ROCK

120° SO'

Figure l.— Morro Bay, Calif. Shaded rectangle is the sam-
pling area.

tions taken in three other California bay-
estuarine habitats with similar ichthyo faunas.

THE STUDY AREA

Morro Bay is characterized by expansive tidal
flats, central channels, and extensive eelgrass
beds. During spring low tides, the bay is essen-
tially reduced to a series of channels. Although
two creeks empty into the bay, salinities are rela-
tively uniform and approach those of the sea, mak-
ing the bay more of a marine lagoon than a true
estuary.

The study was conducted during quarterly
periods (November 1974, May and August 1975,
February 1976) in the shallow mudflat and chan-
nel area of the southeastern section of Morro Bay
adjacent to Baywood Park (Figure 1). The sub-
strate of the area was characterized by a relatively
uniform mud-sand material, a large percentage of
which was covered mainly by eelgrass, Zostera
marina, and also a red alga, Gracilaria sp., and a
green alga, Ulva sp. Water depth over the study
area was as great as 2 m during high tide periods.

Water temperature and salinity were recorded at
30 cm depth at the time each fish sample was
taken. Temperatures (x±l SD, n = 9) were
13.7°±1.4° C in February, 17.9°±0.5° C in May
19.6°±2.9° C in August, and 11.8°±1.9° C in
November. Salinity values were 30.9±0.7%o in
February 30.0±0.8%o in May 31.1±1.0%o in Au-
gust, and 31.8±1.7%o in November. Tidal ranges
during the 24-h sampling periods varied from 1.0
m (3.3 ft) in May 1975 to 2.2 m (7.3 ft) in February
1976.

METHODS

Fish sampling was performed with the use of a
seine 3 m deep by 29.2 m long with a 2.2 x 2.2 x 2.2
m bag of 6 mm mesh size. The seine was set paral-
lel to the beach from a 3 m skiff and hauled to
shore with polypropylene lines. The distance the
seine was set from the water's edge was 60 m
except at extreme low tides when there was water
only in the channels. At these times (the tows at
1500 h and 1800 h in February), successive hauls
covering small areas were made until the total
area sampled was approximately equal to that of
single hauls at higher tide periods. Samples were
taken at randomly selected intervals along a 400
m stretch of shore. The total sampling area was
approximately 2.4 ha (0.4-0.5% of the total area of
the bay) and each seine haul covered about 0.18 ha.
Based on visual surveys, this stretch of inshore
habitat was typical (in terms of substrate, depth,
and position relative to the mouth and main chan-
nel) of the rather uniform shallow-water condi-
tions in the bay.

During each of the four sampling periods, seine
hauls were made at 3-h intervals over a 24-h cycle
for a total of nine samples per visit. For day-night
comparisons, the second of the two 0900-h samples
was not included each period so that equal num-
bers of day and night samples (four) were com-
pared. All fishes captured, or aliquots of the
largest catches of abundant species, were iden-
tified and sorted, and their standard lengths (SL)
and weights recorded.

The Shannon- Wiener information function H'
was calculated as a measure of diversity in which

H' = - IP, log P,

i = l

where P, is the proportion of individuals (or

760

HORN: ABUNDANCE AND DIVERSITY OF MORRO BAY FISHES

biomass) in the ith species. Calculations were
based on the use of natural logs (logp).

The degree of specific change between samples
from one period to the next was calculated using
the percentage similarity index tPS ) developed by
Whittaker and Fairbanks (1958). Percentage
similarity ranges from 0, when two samples con-
tain no species in common, to 100, when the two
samples are identical in both species composition
and relative abundance. The index is calculated as

PS = 100(1.0 - 0.5 V

P.J)

where P,q is the proportion of individuals
(biomass) in the ith species of sample a and P,^ the
same for sample 6. The basic data are the same as
are required for the calculation of//', i.e., the

number or biomass of individuals in each species
of the sample.

RESULTS

A total of 11,627 fishes weighing 197,747 g were
captured in 36 seine hauls taken during the four
sampling periods (Table 1). Of the 21 species col-
lected, three species, Atherinops affinis,
Cymatogaster aggregata, and Leptocottus ar-
matus, composed almost 829^ of the total individu-
als. A fourth species, Engraulis mordax, contrib-
uted 11.2% of the total. Mustelus californicus, A.
affinis, and C. aggregata, accounted for nearly 84%
of the biomass collected. Leptoco^^j/.s armatus con-
tributed an additional 7% to the total biomass.

For the four sampling periods taken together.

T.'XBLE 1. — Number of individuals and biomass of fish species collected by beach seine in Morro Bay during four 24-h periods from
November 1974 to February 1976. The proportion that each species contributed to total numbers and biomass of each sampling period is
expressed as a percentage (%). (Species ranked according to total numbers for the four periods.)

February 1976 May 1975 August 1975 November 1974 Totals

Individuals Biomass Individuals Biomass Individuals Biomass Individuals Biomass Individuals Biomass

Species No. % g % No. % g % No. % g % No. % g % No. % g %

Atherinops

affinis 351 16.0 3.996 8.0 998 23 4 40,940 41.2 309 14 2 9.099 41 1 1,960 65.5 7.856 29.7 3.618 31.1 61.891 31 3

Cymatogaster

aggregata _ _ _ _ i 499 351 41.049 413 1,530 70.4 6.793 30 6 67 2.2 575 2.2 3.095 26.6 48.417 24.5

Leptocottus

armatus 1.668 76.2 2,063 41 644 151 3,649 3.7 272 125 3.725 16 8 196 6.5 4,444 16.8 2.780 23.9 13.881 7.0

Engraulis

mordax — — — — 909 21.3 1.532 1.5 2 0 09 3 — 397 13.3 280 1.1 1,308 11.2 1.815 0.9

Funduius

parvipinnis 25 1.1 50 0.1 1 — 10 — — — — — 229 7.6 728 27 255 2.2 788 04

Syngnathus

leptort)ynchus 18 0.8 24 0 05 35 0.8 200 02 18 0.8 111 0.5 94 31 850 3.2 165 1.4 1.185 0.6

Ouietula

y-cauda 26 1.2 49 01 64 15 158 02 27 1.2 94 04 2 0.1 2 — 119 1.0 303 02

Micrometrus

minimus 7 0.3 152 0.3 77 1.8 152 0.2 — — — — 6 0.2 149 0.6 90 0.8 453 0.2

Lepidogobius

lepidus 43 2.0 6 0.01 — — _——_ — — 1— 4— 44 0.4 10 —

Embiotoca

lacksoni — — — — II 0 3 171 0.2 9 0 4 340 1.5 17 0.6 1,238 4.7 37 0.3 1.749 0 9

Atfierinopsis

californiensis 25 1.1 3.659 7.3 1 — 280 0.3 1 0.05 230 1.0 5 0 2 1,296 4 9 32 0.3 5,465 2.8

IVIustelus

californicus 19 0.9 39,463 79.3 7 0 2 8,322 84 — — — — 3 0 1 7,296 27 5 29 0 3 55.081 27 9

Dama//c/if/7ys

vacca 1 0.05 240 05 19 0.4 2,390 24 — — — — 2 01 450 17 22 0.2 3,080 1.6

Clupea

fiarengus 1 0.05 88 0 2 — — — — — — — — 13 04 1,276 4.8 14 0,1 1.364 0.7

Cleveland! a

ios 2 0.1 2 — 2 — — — 1 005 2— 1— — — 6 0.1 4 —

Hyperprosopon

argenteum _ _ _ _ 3 0.I 121 — — — — — 1 — 50 0.2 4 — 171 0.1

f^yliobatis

californica ________ 3 0.1 1.760 7.9 — — — — 3 — 1.760 0.9

Cittiarictithys

stigmaeus 3 0.1 1 — — — — — — — — — — — — — 3 — 1 —

Hypsopsetta

guttulata _ _ _ _ 1 _ 320 03— — — — — — — — 1— 320 0.2

Platichthys

stellatus — — ______ 1 0.05 8— — — — — 1— 8 —

Sebastes sp. 1 1 _ 1 — 1 —

Totals 2,189 49,793 4,271 99,295 2,173 22,165 2,994 26,494 11,627 197,747

Total species 13 16 11 16 21

761

FISHERY BULLETIN: VOL 78, NO. y

nearly equal numbers of species were collected
during the day (14) and night (15) (Table 2); how-
ever, significantly greater numbers of individuals
and biomass were obtained during the night (Ta-
ble 3). The PS value between day and night sam-
ples was higher for numbers (68.5%) than for
biomass (43.3%). In February, nearly equal num-
bers of species were collected during the day (9)
and night (10). Greater numbers of individuals
were collected at night but the difference was not
significant. Even though the total biomass ob-
tained during the day in February was greater
than that at night, the night samples were more
frequently and significantly larger based on
paired day-night abundances of each species using

the Wilcoxon signed-ranks test (Table 3). The dis-
crepancy was due to the exceptionally large day-
time contribution (34,246 g) of M. californicus
compared with its much smaller contribution
(3,402 g) to the night samples. The PS value be-
tween day and night samples was much higher for
numbers (83.3% ) than for biomass (40.5% ). In May,
more species were collected at night (14) than dur-
ing the day (8). Greater numbers of individuals
and biomass were obtained at night but the differ-
ence was significant only for numbers. The PS
value between day and night samples was higher
for numbers (60.3%) than for biomass (42.0%). In
August, nearly equal numbers of species were col-
lected during the day (eight) and night (seven).

Table 2. — Relative numbers and biomass (expressed as percentage) offish species collected in four daytime (0900-1800 h> and four
nighttime (2100-0600 h) seine hauls for each sampling period and the total collection in Morro Bay. (Species ranking as in Table 1.)

February 1976

May 1975

August 1975

No indi
Day

viduals
Night

Biomass

No. individuals
Day Night

Biomass

No. individuals
Day Night

Biomass

Species

Day

Night'

Day

Night

Day

Night

Athennops affinis

19.8

7.6

1.1

31.8

331

15.9

78.5

262

33.0

19.7

26.6

53.3

Cymatogaster aggregate

—

—

—

—

14.1

49.5

11.2

56.6

50.5

61.2

9.3

28.1

Leptocottus armatus

66.8

883

0.7

16.8

14.7

14.5

4.6

3.4

8.0

16.7

7.0

17.9

Engraulis mordax

—

—

—

—

34.7

13.4

38

0.8

1.0

—

0.1

—

Fundulus parvipinnis

05

08

—

0.4

—

—

—

—

—

—

—

—

Syngnathus leptorhynchus

0.8

01

—

0.2

1.0

0.8

0.5

0.1

5.0

0.3

2.0

0.1

Quietula y-cauda

1.0

1.4

—

0.4

2.0

1.3

0.3

0.1

1.0

1.9

0.1

0.6

Micrometrus minimus

1.5

0.1

0.4

0.1

0.3

2.8

0.1

0.2

—

—

—

—

Lepidogobius lepidus

—

—

—

—

—

—

—

—

—

—

—

—

Embiotoca lacksom

—

—

—

—

—

0.5

—

0,3

—

—

—

—

Atherinopsis californiensis

4.5

0.4

5.5

14.0

0.1

—

1.0

—

1.0

—

6.4

—

Mustelus californicus

4.0

0,1

92.3

33.1

—

0.2

—

78

—

—

—

—

Damalichthys vacca

—

0.1

—

2.3

—

0.7

—

3.8

—

—

—

—

Clupea harengus

—

0.1

—

0.9

—

—

—

—

—

—

—

—

Clevelandia los

—

—

—

—

—

0.1

—

—

—

0.1

—

—

Hyperprosopon argenteum

—

—

—

—

—

0.1

—

0.2

—

—

—

—

Myliobatis californica

—

—

—

—

—

—

—

—

2.0

—

48.6

—

Citharichthys stigmaeus

0.8

—

—

—

—

—

—

—

—

—

—

—

Hypsopsetta gultulata

—

—

—

—

—

0.1

—

0.5

—

—

—

—

Platichthys stellatus

—

—

—

—

—

—

—

—

—

0.1

—

0.1

Sebastes sp.

—

—

—

—

—

0.1

—

—

—

—

—

—

Totals

398

1.540

37,120

10.272

1,751

2.209

27,435

62.706

200

1,149

3,622

14.111

Total species

9

10

8

14

8

7

Table 2.— Continued.

November 1974

Totals

No. Indi
Day

viduals
Night

Biomass

No. individuals
Day Night

Biomass

species

Day

Night

Day

Night

Atherlnops affinis

65.0

66.4

34.4

28.2

44.3

25.3

33,8

30.9

Cymatogaster aggregata

1.0

3.9

1.3

3.8

9.3

29.7

4.4

40.7

Leptocottus armatus

4.2

6.7

14.3

15.2

15.6

31.5

4.5

8.2

Engraulis mordax

25.7

0.2

2.0

0.1

25.8

4.8

1.6

05

Fundulus parvipinnis

1.6

14.8

0.6

5.6

0.7

3.4

0.1

0,7

Syngnathus leptorhynchus

1.3

5.6

1.1

6.5

1.3

1.8

0.4

0,8

Quietula y-cauda

—

0.2

—

—

1.0

1.2

0.1

0,2

Micrometrus minimus

0.3

01

11

—

0.4

1.0

0.4

0.1

Lepidogobius lepidus

—

0.1

—

—

—

—

—

—

Embiotoca jacksoni

0.7

0.5

50

5.4

0.3

0.3

0.8

0.8

Atherinopsis californiensis

0.1

0.2

3.3

8.0

0.6

01

3.7

2.4

Mustelus californicus

0.1

0.1

35.0

12.7

0.4

0.1

47.8

9.9

Damalichthys vacca

0.1

0.1

1.8

2.0

—

0.3

0.3

29

Clupea harengus

—

1.0

—

11.8

—

0.2

—

1.4

Clevelandia los

0.1

—

—

—

0.1

0.1

—

—

Hyperprosopon argenteum

—

0.1

—

0.5

—

0.1

—

02

Myliobatis californica

—

—

—

—

0.1

—

2.2

—

Citharichthys stigmaeus

—

—

—

—

0.1

—

—

—

Hypsopsetta guttulata

—

—

—

—

—

—

—

0.3

Platichthys stellatus

—

—

—

—

—

—

—

—

Sebastes sp.

—

—

—

—

—

—

—

—

Totals

1,535

1,320

13,038

10,791

3,884

6,218

81.215

97.880

Total species

12

15

14

15

762

HORN: ABUNDANCE AND DIVERSITY OF MORRO BAY FISHES

Table 3. — Day and night fish samples in termsof numbers of individuals and biomass for each sampling period and
the total collection in Morro Bay. Percentage similarity iPS) is explained in the text. "Difference" column indicates
whether day samples were significantly (S) or not significantly (NS) different from night samples based on paired
percentage values for each species (Table 2) (Wilcoxon signed-ranks test for paired values, P'SO. 05, two-tailed).

No

of individuals

Biomass

Sampling period

Day

Night

Percentage
similarity

Difference

Day

Night

Percentage
similarity

Difference

February 1976
May 1975
August 1975
November 1974
Totals

398

1.751

200

1,535

3,884

1.540
2.209
1.149
1,320
6.218

83.3
60.3
78.8
74.1
68.5

NS
S (night -day)

NS
S (night >day)
S (night>day)

37,120
27,435
3.622
13,038
81.215

10,272
62.706
14.111
10.791
97.880

40.5
42.0
430
68.5
54.3

S(night>day)

NS

NS
S (night >day)
S (night>day)

Greater numbers and biomass were obtained at
night but the difference was not significant in
either case. The PS value between day and night
samples was much higher for numbers (78.8%)
than for oiomass (43.0%). In November, more
species were collected at night ( 15) than during the
day (12). Even though the total number of indi-
viduals and total biomass obtained during the day
were greater than the totals at night, the night
samples in both cases were more frequently and
significantly larger based on paired day-night
abundances of each species using the Wilcoxon
signed-ranks test (Table 3). The discrepancy for
individuals was primarily due to a relatively large
daytime contribution (394 individuals) of £■. mor-
dax compared with its much smaller number (3
individuals) in the night samples. The inconsis-
tency for biomass was mainly due to the large
daytime contribution (4,560 g) of M. californicus
compared with its smaller contribution (1,368 g) to
the night totals.

Seven species, A. affinis, C. aggregata, L. ar-
matus, E. mordax, Fundulus parvipinnis,
Syngnathus leptorhynchus, andQuietula y-cauda,
were captured at least once in each of the 3-h
sampling intervals of the four periods. No common
species was collected either only during the day or
only at night. Among the uncommon species,
Myliobatis californica and Citharichthys stig-
maeus were captured only during the day whereas
Clupea harengus, Hyperprosopon argenteum,
Hypsopsetta guttulata, Platichthys stellatus, and
Sebastes sp. were obtained only at night (Table 2).

Marked changes in numbers, biomass, and di-
versity occurred between sampling periods al-
though only four species, A. affinis, Cymatogaster
aggregata, L. armatus, and Mustelus californicus,
were, in different combinations, the most abun-
dant (numbers or biomass) fishes in the samples
(Table 1; Figure 2). Numbers of individuals and
biomass both reached highest levels in May and
lowest levels in August. Diversity //' on numbers

]:■:•'.■'.■] A^. offinis

I 1 C. aggregata

I I Other species

"1 L. armotus

FIGURE 2. — Quarterly data on fish numbers (upper) and
biomass (lower) in the Bay wood Park section of Morro Bay Total
diversity is given by // ' in the center of each cycle. The area of
each circle is proportional to the sample size, the number to the
lower left of each circle is the quarterly diversity H ', and the
number on the connecting arrow is the percentage similarity
between months. Sampling dates are February 1976, May and
August 1975, and November 1974.

763

FISHERY BULLETIN; VOL. 78. NO. 3

was highest in May and lowest in February,
whereas H ' on biomass was greatest in November
but also lowest in February. The PS levels for both
numbers and biomass were highest between May
and August. Lowest PS values were obtained for
numbers between August and November and for
biomass between February and May. Total diver-
sity H' on numbers was similar to that for
biomass.

Of the four common species in the samples, A.
affinis was the most abundant species, composing
Sl'/r of both total individuals and biomass (Table
1). For the total collection, significantly more indi-
viduals and biomass of A. affinis were captured at
night than during the day; however, for quarterly
periods, a significant day-night difference was
recorded only for numbers (night >day) in August
(Table 4). Although somewhat larger individuals
were commonly obtained in night compared with
day samples, the differences were not significant
for any collecting period (Table 4). In February, A.
affinis were bimodal in length frequency (Figure
3), intermediate in mean size (Figure 4), and ob-
tained in small numbers and the smallest
biomass. The contribution of A. affinis to the total
February catch was relatively minor for both
numbers (16% of total) and biomass (8*^ ). In May,
the largest fish of the four periods were captured
and in relatively high numbers. The biomass ob-
tained was the greatest of the study for the species
composing >AY7c of the total May sample. In Au-
gust, the fish were strongly bimodal in length fre-
quency and smaller in mean size. Numbers
reached their lowest level and biomass declined

but nevertheless made up >AV/( of the total Au-
gust sample. In November, the smallest fish of the
study were captured, but they occurred in the
greatest numbers and composed >65% of the total
November sample. The biomass value, because of
the smaller fish, was lower than that for August.

Cymatogaster aggregata, even though absent
from February samples, was the second most
abundant species composing >26'7f of total num-
bers and >2A% of total biomass (Table 1). In all
sampling periods that C aggregata was captured,
larger numbers and greater biomass of the species
were collected at night than during the day; how-
ever, the differences were significant only in May
(Table 4). Although somewhat larger individuals
were, in most cases, captured in night compared
with day samples, the difference was significant
only during May (Table 4). In May, the largest fish
of the study were collected (Figure 4) but a wide
size range was also represented (Figure 3). Num-
bers were relatively high and the biomass ob-
tained was the greatest of the study for the species
composing >AV/c of the total May sample. In Au-
gust, the smallest fish of the study were collected.
Biomass declined but numbers increased relative
to the previous period and made up >70% of the
total August sample. Slightly larger fish were col-
lected in November but numbers and biomass
reached low levels, each composing only about 2%
of the totals.

Leptocottus armatus was the third most abun-
dant species, composing almost 24% of total num-
bers but only 7% of total biomass (Table 1). In all
sampling periods, larger numbers and greater

Table 4. — Number of individuals, biomass, and mean weight of the three most abundant fish species for each sampling period and the
total collection in Morro Bay. "Difference" line indicates whether day (D) samples were significantly (S) or not significantly (NS)
different from night (N) samples based on four ranked samples from each day and each night period for each species (Mann-Whitney
C/-test,P«0.05, two-tailed).

Atherinops affinis

Cymatogaster aggregata

Leptocottus armatus

Individuals

Biomass Mean weight

Individuals Biomass

Mean weight

Individuals

Biomass

Mean weight

Item

(no.)

(g) (g)

(no.) (g)

(g)

(no.)

(g)

(g)

February 1976:

Day

79

412 5.2

— —

—

266

265

10

Night

118

3,264 27.7

— —

—

1,360

1,728

1-3

Difference

NS

NS NS

S(N>D)

S(N D)

NS

May 1975;

Day

580

21,548 37,2

247 3,069

12.4

258

1,259

4.9

Night

351

16,441 46.8

1 ,094 35,480

324

321

2,155

6.7

Difference

NS

NS NS

S (N D) S (N >D)

S(N -D)

NS

NS

NS

August 1975;

Day

66

964 14,6

101 337

33

16

255

15.9

Night

226

7,520 33.3

703 3,959

5.6

192

2,520

13.1

Difference

S(N>D)

NS NS

NS NS

NS

NS

NS

NS

November 1974;

Day

997

4.489 4.5

15 163

10,9

65

1.869

28.8

Night

877

3.045 3.5

52 412

7.9

88

1.645

18.7

Difference

NS

NS NS

NS NS

NS

NS

NS

NS

Totals;

Day

1.722

27.413 15.9

363 3,569

9.8

605

3.648

6.0

Night

1,572

30.270 19.3

1,849 39,351

21 6

1,961

8,048

4.1

Difference

S(N--D)

S (N >D) NS

NS NS

NS

S (N ; -D)

S(N -D)

NS

764

HORN: ABUNDANCE AND DIVERSITY OF MORRO BAY FISHES

Atherinops Cymologaster Leptocottus
offinis aggregate ormatus

Standard Length (mm)

Figure 3. — Length frequencies of the three most abundant fish
species for the quarters sampled in Morro Bay. Sampling dates
are February 1976, May and August 1975, and November 1974.

biomass of L. armatus were collected at night than
during the day; the differences were significant for
the February sample and the total collection (Ta-
ble 4). No significant differences in mean size were
found between day and night samples; slightly

-15

100

Leptocottus ormatus

FEB MAY AUG

Sampling Period

35

25

O)

25*r

15

c

0

o

5

15

NOV

Figure 4. — Mean lengths (dots) and weights (circles) of the
three most abundant fish species for the quarterly sampling
periods in Morro Bay. Sampling dates are February 1976, May
and August 1975, and November 1974.

larger individuals were captured at night in Feb-
ruary and May whereas somewhat larger fish
were collected during the day in August and
November (Table 4). In February, the smallest fish
of the study (Figures 3, 4) were collected in large
numbers. The number of individuals composed
>76% of the total sample; however, biomass con-
tributed only about 4% of the total. In May, fish
size and biomass increased whereas numbers de-

765

FISHERY BULLETIN: VOL. 78, NO. 3

creased. This pattern continued through the Au-
gust and November sampling periods and was in
sharp contrast to that recorded for either A. affinis
or C. aggregata. In August, a small number of
relatively large L. armatus were collected. The
corresponding biomass accounted for more than
l&7c of the total sample. In November, a small
number of larger individuals were captured. The
corresponding biomass made up >16% of the total
sample.

Although only 29 individuals of a fourth species,
M. californicus , were captured during the study,
the fish ranked second in biomass and accounted
for almost 28% of the weight of the total collection
(Table 1). The largest number of M. californicus
were caught in February when they were concen-
trated in the channels as a result of the spring low
tide. The corresponding biomass accounted for
>79% of the total February sample (Figure 2).
Mean size was 834 mm total length and mean
weight was 2,077 g. Too few specimens were col-
lected to compare the abundance and mean size of
individuals in day and night samples.

DISCUSSION

The results of this study indicate that the
shallow-water fish populations of Morro Bay un-
dergo both diel and seasonal variations in abun-
dance (numbers and biomass), diversity, and
species composition. A relatively small number of
species (three) accounted for a large proportion
(82% ) of the total number of individuals collected.
These findings are consistent with the results of
several other studies of temperate bay-estuarine
fish populations that have been reviewed by Allen
and Horn (1975). A pattern that emerged from
these studies was that at least 75% of the sampled
fishes belonged to five or fewer species even though
many more species were collected.

In terms of overall diel variation, more indi-
viduals and greater biomass were obtained in
night samples but nearly equal numbers of species
were collected during the day and night. Very few
species, usually the rarer forms, were captured
either only during the day or only at night.

Although surprisingly little is known concern-
ing day-night differences in utilization of various
habitats by fishes (McCleave and Fried 1975), most
of the information that is available on trawl or
seine samples in inshore waters indicate that
greater catches, either of species, individuals, or
biomass, are obtained at night (e.g., Hoese et al.

1968; Allen 1976; Livingston 1976). McCleave and
Fried (1975) collected fewer total individuals at
night and equal numbers of species day and night
with a beach seine in a Maine tidal cove; however,
they found that four numerically important
species were either present only at night or more
abundant at night.

Diurnal-nocturnal activity patterns and day-
time gear avoidance, particularly by larger fish,
are two factors among a complexity of cir-
cumstances that produce day-night differences in
abundance and composition of net-caught fishes.
Little is known about the first factor for bay-
estuarine fishes although McCleave and Fried
(1975) reviewed the diel patterns of a few inshore
species. They and Hoese et al. (1968) both consid-
ered the second factor to be of importance in their
respective studies. In my study, gear avoidance
probably was one of the factors causing the
generally smaller (numerically) daytime catches.
However, size differences of day vs. night captured
individuals of the three most abundant species
were insignificant in almost all cases thus casting
doubt on the assumption that the larger fish avoid
the seine in the daytime. This reasoning is
perhaps most relevant for L. armatus, the only
nonschooling member of the three-species group.

Quarterly fluctuations in biomass (totals, diver-
sity//', and PS values) were of greater magnitude
than those for numbers, but both parameters ex-
pressed the seasonal dynamics offish populations
in the shallow waters of the bay. In February low
numbers and biomass diversity but relatively high
total biomass represented an early influx of pre-
reproductive adults. The peak numbers and
biomass reached in May corresponded to an abun-
dance of A. affinis and C. aggregata of mature size
(see species accounts below) as well as the pres-
ence of several other species in wide size ranges.
Reduced numbers and biomass in August but high
PS values for both numbers and biomass between
May and August indicated that young-of-the-year
fishes remained in the shallow waters while larger
individuals migrated out of the sampling area.
The large number of individuals and high biomass
diversity recorded for November was the result of a
relatively even distribution of biomass among
juvenile fishes which continued to utilize the in-
shore areas late in the year.

Seasonal abundance and diversity were only
partly attributable to variations in physical fac-
tors. Salinity was not an important factor because
values were relatively high and varied little in the

766

HORN: ABUNDANCE AND DIVERSITY OF MORRO BAY FISHES

sampling area, an indication of the marine charac-
ter of the bay. Tidal ranges were smallest in May,
the period of highest fish abundance, and largest
in February, the month of lowest diversity. Tem-
perature, the environmental factor most fre-
quently recognized as having a major influence on
temperate, shallow-water fish populations (e.g.,
Allen and Horn 1975; Subrahmanyam and Drake
1975; Wallace 1975; Hoff and Ibara 1977), did not
consistently correspond to changes in abundance
and diversity of Morro Bay fish populations: The
largest increase in mean temperature (4° C) oc-
curred between February and May, the transition
period marked by the greatest increase in abun-
dance and diversity. In contrast, the greatest de-
cline in temperature between sampling periods ( 8°
C from August to November) was accompanied by
a substantial increase in abundance and diversity.

The life history patterns of the three most abun-
dant species, A. affinis, C. aggregata, and L. ar-
matus, serve not only to help clarify the seemingly
conflicting responses to temperature of the fish
populations but to illustrate the strategies of
utilization of a bay-estuarine environment by in-
shore fishes. These patterns, recognized in previ-
ous studies, are discussed in turn below for each of
the three species and related to the data I recorded
in Morro Bay.

In his study of A. affinis in Newport Bay in
southern California, Fronk (1969) recognized 3
age classes based on length frequencies ( 80-90 mm
fork length in the first year; 120-130 mm by the
second year; 150 mm after the third year) and
found that spawning occurred from February to
August (peak in May) when the fish were in their
second and third years of life. These findings
correspond to the seasonal length frequencies and
abundance I recorded for A. affinis in Morrow Bay.
In February, the bimodal size distribution in-
cluded small numbers of both immature and
larger individuals, some of which had mature
gonads. May was marked by a high abundance of
large fish, many of which released eggs and milt
upon capture. The substrate of the sampling area
apparently is an optimal spawning site since it is
known (Frey 1971) that A. affinis attaches its eggs
to eelgrass and low-growing algae such as Grnci-
laria sp. The egg masses were frequently found on
the vegetation that was obtained in the seine
hauls. By August, the number of small juveniles
had increased but adult numbers had decreased.
The overwhelming domination of the November
catch by first (mainly) and second year fish is con-

sistent with the apparent movement of postrepro-
ductive adults out of the shallow spawning areas
that become nursery grounds for the juvenile fish.

In his study of C. aggregata in Anaheim Bay in
southern California, Odenweller ( 1975) identified
three age classes based on otolith rings and length
frequencies. Fish in their first year ranged be-
tween 3 1 and 87 mm SL ( x 57 mm), in their second
year between 68 and 115 mm ix 88 mm) and in
their third year between 81 and 117 mm (x 101
mm). Cymatogaster aggregata gives birth in the
spring, primarily in May, according to Bane and
Robinson (1970) and Odenweller (1975). Both
Bane and Robinson ( 1970) and Allen ( 1976) found
that in Newport Bay (southern California) the
majority of adults migrate out of the bay after
breeding in the spring leaving juveniles to utilize
the area as a nursery ground. These adults appar-
ently return to the bay to bear young the following
spring. The seasonal abundance and size frequen-
cies of C. aggregata in Morro Bay are in accord
with the patterns found in the southern California
bays and estuaries. The absence of the fish in Feb-
ruary, its abundance in a wide size range in May
and the presence of almost only small juveniles in
August are indicative of the existence of the mi-
gratory breeding pattern in Morro Bay. The
November catch, consisting of a small number of
juveniles slightly larger than the August indi-
viduals, is further support for the existence of the
pattern. Most of the young-of-the-year, which
mature at or soon after birth (Bane and Robinson
1970), apparently moved out of the shallows after
mating in the late summer or early fall.

According to studies carried out by Jones ( 1962)
in Tomales Bay (near San Francisco) and San
Francisco Bay and Tasto (1975) in Anaheim Bay
(near Los Angeles), L. armatus is a winter
spawner with the peak in January and February.
Sexual maturity is reached near the end of the first
year of life at approximately 120-150 mm SL for
females and 110-120 mm SL for males. Tasto
(1975) found that the Anaheim Bay population
consisted almost entirely of juvenile fish and that
postspawning mortality was apparently high,
based on the absence of the older fish in the
population, a sharp reduction in the catch per unit
effort of adults during the breeding season and the
capture of only two spent females. The data I ob-
tained on L. armatus in Morro Bay are generally
consistent with those of the two studies cited. Fol-
lowing the February sample, which was composed
almost entirely of small juveniles, the frequency of

767

FISHERY BULLETIN: VOL. 78, NO. 3

larger fish progressively increased through the
successive quarterly periods so that in November
the catch was made up of primarily large juveniles
and secondarily offish in the reported mature size
range. Winter spawning was evident even though
few adults were collected. The rarity of adults
could have been due to at least four factors: 1) net
avoidance by adults, 2) postspawning mortality by
adults, 3) migration of adults out of the area after
spawning, or 4) migration of young individuals
into the area after spawning occurred elsewhere.
Although the third factor has been discounted by
Tasto (1975), all four possible causes deserve
further investigation.

In terms of Haedrich's (1975) model for assess-
ing the environmental quality of estuaries and
embayments, Morro Bay can be classified as a
relatively unspoiled habitat in that relatively high
total diversity and a wide range of seasonal
similarity values were recorded. It is instructive,
however, to compare the Morro Bay data with
those available for three southern California
bay-estuarine habitats with similar ichthyo-
faunas: 1) Mugu Lagoon (lat. 34.1° N), 2) Colo-
rado Lagoon (lat. 33.8° N), and 3) upper Newport
Bay I lat. 33.6° N). Mugu Lagoon is a rela-
tively unaltered habitat with diversity and
similarity values comparable to those for Morro
Bay whereas Colorado Lagoon and upper Newport
Bay, two more highly perturbated sites, have lower
diversity values yet wider ranging season-to-
season similarity indices than Morro Bay or Mugu
Lagoon (Table 5).

All four habitats are largely marine in charac-
ter with salinities usually approaching those of
the ocean. Upper Newport Bay is the most fre-
quent exception in that during occasional years of
heavy winter rainfall salinities are greatly re-
duced in the extreme upper portions of the habitat.
Although generally considered to be a relatively
unaltered estuary in southern California (Frey et
al. 1970), upper Newport Bay, unlike Morro Bay, is
subject to pollutant inflow from both urban and
agricultural runoff and a high rate of sedimenta-

tion (with accompanying increased turbidity) dur-
ing years of increased rainfall (e.g., Horn and
Allen in press). Colorado Lagoon, the partially
isolated upper arm of Alamitos Bay, receives pol-
lutants and nutrients from street runoff and
heavy recreational use especially during the
summer months when eutrophic conditions
usually develop (Allen and Horn 1975). The lower
reaches of both Newport Bay and Alamitos Bay
have been altered by extensive marina develop-
ment and by modification of their openings to the
sea. Mugu Lagoon is in a relatively undisturbed
condition primarily because it has been for more
than 30 yr under ownership of the U.S. Navy
which restricts access to the area (MacDonald
1976). The fish faunas of these three environments
are basically similar to that of Morro Bay with
three of the five most abundant species in upper
Newport Bay and Mugu Lagoon and four of the five
most abundant species in Colorado Lagoon also in
the top five in Morro Bay.

The sampling procedure (bag seine deployed
from shore) and substrate conditions (varying
mud to sand) were similar for the four habitats.
Collections were made monthly in the locations
other than Morro Bay; quarterly data were ex-
tracted for comparison with the Morro Bay values.
The main difference in the collection of data
among the four locations was the type of beach
seine used. In Colorado Lagoon, as in Morro Bay, a
29.2 m seine with 6 mm mesh in the bag was used,
whereas in Mugu Lagoon and upper Newport Bay
a 15.2 m seine with 3 mm mesh in the bag was
employed. The difference in effectiveness of the
two types of seines is incompletely known but con-
sidered to be slight (M. H. Horn and L. G. Allen
unpubl. data); moreover, the discrepancy is judged
to be of minor importance since it does not parallel
the diversity-similarity differences among the
four ichthyofaunas (Table 5).

Quarterly data (February-November 1977) from
bag seine samples of 29 species in Mugu Lagoon
(Quammen^) yielded a total H ' value of 1.52 and
PS values ranging from 30 to 627f (Table 5). Thus,

Table 5. — Number of species (S), Shannon- Weiner diversity (W), and season-to-season percentage similarity values (PS) based on
quarterly bag seine collections of fishes in four bay-estuarine habitats in California. Environmental status is a qualitative assessment
(see discussion section).

Bay-estuary

Location (latitude)

H'

PS

Environmental status

Data source

Morro Bay
Mugu Lagoon

Colorado Lagoon
Upper Newport Bay

Central California (35.3 N)
Southern California (34 1" N)

Southern California (33.8 N)
Southern California (33.6 N)

21

1.63

24-64

Relatively unaltered

This study

29

1.52

30-62

Relatively unaltered

M L Quammen
(unpubl. data)

16

075

2-57

Highly altered

Allen and Horn (1975)

23

066

13-96

Moderately altered

Horn and Allen (in press)

768

HORN ABUNDANCE AND DIVERSITY OF MORRO BAY FISHES

the diversity and similarity pattern for Mugu La-
goon is close to that for Morro Bay as would be
expected for an unspoiled habitat. Data obtained
during quarterly periods (February-November
19781 from bag seine collections of 23 species in
upper Newport Bay (Horn and Allen in press) re-
sulted in a total H' value of 0.66 and PS indices
ranging from 13 to dWc (Table 5). Quarterly bag
seine data (February-November 1973) for 16
species in Colorado Lagoon (Allen and Horn 1975)
produced a total //' value of 0.75 andPS measures
ranging from 2 to 57Vr (Table 5). According to the
Haedrich (1975) model, the relatively low diver-
sity values for upper Newport Bay and Colorado
Lagoon should be accompanied by high similarity
values and dominance of the community by one or
a few species. However, a combination not
explicitly recognized by Haedrich, that of low di-
versity and wide ranging seasonal similarity, is
evident in these two habitats. Low//' values com-
bined with variable PS values indicate a high
seasonal abundance of one or a few species. This
condition is realized in that in each case there was
an extreme summer abundance of only one
species — A. affinis in upper Newport Bay and £.
mordax in Colorado Lagoon. In the most highly
stressed habitat, low diversity, and a high relative
abundance of a single species over the entire year
(i.e., high seasonal similarity) would be predicted
by the model. Thus, upper Newport Bay and Col-
orado Lagoon would be rated as intermediate in
environmental quality. In general, Colorado La-
goon could be considered as the more highly per-
turbated of the two habitats (Table 5). The heavy
rainfall of 1978, the year in which the upper New-
port Bay data were collected, probably was a
primary factor in producing the low diversity and
divergent similarity values (Horn and Allen in
press).

The use of the two indices in combination ap-
pears to have greater resolution and predictive
strength than the use of only species diversity as
an indicator of pollution, as has been proposed by
Bechtel and Copeland (1970). Diversity H' pro-
vides information on species richness and
equitability but not on species composition. The
absolute replacement of one species by another,
possibly a result of environmental alteration.

^Millicent L. Quammen, graduate student, Department of
Biological Science, University of California, Santa Barbara, CA
93106, pers. commun. August 1979.

would not be detected by a diversity measure nor
would the seasonal succession of individual
species. An index of similarity provides an indica-
tion of the magnitude and direction of seasonal
dynamics.

The diversity-similarity approach holds prom-
ise as one of the procedures for distinguishing the
relative quality of bay-estuarine habitats and de-
serves to be tested in additional localities. The
results for Morro Bay also underscore the need for
a more thorough knowledge of its fish com-
munities since it is a relatively pristine habitat
that may be subject to a number of alterations in
the future (Gerdes et al. 1974).

ACKNOWLEDGMENTS

I especially thank S. Marie Harvey who contrib-
uted significantly to the completion of this study.
She ably assisted in the field work, meticulously
recorded and compiled the data, and carefully
drafted the figures. I greatly appreciate the efforts
of Larry Allen, Gregory Smith, and Wayne White
who showed unwavering support of the project
throughout its duration. They, along with James
Knost, Linda Sims, Robert Sims, and John Tiede-
man, performed tirelessly and enthusiastically
during the long hours of field work. I am grateful
to the numerous other people who assisted with
the data collection, including David Chapman,
Myra Chapman, Gary Devian, Richard Dumke,
Wanda Halbakken, Kathryn Heath, Kheryn
Klubnikin, Lee Lorenzen, Margaret Neighbors,
Sarah Swank, Denise White, and Robert White. I
extend sincere thanks to Millicent Quammen who
kindly made available to me her unpublished data
on Mugu Lagoon fishes. Financial assistance and
material support were provided by the De-
partment of Biology, California State University,
Fullerton.

LITERATURE CITED

Allen, L. G.

1976. Abundance, diversity, seasonality and community
structure of the fish populations of Newport Bay, Califor-
nia. M.A. Thesis, Calif. State Univ., Fullerton, 108 p.
Allen, L. G., and M. H. Horn.

1975. Abundance, diversity and seasonality of fishes in
Colorado Lagoon, Alamitos Bay, California. Estuarine
Coastal Mar. Sci. 3:371-380.

Bane, G., and M. Robin.son.

1970. Studieson i\\e shiner Y)erch,Cymatogasteraggregata
Gibbons, in upper Newport Bay, California. Wasmann J.
Biol. 28:259-268.

769

FISHERY BULLETIN: VOL. 78, NO. 3

BECHTEL, T. J., AND B. J. COPELAND.

1970. Fish species diversity indices as indicators of pollu-
tion in Galveston Bay, Texas. Contrib. Mar Sci. 15:103-
132.

FIERSTINE, H. L., K. F. KLINE, AND G. R. GARMAN.

1973. Fishes collected in Morro Bay, California between
January, 1968, and December, 1970. Calif. Fish Game
59:73-88.

FREY,H.W. (editor).

1971. California's living marine resources and their
utilization. Resour. Agency, Calif. Dep. Fish Game,
148 p.

FREY, H. W, R. F KLEIN, AND J. L. SPRUILL.

1970. The natural resources of Upper Newport Bay and
recommendations concerning the bay's development.
Resour. Agency, Calif. Dep. Fish Game, 68 p.

FRONK, R. H.

1969. Biology of Atherinops affinis littoralis Hubbs in
Newport Bay. M.S. Thesis, Univ. California, Irvine,
106 p.

GERDES, G. L., E. R. J. Primes, and B. M. Browning.

1974. Natural resources of Morro Bay, their status and
future. Calif Dep. Fish Game Coastal Wetlands Ser.
8:1-103.

HAEDRICH, R. L.

1975. Diversity and overlap as measures of environmental
quality Water Res. 9:945-952.

HOESE, H. D.,B. J. COPELAND, F. N. MOSELEY, AND E. D. LANE.
1968. Fauna of the Aransas Pass Inlet, Texas. III. Diel and
seasonal variations in trawlable organisms of the ad-
jacent area. Tex. J. Sci. 20:33-60.

HOFF, J. G., AND R. M. IBARA.

1977. Factors affecting the seasonal abundance, composi-
tion and diversity of fishes in a southeastern New England
estuary. Estuarine Coastal Mar. Sci. 5:665-678.

Horn, M. H., and L. G. Allen.

In press. Ecology of fishes in upper Newport Bay, Califor-
nia: seasonal dynamics and community structure. Calif.
Dep. Fish Game, Mar. Resour. Tech. Rep.

Jones, a. C.

1962. The biology of the euryhaline fish Leptocottus ar-
matus armatus Girard (Cottidae). Univ. Calif. Publ.
Zool. 67:321-367.

Livingston, r. j.

1976. Diurnal and seasonal fluctuations of organisms in a
north Florida estuary. Estuarine Coastal Mar. Sci.
4:373-400.
MACDONALD, K. B.

1976. The natural resources of Mugu Lagoon. Calif. Dep.
Fish Game, Coastal Wetland Ser 17:1-119.

McCleave, J. D., AND S. M. Fried.

1975. Nighttime catches of fishes in a tidal cove in
Montsweag Bay near Wiscasset, Maine. Trans. Am.
Fish. Soc. 104:30-34.
Odenweller, D. B.

1975. The life history of the shiner surfperch Cymatogas-
ter aggregata Gibbons, in Anaheim Bay, California. In E.
D. Lane and C. W. Hill (editors). The marine resources of
Anaheim Bay p. 107-115. Calif. Dep. Fish Game, Fish
Bull. 165.
SUBRAHMANYAM, C. B., AND S. H. DRAKE.

1975. Studies on the animal communities in two north
Florida salt marshes. Part I. Fish communities. Bull.
Mar. Sci. 25:445-465.
TASTO, R. N.

1975. Aspects of the biology of Pacific staghom sculpin,
Leptocottus armatus Girard, in Anaheim Bay. In E. D.
Lane and C. W Hill (editors). The marine resources of
Anaheim Bay p. 123-135. Calif. Dep. Fish Game, Fish
Bull. 165.

Wallace, J. H.

1975. The estuarine fishes of the East coast of South Af-
rica. I. Species composition and length distribution in the
estuarine and marine environments. II. Seasonal abun-
dance and migrations. S. Afr. Assoc. Mar. Biol. Res.,
Oceanogr. Res. Inst. Invest. Rep. 40, 72 p.

Whittaker, R. H., and C. W. Fairbanks.

1958. A study of plankton copepod communities in the
Columbia Basin, southeastern Washington. Ecology
39:46-65.

770

MOVEMENTS OF TAGGED AMERICAN LOBSTER, HOMARUS AMERICANUS,

OFF RHODE ISLAND^

Michael J. Fogarty,^ David V. D. Borden, ^ and Howard J. Russell"

ABSTRACT

In 1974 and 1975 a total of 3,063 American lobster, Homarus americanus. were tagged and released at
five sites along the Rhode Island coast and on the adjacent continental shelf. Analyses were based on
671 returns with sufficient information to assess movement patterns. Lobster movements at inshore
locations were generally localized; the mean distance between release and recovery sites ranged from
5.5 to 10.4 km. Intense fishing effort in inshore areas resulted in a disproportionate number of re-
turns within 30 days of release. Rayleigh tests demonstrated a nonuniform (P<0.01) distribution
of return directions at each site. Mean vector angles ranged from 164.5° to 193.7° from true north at
inshore locations.

Lobsters tagged and released on Cox Ledge, 35 km southeast of Narragansett Bay, migrated to the
outer continental shelf in late fall and winter The mean distance travelled was 41.6 km and the average
time between release and recapture was 235.3 days. A Rayleigh test indicated that the distribution of
return directions was nonuniform iP<0.01) and the mean vector angle was 158.8° from true north.

Analyses of the movement patterns of the Ameri-
can lobster, Homarus americanus, in coastal
waters have typically revealed little evidence of
extensive migrations. In a study designed to
examine seasonal movements, Wilder and Murray
(1958) noted a mean dispersion radius of <1.6 km
for tagged lobsters released off the coast of Nova
Scotia. Wilder (1963) reported movements averag-
ing 13.5 km for tagged lobsters at large 10-12 mo
off Price Edward Island. Bergeron (1967) con-
cluded that lobsters undertake a seasonal
onshore-offshore migration of about 10 km off the
Magdalen Islands of Quebec. In tagging experi-
ments conducted in the Gulf of Maine, Cooper
(1970) and Krouse^ noted generally localized
movements. Dow (1974) indicated, however, that
large lobsters ( >127 mm carapace length, CL) may
undertake migrations of over 140 km. Morrissey

'This study was conducted in cooperation with the U.S. De-
partment of Commerce, National Marine Fisheries Service,
under grant 03-4-043-360.

^Division of Fish and Wildlife, Rhode Island Department of
Environmental Management, Wickford, R.I.; present address:
Northeast Fisheries Center Woods Hole Laboratory, National
Marine Fisheries Service, NOAA, Woods Hole, MA 02543.

^Division of Fish and Wildlife, Rhode Island Department of
Environmental Management, 150 Fowler St., Wickford, RI
02852.

■•Division of Fish and Wildlife, Rhode Island Department of
Environmental Management, Wickford, R.I.; present address:
New England Regional Fisheries Management Council, Pea-
body MA 01960.

^Krouse, J. S. 1977. Lobster tagging project No. 3-228-R.
Project completion report. Maine Department of Marine Re-
sources, West Boothbay Harbor, Maine, 29 p.

(1971) presented evidence for directed movements
averaging 26.1 km for ovigerous and sublegal-
sized lobsters in the southern Gulf of Maine. Lund
et al.^ reported that lobsters tagged in western
Long Island Sound were nonmigratory while
others tagged in eastern Long Island Sound un-
dertook migrations to the edge of the continental
shelf.

In contrast, Cooper and Uzmann (1971) and Uz-
mann et al. (1977) demonstrated an extensive in-
shore spring migration for lobsters tagged on the
outer continental shelf. Saila and Flowers (1968)
reported that ovigerous females displaced from
continental shelf waters to Narragansett Bay, R.I.,
tended to return to the area of first capture.

The present study was designed to examine var-
ious aspects of the population dynamics of lobster
off the coast of Rhode Island. In this paper we
describe the movement and migratory behavior of
lobster in local waters. The work was part of a
coast-wide research effort sponsored by the
State-Federal Lobster Management Program
under the auspices of the U.S. Department of
Commerce, National Marine Fisheries Service,
with the objective of developing a comprehensive
management strategy for lobster in the territorial
waters of the United States. >^

'^Lund.W A., L.L.Stewart, and C.J. Rathbun. 1973. Inves-
tigation on the lobster. Completion report. Commercial Fisheries
Research and Development Act. Project 3-130-R, 189 p. Univ.
Connecticut, Storrs, Conn.

Manuscnpt accepted February 1980.
FISHERY BULLETIN: VOL. 78. NO. 3, 1980.

771 -^7

FISHERY BULLETIN: VOL. 78, NO. 3

METHODS

In 1974 and 1975, 3,063 lobsters (55-176 mm CD
were tagged and released at five general locations
off the Rhode Island coast and on the adjacent
continental shelf (Figure 1).

Lobsters were tagged using the sphyrion anchor
tag(Scarratt andElson 1965). The tag consisted of
an encoded yellow plastic tube (2 mm in diameter)
attached to a stainless steel anchor by a monofila-
ment thread. The anchor was inserted with a
hypodermic needle into the right or left dorsal
extensor muscle of the lobster through the mem-
brane posterior to the margin of the carapace.
Carapace length, sex, molt status, and physical
condition were recorded for each tagged lobster.
We obtained lobsters used in tagging experiments
directly aboard commercial lobster vessels.
Lobsters were tagged at sea and released as close
to the point of capture as possible. However, on 20
December 1974, 231 lobsters captured on the mid-
continental shelf (Midshelf) were released on Cox
Ledge. This displacement ( =60 km) was necessary

to avoid several foreign trawlers which moved into
the area during tagging operations.

Rewards of $2 for the return of the tag alone and
$5 for the return of the lobster and tag were paid.
Information on the date and location of capture
were requested for each recapture. The study was
publicized through the local news media, posters
describing the study distributed to shellfish deal-
ers, and personal contact with fishermen.

For detailed evaluation of directional compo-
nents of movement we followed the approach of
Saila and Flowers (1968). The specific test statis-
tics and directional components computed were

Mean vector angle

0 = arc tan

Lir cos ej

Mean square dispersion coefficient (km^/d)

-4 [^

r^ ( Vr cos e)^ + ( Vr sin O)^
t It

]

North-south directional
component (km/d)

V =

^r cos 9

NARRAGANSEtT BAY

^ SAKONNET RIVER

RHODE ISLAND
SOUND

^'

o

cox lEDCE

MIDSHELF O

Figure l . — Location of tagging sites for American lobster in the
coastal waters of Rhode Island and on the adjacent continental
shelf

East-west directional
component (km/d)

Rayleigh test statistic

y., _ ^r sin 6

Z = RVn

where R = [{^ sin 6)2 + ( V cos 9)2]
n = number of individuals
9 = direction of travel from an arbitrary
reference point
t = time in days from release
r = straight line distance (km) of travel.

All angles are presented as deviations from true
north (°T). The Rayleigh test is a test for uniform
concentration of points around a circle of unit
radius (Batschalet 1965).

The mean square dispersion coefficient is a mea-
sure of undirected or random movement based on
diffusion theory (Beverton and Holt 1957; Jones
1959, 1966). The dispersion coefficient is a com-
pound parameter dependent on both rate of travel
and the mean distance travelled without di-
rectional change (Jones 1959). The quantities V
and V indicate directional or nonrandom compo-
nents of movement. These parameters measure
the mean rate of group movement of tagged indi-
viduals in the north-south and east-west planes.

772

FOGARTY ET AL.: MOVEMENT OF AMERICAN LOBSTER OFF RHODE ISLAND

RESULTS

Inshore Locations

To date, 450 lobsters tagged and released at
coastal sites have been recovered with sufficient
information to assess movement patterns (Table
1). Due to intensive fishing effort for lobster along
the Rhode Island coast, a disproportionate number
of tags were returned within 30 d of release (Fig-
ure 2); the mean time at large was 48.6, 34.7, and
48.6 d for lobsters released in Narragansett Bay,
Rhode Island Sound, and the Sakonnet River. Most
lobsters tagged at inshore locations were recap-

tured within 6 km of the release site (Figure 3),
possibly reflecting the short time at large. The
distance between release and recovery sites aver-
aged 6.9, 10.4, and 5.5 km at the Narragansett Bay,
Rhode Island Sound, and Sakonnet River loca-
tions. Distance travelled tended to increase with
time up to 90 d at large at each inshore location
although high variability made clear trends diffi-
cult to discern (Figure 4).

An initial examination of straight-line tracks
between release and recapture sites revealed a
general southerly trend in movements for lobsters
released at inshore tagging sites ( Figure 5). These
plots also demonstrated that some inshore lobsters

Table l. — Release and recapture data for American lobsters tagged in 1974 and 1975 off Rhode Island. Locales are
given in Figure 1. Number recaptured refers to the number of returns with adequate information to evaluate
movements. Cox Ledge-Midshelf indicates lobsters captured on the midcontinental shelf iMidshelf) and released on
Cox Ledge.

Number

Recapt

jred

Carapace length (mm)

at release

Release site

Release period

released

No.

%

Mean

SE

Range

Sakonnet River

15May-31July 1975

645

147

22.79

80.57

0.257

62.0-1030

Rhode Island Sound

9 May-21 Aug. 1975

543

115

21.18

79.02

.286

55.0-108.0

Narragansett Bay

9May-15Nov. 1975

470

188

40.00

7392

.212

58.0-1020

Cox Ledge

11 Nov.-5Dec. 1974

612

157

25.65

8270

.454

62.0-134.0

Cox Ledge- MIdshelf

20 Dec. 1974

231

29

12.55

96.67

1 201

64.0-1670

MIdshelf

29 0ct.-18Nov. 1974

562

34

6.05

86.92

.637

65.0-176.0

70-1

rn SAKONNET RIVER N=147
H NARRAGANSETT BAY N = 188
■ RHODE ISLAND SOUND N = 115

11-20 21-30

3i-40 ' 41-50 " 51-60 ■ 61-70 71
DAYS AT LARGE

91-100

>100

FIGURE 2. — Number of tag returns for
American lobster released at inshore lo-
cations off Rhode Island as a function of
time at large.

100-

80-

z
cc

CD

s

z-

rn SAKONNET RIVER N=147
^ NARRAGANSETT BAY N=188
■ rHODE ISLAND SOUND N = 115

-8 ' 61-10
DISTANCE TRAVELLED (km)

Figure 3. — Number of tag returns for
American lobster released at inshore lo-
cations off Rhode Island as a function of
distance travelled.

773

FISHERY BULLETIN: VOL. 78, NO. 3

1

172

80-

10-
6-

4-

40-1

-^30-

E

uj 20-
U

z
<

(/)

10-

50-

40-

30-

20-

10

02111 22)

SAKONNET
RIVER

014(4 361

()22

<>1)

o4

♦2

(170

(t4

(})11

149

I t I I I I I I

NARRAGANSETT
BAY

-■10

17

:)12

()4

*2

()18

174

I I I I I I

1-n

(Q3

A3

■6

()6

RHODE ISLAND
SOUND

:'5

D52

4>5

<>2

^)2

' I I I I I I I I I I . ,

0- 16- 31- 46- 61- 76-91- 106-121- 136-151- 166-^on
15 30 45 60 75 90 105 120 135 150 165 180
DAYS AT LARGE

Figure 4. — Distance travelled {x±l SE) as a function of time at
large for tagged American lobster released at inshore locations
off Rhode Island. Open triangles denote single observations for
the time period. Sample sizes are specified beside each mean with
an associated standard error Standard errors are provided in
parentheses for observations falling within ranges of truncated
ordinate.

774

FOGARTY ET AL.: MOVEMENT OF AMERICAN LOBSTER OFF RHODE ISLAND

Figure 5. — Straight linedistance between release and recovery
sites for American lobster at inshore locations off Rhode Island.
Release locations are composites of several release sites in each
area. Total distance travelled is noted for tracks which are trun-
cated by borders.

did undertake extensive movements. Appropriate
test statistics and directional components (Saila
and Flowers 1968) were computed for each total
data set and for data partitioned according to time
at large (Table 2). Missing data for some returns
prevented the use of all the recoveries for these
analyses. Mean vector angles (G) for the three
locations ranged from 164.53°(T) to 193.69°(T),
and Rayleigh tests indicated a nonuniform dis-
tribution of returns at each inshore location (Table
2). In general, the north-south vector components
were consistently stronger than the east-west
components for each location. When partitioned
by time at large, the relative magnitude of the
north-south and east-west vector components
were more nearly equal for the first time period
(0-20 d) at the Sakonnet River site, possibly re-
flecting an initial random dispersal of released
lobsters. The lack of a statistically significant
mean vector bearing for this period (Table 2) sup-
ports this inference.

The consistently low estimates of V ' for lobsters
tagged at inshore locations were due, in part, to
physiographic constraints since east-west move-
ments were often limited by the coastline, particu-
larly in Narragansett Bay ( Figure 1). The negative
north-south vector components were indicative of

net southerly movement since the cosine of angles
ranging from 90° to 270° would be negative. Simi-
larly, negative values of V imply a westerly dis-
placement since the sine of angles from 180° to
360° would be negative.

The mean square dispersion coefficient (a^) var-
ied considerably by location and the time period
under consideration (Table 2). The quantity a^
measures the relative degree of undirected move-
ment of any individual with respect to the group
directional average. Some caution is necessary in
interpreting these values since dispersion coeffi-
cients are likely to be overestimated when move-
ments are nonrandom (Jones 1959).

To examine the possibility of directed seasonal
movements, we pooled data from inshore release
locations and regrouped them according to release
period and time at large. We compared movement
statistics for lobsters released prior to 1 July 1975
and recaptured prior to 1 September 1975 with
those released after 1 July 1975 and recaptured
prior to 1 September 1975 (Table 3). We noted a
nonuniform distribution of returns at all levels of
analysis (Table 3i. The north-south directional
components consistently dominated the east-west
components for both groups. The negative V val-
ues reflect the strong southerly directionality for
both groups while the east-west components ( V")
varied considerably when further partitioned by
time at large (Table 3 ). For lobsters released after 1
July 1975 the north-south vector components were
two to three times higher than for late spring-
early summer releases, indicating a sharp in-

TaBLE 2. — Mean vector angle (B) from true north, mean square dispersion coefficient (a^), north-south (V) and east-west (V)
directional components, Rayleigh test statistics {R and Z ) and sample size (n)for lobsters released in the Sakonnet River, Narragan-
sett Bay, Rhode Island Sound, and Cox Ledge. The mean square dispersion coefficient is a measure of random movements; V and V
indicate nonrandom components of movement. Negative values of V and V are indicative of net southerly and westerly movements.
The Rayleigh test is a test for uniform concentration of points around a circle of unit radius.

Days at

O

a^

V

V

Location

large

(°T)

(km2/d)

(km,d)

(kmd)

R

Z

n

Sakonnet River

0-20

215.236

1,952

-0.077

-0,054

10225

2,133

49

21-60

211.748

4.966

- .119

- .074

11 391

4.805"

27

>61

184.469

25.574

- .104

- .008

6.418

1.647

25

Total

193.694

8.654

- ,105

- .025

26,899

7.164"

101

Narragansett Bay

0-20

175,072

2.870

- .294

.025

34 238

13630"

86

21-60

178.854

11.012

- .293

.006

31.339

20 043"

49

>61

164.301

2,471

- .054

.015

24.982

17336"

36

Total

173.353

5 700

- .123

.014

90.178

47.556"

171

Rhode Island Sound

0-20

167,967

8,597

- .340

.073

26 958

11.913"

61

21-60

163498

2,872

- .246

.073

23.207

17.951"

30

>61

163212

9,840

- .140

.042

12-650

7.620"

21

Total

164,530

7,502

- .199

.055

62.241

34 589"

112

Cox Ledge

0-180

162,690

38,155

-1.244

.388

22559

14.968"

34

181-270

140637

16.365

- .062

.051

8,077

1.553

42

271-360

150 263

6.900

- .048

.027

15.856

4.261

59

>361

150,549

14166

- .104

.059

3 222

1.483

7

Total

154,847

4931

- .120

056

37863

10096

142

•p<o.oi.

775

FISHERY BULLETIN: VOL. 78. NO. 3

Table 3. — Movement statistics for lobsters released prior to 1 July 1975 and recaptured prior to 1 September 1975 (spring-early
summer) and lobsters released after 1 July 1975 and recaptured prior to 1 September 1975 (late summer). Data are pooled over release
locations in Narragansett Bay, Rhode Island Sound, and the Sakonnet River. See Table 2 for explanation of symbols.

Days at

t)

a2

V

V

Season

large

(°T)

(km^/d)

(km/d)

(km/d)

R

Z

n

Spring-early summer

0-15

190.657

3.038

-0.156

-0.029

22.287

5.458"

91

16-30

165.275

1.368

- .104

.027

16 365

5 251"

51

31-45

183151

2.247

- .144

- .008

16.946

9,573

30

46-60

180 343

22126

- .249

- .001

13945

9.260"

21

>61

183380

12 854

- .110

.006

22201

14.935"

33

Total

178854

5852

- .138

.003

91.056

36 687"

226

Late summer

0-15

161.321

7.121

- .473

160

33975

18035"

64

16-30

188.365

4.527

- .479

- .070

15.036

10.765"

21

-30

202-517

8.495

- .434

- 180

4.531

4.105"

5

Total

179.427

6.808

- .469

- 005

52.447

30.563"

90

"P<001

crease in directional movement in this period. Es-
timates of the mean square dispersion coefficient
also increased in the late summer period, indicat-
ing a general increase in activity levels. The rela-
tive magnitude of the increase in random move-
ment (as measured by a'^) was less striking than
the increase in directed movement, however ( Table
3).

A two-way fixed factor analysis of variance was
used to determine the effects of size and sex on
distance travelled for each inshore release loca-
tion. The three inshore sites differed slightly in
release periods (Table 1) and were therefore
treated independently to eliminate any possible
seasonal effects. Lobsters were categorized on the
basis of release size (^60, 61-70, 71-80, 81-90, >91
mm CD and sex (male, female, ovigerous female).
No significant differences (P<0.01) were noted by
size, sex, or the size-sex interaction at any of the
three release locations. The data were treated
with a logg (x+1) transform prior to analysis.

Offshore Locations

In contrast to lobsters tagged at coastal loca-
tions, those tagged and released on Cox Ledge
exhibited extensive movements. The mean dis-
tance travelled was 41.6 km and the average time
between release and recapture was 235.3 d. Re-
turn rates were relatively high for the first 30 d,
and subsequently increased for lobsters at large
over 240 d (Figure 6). Of 157 lobsters recovered
with adequate information to evaluate move-
ments, 117 nA.b'7c ) were recaptured within 60 km
of the release site (Figure 7). Examination of dis-
persal as a function of time at large indicated
large-scale movements within 60-120 d of libera-
tion while recoveries after 240 d were progres-
sively closer to the release site (Figure 8). Plots of

530'

D

cox LEDGE N = 157

3 COX LEDGE- MIDSHELF
N = 29

r-r

rki,.41

61-
VO

1^0 180 210 240
DAYS AT LARGE

2 70 100 330 360 390

Figure 6. — Number of tag returns for American lobster re-
leased on Cox Ledge and lobster displaced from the Midshelf
tagging site to Cox Ledge (Cox Ledge- Midshelf) as a function of
time at large, Rhode Island vicinity.

80-

(rt60'

3

LU

a.

UJ

m

20'

[ 1 COX LEDGE N=157

J COX LEDGE- MIDSHELF
N=29

5 1-' 8f)l-' 'ODn' 120i-' )40l-' -.160 '
80 100 120 MO 160

100 120 140

DISTANCE TRAVELLED (km)

Figure 7. — Number of tag returns for American lobster re-
leased on Cox Ledge and lobster displaced from the Midshelf
tagging site to Cox Ledge (Cox Ledge-Midshelf) as a function of
distance travelled, Rhode Island vicinity.

776

FOGARTY ET AL.: MOVEMENT OF AMERICAN LOBSTER OFF RHODE ISLAM)

200-

COX LEDGE

lAO-

z
<

v>

a

80

40-

^ |:

2 ,3

*27

II I I I I ■ 1 > I I I I I I

0- 31- 61- 91- 121- ISl- 181- 211- 241- 2/1- JOI- 3jl- 361- j.390
30 60 90 120 150 180 210 240 270 300 330 360 390
DAYS AT LARGE

FIGURE 8. — Distance travelled (x±l SE) as a function of time at
large for American lobster tagged and released on Cox Ledge, off
Rhode Island. Sample sizes are specified beside each mean with
an associated standard error.

straight-line distance between release and recov-
ery sites indicated that these long distance mi-
grants travelled to the outer continental shelf
(Figure 9).

Tagging experiments conducted on the outer
continental shelf revealed a shoal ward migration
in late spring and summer (Cooper and Uzmann
1971; Uzmann et al. 1977). The offshore migration
in late fall and winter observed in the present
study complements these findings and indicates a
seasonal interchange between areas.

The mean vector angle for recovered tagged
lobsters was 154.8°(T) at the Cox Ledge site and
Rayleigh tests indicated a nonuniform distribu-
tion of returns (Table 2). The north-south vector
component was substantially higher than the
east-west component for the first 180 d at large,
reflecting the strongly directed offshore move-
ment. The relative magnitude of the north-south
and east-west vector components were more
nearly equal for lobsters at large over 180 d, indi-
cating little directed movement. This is reflected
in the nonsignificant mean vector bearing for
lobsters at large between 181 and 270 d (Table 2).

A two-way fixed factor analysis of variance was
used to examine the effects of size and sex on
distance travelled for lobsters tagged and released
on Cox Ledge. Lobsters were grouped by release
size («90, 91-100, 101-110, 111-120, 121-130, ^131
mm CL) and sex (male, female, ovigerous female)
and the data were transformed (log;.x+l) prior to
analysis. No significant differences (P<0.01) were
noted by size, sex, or the size-sex interaction.

Figure 9. — Straight line distance between release and recap-
ture sites for American lobster tagged and released on Cox
Ledge, off Rhode Island. Release location is a composite of four
release sites on Cox Ledge. Total distance travelled is noted for
tracks which are truncated bv borders.

Low return rates (n=29) for lobsters displaced
from the Midshelf site to Cox Ledge prevented
detailed analysis of movement patterns. The dis-
placed lobsters were treated independently of the
lobsters tagged and released on Cox Ledge at all
levels of analysis. The mean distance travelled for
lobsters transplanted from the Midshelf site to
Cox Ledge was 41.6 km with an average of 274.7 d
between release and recapture. The mean vector
bearing for Cox Ledge-Midshelf lobsters was
170.5°(T); however, the hypothesis of a uniform
distribution of return directions was not rejected
(P<0.01) when the data were subjected to a
Rayleigh test.

Return rates for lobsters tagged and released on
the Midshelf fishing grounds were also low, pre-
venting detailed analysis. The mean distance
travelled for 34 recovered lobsters was 18.2 km and

777

FISHERY BULLETIN: VOL. 78. NO. 3

the mean time at large was 26.9 d. The mean
vector angle for Midshelf lobsters was 167.1°(T)
and the distribution of return directions was
nonuniform (Rayleigh test; P<0.01).

DISCUSSION

Tagging experiments conducted in the coastal
waters of the western North Atlantic have demon-
strated generally localized lobster movements.
Recent in situ observations in restricted regions of
the Gulf of Maine (Cooper et al. 1975) and in Long
Island Sound (Stewart 1972) have supported these
results using seasonal underwater census
techniques. Morrissey (1971) and Dow (1975) dem-
onstrated, however, that lobsters tagged at inshore
locations were capable of undertaking large-scale
movements. Lund et al. (footnote 6) reported that
some lobsters tagged in eastern Long Island Sound
migrated to the outer continental shelf. Direct
comparisons among these inshore studies are
often not possible due to differences in tagging
methodology, seasonal deployment of tags, and
size range of lobsters tagged.

More consistent long-range movement patterns
have been noted for lobsters tagged and released
on the outer continental shelf (Cooper and Uz-
mann 1971; Uzmann et al. 1977). Saila and Flow-
ers (1968) had earlier demonstrated that ovigerous
female lobsters were capable of extensive move-
ments when displaced from offshore sites to Nar-
ragansett Bay.

In the present study, the movements of lobsters
tagged and released at inshore locations were typ-
ically localized. We attributed the small dispersion
radius, in part, to high exploitation rates which
resulted in rapid recovery of released lobsters.
Examination of recapture records indicated that
some inshore lobsters at large for over 180 d exhib-
ited little movement. Unfortunately, it is impossi-
ble to determine the actual trajectories of recov-
ered lobsters and the true extent of movements
between release and recovery is unknown.
Employing an ultrasonic tag, Lund et al. (footnote
6) tracked individual lobster movements and con-
cluded that most lobsters undertake only minor
(<30 m) daily movements in eastern Long Island
Sound.

We consistently noted southerly movements for
recaptured lobsters released at inshore locations.
Constraints on east-west and northerly move-
ments imposed by geographical features of the
area undoubtedly contributed to this result al-

though movement was not totally precluded in
these directions (Figure 1). The Rayleigh test gives
equal weight to each return direction and there-
fore any detectable movement in any direction
would be represented in the analysis.

Nonuniform distribution of fishing effort
further complicates the interpretation of these re-
sults and the potential bias introduced by this
factor cannot be ignored. Nonhomogeneous sam-
pling effort can result in an apparent directional
tendency when superimposed on random move-
ments. In the lobster fishery, effort is concentrated
primarily in areas with available shelter where
lobster density is highest. Lund et al. (footnote 6)
reported that lobster movements at inshore loca-
tions were often transitions between areas of suit-
able habitat. Dispersal of this type is therefore
likely to be detected through returns from the
commercial fishery. Due to high demand for
lobster, the coverage exerted by the fishery is
extensive and it has expanded to areas which were
formerly considered marginal in terms of catch per
unit effort or where operational costs were pro-
hibitive (as on the outer continental shelf). The
distribution of effort therefore generally approxi-
mates the distribution of lobster.

Comparisons between lobsters released at in-
shore locations in spring and early summer with
those released in late summer indicated a sharp
increase in directed movements in the latter
period. A concommitant increase in the mean
square dispersion coefficient indicated that ran-
dom movements also increased, possibly as a re-
sult of increased activity and catchability. The
timing of release differed slightly at each of the
inshore locations; of the 147 lobsters recovered
from the Sakonnet River tagging, 119 (80.9%) had
been released prior to 1 July while 123 (65.4% ) and
59 (51.3%) of the Narragansett Bay and Rhode
Island Sound lobsters were released prior to 1 July.
Since the three inshore release sites were located
in close proximity and were similar habitat types,
we attributed the differences in movements be-
tween locations to the timing of release. Stewart
(1972) noted increased activity and movements in
summer for lobsters tagged in Long Island Sound.

In constrast to the limited movements noted at
inshore release locations, lobsters tagged on Cox
Ledge migrated to the outer continental shelf in
late fall and winter. Little evidence of lateral
movement was noted despite an active fishery to
both the east and west of Cox Ledge. Coupled with
observations of an inshore spring migration from

778

FOGARTY ET AL : MOVEMENT OF AMERICAN LOBSTER OFF RHODE ISLAND

the outer continental shelf (Cooper and Uzmann
1971; Uzmann et al. 1977), these data indicate an
intermixing between offshore and inshore lobster
populations. Independent confirmation of seasonal
inshore-offshore movements has been obtained
using a stratified random trawl survey conducted
in spring and fall by the National Marine
Fisheries Service (Burns et al. ).

Lobster stock identification studies based on
electrophoretic techniques (Tracey et al. 1975) and
linear discriminant analysis of morphometric
data (Saila and Flowers 1969) indicated that in-
shore and offshore groups are discrete. Tracey et
al. (1975) noted generally low levels of genetic
variability, but inshore and offshore lobsters were
differentiable at one locus of the 44 examined.
Saila and Flowers (1969) reported significant pro-
file differences between inshore and offshore
lobsters. These studies would indicate that in-
shore and offshore groups retain their genetic
identity despite seasonal intermixing. Migra-
tional studies do indicate the possibility of genetic
exchange between areas, perhaps explaining the
low levels of genetic variability (Tracey et al. 1975)
and some of the inconsistencies noted by Saila and
Flowers (1969). The period of intermixing does
correspond to periods of molting and mating activ-
ity. Further research on inshore-offshore stock in-
teractions is clearly needed to resolve these ques-
tions. This factor assumes particular importance
since it is possible that coastal sites are depen-
dent on recruitment from offshore areas to sustain
inshore populations that are subjected to ex-
tremely high levels of fishing mortality.

ACKNOWLEDGMENTS

We would like to express our appreciation to
Richard Sisson, Timothy Lynch, Arthur Ganz, and
James Herrmann for assistance in the field. James
Yoder kindly provided a computer program for
analysis of movements. We are grateful to Barbara
Simon and Ellen Yoder for programming and data
management and to Linda Gray for typing the
manuscript. Thomas D. Morrissey, Saul B. Saila,
and J. Stanley Cobb critically read the manuscript
and offered many helpful suggestions.

/'Bums, T. S., S. H, Clark, V. C. Anthony, and R. J, Es-
sig. 1979. Review and assessment of the USA offshore lobster
fishery. Int. Cons. Explor Mer Shellfish Comm. CM. 1979/
K:25,31p.

LITERATURE CITED

Batschalet, E.

1965. Statistical methods for the analysis of problems in
animal orientation and certain biological rhythms. Am.
Inst. Biol. Sci., 57 p.

Bergeron, J.

1967. Contribution a la biologie du homard 'Homarus
americanus M. Edw.) des Iles-de-la Madeleine. [Engl.
Abstr.] Nat. Can. (Que.) 94:169-207.

Beverton, R. J. H., AND S. J. Holt.

1957. On the dynamics of exploited fish populations.
Minist. Agric. Fish. Food (G.B.) Fish. Invest., Ser. II, 19,
533 p.

Cooper, r. a.

1970. Retention of marks, their effects on growth, behav-
ior, and migrations of the American lobster, Homarus
americanus. Trans. Am. Fish Soc. 99:409-417.

Cooper, R. a., R. a. Clifford, and C. D. Newell.

1975. Seasonal abundance of the American lobster,
Homarus americanus, in the Boothbay Region of
Maine. Trans. Am. Fish. Soc. 104:669-674.
Cooper, R, a., and J. R. Uzmann.

1971. Migrations and growth of deep-sea lobsters, Hom-
arus americanus. Science (Wash., D.C.i 171:288-290.

Dow, R, L.

1974. American lobsters tagged by Maine commercial
fishermen, 1957-59. Fish. Bull., U.S. 72:622-623.

JONES, R.

1959. A method of analysis of some tagged haddock re-
turns. J. Cons. 25:58-72.

1966. Manual of methods offish stock assessment. Part IV -
Marking. FAO Fish. Biol. Tech. pap. 51, Suppl. 1, un-
paged.

MORRISSEY, T. D.

1971. Movements of tagged American lobsters, Homarus
americanus, liberated off Cape Cod, Massachusetts.
Trans. Am. Fish. Soc. 100:117-120.

Saila, S. G.. and J. M. Flowers.

1968. Movements and behaviour of berried female lobsters
displaced from offshore areas to Narragansett Bay, Rhode
Island. J. Cons. 31:342-351.

SCARRATT, D. J., AND R F ELSON.

1965. Preliminary trials of a tag for salmon and
lobsters. J, Fish. Res. Board Can. 22:421-423.

Stewart, L. L.

1972. The season movements, population djmamics and
ecology of the, lobster, Homarus americanus, off Ram Is-
land, Connecticut. Ph.D. Thesis, Univ. Connecticut,
Storrs, 112 p.

TRACEY, M. L., K. NELSON, D. HEDGECOCK, R. A. SHLESER,
.\ND M. L. PRESSICK.

1975. Biochemical genetics of lobsters: genetic variation
and the structure of American lobster (Homarus
americanus) populations. J. Fish. Res. Board Can.
32:2091-2101.

Uzmann, J. R., R. A. Cooper, and k. j. Pecci.

1977. Migration and dispersion of tagged American
lobsters, Homarus americanus, on the southern New
England continental shelf. U.S. Dep. Commer, NOAA
Tech. Rep. NMFS SSRF-705, 92 p.
WILDER, D. G.

1963. Movements, growth and survival of marked and

779

FISHERY BULLETIN; VOL. 78, NO 3

tagged lobsters liberated in Egmont Bay, Prince Edward
Island. J. Fish. Res. Board Can. 20:305-318.
WILDER, D. G., AND R. C. MURRAY.

1958. Do lobsters move offshore and onshore in the fall and
spring? [In Engl, and Fr] Fish. Res. Board Can., Prog.
Rep. Atl. Coast Stn. 69:12-15.

780

FACTORS CONTROLLING GROWTH AND SURVIVAL OF

CULTURED SPOT PRAWN, PANDALUS PLATYCEROS,

IN PUGET SOUND, WASHINGTON

John E. Rensel* and Earl F. Prentice^

ABSTRACT

Environmental factors affecting growth and survival of juvenile and yearling spot prawns, Pandalus
platyceros. were studied at two sites in Puget Sound, Washington. It was thought that higher water
temperatures at the southern site would promote increased growth rates, but intense plankton blooms
and rapid fluctuations of water temperature induced high mortalities. Moribund prawns recovered
quickly when placed in epibenthic cages that received cooler, relatively plankton-free water.

Although the cooler central Puget Sound site was judged suitable for prawn culture, fluctuations in
temperature and plankton abundance caused moderate mortalities here as well.

Since 1970, several commercial marine aquacul-
ture projects utilizing floating net pens for the
culture of Pacific salmon, Oncorhynchus spp.,
(Mahnken 1975) have been developed in the
Pacific Northwest. Development of companion
crops to be grown in net pens with the salmon
would enable growers to diversify and increase the
return on their investments. The spot prawn,
Pandalus platyceros Brandt, (herein referred to as
prawn) may be a potential companion crop for
several reasons: 1) it is adaptable to the sides as
well as the bottom of net pens; 2) it can reproduce
in captivity (Rensel and Prentice 1977); 3) it grows
more rapidly and reaches a larger size than other
pandalids (Butler 1964); 4) it consumes a variety
of foods including dead fish; 5) it is gregarious and
is normally not cannibalistic; and 6) it can be cul-
tured in the laboratory (Wickins 1972; Kelly et al.
1976; Prentice^).

The objective of the present study was to deter-
mine the effects of environmental factors on
growth and survival of juvenile and adult prawTis
held separately but near to salmon rearing pens at
two differing salmon aquaculture sites. It was
hypothesized that higher water temperatures at

'Squaxm Island Tribe. Route 1, Box 257, Shelton, WA 98584.

^Northwest and Alaska Fisheries Center, National Marine
Fisheries Service, NOAA, 2725 Montlake Boulevard East,
Seattle, WA 98112.

^Prentice, E.F 1975. Spot prawn culture: status and poten-
tial. In C. W Nygaard (editor). Proceedings of a seminar on
shellfish farming in Puget Sound, Oct. 7, 1975, Poulsbo, Wash.
Processed Rep., lip. Wash. State Univ. Coll. Agric, Coop. Ext.
Serv, Pullman, WA 99163.

the more southern site would produce increased
growth rates.

METHODS

Two sites were utilized for the experiments,
Clam Bay and Henderson Inlet, both in Puget
Sound, Wash. (Figure 1). At the National Marine
Fisheries Service (NMFS) laboratory at Clam Bay,
floating net pens for salmon research were
situated at the end of a pier. Depth under the pens
ranged from 9 to 14 m, depending on the stage of
the tide. Data collected over several years indi-
cated that the site had good water exchange with
tidal currents reaching 0.4 kn at maximum flood
and 1.0 kn at maximum ebb. The growth rate of
prawns cultured previously at the site (Rensel and
Prentice 1978) approximated that found in a wild
population (Butler 1964).

The Henderson Inlet site (Figure 1) was at the
location of a commercial log rafting operation. In
1973, a pilot-scale salmon aquaculture project was
initiated by the Weyerhaeuser Company and the
Washington Sea Grant Office at the site, and hy-
drographic data were collected (Snyder et al.'*).
Because of the inlet's shallow depth (10 m mid-
channel), configuration, and location, seawater
exchange is more restricted and tidal currents less

Manuscnpt accepted December 1979.
FISHERY BULLETIN: VOL. 78, NO. 3, 1980.

••Snyder, B. R, A. J. Didier, Jr., and E. O. Salo. 1974. The
culture of salmon at Willapa Bay Grays Harbor, and Henderson
Inlet in southern Puget Sound. Final Report Jan. 1973 to Feb.
1974. Univ Wash., Coll. Fish., Fish. Res. Inst., Seattle, WA
98195,211 p.

781-

FISHERY BULLETIN: VOL. 78. NO. 3

Figure l.— Puget Sound, Washington,
with sites of spot prawn studies at Hen-
derson Inlet and Clam Bay.

HENDERSON
INLET

than at Clam Bay. Surface water at the inlet was
warmer and more turbid, but dissolved oxygen and
salinity were similar to Clam Bay.

Five-month-old juvenile prawns, reared at the
NMFS Clam Bay laboratory, were used in the
study. The prawns were transferred to net pens
and cultured from July to November 1974 at Hen-
derson Inlet and from July 1974 until March 1975
at Clam Bay. Initial carapace lengths (distance
from the base of the eyestalk to the posterior mid-
dorsal edge of carapace) of the juvenile prawns
averaged 5.3 mm ( n = 135 at each site, SD = 1.70)
for all experimental lots. Weight of the prawns was
not initially determined. We obtained wild prawns
from commercial fishermen on Hood Canal (Puget
Sound) in May 1974 and held them in a common
pen for 3 wk at each site prior to distribution to
rearing pens. The culture period was from June
1974 to March 1975. At the start of the experi-

ment, the average carapace length was 25.8 mm ( n
= 336, SD = 1.68), and the average weight was
11.1 g(SD = 2.25). These prawns are referred to as
yearlings as defined by the weight and length
range (6.4-15.4 g, 21.2-28.5 mm) reported by But-
ler (1964) for a wild population.

Juvenile prawns were cultured in rectangular,
knotless nylon net pens (stretched measure 6.7
mm), 2.16 m square x 1.8 m deep. Weights were
attached externally to the corners of the pens to
maintain their shape. Covers made of black plastic
sheeting were placed over the pens to reduce light
and discourage bird predation. Each pen was di-
vided into three equal chambers by vertical net
panels. The total immersed net area was 6.3 m^/
chamber. Each chamber was stocked with 45
prawns for an initial density of 7.1 prawns/m^.

Pens used for the yearling prawns were also
covered with plastic sheeting. These pens were the

782

RENSEL and PRENTICE: FACTORS CONTROLLING GROWTH AND SURVIVAL

same overall size and depth as the pens for the
juveniles but were made of a larger mesh size
(stretched measure, 9.0 mm) and not divided into
chambers. Polyvinyl chloride pipe frames were
placed in the pen bottoms to maintain the pen's
shape. The total immersed substrate available to
the prawns was 11.5 m^/pen. Each pen was
stocked with 112 prawns for an initial density of
9.7 prawns/ m^.

The prawns were divided into treatment groups
based on age and diet. Juvenile prawns were fed
raw meat of the blue bay mussel, Mytilus edulis.
Yearling prawns were divided into two diet treat-
ments. A "clam-fed" diet consisted of frozen pro-
cessing waste from the geoduck, Panope generosa,
which was fed without limit every other day after
old food was removed. In a second treatment, "un-
supplemented," the prawns were not fed but for-
aged on organisms growing on or drifting into the
net pens. Dead prawns and exuviae were collected
from each treatment every other day. All treat-
ments were replicated three times at both test
sites.

All surviving prawns were measured for length
and weight except juveniles whose weights were
estimated from carapace lengths using the for-
mula log W = 2.93148 log L = 3.07787, where: L =
length in millimeters and W = weight in grams
(Butler 1964). Initially, the carapace of each
juvenile prawn was measured to the nearest 0.1
mm with an ocular micrometer. Carapace length
of yearlings was measured with calipers to the
nearest 0.5 mm. Starting in October, the juvenile
prawns were also measured with calipers. A top
loading balance was used to obtain individual wet
weights (nonblotted) of the prawns to the nearest
0.01 g.

RESULTS AND DISCUSSION
Environmental Data

Salinity at Henderson Inlet and Clam Bay
ranged from 28.4 to 31.0%o, being within the range
reported by Butler ( 1964) for wild prawn popula-
tions. Dissolved oxygen (DO) peaked in May (11.0
ppm at Henderson Inlet and 9.0 ppm at Clam Bay)
and gradually fell to a minimum (5.0 ppm) in Sep-
tember at both sites. This low value at both sites
only lasted a few hours during some tidal cycles.
We believe these DO levels, because of their short
duration and lack of stress on salmon in adjacent
net pens, were adequate for the prawns and never

caused stress. Bottom temperatures at Henderson
Inlet were always higher than those at Clam Bay
(Figure 2).

Light influences the growth of crustaceans.
Forster (1970) reported significantly higher
growth rates for juvenile prawns, Palaemon ser-
ratus, held in total darkness when compared with
those held in other light conditions. A similar
phenomenon has been reported with the Ameri-
can lobster, Homarus americanus (Conklen 1975).
In our study, juvenile and yearling prawns avoided
brightly illuminated areas and stopped feeding
when the black covers were removed. This sudden
increase in light intensity and the presence of an
observer could have affected growth and survival,
but no quantitative information was obtained.

18

o

° 16

UJ

a:

Z3 14

)-
<

S 12

Q.

US 10

Y-

Henderson Inlet 05nn below surfoce

Clam Boy 0.5m below surface

Henderson Inlet I.Om

above bottom

May Jun Jul Aug Sep Oct Nov Dec

Figure 2. — Weekly mean water temperatures for Henderson
Inlet and Clam Bav.

At Henderson Inlet, maximum water transpar-
ency, as measured with a Secchi disc, was from 0.5
to 4.2 m (5-d mean) less than at Clam Bay (Figure
3). Seasonal fluctuation in water transparency at
both sites was caused by plankton blooms and
runoff.

Growth and Survival of Juveniles

Between-site comparison of juvenile prawn
growth was terminated in late November when
Clam Bay juveniles were significantly heavier ( t =
3.61, df = 2,147, P<0. 001) (Figure 4) and longer ( t
= 3.35, df = 2,147, P<0.002) than those at Hen-
derson Inlet. Growth monitoring continued at
Clam Bay until March 1975.

Water temperature is an important factor af-
fecting the growth of the spot prawn, and Wickins
( 1972) indicated that the optimum was at 18° C in
the laboratory During the period from July to
September the maximum water temperatures at

783

FISHERY BULLETIN: VOL, 78, NO. 3

Figure 3.— Water transparency (5-d
averages) at Henderson Inlet and Clam
Bay as measured with a Secchi disc for
the period May 1974 to March 1975.

2 5
UJ

<

Q- ,

in t

z
<

z-

CLAM BAY
HENDERSON

SEPT

1974

JAN FEB MARCH

1975

X
UJ

8.0

Clam Bay
Henderson Inlet

British Columbia wild
population (Butler 1964)

Jul Aug Sep Oct Nov Dec Jon Feb Mar Apr

Figure 4. — Mean weights of juvenile spot prawns reared in net
pens at Clam Bay and Henderson Inlet compared with a wild
population in British Columbia (Butler 1964).

Henderson Inlet and Clam Bay were 19.0° and
16.5° C. Daily fluctuations up to 4° C were seen at
both sites and the daily surface water tempera-
tures at Henderson Inlet averaged 2.5° higher
than at Clam Bay. The weekly mean temperatures
never exceeded the optimal 18° C value at either
site (Figure 2).

To evaluate the effect of temperature on the
growth ofjuvenile prawns, the mean weight of the
prawns was plotted against cumulative degree
days (Figure 5). If temperature were the primary
variable controlling growth within the prawns'

▲ — ▲ Henderson Inlet
Clam Bay

500 1000 1500 2000

CUMULATIVE DEGREE DAYS

FlCiURE 5. — Average weight ofjuvenile spot prawns as a function
of cumulative degree days in the rearing experiments July to
December 1974.

zone of anabolism, then the curves (Figure 5)
would be similar; however, this is not the case, as
growth was depressed at Henderson Inlet. The
slopes of both curves parallel each other after Sep-
tember, indicating that temperature had become
the major factor affecting growth. Beginning in
September there was a general decrease in water
temperature at both sites (Figure 2).

To evaluate the growth of our prawns relative to
the growth of wild populations, we compared our
data with those of Butler (1964) who studied
growth of a wild population in British Columbia.
The data indicate the growth rate (increase in
weight over time) of the cultured prawns was simi-
lar to that of the wild population up to the end of
October (Figure 4). After October, the cultured

784

RENSEL and PRENTICE FACTORS CONTROM.ING GROWTH AND SURVIVAL

prawns continued to increase in weight at a rela-
tively constant rate until the termination of the
study. The wild population showed a decrease in
growth rate during the period of late October to
the end of January which was followed by a growth
rate which approximated that of the cultured
group. Water temperature and decreased avail-
ability of food are among the many factors which
could account for the decreased growth in the wild
populations.

At termination of comparative testing in No-
vember, total mortality of juvenile prawns was sig-
nificantly greater (x^ = 67.2, df = 1, P<0.05) at
Henderson Inlet than at Clam Bay (Figure 6). The
experiment at Clam Bay was continued to 10
March 1975, when survival was 79%.

We partially attribute the high mortality rate
and the reduced growth of juvenile prawns at Hen-
derson Inlet from July to September to plankton
blooms. At the time of stocking in early July, water
transparency was depressed by a plankton bloom
(Figure 3). A 20% mortality occurred during the
first 2 wk of July followed by a decrease in the
mortality rate after the bloom subsided (Figure 6).
During the same period prawns at Clam Bay
showed an estimated 2% mortality as determined
from semidaily pen examination.

Clam Bay
Henderson Inlet

Jul Aug Sep Oct Nov Dec Jan Feb Mar
1974 1975

Figure 6. — Survival of juvenile spot prawns from July 1974 to
March 1975 at Henderson Inlet and Clam Bav.

The mortality of juvenile prawns at Henderson
Inlet increased again in early September during
blooms of the dinoflagellates, Ceratium sp. and
Peridinium sp. Salmon mortalities also increased
in adjacent net pens during this period. Prawn
mortalities at Henderson Inlet decreased with the
end of the intense plankton blooms in the fall
(Figures 3, 6).

Substantial mortalities of Pacific salmon reared
in net pens in British Columbia have also been

associated with algae blooms. Kennedy et al.^
suggested that the algae promoted the production
of suffocating mucus or physically damaged gills
through contact with sharp diatom spicules. At
Henderson Inlet the prawns' gills were noticeably
blackened and had unidentifiable matter on the
lamellae that may have been mucus or deterio-
rated dinoflagellates.

At Henderson Inlet, during the first 2 wk only,
several dead prawns had single lesions — dark in
the center and often surrounded by an area of
reddish tissue. These lesions were not observed on
the prawns at Clam Bay. Lightner and Lewis
( 1975) found the cuticular injuries from handling
of penaeid shrimp resulted in bacterial septicemic
diseases. Handling could partly explain the le-
sions and initial losses of juvenile prawns at Hen-
derson Inlet because the net pens were pulled to
the surface frequently to remove old food and dead
prawns. This procedure was not followed at Clam
Bay where water transparency allowed examina-
tion of the prawns in place.

Growth and Survival of Yearlings

No yearling prawns at Henderson Inlet survived
in either dietary treatment after the first 2.5 mo
(Figure 7). In early June, maximum surface tem-
peratures increased from 11.8° to 21.9^ C in 1 wk.

^Kennedy, W. A., C. T. Shoop, and \V. Griffioen. 1975. Pre-
liminary experiments in rearing Pacific salmon ( 1973 parr).
Environ. Can., Fish. Mar Serv,, Tech. Rep. 541, 17 p. Pac. Biol.
Stn., Nanaimo, B.C. V9R 5K6.

100

80

5 eo

Z
LlJ
O

(T
Ul

a.

40

20

«.,„

\

■•...

"0....

■■• ♦ «

\

"■■"■•^ o „

o

\

CLAM BAY

-

\

• • Clom processing wastes

0-..-0 Unsupplemented

HENDERSON INLET

-

\

A — A Avg of oil treotments

Jun

Aug

Oct

Dec \ Feb Apr \

1974 -

\ 1975 " !

FIGURE 7. — Survival of yearling prawns held in floating net
pens at Henderson Inlet and Clam Bay.

785

FISHERY BULLETIN: VOL. 78, NO. 3

and the weekly mean rose about 5° C. As men-
tioned previously, a plankton bloom also occurred
during this period. The rapid rise in water tem-
perature and the onset of plankton blooms were
the primary factors associated with the rapid rise
in mortality rate of the yearling prawns. Abnor-
malities in appearance and behavior of the prawns
were noted soon after their arrival at Henderson
Inlet in June. The prawns became covered with
fouling organisms, particularly the hydroid,
Obelia sp., and the suctorian protozoan, Ephelota
gemmipara . Heaviest fouling occurred on
periopods and ventral edges of the cephalothorax,
but the gills were unaffected. Within 2 wk many
prawns were dying while survivors seemed
lethargic and did not feed or molt. The entire stock
was given a formaldehyde/malachite green dip (25
to 0.1 ppm ratio for 8 h), but beneficial effects
lasted only a few days.

On 2 July, 49 surviving yearling prawns from
one clam-fed replicate at Henderson Inlet were
removed from the experiment and placed in a vinyl
coated wire mesh cage (0.9 x 0.9 x 0.5 m) that was
placed on the bottom of the Inlet, into water that
was colder (Figure 2), less lighted, and out of the
influence of the surface plankton bloom. Within 2
d the prawns became active and began molting
although many still had .some fouling organisms.
By September, only four mortalities had occurred
in the cage (92% survival), while prawns in the
surface net pens had suffered lOO'^ mortality.
Colder water, reduced light, and the possibility of
being out of the surface plankton bloom could ex-
plain this increase in survival. There are no
natural populations of prawns in the shallow in-
lets of southern Puget Sound (i.e., those inlets to
the west of Henderson Inlet). Berkley ( 1930) noted
that late larval and postlarval prawns in British
Columbia were commonly found inshore at depths
of 3.7-5.5 m. The adverse conditions encountered
in surface waters during this study produced ex-
tensive mortalities and could explain the absence
of natural prawn populations in the shallow inlets
of southern Puget Sound.

Survival of yearling prawns at Clam Bay after
10 mo (5 June 1974-28 March 1975) was 78.6% for
clam-fed treatments and 66.7% for unsupplement-
ed dietary treatments (Figure 7). The difference
in survival was significant (y^ = 9.48, df = 1,
P<0.005).

Temperature fluctuations and plankton blooms
at Clam Bay were associated with increases in
mortality. Over half of the total mortalities oc-

curred in a 2-mo period (August-September) in
which the weekly mean temperature rose to a high
for the year ( 14.2° C) and the lowest transparency
value occurred (Figures 2, 3). In general, yearling
prawn mortality coincided with rapidly decreas-
ing water transparency and increasing water
temperature and not the absolute value of Secchi
disc readings.

Both treatment groups at Clam Bay grew at
essentially the same rate during the June to Au-
gust period. Thereafter the clam-fed prawns were
significantly heavier it = 10.98, df = 2,539,
P<0.00) and longer (Z' = 3.17, df = 2,539, P<0. 001)
than the unsupplemented prawns (Figure 8).

Despite the fact that no food was given, the un-
supplemented group had a positive growth rate
throughout the experiment and a fairly high sur-
vival (66.7% ). About 607^ ofprawns sampled at the
termination of the experiment had materials in
their stomachs, including unidentifiable brown
matter, various algae (brown filamentous forms
and diatoms, particularly Riddulphia sp.), and
fragments of exoskeleton from either the prawns'
exuviae or naturally occurring crustaceans in the
net pens. The prawns had apparently maintained
themselves on net fouling and/or pelagic or-
ganisms and through consumption of dead prawns
or molted exuviae.

Net fouling organisms were preyed upon by
prawns in both treatment groups. Commonly seen
net fouling organisms (mussels, tunicates, and
bryozoans) were noticeably absent from the nets
containing pravvns after 10 mo of immersion. The
only major fouling organisms remaining were
hydroids, Obelia sp., and small entroprocts (both

CLAM BAY

• • Clom processing woste

O O Unsupplemented

18

17

16

1/1

15

F

o

14

t-

\^

1

ID

111

\2

$

1 1

10

9

■■%-:...M^o o-

May Jun Jul Aug Sep Oct Nov Dec Jon Feb Mar

Figure 8. — Seasonal mean weight of yearling spot prawns
reared at Clam Bay compared with a British Columbia wild pop-
ulation (Butler 1964).

786

RENSEL and PRENTICE: FACTORS CONTROLLING GROWTH AND SURVIVAL

restricted to the top 10 cm of the net). By feeding
on net fouling organisms, the prawns not only
make use of a free food supply, but they also pro-
vide net cleaning services that would reduce pen
maintenance.

Molting

The yearling prawns held at Clam Bay showed
five major molting peaks. At each peak, a higher
percentage of clam fed prawns molted than un-
supplemented prawns, but periods of peak molting
generally coincided for each group (Figure 9). TWo
major molting peaks occurred in the summer
about 50 d apart. By winter (November- February),
the peaks were about 75 d apart, and by spring the
intermolt periods were once again shortened to
nearly 50 d. A pattern emerged with molting
peaks occurring at either 1.6- or 2.5-mo intervals,
depending on season. Rickards (1971) found a
highly significant relationship between tempera-
ture and frequency of molting for tank-reared,
juvenile pink shrimp, Penaeus duorarum. In the
present study, the percentage of prawns molting
appears related to temperature (Figure 9), but
molt frequency is not related since it increases in
late winter while water temperatures are still de-
pressed. A previous study of juvenile prawns con-
cludes that molt frequency decreases with age
(Wickens 1972); however, there is no published
account for molt frequency of older prawns.
Kamiguchi (1971) reported that molt frequency of
sexually immature Palaemon pauciden decreased
with size until maturity when a constant interval
between molting peaks was the rule.

In the present study, molting patterns may have
been affected by changing photoperiod (Aiken
1969) and maturation as the prawns became func-
tional males midway through the experiment.

In conclusion, surface waters of Henderson Inlet
were unsuitable for prawn culture due to intense
plankton blooms and rapid fluctuations of water
temperature. These factors outweighed the
growth stimulating effects of elevated water
temperatures. Clam Bay was suitable for prawn
culture although moderate mortalities were as-
sociated with plankton blooms and increases of
water temperatures.

ACKNOWLEDGMENTS

This work was supported in part by the Wash-
ington Sea Grant Office and the Weyerhaeuser
Company.

LITERATURE CITED

AIKEN, D. E.

1969. Photoperiod, endocrinology and the crustacean molt
cycle. Science (Wash., D.C.) 164:149-155.

Berkeley, a. a.

1930. The post-embryonic development of the common
pandalids of British Columbia. Contrib. Can. Biol. Fish.,
New Ser. 6:79-163.
BRETT, J. R., AND J. E. SHELBOURN.

1975. Growth rate of youngsockeye salmon, Oncor/iync/ius
nerka, in relation to fish size and ration level. J. Fish.
Res. Board Can. 32:2103-2110.
Butler, T. H.

1964. Growth, reproduction, and distribution of pandalid
shrimps in British Columbia. J. Fish. Res. Board Can.
21:1403-1452.

Conklen, D. E.

1975. Nutritional studies of lobsters, Homarus ameri-
canus. In K. S. Price, Jr, W. N. Shaw, and K. S. Danberg
(editors). First International Conference on Aquaculture
Nutrition, p. 287-296. Univ Del. Coll. Mar. Stud.

FORSTER, J. R. M.

1970. Further studies on the culture of the prawn, Pal-
aemon serratus Pennant, with emphasis on the p)ost-larval
stages. Fish. Invest. Minist. Agric, Fish. Food (G.B.),
Ser, II, 26(6), 40 p.

Figure 9. — Yearling spot prawn molting cycle 5-d
means) and monthly means and ranges of surface
water temperatures at Clam Bay.

O

O

_l
ID
Q-
O
CL

O

Water Temperature 0 5m below surface

Fed prawns

Unsupplemented prawns

16
15

14

13 o"

12

Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar

UJ

II Q:
10 I-
9 2
8 ^

6 ^

0

787

FISHERY BULLETIN VOL. 78, NO. 3

KAMIGUCHI, T.

1971. Studies on the molting in the freshwater prawn,
Palaemon pauciden. I. Some endogenous and exogenous
factors influencing the intermolt cycle. J. Fac. Sci.
Hokkaido Univ., Ser. VI, Zool. 18( 1): 15-23.

Kelly, R. O. A., A. W. Haseltine, and E. E. Ebert.

1976. Mariculture potential of the spot prawn, Pandalus
platyceros Brandt. Aquaculture 10(11:1-16.
LIGHTNER, D. v., AND D. H. LEWIS.

1975. A septicemic bacterial disease syndrome of penaeid
shrimp. Mar. Fish. Rev. 37(5-6):25-28.
Mahnken, C. V. W.

1975. Status of commercial-net pen farming of Pacific
salmon in I\iget Sound. Proc. 6th Annu. Meet. World
Maricult. Soc, p. 285-298.

Mahnken, C. V. W., A. J. Novotny, and T. Joiner.

1970. Salmon mariculture potential assessed. Am. Fish
Farmer 2(1): 12- 15, 27.

Rensel, J. E., and E. F Prentice.

1977. First record of a second mating and spawning of the
spot prawn, Pandalus platyceros, in captivity. Fish.
Bull., U.S. 75:648-649.

1978. Growth of juvenile spot pravm, Pandalus platyceros ,
in the laboratory and in net pens using different diets.
Fish. Bull., U.S. 76:886-890.

RICKARDS, W, L.

1971. Studies of the use of vertical substrates for improv-
ing production of pink shrimp, Penaeus duorarum Bur-
kenroad. Univ. Miami Sea Grant, Tech. Bull. 10,
152 p.

WICKENS, J. F

1972. Experiments on the culture of the spot prawn Pan-
dalus platyceros Brandt and the giant freshwater prawn
Macrobrachium rosenbergii (de Man). Fish. Invest.
Minist. Agric, Fish. Food (G.B.), Ser II, 27(5), 23 p.

788

NOTES

REARING CONTAINER SIZE AFFECTS

MORPHOLOGY AND NUTRITIONAL CONDITION

OF LARVAL JACK MACKEREL,

TRACHURUS SYMMETRICLS

Container size may be a critical variable in the
rearing of marine fish larvae. Northern anchovy,
Engraulis mordax, grew faster in 500 1 than in
10 1 containers (Theilacker and McMaster 1971),
and Blaxter (1976) suggested that growth of lab-
oratory-reared fish may depend on space avail-
able in tanks as well as food supply and fish
density. On intuitive grounds, large containers
are preferable for rearing studies but small con-
tainers are often used because fewer food orga-
nisms are required, treatments can be replicated
easily, and daily mortality can be easily moni-
tored. Thus, information is needed on the extent
container size affects results of laboratory studies
on marine larvae. In this paper, I compare the
growth, morphology and nutritional condition of
jack mackerel, Trachurus symmetricus, larvae
reared in 10 1 and 100 1 containers.

Methods

jaw to perpendicular at end of notochord), head
length (HL, tip of upper jaw to cleithrum), eye
diameter (ED), body depth at the pectoral fin
(BD-1), and body depth at the anus (BD-2).
Shrinkage of jack mackerel body parts in Bouin's
solution was as follows: SL, 8%; HL, 18^; ED,
10%; BD-1 and BD-2, 25% (Theilacker 1980).
(Data in Table 1 are preserved measurements.)
After measurement, I used standard techniques
(Theilacker 1978) to prepare larvae for histolog-
ical examination.

I examined the tissue microstructure of all
larvae in fed and starved treatments to determine
whether larvae were eating or starving. The onset
of starvation in jack mackerel larvae is charac-
terized by a change in the acinar arrangement of
pancreatic cells and a sloughing of mucosal cells
from the midgut into the lumen (Theilacker 1978).
I graded these characteristics of the pancreas
and gut and classified individual larval nutri-
tional condition as "healthy," "intermediate," or
"starved" (Theilacker 1978). Because histological
assessments of larval condition are based on
tissue microstructure, these assessments are in-
dependent of larval size.

I collected jack mackerel eggs by towing aim
(0.505 mm mesh) plankton net just below the sea
surface 61 km off southern California in May 1976.
Sea surface temperature was 15.3° C. I sorted and
staged normally developing eggs from the plank-
ton and stocked eggs of the same stage at 5/1 into
10 1 and 100 1 black circular rearing containers
containing 5 pim filtered seawater at 15.0° C and a
light cycle of 12 h light and 12 h dark. I used two
treatments for each container size, one fed and the
other unfed. Data from the 100 1 treatments were
reported earlier (Theilacker 1978). Larval diet
consisted of a naked dinoflagellate, Gymnodinium
splendens (50/ml), a rotifer, Brachionus plicatilis
(30-40 /ml), and a copepod, Tisbe sp. (1-2/ml). This
feeding method has been described previously
(Lasker et al. 1970; Theilacker and McMaster
1971; Hunter 1976).

Larvae began to eat 5 d after hatching. I sampled
5-30 larvae daily from fed and starved treatments
beginning on day 6 and preserved the larvae in
Bouin's solution. Four to five weeks after preserva-
tion, I measured standard length (SL, tip of upper

FISHERY BULLETIN; VOL. 78, NO. .3, 1980.

Results

Diameter of jack mackerel eggs collected for this
study averaged 1.0 mm. Larvae hatched at 2.45
mm SL (preserved) on day 0 and began to eat
at 3.35 mm SL at age 5 d when most yolk
was absorbed.

Fed larvae were larger in 100 1 than in 10 1
containers on each day after the onset of feeding
(day 5), but statistically significant differences in
size among larvae in the large and small contain-
ers did not occur until the larvae had fed for 4 d.
age 9 d (P = 0.002; Hotelling T'^ multivariate
analysis; Table 1).

Among groups receiving no food, larvae in 10 1
containers were larger than those starved in 100 1
containers at age 8 d, third day of starvation
(P = < 0.001; Hotelling T^ multivariate analysis;
Table 1.) Also, starved larvae in small containers
survived 2 d longer than those in large containers.
10 d versus 8 d.

Nutritional condition of fed larvae reared in 10 1
and 100 1 containers was similar for 5 feeding days,

789

Table l. — Daily mean body measurements of fed and starved jack mackerel larvae maintained in 10 1 and 100 1 containers.

Day 6

Day

7

Days

Day 9

Day

10

Day 11

Body,
parts

10

100

10

100

1C

100

10

100

10

100

10

mm

SD

mm

SD

mm

SD

mm

SD

mm

SD

mm

SD

mm

SD

mm

SD

mm

SD

mm

SD

mm SD

FED

Standard

length

3.30

0.16

3.35

0.11

3.43

0-05

3.48

0.13

3.38

0.19

3.56

0.13

3.37

0.13

383

0,24

3,35 0,21

3,72

0,20

3,35 015

Head

length

.67

.03

.70

.03

.73

.02

.74

.04

.73

.05

.77

.03

.71

.03

,85

,06

75

,07

85

07

76 ,06

Eye
diameter

.23

.02

.25

.02

26

.01

26

.01

.26

.02

.29

.02

.25

.02

32

,02

27

02

,31

,03

,25 ,01

Body
depth- 1

40

.02

43

.11

.48

.03

.48

-03

.48

.04

.52

.04

,48

.04

,59

,04

46

06

,58

,06

,47 ,03

Body

depfh-2

-18

01

20

.05

.19

.01

20

02

.19

.02

.22

02

.19

-02

,25

,01

,20

,02

23

,02

,18 ,01

n

4

15

5

15

5

15

5

10

17

15

7

'P

0.463

0.523

0.109

0.002

0.001

STARVED

Standard

length

3.31

0.11

3.27

0.15

3.35

0.13

329

0.12

3-04

0.17

299

0.33

3,07 021

Head

length

.66

.04

.68

.03

.69

.02

71

.03

.64

.04

65

.04

.66

,05

.

Eye
diameter

.24

.02

.24

.02

25

.01

.24

.02

.23

.01

.24

.01

.25

,02

Body
depth- 1

.41

.03

.40

.03

,42

.02

38

.02

.42

.03

.36

.02

.35

,02

Body
depth-2

.18

.02

.18

.01

.18

.01

.17

01

.17

.01

.17

,01

.17

,01

n

14

26

15

15

19

ie

26

'P

0.351

< 0.001

Preserved measurements.

Probabilities for equal body measurements between container sizes (multivariate analysis: Hotelling T

Table 2. — Daily histological condition of fed and starved jack mackerel larvae maintained in 10 1 and 100 1 containers.

FED

STARVED

Histological
grade

Day 6

Day 7

Days

Day 9

Day
10

10
100

Day 11
10

Day 6
100

Day

7

Days

Day 9
10

Day 10

10

100

10

100

10 100

10 100

10

100

10 100

10

Starved

(1,00-1-66)
Intermediate

0

1

0

0

1 1

1 1

8

1

3

7

20

6

12 15

8

22

(1,67-2,33)
Healthy
(2,34-3,00)
Average
grade

3
1
2,25

1

12
2,77

0
5
2,90

2

13
2,80

0 3
3 11
2,50 2-62

0 0
4 9
2,60 280

4
4
1,80

2
12
2,65

0
3
2,08

3
3
1,88

3
1
1 32

6
2

1 71

0 1
0 2
1,00 1,25

1
0
1,11

2
0
1,08

'n

4

14

5

15

4 15

5 10

16

15

6

13

24

14

12 18

9

24

'P

>

0,10

_>

0,10

>0,10

>0,10

>0,05

>0 10

>0,10

'Theilacker (1978),

^ Total number of larvae within each treatment does not agree with Table 1, as several larvae were lost during the microtechnique procedure.
Probabilities for equal histological grades between container sizes (two-sample nonparametric Kolmogorov-Smirnov Test)

until age 10 d when it was significantly better in
the large containers (P = <0.05; Kolmogorov-
Smirnov Test; Table 2); fewer larvae were classed
as "starved" in the larger containers. For larvae
given no food, no difference existed in condition of
larvae between large and small containers.

Fed larvae died at ages 12-13 d in the small
containers. On day 13 there was also a major
mortality in the large containers, but a few larvae
survived through the juvenile stage, and one fish
lived for 49 d, 31 mm SL. I did not sample these
survivors unless they appeared to be dying. For
jack mackerel there is no well-defined metamor-
phosis; the juvenile stage begins at the comple-
tion of fin formation, 12-16 mm (Ahlstrom and

Ball 1954). In the large container, fin forma-
tion was complete at 14 mm, 39 d of age (n - \)\
size at age for this laboratory-reared fish was
similar to field-collected fish (age of wild fish is
being determined by reading daily growth incre-
ments in otoliths (MethotM).

Conclusions

Relating experimental results from laboratory
to field conditions must be done with caution.
Blaxter (1975) compared morphology, chemistry,

'R. Methot, Southwest Fisheries Center La Jolla Laboratory,
National Marine Fisheries Service, NOAA, P.O. Box 271, La
Jolla, CA 92038, pers. commun. January 1980.

790

and physiology between reared and wild larvae
and concluded that results on growth, nutrition,
and mortality of laboratory-reared larvae should
not be related to the field. My study shows that
jack mackerel larvae reared with food in 10 1
containers were smaller and in poorer nutritional
condition than larvae reared in 100 1 containers.
These container-effects occurred at an early age,
i.e., morphological differences were evident 9 d
after hatching and histological differences 10 d
after hatching. Larvae may grow faster and show
fewer signs of starvation in large containers
because: 1) there is a lower probability of damage
from contact with the walls; and/or 2) the same
prey density in a larger container may permit the
formation of larger food patches and thereby
elevate the actual density of food encountered by
the larvae; and/or 3) water chemistry in larger
containers may be more favorable.

In contrast to results of the feeding experiments,
larvae starved in 10 1 containers survived 2 d
longer and were larger at age 8 d than those in
100 I containers. This indicates that activity may
be affected by container size. Larvae in small
containers may be less active, consume energy
reserves less rapidly, and therefore live longer
without food.

The effect of container size on growth, nutritive
condition, and possibly activity in jack mackerel
larvae, emphasizes the caution that must be
exercised when relating results from laboratory to
field conditions. The large container may have
had no effect on growth and development of jack
mackerel, but survival was poor. Further studies
are needed to determine the minimum container
size required to simulate natural conditions in the
laboratory. Because spatial requirements of larval
fish depend on locomotory patterns as well as on
genetic adaptations to life near solid surfaces
(Kinne 1977), optimum container size will prob-
ably vary with fish species. In larval fish experi-
ments, container size is a variable that must be
considered with temperature, light, food type and
availability, and stocking density.

Acknowledgments

Thanks to John Hunter and two anonymous
reviewers for critically reviewing the manuscript,
Jack Metoyer for helping me measure larvae,
Susan Picquelle for helping with the statistical
analyses, Kate Coleman for typing the draft and
tables, and Lorraine Prescott for final typing.

Literature Cited

AHLSTROM, E. H., AND O. R BALL.

1954. Description of eggs and larvae of jack mackerel
{Trachurus symmetricus) and distribution and abun-
dance of larvae in 1950 and 1951. U.S. Fish Wildl.
Serv., Fish. Bull. 56:207-245.
BLAXTER, J. H.S.

1976. Reared and wild fish — how do they compare? Proc.
10th Eur. Symp. Mar. Biol. 1:11-26.
Hunter, J. R.

1976. Culture and growth of northern anchovy, Engraulis
mordax, larvae. Fish. Bull., U.S. 74:81-88.

KLNNE, O,

1977. Pisces: Rearing of larvae. In 0. Kinne (editor),
Marine ecology, Vol. 3, p. 968-1004. Wiley N.Y.

Lasker, R., H. M. Feder, G. H. Theilacker, and R. C. May.

1970. Feeding, growth, and survival of Engraulis mordax
larvae reared in the laboratory. Mar. Biol. (Lond.)
5:345-353.

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
anchovy, Engraulis mordax, and other fishes due to
handling and preservation. Fish. Bull., U.S. 78:685-692.
Theil.acker, G. H., and M. E McMa.ster.

1971. Mass culture of the rotifer Brachionus plicatilis and
its evaluation as a food for larval anchovies. Mar. Biol.
(Berl.) 10:183-188.

Gail H. Theilacker

Southwest Fisheries Center La Jolla Laboratory
National Marine Fisheries Service, NOAA
P.O. Box 271
La Jolla, CA 92038

EFFECTIVENESS OF METERING WHEELS FOR

MEASUREMENT OF AREA SAMPLED BY

BEAM TRAWLS

It was the purpose of this study to evaluate the
effectiveness of using an odometer wheel to mea-
sure distance sampled by a trawl. A 3 m beam
trawl has been used extensively in a series of
benthic ecology studies off the coast of Oregon at
depths ranging between 50 and 4,000 m. Two
odometer wheels were attached to the trawl in an
attempt to measure the distance covered during
sampling. The effectiveness of the odometers was
examined statistically from performance data col-
lected during 337 hauls over a 3,950 m depth
range. In spite of repeated use and repeated
suggestions as to the usefulness ( Holme and Mcln-
tyre 1971; Menzies et al. 1973) there have been no

FISHERY BULLETIN: VOL. 78, NO. 3, 1980.

791

critical evaluations and few reports of faunal den-
sity specifically attributed to odometer wheels
(Belyaev and Sokolova 1960; Pearcy 1972; Carey
etal. 1973;Bieri 1974a, b).

Methods

Analysis consisted of comparisons of the actual
wheel performance with the performance ex-
pected of the wheels if working as designed. We
were concerned with accuracy and precision. Did
the wheels actually measure the distance towed,
and how much random variation was there in the
wheel counts? Exacting answers to these ques-
tions would have required a careful calibration of
the wheels under conditions encountered in sam-
pling at various depths. Such a deep-sea calibra-
tion would have required more effort than the
subsequent ecological sampling. However, partial
answers were obtained through the examination
of data collected during extensive ecological
sampling.

As the trawl was dragged along bottom, the
wheels should have rotated with the rotations
counted on the hub odometers. Due to friction in
the wheel mounts and poor consolidation of the
sediment, each wheel slipped some portion of the
distance dragged. Thus the wheel counts should
have normally underestimated the distance actu-
ally towed. We are confident that the wheels did
not rotate while in the water column because in
those accidental cases where the trawl failed to
reach bottom, <10 rotations were registered. On a
single haul variation in slippage caused the left
and right wheel to register different counts. How-
ever, even if biased, the wheel counts should have
shown three relationships. First, wheel counts
should have been positively correlated with other
estimates of distance based on navigational fixes
and towing times. Second, the ratios of wheel
counts accumulated from all hauls should have
provided information on the magnitude of the
variation between wheels due to small-scale
sediment changes and operational characteristics.
Third, if sampling occurred within an area of
faunal uniformity, catch size might have been re-
lated to wheel count. However, since catch was also
determined by the actual, usually patchy, faunal
distribution, the absence of positive correlation
can not be taken as unequivocal evidence that the
wheels did not function as designed.

Estimates of distance sampled based on changes
in loran A position or speed x duration of tow are

792

subject to major random error. In either case the
greatest error component is that associated with
determining the precise moment the trawl is on
and off bottom. Additionally loran A fixes contain
an inherent technical error, and speed x duration
estimates are dependent upon accurate deter-
minations of true speed over bottom. Since both of
these distance estimates were subject to random
error, correlation was the appropriate method of
comparison. The raw data were critically
examined to remove as much obvious misinfor-
mation as possible. If the distance by loran was
greater than it was possible for the ship to have
gone given speed and current conditions, the tow
was excluded. The greatest source of loran A error
seems to have been simple operator error yielding
tow distances that were far too great.

The beam trawl was made of a thick-walled,
hollow aluminum tube bolted across the top of two
steel skids. The skids were lined with netting, and
an otter trawl type net attached to the trailing
edge of the skids (Figure 1). The basic configura-
tion and full operating details have not changed
since the initial report by Carey and Heyamoto
( 1972). This beam trawl had many similarities to
those used for fishing since the 16th century
(Davis 1958). The bicycle wheels of an earlier ver-
sion of the trawl were replaced by heavier, spiked
aluminum disks to decrease damage to the wheels
during launch and recovery and while on bottom.
A Veeder Root^ model 54-794692 (Veeder Root
Corp., Hartford, Conn.) hub odometer was at-
tached to the axle of each wheel, counting once
each revolution (2 m distance). The counter was
housed in a thick-walled brass case filled with
silicon fluid to prevent air spaces which might lead
to crushing at high hydrostatic pressures. The
wheel and its mounting fork were attached to the
outside of each skid, free to pivot about the mount-
ing bolt. Surgical tubing was used to restrict the
angle of swing. Short lengths of angle iron were
welded to the bottom of the skids in front of the
wheels. These were intended to protect the wheels
and to prevent rotation while off bottom. The
trawl was paid out at a ship's speed through water
of approximately 2 kn. No weights were placed on
the bridle or towing line. The time of bottom con-
tact was estimated by an empirically determined
table of wire-out needed to reach bottom. A
Benthos model 1170 (Benthos Corp., Falmouth,

I

'Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

Figure l. — Skid and beam portion of the beam trawl. The towing bridle is attached to the upper leading edge of each skid (points B).
The headline is attached to points N. The lateral angle iron extensions (S) are intended to act as stops to prevent wheel turning when off
bottom. The skids are lined with netting (hatched areas). The main net is not shown, but the footline is represented by F.

Mass.) time-depth recorder was attached to the
trawl, but was lost after only 17 trials.

Results
Consistency of the Two Wheel Counts

Wheel count ratios ranged over a wide span of
values. However, there was good agreement be-

tween the wheels on about 50*^ of the hauls (Fig-
ure 2) with a ratio of 1.105 or less, and SS'^^ of the
ratios were <2.000. Even though the histogram of
ratios showed that close agreement between
wheels was more common than poor agreement, it
was difficult to determine the normal range of
random variation. A high ratio might have been
due to inherent variation or to mechanical failure
of one of the wheels. A wheel might have recorded

40,

30.

20

10-

50 PERCENTILE

■A Wi^y^ PyTxW myrr\ f

56 RATIOS > 2.00

.30 1.40 1.50

HIGH WHEEL COUNT

Y"^ ""^ , r-^'l Fl Fp_JLa — filfi^rrrri — ,i in f\

r

I 90

1.00

.60

.70

1.80

2.00

LOW WHEELCOUNT
Figure 2. — Frequency of occurrence of highrlow wheel count ratios, n = 337.

793

a very low count because it was fouled on the net or
jammed against the frame during some portion of
the tow, but have been in apparently good working
order when retrieved. For consistency during sub-
sequent analyses, all ratios >2.000 were consid-
ered to be due to a malfunction of one wheel caus-
ing a very low reading for the possible distance
towed. We feel that this cut off was justified on the
basis of the shape of the histogram of ratio fre-
quencies (Figure 2). Seventeen percent of all hauls
fell into this malfunction category. The remaining
33% of ratios, between 1.105 and 2.000, rep-
resented a high level of normal operational varia-
tion. In all cases of ratios >2.000 it was an un-
usually low wheel reading which produced the
high ratio, not an unusually high one. Ratios
>2.000 were not further considered in the
analyses.

Consistency with Other Estimates of Distance

Wheel counts were significantly positively cor-
related (959( level) with time duration and loran
determined estimates of distance (Table 1 ), but the
correlations were not high. Much more precise
estimates of time duration distances were avail-
able on the 17 tows employing a time-depth gage.
All the gaged hauls were taken between 2,500 m
and 3,000 m where bottom conditions were rela-
tively uniform. The correlations between the
wheel counts and distance based on gage time on
bottom were significant ( -1-0.89 at the 95% level)
and much higher than with wire-out determined
values. This marked improvement in correlation
indicates that errors in determining actual bottom
contact time were the major source of difference
between wheels and other measures of distance.

The 17 time-depth gage records were compared
with the wire-out time on bottom estimates. On
average the trawl was actually on bottom 23 min

Table l. — Correlation coefficients between measurements of
distance towed. All values are significantly greater than 0.0
(95% level). Asterisk denotes values significantly higher in
selected data. Significance was tested following
2-transformation. Data selection consisted of removing ex-
ceedingly large position changes and samples with a wheel ratio
>2.0 (see text).

Selected datan = 257

Item

Position

Time

High wheel

Low wheel

Raw data n =

337;

Position

0,529-

0,638-

0.628-

Time

0,370

,544

515

High wheel

.183

.591

.972-

Low wheel

,181

.551

.809

longer than predicted, varying from 75 min longer
to 65 min shorter.

The time-depth gage readings were also used to
determine a rough estimate of the amount of
wheel slippage. Using linear regression the gage
measurement of bottom time was taken as the
independent variable and the wheel counts as the
dependent variable. If the average speed over bot-
tom was the intended 2.0 kn, and if no slippage
occurred, then the slope of regression should have
been 30.85 (counts per minute). While sig-
nificantly different from zero, the slope of regres-
sion (19.2) was also significantly lower than the
expected 30.85 at the 95% level. This major dis-
crepancy may have been due to a ship's speed over
bottom consistently much less than 2.0 kn, consid-
erable wheel slippage, or both. If ship's speed over
bottom actually did average 2 kn, then an estimate
of the worst slippage was 40%. If the ship's speed
was consistently low, then the wheels performed
better by slipping less.

Wheel Counts Versus Catch Data

No consistent positive relationships were found
between the catch of the trawl and the wheel count
estimates of distance. This lack of the desired posi-
tive correlation was difficult to evaluate because
catch was controlled by performance of the trawl
and the actual distribution of the fauna. Faunal
variation among areas sampled may have masked
variation in catch due to differences in distance
towed.

In one comparison the echinoderm catch of 22
pairs of consecutive tows in approximately the
same bottom area at continental shelf depths was
examined. According to wire-out determinations
of time on and off bottom all 44 tows were on
bottom 20 min. Echinoderm catch was considered
because these asteroids, echinoids, and
holothuroids represent relatively immobile large
benthic organisms. The number of species and
total specimens were taken separately as mea-
sures of catch size. The number of times the longer
haul of the pair (as indicated by the magnitude of
the low wheel count on each sample) had the
greatest catch was tallied for all pairs of samples
and compared against random expectations using
a nonparametric sign test (Table 2). While having
a greater catch in most cases, the longer tows did
not take significantly higher numbers of
echinoderm species or specimens.

In addition we examined the catch of the abun-

794

Table 2. — Nonparametric sign test of catch sizes for selected
echinoderms in 22 pairs of samples. The long haul in each pair
was that with both wheel counts being greater than both wheel
counts of the other sample in the pair. When the counts over-
lapped, the pair was excluded since there was no unambiguous
longer or shorter haul. All sample pairs were taken at the same
locality on the same day.

Criterion

Highest value in

Significance

Long haul Short haul (PsO.05)

Most echinoderm species
Most echinoderm specimens

15
16

ns
ns

dant megafaunal holothuroids off Oregon at
2,500-3,000 m. The catches for each species were
compared with the wheel count estimates of dis-
tance towed (based on the average of the two
wheels) by computing correlation coefficients. Ac-
cording to wire-out determinations all of these
tows were on bottom 120 min. These coefficients
were computed with the zero holothuroid catches
included and then with zero catches excluded (Ta-
ble 3). There was no consistent pattern of positive
correlation.

Table 3. — Correlation of number of specimens of each species of
holothuroid with distance on bottom sampled as determined by
wheel counts (see text). Correlation coefficients were computed
for each species over all samples (n = 100) and for only those
samples where the species was taken (zeros excluded) to reduce
the effects of possible aggregation.

Correlation

No- of

All Zero catch

No- of

Species

hauls excluded

hauls

specimens

Paelopatides confundens

0-043 0034

90

5.857

Peniagone cf, dubia

0-205- 0-201

79

6.133

Scotoplanes globosa

0-044 0.045

75

4,521

Psychropodes longicaudata

0-210- 0-177

68

396

Molpadia musculus

0011 0-011

33

85

Pseudostichopus nudus

0-061 -0-191

22

48

■P^O.05.

Discussion

The earliest reported use of odometer wheels
was by Bieri and Bradshaw (cited in Gunther
1957) whose system evolved into a more sophisti-
cated opening and closing quantitative trawl
(Bieri and Tokioka 1968). Subsequently, Belyaev
and Sokolova (1960), Riedl (1961i, Gilat (1964),
Richards and Riley (1967i, Pequegnat et al.
(1970), and Carey and Heyamoto ( 1972) reported
the use of similar devices. Additionally, Wolff
( 1961) presented a photograph attributed to Zen-
kevitch of a Soviet beam trawl carrying four
odometer wheels similar to those discussed in this
report.

Positive correlation between counts, duration,
and position change is supportive of the basic con-

tention that the wheels can provide a measure of
the distance sampled. However, major questions
remain as to the accuracy and precision of the
wheels, and the relationship between estimates of
area sampled and the catch results. It must be
stressed that the positive correlation among dis-
tance estimates does not mean that they are either
accurate or precise. Our regression of the limited
time-depth bottom time estimates on odometer
readings indicated that the wheels were inaccu-
rate, being biased by as much as 40^ below the
actual distance. The numerous low wheel count
ratios indicated that the wheels did produce rela-
tively low variance measurements most of the
time.

Photographic evidence indicated that the lack of
a positive correlation between catch and wheel
count might have been due to irregularities that
affected total trawl performance, not just the
operation of the wheels. Using a camera mounted
to the trawl frame it was determined that during a
portion of each haul the trawl skids rocked for-
ward, lifting the footline of the net off bottom. The
odometer wheels, however, remained in contact
with the bottom registering the distance towed.
The severe saltations observed by Rowe and Men-
zies (1967) and Menzies et al. (1973) were not ob-
served in these photographs and did not appear to
be a problem with the beam trawl used in this
study.

The failure of the footline to constantly tend
bottom does not detract from the usefulness of
odometer wheels, but it does make it difficult to
interpret faunal data in terms of density ( Pearcy
1978). Nevertheless, in some preliminary com-
parisons of trawl versus photographic determina-
tions of faunal densities good agreement has been
found. Pearcy (1972) measured populations of the
pink shrimp, Pandalus jordani, at shelf depths
using both techniques and got similar estimates of
about 10 individuals/ m^. Similarly Carey et al.^
measured ophiuroid densities at about 2,500 m
and got similar estimates of 2 or 3 specimens /m'^.

Conclusions

The system of trawl frame and odometer wheels
used in this study did not produce estimates of

^Carey, A. G., Jr., J. Rucker, and R. Tipper. 1973. Benthic
ecological studies of deepwater dumpsite G in the northeast
Pacific Ocean off the coast of Washington. In Proceedings of the
First Conference of the Environmental Effects of Explosives and
Explosions (May 30-31, 1973), p. 120-137. Nav Ord. Lab. Tech.
Rep. 73-32, N.O.R.D.A., Bay St. Louis, MS 39520.

795

distance towed which could be used without reser-
vation to estimate the density of fauna. The posi-
tive correlation between wheel counts and two
other distance measures indicate that the wheels
do reflect distance. However, there is so much un-
certainty concerning accuracy and precision that
it is impossible to decide if apparent faunal density
variation is real or an artifact. The real potential
of bottom measuring wheels lies in the fact that
they are simple, inexpensive, as trawl equipment.
For certain sampling problems trawls will remain
the sampler of choice. If wheels can be improved
then trawl data can be quantified with greater
confidence. Future development should focus upon
improved precision and a method of field calibra-
tion to determine accuracy.

Acknowledgment

We gratefully acknowledge the financial sup-
port of the Biological Oceanography Program of
the National Science Foundation grant GB-4629;
the former Atomic Energy Commission contracts
AT(45-1) and AT(45-1)2227; and the National
Oceanic and Atmospheric Administration In-
stitutional Sea Grant 2-5187. Ship usage was par-
tially supported by National Science Foundation
grant OCE-7600061. The Department of Energy
reference for this manuscript is RLO-227-T12-72.
R. Ruff, M. Kyte, and R. Paul contributed to the
design of the beam trawl. W. Pearcy, D. Cohen, M.
Downey, and anonymous reviewers gave helpful
guidance during writing.

Literature Cited

Belyaev, G., and M. Sokolova.

1960. K voprosu o metodikye kolichestvennie issledovanii
glubokovodnogo bentosa [On the issue of quantitative
methods of investigation of deep-sea benthos]. [In Russ.]
Tr. Inst. Oceanol. 39:96-101,
BIERI, R.

1974a. A new species of Spadella (Chaetognatha) from
California. Publ. Seto Mar. Biol. Lab. 21:281-286.

1974b. First record of the chaetognath genus KrohnitteUa
in the Pacific and description of a ne-w species. Wasmann
J. Biol. 32:297-301.
BIERI, R., AND T. TOKIOKA.

1968. Dragonet II, an opening-closing quantitative trawl for
the study of microvertical distribution of zooplankton
and the meio-epibenthos. Publ. Seto Mar Biol. Lab.
15:373-390.

Carey, a. G., Jr., and H. Heyamoto.

1972. Techniques and equipment for sampling benthic
organisms. In A. T. Pruter and D. L. Alverson (editors),
The Columbia River estuary and adjacent ocean waters;

bioenvironmental studies, p. 378-408. Univ. of Wash.

Press, Seattle.
Davis, F. M.

1958. An account of the fishing gear of England and Wales.

Fish. Invest. Minist. Agric. Fish. Food (G.B.i, Ser II,

21(8), 165 p.
DIXON, W. J., AND F J. MASSEY, JR.

1969. Introduction to statistical analysis. 3d. ed.
McGraw-Hill, N.Y. 638 p.

GILAT, E.

1964. The macrobenthonic invertebrate communities on
the Mediterranean continental shelf of Israel. Bull. Inst.
Oceanogr Monaco 62 (1290), 46 p.
GUNTHER, G.

1957, Dredges and trawls. In J. Hedgpeth (editor).
Treatise on marine ecology and paleoecologj'. Vol, 1 , p, 73-
78, Geol. Soc. Am. Mem. 67.
Holme, N. A,, and A, D, MclNT\TiE (editors),

1971, Methods for the study of marine benthos, IBPdnt,
Biol, Programme) Handb, 16, 334 p.

MENZiES, R, J,, R. Y, George, and G, T Rowe,

1973, Abyssal environment and ecology of the world
oceans. Wiley, N.Y., 448 p.

Pearcy, W. G.

1972. Distribution and diel changes in the behavior of the
pink shrimp, Pandalus jordani , off Oregon. Proc. Natl,
Shellfi.sh, Assoc, 62:15-20,

1978, Distribution and abundance of small flatfishes and
other demersal fishes in a region of diverse sediments and
bathymetry off Oregon, Fish, Bull,, U,S, 76:629-640,
PEQUEGNAT, W, E,, T, J. BRIGHT, AND B, M, JA.MES,

1970. The benthic skimmer a new biological sampler for
deep-sea studies. In W, E. Pequegnat and F, A, Chase,
Jr, (editors). Contributions on the biology of the Gulf of
Mexico, p, 17-20, Tex. A&M Univ. Oceanogr. Stud. 1.

RICHARDS, S. W, AND G, A, RiLEY,

1967, The benthic epifauna of Long Island Sound. Bull.
Bingham Oceanogr. Collect. Yale Univ 19:89-135.
RIEDL, R.

1961, Etudes des fonds vaseux de lAdriatique, Methodes
et resultats. Reel, Trav, Stn, Mar, Endoume 23:
161-169,
ROWE, G, T, AND R. J. MENZIES.

1967. Use of sonic techniques and tension records as
improvement in abyssal trawling. Deep-Sea Res, 14:
271-272,
WOLFF, T

1961, Animal life from a single abyssal trawling, Gala-
thea Rep, 5:129-162,

ROBERT S, Carney

Department of Invertebrate Zoology
U.S. National Museum
Smithsonian Institution
Washington, DC 20560

School of Oceanography
Oregon State University
Corvallis, OR 97331

Andrew G, Carey, Jr,

796

STOMACH CONTENTS AND FECES AS

INDICATORS OF HARBOR SEAL,

PHOCA VITULINA, FOODS IN

THE GULF OF ALASKA

Traditional methods of investigating pinniped
feeding liabits have involved examination of
stomach contents from collected animals (Imler
and Sarber 1947; Spalding 1964; Fiscus and
Raines 1966). Recently, several scientists (Ainely
et al.^; Calambokidis et al.^) have used scats col-
lected from haulouts to study prey utilization of
the California sea lion, Zalophus californianus ,
and the harbor seal, Phoca vitulina. This
technique may be valuable in situations where
killing animals is not feasible or desirable. No
comparative information has been available for
relating the results of scat analysis to stomach
content analysis. Between 1975 and 1978 I iden-
tified food remains in stomachs and in feces from
351 harbor seals collected along the Gulf of Alaska
coast from Yakutat Bay to Kodiak Island and was
able to compare the data resulting from both
sources. The sample of seals included both sexes
and spanned all age-classes. Seals were collected
during all months except December and January.

Methods

Seals were collected by shooting. Stomach con-
tents were removed in the field, wrapped in muslin
and preserved in a 10% Formalin^ solution. Fecal
material from large intestines was washed
through nested sieves (2.00 and 0.84 mm^) and
identifiable materials were recovered and pre-
served in 70% ethanol. Identifications of prey from
both stomach contents and feces were based
primarily on fish otoliths, cephalopod (squid and
octopus) beaks and shrimp exoskeletons; occa-
sionally vertebrae, preopercular bones, and intact
specimens found in stomachs also were used. All
otolith identifications were verified by John E.

'Ainley, D. G., H. R. Huber, R. R. Le Valley, and S. H. Morrel.
1978. Studies of marine mammals at the Farallon Islands, Cal-
ifornia, 1976-77. Final report for MMC contract MM6AC027.
Available National Technical Information Service, 5285 Port
Royal Road, Springfield, VA 22151 as PB-286 603, 48 p.

^Calambokidis, J., K. Bowman, S. Carter, J. Cubbage, R Daw-
son, T. Fleischner, J. Schuett-Hames, J. Skidmore, and B. Tay-
lor. 1978. Chlorinated hydrocarbon concentrations and the
ecology and behavior of harbor seals in Washington State wa-
ters. The Evergreen State Coll., Processed Rep., 121 p.

^Reference to trade names does not imply endorsement by the
National Manne Fisheries Service, NOAA.

FISHERY BULLETIN: VOL. 78, NO. 3, 1980.

Fitch, California Department of Fish and Game,
Long Beach.

Findings were compared by percentage of occur-
rences (number of stomachs or large intestines in
which a prey species was found) in the stomach
and fecal samples.

Results and Discussion

Spearman rank correlation analysis showed a
significant positive correlation (r^. = 0.79,P<0.01)
between the rankings of prey occurrences from
stomach contents and feces (Table 1 ). The greatest
discrepancy in rankings was for cephalopods
which were ranked second in the analysis of
stomach contents and ninth in the fecal analysis.

Occurrences of individual prey categories from
stomach contents and feces showed good agree-
ment when analyzed with contingency tables (Ta-
ble 1). Only one significant statistical difference
(P<0.01) was found among 10 testable categories.
Cephalopods occurred more frequently (P<0.001)
in stomach contents than in feces. The x^ value for
cephalopods was so high (34.76) that rejection of
the null hypothesis seemed justified even in light
of potential type I errors resulting from multiple
tests.

Cephalopods were identified primarily by their
chitinous beaks in both stomach contents and
feces. Beaks that were recovered in fecal material,
although sometimes fragmented, were easily rec-
ognized. Apparently most beaks were regurgi-
tated rather than passed through the intestinal
tract. Captive northern fur seals, Callorhinus ur-
sinus, which had been fed squid were observed
regurgitating beaks (Miller'*). Miller observed
that the beaks appeared to be "trapped" in the
stomach and were regurgitated at about 2-d inter-
vals. This is probably also true in harbor seals as I
have occasionally seen "wads" of beaks packed into
the pyloric ends of stomachs. This would tend to
exaggerate utilization of cephalopods in stomach
contents if the beaks persisted longer than re-
mains of other prey Therefore cephalopods are
apparently substantially underrepresented in
feces and probably somewhat overrepresented in
stomach contents.

••Miller, L. K. 1978. Energetics of the northern fur seal in
relation to climate and food resources of the Bering Sea. Final
report for MMC contract MM5AC025. Available National Tech-
nical Information Service, 5285 Port Royal Road, Springfield. VA
22151asPB-275 296,32p.

797

Table l. — Comparative frequency of major prey identified in stomach contents and feces from 351 harbor seals
collected in the Gulf of Alaska. Prey are ranked in descending order of occurrence. Comparisons of proportion of
occurrence of prey found in stomach contents and feces were made by contingency table analysis when samples
were adequate (minimum cell size &5).

Stomach

Feces

Rank

Occurrences

Rank

Occurrences

Prey

No,

%

No

%

x'

Walleye pollock, Theragra chalcogramma

1

80

24,8

1

104

35.9

4,24

Cephalopods. squids and octopus

2

68

21,1

9

8

2.8

3476-

Capelin. Mallotus villosus

3

33

102

2

33

11.4

0,00

Flatfishes, Pleuronectidae

4

21

6.5

4

21

7.2

0.00

Pacific herring, Clupea harengus pallasi

55

20

62

3

24

8.3

0.39

Pacific cod, Gadus macrocephalus

55

20

6.2

6

17

5.9

0.26

Pacific sand lance, Ammodytes hexapterus

7

15

4.7

5

7

2.4

3.00

Pacific sandfish, Trichodon trichodon

8

10

3 1

10

19

6.6

2,91

Shrimps

9

7

2.2

14

4

1,4

—

Sculpins, Cottidae

10

6

1,9

7

14

4,8

3.29

Eelpouts, Lycodes spp.

11

5

16

10

7

2,4

0.34

Salmon, Oncorhynchus spp

13

4

1 2

15

0

0.0

—

Eulachon, Thaleicthys pacificus

13

4

12

13

5

1.7

—

Rockfishes, Sebastes spp.

13

4

12

10

7

2.4

—

Greenlings, Hexagrammos spp

15

2

0.6

12

6

1,2

—

Others'

23

7,1

14

4.8

Total occurrences

322

290

•p<o.oi.

'Others included unidentified prey and minor prey (those with

5 occurrences in both stomach contents and feces).

Salmon, Oncorhynchus spp., remains were iden-
tified in four stomachs while none were found in
the fecal samples. I have examined nine harbor
seal stomachs containing salmon remains and
only one included a head with otoliths. It appeared
that seals often fragmented large fish such as
salmon while eating them, usually discarding the
head. Thus, studies of feeding habits based on scat
analyses (which require the presence of otoliths)
probably underrepresent utilization of large fishes
such as salmon. One occurrence of a cartilaginous
fish was encountered (listed under others in Table
1). This was a skate, Raja sp., found in a stomach.
It is unlikely that cartilaginous fishes would be
detected in scats, as they have tiny, diffuse
otoliths. (Lagler et al. 1962).

In summary, it appears that analysis of scats
from harbor seals can provide accurate informa-
tion on utilization of most kinds of prey. However,
cephalopods, cartilaginous fishes, and large fishes
such as salmon may be underrepresented.
Cephalopod remains may be overrepresented in
stomach contents.

Acknowledgments

This work was supported by the Alaska De-
partment of Fish and Game and the Marine
Mammal Commission and by the Bureau of Land
Management through an interagency agreement
with the National Oceanic and Atmospheric Ad-

ministration, under which a multiyear program
responding to needs of petroleum development of
the Alaskan continental shelf is managed by the
Outer Continental Shelf Environmental Assess-
ment Program office. The suggestion to compare
results of the two methods of analysis was made by
F. Fay. Field assistance was provided by many
members of the Alaska Department of Fish and
Game. Thanks are due to D. Calkins, F. Fay, K.
Frost, L. Lowry, D. McKnight, K. Schneider, and
two anonymous reviewers for commenting on the
manuscript.

Literature Cited

FISCUS, C. H., AND G. A. BAINES.

1966. Food and feeding behavior of Steller and California
sea lions. J. Mammal. 47:195-200.
IMLER, R. H., AND H. R. SARBER.

1947. Harbor seals and sea lions in Alaska. U.S. Fish
Wildl. Ser\'., Spec. Sci. Rep. 28, 23 p.
Lagler, K. E, J. E. Bardach, and R. R. Miller.

1962. Ichthyology Wiley N.Y, 545 p.

Spalding, D. J.

1964. Comparative feeding habits of the fur seal, sea lion
and harbor seal on the British Columbia coast. Fish.
Res. Board Can., Bull. 146, 52 p.

Kenneth W. pitcher

Alaska Department of Fish and Game
333 Raspberry Road
Anchorage, AK 99502

798

THE 1978 SPRING RECREATIONAL CATCH OF

ATLANTIC MACKEREL, SCOMBER SCOMBRUS,

OFF THE MIDDLE ATLANTIC REGION

Atlantic mackerel. Scomber scomhrus, season-
ally migrate through the Middle Atlantic region,
usually appearing off Virginia in March with a
gradual movement inshore and north until they
move out of the area by mid-June. They spend
the summer and early autumn north of Cape
Cod, only briefly returning to the coastal waters
of the Middle Atlantic in late fall, before migrat-
ing offshore and south in late December or
January (Bigelow and Schroeder 1953). They
are primarily available to recreational anglers
along the Middle Atlantic coast during the
spring migration. As Christensen et al.^ found,
the autumn catch of Atlantic mackerel in New
Jersey in 1975 was <1% of the catch the follow-
ing spring. Recreational catches declined from
an estimated 32,000 t in 1970 (Deuel 1973) to
5,000 t in 1976 (Christensen et al. footnote 1).
Although the recreational catch estimates lack
measures of accuracy and reliability, the decline
follows the steady decline in total stock from 2.4
million t in 1969 to 469,000 t in 1978 (Anderson
1979).

An estimate of total landings and age composi-
tion of the catch is necessary for assessment and
management of the stock. This survey was in-
itiated by personnel of the Northeast Fisheries
Center (NEFC) Sandy Hook Laboratory National
Marine Fisheries Service iNMFS) in cooperation
with State personnel from the Delaware Division
of Fish and Wildlife, the New Jersey Division of
Fish, Game and Shellfisheries, and the New York
State Department of Environmental Conserva-
tion at the request of the Mid-Atlantic Fisheries
Management Council. Although the request was
to determine the 1978 recreational catch of Atlan-
tic mackerel between Virginia and New York, Vir-
ginia and Maryland were not included in the sur-
vey as the Atlantic mackerel fishing season had
already begun in those states.

Methods

Sampling

A list of inlets, grouped into five regions includ-

ing Delaware, southern New Jersey, northern New
Jersey, coastal Long Island, and Long Island
Sound (Table 1) was prepared for the Middle At-
lantic coastline (Figure 1). Inlets were randomly
selected for weekly sampling from the list of inlets
within the regions where Atlantic mackerel were
knowTi or anticipated to be present. The list indi-
cating availability of Atlantic mackerel in an area
was primarily determined by telephone conversa-
tions with marina owners and commercial sport-
fishing vessel operators advertising in two weekly
fishing magazines, The Fisherman'^ and The Long
Island Fisherman.^ These observations were then
confirmed during subsequent on-site interviews
with vessel operators. In this way it was possible to
concentrate sampling efforts in regions where At-
lantic mackerel were available and to determine
the lengths of the regional seasons.

Personnel from cooperating State agencies con-
fined sampling to their respective states and
worked primarily weekdays while NEFC person-
nel sampled in all regions both weekends and
weekdays following the movement of Atlantic
mackerel northward. Data collected before Atlan-

^The Fisherman for the New Jersey, Delmarva, and Hatteras
fisherman. NJF Publishing Corp., Sag Harbor, N.Y.

^The Long Island Fisherman. LIF Publishing Corp., Sag Har-
bor, N.Y.

T.\BLE 1. — Summary of sampling activity and dates of Atlantic
mackerel availability in regions along the Middle Atlantic coast
in 1978.

'Christensen, D. J., B. L. Freeman, and S. C. Turner 1976.
The United States recreational fishery for Atlantic mackerel.
Int. Comm. NW Atl. Fish., Res. Doc. 76/XII/142, ser no. 4038,
7 p.

FISHERY BULLETIN: VOL. 78. NO. .3. 1980.

No. of

Period

No. of days mack-

Inlets sampling

mackerel

erel were present

included >

days in

were

Region

In region
Indian River

region

available

Weekdays

Weekends

1 - Delaware

24

4 Apr.- 8 May

25

10

Roosevelt

II - Southern

Cape May

19

8 Apr -12 May

25

10

New

Hereford

Jersey

Townsend
Corson
Great Egg
Absecon
Beach Haven

III- Northern

Barnegat

22

15 Apr- 14 May

20

10

New

Manasquan

Jersey

Shark River
Sandy Hook

IV - South

Rockaway

21

29 Apr -28 May

20

10

Shore

East Rockaway

Long

Jones

Island

Fire Island

Shinnecock

Montauk

V - North

Greenport

27

5 May-8 June

25

10

Shore

Mattituck

Long

Mt. Sinai

Island

Port Jefferson
Stony Brook
Nissequogue
Northport
Huntington
Oyster Bay
Hempstead
Manhasset Bay
Little Neck Bay
City Island

799

Figure l. — Survey regions along the Middle Atlantic coast for recreational catch of Atlantic mackerel.

tic mackerel arrived or after they departed from a
region were omitted from subsequent analysis.
Boat counts were made at each inlet to determine
the number of vessels sailing through the inlet,
and interviews were conducted concurrently at
associated marinas, docks, and launching ramps
to determine vhe catch per vessel. There were no
adequate data available on which to base propor-
tions of interviews among different types of fish-
ing vessels. Therefore, as many interviews as
possible were made with all vessel types as they re-
turned to port.

Inlet vessel counts were made of party, char-
ter, and private boats. Charter boats are com-
mercial sportfishing vessels which are usually
reserved in advance by a group of fishermen for
their exclusive use for a negotiated single fee.

Party boats (head boats) are commercial sport-
fishing vessels filled on a first-come, first-served
basis at an established fee per person. Party
boats were subdivided into full- and half-day
categories based on their daily activity sched-
ules. Full-day party boats make a single day trip
of about 7-9 h duration while half-day party
boats make a morning and afternoon trip each
of which is usually 4-5 h in duration. Private
boats are noncommercial sportfishing vessels.
The term sportfishing does not exclude the
passengers or crew from selling part or all of
their catch.

Estimation of Fishing Effort

NEFC and Delaware personnel counted boats
either from 0500 to 1300 h or 1300 to 2000 h.

800

Morning counts and afternoon counts were
summed to determine daily counts. New Jersey
personnel counted boats passing through inlets
for entire days while New York personnel con-
centrated efforts obtaining interviews and did
not make inlet counts.

Inlets in the survey area were grouped into
three size classes (small, a; medium, b; large, c)
according to the maximum expected numbers of
each type of vessel using the inlet. The mean and
vai'iance of the number of vessels sailing daily
through inlets in each class was determined
separately for weekend days and weekdays as
boat traffic was frequently much greater on
weekends. The mean and variance for weekend
days and weekdays were combined using the
following formulae (Cochran 1977):

s, =

10 we, + 23 wd,
10 + 23

where s, = estimated mean number of vessels

sailing daily in inlet class /, where

i = a, b, c

we^ = estimated mean number of vessels

sailing daily on weekend days in

inlet class i

wd, = estimated mean number of vessels
sailing daily on weekdays in inlet
class i
10 = mean number of weekend days in

season
23 = mean number of weekdays in season

and the estimated variance of s, is:

vis) =

(.o^y-^.-do^T^'^.

where v (s^) = estimated variance of mean num-
ber of vessels sailing daily in in-
let class i

v (we-) = estimated variance of mean num-
ber of vessels sailing daily on
weekend days in inlet class i

V iwd^} = estimated variance of mean num-
ber of vessels sailing daily on
weekdays in inlet class i
10 and 23 = constants as above.

The mean, variance, and confidence interval of
the number of vessels of each type sailing daily in
all inlet classes was determined by combining the

means and variances according to the following
formulae (Cochran 1977):

s =

NgSg + NhSh + NcSc

where s = mean number of vessels sailing
daily through all inlets where the
vessel type occurs
N^,,Nf^,N^. = number of inlets in inlet classes
a, b, and c
s^, s^, s. = mean number of vessels sailing
daily through inlet classes a, b,
and c

v(s)

(

N, ^'

y

+

+

Na+Nb+ Nc .

V iSa)

(
(

Na+Nb+Nc _

Na ^'

A^a + A^6 + Nc

y
y

V (Sb)

V iSr)

where vis) = estimated variance of s

V (sa),y isb),v isc) = estimated variance of Sq,

Sb , and Sc

CI = s±1.96\ v(s)

where CI = 95*7^ confidence interval about s.

Estimation of Catch Rates

Interviews were made at dock sites, ma-
rinas, and launching ramps to determine vessel
catches. Vessel catches were determined rather
than individual angler catches since most pri-
vate boat and charter boat anglers share their
total catches. In addition, while some party boat
anglers may fish as individuals, it is common
practice for family or social gi'oups to share a
common fish container making it impossible to
determine the exact catch per angler. During
interviews the type of vessel, fishing location,
interview site location, number of Atlantic
mackerel caught, and fork lengths (FL) of
Atlantic mackerel were recorded.

Inspection of the distribution of catch
per vessel indicated a lognormal distribution.
Therefore, the catch numbers were first con-
verted to natural logs and then the means and

801

variances were calculated for each vessel type
over the entire survey area. The log mean and
log variance for each vessel type was trans-
formed, and the 959^ confidence interval about
the retransformed mean was calculated accord-
ing to the following formulae lAitchison and
Brown 1957):

and the 959^ confidence interval about the esti-
mate were calculated as follows:

c = exp

(,.,(.1^).,,,)

where c = mean catch per vessel

L = mean natural log of catch per vessel
V (L) = estimated variance of natural logs
to catch per vessel
n = number of vessels interviewed

The variance of c, v (c), is approximated by:

c
n

{v(L) + y2(v(L))^}

and

c±1.96\ v(c)

is a 957ir confidence interval about c.

Estimated Total Catches

The mean catch per inlet per day, its variance
assuming s and c were independent, and 95'7c
confidence intervals were calculated for each ves-
sel type using the following formulae:

sc = s X c

where 'sc = mean catch per inlet per day
s — mean trips per inlet per day
c = mean catch per vessel

V (sc) = (s)2 V (c) + (c)2 V is) + V (c) V (s)

where v isic) = estimated variance of catch per
inlet per day

V (s) = estimated variance of trips per

inlet per day

V (c) = estimated variance of catch per

vessel

CI = sc ±1. 96 Vv{sc)
where CI = 95% confidence interval about sc

The total estimated catch iTSC) per vessel type
802

where

TSC = [sc ± 1.96 Vv(sc)] x 33NI

TSC = total estimated catch
NI = number of inlets where vessel type

occurred
33 = number of days in fishing season

The total estimated catch and confidence in-
terval for the total survey area and all vessel
types were determined by summing the estimated
catches and extracting the square root of the sum
of the squares of the variances of all four vessel
types.

Lengths, Weights, and Age Compositicjn of Catches

A total of 2,778 Atlantic mackerel were mea-
sured to the nearest centimeter fork length to
determine the length frequencies of the catch.
Each length was converted to a weight using the
formula logio weight = -5.2314 + 3.0796 logio
length (Wilk et al. 1978), and a mean weight was
calculated for all vessel types. The mean weight
was multiplied by the total estimated number
caught to determine the total weight of the
catch.

For age composition analysis, Atlantic mack-
erel were obtained in April from recreational and
commercial fishermen fishing primarily along the
New Jersey coast and transported to the NEFC
Sandy Hook Laboratory where they were mea-
sured to the nearest centimeter fork length and
sexed. The heads were removed, frozen, and sent
to the NEFC Woods Hole Laboratory, NMFS, for
otolith removal and aging. Aging was accom-
plished by placing intact otoliths in black trays,
imbedding them in clear epoxy resin, and count-
ing annular rings using reflected light at 25-75 x
magnification under a binocular microscope. The
number of fish from the length-frequency sample
of 2,778 measured at each centimeter length was
multiplied by the percentage age composition at
that length increment to determine the number of
fish caught in each age-group at each centimeter
increment. The numbers at each age were summed
from all length increments and divided by the
total number of fish measured to determine the
percentage composition of each age in the recrea-
tional catch. The percentage composition at each
age was multiplied by the total estimated Middle

Atlantic catch to determine the estimated total
recreational catch by age-class in the Middle
Atlantic region.

Results and Discussion

Privately owned boats were by far the most
numerous type observed using inlets during the
survey (Table 2). The mean catch per vessel was
lowest for private boats, intermediate for half-
day party and charter boats, and highest for full-
day party boats (Table 2). Full-day party boats
anglers caught the most Atlantic mackerel dur-
ing the season followed in decreasing order by
anglers aboard private boats, half-day party
boats, and charter boats (Table 3). The total
estimated number of mackerel caught in the
survey area was 6,792,000 ±2,415,000.

The mean fork length of all Atlantic mackerel
measured during the survey was 37.9 cm and
the calculated mean weight was 0.515 kg/fish.
The total estimated weight caught was 3,498
±l,244t.

The survey was initiated after Atlantic mack-
erel had already progressed north into waters
off Delaware and southern New Jersey. There-
fore, it was too late to survey catches in the
southern portion of the Middle Atlantic region.
Maryland has a single inlet at Ocean City with a
few party boats, a modest number of charter
boats, and facilities for private boats. Virginia
has several locations such as Chincoteague,
Wachapreague, and Quinby along the coast of
the Delmarva Peninsula where some charter
and private boats have ocean access, and two

Table 2. — Average number of trips and catches of Atlantic
mackerel by sportfishing vessels during the Middle Atlantic
coast survey, 1978.

Mean trips

95°o

Mean catch

95°o

per inlet

confidence

per vessel

confidence

Vessel type

per day

interval

trip

interval

Party boats:

Full-day

3.87

±1.37

1.425

±542

Half-day

3.92

±1.75

352

±154

Charter boats

2.82

±1.11

346

±106

Private boats

56.41

±7.25

45

±8

inlets (Rudee and Lynnhaveni near the mouth
of Chesapeake Bay where a few party boats and a
number of charter and private boats have ocean
access to fish for Atlantic mackerel. The catch
made from Delaware's only two coastal inlets
was about 89^ of the Delaware and New Jersey
total. Assuming similar levels of effort and catch
at the six inlets in Maryland and Virginia, the
Maryland and Virginia catches were approx-
imately 25*7^ of the New Jersey and Delaware
total. The combined catch within the Delaware
and New Jersey regions was about 34% of the
catch (3,498 t) of the three-State area surveyed
or 1,189 t. Thus, the total estimated catch for
Virginia-New Jersey was 125% of 1,189 t or
1,486 t.

The number of party and charter boats in New
York was found to be approximately equal to the
combined fleets in Connecticut through Maine
(Fraser et al. 1977). Assuming similar levels of
Atlantic mackerel caught by commercial sport-
fishing vessels and private vessels in Connecti-
cut-Maine, New York catches accounted for 50%
of the North Atlantic regional catch (New York-
Maine) (Deuel 1973). The New York portion of
the Delaware, New Jersey-New York catch was
about 66% or 2,309 t of the 3,498 t total catch.
Therefore, the Connecticut-Maine catch was as-
sumed to also be 2,309 t, giving a New York-
Maine total of 4,617 t. The total recreational
catch of Atlantic mackerel taken by boat in the
Virginia-Maine area was estimated to be 6,103 t
of which 3,795 t was caught in the New York-
Virginia area.

A total of 278 Atlantic mackerel were aged
from samples collected during the survey. The
ages were found to range from 2 to >11 yr with
considerable overlap of age-classes at >36 cm
FL (Table 4). The range of all fish measured
during the survey was 27-44 cm FL (Table 5)
and the mean was 37.9 cm. It is apparent from
the estimated total catch by ages (Table 5) that
fish caught by recreationsl anglers came mainly
from the older age-groups. The remnants of the

Table 3. — Summary of catches of Atlantic mackerel made by sportfishing vessels encountered during the 1978

survey of the Middle Atlantic coast.

Mean catch per

95°

0 confidence

Number of inlets v^here

Total

95% confidence

Vessel type

inlet per day

interval

vessel type occurred

estimated catch

interval

Party boats:

Full-day

5.515

±3,673

19

3,458,000

±2,303,000

Half-day

1,380

±604

8

364,000

±159,000

Charter boats

976

±483

9

290.000

±143,000

Pnvate boats

2,538

±658

32

2,680,000

±695,000

Total

6,792,000

±2,415,000

803

Table 4. — Percentage age at length of Atlantic mackerel aged from samples collected during the
1978 spring sportfishing season along the Middle Atlantic coast.

Age (years)

Fork length (cm)

No.

2

3

4

5

6

7

8

9

10

11

>11

27

1

100.0

28

1

100 0

29

1

100,0

30

1

100.0

31

1

100,0

32

11

27.3

72.7

33

38

5.3

73.7

21 0

34

57

12.3

632

19,3

5.3

35

41

7.3

41 5

43,9

7.3

36

29

6.9

138

6,9

37.8

139

20.7

37

42

4.8

11,9

7,1

21.4

11.9

23.8

2.4

14.3

2,4

38

29

3.4

13.8

24.1

3.4

20.7

3.4

31.0

39

21

9.5

38 1

4.8

33.0

14.3

40

4

25.1

50.0

25.0

41

1

100.0

Total

278

Table 5. — Numbers, percentage age composition, mean length at age of recreationally caught Atlantic mackerel,
and estimated recreational catch in metric tons from New York through Virginia during 1978.

Age (years)

Fork length (cm)

2

3

4

5

6

7

8

9

10

11

>11

Total

27

1

1

28

2

2

30

2

2

32

1

3

4

33

1

17

5

23

34

8

42

13

4

67

35

9

51

55

9

124

36

18

35

18

96

35

53

255

37

28

69

41

124

69

138

14

83

14

580

38

25

100

176

25

151

25

226

728

39

55

221

28

194

83

581

40

72

143

72

287

41

94

94

42

24

24

43

5

5

44

1

1

Total

3

67

217

157

333

280

80

635

67

740

199

2,778

Percentage of total

0.1

2.4

78

5.7

12.0

10.1

29

229

2.4

26.6

7.2

100.1

Mean length at age. cm

27.7

35.8

35.4

36.0

36.9

37,5

38,7

38.7

382

38.9

—

—

Estimated total catch

(t) by age

4

92

296

214

455

383

109

867

92

1.011

272

3,795

large 1967 and 1969 year classes (Anderson
1979) which were 11 and 9 yr old in 1978 still
contributed nearly 50% of the recreational
catch. The percentage age composition of the
total stock in 1978 was estimated to be 23.1, 17.0,
22.7, 25.2, 7.0, 1.4, 1.2, 0.8, 0.8, 0.5, 0.4, and 0.1 for
ages 1 through 11 and >11 (Anderson 1979).
Comparisons of the two age composition esti-
mates indicates all age-groups older than 5
compose 5.1% of the stock and 84.1% of the
recreational catch. The mean fork length of age-
class 3 through 5 fish was only 2.2 cm less than
the mean fork length of all fish measured during
the recreational survey. Therefore, it does not
seem probable that the hook-and-line fishery is
size selective between age-classes >2 yr old. The
stock assessment (Anderson 1979) was based

partially on NMFS research vess-el trawl sur-
veys which did not include sampling inside the
27.4 m (15 fathom) contour. As most recre-
ational fishing is done inshore of the 27.4 m
contour, it is possible that older Atlantic mack-
erel concentrate inshore. This would result in a
delay in recruitment into the recreational fish-
ery until age 6 or greater.

Acknowledgments

We wish to express our appreciation to the
following personnel who assisted in the collection
of field data: Pernell Lewis, Robert Matus, Wil-
liam Rogers, Russell Terranova, and Paul Yus-
chak, NMFS; Ronal W Smith, Delaware Division
of Fish and Wildlife; Paul G. Scarlett, Barry Preim,

804

Raymond Townsend, and Joseph D. Vaughn, New
Jersey Division of Fish, Game, and Shellfish;
Donald Zacchae, Egbert Howell, and Al Kilthan,
New York State Department of Environmental
Conservation.

We also wish to thank Michael Pennington for
suggesting use of the lognormal transformation to
determine mean vessel catches, and Judy Pentilla
and Louise Dery for determining ages of the
Atlantic mackerel.

Literature Cited

AlTCHISON, J., AND A. C. BROWN.

1957. The log normal distribution with special reference to
its uses in economics. Camb. Univ. Press, Camb., 176 p.
ANDERSON, E. D.

. 1979. Assessment of the Northwest Atlantic mackerel,
Scomber scrombrus, stock. U.S. Dep. Commer, NOAA
Tech. Rep. NMFS SSRF-732, 13 p.
BIGELOW, H. B., AND W. C. SCHROEDER.

1953. Fishes of the Gulf of Maine. U.S. Fish. Wild. Serv.,
Fish. Bull. 74, 577 p.
COCHRAN, W. G.

1977. Sampling techniques. 3d ed. Wiley, N.Y., 428 p.
DEUEL, D. G.

1973. The 1970 salt-water angling survey. U.S. Dep.
Commer, Cur Fish. Stat. 6200, 54 p.
FR.\SER, M. B., J. A. HENDERSON, AND J. F MCNAUS.

1977. Survey of commercial sportfishing boats in the coas-
tal United States. Oreg. State Univ., Sea Grant Coll.
Program, Publ. ORESU-T-77-009, 28 p.

WILK, S. J., W. W. MORSE, AND D. E. RALPH.

1978. Length-weight relationships offish collected in the
New York Bight. Bull. N.J. Acad. Sci. 23(2):58-64.

DARRYL J. Christensen
WALTER J. Clifford

Northeast Fisheries Center Sandy Hook Laboratory
National Marine Fisheries Service, NOAA
Highlands, NJ 07732

than do their Atlantic counterparts. In addition,
the form of the spinous dorsal fin differs in fish
from the two ocean areas. The International Game
Fish Association ( IGFA), which keeps detailed and
precise records of the largest fish caught in various
sportfishing categories, maintains separate rec-
ords for Indo-Pacific and Atlantic sailfish. At pres-
ent, the largest sailfish caught by sportfishing
gear in the Pacific weighed 100.2 kg, and of the 14
different line test categories recorded by IGFA,
only two record Pacific sailfish weighed <70 kg. In
contrast, the largest Atlantic specimen weighed
58.1 kg and over half of the record catches were
<50 kg (International Game Fish Association 1980).
Morrow and Harbo ( 1969) stated that it was prob-
able that improved nutrition, better conditions for
growth, or some other favorable environmental
condition was responsible for the attainment of
the greater size in Indo-Pacific sailfish.

Size data for Atlantic sailfish caught by the
Japanese longline fishery in various areas of the
Atlantic have recently become available in the
annual publications of the International Commis-
sion for the Conservation of Atlantic Tunas. ^
These data show that unusually large sailfish also
occur in the Atlantic, specifically in the eastern
Atlantic off the coast of Africa between lat. 0° and
20° S (Figure 1; Areas F, G). Size frequencies from
the region indicate fish of substantially greater
size than from any of the other areas in the Atlan-
tic where size data from sailfish caught by the
longline fishery were available (Figure 2). I calcu-
lated the weights of eastern Atlantic specimens
using length-weight relationships developed by
various authors (Table 1). The results (Table 2)
show increasing variation in calculated weights as
fish length increases; however, regardless of which

SIZE AND POSSIBLE ORIGIN OF
SAILFISH, ISTIOPHORUS PLATYPTERUS,
FROM THE EASTERN ATLANTIC OCEAN»

Although Morrow and Harbo (1969) considered
the sailfish, Istiophorus platypterus, to be a single
worldwide species, other workers believe that the
Atlantic and Pacific forms are separate species
(Nakamura et al. 1968; Nakamura 1974). It has
long been recognized that Indo-Pacific specimens,
particularly those found along the coasts of
Panama and Mexico, attain a much greater size

'Southeast Fisheries Center Contribution No. 80-05M.

FISHERY BULLETIN: VOL. 78, NO. 3, 1980.

^International Commission for the Conservation of Atlantic
Tunas, Madrid, Data Records Vol. 10, p. 303-304 and Vol. 11, p.
267-270.

Table l. — Coefficients of the length-weight relationship for
western Atlantic sailfish (Lenarz and Nakamura 1974; JoUey
1974) and eastern Pacific sailfish (Kume and Joseph 1969; Wares
and Sakagawa 1974). All lengths are from posterior rim of orbit
to fork except Jolley, which is from orbit to origin of caudal keels.
Calculated weights will be in kilograms except for Lenarz and
Nakamura which will be in pounds.

Author

No. of
specimens

Size range

Iog,o3

b

Lenarz and Nakamura (1974)
Jolley (1974) Male

Female
Kume and Joseph (1969)
Wares and Sakagawa (1974)

244
182
230
28
802

15.8-62.5 in

76-156 cm

47-164 cm

134-205 cm

115-222 cm

-3.895
-5.784
-4.941
-3.936
-4.360

3.158
3.342
2.950
2.416
2.628

805

100 90 80 70 60 50 40 30 ^0 10 0 -10 -20

iiiilniiMiiilnipiiiiljiniinilMiiiiiiilmiinuliiiiiiiiiliiiiiiiiiliiiiiiiiiliiiiiiiiiliiiimiilii jJi'A"'lLi|l"'

-10-3

llll[lllllllll|illllllll[llllTTlll|ffllllill|lllllllll[iilllllli[lllllllll|illlliili|lllllllll|lllllillllllM

100 90 60 70 60 50 >I0 30 20 10 0 -10 -20

Figure l. — Areas and number of sailfish sampled from the Japanese longline fishery in the Atlantic, 1975-76.
Data are from Data Records 10, 11, International Commission for the Conservation of Atlantic Tunas (see text
footnote 2).

Table 2. — Estimated weights of sailfish caught by longline gear
in the eastern Atlantic (Figure 1; Areas F, G) using length- weight
relationships from various authors.

Author

Smallest'
(148^5 cm)

Average
(174,8 cm)

Largest
(223.5 cm)

-estimated weight, kg

21.9

36.7

79.9

229

39.8

91.0

23.2

37 7

78.3

20.5

30.3

54.9

22.2

34.2

65.2

Lenarz and Nakamura (1974)^
Jolley (1974)^ Male

Female
Kume and Joseph (1969)
Wares and Sakagawa (1974)

Average length in other five areas 140.7 cm

Average weight in other five areas 18.6 kg (Lenarz and Nakamura formula)

'There was one specimen measuring 116-120 cm fork length but was
excluded from this demonstration.

^Lenarz and Nakamura conducted their calculations in inches and pounds I
converted results using their formula into kilograms for this demonstration,

^Although Jolley s formula indicates that males in the eastern Atlantic attain a
greater weight at a given length than females, available evidence indicates that
this is not true for western Atlantic sailfish Only a few females in Jolley's sample
were as large as the average-sized eastern Atlantic specimen and the indica-
tion that males attain a greater weight is probably a result of extrapolation of
Jolley's formula beyond the limits of his data.

formula one uses, it is clear that the eastern At-
lantic specimens are unusually large fish (it
should be noted that estimated weights in Table 2
may be significantly affected by an unknown
logarithmic bias inherent in the length-weight

parameters). Using Lenarz and Nakamura's
(1974) formula, for example, the average weight of
sailfish sampled in the eastern Atlantic was only
21.4 kg less than the current all-tackle world rec-
ord for Atlantic sailfish, and the largest specimens
were 21.8 kg larger than the all-tackle record.
There is currently little sport fishing in the east-
ern Atlantic; however, between 1971 and 1975
seven world records were established for Atlantic
sailfish off the coast of Angola, including the cur-
rent all-tackle record of 58.1 kg.

There are striking similarities between the dis-
tribution of sailfish in the Pacific and Atlantic
Oceans. In both oceans, sailfish appear to be most
abundant on the western side and have a greater
north-south range than on the eastern side (Koto
et al. 1959; Kume and Joseph 1969; Ueyanagi et al.
1970). The largest specimens are apparently lo-
cated on the eastern side of their respective oceans
and in a fairly localized area. Size data on sailfish
from the eastern Pacific presented by Kume and
Joseph (1969) and Wares and Sakagawa (1974)

806

u
o

UJ

Q.

30-1

20-

10-

30n

20- M

10-

20-1 D

lo-

se-I

20-

10-

N =61
X =172.2

30-1

20-

10-

T — I — r

T 1 1 1 1 1

"1 c

0-S — 1—1—^ 1

1 — I — I — I

Figure 2— Length frequencies of sailfish captured by the
Japanese longline fishery in the Atlantic, 1975-76. Letters indi-
cate areas from Figure 1.

agree quite well with similar data on eastern At-
lantic specimens sampled off the coast of Africa,
both in range and average length. Additionally,
size frequencies of sailfish from the East China
Sea (Koto et al. 1959) are quite similar to size data
for western Atlantic sailfish given by Jolley (1977).
In both the eastern Pacific and eastern Atlantic,
sailfish occur in an area where a substantial sur-
face fishery for yellow^n and skipjack tunas takes
place. Fox^, in his analysis of the temporal and
spatial relationships among tunas and billfishes
in the Atlantic, showed a strong correlation be-
tween the occurrence of sailfish and yellowfin tuna
in the Atlantic and a strong relationship between
the occurrence of the two species and surface
water temperatures.

There are also similarities in the environment
on the eastern sides of the Atlantic and Pacific
Oceans where the largest specimens of sailfish
occur. Both areas have relatively shallow thermo-
clines. Thermal domes occur in both the eastern
Atlantic (Mazeika 1967) and the eastern Pacific
( Wyrtki 1964) and probably influence the season-
al distribution of at least some oceanic fishes
(Beardsley 1969).

It seems possible, therefore, that environmental
conditions in both the eastern Pacific and eastern
Atlantic favor rapid growth and the attainment of
a large size in sailfish.

There is also the possibility that the group of
large sailfish off Africa are immigrants from the
Indian Ocean around the tip of South Africa.
Other large oceanic fishes, such as the albacore,
Thunnus alalunga, and the black marlin, Makaira
indica, are suspected to have entered the Atlantic
by this route (Koto 1969; Wise and Davis 1973),
and Penrith and Cram (1974) reported that six
species of billfishes have been recorded in waters
west and south of the Cape of Good Hope. The
sailfish, however, was not included in this group.
Even though Penrith and Cram did not find
sailfish in their samples, the presence of other
istiophorids suggests that sailfish probably are
present at times in this area.

The sizes of sailfish from the eastern Atlantic
and the western Indian Ocean are similar. Merrett

EYE-FORK LENGTH, CM

^Fox,W. W., Jr. 197L Temporal-spatial relationships among
tunas and billfishes based on the Japanese longline fishery in the
Atlantic Ocean, 1956-1965. Univ. Miami Sea Grant Tech. Bull.
12, 78 p.

807

(1971) examined 77 sailfish caught on longlines off
East Africa and found that the majority were be-
tween 160 and 185 cm body length (center of orbit
to tip of shortest caudal ray), which is consistent
with the modes found for sailfish off Africa (Figure

2).

It seems possible, then, that when oceanograph-
ic conditions are favorable, sailfish move from the
western Indian Ocean to the eastern Atlantic
around the tip of South Africa. Based on the size
samples available from the longline fishery in
other areas of the Atlantic and size frequencies of
sailfish caught in the sport fishery in the western
Atlantic (de Sylva 1957; Jolley 1977), these fish
apparently remain in a fairly restricted area off
the coast of West Africa.

Acknow ledgmcnts

I thank John Jolley, C. Richard Robins, Donald
P de Sylva, and Francis Williams for reviewing
the manuscript.

Literature Cited

Beardsley.G. L., Jr.

1969. Distribution and apparent relative abundance of yel-
lowfin tuna (Thunnus albacares) in the eastern tropical
Atlantic in relation to oceanographic features. Bull.
Mar Sci. 19:48-56.
DE SYLVA, D. P.

1957. Studies on the age and growth of the Atlantic
sailfish, Istiophorus americanus (Cuvier), using length-
frequency curves. Bull. Mar Sci. Gulf Caribb. 7:1-20.
INTERNATIONAL GAME FiSH ASSOCLATION.

1980. World record game fishes. Int. Game Fish As-
soc, Ft. Lauderdale, Fla., 287 p.
JOLLEY, J. W, JR.

1974. On the biology of Florida east coast Atlantic sailfish
(Istiophorus platypterus). In R. S. Shomura and F Wil-
liams (editors). Proceedings of the International Billfish
Symposium, Kailua-Kona, Hawaii, 9-12 August 1972,
Part 2. Review and contributed papers, p. 81-88. U.S. Dep.
Commer, NOAA Tech. Rep. NMFS SSRF-675.
1977. The biology and fishery of Atlantic sailfish, Is-
tiophorus platypterus, from southeast Florida. Fla. Mar
Res. Publ. 28, 31 p.
KOTO, T.

1969. Studies on the albacore— XIV. Distribution and
movement of the albacore in the Indian and the Atlantic
Oceans based on the catch statistics of Japanese tuna
long-line fishery. Bull. Far Seas Fish. Res. Lab.
(Shimizu) 1:115-129.
KOTO, T, I. FURUKAWA, AND K. KODAMA.

1959. Studies on the tuna longline fishery in the East
China Sea - III. Ecological studies on the sailfish. [In Jpn.,
Engl, abstr] Rep. Nankai Reg. Fish. Res. Lab. 10:88-106.
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.

Lenarz, W. H., and E. L. NAKAMURA.

1974. Analysis of length and weight data on three species
of billfish from the western Atlantic Ocean. In R. S.
Shomura and F. Williams (editors). Proceedings of the
International Billfish Symposium, Kailua-Kona, Hawaii,
9-12 August 1972, Part 2. Review and contributed papers,
p. 121-125. U.S. Dep. Commer, NOAA Tech. Rep. NMFS
SSRF-675.

Mazeika, R a.

1967. Thermal domes in the eastern tropical Atlantic
Ocean. Limnol. Oceanogr. 12:537-539.

MERRETT, N. R.

1971. Aspects of the biology of billfish (Istiophoridae) from
the equatorial western Indian Ocean. J. Zool. (Lond.)
163:351-395.

Morrow, J. E., and S. J. Harbo.

1969. A revision of the sailfish genus /sfjop/iorws. Copeia.
1969:34-44.

Nakamura, I.

1974. Some aspects of the systematics and distribution of
billfishes. In R. S. Shomura and F Williams (editors),
Proceedings of the International Billfish Symposium,
Kailua-Kona, Hawaii, 9-12 August 1972, Part 2. Review
and contributed papers, p. 45-53. U.S. Dep. Commer,
NOAA Tech. Rep. NMFS SSRF-675.

Nakamura, I., T. Iwai, and K. Matsubara.

1968. A review of the .sailfish, spearfish, marlin and sword-
fish of the world. [In Jpn.] Kyoto Univ, Misaki Mar
Biol. Inst., Spec. Rep. 4, 95 p.

Penrith, M. J., and D. L. Cram.

1974. The Cape of Good Hope: a hidden barrier to billfishes.
In R. S. Shomura and F Williams (editors), Proceedings of
the International Billfish Symposium, Kailua-Kona,
Hawaii, 9-12 August 1972, Part 2. Review and contributed
papers, p. 175-187. U.S. Dep. Commer, NOAA Tech. Rep.
NMFS SSRF-675.
UEYANAGI, S., S. KIKAWA, M. UTO, and Y. NISHIKAWA.

1970. Distribution, spawning, and relative abundance of
billfishes in the Atlantic Ocean. [In Jpn., Engl,
synop.] Bull. Far Seas Fish. Res. Lab. (Shimizu) 3:15-55.

WARES, P G., AND G. T. SAKAGAWA.

1974. Some morphometries of billfishes from the eastern
Pacific Ocean. In R. S. Shomura and F. Williams (editors),
Proceedings of the International Billfish Symposium,
Kailua-Kona, Hawaii, 9-12 August 1972, Part 2. Review
and contributed papers, p. 107-120. U.S. Dep. Commer,
NOAA Tech. Rep. NMFS SSRF-675.
WISE, J. R, AND C. W. Davis.

1973. Seasonal distribution of tunas and billfishes in the
Atlantic. U.S. Dep. Commer, NOAA Tech. Rep. NMFS
SSRF-662,24p.
WYRTKI,K.

1964. Upwelling in the Costa Rica Dome. U.S. Fish Wildl.
Serv. Fish Bull. 63:355-372.

GRANT L. BEARDSLEY

Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service. NOAA

75 Virginia Beach Drive

Miami, FL 33149

808

AMMONIA CONCENTRATIONS IN PINK

SALMON, ONCORHYNCHUS GORBUSCHA,

REDDS OF SASHIN CREEK,

SOUTHEASTERN ALASKA

Although the toxic effects of ammonia have been
observed in developing salmonids in hatcheries,
few measurements of ammonia are available from
the natural environment. In the fall of 1969, am-
monia levels in the surface waters of Sashin
Creek, southern Baranof Island, southeastern
Alaska, were measured during and after the run of
pink salmon, Oncorhynchus gorbuscha. Ammonia
levels increased significantly after the run. This
increase was attributed to the large number of
decaying carcasses of spawned-out adult salmon
iBrickell and Goering 1972). Low levels of am-
moniacal nitrogen have been found in samples of
intragravel waters of Sashin Creek taken in Au-
gust, just before most fish spawned (McNeil et al.
1964). Ammonia concentrations have not been
measured in intragravel water taken directly from
salmon redds with known densities of eggs or ale-
vins.

The transition period just before and during
emergence of alevins from the gi'avel is critical for
survival of 3'oung salmon. The young salmon have
a higher rate of metabolism than eggs and early
alevins (Bailey et al. 1980) and are undergoing
physiological changes to enable them to actively
swim and feed rather than reside quietly in the
gravel. Salmonid alevins nearing the end of yolk
absorption excrete ammonia at a higher rate than
eggs or early alevins (Rice and Stokes 1975; Bailey
et al. 1980) and are more sensitive to ammonia
than earlier stages (Penaz 1965; Rice and Stokes
1975; Rice and Bailey 1980). At the same time
(winter and spring), freezing weather usually
causes surface and intragravel water flows to be
low and thus reduces the removal rate of excreted
ammonia. In 1972 we measured ammonia in sam-
ples of intragravel water taken from random sites
in Sashin Creek, including pink salmon redds, and
measured densities of live and dead alevins at each
sample site. In this paper we report the concentra-
tions of total ammonia (un-ionized and ionized)
found in stream and intragravel water and discuss
the effect of ammonia concentrations on develop-
ing alevins.

Methods
In late March we sampled 60 random intra-

FISHERY BULLETIN: VOL. 78. NO. 3. 1980.

gravel sites and 4 typical surface sites. Water flow
in Sashin Creek was low, which was normal for
late March — the rainy season had not begun and
the winter snow was not melting. The water tem-
perature was 1.6' C and pH was 6.7. Samples of
intragravel water were taken from standpipes
(McNeil 1962; McNeil et al. 1964). Water samples
were frozen in glass bottles within 2 h of sampling
and kept frozen until analyzed within 3 d.

We determined concentrations of total ammonia
(NH3 -I- NH4*) using an automated method that
quantitates the intensity of blue indophenol after
reaction of ammonia with alkaline phenol hypo-
chlorite (U.S. Environmental Protection Agency
[EPA] 1974). The EPA method was modified by
stabilizing the heat source during the reaction to
increase sensitivity to a detection limit of 0.004
ppm ammonia. Analyses were made on freshly
thawed water samples. Some samples and stan-
dards of knowTi concentration were measured, fro-
zen, and thawed a second time, and again
measured. The ammonia levels did not change,
indicating that our preserving technique was
adequate. The slightly acid water of Sashin Creek
aided in the retention of ammonia.

The density of eggs and alevins was measured at
each site within 2 h of sampling for ammonia. We
sampled an area of 0.1 m^, centered on the
standpipe site, with a hydraulic egg-pump ( McNeil
1964), and counted dead eggs, live eggs, and ale-
vins.

Concentrations of Ammonia in
Intragravel Water and its Implications

Concentrations of ammonia and densities of
eggs and alevins varied widely. Total ammonia in
intragravel waters ranged from 0.008 to 0.240
ppm, and density of live eggs and alevins ranged
from 0 to 352/0.1 m^ (average 21.2) (Table 1). The
densities of pink salmon eggs and alevins found in
Sashin Creek were typical of many streams in
southeastern Alaska'.

The concentrations of ammonia were not corre-
lated with location in the stream (r = -0.18.
P>0.05 for ammonia concentrations measured in

'The average densities of pink salmon alevins for 96 pink
salmon streams of southeastern Alaska, 1966-1974, varied from
<1 to 30 ale\ins/0.1 m^ (Kingsbury, A., P. Larson, and G. Dow-
ney. 1975. Forecast ofthe 1975 pink salmon returns to south-
eastern Alaska. Alaska Dep. Fish Game, Inform. Leafl. 168,
33 p on file at Northwest and Alaska Fish. Cent.. Auke Bay
Lab., Natl. Mar Fish. Serv., NOAA, PO. Box 155, Auke Bay. AK
99821).

809

Table l. — Density of salmon eggs and alevins, and concentra-
tion of ammonia in intragravel waters of Sashin Creek, south-
eastern Alaska. Pink salmon eggs or alevins predominated, al-
though a few coho salmon, Oncorhynchus kisutch, eggs, <10%,
were occasionally present at the sample sites and are included in
the totals. Four surface samples were also measured, ranging
from 0.005 to 0.019 ppm total ammonia (average 0.013 ppm).

^^"['P'® Number of eqgs and alevins/0.1 m^
site ^-^

Total ammonia

number Dead

Live

Total

(ppm)

Sites with highest numbers of eggs

and alevins

a 12

352

364

0.018

189 138

107

245

0.010

190 232

0

232

0.010

10 6

213

219

0.015

97 193

11

204

0035

Sites with highest concentrations of

ammonia (NH3

1 + NH4 + )

95 0

2

2

0.240

92 10

0

10

0.240

100 4

0

4

0.115

87 3

0

3

0.065

105 41

9

50

0.065

Combined values for all 60 sites

Mean ±95%

confidence

interval 23.6±12,3

21.2±15.0

0.035±0.012

Range 0-232

0-352

0.005-0.240

upstream versus downstream locations) nor with
the density ofeggs and alevins (r = -0.17,P>0.10)
(Table 1). None of the five sample sites with the
highest ammonia concentrations was among the
five sites with the highest densities of eggs and
alevins.

The lack of correlation of ammonia concentra-
tions with alevin densities may be due to the var-
iability of intragravel water flow. Intragravel
water flow varies considerably from site to site in
all streams and is affected by surface water veloc-
ity, volume of water flow, stream gradient, gravel
size, and obstructions such as trees or ice (Vaux
1968). Intragravel flow may differ in adjacent
redds (cross-stream or upstream-downstream).
Brickell and Goering (1972) found that ammonia
concentrations in surface waters of Sashin Creek
during the fall spawning were generally greater at
the downstream sites than at the upstream sites.
In contrast, we found no relation between concen-
trations of ammonia sampled in the spring from
intragravel waters at upstream and downstream
sites at Sashin Creek. Furthermore, the concen-
trations of ammonia in surface water in our study
were much lower and more uniform than the con-
centrations in the intragravel water. We conclude
that measurements of ammonia in surface water
are poor estimates of ammonia concentrations of
intragravel water.

Twice each year, in early spring and in fall, am-
monia concentrations in salmon streams can be

expected to reach levels potentially harmful to
salmon eggs and alevins. In the fall, a large mass
of decaying salmon carcasses may litter the
stream. Brickell and Goering (1972) measured
ammoniacal nitrogen in surface waters of Sashin
Creek during and after a heavy run of salmon and
found concentrations of ammonia to be greater
than concentrations of ammonia that we found in
surface waters in the spring. Brickell and Goering
concluded that the ammonia was from the decay-
ing carcasses and not from excretion by pre-eyed
salmon eggs. Pre-eyed salmon eggs have low
ammonia-excretion rates (Rice and Stokes 1975;
Bailey et al. 1980). Unfortunately, no samples of
intragravel water were measured in the study by
Brickell and Goering, but the potential for harm to
developing eggs is probably low because pink
salmon eggs are quite tolerant of ammonia at this
life stage (Rice and Bailey 1980). In early spring
when water flows are low and excretion rates of
developing alevins are maximum, high concentra-
tions of ammonia could result. We found concen-
trations of ammonia in some of the salmon redds to
be higher than the concentrations in concurrent
samples of surface water and even higher than the
concentrations reported by Brickell and Goering
in the surface water in the fall.

Although the probability of exposure to high
levels of ammonia in spawning grounds is greatest
in the spring when alevins are most sensitive, the
highest level we observed was below dangerous
levels. The highest concentration of ammonia that
we found in the intragravel samples was 0.24 ppm
total ammonia, which is about 0.1 ppb of toxic
un-ionized ammonia at the pH and temperature of
Sashin Creek. This concentration is only about
one-tenth of the lowest concentration that affected
the size of fry resulting from alevins exposed to
ammonia for 61 days (Rice and Bailey 1980) and
about two-thirds of the maximum concentration
found in hatchery incubators containing unusu-
ally high densities of eggs (Bailey et al. 1980). Our
highest value for intragravel water exceeded the
highest concentrations found in surface water of
Sashin Creek (Brickell and Goering 1972) when
many decaying salmon carcasses were present.

In subarctic and arctic streams where water
temperature and pH are low, it seems unlikely
that ammonia will accumulate in intragravel
waters to concentrations that will significantly
affect size or survival of salmon alevins. Ammonia
toxicity may be significant at higher tempera-
tures, especially in more alkaline streams.

810

Acknowledgments

Howard Sears helped us collect the water sam-
ples, and William R. Heard and Roy Martin lo-
cated the random sites and determined the density
of alevins at each site.

Literature Cited

Bailey, J. E., S. D. Rice, J. J. Pella, and S. G. Taylor.

1980. Effects of seeding density of pink salmon, Oncorhyn-
chus gorbuscha, eggs on water chemistry, frj' characteris-
tics, and fry sur\'ival in gravel incubators. Fish. Bull.,
U.S. 78:649-658.

BRICKELL, D. C. and J. J. GOERING.

1972. Chemical effects of salmon decomposition on aquatic
ecosystems. In R. S. Murphy and D. Nyquist (editors).
International Symposium on Water Pollution Control in
Cold Climates, p. 125-138. U.S. Gov. Print. Off., Wash.,
D.C.

McNeil, W. J.

1962. Variations in the dissolved oxygen content of intra-
gravel water in four spawTiing streams of southeastern
Alaska. U.S. Fish Wildl. Serv., Spec. Sci. Rep. Fish. 402,
15 p.

1964. A method of measuring mortality of pink salmon
eggs and larvae. U.S. Fish Wildl. Serv., Fish. Bull.
63:575-588.

McNeil, W. J., R. A. Wells, and D. C. Brickell.

1964. Disappearance of dead pink salmon eggs and larvae
from Sashin Creek, Baranof Island, Alaska. U.S. Fish
Wildl. Serv., Spec. Sci. Rep. Fish. 485, 13 p.

PEN.^Z, M.

1965. Influence of ammonia on eggs and spawns of stream
trout Salmo trutta M. Fario. Zool. Listy, Folia Zool.
14:47-53. [Translated by and available from Foreign
Fisheries (Translations), U.S. Dep. Commer., Wash., D.C]

Rice, S, D., and J. E. Bailey.

1980. Survival, size, and emergence of pink salmon, On-
corhynchus gorbuscha, alevins after short- and long-term
exposures to ammonia. Fish. Bull., U.S. 78:641-648.

Rice, S. D., .>\nd r. m. Stokes.

1975. Acute toxicity of ammonia to several developmental
stages of rainbow trout, Salmo gairdneri. Fish. Bull.,
U.S. 73:207-211.

U.S. Environmental Protection Agency.

1974. Methods for chemical analysis of water and wastes.

U.S. Environ. Prot. Agency EPA-625-16- 74-003, 298 p..

Wash., D.C.
Vaux, W. G.

1968. Intragravel flow and interchange of water in a

streambed. U.S. Fish. Wildl. Serv., Fish. Bull. 66:479-

489.

Stanley D. Rice
Jack E. Bailey

Northwest and Alaska Fisheries Center

Auke Bay Laboratory

National Marine Fisheries Service, NOAA

P.O. Box 155

Auke Bay. AK 99821

EGG CANNIBALISM IN THE
NORTHERN ANCHOVY, ESGRAULIS MORDAX

Anchovies feed on their own eggs. Egg canni-
balism has been reported for the Argentine an-
chovy, Engraiz/is anchoita fde Ciechomski 1967)
Japanese anchovy, E. Japonicus (Hayasi 1967)
anchoveta, E. ringens (Rojas de Mendiola et al/)
and the northern anchovy, E. mordax (Loukashkin
1970). These studies give no indication whether
this cannibalism was a significant part of natural
mortality and incidence of cannibalism was in-
cluded only as part of a general description of food
habits. We provide evidence that egg cannibalism
may account for a considerable proportion of
natural egg mortality in the northern anchovy.

Northern anchovy feed by biting larger prey
and by filtering smaller ones ( Leong and O'Connell
1969). If both large and small prey are offered in
the laboratory, northern anchovy in the front of
the school bite the larger prey, whereas those at
the end of the school feed by filtering the smaller
prey (O'Connell 1972). Our laboratory observa-
tions indicate that adult northern anchovy feed on
their eggs by filtering, whereas even the smallest
anchovy larvae (ca. 3-4 mm long) are bitten. Such
small larvae are digested beyond identification in
30 min, whereas the identifiable whole chorions
and fragments may remain in northern anchovy
stomachs up to 8 h although the contents of the
egg ( embryo and yolk ) are digested after about 2 h.
Northern anchovy eggs are prolate spheroids and
can be easily distinguished from the spherical
eggs of other pelagic spawners in the Southern
California Bight.

Methods

The incidence of cannibalism in northern an-
chovy was estimated from an examination of 31
sets of stomach samples, usually of 10 adults each.
Samples were taken at the peak of the spawning
season, in the Southern California Bight, during
March 1976 and 1977 (Table 1). Northern anchovy
were collected in a midwater trawl or a commercial
lampara net: 28 sets of collections were taken at
night between sunset and sunrise and 3 sets
during the day. Fish were frozen in liquid nitrogen

'Rojas de Mendiola, B., N. Ochoa, R. Calienes, and O.
Gomez. 1969. Contenido estomacal de anchoveta en cuarto
areas de la costa Peruana. Inst. Mar. Peru Inf. Espec.
(IM-27),29p.

FISHERY BULLETIN: VOL. 78, NO. 3, 1980.

811

Table l. — Incidence of anchovy eggs in stomachs of northern anchovy collected in March 1976 and 1977 in the Los Angeles Bight.

Time of day

Collection

Number fish

Mean standard

Mean weight

Mean

Fish with eggs

Mean number

(h)

number'

per collection

length (cm)

(g)

percentage full^

(%)

eggs per fish

1300

31

25

10.0

10.2

7

68

1.9

1500

29

23

11.7

17.9

13

96

8.4

1500

30

11

124

19.9

14

100

6.4

2000

4

10

13.4

22.7

18

50

2.0

2000

5

10

13.4

23.3

18

10

0.1

2000

7

20

13.4

24.9

12

5

1.0

2000

17

10

10.5

11,7

17

30

.7

2100

1

11

10.7

100

82

2.3

2100

8

10

13.5

25.4

15

0

.0

2100

10

10

10.5

12.5

100

3.8

2100

14

10

11.6

16.2

49

40

0.6

2100

20

10

11.4

150

32

20

0.2

2100

23

10

12.1

19.1

38

0

.0

2200

6

10

20

0.2

2200

9

10

13.7

28.5

13

40

0.9

2200

15

10

11 4

15.9

56

50

7.1

2200

18

10

11.9

17.9

18

70

4.9

2300

11

10

11.4

16.5

14

10

0.1

2300

21

10

12.1

17.9

39

0

.0

2300

24

10

11.8

18.4

35

20

0.2

2400

2

10

10.6

12.2

4

50

3.0

2400

16

10

11.2

14.2

17

60

11.3

2400

19

10

11.5

15.3

15

90

4.6

0100

12

10

11.8

16.7

13

70

2.1

0100

13

10

11.1

14.7

25

90

221

0100

25

10

12.9

23.4

30

0

.0

0200

3

28

9.0

7.9

4

86

390

0400

27

10

12.0

17.9

31

90

20.9

0500

22

10

12,3

19.4

18

20

0.4

0500

26

10

12.3

193

28

30

0.9

0700

28

10

11.6

16.3

20

50

1.7

Means ± 2 SE of mean:

Night (W = 28)

11.8±.04

17.5±1.8

23±4

42±12

4.6±3.3

Day (W = 3)

11. 4± 1.4

16.0±5.9

12±5

88=20

5.6±3.5

Collections 1-9. night trawls, March 1976: collections 10-25, night trawls, March 1977: collections 26-28 night lampara sets, March 1977: and collections
29-31 day lampara sets, March 1976.
^ Volume stomach contents/volume maximum contents x 100, Maximum stomach volume was size specific and derived from the relationship developed in the text.

at the time of capture, except for the day collec-
tions where formaldehyde preservation was used.
A standard oblique plankton tow (Smith and
Richardson 1977) from 70 m (depth of water
permitting) to the surface, was taken before and
after each night trawl sample using aim ring net
(505 ^im mesh) or Bongo net (333 /xm mesh) and
was preserved in lO'yf Formalin. The 505 ;um
mesh net was corrected for extrusion of eggs using
the coefficient of Lenarz (1972). These collections
were used to estimate the abundance of northern
anchovy eggs in the regions where anchovy were
sampled by night trawls. For one of the day
samples, two plankton tows were taken in front
and two taken behind the school. The plankton
samples were taken with a 0.5 m ring net with 102
/xm mesh, towed for 2 min at 15 m (the depth of the
school as determined acoustically). These two sets
of plankton samples enabled us to measure direct-
ly the effect of feeding by a school on the egg
density. No plankton tows were associated with
the commercial lampara net samples.

Use of trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

For each fish we determined standard length
( SL) and weight, numbers of eggs and larvae in the
stomach, and compacted stomach volume. The
stomach volume was compacted by centrifuging
the contents for 6 min at 3,700 r/min and then was
measured to the nearest 0.1 ml. Volumes were
expressed as a percentage of the maximum stom-
ach volume. Maximum volume (V) was deter-
mined using the same volumetric technique for
northern anchovy fed to satiation with adult
Artemia salina in the laboratory; it was expressed
as a function of standard length (Din centimeters,
where In V = 2.051 In L - 3.954 and r^ = 0.759.
The length range was 4.6-13.5 cm.

To estimate the ration from observed incidence
of eggs in the stomach, the rate of gastric evacua-
tion of eggs must be known. To estimate this rate,
we fed only northern anchovy eggs to 155 northern
anchovy for 1 h at a density of 38 eggs/1 at 15.2° C,
which approximates typical spawning tempera-
tures. After feeding, fish were transferred to a
tank without food and 10-15 fish sampled at 2-h
intervals until 10 h after feeding. The rate of
gastric evacuation was expressed as the slope of
the regression of natural logarithm of the mean

812

eggs in the stomach as a function of elapsed time

(Figure 1).

Incidence of Cannibalism

No relationship existed between the volume
of the stomach contents and the time of collec-
tion, indicating that anchovy fed throughout the
night and day (Table 1). In the night samples, the
mean stomach volume was 23'7c of that of a
full stomach and was 12'7c in the 3 day samples.
Nearly all stomachs contained greenish to brown-
ish material, presumably phytoplankton remains,
and somewhat less frequently copepods and
euphausiids were mixed with this material.

Larval fishes occurred in only 7 of the 368
stomachs (2%) and only 1 stomach contained
larvae that could be identified as northern ancho-
vy. This stomach contained 21 relatively large
northern anchovy larvae; the only measurable
specimen was 17 mm SL. Northern anchovy eggs
occurred more frequently than larvae. Forty-two

1000

100

X

o
<t

o
t-
cn
\
c/)

<S>

UJ

u.

o

cr

UJ
DD

<

10 I-

Ol

Ln X = 6.432 -OTGlT
r2 = 0 934

4 6 8

ELAPSED TIME (h)

10

percent of the northern anchovy stomachs sampled
at night contained northern anchovy eggs and
88% of those sampled in the day contained eggs.
Other fish eggs were rare, occurring in 4.2±2.7
(±2 SE) of the stomachs. The mean number of
anchovy eggs per stomach, including zeros, was
4.6±3.3 (±2 SE) for night samples, 5.6±3.5 for
day samples, and the mean for night and day was
5.1 eggs/stomach.

The distribution of the number of eggs con-
sumed per fish was highly skewed; about 909^ of
the eggs occurred in only 38% of the stomach
samples containing eggs (19% of all stomachs).
The maximum number of eggs in a single stomach
was 730, which was about 32% of all the eggs
found in stomachs. The patchiness of northern
anchovy eggs in the sea may be responsible for this
skewed distribution. The distribution was not
greatly different from that of northern anchovy
eggs taken in plankton samples. For example,
Smith found that about 90% of northern anchovy
eggs occurred in only 20% of the positive plankton
net hauls (iV = 453).

The mean number of eggs per fish in a sample
(night trawl samples) increased with egg density
in the sea (Figure 2). Although variability was
high (r^ = 0.47), the 99% confidence interval
about the regression coefficient was 1.107-2.095
and did not include a coefficient value of 1. This
indicates that the relation was exponential and
that the mean number of eggs in the stomach was
not increasing in direct proportion to the mean egg
abundance. Patchiness of eggs combined with
selectivity in filtering could explain the exponen-
tial nature of the relationship. Certainly, oblique
net tows provided only a relative measure of egg
density encountered by filtering northern ancho-
vy. Tows were begun at 70 m (below the maximum
depth of northern anchovy larvae (Hunter and
Sanchez 1977), or in shallow water near the bot-
tom to insure that all eggs in the water column
were sampled. Stomach contents, on the other
hand, would be expected to be more closely related
to the size of patches and density of eggs within
egg patches and not to the integrated egg density
for the water column.

Measurements of the density of eggs behind and
in front of a single northern anchovy school were
probably a more realistic measurement of the

Figure l. — Rate of gastric evacuation of northern anchovy fed
northern anchovy eggs. Points are log,, mean number of eggs
per stomach for 10-15 fish sampled at 2-h intervals after feeding.

^P. E. Smith, Southwest Fisheries Center, National Marine
Fisheries Service, NOAA, PO. Box 271, La Jolla, CA 92038,

pers. commun. December 1979.

813

100

X

o

<

s
o

ci^ 10
to

(S>

O

a:

UJ

m

Z

Z

<

LnY= 1601 LnX-4939

r^ = 0 468
LnY= 2 340LnX-7 306

^ I a-al \ — 1— l_L.

10 100

MEAN EGGS/m3

1000

Figure 2. — Mean density of northern anchovy eggs in the sea
and mean number of eggs in northern anchovy stomachs taken
in the Los Angeles Bight in March 1976 and 1977. Points are
means for 10 or more fish and means of 2-4 plankton tows. Upper
equation and the line is the geometric mean regression (Ricker
1973); lower equation is the predictive equation.

actual density of eggs encountered by a school.
These measurements were derived from horizon-
tal tows made at the acoustically determined
depth of the school (15 m). Estimates from the two
tows taken in front of the school were 150 and 122
eggs/m^, whereas those from the two tows taken
behind the school were 75 and 54 eggs/m^. The
ratio of the means for these two sets (65:136)
indicated that 48% of the eggs in the water may
have been consumed by the school. Thus, a school
encountering a density of about 140 eggs/m^ may

have consumed a large proportion of the eggs. The
density of eggs usually encountered by schools
during the peak spawning months may be in
excess of 140 eggs/m^ because the mean number of
eggs per stomach for fish in this school, 1.9 ±0.6
eggs (Collection 31, Table 1) was less than the
mean for all collections, 5.1. The typical density of
northern anchovy eggs within patches is not
known, but a value as high as 31,000 eggs/m^ has
been recorded (Hunter in press).

The daily ration of eggs consumed by northern
anchovy was estimated from the equation, D = A
X B X C where Z) = ration (number of eggs), fi =
rate of gastric evacuation (0.701), A = mean
stomach contents, and C = duration of feeding
(24 h). This function has been used by Tyler (1970),
discussed and used by Eggers (1977), and criticized
and discussed by Elliott and Persson (1978). We
used for mean stomach contents (C), the mean of
the averages for day and night. Using the above
equation, the daily ration was 85.8 eggs/fish or
5.1eggs/gof fish(Table2).

The simplest method for evaluating potential
effects of egg consumption is to calculate the
proportion of the nightly production of eggs con-
sumed by northern anchovy schools. Northern
anchovy produce 371 eggs/g of female per spawn-
ing and during peak breeding periods, about 16%
of the females spawn each night (Hunter and
Goldberg 1980). Thus each night, 0.16 x 371, or
59.4 eggs are spawned per gram of female in a
school. Assuming a sex ratio of 1:1, half this
amount, or 29.7 eggs, are produced per gram
school weight. The percentage of daily egg produc-
tion consumed by a school per day ( eggs consumed/
eggs spawned) was 17.2% (Table 2). Smith (foot-
note 3) estimated the natural mortality of anchovy

Table 2. — Number of anchovy eggs eaten, per day, proportion of egg production consumed, and the proportion
of natural egg mortality attributable to egg Ccinnibalism in northern anchovy.

Variable

Value

SE of mean

Data source

A

Mean eggs/stomach

5.1

'±1.6

Mean of night and day averages (Table 1)

B

Rate of gastric evacuation

.701

±0.092

See text

C

Duration of feeding (h)

24

D

Ration, eggs/fish per day

85,80

A X B X C

E

Mean fish weigfit (g)

16.8

'±0.9

Mean of night and day averages (Table 1)

F

Ration, eggs/grams wet weight

5.1

D/E

G

Eggs spawned/grams ovary-free female weight

389

±30

Hunter and Goldberg 1980

H

Ratio of ovary-free weight to total female weight

.954

Hunter and Macewicz^

1

Eggs spawned /grams total female weight

371

±28

G X H

J

Ratio of females spawnlng/night

16

±0.02

Hunter and Goldberg 1980

K

Ration of females,'school

.50

Assumed 1 :1 sex ratio

L

Eggs/gram school weight

29-7

1 X J X K

M

Percent of egg production consumed /day

17.2

F/L

N

Natural egg mortality percentage/day

53

Smith and Lasker 1978

O

Percentage natural mortality from cannibalism

324

M,N

From the night samples. Table 1.
^Hunter, J. R., and B. J. Macewicz. 1979. Sexual maturity, batch fecundity spawning frequency and temporal pattern of spawning
northern anchovy, Engraulis mordax, during the 1979 spawning season. Manuscript submitted for publication.

814

eggs to be about SS'/c/d. Thus, egg cannibalism
may be the cause of 32% of the natural egg mor-
tality in northern anchovy.

Discussion

We have not tried to trace the error terms
through the pyramid of calculations required to
estimate the proportion of natural egg mortality
attributable to cannibalism, although we give in
Table 2 the standard error of the mean where
estimates are available. The error in our estimate
most likely will be equivalent or higher than that
of the most variable parameter (i.e., mean eggs
per stomach and natural mortality of northern
anchovy eggsi. We have no estimate of the error
for the natural mortality of northern anchovy eggs
but mortality rates of pelagic fish eggs are known
to be high and variable; estimates range from 2 to
957c for various species (Jones and Hall 1974;
Vladimirov 1975). Regardless of the uncertainties,
we believe the results indicate that egg canni-
balism may be a major source of egg mortality in
the northern anchovy and a combination of patchi-
ness of eggs and selectivity in filter feeding may be
important in regulating the consumption of eggs.

Cannibalism is a mechanism for density-de-
pendent regulation of fish populations (Gushing
1977), and egg cannibalism may be one of the
many mechanisms regulating the size of anchovy
populations. A simple model could be developed to
test this hypothesis if random filtering and a
random egg distribution were assumed. Although
the development of such a model is beyond the
scope of this paper, we wish to consider the extent
our observations differ from predictions based on
assumptions of randomness because this would be
a critical decision in the development of the model.

The mean density of eggs in trawl associated
plankton tows was 32 eggs/m^ and the maximum
filtering rate of northern anchovy of mean weight
16.8 g, is 0.158 m^/h (Leong and O'Connell 1969).
For a northern anchovy (weight 16.8 g) to obtain
the estimated ration of 85.8 eggs/d, it would have
to filter continuously for 17 h at a density of 32
eggs/m^. Another approach is to estimate the
percentage of the volume of the habitat that could
be randomly filtered by a group of northern
anchovy schools. The mean weight of northern
anchovy schools in 20' grid squares is 2.05 x 10'
kg (excluding grid squares without northern an-
chovy) (Mais^); assuming the maximum depth of
eggs is 30 m (Hunter and Sanchez 1977), the

volume of the habitat is 2.86 x 10^" m^ These
schools would have to filter for 24 h to consume
17% of the nightly egg production. The number of
hours of filtering required to obtain the average
daily ration of eggs in the first calculation or to
consume 17% of the egg production in the second is
too high. Thus a random encounter model does not
seem to account for the relatively high egg con-
sumption that was observed and patchiness and
selectivity in feeding may be the reasons.

Northern anchovy eggs exist in patches (Hewitt
in press), probably in patterns similar to those
described for sardine eggs (Smith 1973). Our
observations of northern anchovy feeding on eggs
in the laboratory indicate that filtering may be
intensified when egg patches are encountered.
When we added a beaker containing anchovy eggs
to a 3.3 m diameter tank containing about 200
northern anchovy, they soon interrupted their
circuit of the tank, formed a tight mill at the site of
introduction, and filtered the region intensively.
If northern anchovy display such patterns of
behavior in the sea, the ration of eggs would be
expected to be higher than one predicted from
random filtering. Thus, present evidence indi-
cates that an assumption of randomness would be
unacceptable in a model to measure effects of
cannibalism as a regulatory mechanism.

Larval cannibalism might also be significant.
Northern anchovy larvae are readily eaten by
adults in the laboratory. The absence of small
northern anchovy larvae in stomachs may have
been caused by the rapid rate of digestion (<30
min) and the low incidence of larger larvae (0.3% )
caused by their low abundance in the sea. Thus,
cannibalism on larvae as well as that on eggs
might play a role in the regulation of northern
anchovy populations but additional information is
needed on feeding behavior, and on the size and
density of egg and larval patches, before an
evaluation of population effects can be made.

Acknowledgments

Sharon Hendrix and Harold Dorr (Southwest
Fisheries Center, National Marine Fisheries Ser-
vice, NOAA, La Jolla, Calif.) assisted in collection
and processing of adult northern anchovy samples.
Daylight trawl collections and associated plank-
ton tows were made by Anthony Koslow (Scripps

''Mais, K. F. California Department of Fish and Game,
Cruise Reports 76-A-3 and 77-A-3. California Department of
Fish and Game, Marine Resources Region, Long Beach, Calif.

815

Institution of Oceanography, University of Cali-
fornia at San Diego, La Jolla). Alec MacCall
(California Department of Fish and Game, La
Jolla) gave helpful suggestions regarding the
interpretation of the results.

Literature Cited

CUSHING, D. H.

1977. The problems of stock and recruitment. In J. A.

Gulland (editor). Fish population dynamics, p. 116-133.

Wiley, N.Y.
CIECHOMSKI, J. D. DE

1967. Investigations of food and feeding habits of larvae

and juveniles of the Argentine anchovy Engraulis

anchoita. Calif. Coop. Oceanic Fish. Invest. Rep. 11:

72-81.
EGGERS, D. M.

1977. Factors in interpreting data obtained by diel sam-
pling of fish stomachs. J. Fish. Res. Board Can. 34:
290-294.

Elliott, J. M., and L. Persson.

1978. The estimation of daily rates of food consumption
for fish. J. Anim. Ecol. 47:977-991.

HAYASI, S.

1967. A note on the biology and fishery of the Japanese
anchovy, Engraulis japonica (Houttuyn). Calif. Coop.
Oceanic Fish. Invest. Rep. 11:44-57.

Hewitt, R.

In press. The value of pattern in the distribution of young
fish. In R. Lasker and K. Sherman (editors). The early
life history of fish. II, A Second International Symposium
held in Woods Hole, 2-5 April 1979. Rapp. R-V. Reun.
Cons. Int. Explor Mer 178.
HUNTER, J. R.

In press. The feeding behavior and ecology of marine fish
larvae. In J. E. Bardach (editor). The physiological
and behavioral manipulation of food fish as production
and management tools. International Center for Living
Aquatic Resources Management, Manila.
HUNTER, J. R., AND S. R. GOLDBERG.

1980. Spawning incidence and batch fecundity in north-
em anchovy, Engraulis mordax. Fish. Bull., U.S. 77:
641-652.
HUNTER, J. R., AND C. SANCHEZ.

1977. Diel changes in swim bladder inflation of the larvae
of the northern anchovy, Engraulis mordax. Fish. Bull.,
U.S. 74:847-855.

Jones, R.. and W B. Hall.

1974. Some observations on the population dynamics of
the larval stage in the common gadoids. In J. H. S.
Blaxter (editor). The early life history of fish, p. 87-102.
Springer- Verlag, N.Y.
LEN.-\RZ, W. H.

1972. Mesh retention of larvae of Sardinops caerulea
and Engraulis mordax by plankton nets. Fish. Bull.,
U.S. 70:839-848.
LEONG, R. J. H., AND C. R O'CONNELL.

1969. A laboratory study of particulate and filter feeding
of the northern anchovy {Engraulis mordax). J. Fish.
Res. Board Can. 26:557-582.

LOUKASHKIN, A. S.

1970. On the diet and feeding behavior of the northern

anchovy Engraulis mordax (Girard). Proc. Calif Acad.
Sci., Ser 4, 37:419-458.
O'CONNELL, C. R

1972. The interrelation of biting and filtering in the
feeding activity of the northern anchovy i Engraulis
mordax). J. Fish. Res. Board Can. 29:285-293.

RICHER, W E.

1973. Linear regressions in fishery research. J. Fish.
Res. Board Can. 30:409-434.

SMITH, R E.

1973. The mortality and dispersal of sardine eggs and
larvae. Rapp. P.-V. Reun, Cons. Int. Explor Mer 164:
282-292.
SMITH, P E., AND R. LASKER.

1978. Position of larval fish in an ecosystem. Rapp.
P-V. Reun. Cons. Int. Explor Mer 173:77-84.
SMITH, P E., AND S. L. RICHARDSON.

1977. Standard techniques for pelagic fish egg and larva
surveys. FAO Fish. Tech. Pap. 175, 100 p.
TYLER, A. V.

1970. Rates of gastric emptying in young cod, J. Fish.
Res. Board Can. 27:1177-1189.
VLADIMIROV, V. I.

1975. Critical periods in the development of fishes. J.
Ichthyol. 15:851-868. (Engl, transl. of Vopr Ikhtiol.)

john r. hunter
Carol a. kimbrell

Southwest Fisheries Center La Jolla Laboratory
National Marine Fisheries Service, NOAA
P.O. Box 721
La Jolla, CA 92038

DEPTH DISTRIBUTION AND SEASONAL AND
DIEL MOVEMENTS OF RATFISH,

HYDROLAGUS COLLIEI, IN
PUGET SOUND, WASHINGTON'

The ratfish, Hydrolagus colliei, inhabits the
coastal waters of North America from Alaska to
the Gulf of California (Hart 1973). One aspect of
the biology of this species which has attracted
attention is its vision physiology It is generally
accepted that most deepwater fish, regardless of
phylogenetic position, have retinal pigments with
maximum absorption at about 490 nm or less
(Munz 1971; Lythgoe 1972). For example, H.
affinis, the species of chimaeroid found in deep
water of the western Atlantic, has retinal pig-
ments with maximum absorbance at 477 nm ( Den-
ton and Nicol 1964). In contrast, a shallow-water
species of chimaeroid ( Callorhinchus callorhyn-
chus) found off Chile has retinal pigments with

'Contribution No. 514 College of Fisheries, University of
Washington, Seattle, Wash.

816

FISHERY BULLETIN; VOL. 78, NO. 3, 1980.

maximum absorbance at 499 nm, a value which is
typical of coastal fishes (McFarland 1970). Cres-
citelli (1969) and Beatty ( 1969), however, have re-
ported that H. colliei, which can occur in water
only 5 m deep, possesses retinal pigments charac-
teristic of deepwater fish iKmns = 484 nm). Cres-
citelli ( 1969) remarked that it is anomalous to find
such pigments in a coastal species.

Like the retinal pigments, the structures for
regulating the amount of light striking the retina
in this species seem to be adapted to deep water.
Maddock and Nicol ( 1978) found that the pupils of
H. colliei cannot be contracted in bright light, and
the reflective tapetum lucidum has no movable
layer of dark pigments to eliminate eyeshine in
bright light. While Stell has found that there is
an increase in pigmentation on the tapetum after
full light adaptation, he estimated the degree of
occulsion at 209c or less. Stell also indicated that
ratfish appear to have an all-rod retina, a further
adaptation to low light levels. In attempting to
relate the spectral sensitivity of chimaeroid ret-
inal pigments to depth of occurrence, Crescitelli
(1969) and McFarland ( 1970) both noted that the
absence of behavioral or ecological data on H. col-
liei makes it difficult to classify this species as an
inhabitant of deep, shallow, or intermediate
depths.

In the Gulf of California, H. colliei is typically
captured below 275 m, although abundance varied
seasonally (Matthews 1975). In other parts of its
geographic range this species clearly inhabits
shallower water. Jopson (1958) observed ratfish
trapped in tide pools on the Oregon coast, and
Dean ( 1906) reported catching them in about 4 m
of water in Port Townsend Bay, Wash.

Recent studies have suggested that ratfish may
undergo diel onshore migrations in Puget Sound.
Miller et al.^ reported trammel net catches of
ratfish at night in areas where none were observed
by scuba divers during the day. Moulton (1977)
observed ratfish only in the evening and at night
during dives on rocky reef sites. However, other
divers (unpubl. obs.) have reported occasional
sightings of ratfish in shallow water during the
day

^William K. Stell, Professor of Ophthalmology and Anatomy,
Jules Stein Eye Institute, University of California, Los Angeles,
Los Angeles, CA 90024, pers. commun. January 1978.

^Miller, B. S., C. A. Simenstad, and L. L. Moulton.
1976. Puget Sound baseline program: Nearshore fish sur-
vey. Unpubl. manuscr., 196 p. Univ. Wash., Fish. Res. Inst.
FRI-UW-7604.

To further understand the relationship between
visual systems and fish depth distribution, the
present study was designed to focus on three
questions. First, what is the overall bathymetric
distribution of ratfish in Puget Sound? Second, to
what extent do Puget Sound ratfish undergo sea-
sonal and diel onshore migrations? Third, is there
evidence for size- or sex-related patterns of abun-
dance or movements?

Methods

Seven sites in central Puget Sound were sam-
pled between 1965 and 1978: Port Madison, Port
Gardner, Mukilteo, Duwamish Head, Point Pully,
Alki Point, and West Point (Figure 1). Samples
were obtained with a 6 m otter trawl and a 6 m
beam trawl which we have previously found to fish
with approximately the same results. All tows
were on the bottom for 5 min.

■^~^

— n — TFT^

Severe TT

7il T ^

\S f TACOMA

FIGURE 1.— Map of Puget Sound, Wash., with sites where
ratfish were sampled. 1, Eagle Cove; 2, Port Townsend Bay; 3,
Port Gardner, 4, Mukilteo: 5, Port Madison; 6, West Point; 7,
Duwamish Head; 8, Alki Point: 9, Point Pully

817

All sites were sampled during daylight hours
about once a month. The depths sampled varied
among the areas, but all sites were sampled at
discrete depths between 10 and 70 m, several were
sampled between 10 and 120 m, and one site be-
tween 5 and 150 m. When considering seasonal
changes, winter was defined as January-March,
spring as April-June, summer as July-September,
and fall as October-December. Sampling effort was
essentially the same at a given site and depth over
all seasons.

Diel (24-h) studies were conducted at West Point
in central Puget Sound (Figure 1) on 4 Nov. 1975,
13 Feb. 1976, 15 May 1976, 20 Aug. 1976, 19 Nov.
1976, and 5 May 1978. These six studies involved
sampling at depths of 5, 15, 25, 35, 45, and 55 m
every 4 h. The data were grouped into six time
periods (Pacific standard time): 0400-0800, 0800-
1200, 1200-1600, 1600-2000, 2000-2400, and
2400-0400 h.

In addition to the major sampling effort at the
seven sites, a 24-h study was conducted at Eagle
Cove (San Juan Island) in northern Puget Sound,
and some daytime sampling was conducted in Port
Townsend Bay (Figure 1).

All ratfish were counted, and length (measured
to the end of the second dorsal fin ), weight, and sex
recorded.

Results
When all months were combined, data from the

seven principal sampling sites indicated that
ratfish were most abundant in the 55-95 m depth
range. Hauls from depths <50 m and >100 m
generally had a lower catch per unit effort of
ratfish than those made at intermediate depths
(Figure 2).

Port Townsend Bay was an exception to this
pattern. Ratfish from this shallow-depth area (<
30 m) were sampled during June, August, and
September 1978. In a total of 60 hauls at depths
from 3 to 27 m, 182 ratfish were caught. This
relatively high abundance of ratfish (3.03 fish/
haul ) in shallow water was in direct contrast to the
scarcity of ratfish in <30 m at the other sites (1.31
fish/haul). (Actually, this latter average may be
inflated by a few abundant hauls at Port Madison
in the spring. If the Port Madison hauls are omit-
ted, the average drops to 0.70 fish/haul). Not only
was there an unusually large number of ratfish in
shallow Port Townsend Bay, but the fish seemed to
be selecting shallower water within the bay, be-
cause peak catches occurred in water only 10 m
deep.

With the exception of the Port Townsend Bay
samples, the basic depth distribution pattern was
similar at the seven major sites. However, the pat-
tern was subject to seasonal and diel variations.
Catch per unit effort of ratfish was generally high-
est in spring, declined during summer and fall,
and increased again in winter (Figure 3). This
pattern was matched by a minimum average
depth of capture in spring (70.5 m) and a maximum

3
<

X

X

<

cc

3

o

1 : MUKILTEO
2- PORT GARDNER
3= PORT MAD ISON
4^ DUWAMISH HEAD
5= POINT PULLY
6= WEST POINT
7= ALKI POINT
8= PORT TOWNSEND
BAY

Figure 2. — Daytime depth distribution
of ratfish at eight sites in Puget Sound,
Wash., throughout the year.

60 90

DEPTH (M)

818

19
18

17

_i

<16

X

x15

CO

-14
<

LU

o

11

10

SP

W

Figure 3. — Seasoned relationship between ratfish abundance
(CPUE, catch per unit effort) in Paget Sound, Wash, (data aver-
aged for the seven principal sites).

average depth of capture in the fall (76.5 m). These
two trends indicate that ratfish move shallower in
the spring and deeper in the fall, perhaps beyond
the sampling range of this study.

The 24-h studies gave evidence of a nocturnal,
onshore movement. Within the sampling depths of
5-55 m, the number of fish per haul ranged from
0.69 in the 1200-1600 sample series to 5.42 in the
2400-0400 series ( Figure 4). Although the samples
were taken at different times of year, sunrise was
always between 0415 and 0715 h, and sunset was
between 1615 and 1930 h on the dates when the
sampling was done. The data from the 24-h study
at Eagle Cove also showed a peak in nearshore
abundance after sunset and before sunrise, consis-
tent with the West Point data.

The 24-h studies also provided evidence that
large and small ratfish were not behaving alike.
Although large fish were caught at night, there
was a decrease in average length (Figure 4) indi-
cating that the nocturnal onshore migration was
composed principally of small fish.

Analysis of the combined monthly data from
West Point, Alki Point, and Point Pully indicated
that fish caught in shallow water were larger than
those caught in deeper water (Figure 5). This
trend was also apparent for the West Point 24-h
and Port Townsend Bay data as well. The samples
at Port Townsend Bay were from water <30 m

=3
<

x4

I

C/3

<

LLI

u

300
280
260 I

X

I-
240 ^

220

IX

200

TIME OF DAY

Figure 4. — Die! changes in abundance (CPUE, catch per unit
effort) and average size of ratfish caught in shallow water (5-55
m) at West Point, Puget Sound, Wash.; data averaged from six
24-h studies.

O

400

370

340

310

280

IX 250

220

1 - POINT PULLY
2- ALKI POINT
3: WEST PO I NT

20

40 60

DEPTH(M)

80

100

Figure 5. — Relationship between depth of capture and ratfish
length in samples from three sites in Puget Sound, Wash.

deep, and the average length was 360 mm (±74
mm SD), and no ratfish were <200 mm long.

Sex ratios of ratfish at West Point, Alki Point,
and Point Pully were significantly (chi-square)

819

different from 1:1 ratio only in the spring, when
60*^^ of the ratfish caught were females.

Discussion

In Puget Sound, the ratfish was most abundant
from 55 to 99 m. While it should be noted that only
three sites were sampled below 100 m, and none
below 150 m, most of Puget Sound proper is shal-
lower than 150 m. Still, the depth distribution of
ratfish in central Puget Sound differs from that in
the Gulf of California (Matthews 1975).

These southern ratfish were most abundant
from 257 to 400 m. After noting a peak of abun-
dance in February, Matthews ( 1975) speculated
that the ratfish move into very deep water during
the summer and fall, and return to shallower
water in the winter and spring. This would be
generally similar to the seasonal pattern of abun-
dance observed at the Puget Sound sampling sites,
where maximum abundance was in the spring
(April- June); later in the year, the fish were in
slightly deeper water.

While the differences in overall depth distribu-
tion of the Puget Sound and Gulf of California
populations may be temperature related, and the
seasonal movements may be related to reproduc-
tion, these factors do not seem to explain the diel
movements of the Puget Sound population. One
possible explanation for the nocturnal onshore
movements of Puget Sound ratfish is that there is
some food resource which is being exploited in
shallow water. A study of ratfish food habits off the
Oregon coast (Johnson and Horton 1972) found
that 75% of the food items consumed were Am-
phissa sp., a gastropod mollusc. A study of ratfish
food habits from Puget Sound indicates a much
less specialized diet. Stomachs from 71 West Point
ratfish contained a wide variety of items ( Wingert
et al.'*). In general, smaller ratfish (<200 mm) fed
principally on polychaetes, but stomachs of larger
ratfish contained primarily bivalves, fish, and
decapods. While some food items such as limpets
and barnacles indicated shallow-water feeding,
the sample size was not sufficient to establish the
main feeding times or depths. Miller et al.^ and

^Wingert, R.C., C.B.Terry, and B.S.Miller. 1979. Food and
feeding habits of ecologically important nearshore and demersal
fishes in central Puget Sound. Unpubl. manuscr, 83 p. Univ.
Wash., Fish. Res. Inst. FRI-UW-7903.

^Miller, B. S., C. A. Simenstad, L. L. Moulton, K. L Fresh, F C.
Funk, W. A. Karp, and S. F Borton. 1977. Puget Sound
baseline program; Nearshore fish survey. Unpubl. manuscr.,
220 p. Univ Wash., Fish Res. Inst. FRI-UW-7710.

Fresh et al. also found wide prey spectra, with fish
and polychaetes being the most important items.
Ratfish seems to feed opportunistically on the
most abundant, available items and will eat a wide
range of crustaceans, molluscs, annelids, fish,
echinoderms, and algae.

Whether or not the onshore movements are
food-oriented, we still must explain why most of
the small ratfish are found in deep water, and why
they apparently approach shore primarily at
night. One possible explanation is predator avoid-
ance. The large, poisonous dorsal spine and large
size probably make adults relatively safe from
predation, but perhaps not juveniles. During the
day, juveniles may tend to stay in deep water
where their blue-shifted retinal pigment may give
them an advantage over potential predators such
as spiny dogfish, Squalus acanthias (Jones and
Geen 1977).

The Puget Sound ratfish population is exploit-
ing a nearshore niche. Its retinal pigment
(chrysopsin) and eye morphology are similar to
deep-sea chimaeroids, such as H. affinis, yet its
depth distribution is comparable to many fish with
retinal pigments located near 500 mm. By con-
trast, C. callorhynchus seems to be a more well-
established coastal chimaeroid, having a typical
coastal rhodopsin with peak absorbance at 499
mm (McFarland 1970). Hov^^ever, H. colliei has
some adaptations to an environment with moder-
ate light levels. Arnott and Nicol ( 1970) described
the histological basis of the reflective skin of the
species and explained this sheen as a camouflage
device by which the reflected light would match
the background illumination. The authors point
out that this reflective sheen is typical of
chimaeroids from moderate depths, such as
Chimaera monstrosa, C. cubana, C. phantasma,
and Callorhinchus callorhynchus, but that deep-
sea members of the group, such as H. affinis, have
dull-colored skin. Thus, C callorhynchus seems to
be well adapted to its nearshore habitat, H. affinis
is adapted to its deep-sea habitat, and H. colliei is
partly adapted to deep water and partly to shallow
water.

While the visual system of//, colliei is clearly
suited to the deep distribution exemplified by the
Gulf of California population, it also seems com-

^Fresh, K. L., D. Rabin, C. A. Simenstad, E. O. Salo, K. Garri-
son, and L. Matheson. 1978. Fish ecology studies in the Nis-
qually Reach area of southern Puget Sound, Washing-
ton. Unpubl. manuscr., 151 p. Univ. Wash., Fish. Res. Inst.
FRI-UW-7812.

820

patible with the distribution and behavior of
Puget Sound ratfish.

While no quantitative measurements were
made of light intensity or wavelength, to the
human eye, the water in Puget Sound is quite dark
at 25 m during the day, especially in winter. Con-
sidering that the fish is most abundant at about
75 m during the day and generally moves near
shore only at night, McFarland's (1970) as-
sessment that its retinal pigment might be appro-
priate for its depth distribution seems to be cor-
rect. Other aspects of its visual system, such as the
apparently all-rod retina and nearly nonocclusible
tapetum seem generally appropriate to its ob-
served depth distribution. However, only more ex-
tensive studies of the feeding ecology, predators,
and possible competitors of ratfish can explain
why it moves onshore, why in some areas, such as
Port Townsend Bay, it is found in shallow water
during the day, and why in general it is found
closer to shore in Puget Sound than in other areas
in its range.

In summary, the data indicate that in Puget
Sound, large ratfish predominate in shallow
water, and smaller ones in deeper water. The
species is most abundant in about 75 m of water,
and tends to be in slightly shallower water in the
spring and deeper water in the fall. Ratfish has a
pronounced nocturnal onshore movement, which
is composed primarily of smaller ratfish from
deeper water.

Literature Cited

ARNOTT, H. J., AND J. A. C. NICOL.

1970. Reflection of ratfish skin (Hydrolagus colliei). Can.
J. Zool. 48:137-151.

Beatty, d. d.

1969. Visual pigments of three species of cartilaginous

fishes. Nature (Lend.) 222:285.
CRESCITELLI, F.

1969. The visual pigment of a chimaeroid fish. Vision

Res. 9:1407-1414.

Dean, B.

1906. Chimaeroid fishes and their development. Car-
negie Inst. Wash. Publ. 32, 194 p.

Denton E. J., and J. A. C. Nicol.

1964. The chorioidal tapeta of some cartilaginous fishes
(Chondrichthyes). J. Mar Biol. Assoc. U.K. 44:219-258.

Hart, J. L.

1973. Pacific fishes of Canada. Fish. Res. Board Can.,
Bull. 180, 740 p.

Johnson, a. G., and H. F Horton.

1972. Length-weight relationship, food habits, parasites
and sex and age determination of the ratfish, Hydrolagus
colliei (Lav and Bennett). Fish. Bull., U.S. 70:421-429.

JONES, B. C, AND G. H. GEEN.

1977. Food and feeding of spiny dogfish (Squalus acan-
thias) in British Columbia waters. J. Fish. Res. Board
Can. 34:2067-2078.

JOPSON,H.G. M.

1958. A concentration of the ratfish, Hydrolagus colliei.
Cape Arago, Oregon. Copeia 1958:232.

Lythgoe.J. N.

1972. List of vertebrate visual pigments. In H. J. A.
Dartnall (editor), Photochemistry of vision . Handbook of
sensory physiology, Vol. 7, Part 1, p. 604-624. Springer-
Verlag, Berl.
Maddock, R. G., and J. A. C. NiCOL.

1978. Studies on the eyes of Hydrolagus (Pisces:
Chimaeridae). Contrib. Mar Sci. 21:77-87.

Matthews, C. P

] 975. Note on the ecology of the ratfish, Hydrolagus colliei,
in the Gulf of California. Calif. Fish Game 61:47-53.
MCF.ARLAND, W. N.

1970. Visual pigment of Callorhinchus callorhynchus, a
southern hemisphere chimaeroid fish. Vision Res.
10:939-942.

MOULTON, L. L.

1977. An ecological analysis of fishes inhabiting the rocky
nearshore regions of northern Puget Sound, Washing-
ton. Ph.D. Thesis, Univ. Washington, Seattle, 181 p.

MUNZ, F W.

1971. Vision: Visual pigments. In W. S. Hoar and D. J.
Randall (editors). Fish physiology, Vol. 5, p. 1-32. Acad.
Press, N.Y.

Thomas P Quinn
bruce s. miller

College of Fisheries
University of Washington
Seattle, WA 98195

R. CRAIG WINGERT

College of Fisheries, University of Washington
Seattle, Wash.

Present address: Marine Biological Consultants, Inc.
Costa Mesa, CA 92627

DETECTION OF PETROLEUM HYDROCARBONS

BY THE DUNGENESS CRAB,

CANCER MAG I ST ER

Behavioral responses that mitigate the effects of
natural environmental perturbations may also be
effective for contaminants from human activities,
but the occurrence of any behavioral response,
e.g., avoidance, first requires detection of the
contaminant (011a et al. 1980). To predict whether
a behavioral response to a chemical pollutant will
occur, one must ask whether the organism can
detect the pollutant at concentrations likely to
be encountered in field situations. Here we re-

FISHERY BULLETIN: VOL. 78. NO. 3. 1980.

821

port how antennular behavior was used to deter-
mine the concentrations at which the Dungeness
crab, Cancer magister (Dana), detected petroleum
hydrocarbons.

For decapod crustaceans the antennules have
been considered the site of distance chemorecep-
tion (Hazlett 1971), and their flicking may be
analogous to sniffing in vertebrates (Fuzessery
1978). Previous work has shown that in the blue
crab, Callinectes sapidus, the antennular behavior
indicating detection of food substances (Pearson
and 011a 1977) also indicated detection of the
petroleum hydrocarbon naphthalene ( Pearson and
011a 1979, 1980) and the water soluble fraction
of crude oil (Pearson et al. in press). In the
Dungeness crab, similar antennular behavior,
i.e., a change in orientation and increased flicking
rate, also indicated detection of food substances
(Pearson et al. 1979). Here we used these changes
in antennular behavior to determine chemosen-
sory detection thresholds in the Dungeness crab
for naphthalene and the water soluble fraction
(WSF) of Prudhoe Bay crude oil.

Materials and Methods

Dungeness crabs, trapped in the Strait of Juan
de Fuca, Wash., were held outdoors in 1,200 1
tanks under the conditions described by Pearson
et al. (1979). The seawater temperatures (± SD)
during the naphthalene and WSF experiments
were 12.7°±0.6° C and 10.6°±0.3° C; the salin-
ities, 31.6 ±0.91, and 32.0±0.0'L; the dissolved
oxygen, 6.9 + 0.7 mg/1 and 7.3 ±0.5 mg/1; and the
pH, 8.12 ± 0.17 and 8.02 ± 0.16.

Experimental Solutions

Saturated solutions of naphthalene were pre-
pared by adding naphthalene crystals to seawater
filtered through a 0.4 /xm Nucleopore^ membrane.
These stock solutions were stirred continuously at
room temperature on a magnetic stirrer and were
used after at least 18 h of stirring and no more than
5 d from first use. On each day of testing, a portion
of the stock solution was siphoned off and passed
through a 100 ml glass syringe fitted with a
Millipore prefilter (Type A025) to remove any
naphthalene crystals. Less than 1 h before testing,

The use of trademarks does not imply endorsement by
National Marine Fisheries Service, NOAA or Battelle, Pacific
Northwest Laboratories.

serial dilutions of this filtered stock naphthalene
solution were made with seawater freshly filtered
through a 0.4 ^tm membrane. An aliquot of the
filtered seawater used for dilution served as the
control solution. Experimental and control solu-
tions were kept in a water bath at ambient
seawater temperature during testing.

On each day of testing, samples of the stock
solution and 10 ~^ dilution were analyzed for
naphthalene content. Ten milliliters of hexane
were vigorously shaken with 50 ml of sample
solution for 1 min. This hexane was removed and
analyzed for naphthalene content by capillary GC
methods (Bean et al. 1978). The stock naphthalene
solution was 22.9±2.1 mg/1, and the 10~^ dilution
was 2. 2± 0.2 mg/1.

The WSF of Prudhoe Bay crude oil was prepared
freshly each day by methods similar to Anderson
et al. (1974). In a 19 1 glass bottle, one part oil was
gently poured over nine parts membrane-filtered
seawater. Before the oil was added, a glass siphon
tube inserted through a stopper covered with
aluminum foil was placed in the filtered seawater.
With the bottle stoppered, the seawater was slowly
stirred on a magnetic stirrer for 20 h at room
temperature. The stirring speed was adjusted so
that the vortex did not extend more than 25% of
the distance to the bottom of the bottle. After
mixing, the oil and water phases were allowed to
separate for 1 h. The water phase was then
siphoned from below the oil phase and filtered
through a prefilter under very low pressure to
remove any remaining oil droplets. Serial dilu-
tions of the resulting WSF were then immediately
made with freshly membrane-filtered seawater
and kept in a water bath at ambient seawater
temperature during use. The membrane-filtered
seawater used for dilution was the control solu-
tion. The stock WSF was analyzed by capillary gas
chromatography for diaromatic and triaromatic
hydrocarbons (Bean et al. 1978), and by gas
partitioning analysis modified from McAuliffe
(1971) for monoaromatics.

Chemosensory Threshold Determination

The apparatus and procedures of Pearson et al.
(1979) were used here. In brief, glass testing
chambers were arranged on four trays, 10 cham-
bers to a tray, and the trays were surrounded by
blinds. The experimental solutions were intro-
duced into each testing chamber through an inlet
manifold connected to a glass funnel. Seawater

822

from dripper arms entered each funnel at a rate of
1.0 1/min. A Teflon delivery tube carried the
experimental solutions to the funnel from a buret
calibrated to deliver 20 ml in 15 s.

To obtain a dilution factor for estimating the
effective concentration of experimental solutions
within a testing chamber, seawater solutions of
^"*C-naphthalene (sp. act. 3.6 mCi/mmole, Amer-
sham-Searle Corporation) were introduced and
samples taken at timed intervals from the mid-
point of the chamber and counted for radioactivity
by liquid scintillation spectrometry. The chamber
contained a crab model displacing 701 ml, a
volume typical of the crabs tested. The maxi-
mum concentration in the chamber occurred 45 s
after ^^C-naphthalene was added and was 0.0188
(± 0.0058 SDi times the concentration of the
introduced solution. This dilution factor did not
differ significantly from that found by Pearson
et al. (1979) using a visible dye.

Approximately 24 h before testing, crabs were
transferred to the testing chambers from the
holding tanks where they had been fed an ad
libitum diet of the blue mussel, Mytilus edulis.
Because, in preliminary experiments, tidal phase
was found to influence chemosensory responses
(Pearson et al. 1979), testing was synchronized to
begin and end within either a rising or falling tide.
The seawater for the test dilutions and control was
drawn and filtered 1 h after a tidal change. Testing
then began as soon as possible and stopped before
the next tidal change.

Each day a maximum of 40 crabs were presented
individually with 20 ml of either one of nine
dilutions of naphthalene stock solution, one of
eight dilutions of WSF, or a control of filtered
seawater. Molting and mating crabs were not
tested. The order in which individual crabs were
watched and the choice of experimental solution
were randomized except that active crabs and ones
with retracted antennules were passed over. The
observer did not know the identity of any test
solution. Individual crabs were observed for 1.0
min prior to introduction of the experimental
solution, and their antennular flicking rate and
other behavior recorded. The flicking rate of
one antennule was measured using a hand-held
counter. The solution was then introduced, and
the observations continued for 1.0 min after the
beginning of solution addition. The behavior
was scored with the criteria used by Pearson
etal.(1979).

To be scored as detecting an experimental
solution, a crab had to exhibit an abrupt change
in the orientation of the antennules within 30 s
after solution introduction, and the ratio of the
antennular flicking rate for 1.0 min after solution
introduction to that for 1.0 min before had to
be 1.50 or above. This value was determined
previously by Pearson et al. (1979) from observa-
tions of crabs in the testing apparatus without
any solutions present. Because 1.50 was the
95th percentile of these antennular flicking rate
ratios, the a priori probability that a flicking rate
ratio >1.50 represented a spontaneous increase
rather than a reaction to the experimental solu-
tion was <5%.

Results

Composition of the WSF

The monoaromatic hydrocarbons by far dom-
inated the WSF (Table 1) and composed 99.19^ of
the total hydrocarbons measured. The remaining
aromatic hydrocarbons, mostly the naphthalenes,
were present at concentrations 100 times less than
that of the monoaromatics. The hydrocarbons
partitioned into the WSF from the crude oil in
proportion to their solubility in seawater (Clark
and MacLeod 1977; Bean et al. 1978).

Table l. — Composition of the water soluble fraction of Prudhoe
Bay crude oil. Sample size was 3 for the di- and triaromatics and
6 for the monoaromatics.

Fraction

mg liter

Total alkanes

Naphthalene

Total methylnaphthalenes

Total dimethylnaphthalenes

Phenanthrene

Methylphenanthrene

Dimethylphenanthrene

Total polynuclear aromatics

Benzene

Toluene

Ethylbenzene

m- plusp-Xylene

o-Xylene

Total tnmethyl benzenes

Total monoaromatics

Total hydrocarbons measured

< 0.001
.0851 i
.0766 =
.0269 =
.0006-
<.0001
<.0001
.1892 =

10002:0

6.74-0

.30 = 0

1.12 = 0

1.12 = 0

.46 = 0

19.75 = 0

19 94

0.0088
00080
00015
0.0004

:0.0175

29

42

02

06

08

12

86

Detection Thresholds

Whereas Dungeness crabs detected both naph-
thalene and the WSF of Prudhoe Bay crude oil, the
crabs detected the complex WSF mixture more
readily and consistently Because the percentage
of crabs detecting naphthalene varied widely over

823

the range of concentrations presented, the regres-
sion equation relating percentage detection and
the logarithm of concentration was not significant
(F = 1.3, P = 0.30) (Figure 1). The curve for
naphthalene detection was sawtooth-shaped with
only four concentrations where the percentages
of crabs detecting were above the upper 907c
confidence limit about the control value. The
sawtooth curve produced three concentrations at
which 509^ of the crabs could have detected
naphthalene, 10~^ 10~', and 10"** mg/1. Because
the factors producing the sawtooth curve are
unknown, the most conservative approach is to
consider the uppermost concentration, 10 ~^ rng/l,
as the threshold for naphthalene detection. In
contrast to naphthalene, the percentage of crabs
detecting the WSF decreased in a consistent way
with the WSF concentration (Figure 1). The re-
gression equation was significant (F = 60.4,
P<<0.01), and the variability was low iR^ =
91.0%). The SO'/f detection threshold from the
regression equation was 4 x 10""* mg/1, about 100
times lower than that for naphthalene.

When a crab detected naphthalene or WSF, the
response was usually distinct. For crabs meeting
the detection criteria, the median ratios of the
antennular flicking rates did not vary with con-
centration (Median Tests, x^ = 2.38, P = 0.12 for
naphthalene; x^ = 9.07, P = 0.75 for WSF), so that
what varied with concentration was the percent-
age of crabs responding and not the magnitude

60

40

A

NAPHTHALENE

0

WSF

Y = 54.1*

1.22 X

42

r2 = <M

k

43

35 36

1 \
1 \

37

N

34

1
1

\
\

.

A \

44 \

S

35 '
. . / .

0
36

\

34^

^_.

35

__0

29

1

1

44

1

N^/32

1

2')

\

\

\

A

45

1

Figure 1. — Percentage of Dungeness crabs detecting naphtha-
lene and the water soluble fraction (WSF) of crude oil as a
function of the logarithm of concentration (mg/1). The percent-
age of crabs detecting a control of membrane-filtered sea water
was 28.8% ( n = 66) for naphthalene and 26.8% ( n = 41) for WSF
The horizontal dotted line is the 90% confidence limit for
the control values for both naphthalene and WSF (38%).
The number beside each point is the number of trials at
the concentration.

of the response. Also, the magnitudes of the
increase in antennular flicking were the same for
both naphthalene and WSF. For naphthalene, the
grand median of the antennular flicking rate
ratios was 2.04; for the WSF, the grand median
was 1.96.

Discussion

When presented with naphthalene or WSF of
crude oil, Dungeness crabs changed antennular
orientation and flicking rate in the same manner
as when presented with a clam extract. The blue
crab also gives the same detection behaviors
for hydrocarbons as for food (Pearson and 011a
1977. 1979, 1980; Pearson et al. in press). The
similar findings in both species indicate that '
chemoreception by these crustaceans is not re-
stricted to chemical cues for food and, thus, agree
with Ache's (1975) suggestion that the chemical
spectrum sensed by decapod crustaceans is really
quite broad.

While the manner of antennular response to
naphthalene and WSF was the same as that to a
clam extract, the magnitudes of the flicking in-
crease were slightly less and the chemosensory
thresholds were 10^ and 10^ times higher than
those found for the clam extract (Pearson et al.
1979). The grand median ratios of flicking rates
for naphthalene and WSF, 2.04 and 1.96, were
lower than that for the clam extract, 2.67. Also, the
ranges of flicking ratios for the hydrocarbons were
<30% of that for the clam extract. The slightly
less intense response and much higher thresholds
suggest that the petroleum hydrocarbons rank as
much less potent chemical cues than sapid chemi-
cals from a natural food.

Previously, Pearson and 011a (1980) had hy-
pothesized that the chemical and chemosensory
processes producing a higher detection threshold
for a single petroleum hydrocarbon, naphthalene,
than for a complex mixture of hydrocarbons, the
WSF of crude oil, are analogous to the processes
producing a similar relationship of thresholds for
single amino acids and complex mixtures. Usu-
ally, food extracts and complex mixtures of amino
acids and other chemicals have a lower detection
threshold than that of a single amino acid ( Mackie
1973; McLeese 1974). Indeed, with the Dungeness
crab the detection threshold for WSF was about
100 times lower than that for naphthalene. Also,
the variability in detection was much less for WSF
than for naphthalene. This apparent greater dif-

824

ficulty in detecting the single hydrocarbon than
the more complex WSF is presumptive evidence
for the hypothesized analogy. With naphthalene
constituting only 0.49^ of the total hydrocarbons
in the WSF, the crabs were probably responding
primarily to other compounds or, perhaps, to some
sort of odor medley.

One possible explanation for the extreme vari-
ability in naphthalene detection is that detection
at high naphthalene concentrations was inhibited
by some toxic, narcotic, or anesthetic action not
present or much reduced at low concentrations.
The blocking of chemosensory feeding and mating
responses in the crab Pachygrapsus crassipes
after 24-h exposure to naphthalene at 10 ~^ nig/1
(Takahashi and Kittredge 1973) supports the
possibility of such inhibition. If the threshold
concentration for chemosensory inhibition was
within the range of concentrations we presented,
then a sharp increase in the percentage of crabs
detecting naphthalene would be expected below
the inhibition threshold and would produce the
sawtooth-shaped curve seen for naphthalene in
Figure 1. A sawtooth-shaped curve would also
result if the sensitive antennular chemoreceptors
were more impaired than the less sensitive body
chemoreceptors on the dactyls, chelae, and mouth-
parts. If the antennular chemoreceptors were the
more impaired at high naphthalene concentra-
tions, detection would occur primarily through
body chemoreceptors, and the antennular flicking
increases would then derive from a reflex pri-
marily involving the body chemoreceptors rather
than one involving the antennular chemorecep-
tors. If the supposed chemosensory inhibition
lessened or disappeared at low naphthalene levels,
detection would switch to the more sensitive
antennular chemoreceptors from the less sensitive
body chemoreceptors. Whatever the explanation,
the weak and inconsistent detection of naphtha-
lene did not allow estimation of a threshold
concentration by the method used here for WSF
and elsewhere for food extracts (Pearson and 011a
1977; Pearson et al. 1979). Without more evidence
concerning the mechanisms producing the partic-
ular shape of the naphthalene curve, the use of the
apparently real peak in detection at 10~^ rng/1 for
estimating thresholds remains an open question.
The most conservative approach for now is to
consider 10 ~^ rng/1 to be the naphthalene detec-
tion threshold.

For both food extract and petroleum hydro-
carbons, the blue crab has exhibited more acute

chemoreception than the Dungeness crab (Pear-
son and 011a 1977, 1979, 1980; Pearson et al.
in press). Pearson et al. (1979) hypothesized that
the lower detection threshold for clam extract
seen in the blue crab was a consequence of the blue
crab's greater ability to sample the chemical
environment with its higher flicking rate and
larger antennules. This hypothesis would apply
equally to the differences between the two crabs in
the hydrocarbon detection thresholds.

An important practical question is how the
ability of the Dungeness crab to detect petroleum
hydrocarbons compares with the range of hydro-
carbon concentrations likely to be encountered by
the crab. In the water column during an oil spill,
McAuliffe et al. (1975) found concentrations of
dissolved hydrocarbons ranging from 2 x 10"^ to
2 X 10"^ mg/l. Of these dissolved hydrocarbons
about one-half were the monoaromatics domi-
nating the WSF used here. During a spill from a
North Sea platform, Grahl-Nielsen (1978) found
petroleum hydrocarbon concentrations ranging
up to 4 X 10 ~^ mg/1. In the open sea between Nova
Scotia and Bermuda, Gordon et al. (1974) found
petroleum hydrocarbon concentrations of 2.04 x
10"^ 8 X 10"^ and 4 X 10'^ mg/1 at the surface,
1 m, and 5 m. These concentrations roughly agree
with those given for relatively uncontaminated
oceanic areas by Clark and MacLeod (1977), who
also stated that chronically contaminated areas
have hydrocarbon concentrations about two orders
of magnitude higher than those of the open sea.
Unfortunately, analytical difficulties in distin-
guishing petrogenic from biogenic hydrocarbons
at low environmental concentrations make esti-
mates of oil levels in chronically contaminated
areas uncertain. For the North Sea, Grahl-Nielsen
et al. (1979) found that despite considerable oil
production there was no apparent standing crop of
petroleum hydrocarbons, but rather petroleum
contamination occurred as localized, transient
patches. Thus, the petroleum hydrocarbon concen-
trations in uncontaminated (10"'* to 10 ~^ mg/1),
chronically contaminated (10""* to 10~^ mg/1), and
oil spill (10"^ to 10"^ mg/1) situations are all at or
above the WSF detection threshold (10"-* mg/1) so
that Dungeness crabs can detect hydrocarbons
readily at the concentrations found in oil spill
situations, probably in chronically contaminated
situations, and marginally in uncontaminated
situations. In being able to detect the petroleum
hydrocarbons at concentrations at and below those
found in oil spill situations, Dungeness crabs can

825

achieve the first step to any subsequent behavioral
response to petroleum.

Acknowledgments

We thank J. W. Anderson for his valuable dis-
cussions with us. The work was supported by the
National Oceanic and Atmospheric Administra-
tion of the U.S. Department of Commerce under
the Interagency Energy-Environment Program of
the U.S. Environmental Protection Agency.

Literature Cited

ACHE, B. W.

1975. Antennular mediated host location by symbiotic
crustaceans. Mar. Behav. Physiol. 3:125-130.
ANDERSON, J. W., J. M. NEFF, B. A. COX, H. E. TATUM, AND
G. M. HIGHTOWER.

1974. Characteristics of dispersions and water-soluble
extracts of crude and refined oils and their toxicity
to estuarine crustaceans and fish. Mar Biol. (Berl.)
27:75-88.

Bean, R. M., J. W. Blaylock, and R. G. Riley.

1978. Application of trace analytical techniques to the
study of hydrocarbon composition upon dispersion of
petroleum in a flowing seawater system . In Proceedings
of a symposium on analytic chemistry of petroleum
hydrocarbons in the marine aquatic environment, p. 902-
908. Div. Pet. Chem., Am. Chem. Soc.

Clark, R. C, Jr., and W. D. MacLeod, Jr.

1977. Inputs, transport mechanisms, and observed con-
centrations of petroleum in the marine environment.
In D. C. Malins (editor). Effects of petroleum on arctic
and subarctic marine environments and organisms. Vol I.
Nature and fate of petroleum, p. 91-223. Acad. Press, N.Y.

FUZESSERY,Z. M.

1978. Quantitative stimulation of antennular chemore-
ceptors of the spiny lobster, Panulirus argus. Comp.
Biochem. Physiol. 60A:303-308.

Gordon, D. C, Jr., P D. Keizer, and J. Dale.

1974. Estimates using fluorescence spectroscopy of the
present state of petroleum hydrocarbon contamination
in the water column of the northwest Atlantic Ocean.
Mar Chem. 2:251-261.
Grahl-Nielsen, O.

1978. The Ekofisk-Bravo blowout: petroleum hydrocar-
bons in the sea. In Proceedings of the conference on
assessment of ecological impacts of oil spills, p. 476-487.
Am. Inst. Biol. Sci., Arlington, Va.

Grahl-Nielsen, O., K. Westrheim, and S. Wilhelmsen.

1979. Petroleum hydrocarbons in the North Sea. In 1979
Oil spill conference, p. 629-632. Am. Pet. Inst., Wash., D.C.

hazlett, b. a.

1971. Antennule chemosensitivity in marine decapod
Crustacea. J. Anim. Morph. Physiol. 18:1-10.
MACKIE, A. M.

1973. The chemical basis of food detection in the lobster,
Homarus gammarus. Mar Biol. (Berl.) 21:103-108.

McAULIFFE, C. D.

1971. GC determination of solvents by multiple phase
equilibration. Chem. Technol. 1:46-51.

McAULIFFE, C. D., A. E. SMALLEY, R. D. GROOVER, W. M.

Welsh, W. S. Pickle, and G. E. Jones.

1975. Chevron Main Pass Block 42 oil spill: chemical and
biological investigations. In Proceedings of the 1975
joint conference on prevention and control of oil spills,
p. 555-566. Am. Pet. Inst., Wash., D.C.

MCLEESE, D. W.

1974. Olfactory responses of lobsters (Homarus ameri-
canus) to solutions from prey species and to seawater
extracts and chemical fractions of fish muscle and effects
of antennule ablation. Mar Behav. Physiol. 2:237-249.

Olla, B. L., W. H. Pearson, and A. L. Studholme.

1980. Applicability of behavioral measures in environ-
mental stress assessment. In A. D. Mclntyre and J. B.
Pearce (editors). Biological effects of marine pollution and
the problems of monitoring. Rapp. P.-V. Reun. Cons. Int. '
Explor Mer 179:162-173.

Pearson, W H., and B. L. Olla.

1977. Chemoreception in the blue crab, Callinectes sapi-
dus. Biol. Bull. (Woods Hole) 153:346-354.

1979. Detection of naphthalene by the blue crab, Cal-
linectes sapidus. Estuaries 2:64-65.

1980. Threshold for detection of naphthalene and other
behavioral responses by the blue crab, Callinectes sapi-
dus. Estuaries 3:224-229.

Pearson, W. H., S. E. Miller, J. W. Blaylock, and B. L.
Olla.
In press. Detection of the water-soluble fraction of crude
oil by the blue crab, Callinectes sapidus. Mar. En-
viron. Res.

Pearson, W. H., P C. Sugarman, D. L. Woodruff, and
B. L. Olla.

1979. Thresholds for detection and feeding behavior in the
Dungeness crab, Cancer magister (Dana). J. Exp. Mar
Biol. Ecol. 39:65-78.
Takahashi, F. T, and J. S. Kittredge.

1973. Sublethal effects of the water soluble component of
oil: Chemical communication in the marine environ-
ment. In D. G. Ahearn and S. P. Meyers (editors).
The microbial degradation of oil pollutants, p. 259-264.
La. State Univ. Press Publ. LSU-SG-73-01.

Walter H. Pearson

Peter C. Sugarman

Dana L. Woodruff

J. W. Blaylock

Battelle, Pacific Northwest Laboratories
Marine Research Laboratory
358B Washington Harbor Road
Sequim, WA 98382

bori l. Olla

Northeast Fisheries Center Sandy Hook Laboratory
National Marine Fisheries Service, NOAA
Highlands, NJ 07732

826

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Special Scientific Report — Fisheries

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Contents-continued

FOG ARTY, MICHAEL J., DAVID V D. BORDEN, and HOWARD J. RUSSELL.

Movements of tagged American lobster, Homarus americanus, off Rhode Island . . . 771
RENSEL, JOHN E., and EARL F PRENTICE. Factors controlling growth and survi-
val of cultured spot prawn, Pandalus platyceros, in Puget Sound, Washington 781

Notes

THEILACKER, GAIL H. Rearing container size affects morphology and nutritional
condition of larval jack mackerel, Trachurus symmetricus 789

CARNEY, ROBERT S., and ANDREW G. CAREY, JR. Effectiveness of metering
wheels for measurement of area sampled by beam trawls 791

PITCHER, KENNETH W Stomach contents and feces as indicators of harbor seal,
Phoca vitulina, foods in the Gulf of Alaska 797

CHRISTENSEN, DARRYL J., and WALTER J. CLIFFORD. The 1978 spring recre-
ational catch of Atlantic mackerel, Scomber scombrus, off the Middle Atlantic region 799

BEARDSLEY, GRANT L. Size and possible origin of sailfish, Istiophorus platypterus,
from the eastern Atlantic Ocean 805

RICE, STANLEY D., and JACK E. BAILEY. Ammonia concentrations in pink

salmon, Oncorhynchus gorbuscha, redds of Sashin Creek, southeastern Alaska . . . 809

HUNTER, JOHN R., and CAROL A. KIMBRELL. Egg cannibalism in the northern
anchovy, Engraulis mordax 811

QUINN, THOMAS P, BRUCE S. MILLER, and R. CRAIG WINGERT Depth dis-
tribution and seasonal and diel movements of ratfish, Hydrolagus colliei, in Puget
Sound, Washington 816

PEARSON, WALTER H., PETER C. SUGARMAN, DANA L. WOODRUFF, J. W
BLAYLOCK, and BORI L. OLLA. Detection of petroleum hydrocarbons by the
Dungeness crab. Cancer magister 821

Notices
NOAA Technical Reports NMFS published during the first 6 months of 1980 827

* GPO 696-404

^^^*'°'^o.

V

^fArcs o« *■

Fishery Bulletin

h

■Mr lb 1981

Vol. 78, No. 4

October 1 980

BRAY, RICHARD N. Influence of water currents and zooplankton densities on
daily foraging movements of blacksmith, Chromis punctipinnis , a planktivorous
reef fish 829

BREIWICK, JEFFREY M., EDWARD D. MITCHELL, and DOUGLAS G. CHAP-
MAN. Estimated initial population size of the Bering Sea stock of bowhead whale,
Balaena mysticetus: an iterative method 843

RICHARDSON, SALLY L. Spawning biomass and early life of northern anchovy,
Engraulis mordax, in the northern subpopulation off Oregon and Washington . . . 855

DURBIN, ANN G., EDWARD G. DURBIN, PETER G. VERITY, and THOMAS J.
SMAYDA. Voluntary swimming speeds and respiration rates of a filter-feeding
planktivore, the Atlantic menhaden, Breuoortia tyrannus (Pisces: Clupeidae) .... 877

MENDELSSOHN, ROY. Using Box-Jenkins models to forecast fishery dynamics:
identification, estimation, and checking 887

LAROCHE, WAYNE A. Development of larval smooth flounder, Liopsetta putnami,
with a redescription of development of winter flounder, Pseudopleuronectes ameri-
canus (family Pleuronectidae) 897

MODDE, TIMOTHY, and STEPHEN T ROSS. Seasonality of fishes occupying a
surf zone habitat in the northern Gulf of Mexico 911

MATARESE, ANN C, SALLY L. RICHARDSON, and JEAN R. DUNN. Larval
development of Pacific tomcod, Microgadus proximus, in the northeast Pacific
Ocean with comparative notes on larvae of walleye pollock, Theragra chalcogramma,
and Pacific cod, Gadus macrocephalus (Gadidae) 923

Notes

AINLEY, DAVID G., CRAIG S. STRONG, HARRIET R. HUBER, T JAMES LEWIS,
and STEPHEN H. MORRELL. Predation by sharks on pinnipeds at the Farallon
Islands 941

GRISWOLD, CAROLYN A., and JEROME PREZIOSO. In situ observations on
reproductive behavior of the long-finned squid, Loligo pealei 945

LEWIS, ROBERT M., and CHARLES M. ROITHMAYR. Spawning and sexual
maturity of Gulf menhaden, Brevoortia patronus 947

(Continued on next page)

Seattle, Washington

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NATIONAL MARINE FISHERIES SERVICE

Fishery Bulletin

The Fishery Bulletin carries original research reports and technical notes on investigations in fishery science, engineering, and
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Fishery Bulletin

CONTENTS

Vol. 78, No. 4 October 1980

BRAY, RICHARD N. Influence of water currents and zooplankton densities on
daily foraging movements of blacksmith, Chromis punctipinnis , a planktivorous
reef fish 829

BREIWICK, JEFFREY M., EDWARD D. MITCHELL, and DOUGLAS G. CHAP-
MAN. Estimated initial population size of the Bering Sea stock of bowhead whale,
Balaena mysticetus: an iterative method 843

RICHARDSON, SALLY L. Spawning biomass and early life of northern anchovy,
Engraulis mordax, in the northern subpopulation off Oregon and Washington . . . 855

DURBIN, ANN G., EDWARD G. DURBIN, PETER G. VERITY, and THOMAS J.
SMAYDA. Voluntary swimming speeds and respiration rates of a filter-feeding
planktivore, the Atlantic menhaden, Brevoortia tyrannus (Pisces: Clupeidae) .... 877

MENDELSSOHN, ROY. Using Box-Jenkins models to forecast fishery dynamics:
identification, estimation, and checking 887

LAROCHE, WAYNE A. Development of larval smooth flounder, Liopsetta putnami,
with a redescription of development of winter Honnder, Pseudopleuronectes ameri-
canus (family Pleuronectidae) 897

MODDE, TIMOTHY, and STEPHEN T ROSS. Seasonality of fishes occupying a
surf zone habitat in the northern Gulf of Mexico 911

MATARESE, ANN C, SALLY L. RICHARDSON, and JEAN R. DUNN. Larval
development of Pacific tomcod, Microgadus proximus, in the northeast Pacific
Ocean with comparative notes on larvae of walleye pollock, Theragra chalcogram ma,
and Pacific cod, Gadus macrocephalus (Gadidae) 923

Notes

AINLEY, DAVID G., CRAIG S. STRONG, HARRIET R. HUBER, T JAMES LEWIS,
and STEPHEN H. MORRELL. Predation by sharks on pinnipeds at the Farallon
Islands 941

GRISWOLD, CAROLYN A., and JEROME PREZIOSO. In situ observations on
reproductive behavior of the long-finned squid, Loligo pealei 945

LEWIS, ROBERT M., and CHARLES M. ROITHMAYR. Spawning and sexual
maturity of Gulf menhaden, Brevoortia patronus 947

(Continued on next page)

Seattle, Washington
1981

For sale by the Superintendent of Documents. U.S. Government Printing Office. Washington.
DC 20402— Subscription price per year: $14.00 domestic and $17.50 foreign. Cost per single
issue: $4.00 domestic and $5.00 foreign.

Contents-continued

STROUD, RICHARD K., CLIFFORD H. FISCUS, and HIROSHI KAJIMURA. Food
of the Pacific white-sided dolphin, Lagenorhynchus obliquidens , Dall's porpoise,
Phocoenoides dalli, and northern fur seal, Callorhinus ursinus, off California and
Washington 951

MARLIAVE, JEFFREY B. Spawn and larvae of the Pacific sandfish, Trichodon
trichodon 959

McCLELLAN, G. L., and J. K. LEONG. A radiologic method for examination of the
gastrointestinal tract in the Atlantic ridley, Lepidochelys kempi, and loggerhead,
Caretta caretta, marine turtles 965

CLAUSEN, DAVID M. Summer food of Pacific cod, Gadus macrocephalus , in coastal
waters of southeastern Alaska 968

KHILNANI, ARVIND. Use of Griffin's yield model for the Gulf of Mexico shrimp
fishery 973

GOLDBERG, STEPHEN R. Seasonal spawning cycle of the Pacific butterfish,
Peprilus simillimus (Stromateidae) 977

DAVIS, GARY E. Effects of injuries on spiny lobster, Panulirus argus, and impli-
cations for fishery management 979

INDEX, VOLUME 78 985

Vol. 78, No. 3 was published on 11 February 1981.

The National Marine Fisheries Service (NMFS) does not approve, rec-
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or endorses any proprietary product or proprietary material mentioned
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the advertised product to be used or purchased because of this NMFS
publication.

INFLUENCE OF WATER CURRENTS AND ZOOPLANKTON DENSITIES ON

DAILY FORAGING MOVEMENTS OF BLACKSMITH,

CHROMIS PUNCTIPINNIS, A PLANKTIVOROUS REEF FISH

Richard N. Bray*

ABSTRACT

The blacksmith, Chromis punctipinnis , one of the most abundant fishes in kelp forests off southern
California, daily emerges from rock shelters and moves to specific locations where it forages in the
midwater on zooplankton. Midwater transects taken over a reef that experiences occasional reversals
in water currents indicated that large blacksmith (greater than 150 mm total length) consistently
gathered at the incurrent end of the reef. These movements are probably related to the availability of
food. Replicate plankton tows taken near the ends of the reef demonstrated that zooplankton densities
were greater at the incurrent end. Experiments in which large fish were placed in cages suspended in
midwater at both reef ends demon.strated that individuals foraging at the incurrent end consumed
more prey. Small blacksmith (less than 125 mm total length) did not undergo foraging movements.
Instead, most remained in the shallower portions of the reef, close to cover, even though caging
experiments and collections of free-living individuals indicated that these fish would consume more
prey if they moved upcurrent. Since small as well as large blacksmith benefit from foraging at the
incurrent end, the size-specific differences in foraging movements probably reflect differences in the
cost of migrating in terms of time, energy, and predation.

Many fishes on temperate and tropical reefs feed
heavily on zooplankton. They eat either by day or
by night, and school or shelter when inactive
(Hobson 1972, 1973, 1974; Hobson and Chess 1976).
Some planktivores limit their movements to the
water column above their shelters (e.g., Sale 1971;
Hobson 1972, 1973); the distribution and small-
scale movements of these parochial species have
been the subject of recent quantitative investiga-
tions (e.g., Stevenson 1972; Hobson and Chess
1978; de Boer 1978). Other planktivores undergo
extensive horizontal movements (Hobson 1972,
1973), and have received less attention. Nonethe-
less, migrating planktivores are often extreme-
ly abundant and probably import substantial
amounts of extrinsic energy — drift zooplankton
— into reef communities (Stevenson 1972).

The blacksmith, Chromis punctipinnis , aplank-
tivorous pomacentrid that may grow to a total
length (TL) of 300 mm (Miller and Lea 1972),
is one of the most abundant fishes inhabiting
the inshore rocky reefs of southern California.
In aggregations of up to several hundred indi-

' Department of Biological Sciences, University of California,
Santa Barbara, Calif.; present address: Department of Biology,
California State University Long Beach, CA 90840.

Manuscript accepted March 1980.
FISHERY BULLETIN: VOL 78, NO. 4, 1981.

viduals, they feed throughout the day on a variety
of zooplankton, including larvaceans, copepods,
cladocerans, and various larvae (Hobson and
Chess 1976). At dusk, they descend to the reef
surface where they shelter in holes and crevices
until dawn (Ebeling and Bray 1976; Hobson and
Chess 1976). Many tropical congeners of the black-
smith have similar activity patterns (e.g., Hobson
1965, 1972; Collette and Talbot 1972; Emery 1973).
During preliminary observations on rocky reefs
near Santa Barbara, Calif., I found that black-
smith often forage and shelter in different areas.
Large numbers of blacksmith emerge from shel-
ters at dawn, assemble into a school, and move to a
location above a reef, where they disperse into a
loose aggregation in the midwater and forage on
zooplankton. At least some blacksmith near Santa
Catalina Island, Calif., show a similar pattern
(Hobson and Chess 1976). In commenting on the
location of daytime foraging aggregations, Lim-
baugh (1955) observed that, "Thick schools of
young to half-grown blacksmith often form where
a plankton-rich current enters the kelp bed." Such
a response to water currents would enable black-
smith to be among the first of many vertebrate and
invertebrate planktivores to forage on plankton as
it is swept across the reef community. However,

829

FISHERY BULLETIN: VOL. 78. NO. 4

other factors may also affect the distribution of
blacksmith. For example, kelp and high relief
rocks may serve as orientation points or shelter for
fish in the water column (Limbaugh 1955; Quast
1968a, b, c; Ebeling and Bray 1976; Hobson and
Chess 1976).

In this paper, I first examine the distribution of
blacksmith in relation to water currents over a
reef that is subjected to occasional reversals in
current flow to see if they consistently gather at
the incurrent end. Since foraging is the major
activity of blacksmith while assembled in these
midwater aggregations, I then determine if plank-
ton is more abundant at the incurrent end. Finally,
by examining caged and free-living individuals,
I see whether blacksmith that forage at the in-
current end consume more prey.

METHODS

Study Site

Naples Reef is a large rocky outcrop (275 x
80 m) located 24 km west of Santa Barbara and 1.6
km offshore (Figure 1). The substratum is a series
of uplifted sandstone rills and ridges that parallel

the coast. Depths across the reef average 8-10 m,
although some prominences come to within 5 m of
the surface. A sandy bottom 16-20 m deep sur-
rounds the reef, with rocky outcrops inshore and
cobbles offshore. The assemblage of plant and
animal life on and around the reef is among the
richest along the Santa Barbara coast. Giant kelp,
Macrocystis pyrifera, is always present on the reef,
although kelp densities fluctuated considerably
throughout the study period. The species composi-
tion and abundance of fishes at Naples Reef are
listed in Ebeling et al. (1980).

Naples Reef is well suited to study the effects of
water currents on the distribution of fish. The reef
is almost always swept by measurable longshore
currents. Although usually these come from the
east, occasionally they come from the west. A shift
in the distribution of fish when the currents
reverse would provide strong evidence that water
currents affect the fish's distribution.

Surveys

In December 1975, 1 initiated biweekly counts of
all fish in the water column at four sites on the reef
(Figure 1). At each site, I fixed a line from a

Figure l. — Contour map of Naples Reef, southern California. Heavy lines indicate locations of midwater transects: 30 m (to cross
mark) and 60 m (to end) from the starting points ( circles). Letters indicate incurrent and excurrent locations where zooplankton were
sampled: A locations — when current flowed from the east; B locations — when current flowed from the west. Midwater cages were
located at the A locations. The shaded portion indicates the rocky substratum, while the surrounding open area represents ssmd. The
dashed line indicates the margin of the kelp bed. Depths are in meters.

830

BRAY: INFLUENCE OF WATER CURRENTS AND ZOOPLANKTON DENSITIES

permanent anchoring point to a buoy within 1 m of
the surface. At middepth (6 m), I attached a
transect line and swam four transects at a constant
speed, one each to the north, east, south, and west.
Without moving my head, I counted all blacksmith
within my field of view. Fish were tallied in
separate columns on a slate according to their size
as estimated by eye: juveniles (<125 mm TL),
halfgrown fish (125-150 mm), and adults (>150
mm). These classes refer to sizes and not neces-
sarily to stages of sexual maturity. A complete
survey consisted of 16 transects: 4 at each of the
four sites on the reef. During the first 26 surveys
(9 December 1975-2 November 1976), the length of
the transect line was 30 m, so a total of 480 m were
traversed each survey. For the remaining 13
surveys (9 November 1976-23 July 1977), the
length of the transects was doubled to 60 m each
(960 m/survey) to see if large aggregations of
blacksmith occurred beyond the areas that were
initially sampled. I did not conduct surveys when
visibility was <2 m.

I also examined several oceanographic variables
at each site on the reef. Water visibility was
measured during each transect as the distance at
which I could easily discern a fishiike silhouette
attached to the line. Water velocities were mea-
sured several times at each site by timing the
movement of small particles. And surface, mid-
water, and bottom water temperatures were taken
with a small dial thermometer.

Plankton Sampling

Once the movements of blacksmith were deter-
mined, I made replicate zooplankton tows at
known sheltering sites near the excurrent end of
the reef, and known foraging sites at the incurrent
end. Incurrent samples were collected at the
margin of the kelp bed, over the sand bottom that
surrounds the reef. Excurrent samples were taken
within the bed, above rocky areas that provide
shelter for large numbers of blacksmith at night.
The exact location of the sample sites depended on
the direction of the water currents (Figure 1). I
specifically avoided sampling on days when the
current velocity was negligible, when there were
obvious eddies, or when the current flow was not
along the east-west axis of the reef.

Plankton were collected between 1000 and
1400 h with a 0.5 m diameter 0.333 mm mesh
net pushed by a diver. A TSK^ flowmeter, fitted
across the net opening, measured the filtered

volume of water. I randomized (by coin flip) my
choice of which end to sample first, thereby
restricting such variables as collection time, net
clogging, diver fatigue, etc., to random error. Each
tow was double oblique, going from the surface to a
depth of 6 m, then back to the surface. The diver
swam a haphazard pattern through the kelp bed
and avoided sampling within 1 m of a kelp plant or
the bottom. All samples were immediately fixed in
5% buffered Formalin. The time interval between
the first and last tows in a collection ranged from
1.5 to 4.5 h.

In the laboratory, samples were split with a
Folsum plankton splitter: one-half was used for
weighing and the other half was used for counting.
For dry weights, samples were filtered (vacuum
pressure = 725 mm Hg) onto preweighed GF/C
filters, and dried at 60° C to a constant weight. For
counting, samples were split two more times, then
subsampled with three 10 ml aliquots drawn with
a Stemple pipette. The plankton were counted
under a dissecting microscope and sorted into
broad taxonomic categories. Weights and counts
were standardized by conversion to amounts per
cubic meter of water sampled.

I analyzed the data in two ways to compare
densities of zooplankton between incurrent and
excurrent ends of the reef. First, I compared the
individual incurrent and excurrent samples with-
in each collection by Mann-Whitney C/-tests to
look for significant differences in densities be-
tween the reef ends. Second, I compared mean
densities between incurrent and excurrent sam-
ples of each collection, and tested for incurrent-
excurrent differences in these means among the
eight collections with Wilcoxon's signed-ranks
tests; thus, each collection was a paired (incurrent
versus excurrent) observation.

Foraging Experiments

To see if blacksmith near the incurrent end
consume more prey, I compared gut contents of
fish that foraged near the incurrent kelp margin
and excurrent shelter sites. I did not compare free-
living adults because they were relatively rare
near the excurrent end and their major activity
might not have been foraging. Instead, I placed
individuals in cages located at both ends of the
reef. Cages were constructed ofalxlxlm

^ Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

831

FISHERY BULLETIN: VOL. 78, NO. 4

wooden frame covered with galvanized chicken
wire, which allowed fairly free passage of water
through the enclosure. For experiments using
larger fish (>125 mm SL, standard length) the
mesh measured 2.5 x 3.7 cm; mesh size was
halved to 1.3 x 1.9 cm when smaller fish were
used. Seine floats were attached to the top of the
cages to make them positively buoyant, and the
cages were suspended in midwater at a depth of 5
m by a length of rope anchored to the substratum.
The cages were located in the same areas on the
reef from which plankton were sampled. One cage
was placed at the eastern margin of the kelp bed,
60 m east of the reef. The other was placed over the
reef top, 50 m from the extreme west end of the
reef (Figure 1). When half of the experiments were
completed, the cages were translocated.

Blacksmith were captured while in shelters
with the anesthetic quinaldine, or while attracted
to chum stations (broken sea urchins). Fish were
placed in holding tanks on the boat and haphaz-
ardly assigned to a cage. One to five fish were
captured for each cage. Before each experiment,
the cages were scrubbed with a brush to remove
encrusting organisms. When fish were placed in
the cage, they swam to the bottom; by the next
day, they had usually gathered in the middle.
At night, the fish nestled in the bottom corners
of the cage.

Each experiment lasted 7-10 d. Preliminary
experiments indicated that at least 5 d were
required before caged fish began to feed. Fish
were removed from cages in the midafternoon and
fixed in buffered Formalin. On three occasions, I
speared free-living fish in the vicinity of the
incurrent cage at the same time that caged fish
were removed, to see if caging affected the fish's
diet. Since smaller blacksmith do not undergo
large-scale movements and are abundant through-
out the reef, I also compared gut contents of free-
living juveniles speared at the incurrent and
excurrent ends. For all collections, blacksmith at
the incurrent end were removed first; those at the
excurrent end within an hour later. Thus, positive
differences in gut fullness between incurrent and
excurrent fish are conservative because excurrent
fish were able to forage for a longer period of time.

In the laboratory, fish were measured for stan-
dard length, blotted weight, and displaced volume.
The gut was removed and divided into stomach
and intestine. The contents of each were measured
for displaced volume, then examined under a
dissecting microscope and identified into broad

taxonomic categories. Finally, contents were
washed onto a preweighed filter and dried at 60° C
to a constant weight.

To standardize for differences in fish sizes, the
volumes and weights of the gut contents were
expressed as relative measures: 1) volumetric
fullness as (Vg/Vf) x 10^ where Vg is the dis-
placed volume (in milliliters) of the gut contents,
and Vf is the displaced volume (in milliliters) of
the intact fish; 2) gravimetric fullness as: (Wg/Wf)
X 10"*, where Wg and Wf represent weights (in
grams) of the gut contents and intact fish. Finally,
for each experiment, I scaled volumetric and
gravimetric fullness from 1.0 for the largest value,
down toward 0, then averaged the two scaled
values to obtain an overall estimate of gut full-
ness. This enabled me to pool data among experi-
ments to increase sample size.

RESULTS

Physical Measurements

I made 39 surveys between December 1975 and
July 1977. However, since water visibility directly
influenced the volume of water in which I counted
fish, I excluded from further analysis those
surveys when mean visibility was significantly
greater at the incurrent end of the reef (^-tests;
P<0.05) or when variances in visibility at the
incurrent and excurrent ends were heterogeneous
(F-tests, P<0.05). In the remaining 27 surveys,
water flowed over the reef from the east in 23; on 4
occasions (twice in April 1976, once in August
1976, and once in January 1977), the current was
reversed and flowed from the west. Mean monthly
water visibility ranged from 4.5 m in March to
8.7 m in December. Visibility was slightly greater
at the excurrent end of the reef. When the current
flowed from the east, visibility averaged 7.1 m at
the east end and 7.4 m at the west end; when the
current reversed, visibility averaged 6.0 m and
5.1 m at the east and west ends.

Spot checks on the movements of small particles
indicated that the net flow of water was roughly
unidirectional over most of the reef; this general
flow was confirmed on 2 d when pieces of kelp were
followed as they drifted the length of the reef
(Bailey^). Nonetheless, variances in velocity were
significantly heterogeneous between reef ends for

^Thomas Bailey, Marine Science Institute, University of
California, Santa Barbara, CA 93106, pers. commun. June 1977.

832

BRAY: INFLUENCE OF WATER CURRENTS AND ZOOPLANKTON DENSITIES

individual measurements {F-max test, P< 0.001),
and for mean velocities among all 27 surveys
(variances were: 41.10 incurrent, 16.05 excurrent;
P<0.05). These variations were presumably
caused by local turbulence produced by kelp and
rocky prominences.

Current velocities were consistently greater at
the incurrent reef end. When water flowed from
the east, mean incurrent and excurrent velocities
were 11.0 cm/s and 4.6 cms (Wilcoxon's signed-
ranks test, P< 0.001). When currents were re-
versed, incurrent and excurrent velocities were
4.9 and 3.6 cm/s (P>0.25); these differences
probably would be significant with a larger sam-
ple size.

Water temperatures at the surface and mid-
water averaged 15.6° and 15.3° C, and both ranged
from 13° C in April to 20° C in October. Bottom
temperatures showed a similar pattern, but aver-
aged approximately 2° C lower. Temperatures
taken in 21 surveys when the current flowed from
the east did not differ significantly between reef
ends at any of the three depths ( ^tests for paired
samples, P>0.25). I recorded temperatures on
only two of the four surveys when currents flowed
from the west. Surface and midwater tempera-
tures both averaged around 15° C while bottom
temperatures averaged 13° C. I could not detect
differences in temperatures between reef ends.

Role of Water Currents

The patterns in water visibility simplified my
analysis of the fish counts. I treated each of the 27
surveys as a pair of samples, one from the incur-
rent and the other from the excurrent reef end.
Each member of a pair consisted of a total count of
blacksmith from the eight transects taken at one
end of the reef (Figure 1). Differences within each
pair were then analyzed among surveys with one-
tailed nonparametric tests, with the hypothesis
that counts of blacksmith are greater at the
incurrent reef end. The similarity in water visibil-
ity between reef ends automatically standardized
the counts for the volume of water that was
sampled. Actually, the test of the hypothesis was
conservative because visibility (hence the volume
of water sampled) was significantly lower at the
incurrent end in 6 of 27 surveys. I also calculated
for each survey the proportion of blacksmith
counted at each end of the reef. Proportions were
arc sine transformed for computation of 95%
confidence intervals (CI). I checked the preci-

sion of my surveys on two occEisions by having
another diver swim abreast of me and count
blacksmith independently. Our total counts of
adult blacksmith were similar: 103 (RNB) versus
112 (partner), and 254 (RNB) versus 273 (part-
ner). Moreover, the surveys seemed to confirm
our subjective impressions on the relative abun-
dance of adult blacksmith and other fishes in
the midwater.

Blacksmith were the most abundant fish in
the midwater and were recorded on every sur-
vey. Other abundant fishes in the midwater were
kelp bass, Paralabrax clathratus, and senorita,
Oxyjulis californica (Table 1).

Adult blacksmith invariably aggregated at the
incurrent end (Table 2). In each of the 27 surveys,
more adults were counted at the incurrent than at
the excurrent end (Wilcoxon's signed-ranks test,
P< 0.001). Doubling the length of transects had
little effect on the counts of adults at the excurrent
end, but resulted in a 3- to 4-fold increase in counts
of adults at the incurrent end. This was because
large numbers of adults gathered farther upcur-
rent, beyond the area covered in the short tran-
sects. The average proportion of adults at the east
end of the reef was 0.99 (95% CI = 0.92-1.0) when
it was the incurrent end, and 0.09 (95% CI =
0-0.32) when it was the excurrent end.

Adults respond quickly to changes in current
direction. On one occasion around midday, the
current reversed during a survey and the adults

Table l. — Relative abundance (percentage of total individuals)
and frequency of occurrence (percent of total surveys* of fishes
counted in midwater transects at Naples Reef, southern Cali-
fornia. Species are listed in order of decreasing abundance.

Percentage of

Frequency

Species

total individuals

(%)

Chromis punctipinnis

41.58

100.0

Paralabrax clathratus

22.04

100.0

Oxyjulls californica

9.47

81.5

Medialuna callfornlensis

9.00

92.6

Sebastes mystlnus

8.62

55.6

Athermops affinis

2.70

22.2

Trachurus symmetrlcus

1.82

25.9

Phanerodon furcatus

1.68

33.3

Sebastes serranoides

0.64

66.7

Brachylstlus frenatus

0.59

33.3

Emblotoca jacksoni

0.42

33.3

Phanerodon atrlpes

0.39

18.5

Seriola dorsalls

0.29

11.1

Rhacochllus toxotes

0.21

18.5

Sebastes atrovlrens

0.20

25.9

Emblotoca lateralis

0.20

3.7

Damallchthys vacca

0.05

22.2

Heterostlchus rostratus

0.04

14.8

GIrella nigricans

0.03

3.7

Mola mola

0.03

11.1

Torpedo californica

0.01

7.4

Sarda chlllensis

0.01

3.7

Total no. of indivlduaJs

7.767

Total no of surveys

27

833

FISHERY BULLETIN: VOL, 78, NO. 4

Table 2.— Number of blacksmith per survey, average (median), in midwater surveys at the east and west ends of Naples Reef,
southern California. Freq. = frequency of occurrence (percent of surveys). Short transects total 480 m; long total 960 m.

Current
direction

East to
west

West to
east

Length of
transects

No.
surveys

short
long
short
long

Adults

Halfgrowns

Juveniles

Freq.

(°o)

East

West

Freq.
(%)

East

West

Freq.

(%)

East

West

16 100.0 44.2 (32.5) 0.6 (0.1)

7 10C.0 162.3 (171.0) 0.6 (0.4)

3 100.0 6.0 (8.0) 28.3 (25.0)

1 100.0 3 (3) 84 (84)

31.3 0.9 (0.2) 0.3 (0.2) 12.5

85.7 39.1 (18.0) 5.4 (1.6) 71.4

66.7 0.0 (0.0) 2.3 (1.0) 0 0

100.0 3 (3) 3 (3) 100.0

1.9 (1.0) 10.9 (3.4)

6.7 (3.0) 123.9 (198.0)

0 (0) 0 (0)

30 (30) 30 (30)

Table 3. — Abundance of zooplankton at the east and west ends of Naples Reef, southern California. For each collec-
tion, differences in abundance between ends of the reef were tested with a Mann-WTiitney U-test.

Numbers

Biomass

Date

Average no. m

3 ± 95°o CI

Average mg m

' = 95% CI

Direction of

No

No.

No

No

current flow

1977

samples

East

samples

West

samples

East

samples

West

East to west

19 Aug.

6

1,302.2= 101. 3-

5

485.0 = 260.7

6

34.8 = 3.1-

5

14.0=4.7

29 Aug.

10

1,589,2 = 265. 3ns

10

1.467.5 = 590.4

10

19.8 = 2.3ns

10

19.7 = 3.6

15 Sept.

10

3,301.0±375.9-

10

2,809.4 = 214.7

10

48.1 =4.3"

10

37.2 = 3.6

21 Sept.

10

2.585.2=423.9"

10

1,095,8 = 278,5

10

32.0 = 3.4"

10

19.8 = 4.3

29 Sept.

10

2,849. 8±407.2ns

7

2,272,2 = 582.1

10

67.6 = 7.7-

7

53.0 = 6.6

20 Oct.

10

3,277.5=427.5"

10

1,573,5 = 289,1

10

43.2 = 4.8"

10

28.5 ±2.9

West to east

7 Sept.

10

1, 983.2 ±323.2"

10

3,184,3 = 253,8

10

41.7 = 6.3"

10

54.7 = 3.6

1 1 Oct.

10

3,062.2 = 737.0"

10

5,314.2 = 539.9

10

44.3 = 9.3-

10

57.9 = 7.2

-Ps0.05; --PssO.Ol: ns, not significant.

quickly migrated to the opposite end of the reef. I
began the survey by counting fish at the west end.
The current w^as flowing from the east and I did
not count any adult blacksmith, although visibil-
ity averaged 12.2 m. I then started the survey at
the east end and counted 81 adults, when the
currents shifted and flowed from the west. While
swimming the transects, I saw small schools of
adults (5-15 individuals) moving toward the west
(now incurrent) end. I returned to the boat and
followed adults as they swam toward the west end,
where I repeated the transects. Even though
water visibility dropped to 5.0 m, I counted 43
adults over the area where, 2 h earlier, I had
counted none.

The movements of halfgrown blacksmith were
less clear. Counts were generally higher at the
east end when the current came from the east
(Table 2; Wilcoxon's signed-ranks test: short sur-
veys, P = 0.14; long surveys, P = 0.06; short and
long combined, P = 0.05). However, the pattern
was inconsistent, and counts were actually great-
er at the west end in 3 of the 11 surveys in which
halfgrown fish were sighted. The proportion of
halfgrown fish at the east end averaged 0.90 (95%
CI = 0.38-1.0). A similar inconsistency occurred
when the current flowed from the west. All half-
grown fish counted were at the west end on the two
short surveys in which they were seen, but the
three individuals counted in the long survey were
at the east end.

Juvenile blacksmith did not gather at the incur-
rent end. When the current flowed from the east,
all juveniles were at the west end of the reef in the
two short surveys in which they were seen and in
the five long surveys (Table 2; Wilcoxon's signed-
ranks test; long stirveys, P< 0.05). The proportion
of juveniles at the east end averaged only 0.03
(95% CI = 0-0.18). When the current flowed from
the west, juveniles were not seen in the short
surveys, and were equally abundant at both ends
of the reef on the one long survey. However, these
data do not accurately describe the response of
juveniles to water currents. Observations along
the bottom indicate that, regardless of the current
direction, many juveniles occurred throughout the
reef in stationary aggregations that form around
shallow rocky prominences. The large number of
juveniles counted at the west end reflected the
location of the transects on the reef: almost 87% of
the juveniles counted in the midwater surveys
were seen in the two transects at the west end,
which were the only transects over the shallowest
part of the reef (Figure 1).

Zooplankton Densities

I took eight collections of zooplankton from mid-
August to mid-October 1977 (Table 3). In six of the
collections, the current flowed from the east; in the
other two the current was reversed and flowed
from the west.

834

BRAY: INFLUENCE OF WATER CURRENTS AND ZOOPLANKTON DENSITIES

Even though the counts of plankton were stan-
dardized to densities, I attempted to sample the
same volume of water in each tow to make it
equally likely that relatively rare items would be
collected at both ends. In seven of eight collections,
volumes of water sampled did not differ signifi-
cantly between reef ends (^-tests, P>0.10); in
the last collection a significantly greater volume
of water was sampled at the west end of the reef
(P<0.01). The average length of the tows was
57.1 m, which corresponds to a filtered volume
of 11.2 m^.

Small copepods (<4 mm carapace length) and
cladocerans were the most abundant items in
the samples, averaging 1,259/m^ and 836/m^.
Small copepods dominated in 93 samples while
cladocerans dominated in the remaining 55 sam-
ples. Most of the copepods were calanoids, al-
though cyclopoids were also present. The majority
of cladocerans appeared to be Evadne sp., but
Penilia sp. occasionally dominated. Larvaceans
ranked third in abundance, averaging 119. 6/m^.

Densities of zooplankton differed markedly be-
tween the mcurrent and excurrent sample sites at
Naples Reef. For each collection, mean number
and dry weight of plankton pooled in excurrent
samples were lower than those in incurrent sam-
ples, regardless of the current direction. Differ-
ences in counts were significant in six of the
eight individual collections (Table 3), and for
all eight collections tested together (Wilcoxon's

signed-ranks test, P<0.005). Estimates of dry
weights followed a similar pattern (Table 3).

The trend of a decreased abundance near the
excurrent end was shared among many of the
zooplankton groups (Table 4). Cladocerans, lar-
vaceans, and bryozoan larvae were significantly
less abundant at the excurrent end in seven
of eight collections. Other groups were less
abundant near the excurrent end in some collec-
tions but not in others. For example, densities
of small copepods were significantly lower in
excurrent samples in six collections, but were
higher in another collection (Table 4). Overall,
mean densities of 7 of the 15 plankton groups
were significantly lower near the excurrent end.
Cladocerans, small copepods, and larvaceans
showed the greatest decrease near the excurrent
end, while polychaetes and nauplii averaged
slightly greater there.

Foraging Experiments

I attempted eight experiments between late
July and mid-December 1977; three were deleted
because several fish died in the cages. The follow-
ing analysis is based on the 27 of 31 fish in the
remaining five experiments that had food in their
guts and showed no signs of injury. The first four
experiments used larger individuals (117-214 mm
SL); the last experiment used smaller fish (88-117
mm SL). For each experiment, there were only

Table 4. — Zooplankton densities near the incurrent and excurrent ends of Naples Reef, southern
California. Densities are averaged among means of the eight collection days. Columns to the right
indicate number of collections during which plankton densities at the incurrent end were greater,
less than, or equal to those near the excurrent end (Mann-Whitney [/-tests, two tailed; P«0.05).
Symbols next to incurrent densities indicate P values from a one-tailed Wilcoxon's signed-ranks
test for incurrent and excurrent differences in density among all collections combined. Plankton
groups are listed in order of decreasing differences in densities between incurrent and excurrent
ends of the reef

Average number per m

Number of collections

Plankton group

Incurrent

Excurrent Incurrent < excurrent Incurrent > excurrent Incurrent = excurrent

Cladocerans

Small copepods

Larvaceans

Echinoderm larvae

Doliollds

Chaetognaths

Medusae

Large copepods

Bryozoan larvae

Fish larvae

Decapod larvae

Zoea

Ostracods

Nauplii

Polyctiaetes

1,097.2-
1,402.3ns
178.7"
54.6ns
41.8"
32.1-
39.8"
22.8*
15.5"
3.4ns
3.3ns
5.0ns
0.3—
1.0ns
0.9ns

575.7

1,114.8

60.4

15.7

9,7

16.9

25.0

9.7

4.3

1.3

2.0

4.4

0.2

1.2

1.4

0
1

0
0
0
0
0

1

0

1

0
0
0
0
0

1
1
1

'2

3

2

3

'3

'0

5

'3

'5

'1

'2

'3

■PsO.05: "Ps:0.005; ns, not significant; -
' Not present in all eight collections.

• insufficient data;

835

minor size differences between fish in incurrent
and excurrent cages (Table 5). Also, when data
were pooled among experiments to increase sam-
ple size, neither length, weight, nor volume of

FISHERY BULLETIN: VOL. 78, NO. 4

fish differed significantly between cages (f-tests,
P>0.75).

Gut fullness was greater for fish in the incurrent
cage (Table 5). Average fullness for 13 incurrent

Table 5. — Diets of blacksmith in five cage experiments at the incurrent and near the excurrent ends of Naples Reef, southern
California. Only individuals with food in their guts were included in the analyses. Fullness is defined in the text.

Experiment dates, 1977

25 July-

1 Aug.

3-12 Aug

15-22 Aug.

9-19 Sept.

11-18 Oct

Item

Incurrent

Excurrent

Incurrent

Excurrent

Incurrent

Excurrent

Incurrent

Excurrent

Incurrent

Excurrent

No. fish: with food, empty

4,0

5,0

3,0

2.1

1.1

1.1

1,1

2.0

4,0

4,0

SL(mm): x

157.8

165.0

182.7

188.5

175

150

123

121.7

100,5

958

Range

145-179

145-187

167-195

161-214

117-129

90-117

88-117

Fullness: X

0.70

0.30

0.67

0.06

1.0

0,36

1.0

0-47

0,57

0 18

Range

0.37-0.90

0.12-0.54

0.35-1.00

0.04-0.09

0.12-0,82

0,29-1 00

0 05-0,32

Food items

Average nu

imber per fish

Larvaceans

981.3

77.5

148.3

153

452

201.5

482.3

370.3

Large copepods

8.0

67

172

25

70.3

2.3

Small copepods

82.3

186.8

12.7

57

20

148

620

211.0

156.8

Cladocerans

26.0

20.4

1.0

17.8

29.0

Chaetognaths

6.7

0.5

2.3

08

Decapod larvae

0.5

1,0

10.3

0.5

Polychaetes

0.7

10

23

1.5

1.0

3,0

Fish larvae

0,5

Obelia sp.

3.5

7.5

3

Total items

1 ,089.6

289.2

176.4

7.5

287

23

795

270-0

795,0

562,7

Table 6. — Diets of free-living and caged blacksmith at the incurrent end of Naples Reef, southern

California. Fullness is defined in the text.

Collection date, 1977

29 Sept.

18 Oct

6 Dec

Item

Caged

Free

Caged Free

Caged

Free

No fish: with food, empty

3,0

5,0

4,0 5,0

3,1

4,0

SL (mm): Mean

113.7

114,8

100,5 112,2

91,3

100.3

Range

110-118

100-121

90-117 94-127

86-98

91-107

Fullness: Mean

0.34

0.73

0,32 069

0,81

0,46

Range

0.30-0.39

0.48-1 00

0,14-0,58 0,41-1,00

0,78-1.00

032-059

Food items

Average number per fish

Larvaceans

200.3

1 .904.6

482.3 805,4

561,3

865,8

Large copepods

134.0

302.2

70.3 563.6

952,7

267.0

Small copepods

102.0

321.2

211.0 397 6

295,3

615,3

Cladocerans

1.3

150.4

17.8 260

14.3

28.8

Chaetognaths

1.3

34.8

2.3 24.6

4.3

13.0

Decapods

2.7

10.2

10.3 27.8

5.3

2.3

Polychaetes

1.7

20.0

1.0 5.8

1.0

20

Total Items

444.3

2,743.4

795.0 1 ,850.8

1,834.2

1.794.2

Table 7. — Diets of free-living juvenile blacksmith collected near the incurrent and excurrent ends
of Naples Reef, southern California. Fullness is defined in the text.

Collection date. 1977

29 Sept

18 Oct.

20 Mar,

Item

Incurrent

Excurrent

Incurrent

Excurrent

Incurrent

Excurrent

No, fish: with food, empty

5,0

5,0

5,0

4,0

11,0

11,0

SL(mm): Mean

114.8

111.2

112.2

101,5

118,2

105.7

Range

100-121

85-117

94-127

85-116

101-122

98-114

Fullness: Mean

0.73

0.40

0.69

0.26

0,72

0.51

Range

0,48-1,00

0,04-0.61

0.41-1.00

0,02-0.83

0.62-0.93

0.02-0.81

Food items

Average number per fish

Larvaceans

1 .904,6

1,084.2

805,4

339.5

Not analyzed

Large copepods

302,2

107.8

563.6

18,0

Small copepods

321.2

292.8

3976

3133

Cladocerans

150.4

207.2

26,0

34,5

Chaetognaths

34.8

6.6

24.6

28

Decapod larvae

10.2

4.6

27.8

8,0

Polychaetes

20.0

8,6

5,8

1.3

Total items

2,743.4

1.711.8

1,850,8

717.4

836

BRAY: INFLUENCE OF WATER CURRENTS AND ZOOPLANKTON DENSITIES

fish, 0.70, was significantly greater than that for
the 14 excurrent fish, 0.20 (Mann-Whitney (/-test,
P<0.001).

Nine categories of food items were identified
from gut contents of caged blacksmith (Table 5).
Larvaceans and copepods predominated, while
other groups were usually rare or absent. All
items were typically planktonic except for the
sessile stage of the hydrozoan, Obelia sp., which
quickly colonized cages even though they were
scrubbed before each experiment. Obelia sp. oc-
curred in gut contents as small branches (<5 mm
long), and each was counted as one individual.
Eliminating Obelia sp. would decrease gut full-
ness for excurrent fish even more (Table 5).
Dietary variation between cages included differ-
ences in relative abundances of larvaceans and
copepods. and additions of rare items in the
excurrent cages. In the incurrent cage, larvaceans
were the most abundant food items in all experi-
ments, but in the excurrent cage, they were most
abundant in only two experiments. When present,
large copepods (>4 mm) were found mostly in
incurrent-caged fish. Though relatively few in
numbers, the size of these copepods (some nearly
10 mm long) probably made them nutritionally
important. That excurrent fish ate Obelia sp.
during three experiments is difficult to explain.
Tufts of Obelia sp. may have been more abundant
in the excurrent cages, because the excurrent
cages appeared to foul at a faster rate. Sessile
hydroids are not a normal food of blacksmith
(Hobson and Chess 1976).

Caging altered the blacksmith diets, but the
effects were variable. In two of three collections,
free fish had generally consumed more food than
caged fish (Table 6). Seven categories of food items
were identified in the guts of caged and free fish.
As before, larvaceans and copepods were by far the
most abundant. Cladocerans were abundant in a
few individuals, but chaetognaths, decapod larvae,
and polychaetes were uncommon. Free fish ate
mostly larvaceans in all of the collections, but
caged fish were inconsistent. In one collection,
caged fish ate mostly large copepods, but in the
other two, they ate mostly larvaceans.

Free-living juveniles at the incurrent end ate
more food than those at the excurrent end (Table
7). Pooled among collections, gut fullness differed
significantly between reef ends (Mann-Whitney
(/-test, P<0.05). Nonetheless, dietary compo-
sition of all free-living juveniles was similar.
Larvaceans always made up the most abundant

item, with copepods and cladocerans also common.
Numbers of small copepods were slightly less in
excurrent fish, but the difference was not nearly so
great as for larvaceans or large copepods. Num-
bers of cladocerans were greater in excurrent fish.

DISCUSSION

Blacksmith Distribution Patterns
Adults

The midwater surveys indicate that large num-
bers of adult blacksmith (>150 mm TLi swim
to the incurrent end of Naples Reef. Under the
usual current pattern of flow from the east,
almost all adults recorded were at the east end;
when currents reversed, adults were far more
abundant at the west end. During one survey,
adults were actually seen migrating to the oppo-
site end as currents reversed. The only times I saw
large numbers of adults dispersed throughout the
reef occurred when currents were negligible. On
another occasion at To yon Bay, Santa Catalina
Island (190 km southwest of Naples Reef), I saw
a similar response of blacksmith to a current
reversal.

Observations at night indicate that large num-
bers of blacksmith of all sizes take shelter in holes
at the west (usually the excurrent) end of Naples
Reef. Indeed, the density of sheltering blacksmith
at the west end may exceed that at the east
because higher rocky relief and more complex
substratum at the west end provide more refuges.
An investigation of the sheltering behavior of
tagged blacksmith indicated that many individ-
uals tend to return to the same shelter at night
(Bray in prep.). Yet when the current flowed from
the east, extensive searches throughout the entire
reef during the day failed to reveal substantial
numbers of adults anywhere but at the east end.
During the present midwater surveys, I saw one of
these tagged fish in a feeding aggregation at the
extreme eastern margin of the kelp, almost 300 m
away from the hole where it was tagged. This, and
my observation that blacksmith swam the length
of the reef when currents reversed, indicates that
some adults must swim a considerable distance
each day to gather at the incurrent end.

Juveniles

In contrast, juvenile blacksmith (<125 mm TL)

837

FISHERY BULLETIN: VOL. 78, NO. 4

apparently do not congregate at the incurrent
end. Although midwater counts were highest at
the excurrent end, bottom observations indicate
that juveniles occur abundantly throughout the
reef. Some form large stationary aggregations
about reef prominences while others are more
dispersed, hovering within a few meters of the
rocky substratum. Halfgrown fish are most abun-
dant along the reef edge, between aggregations of
adults and juveniles. To simplify the transects,
I tallied blacksmith as though they were com-
prised of two major size classes, juveniles and
adults; halfgrown fish made up but a small group
of intermediate-sized individuals that allowed
clearer distinction between these two classes.
Actually, fish sizes ranged almost continuously
from small juveniles to large adults. The degree of
fish movements vary accordingly, from very short
forays of newly settled juveniles to extensive
migrations of large adults.

Foraging at Incurrent End of the Reef

Adults

In synthesizing day and night observations of
fish residing on temperate and tropical Pacific
reefs, Hobson (1973) concluded that when fish are
active their dominant behavior is feeding, and
when they are inactive they seek security either
by schooling or by sheltering. Hobson (1972)
states, "A suitable feeding location for any given
species may or may not be near areas that offer it
suitable security during its inactive period. Con-
sequently, the major actions of these fishes char-
acteristic of twilight relate to moving between
feeding locations and shelter locations."

The most suitable foraging site for adult black-
smith, in terms of food availability, is likely at the
incurrent end of the reef. The paired caging
experiments indicated that the amount of zoo-
plankton consumed by adults at the incurrent end
was greater than the amount eaten by those over
the reef near the excurrent end. Although the
caging procedure itself did influence blacksmith
foraging, I assume the effect was similar in both
cages, so the differences in gut fullness reflected
the relative availability of food at the reef ends.

There are at least two possible reasons for the
greater food abundance at the incurrent end.
First, plankton is probably replenished there at a
faster rate. Measurements of current velocities

indicated that water crossing the reef is slowed
and deflected by rocky prominences and columns
of giant kelp. When feeding in a current, black-
smith often position themselves in areas of slack
water behind kelp while currents deliver food
(Hobson and Chess 1976). On the other hand, fish
in relatively calm water at the excurrent end may
have to swim about, possibly farther from kelp or
other shelter, to encounter food at a comparable
rate. Hobson and Chess (1976) observed that
feeding rates of blacksmith were greater in a
moderate than a slack current.

Second, the density of zooplankton is greater at
the incurrent end. Under the normal pattern of
current flow with water coming from the east,
zooplankton densities were consistently greater at
the east end of the reef. Even more convincing,
however, was the effect of current reversal; on
these two occasions, zooplankton densities were
significantly greater at the west end, with most of
the differences attributable to decreased densities
of cladocerans, small copepods, and larvaceans. I
feel that the plankton samples provided a good
measure of the abundance of the blacksmith's
potential prey because the most abundant items in
the plankton samples (copepods, cladocerans, and
larvaceans) were also the major items found in the
blacksmith guts. Also, I sampled in areas where
blacksmith normally gather in the appropriate
current conditions, and I was invariably sur-
rounded by foraging adults while I collected
plankton at the incurrent end. Although several
investigators have discussed decreased densities
of plankton in kelp beds (Limbaugh 1955; Quast
1968b; Miller and Geibel 1973; Feder et al. 1974),
to my knowledge, this is the first quantitative
documentation.

Juveniles

The incurrent end of the reef would seem to be
the most suitable foraging site for juveniles — at
least those that forage here consume more prey, as
determined by the caging experiments and exam-
inations of free-living individuals. But the sur-
veys showed that juveniles fail to concentrate
here, which indicates that other factors override
the advantages of incurrent foraging.

Optimization models may be used to inter-
pret foraging movements of planktivorous fishes
(Reese 1978). While the benefits of movements
usually involve energy gains, costs may include a
variety of factors, such as competition, expendi-

838

BRAY: INFLUENCE OF WATER CURRENTS AND ZOOPLANKTON DENSITIES

tures of time and energy, and the threat of
increased predation (e.g., Pyke et al. 1977). The
differences in foraging movements between juve-
nile and adult blacksmith may indicate that
although juveniles apparently benefit from for-
aging at the incurrent end, the cost of migrating to
and maintaining station at the incurrent end
might outweigh the benefit of greater food intake
there. Smaller fish have lower cruising speeds and
expend relatively more energy in swimming a
given distance (Bainbridge 1958, 1960), so juve-
niles sheltering at the excurrent end may find it
too costly to swim across the reef. Juveniles
already at the incurrent end may remain near the
bottom, because they find it too costly to maintain
station in strong roidwater currents. Hobson and
Chess (1976) observed that in strong currents,
blacksmith abandon open places for the lee of kelp
plants. Similarly, when currents are strong over
tropical reefs, diurnal planktivores approach the
bottom (Hobson and Chess 1978).

Predation pressures may limit the movements
of juveniles, which are vulnerable to many more
predators than are the adults. Covich (1976:242)
presented a simple graphic model that showed
how predation can influence distances traveled by
foragers if the threat of predation increased far-
ther away from shelter; he stated, "Often the risk
of predation to the forager and the distribution of
resources are the major interacting variables that
regulate consumer movement." In the tropics,
juvenile fishes remain closer to reefs than adults,
and at dusk when predation is most intense,
smaller individuals seek shelter first (Hobson
1972, 1979). Many coral reef fish seek nearby
shelter when predators approach (e.g., Hartline
et al. 1972), and relocation experiments indicate
that damselfishes released away from shelter
are quickly eaten (Mariscal 1970; Nolan 1975).
Similarly, the threat of predation might dis-
courage juvenile blacksmith from aggregating in
midwater at the incurrent end of Naples Reef.
Paralabrax clathratus ranked second in abun-
dance in my midwater surveys (Table 1), with
larger individuals tending toward the incurrent
end. Although these predators may exceed 700
mm TL (Miller and Lea 1972), they probably
would have difficulty consuming large black-
smith. However, I have observed kelp bass >400
mm TL attacking juveniles, and gut analyses
indicate they feed on a variety of small fishes,
including juvenile blacksmith (Quast 1968d; Love
and Ebeling 1978). Additional predators include

other residential as well as open-water fishes, and
marine birds and mammals.

Zooplankton Distribution Patterns
Residents Versus Nonresidents

Comparing differences in plankton densities
across a reef has often been used to estimate the
importance of plankton to the energetics of reef
communities (e.g., Johannes and Gerber 1974).
However, others have shown that inshore reefs
also contain resident zooplankters with different
habitat preferences. Many of these "demersal
plankters" form a nocturnal component that either
hides in the reef during the day and emerges at
night (e.g., Alldredge and King 1977) or resides in
deeper water during the day and moves into
shallow areas at night (Hobson and Chess 1978,
1979). Thus, as several authors have pointed out
(e.g., Alldredge and King 1977), differences in
plankton densities across a reef might reflect the
habitat preferences or patchiness of resident zoo-
plankton, rather than the consumption of extrinsic
zooplankton by fish or other reef residents.

It is doubtful that the incurrent-excurrent dif-
ferences in plankton densities at Naples Reef
resulted from sampling resident, demersal zoo-
plankton. All samples were taken around midday
in the water column away from reef or kelp
substrata. At this time, most demersal forms
hide in or near shelter or in deeper water (All-
dredge and King 1977; Hobson and Chess 1976,
1978, 1979). Furthermore, typical reef residents —
mysids, cumaceans, polychaetes, and decapods —
were insignificant components in the plankton
collections, while the groups that were consis-
tently less abundant at the excurrent end —
cladocerans and larvaceans — have not been re-
ported as residential forms. However, it would be
risky to conclude that the observed decline in
zooplankton density across Naples Reef was en-
tirely a consequence of predation by fishes and
invertebrates of the kelp-bed community. I did not
follow a specific parcel of water as it drifted across
the reef; in fact, I sampled the excurrent end of
the reef first in five of eight collections. Thus,
at least some of the differences in plankton den-
sities between the two ends may have been due to
my sampling different patches of plankton. This
would explain, e.g., the greater numbers of small
copepods at the excurrent end in one collection
(Table 4).

839

FISHERY BULLETIN. VOL. 78, NO. 4

Impact of Blacksmith Foraging

Most of the food consumed by blacksmith comes
from outside the reef community. Blacksmith
diets, of course, depend on the composition of
the plankton, but consist largely of larvaceans,
cladocerans, and copepods. The same items dom-
inate the diet of blacksmith off Santa Catalina
Island (Hobson and Chess 1976). Some copepods
may be members of the reef community (as dis-
cussed above), but the small calanoids in the
blacksmith's diet are more likely a part of the drift
plankton; residential forms probably would not
occur during the day in the exposed, current-swept
midwater areas of the incurrent end of the reef.

Too little is known about the total population
and daily food consumption of blacksmith, and
about the amount of plankton that passes over the
reef, to accurately assess the effect of blacksmith
foraging on incoming zooplankton. However, sev-
eral lines of evidence indicate that blacksmith are
major predators. The dominant items in their
diets are those that showed the greatest decrease
in abundance. Also, individual blacksmith con-
sume a large amount of food each day. The guts of
blacksmith are empty at dawn (Hobson and Chess
1976; Bray unpubl. data), so guts of individuals
collected at dusk contain food that was consumed
that day. The number of plankters in the stomach
of 14 blacksmith (124-178 mm SL) that were
speared as they sheltered at dusk averaged 1,455
items, 957c of which were larvaceans and small
copepods. And these data underestimate the total
number consumed. They exclude intestinal items,
even though these largely unidentifiable remains
weighed an average of 2.2 times the contents of
the stomach, and they ignore items evacuated
before dusk. Thus, considering that blacksmith
composed over 42% of the 7,800 fish tallied, I
conclude along with Limbaugh (1955) that they
materially affect the plankton that is swept across
southern California kelp beds.

ACKNOWLEDGMENTS

I thank Alfred Ebeling for his guidance and
support throughout this project. Many people
generously assisted me in the field, but I especially
appreciate the help of Jeff Bovee and Philippe
Vigneaud. Discussions with Tom Bailey and Ralph
Larson provided many ideas. Norm Lammer and
Jack Kisch kept the boats running. Larry Leamy
helped with the statistics, and Laurie Farmer,

Esther Escandon, and Michelle Smith assisted in
gut analyses and preparation of the final manu-
script. Alice Alldredge, Joseph Connell, and
Michael Neushul offered excellent suggestions
during the project and, along with Edmund Hob-
son and an anonymous referee, critically reviewed
earlier drafts. Finally, I thank my wife, Cindy, for
her help, encouragement, and tolerance. Finan-
cial support was provided by NOAA, Office of Sea
Grant, Department of Commerce, under grants
2-35208-6 and 04-3-158-22 (Project R-FA-14), by
NSF grants GA 38588 and OCE 76-23301, and Sea
Grants GH 43 and GH 95, all to Alfred Ebeling.
Additional funding at the University of Califor-
nia, Santa Barbara, was provided by Henry Offen,
Director of the Marine Science Institute.

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MaRISCAL, R. N.

1970. The nature of the symbiosis between Indo-Pacific
anemone fishes and sea anemones. Mar Biol. (Berl.)
6:58-65.
MILLER, D. J., AND J. J. GEIBEL.

1973. Summary of blue rockfish and lingcod life histories;

a reef ecology study; and giant kelp, Macrocystis pyrifera,
experiments in Monterey Bay, California. Calif. Dep.
Fish Game, Fish Bull. 158, 137 p.

Miller, D. J., and R. N. Lea.

1972. Guide to the coastal marine fishes of California.
Calif. Dep. Fish Game, Fish Bull. 157, 235 p.
NOLAN, R.S.

1975. The ecology of patch reef fishes. Ph.D. Thesis,
Univ. California, San Diego, 246 p.
Pyke, G. H., H. R. Pulliam, and E. L. CHARNOV.

1977. Optimal foraging: a selective review of theory and
tests. Q. Rev Biol. 52:137-154.

QUAST. J. C.

1968a. Some physical aspects of the inshore environment,
particularly as it affects kelp-bed fishes. In W. J. North
and C. L. Hubbs (compilers and editors). Utilization of
kelp-bed resources in southern California, p. 25-34. Calif.
Dep. Fish Game, Fish Bull. 139.

1968b. Fish fauna of the rocky inshore zone. In W. J.
North and C. L. Hubbs (compilers and editors). Utilization
of kelp-bed resources in southern California, p. 35-55.
Calif. Dep. Fish Game, Fish Bull. 139.

1968c. Observations on the food and biology of the kelp
bass, Paralabrax clathratus, with notes on its sport-
fishery at San Diego, California. In W. J. North and
C. L. Hubbs (compilers and editors). Utilization of kelp-
bed resources in southern California, p. 81-108. Calif.
Dep. Fish Game, Fish Bull. 139.

1968d. Effects of kelp harvesting on the fishes of the kelp
beds. In W. J. North and C. L. Hubbs (compilers and
editors). Utilization of kelp-bed resources in southern
California, p. 143-149. Calif. Dep. Fish Game, Fish
Bull. 139.
Reese, E. S.

1978. The study of space-related behavior in aquatic
animals: special problems and selected examples. In
E. S. Reese and F. J. Lighter (editors). Contrasts in
behavior. Adaptations in the aquatic and terrestrial
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SALE, R F

1971. Extremely limited home range in a coral reef fish,
Dascyllus aruanus (Pisces: Pomacentridae). Copeia
1971:324-327.

Stevenson, R. a., Jr.

1972. Regulation of feeding behavior of the bicolor damsel-
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Press, N.Y.

841

ESTIMATED INITIAL POPULATION SIZE OF THE

BERING SEA STOCK OF BOWHEAD WHALE,

BALAENA MYSTICETUS: AN ITERATIVE METHOD

Jeffrey M. Breiwick,' Edward D. Mitchell,^ and Douglas G. Chapman^

ABSTRACT

Initial stock sizes of bowhead whales were calculated iteratively, using an estimate of removals from
the Bering Sea stock of bowheads, a range of assumed values for size of current stock, and assumed
mortality and recruitment rates of M = 0.04-0.08 and "--Ml^g^ = 0.01-0.05. Estimates of initial
stock size range between 14,000 and 26,000. At a kill level of 25 per annum, time to recover to 9,000
(50% of 18,000) is a minimum of 40 years if the present stock is approximately 2,700 bowheads. A
theoretical model giving the risk of extinction is also discussed.

The International Whaling Commission has re-
cently established quotas on the aboriginal take of
the bowhead whale, Balaena mysticetus, in the
Bering, Chukchi, and Beaufort Seas. This has led
to much discussion of the status of the stock both
now and in relation to its original size.

Bowhead whales are distributed throughout the
Arctic in several presumably discrete stock units.
Tomilin (1957) recognized four circumpolar stock
units and Mitchell'* identified five. Regardless of
various interpretations, the Bering-Chukchi-
Beaufort Sea stock has been regarded by all au-
thors for many years as a discrete stock (Figure 1).

This stock winters in the Bering Sea, but during
the spring it moves through the Bering Strait
along the northwestern and northern coasts of
Alaska at least as far as the Beaufort Sea. The
Beaufort and Chukchi Seas are the main feeding
areas. For convenience we will refer to this stock
hereafter as the Bering Sea stock. This paper con-
centrates solely on this stock, for which commer-
cial exploitation began in 1848, the date to which
"initial" but not "unexploited" stock refers. Es-

'College of Fisheries, University of Washington, Seattle,
Wash.; present address: Northwest and Alaska Fisheries Center
National Marine Mammal Laboratory, National Marine
Fisheries Service, NOAA, 7600 Sand Point Way NE., Seattle, WA
98115.

^Arctic Biological Station, 555 St.-Pierre Blvd., Ste. Anne de
Bellevue, Quebec, Canada H9X 3R4.

^College of Fisheries, University of Washington, Seattle, WA
98195.

••Mitchell, E. D. 1977. Initial population size of bowhead
whale i Balaena mysticetus) stocks: cumulative catch estimates.
Int. Whal. Comm.Doc. SC 29/33, 112 p. The Red House, Station
Road. Histon, Cambridge CB4 4NR Engl.

Manuscript accepted March 1980.
FISHERY BULLETIN: VOL. 78, No. 4, 1981.

kimo utilization of bowhead whales dates back
many centuries, hence the Bering Sea stock was
subject to human influence prior to 1848.

After 1848 the Bering Sea stock was rapidly
depleted by heavy commercial exploitation — thus
following a pattern that had been established ear-
lier with respect to the Spitzbergen, Davis Strait,
and Hudson Bay stocks and which also was to
occur with the putative Okhotsk Sea stock ( Mitch-
ell footnote 4). Of all these depleted stocks, that of
the Bering Sea is now the most abundant, and the
only one from which removals of any consequence
are occurring.

There are few satisfactory estimates of current
population size for other bowhead whale stocks;
estimates of the population sizes of all stocks at the
onset of heavy commercial exploitation are even
less reliable. Accordingly, we here present one ap-
proach to verify the order of magnitude of the early
Bering Sea stock. We have also used some assumed
estimates of the vital parameters in a simulation
study of the expected time of recovery of this stock
with catches at the present level.

The basis of the method is to start with an as-
sumed current stock size and a recruitment rate,
which is a function of stock size. The same form for
the recruitment function is used throughout — a
linear function decreasing from its maximum
value at zero stock level to the natural mortality
rate, M, at the initial stock level. Given current
stock size, maximum net recruitment rate, mor-
tality rate, and lag time between birth and age at
recruitment into the fishery, the program starts
with an estimated initial (1848) level. The pro-

843

FISHERY BULLETIN: VOL. 78. NO. 4

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844

BREIWICK ET AL.: ESTIMATED INITIAL POPULATION SIZE OF BOWHEAD WHALE

gram then calculates forward and adjusts the ini-
tial level until it yields the correct (i.e., assumed)
current stock size. Current population estimates
are based on sightings and therefore are presum-
ably for the total population.

In order to reconstruct the 1848 level, it is neces-
sary to have a record of the catch history since that
time, together with a reasonable range of esti-
mates of the other parameters noted, i.e., mortal-
ity rate, maximum net recruitment rate, and cur-
rent population size. Estimated catches and other
assumed parameter values are discussed below.

the known aboriginal catch iMaher and
Wilimovsky 1963; Durham 1979) with some addi-
tions (Marquette 1976, see footnotes 5 and 6;
Mitchell footnote 4 1 and adjusted by the struck but
lost (and assumed moribund) rates estimated by
Mitchell (footnote 4). These are summarized in
Table 1 (cf. Mitchell's table 9) for the entire period
1848-1977 (see footnotes under Mitchell's table for
discussion of extrapolations and modifications to
these data).

Estimates of Current Stock Size

METHODS

Stock Size Analysis
Estimates of Initial Stock Size

Rice (1974), using data of Clark (1887), esti-
mated a Bering Sea stock size of 4,000-5,000 ani-
mals during a peak harvest from 1868 to 1884.
Mitchell (footnote 4) concluded that the period of
peak catch was earlier and, after examining
methods of extrapolating catch from production
statistics (oil and baleen yield) and catch per ves-
sel, constructed a catch history (1849-1976) based
on these estimates or on known catch. Mitchell
summed the cumulative catch for the peak decade
(1851-60), applied a loss rate of 24^ , and concluded
that a minimum population of 11,647 bowheads
existed in 1850. He then performed the same
cumulative catch summation on what he termed
the "residual stock," which had survived, and
exploitation of which had resulted in another peak
catch period in the 1880's-1890's.

In summing the two cumulative catch estimates
of population size, Mitchell corrected the latter by
subtracting from it an assumed net recruitment of
5% per year over the period between the peaks. He
concluded that the initial stock must have com-
prised approximately 18,000 bowhead whales. The
calculations discussed below are a refinement of
this rough procedure and show that this estimate
is not unreasonable.

Catch History

We have taken the best estimate of commercial
catch for each year or the known catch when avail-
able, and applied the struck but lost (and assumed
moribund) rates estimated by Mitchell (footnote
4). We have added to these commercial removals

There have been few recent surveys or counts
which give quantitative estimates of total popula-
tion abundance. Counts, e.g., from ice edge sight-
ings through the season, were made by Braham
and Krogman,'' who estimated the 1976 inshore
migration from 25 April to 2 June to include 796
animals. Breiwick and Chapman^ extrapolated
these data to account for animals that migrated
earlier than 25 April or later than 2 June and
arrived at a total population of 1,227. However, a
more complete and careftil census was carried out
in 1978, in which whales were counted in the near-
shore lead as they passed Barrow, Alaska, between
15 April and 30 May. The estimate for this compo-
nent of the population was 2,264 (Braham et al.
1979). Aerial surveys were conducted in offshore
leads and no whales were observed. In the model
below we assumed 1978 stock levels of 900, 1,500,
2,100, and 2,700 animals.

Vital Parameters

As stated above, we assume a recruitment model
with appropriate parameter values. If natural
mortality is assumed to be fixed and the net re-
cruitment rate is a linear function of stock size, the

^Marquette, W.M. 1976. National Marine Fisheries Ser\-ice
field studies relating to the bowhead whale harvest in Alaska,
1975. Processed Rep., 31 p. Natl. Mar. Mammal Lab., Natl. Mar
Fish. Serv., NOAA, 7600 Sand Pomt Way NE.. Seattle. WA 98115.

«Marquette,W. M. 1978. The 1976 catch of bowhead whales
iBalaena mysticetus) by Alaskan Eskimos, with a review of the
fishery 1973-1976, and a biological summary of the species.
Processed Rep., 80 p. Natl. Mar Mammal Lab., Natl. Mar
Fish. Serv,, NOAA, 7600 Sand Point Way NE., Seattle, WA 98115.

'Braham, H.W, and B.D.Krogman. 1977. Population biol-
ogy of the bowhead (Balaena mysticetus^ and beluga (Delphinap-
terus leucas) whales in the Bering, Chukchi and Beaufort
Seas. Processed Rep., 29 p. Natl. Mar Mammal Lab., Natl. Mar
Fish. Serv, NOAA, 7600 Sand Point Way NE., Seattle. WA 98115.

^Breiwick, J. M., and D. G. Chapman. 1977, Population
analysis of the Alaska bowhead whale stock. Int. Whal. Comm.
Doc. SC SPC 13, 5 p. The Red House, Station Road. Histon,
Cambridge CB4 4NP Engl.

845

FISHERY BULLETIN; VOL 78, NO. 4

Table l. — Estimated pelagic and Eskimo kill of bowhead whales from the Bering Sea stock.

American pelagic
Loss

fishery
KIM

Eskimo fishery

Kill

American pelagic fishery
Loss Kill

Eskimo fishery

Known

Loss

Kill

Known

Loss

Kill

Kill

Year

Catch

rate'

subtotal

kllP

rate

subtotal

total

Year

Catch rate' subtotal

kil|2

rate

subtotal

total

1848

25

0.24

31

—

0.24

0

31

1913

15 0.24 19

5

056

8

27

1849

1.061

0.24

1.316

—

0.24

0

1.316

1914

— — —

4

0.56

6

6

1850

1,061

0.24

1.440

—

0.24

0

1,440

1915

— — —

3

0.56

5

5

1851

597

0.24

740

—

0.24

0

740

1916

_ _ _

14

056

22

22

1852

1.912

0.24

2,371

17

0.24

21

2,392

1917

— — —

15

0.56

23

23

1853

1.482

0.24

1,838

7

0.24

9

1,847

1918

— — —

9

0.56

14

14

1854

1.326

0.24

1,644

—

0.24

0

1,644

1919

— — —

4

056

6

6

1855

1.315

0.24

1,631

—

0.24

0

1,631

1920

_ _ _

14

0.56

22

22

1856

1,040

0.24

1,290

—

0.24

0

1.290

1921

_ _ _

2

0.56

3

3

1857

819

0.24

1,016

—

0.24

0

1,016

1922

_ _ _

17

056

27

27

1858

975

0.24

1,209

—

0.24

0

1.209

1923

— — —

3

0.56

5

5

1859

811

0.24

1.006

—

0.24

0

1.006

1924

_ _ _

29

056

45

45

1860

549

0.24

681

—

0.24

0

681

1925

— — —

32

056

50

50

1861

412

0.24

511

—

0.24

0

511

1926

_ _ _

18

056

28

28

1862

158

024

196

—

0.24

0

196

1927

_ _ _

7

056

11

11

1863

307

0.24

381

—

0.24

0

381

1928

_ _ _

11

056

17

17

1864

364

0.24

451

—

0.24

0

451

1929

_ _ _

16

0.56

25

25

1865

348

0.24

432

—

0.24

0

432

1930

_ _ _

7

0.56

11

11

1866

551

0.24

683

—

0.24

0

683

1931

_ _ _

18

0.56

28

28

1867

569

0.24

706

—

0.24

0

706

1932

_ _ _

7

0.56

11

ir

1868

450

0.24

558

—

0.24

0

558

1933

_ _ _

5

0.56

8

8

1869

395

0.24

490

—

0.24

0

490

1934

_ _ _

4

0.56

6

6

1870

490

0.24

608

—

0.24

0

608

1935

_ _ _

6

0.56

9

9

1871

75

0.24

93

—

0.24

0

93

1936

_ _ _

10

0.56

16

16

1872

186

0.24

231

—

0.24

0

231

1937

— — —

15

0.56

23

23

1873

162

0.24

201

—

0.24

0

201

1938

— — —

11

0.56

17

17

1874

160

0.24

198

—

0.24

0

198

1939

— — —

8

0.56

12

12

1875

173

0.24

215

—

0.24

0

215

1940

_ _ _

12

0.56

19

19

1876

57

0.24

71

—

0.24

0

71

1941

_ _ _

23

0.56

36

36

1877

102

0.24

126

—

0.24

0

126

1942

— — —

11

0.56

17

17

1878

74

0.24

92

—

0.24

0

92

1943

_ _ _

7

0.56

11

11

1879

130

0.24

161

5

0.24

6

167

1944

_ _ _

2

0.56

3

3

1880

265

024

329

7

0.56

11

340

1945

— — ^

12

0.56

19

19

1881

170

0.24

211

18

056

28

239

1946

— — —

12

0.56

19

19

1882

170

0.24

211

1

0.56

2

213

1947

_ _ _

11

0.56

17

17

1883

170

0.24

211

2

0.56

3

214

1948

_ _ _

5

0.56

8

8

1884

170

0.24

211

10

0.56

16

227

1949

— — —

6

056

9

9

1885

170

0.24

211

40

0.56

62

273

1950

— — —

9

0.56

14

14

1886

170

0.24

211

—

0.56

0

211

1951

_ _ _

14

0.56

22

22

1887

170

0.24

211

11

0.56

17

228

1952

_ _ _

4

0.56

6

6

1888

170

0.24

211

3

0.56

5

216

1953

_ _ _

23

056

36

36

1889

170

0.24

211

7

0.56

11

222

1954

— — —

4

0.56

6

6

1890

170

0.24

211

2

1.00

4

215

1955

— — —

23

0.56

36

36

1891

184

0.24

228

19

1.00

38

266

1956

_ _ _

7

0.56

11

11

1892

201

0.24

249

8

1.00

16

265

1957

_ _ _

3

0.56

5

5

1893

193

0.24

239

1.00

0

239

1958

_ _ _

2

0.56

3

3

1894

118

0.24

146

13

1.00

26

172

1959

— — —

1

056

2

2

1895

70

0.24

87

4

1.00

8

95

1960

— — —

19

0.56

30

30

1896

25

0.24

31

39

1.00

78

109

1961

_ _ _

10

0.56

16

16

1897

173

0.24

215

5

1.00

10

225

1962

— — —

12

0.56

19

19

1898

21

0.24

26

27

1 00

54

80

1963

— — —

10

0.56

16

16

1899

154

0.24

191

1.00

0

191

1964

— — —

16

0.56

25

25

1900

62

0.24

77

19

1.00

38

115

1965

— — —

7

0.56

11

11

1901

11

0.24

14

1

0 56

2

16

1966

— — —

15

0.56

23

23

1902

63

0.24

78

2

0.56

3

81

1967

_ _ _

4

0.56

6

6

1903

58

0.24

72

8

0.56

12

84

1968

— — —

17

0.56

27

27

1904

44

0.24

55

3

0.56

5

60

1969

_ _ _

19

0.56

30

30

1905

41

0.24

51

7

0.56

11

62

1970

_ _ _

25

0.56

39

39

1906

5

0.24

6

6

056

9

15

1971

— — —

24

0.48

36

36

1907

58

0.24

72

9

0.56

14

86

1972

— — —

38

0.48

56

56

1908

20

0.24

25

47

0.56

73

98

1973

— — —

37

0.48

55

55

1909

28

0.24

35

25

0.56

39

74

1974

_ _ _

20

0.48

30

30

1910

6

0.24

7

2

0 56

3

10

1975

_ _ _

15

0.48

22

22

1911

72

0.24

89

4

0.56

6

95

1976

_ _ _

48

0.48

71

71

1912

0

0.24

0

3

056

5

5

1977
Total

21.823 27,068

32
1.234

111
2.025

3111

29.093

' 100% moribund in those lost.

^Includes "commercial" shore-based landings in later years.

^29 killed + recovered; 3 killed + lost; 79 struck + lost.

resulting recruitment in numbers generates a
logistic relationship. At initial stock levels the
recruitment rate is assumed to be equal to the

natural mortality rate (which includes a small
amount of exploitation mortality at the pre-1848
level). As the stock is reduced, recruitment rate

846

BREIWICK ET AL.: ESTIMATED INITIAL POPULATION SIZE OF BOWHEAD WHALE

increases proportionally, attaining its maximum
level when the stock is near zero. However, it is
also recognized that response in rate may occur
with some lag and thus various lag periods are
assumed.

In order to construct the model , various parame-
ter estimates are needed. These are discussed be-
low.

Net Recruitment Rate

Since information on the maximum net re-
cruitment rate is lacking, a range of values (0.01-
0.05) was used, based on analogy with other
baleen whale stocks for which such data are avail-
able. For example, Allen (1972) showed calculated
rates for the fin whale, Balaenoptera physalus, (as
a proportion of exploited stock) to be mostly in the
range 0.021-0.036. The Scientific Committee of the
International Whaling Commission (Interna-
tional Whaling Commission 1978) calculated
maximum gross recruitment rates for the sei
whale, B. borealis, (as a proportion of exploited
female stock) as 0.26 which implies a net recruit-
ment rate of the exploited stock to be 0.06. If we
express these rates as a proportion of the total
stock, they are in the range of 0.01-0.05. (Fur-
thermore, estimates of the 1848 stock level became
unstable and did not converge if maximum net
recruitment rates >0.05 were used in our itera-
tion.)

Natural Mortality

Similarly, there is no information available on
natural mortality in bowheads, and a range of
values of 0.04-0.08 was used. These correspond to
mortality estimates for other baleen species (Doi
et al. 1967; International Whaling Commission
1971).

Lag Time

We have no data on the growth and age of this
species, and there were no regulations in the
fishery. Nor do we have any information on the lag
that may occur between the reduction of stock
density and response of the population through its
presumed increase in recruitment. In a similar
study carried out for porpoise stocks involved in
the yellowfin tuna purse seine fishery (National
Marine Fisheries Service^), lag periods of 1, 3, and
5 yr were used. Because the population response

in larger animals might be delayed, we have arbi-
trarily tried four lag periods: 1, 3, 5, and 7 yr. As
will be shown, this parameter has minor effect.

Model Development

The assumptions outlined above can be formu-
lated in mathematical terms as follows. The re-
cruitment model is

r, =M -Kl -P^_JP )(r - M)

max'

(1)

where r^ = recruitment rate in season t

Pi__^ = population size at the beginning

of season t - t (t = lag time

assumed for population response )

Pq = initial population size (start of

1848 season)

M = natural mortality rate

(r - M)^^^ - maximum net recruitment rate.

The extrapolation model also uses the (approxi-
mate) recursion formula (Allen 1966):

Pt.i = iPt-C,)e-'' +R,

(2)

where Rf - r, Pi_^ is the gross recruitment be-
tween the beginning of season t and season ^ -^ 1.
and C„ Pt are catch in season t and population
size at the beginning of season t. A further ap-
proximation made is thate"'^= 1 -M . Equation (2)
provides a good approximation if the catching
season is relatively short and natural mortality is
low.

The iterative procedure consists of specifying a
current stock level, natural mortality rate, max-
imum net recruitment rate, and iterating on Pq
in Equation (2). Thus

Pn-S^P0'Pl'--^Pn-l^

(3)

where P„ is some current stock level. Due to the
lag time involved in Equation (2), it is not practical
to invert Equation (3) and solve for Py explicitly;
hence the iterative solution of Equation (3) is ob-
tained.

^National Marine Fisheries Service. 1976. Report of the
workshop on stock assessment of porpoises involved in the east-
em Pacific yellowfin tuna fishery. Adm. Rep. LJ- 76-29, 54 p.
Southwest Fish. Cent., Natl. Mar. Fish. Serv, NOAA. PO. Box
271, La Jolla, CA 92038.

847

FISHERY BULLETIN: VOL. 78, NO. 4

Risk Analysis

For any population there is a positive probabil-
ity of its extinction, though for most populations
this is negligibly small. However, the probability
will increase as the population size is reduced, e.g.,
by direct or indirect action of man. Such direct
action may be a harvest which is uncontrolled or
one which is controlled by fixed rules that do not
consider stochastic fluctuations in the environ-
ment.

Random fluctuations in the environment or
population which cause increased mortality or re-
duced births can lead to extinction, particularly if
the population is at a very low level. Moreover, the
longer the population is maintained there, the
greater the probability of extinction. Such risks of
extinction have for a long time been the subject of
study in population theory, but most such models
are rather simple and include only statistical
variation within the population but not externally
imposed stresses. We now develop a model that
expresses probabilities of extinction as a function
of average population growth and variability of
environmental stresses. In this model we assume
that there is an average increment for each year
but, superimposed on this, a variability of the en-
vironment which may result in the actual change
being positive or negative. We define a stochastic
process which is the sum of annual increments
which are normally distributed with mean fx and
variance <j^, and with successive increments inde-
pendent. It is knowm from the theory of stochastic
processes (c.f.. Cox and Miller 1965:58) that the
probability of the process being absorbed by bar-
riers at levels "a" above the initial value or "b"
below the initial value are equal to

1 - exp {2 ixbla-^)

and

exp(-2 fjLa/ar^) - exp{2fib/(T^)

exp(-2 fi/a^) - 1
exp(-2 /Lta/o-2) - exp(2 fx b / cr^)

respectively. If 6 is set equal to the initial value,
the second of these represents the probability of
extinction. It is difficult to specify appropriate
values for a. For example, a = 100 implies that
with 95% probability the actual increase might
vary from 200 above to 200 below the mean. Such
variations are not unreasonable in the Arctic en-
vironment. We do not know if they are this large or
not but catastrophic mortality due to ice condi-

tions has been recorded (Sleptsov 1948, as cited by
Tomilin 1957, in text but no citation given). We
have assumed that stresses are independent
events from year to year. To apply this we consider
the female population which, in a total of 2,000,
will number about 1,000. Extinction clearly occurs
if this component falls to zero. We arbitrarily have
assumed that if the female population reaches
2,000, the population is safe from extinction. If a
larger "safe" upper limit is chosen, then the prob-
abilities of extinction will be greater. It should be
noted that the level of 2,000 females (or any other
upper limit) is not an absorbing barrier in the
sense that zero, the lower limit, is. However, to
simplify the model, we have chosen a range within
which it is reasonable to assume average growth is
approximately constant — over a wider range the
growth parameter must change. Because we have
assumed constant ^t (average increment), the
probabilities of a population becoming extinct
with 1,000 females are easily computed from the
given formula for various levels of average annual
increase and various levels of environmental
stress as expressed by standard deviation.

RESULTS

Risk Analysis

The effect of the level of exploitation on the risk
of extinction is shown in Table 2. A catch of 10
whales shifts the average increase downward by
that amount; i.e., one moves one column to the left
in the table. A continuing kill of 30 whales shifts
the probabilities three columns to the left. Thus, if
present net recruitment were 50 whales and the
environmental perturbation were represented by
o- = 141.4, the probability of extinction according
to this model would be increased from 0.01 to 0.12
with a continuing 30 whale kill.

Initial Stock Size

It can be seen that the initial stock estimates are
little affected by the estimates or assumptions of

Table 2. — Probabilities of extinction for stochastic process with
normally distributed independent additive increments.

Average annual

Increase

■ M

Stress variability a-

10

20

30

40

50

60

0.7

002

—

—

—

—

—

100

12

0.02

0,002

—

—

—

141.4

,27

.12

.05

0.02

0.01

0.002

173.2

.34

.21

.12

.06

03

,02

848

BREIWICK ET AL ; ESTIMATED INITIAL POPULATION SIZE OF BOWHEAD WHALE

the current (1978) stock level given the same val-
ues of the other parameters (r - M)^^^, M, and t
(Figure 2, Table 3). Table 4 shows the initial stock
size estimates from Table 3 (1978 stock level of

2,700) reexpressed as deviations from row and col-
umn medians. The magnitude and direction of
changes in the estimates as a function of the dif-
ferent parameter combinations indicate that in-

2700

1848 1856 1864 1872 1881 1889 1897 1905 1913 1921 1929 1937 1946 1954 1962 1970 1978

SEASON

Figure 2. — Population back projections (where M = 0.06, Lag = 5 yr, ( r - M)max ~ 0.03) which would theoretically result in current
stock sizes of 900, 1,500, and 2,700 bowhead whales according to the model (see text).

Table 3. — Results of iterative solution of Equation (3). Initial stock size estimates (in thousands) for various
values of vital parameters (M, lag time, and maximum net recruitment rate) and 1978 stock level.

Lag time (yr)

1 978 stock level of 900

1978 Stock level of 1,500

1978 Stock level of 2,1 00
'^-W>max

1 978 stock leve

of 2.700

(r

-'W'max

ax

M

0.01

0.03

0.05

0.01

0.03

0.05

0.01

0.03

0.05

0.01

0.03

0.05

0.04

1

25.67

21.95

19.64

25.91

21.98

19.64

26.15

22.02

19.65

26.40

2205

19.65

.06

25.15

21.90

19.23

25.38

21.90

19.23

25.63

21.56

19.24

25.88

21.60

19.24

.08

24.62

21.41

18.82

24.86

21.44

1882

25.10

21.10

18.83

2535

21 14

18.83

.04

3

24.01

20.72

18.68

24.27

20.76

18.69

24.54

20.81

18.69

24.81

20 86

18.70

.06

22.77

19.69

17.78

23.04

19.74

17.79

23.31

19.80

17.80

23.60

1985

17.81

.08

21 61

18.73

16 93

21.89

1878

16.94

22.17

18.64

16.96

22.47

18.90

16.97

.04

5

22.56

19.63

17.83

22.84

19.69

17.84

23.13

19.76

17.86

23.43

1982

17.87

.06

20.82

18.19

16.56

21.12

1826

16.58

21.43

18.33

16.59

21 74

18.41

16.61

.08

19.29

16.90

15.42

19.60

16.98

15.44

19.92

17.11

15.57

20.25

17.16

15.49

.04

7

21.29

18.67

17.07

21.59

18.75

1709

21 90

18.83

17.11

22.22

1891

17.14

.06

19.21

16.92

15.52

19.53

17.02

15.55

1986

17.11

15.57

20.20

17.21

15.61

.08

17.44

15.43

14.18

17 78

15.54

14.22

1813

15.65

14.25

18.49

15.77

14.29

849

FISHERY BULLETIN: VOL. 78. NO. 4

Table 4.— Reexpressed stock sizes of Table 3 (1978 stock level

of2,700).

Lag
time

Row values minus medians

Column

values minus

medians

{r -,

W)max

('■-M)max

M

(yr)

0.01

0.03

0.05

Median

0.01

0.03

0.05

0.04

1

4.35

0.00

-2.40

22.05

0.52

0.45

0.41

06

4.28

.00

-2.36

21 60

.00

00

.00

08

4.21

.00

-2.31

21.14
Median

- .53

- 46

-0.41

25,88

21.60

19.24

.04

3

3.95

.00

-2.16

20.86

1.21

1.01

0.89

.06

3.75

.00

-2.04

1985

.00

.00

.00

.08

3.57

.00

-1.93

18,90
Median

-1.13

- .95

- .84

23.60

19.85

17.81

.04

5

3,61

.00

-1.95

19.82

1.69

1.41

1.26

.06

3.33

.00

-1 80

18,41

.00

.00

.00

.08

3.09

.00

-1.67

17,16
Median

-1.49

-1.25

-1.12

21.74

18.41

16.61

.04

7

331

00

-1.77

18.91

2.02

1.70

1.53

06

299

.00

-1.60

17.21

.00

00

.00

.08

272

.00

-1.48

15.77
Median

-1.71

-1.44

-1.32

20.20

17.21

15.61

creasing values of M, lag time, and maximum net
recruitment tend to decrease the estimate of ini-
tial stock size.

Vital Parameters

The natural mortality rate has somewhat less of
an effect on initial stock estimates than does the
maximum net recruitment rate. This can be seen
from Table 4 where initial stock estimates have
been reexpressed as deviations from row and col-
umn medians. As noted above, net recruitment
rates >0.05 often did not result in convergence of
the iterative procedure. In general, convergence
occurred only if fractions of animals were allowed
in Equation (2). If only integer numbers were
used, it was virtually impossible to arrive at a
prescribed stock level in 1978 from a given stock
level. This is because the time series consists of
over 100 yr, and rounding-off errors become criti-
cal if the convergence criterion is too stringent. We
assumed convergence if the difference between
two successive initial stock estimates was <0.1.

Maximum net recruitment rate and lag time are
the most sensitive of the parameters we use in the
model and natural mortality rate the least. We
have used all combinations of the range of values
of the parameters, although we recognize that cer-
tain combinations are likely to be unreasonable
(for instance, a lag time of 1 yr with a maximum
net recruitment rate of 0.01 is unlikely and there-
fore the initial stock size is unreasonable for these
parameter values).

850

Bockstoce^" examined a sample of maritime
newspapers and logbooks of whaling voyages and
estimated that 22,111 bowheads were killed by
pelagic whalers in the "commercial" fishery be-
tween 1848 and 1915. Mitchell (footnote 4) esti-
mated 27,714 whales killed in both the "commer-
cial" and the "aboriginal" fisheries during this
period. Initial stock size estimates using the data
in Bockstoce (footnote 10) for 1848-1915 and our
Table 1 for 1916-77 are about 15% lower than the
results given in Table 3.

Recovery Times

Using the basic model of Equation (2) and as-
suming that the maximum net recruitment rate
applies in the current season (assuming a popula-
tion of 1,500 and 2,700 animals), the time required
to recover to one-half of an initial stock level of
18,000 was calculated for various parameter val-
ues. These are presented in Table 5 as a ratio of
time to recover to 9,000 with a constant kill 1 5, 10,
15, 20, 25, and 30 animals) compared with the time
to recover without a kill.

If the current stock level were 1,500 animals and
the maximum net recruitment rate was 0.05, M =
0.04, time lag 3 yr, the stock would take 58 yr to
recover to a level of 9,000 with no kill vs. 75 yr with
a kill of 30/year. These numbers are increased to
94 and 153 yr, when the maximum net recruitment
rate is only 0.03 (other parameters unchanged).

DISCUSSION

We believe our model is useful but not fully
adequate. We have reservations about the data
used, limitations of the model, and aspects of the
fishery that we did not have time or data to
adequately address.

Limitations of the Data

The commercial catch data are based mainly on
extrapolations of a consistent number of whales
caught per ship. The statistics for the number of
vessels operating in the bowhead fishery compo-
nent of the North Pacific Ocean are also subject to

'"Bockstoce, J. 1978. A preliminary estimate of the reduc-
tion of the western Arctic bowhead whale iBalaena mysticetus)
population by the pelagic whaling industry: 1848-1915. Report
submitted to U.S. Marine Mammal Commission, Washington,
D.C. Available U.S. Dep. Commer., Natl. Tech. Inf Serv.,
Springfield, VA 22161, as PB-286-797.

BREIWCK ET AL : ESTIMATED INITIAL POPULATION SIZE OF BOWHEAD WHALE

TABLE 5— Estimated recovery times for Bering Sea bowhead whale stock. Recovery time is that calculated with the
parameters indicated, assuming zero kill. The relative increases in recovery time that occur with various levels of
constant kill are tabulated in the last six columns.

Assumed current

Lag time used
in model

{r - /W)^a^ M

Recovery time
(yr) to 9,000

Annual kill

stock level

5

10

15

20

25

30

1,500

3

0.01 0.04

273

1.22

1.63

(')

_

08

302

1.21

1.58

_

.03

04

94

106

1.14

1.22

1.33

1.46

1.63

08

104

1.06

1.13

1.20

1.30

1,41

1.57

.05

04

58

1.05

1.09

1.12

1 17

1,22

1.29

08

64

1.03

1.06

1.11

1.16

1.20

1.27

7

.01

04

315

1.22

1.63

—

__

08

381

1.21

1.58

—

.03

04

110

1.06

1 14

1.22

1.33

1.45

1.63

08

131

1.06

1.13

1.21

1,31

1,43

1.59

.05

04

69

1.03

1.07

1.12

1.16

1,22

1.28

08

81

1.04

1.07

1.12

1.16

1,21

1.27

2,700

3

.01

04

197

1.16

1.39

1 75

2.45

—

08

218

1.15

1.36

1.69

2.28

.03

04

68

1.04

1.09

1.15

1.22

1.29

1.38

08

74

1.05

1.09

1 16

1 22

1,28

1.36

.05

04

42

1.02

1.05

1.07

1.12

1,14

1.19

08

46

1.02

1.04

1.09

1.11

1,13

1.17

7

.01

04

226

1.16

1.39

1.74

2.45

08

274

1.15

1.36

1.69

2.28

—

.03

04

78

1.05

1.10

1 15

1.22

1,29

1.38

08

93

1.04

1 10

1.15

1.22

1,29

1.37

.05

04

48

1.04

1.06

1.08

1.13

1,17

1.21

08

57

1.04

1.05

1.09

1.12

1.16

1.19

'Stock goes to zero.

much interpretation (Mitchell footnote 4), but at
least the extrapolations will approximate true
trends.

The aboriginal catch data for some years may
represent only the minimum landed catch. The
pre-1960 aboriginal catch fluctuates from 0 to 47
(1908) per annum, where presently known. From
1978 back to 1854 there are many years for which
no data were recorded or obtainable. Also, for
many years for which data are available, the num-
bers given may not represent the true total landed
catch. In our analysis, these unrecorded kills have
implications only for the data from 1908 or 1912,
near the end of the commercial pelagic fishery
when the aboriginal catch begin to represent the
majority of the total catch. However, during the
much earlier period of high commercial catches,
the aboriginal catch composed a small percentage
of the total ( 59c or less of the pelagic catch at its
highest). Thus any analysis of recovery patterns
dependent upon the post-1900 data is entirely de-
pendent upon the completeness of the aboriginal
catch. Since few contemporary written records
have been kept and continued library research
yields new figures for given years, the aboriginal
catch must be regarded as minimum and provi-
sional.

Limitations of the Model
All models with published results previously

used on whale populations have been applied to
odontocetes, balaenopterids, or eschrichtiids, but
not to balaenids. Because we are dealing with a
separate zoological family (much older than the
balaenopterids and apparently different in many
behavioral features), caution should be used when
applying balaenopterid vital parameter values, by
analogy, to the balaenid model. No other reason-
able estimates are available, however.

Although the model (Equation 2) used to esti-
mate initial abundance is relatively simple, it does
account for fishing and natural mortality and re-
cruitment as a function of the time-lagged popula-
tion size. It is quite possible, though, given the 130
yr we are considering, that the natural mortality
rate has changed. Such a change, if it has oc-
curred, probably would have had a relatively small
effect on the initial stock estimates. We have also
not considered the effect of a differential sex ratio
in the large pelagic catches, which could have re-
sulted in the 1912 population consisting of (in the
worst possible cases) mostly males, mostly old
females of low fertility, or young animals of either
sex.

Although Figure 2 shows a minimum popula-
tion size occurring around 1912, we have not calcu-
lated the minimum size the population might have
declined to, for the following reasons: assumptions
that the population was much smaller then land
has appreciably recovered) cannot be proven, and
represent only one alternative explanation of the

851

FISHERY BULLETIN: VOL. 78, NO. 4

history of the fishery and of the population since
the early 1900's. For example, we do not know how
the 1912 population was structured. If, as seems
likely with high prices for baleen, selection mainly
for large animals with long baleen occurred near
the end of the fishery, then the remnant population
might have comprised a large proportion of young
animals. The 1977 population might represent a
considerable proportion of this 1912 population,
now old, and we would know little about net re-
cruitment or failure thereof.

The most difficult parameter to estimate in any
whale population is the recruitment rate. In the
absence of better knowledge, we have used a sim-
ple linear model and specified a range of maximum
net recruitment rates. Given that the recruitment
rate function varies between some maximum
value at stock level near zero and M at Pq, the
shape of the curve has less effect than the value of
(r- M)j^3^. During the early history of the fishery,
catches exceeded recruitment, and during the last
half-century the stock was at a relatively low
level. Thus, the recruitment rate was close to its
maximum and varied little. A further study could
consider the effect of a dome-shaped recruitment
curve.

Given our results, it appears likely that stock
size between 1910 and 1978 was probably <10% of
the initial stock level. According to most classical
models used with baleen whale populations, the
net recruitment should have been near its
maximum for about the last 60 yr. Because the
population does not appear to have grown substan-
tially since then, either the recruitment rate has
been low or the kills have been higher than cur-
rently estimated. It is also possible that the
catches during the last half-century represent
survivors of the then young animals.

Aspects of the Fishery

We may have to consider very low net recruit-
ment rates because the changing nature of the
fishery suggests that, as the worst case, the whalers
efficiently decimated a structured population suc-
cessively over its geographic range. The argument
is as follows: females with calves migrate farther
north (later, in the migration stream) and also
inhabit ice fields. They might not have been as
available to the early fishery, 1850-ca. 1870's,
which used sailing vessels at the ice edge and
which was mainly a midsummer to late season
fishery. The greatest removals were during this

time and for a short period. Subsequently, with the
development of steam whaling, overwintering of
the fleet became possible, and heavy fishing oc-
curred in the ice fields at all times. The fishing
season was effectively increased in length between
the 1880's and 1910's. (Even if the population were
not so structured by sex or age, the present spring
and summer distribution is confined to a much
smaller area compared with the data of Townsend
(1935).)

Due to the unique geography, stratification, and
timing of this fishery, the possibility exists that
once the stock is fished to some low level, recruit-
ment failure could occur and that net recruitment
since about 1900 could indeed be as low as 0.01, the
minimum figure used in our calculations.

Any subsequent analysis of annual catch and
effort data (e.g., including number of vessels, etc.)
should consider changing technology. The fishery
changed radically from one of a sailing vessel-ice
edge-early season fishery to a steam vessel-ice
pack-nearly year round fishery. The best measure
of change in effort between sailing and steam ves-
sels to catch the same number of whales might be
the monthly duration of the respective voyages.

ACKNOWLEDGMENTS

We thank M. F. Tillman, D. W Rice, and V M.
Kozicki for critically reading the manuscript. G.
Ferrand drafted Figure 1. J. M. Breiwick acknowl-
edges support under contract MM8AC007 from
the U.S. Marine Mammal Commission.

LITERATURE CITED

Allen, K. R.

1966. Some methods for estimating exploited popula-
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D. RuGH, M. Tillman, J. Johnson, and G. Carroll.

1979. Preliminary report of the 1978 spring bowhead
whale research program results. Rep. Int. Whaling
Comm. 29:291-306.

Clark, A. H.

1887. Part XV The whale fishery. 1. — History and present
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Wash., D.C.

Cook, J. A.

1926. Pursuing the whale. A quarter-century of whaling in
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Cox, D. R., AND H. D. Miller.

1965. The theory of stochastic processes. Wiley, N.Y,
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852

BREIWICK ET AL.: ESTIMATED INITIAL POPULATION SIZE OF BOWHEAD WHALE

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1967. Population assessment of sei whales in the Antarc-
tic. Nor. Hvalfangst-Tidende. 56:25-41.

DURHAM, F. E.

1979. The catch of bowhead whales iBalaena mysticetus)
by Eskimos, with emphasis on the western Arctic. Con-
trib. Sci., Nat. Hist. Mus. Los Ang. Cty. 314, 14 p.

INTERNATIONAL WHALING COMMISSION.

1971. Report of the special meeting on Antarctic fin whale
stock assessment. Rep. Int. Whaling Comm. 21:34-39.

1978. Report of the scientific committee. Rep. Int. Whal-
ing Comm. 28:38-129.

MAHER, W J., AND N. J. WILLMOVSKY.

1963. Annual catch of bowhead whales by Eskimos at
Point Barrow. Alaska, 1928-1960. J. Mammal. 44:16-
20.

MARQUETTE. W M.

1976. Bowhead whale field studies in Alaska, 1975.
Fish. Rev. 38(8):9-17.

Mar.

RICE, D. W

1974. Whales and whale research in the eastern North
Pacific. In W. E. Schevill (editor). The whale problem: a
status report, p. 170-195. Harv. Univ. Press, Camb., Mass.

Sergeant, D. E., and W Hoek.

1974. Seasonal distribution of bowhead and white whales
in the eastern Beaufort Sea. In J. C. Reed and J. E. Sater
(editors). The coast and shelf of the Beaufort Sea, p. 705-
719. Arctic Inst. North Am., Arlington. Va.
TOMILIN, A. G.

1957. Z veri SSSR i prilezhashchikh stran ( Mammals of the
U.S.S.R. and adjacent countries). Kitoobraznye
(Cetacea). Vol. IX. Izd. Akad. Nauk SSSR, Moskva, 756
p. (Translated by Isr Program Sci. Transl.. 1967, 717 p.;
available Natl. Tech. Inf. Serv., Springfield, Va., as TT
65-50086.)
Townsend. C.H.

1935. The distribution of certain whales as shown by log-
book records of American whaleships. Zoologica (N.Y.)
19, 50 p.

853

SPAWNING BIOMASS AND EARLY LIFE OF NORTHERN ANCHOVY,

ENGRAULIS MORDAX, IN THE NORTHERN SUBPOPULATION

OFF OREGON AND WASHINGTON

Sally L. Richardson ^

ABSTRACT

A major spavming center for the northern subpopulation of northern anchovy, Engraulis mordax. is
documented off the Oregon-Washington coast beyond the contmental shelf, based on collections of
planktonic eggs in July 1975 and July 1976. Biomass estimates of northern anchovy in this spawning
concentration ranged from 262,506 to 769,511 metric tons in 1975 and 144,654 to 1,005,263 metric tons
in 1976, based on egg and larva surveys. Spawning biomass was estimated to be 800,000 metric tons in
1977, based on an acoustic survey of adults. The most probable biomass may be more than 100,000 but
less than 1,000,000 metric tons. Potential yield estimates ranged from 86,792 to 633,316 metric tons,
but realizable yields may be considerably lower if management strategies applied to northern anchovy
in the central subpopulation are implemented for the northern subpopulation.

Spawning appears to be associated with waters of the Columbia River plume which may provide
favorable conditions, in terms of stability and productivity for survival of first feeding northern
anchovy larvae. Evidence of larval transport south away from the spawning center leads to questions
about return mechanisms to explain the occurrence of juveniles in Oregon bays and rivers later in the
season. Additional spawning centers within the range of the northern subpopulation have not been
documented although some evidence from the literature indicates another spawning center may occur
in the Strait of Georgia, British Columbia, around the Fraser River plume.

Conditions related to spawning differ between the northern and central subpopulations. Off Oregon,
spawning occurs from mid- June to mid-August, when current flow to the south is at a maximum, water
temperatures are reaching maximum levels for the year, coastal upwelling is at a maximum, and day
length is at or near maximum duration. Off California, peak spawning occurs from January through
April when southward current flow is minimal, water temperatures are reaching minimal levels for the
year, upwelling is minimal, and day length is at minimum duration. These factors are indicative of
some degree of reproductive isolation as well as differing reproductive strategies between the two
subpopulations.

The northern anchovy, Engraulis mordax Girard,
is an abundant pelagic schooling fish that occurs
along the west coast of North America from Cape
San Lucas, Baja California, to the Queen Char-
lotte Islands, British Columbia (Miller and Lea
1972; Hart 1973). It is the object of an expanding
fishery off central and southern California and
Baja California where about 204,000 metric tons
(t) were harvested in 1975, mainly for fish meal
(Pacific Fishery Management Council ). In the
northern part of its range it is utilized only to a
small degree as bait by local fishermen although
its potential as a harvestable resource has been
suggested (Pruter 1966, 1972). Reports of dense
schools off the Oregon and Washington coasts in-

'School of Oceanography, Oregon State University, Corvallis,
Oreg.; present address: Gulf Coast Research Laboratory, East
Beach Drive, Ocean Springs, MS 39564.

^Pacific Fishery Management Council. 1978. Northern an-
chovy fishery management plan. U.S. Dep. Commer, NOAA
Federal Register 43(141) Book 2:31651-31783.

Manuscript accepted March 1980.
FISHERY BULLETLN: VOL. 78, NO. 4, 1981.

dicate northern anchovy biomass may be substan-
tial (Pruter 1966, 1972). Estimates of an annual
consumption of 28,000 t of northern anchovy by
four species of marine birds off the Oregon coast
(Wiens and Scott 1975) further indicates sizeable
biomass.

In the absence of a fishery, biomass estimates
are unavailable for northern anchovy north of
California. We know that in the 1940's northern
anchovy in ocean waters adjacent to the Columbia
River supported a live bait fishery for albacore
tuna (Pruter 1966, 1972). Reported commercial
landings of northern anchovy in Washington in
1947-49 ranged from 20 to 182 1 annually and were
28 and 76 t in Oregon in 1948 and 1953 (Pruter
1966). A small purse seine fishery for canning once
existed around southern British Columbia where
harvests ranged from 64 to 6,201 t annually be-
tween 1939 and 1947 (Roach and Harrison 1948;
Pike 1951).

855

FISHERY BULLETIN: VOL 78. NO. 4

Because of the relatively unfished state of
northern anchovy off Oregon and Washington, the
lack of biomass estimates, and the potential for
fishery development, this study was undertaken to
define spawning centers and provide the first pre-
liminary estimates of spawning biomass within
such defined spawning centers by means of
ichthyoplankton survey. Additional information
on adult school distributions and another inde-
pendent estimate of biomass were obtained by
acoustic survey (Smith ). Ecological data on the
early life of these northern occurring fish were
also examined. Aspects of adult life history, par-
ticularly reproduction, are presented in a separate
paper (Laroche and Richardson 1981).

THE NORTHERN SUBPOPULATION

Northern anchovy occurring north of Cape
Mendicino, Calif., compose the northern subpopu-
lation of E. mordax, one of three subpopulations
(Figure 1) distinguished on the basis of meristic
counts (McHugh 1951) and electrophoretic separa-
tion of blood serum protein (Vrooman and
Paloma ). The central subpopulation occurs
primarily off southern California and northern
Baja California and the southern subpopulation is
off central and southern Baja California. A sepa-
rate subspecies, E. mordax nanus, has also been
described from San Francisco Bay (Hubbs 1925).

Compared with the central and southern sub-
populations, relatively little detailed information
is available on spawning and early life history of
northern anchovy in the northern subpopulation.
Off California and Baja California spawning sea-
sons and locations are well defined (e.g., Ahlstrom
1966, 1967; Baxter 1967; Kramer and Ahlstrom
1968), eggs and larvae have been illustrated ( Bolin
1936; Ahlstrom 1956, 1965; Kramer and Ahlstrom
1968), and spawning biomass has been estimated
on the basis of larva survey (e.g., Pacific Fishery
Management Council footnote 2).

For the northern subpopulation, information on
spawning and early life history had to be pieced
together from a number of sources to provide the
background for the present study. Based on
monthly plankton collections of larvae off Oregon

^P E. Smith, Southwest Fisheries Center La Jolla Laboratory,
National Marine Fisheries Service, NOAA, RO. Box 271, La
Jolla, CA 92038, pers. commun. March 1978.

"Vrooman, A. M., and R A. Paloma. 1975. Subpopulations
of northern anchovy, Engraulis mordax Girard. NOAA NMFS
Southwest Fish. Cent., Admin. Rep. No. LJ-75-62, 10 p.

^-\

^^^

^ BRITISH

50'

-^^^

^, COLUMBIA

1

^^<0> 5//-(7/y of Georgia

^b dui

^'■■" WASHINGTON

y y^olumbia River

45"

y Tillamook Bay

^aqumo Bay qREGON

-^Coos Bay

/^Humboldt Bay

Northern

40'

\

'^.; CALIFORNIA
p^Son Franc/SCO
V/O Monferey

35'

- \

V vVy^'3'^"^'"' Pedro

30'

- '"""\ ^^\

\ ^^\i

25'

Southern V^ ^>

125'

120°

115'

110'

Figure l. — Geographic ranges (hatched) of the three subpopu-
latiiSns (northern, central, southern) of Engraulis mordax (mod-
ified from Smith and Lasker in press). Rectangular area outlined
off Oregon and Washington shows ichthyoplankton survey grid
boundaries for this study. Rectangular area outlined off Califor-
nia and Baja California shows approximate boundaries of the
principal portion of the CalCOFI survey grid (after Kramer et al.
1972).

(Richardson 1973, see footnote 5; Richardson and
Pearcy 1977) and maturity studies involving mea-
surements of ova diameters from ovaries of fish
collected off British Columbia (Pike 1951), the
spawning season is short, lasting from about
mid-June to mid-August. Based on available catch
records ( Williamson 1929 [in Pike 1951]; Pike 1951;

^Richardson, S. L. 1977. Larval fishes in ocean waters off
Yaquina Bay Oregon: abundance, distribution, and seasonality
January 1971 to August 1972. Oreg. State Univ. Sea Grant Coll.
Prog. Publ. No. ORESU-T-77-003, 73 p.

856

RICHARDSON: SPAWNING BIOMASS AND EARLY LIFE OF NORTHERN ANCHOVY

Parsons et al. 1970; Eldridge and Bryan 1972;
Blackburn 1973; Richardson 1973, footnote 5, un-
publ. data; Pearcy and Myers 1974; Laroche 1976;
Misitano 1977; Richardson and Pearcy 1977;
Waldvogel 1977; Robinson ; Cummings and
Schwartz'; Forsberg et al. ) spawning locations
have not been well defined and data are somewhat
contradictory. Before the present study, running
ripe adults had never been collected. Two nearly
ripe females were taken in coastal waters around
British Columbia; one ripening female was taken
in Tillamook Bay in northern Oregon; and large
numbers of ripening adults had been found in
Humboldt Bay in northern California (Figure 1).
Interestingly, the ripening fish in Humboldt Bay
leave in June or July and return again in fall in a
spent condition. Planktonic northern anchovy
eggs had been reported only from certain inlets of
Vancouver, British Columbia, in Puget Sound,
Wash., off the Columbia River mouth, and in
Yaquina Bay, Oreg. Small ( <10 mm) planktonic
larvae had been rarely taken in areas where ripen-
ing adults or planktonic eggs had been found.
Small numbers of these larvae had been reported
only from Yaquina Bay and Humboldt Bay. Large
concentrations of small larvae had been reported
only from ocean waters off Oregon. Larvae ^10
mm had been taken in small numbers in the Strait
of Georgia, British Columbia, inside the mouth of
the Columbia River, in Yaquina Bay, and in Hum-
boldt Bay. As with small larvae, large concentra-
tions had been found only off the Oregon coast.
Juveniles ^35 mm had been taken in ocean waters
off Oregon as well as in the Strait of Georgia,
British Columbia; Puget Sound, Wash., inside the
Columbia River mouth; in Tillamook Bay, Yaquina
Bay, and Coos Bay, Oreg.; and in Humboldt Bay,
Calif. Juveniles taken offshore were usually <50
mm while most of those in bays and sounds were
>50 mm.

These data, and particularly the earlier study
by Richardson (1973), indicated the possible exis-
tence of a spawning concentration of northern an-
chovy within the northern subpopulation located

«F{obinson, D. G. 1969. Data record. Number, size composi-
tion, weight and food of larval and juvenile fish caught with a
I two-boat surface trawl in the Strait of Georgia July 4-6,
' 1967. Fish.Res. BoardCan.,ManuscrRep. SerNo. 1012,71p.
"Cummings, E., and E. Schwartz. 1971. Fish in Coos Bay,
Oregon, with comments on distribution, temperature, and salin-
ity of the estuary. Oreg. Fish. Comm., Res. Div., Coastal Rivers
Invest. Inf Rep. 70-11, 22 p.

sForsberg, B. O., J. A. Johnson, and S. M. Klug. 1976. The
identification, distribution, and notes on food habits offish and
shellfish in Tillamook Bay Oregon. Oreg. Dep. Fish Wildl., Res.
Sect., Fed. Aid Prog. Rep.: Fish., Feb. 1974-June 1976, 117 p.

off the Oregon-Washington coast. Richardson
suggested spawning might be associated with the
Columbia River plume. The present study was de-
signed to test that hypothesis and to estimate the
biomass of spawning adults located therein.

METHODS

Field Procedures

Standard ichthyoplankton surveys (Smith and
Richardson 1977) were conducted off the
Oregon-Washington coast in the region outlined in
Figure 1. This survey area was designed to border
at least the inner bounds of the Columbia River
plume. Cruises were conducted at the presumed
time of peak spawning in mid-July: 10-18 July
1975 and 7-15 July 1976.

A grid of 70 stations along seven east-west
transects (Figure 2) was sampled. Stations ex-

128°

i27»

\2e,'

46'

42'

232 157 83 28 2], ^""""^

269

194

120

128°

127°

126°

Figure 2.— Ichthyoplankton survey grid with 70 cm bongo net
sampling stations occupied in July 1975 and July 1976 off Oregon
and Washington. Numbers on upper transect represent kilome-
ters from the coast and apply to all seven transects.

857

FISHERY BULLETIN: VOL. 78, NO. 4

tended from 2 to 269 km offshore and covered a
north-south distance of 450 km. Transects were
74 km apart and stations on a transect were 46
km apart except the most inshore stations which
were closer together. The grid covered an area of
120,150 km2.

Oblique 70 cm bongo net tows were made at each
station from 150 m ( or just above the bottom ) to the
surface. Vessel speed was 2-3 knots and retrieval
speed was 20 m/min. The bongos were fitted with
0.333 and 0.571 mm mesh Nitex^ nets, TSK flow-
meters and a time-depth recorder. Stations were
occupied when the ship arrived, day or night.
Samples were preserved in 107r buffered Formalin.

Temperature, salinity, and chlorophyll were
monitored at 3 m depth every 9 km along each
transect using a flow-through fluorimeter system
(AMINCO Fluro-colorimeter). At each bongo sta-
tion a bathythermograph cast was made to 140 m
depth (or 5 m above the bottom) and a surface
bucket temperature was recorded. During the
July 1976 cruise, surface drifters, consisting of a
labelled plastic tag made buoyant with Styrofoam,
were released to provide information on surface
water movement. Fourteen drifters were dropped
at each bongo station except on the southernmost
transect (lat. 43°00' N) where only 10 were re-
leased at the 120 km station and none at the 157,
194, 232, and 269 km stations.

Between 18 and 25 July 1977 an acoustic survey
was conducted cooperatively by the National
Marine Fisheries Service (NMFS) in the same
area as the previous ichthyoplankton surveys
(Smith ). The same seven transects plus an
eighth transect to the south along lat. 42°20' N
were surveyed acoustically during daylight using
the methods of Smith (1970). Distance covered on
each line extended from the 91 m depth contour
westward 167 km. In addition to the acoustic work,
temperature and salinity at 3 m depth were moni-
tored every 9 km using a flow-through salino-
graph, and expendable bathythermographs were
cast every 9 km on every other transect. Following
a day's sonar run, nighttime surface trawls were
made with a 40 m modified Cobb pelagic trawl
(Smith footnote 10) on the latter half of the sonar
track in areas of biological aggregations identified

and measured by sonar. Standard oblique 60 cm
bongo tows (Smith and Richardson 1977) were
made at each trawl station from 70 m to the sur-
face. Samples were processed at sea using Cal-
COFI (California Cooperative Oceanic Fisheries
Investigations) techniques (Kramer et al. 1972)
except that the 0.333 mm mesh samples were
preserved in ethyl alcohol for special studies
(Methot").

Laboratory Procedures

Plankton volumes for each 0.333 mm mesh
bongo sample from the 1975 and 1976 cruises were
determined by displacement (Kramer et al. 1972),
and northern anchovy eggs and all fish larvae
were sorted. Northern anchovy eggs were enu-
merated. Measurements of long and short axes of
eggs were made on selected samples using an ocu-
lar micrometer in a stereomicroscope. Northern
anchovy larvae were identified, enumerated, and
measured in 0.5 mm size classes using a plastic
rule beneath a glass slide. The 0.333 mm mesh
bongo samples only from the 1977 cruise were pro-
cessed by personnel from Scripps Institution of
Oceanography and the NMFS Southwest
Fisheries Center according to techniques de-
scribed by Kramer et al. (1972). Numbers of eggs
and larvae in each sample were standardized to
the number under 10 m^ sea surface (Smith and
Richardson 1977):

C, = 10 {a;^b;^c,d,)

(1)

where C, = number of eggs or larvae beneath
10 m^ sea surface at station i

a = mouth area of the bongo net used at
station i in square meters

b = length of tow path in meters estimat-
ed from a calibrated flowmeter at
station i

c = number of eggs or larvae in the ith.
sample

d = maximum depth of tow in meters.

Egg and Larva Census Estimates

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

'"Smith, RE. 1977. Cruise report,^^ David Starr Jordan,
7705(111), Mordax North, Leg A, 13-27 July 1977. Rep. dated 5
December 1977. On file at National Marine Fisheries Service
Southwest Fisheries Center, EO. Box 271, La Jolla, CA 92038.

Census estimates (i.e., estimates of the total
number of northern anchovy eggs and larvae in

"R.D.Methot, Scripps Institution of Oceanography, Graduate
Department, La Jolla, CA 92093, pers. commun. July 1977.

858

RICHARDSON; SPAWNING BIOMASS AND EARLY LIFE OF NORTHERN ANCHOVY

the area represented by the survey grid during
each cruise in 1975 and 1976) were determined by
two methods, the Sette and Ahlstrom Census and
the Smith Census. The Sette and Ahlstrom Census
was the polygon method of Sette and Ahlstrom
( 1948) in which the number of individuals under 10
m^ sea surface at each station was weighted by the
area represented by the station. These areas are
polygons formed "by constructing perpendicular
bisectors of lines drawn from the station to each of
all surrounding stations" (Sette and Ahlstrom
1948). The census estimate is then:

10

n
V

(a, b, c,d,)

(2)

where Cf, = estimate of abundance of eggs or lar-
vae during cruise k
A, = area of a polygon constructed of per-
pendicular bisectors of lines be-
tween station / and all adjacent
stations
n = number of stations.

Polygon areas, determined by planimeter, ranged
from 0.38 to 2.89 x 10^ m^ but were >2.00 x lO^ m^
for all stations 46 km or more from the coast.

The Smith Census was the "regional census es-
timate" of Smith (1972):

Ckr = 10 A,n' 1 (a;'b;\,d,) (3)

1=1

where C^^ = estimate of abundance of eggs or lar-
vae in region r during cruise k
Ar - area of region r in numbers of 10 m^
areas ( in my study,

10 A, = 2 A, = 148.81 X lO^m^).
1=1

Spawning Biomass Estimates

Four methods were used to estimate spawning
biomass, three based on egg census estimates
(Sette and Ahlstrom Egg Method, Simpson Egg
Method, Saville Egg Method) and one based on
larva census estimates (Smith Larva Method).
The use of three egg methods generally follows the
approach of Houde (1977) in estimating spavniing
biomass of round herring, Etrumeus teres. Be-
cause the shape of the egg production curve
throughout the spawning season is unknown for
northern anchovy, the use of these three egg
methods takes into account the range of pos-
sibilities (discussed below) for comparative pur-
poses.

All three egg methods ultimately use the same
formula (Saville 1964) to estimate spawning
biomass:

Es
^ - KF

(4)

where B = biomass of spawning adults

Eg = total number of eggs spawned during
a season, i.e., seasonal egg produc-
tion. (This estimate varies accord-
ing to the egg method used as de-
scribed below.)
K = the proportion of spawning adults
that are females. [In this paper the
overall sex ratio of E. mordax is
assumed to be 1:1 following Smith
(1972) and Klingbiel (1978).]
F = mean fecundity, i.e., the number of
eggs produced per gram of female
per spawning season. [The mean
fecundity of E. mordax in the
northern subpopulation off Ore-
gon is estimated to be 720 ova/g
total weight female (Laroche and
Richardson 1981).]

The Smith Census method can be less tedious than
the Sette and Ahlstrom Census method if the area
represented by the survey can be determined in a
gross manner, i.e., without planimetry. Values of
the Smith Census in my study were always lower
than those of the Sette and Ahlstrom Census. The
Smith Census was computed here primarily to
allow for comparison with CalCOFI data (Smith
1972; Pacific Fisheries Management Council foot-
note 2).

The number of eggs spavined in a season {E^) was
estimated by three methods, each using the two
egg census estimates described above.

The Sette and Ahlstrom Egg Method of estimat-
ing seasonal egg production (£■>,) follows the ap-
proach of Sette and Ahlstrom (1948).

Es -

N

1

1 = 1

or

^ CkrD,

.=1 t,

(5)
859

FISHERY BULLETIN: VOL 78. NO. 4

where N = number of cruises in a season

Z), = number ofdays represented by cruise
i. [Sette and Ahlstrom (1948) de-
fined this to be the days included
in the cruise plus one-half the days
since the previous cruise and one-
half the days to the next cruise; in
this study only one cruise was
made during the spawning season
and the niunber ofdays represent-
ed by the cruise was taken to be
the entire spawning season. Dura-
tion of the spawning season for
E. mordax off the Oregon-Wash-
ington coast was estimated from
monthly or bimonthly collections
of larvae taken off Oregon in 1969,
1971, and 1972 (Richardson 1973,
footnote 5, unpubl. data; Richard-
son and Pearcy 1977). The earliest
that northern anchovy larvae
were taken in those years was 19
June and the latest that small lar-
vae (<10 mm) were collected was
10 August. Peak abundance, >100/
10 m2 or >1, 000/1,000 m^ at a
station, occurred only between 21
July and 6 August. The spawning
season was estimated to last ap-
proximately from 15 June to 15
August, or 62 days.]
ti = the time in days from spawning to
hatching of the egg determined
from the equation given by Zweifel
and Lasker (1976) for incubation
times for northern anchovy:

It = hexp [mil - exp( -ftT))]

(6)

where Iq - 1861

m = -5.4572
13 = 0.0626

T = the mean temperature at 3 m depth
at stations where northern an-
chovy eggs were taken, 15.18° C
in 1975 and 16.09° C in 1976.

The Sette and Ahlstrom Egg Method assumes a
constant egg production throughout the spawning
season.

The Simpson Egg Method of estimating the
number of eggs spawned in a season (Eg) was that
given by Simpson (1959) as modified by Houde

(1977). The cruise census estimate, C^ or C^r, was
used to determine the number of eggs produced per
day during the spawning season

E.

or

^kr

(7)

where E^ — daily egg production

t, is defined under Equation (5).

The seasonal estimate of egg production (Es)
was then determined by plotting the daily egg
production against the middate of the cruise rep-
resentative of the spawning season. The area
under the resulting polygon (triangle in this case),
determined by planimetry, was then equated with
egg production for the entire spawning season.
This method assumes a high egg production mid-
season tapering off to low production at the begin-
ning and end of the spawning season. It ap-
proaches a normal distribution of egg production.
For species with a short spawning season as in
northern anchovy off Oregon and Washington, es-
timates obtained by this method are about one-
half as large as those obtained by the Sette and
Ahlstrom Egg Method.

The Saville Egg Method of estimating seasonal
egg production {Eg) is based on Saville's (1956,
1964) approach. It assumes that egg production
follows a normal distribution throughout the
spawning season. A census estimate iCf, or C^^) of
eggs obtained from a cruise made during the
spawning season represents a proportion of the
area under a normal curve. If the duration and
peak of the spawning season are known, seasonal
egg production (Eg) can be estimated (Houde 1977)
as:

Es =

C,j,

^rt

or

Ckry.

Xitj

(8)

where y = the number ofdays in cruise i

X, = the proportion of the area under the
normal curve represented by
cruise i
t^ is defined under Equation (5).

Duration of the spawning season is assumed to be
62 days, lasting from 15 June to 15 August (see Z),
under Equation (5)). The spawning peak is as-
sumed to be the middate, 15 July.

The Smith Larva Method of estimating spawn-
ing biomass iB) is modified from the method used

860

RICHARDSON: SPAWNING BIOMASS AND EARLY LIFE OF NORTHERN ANCHOVY

in the CalCOFI program (Smith 1972; Pacific
Fishery Management Council footnote 2). It re-
lates the census estimate (C^ or Q^) of northern
anchovy larvae to spawning biomass by means of a
regression. Smith (1972) demonstrated that in the
CalCOFI survey area the annual regional census
estimate (sum of four quarterly estimates) of lar-
vae is related to northern anchovy spawner
biomass in the following way:

B, = 0.098 L,

(9)

where B^ = anchovy spawner biomass in short
tons
La = annual regional census estimate of
larvae x 10^ which is the sum
of the four quarterly census esti-
mates.

This equation was based on yearly data from 1951
to 1966 and 1969, with the zero intercept forced,
giving 18 data points. Data, upon which Smith's
( 1972) equation was based, can be used to obtain a
modification of this relationship, applicable to this
study, if certain assumptions are met, or can be
accounted for: 1) the same relationship between
census estimates of the number of northern an-
chovy larvae and northern anchovy spawning
biomass exists in the northern subpopulation as in
the central and southern subpopulations; 2) the
larva census estimate obtained from one cruise at
the time of peak spawning during the shortened
spawning season in the northern subpopulation is
equivalent to a quarterly census estimate made
during the peak spawning period, i.e., winter or
spring quarter ( Ahlstrom 1967) in the central sub-
population; 3) conditions, primarily temperature,
which influence development time and therefore
length of planktonic life, are similar in the north-
ern and central subpopulations for the time
periods considered; 4) sampling in the two survey
regions is similar; 5) spawning frequency during
the time period considered, i.e., during one quar-
ter in the central subpopulation and during the
2 -mo spawning season in the northern subpopula-
tion, is the same in both areas.

Data from the Pacific Fishery Management
Council (footnote 2) on quarterly larva census es-
timates for the central subpopulation for winter
and spring quarters (Table 1) were regressed on
spawner biomass estimates for the years 1951
through 1966 and 1969, 1972, and 1975, with the
zero intercept forced, giving 20 data points each.

Winter quarter: Ba = 614 + 0.152 L^;

_0 /-» I-I/-1

(10}

r2 = 0.70

Spring quarter: B„ = 645 + 0.151 L. (11)
r2 = 0.72

where L^. = the winter quarterly regional census
estimate of northern anchovy
larvae
Ls = the spring quarterly regional census
estimate of northern anchovy
larvae.

Because Smith's (1972) equation yielded a spawn-
ing biomass estimate in short tons, the values
obtained in Equations (10) and (11) are also in
short tons and may be converted to metric tons (t)
by multiplying by 0.9078. Larvae in my study
were collected with a 0.333 mm mesh net instead
of the 0.55 mm mesh silk net upon which CalCOFI
larva census estimates are based (Lenarz 1972;
Pacific Fishery Management Council footnote 2).
To correct for the increased retention by the
smaller mesh net, larva census estimates were
divided by the factor given by Lenarz (1972):

C.

C

kr

Cl corrected = — or Ct^ corrected =

1.7 L7

Thus, in my study I assumed that

Lj^, = Lj = C^ (or Ckr) corrected

(12)

(13)

T.'VBLE 1. — Census estimates (units x 10') of Engraulis mordax
larvae in the central stock for winter and spring quarters and
spawner biomass estimates ( in 1(P short tons) of the central stock
[from Pacific Fishery Management Council (text footnote 2) A. 14
and A. 15] from which Equations (10) and (11) were derived (see
Methods section).

Year

Winter census

Spring census

Spawner biomass

1951

298

690

180

1952

407

457

156

1953

1.210

373

510

1954

4,469

988

768

1955

5,588

1,709

846

1956

1,911

1,206

485

1957

5,954

4.308

1.172

1958

8,114

5,236

1.479

1959

6,341

8,155

1,514

1960

7,552

7,547

1,540

1961

992

6.714

1,159

1962

4,814

23,567

2,986

1963

17,377

24,818

4.254

1964

8,941

14.383

2.901

1965

19,155

22.690

4,659

1966

15,103

15.865

3.572

1969

19,756

6.538

2,999

1972

8,213

14.335

2.784

1975

29,754

4,071

3.603

861

FISHERY BULLETIN: VOL 78, NO. 4

Yield Estimates

Because the northern anchovy stock under con-
sideration is in a nearly virgin state, an estimate
of potential yield can be obtained using Gulland's
(1971) formula

Y,,, = XMBo

(14)

where Ypot = maximum potential yield

X = a constant coefficient [0.6 for north-
ern anchovy based on MacCall
et al. (1976)]
M - instantaneous natural mortality
rate [1.00-1.05 for northern an-
chovy based on MacCall et al.
(1976) and Pacific Fishery Man-
agement Council (footnote 2)]
Bq = mean virgin biomass, in this case
spawning biomass.

SURVEY RESULTS
Hydrography and Plankton Volume

In all 3 yr, upwelling activity was observed
along the coast, evidenced by the colder, <14° C
water nearshore (Figures 3-5). This is a typical
summer condition when winds blow mainly from
the north, currents tend generally to the south,
upwelling takes place in a narrow band along the
coast with resultant offshore transport of surface
waters (Wyatt et al. 1972; Smith 1974; Huyer et al.
1975; Ingraham and Hastings 1976; and others).
Offshore, especially beyond the continental shelf,
water temperatures were >14° C, well within the
range for successful northern anchovy spawning
and early development (Brewer 1976).

Salinity contours showed that all three surveys
covered the inner bounds of the Columbia River
plume, delineated by the 311. isohaline (Figures
3-5). The outer bounds of the plume, defined by the
32.5%., isohaline (Barnes et al. 1972), were not en-
compassed. This plume is a persistent hydro-
graphic feature off the Oregon coast in summer
(Barnes et al. 1972). The Columbia River reaches
maximum outflow in June and flows southerly,
under the influence of prevailing winds and cur-
rents, as a plume of shallow (20-40 m deep), low
salinity, warm water on top of the more saline and
colder ocean water. It can extend as far as 800 km
offshore and as far south as northern California.
In 1976 the plume extended farther south and was

closer to the coast than in 1975. In 1977 the central
core of the plume was much reduced reflecting the
extreme drought conditions of that year. High
salinities, >33L, along the coast were indicative
of upwelling.

Chlorophyll concentrations at 3 m in 1975 and
1976 were greatest near the coast in regions of
upwelling and generally decreased with distance
from shore (Figures 3, 4). In 1975, relatively mod-
erate concentrations extended beyond the conti-
nental shelf in the region of the lowest salinity
plume water. This may be indicative of higher
productivity associated with nutrient rich plume
waters near the Columbia River mouth ( Anderson
1972).

Of the 920 surface drifters released in July 1976,
24 or 2.6% were returned by 21 August 1976 (Fig-
ure 6). No additional returns were reported as of
February 1977. All but seven of the returns were
from the 2 km stations. All returns that had been
released off Oregon indicated southward trans-
port. Two returns from the 2 km station near the
Columbia River indicated some transport into the
river and one return showed northward move-
ment. Three drifters released 46 km off Grays
Harbor, Wash., were transported toward the coast
while three drifters from the 2 and 9 km stations
were transported moderate distances northward.
The low number of returns ( 2.6% ) probably reflects
the offshore component of surface drift which is
generally observed during the summer upwelling
season (Wyatt et al. 1972; Huyer 1974).

Plankton volumes, which ranged from 30 to
4,726 ml/1,000 m^ in 1975 and 8 to 3,670 ml/1,000
m^ in 1976, were greatest on the continental shelf
with the highest volumes ( >2,000/l,000 m^) oc-
curring at stations 2, 9, and 28 km from shore
(Figures 3, 4). In these areas the plankton con-
sisted largely of phytoplankton and ctenophores
although at 9 and 28 km off Cape Perpetua, Oreg.,
in 1975 it consisted mainly of copepods and
euphausiids. Nearshore low plankton volumes
<100 ml/1,000 m^ were observed at the 2 km sta-
tions off Grays Harbor in both 1975 and 1976 and
off the Columbia River in 1975. High plankton
volumes appeared to be mainly associated with
coastal upwelling with no obvious relationship to
the Columbia River plume. However, plume
waters are a near surface phenomenon while the
plankton was sampled from 150 m to the surface
possibly obscuring any relationship.

862

RICHARDSON: SPAWNING BIOMASS AND EARLY LIFE OF NORTHERN ANCHOVY

JULY 1975

A. TEMPERATURE CO AT 3m

B. SALINITY (%o) AT 3m

C. CHLOROPHYLL (Relotive Units) AT 3m

46°

44'

42°

128° 126° 124°

D. PLANKTON VOLUME (mi/IOOOm')

46°

44c

42'

128°

' 1 ■ ■

",

\

• •

•

f 32

X__ WASH

i{n'iiaea

32.5

\

wL*""

~* —

.y

/-

-

\

/

3iy^^

^/^

-^

.

•r

//W /-I

32

;^.

^ /JP '" -J-iCCWr

•

•(

■^

•

^

V

4 -^n

pfffP£Tua

^

<5I

• f

A

* * * n

LuMPQuA

/

k

^if/

/

.^/^

r33

32

32

• •

v

V

1 . .

, . 1 .

J C4LIF

128° 126° 124°

E. Engraulis mordax EGGS (No. / lOm^ )

128° 126° !24°

F. Engroulis mordox LARVAE (No/IOm*)

• • • / •

0 0 II /19**

0 0 0 0 0 0

0 0 0 0 0 0

LuMPOu^

• ♦ *w^piveR
000^

coos

0 0 0 0 0 0 0-OC

128'

126'

124°

128°

Figure 3. — Results from the July 1975 ichthyoplankton survey off Oregon and Washington; hydrography, plankton volume, Engraulis
mordax eggs and larvae. One chlorophyll unit is equivalent to 46.3 /ng coproporphyrin standard 1 or 6.14 pig chlorophyll a 1. Mean
standard length of northern anchovy larvae on each transect is listed along the left margin of F.

Eggs and Larvae

Northern anchovy eggs were taken at 17 and 23
of the 70 stations sampled in 1975 and 1976 (Fig-
ures 3, 4; Table 2). In 1975 the center of egg abun-

dance was north of the Columbia River plume.
Largest concentrations, up to 17,931 under 10 m^
sea surface, occurred 120-157 km off the mouth of
the Columbia River. In 1976, the center of abun-
dance was located 83 km off the Oregon coast

863

A. TEMPERATURE CO AT 3m

JULY 1976

B. SALINITY (%o) AT 3m

FISHERY BULLETIN; VOL 78, NO. 4

C. CHLOROPHYLL (Relotive Units) AT 3m

46'

44°

42 =

128° 126° 124° !28° 126° 124° 128° 126'

D. PLANKTON VOLUME (ml/IOOOm') E. Engroulis mordox EGGS (No./IOm^) F. Engroulis mordox LARVAE (No./IOm^)

MP

''■•''!'■■

, . . .

] {

• • •

• •

• • • JL-v^-^^fw 1

0 0 0

0 22

0 0 0A7\P^

\ WASH

14 ^fW^

0 0 0

0 1

/^ e 0 ih:::^'^^

-

■1

7^

sooo

28

0 0 0

48/ k0<

221

D Til L 4M30*
8.\r

0 0 0

• •
ei3 318

•

oo*d--

/ '■

U^ rt'pfWr

• • •

0 0 0

0 \770l

8 0 0 I'ff-^-i n.^

\\

V JJ P'"

• • •
0 0 0

• •
0 0

^ o/.„«».-...

0 0 0 0/

• • • •

0 0 0 0

• •
0 0

• • •?
0 O.oZ-jpf

-

'1

1

, 1 . . .

. , , . ] CiLIF

128°

126'

124'

Figure 4. — Results from the July 1976 ichthyoplankton survey off Oregon and Washington: hydrography, plankton volume, Engraulis
mordox eggs and larvae. One chlorophyll unit is equivalent to 46.3 /xg coproporphyrin standard/1 or 6.14 /xg chlorophyll a/1. Mean
standard length of northern anchovy larvae on each transect is listed along the left margin of F.

between the Nehalem River and Cape Perpetua
within the Columbia River plume. The largest egg
concentration, 5,777 under 10 m^ sea surface, was
one-third the highest concentration found in 1975.
Overall mean egg abundance was 642 and 291

under 10 m^ sea surface in 1975 and 1976, and at
positive stations it was 2,645 and 886 under 10 m^.
In both years the egg distribution was bounded to
the south and offshore but not to the north, al-
though relatively few eggs were taken on the

864

RICHARDSON: SPAWNING BIOMASS AND EARLY LIFE OF NORTHERN ANCHOVY

JULY 1977

A. TEMPERATURE CO AT 3m

B SALINITY (%o) AT 3m

C Engroulis mordox EGGS (No / lOm' )

46°

44°

42°

128'

128=

r

124°

128°

D. Engroulis mordox LARVAE (No. /lOm^ )E Engroulis mordox ADULTS (No. /tow)

46°

44'

X = 3.0 mm

T

0 0 24 59

• X.

/

9«3

X = 4.1mm

X = 5.2mm

X = 3 8mm

X = 6.7 mm

X - 16.0 mm

42'

• * • X • •! .

9*50 2007 TBS

1 * «N •
'|409« \ 4818 \
, 3559 5606

22J2 26«

•X

1649

ORE

■ J0( u*

/ / / I I

0 6 0 OC

X = 10 6 mm

75^/ ^^^2,

\ 0 0

• f'\' '1

•p

•X

/

0

X
40

•

• •

1

•

•

1

1 '

/
/

/ ft€Wf>OR7

t r

1 ^ ORE

•

t

•

•

•

1 PfRP€ ToZ
1 p-ff/^f-P

.

•

1

/
/

•

•

•

— •

•

•■;>

X .

•

•

•

1

7 CALIF

128°

126°

124°

128°

126=

124'

Figure 5. — Results from the July 1977 acoustic survey off Oregon and Washington: hydrography, Engraulis mordox eggs, larvae,
adults. Values for adult catches are based on a 30 min surface tow of a pelagic trawl. Dotted lines delimit east and west cruise track
boundary. On C andD,"X" indicates location of the only bongo samples taken during this cruise. On E,"X" indicates location of pelagic
trawl stations. Mean standard length of anchovy larvae on each transect is listed along the left margin of D. Data in C and D courtesy of
Methot (text footnote 111. Data in E from Smith (text footnote 10).

northernmost transect in 1976. No eggs were
taken in regions of active upwelling and few were
taken nearshore over the continental shelf except

at the 9 km station just north of the Columbia
River mouth in 1976 where a patch of warm, <16°
C, surface water occurred. The farthest offshore

865

FISHERY BULLETIN: VOL. 78, NO. 4

128° 127°

-1 — I — I — I — I — I — '

126°

45"

43° — •

42'

128°

127°

126°

_1 I i L

Big Lagoon

North of Trinidad, CA

Figure 6. — Returns of surface drifters released at the sampling
stations off Oregon and Washington during the July 1976
ichthyoplankton survey and returned by 21 August of that year
Lines represent drift paths from release point ( sampling station)
to return location. Depth contour is 183 m.

Table 2. — Summary of collection data on Engraulis mordax
eggs and larvae off the Oregon-Washington coast from ichthyo-
plankton surveys conducted in 1975 and 1976. Seventy stations
were occupied on each survey.

Item

10-18 July
1975

7-15 July
1976

No, positive stations

Eggs

Larvae

Eggs or larvae

Eggs and larvae

Mean no. eggs/10 m^
All stations
Positive stations

Mean no, larvae/10 m^
All stations
Positive stations

17

23

33

40

38

45

12

18

642.49

291.15

2,645,54

886.10

115,89

278,73

245,82

487,78

that eggs were taken was 194 km and few were
found beyond 157 km. All eggs were taken at sta-
tions where surface temperatures were >14° C.
Mean temperature at 3 m depth at positive sta-
tions was 15.18° and 16.09° C and mean salinity
was 30.69 and 30.07 Z. in 1975 and 1976. Egg con-
centrations did not correlate with high surface
chlorophyll levels and greatest concentrations
were in regions of low plankton volumes. Al-
though bongo samples were taken only at trawl
stations during the acoustic survey in 1977 ( Figure
5) catch trends of eggs were similar to the previous
two surveys (Methot' ). Northern anchovy eggs
were taken only on the four northern transects in
concentrations up to 11,165 under 10 m^ sea sur-
face.

Northern anchovy larvae were more widely dis-
persed than northern anchovy eggs with 33 and 40
positive stations in 1975 and 1976 (Figures 3, 4;
Table 2). Thirty-eight and 45 stations had either
eggs or larvae in 1975 and 1976 and 12 and 18
stations had both, respectively. In 1975, highest
numbers of larvae, >1,000 under 10 m^ sea surface,
were found 120 km offshore, near and south of the
highest egg concentrations. In 1976, greatest larva
concentrations occurred 83 and 120 km offshore
between the Nehalem River and Cascade Head,
Oreg.; 194 km off Cape Perpetua; and 120 km off
Cape Blanco, Oreg. Overall mean abundance was
115 and 278 under 10 m^ sea surface in 1975 and
1976, and 487 and 245 under 10 m^ at positive
stations. In 1975 larvae occurred mainly in a cor-
ridor paralleling the coast beyond the continental
shelf while in 1976 they were more widely distrib-
uted and also occurred closer to the coast. The
sampling grid apparently bordered their center of
abundance to the north and offshore but not to the
south. As with the eggs, larvae were generally not
found in regions of active upwelling. Mean length
of larvae on each transect in 1975 increased pro-
gressively from 3.0 mm in the north to 11.2 mm in
the south, evidence of drift south from the spawn-
ing center based on egg distributions and seasonal
flow patterns. In 1976 mean length of larvae per
transect increased from 4.5 mm off the Nehalem
River to 7.0 mm off Cape Blanco but the trend was
not as pronounced as in July 1975. This reduced
trend may be partly a result of decreased north-
erly winds, evidenced by reduced upwelling, and
reduced southward transport compared to 1975.

'2R. D. Methot, Scripps Institution of Oceanography, Graduate
Department. La Jolla, CA 92093, unpubl. data.

866

RICH.^DSON: SPAWNING BIOMASS AND EARLY LIFE OF NORTHERN ANCHOVY

Also, based on egg distribution the spawning
aggregation appeared more widely distributed in
a north-south distance. Mean temperature and sa-
linity at 3 m depth at positive stations in 1975 and
1976 were 15.66° and 15.96° C and 31.07 and
31.281., respectively. Distribution of larvae did not
correlate with high surface chlorophyll levels and
abundance was generally highest in regions of low
plankton volume. During the acoustic survey in
1977, northern anchovy larvae were collected
(Methot footnote 12) on each transect in concentra-
tions up to 5,606 under 10 m^ sea surface (Figure
5). No larvae were found in samples taken within
46 km of the coast. Mean length of larvae on each
transect again showed an increasing trend toward
the south.

125°30' W) between 56 and 130 km offshore (Fig-
ure 5). No adult northern anchovy were collected
at trawl stations on the southern two transects. No
trawls were made on the transects off Cascade
Head or Cape Perpetua.

School concentrations, recorded by sonar, were
presented by Smith (footnotes 10, 3). Based on
sonar traces and results of the pelagic trawl
catches, he concluded schools of spawning adult
northern anchovy were centered 83 km offshore in
the surveyed area and 37 km south of the Colum-
bia River mouth with the inner edge about 37 km
offshore and the western edge between 102 km. and
130 km offshore. The northern edge was not de-
fined above lat. 47 ° N and the southern edge was at
lat. 44°N.

Adults

During the acoustic survey in 1977, running ripe
adult northern anchovy were collected on the
three northern transects (lat. 47°02' N, long.
124°56' W; lat. 46°60' N, long. 126°33' W; lat.
46°19' N, long. 124°54' W; lat. 45°40' N, long.

EGG AND
LARVA CENSUS ESTIMATES

The total area represented by the survey in 1975
and 1976, was 148.81 x 10» m^. Census estimates of
the total number of northern anchovy eggs and
larvae in that area for each cruise are in Table 3.

Table 3. — Egg and larva census estimates (Q, and C^^) and spawning biomass estimates (B) of Engraulis mordax in the survey area
off Oregon and Washington in 1975 and 1976. Values of parameters used in the biomass estimating procedures are presented except
those for K (proportion females) and F (mean fecundity) which are constants, 0.5 and 720. See Methods section for description of
procedures and equations.

Sette and

Sette and

Ahlstrom

Days

Days

Proportion

Ahlstrom

Census

repre-

included

of area

Time to

Census

corrected

sented by

in

under nor-

hatch

Spawning biomass estimating

Year and

'Ck

Lw or 2/.S

cruise

cruise

mal curve

in days

method

season

(units X 10")

(units X 10^)

Di

n

Xi

'f,

Sette and Ahlstrom Egg Metfiod

1975

121.98

62

2.73

[Equations (4) and (5))

1976

54.89

62

2.43

Simpson Egg Method

1975

121 98

2.73

lEquations (4) and (7)]

1976

54.89

2.43

Saville Egg Method

1975

121.98

9

0.3335

2.73

[Equations (4) and (8)]

1976

54.89

9

0.3081

2.43

Smith Larva Method

1975 winter

22.22

1,307

[Equations (10) and (11)]

1975 spring

1976 winter
1976 spring

22.22
52.06
52.06

1.307
3.062
3.062

Seasonal

Spawning

Spawning

Spawning

Daily egg

egg

Biomass

Biomass

Smith

Biomass

production

production

Estimate

Estimate

Census

Estimate

Spawning biomass estimating

Year and

'Ed

Es

'Ba

5B

'Ckr

'e

method

season

(X 10")

(X 10")

(tons)

(t)

(X 10")

(t)

Sette and Ahlstrom Egg Method
[Equations (4) and (5)]

Simpson Egg Method
[Equations (4) and (7)]

Saville Egg Method
[Equations (4) and (8)]

Smith Larva Method
[Equations (10) and (11)]

1975

2,770.24

769,511

95 60

1976

1.400 49

389,025

43.32

1975

44.68

1.316.27

365,631

95.60

1976

22.59

70887

196,909

43.32

1975

1 .205.82

334,951

95.60

1976

659.84

183,289

43.32

1975 winter

812,664

737,736

17.14

1975 spring

842,357

764,692

17.14

1976 winter

1,079,424

979,901

41.48

1976 spring

1,107,362

1 ,005,263

41.48

'Equation (2).
2Equations(12),(l3).
3Equation(6).
"Equation (7).

^Based on Sette and Ahlstrom Census.

"Equation (3).

'Based on Smith Census.

603,094
307,022

294,933
170,694

262,506

144,654

696,479
723,705
894.074
920,001

867

FISHERY BULLETIN: VOL 78, NO. 4

The Smith Census estimate was always lower
than the Sette and Ahlstrom Census estimate.
Both estimates were used to calculate spawning
biomass of adults.

Larva abundance was not corrected for day-
night catch differences. A correction factor could
not be derived from the data. No consistent pattern
of daytime avoidance was apparent based on
cruise plots of night to day catch ratios for each
millimeter length class as Houde (1977) demon-
strated for clupeid larvae. If daytime avoidance
did occur, larva census estimates would be low and
in turn biomass estimates would be low. Net avoid-
ance of larvae increases with age and since 94%
of the larvae captured in 1975 and 98% in 1976
were «10 mm SL (standard length), errors due to
avoidance should be small. Also, Smith (1972)
made no day-night corrections for the CalCOFI
program. Thus data from my study are compara-
ble.

SPAWNING BIOMASS ESTIMATES

is assumed that the eggs collected represented no
more than a single spawning, because batch 1
would hatch before batch 2 was spawned.

The three egg methods of estimating biomass do
not take into account egg mortality. Rates of egg
mortality in the ocean are unknown for northern
anchovy and could not be determined in this study.
Eggs could not be staged due to poor condition
resulting from collection techniques. If mortality
of spawned eggs were high and disintegration
rapid (i.e., dead eggs not occurring in plankton
samples), the estimates of total number of eggs
spawned would be low and the resulting biomass
estimates would also be low. However, Sette and
Ahlstrom (1948) obtained similar biomass esti-
mates for Sardinops caerulea using two
techniques, one that involved aging of eggs and
another, the Sette and Ahlstrom Egg Method used
in my paper, that did not. Presumably egg mortal-
ity was not a major factor influencing their esti-
mates. A similar situation may exist for northern
anchovy which also has a relatively short-lived (2
or 3 d) egg stage.

These biomass estimates apply only to that por-
tion of the spawning population within the north-
ern subpopulation off Oregon and Washington
that was sampled in my survey area. In 1975, the
egg concentration (Figure 3) was bounded inshore,
offshore, and to the south, but the northern
boundary was not encompassed. If major egg con-
centrations occurred north of the sampling area,
the biomass estimates would be low. In 1976, es-
sentially the entire egg concentration was
bounded. In both 1975 and 1976, larva concentra-
tions were bounded to the north and offshore, but
not to the south. The estimates do not account for
any additional spawning concentrations within
the northern subpopulation should they exist.

The three methods of estimating spawning
biomass based on egg abundance (Sette and
Ahlstrom, Simpson, and Saville Egg Methods) in-
clude the assumption that northern anchovy
spawn only one batch of eggs, those in the most
advanced mode and upon which fecundity esti-
mates are based, during the time sampled by the
survey. This is particularly critical since the re-
cent work by Hunter and Goldberg (1980) has indi-
cated that a ripe adult northern anchovy can ma-
ture a batch of eggs and spawn once every 6 or 7 d
in the central subpopulation. In this study the
area in which northern anchovy eggs were col-
lected was sampled in 5 d in 1975 and 6 d in 1976. It

Sette and Ahlstrom Egg Method

The egg census estimate (Table 3 ) for each cruise
was divided by the duration of the egg stage, esti-
mated to be 2.73 d in 1975 and 2.43 d in 1976,
Equation (6), to obtain estimates of daily egg
production. This value was then expanded to the
number of days (62) represented by the cruise.
Equation (5). Biomass estimates for each cruise
were then obtained. Equation (4).

Estimated spawning biomass using the Sette
and Ahlstrom Census was 769,511 t in 1975 and
389,025 t in 1976 (Table 3). Somewhat smaller
values were obtained with the Smith Census
603,094 and 307,022 t. Since the method used to
derive the Smith Census is merely a simplified
version of the method used for the Sette and
Ahlstrom Census, biomass estimates based on the
latter may be better, at least for the egg data.
Confidence limits (95%) based on variance esti-
mates of egg abundance, using methods of Houde
(1977), gave a range around the point biomass
estimates of ±11-15% for all egg methods. How-
ever, the variance estimates were low and statisti-
cally not very precise because of the low number of
data points and are thus not included here. The
Sette and Ahlstrom Egg Method assumes a con-
stant egg production throughout the 62 -d spawn-
ing season. If egg production tapers off at the

868

RICHARDSON: SPAWNING BIOMASS AND EARLY LIFE OF NORTHERN ANCHOVY

beginning or end of the season, the biomass
estimates would be high.

Differences in biomass estimates between the 2
yr based on eggs reflects the fact that more than
twice as many eggs were collected in 1975 than in
1976. This could be the result of a decrease in
spawning biomass between the years although
small sample size is probably just as important.
Biomass estimates based on eggs are likely to be
more variable than those based on larvae. North-
ern anchovy is a schooling fish; therefore eggs
released from spawning schools are clumped, re-
sulting in a sample of high variance (Pacific
Marine Fishery Management Council footnote 2).

Simpson Egg Method

Estimates of daily egg production, Equation (7),
44.68 X 10^1 in 1975 and 22.59 x 10^ in 1976 using
the Sette and Ahlstrom Census ( Table 3 ) and 35.02
X 10" and 17.83 x 10" using the Smith Census,
were plotted against the cruise middate. The area
under the resulting triangle was then equated
with egg production for the entire spawning sea-
son, 1,316.27 X 10" in 1975 and 708.87 x 10" in
1976 with the Sette and Ahlstrom Census and
1,061.76 X 10" and 614.50 x 10" with the Smith
Census. Biomass estimates were then obtained
with Equation (4).

Spawning biomass estimates were 365,631 t in
1975 and 196,909 t in 1976 using the Sette and
Ahlstrom Census and slightly smaller with the
Smith Census (Table 3). These biomass values are
nearly one-half those obtained by the Sette and
Ahlstrom Egg Method. This reflects the different
assumption of this method regarding egg produc-
tion where it is high in mid season and low at both
ends.

Saville Egg Method

Egg production is assumed to follow a normal
curve throughout the 62 -d spawning season from
15 June to 15 August. Each cruise within that
period represents a proportion of the area under
that normal curve. In this study, each cruise was of
9 d duration and was made near the peak of the
spawTiing period. In 1975 the cruise represented
33.35% of the curve and in 1976, 30.81%. Seasonal
egg production was then estimated by Equation
(8) and biomass by Equation (4).

Estimates of biomass using this method were
smaller, 334,951 t in 1975 and 183,289 t in 1976

using the Sette and Ahlstrom Census, than in the
two previous methods (Table 3). If egg production
is skewed from a normal distribution, large errors
could be introduced into the biomass estimate.

Smith Larva Method

This method of estimating spawning biomass
assumes that a similar linear relationship exists
between numbers of larvae and adult spawning
biomass in both the central and northern subpopu-
lations. Although this assumption seems reason-
able, the recent fecundity estimate for northern
anchovy off California, 340 eggs/g total female
weight (Hunter and Goldberg 1980 1, is consider-
ably less than the fecundity estimate obtained for
northern anchovy off Oregon, 720 eggs/g total
female weight (Laroche and Richardson 1981).
These data indicate it would take more planktonic
eggs to represent 1 g offish in the northern than in
the central subpopulation. It follows then that it
would also take more pelagic larvae to represent 1
g offish in the northern subpopulation given that
spawning frequency and larval growth and mor-
tality conditions are similar. Thus, biomass esti-
mates obtained by this method may be too high.

Other assumptions of the method seem reason-
able (see Methods section). The census estimate
obtained from one cruise during the shortened
spawning season in the north should be equiva-
lent to a quarterly census estimate obtained dur-
ing a peak spawning period in the south. Some-
times a quarterly estimate for CalCOFI is based
on only one cruise, other times a mean of several
cruises. However, my cruise dates were purpose-
fully selected at the time of peak spawning. Some-
times CalCOFI quarterly cruises may be con-
ducted near the beginning or end of a quarter and
not necessarily at the peak of spawning. Thus
larger numbers of smaller larvae may have been
collected in our study, and the relationship be-
tween numbers of larvae and biomass may be
biased to give a higher biomass estimate in the
north.

In general, water temperatures at the time of
peak spawning appear to be similar off Oregon
and California (Ahlstrom 1959; Baxter 1967) so
that growth rates and length of time in the water
column are assumed to be similar. Methot (in
press) demonstrated that growth rates of larvae in
the two subpopulations are similar at similar
temperatures.

Sampling techniques used in this study were

869

FISHERY BULLETIN: VOL. 78, NO. 4

similar to those of the CalCOFI program (Kramer
et al. 1972) except we used 0.333 mm mesh net on
70 cm bongos vs. 0.55 mm mesh on a CalCOFI net.
The difference in mesh sizes can be corrected,
Equation (12), but because of the reduced avoid-
ance associated with bongo nets, larva catches
may be relatively greater resulting in high census
estimates and accordingly high biomass esti-
mates.

Spawning frequency during the 2-mo spawning
period in the northern subpopulation is unknown.
Hunter and Goldberg (1980) indicated that north-
ern anchovy in the central subpopulation may
spawn a batch of eggs every 6 or 7 d during peak
spawning. If northern anchovy off Oregon respond
differently, additional error would be introduced
into the biomass estimate. The higher fecundity of
fish in the north may be balanced by less frequent
spawning.

Spawning biomass estimates derived from the
Smith Larva Method are based on larva abun-
dance. Using the larva census estimates corrected
for mesh size differences, Equation (12), biomass
estimates were obtained by Equations (10) and
(11). These estimates were 737,736 and 764,692 t
in 1975 and 979,901 and 1,005,263 t in 1976 with
the Sette and Ahlstrom Census and slightly less
with the Smith Census, 696,479 and 723,705 in
1975 and 894,074 and 920,001 in 1976. In this case,
since the Smith Census is based on procedures and
data (Smith 1972) from which Equations (10) and
(11) are derived, biomass estimates based upon it
are probably better than those based on the Sette
and Ahlstrom Census.

Because of diffusion and dispersion and length
of the larval period (about 30 d compared with 2-4
d for eggs), larvae are more evenly distributed
over a given geographic area than eggs and in turn
yield a less variable biomass estimate than eggs
(Pacific Fishery Management Council footnote 2).
This may, in part, account for the smaller year to
year difference in biomass estimates based on lar-
vae compared with those based on eggs. Interest-
ingly biomass estimates based on eggs decreased
greatly from 1975 to 1976 while those based on
larvae increased.

Most Probable Biomass

Spawning biomass estimates (Table 3) ranged
from 262,506 to 769,511 t in 1975 and 144,654 to
1,005,263 1 in 1976 (Table 3 ). The biomass estimate
based on acoustic survey of adults in July 1977 was

870

about 800,000 t (Smith footnote 3), using methods
given by Smith (1970). A reasonable conclusion is
that the actual spawning biomass of northern an-
chovy in the survey area laid or fluctuated be-
tween the extreme values in 1975 and 1976 (Houde
1977) and is probably <1 million t but >100,000 t.
This line of reasoning is supported by the fact that
the estimates from 1975 and 1976 (for a given
method) are within twofold of each other and less
than tenfold (for any method) from the acoustic
survey.

These estimates only include mature spawoiing
adult fish. Laroche and Richardson ( 1981) reported
that northern anchovy in the northern subpopula-
tion attain first sexual maturity at the end of the
second year, i.e., in the third summer. Thus north-
ern anchovy <2 yr old are not included in the
estimates and may represent additional sizeable
biomass. These immature fish are segregated geo-
graphically from spawning adults during the
spawning season with the young fish occurring in
nearshore coastal areas (Laroche and Richardson
1981).

Based on these estimates, spawning biomass of
northern anchovy off the Oregon-Washington
coast is less than that in the central subpopulation
which had a mean estimate of around 3,631,200 t
for 1965-72 (MacCall et al. 1976), although a re-
cent population decline has been recorded in 1978
(1,183,771 t) and 1979 (1,564,139 t) (Stauffer
1980). My spawning biomass estimates are more
comparable to that for the southern subpopulation
of 544,680 t (mean for 1965-69) (MacCall et al.
1976).

YIELD ESTIMATES

Using Gulland's (1971) formula for potential
yield to a fishery. Equation (14), with the range of
instantaneous natural mortality rates of 1.0-1.05,
estimates for a biomass of 144,654 t are 86,792-
91,132 t. For a biomass of 1,005,263 t they are
603,158-633,316 t. These potential yield estimates
are about 60% of the spawning biomass, which
may be dangerously high values for a species
known to undergo large year-to-year fluctuations
in abundance.

Recommendations for harvest quotas by the
northern anchovy management plan for the cen-
tral subpopulation called for a more conservative
yield estimate of 70% of one-third, or about 23% , of
the spawning biomass in excess of 907,800 t
(Pacific Fishery Management Council footnote 2).

RICHARDSON: SPAWNING BIOMASS AND EARLY LIFE OF NORTHERN ANCHOVY

At an estimated spawning biomass of 3,631,200 t
(MacCall et al. 1976) the harvest quota would be
635,400 t or approximately 17% of the total spawn-
ing biomass. At the recent reduced biomass level of
1,564,100 in 1979, the optimum yield established
for the 1979-80 season in the U.S. Fishery Conser-
vation Zone was 153,100 t (Stauffer 1980), equiv-
alent to only 10% of the total spawning biomass.

Thus the actual realizable yield and in turn the
feasibility of establishing a fishery on this north-
ern stock of northern anchovy is difficult to assess.
Northern anchovy are considered to be important
forage items for fishes such as salmon and albacore
off Oregon and Washington but northern anchovy
biomass actually consumed by these species has
not been adequately estimated. Northern anchovy
are also important items in the diet of marine
birds. Weins and Scott (1975) estimated that four
species of marine birds consume 28,000 t of north-
ern anchovy annually off Oregon.

If the northern anchovy stock off Oregon and
Washington could support a harvest of 10% of the
total biomass, as in the recent quotas on the re-
duced biomass for the central subpopulation, a
yield of about 14,465-100,526 1 might result. If this
is reasonable, the feasibility of establishing such a
fishery still remains to be determined. Feasibility
partly depends on distribution patterns and habits
of the stock and on economic considerations, the
latter of which is beyond the scope of this paper.
Seasonal patterns of distribution were discussed
by Laroche and Richardson (1981). The most com-
pact aggregations appear to occur during the
spawning season in the offshore spawning center.
However, school sizes appear to be small. Smith
(footnote 3) estimated that half of the northern
anchovy schools counted during the acoustic sur-
vey in July 1977 were <4 1 and only 1.1% were over
64 t. Small school size could be a deterrent to
fishery development.

COMPARISON OF NORTHERN AND
CENTRAL SUBPOPULATIONS

Important ecological differences exist between
the northern and central subpcpulations of E.
mordax with respect to spawning times and loca-
tions and associated environmental parameters.
Off California, spawning takes place throughout
the year (Figure 7) with a peak occurring between
January and April (Smith and Richardson 1977).
Off Oregon, spawning takes place over a 2-mo
period (Figure 7) with a peak in July, based on the

15

% 10 -

5 -

CALIFORNIA

1951 - 60

II I I I I I I 1 I I

J FMAMJJ ASOND
100r

OREGON

1971-72

% 50

10-

1

J FMAMJ J ASOND

FIGLT^E 7. — Spawning cycle o{ Engraulis mordax off California
and Oregon. Upper graph is after Smith and Richardson (1977).
Lower graph is based on catches of northern anchovy larvae
given by Richardson (text footnote 5).

collection of small larvae (Richardson 1973, foot-
note 5). These differences in peak spawning times
certainly contribute to reproductive isolation.

Off California (Figure 8), at the initiation of
peak spawning southward flow of the California
Current is minimal (Saur 1972) with resulting
minimal larval transport south away from the
spawning area; temperature at 10 m depth ( Lasker
and Smith 1977) is reaching minimum values in
the annual cycle; upwelling is minimal but in-
creasing (Bakun 1973); day length is beginning to
increase after the shortest day in December. In
contrast, off Oregon (Figure 9), at the time of peak
spawning, current flow to the south is at a
maximum (Huyer 1977); surface temperatures
(Johnson 1961) are reaching maximum values in
the yearly cycle ( excluding the colder waters of the
nearshore upwelling zone); upwelling activity is at
a maximum (Bakun 1973); day length is beginning
to decrease after the longest day in June.

Off California (Figure 10), spawning takes place
closer to the coast (Smith and Duke'^) than off

"Smith, P E., and S. Duke. 1975. Nearshore distribution of
northern anchovy eggs and larvae i Engraulis mordax). NOAA
NMFS, Southwest Fish. Cent., Admin. Rep. No. LJ-75-58, 15 p.

871

mm>^

LLETIN; VOL. 78. NO. 4

E o

^ > 2000

>

0)

q:

0)

E
c

0)

O

O
o

u

0)

in

ro

E

60
50

18
16
(4

400
200

0 -

T — I — r

J L

"T — r

J L

-1 — I — I — I — I — I — I r-
ANCHOVY LARVAE

CALIFORNIA CURRENT
(SAUR INDEX

lOm TEMPERATURE

UPWELLING

I I I I I I I

OCT

JAN

APR

JUL

OCT

JAN

Figure 8. — Yearly cycle o( EngrauHs mordax larva abundance
and selected environmental parameters [mean annual cycles
(1953-60)] off California (reproduced from Lasker and Smith
1976). A) Larva abundance. B) California Current strength
indicated by sea level difference approximations (Saur
1972). C) Temperature at 10 m depth. D) Upwelling (Bakun
1973). Dashed lines indicate period of peak spawning between
January and April. Horizontal lines are for reference only.

Oregon. Relatively little nearshore spawning
takes place in the coastal upwelling zone off Ore-
gon which is probably related to the low water
temperatures there during the spawning season.
Lasker (in press) demonstrated that upwelling
may disperse proper-sized food particles, mostly
dinoflagellates, and thereby reduce survival of
first feeding northern anchovy larvae. These di-
noflagellates are replaced by smaller diatoms
which are nutritionally inadequate for survival of
northern anchovy larvae.

RELATIONSHIP WITH
COLUMBIA RIVER PLUME

Data from this study and that by Richardson
(1973) provide evidence that a northern anchovy
spawning center within the northern subpopula-
tion is closely associated with the Columbia River

100-
80-
60-
40-
20-
0-

40-

. 20

0
0

: 0

5

-20-
-4oL

i8r

16

14-

O
° 12

10

8

100

(A)

(B)

(C)

ANCHOVY
LARVAE

GEOSTROPHIC
FLOW

SURFACE
TEMPERATURE

JFMAMJJASOND

Figure 9. — Yearly cycle of Engraulis mordax abundance and
selected environmental parameters off Oregon. A) Larva
abundance in 1971-72 off Newport, Oreg. (Richardson text foot-
note 5) . B) Estimates of alongshore geostrophic flow between 28
and 46 km off Newport at the surface ( solid line) and 50 m ( dotted
line) after Huyer ( 1977). C) Monthly mean of surface tempera-
tures recorded in six 2° squares off Oregon and Washington ( lat.
42°-48° N; long. 124°-128° W) from 1947 to 1958 from Johnson
(1961). D) Mean monthly values of upwelling indices for the
20 yr period 1948-67 at lat. 45° N, long. 125° W from Bakun
(1973). Dashed lines indicate period of peak spawning. Hori-
zontal lines are for reference only.

plume. Reasons for such an association may be
related to conditions necessary to induce or trigger
spawning in adults or conditions necessary for the
survival of the eggs and larvae. Increased river
flow and plume size, associated with snow melt
and day length, may provide a cue for the offshore
spawming migration of adults. Temperature may
not be a major factor in the association as both
oceanic and plume waters warm to temperatures
>13° C (Johnson 1961) needed for spavming, al-
though plume waters warm earlier (Owen 1968).

872

RICHARDSON: SPAWNING BIOMASS AND EARLY LIFE OF NORTHERN ANCHOVY

3000-

CALIFORNIA

278

km FROM COAST

3000

OREGON

2000

O

z

1000

93 130 167

km F ROM COAST

203

240

278

Figure lO. — Abundance of Engraulis mordax eggs and larvae
with distance from the coast off California and Oregon. Upper
panel based on data collected off Point Arguello, Calif., in
January, April, and July 1964 (Smith and Duke text footnote 13).
Lower panel data collected off Oregon and Washington in July
1975.

The plume may provide an optimal environment,
in terms of stability and productivity particularly
within 100 km or so from the river mouth (Ander-
son 1972; Barnes et al. 1972), to insure good feed-
ing conditions and enhance survival of first feed-
ing larvae. Such an environment may not exist in
the less productive ambient oceanic water or the

highly productive but too cold and dynamic coastal
upwelling zone. Unfortunately data on type and
availability of potential food items in the plume,
which would help validate or refute this
hypothesis, are not available.

LARVAL TRANSPORT AND
JUVENILE NURSERIES

Because of the obvious southward transport of
larvae away from the spawning center off Oregon
and Washington and the later occurrence of
juveniles in Oregon bays and rivers where spawn-
ing is apparently rare or unsuccessful, questions
arise about return mechanisms. The deep (bottom
third of water column) northward flowing coun-
tercurrent that develops in late summer beneath
southward flowing surface waters (Huyer et al.
1975) could provide a mechanism for reduction of
southward transport if larvae utilize it by migrat-
ing vertically Unfortunately we have no depth
distribution data on the larvae related to the depth
of the shear layer between currents off Oregon to
demonstrate this. However, if northern anchovy
larvae come to the surface at night to gulp air and
conserve energy, as off California (Hunter and
Sanchez 1977), then southward and offshore
transport would be enhanced, at least at night.
Changing wind patterns in the fall from northerly
to southwesterly (Wyatt et al. 1972) result in a
shift in surface currents from southward to
northward, cessation of upwelling, and an onshore
drift of surface waters which may contribute to a
northerly onshore movement of juveniles. Also,
northern anchovy spawned later in the season
may not be transported as far south as those
spavined earlier and thus would not have to travel
as far to return to northern bays and rivers.

An additional offshore spawning center to the
north would help explain recruitment of juveniles
to the Oregon rivers but there is no evidence for
the existence of one, as discussed earlier.

The southward transport of larvae may provide
an avenue of gene flow from the northern to cen-
tral subpopulation.

OTHER SPAWNING CENTERS

Whether the area off the Columbia River is the
primary or only spawning center for northern an-
chovy in the northern subpopulation is unknown.
No evidence of spawning to the north exists at
least in offshore waters. Also, no evidence is avail-

873

able for a major spawning center to the south off
northern California although that area has not
been sampled intensively. It is not known where
ripening northern anchovy go after they leave
Humboldt Bay in June (Waldvogel 1977), i.e.,
whether they go north to spawn near the Colum-
bia River plume or whether they spawn off north-
ern California.

Some evidence indicates that another spawning
center may occur in the Strait of Georgia. Ripen-
ing adults (Pike 1951) and larvae as small as 11 mm
(Robinson footnote 6) have been collected there.
The environment created by the Eraser River may
share similarities with that of the Columbia River
plume in terms of stability and productivity
(Waldichuk 1957). Thus the region may provide
another suitable spawning environment. Addi-
tional sampling would be needed for adequate
documentation. If a second major spawning center
were defined in this region, it would be interesting
to investigate the degree of mixing between Co-
lumbia River-spawned and Eraser River-spawned
northern anchovy.

ACKNOWLEDGMENTS

Special thanks are extended to Paul E. Smith,
Southwest Eisheries Center La Jolla Laboratory,
NMES, NOAA, for arranging and conducting an
acoustic survey in July 1977 on the NOAA Ship
David Starr Jordan in cooperation with this re-
search effort and thereby enabling us to obtain a
third year of comparative data on hydrography.
Thanks are also extended to participants on that
cruise, particularly Richard D. Methot, Scripps
Institution of Oceanography, who provided data
from his collections of anchovy eggs and larvae. I
thank George Tinker and his students of Marsh-
field Senior High School, Coos Bay, Oreg., for
making surface drifters and recording returns
from the July 1976 cruise. Technical assistance
was provided by Barbara Dexter, Joanne L.
Laroche, Betsy B. Washington (Oregon State Uni-
versity), and numerous others who helped with the
cruises and in sorting samples. Paul E. Smith,
Richard D. Methot, and Joanne L. Laroche offered
helpful comments on the manuscript.

This work is a result of research sponsored by
the Oregon State University Sea Grant College
Program, supported by NOAA Office of Sea Grant,
U.S. Department of Commerce, under Grant No.
04-6-158-44094.

FISHERY BULLETIN: VOL. 78. NO. 4

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FISHERY BULLETIN: VOL 78. NO. 4

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876

VOLUNTARY SWIMMING SPEEDS AND RESPIRATION RATES OF

A FILTER-FEEDING PLANKTIVORE, THE ATLANTIC MENHADEN,

BREVOORTIA TYRANNUS (PISCES: CLUPEIDAE)

Ann G. Durbin/ Edward G. Durbin,' Peter G. Verity,* and Thomas J. Smayda^

ABSTRACT

Voluntary swimming speeds and respiration rates of a group of adult Atlantic menhaden (mean wet
weight = 302 g) were measured before, during, and after a 7-hour feeding period, during which the
diatom Ditylum brightwelli was made available at a constant rate. Total ration for the 12 fish ranged
between 9.60 and 94.79 g dry weight. Temperature was 20°±1° C. In the absence of food, the routine
swimming speeds and respiration rates of the menhaden were: mean ± 95% confidence limits =
12.2 ± 1.6 cm per second (0.47 ±0.06 body lengths per second), and 0.10±0.009 m.g Oj per gram per hour.
During feeding the fish increased their voluntary swimming speed 2.4- to 3.5-fold, and their respiration
rates 2.2- to 5.4-fold above the routine rates, depending on the concentration of plankton in the water.
There was a linear relationship between logio respiration rate and mean swimming speed during the
feeding and the postfeeding periods. During feeding, the metabolic cost per increment in swimming
speed was about 2.5 times higher than the cost of swimming in other species; this is believed to reflect a
high energetic cost of filter feeding. There was an approximately hyperbolic relationship between the
voluntary swimming speed of the Atlantic menhaden, and the phytoplankton chlorophyll a concentra-
tion in the water The swimming speed and respiration rate of the fish remained constant as long as the
input of phytoplankton into the tank continued at a constant rate. After feeding, the activity levels and
respiration rates of the menhaden quickly returned to prefeeding routine rates.

The Atlantic menhaden, Breuoor^ia tyrannus, is a
schoohng, filter- feeding planktivore (Peck 1894;
Durbin and Durbin 1975) which supports a major
commercial fishery along the Atlantic coast of the
United States.

The present study investigates voluntary
swimming speeds and oxygen consumption rates
of Atlantic menhaden before, during, and after a
7-h period during which the fish were fed a ration
of the diatom Ditylum brightwelli. During this
period the plankton was made available at a con-
stant rate, so that feeding was continuous and the
ingestion rate was constant. The prolonged feed-
ing was designed to reproduce, as much as possi-
ble, natural feeding conditions for menhaden.
During these experiments ammonia and dissolved
organic nitrogen excretion rates, feces production
rates, and assimilation efficiencies were also mea-
sured and will be reported in a second paper. These
studies are part of a larger effort to determine the
energy budget of Atlantic menhaden in Narragan-
sett Bay, R.I.

'Graduate School of Oceanography, University of Rhode Is-
land, Kingston, RI 02881.

^Department of Oceanography, University of Washington,
Seattle WA 98195.

METHODS

Adult Atlantic menhaden were dipnetted from a
commercial purse seine, 2-3 min after it had been
set around a school. These fish were transferred to
a round, 1.2 m diameter tank and brought in good
condition to the laboratory. There the fish were
maintained outdoors, in a circular fiber glass tank
1.85 m in diameter and 0.76 m deep, supplied with
flowing unfiltered seawater. The tank was pro-
tected by a large fiber glass canopy.

Five days after capture, the number offish in the
tank was reduced to 25. Once a day the fish were
fed a ration of RangenV salmon feed, size 00 pow-
der, equivalent to 3% of their dry body weight per
day. Within 3 wk all fish fed readily in the tank.
The fish were held for 6 wk before use in experi-
ments. During this period, the tank was cleaned
every day, and preliminary trials were carried out.
This enabled the fish to become accustomed to
routine sampling procedures, to the presence of
observers near the tank, and also to the presence of
a clear Plexiglas cover, which was lowered onto the
surface of the tank water during respiration mea-

Manuscript accepted March 1980.

FISHERY BULLETIN: VOL. 78. NO. 4, 1981.

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

877

FISHERY BULLETIN: VOL 78, NO 4

surements. The experiments were conducted in
the same tank in which the fish were maintained.
This removed two potential problems: first, the
possibility of injury to the fish as a result of fre-
quent handling; and second, the possibility of
stress resulting from recent handling and transfer
of the fish to an unfamiliar tank. Stress has been
shown to affect the respiration rate and swimming
performance of schooling fishes (i.e., Skazhina
1975; Hartwell and Otto 1978).

One week before the experiments were begun,
one-half of the fish were removed for length and
weight determination, leaving 12 Atlantic
menhaden in the tank. We have found that 12-15
adult fish is an optimum number for a tank of this
size; fewer fish begin to show signs of stress,
whereas more fish begin to interfere with each
other during feeding. Experiments were carried
out between 26 July and 9 September 1977. At the
end of this period the fish were sacrificed for length
and weight determination. All fish appeared to be
in excellent condition thoughout the experimental
period, and showed no evidence of injury or dis-
ease.

Experimental Procedure

The experiments were carried out at 20°±1.0°C
and a salinity of 31%o. Prior to each experiment,
the bottom and walls of the tank were thoroughly
cleaned with a wire brush. The fish were fed their
normal ration, and then deprived of food for 36 h
until the beginning of the experiment to permit
evacuation of the intestine and to avoid any effect
of the previous meal on the metabolism of the fish.
During this 36-h period, the seawater inflow was
filtered through a GAF polypropylene bag filter of
5 fxm nominal pore size. Feces from the last meal
were periodically siphoned from the tank. On the
evening before the experiment, the tank walls
were again scrubbed and the tank rapidly flushed
several times with filtered seawater.

Each experiment was begun at approximately
0630 h, with an initial baseline measurement of
respiration rate and voluntary swimming speed of
the unfed fish. Plankton was then added to the
tank at a constant rate during a 7-h period from
approximately 0800 to 1500 h. During each exper-
iment, respiration rates and voluntary swimming
speeds were measured on 10 occasions, termed
"measurements," which lasted for about 1 h when
the fish were feeding, and iy2-2 h when they were
not. These measurements correspond to the fol-

lowing periods: no. 1, initial (unfed for 36 h); no.
2-4, feeding during the 7-h period of food input; no.
5, the transition from feeding to postfeeding; no.
6-8, during the first 10 h following feeding; and no.
9 and 10, the next morning, 15-20 h after feeding.
To prevent an excessive accumulation of am-
monia in the tank when the fish were fed the
larger rations, the tank was flushed briefly with
filtered water at the conclusion of feeding.

Food

The solitary diatom Ditylum brightwelli was
used as food in the experiments. These large cells
(—80 ixm. long) are readily eaten by menhaden.
Phytoplankton was raised in outdoor batch cul-
tures. Narragansett Bay water was filtered into
400 1 fiber glass tanks, using a series of four car-
tridge filters culminating in a Gelman 0.45 /nm
membrane filter, and then enriched to the level of
Guillard's F/2 (Guillard and Ryther 1962).

Large volumes (up to 2,500 1) of culture were
raised for each experiment, and it was necessary
to concentrate the cells before feeding them to the
fish. Since the duration of the feeding period was 7
h, the culture was divided into seven batches of
equal volume. Each batch was concentrated by
gentle back filtration into a volume of 18 1, which
was then subsampled by filtering onto a precom-
busted glass fiber filter for determination of the C
and N concentration (Hewlett Packard Model
185B CHN Analyzer). On several occasions addi-
tional subsamples were centrifuged to form a pel-
let, from which the water was aspirated off, and
the C, N, ash (combustion at 475°C for 4 h), caloric
(Parr adiabatic bomb calorimeter), and Si (Durbin
1977) contents were determined. Each 18 1 batch of
food was slowly siphoned into the tank over a 1-h
period, to provide an approximately constant rate
of input of food. By changing the concentration of
plankton in these batches, different concentra-
tions of food in the tank and different ration sizes
could be obtained. The volume of water added with
the food was balanced by the volume removed dur-
ing sampling, and thus the volume in the tank
(1,400 1) remained approximately constant. The
chlorophyll a concentration in the tank was also
periodically determined by fluorometry (Yentsch
and Menzel 1963; Lorenzen 1966).

Turbulence produced by the fish stirred the tank
and kept the plankton in suspension. The Atlantic
menhaden were estimated to filter 13-20% of the
tank volume per minute, removing the D.

878

DURBIN ET AL.; SWIMMING SPEEDS AND RESPIRATION RATES OF ATLANTIC MENHADEN

brightwelli with an efficiency of about 25% (Dur-
bin and Durbin 1975).

Respiration Rate

Oxygen consumption by the fish was deter-
mined by closed system respirometry. The water in
the tank was sealed from contact with the atmo-
sphere by means of a circular cover made of clear
1.2 cm Plexiglas, suspended on pulleys over the
tank, which could be gently lowered onto the
water surface. Replicate water samples for oxygen
determinations (Strickland and Parsons 1972)
were siphoned from the tank through a sampling
port every 12 min during feeding measurements,
and every 20 min during nonfeeding mea-
surements. The precision of the method was
±0.019 mg O2/I. Measurements of oxygen from
different locations in the tank demonstrated that
the movement of the fish kept it well mixed at all
times. Control measurements on the tank, filtered
seawater, and tank water after the addition of
phytoplankton demonstrated that these did not
contribute significantly to the change in oxygen
content of the water during respiration mea-
surements. The oxygen level in the tank was not
allowed to drop by more than 2 mg/1 during any
measurement; between measurements, the lid
was raised off the surface of the water, and air was
bubbled through the airstones along the tank
walls. The decline of oxygen in the tank with time
was linear, with a correlation coefficient of 0.98 or
better in all cases; the mean respiration rate of the
fish was calculated from the slope of this regres-
sion. Ninety-five percent confidence limits (CD
were computed for the slope and used to calculate
the 95% CL for the respiraton rate in each mea-
surement. Respiration rates are reported as mil-
ligrams oxygen consumption per gram wet weight
offish per hour (mg 02/g per h).

Swimming Speed

During the respiration measurements the
swimming behavior of the fish was recorded with a
Sankyo ES-44XL 8 mm movie camera, equipped
with a wide angle lens and a remote control and
mounted above the tank. The fish were photo-
graphed with Kodak Ektachrome 160 film, ex-
posed at 9 frames/s. Paired 10 s shots, 1 min apart,
were taken every 6-10 min while the fish were
feeding, and every 15-20 min when they were not
feeding. Films were later analyzed using a Kodak

Model MPG-TH microfilm reader at a magnifica-
tion of 34x. A sheet of clear acetate was placed
over the viewing screen, and the location of each
fish was plotted at every fifth frame (the corres-
ponding time interval at 9 frames/s = 5/9 si when
the fish were feeding and swimming rapidly, and
every 10th frame (or, every 10/9 s) when the fish
were not feeding and swimming slowly. These
measurements were then converted to swimming
speed in centimeters per second and body lengths
(BL) per second. Vertical travel by the fish, which
was not corrected for in this method, was negligi-
ble since the fish tended to maintain themselves at
middepth in the water column.

During each measurement of oxygen consump-
tion, an average of 680 observations of swimming
speed were obtained. The average swimming
speed during each measurement was determined
from the mean of all observations ±95% CL. The
distribution of swimming speeds within each mea-
surement was compared with a normal curve.
Measurements were compared by first testing for
homogeneity of variance, and when appropriate
the significance of the difference between means
was tested using analysis of variance. When var-
iances were nonhomogeneous, differences be-
tween means were tested according to a non-
parametric test.

The mean values of each measurement were
used to determine the relationship between
swimming speed and respiration rate. Mea-
surements were grouped into three categories: ini-
tial and final (unfed), feeding, and postfeeding. In
the latter two categories there was a linear rela-
tionship between swimming speed and log oxygen
consumption. Predictive regressions of y on X are
presented to permit the comparison of present re-
sults with those in earlier studies. However, we
also present the functional regressions (GM)
(Ricker 1973), which represent the geometric
mean of the regression of Y" on X and the recip-
rocal of the regression of X on Y. Although there
has been some controversy on the subject
(Jolicoeur 1975; Ricker 1975) the functional re-
gression nevertheless appears to be the preferable
method of describing the data. Differences in the
slopes and elevations of the regressions were
tested for significance by covariance analysis.

RESULTS

The menhaden were 3 yr old, with a mean fork
length of 25.8 cm (range 23.0-27.9 cm), a mean wet

879

FISHERY BULLETIN: VOL. 78, NO. 4

Table l. — Basic data on feeding experiments with a school of 12 Atlantic menhaden, total wet weight = 3,624
g. Oxycalorific coefficient used was 4.7 cal/ml of oxygen consumed (Kleiber 1961). Column numbers, in brackets,
are for text reference.

Total

respiration In excess of routine

Total

respiration in excess of routine

Experiment
no.

Total ration

d

jring

the 7-h feed

ng period

du

ring

tfie postfeeding period

G dry wt

Kcal

Mq02
(4)

Kcal

% of ration kcal

Mg02
(7)

Kcal % of ration kcal

(1)

(2)

(3)

(5)

(6)

(8) (9)

6

94.79

177.4

10.220

33.62

19.0

1.812

5.96 3.36

4

86.93

162.7

10,075

33.15

20.4

2,040

6.71 413

5

67.46

126.3

9,640

31.72

25.1

1,634

5.38 4.26

9

27.64

51-7

5,871

19.32

37.4

286

0.94 182

7

20.76

38.9

4,711

15.50

39.8

315

1.04 2.66

8

15.43

289

3,914

12.88

44.6

496

1.63 5.65

10

9.60

18.0

2,979

9.80

54.4

573

1.89 10.47

weight of 302 g (range 248-346 g), and a mean dry
weight of 104 g.

The food rations ranged from 0.79 to 7.8% of the
dry weight of the fish, and thus during the 7-h
feeding period the fish fed at rates equivalent to
0.11-1.11% of their dry weight per hour (Table 1).

In a filter feeder such as the Atlantic menhaden,
the food ration obtained depends on the volume of
water filtered, corrected for the filtration effi-
ciency of the gill rakers. The volume filtered is
essentially cylindrical, with cross-sectional area
equal to the area of the fish's open mouth, and
length equal to the distance swum by the fish in a
unit of time. It is shown below that the fish swam
at about the same average speed during feeding,

40

u

20

Q
LlI

^ 20
Q.

in

± 0
5 20

Exp. 4

J- I L

J L

Exp 9

J L

Exp. 7

_L

0600

1200

1800

Tl M E

2400

hour s

0600

1200

Figure l. — Meam voluntary swimming speed of a school of 12
Atlantic menhaden before, during, and after a 7-h period
(indicated by the heavy line on the x-axis) during which they
were fed, at a constant rate, a ration of the diatom Ditylum
brightwelli. Three representative experiments are shown, in
which total rations were: no. 4, 162.7 kcal; no. 9, 51.7 kcal; no.
7, 38.9 kcal. The 95% confidence limits were enclosed by the
symbols; horizontal bars indicate the duration of each experi-
ment.

and since all fish were of similar size, each fish
filtered an approximately equal volume of water
during the 7-h feeding period. Thus we assume
that each fish obtained the same proportion ( 1/12)
of the plankton added to the tank.

The behavior of the fish followed the same gen-
eral pattern in all experiments (Figures 1, 2). The
voluntary swimming speeds and respiration rates
of the fish were low during the initial measure-
ment and then abruptly increased severalfold over
the initial rates during feeding. When the input of
food was stopped, the fish rapidly filtered the re-
maining plankton from the water, decreasing
their swimming speed and respiration rate as the
plankton levels dropped. During the postfeeding
period there was a gradual return to prefeeding
activity levels and respiration rates, a transition
which was completed before the final two mea-
surements on the following morning.

0.4-

3 0.2

a>

S! 0
O

6 02

z
o 0

(r 0.4 -

oc

a.

CO 02

0600

-

^.-►*---^, Exp. 4

1
■

-

^ ^ t 1 - - - y^^ - - - . _

1 1 1 1 1 1 1

1 1 1

^-'--'-'-: Exp. 9

1 ■,

1 1 1 1 1 1 1

1 1 1

Exp. 7

-

1 11

1 ,
_ ^' m - •-•-• t-»-i

1 1 1 1 1 1 1

1 1 1

1200 1800 2400

TIME, hours

0600

1200

Figure 2. — Mean respiration rate for Atlantic menhaden in the
measurements presented in Figure 1. The 95% confidence limits
are shown by vertical bars when they exceed the size of the
symbol.

880

DURBIN ET AL.: SWIMMING SPEEDS AND RESPIRATION RATES OF ATLANTIC MENHADEN

In most measurements the distribution of
swimming speed observations showed small but
Statistically significant ( \2 <o.01 ) departures from
normality. These usually took the form of a slight
positive skewness, and leptokurtosis (data values
concentrated in the region of the mean).

The variance of the swimming speed, which in-
cluded the variability shown by each individual
fish, as well as differences among fish, was posi-
tively correlated with the mean. However, the
coefficient of variation revealed that the fish were
relatively more variable in their swimming be-
havior when they were not feeding (Figure 3).
These results confirmed qualitative observations
during the experiments that the fish were least
excitable, and most consistent in their swimming
behavior, when they were engaged in feeding.

With the exception of measurement no. 5, which
bracketed the transition from feeding to postfeed-
ing, the fish were very consistent in their swim-
ming behavior and respiration rate during indi-
vidual measurements. Thus the 95% CL about the

50r

5 40

<
>

O 30 -

O

77 20

O
o

10

o Initial and Final

• Post -Feeding

•

.0°°

^ Feeding

-

o°o° •
o6^^8

•

•

•

A

1 1

A
1 1 1 1

20 40

SWIMMING SPEED, cmsec"'

60

Figure 3. — Relationship between mean and coefficient of var-
iation (a/x [100%]) in the swimming speeds of a school of 12
Atlantic menhaden during the initial and final, feeding, and
postfeeding measurements.

estimates of mean respiration rate and swimming
speed during each of the measurements were
small, averaging ±8.9% of the mean respiration
rate and ±2.3% of the mean swimming speed.

Initial and Final Measurements
(No. 1, 9, 10)

These may be termed "routine" (Fry 1957) since
the fish were unfed and spontaneously active. Dur-
ing these measurements the fish swam slowly
about the tank without showing any strong school-
ing patterns. The mean swimming speeds and re-
spiration rates were very similar during the initial
and final measurements (Table 2). The range
among the mean voluntary swimming speeds of
the measurements was also fairly small, 10.5-15.2
cm/s (0.41-0.59 BL/s) (Figure 4). The range among

40

E
u

a 30

UJ
LU

a
en

o

20 -

10 -

e

o

-

0

_ft_

o

-

/% 8

0

/
/

/

-

/
1
1

29.62 (A-l)
'^ '^■^' 0.396*(A-I)

—

1

Where S = Swimming speed, cm-sec"'

-

A = XChl.g m tonk, ^L<i■ i '

1

1 1 1

1 1

1 1 1 1 1 1

2_ 4 6

X CHLOROPHYLL a

^g.

8
i-'

10

Figure 4. — Hyperbolic relationship between voluntary swim-
ming speed (S) of a school of 12 Atlantic menhaden feeding on
Ditylum brightwelli, and chlorophyll a concentration in the
water (A). The three measurements of mean swimming speed
obtained during the 7-h feeding period of each experiment are
plotted as a function of the mean chlorophyll a concentration
during each experimental feeding period.

Table 2. — Swimming speeds (S) and respiration rates (R) of Atlantic menhaden in the feeding experiments and their

regression equations.

Measurements (periods)

Initial (no. 1)
Final (no. 9, 10)

Mean s 95% contidence limits

Swimming speed
cm/s

Respiration rate
mg Oz/g per b

12.2±1.6
13.4±1.2

0 10 ±0.009
0.093:^0.007

Denved regressions

Predictive

Functional (GM)

Feeding (no. 2. 3,4)
Postfeeding (no. 6. 7)

log, oft = 0.0271 (S) - 1.446
r = 0.918. SE slope ■

log,ofl = 0.0293 (S) - 1.276
r = 0.856, SE slope ■

Equation (2)
0.0026

Equation (4)
0.0062

log,ofl = 0.0295 (S) - 1.534 Equation (3)
log,ofl = 0.0342 (S) - 1.342 Equation (5)

881

FISHERY BULLETIN: VOL. 78, NO. 4

the respiration rates was similarly narrow and
did not show any clear relationship with swim-
ming speed (Figure 4).

Feeding Measurements (No. 2, 3, 4)

As soon as food was added, the fish began "tast-
ing" the water by flaring their opercula and
swimming rapidly forward for a few seconds. After
1-2 min they began to feed, circuiting the tank and
swimming in the same direction at about the same
speed. Within each experiment, the mean volun-
tary swimming speed and the associated respira-
tion rate remained nearly constant throughout
the entire 7-h feeding period (Figures 1, 2). The
mean swimming speed was established during the
first 15 min of feeding and was related to the
amount of plankton in the water (Figure 4).
Within a range of about 1.5-4 /xg chlorophyll a/1
the voluntary swimming speed and respiration
rate of the fish were roughly proportional to the
chlorophyll a content of the water. Above about 4
^tg chlorophyll a/1 however, the swimming speed
was independent of plankton concentration. In the
three high-ration experiments during feeding, the
mean speed ±95% was 41.3±1.5 cm/s and the cor-
responding mean respiration rate was 0.48 ±0.029
mg 02/g per h. The relationship between
chlorophyll a concentration and the voluntary

o Initial and Final

• Post - Feeding

* Feeding

0.3 —

2 0.2 H
o

I-
<
a:

a.
</>

tr 0.1

009
008 —
0.07 —

0.06

10 20 30 40

SWIMMING SPEED, cm- sec''

Figure 5. — Relationships between mean voluntary swimming
speed and mean respiration rate of a school of 12 Atlantic
menhaden. The x and 95% confidence limits of the initial and
final measurements are shown; functional regressions shown for
the feeding and postfeeding measurements are presented in
Table 2. Inset is an arithmetic plot of Equation (3); extrapola-
tions beyond observed data are dashed.

swimming speed can be described by a rectangular
hyperbola [Equation (1), see Figure 4]. The zero
point for the curve was taken as the mean swim-
ming speed of unfed fish ( 12.2 cm/s) and the ap-
proximate concentration threshold (1 /u.g
chlorophyll a/1) (Durbin and Durbin 1975) of Z).
brightwelli at which Atlantic menhaden will begin
to feed.

In these experiments the mean voluntary
swimming speed of the Atlantic menhaden during
feeding ranged between 29.3 and 43.4 cm/s ( 1.14-
1.68 BL/s). This represented a 2.2-3.3 fold increase
over the mean prefeeding routine swimming speed
(12.2 cm/s). Respiration rates during feeding
ranged between 0.221 and 0.538 mg 02/g per h and
were thus elevated 2.2-5.4 fold over the mean ini-
tial routine respiration rate (0.10 mg 02/g per h).
There was a good linear relationship between the
mean swimming speed during feeding and the
logio transformed mean respiration rate (Figure 5,
Table 2).

Postfeeding Measurements (No. 6, 7, 8)

When the input of food was stopped at the end of
7 h, the fish rapidly depleted the plankton remain-
ing in the tank. Within 5 min the swimming speed
of the fish decreased noticeably, and as plankton
levels continued to decline, the fish progressively
reduced their swimming speed (Figure 1, mea-
surement 5). Respiration rates also declined (Fig-
ure 2). Feeding usually became intermittent
within 15-20 min, and ceased entirely during the
next one-half hour, at which time the plankton in
the tank had been reduced to a negligible level.

After the Atlantic menhaden had removed the
last of the plankton, they continued to "taste" the
water fairly frequently and were somewhat rest-
less, as though searching for additional food. Dur-
ing this postfeeding period, however, there was a
gradual return toward the prefeeding behavior.
Dusk arrived during or shortly after the second
postfeeding measurement. Although it was not
possible to photograph the fish during the third
postfeeding measurement at midnight, their ac-
tivity levels appeared to be very low as indicated
by their low respiration rates, and qualitative ob-
servations of their swimming behavior in the dim
light.

The postfeeding measurements were spaced too
far apart to precisely define the time by which the
fish returned to their routine activity and
metabolic levels. In general the duration of this

882

DURBIN ET AL.: SWIMMING SPEEDS AND RESPIRATION RATES OF ATLANTIC MENHADEN

period was greater with larger ration sizes (-4.5
h, experiment 4); at low food levels (e.g., experi-
ments 7, 9) the respiration rate had essentially
returned to baseline in <2 h (Figure 2).

The mean swimming speed of the first two post-
feeding measurements (no. 6, 7) usually fell
within the range of the routine swimming speeds;
however, the respiration rates tended to be ele-
vated above the routine rates (Figure 5). There
was a linear relationship between mean swim-
ming speed and logj^ respiration rate in these
postfeeding measurements (Figure 5, Table 2).

DISCUSSION

These results demonstrate that the voluntary
swimming speed of adult Atlantic menhaden is
related to the availability of plankton food in the
water. If food is not present, the voluntary swim-
ming speed and respiratory rate of Atlantic
menhaden are low. Swimming speed increases
during feeding, following an approximately hyper-
bolic relationship with increasing plankton den-
sity in the water. Over a wide range of plankton
concentrations the characteristic swimming speed
of the menhaden is about 1.60 BL/s, with a res-
piratory rate of about 0.48 mg 02/g per h. This
approximately 5-fold increase in respiratory rate
above the routine implies that the energy expendi-
tures during feeding will be a major element in the
energy budget of menhaden.

Previous descriptions of menhaden feeding
behavior (Durbin and Durbin 1975), based on
short-term experiments in which the plankton
concentration decreased during the course of each
experiment, were generally confirmed by the
present study. However, respiration rates mea-
sured in the present study indicate that the feed-
ing frenzy, which was observed in the earlier study
after a large amount of zooplankton was added to
the tank, is not likely to persist during prolonged
feeding in nature. Swimming speeds during the
frenzy were estimated to be about 2-2.5 BL/s. The
energy cost of swimming at these speeds, as esti-
mated from Equation 3 (Table 2), would be high
(10-23 times the routine metabolic rate) and would
not appear to be bioenergetically profitable over
prolonged periods.

The same general behavior patterns have been
observed in five groups of Atlantic menhaden col-
lected during three summers. Such consistency
indicates that the behavior of the Atlantic menha-

den in the laboratory can provide insight into
their behavior in the field. However, these labora-
tory based predictions of menhaden swimming
speeds need to be tested in the field.

Satiation has often been observed to be an im-
portant feature which affects the feeding behavior
of fishes (i.e., Ivlev 1961). This is most evident for
"macrophageous" fishes (those which take their
food in large particles). In the present study, how-
ever, there was no evidence of satiation even with
the largest ration, when the fish consumed the
equivalent of 8% of their body weight during a 7-h
period. Evidence of satiation would include a de-
crease in their swimming speed during the exper-
iments or a switch to intermittent feeding. In con-
trast, the fish fed continuously at a constant rate
as long as food was available, and they continued
to search for food after it stopped coming into the
tank. Plankton densities sufficient to saturate the
physical capacity of menhaden to handle and pro-
cess food may not be of much ecological signifi-
cance. This is because natural plankton popula-
tions in the size range which can be filtered by
menhaden are seldom found in concentrations
greater than those used in the present experi-
ments. The high concentrations of chlorophyll a
which occur in coastal and estuarine waters dur-
ing the summer are primarily small flagellates
(e.g., Durbin et al. 1975), which are too small to be
retained on the gill rakers of the menhaden (Dur-
bin and Durbin 1975).

There are comparatively few studies which have
simultaneously measured routine respiration rate
and activity. At very low swimming speeds, respi-
ration rate has been found to be linearly (Spoor
1946) and log linearly (Smit 1965; Muir et al.
1965) related to activity. In the present study, the
routine swimming speeds were clustered within a
narrow range (0.36-0.59 BL/s), and there was no
detectable relationship between respiration rate
and swimming speed.

In all of the nonfeeding (initial, final, postfeed-
ing) measurements, the respiration rates were
higher than those which would have been pre-
dicted from the observed swimming speeds and an
extrapolation of Equation (3) (Table 2, Figure 5).
Thus the respiration rates of the fish when they
were not feeding, and therefore swimming slowly,
were higher per unit swimming speed than when
the fish were feeding and swimming more rapidly.
These results were consistent with previous
studies, in which routine metabolic rates also
tended to be variable, and elevated above those

883

FISHERY BULLETIN: VOL. 78, NO. 4

predicted from respiration rate-swimming speed
relationships during long-term swimming at con-
stant speed (Brett 1964; Smit 1965; Muir and
Niimi 1972). Explanations for this phenomenon
include: 1) stress, which elevates the metabolic
rate, is reduced when the fish are occupied by some
activity such as swimming against a water cur-
rent (Brett 1964), or feeding, if the fish are nonag-
gressive (this study); 2) the intermittent swim-
ming of spontaneously active fish, accompanied by
frequent accelerations and changes in direction, is
hydrodynamically less efficient than the smooth
caudal locomotion of continuous swimming and
thus exacts a relatively higher metabolic cost
(Smit 1965).

The increased respiration rates during feeding
consumed a significant fraction of the energy ob-
tained from the ration (Table 1, column 6). Energy
expenditures above routine during the postfeeding
period averaged 4.61% of the energy contained in
the food ration (Table 1, column 9). The increased
metabolic rate during and soon after feeding ap-
peared to be primarily due to the increased volun-
tary swimming speed. Swimming speed accounted
for 84.3% of the variability in metabolic rate dur-
ing feeding and 73.3% during the postfeeding
period (Table 2). Other factors which may affect
the metabolic rate as a result of feeding include
changes in excitability of the fish, and the
calorigenic effect of the food ration (SDA, the
"specific dynamic affect").

The excitability of the fish is in practice difficult
to measure. Qualitative observations of the behav-
ior of the fish and the degree of variability in their
swimming behavior (Figure 3) indicated that ex-
citability was not a significant factor contributing
to the elevated respiration during feeding, but
could be important during the postfeeding period
of restlessness. The latter evidently resulted from
the abrupt termination of the input of food when
the fish were not satiated.

The cost of digestion and transformation of the
food, or SDA, has generally been measured as an
increase in oxygen consumption following feeding
(Kleiber 1961; Warren and Davis 1967). In several
earlier studies, in which fish were fed a single
meal over a brief period, the increase in oxygen
consumption peaked several hours after the meal,
then gradually subsided over a prolonged period
(as long as 2-3 d) to the prefeeding level (Muir and
Niimi 1972; Pierce and Wissing 1974; Beamish
1974). In these species, digestion of the food also
occurs over an extended period. The energy loss to

SDA was generally estimated to represent about
12-16% of the energy content of the ration.

The Atlantic menhaden results differed consid-
erably from these earlier studies. There was no
peak in oxygen consumption during the postfeed-
ing period, but instead a rapid and continuous
return of the metabolic rate to the prefeeding
level. This rapid return is consistent with the
rapid digestion rates observed for menhaden."*
Food was assimilated within 1-2 h after ingestion,
and approximately 80% of the food ingested dur-
ing the 7-h feeding period was digested and as-
similated within the same period. The amount of
energy expended above the routine during the
postfeeding period was larger in the larger ration
experiments (Table 1, columns 7, 8), which may
appear to indicate some effect of SDA. However;
voluntary activity levels were also higher in these
experiments. SDA is believed to be proportional to
ration size, but if the oxygen consumption at-
tributable to swimming activity. Equation (3) (Ta-
ble 2) is subtracted from the total respiration rate
during the postfeeding period, there was no rela-
tionship between ration size and the amount of
elevated respiration which can be ascribed to
SDA.

Thus, while Atlantic menhaden may be as-
sumed to experience some respiratory costs re-
lated to SDA, the major part of these will be in-
cluded as a part of the total respiratory increase
during feeding. In practice it would be very dif-
ficult to distinguish SDA in the total metabolism
because of the overwhelming effect of swimming
speed on the metabolic rate.

Equations (2) and (3) (Table 2) may be extrapo-
lated to zero activity to obtain an estimate of stan-
dard metabolism. These estimates, 0.036 mg 02/g
per h from Equation (2) and 0.029 mg Og/g per h
from Equation (3) are generally lower than those
reported from most other fishes which have been
studied (Table 3). Respiration rates which
menhaden sustained during feeding were also
high relative to those which can be sustained by
other species, and actually exceeded the active
rate (the maximum which can be maintained for 1
h) (Brett 1 964) of a number of species, including the
aholehole, largemouth bass, rainbow trout, and
tilapia (Table 3). Since the present study mea-
sured only voluntary respiration rates, the active

■'Durbin, E. G., and A. G. Durbin. Assimilation efficiency
and nitrogen excretion of a filter-feeding planktivore, the Atlan-
tic menhaden Brevoortia tyrannus. Unpubl. manuscr.

884

DURBIN ET AL.: SWIMMING SPEEDS AND RESPIRATION RATES OF ATLANTIC MENHADEN

Table 3— Metabolic rates among 10 fish species. Except where noted, rates were extrapolated to a 300 g fish, using
the appropriate weight-swimming speed-respiration relationships.

Temperature

Standard

Active

Species

( C)

mg Oj/g per h

mg Oj g per h

Author

Brook trout, Salvelinus fontinalis

20

0 153

Beamish (1964)

White sucker. Catostomus commersonii

20

0.086

Beamish (1964)

Brown bullhead, Ictalurus nebulosus

20

0 093

Beamish (1964)

Carp. Cypnnus carpio

20

0.043

Beamish (1964)

Tllapia, Tilapia nilotica

25

0086

0.378

Farmer and Beamish (1969)

Largemouth bass, Micropterus salmoides

20

-0.10

0 302

Beamish (1970)

Rainbow trout, Salmo gairdneri'

15

0.073

048

Webb (1971)

Aholehole, Kuhlia sandvicensis

23

0.043

0.387

Muir and Nlimi (1972)

Sockeye salmon, Oncorhynchus nerka

20

0.103

0.799

Brett and Glass (1973)

Atlantic menhaden, Brevoortia tyrannus''

20

0029

(0538)2

This study

'Actual measured values: x wet weight of rainbow trout = 272 g, and Atlantic menhaden
^Maximum voluntary metabolic rate in this study; presumably less than active rate.

302 g.

rate in menhaden remains unknown, though pre-
sumably higher than those reported here. Thus
the metabolic "scope" (Fry 1947) in menhaden ap-
pears to be significantly larger than that of many
species. A large metabolic scope is consistent with
Hartwell and Otto's ( 1978 ) finding that the critical
swimming speeds in juvenile Atlantic menhaden
far exceed those reported from other species: at 20°
C nonfeeding fish averaging 5.8 cm standard
length were able to maintain a speed of 15.8 BL/s
for 64 min and a speed of 20.8 BL/s for 2 min. In
contrast, at 20° C the critical speed of a 6 cm
sockeye salmon, for example, is only about 6.5
BL/s (Brett and Glass 1973).

The respiration during feeding increased sig-
nificantly faster per increment in swimming speed
in menhaden than in other species which have
been studied. In Atlantic menhaden an increase in
swimming speed of 1 BL/s caused a 5.8-fold in-
crease in the respiration rate (Table 2, Equation
(3)); while for eight species reviewed by Beamish
(1978) (Oncorhynchus nerka, Lepomis gibbosus,
Melanogrammus aeglefinus , Tilapia nilotica, Mi-
cropterus salmoides, Liza macrolepis, Cyprinus
carpio, Salmo gairdneri), a similar increase in
speed caused a roughly 2.3-fold elevation in the
metabolic rate. Thus the cost of increasing the
swimming speed is 2.5 times higher in Atlantic
menhaden during feeding than in these eight
species (which were not feeding).

The very steep slope of the swimming speed-
respiration relation for the Atlantic menhaden
indicates that during feeding, the loss in stream-
lining caused by the expanded opercula and the
resistance of the closely spaced gill rakers sub-
stantially increase the hydrodynamic drag of the
fish. It is likely that the respiratory cost for non-
feeding Atlantic menhaden swimming at equiva-
lent speeds would be much lower. It would be of

interest to determine the maximum swimming
performance of nonfeeding adult fish, for compar-
ison with Hartwell and Otto's (1978) data from
juveniles.

The rapidly increasing respiratory cost of
swimming during feeding is perhaps more clearly
illustrated when the relationship is plotted
arithmetically ( Figure 5, inset). The highest mean
voluntary swimming speed in the present experi-
ments, 43.4 cm/s or 1.68 BL/s, is very close to the
inflection of the curve in Figure 5 (inset), beyond
which an increase in swimming speed drastically
increases the metabolic rate. Because of the high
energy cost it is likely that in nature the voluntary
swimming speeds of adult Atlantic menhaden dur-
ing feeding will be <2 BL/s for most of the time.

In conclusion, the Atlantic menhaden, a filter-
feeding planktivore, offers an interesting contrast
to pelagic predaceous fishes, which have been
more widely studied (Durbin 1979). These pred-
ators typically consume their daily ration in a few
large meals (the}' are "macrophagists"). The time
and energy costs of feeding varies in different
species, and the energy lost to SDA is a conspicu-
ous component of their daily metabolism. In con-
trast, a "microphagist," such as the Atlantic
menhaden, consumes its food as a continuous
stream of very small food particles. While the
energy cost associated with feeding is consistently
high, in menhaden there is no extended period of
elevated respiration following feeding, as ob-
served in macrophagists, but rather a continuous
and rapid return to prefeeding rates.

ACKNOWLEDGMENT

We would like to thank Harold Loftes, skipper of
the Ocean State, and Charles Follett, skipper of
the Cindy Bett, for their assistance in obtaining

885

FISHERY BULLETIN: VOL. 78, NO. 4

menhaden. We also thank T. J. Smayda for the use
of his laboratory facilities, and the National Sci-
ence Foundation for support of this research under
grant OCE 7602572.

LITERATURE CITED

BEAMISH, F. W. H.

1964. Respiration of fishes with special emphasis on stan-
dard oxygen consumption. II. Influence of weight and tem-
perature on respiration of several species. Can. J. Zool.
42:177-188.
1970. Oxygen consumption of largemouth bass, Microp-
terus salmoides, in relation to swimming speed and tem-
perature. Can. J. Zool. 48:1221-1228.

1974. Apparent specific dynamic action of largemouth
bass, Micropterus salmoides. J. Fish. Res. Board Can.
31:1763-1769.

1978. Swimming capacity. In W. S. Hoar and D. J.
Randall (editors). Fish physiology, Vol. VII, p. 101-189.
Acad. Press.

Brett, J. R.

1964. The respiratory metabolism and swimming perfor-
mance of young sockeye salmon. J. Fish. Res. Board Can.
21:1183-1226.

Brett, J. R., and N. R. Glass.

1973. Metabolic rates and critical swimming speeds of
sockeye salmon iOncorhynchus nerka) in relation to size
and temperature. J. Fish. Res. Board Can. 30:379-387.
DURBIN, A. G.

1979. Food selection by plankton feeding fishes. In H.
Clepper (editor), Predator-prey systems in fisheries man-
agement, p. 203-218. Sport Fishing Institute, Wash., D.C.

DURBIN, A. G., AND E. G. DURBIN.

1975. Grazing rates of Atlantic menhaden Brevoortia
tyrannus, as a function of particle size and concentration.
Mar. Biol. (Berl.) 33:265-277.

DURBIN, E. G.

1977. Studies on the autecology of the marine diatom
Thalassiosira nordenskioeldii. II. The influence of cell size
on growth rate, and carbon, nitrogen, chlorophyll a and
silica content. J. Phycol. 13:150-155.

IVLEV,V. S.

1961. Experimental ecology of the feeding of fishes. Yale
Univ. Press, New Haven, 302 p.
PECK, J. I.

1894. On the food of menhaden. Bull. U.S. Fish Comm.
13:113-126.

Pierce, R. J., and T. E. Wissing.

1974. Energy cost of food utilization in the bluegill
(Lepomismacrochirus). Trans. Am. Fish. Soc. 103:38-45.

RICKER, W. E.

1973. Linear regressions in fishery biology. J. Fish. Res.
Board Can. 30:409-434.

1975. A note concerning Professor Jolicoeur's comments.
J. Fish. Res. Board Can. 32:1494-1498.

SKAZHINA, E. P

1975. Energy metabolism of anchovy Engraulis encras-
icholus L. when kept in a group or isolated and when
anesthetized with quinaldine. Dokl. Biol. Sci. Engl.
Transl. 225:557-558.
SMIT, H.

1965. Some experiments on the oxygen consumption of
goldfish iCarassius auratus L.) in relation to swimming
speed. Can. J. Zool. 43:623-633.
SPOOR, W. A,

1946. A quantitative study of the relationship between the
activity and oxygen consumption of the goldfish and its
application to the measurement of respiratory metabolism
in fishes. Biol. Bull. (Woods Hole) 91:312-325.

Strickland, J. D. H., and T. R. Parsons.

1972. A practical handbook of seawater analysis. Fish.
Res. Board Can. Bull. 167.

Warren, C. E., and G. E. Davis.

1967. Laboratory studies on the feeding, bioenergetics,
and growth offish. In S. D. Gerking (editor). The bio-
logical basis of freshwater fish production, p. 175-214.
Wiley, N.Y.
WEBB, P W

1971. The svnmming energetics of trout II. Oxygen con-
sumption and swimming efficiency. J. Exp. Biol.
55:521-540.
Yentsch, C. S., and D. W MENZEL.

1963. A method for the determination of phytoplankton
chlorophyll and phaeophytin by flourescence. Deep-Sea
Res. 10:221-231.

886

USING BOX-JENKINS MODELS TO FORECAST FISHERY
DYNAMICS: IDENTIFICATION, ESTIMATION, AND CHECKING

Roy Mendelssohn'

ABSTRACT

Box-Jenkins models are suggested as appropriate models for forecasting fishery dynamics. Unlike
standard production models, these models are empirical, dynamic, stochastic models. Box-Jenkins
models are not biased when estimating relationships between catch and effort, as are standard
production models. The use of these techniques is illustrated on catch and effort data for the skipjack
tuna fleet in Hawaii. An actual 12-month forecast is shown to give a reasonable fit to the observed data.
Most of the discrepancies are explained by changes in the behavior of the fishermen (i.e., economic
factors), rather than by lack of knowledge of the behavior of fish.

Accurate forecasting models would be useful in
fishery management because extended jurisdic-
tion and international agreements require pre-
seasonal predictions of the actual catch of a fleet.
In addition, improved forecasts of fish availability
can lead to improved planning by fishermen or by
processing firms. Forecasting techniques have
expanded greatly in the last years, but few have
been adapted to research in fisheries manage-
ment. Instead, techniques designed to establish
the equilibrium health of the stocks are also being
used to attempt dynamic forecasting.

At present, two least squares procedures are
being used to estimate the general production
model, the search procedure of Pella and Tom-
linson (1969) and the weighted least squares of
Fox (1970, 1971, 1975). The Fox procedure fits
catch per unit effort against a function of lagged
effort. Several authors (Chayes 1949; Eberhardt
1970; Atchley et al. 1976) have demonstrated that
scaling the dependent variable (i.e., catch) by
the independent variables (i.e., effort) biases
the fit by introducing artificial correlation into
the data. Johnston (1972) showed that ordinary
least squares gave biased estimates and an in-
flated F- statistic when used with variables lagged
on themselves. Neither the Fox nor the Pella-
Tomlinson procedure accounts for the effect of
autocorrelated errors in the estimation procedure
which Granger and Newbold (1977) and Newbold
and Davies (1978) have demonstrated bias both
estimation and tests of fit. An examination of the

residuals in Fox (1971, figure 3B) clearly shows
them to be autocorrelated. Residuals from many
spawner-recruit curves display similar behavior.

In this paper, the use of Box-Jenkins models
for modeling and forecasting fisheries dynamics
is explored. Box-Jenkins and other related fore-
casting techniques are specifically designed for
estimating and testing models in the presence
of autocorrelated errors. The fitted models are
stochastic rather than deterministic, thus reflect-
ing the variability found in most fisheries. The
models are constructed empirically, and are best
suited for forecasting. The models tell us little
about the long-term health of the stocks, so that a
judicious use of production, yield per recruit, and
accurate forecasting models is required to give the
best overall picture of the fishery.

My preference for Box-Jenkins models over
other forecasting methods now available is due to
the good documentation (see for example Ander-
son 1975; Box and Jenkins 1976; Granger and
Newbold 1977) and computer accessibility The
results presented here were obtained using a
package originally developed by David Pack at
Ohio State University and now available through
Automatic Forecasting Systems.^

The three-step process of model identification,
model estimation, and model diagnostic checking
is illustrated by developing a model that makes
monthly forecasts of skipjack tuna, Katsuwonus
pelamis, catches in Hawaii. Experience with the
model suggests that for a 12-mo forecast of catch.

'Southwest Fisheries Center Honolulu Laboratory, National
Marine Fisheries Service, NOAA, Honolulu, HI 96812.

Manuscript accepted May 1980.

FISHERY BULLETIN; VOL. 78, NO. 4, 198L

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

887'

FISHERY BULLETIN; VOL. 78, NO 4

during peak months the forecast is within 15% of
the observed catch (and is usually within 8-10% of
the observed catch), most turning points in the
catch trend are predicted, and the important
feature of a low, flat catch during the summer
months or high, peaked catches are accurately
predicted. Moreover, the reasons for forecasts with
large errors appear to be related more to fisher-
men's decisions in face of weather and economic
factors, than to mispredicting the availability
of the fish.

THE DATA AND
UNDERLYING MODEL

The data to be analyzed are landings of skipjack
tuna by approximately 12 boats from Oahu during
1964 through 1978. The raw data consist of the
daily landings (each boat rarely stayed out more
than a day or two), broken dovm by boat, and by
four skipjack tuna size classes: large, medium,
small, and extra small. For purposes of analysis.

the data were aggregated into monthly totals,
with the total number of fishing trips used as the
measure of fishing effort. For monthly catch and
effort during 1964-78 see Figures 1 and 2.

There are several causes for the observed sea-
sonal variability. First, the tuna are only avail-
able in large numbers seasonally. Second, price
considerations, particularly around Christmas
and New Year when there is large demand, tend to
spur fishing even when availability is low. Third,
with only 12 boats fishing, if 1 or 2 boats are not
able to fish for a few weeks, the catch will drop
sharply. Finally, environmental factors, partic-
ularly weather (such as bad seas) will affect the
landings since the boats are unable to fish.

Folklore in Hawaii has it that the catch remains
similar each year, no matter how many boats fish.
Comitini^ examined the fishery using dummy
variables and ordinary least squares to estimate

'Comitini, S. 1977. An economic analysis of the state of
thie Hawaiian skipjack tuna fisliery. Sea Grant Tech. Rep.
UNIHI-SEAGRANT-TR-78-01. 46 p.

800

' 1 1 I 1 1 I I I ■ T 1 1

1 1 1 1 ! 1 1 1 1 1 [

! 1 1 1 1 1 1 1 1 1 1

I I 1 ! I I I ■ 1 I I 1

I I 1 1 I 1 1 1 [ 1 1

600

1974

1975

1976 \

1977

1978

400

, 1 1 1 : i : i , ,

... 1 I , ( 1 1 1 i 1 tH

1 1 1 1 1 ; 1 , 1 1 ,

. . . 1 !

-

200
n

^J'^^

JFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASOND

MONTHS

Figure l. — Level of Hawaiian skipjack tuna catch by month, 1964-78.

888

MENDELSSOHN: USING BOX-JENKINS MODELS IN FISHERY DYNAMICS

a Cobbs-Douglas production function. He con-
cluded, among other things, that natural fluctua-
tions in resource availablity are significant, but
did not include them in his analysis, nor did he
provide a means for forecasting future catch. The
National Marine Fisheries Service, using a re-
gression model based on the previous year's catch,
water temperature, and salinity at the start of the
year, makes yearly predictions that have been
mixed in accuracy.

Box-Jenkins models are autoregressive-inte-
grated-moving-average models, or ARIMA mod-
els. These are linear, stochastic models that can
describe fairly complex behavior, in contrast to
Parrish and MacCall (1978) who use highly non-
linear equations to model the fluctuations in
fishery data.

The modeling is based on the properties of
stationary time series. A time series xt is station-
ary if it has a constant mean, and if the covariance
between events xt, xt-s depends only on s and not
on t. Many series are stationary after removing a

deterministic trend. Others are differenced in
order to achieve stationary. Also, transforming
the time series, particularly using the Box-Cox
family of transformations, often improves the
behavior of the time series. The initial step then is
to transform and difference the data as necessary
to achieve stationary. It is convenient to use the
backshift operator B-i, where B->xt - xt-j, to de-
note lagged variables. Given the new series zt
= (1 - B )xt, a mixture of autoregressive and
moving average models are sought. Autoregres-
sive models are models that depend on the past
history of the time series:

Zt = (b\Zt-i + (b2Zt-2 +■■•+ fi>pZt-p + at

in terms of the backshift operator:

(1 - <i>iB - (i)2fi2 -...- (bpBP)zt = at

while moving average models depend on past
values of the noise or error:

to

0.

UJ

m

IT

o

250

1969

1970

1971 A

1972

1973

200

/\

/\

1 \

/\

150

/ \

/ ^V

/ V

/ \jr\

100

^ / \ /■

\^

'^^\J \.

v_y

50

n

-

jFMAMJJASONDJFMAMJJASONDJfMAMJJASONDJFMAMJJASONDJFMAMJJASOND

MONTHS
Figure 2. — Number of fishing trips per month by the Hawaii skipjack tuna fleet 1964-78, near Oahu, Hawaii.

889

FISHERY BULLETIN: VOL 78, NO. 4

zt = at — O^at-i - 020-1-2 -■■■— Oqat-q

or:

Zt = a - 0,B - 628^ -...- OqB'^)at.

A model that has both moving average and auto-
regressive parameters is a mixed autoregressive
moving average model, whose representation in
terms of the backshift operator is:

(1 - (hiB - 626'' -...- (bpBPMl - B)'^xt

a - e^B - 02B'-

6qB'^)at.

MODEL IDENTIFICATION

The first step in the Box-Jenkins modeling
process is to use properties of the data to tenta-
tively identify a model. Even if a multivariate
model (i.e., a model based on catch and effort) is
the ultimate goal, univariate models of each series
are constructed first. Often the univariate model
produces forecasts that are almost as accurate as
the multivariate model forecast.

My procedure was to identify, estimate, and
check a series of models based on the data from
January 1964 through July 1977. These models
were used to forecast the already observed catch

and effort for the period August 1977-December
1978. The models with the best "fit" were then
reestimated to make the forecast for 1979. To
make clear the feedback nature of identification,
estimation, and checking in Box-Jenkins models,
results from models fixed to 163 and 180 mo of data
are intermingled, but clearly labeled.

A tentative model can be identified by esti-
mating the autocorrelation and partial autocor-
relation functions for each series. These are shown
in Figures 3 and 4. Significant is the undamped
sinusoidal behavior of each, with a period of 12 mo.
Failure of both the autocorrelation and partial
autocorrelation functions to go to zero is a sign
of a nonstationary series, and the need for dif-
ferencing. The 12-mo period suggested a yearly
seasonal model, so that twelfth differences were
taken, i.e., 2? = (1 - B^^)xt.

The estimated autocorrelation and partial auto-
correlation functions for the differenced catch and
effort series are given in Tables 1 and 2. Following
guidelines in appendix 9.1 in Box and Jenkins
(1976), seasonal models with period s of the form:

Zt = (1 - OiB - e2B^)a - eiB'}at da)

or zt= a - BiB - diB^)

(1 - OiB' - Q2B^')at (lb)

0.8

07

06

05

^-^

04

X

(.)

^

03

o

-J

<

02

1-

<.>

1-

0 1

2

o

1-

0

<

_l

llJ
q:

-0 1

(T

o

o

-02

C)

1-

3

<

-03

-04

-05

12

24 30

LAG IN MONTHS

36

42

48

Figure 3. — Estimated total catch autocorrelation function for the catch of skipjack tuna near Oahu, Hawaii, 1964-78.

890

MENDELSSOHN: USING BOX-JENKINS MODELS IN FISHERY DYNAMICS

Table l.— Autocorrelation functions for 12th differenced efTort series of the Hawaii skipjack tuna fleet, 1964-78.

Item

1

2

3

4

5

Lag (mo)
6 7

8

9

10

11

12

13

14

Regular auto.

SE

Partial auto.

039
08

.39

0.17
.09
.03

0.20
.10

.15

0.16
10
03

0.10

10

01

0.04

10
- 04

0.03
10
.00

0.07
.10
.00

-0.02

.10

-.08

-0.08

.10

-.07

-0.20

.10

-.19

-0.45

.10

- 39

-0.18
12

15

-0.08
12
04

Item

15

16

17

18

Lag (mo)
19 20

21

22

23

24

25

26

27

Regular auto.

-0.18

-0.13

-0 12

-0.17

-0.15

-0.17

-0,12

0.05

0.04

0.02

000

-0 07

003

SE

.12

12

12

.12

.12

.12

13

13

13

13

.13

13

13

Partial auto.

- 03

02

-.07

-.14

-.01

-.02

- 05

.16

- 08

-.19

.05

-.12

03

Table 2. — Autocorrelation functions for 12th differenced catch series of the Hawaii skipjack tuna fleet, 1964-78.

Item

1

2

3

4

5

Lag (mo)
6 7

8

9

10

11

12

13

14

Regular auto

0.58

0 40

0.33

0 20

0,11

0.05

0.01

0.02

-0 06

-0 12

-0.21

-0.38

-0.21

-0.15

SE

08

.11

12

12

.12

.12

.12

.12

.12

.12

.13

.13

.14

.14

Partial auto.

.58

09

10

-07

- 03

-.04

-.00

.04

-.11

-.07

-.17

-.29

.28

03

Item

15

16

17

18

Lag (mo)
19 20

21

22

23

24

25

26

27

Regular auto.

-0.16

-0.12

-0,08

-0,09

-0 08

-0.12

-0.10

-0 08

-0.08

-0.09

-0.06

-0.06

-0.05

SE

.14

.14

,14

,14

.14

14

.14

.14

.14

.14

.14

.14

.14

Partial auto

-.01

-.06

- 02

-.07

02

-.05

-.04

-.04

-.11

- 17

-.19

- 01

- 02

were hypothesized as the appropriate univariate
models for both the catch and the effort time

series.

ESTIMATION AND CHECKING

Given a tentative model, such as Model (1), the

next step is a recursive procedure of estimating
the parameters of the model, calculating the
autocorrelation and partial autocorrelation func-
tions of the residuals from the estimated model,
and then testing the residuals for significant
departure from the assumption that they are
white noise. When a final model has been identi-

o

0.7
06
0.5
0.4
0.3
0.2
0.1
0
-0.1
-0.2
-0.3
-0.4
-0 5
-0.6

FIGURE

IT
O
O
O

1-

<

p — I !—

12

18 24 30

LAG IN MONTHS

36

42

48

4. — Estimated effort autocorrelation function for the fishing trips by the Hawaii skipjack tuna fleet near Oahu,

Hawaii, 1964-78.

891

FISHERY BULLETIN: VOL. 78, NO. 4

fied, overfitting is tried, that is extra parameters
are added to see if they are found to be not
significantly different from zero.

To insure that I found the simplest model
possible, I fitted first the model zt = (1 - diB)
(1 - QiB^^)at, and then added parameters as
seemed necessary based on the diagnostic check-
ing. The estimates for Model (1) for catch and
effort are given in Tables 3 and 4. Estimates
using two estimation techniques, one using back-
forecasting and one suppressing it, are presented.
Some programs do not have a backforecasting
feature; my experience is that the estimated
models obtained using backforecasting are far
superior, as can be seen in the tables presented.

Table 3.

Parameter

-Parameter estimates for effort model, Model (1)
(see text). (Based on 180 observations.)

Estimate

supressing

backtorecasting

SE

Estimate using
backforecasting

SE

Si

-0.38349

0.07942

-0,44756 0.07886

«2

-.11326

07996

-.12795 07911

©1

.5894

.08122

.99493 .00650

e.

.00069

08609

— —

X^ statistic

on residuals

26.894 with 44 df

37.31 9 with 45 df

Residual

mean square

1.018.60

755.270

Residual SE

31.915

27.482

Residual mean

1.629

0.5338

Table 4. — Parameter estimates for catch model, Model (1)
(see text). (Based on 163 observations.)

Parameter

Estimate suppressing
backforecasting

SE

^1

-0.54100

0.08190

«2

-.22745

08235

e,

.75314

08718

e.

05184

.09256

X^ statistic on residuals

27,470 witti 43 df

Residual mean square

165,410

Residual SE

406.71

Residual mean

17.506

The estimated autocorrelation and partial auto-
correlation functions of the residuals from both
models are given in Tables 5 and 6. For the effort
series, there is no sign of a lack of fit, while for
the catch series terms of lag three or four are
suggested. An overspecified model:

Zt

= (1 - B^B^ - O2B'' - OsB"" - e^B^)

(1 - QiB^'')at (2)

was estimated for both the catch and effort time
series. The results are summarized in Tables 7 and
8. The estimated autocorrelation and partial auto-

892

correlation functions of the residuals (not shown)
show no sign of additional lags or trend. The test
statistic that the residual series are not signifi-
cantly different from white noise gave no reason
to doubt the models adequacy, and overfitting by
including a GaB^"* term found this term to be
nonsignificant.

TRANSFER FUNCTION MODELS

If both the catch time series, say yt, and the
effort time series, say xt, have been suitably
transformed so that the resulting series are sta-
tionary, a transfer function of the form:

(1 - 81B - SaB^ -...- ^rB'')xt

(ojo — oiiB — oiiB'

o)sB^)yt-b + rjt

can be estimated where rjt is not assumed to be
white noise, but itself can be modeled as an
autoregressive-moving average process of a^.

The procedures for identifying and estimating a
transfer function model are similar to those for the
univariate model, except that attention is focused
on the estimated cross-correlation function be-
tween the "pre whitened" catch and effort series.
Series are prewhitened if they are reduced to the
residuals left from a given model. In this instance,
both series are prewhitened by the univariate
model for effort estimated in the preceding sec-
tion. The estimated correlation function, impulse
response function, and residual noise autocorrela-
tion function are given in Table 9. The estimated
autocorrelation function for the noise is similar
to the original univariate autocorrelations, sug-
gesting a noise model of the form:

T,, = (1 - 0iB - diB"" - dzB^ - d^B^)

(1 - Q^B^'')at. (3)

Based on guidelines in Box and Jenkins ( 1976:386-
388) and knowledge of the fishery, two models
were hypothesized:

a-B^'')yt= {ojo){l-B^'')xt+ y]t (4)

and: {1 - h^B - h^B"") (l - B^^)yt

= (ojo - wi5 - waB^) (1 - B'^)JCi + r]t. (5)

Tables 10 and 11 summarize the estimates when

MENDELSSOHN: USING BOX-JENKINS MODELS IN FISHERY DYNAMICS

Table 5. — Estimated autocorrelation function for residuals of effort model for the Hawaii skipjack tuna

fleet, 1964-78.

Item

1

2

3

4

Lag (mo)
5 6

7

8

9

10

11

12

Auto.
SE

0.01
.07

0.03
.07

009
.07

0.06
08

004 -0.11
08 .08

-0.05
.08

0 04
08

-0 09
08

0.02
08

003
08

-0 01
.08

Item

13

14

15

16

Lag (mo)
17 18

19

20

21

22

23

24

Auto.
SE

0.05
.08

-0.01
08

-0 04
08

-0.09
.08

-0.08 -0.09
.08 .08

-0 07
08

-0.08
.08

-0.16
.08

0.10
.08

0.07
.08

-0 02
.08

Table 6. — Estimated autocorrelation function for residuals of catch model for the Hawaii skipjack tuna

fleet, 1964-78.

Item

1

2

3

4

Lag (mo)
5 6

7

8

9

10

11

12

Auto.
SE

0.04
08

0,11
08

0.23
08

0.06
.09

0 06 -0.05
.09 .09

0.00
09

0.10
.09

-0.03
09

0.04
.09

0.01
.09

0.00
.09

Item

13

14

15

16

Lag (mo)
17 18

19

20

21

22

23

24

Auto.
SE

0.05
.09

-0.01
09

-0.07
.09

-0.01
.09

-0 00 -0.04
09 .09

0.00
.09

-0.01
.09

-0.06
.09

0.01
.09

-0.04
.09

-0.03
09

Table 7. — Parameter estimates for effort model. Model (2)
(see text). (Based on 180 observations.)

backforecasting is used in estimating the pa-
rameters for Models (4) and (5). The chi-square
statistics show no reason to suspect model inade-
quacy. The residuals show no significant cross-
correlation with total catch, when l/V 180 (180
observations in the series) is used as a rough
standard error. The residual autocorrelation func-
tion shows spikes around lag 15 that are higher
than would be desired, but overall the fit is
reasonable, and the model residuals could reason-
ably be modeled as white noise.

DISCUSSION AND FORECASTS

Two transfer function models and one univari-
ate model have been used to forecast the catch and
effort in the skipjack tuna fishery during 1979. It
is worth emphasizing that the original 12-mo fore-
casts were made in January 1979 and the updated
forecasts were made in May 1979, so the reported
results are true forecasts — there was no a priori
knowledge of the data to help improve the "fit" of
the forecasts. The original catch and effort fore-
casts are given in Tables 12 and 13 while the
updated catch forecasts are given in Table 14.

The models used to produce the forecasts are
best understood when written out in difference
equation form. The univariate model for catch is:

yt = yt-s.2 + iat + 0.538a/-i + 0.438a;-2 + 0.412a^-3 + 0.309a;-4) (6)
- (0.996ai-i2 + 0.5350^-13 + 0.436a;-i4 + 0.410a<-i5 + O.SOSa^-ie),

Estimate

Parameter

suppressing
bacldorecasting

SE

Estimate using
backforecasting

SE

«,

-0.36746

0.08004

-0.43862

007930

»2

-.14976

08412

-.18144

.08590

«3

-.16111

.08458

-.15377

08617

«4

- . 1 7096

,08454

-.16298

.08593

h

-.11547

.08089

-.17291

.07998

B,

.59065

.06431

99483

.00033

X^ Statistic

on residuals

20.696 with 42 df

27.494 with 42 df

Residual

mean square

1 ,000.40

752.67

Residual SE

31.629

27.435

Residual mean

.82151

.35175

Table 8. — Parameter estimates for catch model, Model (2)

(

see text). (Based

on 180 observations.)

Parameter

Estimate

suppressing

backforecasting

SE

Estimate using
backforecasting

SE

e,

-0.55368

0.07972

-0.53771

0.07462

»2

-.35882

08989

-.43825

07543

»3

-.33817

.09056

-.41197

.01144

»4

-.24282

09012

-.30909

07479

^5

-.12294

.07994

-.14974

07440

e,

.76951

.05062

.99585

00825

\ Statistic

on residuals

1 5.092 with 42 df

20.384 with 42 df

Residual

mean square

143,240

115.170

Residual SE

37847

339.37

Residual mean

21150

3.3299

893

FISHERY BULLETIN: VOL. 78, NO. 4

i.e., catch this month is equal to the catch during
the same month last year, adjusted by a difference
of the weighted sums of the forecasting errors over
the previous 4 mo. If the forecasts this year have
consistently underpredicted compared with last
year's forecasts, then the estimated catch is in-
creased, while if the forecasts this year have
consistently overpredicted compared with last
year's forecasts, then the estimated catch is
decreased. The forecast maintains a balance be-
tween keeping the catch in equilibrium and keep-
ing the error in equilibrium.

This impression of a yearly cycle with variabil-
ity is reinforced when examining the polynomial

Table 9. — Estimated cross-correlation function, impulse re-
sponse function, and noise autocovariance function for a
catch-effort transfer model for the Hawaii skipjack tuna fleet,
1964-78.

Table ll. — Parameter estimates for transfer model. Model (5)
(see text). (Based on 180 observations.)

Lag
(mo)

Estimated
cross-correlation

Estimated noise
autocovariance

SE

Estimated

impulse

response

weights

0

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

20

21

22

23

24

25

26

0.651

.080

.070

.086

-.033

.044

-.098

.099

.103

-.017

.043

-.040

-.20

.026

-.109

.003

-.098

.014

-.110

-.037

.006

-.006

-.108

.012

-.108

-.001

-.108

0.49

.21

.16

.16

.10

.07

.03

.13

.14

-.05

-.14

-.26

-.05

.05

-.12

-.16

-.01

-.05

-.12

-.12

-.16

-.11

-.18

-.21

-.09

-.08

0,10
.12
.12
.13
.13
.13
.13
.13
.13
.13
.13
.13
.14
.14
.14
.14
.14
.14
.14
.14
.14
.14
.15
.15
.15
.15

8409

1.035

.903

1.111

-.431

.566

-1.269

1.276

1.334

-.215

.556

-.517

- 1 .555

.338

- 1 .404

-.038

-.415

.043

- 1 .271

.185

- 1 .422

-.475

.080

-.075

- 1 .393

.181

- 1 .390

Table 10. — Parameter estimates for transfer model. Model (4)
(see text). (Based on 180 observations.)

Parameter

Estimate

suppressing

backforecasting

SE

Estimate using
backforecasting

SE

O>0

e,

X^ statistic
on residuals

Residual
mean square

Residual SE

Residual mean

7.5989
- 47621
-.32874
-.17034
-.20033
.83384

0.69403
07993
.08734
08803
07905
05271

8.0003
-.48894
-.32633
-.14853
-.17506
.99587

0.83561
.07851
.08541
.08666
07822
.00707

34.953 with 43 df

83,323
288 66
-15.152

32.018 with 43 df

71,300
267.02
0.18650

Estimate

suppressing

Estimate using

Parameter

backforecasting

SE

backforecasting

SE

8,

0.01286

0,30389

0,86672

022308

8j

,88121

28641

- 70763

21659

OJq

7,3488

73352

81855

,82832

CO,

-1,3011

2-16847

6,7421

1,71214

to 2

68509

2,34577

-7.3133

1.58459

",

- 49924

08302

-.46980

08013

Hj

- 29495

,09102

-.33234

08870

"3

-.16384

09191

-.17199

09012

"i

-.13639

,08352

-.21746

08098

Bi

,83311

,05511

.99543

00623

X^ statistic

on residuals

33.067 with 43 df

38,906 with 43 df

Residual

mean square

85,673

69,066

Residual SE

292.70

262.80

Residual mean

-1,9979

-2.4666

Table 12. — Catch forecasts for 1979 for the Hawaii skipjack
tuna fleet from Models (1),(4), and (5) (see text).

Model

Month

(4)

(5)

(1)

Observed catch

Jan.

102.24

157.48

159.97

52.6488

Feb.

7891

123.32

117.81

74,1184

Mar.

121,86

11883

108.40

102,4088

Apr.

202,05

169.75

175.82

131 0658

May

423.40

406.87

423.95

470 5450

June

595.39

605.68

598.17

358,5100

July

666.16

684.99

607,07

600,6930

Aug.

528.09

535.73

523 14

600,5200

Sept.

297.96

294.92

291.97

148,3070

Oct

224.28

216.64

222.96

79.3360

Nov.

173.99

168.83

172.94

27 5084

Dec.

133.22

131.61

132.58

84.7755

Total

3.547.55

3,614.65

3.534.78

2,730,4367

Table 13. — Predicted and observed number of fishing trips for
the Hawaii skipjack tuna fleet in 1979.

Month

Original prediction

Updated prediction

Observed

Jan

Feb,

Mar.

Apr.

May

June

July

Aug.

Sept.

Oct.

Nov.

Dec.

98.93
97.50
101.06
122.30
174.00
196,16
209.37
183.04
139.18
121.20
104.23
100.92

167.71
187.36
206.14
179.81
138.73
120.45
104.83
100.51

53

75

78

118

173

182

200

174

84

84

51

109

Table 14. — Updated forecasts of total catch for 1979 for the
Hawaii skipjack tuna fleet.

Model

Month

(4)

(5)

(1)

Observed catch

May

June

July

Aug,

Sept,

Oct.

Nov.

Dec.

Total

393.214
547.014
644.638
500,151
293,130
220,557
174,567
130,947

2,904.218

382.430
586.400
705.137
527,945
283,067
197.953
164 720
136,831

2.984 483

401,874
589.524
668.895
521.456
289.516
222.806
173.594
133.148

3,000.813

470.545
358510
600.693
600.520
148,307
79,336
27,5084
84,7755
2,370,1949

894

MENDELSSOHN: USING BOX-JENKINS MODELS IN FISHERY DYNAMICS

representation of Model (1). The value of Bi is
nearly one. Thus the term (1 - B^^) appears on
both sides of the equation, and can be cancelled.
Abraham and Box (1978) showed that this is
sufficient reason to suspect a deterministic cosine
function trend with a moving average model
around the trend. Given the high residual mean
square for the model (115, 170), this latter inter-
pretation is consistent with the folklore on the
fishery — highly variable but on the average
things are similar from year to year.
The first transfer function model is:

within 89c of the observed total catch, and for the
period July 1977- December 1978 the model fore-
casted within 12% of the observed total catch.

Except for June 1979, the summer months were
predicted accurately. Experience with the model
on the data from July 1977 suggests that the
summer months are almost always predicted
within 10% of the observed catch. In fact, in March
1979, an industry representative doubted the high
catch forecasted for the summer, due to the low
catch in January and February 1979. Similarly,
the sharp drop in catch in September was pre-

yt = 8.003X? + (yt-i2 - 8.003xr-i2) + (at + 0.489a^-i + 0.326a;-2 + 0.149a(-3 + 0.175a<-
- (0.996a?-i2 + 0.487a;-i3 + 0.325ai-i4 + 0.148a^-i5 + 0.174a/-i6).

) (7)

This model has an interpretation similar to that
of the univariate model, except now catch per
weighted units of effort are compared between
years. The second transfer function model com-
pares lagged values of catch and effort also.

It is difficult to judge the value of a forecast,
since this will depend on the use being made of the
forecast and the alternatives available. Granger
and Newbold (1977) suggested the most appropri-
ate measure of the value of a forecast is a loss
function which reflects the loss from inaccurate
forecast in the actual application for which the
forecasts were developed. For forecasting the skip-
jack tuna fishery in Hawaii, there were four
immediate goals. The first was to give a reason-
ably accurate estimate of total catch over the
year, within a 15-20% error rate. The second
was to predict what kind of summer it would be.
May through September being the main fishing
months. This means predicting what month the
fish start running, what month the fish stop
running, and whether the catch is high and
peaked as in 1979, or flat and low as in 1978. An
important concern is the relative size of the drop
in catch when it occurs in September or October.

A third concern was an accurate forecast of the
catch in December, when the holiday demand for
Sashimi (a Japanese raw flsh delicacy) drives
prices very high. And finally, an increased under-
standing of the dynamics of the fishery was
desired.

Based on these criteria, I feel the forecasts have
performed well, especially compared with any
alternative available. The error in predicting the
1979 total catch is higher than desired. However,
for the last 6 mo of 1977 the model forecasted

dieted by the model. Again, in August 1979 an
industry representative doubted that a sharp
decline in catch would occur in September, but
said that this could be a useful piece of knowledge
since their decisions would change if they knew
they could expect the supply to drop sharply.

The forecasts have provided insight into the
fishery. The major failures of the forecasts were
January 1979 and October-December 1979. Jan-
uary 1979 was a period of unusually bad storms, so
that few fishing trips were made. However, the
observed catch per trip was 0.993 metric tons (t),
while Model (4) predicted a catch per trip of 1.033 1.
The main source of the error in the forecast was
the predicted number of trips to be made.

Similarly, the high summer catches, coupled
with very high catches of yellowfin tuna, drove the
price for skipjack tuna to very low levels. At the
end of September, most of the boats went into
drydock because of the prevailing low prices. The
few boats that remained tended not to be the
industry leaders (i.e., boats with a proven record of
higher catch rates), and made only short forays
rather than their usual fishing trips.

The point of these explanations is that the
causes of the poor forecasts appear to be related
not to the behavior of the fish stocks but rather to
the behavior of the fishermen. Therefore, the
effort to improve the forecasts needs to be di-
rected at understanding the fishery, rather than
the fish. (An economic study of the industry is
near completion.)

Finally, water temperature and salinity data
for one location off Oahu were included in the
transfer function models. These variables added
little to the forecasts, and since there is no

895

mechanistic explanation as to why these variables
should affect the catch and effort, they are not
being used at this time in the forecasts. (How-
ever, the ability to include random environmental
factors into the forecasting model is an advantage
when using stochastic models as compared with
the normal deterministic production models.) Dis-
aggregating by size class might also improve the
forecasts. Prior to 1973, the catch of the large
skipjack tuna and the total catch were highly
correlated. Since 1973, this has not been true and
there has been a definite change in the size
composition of the catch. A disaggregated inter-
vention model may be able to explain this change.

SUMMARY

Box-Jenkins models have been proposed as
an alternate model for forecasting fishery data.
ARIMA models provide maximum likelihood esti-
mators that are not biased when the data is
seasonal and autocorrelated, and when a variable
is lagged on itself. Techniques are explored which
allow the model to be constructed from the data
up, rather than from theoretical models that may
not be supported by the data. The procedure is
illustrated on skipjack tuna catches in Hawaii,
which traditionally has been considered too
variable to forecast on a monthly basis in a
reasonable manner.

ACKNOWLEDGMENTS

I am indebted to Lisa Katekaru for her invalu-
able assistance in performing most of the pro-
gramming for this paper. Robin Allen and two
anonymous referees provided several comments
that have improved the presentation and discus-
sion of this paper.

FISHERY BULLETIN: VOL 78, NO. 4

LITERATURE CITED

ABRAHAM, B., AND G. E. P. BOX.

1978. Deterministic and forecast-adaptive time-
dependent models. Appl. Stat. 27:120-130.
ANDER.SON.O. D.

1975. Time series analysis and forecasting: The Box-
Jenkins approach. Butterworths, Lond., 182 p.

ATCHLEY, W. R., C. T GASKINS, AND D. ANDERSON.

1976. Statistical properties of ratios: I. Empirical re-
sults. Syst. Zool. 25:137-148.

Box, G. E. P., AND G. M. JENKINS.

1976. Time series analysis: forecasting and control. Rev.
ed. Holden-Day, San Franc, 575 p.

CHAYES, F.

1949. On ratio correlation in petrography. J. Geol. 57:
239-254.
EBERHARDT, L. L.

1970. Correlation, regression, and density dependence.
Ecology 51:306-310.
Fox, WW, JR.

1970. An exponential surplus-yield model for optimizing
exploited fish populations. Trans. Am. Fish. Soc. 99:
80-88.

1971. Random variability and parameter estimation for
the generalized production model. Fish. Bull., U.S. 69:
569-580.

1975. Fitting the generalized stock production model by
least-squares and equilibrium approximation. Fish.
Bull., U.S. 73:23-37.

Granger, C. W J., and P Newbold.

1977. Forecasting economic time series. Acad. Press,
N.Y.,333p.

Johnston, J.

1972. Econometric methods. 2d ed. McGraw-Hill, N.Y.,
437 p.

Newbold, R, and n. Davies.

1978. Error mis-specification and spurious regressions.
Int. Econ. Rev 19:513-519.

Parrish, r. h.. and a. D. MacCall.

1978. Climatic variation and exploitation in the Pacific
mackerel fishery. Calif. Dep. Fish Game, Fish Bull. 167,
110 p.

PELLA, J. J., AND R K. TOMLINSON.

1969. A generalized stock production model. Inter-Am.
Trop. lYina Comm., Bull. 13:419-496.

896

DEVELOPMENT OF LARVAL SMOOTH FLOUNDER, LIOPSETTA PUTNAMI,
WITH A REDESCRIPTION OF DEVELOPMENT OF WINTER FLOUNDER,
PSEUDOPLEURONECTES AMERICANUS (FAMILY PLEURONECTIDAE)'

Wayne A. Laroche^

ABSTRACT

Larval development is described lor the first time for Liopsetta putnami and redescribed for Pseudo-
pleuronectes amenca«!/s (Pleuronectidae). These species cooccur as larvae in Gulf of Maine estuaries
during the spring and have previously been difficult to separate, especially as small larvae, due to their
similar development and the lack of adequate published descriptions. Characters which distinguish L.
putnami from P. americanus larvae include: presence of darkly pigmented eyes in yolk-sac larvae; lack
of internal melanophores over the notochord in larvae greater than 3.2 mm; lack of melanophores on
the fins of yolk-sac, preflexion, and flexion larvae; and higher ratio of snout to anus length /standard
length (averages 43.6 and 41.2'7f standard length for yolk-sac and preflexion larvae versus 33.3 and
37.69f standard length for yolk-sac and preflexion larval P. americanus).

The smooth flounder, Liopsetta putnami (Gill),
Family Pleuronectidae, occurs in the western
North Atlantic Ocean from Ungava Bay, Quebec,
to Providence, R.I. It is found chiefly over muddy
bottoms in estuaries and nearshore, marine
waters <10 m deep (Bigelow and Schroeder 1953;
Leim and Scott 1966). The winter flounder,
Pseudopleuronectes americanus (Walbaum), Fam-
ily Pleuronectidae, occurs from Battle Harbour
and Windy Tickle, Labrador (lat. 55°45' N), to
Georgia. It is caught over hard bottoms to depths of
=142 m on the offshore fishing banks and also in
estuaries and nearshore, marine waters (Bigelow
and Schroeder 1953; Leim and Scott 1966). From
Providence, R.I., northwards, L. putnami and P.
americanus cooccur in shallow coastal and es-
tuarine waters where both are known to spawn
(Bigelow and Schroeder 1953).

Previously, two large larvae and one small
juvenile L. putnami have been illustrated and de-
scribed (Laszlo 1972), while larval and juvenile P.
americanus have been illustrated and their devel-
opment briefly described in various publications
(Sullivan 1915; Breder 1923; Bigelow and Welsh
1925; Bigelow and Schroeder 1953; Scotton et al.
1973; Lippson and Moran 1974; Klein-MacPhee

'Contribution No. 139 from the Ira C. Darling Center, Univer-
sity of Maine. Walpole, Maine. Supported in part by a con-
tract from Maine Yankee Atomic Power Company to the Ira C.
Darling Center of the University of Maine, Orono.

^Ira C. Darling Center, University of Maine, Walpole, Maine;
present address: Gulf Coast Research Laboratory, PO. Drawer
AG, Ocean Springs, MS 39564.

1978; Martin and Drewry 1978; and others). How-
ever, existing descriptions of P americanus do not
accurately present all characters necessary for re-
liable separation of small larvae when the species
cooccur.

This paper describes the larval development of
L. putnami for the first time from reared and
field-collected specimens, redescribes the larval
development o{ P. americanus , and compares the
two.

METHODS

Two ripe female and one ripe male L. putnami
were collected from the cooling water intake
screens of the Maine Yankee Atomic Power Plant
located on Montsweag Bay, Wiscasset, Maine, on 7
February 1974. Most L. putnami collected on that
date were spent. The ripe fish were artificially
spawned, and the eggs were fertilized in the field.
Eggs were kept at 5° C in darkened containers of
gently aerated 23%o salinity water, conditions ap-
proximating those at the capture site. Field-
collected larvae were captured in February and
March and also were reared in the laboratory. Lar-
vae were fed field-collected plankton.

Larvae of both L. putnami and P. americanus
were collected and preserved in 3-5% Formalin^
during 1972, 1973, and 1974 from the Sheepscot

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

Manuscnpt accepted April 1980.

FISHERY BULLETIN: VOL. 78. NO. 4, 1981.

897

FISHERY BULLETIN: VOL. 78. NO. 4

and Damariscotta River estuary systems. Larvae
were collected with meter nets, V> m buoyed and
anchored nets, and a small beam trawl. The small-
est L. putnami larvae (3.1 and 3.6 mm) were
hatched from the artificially spawned eggs. The
7.1 and 7.6 mm specimens were field collected as
small larvae and reared in the laboratory. All
other specimens in the series were field collected
and preserved. The P. americanus series includes
only field-collected specimens.

Some specimens were lightly stained with aliza-
rin to facilitate counting of body parts. Illustra-
tions were prepared using a camera lucida. Mea-
surements were taken on the right side of each
specimen with an ocular micrometer mounted in a
dissecting microscope. Measurements taken in-
clude:

Standard length (SL) = snout tip to notochord tip
preceding development of caudal fin, then to
posterior margin of hypural plate.

Total length (TL) = snout tip to tip of caudal fin
membrane or fin rays.

Snout to anus length = horizontal distance from
snout tip to a vertical through posterior margin
of large intestine at anus.

Head length (HL) = snout tip to posterior margin
of otic capsule until cleithrum becomes visible
(5.4 mm in L. putnami vs. 3.7 mm in P.
americanus), then to the cleithrum; to the pos-
terior margin of the operculum on postflexion
larvae >7.0 mm of both species.

Snout length = snout tip to anterior margin of
orbit of right eye.

Upper jaw length = snout tip to posterior margin
of maxillary.

Eye diameter = greatest width of right eye.

Body depth at pectoral fin base = vertical distance
across body at pectoral fin base, not including
depth of dorsal fin pterygiophores.

Maximum body depth at pectoral fin base = verti-
cal distance across body at pectoral fin base in-
cluding depth of dorsal fin pterygiophores.

Body depth behind anus = vertical distance across
body immediately posterior to anus, not includ-
ing depth of dorsal fin pterygiophores.

Maximum body depth behind anus = vertical dis-
tance across body immediately posterior to anus
including depth of dorsal fin pterygiophores.

Pectoral fin length = distance from base to tip of
fin fold or longest fin ray.

Pectoral fin base depth = width of base of pectoral
fin.

Pelvic fin length = distance from insertion of pel-
vic fin to tip of fin fold or longest ray.

Vertebral and fin ray counts were made on
juveniles with the aid of radiographs. All length
measurements are standard length unless other-
wise stated.

TERMINOLOGY

Yolk-sac larva = prior to absorption of yolk mate-
rial.

Preflexion larva = prior to notochord flexion.

Flexion larva = undergoing notochord flexion
from time urostyle begins to slant upward until
urostyle is in flnal upturned position and caudal
fln is formed.

Postflexion larva = from alignment of urostyle in
final upturned position and caudal fin formation
until attainment of adult dorsal and anal fin
complements.

Transforming larva = from onset of migration of
left eye, development of juvenile pigment pat-
tern, and change in behavior from pelagic
swimming to benthic habit until completion of
these processes and attainment of adult pelvic
and pectoral fin ray complements.

IDENTIFICATION

Liopsetta putnami and P. americanus are the only
Gulf of Maine flatfishes that commonly are found
in estuaries and that spawn during late winter-
early spring (Bigelow and Schroeder 1953).
American plaice, Hippoglossoides platessoides ,
and Atlantic halibut, Hippoglossus hippoglossus ,
also spawn during late winter-early spring but
rarely enter Gulf of Maine estuaries (Bigelow and
Schroeder 1953). Larval Hippoglossoides plates-
soides were described by Bigelow and Schroeder
(1953) and have three vertical bands of melanistic
pigment across the postanal region. Martin and
Drewry (1978) compiled and summarized descrip-
tions of larval Hippoglossus hippoglossus which
lack vertical bands of melanistic pigment across
the postanal region and hatch at lengths >8 mm.
All yolk-sac larvae collected from Montsweag Bay
during March had a single vertical band of
melanistic pigment across the postanal region and
were <5.2 mm long.

Since L. putnami spawns from December
through February while P. americanus spawms
from March through May and eggs take 2 or 3 wk

898

LAROCHE: DEVELOPMENT OF LARVAL SMOOTH FLOUNDER

to hatch (Bigelow and Schroeder 1953), larval
flounders collected from Montsweag Bay in early
March 1974 were tentatively identified as L. put-
nami. Yolk-sac larvae hatched from artificially
spawned L. putnami eggs appeared identical to
the field-collected larvae. Since the artificially
spawned larvae were few and did not live beyond
yolk absorption, larvae were collected from
Montsweag Bay and reared in the laboratory to
verify the identification. These larvae attained the
adult dorsal and anal fin ray complement of L.
putnami during the postflexion stage, verifying
the identification. In April 1974, small yolk-sac
flounder larvae matching descriptions of P.
americanus (Martin and Drewry 1978) appeared
in plankton samples collected from Montsweag

Bay. Two of these larvae were reared in the
laboratory to the postflexion stage and attained
the adult dorsal and anal fin ray complements of P.
americanus.

Counts that identify L. putnami and P.
americanus (34-38 and 34-40 vertebrae, 48-60
and 60-76 dorsal fin rays, and 34-41 and 44-58
anal fin rays, respectively) were compiled from
Jordan and Evermann (1898), Norman (1934),
Bigelow and Schroeder (1953), Leim and Scott
(1966), and this study.

LABORATORY OBSERVATIONS

Fertilized L. putnami eggs were nonadhesive
and demersal in 23%o water. Eggs ranged in diam-

3.6 mm

4.8 mm

5.0 mm

Figure L— Yolk-sac larvae ofLiopsetta putnami.

899

FISHERY BULLETIN; VOL. 78, NO. 4

eter from 1.1 to 1.4 mm, averaging 1.2 mm. Yolk
diameter ranged from 0.9 to 1.2 mm, averaging 1.1
mm. No oil globules were obvious in newly fer-
tilized eggs. At 5° C hatching began on the 25th
day after fertilization. Newly hatched larvae were
3.1-3.6 mm long.

DISTINGUISHING FEATURES

Characters useful to distinguish larval L. put-
nami andP americanus from other Gulf of Maine
flatfishes are: number of myomeres, 34-38 and
38-40; hatching length, 3.1-3.6 mm and =2.4 mm;
number of dorsal fin rays, 48-60 and 60-76;
number of anal fin rays, 34-41 and 44-58; and
presence of a single vertical band of melanistic
pigment across the postanal region of both species.

Characters useful to distinguish yolk-sac larvae
of L. putnami from P. americanus are: percentage
snout to anus length/standard length, averaging
43.6% vs. 33.3%; presence of eye pigment at hatch-
ing vs. absence of eye pigment at hatching; length

at hatching, 3.1-3.6 mm vs. =2.4 mm; and length
at yolk-sac resorption, —5.2 mm vs. —3.7 mm.

Characters useful to distinguish larval L. put-
nami from P. americanus are: absence of internal
melanophores over the notochord vs. presence of
internal melanophores over the notochord; length
at which gut loops, =5.5 mm vs. =4.3 mm; and
absence vs. presence of anal fin pigmentation in
specimens <6.3 mm.

GENERAL DEVELOPMENT

(Figures 1-8)

Reared L. putnami were 3.1-3.6 mm long at
hatching. The smallest field-collected L. putnami
larvae were =3.5 mm long. Newly hatched field-
collected f?amer/canus larvae were =2.4 mm long.
Theyolksacisresorbedby =5.2 and =3.7 mm in L.
putnami and P. americanus . The gut loops by =5.5
mm in L. putnami and between 4.2 and 4.4 mm in
P. americanus. The notochord begins to flex in L.
putnami and P. americanus at =6.0 and =5.0 mm;

5.2 mm

5.4 mm

5.9 mm

Figure 2. — Preflexion larvae of Liopsetta putnami.

900

LAROCHE: DEVELOPMENT OF LARVAL SMOOTH FLOUNDER

flexion is completed by —7.1 and =6.6 mm; and the
free tip of the notochord disappears by 7.6 and 7.3
mm. Transition from pelagic to benthic habit oc-
curs at =7.3 mm in L.putnami. The largest pelagic
field-collected L. putnami larva was 7.3 mm, and
the largest specimen, 7.6 mm, had assumed the
benthic habit in the laboratory. Transition from
pelagic to benthic habit usually occurs between
6.0 and 7.0 mm in P. americanus. The smallest
benthic-collected P. americanus was 5.7 mm, and
the largest pelagic-collected larva was 7.4 mm
long. Formation of pectoral and pelvic fin rays is
completed between 8.5 and 13.0 mm (Laszlo 1972)
in L. putnami and by =13 mm in P. americanus,

marking the end of the transformation and begin-
ning of the juvenile period.

MORPHOLOGY

(Tkbles 1-3)

Various body parts were measured on 40 L. put-
nami (3.1-7.6 mm) and 64 P. americanus (2.4-7.3
mm* larvae to examine developmental morphol-
ogy. Body proportions are summarized and com-
pared in Table 3.

The most important morphological character
for separating L. putnami from P. americanus,
particularly during the yolk-sac and preflexion

6.3 mm

6.4 mm

6.6 mm

Figure 3.— Flexion larvae of Liopsetta putnami.

901

FISHERY BULLETIN; VOL. 78. NO. 4

7.3 mm

7.6 mm

Figure 4. — Postflexion and transforming larvae (7.1 and 7.6 mm) of Liopsetta putnami .

stages, is snout to anus length/standard length. In
L. putnami it averages 43.6 and 41.2% for yolk-sac
and preflexion larvae while in P. americanus it
averages 33.3 and 37.6% for yolk-sac and preflex-
ion larvae.

FIN DEVELOPMENT

Newly hatched larvae of both L. putnami and P.
americanus have an undifferentiated fin fold ex-
tending along the body midline from the head
around the notochord tip to the anus. No other fins
were observed on the smallest L. putnami larva
(3.1 mm); however, the smallest P. americanus
larva (2.4 mm) and a 3.8 mm L. putnami larva had
undifferentiated pectoral fin folds.

Pectoral fin rays are the first to begin develop-
ment in both L.pii^namt and P. americanus, by 5.2

902

and 5.3 mm. However, pectoral fin rays are the last
to complete development, completed between 8.5
and 13 mm in L. putnami (Laszlo 1972) and by 13
mm in P. americanus. Pectoral fin length is
greatest in both species during the preflexion and
flexion periods, averaging 7.8 and 7.1% SL in L.
putnami and 7.7 and 7.8% SL in P. americanus , and
shortest during yolk-sac and postflexion stages,
averaging 3.8 and 5.0% SL in L. putnami and 3.0
and 4.7% SL in P. americanus. Dorsal, anal, and
caudal fin rays begin development in preflexion L.
putnami and P. americanus at —5.9 and —5.6 mm.
Adult complements of dorsal and anal fin rays and
principal caudal fin rays are present by —8 and ~7
mm. Fin rays within dorsal and anal fins of both
species seem to form simultaneously except the
two or three posteriormost rays in each fin which
form last. Principal caudal fin rays form first and

LAROCHE: DEVELOPMENT OF LARVAL SMOOTH FLOUNDER

2.4 mm

3.0 mm

3.6 mm

Figure 5. — Yolk-sac larvae of Pseudopleuronectes americanus.

secondary rays are gradually added anteriorly.
The pelvic fin bud appears at =7 mm in postflexion
L. putnami larvae. Fin rays begin to develop by 7.6
mm, and development is completed by 13 mm
(Laszlo 1972). The pelvic fin bud appears at =6.6
mm in postflexion P. americanus larvae; and de-
velopment is complete by 7.3 mm.

PIGMENTATION

Liopsetta putnami

The eyes of L. putnami are darkly pigmented at
hatching. Small external melanophores are scat-
tered over the head of the smallest larva (3.1 mm).
These melanophores appear to migrate ventrolat-
erally, appearing on the ventral surface of the head
between the isthmus and the cleithrum by =4.7
mm, and are aligned here on all specimens >5.4
mm long. This row often appears as a solid line of
pigment due to the expanded condition of indi-

vidual melanophores. A melanophore appears at
the angle of the lower jaw between 4.8 and 5.4 mm,
and one or two melanophores are present at this
location on all specimens >5.4 mm. One or two
melanophores are present at the tip of the lower
jaw on most specimens >5.8 mm. A large stellate
melanophore appears below the lateral midline of
the head, anterior to the cleithrum at 5.2 mm.
Larvae >5.4 mm often have 4-6 melanophores,
internal and external, in this area. A few external
melanophores appear scattered over the head, on
and under the operculum, by 7.3 mm. Flexion and
postflexion larvae >6.6 mm rapidly acquire the
dense scattering of external melanophores charac-
teristic of juveniles.

In the abdominal region small external
melanophores scattered over the dorsolateral sur-
faces of the hindgut are present on the smallest
larva (3.1 mm). An internal patch over the hindgut
is present on all specimens in the series. The small
external melanophores migrate ventrolaterally

903

FISHERY BULLETIN: VOL, 78, NO. 4

4.0 mm

4.4 mm

5.3 mm

Figure 6. — Preflexion larvae (4.0 and 4.4 mm) and flexion larva (5.3 mm) of Pseudopleuronectes americanus.

becoming scattered on only the ventral surface of
the body and yolk sac by 4.8 mm and form a row
along the ventral midline on all specimens larger
than ==5.2 mm. This row extends from the clei-
thrum, where it is continuous with the row on the
ventral midline of the head, to the center of the
abdominal region where it becomes indistinct,
merging with a group of melanophores scattered
on the ventrolateral body surface between 6.6 and
7.0 mm. Specimens >7.0 mm rapidly acquire the
dense scattering of external melanophores over
the body surface characteristic of juveniles.

Small external melanophores are scattered over
the postanal region, and a vertical band of concen-
trated melanophores of various sizes is present
across the center of the postanal region in the
smallest larva (3.1 mm). The scattered external
melanophores migrate ventrolaterally and are
present only on the ventrolateral surfaces by —4.6
mm. An irregular row of melanophores extends

from the anus to the vertical pigment band along
both sides of the ventral midline, and a single
irregular row of melanophores along the ventral
midline extends posteriorly from the pigment
band on specimens 4.3-5.4 mm long. Usually
one to several small melanophores appear some-
what separated from the row and located just
anterior to the notochord tip. The vertical pigment
band is distinct on larvae <5.4 mm, but it is
usually represented by only a few large stellate
melanophores on larger larvae. These melano-
phores become indistinguishable from other ex-
ternal melanophores which become scattered over
the body on large larvae, >6.6 mm, indicating the
initial development of the juvenile pigment pat-
tern.

The fin folds of the smallest L. putnami larva
are not pigmented. At =5.2 mm one or two
melanophores move from the body onto the fin
membrane just anteroventral to the notochord tip.

904

LAROCHE: DEVELOPMENT OF LARVAL SMOOTH FLOUNDER

5.8 mm

6.4 mm

7.4 mm

Figure 7. — Flexion larvae of Pseudopleuronectes americanus.

Several additional melanophores appear at this
location by 6.3 mm and appear on the caudal fin
near the base of the caudal fin rays after they form.
As the pterygiophores associated with the anal fin
rays begin to develop, between 6.3 and 6.4 mm,
melanophores separate from the postanal ventral
midline rows and appear as an irregular row along
the distal margins of the pterygiophores and along
the bases of the dorsal and anal rays by 6.6 mm. A
broken band of melanophores develops in the
proximal one-third of the dorsal and anal fins by
7.6 mm.

Scattered metallic yellow chromatophores were
present over the head and body of newly hatched
larvae. These chromatophores disappear soon
after preservation in Formalin. No additional ob-
servations of chromatophore patterns were possi-
ble on larger field-collected larvae.

Pseudopleuronectes americanus

The eyes of P americanus lack pigmentation at
hatching ( =2.4 mm). Pigmentation begins to ap-
pear in the eyes of P americanus at =2.9 mm, and
the eyes are completely pigmented by 3.5 mm.
Expanded external melanophores are scattered
over the head of the smallest larva (2.4 mm). These
melanophores are faint and may be difficult to see.
Melanophores over the dorsolateral surfaces of the
head disappear by =3.5 mm. A few melanophores
remain on the upper and lower jaws and along the
ventral midline of the head (gular and isthmus
regions). No evidence of melanophore migration
was observed in P. americanus. One to several
internal melanophores are present along the an-
terior edge of the cleithrum often appearing under
the operculum on larvae >2.6 mm. One or two

905

FISHERY BULLETIN: VOL. 78. NO. 4

6.9 mm

^^^^^■■■:

9.8 mm

Figure 8. — Flexion, transforming, larva (6.9 mm) and postflexion, transforming, larva (9.8 ram) oiPseudopleuronectes americanus.

melanophores are present at the articulation of
the lower jaw on larvae >3.4 mm. A few external
melanophores appear on the snout and operculum
of preflexion larvae >6.6 mm. Postflexion larvae
( >5.8 mm) rapidly acquire a covering of external
melanophores, characteristic of juveniles, as
transformation proceeds.

External melanophores are scattered over the
abdominal region of the smallest larva (2.4 mm)
with greatest concentrations along the dorsal sur-
face of the body and on the ventrolateral surface of
the yolk sac. Internal melanophores are present in
a patch over the posterior hindgut near the anus
and over the middle of the gut. By 3.6 mm pigmen-

906

tation disappears from the dorsolateral surface of
the abdominal region, and the melanophores
which had been scattered over the yolk sac are on
the ventrolateral surfaces of the body. Some of
these form a row which is often expanded and
appears as a solid line between the anus and the
cleithrum with some on the ventrolateral surface
on each side of the line. Also, by 3.6 mm, one to
several internal melanophores appear in the vicin-
ity of the pectoral fin base posterior to the clei-
thrum. By 4.4 mm, internal melanophores are
present over the notochord in this region. No
further pigmentation changes occur until exter-
nal melanophores begin to appear scattered over

LAROCHE: DEVELOPMENT OF LARVAL SMOOTH FLOUNDER

Table l. — Measurements (millimeters) of larval Liopsetta putnami. Specimens above dashed line are yolk-sac larvae.

Body depth

Body

Maximum body

Maximum

Snout

Standard

Total

at pectoral

depth

depth at pec-

body depth

to anus

Head

Eye

Upper jaw

Snout

Pectoral fin

length

length

fin base

at anus

toral tin base

at anus

length

length

diameter

length

length

length

3.1

3.2

0,40

0,36

—

—

1.5

0.44

018

_

3.6

3.8

0,40

0,36

—

—

1.8

0.50

024

—

0,16

0,18

4.0

4.1

0,34

0.22

—

—

1.6

0.52

0.24

—

0.14

0,14

4.3

4.4

036

0.24

—

—

2.0

0.56

0.24

—

0,16

4.4

4.5

0 38

026

—

—

1.8

0 60

026

—

0.22

010

4.6

48

040

0.24

—

—

1.8

0.60

0.24

—

0.16

0,18

4.8

5.0

0,50

0.28

—

—

1.9

0.62

0.26

0.14

0.14

0,34

4.8

5.0

0,54

0.28

—

—

—

0.64

0.26

—

0.12

0 14

4.8

5.0

0,46

0.26

—

—

2.1

062

0.24

0.14

0.18

0.16

4.9

5.2

040

0.26

—

—

2.2

0.64

026

—

0.16

0.18

4.9

5 1

0,40

0.26

—

—

2.1

0.60

0.26

—

0.16

0,12

5.0

5.1

038

0.30

—

—

2.2

0.68

0.26

—

0.20

0.18

'5.2

5.3

0,46

0.32

—

—

2.2

0.74

026

0,20

0.18

0.30

'5.2

53

0,54

0.34

—

—

2.4

0.80

0,28

0,18

0.16

0.32

'5.4

5,7

062

040

—

—

2.4

0.80

0,29

0,16

0.12

0.38

'5.4

5.7

0,66

0,42

—

—

2.1

0.80

0,26

0,20

0.14

0.36

'5.5

5,8

0,82

062

—

—

2.1

096

0,30

0,18

0.10

052

'5.5

57

0,76

0,60

—

—

2.4

1,0

029

0,30

0.16

0.56

'5.7

5,9

0,74

0,60

—

—

2.4

1,1

028

026

0.12

0.52

'5.8

6,0

0,78

062

—

—

2.3

1,0

0.30

0,38

0.20

0.52

'5.9

62

0,74

0,44

—

—

2.4

0,96

0.27

028

0.16

0.44

25.9

6,2

0 80

070

—

—

2.6

1,2

0.30

0,32

0.20

0.40

'5.9

6,2

0,78

0,56

—

—

2.3

1.1

0,30

0,36

0.18

040

26.2

6,3

098

0,90

10

0,94

2.5

1.1

0,32

0,42

0.26

0.54

'6.3

66

0,78

0,56

—

—

2.5

1.0

0,30

0,32

0.16

0.48

'6.4

66

1,0

0 92

1,1

0,94

2.7

1.2

0,32

0,46

0.24

050

'6,5

6,7

0,74

052

—

—

2.7

1.1

0.32

0,30

0.16

0.46

'6.6

6,8

078

060

—

—

2.5

1.0

0.31

0,30

0.14

054

26.6

69

1,0

0 80

1,1

0,86

2.7

1.2

0,33

0,40

0.20

0.46

26.6

68

1,1

1 1

1,2

1,1

2.8

1.4

0,34

0,42

0.22

0.54

26.7

6,9

0,92

0,80

096

0,86

2.7

1.0

032

0,40

0,20

0.44

26.8

7,1

0,84

0,72

089

0,74

2.8

1.2

032

0,32

0,18

0.40

26.9

7,1

0,92

0,76

0,96

0,80

2.6

1.2

0,34

0,40

0,20

0.50

27.0

7,4

1,1

11

1,2

1,1

2.8

1.3

0,34

0,40

0,16

0.52

27.0

7,3

1,2

1,1

1,2

1,2

2.8

1.4

0,32

0,40

0.20

0.50

27.0

7,4

1.1

1,0

1,1

1,1

2.8

13

0,32

0,40

0.18

0.50

37.1

8,1

1,5

1,4

1.6

1,5

2.6

1.5

0 36

0,44

0.26

0.60

27.3

7,6

1,1

1,0

1.2

1,1

3.0

1.3

0,36

0,40

0,18

0.50

27.3

7,5

1,1

1,0

1,2

1,1

2.8

1.3

034

0,40

0,20

048

37.6

9,3

—

—

2,4

2,4

2.7

2.1

0,54

0,56

0,28

0.24

' = preflexion larvae; 2

= flexion larvae;

; 3 = postf

lexion larvae.

the abdominal region of preflexion larvae, >6.2
mm, as metamorphosis begins and the juvenile
pattern of dense melanophore covering begins to
develop.

A vertical band of concentrated melanophores of
various sizes is present across the center of the
postanal region in the smallest larva (2.4 mm).
External melanophores are aligned in irregular
rows on both sides of the ventral midline between
the anus and the postanal band. A single irregular
row of melanophores extends along the ventral
surface from the vertical band nearly to the
notochord tip. An irregular row is also present
along the dorsal midline extending posteriorly
nearly to the notochord tip. Only a few scattered
melanophores appear laterally. A row of internal
melanophores over the notochord is present on all
larvae longer than =3.2 mm. The postanal band
becomes less distinct, usually represented by only
a few large stellate melanophores, in larvae >5.0
mm. Scattered external melanophores begin to

appear over the lateral surfaces of preflexion lar-
vae >5.6 mm and continue to increase in number
through the larval period. Concentrated pigment
spots develop along the dorsal and ventral body
surfaces in transforming larvae >5.8 mm.

The fin folds of the smallest P americanus larva
are not pigmented. Various authors ( Sullivan 1915;
Breder 1924; Bigelow and Schroeder 1953; Lippson
and Moran 1974) have illustrated small larvae
with melanophores extending onto the dorsal and
anal fin folds ( probably no melanophores were cen-
tered on the fin folds) from the vertical postanal
band. Their illustrations were of artificially
reared larvae. I observed no melanophores extend-
ing onto the dorsal and anal fin folds of field-
collected larvae; however, reared larvae commonly
have somewhat increased pigment due mostly to
light conditions which can be altered to change the
size of melanophores (Milos and Dingle 1978). A
few small melanophores appear along the margin
of the pectoral fin fold at 3.5 mm and disappear

907

FISHERY BULLETIN: VOL. 78, NO. 4
TalBE 2. — Measurements (millimeters) of larval Pseudopleuronectes americanus. Specimens above dashed line are yolk-sac larvae.

Standard
length

Total
length

Body depth

at pectoral

fin base

Body
depth
at anus

Maximum body
depth at pec-
total fin base

fylaximum

body depth

at anus

Snout
to anus
length

Head
length

Eye
diameter

Upper jaw
length

Snout
length

Pectoral fin
length

2.4

2.5

0.20

0.14

—

—

0.92

0.39

0.17

—

0.08

0.05

2.6

2.7

0.18

0.15

—

—

0.92

0.38

0.16

—

0.10

0.04

2.6

2.6

0.24

0.14

—

—

0.85

0.39

0.17

—

0.11

0.04

2.7

2.7

0.24

0.15

—

—

0.94

0.42

0.17

—

0.10

0.04

2.8

2.8

025

0.14

—

—

0.90

0.39

0.17

—

0.10

008

2.8

2.9

0.24

0.14

—

—

0.98

0.39

0.18

—

0.10

0.05

2.8

3.0

0.24

0.15

—

—

1.0

0.42

0,18

0.16

0,12

—

2.9

3.0

0.19

0.13

—

—

0.96

039

0.17

0.14

0,12

0.06

2.9

3.0

0.21

0.14

—

—

0.90

0.40

0.18

—

0,12

0.04

2.9

3.0

0.24

0.15

—

—

0.96

0.42

0.18

0,16

0.14

0.06

3.0

3.2

0.24

0.15

—

—

1.0

0.42

0.18

0,18

0.14

0.05

3.3

3.4

0.25

0.14

—

—

1.0

0.42

0.18

0.18

010

0.06

3.3

3.5

0.34

0.15

— -

—

1.0

0.42

0.18

0 18

008

0.10

3.4

3.6

0.36

0.14

—

—

1.1

0.42

0.20

0 18

0,08

0.10

3.4

3.6

0.38

0.15

—

—

1.2

0.48

0.20

0.19

0,10

0.20

3.5

3.7

0.33

0.14

—

—

1.1

0.44

0.18

0.17

0,09

0.20

3.5

3.7

0.34

0.15

—

—

1.2

0.46

0.20

0.20

0,09

0.20

3.5

3.7

0.34

0.15

—

—

1.1

0.45

0.18

0.19

0,10

0.19

3.6

3.8

0.33

0.14

—

—

1.2

0.47

0.20

0.21

0.13

0.20

'3.7

3.9

0.48

0.24

—

1.4

0.66

0.24

0.26

0.12

0.30

M.0

4.3

0.42

0.19

—

—

1.5

0.62

—

0.26

—

0.26

U.2

4.3

0.60

0.30

—

—

1.5

0.76

0.27

0.26

0.18

0.32

M.4

4.5

0.50

022

—

—

1.6

0.70

0.26

0.22

0.14

0.32

'4.4

4.5

0.50

0.22

—

—

1.5

0.68

0.24

0.22

0.15

030

'4.5

4.6

0.66

0.32

—

—

1.6

0.80

0.28

0,24

0.12

—

'4.5

4.6

0.70

0.35

—

—

1.7

0.82

0.27

0.26

0.18

0.30

'4.6

4.7

0.74

0.38

—

—

1.8

0.92

0.32

0.38

0.20

0.28

24.8

4.9

0.80

0.46

—

—

1.8

0,88

0.31

0.30

0.18

0.30

'4.9

5.2

0.78

0.44

—

—

1.8

0,98

—

—

—

0.40

'4.9

5.2

—

—

—

—

2.0

1.1

0.34

0.32

020

0.45

'5.1

5.3

0.85

0.54

—

—

2.0

1.0

0.33

0.32

0.14

0.44

'5.2

5.4

0.96

0.64

—

—

2.0

1.0

0.34

0.38

0.24

0.44

25.3

5.5

0.94

0.56

—

—

2.1

0.98

0.33

0.34

0.22

0.44

'5.4

5.5

0.90

0.60

—

—

2.1

1.1

0.33

0.35

0.18

—

25.6

5.7

1.1

0.82

—

—

2.3

1.2

0.34

0.40

0.24

0.48

'5.7

5.8

1.1

0.78

—

—

2.1

1.2

0.34

0.40

0,22

0,45

'5.7

5.8

1.1

0.72

—

—

2.2

1.1

0.34

0.40

0,26

0,46

25.8

6.1

1.1

0.70

—

—

2.3

1.2

0.36

0.36

0,20

0.52

26.0

6.2

1.1

0.80

—

—

2.3

1.3

0.36

0.36

0.20

0,48

=6.2

6.3

1.3

0.88

—

1.0

2.4

1.3

0.36

0.42

0.26

0,55

26.3

6.4

1.3

0.98

1.4

1.2

2.4

1.4

0.40

0.48

0.26

0.54

26.3

6.4

1.3

0.88

—

1.1

2.4

1.4

0.36

0.44

0.28

0.50

26.4

6.5

1.2

0.86

1.3

1.1

2.4

1.3

0.34

0,40

0.20

0.48

26.5

6.7

1.2

0.84

13

1.0

2.6

1.4

0.38

0,42

0.26

0.42

36.6

6.7

1.3

0.96

1.4

1.2

2.5

1.4

0.38

0.42

0.22

0.52

36.6

6.8

1.4

1.1

1.6

1.5

2.4

1.6

0.39

0.48

0.28

0.58

26.8

6.9

1.3

1.0

1.4

1.3

2.5

1.5

0.38

0.40

0.26

0.50

26.9

7.2

1.3

0.96

1.4

1.2

2.6

1,5

0.40

0.46

0.27

0.52

27.0

7.3

1.4

1.1

1.5

1.2

2.7

1.5

0.41

0.44

0.28

0.64

27.1

7.3

1.3

0.94

1.4

1.2

2.6

1.3

0.39

0.44

0.24

0.58

27.3

7.8

1.7

1.4

1.8

1.7

2.6

1.8

0.46

0.44

0.32

0.54

27.4

7.7

1.4

1.1

1.5

1.2

2.4

1.5

0.38

0.44

0.26

0.50

35.7

—

1.7

1,2

1.8

1.6

2.0

1.6

0.48

0.49

0.22

—

36.0

—

1.7

1.3

1.7

1.7

2.4

1.7

0.46

0.48

0.34

0.40

36.2

—

1.9

1.3

2.2

1.8

2.3

1.7

0.46

0.46

0.38

0.34

36.4

—

2.2

1.5

2.4

2.1

2.3

1.7

0.54

0.51

0.34

0,10

36.6

7.7

1.6

1.3

1.8

1.7

2.4

1.8

0.46

0.44

0.38

0.42

36.6

—

1.7

1.4

1.8

1.9

2.5

1.8

0.48

0.44

0.34

0.41

36.9

8.2

1.9

1.5

2.1

2.1

2.3

1.8

0.50

0.46

0.40

0.30

37.0

8.4

1.9

1.5

2.0

2.1

2.4

1.8

0.46

0.42

0.36

0.30

27.0

8.4

2.2

1.7

2.4

2.4

2.2

2.0

0.58

0,56

0.44

0.10

37.1

8.5

2.0

1.5

2.1

1.8

2.4

1.9

0,51

0,40

0.40

0.20

37.3

7.9

2.5

1.8

2.8

2.2

2.4

2.0

0.62

0.38

0.38

—

' = preflexlon

larvae; 2

= flexion larvae

3 = postflexion larvae.

again in flexion larvae by =6.4 mm. Scattered
melanophores appear on the anal fin fold at 3.6
mm, and a few appear at the center of the dorsal fin
fold at =4.2 mm. These melanophores remain
through the larval period with pigment bars,
characteristic of juveniles, developing on the dor-

sal and anal fins in flexion and postflexion larvae
>7.3 mm. By 4.4 mm a few melanophores appear
on the fin fold at about the notochord flexion point.
These melanophores increase in number with de-
velopment and are visible on the caudal fin during
and after development of the caudal fin rays.

908

LAROCHE: DEVELOPMENT OF LARVAL SMOOTH FLOUNDER

Table 3. — Body proportions of larval Liopsetta putnami and
Pseudopleuronectes americanus. Values given are percentage of
standard length (SL) or head length (HL) including mean,
standard deviation, and range in parentheses. Number of
specimens measured may be derived from Tables 1 and 2.

Pseudopleuronectes

Item

Liopsetta putnami

americanus

Body depth at pectoral fir

1 base SL

Yolk sac

9.4a:

1.61(7.6-12.9)

8.8 = 1.23(6.6-11.2)

Preflexion

12.5±

1.74(8.8-13.8)

15.2=2.87(10.5-19.3)

Rexion

15.4±

2.14(12.4-20.5)

19.3 = 1.49(16.7-23.3)

Postflexlon

236±

11 38(15.5-31.6)

28.6 = 3.85(21.2-34,2)

Body depth at anus SL:

Yolk sac

6.4 =

2.08(5 2-11.6)

4.8=0.61(3.9-5.9)

Preflexion

9.2-

2.22(6.2-14.4)

8.6 = 2.99(4.8-13.7)

Flexion

13.5±

1.99(11.0-16.7)

13,9=2,11(9,6-19.2)

Postflexion

25.6 =

8,41(19.7-31.6)

21.3=1.83(16.7-24.3)

Maximum body depth at

pectoral fi

n base/SL:

Yolk sac

9.42:

1.61(7,6-12.9)

8.8 = 1.23(6,6-11,2)

Preflexion

12.6±

1.89(8.8-16.6)

15.2=2.87(10,5-19,3)

Flexion

15.6±

1.52(13,1-17.6)

20.2 = 1.80(16.7-24.7)

Postflexion

28.1 ±

7.50(22,8-33,4)

31.1=4.45(24.2-38.4)

fy^aximum body depth at anus/SL:

Yolk sac

6.42:

2.08(5.2-11.6)

4.8=6.09(3.9-5.9)

Preflexion

9.2 ±

2.28(6.2-14,7)

8 6=2.99(4.8-13.7)

Flexion

14.1 =

2.00(10.9-17.0)

16.1=3.35(10,6-23,3)

Postflexion

26.8 =

7.67(21.4-32.1)

28.8=3.17(22.7-34.3)

Snout to anus length/SL:

Yolk sac

43.6=

3.62(39.1-50.0)

33.3=2.03(30.3-37.7)

Preflexion

41.2 =

2.46(37.9-46,2)

37.6 = 1.72(34 1-40.8)

Flexion

40.5=

1.67(36.6-44.1)

37.9 = 1.95(32.4-41.1)

Postflexion

36.0 =

0.78(35,5-36.6)

35.4=2.39(24.2-28.6)

Head length SL:

Yolk sac

13.2 =

0.53(12.2-14 2)

13,9 = 1,05(12.4-16.0)

Preflexion

15.4 =

4.31(14.2-18.8)

18,7=2,03(15.5-22.4)

Flexion

18.3 =

1.63(14.9-21.2)

21.0=1.61(18.3-24.7)

Postflexion

24.4 =

4.60(21.1-27.6)

27.0 = 1.22(24 2-28.6)

Eye diameter HL:

Yolk sac

41.9±

2.87(38.2-48.0)

43.1=1.81(40.0-47.6)

Preflexion

31.2 =

3.57(25.5-37.5)

33.4 = 2.55(31,1-37,1)

Flexion

26.8 =

2,28(24.3-32.0)

28.3=2.71(25.0-33.7)

Postflexion

24.8 =

1.20(24.0-25.7)

27.1=2.36(24.0-31.4)

Upper jaw length/HL:

Yolk sac

22.6 =

0.00(22.6)

41.0=2.80(35.9-44,7)

Preflexion

28.2 =

5.96(18.8-38.3)

34.5=4.18(30,0-41.9)

Flexion

31.5=

3.57(26.7-40.0)

31.3=2.47(26.7-34.7)

Postflexion

28.0 =

1 ,84(26.7-29.3)

26.0=3.67(19.0-30.6)

Snout length/HL:

Yolk sac

27.5±

4.69(18.8-36.7)

25.2=4.71(19.0-33.3)

Preflexion

16.6 =

3.72(10.4-24.3)

19.8 = 3.37(14.0-24.0)

Flexion

16.2=

3.05(12.3-20.0)

18.3 = 1.92(15.4-22.4)

Postflexion

15.3 =

2.83(13.3-17.3)

19 8=2.40(13.8-22.4)

Pectoral fin length/SL:

Yolk sac

3.8 =

1.38(2.4-7.1)

3.0 = 1.75(1.4-5.9)

Preflexion

7.8 =

1.30(5.8-10.2)

7,7=0,92(6,1-9,2)

Flexion

7.1 =

0.74(5,9-8.5)

7.8 = 0,85(6,2-9.1)

Postflexion

5.0 =

2.55(3.2-6.8)

4,7=2,48(0.8-8.8)

Melanophore numbers on the caudal fin mem-
brane increase through flexion and postflexion
periods with the entire fin becoming covered with
melanophores, including an intense pigment
patch near the fin base, by 9.8 mm.

ACKNOWLEDGMENTS

Special thanks are extended to H. H. DeWitt for
allowing me to use his larval fish collections and
radiographs of juvenile specimens. Additional

specimens were provided by S. M. Fried, J. L.
Laroche, B. P Lindsey, and J. D. McCleave. Gilbert
Jaeger helped with the field collecting. H. H. De-
Witt, J. D. McCleave, S. L. Richardson, and W. G.
Smith read the manuscript and provided usefiil
comments.

LITERATURE CITED

BIGELOW, H. B., AND W. C. SCHROEDER.

1953. Fishes of the Gulf of Maine. U.S. Fish Wildl. Serv.
Fish. Bull. 53, 577 p.
BiGELOW, H. B., AND W W. WELSH.

1925. Fishes of the Gulf of Maine. Bull. U.S. Bur. Fish.
40(1), 567 p.
Breder, C. M., JR.

1924. Some embryonic and larval stages of the winter
flounder. Bull. U.S. Bur. Fish. 38:311-315.
JORDAN, D. S., AND B. W. EVERMANN.

1898. The fishes of North and Middle America: A descrip-
tive catalogue of the species offish-like vertebrates found
in the waters of North America, north of the Isthmus of
Panama. Part II. Bull. U.S. Mus. 47:1241-2183.
Kleln-MacPhee, G.

1978. Synopsis of biological data for the winter flounder,
Pseudopleuronectes americanus (Walbaum). U.S. Dep.
Commer., NOAA Tech. Rep. NMFS Circ. 414, 43 p.
LEiM, A. H., AND W. B. Scott.

1966. Fishes of the Atlantic coast of Canada. Fish. Res.
Board Can., Bull. 155, 485 p.
LIPPSON, A. J., AND R. L. MORAN.

1974. Manual for identification of early developmental
stages of fishes of the Potomac River estuary. Martin
Marietta Corp., Baltimore, Md., 282 p.
Laszlo, R T.

1972. Age-growth, food, and reproduction of the smooth
flounder Liopsetta putnami (Gill) in Great Bay, New
Hampshire. Ph. D. Diss., Univ. New Hampshire, 86 p.

Martin, F. D., and G. E. Drewry.

1978. Development of fishes of the mid-Atlantic Bight: an
atlas of egg, larval and juvenile stages. Vol. VI,
Stromateidae through Ogcocephalidae. U.S. Fish Wildl.
Serv., Off. Biol. Serv, 78/12, 416 p.
MILOS, N., AND A. D. DINGLE.

1978. Dynamics of pigment pattern formation in the ze-
brafish, Brachydanio rerio. I. Establishment and regula-
tion of the lateral line melanophore stripe during the first
eight days of development. J. Exp. Zool. 205:205-216.
NORMAN, J. R.

1934. A systematic monograph of the flatfishes
(Heterosomata). Vol. I. Psettodidae, Bothidae, Pleuronec-
tidae. Br. Mus. (Nat. Hist.), 459 p.

Scotton, L. N., R. E. Smith, N. S. Smith, K. S. Price, and D. P
DE Sylva.

1973. Pictoral guide to the fish larvae of Delaware Bay,
with information and bibliographies useful for the study
offish larvae. Del. Bay Rep. Ser. 7, Coll. Mar Stud. , Univ
Del, 206 p.

Sullivan, W E.

1915. A description of the young stages of the winter floun-
der. Trans. Am. Fish. Soc. 44:125-136.

909

SEASONALITY OF FISHES OCCUPYING A SURF ZONE HABITAT IN

THE NORTHERN GULF OF MEXICO

Timothy Modde* and Stephen T. Ross^

ABSTRACT

The ichthyofauna occupying the surf zone habitat of Horn Island, Mississippi, between 1975 and 1977
was dominated by immature clupeiform fishes. The dusky anchovy, Anchoa lyolepis, and the scaled
sardine, Harengula jaguana , together constituted 80.2^'f of the 154,469 fishes collected. The greatest
number of fishes were collected in the late spring and summer, followed by a secondary peak in late
winter. Occurrence of the fishes within the surf zone is divided into three categories according to
seasonal utilization: spring and summer, summer only, and winter Factors affecting numerical abun-
dance within the surf zone differed among the most frequently appearing species. Differences in the
numbers of clupeiform fishes — A. lyolepis; A. hepsetus, striped anchovy; and H. jaguana — were more
closely associated with diel changes including tidal stage and time of day. The abundance of the Florida
pompano, Trachinotus carolinus, and the gulf kingfish, Menticirrhus littoralis, were more dependent
upon seasonal effects such as temperature.

Relatively few studies have investigated the role of
exposed surf zone habitats in the early life history
of fishes. While Springer and Woodburn (1960) de-
scribed the surf zone region as an "extreme habitat
offering little environmental diversity," this
habitat does provide several benefits to fishes. Ad-
vantages suggested by Warfel and Merriman
(1944) included the abundance of food (concen-
trated by incoming tides), increased metabolic
efficiency via heat acquisition, and protection
from predation.

Surf zone ichthyofaunas are numerically domi-
nated by relatively few species. For instance,
McFarland (1963) stated that 60-80% of the ich-
thyofauna occupying the surf regions along the
south Atlantic and Texas coasts was comprised of
only a few species. Gunter (1958) found high simi-
larity in species composition between Mustang Is-
land, Texas, and Atlantic coast surf zones and
suggested that the surf zone region was dominated
by a small group of species which remained rela-
tively constant over wide geographical areas.

Much of the literature regarding shore zone
fishes is restricted to either descriptions of species
occurrence or seasonal characterizations, seldom
exceeding one annual cycle. Reid (1955a, b),
Schaefer (1967), and Hillman et al. (1977) have

'Department of Biology, University of Southern Mississippi,
SS Box 5018, Hattiesburg, Miss.; present address: Department of
Wildlife and Fisheries Sciences, South Dakota State University.
Brookmgs, SD 57007.

^Department of Biology, University of Southern Mississippi,
SS Box 5018, Hattiesburg, MS 39401.

sampled the same habitats in successive seasons
and have observed annual changes in species com-
position. Fewer studies have attempted to relate
physical or biological parameters to the abun-
dance of fishes within the shallow beach habitat.
Gunter (1945) and Warfel and Merriman (1944)
attributed the distinct seasonal fluctuations in
fish abundance to temperature. Both Anderson et
al. (1977) and de Sylva,^ using multiple regression
analyses and crosstabulation, respectively, also
indicated that temperature was a significant fac-
tor in determining seasonal abundance of the most
numerous fish species.

The present study describes seasonal and an-
nual variations in fish species composition and the
factors affecting fish occurrences within the surf
zone of Horn Island, Miss., a barrier island in the
northern Gulf of Mexico.

METHODS

The study area was located along the southern
shore of Horn Island, Jackson County, Miss. Horn
Island is in a chain of barrier islands lying parallel
to the Mississippi-Alabama Gulf coast (Figure 1).
The island lies approximately 14 km off the main-
land and has a length of 19 km with a maximum
width of 1.2 km. The beach is partially protected
from oceanic wind-driven waves by a series of sand

^de Sylva. D. P. 1962. Fishes and ecological conditions in
the surf zone of the Delaware River estuary, with notes on other
species collected in deeper water. Univ. Del. Mar. Lab Inf
Serv. 5, 164 p.

Manuscript accepted April 1980.

FISHERY BULLETIN: VOL. 78, NO. 4, 1981.

911

FISHERY BULLETIN: VOL. 78, NO. 4

MISSISSIPPI SOUND

GULF of MEXICO

10 KM

Figure l.— Map of Horn Island, Jackson County, Miss., show-
ing the four sampling areas. The southern side of the island
represented the windward shore.

bars which extend the length of the island. The
surf zone habitat is characterized by a sand sub-
strate, the absence of any rooted vegetation, and
sufficient wave activity to be categorized as a high
energy beach (Odum and Copeland 1974).

We began sampling in April 1975 along the
southwestern edge of the island (Station 1), and
collections were made at about 7-wk intervals
until November 1975. From May 1976 to November
1977 we sampled four stations along the windward
shore of Horn Island (Figure 1) at about 5-wk
intervals (Table 1). We also sampled sheltered

Table l. — Sampling dates for fish taken from the surf zone
habitat on the southern shore of Horn Island, Miss., between
April 1975 and November 1977. Each collection represents a set
of seine hauls at a specific location.

1975

1976

1977

Season

Date

No. of
collec-
tions

Date

No. of
collec-
tions

Date

No. of
collec-
tions

Winter

13 Mar.

6

22 Jan.
1 7 Mar.

4
5

Spring
Summer

12 Apr.
21 June
12 Aug.

3
2

3

23 Apr.
28 May
25 June

4

7
11

28 Apr.
27 May
27 June

5
8
5

Fall

1 8 Oct

4

23 July

24 Aug.
2 Sept.
1 Oct.
4 Dec.

8
5
8
6
5

23 July
1 7 Sept.

23 Nov.

5
4

4

beach areas adjacent to Stations 3 and 4 during the
summer of 1976. All of the above collections were
taken between 0900 and 1600 h c.s.t. (central
standard time).

Every month between March and September
1976 (excluding August) we sampled either Sta-
tion 1, 3, or 4 over a 24-h period, taking samples at
about 4-h intervals. The choice of station was
based in part on the availability of a safe an-
chorage for our boat. In order to compare data
throughout the study, collections made between
1600 and 0900 h were not included in seasonal or
annual comparisons.

Fishes were collected with a 3.2 mm Ace"* mesh
bag seine measuring 9.1 x 1.8 m. Hauls were made
perpendicular to the beach face beginning 16-18 m
offshore. The area sampled extended from the
swash zone to the midlongshore trough, and we
made an effort to take regular samples only in
areas directly exposed to surf. We continued sein-
ing at each location until no additional new
species were collected; usually 5-9 hauls sufficed.
Each collection at each location was thus com-
prised of a successive number of seine hauls.
Fishes collected from all seine hauls at a single
station were pooled for analysis. Catch-per-effort
data from all stations were pooled to provide
monthly means. The study included 613 seine
hauls.

Species similarity by months was analyzed by
the unpaired group arithmetic average clustering
(UPGMA) method (Sneath and Sokal 1973). Only
the 15 most abundant species, which were col-
lected in at least 15% of the locations sampled,
were analyzed. Pair similarity based on species
presence or absence (Odum 1971) was determined
by:

S =2C/A +B

where C = number of species common to samples
a and b,
A = number of species in sample a,
B - number of species in sample b.

We used stepwise multiple regression to define
the dominant factors associated with the abun-
dance (fish per seine haul) of the five most fre-
quently occurring species. Environmental para-
meters selected as independent variables were

■'Reference to trade ngimes does not imply endorsement by the
National Marine Fisheries Service, NOAA.

912

MODDE and ROSS: SEASONALITY OF nSHES OCCUPYING A SURF ZONE HABITAT

temperature, salinity, tide level, wave height,
beach slope, wind speed, and wind direction. The
latter two parameters represented means of the
4-wk period preceding each collection. Wind direc-
tion and velocity data were recorded at Keesler Air
Force Base on the adjacent mainland. Tide level
data were entered as the difference from mean low
water and were from tide tables. Because of the
absence of data regarding several environmental
parameters, collections made during 1975 were
not included in the regression analysis.

RESULTS

Annual and Seasonal Occurrence

During the 32-mo study period, 154,469 fishes,
representing 14 orders, 42 families, and 76 species,
were collected (Table 2). These were primarily late
larvae and early juveniles, and only 1.17c exceeded
50 mm SL. The major families represented in the
surf zone, in both percent occurrence and numbers
collected, were the Engraulidae, Clupeidae,

Table 2. — Total number of fishes collected from the surf zone of Horn Island, Miss., between April 1975
and November 1977, and percentage frequency of species occurrence in the collections.

Frequency of

Species

1975

1976

1977

Total

occurrence

Carcharhlnidae

Carcharhinus limbatus . blacktip shark

1

1

0.9

Dasyatldae

Dasyatis sayi, bluntnose stingray

1

1

.9

Megalopidae

Megalops atlantica . tarpon

2

1

3

2.7

Elopldae

Bops saurus. ladyfish

2

3

5

2.7

Albulldae

Albula vulpes . bonefish

4

4

3.6

Ophichthidae

Myrophis punctatus . speckled worm eel

2

2

1.8

Clupeidae

Harengula jaguana . scaled sardine

1,941

45,790

12,001

59,732

64.3

Sardinella anchovia. Spanish sardine

170

107

27

304

17.0

Opisthonema oglinum, Atlantic thread herring

87

88

1

176

8.9

Brevoortia patronus. gulf menhaden

1,069

1,046

6,733

8,848

17.9

Etrumeus teres, round herring

1

1

.9

Engraulidae

Anchoa lyolepis, dusky anchovy

6.855

41,690

1 5,486

64,031

47.3

A. hepsetus. striped anchovy

74

2.656

1,021

3,751

44.6

A mitchilli, bay anchovy

788

275

1,890

2.953

29.5

A. cubana, cuban anchovy

5

2

7

1.8

Anchoviella pertasciata , flat anchovy

507

514

234

1,255

21.4

Synodontidae

Synodus foetens, inshore lizard fish

26

30

11

67

18.8

Ariidae

Arius felis, sea catfish

8

16

6

30

13.4

Gobiesocidae

Gobiesox strumosus. skilletfish

3

10

13

5.4

Gadidae

Urophycis regius. spotted hake

1

1

.9

Polynemidae

Polydactylus octonemus, Atlantic threadfin

2

2

.9

Pomatomidae

Pomatomus saltatix, bluefish

11

28

39

8.0

RachycentrkJae

Rachycentron canadum, cobia

4

4

1.8

Sphyraenidae

Sphyraena borealis. northern sennet

24

106

130

12.5

S. guachancho. guaguanche

7

7

3.6

Scombridae

Scomberomorus maculatus . Spanish mackerel

7

52

4

63

12.5

Lutjanidae

Lut)anus sp., snapper

1

1

.9

Mugilidae

Mugil cephalus, striped mullet

4

323

493

820

24.1

M. curema . white mullet

3

73

420

496

24.1

Stromateidae

Peprilus sp., butterlish

2

1

3

1.8

Gerreidae

Eucinostomus sp., mojarra

142

553

180

875

36.6

Sparidae

Archosargus probatocephalus . sheepshead

2

2

1.8

Lagodon rhomboides. pinfish

27

7

1,216

1,250

18.8

Uranoscopidae

Astroscopus y-graecum , southern stargazer

11

8

19

9.8

913

FISHERY BULLETIN: VOL. 78. NO. 4

Table 2.— Continued.

Species

1975

1976

1977

Total

Frequency of
occurrence

Pomacentridae

Abudefduf saxatilis. sergeant major
Lobotidae

Lobotes surinamensis. tnpletail
Blenniidae

Hypsoblennius sp . blenny
Goblidae

Gobionellus hastatus. sharptail goby
Ophidiidae

Lepophidium sp., cusk eel
Exocoetidae

Hemiramphus brasiliensis. ballyhoo

Hyporhamphus unifasciatus. halfbeak
Belonldae

Strongylura marina. Atlantic needlefish
Cypnnodontidae

Fundulus similis, longnose killifish
Atherinidae

Menidia beryllina. tidewater silverside

Membras martinica, rough silverside
Syngnafhidae

Syngnathus louisianae . chain pipefish

S. floridae. dusky pipefish

S- scovelli. gulf pipefish

Hippocampus zosterae. dwarf seahorse
Sciaenidae

Bairdiella chrysoura. silver perch

Cynoscion arenahus. sand seatrout

C nebulosus. spotted seatrout

Leiostomus xanthurus . spot

Menticirrhus littoralis. gulf kingfish

M. americanus. southern kingfish

M. saxatilis. king whiting

Larimus fasclatus . banded croaker

Micropogonias undulalus , Atlantic croaker
Carangidae

Chloroscombrus chrysurus. Atlantic bumper

Trachlnotus carolinus. Florida pompano

T falcatus. permit

Oligoplites saurus. leatherjacket

Caranx hippos, crevalle jack

Seriola zonata, banded rudderfish

Selene vomer, lookdown
Dactyloscopidae

Dactyloscopus tridigitatus, sand stargazer
Triglidae

Prionotus tribulus . bighead searobin
Cynoglossidae

Symphurus plagiusa, blackcheek tonguefish
Bothidae

CItharichthys macrops, spotted whiff

EIropus sp., flounder

Paralichthys albigutta. gulf flounder

P lethostigma, southern flounder
Tetraodontidae

Sphoeroides sp., puffer
Balistidae

Monacanthus hispidus. planehead filefish

Aluterus schoepfi. orange filefish
Diodontidae

Chilomycterus schoepfi. striped burrfish

Totals

18

18

.9

1

236

5

242

21 4

22

2

24

63

1

1

.9

1

1

.9

3

3

18

1

3

24

28

63

3

1

4

18

2

2

4

36

29

35

109

173

24,1

180

5

317

502

179

2

133

35

170

28.6

7

3

7

17

63

5

2

7

27

1

1

.9

1

2

3

2,7

7

7

9

1

2

3

2.7

6

795

1,415

2,216

188

269

431

694

1,394

670

19

213

40

272

259

10

52

54

116

348

13

5

18

4.5

3

3

1.8

3

9

13

25

8.9

154

528

1

2.586

3,268

1

56.3
9

4

4

2

10

6.3

2

56

14

72

11.6

1

1

.9

1

1

.9

2

2

.9

1

1

.9

1

1

.9

3

16

4

23

6.3

627

2

629

13.4

19

2

21

4.5

2

9

6

17

36

196

35

231

18.8

39

39

4.5

3

3

.9

12.415

96,763

1
45,291

1
154.469

.9

Carangidae, and Sciaenidae. The dusky anchovy,
Anchoa lyolepis, and the scaled sardine, Haren-
gula jaguana, w^ere numerically most important
making up 80.2% of the total number of fishes
collected. These species were abundant in all 3 yr,
although A. lyolepis was most numerous in 1975
and 1977 and H. jaguana in 1976. The families
Sciaenidae and Carangidae were represented by
nine and seven species, respectively. The gulf king-

fish, Menticirrhus littoralis, although only eighth
in number, exhibited the highest frequency of oc-
currence (67%) of any species. The Florida pom-
pano, Trachinotus carolinus, was the only caran-
gid regularly occurring in the surf zone.

Relationships within two genera, Sardinella
(Clupeidae) and Menidia (Atherinidae), are cur-
rently uncertain for the Gulf of Mexico. We fol-
lowed Houde and Fore ( 1973 ) and Hoese and Moore

914

MODDE and ROSS: SEASONALITY OF FISHES OCCUPYING A SURF ZONE HABITAT

(1977) in recognizing the low anal ray count (gen-
erally 16) specimens of Sardinella sp. as Spanish
sardine, S. anchovia. Our specimens of Menidia
generally had three or fewer anal fin rays anterior
to the posterior extension of the swim bladder by
which Johnson (1975) characterized M. pe-
ninsulae (Goode and Bean). However, we have fol-
lowed Edwards et al. ( 1978 ) in retaining tidewater
silverside, M. beryl Una, for this form.

Although some variation occurred in the annual
ranking of species abundance (Table 3), A. lyolep-
is; H. jaguana\ and gulf menhaden, Brevoortia
patronus, were among the four most abundant
species in all 3 yr. Less numerous species showed
more variability. For instance, the striped an-
chovy, A. hepsetus, was third in abundance in 1976
but eighth in abundance in 1977, while T.
carolinus was sixth in abundance in 1976 and
fourth in abundance in 1977.

Table 3. — Rank order of abundance of the 10 most numerous
fish species collected from the Horn Island, Miss., surf zone by
year.

Species

1975

1976

1977

Anchoa lyolepsis

1

2

1

Harengula jaguana

2

1

2

Brevoortia patronus

3

4

3

Anchoa mitchilli

4

—

5

Anchoviella perfasciata

5

9

—

Menticirrhus littoralis

6

10

9

Membras marlinica

7

—

—

Sardinella anchovia

8

—

—

Trachinotus carolinus

9

8

4

Eucinostomus sp

10

7

—

Leiostomus xanthurus

—

5

6

Etropus sp.

—

6

—

Lagodon rhomboides

—

—

7

Anchoa hepsetus

—

3

8

Mugil cephalus

—

—

10

The number of fishes collected from the surf
zone habitat of Horn Island was characterized by
distinct seasonal changes. Peaks in fish per seine
haul (collected between 0900 and 1600 h) occurred
during the warmer months between June and Sep-
tember 1976 and 1977 (Figure 2). In 1975 fishes
were not collected in large numbers until the Au-
gust collection. Large numbers of fishes were col-
lected as early as June in 1976 although few fishes
were collected in July of the same year. In 1977
fishes were not collected in abundance in June, but
were in July.

The number of fishes collected dropped during
the fall and winter months but rose again during
late winter and early spring (Figure 2). This sec-
ondary peak, occurring in March 1976 and 1977,
was composed of denatant migrants (sensu Gush-
ing 1975j which had recently been spawned

9f

J3.

R

JIL

H I h _

AMJ JASONOJFMAMJJASONDJFMAMJ JASON

wre 1976 1977

Figure 2 . — Mean number of fishes collected per seine haul from
Stations 1 through 4 on Kom Island, Miss., between April 1975
and November 1977. Data represents collections made between
0900 and 1600 h c.s.t.

offshore and were drifting into Mississippi Sound
via the barrier island passes. Following the late
winter (March) peak there was another period of
low catch per effort between April and June in
1976 and 1977.

The numerically dominant species collected
within the surf zone exhibited distinct seasonal
occurrence patterns. Gluster analysis among
these species indicated three modes of occurrence
(Figure 3). Although data for the cluster analysis
included only fishes collected between 0900 and
1600 h, there was no significant difference ( x^, 5%
level) in the monthly presence offish species col-
lected at this time period and those collected be-
tween 1600 and 0900 h. The most numerous
species, A. lyolepis and H. jaguana, showed the
highest similarity in seasonal occurrence and
were most common during spring and summer.
Other species also characteristic of spring and
summer included Eucinostomus sp. and T. caroli-
nus. Anchoa hepsetus and Menticirrhus littoralis
had less seasonal affinity with the above species
since they also occurred well into fall.

A second seasonal group included flat anchovy,
Anchoviella perfasciata; S. anchovia; and white
mullet, Mugil curema, which were representa-
tives of the summer fauna (Figure 3). These
species were never collected at water tempera-
tures below 24.5° G.

915

FISHERY BULLETIN: VOL. 78, NO. 4

% SIMILARITY
25 50 75

100

SUMMER

SPR^G-
SUMMER

-WIMER

— Anchoviella perfasciata
-Sardinella anchovia
-Mugil curema
— Membras martinica
— Anchoa mitchiili
— Eucinostomus sfi.
r—Anchoa lyolepis
*— Harenguia jaguana
— Trachinotus carolinus
— Anchoa hepsetus
— Menticirrhus littoralis
— Brevoortia patron us
— Lagodon rhomboides
— Leiostomus xanthurus
— Mugil cephalus

Figure 3. — Similarity dendrogram for species by month, based
on presence or absence data, for fishes collected from the surf
zone of Horn Island, Miss.

The third seasonal species group, B. patronus;
pinfish, Lagodon rhomboides; spot, Leiostomus
xanthurus; and striped mullet, Mugil cephalus,
was prevalent during winter or early spring, gen-
erally in water temperatures below 24.5° C, with
the first three occurring at temperatures as low as
11.5° C. Together these four species composed the
secondary abundance peak of March 1976 and
1977 (cf. Figure 2).

Rough silverside, Membras martinica, and bay
anchovy, Anchoa mitchiili, did not fit within the
three seasonal categories. Anchoa mitchiili was
collected in greatest abundance during the spring
and in the fall, while M. martinica was most com-
mon in the spring, but only during 1975 and 1977.
Membras martinica was infrequent in 1976.

Multiple regression analysis explained little of
the variation associated with fish abundance (i.e.,
fish per seine haul). However, while tentative, the
analysis may indicate the relative importance

of these variables in controlling fish occurrence
(Table 4). The dominant factor affecting the clu-
peiform fishes was tide level. Tide contributed
only 5.1% and 8.9% in the regression equations
for H. jaguana and A. hepsetus, and accounted for
19.2% of the model for A. lyolepis (P<0.05). The
remaining variables contributed little to the pre-
dictive ability of the regression equations, al-
though salinity composed 5.6% of the variance
model for A. hepsetus (P<0.05). Temperature was
the dominant parameter in the model for T.
carolinus (not significant) and Menticirrhus lit-
toralis (P<0.05).

While not apparent from Table 4, our observa-
tions indicate that catch per effort (cf. Figure 2)
may coincide with wind direction. Wind patterns
in the study area undergo annual cycles in which
direction is primarily from the north during the
winter and from the south during the summer.
Fishes were collected in greatest numbers during
the summer when southerly winds predominated.

Daily Activity Patterns

The greatest number of fishes were present
within the surf zone during the early morning

Table 4. — Stepwise multiple regression of the five major
environmental parameters contributing to the average number
offish collected per seine haul in the surf zone of Horn Island,
Miss.

Species and

Cumula-

Cumula-

parameter

tive fl

fl2

tive fl2

F

df

Anchoa lyolepis

Tide

0.438

0.192

0.192

15,72-

6,75

Wave height

.452

.012

,205

,16

Wind direction

.457

.005

.209

,23

Temperature

.461

.003

.212

,22

Wind speed

.462

.001

.213

06

Harengula jaguana

Tide

.227

.051

.051

3,96-

5.76

Temperature

.255

.014

.065

,82

Wind direction

.274

.010

.075

,69

Salinity

.278

,002

,077

,20

Wave height

.279

.001

.078

,06

Anchoa hepsetus

Tide

.297

.089

,089

8,96-

6,76

Salinity

.380

.056

,144

5.00'

Temperature

.398

.014

,158

,90

Wind direction

,411

.011

,169

1 00

Slope

.415

.003

,172

,32

Trachinotus carolinus

Temperature

.199

,040

,040

2,14

7,74

Salinity

.241

,018

,058

1,02

Wind speed

.254

.007

.065

,93

Tide

.262

,004

.068

,68

Wind direction

.268

,004

.072

,60

Menticirrhus littoralis

Temperature

.309

.095

,095

8,62-

6.75

Tide

.329

.013

108

,77

Salinity

.333

.002

,111

,21

Wave height

.334

.001

,112

,52

Slope

.338

.002

,113

,38

•Significant (P<0,05),

916

MODDE and ROSS: SEASONALITY OF FISHES OCCUPYING A SURF ZONE HABITAT

(0300-0900) for all six 24-h samples made in 1976
(Figure 4). From May to September, excluding
August when diel collections were not taken,
fishes exhibited a distinct rise in abundance be-
tween 0300 and 0600 h c.s.t. with peak occurrences
just after sunrise. The number of fishes collected
during this time period far exceeded those cap-
tured during the later daylight hours; in June no
collection was made during this time period.

The daily pattern of catch per effort reflected the
numerical dominance of H. jaguana and A. lyo-
lepis. The greatest number offish for both species
was collected during the early morning with a
subsequent decline throughout the day (Figure 5).
Peak capture rates for H . jaguana and A. lyolepis
were 1,712 and 2,339 fish/seine haul, whereas the
lowest mean rates were 6 and 0.1 fish/seine haul
during the 1200-1500 h period for H . jaguana and
the 1800-2100 h period for A. lyolepis. A secondary
peak in abundance occurred between 1500 and

2400- 0300- 0600- 0900- 1200- 1500- 1800- 2100-
0300 0600 0900 1200 1500 1800 2100 2400

TIME OF DAY

Figure 4. — Monthly mean number of fish per seine haul
collected during the designated time intervals from the surf zone
of Horn Island, Miss., between March and September 1976,
excluding August.

2400- 0300- 0600- 0900- 1200- 1500- 1800- 2100-
0300 0600 0900 1200 1500 1800 2100 2400

TIME OF DAY

Figure 5. — Daily changes of mean number offish per seine
haul for the Horn Island, Miss., surf zone (April 1976-September
1976). Data are for the numerically most important species.
A = Anchoa lyolepis (broken line) and Harengula jaguana
(solid line). B = Anchoa hepsetus. C = Trachinotus carolinus
(broken line) and Menticirrhus littoralis (solid line).

1800 h with 252 and 545 fish collected per seine
haul for H. jaguana and A. lyolepis. High numbers
of A. hepsetus also occurred during the morning;
however, peak catch per effort occurred between
0600 and 0900 h. This species was less abundant
than H. jaguana and A. lyolepis, with only 33 fish
collected per seine haul. Anchoa hepsetus re-
mained within the beach area through 1200-
1500 h, but no fish were captured between 1500 and
1800 h.

Menticirrhus littoralis and T. carolinus did not
exhibit distinct daily activity patterns, but tended
to be more abundant during midafternoon or even-
ing. The greatest number of M. littoralis collected
was only 2.0 fish/seine haul between 1800 and
2100 h while the greatest number of

917

FISHERY BULLETIN: VOL. 78, NO. 4

T. carolinus per seine haul was 0.8 fish between
1500 and 1800 h.

DISCUSSION

Species Composition

The ichthyofauna of the Horn Island surf zone
resembles that of other surf zone habitats within
the Gulf of Mexico. Using similar collecting gear,
Gunter (1958) reported that over a 3-yr period
T. carolinus and H. pensacolae ( = H. jaguana)
were the numerical dominants from the surf zone
ofMustang Island, Texas. McFarland{ 1963), using
a much larger seine (193 m long with 1.9 cm mesh),
found that Mugil cephalus and Atlantic threadfin,
Polydactylus octonemus, were dominant by weight
and number, respectively, of the same area. While
fishes collected by McFarland were generally >100
mm, many of the same species were collected by
Gunter (1958) and in our study as larvae and
juveniles.

Springer and Woodburn (1960) described a
faunal assemblage for the surf habitat (exposed
beach) near Tampa Bay, Fla., which was very simi-
lar to that of Horn Island. Har en gula jaguana was
the numerically dominant species collected during
the warmer months, followed numerically
by Lagodon rhomboides and Menticirrhus littor-
alis.

Although a numerically dominant species in the
present study, Anchoa lyolepis has never been re-
ported as common within a Gulf of Mexico coastal
surf habitat. Gunter (1958) reported that A.
lyolepis was taken only occasionally in the surf
zone ofMustang Island, and Naughton and Salo-
man (1978) found it to be rare in a western Florida
surf area. Springer and Woodburn (1960) collected
only A. hepsetus and A. mitchilli from exposed
beaches near Tampa Bay. Daly (1970) found A.
nasuta (synonymized with A. lyolepis by
Whitehead 1973) to be uncommon on the western
tip of south Florida, although it ranges from Cape
Hatteras, N.C., into the Gulf of Mexico through
the West Indies to the Gulf of Venezuela (Daly
1970). In Mississippi Sound, Christmas and Waller
(1973) occasionally collected A. nasuta of 36-59
mm SL in higher salinity water (20.0-35.51).
Their data, based on several years of observation,
indicated that A. nasuta occurred only in the
summer and fall and was never abundant.

In comparing latitudinal variation of surf zone
ichthyofaunas Gunter (1958) suggested that the

major species occupying the Texas beach were the
same or cognates to species observed in North
Carolina which were cognates to those reported
from New England beaches. Springer and Wood-
burn (1960) acknowledged that certain similari-
ties existed within broad geographical ranges;
however, they pointed out that many dissim-
ilarities existed between temperate and tropical
faunas within the eastern United States.

Between-study comparisons are made difficult
due to differences in sizes of collecting gear and
sampling designs. For instance, McFarland (1963)
stated that the small clupeids, particularly the
scaled sardine and engraulids, were undersam-
pled because his collecting gear generally elimi-
nated fishes <40 mm SL. However, for the warm-
temperate to tropical regions of the Atlantic and
Gulf of Mexico there seems to be a very character-
istic species assemblage utilizing surf zone areas.
Species listed as numerically important in both
warm-temperate to tropical Gulf of Mexico and
western Atlantic studies (Table 5) were A. mitch-
illi, A. lyolepis (= A. nasuta), T. carolinus, M.
littoralis, and H. jaguana (= H. pensacolae). In
addition, Atlantic silverside, Menidia menidia,
and Atlantic menhaden, B. tyrannus, in the At-
lantic and M. beryllina and B.patronus in the Gulf
were numerically important. Harengula jaguana
was most frequently reported as numerically
dominant along Gulf of Mexico beaches; only Gil-
more (1977) found it to have high abundance in the
Atlantic surf zone off the Indian River area of
Florida. However, the northern limit of this species
is in the area of Cape Kennedy on the Florida
Atlantic coast (Rivas 1963). Gilmore (1977) also
found A. nasuta to be abundant in the surf zone
along the eastern Florida coast. While Menticir-
rhus littoralis was not among the five most abun-
dant species in some Gulf of Mexico studies (in-
cluding ours), its high frequency of occurrence in
our study indicates that it is an important surf
zone species. Based on Table 5, atherinids, primar-
ily of the genus Menidia, were more often among
the five most abundant species collected in the
Atlantic (seven out of nine studies) than Gulf of
Mexico surf zones (two out of six studies).

Seasonal and Annual Variations

Temporal changes in both abundance and com-
position were primary characteristics of the ich-
thyofauna utilizing surf zone habitats of Horn Is-
land. Fishes collected in our study were most

918

MODDE and ROSS: SEASONALITY OF FISHES OCCUPYING A SURF ZONE HABITAT

STABLE 5.— List of the first five numerically abundant fish species collected from the surf zone habitat of marine sandy beaches of the

Gulf of Mexico and temperate Atlantic coast states.

Region

Gulf coast:
Mustang Island.

Texas
Mustang Island.

Texas
Gilchrist.

Texas
Horn Island,

Miss.

Panama City.

Fla
Tampa Bay,

Fla.
East coast:
Indian River,

Fla.
Statewide.

South Carolina

Folly Island,

S.C
Beaufort,

N.C.
Beaufort,

N.C.

Fire Island,
N.Y

Long Island.
Conn.

Pine Orchard.
Conn.

Morris Cove,
Conn.

Major species

Trachinotus carolmus. Harengula jaguana. Mugil curema. Anchoa mitchilli,
Micropogonias undulatus

Polydactylus octonemus. Menidia beryllina. Mugil cephalus. Menticirrhus

littoralis. Chloroscombrus chrysurus
Brevoortia palronus.' Anchoa mitchilli. Polydactylus octonemus. Arius

fells. Chloroscombrus chrysurus, Trachinotus carolinus

Anchoa lyolepis. Harengula jaguana, Brevoortia patronus, Anchoa hepsetus

Trachinotus carolmus

Harengula laguana. Menidia beryllina, Lagodon rhomboides. Trachinotus
carolmus. Mugil curema

Harengula jaguana. Lagodon rhomboides, Menticirrhus littoralis,
Leiostomus xanthurus, Trachinotus carolinus

Harengula jaguana, Ophisthonema oglinum. Sardinella anchovia. Anchoa
hepsetus, A. mitchilli. A nasuta^

Menidia menidia. Anchoa mitchilli. Trachinotus carolinus, Menticirrhus
littoralis. Anchoa hepsetus

Menidia menidia. Anchoa hepsetus, Menticirrhus littoralis, Trachinotus
carolinus, Mugil curema

Menidia menidia. Anchoa mitchilli, Trachinotus carolinus, Menticirrhus
sp., Fundulus maialis

Brevoortia tyrannus. Anchoa hepsetus. Membras martlnica. Lagodon
rhomboides. Menticirrhus littoralis

Sphoeroides maculatus, Alosa aestivalis, Poronotus triacanthus, Morone
saxatilis, A. mediocris

Menidia menidia. Fundulus maialis. Menidia sp. (immature). Brevoortia
tyrannus. Fundulus heteroclitus

Menidia menidia, Sphoeroides maculatus, Brevoortia tyrannus.

Pseudopleuronectes americanus, Syngnathus peckianus
Menidia menidia, Brevoortia tyrannus, Syngnathus fuscus, Clupea harengus

Pseudopleuronectes americanus

Total no.
of species

Reference

1,

44

Gunter(l958)

48

McFarland(1963)

25

Reid (1955b)

fus

76

Present study

44

Naughton and

Saloman (1978)

47

Springer and
Woodburn(1960)

78

Gilmore(1977)

39

Cupka(1972)

43

Anderson et al.
(1977)

8

Pearse et al.

(1942)

40

Tagatz and
Dudley (1961)

71

Schaefer(1967)

35

Hillman el al.
(1977)

13

Merriman (1947)

lUS,

32

Warfel and

Merriman (1944)

'Abundance of Brevoortia patronus was considered distorted due to the coincidence of a large school of adults moving inshore during the sampling effort.
^Equal numbers of Anchoa mitchilli and A. nasuta collected.

abundant during the summer, although the onset
of high fish density varied somewhat between
years. High numbers of fishes first appeared in
June in 1976, but not until August in 1975 and
July in 1977. Annual variability in the time of
peak catch may be due, in part, to short-term vari-
ation in local water conditions. The low numbers
of fishes collected in July 1976 may have been due
to unusually calm and clear water which in-
creased net avoidance. Large numbers of fishes
were collected during the predawn hours of July
1976, indicating that fishes were abundant along
the beach during this period.

Similar changes in the abundance of surf zone
fishes have been observed in other studies. Gunter
(1958) reported that fishes occupying the exposed
beach of Mustang Island underwent seasonal suc-
cession during which fish abundance was greatest
during the summer and least in the winter. Sea-
sonal changes in abundance were also reported by
Springer and Woodburn (1960), McFarland (1963),
Schaefer (1967), and Anderson et al. (1977).
McFarland (1963) proposed four categories of sea-
sonal occurrence for surf zone fishes: all-year resi-

dents, spring-summer residents, summer resi-
dents, and winter residents. Of the major species
common to both McFarland's study and ours, sea
catfish, Arius felis; Mugil cephalus; and L. rhom-
boides were considered as all-year residents,
whereas H. jaguana; Anchoa sp.; T. carolinus;
Menticirrhus littoralis; king whiting, M. saxatilis;
and southern kingfish, M. americanus, were clas-
sified as spring-summer residents. McFarland
noted, as we have, that fishes characteristic of the
spring and summer dominated the numerical
component of the ichthyofauna.

The influx of denatant migrants collected
within the surf zone during the winter in our study
has not been reported previously. However, the
annual movement of larval menhaden and sciae-
nids into estuaries along the Gulf of Mexico and
Atlantic coasts during the winter is well docu-
mented (Gunter 1967; Dahlberg 1972; Christmas
and Waller 1973). These species likely did not
utilize the surf zone specifically, but were concen-
trated along the island before moving through the
barrier island passes. Therefore, their appearance
within the surf zone habitat appears dependent

919

FISHERY BULLETIN: VOL. 78, NO. 4

more upon wind and current movements rather
than habitat preference.

Throughout our study A. lyolepis and H.jagua-
na clearly dominated the numerical component
of the surf zone ichthyofauna; however, differences
in the rank of the remaining species did occur.
Gunter (1958) suggested that intraseason species
abundance in the surf zone of Mustang Island
changed annually, although T. carolinus and H.
jaguana were generally present in considerable
numbers. Reid (1956) observed that the greater
number of the surf zone ichthyofauna along the
Texas coast, with the exception oiB.patronus , was
similar during successive summers. Star drum,
Stellifer lanceolatus, was considerably more
abundant during the second summer as were T.
carolinus, M. littoralis, and M. americanus. Dur-
ing the first simimer of a 3-yr study, Schaefer
(1967) observed butterfish, Peprilus triacanthus ,
as the numerically dominant species within the
surf zone of Fire Island, N.Y. In the remaining two
summers of his study, northern puffer, Sphoeroi-
des maculatus, was the most numerous species.

Factors Affecting Occurrence

The dominant factors affecting the abundance
of fishes within the surf zone of Horn Island were
tide level, time of day, and temperature. The fre-
quency of engraulids and clupeids was closely as-
sociated with time and tide. However, during the
summer sampling periods, when fish abundance
was greatest in the early morning, tide levels were
also highest. Consequently, the effect of the two
factors is difficult to separate. Subsequent re-
search (Ross unpubl. data) indicates that both may
be important, although Roessler (1970) found that
the frequency of H. jaguana collected from south-
ern Florida was not significantly related to tidal
fluctuation. Seasonal changes in temperature ap-
peared to be of most importance in affecting the
frequency of T. carolinus and M. littoralis.

The pronounced daily variation in occurrence
of the most abundant fishes (i.e., A. lyolepis,
A. hepsetus, and H. jaguana) indicates that they
are not as permanently associated with the surf
zone habitat as the gulf kingfish and the Florida
pompano. Diel catch rates showed that engraulids
and clupeids largely moved out of the surf zone
during the day, whereas, the gulf kingfish and
Florida pompano exhibited little change in daily
abundance. Predator avoidance may be an impor-

tant reason for the high early morning densities of
the clupeoid fishes.

Other studies have also documented the influ-
ence of time of day and tidal cycle on fish abun-
dance in surf areas. Merriman (1947) found that
shore zone fishes in Connecticut had activity pat-
terns associated with tide level. The greatest
number of fishes occurred during high tide when
fish appeared to be actively feeding. Daly (1970)
also described daily activity patterns in anchovies
collected along south Florida beaches. Anderson et
al. (1977) suggested that temperature was the
primary factor affecting fish abundance along a
South Carolina beach; however, diel changes were
not investigated, de Sylva et al. (footnote 3) also
found that temperature was the greatest factor in
determining frequency of most fishes, whereas sa-
linity was secondary in importance and turbidity
had little effect. The importance of temperature
and salinity to the abundance and distribution of
fishes has been discussed in depth by Gunter
(1938, 1945, 1950, 1957) and to some extent by
Warfel and Merriman (1944). Warfel and Merri-
man reported that the greatest and lowest number
of fishes appeared relative to high and low temper-
atures, but that no direct correlation could be
made. Gunter (1945, 1957) suggested that temper-
ature was the dominant factor in initiating sea-
sonal migrations and other cyclic activities of
fishes along the Texas coast. The interaction of
wind direction (i.e., inshore winds) with tempera-
ture may further increase the number of fishes in
the Horn Island surf zone.

In summary, the Horn Island surf zone is
utilized primarily by H. jaguana, A. lyolepis, A.
hepsetus, M. littoralis, and T. carolinus. There is
strong seasonal periodicity with the greatest
abundance in spring and summer, as well as daily
fluctuations due to tide level and time of day. Since
the individuals of the above species were primarily
late larval and juvenile forms, the importance of
surf zone habitats as nursery and refuge areas for
certain species should be recognized.

ACKNOWLEDGMENTS

We wish to express our appreciation to Kathleen
Clark and John Baker for their consistent will-
ingness to assist in the field. We are also indebted
to Harriet Perry and her staff at the Gulf Coast
Research Laboratory for the use of their facilities
and equipment, and to the National Park Service
for allowing us to collect on Horn Island. Wind

920

MODDE and ROSS: SEASONALITY OF FISHES OCCUPYING A SURF ZONE HABITAT

data were provided by the Physical Oceanography
Section of the Gulf Coast Research Laboratory. We
thank Sally L. Richardson for her constructive
comments on an earlier draft of the manuscript.

Financial aid during this study was provided by
two Sigma Xi Grants-In-Aid of Research (to T.
Modde) and by the University of Southern Missis-
sippi Biology Department. This study is adapted
from a portion of a doctoral dissertation submitted
by T. Modde to the Biology Department of the
University of Southern Mississippi.

LITERATURE CITED

ANDERSON, W. D., Jr., J. K. DIAS, R. K. DIAS, D. M. CUPKA,
AND N. A. Chamberlain.

1977. The macrofauna of the surf-zone off Folly Beach,
South Carolina. U.S. Dep. Commer., NOAA Tech.
Rep., NMFS SSRF-704, 23 p.

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CUPKA, D. M.

1972. A survey of the ichthyofauna of the surf- zone in
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GUSHING, D. H.

1975. Marine ecology and fisheries. Camb. Univ. Press,
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1963. Genus Harengula Cuvier and Valenciennes 1847
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FISHERY BULLETIN: VOL. 78. NO. 4

SCHAEFER. R. H. TAGATZ, M. E., AND D. L. DUDLEY.

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922

LARVAL DEVELOPMENT OF PACIFIC TOMCOD, MICROGADUS PROXIMUS,

IN THE NORTHEAST PACIFIC OCEAN WITH COMPARATIVE NOTES ON

LARVAE OF WALLEYE POLLOCK, THERAGRA CHALCOGRAMMA, AND

PACIFIC COD, GADUS MACROCEPHALUS (GADIDAE)

Ann C. Matarese, Sally L. Richardson, and Jean R. Dunn^

ABSTRACT

A developmental series from yolk-sac larvae through juveniles (2.7-46.6 mm SL) of Microgadus
proximus from the northeast Pacific Ocean is described and illustrated. Larvae hatch at approximately
2.7 mm SL and the yolk is absorbed by 3.0 mm SL. Notochord flexion begins between 8.0 and 10.0 mm
SL, is completed at 15.0 mm SL, and transformation occurs between 22.0 and 28.0 mm SL. Larvae have
specific pigment patterns, particularly in the postanal region where melanophores are arranged in two
bars, anterior and posterior. At 5.0-6.0 mm SL, the anterior bar is located at 41-53% SL and the
posterior bar is at 61-74*^^ SL. Melanophore patterns on the head, gut, and caudal region also distin-
guish M. proximus. The occurrence of larvae taken within 18 km of shore off Oregon during plankton
surveys in 1971-72 is discusssed, and data indicate a winter-spring spawning period.

A combination of pigmentation characters, primarily the length and position of the anterior and
posterior pigment bars, and meristic counts can distinguish larvae of M. proximus from Theragra
chalcogramma and Gadus macrocephalus . The anterior bar is located at 47-55% SL in T. chalco-
gramma and at 40-57% SL in G. macrocephalus. The posterior bar is located at 69-79% SL in T.
chalcogramma and at 59-81% SL in G. macrocephalus. Both T. chalcogramma and G. macrocephalus
have 4 rays on the superior hypural element while M. proximus has 5 rays. Other characters useful in
separating the three species include head, gut, mediolateral, postanal, and caudal pigment and stripe
continuitv.

Problems have been encountered in distinguish-
ing larvae of Pacific tomcod, Microg'adusproximas
(Girard); walleye pollock, Theragra chalco-
gramma (Pallas); and Pacific cod, Gadus mac-
rocephalus (Tilesius), in samples from the north-
eastern Pacific Ocean where these three species
might cooccur (Waldron 1972; Dunn and Naplin^).
Larvae of T. chalcogramma were described by
Gorbunova (1954) and Yusa (1954). Larvae of G.
imorhua ) macrocephalus larvae were described by
Gorbunova (1954), Uchida et al. (1958), and
Mukhacheva and Zviagina (1960). In this report
we provide the first published description of the
larvae of M. proximus and comparative material
on larvae of T. chalcogramma and G. mac-
rocephalus that should enable workers to identify

larvae of these three gadids in mixed samples.
Eggs and larvae of the Atlantic tomcod, Micro-
gadus tomcod, were described by Booth ( 1967), but
eggs of M. proximus are unknown.

The geographic range of M. proximus extends
from off central California (Isaacson 1965) to the
Gulf of Alaska and Unalaska Island (Wilimovsky
1964). Their presence in the Bering Sea remains
unconfirmed , although they were reported to occur
in the Bering Sea by Tanner (1894) and Hart
( 1973). Microgadus proximus was not captured in
the eastern Bering Sea during extensive multives-
sel groundfish surveys in 1974 (Pereyra et al. ) or
in 1976 (Bakkala and Smith ). Microgadus prox-
imus is found from near-surface waters to ap-

^Northwest and Alaska Fisheries Center, National Marine
Fisheries Service, NOAA, 2725 Montlake Boulevard East,
Seattle, WA 98112.

^Gulf Coast Research Laboratory, East Beach Drive, Ocean
Springs, MS 39564.

^Dunn, J. R., and N. A. Naplin. 1974. Fish eggs and larvae
collected from waters adjacent to Kodiak Island, Alaska, during
April and May, 1972. Unpubl. manuscr.. 61 p. Northwest and
Alaska Fisheries Center, National Marine Fisheries Service,
NOAA, 2725 Montlake Blvd. E., Seattle, WA 98112.

Manuscript accepted May 1980.

FISHERY BULLETIN: VOL. 78, NO. 4, 198L

■•Pereyra, W. T, J. E.Reeves, and R.G. Bakkala. 1976. De-
mersal fish and shellfish resources of the eastern Bering Sea in
the baseline year 1975. Unpubl. manuscr. Vol. 1, 619 p.; Vol.
2, 534 p. Northwest and Alaska Fisheries Center, National
Marine Fisheries Service, NOAA, 2725 Montlake Blvd. E.,
Seattle, WA 98112.

^Bakkala, R. G., and G. B. Smith. 1978. Demersal fish re-
sources of the eastern Bering Sea: Spring 1976. Unpubl.
manuscr, Vol. 1. 234 p.; Vol. 2. 404 p. Northwest and Alaska
Fisheries Center, National Marine Fisheries Service, NOAA,
2725 Montlake Blvd. E., Seattle, WA 98112.

923

FISHERY BULLETIN; VOL. 78, NO. 4

proximately 220 m (Miller and Lea 1972).
Planktonic larvae of M. proximus were the
dominant gadid and fourth most abundant taxon
in a coastal assemblage offish larvae occurring off
Yaquina Bay, Oreg., in 1971-72 (Richardson and
Pearcy 1977).

Information on the biology and taxonomy of M.
proximus is limited. Schultz and Welander (1935)
presented counts of meristic structures and mor-
phological measurements of M. proximus.
Svetovidov (1948), in his review of Gadiformes,
provided some meristic data and a brief os-
teological description of M. proximus based on two
skeletons. Brief notes on the biology of the species
are included in Clemens and Wilby (1961), Miller
and Lea (1972), and Hart (1973). It is not of com-
mercial importance in part because of its small
size (to 30 cm) but it is taken in recreational
catches (Beardsley and Bond 1970; Hart 1973).

METHODS

Specimens

Several hundred larvae of the three species were
examined in the course of this study. Microgadus
proximus larvae and juveniles were obtained from
plankton and trawl samples collected off Oregon
in 1971-1973 and 1979, by the School of Oceanog-
raphy, Oregon State University (OSU), Corvallis,
and off Washington in 1972 by the Northwest and
Alaska Fisheries Center (NWAFC). Additional
specimens were obtained from plankton collected
in Puget Sound, Wash., in 1977-79 by the Fisheries
Research Institute (FRI), University of Washing-
ton, Seattle; and in 1978 by Ecology Consultants,
Inc., Fort Collins, Colo. Larvae were also collected
from near Kodiak Island, Alaska, in 1977-79 by
FRI.

Theragra chalcogramma larvae were collected
in the eastern Bering Sea (1971, 1976-78) and off
Kodiak Island (1972, 1977-78) by NWAFC. Ad-
ditional specimens from Puget Sound, Wash.,
( 1977, 1978) were provided by FRI and by Ecology
Consultants, Inc., and from off Kodiak Island
(1978) by FRI.

Gadus macrocephalus larvae were collected
near Kodiak Island in 1978 by NWAFC and FRI
and from Puget Sound, Wash., in 1977-79 by FRI.

Radiographs were examined of juvenile and
adult M. proximus and G. macrocephalus speci-
mens in the collections in the Department of
Fisheries and Wildlife, OSU, and NWAFC, and of

adult T. chalcogramma specimens at NWAFC and
from the Institute of Animal Resource Ecology,
University of British Columbia, Vancouver.

Illustrations of larvae were made with the aid of
a camera lucida. All specimens had been preserved
in either 3-5% Formalin,*^ buffered with sodium
borate, or 95% ethanol. Illustrations of caudal fin
development were drawn from cleared and stained
specimens.

Measurements

The following measurements were made on 72
unstained larvae and juveniles (2.7-46.6 mm SL)
of M. proximus using an ocular micrometer in a
stereomicroscope:

Standard length (SL) — Snout tip to notochord tip
prior to development of caudal fin, then to pos-
terior margin of hypural element. (All body
lengths in this study are standard lengths.)

Head length (HL) — Snout tip to posterior edge of
opercle (to pectoral fin base in yolk sac and very
small larvae before opercular margin is visible).

Snout length — Snout tip to anterior margin of
orbit of left eye.

Upper jaw length — Snout tip to posterior margin
of maxillary.

Eye diameter — Greatest diameter of left orbit.

Body depth at pectoral — Vertical distance from
dorsal to ventral body margin at pectoral fin
base.

Body depth at anus — Vertical distance from dor-
sal to ventral body surface at center of anal
opening.

Snout to anus — Distance along body midline from
snout tip to vertical through center of anal open-
ing.

Snout to first dorsal fin — Distance along the body
midline to vertical through origin of anterior-
most dorsal fin ray of first dorsal fin.

Snout to second dorsal fin — Distance along body
midline to vertical through origin of anterior-
most fin ray of second dorsal fin.

Snout to third dorsal fin — Distance along body
midline to vertical through origin of anterior-
most fin ray of third dorsal fin.

Snout to first anal fin — Distance along body mid-
line to vertical through origin of anteriormost
fin ray of first anal fin.

^References to trade names do not imply endorsement by the
National Marine Fisheries Service, NOAA.

924

MATARESE ET AL.: LARVAL DEVELOPMENT OF PACIFIC TOMCOD

Snout to second anal fin — Distance along body
midline to vertical through origin of anterior-
most fin ray of second anal fin.

Meristic Structures

Counts of meristic structures were made on 128
stained M. proximus larvae and juveniles. Sixty-
six specimens (3.1-41.1 mm SL) were cleared and
stained with Alizarin Red S (Taylor 1967), and 62
larvae (5.1-23.4 mm SL) were stained with Aliza-
rin Red and Alcian Blue (Dingerkus and Uhler
1977). Both series of stained samples were used to
make counts of meristic structures and to deter-
mine the onset and sequence of ossification as in-
dicated by the uptake of Alizarin Red. Structures,
including teeth, were considered ossified even if
only slightly stained with Alizarin Red.

Counts on stained larvae and early juveniles
were made of first, second, and third dorsal fin
rays, first and second anal fin rays, caudal fin rays,
left pectoral and pelvic fin rays, branchiostegal
rays, gill rakers, abdominal and caudal vertebrae
(including the postural centrum), and neural and
haemal spines. Counts were made of premaxillary
and dentary teeth on 12 specimens (11.9-41.1 mm
SL).

Counts of meristic structures of juveniles and
adults of M. proximus, T. chalcogramma, and G.
macrocephalus were made from radiographs.
Counts were made of first, second, and third dorsal
fin rays, first and second anal fin rays, caudal fin
rays, and abdominal and caudal vertebrae (includ-
ing the postural centrum).

IDENTIFICATION OF
MICROGADVS PROXIMUS

development of dorsal and ventral procurrent
caudal rays before the development of hypurals.

Considering the collection locations (coastal
Oregon and Washington) and the range of myo-
mere counts, the specimens could have been one of
only three potential species, M. proximus, T. chal-
cogramma, or G. macrocephalus . Meristic charac-
ters in the literature (e.g., Svetovidov 1948; Miller
and Lea 1972; Hart 1973) are inadequate to sepa-
rate all three species. Additional counts obtained
in this study, particularly caudal vertebrae and fin
rays on the superior hypural (Tables 1,2), enabled
positive identification of the series as M. prox-
imus.

DEVELOPMENT OF
MICROGADUS PROXIMUS

Pigment Patterns (Figures 1, 2)

Pigmentation varies in M. proximus larvae but
basic trends persist and are usefiil in distinguish-
ing the larvae. The importance of these pigment
patterns is stressed by Russell ( 1976) for the entire
family Gadidae. He feels many of the early larvae
can be identified exclusively by specific pigment
patterns. We follow his terminology by referring to
the postanal pigment as bars according to their
position, anterior and posterior. Russell's use of
the term "bar" can be confusing, however, when
referring to specific areas within a bar. We define
bar as: anterior and posterior pigment area each
composed of a dorsal and ventral stripe. Descrip-
tions of pigment patterns for M. proximus are
based primarily on 49 (2.7-31.0 mm SL) recently
preserved ( <2 yr) specimens in which fading was
minimal.

A developmental series of M. proximus speci-
mens ranging from late yolk-sac larvae to early
juveniles was linked by pigment patterns, myo-
mere counts, fin development, and meristic counts
in larger specimens. They were identified as
gadids based on three criteria: 1 ) Distinctive pig-
ment patterns, which in small larvae consist of an
anterior and posterior pigment bar, each composed
of a dorsal and ventral stripe. With further growth
of larvae, these bars diffuse into dorso- and ven-
trolateral rows of pigment accompanied by devel-
opment of a mediolateral line of melanophores. 2)
Relatively high (54-58) myomere counts. 3) Pres-
ence of a "pseudocaudal" fin ( Ahlstrom and Counts
1955) at about 8.5 mm SL, as indicated by the

Head Region

Pigment on the head of the smallest larvae
(2.7-3.6 mm SL) is limited to a spot posterior to the
pigmented eye and some melanophores on the
lower jaw (Figure lA). By 4.0 mm SL, 6 or 7
melanophores appear on the nape, 5 or 6 on the
lower jaw, and a few internal as well as external
melanophores on the forebrain. By 5.0 mm SL,
added pigment occurs between the eyes, on both
jaws and at the jaw angle, and internally, posterior
to the eye (Figure IB). Snout pigment appears at
8.0 mm SL (Figure IC), and by 10.0 mm SL, pig-
ment is added over the dorsal region of the head
(Figure IE). Pigment is added to these areas with

925

FISHERY BULLETIN: VOL. 78, NO. 4

B

i^*.*/ « *

mly^J'T * ^^ ^ -tfl?^^f#-y.^^.Ay^^ *'" '•'■••'" '

■ • * •• >»

Figure l. — Larval stages of Microgadus proximus: A. 3.6 mm SL; B. 5.7 mm SL; C. 8.4 mm SL; D. 8.4 mm SL (ventral view);

E. 10.7 mm SL.

926

MATARESE ET AL.: LARVAL DEVELOPMENT OF PACIFIC TOMCOD

m
p

c
>

3

u

0)

a>

CQ

J"
W

g
S

o

of

t

as

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CO

3

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o

927

FISHERY BULLETIN: VOL. 78, NO. 4

Table l. — Summary of adult meristic counts for MicrogaduK proximua, Thcragra chal-
cogramma, and Gadus macrocephalus. Data for T. chalcogramma is after Wilimovsky et
al. (1967)' except where noted.

Fin rays

Vertebrae

First
dorsal

Second
dorsal

Third
dorsal

First
anal

Second
anal

Species

Total

Precaudal Caudal

M. proximus ;
Sample size

37

38

39

38

38

38

38

38

Mean

12.8

188

207

252

229

557

193

36.4

Range

9-15

16-21

17-24

22-28

20-28

54-58

17-20

34-38

T chalcogramma :
Sample size

242

229

235

237

237

98

^49

249

Mean

11.7

14.6

17.7

18.9

188

498

18,7

32.6

Range

10-14

12-18

15-21

16-22

16-23

48-52

18-20

31-34

G macrocephalus:
Sample size

40

41

42

42

41

40

40

40

Mean

12.4

15.6

15.4

ig-r

17,2

53,2

19,9

33.3

Range

10-15

11-22

10-20

17-27

12-25

49-56

18-21

31-35

'From Wilimovsky, N. J.. A. Peden, and L. Peppar. 1967.
Pacific Ocean. Fish. Res. Board Can.. Tech. Rep. 34, 95 p.
^From this study.

Systematics of six demersal fishes of the North

Table 2. — Distribution of caudal rays on the superior hypural
element in Microgadus proximus, Theragra chalcogramma.
andGadus macrocephalus (Walters' and this study).

No. of
specimens

Percentage of caudal rays
on superior hypural

Species

3 4 5 6

M. proximus

T chalcogramma

G. macrocephalus

1.335

241

87

0.0 8.0 92.0 • 0.1
0.0 99.0 10 0 0
0.3 97.0 0.0 0.0

'G. E. Walters, College of Fisheries, University of Washington, Seattle, WA
981 15, pers. commun. January 1979.

development, and by 16.0 mm SL it becomes more
concentrated on the jaws, jaw angle, snout, be-
tween the eyes, and over the head extending to the
nape (Figure 2A). Several melanophores appear
ventrally along the median cartilage between the
dentaries and urohyal. With transformation
(completion of fin development) at 22.0-28.0 mm
SL, small and densely concentrated melanophores
are added to the jaws and dorsal head (Figure 2B).
The opercular area is unpigmented.

Gut Region

Melanophores line the dorsal surface of the gut
cavity in the smallest larva (2.7 mm SL), and
several spots are on the ventral abdominal surface
anteriorly. The isthmus is pigmented by 4.0 mm
SL. Melanophores increase in number on the dor-
sal and ventral gut surface with development.
Melanophores are added laterally, occurring first
anteriorly near the base of the pectoral fin at 5.0
mm SL (Figure IB). The melanophores on the ven-
tral surface of the gut extend more posteriorly,
forming a rough line nearly to the anus by 8.0 mm
SL (Figure IC, D). Gut pigmentation changes

little through transformation, except for ad-
ditional melanophores on the lateral surface (Fig-
ure 2A). In early juveniles, the lateral pigment is
more internal than external and the overlying
skin is unpigmented (Figure 2B). Along the ven-
tral surface of the gut is a single row of small
melanophores. The base of the pectoral fin is pig-
mented.

Postanal Region

Pigment in the postanal region is an important
diagnostic character for M. proximus larvae. The
smallest larvae (2.7-3.6 mm SL) have two pigment
bars, anterior and posterior. The stripes within the
pigment bars are double rows of melanophores
with pigment on both sides of the body along the
dorsal and ventral midline. At first, the dorsal
stripes consist of only 1 or 2 melanophores on each
side, but increase to 2 or 3 anteriorly and 6-8
posteriorly by 3.6 mm SL (Figure 1 A). The ventral
stripes on each side have 4 or 5 spots anteriorly
and 7 or 8 spots posteriorly by 3.6 mm SL (Figure
lA). At 3.6 mm SL the anterior bar is located at
42-50% SL (myomeres 16-22) and the posterior bar
is at 59-72% SL (myomeres 29-37). With develop-
ment, melanophores are added along the ventral
stripes between the bars, becoming continuous
with them by 5.7 mm SL (Figure IB). The two
dorsal stripes remain separate until 15.0 mm SL,
although occasionally a few melanophores may be
seen between them. Pigment is added along the
body midline, externally at 7.5 mm SL and in-
ternally at 9.5 mm SL (Figure IC, E). Postanal
pigmentation changes are minimal for larvae be-
tween 10.0 and 14.0 mm SL, except for the addi-

928

MATARESE ET AL : LARVAL DEVELOPMENT OF PACIFIC TOMCOD

tion of some spots laterally and in the dorsal and
anal fin folds. By 15.0-16.0 mm SL, additional
melanophores occur along the dorsolateral and
ventrolateral surface, but those in the bars remain
enlarged and distinctive (Figure 2 A). After trans-
formation, the larval pigment bars are no longer
visible and the entire lateral area is pigmented, as
are the dorsal and anal fins (Figure 2B).

Posterior to the second pigment bar, mela-
nophores occur in the caudal region along the
ventral body margin in the smallest larvae, con-
nect with the ventral stripes by 5.7 mm SL (Figure
IB), and extend to the notochord tip by 6.2 mm SL.
Caudal melanophores are smaller and less den-
dritic than those in the bars and appear as a single
ventral midline row (Figure ID). Several
melanophores are added on the dorsal body mar-
gin posterior to the second pigment bar by 10.0
mm SL and, eventually, to the caudal fin fold ven-
trally and posteriorly by 15.0 mm SL. By 16.0 mm
SL the dorsal and ventral midlines are dis-
tinctively lined with melanophores, and the
lateral midline pigment, both internal and exter-
nal, extends to the tail tip (Figure 2A). The pro-
ximal portion of the caudal fin is pigmented. After
transformation pigment covers most of the fin
(Figure 2B).

Morphology (Tables 3, 4)

Larvae of M. proximus are moderately elongate
with the greatest body depth, about 19% SL, oc-
curring at or near the pectoral fin base. The body
tapers slightly toward the anus and then narrows
abruptly posterior to the anus. The gut is only
moderately long. The distance from snout to anus
ranges from 41% to 48% SL in larvae and declines
to 45% SL in juveniles. In our smallest yolk-sac
larva (2.7 mm SL), the vent opens laterally to the
right near the ventral fin fold and does not become
vertical until the larvae reach about 7.5-8.5 mm
SL. This lateral position of the anus in small gadid
larvae was reported by Marak ( 1967) and Russell
(1976). All yolk is absorbed by 3.0 mm SL.
Notochord flexion is protracted, beginning at
about 8-10 mm SL and ending at about 15 mm SL.
Transformation begins at about 22 mm SL and is
completed at about 27-28 mm SL. The largest
pelagic specimen collected was 46.6 mm SL.

Head length as a proportion of standard length
increases from 22% SL in preflexion larvae to 32%
SL in transforming specimens. It declines to 30%
SL in pelagic juveniles. Eye diameter as a propor-

tion of head length decreases from 35% HL in
preflexion larvae to 25% HL in pelagic juveniles,
whereas snout length/head length increases from
18% HLto29% HL. Upper jaw length/head length
and body depth at pectoral fin base/standard
length remain relatively constant, increasing only
slightly from preflexion larvae to the pelagic
juvenile stage. Depth at anus/standard length in-
creases from 11% SL in preflexion larvae to 19%
SL in juveniles.

The distance from the snout to the origin of the
first dorsal fin as a proportion of standard length
decreases slightly during development while the
distance from the snout to the second dorsal fin/
standard length remains nearly constant. The
length from the snout to the origin of the third
dorsal fin/standard length increases slightly dur-
ing development.

Distances from the snout to the origin of the first
anal fin/standard length decreases slightly from
47% SL in larvae undergoing notochord flexion to
45% SL in pelagic juveniles, whereas the snout to
second anal fin distance/standard length increases
slightly from 63% SL in larvae undergoing
notochord flexion to 68% SL in pelagic juveniles.

Meristic Structures
(Tables 5, 6; Figure 3)

Considerable variation occurs in the develop-
ment of meristic structures as the size at which
bones ossify varies from specimen to specimen
(Table 5). The following discussion approximately
parallels the sequence of development of meristic
characters in M. proximus. Terminology of bones
follows Ahlstrom and Counts (1955) and
Ahlstrom.'^

Head and Axial Skeleton

Branchiostegals can be discerned in some
specimens as small as 3.9 mm SL. Ossification
begins in some larvae at 8.1 mm SL, but the full
complement of seven branchiostegals is not consis-
tently ossified until the larvae are about 19 mm
SL. The sequence of ossification of branchiostegals
is from upper to lower.

Teeth begin ossifying on the dentary in 11.9 mm
SL larvae (Table 6). Initially, the number of teeth

'E. H. Ahlstrom, Southwest Fisheries Center, National Ma-
rine Fisheries Service, NOAA, La Jolla, CA 92038, pars, com-
mun. Julv 1979. (Deceased.)

929

Table 3.

FISHERY BULLETIN; VOL. 78. NO. 4

-Morphometric measurements, in millimeters, of larvae and juveniles of Microgadus proximus. Specimens between

dashed lines are undergoing notochord flexion.

Upper

Depth

Depth

Snout

Snout to

Snout to

Snout to

Snout to

Snout to

Standard

Head

Eye

Snout

jaw

at

at

to

first

second

third

first

second

length

length

diameter

length

length

pectoral

anus

anus

dorsal

dorsal

dorsal

anal

anal

2.7

0.6

0.2

0.1

0.5

0.3

1.0

2.9

0.6

0.2

0.1

0.5

0.3

1.1

3.4

0.7

0.3

0.1

0.4

0.3

1.4

3.8

0.8

0.3

0.1

0.5

0.4

1.4

4.1

0.8

0.3

0.1

0.6

0.4

1.7

4.2

0.7

0.3

0.2

0.5

0.9

0.5

1.5

4.5

1.2

0.3

0.1

0.3

1.1

0.5

1.9

4,7

0.9

0.4

0.1

0.3

0.8

0.5

20

5.1

1.2

0.4

0.2

0.9

0.6

2.3

5.4

1.0

0.4

0.1

0.9

0.5

2.0

55

1.2

0.4

0.2

0.3

1.0

0.5

2.4

5.9

1.5

0.5

0.2

0.4

1.0

0.6

2.6

6.1

1.5

0.5

0.3

0.4

1.1

0.7

2.4

6.6

1.6

0.5

0.3

0.6

1.1

0.7

2.9

6.9

1.4

0.5

0.4

0.6

1.2

0.8

2.6

7.1

1.7

0.6

0.4

0.7

1.3

0.9

3.3

7.3

1.8

0.5

0.4

0.7

1.3

0.9

3.1

7.5

1.6

0.5

0.4

0.6

1.2

0.8

3.3

7.9

1.7

0.6

0.4

0.6

1.3

0.9

3.4

8.1

2.0

0.7

0.5

0.7

1.6

1.2

3.6

8.3

2.1

0.7

0.6

0.9

1.6

1.2

3.6

8.7

2.0

0.7

0.4

0.9

1.6

1.3

4.0

8.9

2.3

0.7

0.6

0.8

1.6

1.3

4 1

9.0

2.2

0.7

0.6

1.0

1.6

1.2

4.0

9.2

2.2

0.7

0.6

1.0

1.7

1.2

4.0

9.3

2.3

0.7

0.6

1.0

1.9

1.5

4.1

3.3

4.2

6.0

9.6

2.2

0.7

0.6

0.9

1.8

1.4

4.4

9.7

2.5

0.7

0.7

1.0

1.8

1.5

4.5

10.1

3.0

0.8

0.9

1.2

2.1

1.9

4,8

36

4.8

6.7

4.9

6.7

10.2

2.2

0.8

0.6

1.0

1.8

1.4

4.4

10.5

2.8

0.9

0.7

1.2

2.1

1.7

4.8

3.6

4.9

4.9

10.8

2.9

0.9

0.7

1.2

2.1

1.7

4.6

3.7

4.9

4.7

11.4

2.9

0.9

0.7

1.3

2.1

1.9

5.2

4.1

5.1

5.3

11.7

2.8

0.9

0.8

1.2

2.1

1.9

5.1

3.9

5.2

7.4

5.2

12.0

3.0

1.0

0.8

1.2

2.3

2.1

5.3

3.9

5.3

7.8

5.3

12.5

3.4

1.0

0.8

1.2

2.5

2.2

58

4.5

6.0

6.0

12.7

3.5

1.2

0.9

1.4

2.6

2.2

6.0

4.4

6.0

8.4

6.0

8.6

12.9

3.5

1.2

0.9

1.4

2.6

2.6

6.3

4.7

6.4

8.8

6.5

8.8

13.5

3.5

1.1

1.0

1.4

2.6

2.4

6.3

4.7

6.2

8.6

6.4

9.1

13.7

3.8

1.2

1.1

1.4

2.6

2.5

6.6

4.9

6.4

9.2

6.6

9-8

14.0

3.8

1.1

1.0

1.7

2.8

2.8

6.5

4.7

6.2

9.0

6.5

9.3

14.2

4.0

1.2

1.0

1.5

2.8

2.5

6.7

5.0

6.7

9.2

6.7

9.3

14.5

4.3

1.3

1.3

1.7

3.0

2.7

7.2

5.3

7.0

9.7

7.2

9.8

14.7

4.5

1.3

1.3

1.7

3.0

2.7

7.3

5.7

7.3

10.5

7.5

10.2

15.2

4.5

1.3

1.2

1.7

3.0

2.7

7.2

5.2

6.8

10.0

7.2

10.0

15.3

4.5

1.3

1.2

1.8

3.3

3.0

7.5

5.7

7.3

10.8

7.5

10.5

15.5

4.3

1.3

1.3

1.7

3.0

2.8

7.3

5.7

7.5

10.2

7.5

10.2

16.2

5.0

1.4

1.4

1.8

3.5

3.3

7.8

5.8

7.8

10.7

8.0

9.2

16.5

4.7

1.3

1.3

1.7

3.5

3.2

8.0

5.8

7.7

11.0

8.2

10.8

17.0

4.8

1.4

1.4

1.8

3.4

2.7

8.5

6.2

8.0

11.5

8.7

11.3

18-3

5.3

1.5

1.7

2.0

3.8

3.3

8.8

6.7

8.8

12.3

9.0

12.5

19.0

5.5

1.5

1.7

2.0

3.5

3.5

93

6.5

9.5

12.8

9.5

12.7

20.0

5.7

1.6

1.7

2.2

4.2

3.7

9.3

7.2

9.5

13.6

9.5

13.2

21.0

6.2

1.7

1.8

2.3

4.3

4.2

10.0

7.5

10.3

14.7

10.0

14.7

'22.1

6.1

1.8

1.7

2.7

4.7

4.3

10.5

7.8

10.8

15.3

10.5

14.8

'23.5

6.8

1.9

2.0

2.7

4.8

4.5

10.6

8.2

10.8

16.0

10.8

16.2

'24.0

8.2

1.9

2.0

2.8

5.2

4.7

11.3

8.5

11.5

16.2

11.5

16.3

'25.2

7.8

2.1

2.3

3.0

5.5

5.2

11.8

8.8

12.2

17.5

12.0

175

'26.3

9.5

2.2

2.5

3.2

5.5

5.5

12.5

9.2

12.2

18.0

12.5

18.2

=27.3

8.2

2.2

2.5

3.3

5.7

5.3

13.5

9.5

12.9

18.3

13.7

20.0

228.0

8.7

2.3

2.5

3.5

6.0

5.7

14.3

9.7

13.2

19.7

14.8

20.6

^29.3

9.2

2.3

2.7

3.7

6.3

5.7

14.2

10.3

13.8

20.5

14.2

20.3

231.3

9.5

2.5

2.8

3.8

6.3

5.7

14.2

11.2

14.7

21.7

14.3

20.8

232.1

9.7

2.5

2.8

3.7

6.5

5.8

14.2

11.2

14.7

21.3

14.5

22.0

234.3

10.8

2.5

2.8

4.0

7.5

7.2

15.3

11.7

16.0

22.8

15.8

23.3

236.7

10.8

2.7

3.0

4.5

7.7

7.3

15.2

11.7

16.8

24.6

15.7

24.6

238.0

10.8

3.0

3.2

4.5

7.8

7.5

16.5

12.8

17.5

25.5

16.5

25.8

238.2

11.0

2.7

3.5

4.5

7.8

7.2

15.5

13.0

17.8

25.7

16.2

25.8

240.1

11.7

2.8

3.5

4.7

7.9

7.2

16.7

12.8

18.0

26.0

17.0

26.3

241.1

11.2

2.9

3.5

3.3

8.2

7.2

17.3

13.3

17.8

25.8

17.3

24.0

241.3

12.5

3.0

3.8

5.0

8.3

8.2

183

14.0

19.0

27.8

18.0

27.3

246.6

14.0

3.3

4.0

5.8

9.7

9.5

20.0

15.0

21.0

31.5

20.2

32.1

'Transforming.
2Pelaglc juvenile.

930

MATARESE ET AL.: LARVAL DEVELOPMENT OF PACIFIC TOMCOD

Table 4. — Body proportions of larvae and juveniles of Microgadus proximus. Values given for each body proportion are expressed
as percentage of standard length (SL) or head length (HL): mean, standard deviation, and range.

Body proportion

Preflexion

Flexion

Postflexion

Transforming

Pelagic juvenile

Sample size

'19

225

10

5

13

Standard length (mm)

5.3±1.6 (3-8)

11.2=2,1 (8-15)

17.4=2.1(15-21)

24.2 = 1.6(22-26)

35.7 = 5.9(27-47)

Snout to anus ler.gtti SL

41.2*3.3 (36-47)

45.9 = 2.0(43-50)

48.1 = 1.0(47-50)

46.8 = 1.0(45-48)

44.6 = 3.3(41-51)

Head length SL

21.9=2.6 (17-27)

26.0 = 2.2(22-31)

29.0=0.9(28-31)

31.6 = 3.6(28-36)

29.9=1.2(27-32)

Eye diameter HL

35.1 ±5.0 (25-44)

31,6 = 2.3(27-36)

28.4=0.9(27-30)

26.1=2.8(23-30)

25.3 = 1.4(23-28)

Snout length HL

17.8±7.0 (5-29)

26.6=2.3(20-30)

29 0 = 1.8(27-32)

27.5 = 2.2(24-30)

29.4 = 1.5(26-32)

Upper jaw length HL

36.8=12.7(25-71)

40.9 = 3.4(35-46)

37,7 = 1,4(36-40)

38.1=4.4(34-44)

39.3=3.2(30-42)

Body depth at pectoral fin base/SL

17.3=2.7 (12-24)

19.3 = 1.0(18-21)

20,4 = 1,0(18-22)

21.2=0.6(20-22)

20.7 = 0.7(20-22)

Depth at anus/SL

10.8 = 1.1 (9-13)

16,5 = 2,0(13-20)

18,6 = 1,3(16-20)

20.0=0.7(19-21)

19.3 = 1 1(18-21)

Snout to first dorsal fin SL

35,2 = 1,5(33-39)

35.8 = 1,0(34-37)

35.1=0.2 (35)

33.8 = 1.3(31-36)

Snout to second dorsal fin SL

46,6 = 1,8(44-50)

47,7=1,4(45-50)

47,5 = 1,3(46-49)

46.1=1.1(43-47)

Snout to third dorsal fin SL

66,0 = 2,3(63-71)

67.5 = 1,7(66-71)

68,5 = 0.8(68-69)

67.2 = 2.0(63-70)

Snout to first anal finSL

47,3=2,2(44-51)

48,9=1,2(47-51)

47.3=0.7(46-48)

45.3 = 3.4(42-53)

Snout to second anal fin SL

62.5 = 1.6(19-72)

66,0=3.6(57-70)

68.5=1.0(67-69)

67.7=3.7(58-74)

'Sample size is 12 for upper jaw length,

^Sample size is 1 6 each for distances from snout to first dorsal fin and snout to second dorsal tin; 1 2 for distance from snout to third dorsal fin; 1 5 for distance
from snout to first anal fin; and 9 for distance from snout to second anal fin.

on the dentary exceeds the number on the pre-
maxilla, but this is reversed at about 23 mm SL
with the difference increasing with growth. A
similar change in number and location of teeth
was reported to occur on the Pacific whiting, Mer-
luccius productus (Ahlstrom and Counts 1955).

In larval and transforming specimens (11.9-22.3
mm SL), teeth are irregularly spaced and clus-
tered in groups. Some are caninelike and others
are recurved. As the larvae grow, the teeth become
more closely spaced as the numbers of teeth in-
crease and approach biserialization in 34.3 mm SL
juveniles, similar to that described for Pacific
whiting (Ahlstrom and Counts 1955).

Gill rakers begin ossifying at 9.6 mm SL and all
(3 + 20 = 23) gill rakers are ossified in a 24.3 mm
SL larva.

Neural spines in the abdominal region begin to
ossify at about 8.7 mm SL and all are ossified by 11
or 12 mm SL. Ossification generally proceeds pos-
teriorly. Neural spines of the caudal region also
begin ossifying at about 8.7 mm SL but ossification
is not complete until specimens are 17 mm SL. The
neural and haemal spines of the third to sixth
vertebrae preceding the postural centrum begin to
accept alizarin stain before other neural spines in
the caudal region. Haemal spines ossify in a se-
quence similar to neural abdominal spines; all
spines are ossified by 17 mm SL. The last neural
and haemal spines to ossify are those associated
with the terminal preural vertebrae. These spines
are broadly flattened and ossify simultaneously
with other bones of the caudal complex, as dis-
cussed later (Figure 3).

Vertebral centra in both the abdominal and
caudal regions begin to ossify at about 8.7 mm SL
and ossification is completed by 11 mm SL and

about 19 mm SL. Ossification proceeds from an-
terior to posterior.

Fins

Median and paired fins showed some variation
in development, with fin rays first forming at dif-
ferent body lengths in individual specimens (Table
5). Fin formation occurs in the sequence: larval
pectoral fins; caudal fin; first anal fin; second anal
fin; third, second, and first dorsal fins (nearly
simultaneously); pelvic fins; and pectoral fins with
rays.

The pterygiophores supporting anal and dorsal
fin rays begin ossifying at 23.4 mm SL and os-
sification is complete by 31.1 mm SL. Too few
specimens were available to follow the sequence of
ossification.

Larval pectoral fins are present in our smallest
specimen (2.7 mm SL). They consist of a fleshy
base and an undifferentiated membrane. They
persist until rays begin differentiating late in the
larval period.

The caudal fin of M. proximus is associated with
a complex of 16 centra (2 ural and 14 preural
centra), 14 neural and haemal spines. 2 epurals, 1
superior hypural (HY 4-6), and 2 inferior hypurals
(HY2-3,HY1) (Figure 3).

Caudal rays total 49-56, of which 22-25 are dor-
sal in origin, 22-26 are ventral in origin, and five
are normally supported by the superior hypural.
Principal caudal rays number 32-33; of these, 12 or
13 are dorsal in origin and 13 or 14 are ventral in
origin. One each is attached to the two epurals, five
are carried on the superior hypural, two on
hypural 2-3, and one on hypural 1.

As with the Pacific whiting (Ahlstrom

931

FISHERY BULLETIN; VOL 78. NO. 4

and Counts 1955), some of the anterior caudal
rays, both dorsally and ventrally, articulate with
unmodified neural and haemal spines; other rays
lie between the spines with no basal supports
(Figure 3).

A symmetrical fin fold surrounds the tip of the
notochord in specimens 3.1-5.5 mm SL (Figure 3).
In 7.5 mm SL larvae, mesenchymal thickenings
occur dorsal and ventral to the notochord. By 7.8
mm SL, the ventral thickening is differentiated
into three cartilaginous plates constituting
hypurals 1, 2, and 3 anteriorly, and hypurals 4-6
posteriorly (Figure 3B). In 9.5 mm SL specimens
fin rays are considerably increased in number
( Figure 3C). In 10.5 mm SL specimens the urostyle
begins to flex, and the unossified hypurals 1, 2-3,
and 4-6, as well as epurals 1 and 2 are differen-
tiated (Figure 3D). Ossification proceeds rapidly
during notochord flexion from anterior to posterior
regions of the caudal complex. By 11.9 mm SL
(Figure 3E), all preural centra are ossified, and all
hypurals and both epurals have begun ossifying.
Caudal fin rays have begun ossifying, beginning
ventrally in the region of the inferior hypurals.

By 15.0 mm SL, all centra except the postural
centrum are ossified; the hypurals and epurals are
incompletely ossified (Figure 3F). Rays continue

ossifying, proceeding posteriorly on the ventral
margin and on the superior hypural and pro-
gressing anteriorly from epural number 2. By 19.4
mm SL all caudal rays posterior to preural cen-
trum 12 are ossified. By 25.0 mm, the caudal fin is
completely ossified (Figure 3G) and resembles in
all details that of a 41.1 mm SL juvenile (Figure
3H).

We were unable to detect fusion of hypurals in
the caudal fin of M. proximus during ontogeny. In
the smallest larvae in which we could detect de-
velopment of hypural elements (7.8-8.1 mm SL),
only three hypurals could be observed. We believe,
however, that these hypurals represent 1) an an-
terior, inferior hypural 1 (parhypural); 2) an in-
ferior hypural representing a fusion of hypurals 2
and 3; and 3) a superior hypural representing a
fusion of hypurals 4-6. This reasoning is predi-
cated on 1) it is generally accepted that the
evolutionary trend in fishes is toward a reduction
in the number of hypurals, presumably by fusion
of the constituent elements (Gosline 1961; Rosen
and Patterson 1969; Marshall and Cohen 1973); 2)
members of the family Moridae, generally consid-
ered a more primitive family than Gadidae
(Svetovidov 1948; Greenwood et al. 1966; Rosen
and Patterson 1969), possess three inferior and

B

//Z^z/lz2z^

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Saf

932

MATARESE ET AL.: LARVAL DEVELOPMENT OF PACIFIC TOMCOD

NS

FIGURE 3.— Development of the caudal fin oiMicrogadus proximus: A. 5.2 mm SL; B. 7.8 mm SL: C. 9.5 mm SL; D. 10.5 mm SL; E. 1 1.9
mm SL; F.15.8 mm SL; G. 25.0 mm SL; H. 41 . 1 mm SL. AUG = anterior ural centrum; EP = epural; HS = haemal spine; HY = hj^pural;
NG = notocord; NS = neural spine; PG = preural centrum; PUG = postural centrum; TPG = terminal preural centrum. Ossified
elements are stippled.

three superior hypurals (Fitch and Barker 1972);
and 3) presumably more advanced families of
fishes in the same evolutionary line as gadids ( e.g.,
order Batrachoidiformes) have tw^o hypurals, ap-
parently representing fusion of component parts
(Rosen and Patterson 1969).

Barrington (1937), who figured and described
the development of the caudal fin in G. morhua,
provides the only other description of caudal de-
velopment in gadids. His illustrations also depict
only three hypural elements. Barrington, how-
ever, considered it unlikely that fusion of hypural
bones could occur without some evidence of com-
pound origin remaining in the fused bones. Our

terminology of the caudal fin bones differs from
that used by Barrington ( 1937) for G. morhua. We
consider his ventral radial as hypural 1 and his
dorsal radials 1 and 2 to be epurals 1 and 2.

Also we found no evidence of a uroneural in the
development of the caudal fin of M. proximus.
Rosen and Patterson ( 1969) consider the presence
of one uroneural as a characteristic of the
Gadiformes.

An anlage of the first anal fin is evident by 8.7
mm SL and the base of the second anal fin is
present at 9.3 mm SL. Rays in the first anal fin
begin ossifying at about 11.9 mm SL and in the
second anal fin at 12.7 mm SL. Ossification is

933

FISHERY BULLETIN: VOL. 78. NO. 4

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934

MATARESE ET AL.: LARVAL DEVELOPMENT OF PACIFIC TOMCOD

Table 6. — Numbers of teeth on premaxillary and dentary bones
in selected sizes of larval and juvenile Microgadus proximus.

Teeth on left side

Size of specimen

(mm SL)

Premaxilla

Dentary

Larvae:

11.9

0

1

13.2

0

6

15.0

0

6

15.8

0

6

17.2

8

10

18.0

6

8

Transforming:

223

10

14

23.4

30

24

24.3

32

27

Juveniles:

28.6

36

24

34.3

44

35

41.1

49

38

complete in the first anal fin at 23.0 mm SL and in
the second anal fin at 27 or 28 mm SL. Ray develop-
ment within a fin proceeds anterior to posterior.

Dorsal fins develop in a manner analogous to the
anal fins and the three dorsal fins develop almost
simultaneously. Dorsal fins 2 and 3 commence os-
sification at 12.9 mm SL, and dorsal fin 1 begins
accepting stain at 13.2 mm SL. Ossification is
complete in the first and second dorsal fins at 22.0
mm SL and in the third dorsal at 28.0 mm SL. Rays
ossify from anterior to posterior.

Pelvic buds appear at about 8.0 mm SL. Pelvic
fins begin ossifying at about 14.0 mm SL and are
consistently ossified in 26.0 mm SL early juve-
niles. Pectoral fins initiate ossification at 15.0 mm
SL and reach their full complement of 18-20 rays
in 28.0 mm SL juveniles.

Scales

Scales begin developing in the anterior portion
of the body near the dorsal tip of the cleithrum in
28.6 mm SL specimens. Development appears to
progress along the lateral line as the juveniles
grow. Scale development was not complete in our
largest specimen, 41.1 mm SL.

Occurrence of Microgadus proximus
(Figure 4)

Although a number of ichthyoplankton studies
have been conducted in the northeastern Pacific
Ocean, data on occurrence of M. proximus are
limited because of past difficulties in distinguish-
ing the larvae from other gadids. Larvae of this
species may be included under the broader cat-
egory of Gadidae listed in some papers (e.g.,

Waldron 1972; Pearcy and Meyers 1974). Some
data on distribution and seasonal abundance,
however, are available.

Larvae of M. proximus are found in coastal
waters off Oregon occurring mainly within 18 km
of shore with abundance peaks at about 6 and 9 km
(Richardson and Pearcy 1977; Richardson^). A few
specimens have been reported as far as 74 km
offshore (Richardson footnote 8).

The larvae have been collected in the plankton
off Oregon from February through August with
peak abundance from March through July
(Richardson footnote 8). Misitano ( 1977) also col-
lected four specimens, 5-61 mm SL, from March to
July in the Columbia River mouth.

Monthly length frequencies and median lengths
of larvae collected in 1971 and 1972 off Oregon
indicate a winter-spring spawning period (Figure
4). Small larvae, ^5 mm SL, were collected Feb-
ruary through June.

Larvae of M. proximus were collected 24 km off
coastal Washington (Cruise K-72-2-III) in early
June 1972, by the NWAFC^. This species ac-
counted for 22.2% of the total catch offish larvae,
and specimens ranged from 5.0 to 26.0 mm SL.

COMPARATIVE NOTES ON

THERAGRA CHALCOGRAMMA AND

GADUS MACROCEPHALUS

(Figure 5, Table 7)

In the northeastern Pacific Ocean, larvae of M.
proximus are similar to those of T. chalcogramma
and G. macrocephalus at sizes <16.0 mm SL. Iden-
tification of all three species in mixed samples is
difficult with previously available literature,
which describes T. chalcogramma and G. mac-
rocephalus from the northwestern Pacific Ocean
(e.g., Gorbunova 1954; Uchida et al. 1958;
Mukhacheva and Zviagina 1960). We have sum-
marized characters which are useful to distin-
guish each species at sizes <16.0 mm SL based on
our examination of specimens of all three species
(Table 7).

The most useful character to separate the
smaller larvae (hatching to 10.0 mm SL) of the

»Richardson, S. L. 1977. Larval fishes in ocean waters off
Yaquina Bay, Oregon: abundance, distribution, and seasonality
Januarv 1971 to August 1972. Oregon State Univ., Sea Grant
Coll. Program Publ. ORES-T-77-003, 73 p.

^Data on file for Cruise K-72-2 (III), 1972, Northwest and
Alaska Fisheries Center, National Marine Fisheries Service,
NOAA, 2725 Montlake Blvd. E., Seattle, WA 98112.

935

FISHERY BULLETIN VOL. 78, NO. 4

CD

E

10

0

10

^ 0

=! 40

T3

.- 30

■o

- 20

10

0

20

10

0

0
0

11^

X o

ia^^^^KilMMUi

JZZL

O X

February N = n (I97i:

March N = 52 (1971)
N = 32 (1972)

April N = 48 (1971)
N = 28 (1972)

May N = 228 (1971)
N = 15 (1972)

June N = 223 (1971)
N = 13 (1972)

iiii ■:-S:g>^ I I C3 cm CZL

July N = 103 (197i:
N = 5 (1972)

I I i I I I I I I
5 10

rt.

1

August N = 7 (1971)
N = 3 (1972)

I ' I' I' I I' I • r t i' I I I I I Id)"' I ' I ' I I ' 'f

15 20 25 30 35

Length class (mm)

Figure a. — Length-frequency histograms of Microgadus proximus larvae collected in 70 cm bongo nets off Oregon in 1971 (unshaded)
and 1972 (shaded). X = median length class of larvae in 1971; O = median length class of larvae in 1972.

three species is the length and position of the an-
terior and posterior postanal pigment bars. In M.
proximus larvae 5.0-6.0 mm SL (Figure IB), the
anterior bar begins just posterior to the anus at

41-53% SL (myomeres 14-23) and the posterior bar
is at 61-74% SL (myomeres 28-39). In T. chalco-
gramma larvae of the same size range (Figure 5A),
the anterior bar begins posterior to the anus at

936

MATARESE ET AL.: LARVAL DEVELOPMENT OF PACIFIC TOMCOD

47-55^ SL( myomeres 2 1-26) and the posterior bar
is at 69-79^f SL (myomeres 36-43). The anterior
bar begins posterior to the anus for similar size G.
macrocephalus larvae (Figure 5C) at 40-57% SL
(myomeres 16-261 and the posterior bar is at
59-8 IT^ SL (myomeres 26-42). Differences also
exist in the number of melanophores in the stripe
within a bar and associated bar length. This latter
character, however, is only useful at small sizes
(2.5-4.5 mm SL) because melanophores increase
with development and the stripes become continu-
ous. At 3.6 mm SL (Figure lA), M. proximus lar-
vae have on each side two dorsal and four ventral
melanophores in the stripes within the small an-
terior bar, and seven melanophores each in the
longer dorsal and ventral stripes within the pos-
terior bar. Similar sized T. chalcogramma larvae
(4.1 mm SL) have evenly sized stripes with five
melanophores on both the dorsal and ventral
stripe of the anterior bar. and five dorsal and seven
ventral melanophores in each stripe of the pos-
terior bar. Gadus macrocephalus larvae (4.4 mm
SL) have longer stripes than the other two species,
with 7 dorsal and 8 ventral melanophores on the
anterior bar, and 11 dorsal and 10 ventral
melanophores on the posterior bar.

With development these pigment stripes within
the bars variously remain separate or become
connected depending on the species. In M. prox-
imus larvae the ventral stripes become continuous

at 5.0-6.0 mm SL (Figure IB) while the dorsal
stripes remain separate until 13.0 mm SL. The
dorsal stripes become continuous in T. chalco-
gramma larvae at 13.0 mm SL whereas the ven-
tral stripes never connect. Gadus macrocephalus
larvae have continuous dorsal and ventral stripes
of melanophores by 5.0-6.0 mm SL (Figure 5C).

Other pigment differences may help in distin-
guishing species at certain size ranges. Early G.
macrocephalus larvae (4.0-8.0 mm SL) have more
head pigmentation than the other two species,
particularly on the dorsal surface and in the snout
area (Figure 5C). Theragra chalcogramma larvae
(<13.0mm SL) have much less lateral pigment on
the surface of the gut than either M. proximus or
G. macrocephalus larvae (Figure 5B). Gadus mac-
rocephalus larvae (5.0-8.0 mm SL) have more
mediolateral pigmentation between the postanal
bars than the other two species in that size range
(Figure 5C). Caudal pigment also differs and at
sizes <10.0 mm SL can separate M. proximus.
Only M. proximus larvae have a single row of
ventral caudal melanophores posterior to the anal
fin (Figure ID) whereas both T. chalcogramma
and G. macrocephalus larvae have isolated pig-
ment spots (Figure 5B, D).

Also helpful in distinguishing M. proximus lar-
vae from the other two species is the possession of
five rays on the superior hypural compared with
four rays for T. chalcogramma and G. mac-

TabLE 7. — Characters useful in separating lar\'ae of Microgadus proximus, Theragra chalcogramma, and Gadus macrocephalus at

specific size ranges.

Character

Size range
(mm)

Microgadus
proximus

Theragra
chalcogramma

Gadus
macrocephalus

Anterior pigment bar
Percentage of SL
Located at myomeres
Posterior pigment bar
Percentage of SL
Located at myomeres
Number of melanophores in each stripe of;
Anterior bar
Dorsal
Ventral
Posterior bar
Dorsal
Ventral
Degree of stripe continuity;
Anterior bar:
Dorsal
Ventral
Posterior bar;
Dorsal
Ventral
Head melanophores

fvlelanophores on ventral surface of gut

Lateral pigment on gut surface
Mediolateral pigment In postanal region
Ventral caudal pigment
Number of rays on superior hypural element

5-6

41-53

47-55

40-57

14-23

21-26

16-26

5-6

61-74

69-79

59-81

28-39

36-43

26-42

3-4

2

5

7

4

5

8

3-4

7

5

11

7

7

10

5-13

Separate

Separate

Continuous

Continuous

Separate

Continuous

13-16

Separate

Continuous

Continuous

Continuous

Separate

Continuous

4-8

—

—

More on dorsal surface
and snout

>13

1 -2 rows of spots

No spots or a few reduced
spots

1-2 rows of spots

<13

—

Much less

—

5-8

—

—

More

<10

Row of spots

Isolated spots

Isolated spots

>13

5

4

4

937

FISHERY BULLETIN: VOL. 78, NO. 4

B

Figure 5. — Larvae of Theragra chalcogramina and Gadus macrocephalus: A. T. chalcogramma, 6.2 mm SL; B. T. chalcogramma,

9.8 mm SL; C. G. macrocephalus, 5.6 mm SL; D. G. macrocephalus, 8.5 mm SL.

rocephalus . This character can be useful in a size
range O13.0 mm SL) which may be troublesome
when pigment patterns are no longer helpful and
adult characters (e.g., barbel length, mouth and
anus position, or shape of fins) are not fully de-
veloped. Larvae >20.0 mm SL may also be dis-
tinguished by a combination of meristic counts
(Table 1).

ACKNOWLEDGMENTS

We thank the following at the NWAFC, NMFS,
938

NOAA: Beverly Vinter who provided great assis-
tance in the interpretation of distinguishing
characteristics in gadid larvae and illustrated the
larvae and caudal fin; Bernie Goiney and Jay
Clark for technical assistance; and Arthur Ken-
dall for helpful discussions.

April G. Maclean, formerly OSU, assembled a
large portion of the M. proximus series and made
some of the counts and measurements. Joanne
L. Laroche (OSU) helped gather additional
specimens from OSU collections.

Gary Walters, FRI, has a continuing interest in

MATARESE ET AL.: LARVAL DEVELOPMENT OF PACIFIC TOMCOD

gadid larvae and juveniles and provided us with
unpublished data and gave other assistance.

A number of workers graciously provided us
with samples of larval and juvenile gadids without
which we could not have completed this work. We
therefore thank: Douglas Rabin, Gary Walters,
William Karp, and Bruce Miller, FRI; T. Saunders
English, Department of Oceanography, University
of Washington; Jay Quast and Bruce Wing,
NWAFC Auke Bay Laboratory, NMFS, NOAA;
James Blackburn, Alaska Department of Fish and
Game (ADF&G), Kodiak; Lou Barton, ADF&G,
Anchorage; and Rollin Daggett, Ecology Consul-
tants, Inc., Fort Collins, Colo.

Norman Wilimovsky, University of British Co-
lumbia, Vancouver, loaned us radiographs of adult
pollock. Elbert Ahlstrom, Southwest Fisheries
Center La Jolla Laboratory, NMFS, NOAA, pro-
vided stimulating discussions on gadid osteology
and on the interpretation of caudal fin develop-
ment.

A draft of this manuscript benefited from re-
views by Michael Fahay, Northeast Fisheries
Center Sandy Hook Laboratory, NMFS, NOAA,
and Arthur Kendall.

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Wash.)

fishery bulletin: vol. 78, no. 4
waldron, k. d.

1972. Fish larvae collected from the northeastern Pacific
Ocean and Puget Sound during April and May 1967.
U.S. Dep. Commer., NOAA Tech. Rep. NMFS SSRF-663,
16 p.

WlLIMOVSKY,N. J.

1964. Inshore fish fauna of the Aleutian Archipelago.
Proc. Alaska Sci. Conf 14:172-190.

YUSA. T

1954. On the normal development of the fish, Theragra
chalcogramma (Pallas*, Alaska pollock. | In Jpn.. Engl,
summ.l Bull. Hokkaido Reg. Fish. Res. Lab. 10:1-15.

940

NOTES

PREDATION BY SHARKS ON PINNIPEDS AT
THE FARALLON ISLANDS'

What we know about mortality in pinnipeds has
largely been derived indirectly. For example,
pinnipeds or parts thereof have occasionally been
found in shark stomachs. Sharks have thus be-
come known as pinniped predators (e.g., Gogan^ ),
but, since few direct observations of shark/pinni-
ped interactions exist, we do not know the extent
of such predation. The present paper summarizes
observations of shark/pinniped encounters at the
Farallon Islands between 1970 and 1979. We
relate the frequency of observed encounters to
annual and seasonal changes in pinniped popula-
tion, and the marine climate, and assess the effect
of shark-bite injury on the reproductive perfor-
mance of seals.

Methods

The South Farallon Islands, San Francisco
County Calif, (lat. 37.4° N, long. 123.0° W), lie at
the inward edge of the California Current, 30 km

west of the California coast. Southeast Farallon,
West End, and accompanying rocks compose the
South Farallones and in all are about 44 ha
(Figure 1). Over 250,000 seabirds of 12 species
breed there (Ainley and Lewis 1974). Pinnipeds
reach a peak of 2,500 animals — three species
breed and occur there year-round: harbor seal,
Phoca vitulina, northern elephant seal, Mirounga
angustirostris , and northern sea lion, Eumetopias
jubatus; a fourth, California sea lion, Zalophus
californianus , the most numerous of Farallon
pinnipeds, occurs most abundantly in spring,
but few breed there; and a fifth, northern fur
seal, Callorhinus ur sinus, occasionally hauls out
(Pierotti et al. 1977; Ainley et al.^).

Since 1968, the Point Reyes Bird Observatory
has maintained a year-round research station on
Southeast Farallon. On a rotating but continual
schedule at least two biologists, plus several
volunteer workers, have operated the station.
Every day, weather permitting, a census of birds
and a general visual survey of inshore waters was
made. Beginning in 1970 elephant seals were

'Contribution 169 of the Point Reyes Bird Observatory.

^Gogan, P. J. P. 1977. A review of the population ecology
of the northern elephant seal, Mirounga angustirostris. Un-
pub. manuscr, 68 p. Natl. Mar. Mammal Lab., NMFS, NOAA,
7600 Sandpoint Way, NE., Seattle, WA 98115.

^Ainley, D. G., H. R. Huber, R. P Henderson, T. J. Lewis, and
S. H. Morrell. 1976. Studies of marine mammals at the
Farallon Islands, California, 1975-76. Final report, Marine
Mammal Commission (Contract No. MM5AC027), Wash., D.C.,
available Natl. Tech. Inf. Serv., Springfield, VA 22151 as
PB 2-266249, 32 p.

HAUL-OUT AREAS
SEA LIONS

El ELEPHANT
SEALS

SHARK
ATTACKS A
SIGHTINGS •

EAST •••

LANDING AAA
AA

SEA PIGEON

GULCH A A

• ••AA
AAAA

HEAD

FIGURE 1.— South Farallon Islands, central
California, and location of observed shark/
pinniped encounters and major haul-out areas
of sea lions and elephant seals.

FISHERY BULLETIN: VOL. 78. NO. 4, 1981.

941

censused weekly during most of the year and daily
during the breeding season. Regular weekly cen-
suses of other pinnipeds have been conducted
since 1972, and as far back as 1970 irregular
counts were made. Since we found shark activity
to be seasonal (see below), we included comments
on the seasonal changes in sea-surface tempera-
ture and salinity. Such information was derived
from daily readings made at noon (P.s.t.).

Results

We recorded events involving sharks 58 times
between 9 September 1970 and 9 February 1979.
Of these, 37 were definite observations of sharks
eating pinnipeds (i.e., "shark attacks") and the
remainder (21) were mostly of sharks seen within
1 km of the island. In definite shark attacks, we
were first (36 of 37 times) alerted to the incident
by a flock of gulls (mostly the western gull, Larus
occidentalis), hovering above a large bloody area
(5 m^) in the water. Usually we saw the shark's
head and dorsal and caudal fins which offered
clues to species identification and estimation of
size and number. We often saw the pinniped prey
as well. On five occasions only an area of bloody
water and the hovering gulls were observed.
These, too, were likely shark attacks on pinnipeds,
but we did not include them in the 37 known
attacks. Observations, from discovery of the gull
fiock to dissipation of blood and gulls, lasted from
3 to 15 min. If the carcass was not consumed in
that time, then its disappearance was probably
due to sinking. In the areas of most shark/
pinniped interactions the water was 4-12 m deep.

In 20 interactions we saw the pinniped prey
sufficiently well for a positive identification. Two
involved sea lions, one or perhaps two involved
harbor seals, and the remainder involved elephant
seals. Based on size, we could tell that seven
elephant seals were young individuals, about 3 yr
old or less, and an eighth was an adult female. On
rare occasions, we have observed sea lions with
obvious, fresh shark-bite wounds. However, the
location of most shark attacks in the vicinity of the
elephant seal hauling out areas (Figure 1) further
supports what other data indicate, that at South-
east Farallon, sharks more frequently ate ele-
phant seals than other pinnipeds.

In 30 instances, the white shark, Carcharodon
carcharias, was identified as the species seen
preying on seals. All were at least 3 m long and
most about 3.5-5 m long. In 16 of 21 nonattack

observations within 1 km of the island, the shark
was also identified: 14 involved white sharks and
two involved the blue shark, Prionace glauca.
How many sharks were present at any one time is
not known. On at least three occasions two sharks,
and once three sharks, simultaneously fed on one
pinniped. On 8 January 1976, a 3 m long white
shark was caught in Fisherman's Bay and 7 d later
two larger white sharks were seen on the opposite
side of the islands.

Sharks were more abundant or more active
during the late fall and winter over the 9 yr
(Figure 2). The number of attacks in December
and January was perhaps artifically low (see
below) because on many days during those months
few if any gulls were present to alert observers.
The possibility that attacks were missed was
particularly likely in December 1976 and January
1977. Sharks were known to be present then
because several seals hauled out with fresh shark-
bite wounds and part of another was seen floating
in the water. Yet no attacks were seen. The timing
of greatest shark activity corresponded closely
with the Davidson Current period (October-
February) which, as described by Bolin and Abbott
(1963), is characterized by slowly declining sea-
surface temperatures and salinities and the ap-
pearance of a northward flowing countercurrent
(shoreward of the south-flowing California Cur-
rent). White sharks were thus present (or at least
active, see below) when waters were warm but not
necessarily the warmest (Figure 2). Blue sharks,
on the other hand, were definitely most abundant
during the warm oceanic period (July -September),
when the California Current slackens, allowing
warm saline oceanic waters to flow shoreward.
They were observed commonly but only at 3 km or
more away from the island. Few were involved in
the observations reported here.

The timing of most shark attacks also cor-
responded closely with the late autumn peak in
elephant seal numbers (Figure 2). Each year the
elephant seals reached maximum numbers twice,
during midspring and again during late fall (Le
Boeuf et al. 1974). A third, smaller peak occurred
during the winter breeding season. Only two
shark attacks, both involving elephant seals, were
observed during the upwelling period (March-
July), when the California Current flows most
strongly and temperatures reach their lowest.
One of these attacks occurred during the spring
peak in elephant seal numbers. During the
fall, when most shark attacks were observed.

942

the populations of other pinniped species at the
Farallones were usually near their annual low
(Ainley et al. footnote 3), which indicates even
further that elephant seals were the usual prey
of sharks. Rather exceptional were the high num-
bers of California sea lions present in the fall 1978
(Huber et al."*). Sharks and shark incidents were
seen often then but we could identify few of the
pinniped prey. One incident definitely involved
a sea lion but most others occurred in areas
frequented by elephant seals and not by sea lions.
Several elephant seals arrived at the Farallones
for the breeding season bearing shark-bite
wounds, some fresh and some healed. The his-
tories of these animals are noteworthy, particu-
larly since their being severely wounded may
have affected their reproductive performance.
Twenty-four breeding attempts by females identi-
fiable as individuals were available for analysis.
In 10 attempts, females arrived with fresh wounds.
In only one (10% ) did she successfully rear a pup by
herself, three lost their pups, three received help
from other cows (i.e., they shared suckling), and
three apparently did not pup. In 1977 three newly
wounded cows disappeared (not even present dur-
ing spring molt) after leaving the island with
healed wounds. In 14 pupping attempts by known
females with no wounds (but wounded in a later
year) or with old, healed wounds, all but two

"Huber, H. R., D. G. Ainley, S. H. Morrell, R. R. LeValley and
C. S. Strong. 1978. Studies of marine mammals at the
Farallon Islands, California, 1977-78. Final report, Marine
Mammal Commission (Contract No. MM7AC025), Wash., D.C.,
available Natl. Tech. Inf. Serv., Springfield, VA 22151 as
PB 80-111602, 50 p.

0

/
1

\
\

-J

^ SEAL _p-/

A

<

LJ

^ NUMBERS '

\
\

CO

H

< /

0^ 141 1

I TEMPERATURE

■200<

Ui

a

2

1

/
I

1

\ V
* /

\ /

/—

X
UJ

iii

<

/
/

/

\

-1
U

q:
iij

LU

> 12-

I

Z

o

2 ■
z

<

1

s

^^ —

/
/
/
/

/ \
/ \

SHARK
ATTACKS^

CD

S
•lOoi

_l

X

Z
O

UJ

3 10 0

1 0 1

2

3 II 12

3

z
<

J F M A

M J J
MONTHS

— 1

A

SON

D

UJ

S

Figure 2. — Annual cycles in monthly mean sea-surface tem-
perature, elephant seal numbers and number of shark/pinniped
interactions in the Farallon Islands, central California, vicinity,
1970-78. Seal numbers are from Ainley et al. (text footnote 3) and
Huber et al. (text footnote 4).

(86%) successfully raised a pup without help. The
difference is significantly different from the 10
attempts mentioned above {t = 3.3, P< 0.001).
Since many of the freshly wounded females were
probably pupping for their first time, it could have
been lack of experience that resulted in their poor
record rather than being wounded. Two females,
however, without wounds raised their first pups
successfully but the next season, each with a fresh
wound, they either allowed another cow to help in
suckling or failed to pup successfully. In addition,
of 11 females pupping for their first time in 1977
and not having shark-bite wounds, 7 (64%) were
successful, and only 1 allowed its pup to be nursed
by another female. Thus females with fresh,
severe shark-bite wounds were less successful in
pupping than others. Perhaps the energy and
tissue-building resources needed to heal a severe
wound were taken from those required in the
rearing of a pup. None of the 6 females with fresh
shark wounds in the 1977 breeding season was
observed to copulate; among other females 99
(77%) were observed in copulation.

Two male elephant seals have also hauled out at
the Farallones, bearing shark-bite wounds. One
first visited in December 1972 as a subadult bull
(probably about 5 yr old) and had an old shark-bite
wound. He returned each season through the 1976
breeding season. Another was first seen in 1972 as
a young adult (Le Boeuf et al. 1974) and was the
alpha bull in the breeding hierarchy during 1972,
1973, and 1974. In 1975 he arrived for the fourth
year, was initially the alpha bull, but was de-
throned before the end of the breeding season. In
1976 he appeared on the island with two fresh
shark wounds. Thereafter he visited the breeding
colony intermittently, but was not part of the
hierarchy of breeding bulls.

Discussion

It is obvious that the frequency of shark attacks
on pinnipeds and other shark observations have
been increasing at the South Farallon Islands
(Table 1). We are convinced this is not an artifact
of increasing observer awareness for a number of
reasons, because a flock of 50-1- gulls hovering for
10-15 min above a large, blood-red patch of water
within 50 m of shore is not easy to miss, particu-
larly from such a small island; and daily censuses
have been conducted consistently since 1970.

Since the seasonal occurrence of some sharks
is related to water temperatures (e.g., O'Gower

943

Table l. — Annual data on elephant seal numbers, shark attacks, water temperatures, and frequency of attacks relative

to seal numbers at the Farallon Islands, central California.

Winter (late December-February)

Summer (late March-early July)

Fall (late August-

mid -December)

A

B

C

Mean

A

B

C

Mean

A

B

C

Mean

Max no.

No.

Ratio

sea

Max no.

No.

Ratio

sea

Max no.

No

Ratio

sea

Year

seals

attacks

A:B

temp

seals

attacks

A:B

temp

seals

attacks

A:B

temp

1970

0

0

0

11.3

60

0

0

10.0

35

'l

0

15.5

1971

0

0

0

11.5

50

0

0

'8.8

120

0

0

16.8

1972

3

0

0

11.5

120

0

0

10,0

155

1

01

17.0

1973

10

0

0

12.1

176

0

0

108

170

2

01

14.5

1974

20

0

0

11.0

290

1

.003

88

300

2

01

15.0

1975

30

'0

0

10.9

305

0

0

10.0

330

6

02

13.5

1976

55

0

0

10.5

460

0

0

9.3

450

4

01

160

1977

110

^0

0

12.7

523

0

0

10,0

507

7

01

136

1978

182

4

.02

13.6

717

1

.001

12,4

609

7

01

120

1979

250

^1

.004

11.6

776

0

0

11,2

' Ttiought to be an attack on a sea lion,

'Cows arrived witti fresh shark-bite wounds; in 1979 the remains of a cow, likely a shark victim, was seen floating in the water.

and Nash 1978), it was worthwhile to consider
the relationship between temperature and sharks
at the Farallones. As shown in Table 1, water
temperature during the fall when most shark
attacks and sightings occurred, compared among
the years, fluctuated up and down but did not
relate clearly to yearly fluctuation in shark attack
frequency. The same was true for temperatures
during the winter elephant seal breeding season.
The year 1978 provides an instructive example
of this. In the spring-summer, temperatures were
unusually high. In spite of record numbers of
elephant seals only one shark attack was ob-
served, and that occurred in July, long after the
seal population peak (only 24 were present; 452
sea lions, though, were present). Later in the fall,
temperatures were lower than during spring but
much shark activity was evident (Table 1). The
only major relationship that was evident be-
tween shark attacks and water temperature was
that all but one observed attack occurred when
temperature generally exceeded 12° C (as sum-
marized in Figure 2). Unfortunately, there is no
published information of the seasonality of white
sharks to explain this. Off Durban, South Africa,
where water temperatures are higher than at the
Farallones, Bass (1978) found small white sharks
more abundant when temperatures dropped to the
annual low (equivalent to highest Farallon tem-
peratures), but the number of white sharks the
size of those at the Farallones did not change.

The factor that best relates to the general
increase in white sharks is an increase in elephant
seal numbers. The fall, winter, and spring popula-
tions of elephant seals have been increasingly
rapidly at the Farallones over the past several
years (see Le Boeuf et al. 1974; Ainley et al.
footnote 3; Table 1). The seal population during

the fall, the period of most shark attacks, has
increased about 3.9 fold since 1972, the first year
of the period when shark attacks have been seen
consistently year after year. In the fall data there
is a direct relationship between the number of
shark attacks and the number of seals (r = 0.895;
P<0.01). The ratio of attacks to the number of
seals, except during spring and the 1979 seal
breeding season, has remained at about 0.01-0.02.
Shark attacks during the elephant seal breed-
ing season (winter) have been observed less often
than during the fall but they may be increasing
during that period, too, if the 1977-79 seasons are
any indication. Interestingly, attacks were first
seen during winter in the year when the elephant
seal population surpassed 120 animals (1978), the
same population level that occurred in conjunc-
tion with the first fall sighting of elephant seal/
shark interactions (1972). This further indicates
a density-dependent relationship between shark
predation and elephant seal populations.

Acknowledgments

The Farallon Island field station of the Point
Reyes Bird Observatory was supported financially
by members and donors and by contracts from
various agencies. In addition to our members,
we wish especially to thank the Lucius M.
Beebe Foundation, Charles E. Merrill Trust,
McNaughton Foundation, Dean Witter Founda-
tion, San Francisco Foundation, Packard Founda-
tion, Standard Oil of California, and the U.S. Fish
and Wildlife Service. Marine mammal observa-
tions from 1975 to 1979 were under contract from
the Marine Mammal Commission. We also wish to
thank the U.S. Coast Guard and particularly the
Oceanic Society for logistic support. William I.

944

FoUett kindly reviewed some photographs that we
took of sharks, thus confirming our identifica-
tions, and checked an earlier version of this paper.

Literature Cited

AINLEY, D. G., AND T. J. LEWIS.

1974. The history of Farallon Island marine bird popula-
tions, 1854-1972. Condor 76:432-446.

Bass, a. J.

1978. Problems in studies of sharks in the southwest
Indian Ocean. In E. S. Hodgson and R. F. Mathewson
(editors), Sensory biology of sharks, skates, and rays,
p. 545-549. Off. Nav. Res., Arlington.
BOLIN, R. L., AND D. P ABBOTT.

1963. Studies on the marine climate and phytoplankton
of the central coastal area of California, 1954-1960.
Calif. Coop. Oceanic Fish. Invest. Rep. 9:23-45.
LE BOEUF, B. J., D. G. AINLEY, AND T. J. LEWIS.

1974. Elephant seals on the Farallones: population struc-
ture of an incipient breeding colony. J. Mammal. 55:
370-385.
O'GowER, A. K., AND A. R. Nash.

1978. Dispersion of the Port Jackson shark in Australian

waters. InE.S. Hodgson and R. F. Mathewson ( editors).

Sensory biology of sharks, skates, and rays, p. 529-544.

Off. Nav. Res., Arlington.

PIEROTTI, R. J., D. G. AINLEY, T. J. LEWIS, AND M. C. COULTER.

1977. Birth of a California sea lion on southeast Farallon
Island. Calif Fish Game 63:64-66.

David G. Ainley

Craig S. Strong

Harriet R. Huber

T. James Lewis

Stephen H. Morrell

Point Reyes Bird Observatory
Stinson Beach, CA 94970

IN SITU OBSERVATIONS ON

REPRODUCTIVE BEHAVIOR OF

THE LONG-FINNED SQUID, LOLIGO PEALEI

There are several published accounts of reproduc-
tive behavior, including copulation and egg laying,
of the long-finned squid, Loligo pealei Lesueur, in
the laboratory (Drew 1911; Arnold 1962); but with
the exception of Stevenson's (1934) field observa-
tions of L. pealei s behavior around an egg mass, no
in situ observations of egg-laying behavior have
been documented for this species. Field and
laboratory observations of reproductive behavior
have been made for the California market squid,
L. opalescens (McGowan 1954; Fields 1965; Hobson
1965; Hurley 1977), the tropical arrow squid, L.

plei (Waller and Wicklund 1968), L. bleekeri
(Hamabe and Shimizu 1957), L. vulgaris (Tardent
1962), the broad squid, Sepioteuthis bilineata
(Larcombe and Russell 1971, and S. sepioidea (Ar-
nold 1965). However, each species' in situ egg-
laying behavior differed from the behavior we ob-
served in L. pealei.

Observations

Each summer L. pealei and its egg masses are
common in shallow coves along the coast of Rhode
Island, such as our study site at Fort Wetherill on
Conanicut Island in Narragansett Bay. Scuba di-
vers, including ourselves, have observed squid to
be numerous in these areas, particularly at night
when they occur singly or in small, loosely formed
schools.

On 16 June 1979, at 1230 h on an incoming tide
(temperature 14.5°- 15.0° C, depth 6 m) using scuba
we observed a large squid egg mass (50-60 cm
across) attached to one side of a small boulder. The
surrounding area was a sandy/mud bottom with
unattached fragments of the seaweeds Ulva lac-
tuca , Laminaria sp. , and Porphyra sp. Because the
egg mass was larger than the 12-15 cm masses we
regularly see in this area while diving, we spent
some time observing it. Squid began to appear at
the limit of the water visibility (about 4.0 m) and
moved toward the egg mass in a semicircle. They
stopped about 2.5-3,0 m from the mass and re-
mained stationary approximately 1-m off the bot-
tom. The squid were in well-defined pairs with the
smaller females (mantle length 16-18 cm) parallel
to and on the left of each male (20-22 cm) as we
faced them (Figure 1). Eight pairs were visible at
that time. The animals had moderate pigmenta-
tion over the mantles, but we did not observe the
distinctive spots of color at the base of the arms as
were reported by Arnold (1962), nor did we observe
color changes during the observation period. Con-
trary to McGowan's (1954) observations on L.
opalescens , all of the animals appeared to be in
good condition; no torn epithelium was obvious
and no dead or dying individuals had been seen in
the area of the egg mass or anywhere else in the
cove during the hour-long dive.

One pair of squid at a time approached the egg
mass with their arms held forward and tentacles
extended. Because of our position directly facing
the squid, it was impossible to observe the begin-
nings of an egg finger protruding from the funnel
as Drew (1911) and Tardent (1962) had observed in

FISHERY BULLETIN: VOL. 78. NO. 4, 1981.

945

■1.5 M

Figure l. — Pairs of squid formed a semicircle and one pair at a time approached the egg mass. The female and male intertwined arms
as they extended them into the egg mass. We surmise that the female was depositing an egg capsule and that the male was exhibiting
parental care or "grooming" behavior Water depth was 6 m.

L.pealei andL. vulgaris held in aquaria. However,
comparing the behavior of the animals with that
described in literature on squids' reproductive be-
havior, we concluded that the females were de-
positing egg capsules. They intertwined arms as
they extended them into the egg mass. The arms of
the male appeared to move delicately over and
among the existing fingers of eggs (Figure 1). Each
pair that approached the egg mass stayed 2-4 s
then moved backward into the same position it had
previously occupied in the semicircle. At that time
another pair moved forward. There did not appear
to be any order in which pairs approached the egg
mass; however, no more than one pair approached
at any given time. The same pair approached more
than once.

Although most accounts indicate that copula-
tion occurs just before egg deposition, our observa-
tions cannot substantiate this because egg laying
had already commenced. No agonistic behavior
which is often associated with reproduction was
evident during the 10-min observation period.

Discussion

The social hierarchy involving egg deposition
differs from species to species. Observations of L.

946

opalescens and L. plei in the field indicate that
once copulation occurs, individual pairs break
apart and the female approaches the egg mass and
deposits a capsule alone, although Hurley (1977)
did observe an L. opalescens male pushing a
female toward an egg mass. Sepioteuthis sepioidea
remains paired after copulation, but only the
female approaches the egg mass during egg laying
(Arnold 1965). Larcombe and Russell (1971) re-
ported that S. bilineata also remains paired, but
the male escorts the female to the egg mass. How-
ever, the male assumes a protective role and fol-
lows about 0.5 m behind and above the female so
he is between her and the other squid during the 2
s period in which she deposits a capsule. In con-
trast, L. pealei pairs formed and maintained a
semicircle throughout egg laying (Figure 1). One
pair at a time approached the egg mass; the male
did not appear to assume a protective role, but
might have been involved in "grooming" such as
Tardent ( 1962) described for L. vulgaris held in an
aquarium. Parental care or guarding egg masses
has been documented for L. pealei by Stevenson
(1934), who noted that both solitary males and
pairs patrolled and guarded an egg mass. Similar
guarding behavior has also been reported for L.
opalescens (Hurley 1977).

Although there are similarities in reproductive
behavior among several squid species, our obser-
vations of L. pealei indicate a social structure
which is well defined and different from that de-
scribed for other species with the possible excep-
tion of S. bilineata and S. sepioidea. Since there are
relatively few published accounts of in situ
copulation and egg-laying activities, it is difficult
to know what is normal and what might be altered
behavior patterns due to the presence of human
observers, submersibles, lights, etc. However, our
observations and those of other divers, including
two in the same area a week earlier who reported
12-15 pairs of squids in a semicircle (TurcoM, indi-
cate that the social structure associated with egg-
laying behavior is not an isolated phenomenon,
but a pattern which is recurrent in populations of
L. pealei which frequent New England coastal
waters in the summer.

Acknowledgments

The authors extend their gratitude to Roger
Hanlon for his review of the manuscript. We also
thank William K. Macy III for his help during the
development of the manuscript. We are grateful to
Lianne Armstrong, who prepared the illustration,
and to Jennie Dunnington for typing the manu-
script.

Literature Cited

ARNOLD, J. M.

1962. Mating behavior and social structure in Loligo

pealii. Biol. Bull. (Woods Hole) 123:53-57.
1965. Observations on the mating behavior of the squid

Sepioteuthis sepioidea . Bull. Mar Sci. 15:216-222.

Drew, G. A.

1911. Sexual activities of the squid Loligo pealii (Les.). I.
Copulation, egg-laying and fertilization. J. Morphol.
22:327-359.

Fields, W. G.

1965. The structure, development, food relations, repro-
duction, and life history of the squid Loligo opalescens
Berry Calif. Dep. Fish Game, Fish Bull. 131, 108 p.
Hamabe, m., and T. SHIMIZU.

1957. The copulation behavior of Yariika, Loligo bleekeri
K. Rep. Jpn. Sea Reg. Fish. Res. Lab. 3:131-136.
HOBSON. E. S.

1965. Spawning in the Pacific Coast squid, Loligo opales-
cens. Underwater Nat. 3( 3 ):20-21.

Hurley, a. C.

1977. Mating behavior of the squid Loligo opalescens.
Mar. Behav Phvsiol. 4:195-203.

Larcombe. M. r., and B. C. Russell.

1971. Egg laying behaviour of the broad squid,
Sepioteuthis bilineata. N.Z. J. Mar. Freshwater Res. 5:3-
11.
MCGOWAN, J. A.

1954. Observations on the sexual behavior and spawning
of the squid. Loligo opalescens , at La Jolla, California.
Calif Fi.sh Game 40:47-54.

Stevenson, J. A.

1934. On the behaviour of the long-finned squid (Loligo

pealii [Lesueur]). Can. Field-Nat. 48:4-7.
TARDENT, P

1962. Keeping Loligo vulgaris L. in the Naples

Aquarium. I^'^ Congres International d'Aquariologie,

Monaco— 1960. Vol. A, p. 41-46.
WALLER, R. A., AND R. I. WICKLUND.

1968. Observations from a research submersible — mating

and spawning of the squid, Doryteuthis plei . BioScience

18:110-111.

Carolyn a. Griswold
jerome p^ezioso

Northeast Fisheries Center Narragansett Laboratory
National Marine Fisheries Service, NOAA
R.R.7A, South Ferry Road
Narragansett, RI 02882

SPAWNING AND SEXUAL MATURITY OF
GULF MENHADEN, BREVOORTIA PATRONUS^

Earlier studies of egg and larva collections
(Turner 1969; Fore 1970; Christmas and Wal-
ler^) have shown that Gulf menhaden, Brevoortia
patronus, which range throughout the northern
Gulf of Mexico from Cape Sable, Fla., to Veracruz,
Mexico, spawn from about October to March from
near shore to about 97 km offshore at depths of
from 2 to 111 m. There have been two previous
studies to determine the age of spawning, the
number of ova produced, and the peak time of
ovary maturation ( Suttkus and Sundararaj 1961;
Combs 1969). Our objectives in the present study
were to: 1) estimate the minimum number of
maturing ova for specific age-groups and size
groups, 2) estimate the percentage of fish that
spawTi at each age, 3 ) determine the time of spawn-
ing, and 4) determine the frequency of spawning.
Gulf menhaden make annual inshore-offshore
movements. The larvae spend 3-5 wk in offshore
waters before moving into estuaries where they

'Anthony Turco, West Main St., North KingstowTi, R.I., pers.
commun. June 1979.

'Southeast Fisheries Center Contribution No. 81-12B.

^Christmas, J. Y, and R. S.Waller. 1975. Location and time
of menhaden spawning in the Gulf of Mexico. Unpubl. man-
user, 20 p. Gulf Coast Res. Lab., Ocean Springs, Miss. (NMFS
contract no. 03-4-042-24).

FISHERY BULLETIN: VOL. 78. NO. 4. 1981.

947

transform into the adult form (Reintjes 1970). The
following autumn the juveniles, ranging in fork
length from about 55 to 130 mm FL, migrate from
the estuaries to offshore waters (Tagatz and Wil-
kens 1973), along with all other age-groups that
are moving from inshore waters of the gulf at this
time. Fish of all age-groups migrate to inshore
waters again the following spring.

While in inshore waters, age 1 and older Gulf
menhaden are subject to an intensive purse seine
fishery that extends from Florida to eastern Texas
from about mid- April to early October. The fish are
processed into meal, oil, and solubles at plants in
Mississippi and Louisiana.

During the purse seine season Gulf menhaden
are sexually inactive. Therefore, gonads collected
at that time are of no use for fecundity studies. The
only source of Gulf menhaden during the spawn-
ing season is the offshore groundfish trawl fishery,
which takes Gulf menhaden incidentally along
with the primary species. Catches are landed at
plants in Mississippi and Louisiana and processed
as canned pet food (Roithmayr 1965). The number
of Gulf menhaden taken varies, but is never large.
From October 1976 to February 1977, 241 females
(124-257 mm FL) and 516 males (113-240 mm FL)
were collected from the groundfish landings. After
January, we were able to collect only 4 maturing
females in February and none in March or April.

To assure that Atlantic menhaden, B. tyrannus,
were assigned to the correct year class, June and
Reintjes (1959) developed specific criteria for as-
signing fish to year classes on the basis of annulus
formation. These criteria also were adopted when
the investigation of Gulf menhaden was begun in
1964. March 1 was designated as an arbitrary date
on which all fish of a given year class were ad-
vanced 1 yr in age, regardless of whether or not a
new annulus had formed. Since all fish used in this
study were collected from October to February,
an age-1 fish is one that has one annulus, but
has completed two growing seasons; an age-2 fish
has two annuli but has completed three growing
seasons.

All fish were caught in the northern Gulf of
Mexico from lat. 28°35 ' to 30°15 ' N and from long.
87°45 ' to 9r28 'W. Fork lengths were measured to
the nearest millimeter and wet weights to the
nearest 0.1 g. Scale samples for aging were taken
from the left side of the body along the midline and
below the origin of the dorsal fin. Paired gonads
were preserved in a 10% buffered Formalin^ solu-
tion.

Stages of Sexual Maturity

Preserved gonads were blotted to remove excess
moisture and weighed to the nearest 0.01 g. A
sample of 0.1 g or less was cut from the central
portion of an ovary and examined microscopically
to describe morphology of developing ova and to
determine the mean diameter of the largest ova
present.

Four groups of ova were found in the most ad-
vanced ovaries, while only one to three groups
were found in less developed ovaries. Immature
ova were under 0.20 mm in diameter, translucent,
and contained an irregular spherical nucleus. In-
termediate ova ranged from 0.20 to 0.35 mm and
had a dark or opaque center surrounded by a wide
sphere of dull yellowish to brownish speckling.
Maturing ova were 0.36 to 0.72 mm, opaque, and
had an outer translucent covering or tissue. Ripe
ova were similar to maturing ova except they were
>0.72 mm.

Three stages of sexual maturity were recognized
on the basis of the most advanced group of ova
present: immature, intermediate, and maturing.
Fish classified as maturing contained either
maturing or both maturing and ripe ova. All
maturing or ripe ova in a sample were counted and
about 100 were selected randomly and measured
for diameter.

Age and Size of First Spawning

Gulf menhaden <135 mm can be considered as
age-0 fish (Nicholson and Schaaf 1978). All fish
<100 mm FL that we examined showed no evi-
dence of maturing ova. Through December, 63% of
age-1 fish and 71% of all fish age 2 or older in our
samples contained maturing ova. By January all
fish age 1 or older contained maturing ova (Table

^Reference to trade name does not imply endorsement by the
National Marine Fisheries Service, NOAA.

Table l. — Number of female Gulf menhaden sampled from Oc-
tober 1976 to February 1977 by age, month, and stage of sexual
maturity (immature or mature).

Age 1

Age 2

Age 3

Age 4

Montti

Imma- Ma-
ture' ture

Imma- Ma-
ture ture

Imma- Ma-
ture ture

Ma-
ture

Oct

Nov.

Dec.

Jan.

Feb.

5 6

4 15

4 1

19

3

3 10

3

4 3
3
1

1 3
2

1

' Flsti with Intermediate ova (as ttie largest ova present) were included in ttiis
category.

948

Table 2. — Number of female Gulf menhaden sampled from
October 1976 to February 1977 by fork length, month, and stage
of sexual maturity (immature or mature).

Oct

Nov,

Dec.

Fork
length
(mm)

Imma- Ma-
ture' ture

Imma- Ma-
ture ture

Imma- Ma-
ture ture

Jan.

Ma-
ture

Feb.

Ma-
ture

120-129
130-139
140-149
150-159
160-169
170-179
180-189
190-199
200-209
210-219
220-229
230-239
240-249
250-259

1

15

17

20

14

3

3

1

1

3
8

15

15

12

11

1

1

4

1

1
6
10
2
2
3
1
2
5
1
1

' Fish with intermed late ova (as the largest ova present) were included in this
category.

1). For both aged and unaged fish >140 mm that we
examined, 73% contained maturing ova in Oc-
tober, 91% in November, 55% in December, and
100% in January and February (Table 2). From
this information we concluded that Gulf menha-
den spawn for the first time at age 1, after they
have completed two seasons of growth, and then
continue to spawn each year thereafter.

<
z
o
o

>-
O
O
m

<

UJ

.11
.10
.09
.08
.07

"

.061-
.05
.04
.03
.02
.01
0

Age 1 FEMALES

, Age 2

Age 3

, Aged and Unaged Fish
Combined

j-

-L

\ X

_L

OCT NOV DEC JAN FEB

1976 1977

Figure l. — Relation between mean of gonad weight/body
weight and month for unaged and different age-groups of female
Gulf menhaden.

Time and Frequency of Spawning

Previous studies of egg and larva collections
(Turner 1969; Fore 1970; Christmas and Waller
footnote 2) and of increases in gonad weights
(Suttkus and Sundararaj 1961; Combs 1969) have
indicated that spawning begins in October and
ends about March. Our data also show that spawn-
ing occurs within this time period. For each month
we plotted the mean gonad weight as a percentage
of body weight for those fish we were able to age
(Figure 1). For females the means, which were
already high in October, indicating that gonadal
development had begun, increased in November
and December and then decreased in January and
February. Generally, males followed the same pat-
tern as females when both aged and unaged were
combined (Figure 2). We can not explain why the
relative gonad weights of age-1 females were
higher than those of older fish, unless some of the
older fish had partially spawned by the time they
were collected, thereby decreasing their gonad
weight.

The number of times an individual fish will
spawn during a season may be inferred from the
difference in size between groups of ova. If there is

a

<
z
o

CD

>
O

O

CQ

Z
<
UJ

.11

.10
.09
.08
.07
.06
.05
.04
.03
.02
.011-
0

Age 1

Age 2 MALES

Age 3

. Aged and Unaged Fish

Combined

j-

OCT NOV
1976

DEC

J_

_L

JAN FEB
1977

FIGURE 2. — Relation between mean of gonad weight/body
weight and month for unaged and different age-groups of male
Gulf menhaden.

949

a large difference in size between immature ova,
developing intermediate ova, and maturing ova,
the spawning period will be short and definite. If
there is only a gradual change in size between
these groups of ova, individual fish may spawn
several times over an extended period (Hickling
and Rutenberg 1936; de Vlaming 1974).

Since there was a gradual change in size be-
tween groups of ova, and since the number and
diameter of maturing or ripe ova for fish of the
same length varied considerably, we inferred that
Gulf menhaden were intermittent, or fractional
spawn ers. The number of maturing ova did not
change markedly from month to month, or even
within the same month. The ripe ova, after being
spawned, probably are replaced by a group of the
largest maturing ova which in turn are replaced
by a group of intermediate ova. Perhaps four or
five different groups of ova ripen and are spawned
during a single spawning season, although the
exact number cannot be estimated.

Higham and Nicholson (1964) stated that, from
available evidence, it is impossible to decide con-
clusively the frequency of spawning of individual
Atlantic menhaden but they favored the
hypothesis of maturation and fractional spawning
of more than one group of ova during the season.

Combs (1969) concluded that B. patronus
spawns several times from October to February.
He found that over a period of months spawnable
oocytes occurred together with advanced stages
of ova that were potentially spawnable. He de-
scribed the histological events in the development
of Gulf menhaden ova from formation to maturity
and found that once the provisional yolk had
formed, ova lost all potential to remain in the
ovary and had to complete their development prior
to spawning or be aborted.

Number of Ova Spawned

Since analysis of variance tests showed no sig-
nificant difference in the size or number of matur-
ing ova in gram samples from the left and right
ovaries, we used either ovary for measurements
and counts. (Counts were made of the number of
maturing ova in a sample of 0.1 g or less from an
ovary. ) The number of maturing or ripe ova in each
female was estimated by dividing the combined
weight of the left and right ovaries by the sample
weight and multiplying this number by the
number of maturing or ripe ova in the sample.

If fractional spawning occurs, the number of ova

estimated to have been spawned by fish of any
given age or size would necessarily be minimal,
since some ova probably would have been spawned
by the time some ovaries were collected. Fractional
spawning also would increase the variability in
the number of ova estimated for fish of the same
age or size (Bagenal and Braum 1971). Of the 70
maturing females that we could age, 44 were age 1,
20 were age 2, 5 were age 3, and 1 was age 4. The
mean number of ova and its standard error for
each age-group respectively were 37,100 ±3,467;
47,900±5,038; 61,800±9,486, and 151,000.

Three relationships that are most useftil in ex-
plaining and understanding population dynamics
of a species are those of fecundity with age, length,
and weight. To determine what mathematical
models would be most appropriate in describing
these relations, we used Statistical Analysis Sys-
tem"* to test various statistical regression models.
We chose those which had the greater r^ values
and the minimum deviations from the regression
line. In the following models F - fecundity, A -
age, L = fork length, and W = body weight. For
fecundity on age (Figure 3):

■•Statistical Analysis System; Barr, Goodnight, Sail and Hel-
wig, SAS Institute Inc., PO. Box 10066, Raleigh, NC 27506.

c
o

<
>
O

Z

1601-

150-

140-

130-

120-

110-

100-

90-

80-

70-

60-

50-

40-

30-

20-

10-

0 —

F = 21402(1.44156)*^^

AGE

Figure 3. — Relation between number of maturing ova and i
for Gulf menhaden.

950

log.F = 9.9713 + 0.3657(A)

(r2 -0.1804,5^.;, = 0.5466).

For fecundity on fork length (Figure 4):

log^F = -9.8719 + 3.8775(log,L)

(r2 = 0.6490, s,^ = 0.3751).

For fecundity on weight:

F = 12,064.2908 + 374.8848(W)

(r2 = 0.4445, Sy., = 20,427.0752).

■D
C
0

>

o

2
z

140

160 180 200 220 240

FORK LENGTH (mm)

260

Figure 4. — Relation between mean number of maturing ova
and fork length for Gulf menhaden.

Literature Cited

Bagenal, T. B., and E. Braum.
1971. Eggs and early life history. In W. E. Ricker (editor),
Methods for assessment offish production in fresh waters,
2d ed.. p. 166-198. IBP (Int. Biol. Programme) Handb. 3.

Combs, R. M.

1969. Embryogenesis, histology and organology of the
ovary ofBrevoortiapcUronus. Gulf Res. Rep. 2:333-434.

DE VLAMING, V L.

1974. Environmental and endocrine control of teleost re-
production. In C. B. Schreck (editor). Control of sex in
fishes, p. 13-83. Va. Polytech. Inst. State Univ., VPI-SG-
74-01.

FORE,P L.

1970. Oceanic distribution of eggs and larvae of the Gulf
menhaden. In Report of the Bureau of Commercial
Fisheries Biological Laboratory, Beaufort, N.C., for the

fiscal year ending June 30, 1968, p. 11-13, U.S. Fish Wild!.

Serv. Circ. 341.
Hickling, C. F, and E. RUTENBERG.

1936. The ovary as an indicator of the spawning period in

fishes. J. Mar Biol. Assoc. U.K. 21:311-317,
HIGHAM, J. R., AND W R, NICHOLSON.

1964. Sexual maturation and spawning of Atlantic
menhaden. U.S. Fish Wildl. Serv., Fish. Bull. 63:255-
271,

JUNE, F, C„ AND J, W, REINTJES,

1959. Age and size composition of the menhaden catch
along the Atlantic coast of the United States, 1952-1955;
with a brief review of the commercial fishery. U.S. Fish
Wildl. Serv, Spec, Sci, Rep, Fish, 317, 65 p,
NICHOLSON, W R„ AND W E. SCHAAF,

1978. Aging of Gulf menhaden Brevoortia pat-
ronus. Fish, Bull,, U,S, 76:315-322.
REINTJES, J, W

1970, The Gulf menhaden and our changing estuaries.
Proc. Gulf Caribb, Fish, Inst, 22:87-90.
ROITHMAYR, C, M,

1965, Industrial bottomfish fishery of the northern Gulf of
Mexico, 1959-63, U,S, Fish Wildl, Serv, Spec. Sci, Rep,
Fish, 518, 23 p,

SUTTKUS, R, D,, AND B, I, SUNDARARAJ,

1961, Fecundity and reproduction in the largescale
menhaden, Brevoortia patronus Goode. Tulane Stud.
Zool. 8:177-182,
TAGATZ, M. E., AND E, P H, WILKENS.

1973. Seasonal occurrence of young Gulf menhaden and
other fishes in a northwestern Florida estuary. U.S. Dep.
Commer., NCAA Tech, Rep. NMFS SSRF-672, 14 p,
TURNER, W R,

1969, Life history of menhadens in the eastern Gulf of
Mexico, Trans, Am. Fish. Soc, 98:216-224,

ROBERT M, LEWIS

Southeast Fisheries Center Beaufort Labortory
National Marine Fisheries Serivce, NOAA
P.O. Box 570
Beaufort, NC 28516

CHARLES M. ROITHMAYR

Southeast Fisheries Center Pascagoula Laboratory
National Marine Fisheries Service, NOAA
PO. Drawer 1207
Pascagoula, MS 39567

FOOD OF THE PACIFIC WHITE-SIDED

DOLPHIN, LAGENORHYNCHUS OBLIQUIDENS,

DALLS PORPOISE, PHOCOENOIDES DALLI,

AND NORTHERN FUR SEAL,

CALLORHINUS URSINUS,

OFF CALIFORNIA AND WASHINGTON

Our knowledge of the feeding habits of the Pacific
white-sided dolphin, Lagenorhynchus ob-
liquidens, and the Ball's porpoise, Phocoenoides

FISHERY BULLETIN: VOL. 78. NO, 4. 1981,

951

dalli, is based on examination of the stomach con-
tents of stranded animals, animals accidentally
taken in commercial fishing gear, those taken in
the western Pacific commercial fishery, and ani-
mals that died during capture attempts. Of these
only a few were normally feeding animals taken at
sea, whose stomach contents were thoroughly
examined. Fishes and squids previously identified
from stomachs of dolphins and porpoises by vari-
ous investigators are listed in Table 1.

This paper documents the stomach contents of
44 Pacific white-sided dolphin and 9 Dall's por-
poise collected at sea off California and Washing-

ton. All animals were collected by the authors
during pelagic fur seal studies with the exception
of three dolphins which were collected by a staff
biologist during whale research voyages off
California. Comparisons of stomach contents are
made between the Pacific white-sided dolphin,
Ball's porpoise, and northern fur seal, Callorhinus
ursinus, collected near the same locations and
usually on the same day. Mention of the dolphin,
porpoise, and seal in this paper refers to the
above-named species only unless noted otherwise.
The Pacific white-sided dolphin ranges the east-
ern North Pacific Ocean, from Baja California

Table l. — List of fishes and squids previously identified in stomachs of Pacific white-sided dolphin and Ball's porpoise from the North

Pacific Ocean by localities.

Reference source

Locality and species

Pacific white-sided dolphin

Dall's porpoise

California:
Pacific herring, Clupea harengus pallasi
Pacific sardine, Sardinops sagax
Northern anchovy, Engraulis mordax

Night smelt, Spirinchus starksi
California smoothtongue, Bathylagus stilbius
Pinpoint lampfish, Lampanyctus regalis
Blue lanternfish, Tarletonbeania crenularis
Pacific whiting, Merluccius productus

Cusk-eel, Otophidium taylori

Eeelpouts, Zoarcidae

Grenadier, Macrouridae

Pacific saury, Cololabis saira

Jack mackerel, Trachurus symmetricus

Pacific pompano, Peprilus simillimus

Rockfish, Sebastes spp., juvenile

Sablefish, Anoplopoma fimbria, juvenile

Snailfish, Liparis sp.

Pacific sanddab, Citharichthys sordidus

Eels, Anguilliformes

Squid, Loligo opalescens

Squid, Abraliopsis sp.

Squid, Gonatus sp.

Squid, Onychoteuthis borealijaponicus

Octopus, Octopus bimaculatus
British Columbia:

Pacific herring, Clupea harengus pallasi
Gulf of Alaska:

Capelin, Mallotus villosus
Japan:

Anchovy Engraulis japonica

Sudidae, Paralepis sp.

Lanternfish , Myctophidae — Scopelidae

Lanternfish, Notoscopetus sp.

Lanternfish, Diaphus sp.

Lanternfish, Tarletonbeania taylori

Lanternfish, Lampanyctus sp.

Lanternfish. Myctophum sp.

Cod, Laemonema longipes

Hake, Laemonema morsum

Mackerel, Scomber japonicus

Squid, Watasenia scintillans

Squid, Omnastrephes sloani paclficus
Northwestern Pacific and western Bering Sea:

Sockeye salmon, Oncorhynchus nerka

Unidentified small fish

Unidentified fish

Squids

Shrimp

Higgins 1919

Brown and Norris 1956; Norris and Prescott 1961:
Fiscus and Niggol 1965: Fitch and Brownell 1968

Best 1963; Fiscus and Niggol 1965; Fitch and
Brownell 1968

Houck 1961

Scheffer 1953; Norris and Prescott 1961 ; Houck
1961

Brown and Norris 1956; Ridgway 1966
Fiscus and Niggol 1965

Hotta etal. 1969
Wilkeetal. 1953

Wilkeetal. 1953
Wilkeetal. 1953
Hotta etal 1969

Best 1963; Loeb

Loeb 1972

Loeb 1972

Loeb 1 972
Loeb 1 972
Loeb 1972
Loeb 1972
Norhs and Prescott 1 961 ;

1972
Loeb 1972
Loeb 1972
Loeb 1972

Norris and Prescott 1961

Loeb 1972

Loeb 1972

Loeb 1972

Loeb 1 972

Loeb 1972

Loeb 1 972

Norris and Prescott 1961 ; Loeb 1972

Loeb 1972

Loeb 1972

Loeb 1972

Loeb 1972

Cowan 1 944

Scheffer 1 953

Wilke
Wilke
Wiike
Wilke
Wilke
Wilke
Wilke
Wilke
Wilke

and Nicholson
etal. 1953
and Nicholson
and Nicholson
and Nicholson
and Nicholson
and Nicholson
and Nicholson
etal. 1953

1958

1958
1958
1958
1958
1958
1958

Wilke and Nicholson 1958

l\/lizue et al. 1966

Koga 1 969

Mizue and Yoshida 1965; Mizue et al. 1966

(Vlizue and Yoshida 1965; l^izue etal. 1966;

Koga 1 969
IVIizue and Yoshida 1965; Mizue etal. 1966;

Koga 1 969

952

northward in the summer to the Gulf of Alaska; it
ranges the western North Pacific Ocean, from
Japan northward to the Kurile Islands (National
Marine Fisheries Service 1978). During pelagic
fur seal research voyages off California (1958-66)
and Washington (1958-72), 767 pods of dolphin
totalling 8,803 animals were sighted^ (297 pods,
5,555 dolphin, and 490 pods, 3,248 dolphin, respec-
tively). Dolphin pod size ranged from 1 to 1,000 +
animals. The dolphin reported here were collected
from pods ranging from 4 to 300 animals.

The Dall's porpoise ranges the North Pacific
Ocean from northern Baja California and Japan in
the south to the Bering and Okhotsk Seas, moving
into the southern portion of its range during
winter. The porpoise usually occur in smaller
groups than do the dolphin. During pelagic fur
seal research cruises off California and Washing-
ton, 868 pods totalling 3,575 porpoise were sighted
(657 pods, 2,845 porpoise, and 211 pods, 730 por-
poises, respectively). Porpoise pods generally con-
tained fewer than 20 animals. The porpoise re-
ported here came from pods of three to five ani-
mals. Sightings and collections of dolphin and
porpoise were obtained during 388 d at sea off
California in 1958-66 and 368 d at sea off Wash-
ington in 1958-72.

The northern fur seal ranges across the subarc-
tic waters of the North Pacific Ocean and numbers
about 1.8 million animals (Lander and Kajimura
1976). Most seal are found near their breeding
islands in the Bering and Okhotsk Seas from July
into early November except for the very small San
Miguel Island, Calif., population that numbers
about 2,000 animals. In the eastern North Pacific
Ocean few adult males are found south of the Gulf
of Alaska. Mature females and immature males
and females begin to appear in coastal waters be-
tween British Columbia and central California in
late November and early December, the pups
slightly later in January or February. The move-
ment is generally southward along the continen-
tal shelf and slope in January into March with
some animals ranging south to about lat. 32° N;
however, most of the wintering population can be
found between about lat. 35° and 49° N. Some
northward migration out of this region may begin
as early as March. Most wintering seal are found

from over the continental shelf seaward as much
as several hundred miles (Fiscus 1978).

Northern fur seal are most frequently observed
alone rather than in company with other seal of
their species; however, concentrations do occur in
areas of abundant food supply. In 1966 (January-
March) off California when most of the dolphin
and porpoise were collected, 1,441 groups of seal
were observed, of which 31% were single animals;
22% were in groups of 2; 16.9% in groups of 3;
10.5% in groups of 4; and 10.2% in groups of 5-20
(Marine Mammal Biological Laboratory 1969).

In 1967-68 (November-February) off Washing-
ton, when most of the dolphin and porpoise were
collected, 669 groups of seal contained 40.8%
single animals; 24.9%, groups of 2; 13.6%, groups
of 3; 9.3%, groups of 4; and 14%, groups of 5-9
(Marine Mammal Biological Laboratory 1970).

There are no reliable estimates of the numbers
of Pacific white-sided dolphin and Dall's porpoise
that inhabit the eastern Pacific offshore waters
from California to Washington; however, these two
species are the most frequently sighted cetaceans
in these waters.The northern fur seal is the only
pinniped regularly inhabiting this region. It is a
seasonal visitor, from December through May; as
many as 500,000 may be here during the peak of
the wintering period (Fiscus 1979).

Methods

Hand harpoons or shotguns were used to collect
the Pacific white-sided dolphin and Dall's porpoise
as they rode the bow wave of the research vessel or
dory. Northern fur seal were collected from the
vessel or dory with shotguns. The dolphin and
porpoise were taken off California, 1-130 km sea-
ward of the continental shelf; those from Washing-
ton waters were taken near or over the continental
shelf.

Standard measurements and weights of each
cetacean and seal were recorded (American Soci-
ety of Mammalogists, Committee on Marine
Mammals 1961, 1967). Reproductive tracts, skulls,
stomachs, and tissue samples were collected.
Stomachs were tied with string at the esophagus
and pyloris and then injected with and preserved
in 10% Formalin^ for laboratory examination. The
contents of each stomach were gently washed and
drained in a small mesh sieve. The stomach rugae

'NMFS, Natl. Mar. Mammal Lab. 1958-74. Birds and
mammals observed at sea. Unpubl. data listing, various pagi-
nation. Natl. Mar. Mammal Lab., Natl. Mar. Fish. Serv., NOAA,
7600 Sand Point Way NE., Seattle, WA 98115.

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

953

were carefully checked for squid beaks, fish
otoliths, and other small remains of food items.
After excess fluid was drained off, the total weight
of stomach contents was recorded and a total vol-
ume determined by water displacement. Indi-
vidual food items were identified, counted, and the
percentage of the total volume represented by
each type of food item estimated. Fragments of
prey species may remain in the stomachs of these
animals from 12 to 24 h after feeding; hence hard
parts of prey species consumed over the shelf, such
as chitinous beaks of squids, fish otoliths, and par-
ticularly dense fish bones, may still persist in the
stomachs of animals taken well offshore of the
shelf. Identification was made by comparison with
reference specimens and to descriptions in
taxonomic keys or other references.

Of the 33 dolphin taken off California, 25 were
females (9 adult, 15 subadult, 1 probably adult)
and 8 were males (3 adult, 5 subadult). Of 11 dol-
phin taken off Washington, 8 were females (2
adult, 6 subadult) and 3 were males (1 adult, 2
subadult). All nine of the Ball's porpoise were
adults.

Scientific names of marine mammals follows
Marine Mammal Commission^; of fish, Bailey et
al. (1970) and Fitch and Lavenberg (1971); of
cephalopods. Young (1972).

Results

Pacific White-Sided Dolphin and Northern Fur Seal

Northern anchovy, Engraulis mordax, was the
most frequently occurring fish in the stomachs of
white-sided dolphin and northern fur seal taken in
all collection months and across the latitudinal
range of the collections off California. Most dol-
phin were taken off central California between Pt.
Conception and Pt. Reyes in the following num-
bers by month: 1 in January, 11 in February, 18 in
March, 2 in June, and 1 in December. Seal used in
comparisons were taken in the same localities at
the same times. Northern anchovy remains were
identified from 58% (19 occurrences) of the dolphin
stomachs and 32% (13 occurrences) of seal
stomachs collected in the same localities.

Pacific whiting, Merluccius productus, was
found in 33% (10 occurrences) of the dolphin

''Marine Mammal Commission. 1976. Marine mammal
names. Unpubl. manuscr., 8 p. Marine Mammal Commission,
1625 Eye Street, NW, Wash., DC 20006.

stomachs and 34% (14 occurrences) of the seal
stomachs. Pacific whiting was particularly impor-
tant in the March 1966 collections at lat. 35° to 38°
N (Morro Bay to San Francisco). Pacific saury,
Cololabis saira, the third ranking fish, was found
in 28% (9 occurrences) of the dolphin but in only
7% (3 occurrences) of the seal from the same area.

Squids of the family Gonatidae were the most
frequently occurring cephalopods. Both Loligo
opalescens (64% occurrence) and Onychoteuthis
borealijaponicus (45% occurrence) were found
in the dolphin stomachs in trace amounts only
(beaks); however, both species are important seal
prey. Abraliopsis sp. was identified only once in
seal but found in 16 dolphin stomachs from seven
collection locations off California. Stomachs of the
nine dolphin collected 25 February 1966 off Pt.
Reyes contained a greater variety of fishes and
squids than those collected in other locations.

The food items consumed by 11 dolphin and 14
seal collected in the same locality off Washington
show salmonids, Oncorhynchus spp., composed
most of the stomach contents of 10 dolphin and 12
seal taken 25 and 26 February 1968 over the As-
toria Canyon, approximately 37-44 km west of the
Columbia River (8 occurrences in dolphin, 3 in
seal). Flatfishes (Pleuronectidae) were present in
one seal stomach. Squid beaks representing nine
families, genera, or species of squids were iden-
tified from the stomachs of dolphin, but these taxa
were of minimal importance in the stomachs of
seal collected from the same area, occurring in
only 4 of 12 stomachs. One dolphin, taken off the
continental shelf, 25 April 1972, contained trace
amounts of unidentified fishes and squids repre-
senting at least five genera. The stomachs of two
seal collected in the same area the same day were
empty.

Dall's Porpoise and Northern Fur Seal

The stomach contents of 9 Ball's porpoise and 17
northern fur seal taken from the same location off
California and Washington from 1964 to 1968 were
examined. One porpoise was taken in January off
southern California and four were taken in Feb-
ruary and one in April off central California.
Three were taken off Washington, two in January
(one taken in the entrance to the Strait of Juan de
Fuca) and one in February. Off California, north-
ern anchovy. Pacific whiting. Pacific saury, and
squids, L. opalescens and O. borealijaponicus,
formed major portions of the most recent feedings.

954

Unidentified fishes and six species of squids were
also found in trace amounts. The stomachs of three
porpoise taken 56 km southwest of Pt. Reyes on 21
February 1966 contained no northern anchovy but
did contain typical open ocean dwelling fishes and
squids. Off Washington trace amounts of
eulachon, Thaleichthys pacificus., rockfish,
Sebastes spp.; sablefish, Anoplopoma fimbria;
flatfish, Pleuronectidae; American shad, Alosa
sapidissima; capelin, Mallotus villosus; and
squids, L. opalescens , Gonatidae, Gonatus sp., and
0. borealijaponicus , were found in stomachs of
three porpoise.

Discussion

Distribution of Prev

Based on identified prey species, it appears that
all three of the mammals feed in the epipelagic
(0-200 m) and mesopelagic (200-1,000 m) zones of
the ocean and that over the continental shelf, they
may descend to the bottom (200 m or less) on occa-
sion as demonstrated by the presence of demersal
species in their stomachs. Many of the fishes and
squids rise to or toward the surface at night,
thereby becoming more readily available and
perhaps ruling out the necessity for long, deep
dives. Kooyman et al. (1976), reporting on fiar seal
diving behavior, indicated that dives between the
surface and 20 m lasting <1 min may be for shal-
low feeding or travel and that dives between 20
and 140 m of 3.3-3.4 min duration may be hunting
and feeding dives. They reported dives deeper than
140 m; the deepest reported dive lasted 5.4 min and
reached 190 m. A study of blood oxygen levels of
three genera of porpoise by Ridgway and Johnston
(1966) reported that the Pacific white-sided dol-
phin cannot swim as fast and probably cannot dive
as deep as the Ball's porpoise.

Prey Species

Off the California coast all three of the mam-
mals feed primarily on small schooling fishes and
cephalopods, including the northern anchovy,
Pacific saury, and Pacific whiting. Other species of
fish were probably taken as the opportunity arose.
The primary fish species in dolphin collected off
the Washington coast were salmonids (genus On-
corhynchus). Because the latter collection was
made in a small area over a 3-d period, the taking
of salmonids may have been opportunistic and

short term rather than typical of more routine
feeding. This sample is too small to conclude that a
major predator-prey relationship exists between
the Pacific white-sided dolphin and the salmonids.

Cephalopods are probably more important as
prey species than indicated by the relative volume
of stomach contents in the collection. Except for
the chitinous beaks, cephalopods are probably
more rapidly digested than fish. Marine mammals
are more likely to feed on squids during the night
because the vertical migration of many species
brings them closer to the surface waters (Roper
and Young 1975; Pearcy et al. 1977). Collection of
dolphin during the day would give adequate time
for digestion of fleshy parts, thus leaving the large
numbers of indigestible chitinous beaks often
found in stomachs.

The fishes and squids identified in the stomachs
of the dolphin, porpoise, and seal taken during this
study are presented in Table 2.

Stomach Capacity of Predators

The 44 Pacific white-sided dolphin were all
adult or subadult animals, presumably with
stomachs of maximum size. Eleven stomachs con-
tained only trace amounts of food, and 33 con-
tained food contents varying from 10 to 3,490 cm^
(10-3,745 g).

The dolphin whose stomach contained the most
food from California waters had eaten 68 anchovy
(1,770 cm^ or 1,895 g). Anchovy grow to 18-20 cm
and may weight 57 g (Fitch and Lavenberg 1971).

Off Washington, the largest dolphin stomach
examined contained the remains of nine salmon
(including identifiable remains of four coho salm-
on and two pink salmon) which measured 26.0,
27.0, 31.0, 31.5, 31.5, 33.0, 33.0, 33.0, and 33.5 cm.
The full stomach measured 40 cm long and 24 cm
at the widest point (outside stomach dimensions),
and the stomach contents represented 4.4% (3,490
cm^ or 3,745 g) of the total body weight of the
animal.

The largest stomach content from a Ball's por-
poise off California contained 58 northern anchovy
(1,000 cm3 or 1,090 g). Off Washington, the largest
stomach content contained fragments of five cape-
lin, four eulachon, one flatfish (family Pleuronec-
tidae), and trace amounts of squids (Gonatus sp.
and Gonatidae) (130 cm^ or 125 g). Five stomachs
contained food volumes varying from 5 to 1,000
cm^ (5-1,090 g) whereas four stomachs contained
only trace amounts of food. Except for occasional

955

Table 2.— Size offish and frequency of occurrence of fishes and cephalopods found in the stomachs of Pacific white-sided dolphin , Dall's
porpoise, and northern fur seal' collected off California and Washington, 1964-72.

California

Washington

MpQcijr^hlo

length

Northern

Northern

of fish

White-sided

Dall's

fur seal

White-sided

Dall's

fur seat

in stomachs^

dolphin

porpoise

(M1''10

dolphin

porpoise

(314-7

Taxon

(cm)

(33 coll)

(6 coll.)

coll.)

(11 coll.)

(13colL)

coll.)

Fish:

Pacific lamprey. Enlosphenus tridentatus^

—

—

—

—

1

—

—

American shad. Alosa sapidissima

—

—

—

—

—

—

1

Pacific herring, Clupea harengus pallasi

28,5-31.3(11)

—

—

—

—

—

—

Northern anchovy, Engraulis mordax

14.5-17.8(19)

19

2

313''5

—

—

—

Salmon. Oncorhynchus spp.^

—

—

—

—

8

—

2

Pink salmon. 0. gorbuscha^

25.0-40.5 (3)

—

—

—

—

—

2

Chum salmon. 0. keta^

—

—

—

—

1

—

1

Coho salmon, 0 kisutch^

21.0-33.0 (5)

—

—

—

2

—

2

Chinook salmon, O. tshawytscha^

21.0-24.5 (2)

—

—

—

—

—

—

Capelin, Mallolus villosus

10.9-15.5(26)

—

—

—

—

1

—

Eulachon, Thaleichthys pacificus^

15.3-20.5 (4)

—

—

—

—

1

1

California lanternfish. Symbolophorus californiensis^

—

1

—

—

—

—

—

Pacific saury. Cololabis saira^

—

9

1

3

—

—

—

Pacific whiting. Merluccius productus

—

10

2

^u-'i

—

—

—

King-of-the-salmon, Trachipterus altivelis^

—

1

—

—

—

—

T-

Jack mackerel, Trachurus symmetricus

—

1

—

—

—

—

Drum, Sciaenidae

—

—

—

1

—

—

Medusafish. Icichthys lockingtonfi

—

1

—

—

—

—

Rockfish, Sebastes spp,^

—

1

—

1

—

—

2

Sablefish. Anoplopoma fimbria

25.0 (1)

—

—

—

—

—

1

Pacific sanddab, Citharichthys sordidus^

—

1

—

—

—

—

—

Righteye flounder, Pleuronectidae^

—

—

—

—

—

1

1

Cephalopods:

Squid. Loligo opalescens

21

1

32" 1

3

1

3142

3

Squid. Abraliopsis sp.^

Squid. Octopoleuthis sp.^'^

Squid. Gonatidae

Squid. Gonatus sp.

Squid. Gonatopsis borealis^

Squid, Onychoteuthis borealijaponicus^

Squid, Chiroteuthis sp.^

Squid, Cranchiidae^

Pelagic octopus, Ocythoe tuberculata^

'A complete list of prey species of the northern fur seal appears in North Pacific Fur Seal Commission Reports on Investigations, 1962, 1969, 1971, 1975.

^Length measurement of Chinook salmon and sablefish is standard length, other measurements are total length. The numbers in parentheses indicate sample size.

^Northern fur seal in association with Pacific white-sided dolphin.

"Northern fur seal in association with Dall's porpoise.

^Identified for the first time as prey of the Pacific white- sided dolphin.

'Identified for the first time as prey of the Dal! s porpoise

16

3

1

12

1

—

14

2

3142

23

7
15

1

2

2

4 1

2

3

1

—

2

—

—

11

9

11

11

2

11

3
3

squid beaks, bone fragments, and otoliths, which
were found in the fundic (or pyloric) stomach and
the duodenal ampulla, all undigested or
semidigested food items were found in the fore-
stomach. Stomach volumes were highly variable
depending on the time of day the animal was col-
lected and the digestibility of the species offish or
squid ingested. Of 30 dolphin taken off California,
those taken before 1000 h averaged more than
twice the volume of food in their stomachs than
those taken after 1000 h.

During the course of pelagic fur seal research,
thousands of seal stomachs have been examined
by the authors. The stomach containing the most
food was from a 17-yr-old male collected in the
eastern Bering Sea at 1330 h, 9 August 1968. The
animal had consumed 13 walleye pollock,
Theragra chalcogramma, and 4 squid, Ber-
ryteuthis magister. The contents weighed 9.8 kg
(9,175 cm^ volume representing 7.2% of body

weight) with walleye pollock composing 80%
(7,340 cm^) of the total stomach volume. The
stomach of an adult female fur seal contained food
weighing 5.9 kg (5,565 cm^ volume representing
13.1% of body weight). This 15-yr-old animal was
collected at 0645 h on 19 April 1964 off California
and had fed on 31 Pacific whiting.

The energy requirements of the northern fur
seal are poorly knowoi. Keyes (1968) reported that
seal and other pinnipeds kept in captivity sub-
sisted well on 6-12% of body weight daily, with
vitamin supplements. Studies indicate possibly
higher daily consumption rates among growing
immature animals. Sergeant (1969) summarized
the feeding rates per day of several captive ceta-
ceans including two dolphin which consumed 7.9%
of their body weight in herring and mackerel and a
porpoise that consumed 11.3% of its body weight of
mackerel. Ridgway (1972) reported food require-
ments in captive animals equalled 7-8% of body

956

weight/d for dolphin and 10-127r for porpoise. The
species fed to these captive animals were not iden-
tified.

Size of Prey

Higgins (1919) mentioned a stomach containing
six large Pacific sardine, Sardinops sagax, each
about 30 cm long. Houck (1961) reported a dolphin
with a stomach full of Pacific saury and with a 33
cm jack mackerel, Trachurus symmetricus,
wedged in its throat. Unfortunately, no count of
the Pacific saury was given. Fitch and Brownell
(1968) reported that otoliths representing 29
Pacific whiting 40-50 cm long and 14 Pacific whit-
ing about 20 cm long were recovered from a dol-
phin stomach. The sizes offish in stomach contents
were measured only from whole or nearly whole
specimens or those with complete vertebral col-
umns (Table 2). All salmon consumed by dolphin
were generally immature, showing 0-age ocean
growth, although a few showed 1, 2, and 3 ocean
annuli.

Scheffer (1953) reported on stomach contents of
two Ball's porpoise taken off Oregon, each of which
contained four Pacific whiting about 45 cm long.
These records represent the largest fish recovered
from porpoise stomachs. Mizue et al. (1966) re-
ported only one occurrence of sockeye salmon, O.
nerka, from stomachs of 148 porpoise taken in con-
junction with the high-seas salmon gill net fishery.
No mention was made of the size of this fish, al-
though they did state that adult salmon are prob-
ably not taken by animals of this species.

In our collections, there was no evidence of large
fish being broken up prior to ingestion by either
dolphin or porpoise. Captive bottlenose dolphin,
Tursiops truncatus, have been observed to break
up food species."* The teeth, jaw structure, and
relative neck mobility of the white-sided dolphin
are similar to those of the bottlenose dolphin and
would allow such behavior in this species more so
than in the Ball's porpoise. The maximum size of
prey eaten is apparently limited by the predator's
ability to capture and swallow whole fish.

The size of prey listed in Table 2 does not neces-
sarily indicate that these fish are the largest con-
sumed by the seal. Seal generally swallow smaller
fish and squid whole below the surface whereas
larger fish are brought to the surface and broken

••William Gilmartin, Naval Ocean Systems, San Diego, Calif.,
pers. commun. 1978.

into smaller pieces by grasping them with their
teeth and shaking them violently from side to side.
The largest fish we have seen taken by a seal was a
king-of-the-salmon (length 170 cm) which we took
away from the animal as it attempted to break the
fish into smaller pieces at the surface.

Conclusions

The Pacific white-sided dolphin and the Ball's
porpoise feed primarily on small schooling fishes
and cephalopods. They, like the northern fur seal,
are opportunistic feeders, preying on available
species, including some that are commercially im-
portant such as salmon, anchovy, jack mackerel,
and Loligo opalescens. Meaningful estimates of
the dolphin and porpoise populations are unavail-
able, and too few stomachs have been examined to
make any estimate of the percentage of commer-
cially important fishes included in the diet.

Regardless of the time of day collected, stomachs
may contain undigested fish indicative of recent
feeding. Based on stomach content volume and
time of collection, large stomach volumes were
most often observed in animals collected before
1000 h in the morning, indicating that most feed-
ing is done at night or in the morning.

Northern fur seal tend to congregate in areas of
abundant food supply and usually feed at night,
probably because most prey species rise toward
the surface after dark and are more readily avail-
able (Fiscus et al. 1964). Food species consumed by
the seal vary by area, but the important food in the
diet of this mammal in a given area, based on
percentage of stomach content volume, generally
does not change — only ranking by volume
changes. The animals collected on the continental
shelf appear to feed on fishes, whereas those taken
beyond the shelf feed primarily on squids.

Acknowledgments

The authors wish to thank John Fitch, Califor-
nia Bepartment of Fish and Game, for identifica-
tion of fish otoliths from the stomachs of two dol-
phins; Eric Hochberg, Curator of Invertebrate
Zoology, Santa Barbara Museum of Natural His-
tory, for identification of the pelagic octopus,
Ocythoe tuberculata, beaks; and Bale Rice, North-
west and Alaska Fisheries Center, NMFS, NOAA,
for his review of the manuscript.

957

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1953. Measurements and stomach contents of eleven del-
phinids from the northeast Pacific. Murrelet 34:27-30.

Sergeant, B. E.

1969. Feeding rates of cetacea. Fiskeridir Skr. Ser.
Havunders. 15:246-258.
WiLKE, F, AND A. J. NICHOLSON.

1958. Food of porpoises in waters off Japan. J. Mammal.
39:441-443.
WILKE, F, T. TANIWAKI, AND N. KURODA.

1953. Phocoenoides and Lagenorhynchus in Japan, with
notes on hunting. J. Mammal. 34:488-497.
YOUNG, R. E.

1972. The systematics and areal distribution of pelagic
cephalopods from the seas off Southern California.
Smithson. Contrib. Zool. 97, 159 p.

958

RICHARD K. STROUD

Northwest and Alaska Fisheries Center
National Marine Fisheries Service. NOAA
7600 Sand Point Way NE., Seattle, WA 98115
Present address: Department of Veterinary Medicine
Oregon State University
Corvallis, OR 97331

Clifford H. Fiscus

HIROSHI KAJIMURA

Northwest and Alaska Fisheries Center
National Marine Fisheries Service, NOAA
7600 Sand Point Way NE., Seattle. WA 98115

SPAWN AND LARVAE OF THE PACIFIC
SANDFISH, TRICHODON TRICHODON

Little is known about the biology of the Pacific
sandfish, Trichodon trie ho don, other than that the
adults are characteristic of inshore, sand-gravel
communities (Isakson et al. 1971); they occur from
San Francisco, Calif., to Kamchatka, USSR (Hart
1973); and they burrow into a sandy substrate
(Clemens and Wilby 1961). Clemens and Wilby
reported that a mature female taken on Long
Beach, Vancouver Island, Canada, extruded ma-
ture eggs (upon disturbance) in February.

The first discovery of natural spawn of T. tricho-
don and subsequent rearing of larvae through
metamorphosis at the Vancouver Public
Aquarium has provided information about the re-
production and early life history of this species. In
addition to life history notes, this paper presents a
description of larvae of T. trichodon.

Methods

A portion of an egg mass was collected at lat.
48°56 ' N, long. 125°43 ' W, 16 km southeast of Long
Beach, Vancouver Island, on 12 June 1976 and
transported in a plastic bag with oxygen and sea-
water to the Vancouver Aquarium, where it was
incubated in an aerated aquarium with seawater
(25-29'L, 8°-13° C) provided at an inflow rate ex-
ceeding 100 tank volumes/d. The seawater tem-
perature changed seasonally with changes in av-
erage ambient seawater surface temperatures, so
that the salinity/temperature regime was com-
parable with that which the eggs would have en-
countered intertidally. The eggs were fixed in a
bag of nylon mesh in front of the inlet pipe. In
October, December, and January, embryos were

excised from a few of the eggs to determine
whether development was continuing. About once
per month egg membranes were scrubbed with a
bottle brush to remove diatom growth.

As they hatched the larvae were collected with a
beaker and transferred to a 1,000 1 rearing tank
(ca. 1 m depth x 1 m in diameter) with seawater
(25-271,, 10°-12° C) inflow at a rate exceeding one
tank volume per day and a light cycle of 14 h light
and 10 h dark, including simulated twilight
periods. Larvae were provided brine shrimp, Ar-
temia salina, nauplii daily in excess quantities.
Debris was siphoned from the tank bottom daily
and examined for dead fish larvae. Juveniles were
placed in a tank with a sand bottom and flow-
through seawater and were fed frozen euphausiids
and frozen brine shrimp.

At various ages specimens were preserved in 3%
Formalin^ in seawater, with borax and lonol.
Freshly killed specimens were measured to the
nearest 0.5 mm standard length (SL), then mea-
sured again 1 yr after preservation, to determine
shrinkage. Line drawings, morphometric data,
and meristic characters were based on preserved
specimens.

Life History Notes

The egg mass was found in a surge channel on a
rocky shoreline between 0.6 and 1.0 m tide levels.
The mass was visually estimated to have about
1,000 eggs, was irregularly shaped, and adhered
firmly to the rock surface.

Adults of this species are known to inhabit
sandy beaches, whereas the egg mass is suited
only to rocky substrate to which it can adhere.
Presuming an incubation period of about 1 yr as
discussed below, most plant substrates would be
too ephemeral for an egg deposition site and bed-
rock on sand beaches could be covered by seasonal
shifting of sand. Rocky shoreline removed from
sandy areas would therefore provide the most sta-
ble substrate for the adhesive eggs. The precise
location on the wall of a fully exposed surge chan-
nel might provide a refuge from egg predation as
well as high flow velocities for gas exchange. The
rocky intertidal area in which this egg mass oc-
curred is located 8 km from the nearest sandy
intertidal area. Thus, a limited spawning
movement along the shore must occur.

^Reference to trade names does not imply endorsement by the
Vancouver Aquarium or by the National Marine Fisheries Ser-
vice, NOAA.

FISHERY BULLETIN: VOL. 78. NO. 4, 1981.

959

The T. trichodon eggs were amber colored and
large in size (3.52 mm in diameter ±0.10 SE, n =
17 eggs), and slightly flattened at points of at-
tachment. About 25% of the collected eggs were
dead at the time they were taken. When collected
the embryos had developed both melanic choroid
pigment and guanine iris pigment on the eyes.

Considering the state of development of these
embryos, it was expected that these eggs would
mature and hatch within a month after collection,
since benthic egg masses of many northeast
Pacific fishes mature to hatching within 1 to 3 mo
after fertilization (pers. obs. on 28 species). The T.
trichodon eggs, however, continued to develop for
over 8 mo after they were collected, then all
hatched within a 24-h period.

As a basis for comparison, wolf-eel, Anar-
rhichthys ocellatus, eggs are large (ca. 5 mm in
diameter) and have a relatively long incubation of
3 mo at 10°-12° C (pers. obs. on captive spawn). At 1
mo after fertilization (one-third of incubation
period), A. ocellatus embryos reach a devel-
opmental state comparable with that of the T.
trichodon at the time of the collection, with pig-
mented eyes on an embryo still many times small-
er than the yolk sac. Assuming comparability in
relative rates of development, a full incubation
period of 12 mo could therefore be calculated for
the T. trichodon. An incubation period of 1 yr
would indicate February as the time of spawning,
which coincides with the finding of a ripe female in
February in the same area of Vancouver Island
(Clemens and Wilby 1961).

About 90% of the hatch occurred within 4 h, in
late afternoon, the remainder the next morning.
The T. trichodon eggs had not been handled for 2
wk prior to hatching and no other fish eggs had
hatched in the incubation tank for a week prior to
this hatch, so it appears unlikely that this abrupt
hatch was unnaturally stimulated. Only a few egg
mortalities occurred during the incubation period
in the laboratory; this low egg mortality, together
with the occurrence of an abrupt and fully viable
hatch, indicates that the observed incubation
period was normal for this species, as an abnormal
incubation should adversely affect viability. Al-
though incubation periods of about 1 yr have been
reported for an unrelated fish species, Agonus
cataphractus (see Breder and Rosen 1966 for re-
view), such prolonged incubation is evidently rare.

The larvae were reared in the laboratory from
hatching through metamorphosis with no mor-
talities (maximum age 29 mo, 137 mm SL). Larvae

hatched on 15 and 16 February 1977 at 14.5 mm SL
(16 mm TL) and grew to 40-43 mm SL (45-50 mm
TL) in 70 d, by which time the fish resembled small
adults. Allometric growth in the deeping and
lateral compression of the ventral body continued
to about 50 mm SL, along with upturning of the
jaw and development of fringed lips, as shall be
discussed in the following section.

Immediately upon hatching the larvae swam to
the water surface and began schooling at the sur-
face in a two-dimensional array (one-fish deep).
This neustonic schooling behavior shifted to a pat-
tern of subsurface schooling (three-dimensional
schools, usually within 10 cm of the surface) at
about 48 h after hatching. At this time, feeding
was first noted. By 72 h after hatching, about half
the larvae had food in the guts within 4 h of the
daily food introduction; about 80% had full guts
after introduction of food on day 4 (96 h). Schooling
behavior was characteristic of the entire period of
larval development; these schooling tendencies
decreased progressively during metamorphosis
(from about 30 to 50 mm SL) and the juveniles did
not show true schooling behavior in the confines of
aquaria.

The larval T. trichodon were rapid swimmers.
Alexander ( 1967 ) mentioned 10 body lengths/s as a
maximum burst speed for teleosts of any size and
3-5 body lengths/s as a maximum sustained speed
(maintained for at least several minutes). Al-
though no effort was made to determine precisely
the cruising speed of larval T. trichodon, observa-
tions of the distance traversed in 5 s intervals re-
vealed a cruising speed of about 10 body lengths/s
and always over 5 body lengths/s. This rapid
swimming occurred abruptly upon hatching, be-
fore the onset of feeding. Synchronized hatching,
the abrupt onset of schooling, and rapid swimming
may have evolved as mechanisms for larvae to
escape the physical dangers of the wave-swept in-
cubation site.

Trichodon trichodon first burrowed into sand as
metamorphosed juveniles of 50-60 mm SL. They
burrowed by simultaneously undulating the body
laterally while fanning the pectoral fins upward
and forward, so that the body sank downward and
backward into the sand. The eyes and nostrils
usually remained exposed above the sand, al-
though the entire body could be buried. Burrowing
did not occur until fleshy fringes had developed on
the jaws. The fringed lips may permit water to be
inhaled without allowing sand to enter the buccal
cavity. The allometric growth prior to inital bur-

960

rowing may indicate a functional role of the deep,
narrow form of the ventral part of the body in
burrowing.

Larval Development

Morphometric and meristic features of an ex-
cised embryo ( 2 wk prior to hatching) and larvae of
nine posthatching ages are presented in Table 1.
The outstanding feature of the late embryo was
the presence of caudal fin rays and a flexing
notocord with the posterior margins of the hypural
plates about 45° to the horizontal body axis. This
precocious development of the caudal fin remained
a diagnostic character throughout the larval
period and probably contributed to the rapid
swimming speeds discussed earlier.

The late embryo and the newly hatched larvae
have a large oil droplet positioned anteriorly in the
yolk. The abdomen has about 40 melanophores
radiating from the dorsal gut surface. In addition
to the features detailed in Table 1, these early ages
have a few external melanophores in the nasal
region, lower jaw angle, cranial region (7-10), and
anterior mandibles (Figure 1). There is also an
internal melanophore anterior to each otic capsule
and, in fresh material, about 30 xanthophores over
the cranium. Three preopercular spines are pres-
ent as are the pectoral fin rays.

By 9 d hatching age, the posterior margins of the
hypural plates are approaching a vertical orien-
tation and have an increased number of
melanophores, while the caudal and pectoral fin
rays have increased in length. There is a row of 4 or
5 small melanophores along each side of the an-
terior insertion of the dorsal fin fold and an inter-
nal row of about 24 melanophores along the
notocord (less clearly visible than external pig-
ment, therefore not illustrated). Eight small
melanophores have appeared in the cranial re-
gion, clustered among six larger ones, previously
developed. A single melanophore has appeared on
the ventral midline of the lower jaw (not visible in
side view). Rows of melanophores have also ap-
peared along the anterior end of the mandibles
and horizontally on the dorsal portion of the oper-
culum. Snout melanophores become prominent by
this stage, as do teeth on the lower jaw. These teeth
are easily visible at this stage, becoming progres-
sively reduced until, at 25 d hatching age, they are
no longer noticeable.

The 18 -d specimen has vertical posterior mar-
gins on the hypural plates, a forked caudal fin, and

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961

secondary caudal fin rays. Melanophores are more
numerous along the insertion of the dorsal fin fold
(18-19 each side), internally along the notocord
(27; vague, not illustrated), along the ventral mid-
line of the lower jaw (10), in the cranial region (7
large, 23 small ), and on the posterior margin of the
hypurals (6). Melanophores appear larger and
more dense on the dorsal gut surface as well. Two
melanophores are present laterally at the angle of
the notocord and 10 melanophores are visible on
the principal caudal rays. Pectoral fin ray devel-
opment is complete (21 rays ) and four preopercular
spines are evident.

By 25 d hatching age the melanic pigmentation
of the dorsal body surface, jaw, and snout has pro-
liferated considerably, while dorsal and anal fin
ray development has started (Table 1) and pelvic
fin buds are visible. Paired rows of 38 large
melanophores occur on the dorsal body along the
entire length of the dorsal fin. Cranial
melanophores appear as a pair of dense patches
(one on each side) with a third median patch on the
nape region. The postanal ventral midline
melanophores appear more internal than at

younger ages. A new row of superficial
melanophores has appeared on the mediolateral
trunk musculature (posterior half of body), while
the angle of the notocord is overlaid by an angular
"bracket" of small melanophores, the dorsal leg of
which continues anteriorly as a faint internal row
dorsal to the notocord. The melanophores at the
posterior margin of the hypurals form continuous
vertical bands on each plate. Finally, a fifth
preopercular spine is becoming visible ventrally.

The 29-d specimen I not illustrated in Figure 1)
is marked by the appearance of a ring of small
melanophores around each eye, the development
of both internal and superficial ventral midline
melanophores (Table 1) and doubled rows of
melanophores along each side of the dorsal fin base
on the anterior half of the body. Cranial and dorsal
gut melanophores have continued to become more
dense and the pelvic fins are formed, without
elements.

At 35 d hatching age, melanophores are on the
dorsal margin and dorsal insertion of the pectoral
fin and melanophores are arrayed in double or
triple rows on each side of the dorsal fin bases

5 mm

B

962

-^g

Figure l. — Larvae and early juveniles of Trichodon tnchodon (preserved lengths). A. 0 d, 13 mm SL;
B. 9 d, 14.5 mm SL; C. 18 d, 17.2 mm SL; D. 25 d, 20 mm SL; E. 35 d, 27 mm SL; F. 56 d, 32 mm SL.

posteriorly to the middle of the second dorsal, con-
tinuing as single rows across the peduncle.
Melanophores are on the first three elements of
the first dorsal fin. On the lower jaw, melanin has
extended posteriorly to the juncture with the
maxillaries. A patch of melanophores has devel-
oped on the dorsal preoperculum. About 26 scat-
tered melanophores appear dorsolaterally on the
trunk musculature, above the mediolateral row,
and melanophores occur closely spaced, lining the
edges of principal caudal rays. The melanophores
on the hypural margins have spread anteriorly
along the insertion of the secondary caudal rays.
Allometric growth at this age includes an increase
in the relative snout-anus length (Table 1) and a
slight upturning of the jaw.

The 43-d specimen (not illustrated) exhibits
more regular arrays of the most recently devel-
oped melanophore patterns: the mediolateral row

consists of 33 melanophores, the dorsolateral
melanophores now form broken rows along the
margins of myomeres, and the caudal rays are
lined with rows of melanophores. By this age, gut
melanophores appear internal rather than exter-
nal. Only superficial ventral midline
melanophores (25) are visible.

The 56-d specimen is easily recognized as a
young sandfish. The entire snout, jaw, cranium,
and nape regions are densely covered with
melanophores, continuous with rows along the
dorsal fin bases. The upper pectoral fin rays are
lined with melanophores, as are the spines on the
anterior half of the first dorsal fin. More
melanophores have appeared over the caudal
peduncle. All fins are completely formed by this
stage and the five preopercular spines appear to
radiate from a centrum.

By 70 d hatching age the body proportions re-

963

semble those of the adult. Hart (1973) listed body
depth as 0.28 SL for adults, which compares with
0.27 SL for the 70-d specimen (Table 1). The
snout-anus length has reached the adult propor-
tion of 0.5 SL (Hart 1973) by this stage. The jaw
angle and eye position have not attained adult
character by 70 d, however, and the fringed lips
and elongate nostrils of the adult are not evident.
These features are present by the time burrowing
behavior first appears at sizes of about 55-60 mm
SL (165 d).

Discussion

Larvae of T. trichodon are distinct and easily
identified. Myomere counts alone would separate
T. trichodon from other elongate larvae in the
northeastern Pacific. As mentioned, the early de-
velopment of the caudal fin is a distinguishing
character of all early larval stages of T. trichodon.
The newly hatched yolk-sac larva has a flexed
notocord and developing caudal rays. The caudal
fin is forked and has secondary rays developing
prior to the development of elements of other me-
dian fins.

The melanophore patterns developed in gradual
stages with little variation among the individuals
from this particular hatch. The most distinctive
melanophores are perhaps those in the caudal re-
gion, on the hypural margins, and at the notocord
bend. The overall melanophore patterns for each
stage could probably be used as a basis for diag-
nosis, certainly when taken together with the
morphometry and fin development patterns.

The preopercular spines are present at hatching
and seem unique among sympatric elongate lar-
vae. The stellate arrangement of these spines in
the later development stages is unique.

Altogether, there appears to be little chance for
misidentification of this species in the northeast
Pacific region. This is of interest in light of the
absence of these larvae from records of ichthyo-
plankton surveys in this region (e.g., Richardson
and Pearcy 1977). In the Gulf of Alaska, where T.
trichodon is an abundant inshore fish species, only
one larva has been taken by plankton nets in an
extensive ichthyoplankton survey (Kendall^). The
only other northeast Pacific larvae, of which I am
aware, with such high-speed schooling in a

laboratory situation are those of Ascelichthys
rhodorus (pers. obs.), which also do not appear in
plankton nets (Richardson and Pearcy 1977). Al-
though this behavior may enhance evasive
capabilities in areas sampled for plankton, a
further possibility is that this behavior may en-
able larvae to inhabit the extreme nearshore,
which is usually not included in regular plankton
surveys.

Acknowledgments

I thank Murray Newman, Director of the Van-
couver Aquarium, for encouraging and supporting
this study, and Arthur W Kendall, Northwest and
Alaska Fisheries Center, NMFS, NOAA, for
critical review of the text. James Cave collected
the eggs and Robin Ade drew the illustrations.

Literature Cited

ALEXANDER. R.

1967. Functional design in fishes. Hutchinson, Lond.,
160 p.
BREDER, C. M., Jr., and D. E. ROSEN.

1966. Modes of reproduction in fishes. Natural History
Press, Garden City, N.Y., 941 p.
CLEMENS, W. A., AND G. V WILBY.

1961. Fishes of the Pacific coast of Canada. Fish. Res.
Board Can., Bull. 68, 443 p.

Hart, J. L.

1973. Pacific fishes of Canada. Fish. Res. Board Can.,
Bull. 180, 740 p.
ISAKSON, J. S., C. A. SIMENSTAD, AND R. L. BURGNER.

1971. Fish communities and food chains in the Amchitka
area. BioScience 21:666-670.
RICHARDSON, S. L., AND W. G. PEARCY.

1977. Coastal and oceanic fish larvae in an area of upwell-
ing off Yaquina Bay, Oregon. Fish. Bull., U.S. 75:125-
145.

JEFFREY B. MARLIAVE

Vancouver Public Aquarium

P.O. Box 3232

Vancouver, B.C. V6B 3X8 Canada

^Arthur W. Kendall, Jr., Fishery Biologist, Northwest and
Alaska Fisheries Center, NMFS, NOAA, 2725 Montlake
Boulevard East, Seattle, WA 98112, pers. commun. August 1979.

964

A RADIOLOGIC METHOD FOR EXAMINATION

OF THE GASTROINTESTINAL TRACT IN THE

ATLANTIC RIDLEY, LEPIDOCHELYS KEMPI,

AND LOGGERHEAD, CARETTA CARETTA,

MARINE TURTLES'^

In the past 2 yr the National Marine Fisheries
Service of the U.S. Department of Commerce has
been raising hatchlings of the Atlantic ridley,
Lepidochelys kempi, and loggerhead, Caretta
caretta, marine turtles. These are classified as en-
dangered and threatened species under the U.S.
Endangered Species Act of 1973 (U.S. Fish and
Wildlife Service 1977, 1978). The rearing activity
was undertaken to provide a better understanding
of the early life histories of those species.

Of immediate concern was the evaluation and
treatment of skin, gastrointestinal, lung, and sys-
temic diseases, which emerged rapidly in the cap-
tive turtles. Radiologic examination was sought as
a possible diagnostic modality for various prob-
lems. To this end we have attempted to develop
radiologic techniques for the study of normal and
diseased animals.

In this paper we report on the use of barium
sulfate contrast agent in studying the gastro-
intestinal (GI) tract of normal turtles and propose
its use as an aid in the diagnosis of turtle GI
diseases.

Methods

The GI tracts of two loggerhead and two ridley
turtles, between the ages of 4 and 10 mo, were
examined by means of commercially available
44% (wt/wt) aqueous barium sulfate suspension.^
Similar suspensions are frequently used in the
examination of the GI tract of humans (Margulis
1973; Miller 1973).

Preparation of the GI tract was accomplished by
not feeding the animals for 2 d and then giving 0.5
ml of X-Prep, a commercial laxative of extract of
senna fruit (Gray Pharmaceutical Company, Nor-
walk, Conn.), on the day prior to the examination.
Next, the esophagus was intubated using a plastic

'The investigations involving the Atlantic ridley turtle were
conducted under Permit No. PRT 2-1770 (U.S. Federal Fish and
Wildlife Service), permits 1978-ABC-IV-0751, No. 27611-8786,
and 1979-ABC-IV-1258, Exp. 4287 (Mexican Government).

^Contribution Number 81-lG, Southeast Fisheries Center
Galveston Laboratory, National Marine Fisheries Service,
NOAA.

^E-Z-EM Company, Cat. No. 750, Westbury, N.Y. Reference to
trade names or commercial companies does not imply endorse-
ment by the National Marine Fisheries, NOAA.

FISHERY BULLETIN: VOL. 78. NO. 4, 1981.

umbilical artery catheter (Argyle, Cat. No. 8888-
160-226, Sherwood Medical Co., St. Louis, Mo.)
measuring 5 mm in circumference. The intubation
of the ridley turtle s esophagus proved more dif-
ficult than the loggerhead's as they resisted pas-
sage of the catheter through the oropharynx.
Therefore, a dose of 0.25 mg of succinylcholine
chloride'* was given subcutaneously in the neck to
effect partial skeletal muscle paralysis. Paralysis
was adequate in 4 or 5 min, rapidly diminished,
and was nearly undetectable in 20 min. (No unto-
ward side effects occurred.) Also, a plastic hollow
guide (4 mm in diameter) was placed in the
oropharynx and upper esophagus through which
the umbilical artery catheter was threaded into
the esophagus and stomach. Both the hollow guide
and catheter were lubricated with small amounts
of surgical lubricant. The placement of the cathe-
ter tip in the stomach and injection of ap-
proximately 5 ml of contrast material were done
under fluoroscopic control. Radiographic films
were then exposed using either the phototimed
fluoroscopic filming device or manual techniques
utilizing standard radiographic equipment, film,
and film cassettes. The fluoroscopic unit, radio-
graphic equipment, radiographic film, and film
cassettes which were used are of standard med-
ical grade and are available in most radiology
departments. Serial filming consisting of fluoro-
scopic spot films, made in various degrees of ob-
liquity and standard medical radiographic film^ in
cassettes (Halsey Rigidform, Halsey X-Ray Prod-
ucts, Brooklyn, N.Y.) equipped with par speed
intensifying screens (Radelin TA-3, GAF Corp.,
Brooklyn, N.Y), and industrial grade film^ in
cardboard cassettes made in the dorsoventral (DV)
position were done on the day of the examination.
For the following 2 d DV par speed medical films or
industrial grade films were made on each consecu-
tive day. Thereafter, DV films were exposed every
other day for 4 d. Radiographic technique and film
types are given in Table 1.

Radiation exposure using industrial film ex-
posed at 60 kV peak and 400 mAs and par speed
medical film exposed at 50 kV peak and 10 mAs
with a target film distance of approximately 100
cm was 0.98 and 0.14 Roentgen/exposure, respec-
tively. These measurements were obtained using a
0.6 cm^ Baldwin-Farmer air ionization chamber

^Succinylcholine HCl injection U.S.R, Oraganon, Inc., West
Orange, N.J.

sRodak XRP-1, Eastman Kodak Co., Rochester, N.Y.
«Kodak RP M, Eastman Kodak Co., Rochester, N.Y.

965

Table l. — Radiographic technique for turtle examinations.

Weight

Carapace

Turtle

Voltage

Tube-film

(9)

length (cm)

position

tkV)

Current (mAs)

distance (cm)

Film type

400

15.0

DV

60

400

100

Industrial

300

12,5

DV

50-55

300-360

100

Industrial

350

13.5

DV

50

40

100

Industrial

400

13.0

DV

50

10

100

Medical

300-400

13-15

Variable

55-60

Phototi

med (fluoroscopy unit)

—

Medical

'DV = Dorsoventral projection.

(Nuclear Enterprises, Inc., San Carlos, Calif.) on
an electrometer'^ at 300 V collection potential.

Results

Adequate clearing of food residue was obtained
after the subjects were prepared in the manner
described in Methods. The experimental animals

'Model 602 Electrometer, Keithley Co., Cleveland, Ohio.

were quite small (0.3-0.4 kg) and good resolution
and detail are a necessity if mucosal detail is to be
adequately examined and appraised. Excellent
detail of the esophagus, stomach, and small intes-
tinal mucosa was obtained by using industrial
grade film while adequate detail was obtained on
par speed medical film. The radiologic anatomy
of the esophagus, stomach, and small intestine
correlated well with the findings noted at gross
necropsy of turtles of similar age and size that had

Figure l. — Dorsoventral view of a 15 cm carapace length, 400 g, 8-mo-old loggerhead turtle made on the
second day after barium instillation. Industrial grade film was used for this exposure. 1 — stomach, 2 — proximal
small bowel, 3 — tracheal air shadow, 4 — lungs. The arrowheads demonstrate the longitudinal mucosal pattern
in the proximal small bowel (1.8 x).

966

died of various causes. Figure 1 shows the rel-
atively smooth mucosa of the stomach which has
been distended with barium. The smooth lon-
gitudinal folds of the proximal small bowel are
also easily identified. Also in Figure 1 just to the
left of the tracheal air shadow (3) and superim-
posed over the cervical vertebrae, a few
esophageal papillae are faintly outlined by small
amounts of barium. Incidently, injection of con-
trast directly into the esophagus demonstrated the
esophageal papillae and the narrowing in the re-
gion of the gastroesophageal junction with greater
clarity than in Figure 1. The size and position of
the GI structures were also easily assessed. Con-
tinued filming over several days demonstrated
slow progression of the barium sulfate suspension
through the small intestine into the colon. In the
colon residual fecal contents mixed with the
barium and obscured the mucosal detail some-
what. Transit time was noted to be at least 4 or 5 d
from the stomach to the proximal colon in all four
animals studied.

Discussion

The radiologic examination of the upper GI tract
of marine turtles by using barium sulfate as a
contrast material provides a potential tool in the
evaluation of various diseases in turtle popula-
tions. The radiographic information from these
studies should aid in evaluating turtles for partial
or complete small bowel obstruction, with as-
sociated changes in motility and bowel size, and
foreign bodies within the intestinal tract such as
parasites or bezoars. Diseases altering the
mucosal pattern such as ulceration, gastritis, en-
teritis, or colitis caused by various infectious or
inflammatory processes could be demonstrated.
The disease states listed above are frequently
demonstrated by similar GI studies performed in
humans (Paul and Juhl 1972).

The use of succinylcholine chloride in these
animals should be approached with caution. The
total dose should be divided and given incremen-
tally over 3-5 min until the desired effect is ob-
tained. The use of a well lubricated plastic hollow
guide is recommended prior to the decision to use a
paralytic agent.

Radiation exposure was of concern but the cal-
culated doses of 0.98 and 0.14 Roentgen/exposure
for industrial and par speed medical film were well
below the harmful radiation dose in several
species of turtles found by Altland et al. (1951) and

Cosgrove (1971). They resemble dosage levels used
by Gibbons and Greene (1979), which produced no
apparent harm to the freshwater turtles in their
study. To reduce radiation exposure during the
examination the use of par speed medical film
which requires a lower radiation dose is recom-
mended when the clinical situation permits. For
instance, intestinal obstruction would require
only par speed medical film technique, as dem-
onstration of mucosal detail would be unneces-
sary when assessment of dilatation of the bowel,
stasis of contents, and site of the obstructing pro-
cess would be primary concerns. In examinations
where mucosal detail is desirable such as detec-
tion of small ulcerations, industrial film and its
attendant higher exposures may become neces-
sary.

Acknowledgments

We appreciate the help, encouragement, and
support of M. H. Schreiber, Chairman, Depart-
ment of Radiology, University of Texas Medical
Branch, (UTMB), as well as his comments on
preparation of this paper; to Robert Perry, health
physicist. Department of Radiology, UTMB, for his
assistance in taking and calculating the radiation
doses; and to Peggy Seibel, residents' secretary,
UTMB, for typing the manuscript.

Literature Cited

ALTLAND, P D., B. HIGHMAN, AND B. WOOD.

195L Some effects of x-irradiation on turtles. J. Exp.
Zool. 118:1-19.
COSGROVE, G. E.

1971. Reptilian radiobiology. J. Am. Vet. Med. Assoc.
159:1678-1684.

GIBBONS, J. W, AND J. L. GREENE.

1979. X-ray photography: a technique to determine repro-
ductive patterns of freshwater turtles. Herpetologica
35:86-89.

margulis, a. R.

1973. Use of iodinated water-soluble contrast agents in
acute gastrointestinal disease. In A. R. Margulis and H.
J. Burhenne (editors*, Alimentary tract roentgenology.
Vol. 1, p. 271-280. 2d ed. C. V Mosby Co., St. Louis, Mo.
Miller, R. E.

1973. Barium sulfate as a contrast medium. In A. R.
Margulis and H. J. Burhenne (editors). Alimentary tract
roentgenology. Vol. 1, p. 114-126. 2d ed. C. V Mosby Co., St.
Louis, Mo.

Paul, L. W, and J. H. Juhl.

1972. The abdomen and gastrointestinal tract. In The es-
sentials of roentgen interpretation, p. 411-643. 3d ed.
Harper and Row, HagerstowTi, Md.

U.S. FISH AND WILDLIFE SERVICE.

1977. A guide to endangered species regulations — The

967

Endangered Species Act (with attachment: 50 CFR17
(Rev. 8/77), p. 1-16.
1978. The Endangered Species Act — The green
loggerhead, and olive ( Pacific) ridley sea turtles. T-1, p. 1-3.

G. L. MCLELLAN

Department of Radiology
University of Texas Medical Branch
Galveston, TX 77550

Southeast Fisheries Center Galveston Laboratory
National Marine Fisheries Service, NCAA
Galveston, TX 77550

J. K. LEONG

SUMMER FOOD OF PACIFIC COD,

GADUS MACROCEPHALUS, IN COASTAL

WATERS OF SOUTHEASTERN ALASKA

The Pacific cod, Gadus macrocephalus Tilesius, is
ecologically important in the Gulf of Alaska and
may be more extensively utilized in future com-
mercial fishing efforts. Although Pacific cod is one
of the most abundant demersal fish in shallower
(<200 m depth) waters of the Gulf of Alaska (Al-
verson et al. 1964; Ronholt et al.^), it has not been
extensively fished. The total harvest of Pacific cod
from the Gulf of Alaska (mostly by foreign fishing
fleets) is estimated to be a "small fraction of the
maximum sustained yield" and "substantially
higher catches" could be supported (North Pacific
Fishery Management Council^). Because of the
recent establishment of the 200-mi United States
Fishery Conservation Zone and a concurrent
interest in bottomfishing, a domestic fishing in-
dustry may develop that could also exploit Pacific
cod.

Little research has been done on the Pacific cod
in Alaskan waters, especially concerning its foods.
Most of the studies on Pacific cod have been con-
ducted by Soviet investigators in the northwestern
Pacific Ocean (summarized by Moiseev 1953).
Jewett (1978) investigated the diet of Pacific cod
near Kodiak Island, Alaska. In this note, I report

■Ronholt, L. L.,H, H.Shippen, and E.S.Brown. 1978. De-
mersal fish and shellfish resources of the Gulf of Alaska from
Cape Spencer to Unimak Pass 1948-1976 (a historical re-
view). Processed rep., 955 p. Northwest and Alaska Fisheries
Center, Natl. Mar. Fish. Serv., NOAA, 2725 Montlake Blvd. E.,
Seattle, WA 98112.

'^North Pacific Fishery Management Council. 1978.
Fishery management plan for the Gulf of Alaska groundfish
fishery during 1978. Unpubl. rep., 220 p. North Pacific Man-
agement Council, PO. Box 3136DT, Anchorage, AK 99510.

the foods of Pacific cod in a different region of
Alaska, southeastern Alaska.

Methods

Pacific cod were sampled during a cruise con-
ducted by the National Marine Fisheries Service
primarily to assess cod resources and evaluate dif-
ferent types of fishing gear used. During a 17-d
period in July 1977, 520 Pacific cod stomachs were
collected in two regions of southeastern Alaska
coastal waters: 17 sites in the Gulf of Alaska be-
tween Cape Spencer and Yakutat Bay (outside
waters, Figure 1) and 34 sites in protected waters
between northern Lynn Canal and Frederick
Sound (inside waters, Figure 2). Each site was
sampled once.

Pacific cod were caught with traps (360 fish) and
gill nets (160 fish) in water 38-176 mdeep (Table 1).
Most fish were caught in waters <90 m deep.
Traps, 0.8x0.8x2.4 m rectangular structures
with tunnel openings, were baited with chopped
frozen Pacific herring, Clupea harengus pallasi,
and set on the bottom. Gill nets, 180 m long, made
of 15 cm or 17.5 cm diagonal-stretched-mesh
monofilament, were set on the bottom or 0.6 m
above the bottom. Both gear were set during day-
light hours, fished overnight, and retrieved the

FIGURE 1. — Locations where Pacific cod were sampled in outside
waters, southeastern Alaska, July 1977.

968

FISHERY BULLETIN: VOL. 78. NO. 4, 1981.

• trap sampling site

♦ cillnet sampling site

Figure 2. — Locations where Pacific cod were sampled in inside
waters, southeastern Alaska, July 1977.

Table l. — Summary of samples of Pacific cod caught in gill nets
and traps in southeastern Alaskan waters, July 1977. Each site
was sampled once.

Caught in

gill nets

Caught

In traps

Mean

Mean

Mean

Mean

Sites

depth

Cod

length

Sites

depth

Cod

length

Area

(no.)

(m)

(no.)

(cm)

(no.)

(m)

(no.)

(cm)

Outside

waters

7

149

81

73.9

10

63

135

60.7

Inside

waters

7

52

79

72.7

27

70

225

66.0

Both

14

101

160

73.3

37

68

360

640

next day. Usually, stomachs were removed from all
Pacific cod caught, but random subsamples were
taken from a few large catches. Stomachs and re-
gurgitated or undigested food in the esophageal
and mouth areas were preserved in Formalin.^ The
sex of each Pacific cod was identified, if possible,
and the total length (TL, tip of snout to end of tail)
was measured.

^Reference to trade names does not imply endorsement by the
National Marine Fisheries Service, NOAA.

Estimated percentage volume of major food
categories and frequency of occurrence of each
food were determined. The volume of each major
food category (i.e., fish, pandalid shrimp) was vi-
sually estimated to the nearest 5% for each
stomach that arbitrarily appeared to be at least
one-fourth full. Foods in stomachs less than one-
fourth full were listed only as present and often
were slowly digested items, such as fish otoliths or
cephalopod beaks in trace amounts. No other
allowances were made for stomach fullness. When
pooling results, I averaged equally the percent-
ages of each food in all stomachs one-fourth or
more full. Visual estimates of the percentage vol-
ume of food in each category were generally within
10% of percentages determined by actual mea-
surements of displacement volume. I identified all
foods in all stomachs to the lowest taxonomic level
possible and calculated the overall frequency of
occurrence (expressed as the percentage of
stomachs containing the food) of each food.

Volume data on each major food category were
analyzed to determine whether relationships
existed between foods eaten by Pacific cod and 1)
size and sex of Pacific cod, 2) the location at which
they were caught (inside waters vs. outside
waters), and 3) the type of gear. I arbitrarily sepa-
rated the Pacific cod into three total length
categories to determine whether the different
foods eaten were related to size of Pacific cod. The
size categories were ^60 cm, 61-70 cm, and >70
cm. Too few samples were taken at different
depths in the same localities to allow analysis of
Pacific cod foods by depth.

Results

If data from all areas are combined, regardless
of size and sex of Pacific cod and gear type, fish
were the most important food of Pacific cod both
volumetrically and in frequency of occurrence.
Fish accounted for more than 40% of the stomach
contents by volume (Table 2) and were in nearly
60% of the stomachs (Table 3). The largest percent-
age of fish in the stomachs was unidentifiable;
however, of the identifiable fish, Pacific herring
and walleye pollock, Theragra chalcogramma,
were eaten most often. Pacific herring ranged from
9 to 25 cm long (mean, 18 cm); walleye pollock,
identified by their large and characteristic
otoliths, were juveniles and ranged from 10 to 31
cm long (mean, 22 cm). Some of the unidentified
fish were probably Pacific herring, pricklebacks

969

Table 2.— Mean estimated percentage volume of foods in stomaciis of Pacific cod in southeastern Alaskan waters, July 1977 (stomach

fullness one-fourth or greater).

All areas

Outside waters

Inside waters

All

All

All

61-

All

61-

All

61-
70 cm

Food Item

fish

males

females

s60cm

70 cm

■70 cm

fish

eeOcm

70 cm

■70 cm

fish

s=60cm

-70 cm

Fish

42.5

39.4

44.9

17.1

35,4

66.0

35.1

11.9

278

61.9

48.0

22,7

40,5

687

Crab

26.1

26.5

25.2

38.0

30.3

14.3

449

57.7

56,7

21 1

12,1

163

124

98

Shrimp

16.9

21.8

13.9

23.0

20.3

9.1

4.7

6.3

50

2,7

26,1

41,6

30 7

13,4

Pandalid

9.7

14.2

7.3

5.6

13.7

7.1

1.0

1,7

5

9

16,2

9,9

22,7

11,2

Crangonid

3.5

3.4

3.4

9.6

2.6

1.1

2.6

3,5

2.7

1,5

4.3

16,3

26

9

Hippolytid

23

29

20

4.9

2,5

.6

3

1 1

1

0

3.8

9,2

4,0

9

Unidentified

1.4

1.3

1.2

29

1.5

.3

,8

0

1,7

,3

18

62

14

,4

Gammarid amphipods

3.5

4.3

3.0

69

3.8

1,1

3,8

87

2,1

2.3

3,2

4 9

50

2

Cephalopods

3.1

2.2

3.9

2.8

3.6

29

1,0

29

,5

2

4 7

2 8

5 6

4 6

Mollusl<s other than

cephalopods

1.7

1.2

1.9

2.7

1.8

1,0

,9

,7

1,5

,9

2,3

4,8

2,0

1,2

Polychaetes

2.2

1,1

29

3.0

2.3

1,7

4,2

5,0

3,6

4,3

7

8

1,4

0

Other food items

and unidentified

4.0

3.5

4,3

6-5

2.5

3,9

54

6,8

2,8

6,6

29

6,1

24

2,1

Cod sampled (no.)

439

163

266

90

193

156

187

47

78

62

252

43

115

94

Mean total length (cm)

67.0

65.2

686

53.7

65.6

77,0

657

522

65.4

776

67,7

55,4

658

76,6

(Stichaeidae), and eelpouts (Zoarcidae), which are
not as distinguishable as walleye pollock and may
have been eaten more frequently than the values
in Table 3 indicate. Flatfish (Pleuronectidae) were
easily recognized and, because few were found,
were probably not an important food for Pacific cod
in these waters during July.

Crab and shrimp were the next most important
foods. The volume of crab in Pacific cod stomachs
was greater than the volume of shrimp; however,
the frequency of occurrence of shrimp was greater
than the frequency of occurrence of crab. Snow
crab, Chionoecetes bairdi, the crab most often
eaten by Pacific cod, were juveniles and ranged
from 5 to 42 mm carapace width (mean, 20 mm).
As many as 30 snow crabs were found in some
stomachs. Dungeness crab. Cancer magister, was
the only other crab eaten in more than incidental
numbers. Pagurids (hermit) and other anomuran
crabs were rarely eaten. Pandalid shrimp, par-
ticularly Pandalus tridens and P. borealis, were
more frequently eaten than either crangonid or
hippolytid shrimp, and all three families of shrimp
were often found together in stomachs.

Other invertebrates were found in the Pacific
cod stomachs, but their volumes and frequencies
were small. Cephalopods were in more than 14% of
the stomachs but constituted only 3.1% of the
mean volume. Often only the cephalopod's horny
beaks were present; however, whole Octopus sp.
formed the bulk of the stomach contents of a few
Pacific cod. Gammarid amphipods were in 14% of
the stomachs. Pelecypods, mostly Nuculana sp.,
were infrequently eaten. The large polychaete
Aphrodita sp. ("sea mouse") was found in some
stomachs and composed most of the volume for

970

the polychaetes. Planktonic foods, such as
euphausiids or mysids, were rarely found and
then, only in trace amounts.

At all locations, the size of the Pacific cod af-
fected the kinds of food eaten (Table 2). Small
Pacific cod («60 cm) fed mostly on crab and
shrimp; only 17% of the estimated volume of their
stomach contents was fish. Large Pacific cod ( >70
cm long) fed predominately on fish (66% by vol-
ume). The diet of intermediate-sized Pacific cod
(61-70 cm) was transitional between the diets of
the small and large Pacific cod.

Sex of Pacific cod did not appear to be related to
the major foods eaten (Table 2). Fifty-nine percent
of the Pacific cod were females, 38.7% were males,
and 2.3% were of unidentified sex. Females had a
mean of 68.6 cm TL; males, 65.2 cm TL. The minor
differences that did arise between the foods of each
sex can probably be attributed to the greater mean
length of females.

Foods of Pacific cod in outside waters were dif-
ferent from foods of those in inside waters (Tables
2, 3). Pacific cod in outside waters ate a larger
volume of crabs (mostly juvenile snow crab) than
those in inside waters; however, in inside waters,
the volume of shrimp (particularly pandalid
shrimp) in the stomachs was much higher than in
outside waters. These differences in the volume of
foods eaten were especially pronounced for small
and intermediate-sized Pacific cod. All sizes of
Pacific cod ate more fish in the inside waters than
in the outside waters. Pacific herring, especially,
were heavily consumed in inside waters.

The two gear (gill nets and traps) probably did
not significantly bias the results. Comparison of
foods in Pacific cod caught by gill nets and foods in

Table 3. — Frequency of occurrence of food items ^1.0% in
stomachs of 492 Pacific cod, southeastern Alaskan waters, July
1977 (based only on stomachs containing food).'

Frequency of occurrence (%)

All

Outside

Inside

Food Item

areas

waters

waters

Fishes

585

542

61 5

Clupea harengus pallasi

96

10

15,5

Theragra chalcogramma

87

85

89

Stichaeidae

2.8

5

45

Unidentified stichaeids

22

.5

3,4

Pleuronectidae

18

2.5

14

Unidentified pleuronectids

1.0

.5

1,4

Zoarcidae

1.2

.5

1.4

Unidentified

36.4

383

35,1

Shrimps

46.5

24.9

61 5

Pandaiidae

254

70

38,1

Pandalus trldens

5.5

45

62

P. borealis

4.7

0

7,9

P danae

1.8

0

3,1

P hypsinotus

16

0

2,7

Unidentified pandalids

15,2

1,7

24,1

Crangonidae

18.9

16-9

203

Crangon spp.

8.9

6,0

10,7

Argis sp.

1.0

2,0

,3

Unidentified crangonids

92

90

86

Hippoiytidae

9.6

1,5

15,1

Unidentified shrimp

7.7

4.5

10,0

Crabs

39.6

62.7

23.7

Brachyuran crabs

32.3

58.2

14,4

Chionoecetes bairdi

26.2

44,8

13.4

Cancer magister

4.1

10,0

0

Hyas lyratus

1.0

1,5

.7

Unidentified brachyurans

2.2

4,0

1,0

Anomuran crabs

3,7

1.0

5,5

Unidentified pagurids

28

5

4,5

Unidentified crabs

2,6

2.5

2,7

Cephalopods

14,4

9.5

17.9

Octopus sp.

4,1

1.5

5,8

Unidentified cephalopods

10,0

7.0

12.0

Gammarid amphipods

14,0

16,4

12,4

Pelecypods

11,4

7,5

14.1

Nuculana sp.

7.5

3,0

10.7

Unidentified pelecypods

3.3

3-0

3.4

Polychaetes

6.5

10,9

3.4

Aphrodita sp.

3.7

8.5

.3

Unidentified polychaetes

2.6

2.5

2.7

Gastropods

3.9

2.5

4,8

Natica sp.

1.2

2,0

.7

Unidentified gastropods

2.2

0

3,8

Algae

3.0

3.0

3.1

Euphausiids

3.0

0

5.1

Isopods

1.6

2.5

.3

Rocinela sp.

1.6

2.5

.3

Mysids

1,0

0

1,7

Unidentified food items

2.6

3.5

2,1

'Also present at frequencies <1.0%: Fishes — Lumpenus maculatus. L.
sagitta, Hippoglossoides elassodon. Lepidopsetta bilineata, Lycodes bre-
vipes. L. palaeris. Dasycottus setlger, Coryphaenoides sp,, Ra/a sp, embryo,
unidentified fish eggs: shrimps — Pandalus stenolepls. P. goniurus. P.
platyceros: crabs — Oregonia gracilis. Lopholithodes sp., Labidochirus
splendescens: cephalopods — Rossia pacifica, pelecypods — Siliqua patula.
Chlamys rubidus. Serripes groenlandicus: polychaetes — Abarenicola sp.:
gastropods — Lora sp., Neptunea sp.: barnacles — Lepas sp.. unidentified bar-
nacles: sipunculids; hydroids; ophiuroids; nemerteans; anthozoans; porife-
rans: foraminifera: unidentified invertebrate eggs.

Pacific cod caught by traps was difficult because
the two gear, which tend to catch different sizes of
fish, were frequently set at different localities or
depths (Table 1; Figures 1, 2). However, when traps
and gill nets caught similar-sized fish in the same
areas, foods were also similar (see Table 4, Pacific
cod 61-70 cm TL in outside waters and >70 cm TL
in inside waters). In other cases, locality rather

than gear appeared to be the overriding factor
determining kinds of food eaten. Of the 24 Pacific
cod sampled in the 61-70 cm TL gill net category in
inside waters, 15 were taken in Idaho Inlet. There,
Pacific herring apparently were so abundant that
all sizes of Pacific cod caught in both gill nets and
traps fed upon them.

The volume of gammarid amphipods in the
stomachs of Pacific cod caught in traps may have
been artificially high. Gammarid amphipods were
almost exclusively found in Pacific cod caught in
traps (Table 4). These amphipods were probably
attracted to the baited traps where Pacific cod in
the traps fed upon them. In contrast, other inver-
tebrates, such as shrimp or crabs, appeared to be
found equally in stomachs of Pacific cod caught in
either traps or gill nets.

Discussion

The major foods identified in this study are simi-
lar to the major foods of Pacific cod in other regions
of the North Pacific Ocean. Walleye pollock and
Pacific herring were among the predominate fish
species in stomachs of Pacific cod from Asian
waters, and the crab Chionoecetes sp. was the most
common invertebrate (Moiseev 1953). Flatfish and
the sand lance, Ammodytes sp., however, appeared
frequently in Moiseev's samples of Pacific cod
stomachs but were rare or absent in my samples.
The results of Jewett's (1978) study are in close
agreement with the results of my study: he found
fish, crab, and shrimp to be the most frequent
items in Pacific cod stomachs collected near
Kodiak, Alaska, during summer. In Jewett's study,
walleye pollock was the most common fish eaten,
and snow crab was the most common crab; Pacific
herring were rarely eaten.

Other studies have demonstrated, as did my
study, that larger codfishes become more piscivo-
rous. As the size of Atlantic cod, Gadus morhua,
increased, the diet changed from smaller inver-
tebrates to larger fish (Powles 1958; Popova 1962;
Rae 1967). Both Moiseev (1953) and Jewett (1978)
found similar trends in their investigations of
Pacific cod: cod < 50-60 cm long ate mostly crusta-
ceans; cod >60 cm primarily ate fish.

Some of the differences I found in foods of Pacific
cod in outside and inside waters may be related to
the availability of pandalid shrimp and Pacific
herring. The results of my food study appear to
reflect an increased abundance of both of these two
foods in inside waters. Data from exploratory

971

Table 4. — Mean estimated percentage volume of food in stomachs of Pacific cod. by total length of cod and gear type,
southeastern Alaskan waters, July 1977 (stomachs one-fourth full or greater!.

Outside waters

Inside waters

«60

cm

61-70

cm

>70

cm

s60

cm

61-70

cm

-70

cm

Item

Nets

Traps

Nets

Traps

Nets

Traps

Nets

Traps

Nets

Traps

Nets

Traps

Fish

80.0

10.4

31.0

26.2

69,8

37,4

68,3

19.3

672

33,5

74,2

63.3

Crab

0

588

54.2

57.8

12,4

48,3

1,7

17.5

5,2

14,5

7,9

11.8

Shrimp

10.0

6.4

8.2

3.6

2,4

3,7

30,0

42-4

17,7

339

11,1

15.7

Pandalid

0

1.7

.6

,5

,4

24

30,0

84

16,2

24 2

80

14.5

Crangonid

10.0

3.6

30

2.6

1,6

1,3

0

17.5

1,5

2,9

1,5

2

Hippolytid

0

1.1

,2

0

0

0

0

9.9

0

5,1

1,3

6

Unidentified

0

0

4,4

.5

,4

0

0

6.6

0

17

,3

.4

Gammarid amphipods

5.0

8.8

.6

2.8

0

9,7

0

5.2

0

64

0

1.5

Mollusks

Cephalopods

0

2.9

1.0

.3

.2

.3

0

3.0

96

45

46

3.5

Other mollusks

0

.8

0

1-7

.7

3

0

6,0

3

23

1,3

9

Polychaetes

0

5.1

3.4

38

5.5

3

0

0

0

2,0

,1

0

Other foods and

unidentified

5.0

6.8

16

3.8

9,0

0

0

6.6

0

29

8

3.3

Cod caught (no.)

1

46

25

53

47

15

3

40

24

91

47

47

Mean total length (cm)

44.0

52 4

65.4

65.4

78,8

73,7

58.3

55,2

66,9

65.5

76,4

76,7

trawling surveys indicate pandalid shrimp are
very low in abundance in outside waters (Schae-
fers and Smith 1954; Hitz and Rathjen 1965;
Ronholt et al.^). From 1969 to 1975, no pandalid
shrimp were commercially landed in this area
(Ronholt et al. footnote 1). However, in the inside
waters of southeastern Alaska around Petersburg,
near the southern portion of my sample area, pan-
dalid shrimp have been fished commercially since
1916 (Barr 1970). In northern inside waters, pan-
dalid shrimp have also been reported as abundant
(Ellson and Livingstone 1952). Similarly, since
commercial fishing records were first kept in the
1920's, Pacific herring have been abundant in in-
side waters south of Cape Spencer (Reid 1971). No
catches of Pacific herring have ever been reported
for outside waters north of Cape Spencer appar-
ently because of the scarcity of Pacific herring in
this area.

Acknowledgments

I thank Don Mortensen of the Northwest and
Alaska Fisheries Center Auke Bay Laboratory,
NMFS, and the crew of the NOAA Ship John N.
Cobb who collected the samples for this study, H.
Richard Carlson who provided guidance through-
out the study, Bruce Wing who aided in inverte-
brate indentification, and Lin Sonnenberg and
Evan Haynes who reviewed the manuscript.

■'Ronholt, L. L., H. H. Shippen, and E. S. Brown. 1976. An
assessment of the demersal fish and invertebrate resources of the
northeastern Gulf of Alaska. Yakutat Bay to Cape Cleare, May-
August 1975. NEGOA Annual Report, 183 p. Processed rep.
Northwest Fisheries Center, Natl. Mar. Fish. Serv., NOAA, 2725
Montlake Boulevard E., Seattle, WA 98112.

Literature Cited

ALVERSON, D. L., A. T. PRUTER, AND L. L. RONHOLT.

1964. A study of demersal fishes and fisheries of the north-
eastern Pacific Ocean. H.R. MacMillan Lect. Fish., Inst.
Fish., Univ. B.C., Vancouver, 190 p.

BARR, L.

1970. Alaska's fishery resources. The shrimps. U.S. Fish
Wildl. Serv., Fish. Leafl. 631, 10 p.

ELLSON, J. G., AND R. LIVINGSTONE, JR.

1952. The John N. Cobb's shellfish explorations in certain
southeastern Alaskan waters, spring 1951. Commer
Fish. Rev 14(4):l-20.

HiTz, c. R., AND W. F Rathjen.

1965. Bottom trawling surveys of the northeastern Gulf
of Alaska (summer and fall of 1961 and spring of
1962). Commer. Fish. Rev 27(9):1-15.

JEWETT, S. C.

1978. Summer food of the Pacific cod, Gadus mac-

rocephalus, near Kodiak Island, Alaska. Fish. Bull.,

U.S. 76:700-706.
MOISEEV, P A.

1953. Cod and flounders of far-eastern waters. Izv.
Tikhookean. Nauchno-issled. Inst. Rybn. Khoz. Okeanogr.
40:1-287. (Translated from Russ., 1956, Fish. Res. Board
Can. Transl. Ser. 119, Pt. I, 241 p.)

POPOVA, O. A.

1962. Some data on the feeding of cod in the Newfoundland
area of the Northwest Atlantic. In Yu. Yu. Marti (editor),
Soviet fishery investigations in the northwest Atlantic, p.
228-248. (Translated from Russ. by Isr. Program Sci.
Transl., 1963, 370 p.; available U.S. Dep. Commer, Natl.
Tech. Inf. Serv, Springfield, Va., as OTS 63-11102.)

POWLES, P M.

1958. Studies of reproduction and feeding of Atlantic cod
{Gadus callarias L.) in the southwestern Gulf of St. Law-
rence. J. Fish. Res. Board Can. 15:1383-1402.

RAE,B. B.

1967. The food of cod in the North Sea and on the west of
Scotland grounds. Dep. Agric. Fish. Scotl. Mar. Res.
1967(1), 68 p.

REID, G. M.

1971. Age composition, weight, length, and sex of herring,

972

Clupea pallasi. used for reduction in Alaska, 1929-
66. U.S. Dep. Commer, NOAA Tech. Rep. NMFS
SSRF-634, 25 p.
SCHAEFERS. E. A., AND K. A. SMITH.

1954. Shellfish explorations in the Yakutat Bay area,
Alaska, by the John N. Cobb, spring 1953. Commer.
Fish. Rev. 16(3):1-12.

David M. Clausen

Northwest and Alaska Fisheries Center Auke Bay Laboratory

National Marine Fisheries Service, NOAA

P.O. Box 155

Auke Bay, AK 99821

USE OF GRIFFIN'S YIELD MODEL FOR
THE GULF OF MEXICO SHRIMP FISHERY*

For analyzing the harvest of the Gulf of Mexico
shrimp fishery, Griffin et al. (1976) have developed
an equation that relates shrimp yield to freshwa-
ter discharge of the Mississippi River and fishing
effort of Gulf shrimp vessels. The yield equation
(referred to as Griffin's equation) is a modified
Spillman production function (Heady and Dillon
1972). The Spillman function had its origin in ag-
riculture where it was derived to predict the re-
sults of fertilizer experiments on tobacco yield in
North Carolina. An important feature of the func-
tion is that it allows for environmental consider-
ations in predicting yield. The modified form of the
equation proposed by Griffin et al. (1976) is:

y = /3o^'Mi-^f)

(1)

where Y = yield of shrimp (million pounds),
D = average daily discharge of the
Mississippi River during the
months that shrimp are in their
nursery grounds (cubic feet per
second),
E = vessel effort (thousand units),
)8q, /3j, /Sg = parameters to be estimated from
data of the fishery.

The coefficients of Equation (1) were estimated
from individual vessel records collected by the
National Marine Fisheries Service and from mea-

surements of water flow rates on the Mississippi
River for the years 1962-74. According to Griffin
and Beattie (1978), the fit was quite good, namely:
"All estimated coefficients were significant at the
1% level; R^ was 78.5; and the Durbin-Watson
statistic was 2.25. The simple correlation
coefficient between catch and effort was 0.64 and
between catch and discharge was -0.63."

Griffin's equation has found numerous uses in
the Gulf shrimp management literature. Griffin
and Beattie (1978) used the equation to estimate
the impact of effort reallocation as a result of Mex-
ican extended jurisdiction; the Gulf Coast Re-
search Laboratory at Ocean Springs, Miss.,
(Christmas and Etzold 1977) used the equation for
similar purposes; and the Center for Wetland Re-
sources, Louisiana State University^ used the
equation to estimate maximum sustainable yield
for management considerations.

Despite the extensive usage, users have not
critically reviewed Griffin's equation. Such a re-
view is necessary because of the large-scale poten-
tial impact of proposed shrimp management
plans. In view of this need, therefore, I subjected
Griffin's equation to such a review.

The review consisted of two tests relevant to the
usage of Griffin's equation in management deci-
sions. In the first test, I estimated the error in
expected yield introduced by the typical user who
ignored the fact that the independent vari-
ables— effort and river discharge — have var-
iances. For convenience, this was termed the "ex-
pected value test." In the second test, I depicted the
error in yield estimate that would result from mis-
specification of model parameter estimates. For
convenience, this test was termed the "sensitivity
test."

The results were mixed. The expected value test
produced a large absolute error in expected yield
of shrimp. However, when compared with expected
yield, the error was proportionally small. The sen-
sitivity test produced some startling results. Yield
turned out to be very significantly sensitive to a
fixed model parameter whose constancy was con-
ceptually questionable in the first place. This ex-
treme sensitivity of yield raises questions regard-
ing the reliability of Griffin's equation as a shrimp
management tool.

Each test is discussed below in detail.

'Contribution No. 80-54M, Southeast Fisheries Center,
National Marine Fisheries Service, NOAA, Miami, Fla.

^The original equation was estimated by Griffin et al. (1976) in
nonmetric units and its nonlinear nature excludes conversion to
metric units.

^Louisiana State University. 1979. Draft fishery- manage-
ment plan for shrimp fisherv-. Prepared by Center for Wetland
Resources, L.S.U., Baton Rouge, 226 p.

FISHERY BULLETIN: VOL. 78. NO. 4, 1981.

973

Expected Value of Yield

Most users of Griffin's equation (Griffin et al.
1976; Louisiana State University (footnote 3) es-
timated yield by using the mean (or expected)
value of the independent variables, discharge and
effort. Yet it can easily be shown that, for a general
two- variable function, ifx,y are random variables
and g an arbitrary twice differentiable function of
X, y such that:

z=gix,y) (2)

then E[z] =E\g{x,y)] ^ g(E[xl Ely]) (3)

or if E[x] = iq^ and E\y] 7]y

then E[z]-^g(r]^,r]y)

(4)

where Ei ) denotes expectation of random vari-
able.

Hence, yield estimates obtained using mean
values as in Equation (4) are generally not accu-
rate. It may be shown (Papoulis 1965) that Equa-
tion (4) may be correctly approximated as:

To compute the estimated yield and its variance
we required the first, second, and cross partial
derivatives of the yield equation. The derivation
was tedious and hence not reproduced here. By the
necessary partial differentiation of Equation (1)
we could write:

ay

15 ' "^''"^

32-1

(1-^0

dD

02-2

dY
dE

bDdE

-doD^- i3f log J,

-/3o£>^^/3f (log./?,)'

-U^D^'-'' |3f log^/3,

(9)

2 = ^2^2-1) l^oD'''^ (l-i3f ) (10)

(11)

(12)
(13)

Griffin et al. (1976) have estimated the equation
parameters to be: Po = 6593, A = 0.995701, and fi^
= -0.60134.

^l^] =^(r?.,r?j4(B ol .0 ol .|^ cov(.,y)}

2 ^dx

dy

bxdy

(5)

where the o^'s are the variances of variables x,y. The variance of the estimate is as follows:

o:

^dx^

^"^^(^

^dx by'

cov(x,y) +

(6)

Thus, Equation (4) is only a first approximation,
with Equation (5) providing the second term. Ad-
ditional terms may be obtained by continuing
Taylor's series expansion ofg{x,y) around^(T7^, 17^).
For the purpose of the test, however, the second
term was sufficient.

For Griffin's equation the independent (random)
variables were river discharge D and vessel effort
E. So, the expected value of the dependent (ran-
dom) variable yield Y could be expressed as:

Expected yield of shrimp can be determined by
using the means, variances, and covariances of
river discharge and effort. Following the approach
of one user of Griffin's equation (Christmas and
Etzold 1977), yield was estimated by using mean
values of variables for the years 1970-74. A listing
of the data and numerical values of means and
covariances are given in Table 1.

E[Y] = y(r7^,r7^)4{0

^D

2 9'r

Ve

2 o ^^Y

^D'^E

COX {D,E)). (7)

Similarly, the variance of the estimate was given by:

o

^D

D

^dE'

Ve

a| +

^dD dE'

rjij ,Ve

co\{D,E)

(8)

974

Table l. — Data, including mean and variance of Mississippi
River discharge i thousand cubic feet per second) at Tarbert
Landing, Mi.ss.. and Gulf of Mexico commercial shrimp effort
ithousands of davsi from U.S. waters bv vessel, 1970-74.'

s(y|« ^ ^°^'^>

D

scharge

Mean Jan.-

Year

Jan.

Feb

Mar

Apr

May

May

Effort

1970

448

430

529

652

852

582.2

249 1

1971

482

481

865

449

431

541.6

2590

1972

560

427

602

536

749

574.8

282 6

1973

842

857

779

1.284

1,373

1,027

2697

1974

971

1,083

828

792

576

850.00

243.6

Averages

r,D =

715.1

VE

= 260.8

SD

o-D =

213.9

<tE

= 15 74

Covariance

mD. e =

-141.92

'Sources: U.S Army Corps of Engineers, Stages and discharges of the
Mississippi River and its tributaries and other watersheds in New Orleans
District. U.S. Army Engineer District. New Orleans Corps of Engineers,
Louisiana, and Christmas and Etzold 1977:28).

Appropriate insertion of these numerical values
in Equation (7) produced the following estimates
of yield:

EiY) = 89.09 million lb, a^ = 247.72.

Ignoring the variances and covariances, as most
users of Griffin's equation do, we computed the
corresponding estimated yield to be: ,E(y) = 85.48
million lb.

The expected value test indicated that an abso-
lute error of 3.6 million lb of shrimp is introduced
by ignoring the variances and covariances of the
independent variables. While an error of 3.6 mil-
lion lb is large in absolute terms, its significance is
diminished to 4% in relative terms. Furthermore,
although 4% error is sizable, it is probably in-
sufficient to alter economic management conclu-
sions. We may conclude, therefore, that the ex-
pected value test, if applied to other applications of
Griffin's equation, would not drastically alter
management conclusions.

Parameter Sensitivity Test

Griffin's equation contains three parameters,
each with its own significance and sensitivity. (Ab-
solute and relative definitions of sensitivity can be
found in Tomovic and Vukobratovic (1972) and
Truxal (1972).) In assessing the sensitivity of yield
to these parameters, I will relate proportional
changes in parameter values to proportional
changes in yield. (For this application of the sen-
sitivity test, the relative measure of sensitivity is
preferred because the results obtained are inde-
pendent of the units of measure used for effort and
discharge.) Mathematically, the sensitivity S of
yield to parameter ^ may be expressed as:

^ dYlY

9 (log J) a/3//3

dYP
d(i Y

= tf-T7. (14)

In considering parameter ^o, note that it is the
dimensioned constant relating effort, discharge,
and yield. The sensitivity of yield to fio is ex-
pressed:

S(r|/3o) = 1.0

(15)

In Equation (15), the sensitivity is small and
constant. Thus, small errors in misspecification of
/^o will not significantly affect yield estimates.

Parameter (32 governs the relationship between
discharge of the Mississippi River and yield. Its
sensitivity can be expressed as:

SiY\(i2) = 132 log,/)

(16)

The relationship is clearly linear and the sen-
sitivity relatively small (Figure 1). Again, the im-
plication being that misspecification of /Jj or fu-
ture changes in its value would have small impact
on yield.

Figure l.— Sensitivity (S) of yield to parameter /Sa; i.e,, the
percentage change in yield corresponding to a l'7c change in Az.

975

The parameter ySj is a little more difficult to
understand. In the context of the model, fSi is the
constant that relates marginal yield correspond-
ing to two successive units of effort. By appropriate
manipulation of Equation (1) we can derive the
following expression:

i3, =

ay
dE

ay

dE

E+ 1

(17)

Rational physical arguments may be used to
show that ^1 is bounded by 0 and 1 (0<yQi <1). The
law of diminishing returns provides the simplest
argument, although there are others. Never-
theless, whatever the interpretation of yQi, sen-
sitivity of yield to the parameter can be expressed

as:

s(y\(3,) =

-E

^:'-l

(18)

Since we have already established 0</3i<l,
Equation (18) can be sketched as shown in Figure
2.

Yield is not very sensitive to ^i for small values
of ^i( ~0). The sensitivity increases hyperbolically,
however, asymptotically approaching infinity as
^1 approaches the value unity.

Griffin's estimate of ^Sj is 0.995701. This is about
as close as one could get to the most sensitive
region in Figure 2. For a value of efforts of 260.8,
the sensitivity is -125.63. Thus any small
misspecification of /3i would produce very large
errors in yield estimates.

It has already been shown that the parameter /3i
is related to marginal product of effort. At this
point I question the assumption of fii as being a
constant parameter. The marginal product of ef-
fort in any fishery is intimately related to stock
and fleet characteristics. Realistically, one would
expect marginal product and therefore its ratio to
vary over time. Even if one could consider f3i to be a
constant over 1 yr, it would most certainly change
over the course of the 12 yr that were used to
estimate the given value (Griffin et al. 1976). Since
I have already shown ^i to be the most sensitive
parameter of Griffin's equation, any misspecifica-
tion or future change of (S^ would have enormous
consequences on yield estimates.

Thus a user of Griffin's equation, who assumes a
value of (Si based on previous estimates of stock,

976

125.63--

FlGURE 2.— Sensitivity (S) of yield to parameter /i,; i.e., the
percentage change in yield corresponding to a 1% change in /S,.

effort, etc., may make incorrect predictions in the
face of changing conditions. This observation se-
verely limits the applicability of Griffin's equation
for management purposes.

Acknowledgments

I wish to express my thanks to Lynn M. Pulos
who carefully critiqued several drafts of this paper.
Her patience is much appreciated.

Literature Cited

Christmas, j. y, and d. j. etzold (editors).

1977. The shrimp fishery of the Gulf of Mexico United
States: A regional management plan. Gulf Coast Res.
Lab., Tech. Rep. Ser. 2, 128 p.

Griffin, w. l., and b. r. Beattie.

1978. Economic impact of Mexico's 200-mile offshore fish-
ing zone on the United States Gulf of Mexico shrimp
fishery. Land Econ. 54:27-38.

Griffin, w. l., r. d. lacewell, and J. R Nichols.

1976. Optimum effort and rent distribution in the Gulf of
Mexico shrimp fishery. Am. J. Agric. Econ. 58:644-652.

HEADY. E. O.. AND. J. L. DILLON.

1972. Agricultural production functions. Iowa State Univ.
Press. Ames, 667 p.

papoulis, a.

1965. Probability, random variables and stochastic pro-
cesses. McGraw-Hill. N.Y., 583 p.
TOMOVIC. R.. AND M. VUKOBRATOVIC.

1972. General sensitivity theory. .■Xm. Elsevier, N.Y., 258 p.
TRUX.\L. J.G.

1972. Introductory systems engineering. McGraw Hi
N.Y., 596 p.

Southeast Fisheries Center Miami Laboratory
National Marine Fisheries Service, NOAA
75 Virginia Beach Drive. Miami, Fla.
Present address: Department ofEngineeri
Stanford University, Stanford, CA 94305

from preserved fish. Ovaries were histologically
classified into four stages (Table 1).

Table l. — Monthly di.stribution (percent) of ovarian stages in
the yearly spawning cycle of Peprilus simillimus, September
1978-August 1979.

Regressed or Pre- Pre-

Month N regressing vitellogenic Vitellogenic spawning

ing. ivicvjraw niii.

Sept

25

100

0

0

0

Oct

18

100

0

0

0

Nov.

15

100

0

0

0

Dec.

17

53

47

0

0

ARVIND KHILNAM

Jan

21

52

43

5

0

Feb.

19

26

42

16

16

y

Mar

20

10

15

0

75

Apr.

20

5

5

0

90

May

16

44

19

0

37

June

20

95

0

0

5

-Economic Systems

July

17

100

0

0

0

Aug

24

92

8

0

0

Results

SEASONAL SPAWNING CYCLE OF

THE PACIFIC BUTTERFISH,

PEPRILUS SIMILLIMUS (STROM ATEI DAE)

There is little information on the reproductive bi-
ology of the Pacific butterfish, Peprilus simillimus ,
which ranges from Magdalena Bay, Baja Califor-
nia, to the Fraser River, British Columbia, and
occurs at depths of 9-91 m (Miller and Lea 1972). It
is commercially fished with purse seine, lampera,
and bait net (Fitch and Lavenberg 1971). In 1976,
34.18 t were taken in California (Oliphant 1979).
Fitch and Lavenberg (1971) reported spawning oc-
curs in spring and extends perhaps into July. Horn
(1970) studied the systematics and biology of the
genus Peprilus. My purpose is to describe his-
tologically the seasonal spawning cycle of the
Pacific butterfish.

Methods

Fish were collected with the use of a lampera net
between depths of 2 and 20 m from the vicinity of
Oceanside, southern California (lat. 33°10' N,
long. 117°25' W), during the period September
1978 through August 1979. Only female specimens
were examined. Fish were fixed and preserved in
10% Formalin. 1 Ovarian histological sections from
232 specimens were cut at 8 /zm and stained with
iron hematoxylin. Seasonal gonosomatic indices
(ovary weight/fish weight x 100) were calculated

'Reference to trade names does not imply endorsement by the
National Marine Fisheries Service. NOAA.

FISHERY BULLETIN: VOL. 78. NO. 4, 1981.

Ovaries were regressed ( Stage 1 ) during autumn
(September- November) and consisted of primary
oocytes <100 /u,m in diameter (Table 1). Gonosomat-
ic indices (Figure 1) were reduced at this time.
The first signs of ovarian activity for the new
spawning cycle were noted during December. This
was determined by an abundance of previtel-
logenic (vacuolated) (Stage 2) oocytes (130-200
fjLTn) which typically appear before yolk deposition
begins (Table 1). Enlarging (Stage 3) vitellogenic
oocytes (yolk deposition in progress) were first
noted in January. The first ripe (prespawning or
gravid) (Stage 4) females with ovaries containing

12.0

o
o

>-

Q
O

m

>-
cr
<
>
o

10.0

8.0

SEP OCT NOV DEC JAN FEB MAR APR MAY JUN JUL AUG
1978 1979

Figure l. — Seasonal gonosomatic indices for Peprilus similli-
mus. Vertical line = range: horizontal line = mean: rectangle =
95*7^ confidence interval. Sample size above each month.

977

mature yolk-filled oocytes O400 /xm) were col-
lected in February. Since only a small fraction of
my February sample was gravid, the spawning
period for the majority of the population under
study appeared to encompass March-May (Table
1). The smallest reproductively active female mea-
sured 114 mm standard length ( SL); the largest 172
mm SL. Gonosomatic indices were at maximum
sizes in March (Figure 1) and a progressive de-
crease was indicated through spring with minimal
sizes occurring by June. A May increase in the
incidences of follicular atresia indicated the end of
spawning was near. Atretic oocytes are most
abundant near the termination of spawning when
oocytes that initiated but failed to complete yolk
deposition degenerate.

My observation of follicles in various stages of
yolk deposition during ,the spawning period
suggests that successive batches of eggs are ma-
tured and spawned. The number of spawnings per
individual per season are not known, but the pres-
ence of a mode of mature oocytes (imminent
spawning), postovulatory follicles (transitory
remnant of the follicle wall from a recent spawn-
ing), and a vitellogenic oocyte mode for a sub-
sequent spawning indicates that females are ca-
pable of spavming more than once per season.
Postovulatory follicles were similar in morphol-
ogy to those reported in other teleosts (Hunter and
Goldberg 1980).

Discussion

Peprilus simillimus undergoes a distinctly
seasonal spawning cycle characterized by an
abrupt increase in ovarian sizes during late
winter with spawning essentially completed by
the end of spring. Fitch and Lavenberg (1971) re-
ported that spawning may extend into July. Horn
(1970) similarly reported that spawning in P.
triacanthus, P. burti, P. paru, and P. simillimus
generally occurs in spring and early summer. This
contracted type of cycle differs from that of some
southern California fishes that have a consider-
ably longer spawning period. Goldberg (1980) re-
ported that gravid female Chitonotus pugetensis
and Icelinus quadriceriatus (both Cottidae) were
found throughout the year with maximum num-
bers in winter and early spring. The northern an-
chovy, Engraulis mordax, may have the ability to
spawn all year but is likely limited by food avail-
ability and energy reserves (Brewer 1978; Hunter
and Goldberg 1980).

The P. simillimus spawning cycle is more rem-
iniscent of northern fishes (Quasim 1956), which
have a short reproductive period (generally
winter-early spring) with a single spawning. The
multiple spawnings over a brief period exhibited
by P. simillimus may represent a compromise be-
tween a short reproductive period with a single
spawning (characteristic of high latitude fishest
and a long reproductive period with repeated
spawnings typical of tropical fishes (Nikolsky
1963).

Acknowledgments

I am grateful to Edward DeMartini and Robert
Fountain (University of California at Santa Bar-
bara) for assistance in obtaining specimens. Trang
Nguyen assisted with histological preparations.
This study was aided by a Whittier College faculty
research grant.

Literature Cited

Brewer. G. D.

1978, Reproduction and spawning of the northern anchovy,
Engraulis mordax. in San Pedro Bay, California. Calif.
Fish Game 64:175-184.

FITCH. J. E., AND R. J. Lavenberg.

1971. Marine food and game fishes of California. Univ.
Calif. Press. Berkeley, 179 p.

GOLDBERG, S. R.

1980. Seasonal spawning cycles oftwo marine cottid fishes,
Chitonotus pugetensis and Icelinus quadriceriatus from
southern California. Bull. Mar Sci. 30:131-135.
HORN, M. H.

1970. Systematics and biology of the stromateid fishes of
the genus Pepn/ws. Bull. Mus. Comp.Zool. 140:165-261.
HUNTER, J. R., AND S. R. GOLDBERG.

1980. Spawning incidence and batch fecundity in northern
anchovy, Engraulis mordax. Fish. Bull., U.S. 77:641-
652.
MILLER, D. J., AND R. N. LEA.

1972. Guide to the coastal marine fishes of California.
Calif. Dep. Fish Game, Fish Bull. 157, 235 p.

NIKOLSKY, G. Y

1963. The ecology of fishes. Acad. Press, N.Y., 352 p.
OLIPHANT. M. S.

1979. Califoniia marine fish landings for 1976. Calif.
Dep. Fish Game, Fish Bull. 170, 56 p.

Quasim, S. z.

1956. Time and duration of the spawning season in some
marine teleosts in relation to their distribution. J. Cons.

21:144-154.

STEPHEN R. GOLDBERG

Department of Biology
Whittier College
Whittier. CA 90608

978

EFFECTS OF INJURIES ON SPINY LOBSTER,

PANULIRUS ARGUS, AND IMPLICATIONS

FOR FISHERY MANAGEMENT

The spiny lobster, Panulirus argus, supports im-
portant commercial and recreational fisheries
throughout its range from Bermuda to Brazil. Its
ecology- and physiology are typical of a number of
other commercially important palinurid species,
which collectively have pantropic distributions
(Phillips and Cobb 1977).

A variety of decapod crustacean responses to
injuries, primarily limb loss, have been recorded.
Aiken 11977) summarized a number of studies
conducted in laboratories, some of which found
that limb loss greatly accelerated ecdysis. Other
observers noted limb loss resulted in reduced
growth rates (Chittleborough 1975; Ford 1977;
Savage and Sullivan 1978). This paper reports the
effects of injuries on growth rates of wild juvenile
spiny lobsters, P. argus, in Florida and discusses
the implications of these effects on P. argus biol-
ogy and its fishery.

Spiny lobsters (Palinuridae) have complex life
cycles. Larval, early juvenile, and adult stages of
the spiny lobster in Florida, P. argus, are
ecologically dissimilar and are found separately in
relatively discrete habitats. The planktonic phyl-
losoma larvae spend 5 to 9 mo in the open ocean
before metamorphosing into actively swimming
postlarvae, called pueruli (Lewis 1951). Pueruli
swim into shallow coastal waters where they set-
tle onto the bottom, assuming the benthic exis-
tence they will follow the rest of their lives. Post-
larval and small juvenile spiny lobsters are found
scattered throughout seagrass beds, particularly
in shallow inshore areas like Biscayne Bay. Larger
juveniles concentrate around rocky outcrops,
sponges, and groups of sea urchins for shelter dur-
ing the day (Khandker 1964; Davis 1971; Berrill
1975). They forage nightly on adjacent grassbeds
and open sand areas for small mollusks, echinoids,
and crustaceans (Herrnkind et al. 1975). Mature
lobsters are generally associated with coral reefs,
or other hard bottom, offshore to depths >150 m.
The transition from inshore juvenile habitat to
habitat offshore is sometimes accomplished by
spectacular mass migrations, marked by long
queues of lobsters (Herrnkind and Cummings
1964; Kanciruk and Herrnkind 1978).

The fishing season for P. argus in Florida ex-
tends slightly more than 8 mo from late July
through March, with a special 2-d sport fishing

season 5 d prior to the beginning of the regular
sport and commercial season (Florida Statute
370.14). Recreational diving activity directed at
spiny lobster harvest is particularly intense in
nearshore areas during the first 6 to 8 wk of each
season (Austin 1976). There are also over 1,000
commercial trappers, fishing up to 2,000 traps
each, in the fishery (Beardsley et al. 1975).

Methods

At weekly or monthly intervals during 1976 and
1977, spiny lobsters were captured in southern
Biscayne Bay, Fla., by hand, bully net, or tail
snare and marked with spaghetti tags. The details
and efficacy of this tagging procedure were re-
ported by Davis (1978). Data on size (as carapace
length, CL), injuries, molt condition, location, and
water temperature were recorded. Injuries were
recorded as the number of missing legs or anten-
nae, or damage to the abdomen, cephalothorax, or
supraorbital horns.

Grovvi:h of spiny lobsters takes place as the re-
sult of a series of molts, during which discontinu-
ous size changes occur. The rate of growth is de-
pendent on both magnitude of change in size with
each molt (molt increment) and the length of the
intermolt period. In this study, growth rate was
expressed as change in carapace length per week,
since nearly all observations of marked lobsters
were made at weekly intervals. To reduce the var-
iability inherent in measuring discontinuous
changes in carapace length that resulted from
random observations of growi:h during the molting
cycle, all changes in size were summed over each
class of observations (i.e., wdnter, summer, injured,
or uninjured) and expressed as rates per week.

Results

A total of 7,643 P. argus were examined from
February 1976 to December 1977. They ranged
from 15 to 101 mm CL, with a mean of 60.7 mm CL
(Table 1). Mean monthly water temperatures var-
ied from 16° to 32° C.

Observations of growth were made for 844 time
intervals, ranging from 1 to 82 wk (mean 20 wk),
on 534 individual lobsters in the wild, ranging
from 38 to 83 mm CL. Carapace length mea-
surements were replicated by independent obser-
vers on the same day for 153 lobsters during the
22-mo tagging period to evaluate the precision of
the carapace length measurements by various

FISHERY BULLETIN: VOL. 78. NO. 4, 1981.

979

Table l. — Monthly summary of size, molting activity, and
condition of spiny lobsters, and water temperatures in eastern
Biscayne Bay, Fla., 1976-77.

Mean

Number

of
lobsters

S

ze (mm

CL)

Percentage
Molting Injured

water
temp
(°C)

Month

Min

Max

Mean

1976:

Feb.

1.247

34

84

56 1

8

53

16

Mar.

353

33

83

56.4

9

51

26

Apr.

464

38

86

600

12

45

25

May

362

34

79

594

12

39

27

June

340

43

87

63.2

14

46

29

July

414

15

85

61.6

8

31

31

Aug.

398

37

83

635

7

38

31

Sept.

217

40

96

63.1

6

42

30

Oct.

25

35

89

64,6

12

24

26

Dec.

139

38

85

54,7

13

42

17

1977:

Jan.

86

33

85

57,7

43

37

16

Feb.

619

30

81

55,5

11

50

18

Mar.

387

31

88

57,3

7

49

23

Apr.

272

39

80

59,2

12

47

25

May

220

39

101

61,8

17

40

26

June

268

27

85

636

26

41

28

July

322

35

86

62,1

8

35

32

Aug.

414

30

84

636

17

31

32

Sept.

454

30

97

66,9

11

29

30

Oct.

335

32

99

653

13

35

27

Nov

307

32

92

60 1

2

41

24

Total

7.643

Mean

33.6

87.4

60.7

12,8

40.3

25.7

technicians. The mean error was 0.3 mm, with a
range of -1.8 to +2.1 mm. Consequently, only
changes in carapace measurements >2.0 mm were
recorded as growth, others were considered mea-
surement errors.

Two factors appeared to affect growth rates:
water temperature and lobster condition. Growth
rate did not vary with either sex or size within the
range observed. Mean intermolt periods were es-
timated by doubling the time interval over which
SO*??^ of the lobsters observed had molted. This as-
sumed that at the time of tagging the lobsters were
randomly distributed throughout their molting
cycle (Munro 1974). This appeared reasonable
since we observed molting activity throughout the
year (Table 1), and direct observations of indi-
vidual lobsters through periodic recaptures con-
firmed the mean values obtained for the popula-
tion in this manner (Davis 1978). For example,
during winter, the percentage of tagged lobsters
that had molted increased weekly from 12% after 1
wk to 22, 31, 32, 40, 44, and 58% after 8 wk,
indicating that 50% had molted after about 7.5 wk,
resulting in a mean intermolt period of 15 wk
(Figure 1). In contrast, the mean intermolt period
during summer was only 8 wk (Table 2). The mean
intermolt period of injured lobsters was 15 wk, and
for uninjured lobsters it was 10 wk (Table 2). The
mean growth increments were estimated by exa-

980

O 0

• Uninjured —

* Injured --

• Summer —

* Winter ' --

9 11 13 15 17

Weeks

Figure l.— Comparison of molting activity as a function of
condition ( Ai and season i B) for .spiny lobsters in Biscayne Bay,
Fla.

Table 2.— Mean growth variables determined from 1,688
observations on 534 tagged juvenile spiny lobsters in Biscayne
Bay Fla., 1976-1977.

Item

Number
of growth

intervals
observed

Intermolt

period

(wk)

Observed

growth

rate

(mm CL/wk)

Water
temp

rc)

Season:

Winter
Summer
Condition:

656
146

15
8

0,31
0,75

21.1
29.1

Injured
Uninjured
All observations

465
379
844

15
10
12

0,31
0,51
0-41

(')

(')

25,7

'Not available.

mining frequency distributions of observed
changes in carapace length. Mean single molt
growth increments were significantly larger dur-
ing the summer and for uninjured lobsters than
during the winter and for injured lobsters, respec-
tively (Table 3). Effects of season and lobster con-
dition on growth rate were independent (Table 4).
Predictably, higher summer (May-October)
temperatures and longer daylight periods were
related to a greater growth rate (0.75 mm CL/wk)
than that observed during winter, November
through April (0.31 mm CL/wk). This 59% de-
crease in growth rate between summer and winter
was apparently related to the 8.0° C decrease in
mean water temperature, from 29.1° to 21.1° C, and
the increased frequency of injuries incurred dur-

Table 3. — Comparison of mean molt increments (millimeters of
change in carapace length) of juvenile spiny lobsters, in Biscayne
Bav. Fla.

Season

Conditions

Item

Summer

Winter

Injured

Uninjured

X

Sx

t. 306 df

6.0 4.7

32 3.6

7.75"

4.7
3.8

5.2
38

2.25-

••Ps0.01;-Ps0 05.

Table 4. — Two-way fixed factor ANOVA of effects of season and
spiny lobster condition as evidenced by growth rate.

Source of variation

df

SS

MS

Subgroups
A (columns; condition)
B (rows: season)
A ■ B (interaction)

Within subgroups (error)

3
1
1
1
3.784

106,50

34.60

68 67

323

28.24973

3550

34.60

68.67

3 23

744

465-

923"

0.43n.s.

Total

3.787

28.35623

•Ps0.05;-"Ps0.01.

ing the fall and winter fishing season. Growth
rates were lowest for injured lobsters during
winter and highest for uninjured animals during
summer, but injured lobsters grew faster in sum-
mer than injured ones in winter. Both of these
factors, reduced temperature and injuries, caused
increased intermolt periods and reduced molt in-
crements, which resulted in reduced growth rates
{Table 2). Change in the length of the intermolt
period was the major effect of both factors, but by
inspection of the values in Tables 2 and 3, it was
apparent that intermolt period was propor-
tionately more important for the injury-caused
reduction, whereas decreased molt increment was
proportionately more important for the season-
related growth reduction.

Discussion

The growth data presented here generally con-
form both in magnitude and character to that in
the published literature for decapod crustaceans,
but the precise effect of injuries in the wild and
definition of their origin is apparently new infor-
mation, particularly for P. argus. Estimated
growth rates for juvenile P. argus in the Carib-
bean, Florida, and Bermuda, range from 0.43 to
0.65 mm CL/wk (Smith 1951; Travis 1954;
Sutcliffe 1957; Buesa M. 1965; Witham et al. 1968;
Sweat 1968; Little 1972; Eldred et al. 1972; Ting
1973; Munro 1974; Peacock 1974; Olsen and Koblic
1975). The estimates for Biscayne Bay from this
study ranged from 0.31 to 0.75 mm CL/wk, but the
mean of 0.41 mm CL/wk was the lowest reported.
The 1977 winter in Biscayne Bay was the coldest

in the previous century (Molinari et al. 1977;
McGuirk 1978), and the Bay is already near the
northern limit of P. argus distribution. That cold
winter depressed the mean growth rate somewhat,
but another significant factor was that the Bis-
cayne Bay lobster population was the most heavily
fished by sport divers of all of those for which
growth rates were reported. The injuries resulting
from diver activity also depressed the growth rate.
It appeared that a combination of cold weather and
extremely high fishing activity caused the low
growth rate reported in this study.

Variations in growth rates of lobsters have been
attributed to several factors, the most common of
which is temperature (Crawford and De Smidt
1922; Newman and Pollock 1974; Phillips et al.
1977). Limited food (Sutcliffe 1957; Chittle-
borough 1970; Newman and Pollock 1974), shelter
(Chittleborough 1970), salinity and light (Travis
1954), and injuries (Chittleborough 1974a; Aiken
1977; Ford 1977) have also been cited as factors
affecting lobster growth (see Aiken 1977, Dall
1977, and Ford 1977 for a review of lobster growth i.
The effects of these factors are translated into
growth rate variations by changing either inter-
molt period, molt increment, or both. Most com-
monly, intermolt is shortened by warm tempera-
tures, darkness, or autotomy of appendages; and
lengthened by age, cold, or low salinity. Under
some conditions, as in this study, both changes in
molt increment and intermolt period occurred
(Mauviot and Castell 1976; Aiken 1977; Pollock
and Roscoe 1977).

While autotomy may stimulate molting, Chit-
tleborough (1974a) reported that repeated loss of
two or three legs or a large number of appendages
resulted in decreased molt increment, so the net
result was a reduction in growth rate. The results
of the current study in Biscayne Bay also clearly
demonstrated the adverse impact of injuries on
growth rates. However, our observations did not
demonstrate any proportional relationship be-
tween the degree of injury and the degree of molt
increment depression as demonstrated for shore
crabs by Kuris and Mager (1975). Most injured
lobsters in Biscayne Bay were missing one or both
antennae and one or two legs. The growth rate of
P. argus with these minor injuries, five or fewer
missing appendages, was virtually identical to the
growth rate of more seriously injured lobsters that
survived and which were missing up to nine legs
and both antennae. It appeared that even minor
losses caused a significant shift in growth pattern.

981

At the mean growth rate of 0.51 mm CL/wk
observed for uninjured lobsters, it took about 51
wk for a juvenile to reach the minimum legal size
of 76.2 mm CL from a size of 50 mm CL at age 2
(Lewis 1951; Sweat 1968). At 50 mm CL they began
to associate gregariously with the larger juveniles
in the eastern bay where they were subjected to
fishery pressure. At the injury -depressed growth
rate of 0.31 mm CL/wk, it required 84 wk to reach
legal harvest size and enter the fishery 33 wk later
than uninjured lobsters. During the additional 33
wk required to reach legal harvest size, natural
mortality from groupers and other predators un-
doubtedly eliminated significant numbers of
lobsters before they could enter the fishery. Olsen
and Koblic (1975) estimated natural mortality of
juvenile P. argus in Virgin Islands National Park
at 34.8% /yr, at that rate, about 22% (33/52 of an-
nual mortality) of the injured lobsters in Biscayne
Bay were lost to the fishery as a direct result of
their injuries. By the end of the open season, about
half of the lobsters in Biscayne Bay were missing
several legs and/or antennae. The frequency of
injured lobsters dropped through the 4-mo closed
season to about 30%, as the population molted at
least once without harrassment from fishermen
(Table 1). Less than 25% of 963 juvenile lobsters
examined from an unfished population at Dry Tor-
tugas, Fla., displayed similar injuries, which were
presumably due to encounters with natural pre-
dators, difficulties with molting, or other normal
stresses (Davis unpubl. data). Fishery induced in-
juries reduced the yield per postlarval recruit by
reducing growth rate and consequently allowing
natural mortality to occur over a significantly
longer than normal period of time.

Another aspect of injury slowed growth rates is
its effect on size of maturity. Maturity in spiny
lobsters is apparently more a Sanction of age than
size (Chittleborough 1974b). Therefore if growth
rate is significantly reduced by fishing activities
through injuries, the size of mature lobsters would
be reduced in areas of intense fishing activity. In
the light to moderately fished Dry Tortugas
fishery, the size of first maturity of female P. argus
was about 90 mm CL for most of the population ( 78
mm CL smallest ovigerous) (Davis 1975). In the
intensely fished lower keys fishery, the size of first
maturity was reported at about 80 mm CL (small-
est ovigerous 71.4 mm CL) (Warner et al. 1977).
However, while age induces onset of maturity,
female size is a major limit to fecundity. Creaser
( 1950) pointed out that a single 130 mm CL female

P. argus produced as many eggs as four 87 mm CL
females. Under the same environmental condi-
tions, a population of injury-stunted lobsters could
not produce the number of larvae that a popula-
tion of normal -sized animals would (Kanciruk and
Herrnkind 1976 ). Spawning fewer larvae may also
result in reduced genetic diversity in the P. argus
population, which would have further detrimental
consequences for the management of this valuable
resource (Miller 1979).

Intense fishing pressure on commercial concen-
trations of spiny lobsters inflicts injuries in several
ways. Recreational divers inadvertently damage
juvenile lobsters in attempting to catch associated
larger animals, and by repeatedly catching nearly
legal-sized lobsters to measure them. Florida law
permits the capture, transportation, and use of
sublegal-sized juveniles for attractors (bait) in
commercial traps (Florida Statute 370.14), and
juveniles are occasionally caught in traps along
with adults. These sources of injury to the lobsters
are all amenable to standard lobster trap fishery
management techniques. Escape vents on traps
that would allow small lobsters to leave and a
prohibition on handling and transporting juvenile
lobsters could eliminate the sources of injury from
the trapping segment of the fishery (Bowen 1971).
Nursery sanctuaries in which no fishing activity is
allowed, and regulations prohibiting the use of
hooks and spears by divers could eliminate diver
and trap induced injuries.

The response of P. argus to injuries is probably
representative of most tropical palinurids, and the
information developed here could have wide
application for fisheries management.

Acknowledgments

I would like to thank G. Y. Hendrix and J. A.
Kushlan for their assistance and encouragement,
and W F. Herrnkind and R Kanciruk for their
helpful critical review of the manuscript.

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grounds. S. Afr. Sea Fish. Branch Invest. Rep. 107:1-16.

OLSEN, D. A., AND I. G. KOBLIC.

1975. Population dynamics, ecology and behavior of spiny
lobsters, Panulirus argus, of St. John, U.S. V.I.: (II)
Growth and mortality In S. A. Earle and R. J. Lavenberg
(editors). Results of the Tektite program: coral reef inver-
tebrates and plants, p. 17-21. Nat. Hist. Mus. Los Ang.
Cty., Sci. Bull. 20.

983

Peacock, N. a.

1974. A study of the spiny lobster fishery of Antigua and
Barbuda. Proc. Gulf Caribb. Fish. Inst. 26:117-130.

PHILLIPS, B. E, N. A. Campbell, and W. A. Rea.

1977. Laboratory growth of early juveniles of the we.stem
rock lobster Pan u I irus longipescygnua. Mar Biol. ( Berl.)
39:31-39.
PHILLIPS, B. F, AND J. S. COBB (editors).

1977. Workshop on lobster and rock lobster ecology and
physiology. CSIRO Div. Fish. Oceanogr. Circ. 7, 300 p.
POLLOCK, D. E., AND M. J. ROSCOE.

1977. The growth at molting of crawfish Jasus tristam at
Tristan da Cunha, South Atlantic. J. Cons. 37:144-146.

SAVAGE, T, AND J. R. SULLIVAN.

1978. Growth and claw regeneration of the stone crab,
Menippe mercenaria . Fla. Mar. Res. Publ. 32, 23 p.

SMITH, FG.W.

1951. Caribbean spiny lobster investigations. Proc. Gulf
Caribb. Fish. Inst., 3d Annu. Sess., p. 128-134.

Sutcliffe.W. H, Jr.

1957. Observations on the growth rate of the immature
Bermuda spiny lobster, Panulirus argus. Ecology
38:526-529.

Sweat, d. e.

1968. Growth and tagging studies on Panulirus argus
(Latreille) in the Florida Keys. Fla. Board Conserv.,
Tech.Ser. 57, 30p.

TING, R. Y.

1973. Investigation on the resource potential of the spiny
lobster (Pa«(///>(/s' argus Latreille) in Puerto Rico. Con-
Irib. Agropec. Pesq. Organo Of Serv. Aux. Oper. Cent.
5(2):1-18.

TRAVIS, D. F

1954. The molting cycle of the spiny lobster, Panultrus
argus Latreille. I, Molting and growth in laboratory-
maintained individuals. Biol. Bull. (Woods Hole)
107:433-450.

Warner, R. E., C. L. Combs, and D. R. Gregory, Jr.

1977. Biological studies of the spiny lobster, Panulirus
argus (Decapoda; Palinuridae), in south Florida. Proc.
29th Annu. Sess. Gulf Caribb. Fish. Inst., p. 166-183.

wiTHAM, R., R. M. Ingle, and e. a. Joyce, jr.

1968. Physiological and ecological studies of Panulirus
argus from the St. Lucie estuary. Fla. Board Conserv.
Mar. Lab. Tech. Ser. 53, 31 p.

Gary E. Davis

U.S. National Park Service, South Florida Research Center

Everglades National Park

Homestead, Fla.

Present address: Channel Islands National Park

1699 Anchors Way Drive

Ventura, CA 93003

984

INDEX

Fishery Bullet iu Vol. 78, 1-4

ADAMS. PETER B.. "Life history patterns in marine
fishes and their consequences for fisheries management"

ADAMS. PETER B.— see LENARZ and ADAMS

"Additional records of the sculpin Psychrolutefi phrictus
in the eastern Bering Sea and off Oregon." by Ann C.
Matarese and David L. Stein

AINLEY. DAVID G,, CRAIG S. STRONG. HARRIET R.
HUBER. T JAMES LEWIS, and STEPHEN H. MOR-
RELL. "Predation by sharks on pinnipeds at the Farallon
Islands"

Alaska, southeastern
cod. Pacific

summer food

169

941

968

ALEVIZON, WILLIAM S.— see EBELING et al.

AMBLER. JULIE W. "Species of Mumdopsis (Crusta-
cea, Galatheidae) occurring off Oregon and in adjacent
waters" 13

"Ammonia concentrations in pink salmon, Oncorhyn-
chus gorbuscha, redds of Sashin Creek, southeastern
Alaska," by Stanley D. Rice and Jack E. Bailey 809

"(AnI analysis of the United States demand for fish
meal," by D. D. Huppert 267

Anchovy, northern

changes in body measurements of larvae due to hand-
ling and preservation

eye diameter 690

laboratory shrinkage 687

live body parts 686

net-treatment shrinkage 688

preser\'ation shrinkage (after net treatment! 690

direct method for estimating spawning biomass 541

effects of copper on early life historj' stages 675

egg cannibalism 811

larvae, percentage of starving in southern California
Bight

classification of larvae 481

digestive tract 479

geographical distribution 481

other organs 481

plankton volume 486

standard length 481

surface temperature 485

trunk musculature 476

reproduction off Oregon and Washington

fecundity 611

gonadal condition 606

length and age at sexual maturity 606

ovarian maturation 607

seasonal distribution 615

sex ratio 607

spawning frequency 612

respiration and depth control as possible reasons for

swimming of larvae 109

spaw-ning biomass and early life off Oregon and
Washington

comparison of northern and central subpopulations 871

egg and larva census estimates 858, 867

field procedures 857

hydrography and plankton volume 862

laboratory procedures 858

larval transport and juvenile nurseries 873

relationship with Columbia River plume 872

spawning biomass estimates 859, 868

subpopulation, northern 856

yield estimates 862, 870

Anglerfishes, ceratioid

Philippine Archipelago

Caulophrynidae 380

Caulophrynidae genera and species key 380

Centrophrynidae 395

Ceratiidae 395

Ceratiidae genera and species key 395

Ceratioidei family key 379

Diceratiidae 381

Diceratiidae genera and species key 381

Gigantactinidae 396

Himantolophidae 381

Linophrynidae 396

Linophrynidae genera and species key 396

Melanocetidae 381

Melanocetus species key 381

Oneirodes species key 382

Oneirodidae 382

Oneirodidae genera key 382

Thaumatichthyidae 395

systematics and distribution

distribution 83

evolutionary relationships 84

genus Melanocetus 70

key to species based on females 70

Melanocetus eustalus n. sp 79

Melanocetus johnsoni 71

Melanocetus murrayi 81

Melanocetus niger 78

Melanocetus polyactis 77

Melanocetus species 83

osteology of females 61

type genus Melanocetus 67

985

"Annual variability of reef-fish assemblages in kelp for-
ests off Santa Barbara, California," by Alfred W. Ebe-
ling, Ralph J. Larson, William S. Alevizon, and Richard
N. Bray 361

"Aspects of larval ecology of Squilla empusa (Crustacea,
Stomatopodai in Chesapeake Bay," by Steven G. Morgan 693

ASPER, EDWARD D.— see ODELL et al.

Atlantic Bight, Middle

Callinectes larvae, 1975-77 251

mackerel, Atlantic
spawning and fecundity 103

Atlantic Ocean
tuna, bluefin

shedding rates of plastic and metal dart tags 179

Atlantic Ocean, eastern
sailfish
size and possible origin 805

Atlantic Ocean. Middle region
mackerel, Atlantic

1978 spring recreational catch 799

Atlantic Ocean, northwest
fishes
organochlorine residues 51

Atlantic Ocean, western North
dolphin, Atlantic whitesided
southern distribution 167

Benng Sea
whale, bowhead
estimated initial population size of stock 843

Bering Sea, eastern
Psychrolutes phrlctus

additional records 169

Bikini, Marshall Islands

ciguatera sui-vey 201

BISHOR JAMES M., JAMES G. GOSSELINK, and
JAMES H. STONE, "Oxygen consumption and hemo-
lymph osmolality of brown shrimp. Penaeus aztecus" . . . 741

Blacksmith

influence of water currents and zooplankton den.sities
on daily foraging movements

distribution patterns 837

foraging at incurrent end of reef 838

foraging experiments 831, -835

physical measurements 832

plankton sampling 831

study site 830

surveys 830

zooplankton distribution patterns 839

BLAYLOCK, J, W— see PEARSON et al.

"Bomolochid copepods parasitic on the eyes of Indo-West
Pacific clupeid fishes," by Roger Cressey and Hillary
Boyle Cressey 715

BORDEN, DAVID V D.— see FOGARTY et al.

BAGLIN, RAYMOND E., JR., MARK I. FARBER, WIL-
LIAM H. LENARZ, and JOHN M. MASON, JR., "Shed-
ding rates of plastic and metal dart tags from Atlantic
bluefin tuna. Thunnus thynnus"

BAILEY JACK E.— see RICE and BAILEY

BAILEY JACK E., STANLEY D. RICE, JEROME J.
BELLA, and SIDNEY G. TAYLOR, "Effects of seeding
density of pink salmon, Oncorhynchus gorbuscha . eggs
on water chemistry, fry characteristics, and fry survival
in gravel incubators"

Bairdiella chrysoura — see Perch, silver

Balaena mysticetus — see Whale, bowhead

BAUCOM, JOE — see ODELL et al.

BEARDSLEY, GRANT L., "Size and possible origin of
sai\fish, Istiophorus platypterus, from the eastern Atlan-
tic Ocean"

BENIRSCHKE. K., MARY L. JOHNSON, and ROLF J.
BENIRSCHKE, "Is ovulation in dolphins, Stenella longi-
rostris and Stenella attenuata, always copulation-
induced?"

BENIRSCHKE, ROLF J.— see BENIRSCHKE et al.
986

179

649

805

507

Box-Jenkins models
using to forecast fishery dynamics

BRANSTETTER. STEVEN, and ROBERT L. SHIPP
"Occurrence of the finetooth shark, Carcharhinus iso-
don, off Dauphin Island, Alabama"

887

177

BRAY, RICHARD N., "Influence of water currents and
zooplankton densities on daily foraging movements of
blacksmith, Chromis punctipinnis, a planktivorous reef
fish" 829

BRAY, RICHARD N.— see EBELING et al.

BREIWICK, JEFFREY M., EDWARD D. MITCHELL,
and DOUGLAS G. CHAPMAN. "Estimated initial pop-
ulation size of the Bering Sea stock of bowhead whale,
Balaena mysticetus: An iterative method" 843

Brevoortia patronus — see Menhaden, Gulf

Brevoortia tyrannus — see Menhaden, Atlantic

BULLARD, FERN A., and JEFF COLLINS, "An im-
proved method to analyze trimethylamine in fish and the
interference of ammonia and dimethylamine" 465

Butterfish, Pacific
seasonal spawning cycle ,

977

California
food of Pacific white-sided dolphin. Ball's porpoise, and
northern fur seal off 951

California Bight, southern
anchovy, northern

{percentage of starving larvae 475

Callinectes

larvae in Middle Atlantic Bight, 1975-77

cooccurring decapods 259

distribution 255

identification 254

"Callinectes (Decapoda: Portunidae) larvae in the Middle
Atlantic Bight, 1975-77," by Peter 0. Smyth 251

Callinectes sapidus — see Crab, blue

Callorhinus ursinus — see Seal, northern fur

CAMPBELL, DOUGLAS W— see MILLER et al.

Cancer magister — see Crab, Dungeness

Cape Fear River, North Carolina
fishes, postlarval

retention in an intensively flushed tidal estuary . . . 419

Cape Hatteras, North Carolina
croaker, Atlantic

maturity, spawning, and fecundity north of 190

Carcharhinus isodon — see Shark, finetooth

Caretta caretta — see TYirtle, loggerhead

CAREY, ANDREW G., JR.— see CARNEY and CAREY

CARNEY ROBERT S.. and ANDREW G. CAREY JR.,
"Effectiveness of metering wheels for measurement of
area sampled by beam trawls" 791

CASTAGNA, MICHAEL — see KRAEUTER and
CASTAGNA

"Ceratioid anglerfishes of the Philippine Archiepelago,
with descriptions of five new species," by Theodore W
Pietsch and Jeffrey A. Seigel 379

"Changes in body measurements of larval northern
anchovy, Engraulis mordax, and other fishes due to
handling and preservation," by Gail H. Theilacker 685

CHAPMAN, DOUGLAS G.— see BREIWICK et al.

CHENG, LANNA, and ERIC SHULENBERGER, "Dis-
tribution and abundance of Halobates species ( Insecta:
Heteroptera) in the eastern tropical Pacific" 579

Chesapeake Bay
Squilla empusa

larval ecology 69.3

CHRISTENSEN, DARRYL J., and WALTER J. CLIF-
FORD, 'The 1978 spring recreational catch of Atlantic
mackerel, Scomber scombrus, off the Middle Atlantic
region" 799

Chromis punctipinnis — see Blacksmith

Ciguatera

survey at Enewetak and Bikini, Marshall Islands

Acanthuridae 240

Balistidae 243

Carcharhinidae 206

Crangidae 233

Dasyatidae 211

Holocentridae 213

Kyphosidae 232

Labridae 237

Lethrinidae 228

Lutjanidae 223

Mugilidae 215

Muraenidae 212

Orectolobidae 205

Scaridae 238

Scombridae 235

Serranidae 216

Sphyraenidae 214

Clam, hard
effects of large predators on field culture 538

CLARKE, THOMAS A., "Diets of fourteen species of
vertically migrating mesopelagic fishes in Hawaiian
waters" 619

CLAUSEN, DAVID M., "Summer food of Pacific
cod, Gadus macrocephalus, in coastal waters of south-
eastern Alaska" 968

CLIFFORD, WALTER J.— see CHRISTENSEN and
CLIFFORD

Clupeid fishes
Pacific. Indo-West

bomolochid copepods parasitic on eyes 715

Cod, Pacific
Alaska, southeastern

summer food 968

larval development in northeast Pacific Ocean

compared with Pacific tomcod 923

COE, JAMES M., and WARREN E. STUNTZ, "Passive
behavior by the spotted dolphin, Stenella attenuata, in
tuna purse seine nets" 535

COLLINS, JEFF— see BULLARD and COLLINS

Columbia River

transportation of smolts

salmon, chinook 491

steelhead ^91

"Comparison of sampling devices for the juvenile blue

987

crab, Callinectes sapidus" by Robert E. Miller, Douglas

W, Campbell, and Pamela J. Lunsford 196

Copepods, bomolochid

parasitic on eyes of Indo-West Pacific clupeid fishes

Pseudorbitacolax fimhriatus 716

Pseudorbitacolax nudus 724

Pseudorbitacolax Pillai 1971 715

Pseudorbitacolax varunae ( Bennet 1966) 720

Pumlliopes jonesi ( Bennet 1967) 729

Pumiliopes opisthopteri Shen 1957 729

Pumilwpes Shen 1957 729

Pumiliopes squamosus Cressey and Boyle 1973 .... 730

Pumiliopsis Pillai 1967 724

P(/wi7(ops/sp/a«^w.s Cressey and Boyle 1973 726

Pumiliopsis sardinellae (Bennet 1964) 726

Copper
effects of an early life history stages of northern

anchovy 675

CORNELL, LANNY H.— see ODELL et al.

"Depth distribution and seasonal and die! movements of
ratfish, Hydrolagus colliei, in Puget Sound, Washing-
ton," by Thomas R Quinn, Bruce S. Miller, and R. Craig
Wingert 816

"Descriptions of larval silver perch, Bairdiella chry-
soura, banded drum, Larimus fasciatus, and star drum,
S/e////e/- /a«ceo/a/(/.s (Sciaenidae)," by Howard Powles ,. 119

"Detection of petroleum hydrocarbons by the Dungeness
crab. Cancer magister" by Walter H. Pearson, Peter C.
Sugarman, Dana L. Woodruff, J. W. Blaylock, and Bori
L. 011a 821

"Development and structure of fins and fin supports in
dolphin fishes Coryphaena hippurus and Coryphaena
e^i/zse/is (Coryphaenidae)," by Thomas Potthoff 277

"Development of larval smooth flounder, Liopsetta put-
nami, with a redescription of development of winter
flounder, Pseudopleuronectes americanus (Family
Pleuronectidae)," by Wayne A. Laroche 897

Coryphaena equiselis

development and structure of fins and fin supports . . . 277

Coryphaena hippurus

development and structure of fins and fin supports . . . 277

Crab, blue
sampling devices for juvenile, comparison 196

Crab, Dungeness
petroleum hydrocarbon detection by

chemosensory threshold determination 822

composition of water soluble fraction 823

detection thresholds 823

experimental solutions 822

CRESSEY, HILLARY BOYLE — see CRESSEY and
CRESSEY

CRESSEY ROGER, and HILLARY BOYLE CRESSEY,
"Bomolochid copepods parasitic on the eyes of Indo-West
Pacific clupeid fishes" 715

Croaker, Atlantic
Cape Fear River, North Carolina

retention of postlarval in tidal estuary 419

maturity, spawning, and fecundity north of Cape
Hatteras, North Carolina 190

"Daily time of spawning of 12 fishes in the Peconic
Bays, New York," by Steven P Ferraro 455

Dauphin Island, Alabama
shark, finetooth
occurrence off 177

D.^IS, GARY E., "Effects of injuries on spiny lobster,
Panulirus argus, and implications for fishery manage-
ment" 979

988

"Diel and seasonal variation in abundance and diversity
of shallow-water fish populations in Morrow Bay, Cali-
fornia," by Michael H. Horn 759

"Diets of fourteen species of vertically migrating meso-
pelagic fishes in Hawaiian waters," by Thomas A. Clarke 619

"(A) direct method for estimating northern anchovy,
Engraulis mordax, spawning biomass," by Keith Parker 541

"Distribution and abundance of Halobates species
(Insecta: Heteroptera) in the eastern tropical Pacific,"
by Lanna Cheng and Eric Shulenberger 579

Dolphin, Atlantic whitesided
Atlantic Ocean, western North

southern distribution 167

Dolphin, bottlenose
occurrence, movements, and distribution in southern
Texas 593

Dolphin, Pacific white-sided
food of, off California and Washington

prey distribution 955

prey size 957

prey species 955

stomach capacity of predators 955

Dolphin, spinner

is ovulation always copulation-induced?

early pregnancy 512

immature females 508

lactating females 518

late pregnancy 515

mature females 509

nonpregnant animals with corpus luteum 518

observations on mass stranding, west coast of Florida

circumstances 353

morphology, external 358

necropsy 355

physical maturity 358

productive seasonality 357

reproductive data 355

weights 360

Dolphin, spotted

is ovulation always copulation-induced?

early pregnancy 512

immature females 508

lactating females 518

late pregnancy 515

mature females 509

nonpregnant animals with corpus luteum 518

passive behavior in tuna purse seine nets 535

Dolphin fishes
development and structure of fins and fin supports

anal fin 290

anal fin pterygiophores 291

caudal fin 295

caudal fin supports 296

dorsal fin 278

dorsal fin pterygiophores 281

pectoral fin and supports 300

pelvic fin and supports 304

vertebral column 278

Di-um. banded

comparison with earlier descriptions 133

comparison with other larval Sciaenidae 134

description 125

spawning seasons and areas 133

Dium, star

comparison with earlier descriptions 133

comparison with other larval Sciaenidae 134

description 129

spawning seasons and areas 134

DUNN. JEAN R.— see MATARESE et al.

DUNN, JEAN R.— see RICHARDSON et al.

DURBIN, ANN G., EDWARD G. DURBIN, PETER G.
VERITY, and THOMAS J. SMAYDA, "Voluntary^ swim-
ming speeds and respiration rates of a filter-feeding
planktivore, the Atlantic menhaden, Brevoortia tyran-
nus ( Pisces: Clupeidae)"

DURBIN, EDWARD G.— see DURBIN et al.

"Early life history of Pacific mackerel, Scomber ja-
ponicus:' by John R. Hunter and Carol A. Kimbrell

EBEL, WESLEY J., "Transporation of chinook salmon,
Oncorhynchus tshawytscha, and steelhead, Salmo
gairdneri, smolts in the Columbia River and effects on
adult returns"

EBELING, ALFRED W, RALPH J. LARSON, WILLIAM
S. ALEVIZON, and RICHARD N. BRAY, "Annual vari-
ability of reef-fish assemblages in kelp forests off Santa
Barbara, California"

"Effect of zinc on fin regeneration in the mummichog,
Fundulus heteroclitus. and its interaction with methyl-
mercurjC by Peddrick Weis and Judith Shulman Weis .

163

877

89

491

"Effectiveness of metering wheels for measurement of
area sampled by beam trawls," by Robert S. Carney and
Andrew G. Carey, Jr. 791

"Effects of copper on early life history stages of northern
anchovy, Engraulis mordax" by D. W. Rice, Jr., F. L.
Harrison, and A. Jearld, Jr 675

"Effects of injuries on spiny lobster, Panulirus argus, and
implications for fishery management," by Gary E. Davis

979

"Effects of large predators on the field culture of the
hard clam, Mercenaria mercenaria" by John N. Kraeuter
and Michael Castagna 538

"Effects of seeding density of pink salmon, Oncorhyn-
chus gorbuscha, eggs on water chemistry, fry character-
istics, and fry survival in gravel incubators," by Jack
E. Bailey, Stanley D. Rice, Jerome J. Bella, and Sidney
G. Tavlor

"Egg and larval development of the spot, Leiostomus
xanthurus (Sciaenidae)," by Allj-n B. Powell and Her-
bert R. Gordy

"Egg cannibalism in the northern anchovy, Engraulis
mordax" by John R. Hunter and Carol A. Kimbrell

"Eggs and larvae of butter sole, Isopsetta isolepis
(Pleuronectidae), off Oregon and Washington," by Sally
L. Richardson, Jean R. Dunn, and Nancy Anne Naplin .

649

701

811

401

361

Enewetak, Marshall Islands

ciguatera survey 201

Engraulis mordax — see Anchovy, northern

Enhydra lutris — see Otter, sea

"Estimated initial population size of the Bering Sea
stock of bowhead whale, Balaena mysticetus: An itera-
tive method," by Jeffrey M. Breiwick, Edward D. Mit-
chell, and Douglas G. Chapman 843

Euphausia eximia
larval development

distribution, vertical 331

larval stages described 315

observations of reared animals 315

population, South Pacific 328

"Factors controlling growth and survival of cultured
spot prawn, Pandalusplatyceros, in Puget Sound, Wash-
ington," by John E. Rensel and Earl F Prentice 781

Farallon Islands
pinnipeds
predation by sharks

FARBER, MARK I.— see BAGLIN et al.

989

"Feeding ecology of Lagodon rhomboides (Pisces:
Sparidae): Variation and functional responses," by Allan
W. Stoner 337

FERRARO, STEVEN P., "Daily time of spawning

of 12 fishes in the Peconic Bays, New York" 455

FISCUS, CLIFFORD H.— see STROUD et al.

Fish

trimethylamine
improved method to analyze, and interference of
ammonia and dimethylamine 465

Fish assemblages, reef

annual variability in kelp forest off Santa Barbara,

California

cinetransects 363

sampling 372

spatial differences 365

statistical analyses 364

study sites 362

yearly differences 369, 373

Fish larvae
anchovy, northern

percentage of starving in southern California Bight

475

Fish meal

demand model for United States

functional form 270

lagged response mechanisms 271

simultaneity bias 270

specification 268

statistical procedures 272

Fish populations
diel and seasonal variation in abundance and diversity

of shallow-water, in Morrow Bay, California 759

multistage recruitment process for laboratory

data collection 558

experimental design 559

experimental environments 557

feeding 558

marking 558

mathematical model, development 569

phase I 561

phase II 566

Fishery dynamics
using Box-Jenkins models to forecast

data and underlying model 888

estimation and checking 891

forecasts 893

model identification 890

transfer function models 892

Fishes

Atlantic Ocean, northwest, and Gulf of Mexico

organochlorine residues

daily time of spawning in the Peconic Bays, New York
seasonality of, occupying surf zone habitat in Gulf of
Mexico

annual and seasonal occurrence

51

455

913

daily activity patterns 916

factors affecting occurrence 920

seasonal and annual variations 918

species composition 918

Fishes, marine

life history patterns and consequences for fisheries

management

r and K selection 2

response of r and K selected species to harvesting . 4

theory of r and K selection 1

Fishes, mesopelagic
diets of vertically migrating in Hawaiian waters

Benthosema suborbitale 630

Bolinichthys longipes 629

Bregmaceros japonicus 632

Ceratoscopelus warmingi 628

Diaphus fragilis 632

Diaphus perspicillatus 631

Diaphus schmidti 630

Diaphus trachops 632

Diogenichthys atlanticus 630

field collections 619

laboratory procedures 620

Lampanyctus nobtlis 623

Lampanyctus steinbecki 623

Melamphaes danae 632

Notolychnus valdiviae 628

Triphoturus nigrescens 625

Fishes, postlarval

retention of three taxa in tidal estuary. Cape Fear

River, North Carolina

behavior, diel 423

length -frequency distributions 429

tide response 426

Florida
whale, false killer

recurrent mass stranding 171

Florida, west coast
dolphin, spinner

observations of mass stranding 353

Flounder, smooth
development of larval with redescription of develop-
ment of winter flounder

distinguishing features 900

fin development 902

general development 900

identification 898

laboratory observations 899

morphology 901

pigmentation 903

terminology 898

Flounder, winter

redescription of development 897

Flounder, yellowtail
temperature effects on growth and yolk utilization in

yolk-sac larvae 731

990

FOGARTY. MICHAEL J.. DAVID V D. BORDEN, and
HOWARD J. RUSSELL. "Movements of tagged Ameri-
can \ohstei: Homan/s americaniis. off Rhode Island" . . . 771

"Food of the Pacific white-sided do\phm, Lagenorhynchus
ohliquidens. Dall's porpoise, Phocoenoides dalli. and
northern furseal, Callorhmus urKinuK, offCalifomia and
Washington." by Richard K. Stroud, Clifford H. Fiscus,
and Hiroshi Kajimura 951

"Food of the harbor seal, Phoca vitulina nchardsi , in the

Gulf of Alaska," by Kenneth W. Pitcher 549

Fundulus heteroclitus — see Mummichog

Gadus macrocephalus — see Cod, Pacific

GERRY LAWRENCE R.— see WEINSTEIN et al.

GOLDBERG. STEPHEN R., "Seasonal spawning cycle of
the Pacific butterfish, Peprilus simillimus (Stroma-
teidae)" 977

GORDY HERBERT R— see POWELL and GORDY

GOSSELINK. JAMES G— see BISHOP et al.

GRAY, ROBERT J— see HAYNES and GRAY

GRIMES, CHURCHILL B.. and GENE R. HUNTSMAN,
"Reproductive biology of the vermilion snapper, Rhom-
hoplites aurorubens. from North Carolina and South
Carolina" 137

GRISWOLD, CAROLYN A., and JEROME PREZIOSO,
"In situ observations on reproductive behavior of the
long-finned squid, Loligo pealei" 945

Gulf of Alaska
seal, harbor

food of 549

stomach contents and feces as indicators of foods .. 797

Gulf of Mexico
fishes

organochlorine residues 51

shrimp fishery

use of Griffin's yield model 973

Gulf of Mexico, northern
fishes

seasonality of, occupying surf zone habitat 911

Halobates species

distribution and abundance in eastern tropical Pacific

cooccurrence 589

temperature effects 589

HANKIN. DAVID G., "A multistage recruitment pro-
cess in laboratory fish populations: Implications for
models offish population dynamics" 555

HARRISON, F. L.— see RICE et al.

Hawaii

fishes, mesopelagic
diets of vertically migrating 619

HAYNES, JAMES M., and ROBERT H. GRAY,
"Influence of Little Goose Dam on upstream movements
of adult chinook salmon, 0/icor/iync/ius ^s/iaityfsc/ia" .. 185

HINES, ANSON H., and THOMAS R. LOUGHLIN,
"Observations of sea otters digging for clams at Mon-
terey Harbor, California" 159

HODSON, RONALD G.— see WEINSTEIN et al.

Homarus americanus — see Lobster, American

HORN, MICHAEL H., "Diel and seasonal variation
in abundance and diversity of shallow-water fi.sh pap-
ulations in Morrow Bay, California" 759

HOWELL, W, HUNTTING, "Temperature effects on
growth and yolk utilization in yellowtail flounder,
Limanda ferruginea. yolk-sac larvae" 731

HUBER, HARRIET R.— see AINLEY et al.

HULBERG, LARRY W— see OLIVER et al.

HUNTER. JOHN R., and CAROL A. KIMBRELL,

"Early life history of Pacific mackerel. Scomber
japonicus" 89

HUNTER, JOHN R., and CAROL A. KIMBRELL,
"Egg cannibalism in the northern anchovy, Engraulis
mordax" 811

HUNTSMAN, GENE R.— see GRIMES and HUNTS-
MAN

HUPPERT. D. D.. "An analysis of the United States
demand for fish meal" 267

Hydrolagus colliei — see Ratfish

"(An) improved method to analyze trimethylamine in
fish and the interference of ammonia and dimethyl-
amine," by Fern A. BuUard and Jeff Collins 465

"In situ observations on reproductive behavior of the
long-finned squid, Loligo pealei" by Carolyn A. Gris-
wold and Jerome Prezioso ^5

Incubators, gravel

effects of seeding density of pink salmon eggs on water
chemistry and fry characteristics and survival 649

"Influence of Little Goose Dam on upstream movements
of adult Chinook salmon, Oncorhynchus tshauytscha"
by James M. Haynes and Robert H. Gray 185

"Influence of water currents and zooplankton densities
on daily foraging movements of blacksmith. Chromis
punctipinnis, a planktivorous reef fish," by Richard
N. Bray ^^9

991

Invertebrate communities, benthic

relationships between wave disturbance and zonation

in Monterey Bay, California

canyon ridge transect 448

crustacean zone 443

environmental setting 439

polychaete zone 446

sandflat, northern 447

seasonal patterns 449

"Is ovulation in dolphins, Stenella longirostris and Sten-
elta attenuata, always copulation-induced?," by K. Ben-
irschke, Mary L. Johnson, and Rolf J. Benirschke 507

Isopsetta isolepis — see Sole, butter

Istiophoru f: platypterus — see Sailfish

JEARLD, A., JR.— see RICE et al.

JOHANSEN, R H.— see PETERSON et al.

JOHNSON, JAMES H., "Production and growth of sub-
yearling coho salmon, Oncorhynchus kisiitch. chinook
salmon, Oncorhynchus tshawytscha. and steelhead,
Salmo gairdneri, in Orwell Brook, tributary of Salmon
River, New York" 549

JOHNSON, MARY L.— see BENIRSCHKE et al.

KAJIMURA, HIROSHI — see STROUD et al.

KHILNANI, ARVIND, "Use of Griffin's yield model

for the Gulf of Mexico shrimp fishery" 973

KIMBRELL, CAROL A.— see HUNTER and KIM-
BRELL

KNIGHT, MARGARET D., "Larval development of
Euphausia exiniia (Crustacea: Euphausiacea) with notes
on its vertical distribution and morphological divergence
between populations" 313

KRAEUTER, JOHN N., and MICHAEL CASTAGNA,
"Effects of large predators on the field culture of the
hard clam, Mercenaria mercenaria" 538

Lagenorhynchus acutus — see Dolphin, Atlantic white-
sided

Lagenorhynchus obliquidens — see Dolphin, Pacific
white-sided

Lagodon rhomboides — see Pinfish

"(A I large, opening-closing midwater trawl for sampling
oceanic nekton, and comparison of catches with an
Isaacs-Kidd midwater trawl," by William G. Pearcy .... 529

LarimuH fasciatus — see Drum, banded

LAROCHE, JOANNE LYCZKOWSKI, and SALLY L.
RICHARDSON, "Reproduction of northern anchovy,
Engraulis mordax, off Oregon and Washington" 603

992

LAROCHE, WAYNE A., "Development of larval smooth
flounder, Liopsetta piitnami . with a redescription of de-
velopment of winter flounder, Pseudupleiironccti's amcn-
canus I Family Pleuronectidaei" 897

LARSON, RALPH J.— see EBELING et al.

Larvae, fish — see Fish larvae

"Larval development of Euphausia eximia (Crustacea:
Euphausiacea I with notes on its vertical distribution and
morphological divergence between populations," by
Margaret D. Knight 313

"Larval development of Pacific tomcod, Microgadus
proximus, in the northeast Pacific Ocean with compar-
ative notes on larvae of walleye pollock, Theragra chal-
cogramma, and Pacific cod, Gadus macrocephalus (Gad-
idael," by Ann C. Matarese, Sally L. Richardson, and
Jean R. Dunn 923

Leiostomus xanthurus — see Spot

LENARZ, WILLIAM H.— see BAGLIN et al.

LENARZ, WILLIAM H., and PETER B. ADAMS, "Some
statistical considerations of the design of trawl surveys
for rockfish (Scorpaenidae)" 659

LEONG, J. K.— see McLELLAN and LEONG

Lepidochelys kempt — see Turtle, Atlantic ridley

LEWIS, ROBERT M., and CHARLES M. ROITHMAYR,
"Spawning and sexual maturity of Gulf menhaden,
Brevoortia patronus" 947

LEWIS, T JAMES— see AINLEY et al.

"Life history patterns in marine fishes and their con-
sequences for fisheries management," by Peter B. Adams 1

Limanda ferruginea — see Flounder, yellowtail

Liopsetta putnami — see Flounder, smooth

Lobster, American
movements of tagged off Rhode Island 771

Lobster, spiny
effects of injuries and implications for fishery manage-
ment 979

Loligo pealei — see Squid, long-finned

LOUGHLIN, THOMAS R.— see HINES and LOUGHLIN
LUNSFORD, PAMELA J.— see MILLER et al.

Mackerel, Atlantic

Middle Atlantic region, 1978 spring recreational

catch

catch rate estimation 801

fishing effort estimation 800

lengths, weights, and age composition 802

sampling 799

spawning and fecundity in Middle Atlantic Bight .... 103
voluntary swimming speeds and respiration rates

experimental procedure 878

feeding measurements 882

initial and final measurements 881

postfeeding measurements 882

Mackerel, jack
rearing contamer size affects morphology and nutri-
tional condition of larval 789

Mackerel. Pacific
life history, early

feeding behavior 94

growth 93

hatching, onset of feeding, and starvation 91

laboratory experiments and sea samples 89

larvae culture 91

ration, growth efficiency, and metabolism 97

swimming behavior 94

Markov decision models

using, and related techniques for purposes other than

simple optimization

defining the model on a discrete grid 37

model 36

policy analysis 39

MARLIAVE, JEFFREY B., "SpawTi and lar\'ae of the

Pacific sandfish, Trichodon trichodon" 959

to forecast fishery dynamics: Identification, estimation,
and checking"

887

MENDELSSOHN. ROY, 'Using Markov decision models
and related techniques for purposes other than simple
optimization: Analyzingtheconsequencesof policy alter-
natives on the management of salmon runs" 35

Menhaden, Gulf

spawning and sexual maturity

age and size of first spawning 948

ova spawned, number 950

stages of sexual maturity 948

time and frequency of spawning 949

Mercenaria mercenaria — see Clam, hard

METCALFE, J. L.— see PETERSON et al.

Microgadus proximus — see Tomcod, Pacific

Microgadus tomcod — see Tomcod. Atlantic

Micropogonias undulatus — see Croaker, Atlantic

MILLER, BRUCE S.— see QUINN et al.

MILLER. ROBERT E.. DOUGLAS W CAMPBELL, and
PAMELA J. LUNSFORD, "Comparison of sampling de-
vices for the juvenile blue crab, Ca//mecfe.s sapic^ii.s" ... 196

MITCHELL, EDWARD D.— see BREIWICK et al.

MASON, JOHN M., JR.— see BAGLIN et al.

MATARESE. ANN C, SALLY L. RICHARDSON, and
JEAN R. DUNN, "Larval development of Pacific tomcod,
Microgadus proximus, in the northeast Pacific Ocean
with comparative notes on larvae of walleye pollock,
Theragra chalcogramma . and Pacific cod, Gadus macro-
cephalus ( Gadidael" 923

MATARESE, ANN C, and DAVID L. STEIN, "Addi-
tional records of the sculpin Psychrolutes phrictus in the
eastern Bering Sea and off Oregon" 169

"Maturity, spawning, and fecundity of Atlantic croaker,
Micropogonias undulatus. occurring north of Cape Hat-
teras. North Carolina," by Wallace W. Morse 190

McLELLAN, G. L., and J. K. LEONG, "A radiologic
method for examination of the gastrointestinal tract in
the Atlantic ridley, Lepidochelys kempi, and logger-
head, Caretta caretta, marine turtles"

965

MEAD, JAMES G.— see TESTAVERDE and MEAD

MEAD, JAMES G., DANIEL K. ODELL, RANDALL S.
WELLS, and MICHAEL D. SCOTT, "Observations on a
mass stranding of spinner dolphin. Stenella longiros-
tris, from the west coast of Florida"

MENDELSSOHN, ROY, "Using Box-Jenkins models

353

MODDE. TIMOTHY and STEPHEN T ROSS. "Season-
ality of fishes occupying a surf zone habitat in the north-
em Gulf of Mexico"

911

Monterey Bay, California

invertebrate community, benthic

relationships between wave disturbance and zona-

tion along a subtidal high-energy beach 437

Monterey Harbor, California
otter, sea

observations on digging for clams 159

MORGAN, STEVEN G., "Aspects of larval ecology
of Squilla empusa (Crustacea, Stomatopoda) in Chesa-
peake Bay" 693

MORRELL, STEPHEN H.— see AINLEY et al.

Morro Bay, California
fish populations, shallow-water

diel and seasonal variation in abundance and
diversity

MORSE, WALLACE W, "Maturity, spawning, and fe-
cundity of Atlantic croaker, Micropogonias undulatus,
occurring north of Cape Hatteras, North Carolina"

MORSE, WALLACE W, "Spawning and fecundity of
Atlantic mackerel. Scomber scombrus, in the Middle
Atlantic Bight"

759
190
103

993

"Movements of tagged American lobster, Honiarus
americanus, off Rhode Island," by Michael J. Fogarty,
David V. D. Borden, and Howard J. Russell 771

"(A) multistage recruitment process in laboratory fish
populations: Implications for models offish population
dynamics," by David G. Hankin 555

Mummichog
fin regeneration
effect of zinc on and its interaction with methyl-
mercury 163

Munidopsis

species occurring off Oregon and adjacent waters

characters of taxonomic importance 16

key to species 16

Munidopsis anes 17

Munidopsis bairdii 18

Munidopsis beringana 24

Munidopsis cascadia n. sp 21

Munidopsis ciliata 19

Munidopsis latirostris 28

Munidopsis quadrate 17

Munidopsis sp 18

Munidopsis subsquamosa 26

Munidopsis tuftsi n. sp 24

Munidopsis verrucosus 27

Munidopsis yaqumensis n. sp 20

vertical and geographic distribution 29

NAPLIN, NANCY ANNE— see RICHARDSON et al.

Nekton, oceanic
opening-closing midwater trawl vs. Isaacs-Kidd mid-
water trawl

Nets
tuna purse seine

passive behavior of spotted dolphins

"(The) 1978 spring recreational catch of Atlantic
mackerel. Scomber scombrus, off the Middle Atlantic
region," by Darryl J. Christensen and Walter J. Clifford

North Carolina

529

535

799

snapper, vermilion
reproductive biology

137

NYBAKKEN, JAMES W— see OLIVER et al.

"Observations of sea otters digging for clams at
Monterey Harbor, California," by Anson H. Hines and
Thomas R. Loughlin

159

"Observations on a mass stranding of spinner dolphin,
Stenella longirostris, from the west coast of Florida," by
James G. Mead, Daniel K. Odell, Randall S. Wells, and
Michael D. Scott 353

"Observations on early life stages of Atlantic tomcod,
Microgadus tomcod" by R. H. Peterson, R H. Johansen,
and J. L. Metcalfe 147

"Occurrence, movements, and distribution of botllenose
dolphin, Tursiops truncatus, in .southern Texas," by
Susan H. Shane 593

"Occurrence of the finetooth shark, Carcharhinus
isodon . off Dauphin Island, Alabama," by Steven Bran-
stetter and Robert L. Shipp 177

O'CONNELL, CHARLES R, "Percentage of starving
northern anchovy, Engraulis mordax. larvae in the sea
as estimated by histological methods" 475

ODELL, DANIEL K.— see MEAD et al.

ODELL, DANIEL K., EDWARD D. ASPER. JOE BAU-
COM, and LANNY H. CORNELL, "A recurrent mass
stranding of the false killer whale, Pseudorca crassi-
dens. in Florida" 171

OLIVER, JOHN S., PETER N. SLATTERY LARRY
W. HULBERG, and JAMES W NYBAKKEN, "Relation-
ships between wave disturbance and zonation of ben-
thic invertebrate communities along a subtidal high-
energy beach in Monterey Bay, California" 437

OLLA, BORI L.— see PEARSON et al.

Oncorhynchus gorbuscha — see Salmon, pink

Oncorhynchus kisutch — see Salmon, coho

Oncorhynchus tshauytscha — see Salmon, chinook

Oregon

anchovy, northern

reproduction off 603

spawning biomass and early life in northern sub-
population 855

Psychrolutes phrictus

additional records 169

sole, butter

eggs and larvae off 401

Organochlorine residues
fiishes, northwest Atlantic Ocean and Gulf of Mexico

51

"Organochlorine residues in fishes from the northwest
Atlantic Ocean and Gulf of Mexico," by Virginia F. Stout 51

Orwell Brook, New York
production and growth of subyearling

salmon, chinook 549

salmon, coho 549

steelhead 549

Otter, sea
Monterey Harbor, California

observations on digging for clams 159

"Oxygen consumption and hemolymph osmolality of
brown shrimp, Penaeus aztecus" by James M. Bishop,
James G. Gosselink, and James H. Stone 741

994

Pacific Ocean, eastern North
anglerfishes. ceratioid
description of new species 59

Pacific Ocean, eastern tropical
Halobates species

distribution and abundance 579

Pacific Ocean, Indo-West

clupeid fishes

bomolochid copepods parasitic on eyes of 716

Pacific Ocean, northeast
tomcod, Pacific

larval development 923

Pandalus platyceros — see Prawm. spot

Panulirus argus — see Lobster, spiny

PARKER, KEITH, "A direct method for estimating
northern anchovy, Engraulis mordax , spawning
biomass" 541

"Passive behavior by the spotted dolphin, Stenella atten-
uata, in tuna purse seine nets," by James M. Coe and
Warren E. Stuntz 535

PEARCY WILLIAM G., "A large, opening-closing mid-
water trawl for sampling oceanic nekton, and compar-
ison of catches with an Isaacs-Kidd midwater trawl" . . . 529

PEARSON, WALTER H.. PETER C. SUGARMAN,
DANA L. WOODRUFF, J. W. BLAYLOCK, and BORI
L. OLLA, "Detection of petroleum hydrocarbons by the
Dungeness crab, Cancer magister" 821

Peconic Bays, New York

fish spawning, daily time of 455

PELL A, JEROME J— see BAILEY et al.

Penaeus aztecus — see Shrimp, brown

Peprilus simillimus — see Butterfish, Pacific

"Percentage of starving northern anchovy, Engraulis
mordax, larvae in the sea as estimated by histological
methods," by Charles P O'Connell 475

Perch, silver

comparison with earlier descriptions 132

comparison with other lar\-al Sciaenidae 134

description 122

spawning seasons and areas 133

PETERSON, R. H., P H. JOHANSEN, and J. L. MET-
CALFE, "Observations on early life stages of Atlantic
tomcod, Microgadus tomcod" 147

Philippine Archipelago
anglerfishes, ceratioid

descriptions of five new species 379

Phoca vitulma — see Seal, harbor

Phoca vitulina richardsi — see Seal, harbor

Phocoenoides dalli — see Porpoise, Dall's

PIETSCH, THEODORE W, and JEFFREY A. SIE-
GEL, "Ceratioid anglerfishes of the Philippine Archi-
pelago, with descriptions of five new species"

379

PIETSCH, THEODORE W.. and JOHN P VAN
DUZER, "Systematics and distribution of ceratioid an-
glerfishes of the family Melanocetidae with the descrip-
tion of a new species from the eastern North Pacific
Ocean" 59

Pinfish

feeding ecology
variation and functional responses 337

Pinnipeds
predation by sharks at Farallon Islands 941

PITCHER. KENNETH W. "Food of the harbor seal,
Phoca vitulina richardsi,m\he GuMoi Maska" 549

PITCHER, KENNETH W, "Stomach contents and feces
as indicators of harbor seal, Phoca vitulina, foods in
the Gulf of Alaska" ''97

Pollock, walleye

larval development in northeast Pacific Ocean

compared with Pacific tomcod 923

Porpoise, Dall's

food of, off California and Washington

prey distribution 955

prey size 957

prey species 9oo

stomach capacity of predators 955

POTTHOFF, THOMAS, "Development and structure
of fins and fin supports in dolphin fishes Coryphaena
hippurus and Coryphaena equiselis (Coryphaenidae)" . .

277

POWELL. ALLYN B., and HERBERT R. GORDY "Egg
and larval development of the spot, Leiostomus
xanthurus ( Sciaenidae)" ^^^

POWLES, HOWARD. "Descriptions of larval silver
perch, Bairdiella chrysoura, banded drum, Larimus
fasciatus, and star drum, Stellifer lanceolatus
(Sciaenidae)" ^^^

Prawn, spot

factors controlling growth and survival of cultured in
Puget Sound, Washington

TOO

environmental data

783
juveniles

-°^r ■ ^85

yearlings

"Predation by sharks on pinnipeds at the Farallon
Islands," by David G. Ainley, Craig S. Strong, Harriet
R. Huber, T James Lewis, and Stephen H. Morrell 941

995

PRENTICE, EARL F.— see RENSEL and PRENTICE

PREZIOSO, JEROME— see GRISWOLD and PREZIO-
SO

"Production and growth of subyearling coho salmon,
Oncorhynchus kisutch, chinook salmon, Oncorhynchus
tshawytscha . and steelhead, Salmo gairdneri. in Orwell
Brook, tributary of Salmon River, New York," by James
H, Johnson 549

Pseudopleuronectes americanus — see Flounder, winter

Pseudorca crassidens — see Whale, false killer

Psych ralutes ph rictu s

additional records from eastern Bering Sea and

off Oregon 169

Puget Sound, Washington
prawn, spot

factors controlling growth and survival of cultured 781
ratfish

depth distribution and seasonal diel movements . . . 816

QUINN, THOMAS P, BRUCE S. MILLER, and R.
CRAIG WINGERT, "Depth distribution and seasonal
and diel movements of ratfish, Hydrolagus colliei, in
Puget Sound, Washington" 816

"(A) radiologic method for examination of the gastro-
intestinal tract in the Atlantic ridley, Lepidochelys
kempi, and loggerhead, Caretta caretta. marine turtles,"
by G. L. McLellan and J. K. Leong 965

RANDALL, JOHN E., "A survey of ciguatera at Ene-
wetak and Bikini, Marshall Islands, with notes on the
systematics and food habits of ciguatoxic fishes" 201

Ratfish

Puget Sound, Washington
depth distribution and seasonal and diel movements 816

"Rearing container size affects morphology and
nutritional condition of larval jack mackerel, Trachurus
symmetricus',' by Gail H. Theilacker 789

"(A) recurrent mass stranding of the false killer whale,
Pseudorca crassidens, in Florida," by Daniel K. Odell,
Edward D. Asper, Joe Baucom, and Lanny H. Cornell . . 171

"Relationships between wave disturbance and zonation
of benthic invertebrate communities along a subtidal
high-energy beach in Monterey Bay, California," by John
S. Oliver, Peter N. Slattery, Larry W. Hulberg, and
James W Nybakken 437

RENSEL, JOHN E.. and EARL R PRENTICE, "Factors
controlling growth and survival of cultured spot prawn,
Pandalus platyceros, in Puget Sound, Washington" 781

"Reproduction of northern anchovy, Engraulis nwrdax,
off Oregon and Washington," by Joanne Lyczkowski
Laroche and Sally L. Richardson 603

996

"Reproductive biology of the vermilion snapper, Rhom-
hiiplites uuroriibens. from North Carolina and South Car-
olina," by Churchill B. Grimes and Gene R. Huntsman .

"Respiration and depth control as possible reasons for
swimming of northern anchovy, Engraulis nwrdax, yolk-
sac larvae," by Daniel Weihs

"Retention of three taxa of postlarval fishes in an
intensively flushed tidal estuary. Cape Fear River,
North Carolina," by Michael P Weinstein, Sidney L.
Weiss, Ronald G. Hodson, and Lawrence R. Gerry

Rhode Island

lobster, American
movements of tagged off

137

109

419

771

Rhomboplites aurorubens — see Snapper, vermilion

RICE, D. W. JR., F L. HARRISON, and A. JEARLD, JR.,
"Effects of copper on early life history stages of northern
anchovy, Engraulis nwrdax''

RICE. STANLEY D.— see BAILEY et al.

RICE, STANLEY D., and JACK E. BAILEY "Ammonia
concentrations in pink salmon, Oncorhynchus gorbus-
cha, redds of Sashin Creek, southeastern Alaska"

RICE. STANLEY D.. and JACK E. BAILEY "Survival,
size, and emergence of pink salmon, Oncorhynchus gor-
buscha, alevins after short- and long-term exposures to
ammonia"

RICHARDSON, SALLY L., "Spawning biomass and
early life of northern anchovy, Engraulis mordax. in the
northern subpopulation off Oregon and Washington" . .

RICHARDSON, SALLY L.— see LAROCHE and RICH-
ARDSON

RICHARDSON. SALLY L.— see MATARESE et al.

RICHARDSON. SALLY L.. JEAN R. DUNN, and
NANCY ANNE NAPLIN, "Eggs and larvae of butter
sole, Isopsetta isolepis (Pleuronectidae), off Oregon
and Washington"

Rockfish
trawl surveys, statistical considerations of design
comparisons of random, stratified random, and sys-
tematic sampling

examination of trade offs between tow length and
number of tows

ROITHMAYR, CHARLES M.— see LEWIS and ROITH-
MAYR

ROSS, STEPHEN T— see MODDE and ROSS

RUSSELL. HOWARD J.— see FOGARTY et al.

Sailfish
size and possible origin from eastern Atlantic Ocean .

675

809

641

855

401

660
667

805

Salmo gairdnen — see Steelhead

SCOTT, MICHAEL D.— see MEAD et al.

Salmon, chinook
influence of Little Goose Dam on upstream movements

of adult 185

production and growth of subyearling in Orwell Brook,

New York 549

smolts, transportation in Columbia River and effects
on adult returns

collection and marketing of fish and fi.sh hauling

procedures 493

compari.son of results with other studies 502

effect of transportation on homing 503

evaluation of returning adults 494

experimental design 493

factors influencing assessment of data 494

percentage adult returns of transported releases . . 498
recovery of marked in commercial and sport

fisheries 500

returns of adult experimental fish to hatcheries

and spawning grounds 501

returns of adult experimental fish to Little Goose

Dam 496

size and years-in-ocean of adult experimental fish . 500

straying of experimental groups 502

timing of adult returns 499

Salmon, coho
production and growth of subyearling in Orwell
Brook, New York 549

Salmon, pink

effects of seeding density of eggs on water chemis-
try and fry characteristics and survival in gravel
incubators

dissolved oxygen 652

quantity and quality of fry produced 653

temperature, pH, and total ammonia in effluent . . . 650

water quality and fry production 655

Sashin Creek, southeastern Alaska

ammonia concentrations in redds 809

survival, size, and emergence of alevins after ex-
posure to ammonia

early emergence 644

effect of long-term exposures on fry size at

emergence 644

sensitivity of different life stages 643

Sandfish, Pacific
spawn and larvae

larval development 961

life history notes 959

Santa Barbara, California
fish assemblages, reef

annual variability in kelp forests off 361

Sashin Creek, southeastern Alaska
salmon, pink

ammonia concentrations in redds 809

Scomber japonicus — see Mackerel, Pacific

Scomber scombrus — see Mackerel, Atlantic

Seal, harbor

food of, in Gulf of Alaska 549

Gulf of Alaska

stomach contents and feces as indicators of foods .. 797

Seal, northern fur
food of, off California and Washington

prey distribution 955

prey size 957

prey species 955

stomach capacity of predators 955

"Seasonal spawning cycle of the Pacific butterfish,
Peprilus simillimus ( Stroma teidae)," by Stephen R.
Goldberg 977

"Seasonality of fishes occupying a surf zone habitat
in the northern Gulf of Mexico," by Timothy Modde and
Stephen T. Ross 911

SEIGEL, JEFFREY A.— see PIETSCH and SEIGEL

SHANE, SUSAN H., "Occurrence, movements, and dis-
tribution of bottlenose dolphin, Tursiops truncatus, in
southern Texas" 593

Shark, finetooth

occurrence off Dauphin Island, Alabama 177

Sharks

Farallon Islands
predation on pinnipeds 941

"Shedding rates of plastic and metal dart tags from
Atlantic bluefin tuna, Thunnus thynnus" by Raymond
E. Baglin, Jr., Mark I. Farber, William H. Lenarz, and
John M. Mason, Jr 179

SHIPP ROBERT L.— see BRANSTETTER and SHIPP

Shrimp, brown

oxygen consumption and hemolymph osmolality

crowding effects 743, 745

disturbance effects 743, 745

diurnal effects 743, 744

energy considerations 752

reduced-light effects 743, 745

salinity effects 744, 745, 749

size effects 744, 746, 750

temperature effects 744, 745, 751

variability sources 746

Shrimp fishery
use of Griffins yield model for Gulf of Mexico

expected value of yield 974

parameter sensitivity test 975

SHULENBERGER, ERIC-
BERGER

-see CHENG and SHULEN-

"Size and possible origin of sailfish, Istiophorus pla-
typterus, from the eastern Atlantic Ocean," by Grant

997

L. Beardsley 805

SLATTERY PETER N.— see OLIVER et al.

SMAYDA, THOMAS J.— see DURBIN et al.

SMYTH, PETER O., "Callinectes ( Decapoda: Portuni-

dae) larvae in the Middle Atlantic Bight, 1975-77" .... 251

Snapper, vermilion

reproductive biology, North and South Carolina

fecundity 142

maturation 140, 144

seasonality, frequency, and duration of spawning . . 139
sex ratio 141, 144

Sole, butter
eggs and larvae off Oregon and Washington

features, distinguishing 403

identification verification 403

morphology 405, 408

occurrence 412

ossification of meristic structures 409

pigmentation 404, 405

"Some statistical considerations of the design of trawl
surveys for rockfish (Scorpaenidae),'" by William H.
Lenarz and Peter B. Adams 659

South Carolina
snapper, vermilion

reproductive biology 137

"Southern distribution of the Atlantic whitesided dol-
phin, Lagenorhynchus acutus, in the western North
Atlantic," by Salvatore A. Testaverde and James G.
Mead 167

"Spawn and larvae of the Pacific sandfish, Trichodon
trichodon ," by Jeffrey B. Marliave 959

Spawning

daily time of in the Peconic Bays, New York 455

"Spawning and fecundity of Atlantic mackerel. Scomber
scombrus, in the Middle Atlantic Bight," by Wallace
W. Morse 103

"Spawning and sexual maturity of Gulf menhaden,
Brevoortia patronus" by Robert M. Lewis and Charles
M. Roithmayr 947

"Spawning biomass and early life of northern anchovy,
Engraulis mordax, in the northern subpopulation off
Oregon and Washington," by Sally L. Richardson 855

"Species of Munidopsis (Crustacea, Galatheidae) occur-
ring off Oregon and in adjacent waters," by Julie W
Ambler 13

Spot

Cape Fear River, North Carolina
retention of postlarval in tidal estuary 419

998

egg and larval development

body proportions 704

distinguishing from other sciaenids 712

embryonic development 702

fins 705

pigmentation 710

pterygiophore development and arrangements .... 709

Squid, long-finned
reproductive behavior, in situ observations 947

Squilla empusa

larval ecology in Chesapeake Bay

Cape Henry survey 694

research applied to national needs ( RANN) survey 694

seasonal occurrence 695

temperature and salinity tolerence 697

Steelhead
production and growth of subyearling in Orwell Brook,

New York 549

smolts, transportation in Columbia River and effects
on adult returns

collection and marketing of fish and fish hauling

procedures 493

comparison of results with other studies 502

effect of transportation on homing 503

evaluation of returning adults 494

experimental design 493

factors influencing assessment of data 494

percentage adult returns of transported releases .. 498
recovery of marked in the Indian and sport fisheries 501
returns of adult experimental fish to hatcheries and

spawning grounds 501

returns of adult experimental fish to Little Goose

Dam 496

size and years-in-ocean of adult experimental fish . 500
straying of experimental groups 502

STEIN, DAVID L.— see MATARESE and STEIN
Stellifer lanceolatus — see Drum, star
Stenella attenuata — see Dolphin, spotted
Stenella longirostris — see Dolphin, spinner

"Stomach contents and feces as indicators of harbor seal,
Phoca vital ina. foods in the Gulf of Alaska," by Kenneth
W Pitcher

STONE. JAMES H.— see BISHOP et al.

STONER, ALLAN W, "Feeding ecology of Lagodon
rhomboides (Pisces: Sparidae): Variation and functional
responses"

STOUT, VIRGINIA F, "Organochlorine residues in
fishes from the northwest Atlantic Ocean and Gulf
of Mexico"

STRONG, CRAIG S.— see AINLEY et al.

797

337

51

STROUD. RICH.\RD K.. CLIFFORD H. FISCUS. and
HIROSHI KAJIMURA, "Food of the Pacific white-sided
dolphin, Lagenorhynchus obliquidens. Dall's porpoise,
Phocoenoides dalli. and northern fur seal, Callorhinus
ursinii.s. off California and Washington" 951

SUGARMAN, PETER C— see PEARSON et al.

"Summer food of Pacific cod, Gadus macrocephalus,
in coastal waters of southeastern Alaska," by David M.
Clausen 968

"(A) survey of ciguatera at Enewetak and Bikini, Mar-
shall Islands, with notes on the systematics and food ha-
bits of ciguatoxic fishes," by John E. Randall 201

"Survival, size, and emergence of pink salmon. Onco-
rhynchus gorhuscha. alevins after short- and long-term
exposures to ammonia," by Stanley D. Rice and Jack E.
Bailey 641

"Systematics and distribution of ceratioid anglerfishes of
the family Melanocetidae with the description of a new-
species from the eastern North Pacific Ocean," by Theo-
dore W. Pietsch and John R Van Duzer 59

specific gravity of egg solids 154

statistical procedures 149

survival to hatch and length at hatching 152

water content 152

Tomcod, Pacific

larval development in northeast Pacific Ocean
comparative notes on Theragra chalcogramma and

Gadus rnacrucephalus 935

fins 931

head and axial skeleton 929

identification 925

measurements 924

morphology 929

occurrence 935

pigment patterns 925

scales 935

specimens 924

Trachurus symmetricus — see Mackerel, jack

"Transportation of chinook salmon, Oncorhynchus

tshawytscha . and steelhead. Salmo gairdneri, smolts in
the Columbia River and effects on adult returns," by

Weslev J. Ebel 491

TAYLOR, SIDNEY G.— see BAILEY et al.

"Tempei'ature effects on growth and yolk utilization in
yellowtail flounder, Limanda ferrugmea, yolk-sac lar-
vae," by W. Huntting Howell

TESTAVERDE, SALVATORE A., and JAMES G.
MEAD, "Southern distribution of the Atlantic white-
sided dolphin, Lagenorhynchus acutus, in the western
North Atlantic"

Texas, southern
dolphin, bottlenose

occurrence, movements, and distribution

731

167

593

685

789

THEILACKER, GAIL H., "Changes in body measure-
ments of larval northern anchovy, Engraulis mordax.
and other fishes due to handling and preservation" ....

THEILACKER, GAIL H., "Rearing container size
affects morphology and nutritional condition of larval
jack mackerel, Trachurus symmetricus"

Theragra chalcogramma — see Pollock, walleye

Thunnus thvnnus — see Tuna, bluefin

Tomcod. Atlantic

observations on early life stages

developmental stages 150

dry weight 153

egg collection 148

egg diameter 153

field observations 150

field studies 147

laboratory studies 148

specific gravity 152

Trawl, beam

wheels, metering

effectiveness for measurement of area sampled

791

Trawl , midwater nekton

compared with Isaacs-Kidd midwater trawl

effective cross-sectional area of the pelagic trawl .. 533

flushing of the pelagic trawl 531

length-frequency comparisons 532

midwater trawl description and operation 529

pelagic trawl-IKMT comparisons 532

Trichodon trichodon — see Sandfish, Pacific

Trimethylamine

improved method to analyze in fish

cold method of analysis for TMA 472

comparative analyses using fish flesh 470

extraction offish flesh with added TMA and DMA . 471

extraction of TMA 470

extraction procedure for fish flesh 466

purification procedures 466

reaction of ammonia 46 <

reaction of DMA 468

TMA, methods of analyses 466

Tuna, bluefin
Atlantic Ocean
shedding rates of plastic and metal dart tags 179

Tursiops truncatus — see Dolphin, bottlenose

Turtle, Atlantic ridley

radiologic method for examination of gastrointestinal

tract

Turtle, loggerhead

radiologic method for examination of gastrointestinal

965

999

tract 965

United States
fish meal demand analysis 267

"Use of Griffin's yield model for the Gulf of Mexico
shrimp fishery," by Arvind Khilnani 973

"Using Box-Jenkins models to forecast fishery dynamics:
Identification, estimation, and checking," by Roy Men-
delssohn 887

"Using Markov decision models and related techniques
for purposes other than simple optimization: Analyzing
the consequences of policy alternatives on the manage-
ment of salmon runs," by Roy Mendelssohn

35

VAN DUZER, JOHN R-
ER

-see PIETSCH and VAN DUZ-

VERITY, PETER G.— see DURBIN et al.

"Voluntary swimming speeds and respiration rates of
a filter-feeding planktivore, the Atlantic menhaden,
Brevoortia tyrannus (Pisces; Clupeidae)," by Ann G.
Durbin, Edward G. Durbin, Peter G. Verity, and Thomas
J. Smayda 877

Washington

anchovy, northern

reproduction off 603

spawning biomass and early life in northern sub-
population 855

food of Pacific white-sided dolphin, Ball's porpoise,

and northern fur seal off 951

sole, butter
eggs and larvae off 401

Water currents

influence of on daily foraging movements of black-
smith 829

WEIHS, DANIEL, "Respiration and depth control as
possible reasons for swimming of northern anchovy, En-
graulis mordax, yolk-sac larvae" 109

WEINSTEIN, MICHAEL R, SIDNEY L. WEISS, RON-
ALD G. HODSON, and LAWRENCE R. GERRY, "Reten-
tion of three taxa of postlarval fishes in an intensively
flushed tidal estuary. Cape Fear River, North Carolina" 419

163

WEIS, JUDITH SHULMAN — see WEIS and WEIS

WEIS, PEDDRICK, and JUDITH SHULMAN WEIS,
"Effect of zinc on fin regeneration in the mummichog,
Fundulus heteroclitus, and its interaction with methyl-
mercury"

WEISS, SIDNEY L.— see WEINSTEIN et al.

WELLS, RANDALL S.— see MEAD et al.

Whale, bowhead

estimated initial population size of Bering Sea stock

aspects of fishery 852

catch history 845

data limitations 850

estimates of current stock size 845

estimates of initial stock size 845

lag time 847

model development 847

model limitations 851

natural mortality 847

net recruitment rate 847

recovery times 850

risk analysis 848

vital parameters 850

Whale, false killer
recurrent mass stranding in Florida

behavior in captivity 174

hematology 174

relationships among strandings 175

sequence of events 171

Wheels, metering

effectiveness for measurement of area sampled by

beam trawls

consistency with other estimates of distance 794

count consistency 793

wheel counts versus catch data 794

WINGERT R. CRAIG— see QUINN et al.
WOODRUFF, DANA L,— see PEARSON et al.

Zooplankton

influence of density on daily foraging movements of
blacksmith 829

1000

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Contents-continued

STROUD, RICHARD K., CLIFFORD H. FISCUS, and HIROSHI KAJIMURA. Food
of the Pacific white-sided dolphin, Lagenorhynchus obliquidens, Dall's porpoise,
Phocoenoides dalli, and northern fur seal, Callorhinus ursinus, off California and
Washington 951

MARLIAVE, JEFFREY B. Spawn and larvae of the Pacific sandfish, Trichodon
trichodon 959

McCLELLAN, G. L., and J. K. LEONG. A radiologic method for examination of the
gastrointestinal tract in the Atlantic r\d\ey, Lepidochelys kempi, and loggerhead,
Caretta caretta, marine turtles 965

CLAUSEN, DAVID M. Summer food of Pacific cod, Gadus macrocephalus , in coastal
waters of southeastern Alaska 968

KHILNANI, ARVIND. Use of Griffin's yield model for the Gulf of Mexico shrimp
fishery 973

GOLDBERG, STEPHEN R. Seasonal spawning cycle of the Pacific butterfish,
Peprilus simillimus (Stromateidae) 977

DAVIS, GARY E. Effects of injuries on spiny lobster, Panulirus argus, and impli-
cations for fishery management 979

INDEX, VOLUME 78 985

V-/

* GPO 696-404

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