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U.S. Department
of Commerce

Volume 108
Number 4
October 2010

Fishery

Bulletin

U.S. Department
of Commerce

Gary Locke

Secretary of Commerce

National Oceanic
and Atmospheric
Administration

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Administrator of NOAA

National Marine
Fisheries Service
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for Fisheries

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The Fishery Bulletin carries original research reports and technical notes on investigations in
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U.S. Department
of Commerce

Seattle, Washington

Volume 108
Number 4
October 2010

Fishery

Bulletin

Contents

Articles

365-381 Jones, Ashlee A., Norman G. Hall, and lan C. Potter

Species compositions of elasmobranchs caught by three different
commercial fishing methods off southwestern Australia,
and biological data for four abundant bycatch species

382-392 Hurst, Thomas P., Benjamin J. Laurel, and Lorenzo Ciannelli

Ontogenetic patterns and temperature-dependent growth rates
in early life stages of Pacific cod ( Gadus macrocephcilus)

The National Marine Fisheries
Service (NMFS) does not approve,
recommend, or endorse any proprie-
tary product or proprietary material
mentioned in this publication. No
reference shall be made to NMFS,
or to this publication furnished by
NMFS, in any advertising or sales
promotion which would indicate or
imply that NMFS approves, recom-
mends, or endorses any proprietary
product or proprietary material
mentioned herein, or which has
as its purpose an intent to cause
directly or indirectly the advertised
product to be used or purchased
because of this NMFS publication.

The NMFS Scientific Publications
Office is not responsible for the con-
tents of the articles or for the stan-
dard of English used in them.

393-407 Bollens, Stephen M., Rian vanden Hooff, Mari Butler,

Jeffery R. Cordell, and Bruce W. Frost

Feeding ecology of juvenile Pacific salmon ( Oncorhynchus spp.)
in a northeast Pacific fjord: diet, availability of zooplankton,
selectivity for prey, and potential competition for prey resources

408-419 DeCelles, Gregory R., and Steven X. Cadrin

Movement patterns of winter flounder ( Pseudopleuronectes
americanus) in the southern Gulf of Maine: observations
with the use of passive acoustic telemetry

420-432 Heupel, Michelle R., Ashley J. Williams, David J. Welch,
Campbell R. Davies, Ann Penny, Jacob P. Kritzer,

Ross J. Marriott, and Bruce D. Mapstone

Demographic characteristics of exploited tropical lutjanids:
a comparative analysis

433-441 Graves, John E., and Andrij Z. Horodysky

Asymmetric conservation benefits of circle hooks in multispecies billfish
recreational fisheries: a synthesis of hook performance and analysis of
blue marlin ( Makaira nigricans) postrelease survival

II

Fishery Bulletin 108(4)

442-449

Laidig, Thomas E.

Influence of ocean conditions on the timing of early life history events for blue rockfish
( Sebastes mystinus) off California

450-465

Dunton, Keith J., Adrian Jordaan, Kim A. McKown, David O. Conover, and Michael G. Frisk

Abundance and distribution of Atlantic sturgeon (Acipenser oxyrinchus) within the Northwest Atlantic
Ocean, determined from five fishery-independent surveys

466-477

Hart, Ted D., Julia E. R. Clemons, W. Waldo Wakefield, and Selina S. Heppell

Day and night abundance, distribution, and activity patterns of demersal fishes on Heceta Bank, Oregon

478-490

Simms, Jeffrey R., Jay R. Rooker, Scott A. Holt, G. Joan Holt, and Jessica Bangma

Distribution, growth, and mortality of sailfish Ustiophorus platypterus) larvae
in the northern Gulf of Mexico

491

Acknowledgment of reviewers

492

List of titles

494

List of authors

495

Subject index

498

Guidelines for authors

Subscription form (inside back cover)

365

Species compositions of elasmobranchs
caught by three different commercial fishing
methods off southwestern Australia, and
biological data for four abundant bycatch species

Ashlee A. Jones (contact author)1
Norman G. HalS1
Ian C. Potter1

Email address for contact author: ashlee.|ones@murdoch. edu.au

1 Centre for Fish and Fisheries Research
Murdoch University

Murdoch, Western Australia, 6150, Australia

Abstract — Commercial catches taken
in southwestern Australian waters
by trawl fisheries targeting prawns
and scallops and from gillnet and
longline fisheries targeting sharks
were sampled at different times of
the year between 2002 and 2008. This
sampling yielded 33 elasmobranch
species representing 17 families.
Multivariate statistics elucidated
the ways in which the species com-
positions of elasmobranchs differed
among fishing methods and provided
benchmark data for detecting changes
in the elasmobranch fauna in the
future. Virtually all elasmobranchs
caught by trawling, which consisted
predominantly of rays, were discarded
as bycatch, as were approximately a
quarter of the elasmobranchs caught
by both gillnetting and longlining. The
maximum lengths and the lengths at
maturity of four abundant bycatch
species, Heterodontus portusjacksoni,
Aptychotrema vincentiana , Squatina
australis, and Myliobatis australis,
were greater for females than males.
The L50 determined for the males of
these species at maturity by using full
clasper calcification as the criterion of
maturity did not differ significantly
from the corresponding L50 derived
by using gonadal data as the crite-
rion for maturity. The proportions of
the individuals of these species with
lengths less than those at which 50%
reach maturity were far greater in
trawl samples than in gillnet and
longline samples. This result was
due to differences in gear selectiv-
ity and to trawling being undertaken
in shallow inshore waters that act
as nursery areas for these species.
Sound quantitative data on the spe-
cies compositions of elasmobranchs
caught by commercial fisheries and
the biological characteristics of the
main elasmobranch bycatch species
are crucial for developing strategies
for conserving these important spe-
cies and thus the marine ecosystems
of which they are part.

Manuscript submitted 15 December 2009.
Manuscript accepted 28 January 2010.
Fish. Bull. 108:365-381 (2010).

The views and opinions expressed
or implied in this article are those of the
author (or authors) and do not necessarily
reflect the position of the National Marine
Fisheries Service, NOAA.

The impact of commercial fisheries
on the populations of sharks and rays
has, in recent years, become an issue
of international concern (Stevens
et al., 2000; Walker et al., 2005). It
is important to recognize, however,
that elasmobranchs are not only tar-
geted by certain fisheries, but also
comprise a substantial component of
the bycatch of commercial fisheries,
such as those employing trawl nets,
gillnets, and longlines (Stevens et al.,
2000; Stobutzki et al., 2001; Walker,
2005a). An assessment of the impacts
of commercial fishing on the elasmo-
branchs taken as bycatch is hindered
by the fact that most of that catch
is typically reported as “unidentified
shark” or “mixed fish,” or not reported
at all (Walker, 2005a). The numbers
of sharks and rays taken as bycatch
by commercial fisheries may, in some
cases, exceed those of the targeted
species, and many of those individuals
die either during capture or after they
are discarded (Bonfil, 1994; Stobutzki
et al., 2002; Walker, 2005a). Although,
in most studies of commercial fisher-
ies, nontargeted species are referred
to as bycatch, Walker et al. (2005)
emphasized that some of those species
are usually retained and thus consti-
tute byproduct, whereas the others
are usually discarded and therefore
constitute bycatch in the strict sense.

In an assessment of various com-
mercial fisheries throughout the world,
it was shown that trawl fisheries tar-
geting prawns generate the largest

amount of bycatch (Cook, 2003) and
that the mortality of individuals in
that bycatch is substantial (Bonfil,
1994). Indeed, it has been estimated
that approximately two thirds of the
elasmobranchs caught as bycatch in
Australia’s northern prawn trawl fish-
ery die while in the net (Stobutzki et
al., 2002). Furthermore, that study
demonstrated that most of these indi-
viduals are small, and more than half
are immature and some are caught
immediately after birth.

Many elasmobranchs are at or near
the apex of marine food webs and
thus their removal can have a sig-
nificant impact on the trophic struc-
ture of an ecosystem (Camhi et al.,
1998; Stevens et al., 2000; Shepard
and Myers, 2005). Furthermore,
certain biological characteristics of
elasmobranchs, such as their long life
spans, low fecundities, and late ages
at maturity, limit their ability both
to withstand fishing pressure, either
when targeted or caught incidentally,
and to recover from overexploitation
(Stevens et al., 2000; Walker, 2005a;
Gallucci et al., 2006). In general,
the populations of endemic species
or those that have localized distribu-
tions tend to be most prone to over-
fishing (Stevens et al., 2000). More-
over, there are little or no data on the
reproductive biology of most bycatch
species. Such data are required for
determining the resilience of these
species to fishing pressure, thereby
enabling the development of manage-

366

Fishery Bulletin 108(4)

ment plans for conserving their populations (Frisk et
al., 2001; Stobutzki et al., 2002; Walker, 2005b).

Most of the species in Australia’s rich diversity of
elasmobranchs are endemic and occupy demersal habi-
tats on the continental shelf or slope (Last and Ste-
vens, 2009) and are thus potentially prone to depletion
by demersal fishing methods such as trawling, gill-
netting, and longlining (Stobutzki et al., 2001, 2002;
Coelho et al., 2003; Perez and Wahrlich, 2005, Walker
et al., 2005). Analyses of fisheries data for 1994 to
1999 showed that the bycatch species Heterodontus
poi'tusjacksoni (Heterodontidae) and Myliobatis australis
(Myliobatidae) are abundant in catches of the temperate
demersal gillnet and longline fisheries of southwestern
Australia (McAuley and Simpfendorfer, 2003). These
two species and the rhinobatid Aptychotrema vincentia-
na and the squatinid Squatina australis, which are also
caught as bycatch by commercial fisheries, collectively
contributed as much as 17% to the total biomass of the
172 species of fish caught during extensive trawling
along the lower west coast of Australia (Hyndes et al.,
1999). It has been estimated that approximately half
of the elasmobranchs taken as bycatch by commercial
trawlers in this region are likely to die during or after
capture (Laurenson et al.1). Despite the potentially det-
rimental effects of commercial fishing on the above four
elasmobranch species and their ecological importance in
the temperate waters of southern Australia, sound bio-
logical data have been collected only for H. portusjack-
soni (McLaughlin and O’Gower, 1971; Tovar-Avila et al.,
2007; Jones et al., 2008; Powter and Gladstone, 2008).

The families to which the above four species belong
are represented elsewhere in the world by species that
are taken in substantial numbers as bycatch. For ex-
ample, in the eastern Pacific, up to a thousand individu-
als of the heterodontid shark Heterodontus mexicanus
may be caught in a single gillnet set, many of which die
(Garayzar, 2006). In some parts of the world, the popu-
lations of several species of rhinobatid and squatinid
have been so drastically depleted from overfishing that
they have been listed as critically endangered (Morey
et al., 2006; Lessa and Vooren, 2007). In eastern Aus-
tralia, the commercial landings of Myliobatis australis
have been steadily increasing to the point where their
stocks now need to be monitored (White et al., 2006).

The first aim of the present study was to determine
the numbers, and thereby the percent contributions, of
the females and males of each shark and ray species in
samples of commercial catches taken in southwestern
Australian waters by demersal trawling for prawns and
scallops and by demersal gillnetting and longlining for
sharks. These data enabled the percent contributions
made by the bycatch and byproduct to the total elasmo-

1 Laurenson, L. J. B., P. Unsworth, J. W. Penn, and R. C. J.
Lenanton. 1993. The impact of trawling for saucer scallops
and western king prawns on the benthic communities in
coastal waters off south-western Australia, 93 p. Fisheries
Res. Report, Department of Fisheries, no. 100 (part 1), Western
Australia.

branch catch to be estimated for each fishing method.
The percent contributions of each species to the catches
obtained by trawling, gillnetting, and longlining were
then used to compare statistically the species composi-
tions of the elasmobranchs in the catches taken by each
of these fishing methods.

Emphasis was next placed on determining the length
compositions of the bycatch species H. portusjacksoni,
A. vincentiana, S. australis , and M. australis in samples
collected by trawling, gillnetting, and longlining and
on estimating the lengths at maturity of the last three
of these ecologically important species. The lengths of
both the females and males at which 50% are mature
(L50) were first determined by using gonadal data as the
criterion for determining maturity and then, in the case
of males, by employing full clasper calcification as that
criterion. The L50 calculated for the males of each species
by using the two maturity criteria were then compared
to ascertain whether the L50 derived by using clasper cal-
cification as the index of maturity is a reasonable proxy
for that derived using gonadal stage as that criterion.
The L50 at maturity of A. vincentiana, S. australis, and
M. australis and of H. portusjacksoni (Jones et al., 2008)
were then employed to determine the proportions of both
sexes of each of these four species that were caught by
each fishing method before they had the opportunity to
reproduce. Finally, the management and conservation
implications of our data are considered.

Materials and methods

Sampling regime

The elasmobranchs were examined in commercial catches
from 69 demersal trawls, 24 demersal gillnets, and 19
longline sets of fishing vessels operating in southwestern
Australian waters southwards of 32° S lat. on the west
coast and then eastwards to 118° E long, on the south
coast (Fig. 1). Trawling targets the western king prawn
(Melicertus latisulcatus) and the Ballot’s saucer scallop
(Amusium balloti), whereas demersal gillnetting and
longlining target mainly the gummy shark (Mustelus
antarcticus ), the dusky shark ( Carcharhinus obscurus),
and the whiskery shark ( Furgaleus macki) (McAuley
and Simpfendorfer, 2003). Sampling, which was under-
taken between November 2002 and November 2008,
was designed to ensure that the catches of each fishing
method were sampled at least once, and generally on
at least three occasions, in each season of the calendar
year. The trawl, gillnet, and longline fishermen, whose
catches were selected for sampling, were those that
fished regularly and readily allowed us onboard, and
whose methods were representative of those used in the
area that is fished. The numbers of each elasmobranch
species caught by each fishing method on each sampling
occasion were recorded, as also were the sexes of all
individuals except for those of a few species in a small
number of trawl samples when the catches of those spe-
cies were particularly large, in which case the sexes of

Jones et al.: Species compositions of elasmobranchs caught by three commercial fishing methods

367

each individual in a large, randomly selected subsample
were recorded. Each elasmobranch species caught by
gillnetting and longlining was categorized as either
targeted, byproduct, or bycatch, whereas those taken by
trawling, where prawns and scallops are the target spe-
cies, were categorized as either byproduct or bycatch.

Trawling was undertaken mainly at depths of 8 to
13 m in a marine embayment on the lower west coast
of Western Australia and, to a lesser extent, at depths
<32 m and at distances within 20 km from the main-
land along that coast. The trawl net, in which the co-
dend consisted of 45-mm mesh, was towed for 60-180
min at a speed of ~6.5 km/h. Commercial gillnet fisher-
men deployed up to 7000 m of either 165- or 178-mm
stretched mesh net that was set for up to 24 hours at
depths of 24-73 m, whereas longlines, consisting of 360
hooks attached to approximately 6400 m of mainline,
were set for an average of 3 hours at depths of 65-73 m.

Multivariate analysis

The square root of the percent contribution of the number
of each elasmobranch species to the total catch of all
elasmobranchs recorded in each sample during regular
onboard observations of the catches taken by each fishing
method was used to construct a Bray-Curtis similarity
matrix, which was then subjected to nonmetric multidi-
mensional scaling (nMBS). One-way analysis of simi-
larities (ANOSIM) was used to test whether the species
compositions of the elasmobranch catches taken by the
three fishing methods were significantly different and,
if so, pair-wise ANOSIM tests were used to test for dif-
ferences between the compositions of the elasmobranchs
obtained by each pair of methods. The R-statistic value
was then employed to ascertain the extent of any differ-
ences between the compositions of those catches (Clarke,
1993). R-statistic values approaching 1 demonstrate
that the species composition of the a priori groups dif-
fered markedly, and a value of approximately 0 indi-
cates that the species compositions of those groups are
very similar. Similarity percentages (SIMPER; Clarke,
1993) were used to identify the species that typify the
samples obtained by each fishing method and which
species are responsible for discriminating between the
samples caught by each pair of methods. The ordination
and associated tests were undertaken with the PRIMER
vers. 6 statistical package (Clarke and Gorley, 2006).

Length and weight measurements

A randomly selected subset of individuals collected
during regular onboard observations, together with
additional randomly selected individuals provided by
commercial fishermen, yielded a total of 516 H. portus-
jacksoni, 340 A. vincentiana, 362 S. australis, and 218
M. australis, which were brought to the laboratory and
processed. The data derived from the samples were used
to construct length-frequency histograms and to derive
sex ratios and reproductive data for the species. The sex
of each individual was recorded and the total length

114°E 115°E 116°E 117°E 118°E 119°E

Figure 1

Map showing the region between the northernmost and east-
ernmost limits of southwestern Australia from which elas-
mobranchs were recorded onboard commercial trawling (dark
gray area) and gillnetting and longlining vessels (light and
dark gray areas).

(TL — tip of snout to tip of tail) and total weight (W) of
each H. portusjacksoni, A. vincentiana and S. australis
were measured and weighed to the nearest 1 mm and
1 g, respectively. The disc length ( DL — tip of snout to
the junction of the tail and pelvic fins) of each M. aus-
tralis was measured to the nearest 1 mm and the disc
width (DW) and weight of each fully intact individual
were recorded to the nearest 1 mm and 1 g, respectively.
The relationships between DW and DL, DL and DW,
and between the natural logarithms of W and DL and
of W and DW for intact M. australis were calculated by
using least trimmed squares (LTS) regression. A resam-
pling test was used to demonstrate that the above data
for the two sexes could be pooled. The above relation-
ships were used to estimate the DW and W of the small
number of M. australis (-15%) whose pectoral fins had
been removed by fishermen for commercial sale. Note
that, in the results, the sample size (n) and coefficient
of determination (r2) refer to the trimmed data for the
individuals used for the analyses.

Length at maturity

The reproductive tracts of the females and males of A.
vincentiana, S. australis, and M. australis were assigned
to one of the following maturity stages by using the crite-
ria outlined in White et al. (2001). For females, stage 1 =
uteri small and thin and oocytes not macroscopically vis-
ible; stage 2 = uteri enlarging but still thin and oocytes
becoming visible but not yet containing yolk; stage 3 =
uteri enlarged and oocytes yolked; stage 4 = pregnant,
and stage 5 = uteri or cloaca distended, indicating that
parturition had recently occurred. For males, stage 1
= seminal vesicles small and thin and testes not well
defined; stage 2 = seminal vesicles enlarging and start-
ing to become coiled, but testes not yet lobed; stage 3 =

368

Fishery Bulletin 108(4)

seminal vesicles tightly coiled and testes lobed; and
stage 4 = similar to stage 3, but with semen present
in the distal portion of the seminal vesicle. Individuals
with reproductive tracts at stages 1 and 2 are regarded
as sexually immature, whereas those at stages 3 and 4
and, in females, also at stage 5, can reproduce or have
reproduced and are therefore considered mature. When
we alternatively employed full clasper calcification as
the indicator of maturity, we considered that males with
noncalcified and partially calcified claspers were sexu-
ally immature, and those with fully calcified claspers
were mature because they have the ability to copulate.

The probability (P) that an individual is mature was
assumed to be a logistic function of its length (L):

P = jl + exp[-(a + /?L)]} , (1)

where a and /3 are parameters that determine the loca-
tion and shape of the logistic curve.

The parameters a and ft were transformed to the
lengths L50 (TL50 or DL50) and L95 (TL95 or DL95) by
which 50% and 95% of fish have attained maturity,
respectively, using the equations

^50 ~ Otl P,

(2)

L95 = D°ge(19) -«]/£■

(3)

The equation for the probability that a fish is mature
thus becomes

P = {l + exp[-loge(19)(L-L50)/(L95-L50)]} \ (4)

Logistic relationships of the above form were derived
for females and males of A. vincentiana, S. australis ,
and M. australis by using gonadal maturity status, i.e.,
>stage 3, as the criterion for maturity and, in addition,
for males, employing full clasper calcification as the
criterion for maturity. Logistic regression analysis was
used to fit these logistic curves by using Solver in Excel
(Microsoft, Redmond, WA) to maximize the log-likeli-
hood. We used likelihood-ratio tests (Cerrato, 1990) to
compare the L50 of the females and males of each spe-
cies at maturity using gonadal status as the criterion
for maturity and to compare the L50 derived for males
using both gonadal and clasper calcification status as
the criteria for maturity. For the likelihood-ratio tests,
the hypothesis that the data for both the females and
males of each species could be described by a common
logistic curve was rejected at the a=0.05 level of signifi-
cance if the test statistic, calculated as twice the dif-
ference between the log-likelihoods obtained by fitting
maturity curves with a common value of L50 for both
sexes and by fitting separate maturity curves for each
sex, exceeded ^2„(q), where q is the difference between
the numbers of parameters in the two approaches. Note
that the L50 of females and males of H. portusjacksoni
at maturity had been determined previously with this
approach (Jones et al., 2008). WinBUGS (Lunn et al.,
2000) was also used to fit the logistic curves to the

maturity-at-length data for the females and males of
each species and to calculate the proportion that were
mature at length, thereby enabling derivation of the
upper and lower confidence intervals for the L50 and
L95 values and for the proportion of mature males and
females in each 50-mm length class (see Jones et al.
[2008] for further details of this WinBUGS analysis).

Results

Species compositions by fishing method

A total of 4820 individual elasmobranchs, representing

10 families and 22 species of sharks and 7 families and

11 species of rays, were recorded during regular onboard
examinations of the catches of commercial trawl, gillnet,
and longline vessels operating off the southwestern coast
of Australia (Tables 1-3).

The 2986 elasmobranchs caught by prawn and scal-
lop trawling were dominated by rays, which comprised
10 of the 14 species and contributed 87% to the total
elasmobranch catch (Table 1). The species of a single
family of rays, the Urolophidae, comprising four spe-
cies and two genera, contributed as much as 67% to
the total trawl catch of elasmobranchs. The two species
of shark ( H . portusjacksoni and S. australis) and the
two species of ray (A. vincentiana and M. australis),
whose biological characteristics were determined (see
later), each contributed between 4.5% and 8% to the
total number of elasmobranchs caught by trawling and
collectively as much as 25% (Table 1). Two species of
shark, M. antarcticus and C. brevipinna, which were
caught in very small numbers, were retained and thus
constituted byproduct.

Gillnet catches yielded 1260 elasmobranchs, repre-
senting 19 species of shark and 6 species of ray, with
sharks contributing 96% to the total catch of elasmo-
branchs (Table 2). The most abundant species in the
gillnet catches was a targeted shark, Carcharhinus
obscurus, which contributed more than a third to the
total elasmobranch catch. The other two targeted spe-
cies, Mustelus antarcticus and Furgaleus macki, which
were dominated by females, ranked third and fifth in
terms of abundance, respectively, and contributed an
additional 14.2% and 6.5%, respectively (Table 2). The
second most numerous species, however, was the shark
H. portusjacksoni, a bycatch species, which constituted
one-fifth of the total catch. None of the six species of
ray caught by gillnetting was abundant in the catches
obtained by this method. The byproduct and bycatch
species contributed 18.7% and 25.7%, respectively, to
the total gillnet catch. Thirteen of these species, which
contributed more than one third to the total number
of individuals of elasmobranchs caught, were always
discarded as bycatch.

The 22 species of elasmobranch caught by longlining
were dominated by one of the three targeted species, M.
antarcticus, which made up 63% of the total catch of 574
individual elasmobranchs (Table 3). The next four most

Jones et al.: Species compositions of elasmobranchs caught by three commercial fishing methods

369

Table 1

Number of females and males and percentage contribution of females of each elasmobranch species (sex determined during regu-
lar onboard observations) in the catches of trawl vessels fishing for prawns and scallops on the lower west coast of Australia. The
total number of individuals of each species (including those whose sex could not be determined owing to logistic constraints) and
the percent contribution of each species to the total elasmobranch catch are also given. Plain font* = byproduct species, i.e., those
that are not targeted but usually retained; Bold font = bycatch species, i.e., those that are usually discarded.

Common name

Species name

Female

n

Male

n

Female

%

Total

n

Total

%

Lobed stingaree

Urolophus lobatus

422

288

59.4

851

28.5

Sparsely-spotted stingaree

Urolophus paucimaculatus

235

349

40.2

726

24.3

Masked stingaree

Trygonoptera personata

84

66

56.0

277

9.3

Western shovel nose ray

Aptychotrema vincentiana

124

99

55.6

237

7.9

Port Jackson shark

Heterodontus portusjacksoni

112

110

50.5

223

7.5

Southern fiddler ray

Trygonorrhina dumerilii

94

118

44.3

220

7.4

Western shovelnose stingaree

Trygonoptera mucosa

23

27

46.0

153

5.1

Southern eagle ray

Myliobatis australis

67

81

45.3

148

5.0

Australian angelshark

Squatina australis

67

66

50.4

135

4.5

Smooth stingray

Dasyatis brevicaudata

2

6

25.0

8

0.3

Gummy shark*

Mustelus antarcticus*

4

1

80.0

5

0.2

White-spotted guitarfish

Rhynchobatus australiae

1

0

100.0

1

< 0.1

Spinner shark*

Carcharhinus brevipinna *

0

1

0

1

< 0.1

Coffin ray

Hypnos monopterygius

0

1

0

1

< 0.1

Total

1235

1213

2986

abundant species, which were all bycatch, consisted of
three species of rays and the shark H. portusjacksoni
and collectively contributed nearly a quarter of the
individual elasmobranchs obtained by longlining. The
other two targeted species, C. obscurus and F. macki,
contributed only 3.8% and 0.9%, respectively, to the
total catch taken by longlining. The 19 nontargeted spe-
cies caught by longlining comprised eight species that
were always discarded as bycatch and represented one
quarter of the total catch.

On the ordination plot, derived from the similarity
matrix constructed by using percent contributions of the
various species to the elasmobranch catches obtained
by the three fishing methods, the samples for longlin-
ing lie above those for gillnetting, and both of these lie
to the right of the discrete group comprising the trawl
samples (Fig. 2). One-way ANOSIM confirmed that
the compositions of the samples obtained by the three
fishing methods were significantly different (P=0.001,
global R = 0.753). Pair-wise ANOSIM tests revealed
that the compositions in the samples collected by each
method differed significantly from those in the samples
obtained by each other method (all PcO.OOl), and the R-
statistic was similarly high for trawling vs. gillnetting
(0.797) and trawling vs longlining (0.774) and greater
than that for gillnetting vs longlining (0.515).

The most important of the typifying species for the
trawl samples, i.e., those that were most abundant and
were found most frequently, comprised two ray spe-
cies, A. vincentiana and Urolophus paucimaculatus,
and two shark species, H. portusjacksoni and S. aus-
tralis (Table 4). Heterodontus portusjacksoni and M.

Figure 2

Nonmetric multidimensional scaling (nMDS) ordina-
tion plot, derived from the matrix constructed from
the percentage contribution (square root transformed)
of each elasmobranch species recorded during each of
the regular onboard observations of the catches of com-
mercial trawling (open circles), gillnetting (gray circles),
and longlining vessels (black circles).

antarcticus were also important typifying species for
the elasmobranch catches taken by both gillnetting
and longlining. Carcharhinus obscurus is a particularly
important typifying species for the gillnet samples and
the same is true for the bycatch ray species Dasyatis
brevicaudata for the longline samples. Relatively greater

370

Fishery Bulletin 108(4)

Table 2

Number of females and males, percent contribution of females, and the total number and percent contributions of each elasmo-
branch species that were recorded during regular onboard observations of catches from gillnet vessels on the southwest coast of
Australia. Plain font = targeted species; Plain font* = byproduct species i.e., those species not targeted but usually retained; Bold
font = bycatch species, i.e., those species that are usually discarded.

Common name

Species name

Female

n

Male

n

Female

%

Total

n

Total

%

Dusky shark

Carcharhinus obscurus

229

208

52.4

437

34.7

Port Jackson shark

Heterodontus portusjacksoni

131

120

52.2

251

19.9

Gummy shark

Mustelus antarcticus

151

28

84.4

179

14.2

Sandbar shark*

Carcharhinus plumbeus*

86

59

59.3

145

11.5

Whiskery shark

Furgaleus macki

69

13

82.9

82

6.5

Southern eagle ray

Myliobatis australis

18

14

56.3

32

2.5

Spinner shark*

Carcharhinus brevipinna*

17

8

68.0

25

2.0

Western wobbegong*

Orectolobus hutchinsi*

7

11

38.9

18

1.4

Gulf wobbegong*

Orectolobus halei*

3

12

20.0

15

1.2

Smooth hammerhead*

Sphyrna zygaena*

8

4

66.7

12

1.0

Cobbler wobbegong

Sutorectus tentaculatus

7

4

63.6

11

0.9

Bronze whaler*

Carcharhinus brachyurus *

10

1

90.9

11

0.9

Spotted wobbegong*

Orectolobus maculatus*

2

7

22.2

9

0.7

Western shovelnose ray

Aptychotrema vincentiana

2

4

33.3

6

0.5

Australian angelshark

Squatina australis

2

4

33.3

6

0.5

Common sawshark

Pristiophorus cirratus

4

1

80.0

5

0.4

Southern fiddler ray

Trygonorrhina dumerilii

3

2

60.0

5

0.4

Grey nurse shark

Carcharias taurus

2

0

100.0

2

0.2

Lobed stingaree

Urolophus lobatus

1

1

50.0

2

0.2

Floral banded wobbegong

Orectolobus floridus

2

0

100.0

2

0.2

Smooth stingray

Dasyatis brevicaudata

1

0

100.0

1

< 0.1

Pencil shark*

Hypogaleus hyugaensis*

0

1

0.0

1

<0.1

Ornate angelshark

Squatina tergocellata

1

0

100.0

1

<0.1

Scalloped hammerhead*

Sphyrna lewini*

0

1

0.0

1

<0.1

Western shovelnose stingaree Trygonoptera mucosa

0

1

0.0

1

<0.1

Total

756

504

1260

and more consistent numbers of A. vincentiana were
particularly important for discriminating between the
compositions of the samples caught by trawling and
those obtained by both gillnetting and longlining, and
greater and more consistent numbers of C. obscurus
were especially important for discriminating between
the samples taken by gillnetting from those obtained
by both trawling and longlining (Table 4). The longline
samples were discriminated from those obtained by
both trawling and gillnetting by consistently greater
numbers of D. brevicaudata.

Length-frequency compositions of the four selected
bycatch species by fishing method

Wide size ranges of H. portusjacksoni, A. vincentiana ,
and S. australis and, to a certain extent, M. australis,
were caught by trawling. However, the lengths of most
H. portusjacksoni and M. australis were small and thus
lay toward the lower end of their length ranges (Fig. 3).
Although gillnetting also caught a broad size range

of both H. portusjacksoni and A. vincentiana, it yielded
predominantly larger S. australis and medium-size M.
australis (Fig. 3). Although longline catches contained
a wide size range of H. portusjacksoni and M. australis,
they did not include the smallest individuals of these
two species and only one of the A. vincentiana caught
by this method was small (Fig. 3). No S. australis was
caught by longlining.

The H. portusjacksoni obtained by all three fishing
methods ranged from 180 to 1300 mm TL (Table
5), the latter length rarely being exceeded by this
species throughout its range (Last and Stevens, 2009).
The smallest individuals possessed conspicuous um-
bilical scars and were therefore neonates. The length-
frequency distribution of female H. portusjacksoni is
trimodal, whereas that of males is bimodal, and these
modes correspond to the first two modes of females
(Fig. 4). These differences account for the lengths of
many females greatly exceeding the maximum length
of 815 mm for males (Table 5). The weights of H. por-
tusjacksoni ranged from 39 to 12,250 g (Table 5). The

Jones et al.: Species compositions of elasmobranchs caught by three commercial fishing methods

371

TabSe 3

Number of females and males, percent contribution of females and the total number and percent contributions of all individuals
of each elasmobranch species that were recorded during regular onboard observations of the catches from longline vessels on the
southwest coast of Australia. Plain font = targeted species; Plain font* = byproduct species, i.e., those that are not targeted but
usually retained; Bold font = bycatch species, i.e., those species that are usually discarded.

Common name

Species name

Female

n

Male

n

Female

%

Total

n

Total

%

Gummy shark

Mustelus antarcticus

234

129

64.5

363

63.2

Smooth stingray

Dasyatis brevicaudata

21

20

51.2

41

7.1

Southern eagle ray

Myliobatis australis

15

19

44.1

34

5.9

Southern fiddler ray

Trygonorrhina dumerilii

24

8

75.0

32

5.6

Port Jackson shark

Heterodontus portusjacksoni

20

11

64.5

31

5.4

Dusky shark

Carcharhinus obscurus

16

6

72.7

22

3.8

Smooth hammerhead*

Sphyrna zygaena*

8

1

88.9

9

1.6

Bronze whaler*

Carcharhinus brachyurus *

4

1

80.0

5

0.9

Whiskery shark

Furgaleus macki

5

0

100.0

5

0.9

Western wobbegong*

Orectolobus hutchinsi *

1

4

20.0

5

0.9

Common sawshark*

Pristiophorus cirratus *

4

1

80.0

5

0.9

School shark*

Galeorhinus galeus*

2

2

50.0

4

0.7

Western shovelnose ray

Aptychotrema vincentiana

3

0

100.0

3

0.5

Gulf wobbegong*

Orectolobus halei*

1

2

33.3

3

0.5

Sandbar shark*

Carcharhinus plumbeus*

2

0

100.0

2

0.4

Spotted wobbegong*

Orectolobus maculatus *

0

2

0.0

2

0.4

Rusty carpetshark

Parascyllium ferrugineum

0

2

0.0

2

0.4

Melbourne skate

Spinirija whitleyi

2

0

100.0

2

0.4

Spinner shark*

Carcharhinus brevipinna*

0

1

0.0

1

0.2

Australian sawtail catshark

Figaro boardmani

1

0

100.0

1

0.2

Pencil shark*

Hypogaleus hyugaensis*

0

1

0.0

1

0.2

Scalloped hammerhead*

Sphyrna lewini*

1

0

100.0

1

0.2

Total

364

210

574

ratio of females to males of H. portusjacksoni differed
significantly from parity among all individuals collec-
tively (1 female:0.76 males; j2=9.46, PcO.Ol), but not for
juveniles (1 female:1.20 males; ^2=2.65, P>0.05). Note
that, when calculating the sex ratios for juveniles, the
term juvenile refers to females and males with lengths
less than the smallest mature individual of their re-
spective sex.

The A. vincentiana caught by all three fishing meth-
ods ranged from 201 to 1001 mm TL (Fig. 4; Table
5), and the smallest individuals lay within the length
range recorded for the embryos of this species (A. Jones,
unpubl. data) and the largest individuals exceeded the
length of “at least 840 mm” reported for this species
by Last and Stevens (2009). The length-frequency dis-
tributions of female and male A. vincentiana were both
broadly bimodal and the numbers of both sexes were rel-
atively low, between 500 and 699 mm (Fig. 4). However,
the modal length class of 850-899 mm for the group of
large females far exceeded that of 700-749 mm for the
group of large males. Furthermore, the largest female
A. vincentiana was both far longer (1001 mm) and heavi-
er (3634 g) than the largest male, i.e., 872 mm and 1886
g, respectively (Table 5). The ratio of females to males

differed significantly from parity among all individu-
als (1 female:0.67 males; ^2=12.81, PcO.001), but not
among juveniles (1 female:0.76 males; ^2=3.52, P>0.05).

The smallest S. australis caught by all three fishing
methods was 228 mm in TL (Fig. 4; Table 5) and thus
only slightly longer than the length of 220 mm recorded
for the largest embryo of this species in a concomitant
study (A. Jones, unpubl. data). Although the maximum
length of 1004 mm for S. australis in our samples is
considerably less than the maximum length reported
for this species by Last and Stevens (2009), it is still
far greater than the TL50 for either females or males at
maturity in southwestern Australian waters. Although
individuals were represented in all 50-mm length class-
es between 200 and 1049 mm, the length-frequency
distributions of females and males were both dominated
by their 250-299 mm length classes (Fig. 4). The larg-
est female S. australis was far longer (1004 mm) and
heavier (10,970 g) than the largest male (859 mm and
5500 g) (Table 5). The ratio of females to males of S.
australis did not differ significantly from parity among
either all individuals collectively (1 female:1.05 males;
j2 = 0.18, P>0.05) or among juveniles (1 female:l.ll
males; j2=0.75, P>0.05).

372

Fishery Bulletin 108(4)

Table 4

Main species that typified the catches of elasmobranchs recorded onboard trawl, gillnet, and longline vessels (shaded back-
ground), and those that discriminate between the catches of elasmobranchs obtained by each pair of fishing methods (unshaded
background). Plain font = targeted species; Bold font = bycatch species; * Denotes that the species is relatively more abundant
and consistently caught by the sampling method on the top (horizontal) row than on the side (vertical) column.

Trawl

Gillnet

Longline

Trawl

Aptychotrema vincentiana

Heterodontus portusjacksoni

Urolophus paucimaculatus

Squatina australis

Gillnet

Carcharhinus obscurus

Aptychotrema vincentiana*

Carcharhinus obscurus

Heterodontus portusjacksoni

Heterodontus portusjacksoni

Mustelus antarcticus

Mustelus antarcticus

Myliobatis australis*

Furgaleus macki

Furgaleus macki

Longline

Dasyatis brevicaudata

Carcharhinus obscurus*

Aptychotrema vincentiana *

Dasyatis brevicaudata

Dasyatis brevicaudata

T rygon orrh in a dumerilii*

Mustelus antarcticus

Mustelus antarcticus

Heterodontus portusjacksoni*

Heterodontus portusjacksoni*

Trygonorrhina dumerilii

Furgaleus macki*

Heterodontus portusjacksoni

Table 5

Biological characteristics of four elasmobranch species caught as bycatch by commercial trawl, gillnet, and longline fisheries
operating off southwestern Australia. Length measurements are given as total lengths (TL) for Heterodontus portusjacksoni,
Aptychotrema vincentiana , and Squatina australis, and as disc lengths ( DL ) for Myliobatis australis. * denotes a value extrapo-
lated from the regression equation of the relation between DL and W. The true weight could not be recorded because the pectoral
fins had been removed by fishermen. Sample size for each sex of each species is shown on Figure 4.

Heterodontus

portusjacksoni

Aptychotrema

vincentiana

Squatina

australis

Myliobatis

australis

Females

Length range (mm)

198-1300

201-1001

228-1004

118-800

Weight range (g)

39-12,250

32-3634

94-10,970

117-37,811*

Smallest mature (mm)

715

754

825

444

Largest immature (mm)

869

895

834

472

Males

Length range (mm)

180-815

214-872

246-859

129-545

Weight range (g)

39-3920

33-1886

115-5500

152-12,373*

Smallest mature (mm)

595

642

754

365

Largest immature (mm)

654

792

707

433

The relationships between DW and DL for females
and males of M. australis collectively are described by
the following equations:

DW = 1.70 DL + 8.16 (r 2=0.997, n = 96), (5)

DL = 0.58 DW - 3.01 (r 2=0.998, n = 96). (6)

From the values obtained from the above equations,
the following relationships between the natural loga-

rithms of W and DL, and of W and DW for both sexes
are described as

loge W = 2.91 loge DL - 8.92 (r 2=0.999, n=91), (7)

loge W = 3.19 loge DW - 12.25 (r 2=0.999, n= 91). (8)

After correction for bias (Beauchamp and Olson,
1973), the respective back-transformed relationships
became

Jones et al.: Species compositions of elasmobranchs caught by three commercial fishing methods

373

B Gillnet

0 200 400 600 800 1000 1200 1400

Length (mm)

Figure 3

Length-frequency distributions for all males and females of
Heterodontus portusjacksoni, Aptychotrema viticentiana, Squatina
australis, and Myliobatis australis obtained from the commercial
catches of (A) trawl, (B) gillnet, and (C) longline vessels. Length
refers to total length ( TL ), except in the case of M. australis
where it refers to disc length (DL).

W = 0.0001344 DL2 91, (9)

W = 0.000004787 DW3 19 (10)

The M. australis caught by using the three
sampling methods ranged from 118 to 800
mm DL (Fig. 4, Table 5), which corresponds
to 198-1192 mm DW. The minimum DW is at
the extreme lower end of the range reported for
this species at birth, and the maximum DW is
appreciably less than the maximum DW of 1600
mm recorded for M. australis (Last and Stevens,

2009). The largest female caught was 800 mm
DL and 37,811 g W, which greatly exceeded the
545 mm DL and 12,373 g W of the largest male
(Table 5). Both sexes were represented in each
DL class between 100 and 549 mm, and females
were also present in each subsequent size class
up to 800-849 mm (Fig. 4). The length-fre-
quency distributions for both sexes contained a
single prominent modal length class at 150-199
mm. The ratio of 1 female:1.27 males of M.
australis among the individuals caught by all
methods collectively did not differ significantly
from parity (^2=3.10, P>0.05), and the same
was true for juveniles, i.e., 1 female:1.04 males
(^2=0.06, P>0.05).

Lengths of females and males at maturity

The smallest female and male of H. portusjack-
soni with mature gonads measured 715 and 595
mm TL, respectively (Table 5). Using gonadal
stage as the index, we found that the TL50 for
female H. portusjacksoni at maturity was 805
mm, and the TL50 for males was 593 mm, which
represent 62% and 73% of their respective maxi-
mum TL. The TL50 for males was only 12 mm
greater and not significantly different from the
581 mm derived by using full clasper calcifica-
tion as the index of maturity (Table 6, see also
Jones et al., 2008).

The smallest female and male of A. vin-
centiana with mature gonads were 754 and
642 mm, respectively, and all females >896
mm and males >793 mm were mature (Fig. 5,

Table 5). The TL50 for females of 798 mm at
maturity differed significantly (P<0.001) from
the corresponding TL50 for males of 671 mm
when using gonadal stage as the criterion for maturity
(Table 6). The latter TLg0 for males did not differ sig-
nificantly from the TL50 of 654 mm derived by using
full clasper calcification as the criterion for maturity
(P> 0.05) (Fig. 5, Table 6). The TL50 for female and
male A. vincentiana at maturity, using gonadal status
as the criterion for maturity, were 80% and 77% of
their respective maximum TL.

On the basis of gonadal data, the TL of the smallest
mature female and male S. australis were 825 and 754
mm, respectively, and all females >840 mm and all

males >754 mm were mature (Fig. 5, Table 5). The TL50
for females (823 mm) and males of S. australis (734
mm), derived by employing gonadal stage as the crite-
rion for maturity, were significantly different (PcO.001;
Table 6). The latter TL50 was not significantly different
(P> 0.05) from the TL50 of 721 mm derived for male S.
australis when using clasper calcification as the crite-
rion for maturity (Fig. 5, Table 6). The TL50 calculated
for females and males of S. australis, with gonadal
stage as the criterion for maturity, were 82% and 85%
of their respective maximum TL.

374

Fishery Bulletin 108(4)

The DL of the smallest females and males of M. aus-
tralis with mature gonads were 444 and 365 mm, re-
spectively, and all females and males with DL >513
and 433 mm, respectively, were mature (Fig. 5, Table
5). The DL50 of 511mm (DW50 = 879 mm) for females at
maturity differed significantly (P<0.001) from the 399
mm (Z)W50 = 689 mm) of males when gonadal status was

used as the criterion for maturity (Table 6). The latter
DL50 did not differ significantly (P>0.05) from the 388
mm (DW50 = 670 mm) derived for males at maturity
with clasper calcification as the criterion for maturity
(Table 6). On the basis of gonadal criteria, the DL50 for
females and males of M. australis at maturity were 64%
and 73% of their DLmax, respectively.

40 r

B Aptychotrema vinceritiana

D Myliobatis australis

females n=203

males a=137

females n=96

males n=122

i . i

0 200 400 600 800 1000 1200 1400

Length (mm)

Figure 4

Length-frequency distributions for females (white histograms)
and males (black histograms) of (A) Heterodontus portusjacksoni,
(B) Aptychotrema vinceritiana, (C) Squatina australis , and (D)
Myliobatis australis obtained collectively by all three fishing
methods. Length refers to total length ( TL ), except in the case
of M. australis where it refers to disc length (DL).

Percentage of females and males caught
by each fishing method

The percentage of females of H. portusjacksoni, A.
vincentiana, S. australis and M. australis caught
in trawls with lengths below the L50 (TL5 0 or
DL50) at maturity were very high and similar to
those of males (Table 7). The percentage in trawl
samples of both sexes with lengths less than their
L50 at maturity ranged from 63% for A. vincen-
tiana, to 90% for both M. australis and S. aus-
tralis, respectively, to 97% for H. portusjacksoni
(Table 7). In the case of gillnet samples for three
of the four species, the percentage of females with
lengths less than their L50 at maturity exceeded
those of males and particularly so for M. australis,
for which the values were 86% and 40%, respec-
tively (Table 7). In longline samples, the percent-
age of males of H. portusjacksoni with lengths
below their L50 at maturity slightly exceeded the
corresponding value for females (37% and 32%,
respectively).

Discussion

This study is the first to quantify the contribu-
tion of each elasmobranch species to the total
elasmobranch catch obtained by co-occurring
trawl, gillnet, and longline fisheries, and to cal-
culate the contributions made by the bycatch
and byproduct species to the catches taken by
each fishing method. In addition, our results
indicate that nMDS ordination and associated
tests would be invaluable for detecting whether
the species composition of elasmobranchs in the
catch produced by each fishing method changes
in the future in response to either variations in
fishing activity or environmental factors and,
if so, also for elucidating the magnitude of that
effect. This study has also produced, for four
abundant bycatch species, the sound quantitative
biological data of the types required by manag-
ers for developing plans for conserving stocks
and which are deficient for the vast majority
of bycatch species (Stobutzki et al., 2002). The
sizes at maturity that were determined for the
four bycatch species in this study enabled the
proportion of each species, which was caught by
each fishing method before it had the potential
to reproduce, to be estimated.

Jones et al.: Species compositions of elasmobranchs caught by three commercial fishing methods

375

Table 6

Estimates of the L50 and L95 at maturity, and the upper and lower 95% confidence limits (CL), for females and males of Heter-
odontus portusjacksoni, Aptychotrema vincentiana, and Squatina australis recorded as total length (TL). For Myliobatis austra-
lis, these values were recorded as disc length ( DL ); extrapolated values for disc widths (DW) are also provided. Estimates were
derived by using gonadal status as an index of maturity for females and males and also by using full clasper calcification as that
index for males. Sample sizes for females and males of each species are provided in Figure 4.

Female (gonads)

Male (gonads)

Male (claspers)

^50

■^95

^50

■^95

■^50

•^95

Heterodontus portusjacksoni

Estimate

805

896

593

647

581

652

Upper 95% CL

826

931

605

674

594

689

Lower 95% CL

781

866

579

628

563

629

Aptychotrema vincentiana

Estimate

798

877

671

766

654

707

Upper 95% CL

815

920

695

833

676

756

Lower 95% CL

774

855

631

736

618

679

Squatina australis

Estimate

823

852

734

735

721

723

Upper 95% CL

842

927

753

806

753

806

Lower 95% CL

771

826

673

714

674

714

Myliobatis australis

Estimate

511

585

399

472

388

453

Upper 95% CL

558

696

416

518

404

491

Lower 95% CL

480

538

376

440

366

420

Female (gonads)

Male (gonads)

Male (claspers)

dw50

dw95

dw50

dw95

dw50

dw95

Myliobatis australis

Estimate

879

1006

689

813

670

781

Upper 95% CL

960

1195

717

891

697

845

Lower 95% CL

827

926

649

758

632

724

Table 7

Numbers of females and males and total number of Heterodontus portusjacksoni , Aptychotrema vincentiana, Squatina australis,
and Myliobatis australis that were caught by each fishing method and examined in the laboratory, and the percentages of indi-
viduals with lengths less than their L50 at maturity when using gonadal status as the index of maturity. L50 refers to total length
(TL50), except in the case of M. australis where it refers to disc length ( DL50 ).

Fishing method

Species name

Females

Males

Sexes combined

n

% < L50

n

% < L50

n

% < L50

Trawl

Heterodontus portusjacksoni

121

98

128

96

249

97

Aptychotrema vincentiana

182

62

116

66

298

63

Squatina australis

155

89

169

91

324

90

Myliobatis australis

71

92

83

87

154

90

Gillnet

Heterodontus portusjacksoni

115

44

76

30

191

38

Aptychotrema vincentiana

16

38

20

30

36

33

Squatina australis

22

18

16

19

38

18

Myliobatis australis

14

86

25

40

39

56

Longline

Heterodontus portusjacksoni

57

32

19

37

76

33

Aptychotrema vincentiana

5

0

1

100

6

17

Squatina australis

—

—

—

—

—

—

Myliobatis australis

11

36

14

7

25

20

376

Fishery Bulletin 108(4)

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Jones et al.: Species compositions of elasmobranchs caught by three commercial fishing methods

377

Compositions of the catches taken by the three
fishing methods

Our results indicate that the elasmobranch component of
the catches taken by demersal trawlers on the lower west
coast of Australia is dominated by rays, which comprise
10 of the 14 elasmobranch species caught by this method.
Furthermore, these batoids were either small species,
e.g., stingarees, or represented by smaller individuals,
e.g ., Aptychotrema vincentiana and M. australis. Indeed,
the four small species of stingaree (Urolophidae) caught
by trawling contributed as much as two-thirds to the
total trawl catch of elasmobranchs and were so abun-
dant in samples collected during an extensive trawling
study along the lower west coast of Australia that they
collectively contributed 17.5% to the total biomass of
the 172 fish species caught during that study (Hyndes
et al., 1999). The large number of small batoids caught
paralleled the situation recorded for other trawl fisher-
ies, including the multispecies bottom trawl fishery off
Argentina (Tamini et al., 2006). As with the large ray
species, the only two shark species taken in appreciable
numbers in our study, H. portusjacksoni and S. australis,
were represented predominantly by small individuals.

The large number of elasmobranchs taken by prawn
and scallop trawling emphasizes the lack of selectivity
of this fishing method for its targeted species. Indeed,
Bonfil2 has stated that towed nets are the most indis-
criminant of all fishing gears because they are designed
to capture everything in their path and thus inevitably
encounter a large number of nontarget species. The
susceptibility of small demersal elasmobranchs to cap-
ture by trawling is due to their limited mobility and
benthic lifestyle (see also Stobutzki et al., 2001, 2002;
Walker, 2005a; Tamini et al., 2006) and to the trawlers
often operating in nearshore waters, which typically
act as nursery areas for several elasmobranch species,
including H. portusjacksoni (White and Potter, 2004;
Jones et al., 2008; Kinney and Simpfendorfer, 2009).
The catches of elasmobranchs taken by trawls in our
study comprised only six individuals that were retained
as byproduct compared with the 2980 individuals dis-
carded as bycatch.

Although the three species targeted by gillnetting,
C. obscurus, M. antarcticus, and Furgaleus macki, col-
lectively accounted for just over half of the total number
of elasmobranchs caught by this method, the contri-
bution of all retained species (i.e. including byprod-
uct), accounted for three quarters of the total. This
is very similar to the situation recorded for a gillnet
fishery in southeastern Australia (Walker et al., 2005).
The remainder of the catch (i.e., the bycatch) was still
substantial, however, emphasizing that a considerable
number of the sharks and rays caught by gillnet were

2 Bonfil, R. 2000. The problem of incidental catches of sharks
and rays, its likely consequences, and some possible solu-
tions. Shark Conference 2000 online documents, 8 p. (Pacific
Fisheries Coalition, http://www.pacfish.org/sharkcon/docu-
ments/bonfil.html, accessed May 2010).

discarded, as has been reported in gillnet fisheries else-
where in the world (e.g., Perez and Warhlich, 2005).

The mesh sizes of the gillnets (165 and 178 mm) were
selected to catch the three targeted species, C. obscu-
rus, M. antarcticus, and F. macki, at a marketable size
which, depending on the species, typically corresponded
to modal fork lengths of between 800 and 1200 mm
(McAuley and Simpfendorfer, 2003). This mesh selec-
tivity accounts for the fact that the TL of the majority
of A. vincentiana and S. australis in our gillnet catch-
es fell within a relatively narrow range of 700-1000
mm, with the latter length closely approximating the
maximum length recorded for these two species dur-
ing the present study (Table 5). However, the TL for
H. portusjacksoni, the second most abundant species
in the gillnet catches, spanned the full range of this
species in southwestern Australian waters (Jones et al.,
2008). The capture by gillnet of a substantial number
of H. portusjacksoni with lengths less than 700 mm is
attributable to the tendency for all sizes of H. portus-
jacksoni to become entangled in gillnets as a result of
their possessing prominent dorsal fin spines (Walker,
2005a). In the case of the ray M. australis, the larger
individuals were proportionately less in gillnet than
longline catches because this wide disc-shaped species
becomes increasingly deflected from the net as it grows
larger (Walker, 2005a).

Longlining was so successful at targeting M. ant-
arcticus that this shark contributed nearly two thirds
to the total elasmobranch catch taken by this method
and, together with the other two targeted species, C.
obscurus and F. macki, represented nearly 70% of that
total catch. However, those last two species were not
abundant in these catches. In fact, the second to fifth
most abundant species were bycatch species. Although
11 of the 19 nontargeted elasmobranch species were
typically retained as byproduct, none of those species
was numerous and collectively accounted for only ~7%
of the elasmobranch catch. From the above, it follows
that the contribution of bycatch to the longline catches
(-26%) was similar to that in the gillnet catches. How-
ever, unlike the situation with gillnetting, the bycatch
species S. australis was never caught on longline hooks,
presumably because this squatinid is an ambush preda-
tor that targets mobile prey such as teleosts and cepha-
lopods (E. Sommerville, personal commun.3).

Although the use of nMDS ordination and associ-
ated tests emphasized that the species compositions of
the elasmobranchs caught by trawling, gillnetting, and
longlining differed markedly, SIMPER showed that H.
portusjacksoni was a major typifying species for the
elasmobranchs taken by trawling in relatively shal-
low waters and by gillnetting and longlining in deeper
and more offshore waters. This bycatch species is thus
clearly abundant and widely distributed throughout the
inshore and more offshore coastal waters of southwest-

3 Sommerville, Emma. 2007. Centre for Fish and Fisher-
ies Research, Murdoch Univ., Murdoch, Western Australia,
6150.

378

Fishery Bulletin 108(4)

ern Australia. The finding that the ray D. brevicaudata
was the most important typifying species in the long-
line samples indicates that this bycatch species was
consistently present in reasonable numbers in water
depths of approximately 70 m. Although the total num-
ber of M. antarcticus obtained by longlining was far
greater than that of D. brevicaudata , M. antarcticus
was occasionally taken in large numbers and, at other
times, not caught at all, reflecting the tendency for this
shark species to school (Lenanton et al., 1990; Last and
Stevens, 2009).

Length compositions, sex ratios, and habitats
of the four selected bycatch species

Our data indicate that the maximum lengths of the
females of H. portusjacksoni, A. vincentiana, S. austra-
lis, and M. australis exceed those of males by 37%, 13%,
14%, and 31%, respectively. Moreover, for each species,
the sex ratio did not differ significantly from parity
among their juveniles, and the females dominated the
length classes of the larger individuals. The resultant
trend for the overall sex ratios for H. portusjacksoni and
A. vincentiana to significantly favor females indicates
that the females of at least these two species live longer
than their males. Such a conclusion for H. portusjack-
soni in southwestern Australian waters is consistent
with the results of Tovar-Avila et al. (2009), who showed
that, in southeastern Australia, the maximum age of the
females (35 years) of this species is greater than that
of males (28 years). Although the overall sex ratios of
S. australis and M. australis did not differ from parity,
those ratios were almost certainly attributable to the
larger individuals of these two species being propor-
tionately less well represented in the overall samples
of those species. In the case of S. australis, the capture
of fewer larger individuals was mainly due to this spe-
cies not being taken by longlining fisheries in deeper,
offshore waters, where they had been caught by gillnet-
ting, and thus the overall samples were swamped by
juveniles caught by trawls in their nursery areas. The
conclusion that larger females were under-represented
in the overall catch of M. australis is consistent with
a tendency for the larger individuals, which would
presumably have been predominantly females, to be
deflected from the net.

The difference between the maximum lengths of the
females and males of H. portusjacksoni in southwestern
Australian waters (37%) was far greater than the 19%
and 10% differences recorded for two populations of
this species in southeastern Australian (Tovar-Avila et
al., 2007) and the 15% difference found farther north
in eastern Australia (Powter and Gladstone, 2008).
The trend for females to attain a larger size than that
of males parallels that reported by Cortes (2000) for
populations representing 164 species and 19 families
of sharks. However, the average difference between the
sizes of females and males reported by Cortes (2000)
was 10% and thus smaller than the differences observed
for particularly H. portusjacksoiii and M. australis.

Comparisons of the length-frequency distributions for
each of H. portusjacksoni, A. vincentiana, S. australis,
and M. australis in samples obtained from trawling
in inshore waters, and by gillnetting and longlining
farther offshore, indicated that all four species use
shallow, inshore waters as nursery areas and that sub-
stantial numbers of the adults of S. australis and M.
australis are also present in these inshore habitats.
The tendency for M. australis to use inshore areas as
nursery areas in southwestern Australia is emphasized
by the considerable numbers of juveniles of this species
that were caught during a study of a permanently open
estuary on the south coast of Western Australia (Pot-
ter and Hyndes, 1994). Furthermore, the juveniles of
H. portusjacksoni are also abundant in inshore waters
off eastern Australia (McLaughlin and O’Gower, 1971).
Because several of the mature females of A. vincentiana
caught in inshore waters contained full-term embryos,
they would have been poised to give birth in those wa-
ters. However, because adults of H. portusjacksoni, A.
vincentiana, and M. australis were caught by gillnetting
and longlining, and S. australis was caught by longlin-
ing, some individuals of each of these species move
offshore as they increase in size and some may even
live permanently in offshore waters.

Lengths at maturity and their implications

The greater maximum length attained by females than
by males of each of the four elasmobranch species was
accompanied, on the basis of gonadal criteria, by a
greater L50 at maturity, and the differences in L50
ranged from 12% for S. australis and 19% for A. vin-
centiana to as high as 28% for M. australis and 36% for
H. portusjacksoni. The trend for the females of these
species to mature at a larger size than that of males
follows the overall trend exhibited by shark species
(Cortes, 2000).

The values derived for the L50 at maturity for the
males of A. vincentiana, S. australis, and M. australis
by using full clasper calcification as the criterion for
maturity did not differ significantly from the corre-
sponding values derived by using gonadal maturity as
that criterion. This result parallels that recorded for H.
portusjacksoni by Jones et al. (2008), for Squalus maga-
lops by Braccini et al. (2006), and for Trygonorrhina
dumerilii by Marshall et al. (2007). Thus, to obtain data
that can subsequently be used to derive a reasonable
proxy for the L50 for males at maturity, scientists can
rapidly record the lengths of males, determine whether
or not their claspers are calcified, and then immediately
return them live to the sea. Furthermore, for each of
the four species, all of the males with uncalcified clasp-
ers and most of those with partially calcified claspers
possessed immature (stage 1 or 2) gonads, whereas
those with fully calcified claspers almost invariably
contained mature (stage 3 or 4) gonads and this finding
thus accounts for the L50 at maturity not being signifi-
cantly different when gonadal and clasper calcification
criteria are used.

Jones et al.: Species compositions of elasmobranchs caught by three commercial fishing methods

379

On the basis of our calculations of the L50 at matu-
rity for females and males of each of the four selected
bycatch species, the overall percentages, in trawl sam-
ples, of H. portusjacksoni, S. australis, and M. australis,
whose individuals would not typically have had the
potential to reproduce, were particularly high, with
values ranging from 90% to 97%. These high values
are attributable to trawling taking place mainly in
shallow inshore waters that typically act as nursery
areas. The importance of protecting the newborn and
young juveniles of species that have well-defined nurs-
ery areas has been emphasized by Walker (2005a). The
far lower percentage of A. vincentiana with lengths less
than the L50 at maturity in trawl samples than was
the case with the other three species is attributable to
the tendency for this species to occupy inshore waters
throughout its life.

The smaller proportion of individuals of H. portus-
jacksoni, A. vincentiana, S. australis, and M. austt'alis
with lengths less than their Lgo at maturity in gillnet
than in trawl catches reflects a combination of the fol-
lowing: 1) differences in gear selectivity; the mesh sizes
of gillnets are chosen with the purpose of catching
targeted species at a sufficient size to be commercially
marketed (Simpfendorfer and Unsworth, 1998; McAu-
ley and Simpfendorfer, 2003) and thereby obtaining
proportionately more of the larger, mature individuals
of these four bycatch species than their juveniles; and
2) the location of gillnetting in deeper, offshore waters
and thus beyond typical nursery areas.

Mortality

Onboard sampling of the catches obtained by the three
fishing methods during commercial operations was made
difficult by the small size of the fishing boats and the
rapidity with which the fishermen worked to retrieve the
retained species and discard the bycatch. It was thus not
possible to determine precisely the fishing-induced mor-
tality of the individuals of each bycatch species taken
by each fishing method and, in particular, the mortality
of H. portusjacksoni, A. vincentiana, S. australis, and
M. australis. From our observations, however, it is appar-
ent that, in the case of trawling, many individuals died
while in the net and those that survived were often so
badly injured during sorting that they would have been
unlikely to survive after release. From our observations,
we believe that the level of mortality associated with
trawling is greater than that suggested by Laurenson et
al.1, who proposed that approximately half of the elasmo-
branchs taken by trawling during a research project on
the lower west coast of Australia was likely to die during
capture or after being discarded. Indeed, in a detailed
study of the bycatch of Australia’s northern prawn trawl
fishery, Stobutzki et al. (2002) showed that as much as
two-thirds of the sharks and rays caught by this method
died while still in the net, and thus the overall mortal-
ity, i.e., including individuals that subsequently died
from the trauma of capture, would have been higher.
It should also be recognized that the pregnant females

of the smaller species of rays (White and Potter, 2004)
and S. australis and M. australis tended to abort after
capture, thus adding a further detrimental effect to the
populations of those species.

It was evident that the individuals of most species,
including those of the three targeted species, M. ant-
arcticus, C. obscurus, and F. macki, and several bycatch
species, such as M. australis and S. australis, had died
by the time the gillnet was retrieved. It is proposed that
this high mortality was related to the very long soak
times of the gillnets (up to 24 h), which is consistent
with the observation that mortality was far lower in
a gillnet study conducted in southeastern Australia
in which soak times were only ~8 h (Walker et al.,
2005). Furthermore, the long soak times led to the
elasmobranchs in the nets becoming infested by sea lice
( Cirolana sp.) and to attack by leatherjackets (Mona-
canthid spp.), thus hastening the death of species such
as M. australis. Moreover, although H. portusjacksoni
frequently survived capture by gillnets, the individuals
of this species were often severely injured while being
forcibly removed from the gillnets.

In contrast to the situation with gillnetting, the ma-
jority of elasmobranchs survived capture by longlining
and thus, in general, the individuals of bycatch species
caught by hooks were able to be returned to the sea
alive. The high survival of elasmobranchs caught by
longlining in southwestern Australia is presumably at-
tributable, at least in part, to the short set times (~3
h) for this fishing method.

Implications for ecosystem-based fisheries management

Traditional fisheries management has focused on
ensuring that the populations of targeted species are
maintained at levels that are considered sustainable.
However, fisheries regulations aimed at constraining the
exploitation of targeted species may provide little protec-
tion for bycatch species, and thus commercial fisheries
can have an equal or even greater impact on the popu-
lations of bycatch species. In contrast, ecosystem-based
fisheries management, i.e., an ecosystem approach to
fisheries, requires that the populations of bycatch spe-
cies in an ecosystem, as well as those of the targeted
and byproduct species, are sustained. It is thus relevant
that our study revealed that many individuals of the
elasmobranch bycatch species caught by commercial
fisheries, and particularly by trawling, were immature
and, together with our observations and the results of
other studies, strongly indicated that mortality is high
among these individuals. The problems posed by such
fisheries-induced mortalities on these bycatch species
are exacerbated because elasmobranchs have low biologi-
cal productivity and are therefore susceptible to over-
exploitation (Stevens et al., 2000; Walker, 2005a). Thus,
while it is recognized that the trawl, gillnet, and longline
fisheries of southwestern Australia are not large, the
removal of even moderate numbers from the population
of any elasmobranch species has the potential to affect
that population at a local level (Walker, 2005a).

380

Fishery Bulletin 108(4)

In the context of the ecosystem-based fisheries man-
agement framework, every attempt should be made to
reduce, where practical, the amount of bycatch. In view
of the high mortality of the bycatch species taken by
trawlers and gillnetters, commercial fishermen should
be encouraged to explore ways of reducing the amount
of bycatch and of increasing survival among discarded
individuals. Thus, with trawling for example, fisher-
men could explore the effectiveness of bycatch reduc-
tion devices, reduce the duration of trawls and onboard
handling time, and unload the catch into water tanks
before sorting. In the case of gillnetting, fishermen
could explore whether a reduction in the soak time of
their nets leads to a decrease in the mortality of the
bycatch and an increase in the market quality and
thus the value of the flesh of the retained species.

The biological and catch data produced during this
and other studies on locally abundant bycatch species
of elasmobranchs (White et al., 2001; 2002; White
and Potter, 2005; Marshall et al., 2007) indicate that
trawl, gillnet, and longline fisheries may be having
a direct impact on the populations of these species
in southwestern Australia. The acquisition of these
data now enables managers to determine whether the
impacts of commercial fisheries on the populations of
bycatch species justify modifying fishing regulations
to ensure that the risks to the sustainability of these
species are reduced and that the integrity of the eco-
system is thus maintained. Such risks could readily
be achieved through the use of rapid assessment tech-
niques, such as those described by Stobutzki (2001;
2002) and Walker et al. (2005).

Acknowledgments

Special thanks are extended to the commercial fisher-
men, and particularly to H. Gilbert, P. Dyer and A.
Butler, whose help was invaluable for obtaining samples,
to P. Coulson, D. French, and B. Farmer, who assisted
in sampling, and to A. Hesp for his statistical advice.
We also thank three anonymous referees for their con-
structive comments, which have led to an improved
manuscript. Funding for this project was provided by
FISHCARE WA and Murdoch University.

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382

Abstract — Pacific cod (Gadus macro-
cephalus ) is an important component
of fisheries and food webs in the North
Pacific Ocean and Bering Sea. How-
ever, vital rates of early life stages of
this species have yet to be described
in detail. We determined the ther-
mal sensitivity of growth rates of
embryos, preflexion and postflexion
larvae, and postsettlement juveniles.
Growth rates (length and mass) at
each ontogenetic stage were measured
in three replicate tanks at four to five
temperatures. Nonlinear regression
was used to obtain parameters for
independent stage-specific growth
functions and a unified size- and tem-
perature-dependent growth function.
Specific growth rates increased with
temperature at all stages and gener-
ally decreased with increases in body
size. However, these analyses revealed
a departure from a strict size-based
allometry in growth patterns, as
reduced growth rates were observed
among preflexion larvae: the reduc-
tion in specific growth rate between
embryos and free-swimming larvae
was greater than expected based on
body size differences. Growth reduc-
tions in the preflexion larvae appear
to be associated with increased meta-
bolic rates and the transition from
endogenous to exogenous feeding. In
future studies, experiments should
be integrated across life transitions
to more clearly define intrinsic onto-
genetic and size-dependent growth
patterns because these are critical for
evaluations of spatial and temporal
variation in habitat quality.

Manuscript submitted 12 March 2010.
Manuscript accepted 8 June 2010.
Fish. Bull. 108:382-392 (2010).

The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not
necessarily reflect the position
of the National Marine Fisheries
Service, NOAA.

Ontogenetic patterns and
temperature-dependent growth rates
in early life stages of Pacific cod
( Gadus macrocephalus )

Thomas P. Hurst (contact author)1
Benjamin J. Laurel1
Lorenzo Ciannelli2

Email address for contact author: thomas.hurst@noaa.gov

1 Fisheries Behavioral Ecology Program

Resource Assessment and Conservation Engineering Division
Alaska Fisheries Science Center,

National Marine Fisheries Service, NOAA
Hatfield Marine Science Center
Newport, Oregon 97365

2 College of Atmospheric and Oceanographic Sciences
Oregon State University

Corvallis, Oregon 97331

Fluctuations in the distribution and
abundance of marine species are
highly influenced by climate-driven
changes in ocean conditions (Perry et
al., 2005). In the Gulf of Alaska and
Bering Sea, oceanographic regimes
linked to climate conditions (Hollowed
et al., 2001; Peterson and Schwing,
2003) occur across a variety of time
scales, from seasonal to multidecadal
(Hunt and Stabeno, 2002). These cli-
mate cycles have been linked to major
shifts in the composition of valuable
groundfish communities (Anderson
and Piatt, 1999). Imposed upon this
variation is the potential for longer-
term climate changes, such as the
warming of surface waters and loss of
sea ice (e.g., Hunt et al., 2002). Such
warming trends have already been
observed in the Gulf of Alaska (Royer
and Grosch, 2006) and Bering Sea
(Stabeno et al., 2007). The response
of individual populations and entire
communities to environmental forcing
depends upon the physiological and
behavioral traits of individual spe-
cies and the cumulative set of trophic
interactions between species (Freitas
et al., 2007; Yatsu et al., 2008; Hurst
et al., 2010).

Spatial and temporal variation in
temperature and prey availability
are considered to be primary driv-
ers of growth and survival in early

life stages of fishes and their influ-
ence on recruitment has been central
to various generalized models of re-
cruitment (see review by Cowen and
Shaw, 2002). The oscillating control
hypothesis (OCH) states that popu-
lation production of groundfish in
the Bering Sea is linked to climate-
driven patterns of prey production:
cold winters with extensive sea ice
result in early, low-density blooms
in cold water, resulting in reduced
survival of larvae (Hunt and Sta-
beno, 2002). Evaluation of the OCH
and predicting potential responses
to future aspects of climate change
require detailed information on the
temperature-dependent vital rates of
early life stages of fish (Kristiansen
et al., 2007; Hollowed et al., 2009;
Rijnsdorp et al., 2009).

Pacific cod (Gadus macrocephalus)
is a widespread marine species on
continental shelves throughout the
eastern and western North Pacific
and Bering Sea. They are an im-
portant component of North Pacific
and Bering Sea fisheries and food
webs. In recent years, U.S. land-
ings of Pacific cod trail only those
of Alaska walleye pollock (Theragra
chalcogramma ) and Atlantic and gulf
menhaden (Brevoortia tyrannus and
B. patronus) (NMFS, 2008). Between
2002 and 2006, U.S. landings of Pa-

Hurst et al.: Growth rates of Gadus macrocepha/us

383

Table 1

Summary of experiments conducted at the Alaska Fisheries Science Center laboratory in Newport, Oregon, where growth rates
were determined for early life stages of Pacific cod (Gadus macrocephalus ) collected from the central Gulf of Alaska.

Stage

Temperatures

(°C)

Year

Experiment duration
(dah=days after hatching)

Sample type

No of tanks

n fish

Eggs

0, 2, 4, 6, 8

2006

Fertilization to hatching

Measured at hatching

15

30/sample

Preflexion larvae

3, 8

2007

Hatching to 35 dah

Tank sample

6

10/sample

2, 5, 8

2008

Hatching to 36 dah

Tank sample

9

10/sample

Postflexion larvae

2, 4, 8, 11

2007

50 to 105 dah

Tank sample

12

10/sample

Juveniles

2, 5, 8, 11

2008

approx. 132 to 150 dah

Serial measures

12

10/tank

cific cod averaged 28 times those of Atlantic cod ( Gadus
morhua ).

Despite the pervasive influence of temperature on all
aspects of biology and its potential linkage to recruit-
ment patterns, there has been little examination of
the thermal ecology of Pacific cod. The effects of tem-
perature on the vertical distribution of larvae (Hurst
et al., 2009) and juveniles (Davis and Ottmar, 2009)
have been examined. Thermal effects on growth of Pa-
cific cod has been examined in only the very early life
stages: development rates of eggs and prefeeding larvae
(Alderdice and Forrester, 1971; Laurel et al., 2008) have
been examined across a wide range of temperatures.
In addition, B. J. Laurel (unpubl. data) compared the
effects of prey density on growth of preflexion larvae at
two temperatures. However, these studies are insuffi-
cient to describe the functional response to temperature
for larvae, and as of yet, no data exist for later larval
stages or juveniles.

In this article we describe the growth of early life
stages of Pacific cod as a function of temperature and
body size. Separate experiments were conducted with
preflexion larvae, postflexion larvae, and postsettlement
juveniles. From these experiments and published data
on embryos, we determined the parameters for models
of stage-specific growth and for an integrated model of
size- and temperature-dependent growth. These func-
tions will be used to evaluate the relative contribu-
tions of temperature and feeding conditions to observed
variation in growth among wild Pacific cod (Folkvord,
2005; Hurst et al., 2010).

Materials and methods

We determined the thermal sensitivity of growth rates
at three life stages: preflexion larvae, post-flexion larvae,
and postsettlement juveniles (Table 1). Growth rates at
each ontogenetic stage were measured in three replicate
tanks at four to five temperatures, encompassing the
range likely to be encountered by fish in the Gulf of
Alaska and Bering Sea. Nonlinear regression was used
to describe the relationship between growth rate and
temperature at each developmental stage and to describe

the combined effects of temperature and body size on
growth rates of early life stages.

Preflexion larvae

Two experiments were conducted to describe the growth
of Pacific cod larvae after hatching. In 2008, fish were
reared at 2°, 5°, and 8°C to 36 days after hatching (dah).
These data were combined with data on fish reared
under identical conditions to 35 dah at 3°C and 8°C in
2007 (B. J. Laurel, unpubl. data). The 8°C treatment
was conducted in both experiments to evaluate potential
differences in overall growth rates between years.

Fish for the larval growth experiments were reared
in the laboratory from eggs collected from spawning
adults. Female and male Pacific cod were caught by
commercial jigging gear from spawning grounds in
Chiniak Bay, Kodiak Island, Alaska. The gametes were
mixed and placed into 4-L incubation trays at 4°C. At
24 hours after fertilization, fertilized eggs were shipped
in insulated containers to the Alaska Fisheries Science
Center’s (AFSC) laboratory facilities in Newport, Or-
egon. Eggs were transferred to flow-through 4-L plastic
trays and incubated at 4°C. Hatching occurred 19-22
days after fertilization, after which larvae were trans-
ferred to larval rearing tanks.

Experimental rearing tanks were 100-L cylinders
with conical bottoms and dark green walls. Water was
supplied to the tanks at a rate of 250 mL/min. Weak
upwelling circulation was maintained in the tank by
positioning the in-flow at the bottom center of the tank
and with light aeration. Light regime during larval
rearing was maintained at 12:12 h light:dark; light was
provided by overhead fluorescent bulbs at a level of 6.7
pE/m2s at the water surface.

Larval growth experiments were initiated by stocking
rearing tanks (maintained at the egg incubation tem-
perature of 4°C) with 400 larvae which hatched over a
4-day period in the middle of the hatch cycle. The last
day that newly hatched fish were stocked into rearing
tanks is nominally referred to as experimental day 0.
After the tanks were stocked with fish, tank tempera-
tures were adjusted to treatment temperatures over 2
days. Larvae were reared on a combination of rotifers

384

Fishery Bulletin 108(4)

( Brachionus plicatilis) enriched with Algamac 2000
(Aquafauna, Hawthorne, CA; Park et al., 2006) and mi-
croparticulate dry food (Otohime A, Marubeni Nisshin
Feed Co., Tokyo). Rotifers were supplied at densities of
4 prey/mL twice daily and dry food was provided 2-3
times per day.

At periodic intervals, a subsample of 10 larvae was
removed from each tank to determine the mean size
of larvae in the tank. For the 2007 experiments, six
samples were drawn at 7-d intervals (starting on day
0). For the 2008 experiments, all tanks were sam-
pled on days 0, 10, 23, and 36. Sampled larvae were
individually photographed under magnification and
measured from calibrated digital photographs using
ImagePro® (Media Cybernetics, Bethesda, MD) soft-
ware. The morphometries used in these analyses were
standard length (Ls) and body depth of the myotome
at the anus CD).

Dry weight of individual larvae was calculated us-
ing a two-step model with Ls and D developed from an
independent collection of similar size Pacific cod larvae
reared in the laboratory under identical conditions.
These fish were individually photographed and dried on
preweighed foil at 68°C for at least 24 hours before de-
termination of dry mass (to 1.0 pg) with a microbalance.
Fourty-four fish with Ls of 5 to 11 mm were sampled
periodically over the first 45 dah. First, the body depth
deviation (DDev) was calculated for each fish, reflecting
variance in “condition” from the equation

DDev = D - 0.0873-e°-2164 Ls. (1)

Individual dry mass (MD mg) was calculated from DDev
and Ls from the equation

Md = 0.0204-e° 3734' Ls + (0.9685- DDev - 0.1113). (2)

These equations explained 97.8% of the variation in dry
mass of fish in the sample.

Growth rates were calculated for each replicate tank
from the increase in mean size of fish in measured sub-
samples. Growth in length (gL, mm/d) and mass (gM, /d)
were calculated from linear regression of mean length
and ln-transformed mass against sampling date.

Postflexion larvae

Growth rates of postflexion larvae were measured in
a separate experiment applying similar procedures.
Experiments were established with fish 50 dah, reared
at 8°C under conditions similar to those described above
for preflexion larval experiments. Given the variation in
body size among cultured fish, each fish was assigned
to one of three size categories on the basis of visual
estimation. This sorting by size was done to minimize
the potential for intracohort cannibalism frequently
observed in larval and juvenile gadids (Folkvord and
Ottera, 1993, Sogard and Olla, 1994). One group of
35-40 larvae from each size category was assigned to
each temperature treatment (2°, 4°, 8°, 11°C). In addi-

tion, a sample of 15-20 fish from each size category was
sacrificed to determine initial size distributions.

After establishment of experimental groups (day 0),
temperatures were adjusted to target temperatures at
a rate of 2°C per day. Larvae were offered particulate
food three to four times per day, supplemented with
enriched rotifers twice per day (first 20 d only). As fish
grew, larger size particulate food (up to 620 pm) was
included in daily feedings. A subsample (7-10 fish) was
drawn from the 8°C and 11°C treatments on day 18
and from the 2°C and 4°C treatments on day 24. The
experiments were ended and all surviving larvae were
measured on day 32 for the 8°C and 11°C treatments
and on day 45 for the 2°C and 4°C treatments. Lengths
(Ls and LT) of all sampled larvae were measured with
digital calipers under a dissecting microscope and wet
masses (Mw) were measured with a microbalance. Dry
mass (Md) of each larvae was determined after 48 hours
in a drying oven at 50°C.

Growth rates were calculated from the increase in
mean size of fish in measured subsamples. Growth in
length (gL, mm/d) and mass (gM, /d) were calculated
from linear regression of mean length and ln-trans-
formed mass against sampling date.

Postsettlement juveniles

Age-0 Pacific cod were captured from Kodiak Island
juvenile nurseries in July 2008 with a 36-m beach seine.
Fish were maintained for at least 48 hours at the AFSC
Kodiak Laboratory in ambient seawater before shipment
to the AFSC’s laboratory in Newport, Oregon. Fish were
shipped overnight in insulated containers filled with sea-
water and oxygen. Before use in laboratory experiments,
fish were maintained in 1-m diameter round tanks with
flow-through seawater maintained at 8-10°C. Fish were
fed thawed krill and commercially available pellets on
alternating days.

The experiment was initiated by assigning fish-size
categories based on visual estimation and stocking fish
into experimental tanks. One tank of each size catego-
ry (n= 3) was assigned to each temperature treatment
{n= 4; 12 tanks total). After establishment of experimen-
tal groups, temperatures were adjusted to treatment
temperatures (2°, 5°, 8°, and 11°C) and fish were accli-
mated to the treatment temperature for 10 days.

Experimental tanks were 66x45.7 cm, filled to a
depth of 23.2 cm. During the experiment fish were fed
thawed krill to apparent satiation once per day. In ad-
dition, a gelatinized combination of squid, krill, her-
ring, commercial fish food, amino acid supplements, and
vitamins was provided three times per week. Lights
were maintained on a 12:12 h light:dark photoperiod
for all experiments. Tanks were checked twice daily
for mortalities, and dead fish were removed, weighed,
and measured.

Growth rates were estimated by measuring (LT to 1
mm) all fish in the experiment three times at 10-d in-
tervals. To minimize stress to small fish from repeated
handling, wet masses were measured only at the end

Hurst et al.: Growth rates of Gadus macrocephalus

385

of the experiment. Wet mass (Mw) of individual fish
at earlier sampling points was estimated from regres-
sions based on measurements of fish collected but not
used in this experiment and the final experimental
measurements.

Growth rates (gL and gM) of juvenile cod were deter-
mined by regression of the measurements of fish length
and ln-transformed mass against sampling date. In lieu
of marking the 7-10 individual fish in each tank, we
assumed that size rank was maintained within each
replicate tank during the experiment. Fish that died
during the experiment were not included in statistical
analyses.

Growth models

For each of the life stages examined (egg-embryos,
preflexion larvae, postflexion larvae, juveniles), tem-
perature-dependent growth functions were estimated
for growth in length and mass. For consistency with
the most commonly applied field measures of body size,
growth rates of embryos and larvae were expressed in
terms of Ls and MD , and juvenile growth rates as LT
and Mw. Growth of postflexion larvae were expressed
in both sets of measures.

For each life stage, a second-order polynomial func-
tion was fitted to describe the relationship between
temperature and growth rate. For consistency in best-
fit models, the second-order term was maintained, al-
though it was not statistically significant in some cases.
For these models, mean temperatures measured during
the growth interval were applied, rather than experi-
mental target temperatures. The mean growth rate
measured in each replicate tank (n- 3 per temperature)
was used as the level of observation.

In addition to stage-specific models, an integrated
model of size- and temperature-dependent growth
(STDG) was developed (Folkvord, 2005). Data for the
model were derived from the above experiments on
larvae and juveniles and from previously published
data on the hatching times and sizes as a function of
temperature (Laurel et ah, 2008). Despite represent-
ing easily identified discrete life stages with differing
habitats, data on growth of embryos before hatching
were included with posthatch data to clarify intrinsic
patterns in potential growth rates through the early
life stages. Growth rates of prehatch embryos were es-
timated from the size and age (days after fertilization)
at hatching, assuming MD= 0.01 pg and Ls=0.0 mm at
fertilization. In order to standardize measures across
life stages, measured Mw for juveniles was converted
to Md and measured Lr was converted to Ls on the
basis of measurements of similarly size fish (Hurst,
unpubl. data).

The integrated STDG model was initially fitted with
generalized additive models (GAM) to examine the po-
tential effects of nonlinear interactions between mass
and temperature on growth. These nonlinear, nonpara-
metric regression techniques do not require a priori
assumptions on the shape of the relationship between

the dependent and independent variables. After evalu-
ation of potential interactions based on evaluation of
the generalized cross validation (GCV), a parametric
model formulation was selected that best represented
patterns in the growth data. Final models were fitted
with parametric nonlinear regression in Statistica (vers.
6.0, StatSoft, Tulsa, OK). This approach was under-
taken separately to provide STDG models for growth
expressed in mass (MD) and length (Ls).

Results

Preflexion larvae

Mean size of larvae at hatch was slightly larger in the
2007 experiment than in the 2008 experiment (Ls 5.16
vs. 4.90 mm; F (1 60] = 45.4, PcO.001). However, there was
no significant difference among years in growth rates of
preflexion larvae reared at 8°C (gL F ^ 4) = 1.52, P- 0.237;
gM F[14j = 3.90, P=0.119), therefore data from the two
experiments were combined to describe the effect of
temperature on growth rate. In addition, there were no
differences in growth rates among replicate tanks at a
given temperature (tested as the interaction between
day and tank on mean size, all P>0.05).

Growth in length and mass of Pacific cod larvae was
significantly affected by rearing temperatures across
the range examined (Fig. 1; gM F(311| = 30.0, P<0.001;
gL (F|3 h]= 59.4, PcO.001). After 35 days, fish reared at
8°C were 2.6 times larger than fish reared at 2°C (MD
0.271 vs. 0.104 mg). Growth rates were fitted as a sec-
ond-order function of temperature (Table 2).

Postflexion larvae

The sorting of fish by size before the establishment of
experimental groups produced significant differences
in initial sizes of experimental fish (group mean Ls
14.02 to 16.10 mm; P- 0.004). Differences among size
groups within temperature treatment were generally
maintained throughout the experiment but growth rates
were slightly higher in the small-size groups than the in
large-size groups. The effect of size group was significant
for growth expressed as gM (P|26j=15.7, P=0.004) but not
for gL (F[2 6] = 1.78, P=0.248).

Growth in length and mass of postflexion Pacific cod
larvae was significantly affected by rearing tempera-
tures across the range examined (Fig. 2; gM Fj3 g]=34.3,
P<0.001; gL (P[36j = 63.0, P<0.001). Growth rates (for
gM and gL) at 11°C averaged 2.2 and 3.0 times, respec-
tively those observed at 3°C in similar size treatments.
Growth rates were described as a second-order function
of temperature (Table 2).

Juveniles

Sorting of fish by size before the experiment resulted
in significant differences in initial size among repli-
cates within temperature treatments (LT P[8 83) = 9.46,

386

Fishery Bulletin 108(4)

Temperature (°C)

Figure t

Temperature-dependent growth rates of preflexion
larval Pacific cod ( Gadus macrocephalus ) in (A) stan-
dard length and (B) dry mass. Fish used in experiments
were the offspring of spawning adults collected in the
central Gulf of Alaska in April 2007 (open symbols)
and 2008 (filled symbols). Values are the mean growth
rates (±standard error) for three replicate tanks at four
temperatures. Overlapping points are displaced hori-
zontally for clarity.

0.6

■O

E

£

6>

0.5

0.4

O)

c

<D

O

O

0.3

0.2

0.1

A

0.0 \ T , r r-

2 4 6 8 10

Figure 2

Temperature-dependent growth rates of postflexion
larval Pacific cod ( Gadus macrocephalus) in (A) standard
length and (B) dry mass. Fish used in the experiment
were the offspring of spawning adults collected in the
central Gulf of Alaska in April 2007. Values are the
mean growth rates (+standard error) for three replicate
tanks at four temperatures. Symbols represent groups
based on initial size sorting of larvae (circle: small;
triangle: medium; square: large). Overlapping points
are displaced horizontally for clarity.

P<0.001). Differential growth during the temperature
acclimation period resulted in slight differences in initial
sizes among temperature treatments (treatment mean LT
range: 48.8-51.8 mm; F|3 83]=2.70, P=0.051). Although
there were significant differences in growth rates among
tanks within temperature treatments, these were not
consistent across size groups, resulting in a significant
interaction between temperature and size group (gM
[6 ,60] = 2 . 2 3 , P= 0.052; gL: Pj6 60j=2.34, P=0.042).

Growth in length and mass of juvenile Pacific cod was
significantly affected by rearing temperatures across
the range examined (Fig. 3; gM F[36] = 59.3, P<0.001;
gL (F[36] = 26.7, PcO.001). Growth rates at 11°C aver-
aged 2.9 and 3.7 times (gM and gL, respectively) greater
than those observed at 2°C in similar size treatments.
Best-fit functions describing growth as a second-order
function of temperature are shown in Table 2.

General growth model

Models of growth rates of early life stages of Pacific cod
indicated a discontinuity from strict allometric scaling
during the early larval stage. Growth rates of preflex-
ion larvae were lower than predicted based on a purely
ontogenetic model incorporating growth-rate data from
embryos to settled juveniles. Therefore, two-stage models
were developed to describe growth in the egg stage
separately from the posthatch, free-swimming stages.
Although growth was a function of both temperature
and body size, it was effectively modeled as the product
of independent functions of temperature and body size.
There were no significant interactions in the sense that
the parameters of the temperature-dependence function
were not themselves a function of body size. Therefore,
embryonic and free-swimming stages shared a single

Hurst et al.: Growth rates of Gadus macrocephcilus

387

Table 2

Stage-specific growth models for early life stages of Gulf of Alaska Pacific cod ( Gadus macrocephalus) . Models describe growth in
mass ( gM ) and length ( gL ) as a function of temperature (T) for each stage, r2 is the coefficient of determination.

Stage

Growth functions

r 2

Eggs-embryos

temperature range: 0-8°C
dry weight (fig)

gM= 3.807 + 1.493 • T- 0.032 ■ T2

0.929

standard length (mm)

gL=0.104 + 0.024 • T- 0.00002 • T2

0.939

Preflexion larvae

temperature range: 2-ll°C
dry weight (fig)

gM= 2.990 + 0.772 • T- 0.077 • T 2

0.897

standard length (mm)

gL = 0.179 + 0.015 • T - 0.0001 ■ T2

0.941

Postflexion larvae

temperature range: 3-1 1°C
dry weight (g)

gM= 1.652 + 1.059 • T - 0.028 • T2

0.830

wet weight (g)

gM= 0.531 + 0.857 • T - 0.024 • T2

0.897

standard length (mm)

g, =0.034 + 0.043 • T- 0.0008 ■ T2

0.882

total length (mm)

gL= 0.044 + 0.019 • T- 0.001 • T2

0.889

Juveniles

temperature range: 2-12°C
wet weight (g)

gM=- 0.998 + 0.579 • T- 0.022 • T2

0.826

total length (mm)

gL = -0.081 + 0.079 • T - 0.003 • T 2

0.762

temperature-dependence function, differing only in ele-
vation through ontogeny (Fig. 4).

Growth rates of Pacific cod through the early life
stages were described by the equations

§ l ~

0.076 + 0.029 T - 0.00002 T2
0.076 + 0.029 • T - 0.00002 T2

f0.0758

1-0.059/e s

if stage = embyro
if stage > embryo

allometric scaling, wherein growth rates after hatching
are lower than those predicted by body size allometry.
We determined parameters for temperature-dependent
growth functions in length and mass for specific life
stages and for a unified STDG function. These measures
of growth potential can be used to evaluate the biotic
and abiotic factors regulating the growth and survival
of early life stages of Pacific cod in the wild (Folkvord,
2005; Hurst et al., 2010).

and

(0.454 + 1.610 T- 0.069 T2)-

g-6.725 Md _j_ 3 705 if stage = embryo

8m = ' (4)

(0.454 + 1.610 T - 0.069 T2)-
g-6.725 md if stage > embryo

These equations explained over 88% of the observed
variance in growth rates of Pacific cod embryos to post-
settlement juveniles (gM r=0.969; gL r=0.940). Analysis
of residuals from these models indicated greater vari-
ance at higher growth rates (small body sizes and higher
temperatures), but there were no trends in residuals in
relation to experimental temperature or body size that
would indicate significant departures from the model.

Discussion

Temperature is the dominant regulator of growth in
early life stages of fishes. In this study we examined
the ontogenic pattern in growth rate for early life stages
of Pacific cod. We demonstrated a deviation from strict

Experiments

Because these experiments were conducted across a
range of life stages, many aspects of our experimental
method had to be adapted for each specific experiment,
such as tank volume, prey type, and fish density. How-
ever, the most significant differences in method between
egg-larval and juvenile experiments were the level of
observation and source of fish. To estimate growth rates
of embryos and larvae, subsamples of fish were drawn
from a large tank population to determine mean size at
a specific age (Otterlei et al., 1999; Monk et al., 2008).
Change in mean size at age was then used to determine
growth rate in each replicate tank. With this approach,
there is the potential for size-selective mortality in the
experiments to affect estimates of mean growth rates.
Such size-selective mortality is most commonly assumed
to be the result of predation (including cannibalism
in single species culture). However, such an effect is
unlikely to have occurred in these experiments: postflex-
ion larvae were sorted by size before growth experiments
specifically to avoid potential cannibalism, and we saw
no evidence of cannibalism in the experiment (no larvae
in samples with fish in their stomachs). Because juvenile
fish could be handled, they were measured and returned
to the tank and subsequently remeasured, providing

388

Fishery Bulletin 108(4)

°-6 I A

O 0.1 T

0.0 I T T T ^

2 4 6 8 10

Figure 3

Temperature-dependent growth rates of postsettlement
juvenile Pacific cod (Gadus macrocephalus) in (A) total
length and (B) wet mass. Fish used in the experiment
were collected from nearshore nursery areas at Kodiak
Island, Alaska in July 2008. Values are the mean growth
rates (± standard error) for three replicate tanks at
four temperatures. Symbols represent groups based
on initial size sorting of fish (circle: small; triangle:
medium; square: large). Overlapping points are displaced
horizontally for clarity.

growth trajectories for individual fish. These individual
growth rates were then averaged to estimate mean
growth rates of fish in each tank (Hurst and Abookire,
2006; Wijekoon et ah, 2009).

For experiments with eggs and larvae, we used the
offspring of field-caught spawning adults. In each year
of experiments, gametes from one or two females were
mixed with those of three to five males. Juvenile fish
used in experiments were naturally produced and cap-
tured after recruitment to juvenile nearshore habitats.
Therefore, the genetic diversity among experimental ju-
veniles was significantly greater than that found in ex-
perimental eggs and larvae. This difference in potential
genetic contributions to growth rates is not expected to
have a significant influence on the overall growth pat-
terns described here because maternal and genetic ef-

fects on growth have been shown to be small in relation
to environmental factors such as temperature (Benoit
and Pepin, 1999; Green and McCormick, 2005) and prey
availability (Clemmesen et al., 2003).

Ontogenetic patterns of growth

By combining results across life stages, we clarified
ontogenetic patterns in growth and length. With the
exception of a departure during the preflexion stage,
growth patterns followed expected size-dependent allo-
metric patterns throughout much of the early devel-
opment (Elliott and Hurley, 1995). Growth in mass
(gM) decreased with increases in body size (Wootton,
1990) and growth in length (gL) was constant across life
stages. Although the constancy of gL across a range of
body sizes in early life stages has been noted in other
studies (Jones, 2002; Sigourney et al., 2008), those
experiments have not generally included the presettle-
ment egg and larval stages incorporated here. Interest-
ingly, in Pacific cod, the general pattern of across-stage
similarity in gL extended from the egg-embryo stage
into the juvenile stage.

There was a significant departure from the expect-
ed ontogenetic pattern in the preflexion larval period,
most clearly observable in the gL results. Measured gL
among preflexion larvae averaged only 41% of the rates
measured for embryos, postflexion larvae, and settled
juveniles. Although less readily apparent, a similar de-
parture was observed in mass growth as the decline in
gM between the egg-embryo and preflexion larval stages
was greater than expected from allometric patterns
accounting for the observed differences in body size. In
several studies on the growth of first-feeding gadids,
higher growth rates were reported for fish reared on
copepods than on cultured rotifers (Conceicao et al.,
2010). Unfortunately, technical limitations preclude
rearing sufficient quantities of copepods for use in ex-
periments such as ours. For our study, larval Pacific cod
were reared on essential-fatty-acid-enriched rotifers, as
the best of the practicable prey alternatives. Therefore,
it is possible that growth rates of preflexion larvae are
under-estimates of maximum potential growth at this
stage. However, the effect of prey type is insufficient to
completely explain the significantly lower growth rate
observed at this stage when compared to other stages.
Further, similar observations of reduced growth rates of
fishes in the early posthatch phase have been observed
in several other studies. Experiments in which growth
of haddock ( Melanogrammus aeglefinus; Martell et al.,
2005) was tracked through the egg-larva transition
revealed a similar reduction in growth associated with
hatching. A similar pattern is apparent in Atlantic
cod, but without measurements of embryonic growth
rates, the magnitude of decline at hatching could not
be determined (Otterlei et al., 1999; Folkvord, 2005).
However, these studies document a period of increas-
ing growth rates after hatching, followed by growth
rate declines along allometric expectations, indicating
a similar overall pattern.

Hurst et al. : Growth rates of Gadus macrocephalus

389

Figure 4

Size- and temperature-dependent growth rates of early life stages of Pacific cod (Gadus macrocephalus) from the central
Gulf of Alaska in (A) standard length and (B) dry mass. Points are the tank mean growth rates measured in laboratory
experiments. Surfaces are best-fit descriptions of growth rates. Parameter values are presented in Equations 3 and 4.

This reduction in growth during the egg-larva tran-
sition appears to be the result of increased metabolic
expenditures associated with swimming in posthatch
larvae and possibly a reduction in energy available for
growth associated with the transition from reliance on
endogenous energy stores to exogenous feeding (Torres
et al., 1996; Yufera and Darias, 2007). In Pacific cod,
yolk reserves are depleted 3-12 dah, depending on
water temperature (Laurel et al., 2008) and stomach
fullness increased through the first 28 dah (B. J. Lau-
rel, unpubl. data). The increase in growth rates after
the preflexion transitional feeding stage coincides
with the onset of diel vertical migrations (Hurst et
al., 2009) and increased responsiveness to prey (Colton
and Hurst, 2010) among postflexion Pacific cod larvae.
The negative departure from an allometrically defined
growth pattern after hatching indicates that the first-
feeding stage represents a “critical period” in the early
life history of Pacific cod and that the consequences
for recruitment of this low growth may be greater at
low temperatures (Kamler, 1992; Houde, 1996). In
addition to inclusion of embryo measurements into
larval studies, future studies with other species should
encompass other major life history and habitat transi-
tions, such as metamorphosis and settlement in flat-
fishes (Christensen and Korsgaard, 1999; Neuman et
al., 2001) in order to clarify the physiological basis
of growth patterns and to determine parameters for
growth models.

Based on exploration of model structures for a unified
STDG for early life stages of Pacific cod, a two-stage
model was developed. The first stage described growth
in the egg stage as a direct function of water tempera-
ture. The second stage described growth in posthatch

fish as a function of water temperature and fish size.
In addition to providing the best fit to experimental
data, this formulation is logically consistent with the
life history. Explicit discrimination between life stages
coincides with hatching, whereas the function provides
a continuous growth surface for all free-swimming stag-
es. This stage-independent model for posthatch fish
provides more realistic growth trajectories in modeling
applications where fish are tracked over multiple stages.

Applications of growth models

By quantitatively accounting for the influence of tem-
perature variation, laboratory-determined growth rates
are being increasingly used to evaluate factors regulat-
ing growth rates of fishes in the wild (Folkvord, 2005;
Rakocinski et al., 2006; Hurst et al., 2009). In these
analyses, “realized growth” expresses observed growth
in the field as a fraction of the potential growth at the
encountered field temperatures (Hurst and Abookire,
2006), with field growth rates estimated from changes
in mean size, otolith increment measures, or biochemi-
cal measures (RNA:DNA). In these studies it is impor-
tant to recognize that growth rates of individuals are
determined by both genetic and environmental factors.
Growth models from laboratory experiments generally
describe mean growth of a representative population
under optimal foraging conditions, which should not be
mistaken for the maximum growth rates that would be
observed for the fastest growing individual. Therefore,
field growth rates should be similarly expressed as a
population mean rather than at the individual level.
Realized growth rates near 100% indicate that growth
rates in the population are directly limited by ambient

390

Fishery Bulletin 108(4)

temperature variation. In studies of juvenile flatfishes,
this temperature regulation of growth has been referred
to as the “maximum growth/optimal food condition”
hypothesis (Karikiri et al., 1991; van der Veer and
Witte, 1993). Conversely, realized growth rates signifi-
cantly below 100% indicate that growth is regulated by
nonthermal environmental factors such as light regime
or prey availability (Buckley et al. 2006; Kristiansen et
al., 2007; Hurst et al., 2009).

Unfortunately, many studies of growth rates in fishes
are conducted over a limited size range and usually
within a single life stage. Therefore, these data have
limited application where growth rates of wild fish are
tracked over longer time periods or through early life
history stage transitions. For example, in evaluating
the mechanisms responsible for variation in survival
and recruitment, it is critical to determine whether
growth reductions among wild fish are due to inher-
ent physiologically based patterns (as appears in post-
hatch gadids) or are imposed by an unfavorable growth
environment (Jones, 2002). In another application of
laboratory data to field studies, the back-calculation
of hatch dates from estimated temperature-dependent
growth rates (Lanksbury et al., 2007) could be biased
if ontogenetic patterns in growth variation are not ac-
counted for.

Conclusion

Growth variation in early life stages can result in body-
size variation that persists over time and has signifi-
cant implications for the survival and recruitment of
marine fish larvae (Houde, 1996; Jones, 2002). Success-
ful evaluation of the biotic and abiotic factors regulating
this underlying variation in growth requires detailed
information on the size- and temperature-dependency
of potential growth throughout the early life history.
Identifying the intrinsic patterns in growth-rate allom-
etry and reductions among preflexion larval Pacific
cod was based on the integration of experimental data
on embryos and larvae, — stages generally considered
in isolation from each other. We suggest that data on
embryos be routinely incorporated with larval data to
clarify ontogenetic and temperature-dependent growth
patterns in the early life history stages of fish.

Acknowledgments

We thank T. Tripp, M. Spencer, and B. Knoth for assis-
tance with fish collection and shipping. Staff and stu-
dents in the Fisheries Behavioral Ecology Program,
including L. Copeman, S. Haines, M. Ottmar, P. Iseri, A.
Colton, L. Logers, E. Seale, and J. Scheingross assisted
with various laboratory experiments. S. Munch, L.
Tomaro, A. Stoner, and three anonymous reviewers
provided helpful comments on earlier versions of this
manuscript. This research was supported in part by
a grant from the North Pacific Research Board (no.

R0605). This is publication no. 248 of the North Pacific
Research Board.

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393

Feeding ecology of juvenile Pacific salmon
( Oncorhynchus spp.) in a northeast Pacific fjord:
diet, availability of zooplankton, selectivity for prey,
and potential competition for prey resources

Email address for contact author: sbollens@vancouver.wsu.edu

1 School of Earth and Environmental Sciences

and School of Biological Sciences
Washington State University
14204 NE Salmon Creek Avenue
Vancouver, Washington 98686

2 School of Arts & Sciences
Endicott College

376 Hale Street

Beverly, Massachusetts 01915

3 School of Aquatic and Fishery Sciences
University of Washington

1122 Boat Street
Seattle, Washington 98195

4 School of Oceanography
Campus Box 357940,

University of Washington
Seattle, Washington 98195

Abstract — We investigated the feed-
ing ecology of juvenile salmon during
the critical early life-history stage
of transition from shallow to deep
marine waters by sampling two sta-
tions (190 m and 60 m deep) in a
northeast Pacific fjord (Dabob Bay,
WA) between May 1985 and October
1987. Four species of Pacific salmon—
Oncorhynchus keta (chum), O.
tshawytscha (Chinook), O. gorbusclia
(pink), and O. kisutch (coho) — were
examined for stomach contents. Diets
of these fishes varied temporally, spa-
tially, and between species, but were
dominated by insects, euphausiids,
and decapod larvae. Zooplankton
assemblages and dry weights differed
between stations, and less so between
years. Salmon often demonstrated
strongly positive or negative selection
for specific prey types: copepods were
far more abundant in the zooplank-
ton than in the diet, whereas Insecta,
Araneae, Cephalapoda, Teleostei, and
Ctenophora were more abundant in
the diet than in the plankton. Overall
diet overlap was highest for Chinook
and coho salmon (mean=77.9%) — spe-
cies that seldom were found together.
Chum and Chinook salmon were
found together the most frequently,
but diet overlap was lower (38.8%)
and zooplankton biomass was not
correlated with their gut fullness (%
body weight). Thus, despite occasional
occurrences of significant diet overlap
between salmon species, our results
indicate that interspecific competition
among juvenile salmon does not occur
in Dabob Bay.

Manuscript submitted 10 September 2009.
Manuscript accepted 16 June 2010.

Fish. Bull. 108:393-407 (2010).

The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not
necessarily reflect the position
of the National Marine Fisheries
Service, NOAA.

Stephen M. Bollens (contact author)1

Rian vanden Hooff 1

Mari Butler2

Jeffery R. Cordell3

Bruce W. Frost4

Juvenile salmon migrating into coastal
waters face a variety of challenges
as they adjust to a rapidly changing
environment, such as outmigration
timing, physiological acclimation, new
prey fields, new predators, and com-
petition for resources (Pearcy, 1992;
Magnusson and Hilborn, 2003). High
rates of natural mortality have been
attributed to the ocean entry transi-
tion (Parker, 1971; Bax, 1983), yet
we still have a poor understanding of
the processes governing this mortal-
ity. Several mechanisms have been
hypothesized — disruption of freshwa-
ter hydrological conditions, degrada-
tion of estuarine nursery conditions,
and interannual variability of preda-
tor abundance and prey resources
in the marine environment (Levings
and van Densen, 1990; Willette, 2001;
Logerwell et ah, 2003).

Comprehensive management of
salmon fisheries, including their
conservation and recovery, requires
detailed understanding of juvenile
salmon ecology during this critical
transition. Increased understanding
of feeding relationships and poten-
tial density-dependent effects, such
as diet overlap among co-occurring
species and resource limitation could

allow for a more ecologically based
approach for rebuilding threatened
salmon stocks. Specifically, species in-
teractions and their response to vari-
ability in prey resources could be im-
portant factors for predicting marine
survival and the forecasting of adult
returns (Logerwell et al., 2003).

Juvenile salmon have been docu-
mented feeding in a variety of habi-
tats, including freshwater (Keeley
and Grant, 2001; Hampton et ah,
2006), estuaries (Healey, 1980; Mur-
phy et ah, 1988; Reese et al., 2009),
and in the coastal ocean (e.g., Bro-
deur and Pearcy, 1990; Daly et al.,
2009). Inland marine waters (e.g.,
bays, straits, sounds, fjords, etc.)
have been characterized less fre-
quently (Sturdevant et al., 2004;
Romanuk and Levings, 2005; Saito
et al., 2009). Like estuaries, these
inland marine salmon habitats are
more geographically and ecologically
diverse than offshore habitats, and
thus it may be more difficult to gen-
eralize about juvenile salmon feeding
ecology in these areas.

Dabob Bay, a temperate marine
fjord in Puget Sound, northwestern
Washington, has been the site of nu-
merous studies of plankton dynamics

394

Fishery Bulletin 108(4)

(e.g., Frost, 1988; Bollens et al., 1992a, 1992b; Frost,
2005 and references therein). Although these stud-
ies have provided extensive insight into zooplankton
population dynamics and predator-prey interactions,
none has specifically reported on the seasonality of zoo-
plankton community composition from this area. Four
juvenile salmon species reside in Dabob Bay temporarily
during outmigration to the Pacific Ocean (Bollens and
Frost, 1989): Oncorhynchus keta (chum), O. tshawytscha
(Chinook), O. gorbuscha (pink), and O. kisutch (coho).
Diets of these four species in the fjord have not been
described. Feeding habits of juvenile chum salmon in
neritic waters have been described for a nearby location
in Hood Canal (Simenstad and Salo, 1980) and feed-
ing habits of juvenile salmon in other nursery areas of
Puget Sound have also been described (Simenstad et
al., 1982; Duffy et al., 2005).

Much of our understanding of juvenile salmon feed-
ing ecology in northeast Pacific marine waters has been
based on detailed analyses of stomach contents, but

Figure t

Map of Dabob Bay, Washington. Four species of juvenile
Pacific salmon — chum ( Oncorhynchus keta), Chinook (O.
tshawytscha ), coho (O. kisutch ), and pink (O. gorbuscha) — and
zooplankton were sampled at two stations between April
1985 and October 1987 to examine salmon diet, zooplank-
ton availability, feeding selectivity, and potential competi-
tion for prey. D=location of the deep (190-m) central bay
tstation, and S=the location of the shallow (60-m) near-
shore station.

has been limited by a lack of corresponding analyses
of prey fields. Some recent studies have identified the
importance of prey selectivity as a factor in assess-
ing the trophic ecology of salmon during early marine
residence (Landingham et al., 1998; Schabetsberger
et al., 2003). Furthermore, the highly variable diets
demonstrated within and between studies indicate that
temporal (seasonal, interannual, and interdecadal) and
spatial scales of variability are important, and therefore
pose a significant challenge for the design of field stud-
ies. The result has been an incomplete understanding
of juvenile salmon response to dynamic zooplankton
prey fields, particularly during one of the most critical
life-history stages, i.e., the early ocean transition phase
(Beamish and Mahnken, 2001).

Our objectives were 1) to investigate the diet compo-
sition of four salmon species ( Oncorhynchus spp.) col-
lected from two stations (nearshore-shallow and central-
basin-deep) in Dabob Bay over three years and several
seasons; 2) to determine salmon feeding selectivity
(i.e., their diet in relation to prey availability);
and 3) to explore potential resource competition
among these species during their early marine
residence.

Materials and methods
Fish collection and processing

Between May 1985 and October 1987 we sampled
two stations in Dabob Bay, WA (47°45'-50'N lat.,
122°50/W long.): a deep (190 m), central station,
and a shallow (60 m), nearshore station 9 km apart
(Fig. 1). Fish were sampled at night (just after
dusk, i.e., when there was no apparent daylight)
with two gear types: a midwater trawl with a
mouth area of 81.0 m2 (9. 0x9.0 m), and a surface
tow net with a mouth area of 18.3 m2 (3. 0x6.1
m) (see Bollens and Frost, 1989 for details). The
midwater trawl was towed obliquely from a 50-m
depth to the surface at a mean speed of 150 cm/s.
Because of concerns about possible avoidance of
this net by fish in the upper few meters of the
water column (e.g., due to ship wake and propeller
wash), we also deployed the surface tow net in the
upper three meters of the water column, towed at a
mean speed of 80 cm/s behind (50 m) and between
(at a midpoint of 50 m) two different vessels (one
vessel 5 m and one 15 m in length). Fish were col-
lected at each station during each of four seasons
(spring: April-May; early summer: June-July; late
summer: August; and autumn: October) in each of
three years (1985-87), except for spring of 1985,
when no fish were collected (Table 1).

Fish collected with the midwater or surface
trawls were sorted and counted, and the catch
was weighed by species, lengths were measured,
and then individuals of five predetermined size
(fork length [FL] ) classes (<49 mm, 50-74 mm,

Bollens et al.: Feeding ecology of juvenile Oncorhynchus spp.

395

Table 1

Number of juvenile Chinook (Oncorhynchus tshawytscha), chum (O. keta ), coho (O. kisutch), and pink (O. gorbuscha) salmon
stomach samples and zooplankton samples collected during 12 visits to each of two stations in Dabob Bay, Washington, 1985-87.
Sampling dates are grouped by year within season, number of samples for the deep (D, 190 m) station are indicated on the left
and those for the shallow (S, 60 m) station indicated on the right. Diet samples were pooled from midwater trawl and surface
trawl collections at each station for each date or dates; duplicate zooplankton samples were collected at each station on each date
by vertical hauls of plankton nets. Fish samples were not collected in spring of 1985.

Number of juvenile salmon stomachs

Number of
zooplankton
samples

Chinook

Chum

Coho

Pink

Season and sampling dates

D

S

D

S

D

S

D

S

D

S

Spring

1985

30 Apr and 29 May 1986

0

0

16

15

0

0

3

7

2

2

2

2

6-7 May 1987

0

0

6

10

0

0

0

0

2

2

Subtotal

0

0

22

25

0

0

3

7

6

6

Early summer

19-20 Jun 1985, 24-25 Jun 1985,

26 Jul 1985

5

10

14

9

0

0

0

0

2

2

4-5 Jun 1986

4

3

10

4

5

1

0

0

2

2

17-18 Jun 1987, 13 Jul 1987

3

5

0

14

1

2

0

0

2

2

Subtotal

12

18

24

27

6

3

0

0

6

6

Late summer

19-20 Aug 1985, 26-27 Aug 1985

4

5

10

12

0

0

0

0

2

2

12 Aug 1986, 14 Aug 1986

5

7

7

3

0

0

0

0

2

2

19-20 Aug 1987

11

6

7

0

1

0

0

0

2

2

Subtotal

20

18

24

15

1

0

0

0

6

6

Autumn

7-9 Oct 1985

0

6

5

0

0

0

0

0

2

2

22 Oct 1986

6

10

7

0

0

0

0

0

2

2

14-15 Oct 1987

29

3

3

0

0

0

0

0

2

2

Subtotal

35

19

15

0

0

0

0

0

6

6

Total

67

55

85

67

7

3

3

7

24

24

75-99 mm, 100-149 mm, >150 mm) were removed and
0. 5-3.0 cc of undiluted formaldehyde were injected into
their gut cavity to halt digestion. Each fish was then
stored in dilute (5%) formalin-seawater solution. Fish
from both trawl types were combined to yield a repre-
sentative sample of fish residing in the upper 50 m of
the water column at night. Subsequently, each fish was
weighed (g, wet weight) and measured in the labora-
tory, and its stomach excised. Stomach contents were
weighed (wet weight), digestion stage was recorded, and
then prey were identified to the lowest possible taxon
(often to species), and enumerated and weighed (wet
weight) by category. Diet composition was summarized
as the normalized average percent prey biomass ( [bio-
mass of taxonomic group]/[total weight of stomach - the
weight of the unidentified portion of the stomach con-
tents]). A total of 294 salmon stomachs were examined;
six were empty and were not considered further.

For ease of comparison, we pooled the original 122
prey taxa observed into 13 categories that made up at

least 10% of any one fish’s total normalized prey bio-
mass. Data were stratified by salmon species and size
class, season, and station across the three years pooled.
In most cases the pooled data were a good representa-
tion of the three individual years of data, but in some
cases there were interesting interannual differences,
as discussed below.

Collection and processing of zooplankton

Zooplankton collections were made at the two stations
within 1-2 hours of the fish trawls by using a 1-m2
mouth opening and 333-pm mesh multiple net sampler
(Frost, 1988) in 1985 and 1986 and a 1-m diameter
mouth opening and 216 pm mesh Puget Sound net
(Research Nets Inc., Seattle) (Miller et al., 1977) in
1987. Duplicate zooplankton samples were collected at
each station and on each date (Table 1). A subsample
(collected with a Stempel pipette) of 1-2% of the ani-
mals was taken and the species were enumerated and

396

Fishery Bulletin 108(4)

identified for all dates and stations at which fish were
collected. Identification of gelatinous animals was gen-
erally poor because of their damage during collection.
Abundances (densities) were calculated from the sub-
sample counts and volumes (m3) of water filtered (as
measured by a flow meter). Data from different depth
strata were weighted by the size (height, m) of the
depth strata and then averages for the upper 50 m were
computed. Zooplankton community composition was
described by station by using the data from duplicate
zooplankton tows to compute average abundances for
each taxonomic group for each of four seasons (spring,
early summer, late summer, and autumn) over the
three years studied (1985-87). Dry weights (g/m2) for
zooplankton >216 pm were measured as described in
Bollens et al. (1992b).

For ease and clarity of presentation of the zooplank-
ton compositional data, the category “other Copepoda”
that is used in presenting juvenile salmon gut contents
was partitioned into several subcategories, i.e., the gen-
era Oithona, Metridia, and Pseudocalanus. In addition,
several taxonomic groups that were common in salmon
gut contents were rarely or never observed in the zoo-
plankton samples (e.g., Insecta and Araneae, Cepha-
lopoda, Teleostei, and Ctenophora) and were therefore
placed into the “other” category for characterizing zoo-
plankton community composition.

Data analysis

We estimated interspecific diet overlap between co-occur-
ring juvenile salmon species on the basis of biomass of
prey in common, using Schoener’s (1970) percent simi-
larity index (PSI):

PS/,,y = 10°(l-0.5(^|Pxv-PVii|)), (1)

where Pxi = percent biomass of food category ( i ) in the
stomach of species x; and
Pyi = percent biomass of food category ( i ) in the
stomach of species y.

We first pooled the prey biomass data by size class
for each salmon species. PSI calculations were made
for the subset of samples with a minimum of three
stomachs per species. We examined intraspecific spa-
tial variation in diet by calculating the PSI of juvenile
salmon between the two stations. PSI values >60%
were considered significant (Brodeur and Pearcy, 1992;
Landingham et al., 1998).

Prey selectivity by juvenile salmon species was exam-
ined by using Ivlev’s (1961) electivity index (Et):

E, = {ri-pi)Hri +Pl), (2)

where El = the electivity index;

r- = the numerical proportion of the ith taxon in
the stomachs; and

pt = the proportion of the same taxon in the
environment.

The electivity values provide a species-specific mea-
sure of prey selection by allowing a comparison of salm-
on gut contents to available prey. Values for Et range
from -1 to 1, where 1 indicates the highest selectivity
(i.e., present in the diet, but never in the zooplankton
samples), and -1 indicates lowest selectivity (i.e., never
in the diet, but present in the zooplankton samples).
We summarized these observations as average species-
specific electivity scores for all size classes, seasons,
and years combined to compare selection across salmon
species.

We compared juvenile salmon gut fullness (% body
weight) and zooplankton abundance (dry weight) at each
station, as well as each salmon species’ gut fullness be-
tween the two stations, using Spearman’s rank correla-
tions (Zar, 1999). The difference in mean zooplankton
abundance (dry weight) between the two stations was
tested by using a Mann-Whitney U test (Zar, 1999).

Results

Juvenile salmon diet

Juvenile salmon in Dabob Bay showed species-specific
patterns of occurrence throughout the April-October
time period across years. In general, more and smaller
juvenile salmon were caught at the nearshore shallow
station during spring and early summer, and more and
larger juvenile salmon were caught at the central-bay
deep station during late summer and autumn. Chum
salmon were most prominent during the spring and early
summer, whereas Chinook salmon were caught more
frequently later in the year, particularly at the deep sta-
tion (190 m). All four salmon species were predominantly
planktivorous, although there were some exceptions as
described below. Because of the greater occurrence of
chum and Chinook salmon diet samples, our analyses
were focused on these two species.

Juvenile chum salmon

Chum salmon exhibited striking ontogenetic and spatial
variation in diets, including a tendency for fish <100 mm
FL to consume more insects and larvaceans and those
>100 mm to consume more amphipods and decapod
larvae. At the deep station in late spring, euphausiids
were the dominant prey type by weight (Fig. 2). Small
(<49 mm) fish also consumed insects, arachnids, and
copepods other than Calanus pacificus, whereas larger
fish (75-99 mm) consumed high percentages of teleosts
(primarily unidentified species), hyperiid amphipods,
and decapod larvae. The single fish of the 50-74 mm
size range captured during early summer at the deep
station consumed mostly insects and arachnids, whereas
fish between 75 and 150 mm consumed predominantly
larvaceans and hyperiids. The single large fish (>150
mm) contained exclusively euphausiids. In late summer
at the deep station, fish 100-149 mm consumed mostly
hyperiid amphipods, whereas fish >150 mm consumed

Bollens et al.: Feeding ecology of juvenile Oncorhynchus spp.

397

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~Y\ Calanus pacificus
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Decapoda
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Size class (mm)

Figure 3

Stomach contents of juvenile Chinook salmon (Oncorhynchus tshawytscha) caught at the deep station (A) and shallow sta-
tion (B) of Dabob Bay, Washington, during different seasons. Collections were made with a midwater trawl and a surface
tow net at each station on each date. Data were pooled over three years (1985-87) for each season and calculated as the
normalized biomass of each taxonomic group.

mostly euphausiids, and the remainder consumed mainly
gammarid and hyperiid amphipods. In autumn, the
diet of fish >150 mm from the deep station was com-
posed more evenly of several prey categories, including
euphausiids, copepods other than C. pacificus, gammarid
and hyperiid amphipods, larvaceans, and cephalopods.

In contrast, prey of chum salmon <150 mm at the
shallow station were more varied, and few euphausiids
were present (Fig. 2B). Teleosts and larvaceans, how-
ever, were represented in similar proportions to those
at the deep station. Larger chum salmon (>100 mm)
sampled in early summer were the only group that
consumed relatively large amounts of ctenophores; the
remainder of their prey consisted mainly of decapod
larvae and hyperiids. During late summer at the shal-
low station, chum salmon consumed decapod larvae,
gammarid amphipods, copepods other than C. pacificus ,

and larvaceans. Large fish (>150 mm) collected in au-
tumn fed almost entirely on euphausiids.

Juvenile Chinook salmon

There was substantial variation in Chinook salmon
diets across size classes, seasons, and stations. At the
deep station during early summer, euphausiids consti-
tuted a large proportion of the diet of Chinook salmon
between 75 and 99 mm (Fig 3A). Fish 100-149 mm
consumed a more evenly distributed mix of prey, domi-
nated by teleosts and euphausiids. In late summer,
fish 100-149 mm at the deep station consumed mostly
hyperiid amphipods and euphausiids. In autumn, fish
>100 mm at the deep station consumed mostly gam-
marids, euphausiids, insects, arachnids, cephalopods,
and hyperiids.

Bollens et al.: Feeding ecology of juvenile Oncorhynchus spp.

399

At the shallow station in early summer, decapod
larvae dominated the diet of Chinook salmon >75 mm
(Fig. 3B). During both late summer and autumn, in-
sects and arachnids dominated the diets of all three
size classes of Chinook salmon, but in autumn, those
Chinook salmon >150 mm also consumed hyperiid
amphipods.

Diet of other salmon species

Fewer diet samples were available for juvenile pink and
coho salmon than for juvenile chum and Chinook salmon.
Diet samples of pink salmon were available only for
small fish (<49 mm) in spring. At the deep station these
fish contained about 50% euphausiids, and gammarids,
copepods other than C. pacificus, insects, and arachnids
made up the other 50%. At the shallow station, their diet
included a variety of prey consisting mainly of teleosts,
pteropods, copepods other than C. pacificus, and fewer
insects, decapod larvae, gammarids, and “others.” The
“others” in this case were mostly bivalves, whereas the
“others” for the co-occurring juvenile chum salmon were
mostly chaetognaths.

A few juvenile coho salmon were also caught at the
two sample stations. At the deep station, diet of coho
salmon 100-149 mm consisted primarily of decapod
larvae and euphausiids, and a single larger (>150 mm)
coho salmon consumed mostly decapod larvae in early
summer and another large coho, only gammarid am-
phipods in late summer. At the shallow station, three
coho salmon were caught in June: one (75-99 mm) con-
sumed about 75% “other” taxa (mostly the ostracod
Euphilomedes), and the two other fish consumed almost
exclusively decapod larvae (like the five co-occurring
Chinook salmon).

Juvenile salmon gut fullness in relation
to zooplankton abundance

Juvenile salmon gut fullness (% body weight) was not
related to zooplankton abundance (dry weight) (Fig.
4; Spearman’s rank correlation, P>0.05). For all four
species of salmon, gut fullness was generally greater
in spring and early summer and declined somewhat
during late summer and autumn (chum salmon at the
deep station in 1985 was an exception to this). In con-
trast, zooplankton dry weight at the deep station peaked
in the fall, and minima occurred in the spring. At the
shallow station, peaks in zooplankton dry weight tended
to occur in the summer, and less pronounced minima
occurred in spring and autumn. Zooplankton dry weight
was substantially greater at the deep station than at
the shallow station (P<0.001, Mann-Whitney U test;
Zar, 1999), generally by one order of magnitude. Some
of this difference may have been due to the three-fold
greater water column depth at the deep station, whereas
a generally larger part of this difference was due to
greater abundances of large-body zooplankton in the
deep station samples. In addition, no significant cor-
relation was found for individual salmon species’ gut

1985 1986 1987

• Chum O Chinook ▼ Pink a Coho
<=) Zooplankton dry weight

Figure 4

Zooplankton (>216 pm) dry weights (g/m2) and fish
stomach fullness (mean % body weight) for four spe-
cies of Pacific salmon — chum ( Oncorhynchus keta), Chi-
nook (O. tshawytscha), pink (O. gorbuscha), and coho
(O. kisutch) — sampled between April 1985 and October
1987 at a deep station (A) and a shallow station (B) in
Dabob Bay, Washington. Fish collections were made
with a midwater trawl and a surface tow net, and zoo-
plankton collections were made with vertical hauls of
a plankton net at each station on each date. Dashed
vertical lines separate years. Note the different scales
for zooplankton dry weights on the two y axes.

fullness at the two different stations (Spearman’s rank
correlation, P>0.05; Zar, 1999).

Community composition of zooplankton

Zooplankton communities (upper 50 m at night) were
numerically dominated by copepods at both stations (Fig.
5). The most striking contrast between our zooplankton
composition and our juvenile salmonid diet composi-
tion was the far greater abundance of copepods in the
zooplankton. Substantially different seasonal patterns
in zooplankton community composition were observed
between stations during 1985 and 1986, but not in 1987.
At the deep station, the greatest species richness was
typically observed during early spring, whereas two spe-
cies— Metridia lucens and Calanus pacficus — dominated

400

Fishery Bulletin 108(4)

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a plankton net at each station during each of the four seasons during 1985, 1986 and 1987. Dashed
vertical lines separate years.

in summer and autumn. In contrast, Oithona sp. and
larvaceans dominated the shallow station in summer
and autumn. In 1987, however, zooplankton commu-
nity composition between the two sites was remarkably
similar (Fig. 5) and was dominated by Oithona sp. and
“other Copepoda” (predominantly unidentified stages
1 and 2 calanoid copepodites) throughout the entire
sampling period.

Electivity indices for juvenile salmon

All salmon species consistently and strongly selected for
insect, arachnid, and cephalopod prey (£;>0.75) and rou-
tinely selected against Calanus pacificus, copepods other
than C. pacificus, ctenophores, larvaceans and pteropods
(£,•<-0.25). All salmon species except pink salmon typi-
cally selected for decapod prey (0.25< £,<0.75; both cari-
dean shrimp and brachyuran crab larvae were present
in the spring, but brachyurans dominated the decapod
prey in summer). Hyperiid amphipods and teleosts were
generally selected for by chum and Chinook salmon

(0.25<£;<0.75) but were consumed in proportion to their
relative abundance or were selected against by coho and
pink salmon (-0.75<£(<0.25). Euphausiids were gener-
ally neutrally selected (-0.25<£;<0.25). However, elec-
tivity scores varied substantially within a given salmon
species. For example, in 26 Chinook salmon diet samples,
electivity indices for euphausiid prey ranged from -1.0 to
0.99 (data not shown), but were not consistently related
to predator size, season, or prey abundance.

Important ontogenetic changes in prey-selection
behavior were revealed by size-specific electivity val-
ues (Fig. 6). For instance, smaller size chum salmon
strongly avoided larvacean prey, whereas larger chum
(>75 mm) showed roughly neutral or positive selectivity.
Similarly, small (75-99 mm) Chinook salmon tended to
avoid gammarid amphipods, whereas larger individuals
(>100 mm) tended to select gammarids. Also, smaller
Chinook salmon individuals tended to consume Calanus
pacificus at rates proportional to their abundance in the
environment, but the larger Chinook salmon strongly
avoided these prey. In general, it seemed that larger fish

Bollens et al.: Feeding ecology of juvenile Oncorhynchus spp.

401

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402

Fishery Bulletin 108(4)

selected for larger prey. However, prey selection by coho
and pink salmon showed little ontogenetic variation,
although we had far fewer data for these taxa to make
a definitive statement. Patterns of prey selectivity were
fairly similar between stations for each juvenile salmon
species, although there were occasionally some differ-
ences, e.g., for 100-149 mm Chinook salmon, which
selected euphausiids at the deep station but avoided
them at the shallow station.

Juvenile salmon diet overlap

Juvenile salmon diets rarely overlapped significantly.
Diet overlap for the most frequently co-occurring (n=ll
hauls) species, chum and Chinook salmon, ranged from
10.5% to 66.8%, and averaged 38.3%. PSI was significant
only on June 1985 and August 1987, when both species
consumed euphausiids, hyperiid amphipods, and C.
pacificus. We observed the greatest diet overlap between
coho and Chinook salmon, which both ate decapod prey
in June 1986 and 1987, for an average PSI of 77.9%. Diet
similarities varied for the other juvenile salmon species
and were based on only one or two co-occurrences. For
juvenile chum and coho salmon, the PSI was only 10.8%;
for juvenile pink and chum salmon, the PSI was 58.9%
in April 1986.

Salmon diets also varied spatially; however, the PSI
was not significant for any of the 13 intraspecific com-
parisons between stations, and averaged only 26.5%.
Chinook salmon PSI was approximately 30% (/?= 7), and
that of chum (n = 5) and pink (n= 1) salmon was <20%.

Discussion

Juvenile salmon diets, zooplankton abundance and com-
position, and salmon feeding selectivity in Dabob Bay
exhibited considerable spatial, seasonal, and interan-
nual variability. Some notable patterns and trends were
nevertheless evident, and provide important implications
for our understanding of feeding ecology and potential
resource competition among juvenile salmon as they
migrate from nearshore environments to more open
waters.

Food resources and salmon gut fullness

Dramatic differences in the zooplankton communities
between the deep water and nearshore stations occurred
in two of three years. The most striking difference was
the greater biomass of zooplankton, often an order of
magnitude higher, at the deep station compared to the
shallow station (Fig. 4; Bollens et ah, 1992b), primar-
ily because of the greater abundance of large, verti-
cally migrating zooplankton at the deeper station (e.g.,
euphausiids and large calanoid copepods). Because zoo-
plankton biomass represents a measure of overall food
abundance (although see below for an alternative inter-
pretation), we expected to see differences in gut fullness

between the two stations if juvenile salmon were food
limited and did not often migrate between the sites (a
distance of 9 km). However, despite this large difference
in prey resources between sites, we found no evidence
for fuller salmon guts at the deep station. In addition,
different zooplankton communities were consistently
observed between stations (Fig. 5), which could explain
the low diet overlap of each salmon species between sta-
tions (mean PSI=27%).

Gut fullness can be a useful indicator of feeding suc-
cess. However, gut fullness does not account for poten-
tial differences in prey nutritional quality (Brodeur,
1992; Armstrong et al., 2008). Given equal gut fullness,
feeding success may be greater for fish that consumed a
larger proportion of high quality prey than were eaten
by congener species. We observed very high gut fullness
(9% of body weight) in juvenile chum salmon during
early summer 1986, but much of the diet was composed
of low-quality food items such as larvaceans. Data on
prey quality would enhance future comparisons of ju-
venile salmon diets and gut fullness.

Electivity patterns and ontogeny

The nearshore feeding ecology of the earliest marine
stages of juvenile salmon <100 mm has been studied well
in the past (e.g., Kaczynski et al., 1973; Sturdevant et
al., 1996), and juvenile salmon feeding ecology, species-
specific feeding preferences, and prey selection for fish
>100 mm in length captured in highly variable near-
shore coastal environments have been examined in more
recent studies (Moulton, 1997; Landingham et al., 1998;
De Robertis et al., 2005, Armstrong et al., 2008). Ours
is one of few studies where larger juvenile fish from
transitional inland marine habitats have been examined
(Willette, 2001; Sturdevant et al., 2004; Armstrong et
al., 2008).

A variety of zooplanktivorous fish select prey dis-
proportionate to their abundance in the environment
(e.g., Lazzaro, 1987; Gerking, 1994). For salmon and
other fishes, these patterns have been attributed to
multiple factors, including: prey size (Brodeur, 1991);
prey pigmentation or other visual indicators (Peterson
et al., 1982; Schabetsberger et al., 2003); and verti-
cal migration behavior of predator and prey (Bollens
and Frost, 1989; Viitasalo et al., 2001). Our three-year
study of juvenile salmon feeding in Dabob Bay provides
additional evidence that juvenile chum, Chinook, coho,
and pink salmon exhibit ontogenetic shifts in prey size
selection and that they select for larger and more visu-
ally conspicuous prey. Previous studies showed that diel
vertical migration is an important mediator of plank-
tivore trophic interactions in Dabob Bay (e.g., Bollens
and Frost, 1989; Frost and Bollens, 1992; Bollens et
al., 1993).

Juvenile salmon in Dabob Bay used a diverse prey
field and demonstrated species-specific prey preferences.
Chum and Chinook salmon both highly preferred in-
sects, cephalopods, decapod larvae, hyperiid amhipods,

Bollens et al.: Feeding ecology of |uvenile Oncorhynchus spp.

403

and teleost prey. Coho and pink salmon both strongly
selected for insects, whereas decapod larvae were im-
portant to the former and gammarid amphipods to the
latter. Our study supports the importance of insect prey
to young juvenile salmon in transitional environments
(Moulton, 1997; Romanuk and Levings, 2005; Weitkamp
and Sturdevant, 2008).

The diet of juvenile chum salmon further differed
from the other salmon species by the abundance of lar-
vaceans (primarily Oikopleura sp.) in their gut contents,
and their consumption of ctenophores. These observa-
tions are consistent with other reports (Simenstad and
Salo, 1980; Black and Low, 1983; Landingham et ah,
1998) and may be related to anatomical gut specializa-
tion, which enables chum salmon to assimilate prey
items that other salmon cannot digest (Welch, 1997;
Arai et al., 2003).

Calanoid copepods have been described as a major
diet item for juvenile salmon generally (Pearcy, 1992),
and for chum and pink salmon specifically (Godin, 1981;
Sturdevant et al., 2004). However, despite a diverse and
abundant assemblage of copepod species in Dabob Bay,
copepods only represented a modest component of our
salmon diets and were particularly limited to smaller
predators. Instead, juvenile salmon in Dabob Bay were
found more often feeding on numerically less abundant
macrozooplankton such as euphausiids, hyperiid am-
phipods, and decapod larvae. Similarly, Peterson et al.
(1982) showed that juvenile coho and Chinook salmon
off Oregon fed more on hyperiid amphipods than on
the numerically dominant copepods. These results sup-
port the results from other studies that indicate that
salmon are more likely to feed on larger, more visible
prey items (Healey, 1980; Schabetsberger et al., 2003),
in which case abiotic factors (e.g., light intensity and
turbidity) and biotic processes (e.g., vertical migration
and predator evasion behavior) will be important vari-
ables that will help determine stomach fullness and
feeding success.

Ontogenetic diet thresholds for juvenile salmon at
approximately 80 mm, before which teleost prey are
less important, have been indicated by other studies
(Brodeur, 1991; Keeley and Grant, 2001). In contrast,
our electivity results provide evidence that teleost prey
were strongly selected for by small (<75 mm) chum and
pink salmon during spring, when fish larvae may have
been particularly small (Bollens et al., 1992a; Fulmer
and Bollens 2005). Simenstad and Salo (1980) found
that juvenile chum salmon transitioned from nearshore
habitats with epibenthic food sources to neritic habi-
tats with pelagic and nektonic food sources when they
reached approximately 45-55 mm FL. In other studies,
seasonal variability in salmon gut contents has been at-
tributed to ontogenetic shifts in feeding preferences or
feeding behavior (Beacham, 1986; Brodeur, 1991; Daly
et al., 2009). Similarly, our results indicate that small
chum, Chinook, and coho salmon select small prey,
then larger prey as the fish develop. Small Chinook
and coho salmon selected Calanus pacificus roughly in

proportion to its abundance, but other copepods were
avoided. Similarly, only small coho salmon selected
gammarid and hyperiid amphipods. In contrast, only
large Chinook salmon selected for gammarids. Thus,
both species-specific and ontogenetic shifts in prey pref-
erence were observed.

Our diet and electivity results should be interpret-
ed cautiously because our samples were pooled across
broad size, temporal, and spatial scales, and because
of limitations associated with sample sizes, net sam-
pling biases, and pooling of prey species and life history
stages. For example, the range of euphausiid electivity
values observed may be due to the pooling of euphausiid
species and life-history stages, potentially obscuring
euphausiid prey selection patterns observed in other
studies (Schabetsberger et al., 2003).

Another major caution concerns our ability to deter-
mine “available prey” with plankton nets. More mo-
bile and larger nektonic prey, such as cephalopods and
young fish, are able to avoid conventional plankton nets,
with the consequence that electivity indices for these
prey types would be biased upward. Conversely, small
prey types that are unable to avoid the plankton net
(e.g., small copepods) would be proportionately over-
represented in the net samples, with the consequence
that electivity indices for these forms would be biased
downward. We recommend that further research be
undertaken into adequately sampling macrozooplank-
ton and micronekton (e.g., Gewant and Bollens, 2005),
such that a broader and potentially more appropriate
range of potential prey for fishes can be quantitatively
sampled.

Several additional complicating factors should be
considered when interpreting electivity indices. First,
strongly positive electivity (e.g., E; = 1.00) often results
from a rare presence of a species in the gut contents
and a corresponding absence of that same species in
the plankton. In some cases zero abundance in the
plankton may be due to low-volume plankton hauls
which under-sample the available prey field. Conversely,
an Ex of —1.00 could result from a rare (but nonzero)
occurrence of a species in the environment, combined
with its absence from the gut contents, perhaps simply
because of a low probability of encounter between preda-
tor and prey.

A final caution concerns the vertical resolution of
sampling. Landingham et al. (1998) used both neuston
and oblique plankton tows and showed that salmon
diet most closely resembled that of the neuston assem-
blage. The upper 50 m were sampled with our sampling
methods and therefore electivity values may have been
biased. For example, if juvenile salmon are primarily
feeding near the surface, abundant zooplankton (i.e., co-
pepods) that are more deeply distributed may not fully
be part of the “available” prey community. We recom-
mend finer-scale, vertically resolved sampling of juve-
nile salmon and their potential prey in future studies.

Dabob Bay has been the site of numerous studies for
which the interactions between planktivorous fishes and

404

Fishery Bulletin 108(4)

the behaviors exhibited by their potential prey have
been explored (Ohman, 1986; Frost, 1988; Bollens and
Frost, 1989; Bollens et al., 1992a; Bollens et ah, 1993).
Field studies by Bollens and Frost (1989) indicated
that abundances of actively feeding planktivorous fish
(including Oncorhynchus spp.) are directly linked with
the strength and timing of vertical migration exhibited
by the copepod Calanus pacificus. Our results indicate
that the adaptive response exhibited by species such
as Calanus pacificus seems to be an effective mecha-
nism for avoiding predation by species such as juvenile
salmon. Thus, “available” prey items are not only those
that are abundant or of the desired size, but those that
are also available for visual detection. Availability may
be affected by the prey’s presence or absence from the
photic zone, or by the presence of pigmentation that
makes the prey more detectable visually. Most of the
prey items that were consistently consumed by salmon
in this study (e.g., euphausiids, hyperiid and gammarid
amphipods, and decapod larvae) possess characteristi-
cally dark or large eyes. The ability of salmon to detect
these potential prey items may be increased by heavy
pigmentation, large body size, and their frequently not-
ed association with the near surface layer (Lough, 1976;
Peterson et al., 1982) where salmon typically feed.

Diet overlap and potential interspecific competition
among salmon species

A variety of studies have relied on diet overlap as a pri-
mary indicator of potential resource competition between
co-occurring species. Although there is little consensus
among studies of salmon, diet overlap has been most
frequently observed between Chinook and coho salmon in
Oregon and Washington (Peterson et al., 1982; Emmett
et al., 1986; Brodeur and Pearcy, 1990; Brodeur, 1991),
and to a lesser extent between chum, pink, and sockeye
salmon ( Oncorhynchus nerka) in British Columbia and
Southeast Alaska (Healey, 1980; Beacham, 1993; Land-
ingham et al., 1998). Our results from Dabob Bay show
the greatest spatial and temporal overlap between chum
and Chinook salmon but also provide evidence only for
resource partitioning (low diet overlap) between these
two species, not necessarily competition (which would
require resource limitation).

In contrast, our data show significant diet overlap
between Chinook and coho salmon (average PSI=77.9%),
supporting earlier reports of potential resource com-
petition between these two species. Although Brodeur
and Pearcy (1990) did not see evidence for significant
overlap between four salmon species when all observa-
tions were combined, they observed significant overlap
between Chinook and coho salmon during May and
June, as well as during the 1983 El Nino. Likewise we
found that significant overlap between Chinook and
coho salmon occurred during June (of 1986 and 1987),
largely because of the shared consumption of decapod
larvae, which are visually conspicuous and seasonally
abundant at this time of year. However, the co-occur-
rence of juvenile Chinook and coho in Dabob Bay was

less prominent than in coastal Oregon (Peterson et al.,
1982; Brodeur and Pearcy, 1990; Brodeur and Pearey,
1992); however, our results are based on far fewer data.

Despite the co-occurrence of different juvenile salmon
species in Dabob Bay, and the occasional occurrence of
significant diet overlap between these species, we did
not see any indication of food limitation. That is, there
was never a significant relationship between stomach
fullness and zooplankton biomass, as might be expected
if food was limited. However, just as with the electivity
indices discussed above, we caution that our vertical
plankton net hauls may not adequately sample the po-
tential prey of juvenile salmon. Testing for food limita-
tion by correlating salmon stomach fullness and the
abundance of potentially more appropriate prey (e.g.,
macrozooplanktonic, micronektonic, and neustonic prey)
would prove interesting, but was not possible given our
sampling method. Similarly, our comparison of zoo-
plankton dry weights with salmon stomach wet weights
complicates the interpretation of food limitation and po-
tential competition because conversions from wet-weight
to dry-weight would be expected to vary between prey
taxa (e.g., between gelatinous and crustacean prey).

Resource limitation by juvenile salmon during their
early marine transition may be influenced by several
other factors not addressed in our study, including di-
rect and indirect effects of hatchery production in the
region (Quinn et al., 2005) and potential diet overlap
with other zooplanktivores (Purcell and Sturdevant,
2001). Furthermore, zooplankton dynamics in temper-
ate marine waters are clearly influenced by interan-
nual (El Nino cycles) and interdecadal (Pacific Decadal
Oscillation) scales of climate variability (Mackas et
al., 2001; Hooff and Peterson, 2006) and there are im-
portant linkages to salmon survival during multiple
life-history stages (Beamish and Bouillon, 1993; Loger-
well et al., 2003). Although diet data from our three-
year study could be averaged across years (as opposed
to size classes, etc.), interannual climate factors can-
not be overlooked. Indeed, based on a multivariate El
Nino-Southern Oscillation index (MEI), 1987 ranks
as a moderate to strong El Nino year (April-October
MEI average = 1.91), and likewise represents the most
anomalous year of our study for seasonal plankton com-
position in Dabob Bay. This was particularly apparent
at the deeper station, where the abundance of Oithona
sp. and larvaceans seemed to be more characteristic
of the shallow, nearshore station in 1985 and 1986.
Mechanisms underlying the interannual variability of
zooplankton composition in Dabob Bay warrant further
exploration.

Our combination of detailed analyses of prey fields
and fish diets is clearly only one approach to under-
standing juvenile salmon feeding ecology. Biochemical
methods of studying energetics and feeding relation-
ships (e.g., Johnson and Schindler, 2009) provide ad-
ditional insight into juvenile salmon trophic dynamics.
Studies across the variety of habitats encountered by
salmon during their outmigration and early residence
in marine environments will be necessary to fully un-

Bollens et al.: Feeding ecology of juvenile Oncorhynchus spp.

405

derstand species-specific responses to resource and en-
vironmental variability. Our results from Dabob Bay
indicate that periodic high diet overlap between salmon
species may occur. However, evidence of resource parti-
tioning, especially between frequently co-occurring spe-
cies (e.g., chum and Chinook salmon), combined with a
lack of evidence for food limitation (although this should
be more explicitly tested in the future), indicates that
competition between juvenile salmon is unlikely to oc-
cur in this marine fjord.

Acknowledgments

We thank D. Thoreson, S. Jonasdottir, C. Mobley, and
the crew of the RV Barnes for assistance with field work,
W. Peterson for assistance with zooplankton analyses,
and J. Breckenridge and J. Emerson for assistance with
graphics. R. Brodeur and three anonymous reviewers
provided comments that substantially improved the
manuscript. Special thanks go to S. Simenstad and
K. Fresh for helping a young oceanography graduate
student bridge the gap between fisheries and biological
oceanography. We also thank the University of Otago’s
Departments of Zoology and Marine Sciences for provid-
ing office space and other support to S. Bollens during
the writing of this article. This research was supported
by National Science Foundation grant 84-08929 to B.
Frost, and Washington State University institutional
funds (including a sabbatical leave) made available to
S. Bollens.

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408

Abstract — Despite its recreational
and commercial importance, the move-
ment patterns and spawning habitats
of winter flounder (Pseudopleuronectes
americanus) in the Gulf of Maine
are poorly understood. To address
these uncertainties, 72 adult winter
flounder (27-48 cm) were fitted with
acoustic transmitters and tracked by
passive telemetry in the southern Gulf
of Maine between 2007 and 2009. Two
sympatric contingents of adult winter
flounder were observed, which exhib-
ited divergent spawning migrations.
One contingent remained in coastal
waters during the spawning season,
while a smaller contingent of winter
flounder was observed migrating to
estuarine habitats. Estuarine resi-
dence times were highly variable, and
ranged from 2 to 91 days (mean = 28
days). Flounder were nearly absent
from the estuary during the fall
and winter months and were most
abundant in the estuary from late
spring to early summer. The observed
seasonal movements appeared to be
strongly related to water temperature.
This is the first study to investigate
the seasonal distribution, migra-
tion, and spawning behavior of adult
winter flounder in the Gulf of Maine
by using passive acoustic telemetry.
This approach offered valuable insight
into the life history of this species in
nearshore and estuarine habitats and
improved the information available for
the conservation and management of
this species.

Manuscript submitted 4 February 2010.
Manuscript accepted 30 June 2010.
Fish. Bull. 108:408-419 (2010).

The views and opinions expressed or
implied in this article are those of the
author (or authors) and do not
necessarily reflect the position
of the National Marine Fisheries
Service, NOAA.

Movement patterns of winter flounder
(Pseudopleuronectes americanus )
in the southern Gulf of Maine: observations
with the use of passive acoustic telemetry

Gregory R. DeCelles (contact author)

Steven X. Cadrin

Email address for contact author: gdecelles@umassd.edu
National Oceanic and Atmospheric Administration

and University of Massachusetts Cooperative Marine Education and Research Program
School for Marine Science and Technology
200 Mill Rd„ Suite 325
Fairhaven, Massachusetts 02719

Winter flounder ( Pseudopleuronectes
americanus) is a commercially and
recreationally important flatfish spe-
cies that is distributed along the east
coast of North America from North
Carolina northward to Newfoundland
(Bigelow and Schroeder, 1953). Within
U.S. waters, this species is managed
as three stock units: the southern New
England and Mid-Atlantic (SNE-MA);
Gulf of Maine; and Georges Bank. To
date, there has been less research on
the Gulf of Maine stock than on the
SNE-MA stock. Seasonal distribution
patterns of winter flounder in the Gulf
of Maine have emerged from fisheries
catch data (McCracken, 1963), mark
recapture experiments (Perlmutter,
1947; Howe and Coates, 1975) and
annual trawl surveys. However, these
sources of data offer limited insight
into patterns of estuarine residence
and nearshore habitat use for winter
flounder because trawl fisheries and
research surveys in the Gulf of Maine
are typically limited to coastal and
offshore waters. In addition, these tra-
ditional sampling sources for obtain-
ing distribution data cannot identify
individual variability in movement
or spawning behavior. In the present
study, we sought to investigate spawn-
ing patterns and seasonal distribu-
tion of winter flounder in nearshore
and estuarine waters in the southern
Gulf of Maine using passive acoustic
telemetry.

The magnitude of variability in in-
dividual migration patterns remains

poorly understood for even the most
economically valuable fish species
(Able and Grothues, 2007), in part
because we have yet to recognize the
importance of contingent behavior.
Contingents are cohesive groups of
fish within a population that ex-
hibit a common migration pattern
(Cadrin and Secor, 2009). Acoustic
telemetry offers new opportunities to
investigate the fine-scale movements
and behavior of individual fish. This
technology allows for the recognition
of contingent groups within popula-
tions (Secor, 1999) and offers insight
into the amount of connectivity be-
tween estuarine and coastal popula-
tions (Able, 2005). Acoustic telem-
etry has been used to gather high
resolution data on the behavior of
juvenile winter flounder in the Gulf
of Maine (Fairchild et al., 2009).
However, before the present study,
this technology had not been used
to study adult winter flounder in the
Gulf of Maine.

Traditionally, winter flounder
spawning in the Gulf of Maine was
thought to be restricted to estuarine
habitats (Bigelow and Schroeder,
1953). This assumption was subse-
quently reflected in designations of
Essential Fish Habitat (EFH) for
this species (NMFS, 1999). How-
ever, other observations indicate
that winter flounder in the Gulf of
Maine also use coastal waters as
spawning grounds (i.e., Howe and
Coates, 1975). If a proportion of in-

DeCelles and Cadrin: Movement patterns of Pseudopleuronectes americanus in the southern Gulf of Maine

409

70“42'W 70°40'W 70‘38'W 70‘36'W 70'341/V

Map of the study site showing the locations of Plymouth Bay and
Plymouth Estuary in the Gulf of Maine where the movements of winter
flounder (Pseudopleuronectes americanus) were tracked with passive
acoustic telemetry. Locations of tag releases and acoustic receivers
are shown. Receivers used to track winter flounder movements from
November 2007 to November 2008 are shown as solid black circles
and receivers added to the array in December 2008 are shown as
open circles. Circles are not drawn to scale and do not represent the
detection radii of acoustic receivers.

dividuals spawn in coastal, rather than
estuarine habitats, these fish would
represent contingents within the larger
population. Contingents may provide
populations with enhanced stability
and resilience because of the variable
survival rates of early life history stag-
es in different habitats (Secor, 2007;

Kerr et al., 2010). Divergent spawning
migrations increase the distribution
of eggs and larvae, which may reduce
the probability of a failed recruitment
event (Lambert, 1990). For winter
flounder that spawn demersal eggs, the
conditions encountered by the early life
history stages are largely determined
by the locations where the adults
spawn. Therefore, divergent spawning
migrations may have a large effect
on the recruitment success of local
populations.

We chose to monitor adult winter
flounder in Plymouth Bay and the ad-
jacent Plymouth Harbor, Kingston Bay,
and Duxbury Bay estuary. Plymouth
Harbor, Kingston Bay, and Duxbury
Bay estuary are commonly referred
to as the Plymouth Estuary, and that
name will be used throughout this ar-
ticle. Winter flounder is a dominant
member of the groundfish community in
the Plymouth Estuary, and the estuary
serves as an important nursery area
for this species (Lawton et ah, 1984).

Winter flounder are known to spawn
in the Plymouth Estuary, where peak
spawning occurs in March and April
(Entergy1). In addition, Plymouth Bay
has been identified as an area where
coastal spawning likely occurs (NMFS,

1999).

The goal of this study was to obtain
high-resolution data on the seasonal
distribution, migrations, and spawning
behavior of winter flounder in the southern Gulf of
Maine. In particular, three primary objectives were
addressed during this study: 1) to determine if adults
in this region exhibit divergent spawning migrations;
2) to investigate the seasonal distribution of winter
flounder in the region, in association with water tem-
perature; and 3) to compare the seasonal distribution
observed in this study to that observed in past research
in the Gulf of Maine where static sampling methods
were used.

1 Entergy. 2001. Ichthyoplankton entrainment monitoring
at Pilgrim Nuclear Station, January-December, 2000. In
Marine ecology studies related to operation of Pilgrim Station.
Report no. 57, 65 p. Entergy Nuclear Generation Company.
Plymouth, MA.

Materials and methods
Study site

The Plymouth Estuary and Plymouth Bay are located in
the southern portion of the Gulf of Maine (Fig. 1). The
Plymouth Estuary is bordered on its seaward side by two
barrier beaches. Tidal exchange between the Plymouth
Estuary and Plymouth Bay occurs through a 2020-m
opening between Saquish Head and the northern extrem-
ity of Plymouth Beach. The estuary is well mixed and
approximately 66% of the water is replaced during each
tidal cycle, creating strong tidal currents (Davis, 1984).
Plymouth Bay is bordered by Cape Cod Bay to the east.

The average depth within Plymouth Estuary is 3.3 m
at mean high water and 2.1 m at mean low water, and

410

Fishery Bulletin 108(4)

Figure 2

An example of the external attachment method that was used to secure the acoustic transmitters to winter
flounder (Pseudopleuronectes americanus) to monitor their movements in the southern Gulf of Maine. The Vemco
V92L transmitters were fitted into a harness of 9/16” soft latex tubing and secured in the harness with two-part
epoxy (A). Two nickel tagging pins were passed upwards through the blind side of the fish, through the dorsal
musculature (B).

salinity in the estuary ranges from 0.0 to 33.0 (Iwano-
wicz et al.2). The bathymetry of the estuary is complex,
and extensive sand and mud flats are exposed at low
tide when the surface area of the estuary is reduced
front 10,057 acres to 5465 acres (Iwanowicz et al.2).
A deeper channel is present between Saquish Head
and Plymouth Beach, where depths reach nearly 26 m.
There are four main sources of freshwater input to the
Plymouth Estuary: the Back River, Bluefish River, Jones
River, and Eel River.

Acoustic telemetry

Adult flounder were captured by using either a small
otter trawl, a commercial trawl vessel, or by hook and
line. Sampling was nonrandom, and sampling locations
were chosen from areas where adult winter flounder
have historically been abundant. Tow times with the
small otter trawl varied from 10 to 30 minutes, and tows
with the commercial vessel were 30 minutes in duration.
The total length of each fish was measured to the near-
est centimeter, and only adult fish (>27 cm) in good or
excellent condition were fitted with acoustic tags. After
tagging, fish were held onboard for observation until
they were deemed healthy enough for release. All fish
were released in close proximity to the capture site in
order to minimize tagging-induced stress.

In total, 72 adult winter flounder (27-48 cm) were
fitted externally with acoustic transmitters (model
V92L, 69 kHz, 9 mmx21 mm, Vemco Ltd., Halifax,
NS, Canada) between November 2007 and May 2009.

2 Iwanowicz, H. R., R. D. Anderson, and B. A. Ketschke. 1974. A
study of the marine resources of Plymouth, Kingston and
Duxbury Bay. Monograph Series Number 17, 37 p. Divi-
sion of Marine Fisheries, Boston, MA.

Each transmitter had an average pulse rate of 80 sec-
onds (range = 40-120 seconds) and an expected battery
life of 384 days. A novel external attachment method
was developed for this study. Acoustic transmitters
were secured into a harness of 9/16 inch (14.3 mm)
soft latex tubing by using two-part epoxy (Fig. 2). Two
nickel tagging pins were passed upwards from the blind
side of the flounder through the dorsal musculature.
The harness was then secured to the nickel pins on
the eyed-side of the fish with plastic earring backings.
The tagging procedure took an average of two to three
minutes per fish. A laboratory holding study indicated
100% transmitter retention and 100% survival over a
seven-month period. A separate holding study conducted
at the University of New Hampshire in 2009 indicated
that the tag attachment method did not interfere with
the swimming or spawning behavior of tagged fish (E.
Fairchild, personal commun.3).

In November 2007, 24 prespawning winter flounder
were tagged in Plymouth Bay, approximately 5 km from
the mouth of the Plymouth Estuary (Fig. 1). Three
of these winter flounder were observed to be gravid
females at the time of release. Repeated efforts were
made to capture spawning flounder within the estuary
during March, April, and early May of 2008, but we
were not able to capture adult fish until late May 2008.
Twenty three adult winter flounder were tagged within
the Plymouth Estuary between 24 May and 16 June
2008 (Fig. 1). In the second year of the study, an addi-
tional 25 winter flounder were tagged in Plymouth Bay
between December 2008 and May 2009 (Fig. 1). Eight
winter flounder tagged on 8 May 2009 were observed to
be gravid females that were in spawning condition.

3 Fairchild, Elizabeth. 2009. Department of Biological Sci-
ences, Univ. New Hampshire, Durham, NH 03824.

DeCelles and Cadrin: Movement patterns of Pseudopleuronectes americanus in the southern Gulf of Maine

411

Winter flounder tagged between November 2007 and
June 2008 (n = 47) were tracked within the Plymouth
estuary by using a moored array of 15 wireless receiv-
ers (model VR2 and VR2W, Vemco Ltd.; Fig. 1). Six of
these receivers (I, J, K, M, N, and O; referred to as the
“inner gate”) were configured as a parallel curtain that
spanned the mouth of the Plymouth estuary, allowing
the movements of fish traveling between Plymouth Bay
and Plymouth estuary to be recorded precisely. Parallel
curtain arrays are advantageous because they allow the
direction of movement for each fish to be obtained ( Heu-
pel et al., 2006). Range testing was performed at the
mouth of the estuary by placing transmitters on the bot-
tom in different locations for ten-minute intervals. After
range testing, receivers within the parallel curtain
were positioned to ensure that overlap existed between
the detection radii of adjacent receivers. Tagged winter
flounder were monitored within the upper reaches of
the Plymouth estuary by using nine receivers positioned
in a nonoverlapping grid array. These receivers were
placed within the deeper channels of the Plymouth
estuary to maximize their detection radii.

During the second year of the study, the receiver
array was expanded from 15 to 30 wireless receivers
(Fig. 1). Ten receivers (P-Y; referred to as the “outer
gate”) were deployed across the mouth of Plymouth
Bay, from Gurnet Point in Duxbury southward to
Rocky Point in Plymouth. This arrangement allowed
us to track the movement of tagged winter flounder
between Cape Cod Bay and Plymouth Bay. An ad-
ditional five receivers (Z-DD) were placed within the
upper reaches of the Plymouth estuary. Expanding the
receiver array allowed us to test more directly our hy-
potheses about the spawning behavior of the 25 winter
flounder that were tagged between 10 December 2008
and 8 May 2009.

Before their retrieval in 2009, six of the 30 acoustic
receivers were lost, likely because of boat traffic, in-
teractions with commercial fishing gear, or because of
winter storms. Receivers P and Y were lost from the
outer gate between Cape Cod Bay and Plymouth Bay.
Receivers I, M, and O were lost from the parallel cur-
tain between Plymouth Bay and the Plymouth estuary.
Subsequently, receiver G was moved from the “Cowy-
ard” and placed adjacent to the position of receiver M
to improve the coverage in this area. Receiver H in
Plymouth Harbor was also lost, likely because a high
volume of boat traffic in the area.

Data analysis

The movement track of each tagged fish was visualized
by using GIS software (ArcMap vers. 9.3, ESRI, Red-
lands, CA). Estuarine residence time was calculated as
the time elapsed between the first and last detection
for each individual within the Plymouth estuary. If a
tagged winter flounder was recorded within the estuary
on more than one occasion, the total days spent within
the estuary during each visit were combined to calculate
residence time for that individual.

Winter flounder were classified as either estuarine
or coastal spawners on the basis of their observed lo-
cations during the peak spawning months of March
through May. Fish that were detected within the Plym-
outh estuary at any time over this three month span
were classified as estuarine spawners, whereas winter
flounder that remained in coastal waters were classified
as coastal spawners. A G-test for independence (Sokal
and Rohlf, 2001) was performed to examine whether
significant interannual variability was present in the
proportion of tagged winter flounder that were classi-
fied as estuarine spawners in 2008 and 2009. The ratio
(with 95% confidence intervals) of estuarine to coastal
spawners observed over the two-year period was calcu-
lated (Sokal and Rohlf, 2001).

Abiotic monitoring

During the study, bottom water temperature was moni-
tored at four locations within the study site. Three
temperature loggers (Vemco Ltd.; 8-bit minilog TR)
were attached to the moorings of receivers A, E, and
K within the Plymouth Estuary. These temperature
loggers were placed 0.5 meters above the bottom and
were programmed to record bottom water temperature
every 30 minutes. A temperature logger placed in the
southeastern portion of Plymouth Bay recorded bottom
water temperature once every two hours in 2007 and
2008. In September 2008, another temperature logger
was placed on the mooring of receiver T to record bottom
temperature in Plymouth Bay. In 2009 some of the tem-
perature loggers failed. When available, bottom water
temperature data were averaged weekly at each site.

Results

With passive acoustic telemetry, we successfully gath-
ered high-resolution data on the migration, spawn-
ing behavior, and seasonal distribution of adult winter
flounder in the southern Gulf of Maine. Twenty eight of
the 47 winter flounder tagged during the first year of
the study were later detected within the Plymouth estu-
ary, yielding a total of 16,956 detections in our array
of acoustic receivers. Twenty two of the 25 fish tagged
during the second year of the study were later detected
in the receiver array, resulting in 97,394 unique detec-
tions. A summary of data for each tagged winter flounder
that was later detected is given in Table 1.

Spawning behavior

Based on the observed movements of tagged winter
flounder during the spawning season, the presence of
two contingent spawning groups of flounder was evident
in the region: coastal spawners and estuarine spawners.
In both years of the study, the majority of tagged winter
flounder exhibited coastal spawning behavior. Only five
of the 24 winter flounder (21%) tagged in Plymouth Bay
in 2007 were classified as estuarine spawners. Seven of

412

Fishery Bulletin 108(4)

Table 1

Summary of information for tagged winter flounder ( Pseudopleuronectes americanus ) that was detected during the study. For
each tagged winter flounder, the date of release and date of last location are given. The total number of detections, and receivers
at which that winter flounder was detected, is provided. For the release locations, PB=Plymouth Bay and PE=Plymouth Estuary.

Tag ID

Length (cm)

Release date

Release location

Last detection

No. of detections

Receiver stations

5837

34

11/30/2007

PB

8/26/2008

27

Outer Cape

5839

28

11/30/2007

PB

10/30/2008

63

C,F,G,N

5850

30

11/30/2007

PB

11/19/2008

2030

C,J,K,M,N,0

5852

32

11/30/2007

PB

6/1/2008

735

J,K,N,0

5862

29

11/30/2007

PB

6/12/2008

100

C,D,K,M,0

5867

36

11/30/2007

PB

5/28/2008

1

K

5868

34

11/30/2007

PB

8/25/2008

1458

J,K,M,N,0

5877

32

11/30/2007

PB

6/22/2008

799

E,F,G,I,M,0

5832

29

5/24/2008

PE

6/17/2008

44

B,C,J

5833

27

5/24/2008

PE

9/30/2008

3227

B,C,J,K,N

5840

33

5/24/2008

PE

6/10/2008

1681

C,J

5844

27

5/24/2008

PE

6/12/2008

957

C,J,K,M,0

5845

35

5/24/2008

PE

6/13/2008

338

C,J,N

5847

42

5/24/2008

PE

7/30/2008

3198

C,J,K,M,N,0

5855

36

5/24/2008

PE

5/26/2008

90

D

5858

29

5/24/2008

PE

6/15/2008

30

K,M

5859

35

5/24/2008

PE

7/7/2008

18

C,J,N

5866

42

5/24/2008

PE

6/15/2008

119

A,C,J

5873

27

5/24/2008

PE

6/13/2008

267

B,K,M

5878

35

5/24/2008

PE

6/13/2008

217

B,C,J

5835

39

6/6/2008

PE

6/10/2008

55

J,K,M,0

5846

30

6/6/2008

PE

6/21/2008

18

C,J

5856

33

6/6/2008

PE

8/18/2008

211

C,J

5864

27

6/6/2008

PE

6/23/2008

27

B,I,M

5874

38

6/6/2008

PE

6/15/2008

636

B,C,J,N

5871

27

6/9/2008

PE

6/14/2008

9

M,0

5876

36

6/9/2008

PE

9/14/2008

546

C,J,K,N,0

5843

28

6/16/2008

PE

10/6/2008

18

C,K

5872

27

6/16/2008

PE

7/24/2008

37

C,N

53876

33

12/10/2008

PB

5/2/2009

10346

G,K,N,X

53877

31

12/10/2008

PB

8/26/2009

6750

G , Q , R ,T,U,V, W, X , MA Bay

53879

36

12/10/2008

PB

7/25/2009

19394

V,W,X

53884

36

12/10/2008

PB

5/13/2009

1484

Q,R,S,T,U,V,W,X

53886

31

12/10/2008

PB

7/8/2009

14089

G,K,N,S,T,U

53887

30

12/10/2008

PB

7/20/2009

5061

Q,R,S,T,U,V,W,X

53888

31

12/10/2008

PB

6/14/2009

23842

G,J,K,N,R,S,T,U

53890

29

12/10/2008

PB

6/27/2009

57

X

53891

32

12/10/2008

PB

5/22/2009

443

G,K,N,R,S,T,U.V

53894

41

12/10/2008

PB

7/28/2009

3611

C,E,Q,R,S,T,U,V,W,X

53896

31

12/10/2008

PB

6/26/2009

361

X

53892

37

3/10/2009

PB

6/18/2009

1215

R,U,V,W,X

53893

34

3/10/2009

PB

7/8/2009

288

X

53874

33

4/9/2009

PB

4/11/2009

1061

R,S,T,U

53883

35

4/9/2009

PB

5/4/2009

3018

Q,R,S

53885

31

4/9/2009

PB

7/14/2009

2074

G,K,J,N,Q

53873

39

5/8/2009

PB

5/24/2009

620

Q,U,S,T,U,V,W,X

53875

37

5/8/2009

PB

5/12/2009

177

Q,R,S,T,U,V,W

53878

36

5/8/2009

PB

6/12/2009

2230

G,K,Q,R,S,T,U.X

53881

36

5/8/2009

PB

7/25/2009

479

Q,R,S,T,U,V,W,X

53895

36

5/8/2009

PB

6/25/2009

701

B,C,G,J,N,W,X

53897

48

5/8/2009

PB

5/10/2009

93

V,W,X

DeCelles and Cadrin: Movement patterns of Pseudopleuronectes americanus in the southern Gulf of Maine

413

T3

O

A

J

L i.i

Ial .iiii l

f />VV /// ^vv

Total number of detections per day

C?5 o?5

0*0 rtO o'O nV> AO 00 nO nO" nO nO 00~ nO nO rO

^ ■/ / /- / /■ /• ^ ,# /• &

Number of fish detected per day

B

1.

1

»

_u Al . lift

Kt Jm 1 1 ii i ii

8

u

A

cS?

^ ^ ^

F 4? 4? # jr 4P 4? ^ n# 4$ 44 4P1 4P3

D dp -A3 .rf? AV .Ay o5> 'r'b ■*>

$> r5t> rSb rSb

kN 3> J 4

4? 4? <r ^ <r & # ^

Percentage of receivers with detections, per day

Figure 3

Temporal patterns of winter flounder (Pseudopleuronectes americanus)
detections obtained by using passive acoustic telemetry in the Plymouth
Estuary, MA, between January 2008 and October 2008. (A) The total
number of detections each day. (B) The number of tagged winter flounder
that were detected each day. (C) The percentage of acoustic receivers that
detected a tagged winter flounder during each day of the study.

the 25 winter flounder (28%) released
in Plymouth Bay during 2008 and 2009
were observed to be estuarine spawn-
ers. A G-test for independence revealed
no significant interannual variability
(P=0.56) in the ratio of coastal and
estuarine spawners between the two
years. In total, only 12 of the 49 (25%)
tagged winter flounder were noted to
be estuarine spawners. The 95% upper
confidence limit for this proportion was
calculated to be 0.70. If spawning was
restricted to estuaries, the proportion of
winter flounder classified as estuarine
spawners would be one (100%). There-
fore, our results demonstrate that in
the Plymouth Bay region of the Gulf of
Maine, winter flounder spawning is not
restricted to estuaries.

Eleven winter flounder were observed
to be gravid females at the time of
release. Only one of the three gravid
females tagged in Plymouth Bay in
November 2007 was later detected in
the estuary, but not until May of the
following year. Eight gravid females
were tagged in Plymouth Bay on 8
May 2009. Two of these individuals
migrated rapidly to the mouth of the
estuary. These females were detected
at the mouth of the estuary six and
ten days after release, respectively.

Whether these individuals spawned in
the estuary, or migrated to the estuary
after spawning in coastal waters is un-
known. It was apparent that the six of
eight gravid winter flounder remained
in Plymouth Bay after being tagged.

Seasonal distribution

The seasonal distribution of tagged
winter flounder in the Plymouth Bay
region became apparent after two years
of passive telemetry. Adult winter flounder were largely
absent from the Plymouth estuary during the winter
months in both years. Only four of the 38 tagged winter
flounder at large during the winter of 2008 and 2009
were detected in the Plymouth estuary (Figs. 3 and 4). In
the winter of 2008, temperatures were warmer and more
stable in Plymouth Bay (range = 1.2-5.0°C) than in the
Plymouth estuary (range = -1.24-5.2°C) (Fig. 5). In the
winter of 2009, the observed temperature ranges were
similar in Plymouth Bay (— 0.6-5. 0°C) and the Plymouth
estuary (-0.9-5.9°C).

The movement of winter flounder into the Plymouth
estuary began during the spring and was coincident
with an increase in water temperature. Some tagged
winter flounder began to migrate into the estuary in
mid-April, when estuarine temperatures ranged from

9° to 12°C. In 2008, the mean temperature observed
when winter flounder migrated from Plymouth Bay in
to the Plymouth Estuary was 10.9°C. Tagged floun-
der were most abundant within the estuary between
May and early June (Figs. 3 and 4) when temperatures
ranged from 9° to 16°C, and this was also the only
period when we were able to capture adult flounder in
the estuary. The majority of winter flounder tagged in
2009 remained in the coastal waters of Plymouth Bay
in late spring, where water temperatures ranged from
9° to 13°C.

We observed an emigration of tagged winter flounder
from the Plymouth estuary during the onset of summer,
as water temperatures increased. The mean observed
temperature when tagged winter flounder emigrated
from the estuary was 13.9°C, and 89% of all recorded

414

Fishery Bulletin 108(4)

departures from the estuary occurred when bottom
temperatures were >12°C. In 2008, 18 of the 23 (78%)
winter flounder tagged within the estuary migrated to
coastal waters over a three week period from 30 May to
19 June (Fig. 6). This emigration coincided with a sharp
increase in water temperature throughout the estuary.
As of 19 June 2008, water temperatures exceeded 15°C
in all but the deepest portion of the estuary. During
July and August of 2008 when temperatures reached
their seasonal maxima, no winter flounder were detect-
ed in the upper reaches of the estuary, and six winter
flounder were detected at the mouth of the estuary,
where temperatures were the coolest. In July 2009, only

one winter flounder was detected in the estuary, for a
period of one day.

Our observations on the autumn distribution of win-
ter flounder in the Plymouth estuary were limited to
2008. Results indicated that five tagged individuals re-
turned to the estuary as water temperatures decreased
below their seasonal maxima.

For tagged winter flounder that were detected in the
estuary, residence times within the estuary ranged from
2 to 91 days (mean=29 days). The estuarine residence
times of fish tagged in Plymouth Bay (mean =40 days)
were significantly greater than the residence times for
winter flounder tagged in the estuary (mean=22 days)
(single-factor ANOVA; P=0.025). No re-
lationship was found between fish size
and estuarine residence time (P=0.88).
For winter flounder tagged within the
Plymouth estuary in 2008, the observed
residence time is almost certainly an
underestimate because it is unknown
how long these fish were present in the
estuary before being tagged.

Detections of tagged winter floun-
der were not uniformly distributed
throughout the study site. In the first
year of the study, the inner gate of
acoustic receivers typically detected
more flounder and had more detections
than receivers located within the estu-
ary (Fig. 7, A and B). Tagged winter
flounder were detected throughout the
estuary, and seven of the nine receiv-
ers inside the estuary detected at least
one tagged flounder. In the second year
of the study, tagged winter flounder
were most commonly detected in the
coastal waters of Plymouth Bay. The
outer gate of receivers in Plymouth Bay
typically detected the greatest number
of winter flounder and had the larg-
est number of detections (Fig. 7, C
and D). Two tagged winter flounder
(Tags 53876 and 53886) remained at
the inner gate for long periods of time
within the detection radii of receivers
G and K, which accounted for the large
number of detections by these receiv-
ers (Fig. 7D). In 2009, tagged winter
flounder were detected at only three of
the 12 receivers inside the estuary, and
the low number of detections (<1000 )
at these three receivers indicates that
residence within the estuary was brief.
The bimodal distribution of receiver
detections (e.g., Fig. 70 supports the
inference of divergent habitat use,
spawning behaviors, and contingent
structure.

Two tagged winter flounder were
detected at receivers used by other

Total number of detections per day

Vi6 X? X? X? aC? X? aC? ^ x? ^ x? x? ^

T> T>1' " vv -->■

Number of fish detected per day

■o

nj

2 ^ XS° a<5° VT aO3 nX5° XT’ rS>J .XT aO

Percentage of receivers with detections, per day

Figure 4

Temporal patterns of winter flounder ( Pseudopleuronectes americanus )
detections obtained by using passive acoustic telemetry in the Plym-
outh Estuary and Plymouth Bay, MA, between December 2008 and July
2009. (A) The total number of detections each day. (B) The number of
tagged winter flounder that were detected each day. (C) The percentage
of acoustic receivers that detected a tagged winter flounder during each
day of the study.

DeCelles and Cadrin: Movement patterns of Pseudopleuronectes americanus in the southern Gulf of Maine

415

O

J5P <SP <5P ss“ . 52P <? .Sf' jSf

* * & ^ & v# cf * ~ '■

<? ^ <(e' ^ ^sr ^ ^ V

o° <?

S? & J? s? j? . s?>
/■ ^ ^ xT

Figure 5

Weekly averaged bottom water temperatures observed between November
2007 and July 2009. Water temperature was recorded every 30 minutes at
four locations during the study: Plymouth Bay; the mouth of the Plymouth
Estuary; Kingston Bay (western portion of Plymouth Estuary); and Duxbury
Bay (northern portion of Plymouth Estuary).

O

2008

Figure 6

The relationship between water temperature and the emigration of tagged
winter flounder (Pseudopleuronectes americanus ) from the Plymouth Estu-
ary in 2008. Winter flounder emigrated rapidly from the Plymouth Estuary
as water temperatures increased from 10° to 15°C at the beginning of the
summer.

researchers (W. Hoffman, personal
commun.4), documenting more sub-
stantial movements beyond the
study area. One tagged winter floun-
der (tag 5837) moved from the Gulf
of Maine stock area to the SNE-MA
stock area and was detected east of
Cape Cod on 26 August 2008 (Table
1). This individual was tagged in
Plymouth Bay on 30 November 2007
and was never detected in our re-
ceiver array. Tag 53877 was detected
throughout our array in 2009 and
was later detected in Massachusetts
Bay on 26 August 2009 (Table 1).

Receiver efficiency

Despite the loss of some receivers, it
appears that the array was efficient
for the detection of the migrations
of winter flounder. Twenty eight
winter flounder released during the
first year of the study were later
detected in the estuary. Each fish
was detected in the estuary an aver-
age of 416 times (range = l-3227
detections) at an average rate of 1.9
detections/day at liberty. Seventeen
of the 24 winter flounder released in
Plymouth Bay were never detected
inside the estuary. These 24 winter
flounder were released outside the
receiver array that was used in the
first year (Fig. 1); therefore, if these
fish remained in coastal waters they
would not have been detected by our
array. Twenty two of the 25 winter
flounder released in the second year
of the study were later detected in
our array. On average, each tagged
winter flounder was detected 2861
times (range 57-23,842 detections)
at an average rate of 14.1 detec-
tions/day at liberty. Winter flounder
tagged on 8 May 2009, were released
slightly eastward of the receiver
array (Fig. 1), and this location may
explain why two of these tagged fish
were never detected again.

In the fall of 2008, receivers I and M were lost from
the inner gate of receivers that spanned the mouth of
the estuary. After these receivers were lost, two tagged
winter flounder (tags 5833 and 5873) were detected in-
side the estuary at the end of September and October,
respectively, without being detected at the inner gate of
receivers. One flounder (tag 5855) was released inside

4 Hoffman, William. 2009. Massachusetts Division of Marine
Fisheries, Gloucester, MA 01930.

the estuary on 24 May 2008, and was detected two days
later at receiver D. However, this individual was never
detected at another receiver during the study. The fate
of this fish is unknown. It may have been captured in
the recreational fishery, eaten by another animal, or
died after having been tagged. This was the only win-
ter flounder that was released and detected inside the
estuary (tag 5855) that was never detected at the inner
gate. In the second year of the study, only one tagged
winter flounder (tag 53894) that was detected inside

416

Fishery Bulletin 108(4)

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of the estuary without first being
detected at the inner gate. However,
this individual was later detected
at the inner gate when it emigrated
from the estuary in May.

A quantitative assessment of the
efficiency of the outer gate receivers
in Plymouth Bay is more difficult.
It is unlikely that winter flounder
were able to pass between adjacent
receivers without being detected,
because tagged winter flounder were
commonly detected simultaneously
at two or three adjacent receivers
in Plymouth Bay, indicating that
these receivers had overlapping
detection radii. Unfortunately, the
receivers that were lost (P and Y)
were each at the edges of the outer
gate. Therefore, it is difficult to as-
sess how many fish may have moved
from Plymouth Bay to Cape Cod
Bay without being detected.

Discussion

Using acoustic telemetry, we were
able observe the movements of adult
winter flounder in the southern Gulf
of Maine with high spatial and tem-
poral resolution. In particular, we
were able to investigate the spawn-
ing behavior of tagged winter floun-
der in the vicinity of Plymouth Bay
and assess the seasonal distribution
of tagged flounder in the region. This
approach yielded valuable insight
into the life history of this species.

Spawning behavior of
winter flounder

Our observations support the hypoth-
esis that winter flounder spawning
in the Gulf of Maine is not restricted
to estuaries. Two sympatric con-
tingents of winter flounder were
observed, both of which exhibited
divergent spawning migrations. The
majority of adults tagged in coastal
waters (76%) were absent from the
estuary during the peak spawning
months of March through May. In
addition, eight of the eleven tagged
winter flounder that were observed
to be gravid did not enter the estuary
during the spawning period.

Evidence of coastal spawning by
winter flounder in Plymouth Bay

DeCelles and Cadrin: Movement patterns of Pseudopleuronectes americanus in the southern Gulf of Maine

417

was also found in previous studies. Ichthyoplankton
sampling has been conducted in this region for decades
to assess the impacts of the Pilgrim Nuclear Power
Station (PNPS), which is on the southeast shore of
Plymouth Bay. Researchers at Marine Research, Inc.5
used a physical model to estimate the time it would
take for eggs spawned in the Plymouth estuary to drift
to Plymouth Bay near the power plant. They collected
and aged eggs at PNPS and found that a proportion
of the eggs had been spawned too recently to have
originated from the estuary. They concluded that these
eggs had been spawned in Plymouth Bay, rather than
the estuary.

Evidence for coastal spawning has also been not-
ed in other regions of the Gulf of Maine. Howe and
Coates (1975) suggested that coastal spawning groups
may exist on the basis of their observations of tagged
flounder captured in coastal and offshore waters dur-
ing the spawning season. Data collected during the
NOAA Northeast Fisheries Science Center annual
spring trawl survey have shown that the mean depth
occupied by winter flounder in the Gulf of Maine has
increased significantly over the last 40 years (Nye et
al., 2009). This increase in depth may reflect a broad
shift from estuarine to coastal spawning in the Gulf
of Maine stock.

Winter flounder do not require estuaries as spawning
habitat. This is evidenced by the large, self-sustaining
stock of winter flounder that is present on Georges
Bank (NMFS, 1999). Rather, estuarine spawning ap-
pears to be a strategy to maintain localized population
structure. Tagging studies have shown that winter
flounder display homing to their spawning grounds
(Perlmutter, 1947; Saila, 1961). Dispersal is limited or
nonexistent during the egg stage. In addition, larval
behavior and estuarine hydrographic features promote
the retention of larvae within estuarine spawning areas
(Pearcy, 1962; Crawford and Carey, 1985; Chant et al.,
2000). These characteristics, which promote local popu-
lation structure, also make winter flounder vulnerable
to human impacts.

Anthropogenic impacts such as dredging, pollution,
eutrophication, and elevated temperatures often occur
in estuaries (Nelson et al., 1991), and these activities
can reduce the survival of winter flounder eggs, larvae,
and juveniles. Estuaries are relatively small in size and
are more susceptible to changes in water temperature
than are coastal waters (Abood and Metzger, 1996).
Elevated temperatures have been shown to reduce the
survival and fitness of winter flounder eggs (Keller and
Klein-MacPhee, 2000) and winter flounder has been
identified as a species that is particularly vulnerable
to global warming (Rose, 2005). A closed population

5 Marine Research, Inc. 1986. Winter flounder early life
history studies related to the operation of Pilgrim Station — A
review 1975-1984. Pilgrim Nuclear Power Station Envi-
ronmental Monitoring Program - Report Series No. 2, 111
p. Boston Edison Company, Boston, MA.

of winter flounder that relies solely on an estuary as a
spawning and nursery ground will likely exhibit poor
recruitment, if that estuary has been degraded by hu-
man activities. Homing to spawning grounds by adults
may be unfavorable when conditions do not inhibit the
act of spawning but do diminish the survival of eggs
and larvae (Harden Jones, 1968). Harden Jones (1968)
also concluded that strict natal homing was not a sus-
tainable life history strategy and that diverse migration
behaviors are needed for a population to persist in a
changing environment.

Divergent migrations impart resilience to populations
against spatial variability in mortality (Secor, 1999).
Passive telemetry revealed that winter flounder in the
southern Gulf of Maine exhibit spatial heterogeneity in
their use of spawning habitat and that coastal spawn-
ing was prevalent. Compared to estuarine spawning,
coastal spawning likely leads to a greater dispersal of
larvae. Therefore, a single coastal spawning contingent
may provide a larval source for one or more estuarine
nursery grounds. Coastal spawning contingents may
confer resilience in a regional population during periods
when estuarine productivity is low.

Our results indicate that coastal waters may provide
essential spawning habitats for winter flounder in the
Gulf of Maine. However, future research is needed to
identify the prevalence of coastal spawning in other
regions of the Gulf of Maine. Acoustic telemetry is a
promising tool for conducting this research. For exam-
ple, receiver gates could be placed across the mouths
of estuaries along the coast, in a design similar to
the one proposed by Grotheus and Able (2007). Ich-
thyoplankton studies could also be used to compare
the densities of winter flounder eggs in estuarine and
coastal waters. High-resolution trawl surveys could
be used to sample the reproductive condition of win-
ter flounder throughout the Gulf of Maine. Finally,
coupled biophysical models would allow an examina-
tion of the dispersal of coastal spawned larvae in the
Gulf of Maine.

Seasonal distribution of winter flounder

Bigelow and Schroeder (1953) and McCracken (1963)
observed that flounder north of Cape Cod are more
abundant in deeper, coastal waters during the winter
months. Our observations in one region of the Gulf of
Maine support this claim because only 10% of tagged
of winter flounder at large during the winter months
were detected within the shallow waters of the Plym-
outh estuary. Contrary to our observations, Howe and
Coates (1975) claimed that flounder in the Gulf of
Maine moved farther inshore into estuaries during the
winter months. However, their analysis may have been
hampered by a lack of tag returns during the fall and
winter months.

Winter flounder in Newfoundland are thought to move
to deeper coastal waters during the winter to avoid ice
formation and extreme turbulence during storm events
(Van Guelpen and Davis, 1979). Winter flounder may

418

Fishery Bulletin 108(4)

also migrate to deeper waters during the winter to
prevent their blood serum from freezing, which occurs
between -1.25 and -1.38°C (Fletcher, 1977). Tempera-
tures in the Plymouth estuary dropped to as low as
-1.55°C during the winter of 2008, whereas the mini-
mum recorded temperature in Plymouth Bay was 1.2°C.
Therefore, the deeper waters of Plymouth Bay may act
as a refuge from the extreme cold temperatures and
ice formation that are present in the Plymouth estuary
during the winter.

Tagged winter flounder were most commonly present
in the estuary during the late spring, when water tem-
peratures ranged from 9° to 16°C, which is within the
preferred temperature range (12-15°C) of this species
(McCracken, 1963; Reynolds, 1977). Although winter
flounder were common in the estuary during the late
spring, the majority of the tagged winter flounder
remained in coastal waters during this period. Howe
and Coates (1975) also reported that winter flounder
are concentrated in shoal areas during the spring
months. Although we were unable to capture adult
winter flounder in the estuary from March through
early May 2008, we cannot conclude that winter floun-
der were not present in the estuary during this time.
Winter flounder in spawning condition often cease
feeding or reduce their food intake (NMFS, 1999) and
therefore it is less likely that we would have captured
flounder using hook-and-line gear during the spawn-
ing season. In addition, flounder that were buried in
the sediment may not have been available to the small
trawl net that we were using to capture flounder in
the estuary.

The emigration of winter flounder from the estu-
ary coincided with rising temperatures at the onset
of summer. Between 30 May and 19 June 2008 the
majority of tagged winter flounder emigrated from
the estuary as water temperature increased from 10°
to 15°C (Fig. 6). These observations were consistent
with previous reports that revealed that winter floun-
der will migrate to cooler waters when temperatures
exceed 15°C (Bigelow and Schroeder, 1953; McCracken,
1963). Perlmutter (1947) found that the movements of
winter flounder north of Cape Cod are typically local-
ized, and Howe and Coates (1975) calculated that the
average displacement of winter flounder tagged in
Plymouth Bay was only 3 km. They also found that in
the Gulf of Maine, winter flounder could find suitable
temperatures (between 12° and 17°C) within 2 km
of the shore zone during the summer. Weekly aver-
aged temperatures in Plymouth Bay only exceeded
15°C twice in 2008, and did not exceed 15°C in 2009.
Therefore, winter flounder leaving the Plymouth estu-
ary were not forced to migrate long distances to reach
suitable temperatures.

During the autumn months of 2008 five tagged indi-
viduals returned to the estuary as water temperatures
decreased below their seasonal maxima. Bigelow and
Schroeder (1953) also noted that winter flounder will
return to the Plymouth estuary during the autumn
months when temperatures start to cool.

Conclusions

By collecting large amounts of high-resolution data, we
are able to offer insight into the fine-scale behavior and
distribution of winter flounder in the southern Gulf of
Maine. Our results indicate that winter flounder exhibit
divergent spawning behaviors which support inferences
of contingent structure and that coastal waters may
provide essential spawning grounds for this species. As
such, coastal waters should merit consideration in the
assignment of Essential Fish Habitat for this species in
the Gulf of Maine. In this region of the Gulf of Maine,
estuarine residence appears to be brief, and dependent
upon water temperature.

Acknowledgments

The Massachusetts Marine Fisheries Institute provided
the funding for this research. T. Grothues and two
anonymous reviewers provided valuable comments on
this manuscript. We would also like to thank M. Mather,
G. Skomal, and G. Cowles for their guidance and advice
during this experiment. We thank J. Manderson and M.
Armstrong for allowing us to borrow acoustic receivers.
We would also like to thank V. Malkoski, V. Manfredi,
P. Milligan, B. Courchene, H. Bourbon, C. Sarro, and
M. Marino for assistance in the field. Finally, we would
like to thank the dozens of other people whose help at
sea made this project possible.

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420

Abstract — Demographic parameters
from seven exploited coral reef lutja-
nid species were compared as a case
study of the implications of intra-
family variation in life histories for
multispecies harvest management.
Modal lengths varied by 4 cm among
four species {Lutjanus fulviflamma, L.
vitta, L. carponotatus, L. adetii), which
were at least 6 cm smaller than the
modal lengths of the largest species
(L. gibbus, Sympliorus nematophorus,
Aprion virescens ). Modal ages, indicat-
ing ages of full selection to fishing
gear, were 10 years or less for all spe-
cies, but maximum ages ranged from
12 (L. gibbus) to 36 years (S. nema-
tophorus). Each species had a unique
growth pattern, with differences in
length-at-age and mean asymptotic
fork length (L„), but smaller species
generally grew fast during the first
1-2 years of life and larger species
grew more slowly over a longer period.
Total mortality rates varied among
species; L. gibbus had the highest
mortality and L. fulviflamma , the
lowest mortality. The variability in
life history strategies of these tropical
lutjanids makes generalizations about
lutjanid life histories difficult, but the
fact that all seven had characteristics
that would make them particularly
vulnerable to fishing indicates that
harvest of tropical lutjanids should
be managed with caution.

Manuscript submitted 5 November 2009.
Manuscript accepted 7 July 2010.

Fish. Bull. 108:420-432 (2010).

The views and opinions expressed
or implied in this article are those
of the author (or authors) and do not
necessarily reflect the position
of the National Marine Fisheries
Service, NOAA.

Demographic characteristics of exploited
tropical lutjanids: a comparative analysis

Michelle R. Heupel (contact author)'
Ashley J. Williams2 3
David J. Welch2'4
Campbell R. Davies5

Ann Penny2
Jacob P Kritzer6
Ross J. Marriott7
Bruce D. Mapstone5

Email address for contact author: michelle.heupel@jcu.edu.au

1 School of Earth and Environmental Sciences
James Cook University

Townsville, Queensland, 4811, Australia

2 Fishing and Fisheries Research Centre
School of Earth and Environmental Sciences
James Cook University

Townsville, Queensland, 4811, Australia

3 Oceanic Fisheries Program
Secretariat of the Pacific Community
BP 5, 98848 Noumea, New Caledonia

4 Queensland Primary Industries and Fisheries
PO Box 1085

Oonoonba, Queensland 4811, Australia

5 CSIRO Marine and Atmospheric Research
GPO Box 1538

Hobart, Tasmania, 7001, Australia

6 Environmental Defense Fund
18 Tremont Street, Suite 850
Boston, Massachusetts 02108

7 Department of Fisheries WA
Western Australian Fisheries and

Marine Research Laboratories
PO Box 20

North Beach, Western Australia 6920
Australia

Knowledge of the life history charac-
teristics of an exploited species can
help elucidate inherent resilience to
anthropogenic effects such as fishing
(Parent and Schriml, 1995; Jennings
et ah, 1998; Musick et al., 2000).
Interspecific variation in life history
characteristics may indicate that
some species are more susceptible to
overfishing than others. Life history
characteristics vary widely among
families of coral reef fish (Sale, 1991;
Gust et al., 2002) — a feature particu-
larly evident within the Lutjanidae.
Some lutjanid species grow to sizes
in excess of 1 m (e.g., cubera snapper
[. Lutjanus cya?iopterus], red snapper
[. L . sebae ]) and others reach smaller
maximum sizes of less than 30 cm
(e.g., two-spot banded snapper [L.
biguttatus], bluestriped snapper [L.
notatus]). Variable life spans and
spatial distributions also have been
recorded within the family. Lutja-
nids are typically gonochoristic (i.e. ,
do not change sex) and often exhibit
sex specific variation in life history
traits (Polovina and Ralston, 1987).
A high degree of variation in life his-
tory strategies among reef fish spe-
cies within a family would suggest

it is inappropriate to apply the same
management strategy to all those
species. Here we consider the lutja-
nids as a case study.

The Lutjanidae comprises approxi-
mately 103 species with a wide ar-
ray of size and body form, making it
one of the largest and most diverse
families of fish (Carpenter and Niem,
2001). Lutjanids are found in tropi-
cal waters around the globe and are
often associated with reef habitats
(Carpenter and Niem, 2001). Lutja-
nids are of high commercial value
throughout the world and are taken
regularly in artisanal, recreational,
and commercial fisheries (Newman et
ah, 1996; Kaunda-Arara and Ntiba,
1997; Marriott et al., 2007; Amezcua
et al., 2006). The propensity of lut-
janids to aggregate, particularly for
spawning, and their predictably reef-
associated distribution, make them
potentially susceptible to overfishing.
Concerns have been raised about the
level of harvest and sustainability
of fishing for lutjanid populations in
some regions (Kamukuru et al., 2005;
Amezcua et al., 2006).

Little is known about the specific
spatial distribution and demograph-

Heupel et al.: Demographic characteristics of exploited tropical lutjamds

421

Figure 1

Map of the Great Barrier Reef region off the east coast of Australia
showing the four sampling regions where lutjanids were collected for
use in this study.

ic characteristics of many lutjanid species
(but see Newman et al., 1996, 2000a; Kaun-
da-Arara and Ntiba, 1997; Kritzer, 2002,

2004; Amezcua et al., 2006; Marriott et al.,

2007). Many species remain unstudied and
comparisons among species are few, even
though research has covered much of the
family’s geographic range, including Mexico
(Arreguin-Sanchez and Manickchand-Heile-
man, 1998; Amezcua et al., 2006), Kenya
(Kaunda-Arara and Ntiba, 1997), the United
States (Wilson and Nieland, 2001; Meyer et
al., 2007), Japan (Shimose and Tachihara,

2005), the Great Barrier Reef (Newman et
al., 1996, 2000a; Marriott et al., 2007), Ara-
bian Gulf (Grandcourt et al., 2006), and the
Indian Ocean (Newman and Dunk, 2003;

Pilling et al., 2000). The few data that do
exist indicate that at least some lutjanid
species are long lived with life spans over
30 years (Newman et al., 1996; Wilson and
Nieland, 2001; Newman and Dunk, 2003;

Marriott et al., 2007).

In this study we compared the demo-
graphic characteristics of seven lutjanid
species on mid and outer shelf reefs of the
Great Barrier Reef (GBR), Australia, as
a case study of the implications for intra-
family demographic diversity for managing
multispecies fisheries. The species exam-
ined included the following: chinamanfish
[Symphoj'us nematophorus ]; green jobfish
[Aprion virescens\\ dory snapper [Lutjanus
fulviflamma] \ yellow-banded snapper [L. adetii]\ hump-
back red snapper [L. gibbus]; brownstripe red snapper
[L. vitta\; and Spanish flag snapper [L. carponotatus] .
These species are among the most common lutjanids
caught on the GBR after the highly valued red snap-
pers (L. erythropterus, L. malabaricus, L. sebae) (New-
man et al., 2000b).

Demographic characteristics examined for each
species included size, age, growth, mortality, and
sex-specific patterns. Demographic parameters were
compared to quantify differences in life history strat-
egies among species and to infer the likely resilience
of each species to fishing impacts. This information
was used to assess whether common management
measures would be appropriate across species within
the lutjanid family. Such descriptive field studies also
can be useful for providing the data sets to be used
in meta-analyses for further developing our collective
understanding of life history theory (e.g., Roff, 1984;
Molloy et al., 2007). In this study we describe differ-
ent aspects of biology across these closely related spe-
cies. Samples from the same shallow coral reef habi-
tats allowed us to control for taxonomic, geographic,
and environmental effects to provide insight into the
similarities or differences in life history strategies
and thus theoretical trade-offs in evolved traits for
moderate-size gonochoristic teleosts.

Materials and methods

Sample collection

Individuals of the seven lutjanids considered here were
collected during the effects of line fishing (ELF) experi-
ment1 (Campbell et al., 2001) between 1995 and 2005
from four regions of the GBR spanning 7° of latitude:
Lizard Island, 14°S; Townsville, 18°S; Mackay, 20°S; and
Storm Cay, 21°S (Fig. 1). All fishing was done by hand-
line with the same gear as that used in the operational
commercial fishery, but survey effort was stratified to
ensure roughly equal distribution around each reef and
over two depth strata (above 12 m and below 15 m). Oto-
liths (sagittae) and gonads of fish were either dissected
on the day of capture and processed as described below
or fish heads were removed from filleted fish carcasses in
the field, frozen, and otoliths were dissected upon return
to the laboratory. Otoliths of five of the seven species
were examined for age analysis (A. virescens, S. nema-

1 Mapstone, B.D., C. R. Davies, L. R. Little, A. E. Punt, A. D.
M. Smith, F. Pantus, D. C. Lou, A. J. Williams, A. Jones, A.
M. Ayling, G. R. Russ, and A. D. McDonald. 2004. The
effects of line fishing on the Great Barrier Reef and evalu-
ations of alternative potential management strategies. CRC
Reef Research Centre Technical Report no 52, 205 p. CRC
Reef Research Centre, Townsville, Australia.

422

Fishery Bulletin 108(4)

tophorus, L. carponotatus, L. gibbus, L. fulviflamma) .
Sufficient specimens were collected for comparisons
among regions for only one species (L. carponotatus)
and specimens for all other species were pooled across
regions and years for analyses.

Fish processing

All fish were measured to the nearest millimeter fork
length (FL) and weighed to the nearest gram before
dissection. Otoliths were dissected from a subsample of
specimens, cleaned, and stored dry in paper envelopes.
Otoliths were embedded in epoxy resin and cut trans-
versely through the primordium with a diamond-tipped
blade on a low-speed saw to produce a thin section of
300-400 pm. Sections were mounted on glass slides
by using Crystalbond adhesive (Aremco Products Inc.,
New York). Otoliths were read under reflected light at
40 x magnification and opaque growth increments were
counted from the primordium to the proximal (in situ)
margin along the ventral ridge of the sulcus acousticus.
Sectioned otoliths were read by one or more individuals.
Where more than one reader was used, otoliths were
read at least once by each of two independent read-
ers and the age was accepted if these first two counts
agreed. A third count was made by one of the two read-
ers if the first two counts did not agree and a match
between this third count and either of the previous two
was accepted as the age of the fish or, if the third count
did not match either of the first two counts, the median
count was assigned as a final age estimate. The remain-
ing otoliths were read by a single, experienced reader
who counted each otolith at least twice with a minimum
of 24 hours between consecutive counts. If the first two
counts did not agree, a third count was completed to
assign a final age through count agreement or to assign
a median age, as described above.

Opaque increments were assumed to be annuli for the
five species examined. Supportive evidence for annual
periodicity in opaque increment deposition in otoliths
has been demonstrated for the majority of tropical reef
fish (Fowler, 1995; Choat and Robertson, 2002), lutja-
nids (e.g., Cappo et al., 2000), and for most of the study
species: L. vitta (Davis and West, 1992; Newman et al.,
2000a), L. carponotatus (Newman et al., 2000a; Kritzer,
2002), L. adetii (Newman et al., 1996), L. fulviflamma
(Grandcourt et al., 2006), and A. virescens (Pilling et
al., 2000). Age estimates derived from the otoliths for
L. gibbus and S. nematophorus have not been validated
hitherto, but we assumed that increment deposition also
occurs on an annual basis for these species, as has been
demonstrated for the majority of other tropical lutjanids.
A violation of this assumption is likely to result in bi-
ases in the parameter estimates we present, such as for
the von Bertalanffy parameter K and the instantaneous
total mortality coefficient, Z. The magnitude of bias
would likely inflate estimates for older-age species, and
these estimates would vary among parameters, with a
likely smaller influence on estimates of L x (mean as-
ymptotic fork length) (Choat et al., 2009). Gonads were

examined to define the sex and maturity of individuals,
but low sample sizes prevented meaningful analysis of
detailed histological staging or gonadosomatic index
analyses. Gonads were dissected and either frozen or
preserved in FAACC (formaldehyde 4%, acetic acid 5%,
calcium chloride 1.3%) or 10% buffered formalin imme-
diately after removal. Tissues were preserved in FAACC
before May 1999 and 10% buffered formalin thereafter.
The sex and maturity of L. carponotatus was estab-
lished by macroscopic methods (Kritzer, 2004). The sex
and maturity for a subset of individuals of other species
were further assessed by histological analysis. Trans-
verse histological sections were taken from the medial
region of all gonads after the procedures outlined by
Adams (2003). Female maturity was determined by
the presence of vitellogenic oocytes, and the presence of
brown bodies, atretic oocytes, vascularization, and the
relative thickness of the gonad wall, all of which may
indicate prior spawning (Sadovy and Shapiro, 1987;
Ferreira, 1995; Adams, 2003). Male maturity was deter-
mined by the presence of sperm in the sperm sinuses.

Estimation of demographic parameters

Length- and age-frequency distributions were constructed
from pooled samples and compared among species quali-
tatively. Differences in length and age frequencies by sex
were assessed by using two-sample Kolmogorov- Smirnov
tests where the largest of absolute discrepancies between
relative cumulative frequency distributions (c?max) was
compared with an approximate two-tailed critical value
(D\ Sokal and Rohlf, 1995). Growth was modeled with
the von Bertalanffy growth function (VBGF) fitted by
using a nonlinear least-squares regression of FL on age.
The form of the VBGF was

where Lt =
L„ =
K =

*0 =

the length at age t\

the mean asymptotic fork length;

the growth coefficient or rate at which

is approached; and

theoretical age at zero length.

The VBGF model was fitted to Lt on t data groups where
t0 was either constrained to zero (t0=0) or unconstrained
(estimated). This was done to examine the effects of
the absence of smaller individuals in the sample and
(for t0 = 0) to allow biologically sensible comparisons of
growth among species if lengths at age of younger fish
(not sampled) extrapolated by the model were biologically
unrealistic. VBGFs for L. carponotatus for all regions
were compared by likelihood ratio tests.

Analysis of covariance (ANCOVA) was used to com-
pare log-transformed length data from individuals
across a common age range (5-12 years) among the
five species with age as a covariate. A Tukey’s post hoc
test (P=0.05) was used to test for differences among
species when a significant difference among the groups
was detected by the ANCOVA.

Heupel et at: Demographic characteristics of exploited tropical lutjanids

423

Age-based catch curves (Rick-
er, 1975) were used to estimate
the instantaneous rate of total
mortality ( Z ) for each species.
The natural log-transformed
number of fish in each age class
was regressed against the cor-
responding age on the descend-
ing slope of the age-frequency
distribution to provide an es-
timate of total mortality, Z.
Regressions were fitted from
the first modal age class, pre-
sumed to be the first age class
fully selected by the sampling
gear, through the oldest age
class that was preceded by
no more than two consecutive
zero frequencies. An ANCOVA
was used to determine whether
there were differences in mor-
tality among regions for L. car-
ponotatus. Z also was estimated
by using the Hoenig (1983) esti-
mator for fish populations from
logeZ= 1.46-1.01 log etmax, where
tmax was the maximum observed
age in years.

Sex ratios and size- and age-
frequency distributions were ex-
amined to describe sex-specific
aspects of population structure.
Departure from a 1:1 sex ratio
was tested with a chi-squared
test by using Yates’s correction
for continuity (Zar, 1999).

Results

A total of 7307 individuals of
the seven lutjanid species were
sampled, of which L. carponota-
tus was the most abundant. The
modal length in the sampled
distributions differed among
species (Fig. 2) and was larg-
est for S. nematophorus (400-
449 mm FL) and A. virescens
(450-499 and 600-649 mm FL)

Figure 2

Length-frequency distributions for seven lutjanid species on the Great Barrier
Reef between 1995 and 2005 (note difference in y axes).

and smallest for L. fulviflamma

(260—279 mm FL). Symphorus nematophorus and A.
virescens had the largest maximum fork lengths of 885
mm and 810 mm FL, respectively. Of the seven species,
the sampled length ranges of L. carponotatus, L. ful-
viflamma, and L. adetii were most similar, with 72%,
89%, and 81% coming from the size range of 200-300
mm FL, respectively.

Age-frequency distributions varied considerably among
the five species for which age was estimated. The modal

age in the catch was 2 years for A. virescens, 3 years
for S. nematophorus, 7 years for L. carponotatus, 8 years
for L. gibbus, and 10 years for L. fulviflamma (Fig. 3).
The catch of the two largest species (S. nematophorus
and A. virescens ) consisted predominately of younger
age classes (<6 yr), whereas the catch of smaller species
(L. carponotatus, L. gibbus, L. fulviflamma ) included a
higher proportion of fish sampled from older age classes
(>8 yr; Fig. 3). The maximum age in the catch also

424

Fishery Bulletin 108(4)

differed among species (Fig. 3) and the oldest fish was
a 36-year-old S. nematophorus.

Regional and sex-specific differences in length- and
age-frequency distributions could only be analyzed for
L. carponotatus because of low sample sizes for all
other species. There was a significant effect of sex on
lengths (Kolmogorov-Smirnov test: n1=1279, n2= 399,
dmax=0-336, D = 0.078, P<0.05) and ages (n1 = 1279,
n2- 399, c?max=0.281, .0=0.078, P<0.05) for the frequency
distributions and a greater proportion of males than fe-
males in the larger size classes and younger age classes
(Fig. 4). Differences in growth by sex were significantly
different (^2 = 68.34, PcO.OOOl), with males reaching
a significantly greater maximum size than females

(female: L^- 278, ,K=0.43, t0=-2.55; male: 0^=293,
K= 0.55, f0=-1.43).

The unconstrained fits of the VBGF differed substan-
tially among species with L. carponotatus, A. virescens,
and L. fulviflamma reaching a maximum size relatively
early in life (Fig. 5). Symphorus nematophorus reached
a maximum size somewhat later in life, and the growth
curve for L. gibbus was not asymptotic. The lack of
juvenile fish collected for all species, but particularly
for L. carponotatus, L. fulviflamma, and L. gibbus, re-
sulted in relatively flat fits of the unconstrained VBGF.
The nonasymptotic growth pattern for L. gibbus indi-
cates that under-sampling of larger individuals may
also have occurred. VBGF parameter estimates for all
species from the unconstrained
fit are likely to be biased and
should be interpreted with some
caution.

Constraining the VBGF by
setting t0=0 produced similar
estimates of K and Lx to those
for the unconstrained estimates
for L. carponotatus and L. ful-
viflamma. Despite limited sam-
pling of the youngest individu-
als, this similarity indicates
that a sufficiently wide range
of age classes were sampled in
these populations to produce bi-
ologically reasonable estimates
of growth without the need to
constrain tQ. Constraining t0 re-
sulted in faster initial growth
estimates (greater estimate
of K) and smaller asymptotic
length (LJ than the uncon-
strained fits for S. nematopho-
rus, A. virescens, and L. gibbus.
The constrained fit produced a
more asymptotic growth curve
for L. gibbus, indicating that
constraining t0 may have pro-
vided a more biologically realis-
tic estimate of length-at-age for
this species.

Both constrained and uncon-
strained growth curves differed
across species. These species
showed distinct differences in
the rate of growth at young
ages and the age at which
they reached average maxi-
mum length: smaller species
grew fast in the first couple of
years and reached asymptotic
length early, whereas larger
species grew slightly slower in
the first few years to reach an
asymptotic FL later. The lack of
small-size individuals resulted

S. nematophorus
o= 168

i£U

ri n~HT-n

,[_ixi

□ , n n n

■(NICMCMCNCNIfOfOfOCO

ill

L gibbus
a=166

10

L fulviflamma
o=55

IQ

Age

Figure 3

Age-frequency distributions for five lutjanid species on the Great Barrier Reef
between 1995 and 2005 (note difference in y axes).

Heupel et al. : Demographic characteristics of exploited tropical lut|anids

425

in a lack of definition of early growth in the un-
constrained curves when compared to constrained
estimates. Both constrained and unconstrained
growth curves for L. carponotatus and L. fulvi-
flamma were relatively “square-shaped” (Choat and
Robertson, 2002), revealing little growth over most
of their life spans. Several species had K values
>0.30/yr, indicating rapid growth to maximum size
at a young age.

Comparison of growth rate among 5-12 year
olds revealed significant differences among species
(F4 2503=1543.8, PcO.OOOl). Post hoc tests indicated
that each species had a unique growth rate. Exami-
nation of age at 50% Lx indicated some differences
between constrained and unconstrained fits (Table
1), but in all cases, 50% of asymptotic length was
reached at relatively young ages compared with
estimated longevity, and only L. gibbus took longer
than 10% of expected longevity to reach 50% of
asymptotic size (Table 1).

Lutjanus carponotatus was the only species with
a sample size sufficient for regional analysis of
growth data. Likelihood ratio tests indicated that
patterns of growth differed significantly between
Lizard Island, Mackay, and Storm Cay regions
(^2 = 68.34, P<0.001) but there were similar Lx
values among regions, and quite variable K val-
ues (Table 1). The most notable difference was the
greater (and lower K) in the Storm Cay region
(Table 1).

Total mortality (Z) estimates calculated from
catch curves varied significantly among the five
species examined (F441=5.61, P=0.001) (Fig. 6).

Z was highest for L. gibbus and A. virescens and
lowest for L. fulviflamma (Table 2). Mortality rates
calculated by the Hoenig method resulted in more
homogeneous estimates, of which highest rates were
for L. gibbus and lowest for S. nematophorus. Mor-
tality estimates calculated from catch curves were
higher than those estimated by Hoenig’s method for
all species except L. fulviflamma (Table 2). Z for L.
carponotatus did not vary significantly among the three
regions (P2 29 = 2.24, P=0.15) and therefore a single catch
curve was fitted to data pooled across regions.

All except one of the individuals sampled (282-mm
L. gibbus ) were sexually mature, making analysis of
size and age at maturity impossible. Adult sex ratios
in a few of the sampled populations differed from a 1:1
sex ratio (Table 3), despite the expected gonochoristic
nature of these species. Sex ratios of L. carponotatus,
L. gibbus, and L. vitta were biased significantly toward
males.

Discussion

Many coral reef fish species have overlapping spatial
distributions, are found in similar habitats, and grow to
roughly similar sizes. It might be expected that superfi-
cially similar species from the same family would have

similar demographic characteristics and life history
strategies. The results of this case study of lutjanid
species, however, indicate that it is impossible to make
generalizations about the life histories of members of a
family, even where they grow to similar sizes and coexist
in the same habitats. Even this small subset of seven
lutjanid species had quite different growth, mortality,
and longevity characteristics. Our results support pre-
vious findings for individual species but also provide
evidence of the considerable differences among species
in this family and highlight the need for careful, and
potentially species-specific, approaches to managing the
harvest of lutjanid assemblages.

Demographic characteristics of the lutjanid species
described here must be considered in the context of
the limitations of size selectivity of the fishing gear
used to sample populations. No individuals below 200
mm FL were collected for any species, meaning the
youngest age classes were not fully selected, resulting

426

Fishery Bulletin 108(4)

in an absence of immature individuals for all, but one
species. However, some individuals of most species were
sampled in their first or second year indicating that
these species mature at a very early age. The fact that
full recruitment to the gear occurred at age 2 for S.
nematophorus and at age 3 for A. virescens, the larg-
est species sampled, illustrated the rapid early growth
characteristic of many lutjanid species (Newman et al.,
1996, 2000a; Kritzer, 2004; Grandcourt et al., 2006).
It is important to note that the same sampling gear

was used in this project as that most commonly used
by commercial and recreational fisheries on the GBR
and therefore the biological characteristics described
here should reflect those characteristics of individuals
of these species harvested by the fishery. Importantly,
the sampled age distributions revealed the age range
of these populations susceptible to fishing gear. It is
also likely that many fish were not sampled because
sampling was constrained to depths shallower than 30
m and to daylight hours, which are the most common

Heupel et al.: Demographic characteristics of exploited tropical lutjanids

427

Table 1

Parameter estimates for the von Bertalanffy growth function parameters age at 50% (mean asymptotic fork length) and per-

cent longevity at 50% Lx for five lutjanid species from the Great Barrier Reef. K is the von Bertalanffy growth coefficient, and
t0 is the theoretical age at length zero. “U” indicates an unconstrained estimate, “C” indicates an estimate constrained by t0= 0.
Region-specific growth curves for L. carponotatus were not constrained.

Species

L ^ (mm)

K (/yr)

t0{ yr)

Age (yr)
at 50%

% longevity
at 50%

S. nematophorus — U

820

0.12

-2.83

3

8.33

S. nematophorus — C

732

0.26

0

3

8.33

A. virescens — U

683

0.35

-1.53

0.5

3.13

A. virescens — C

623

0.85

0

1

6.25

L. gibbus — U

544

0.06

-9.48

2

16.67

L. gibbus — C

352

0.51

0

3

25.0

L. fulviflamma — U

265

0.61

1.66

1

5.88

L. fulviflamma — C

267

0.41

0

1

5.88

L. carponotatus — U

295

0.37

-2.58

0

0

L. carponotatus — C

291

0.66

0

1

4.35

L. carponotatus — Lizard Is

293

0.67

-0.17

—

—

L. carponotatus — Mackay

292

0.47

-1.68

—

—

L. carponotatus — Storm Cay

302

0.16

-9.35

- —

—

Estimates of mortality for five lutjanid species using catch
used in mortality estimation are indicated.

Table 2

curve and Hoenig (1983) estimators. Maximum

age and age range

Species

Maximum age (yr)

Age range
(yr)

Catch curve Z
(/yr) [SE]

Hoenig Z
(/yr)

S. nematophorus

36

3-17

0.20 [0.05]

0.11

A. virescens

16

2-9

0.56 [0.07]

0.26

L. gibbus

12

8-12

0.63 [0.08]

0.35

L. carponotatus

23

7-23

0.30 [0.02]

0.18

L. fulviflamma

17

10-17

0.14 [0.06]

0.25

depth and time fished by commercial and recreational
fishing crews. A small number of fishing crews fish dur-
ing the night in deeper water (> 50 m) where a greater
proportion of larger lutjanids are caught (Marriott,
personal commun.).

Limited sample sizes prevented the statistical analy-
ses of sex- and region-specific variation in life history
characteristics except for L. carponotatus. As with pre-
vious findings, L. carponotatus displayed sex-specific
differences in these characteristics, with males reach-
ing larger maximum sizes than females. Reasons for
sex-specific size and age distributions may be due to a
wide array of factors, including regional conditions and
physiological costs of sperm and egg production. Kritzer
(2004) also found male L. carponotatus to be larger
than females and suggested that this is an Indo-Pacific
trait within the lutjanids because it does not always
occur in other geographic areas. Such sex-specific differ-

ences in lutjanid populations also may vary by region,
although the magnitude of any sex-dependent variation
within a geographic area remains poorly understood.
Hence, our parameter estimates for the remaining spe-
cies from samples pooled over regions of the GBR may
not be as informative as we would like, but they nev-
ertheless provide a good starting point for comparison
and applicability to other regions where data remain
scarce or absent.

Age and growth

Five of the seven species examined grew to similar sizes,
but three of these demonstrated different longevities
and the two largest species showed a twofold range in
longevity for roughly similar maximum sizes, again
illustrating the lack of a relationship between length
and age across tropical lutjanids. High maximum ages

428

Fishery Bulletin 108(4)

Table 3

Number and size of male and female lutjanid individuals sampled from the Great Barrier Reef between 1995 and 20o5 for re-
productive analysis. Size range is included in parentheses; values in bold indicate significant difference from an even sex ratio.

Species

Female

Male

Sex ratio
F/M

n

Mean size
(mm FL)

n

Mean size
(mm FL)

L. fulviflamma

28

263

16

250

1.75

(209-315)

(219-285)

S. nematophorus

32

533

41

485

0.78

(340-772)

(320-789)

A. virescens

50

511

32

509

1.56

(332-810)

(334-778)

L. adetii

18

284

22

290

0.82

(254-374)

(243-341)

L. gibbus

8

277

48

330

0.17

(227-356)

(262-418)

L. vitta

7

266

18

270

0.39

(204-307)

(226-310)

L. cai'ponotatus

520

274

1722

292

0.30

(203-355)

(205-405)

of 36 and 23 years were evident in S. nematophorus (the
largest species) and L. carponotatus (the second smallest
species), respectively, despite their different maximum
sizes. Lutjanus gibbus, A. virescens, and L. fulviflamma
had shorter life spans and maximum ages of 12, 16, and
17 years, respectively. Lutjanus carponotatus have previ-
ously been reported to have maximum ages of 18 and 20
years (Newman et al., 2000a; Kritzer, 2002, 2004) which
are consistent with the 23 year maximum obtained here.
Shorter longevities recorded for L. gibbus, A. virescens,
and L. fulviflamma align with those from other lutja-
nid species such as L. vitta (12 years, Newman et al.,
2000a), L. guttatus (rose snapper, 11 years, Amezcua et
al., 2006), and L. fulviflamma (14 years, Grandcourt et
al., 2006). In contrast, L. adetii, a small species simi-
lar in size and appearance to L. vitta, has a reported
maximum age of 24 years (Newman et al., 1996), further
demonstrating the variability in life histories of similar
size lutjanid species.

This and most previous studies reveal that these
species have rapid initial growth despite differences
in size and longevity; however, they reach asymptotic
sizes at relatively young ages (Newman et al., 1996,
2000a; Kritzer, 2002, 2004; Grandcourt et al., 2006).
Newman et al. (1996) suggested that size could not be
used to infer age for L. adetii beyond five years of age.
This principle is probably applicable for many lutjanid
species and is supported by the growth patterns for four
of the five species for which growth was analyzed, the
exception being L. gibbus. All five species reached 50%
of before reaching 4 years of age. Caution should be
used when generalizing, however, because red bass (L.
bohar) and goldband snapper ( Pristipomoides multidens)
have been shown to be slow growing, long lived, and

late maturing, showing a classic K-selected life history
(Newman and Dunk, 2003; Marriott et al., 2007). That
result contrasts with the fast growth observed in most
other lutjanid species so far examined.

Lutjanus gibbus was the only species that did not
reach an asymptote in the unconstrained growth curve.
This may have been the result of the gear excluding
smaller and younger individuals, a proposition support-
ed by the fact that the constrained VBGF curves did
produce an asymptote and the unconstrained functions
produced an unrealistic t0 value of -9.48. Observations
that larger individuals were collected from deeper water
indicate that the largest size and oldest age classes of
L. gibbus and S. nematophorus may have been under-
sampled. Alternatively, these species may indeed have
a long growth period and not stop growing throughout
life, as does L. bohar (Marriott et al., 2007). The larg-
est reported L. gibbus, however, was 50 cm total length
(TL) (Carpenter and Niem, 2001) — only 5 cm larger
than the largest individual sampled in this study (418
mm FL, =500 mm TL). Lutjanus gibbus was also the
species with the highest mortality estimates from both
catch curve and Hoenig’s estimators, indicating that it
had the highest turnover rates. Further sampling will
be required to gain a better understanding of the age
and growth characteristics of this species and resolve
whether the differences in characteristics between L.
gibbus and the other species examined were attribut-
able to different life history strategies or to the effects
of species-specific sampling biases.

All five species for which age was estimated reached
50% of the estimated L „ at young ages in relation to
their maximum age. The percentage of longevity at
which 50% was reached was similar for most spe-

Heupel et al.: Demographic characteristics of exploited tropical lutjanids

429

4

5

3

•

• •

S. nematophorus 4

\ * A. virescens

2

1

3

• \

X 2

• •

• • X • • i

• \

• X*

0

Xv

2 4 6 8 10 12 14 16 18 20 0

2 4 6 8 10 12

8

6

In frequency

hO •&. O)

\ 5

L. carponotatus

•

4

* .

•

2

•

• 1
•

L. gibbus

• X.

0

o

8 10 12 14 16 18 20 22 24

6 8 10 12

3

L. fulviflamma

2

x. •

1

• • Xs^ •

0

• •

5 8 10 12 14 16 18 20

Age (yr)

Figure 6

Catch curves for five lutjanid species from the Great Barrier Reef between 1995 and
2005. The slopes of the regressions provided estimates of the rate of total mortality ( Z )
for each species.

cies, and L. gibbus was the only species taking greater
than 10% of its longevity to attain 50% Lm. Growth
of L. carponotatus varied significantly among regions
spanning 7° latitude, growing more quickly to smaller
asymptotic lengths in the more equatorial regions than
in the south. Although statistically significant, the dif-
ference in growth may have little biological signifi-
cance with varying only about 3% among regions.
Regional variation in growth for the other species re-
mains unknown because of a lack of data but results for

L. carponotatus reveal potential environmental influ-
ences on observed patterns for these other species.

Mortality

Estimates of mortality were likely biased because of
selectivity of the sampling gear. For example, the posi-
tively skewed age distributions for S. nematophorus
and A. virescetrs indicate that older fish were less avail-
able to the sampling gear and were likely to be under-

430

Fishery Bulletin 108(4)

represented in the sample, resulting in overestimates
of Z from catch curves. Estimates of Z derived from
Hoenig’s equation may be more appropriate for these
species. Similarly, older individual L. gibbus and L.
fulviflamma may not have been collected by the gear
and if so, under-sampling may have resulted in overes-
timates of Z from the catch curves and Hoenig’s method.
Notwithstanding these potential biases, comparison
of mortality rates revealed that A. virescens had a
similar mortality rate to that of L. gibbus, indicating
that A. virescens also has a relatively high population
turnover rate. Aprion virescens grows quickly to a large
size but may not live as long as other lutjanid species,
despite attaining relatively large sizes. Symphorus
nematophorus, for example, attained the largest size
and had the second lowest mortality rate of the species
examined. Lutjanus fulviflamma mortality estimates
differed most between estimation methods, with catch
curve estimates resulting in lowest mortality rates for
this species (0.14/yr), but the Hoenig estimate revealed
higher mortality rates (0.25/yr), similar to those for
A. virescens and L. gibbus. The Hoenig estimate was
also similar to rates previously reported for L. fulvi-
flamma (0.29/yr, Grandcourt et ah, 2006), indicating
some bias in the estimate from catch curves. Like L.
gibbus, L. carponotatus under six years of age could
not be used in catch curve estimates of mortality, but
the 6-23 year age classes yielded mortality estimates
for L. carponotatus of 0.30/yr (catch curve) and 0.18/yr
(Hoenig), similar to estimates calculated previously for
this species (0.20/yr, Newman et al., 2000a; 0.26-0.29/
yr, Kritzer, 2004). The range of mortality estimates for
the species examined in this analysis agree well with
those for other lutjanids (Newman et ah, 1996, 2000a;
Amezcua et al., 2006) and are another indication of the
variability in life history strategies within the family.

Maturity and sex ratio

All except one individual sampled across all species
were sexually mature, supporting the conclusion that
these lutjanids reach sexual maturity early in life.
Biased sex ratios were observed for all of the species
sampled although the apparent biases were statistically
significant for only three species. Two species (L. fulvi-
flamma, A. virescens ) showed large but nonsignificant
female-biased sex ratios, whereas all others showed a
male-biased ratio, and three (L. carponotatus, L. vitta,
L. gibbus) were not significantly different from 1:1.
Lutjanids are gonochoristic species and therefore it
may be expected that adult sex ratios would be close
to 1:1 in local populations, although at least three
other studies have revealed biased sex ratios. Kritzer
(2004) found that L. carponotatus had a female-biased
sex ratio, whereas Newman et al. (2000a) reported a
strongly male-biased sex ratio for the same species in
similar locations to those that we examined. Studies of
L. fulviflamma from different locations showed widely
variable sex ratios. Kaunda-Arara and Ntiba (1997)
reported a male-biased sex ratio in Kenya, and Grand-

court et al. (2006) reported a female-biased sex ratio in
the southern Arabian Gulf. It is difficult, therefore, to
establish generic patterns of sex ratios across, or even
within, lutjanid species given the contradictory patterns
in the literature and among the species sampled here. It
is possible that sex-ratio bias is a result of a differential
survival of males and females or sex-specific patterns
in distribution that would result in males and females
having different probabilities of capture in the sampling
strategies used in various studies, including the present
one. Kritzer (2004) was one of the few to have examined
mortality by sex, but no difference in mortality by sex
was found. This single result may indicate that differ-
ential spatial distributions may be a more likely cause
of sex-ratio biases in samples of lutjanid populations.
It has been suggested that sex ratio may be more even
during spawning events (Kritzer, 2004), but no data are
available to test this hypothesis.

Implications for management of lutjanid populations

An improved understanding of the demographic param-
eters of gonochoristic species is crucial to furthering
research on the effects of fishing on their populations.
Results here clearly demonstrate that all or even super-
ficially similar (e.g., in size) subsets of lutjanid species
should not be treated in the same manner in these types
of analyses and that vulnerability is likely to be variable
within the family. Careful consideration of the inherent
life history variability of these species is required in the
development of theories and generalizations about this
family and others.

This case study of seven lutjanid species clearly in-
dicates that data from one species cannot be applied
to another in determining appropriate management
measures for these populations. Some species appeared
to be more susceptible than others to overexploitation
by fisheries because of their longer life spans and lower
rates of mortality. Symphoi'us nematophorus is a good
example of a species with a long life span, large size,
and low mortality. The combination of these factors
could make this species a desirable fisheries target
(owing to its larger size than other lutjanids), but also
one of the most vulnerable because of its life history
characteristics. Symphorus nematophorus and L. gibbus
are currently no-take species within the GBR and have
historically been avoided because of a potential risk of
ciguatera (a form of food poisoning from eating large
reef fish), and therefore these species are largely pro-
tected from harvest within this region, although this
may not be the case in other parts of their range.

In comparison, the longevity of L. carponotatus and
L. adetii in relation to other lutjanid species may make
them more vulnerable to overfishing than sibling spe-
cies (Newman et al., 1996). Despite their small size and
fast growth, these populations may be more vulnerable
than similar species such as L. vitta which have shorter
longevities and hence potentially faster population turn-
over rates (Newman et al., 2000a). Notably, most of the
species examined here recruited to the fishing gear at

Heupel et al.: Demographic characteristics of exploited tropical lutjamds

431

relatively early ages but also apparently reached sexual
maturity before recruitment to the fishery. The exis-
tence of early maturity in relation to longevity indicates
a life history strategy with high reproductive potential
in older individuals — perhaps indicative of adaption to
low-frequency episodic recruitment successes (Kritzer,
2002, 2004). These characteristics may mean that lu-
tjanids are particularly vulnerable to recruitment col-
lapse from sustained harvest at relatively low rates of
fishing-induced mortality.

Current management measures for lutjanid species
within the GBR are precautionary to protect the wid-
est possible range of lutjanid family members, but this
may not be the case in other parts of their range and
implications of differences among species should be con-
sidered in such situations. The presence of substantial
variation in life histories among species would indicate
that the data presented here could serve as a bench-
mark for these species in other regions, but should not
be applied to different species that may not have com-
parable demographic parameters despite morphometric
similarities to the species examined here. Failure to
recognise differences in life histories when implement-
ing management strategies across species may result in
over-exploitation of some species, under-exploitation of
others, or both. Furthermore, we recommend that local
species-specific estimates of population parameters are
obtained wherever possible because significant regional
and local variation in population parameters is becom-
ing increasingly apparent for tropical reef fish popula-
tions (e.g., Adams et al., 2000; Kritzer, 2002; Williams
et al., 2003). Consequently, estimates derived from local
populations are likely to significantly improve assess-
ments and advice for the management of particular
stocks.

Acknowledgments

Funding for the ELF experiment was provided by the
CRC Reef Research Centre, the Fisheries Research
and Development Corporation, the Great Barrier Reef
Marine Park Authority, Queensland Primary Industries
and Fisheries, and James Cook University. The authors
would like to thank the many commercial fishermen
who participated in the ELF experiment, in particular
R. Stewart, M. Petersen, T. Must, K. Holland, and M.
Bush. Funding to process and analyze samples from
the ELF experiment was provided by the Australian
Government’s Marine and Tropical Sciences Research
Facility through the Reef and Rainforest Research
Centre. This manuscript is a contribution from the
ELF project.

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433

Abstract — We evaluated the conser-
vation benefits of the use of circle
hooks compared with standard J
hooks in the recreational fishery for
Atlantic istiophorid billfishes, noting
hooking location and the presence of
trauma (bleeding) for 123 blue marlin
(Makaira nigricans ), 272 white marlin
(Kajikia albida), and 132 sailfish
(Istiophorus platypterus ) caught on
natural baits rigged with one of the
two hook types. In addition, we used
pop-up satellite archival tags (PSATs)
to follow the fate of 61 blue marlin
caught on natural baits rigged with
circle hooks or on a combination of
artificial lure and natural bait rigged
with J hooks. The frequencies of inter-
nal hooking locations and bleeding
were significantly lower with circle
hooks than with J hooks for each of
the three species and were signifi-
cantly reduced for blue marlin caught
on J hooks than for white marlin
and sailfish taken on the same hook
type. Analysis of the data received
from 59 PSATs (two tags released
prematurely) indicated no mortali-
ties among the 29 blue marlin caught
on circle hooks and two mortalities
among the 30 blue marlin caught on
J hooks (6.7%). Collectively, the hook
location and PSAT data revealed that
blue marlin, like white marlin and
sailfish, derive substantial conserva-
tion benefits from the use of circle
hooks, and the negative impacts of
J hooks are significantly reduced for
blue marlin relative to the other two
species.

Manuscript submitted 6 April 2010.
Manuscript accepted 22 July 2010.
Fish. Bull. 108:433-441 (2010).

The views and opinions expressed
or implied in this article are those
of the author (or authors) and do not
necessarily reflect the position
of the National Marine Fisheries
Service, NOAA.

Asymmetric conservation benefits of circle hooks
in multispecies hillfish recreational fisheries:
a synthesis of hook performance and analysis
of blue marlin ( Makaira nigricans )
postrelease survival

John E. Graves (contact author)1
Andrij Z. Horodysky2

Email address for contact author: graves@vims.edu

1 Department of Fisheries Science
Virginia Institute of Marine Science
College of William & Mary

Rt. 1208 Greate Road
Gloucester Point, Virginia 23062

2 Living Marine Resources Cooperative Science Center
Department of Marine and Environmental Science
Hampton University

100 E. Queen St.

Hampton, Virginia 23668

Istiophorid billfishes in the Atlantic
Ocean experience considerable fish-
ing pressure and most stocks are
overfished. The greatest source of
fishing-induced mortality for istio-
phorids results from the pelagic long-
line fishery that targets tunas and
swordfish; however, artisanal and rec-
reational fisheries also represent sig-
nificant sources of mortality for some
species (Arocha and Ortiz, 2006).
The United States National Marine
Fisheries Service (NMFS) man-
ages the recreational hillfish fishery
with relatively large minimum sizes
released to ensure that the major-
ity of billfishes are released: 251 cm
(99 in) lower jaw fork length (LJFL)
for blue marlin (Makaira nigricans),
168 cm (66 in) LJFL for white marlin
(Kajikia albida ), and 152 cm (60 in)
LJFL for sailfish (Istiophorus platyp-
terus). No recreational landings are
allowed for longbill spearfish (Tet-
rapturus pfluegeri), and no manage-
ment measures currently exist for
roundscale spearfish (T. georgii). As
a result of these management mea-
sures and changes in angler behavior
promoting live release of these species
(Ditton and Stoll, 2003), the U.S. rec-
reational hillfish fisheries are primar-
ily catch-and-release fisheries, and up

to 99% of white marlin are released
alive annually (Goodyear and Prince,
2003). However, not all billfishes that
are released alive survive capture;
postrelease mortality can be signifi-
cant in some fisheries (Domeier et ah,
2003; Horodysky and Graves, 2005).

A growing body of evidence indi-
cates that the use of circle hooks can
greatly reduce the incidences of in-
ternal (deep) hooking, hook induced
trauma (bleeding), and postrelease
mortality of piscivorous fishes (Mu-
oneke and Childress, 1994; Skomal
et al., 2002; Cooke and Suski, 2004),
including billfishes (see Serafy et ah,
2009). For istiophorid billfishes, live
and dead natural baits rigged with J
hooks reveal higher frequencies of in-
ternal hooking locations and trauma
for sailfish, striped marlin (K. audax),
and white marlin than the same baits
rigged with circle hooks (Prince et
al., 2002, 2007; Domeier et al., 2003;
Horodysky and Graves, 2005). Using
pop-up satellite archival tags (PSATs)
to follow the fate of released fish, Do-
meier et al. (2003) noted a reduced
but nonsignificant postrelease mortal-
ity for striped marlin caught on live
natural baits rigged on circle hooks,
and Horodysky and Graves (2005) re-
ported a highly significant reduction

434

Fishery Bulletin 108(4)

in postrelease mortality of fish caught on circle hooks
compared to those caught on J hooks. In response to the
depleted stock condition of Atlantic billfishes and the re-
duction in undesirable hooking locations and postrelease
mortality resulting from the use of circle hooks, NMFS
in 2008 implemented a management measure requiring
the use of non-offset circle hooks in natural baits for all
Atlantic billfish tournaments. During the rule-making
process, NMFS received several comments stating that
blue marlin have lower rates of deep hooking with J
hooks than white marlin or sailfish, especially when
caught on artificial lure and natural bait combinations
rigged with J hooks, a common terminal tackle used in
the Atlantic recreational fishery. It was also suggested
that blue marlin released from the recreational fishery
have high rates of survival.

Little is known about the effects of hook type on
postrelease survival of blue marlin. A preliminary study
on the use of PSATs to investigate postrelease survival
of blue marlin inferred survival for at least eight of
nine individuals caught on lures or skirted baits with J
hooks trolled at relatively high speeds in the Bermuda
recreational fishery (Graves et ah, 2002). Flowever,
there were no data to directly compare the postrelease
mortality of blue marlin caught on natural baits or on
a combination of artificial lure and natural bait rigged
with either circle hooks or J-hooks. To gain insights into
the relative conservation benefits of circle hooks in the
recreational fishery for Atlantic blue marlin and other
istiophorids, we compiled data on hooking location and
the incidence of trauma (bleeding) for 123 blue marlin,
272 white marlin, and 132 sailfish caught on natural
baits rigged with either J hooks or circle hooks. Fur-
thermore, to estimate the postrelease mortality of blue
marlin caught on natural baits with circle hooks or ar-
tificial lure and natural bait combinations with J hooks,
we deployed 61 PSATs to follow the fate of blue marlin
caught on one of the two types of terminal tackle.

Materials and methods
Hooking location

Information on hook type, hooking location, and trauma
(the presence of bleeding) was collected by the authors
for all blue marlin, white marlin, and sailfish caught
on trolled plain (naked) ballyhoo ( Herniramphus brasil-
iensis) baits during our PSAT tagging operations in the
western North Atlantic from 2006 through 2009. Similar
information was recorded by three cooperating charter
captains (one from Oregon Inlet, NC, USA, and two
from La Guaira, Venezuela) for billfishes caught during
fishing operations in 2006. To accommodate captain and
charter angler preferences, a variety of hook models and
sizes were employed in the different fishing operations,
but the most common J hook model was the Mustad 9175,
size 7/0 (Mustad, Gjovik, Norway), and the most common
circle hook model was the Eagle Claw L2004EWF, size
8/0 (Eagle Claw, Denver, CO). As is typical for this fish-

ery, circle hooks were left exposed, rigged to the head
of the bait, whereas J hooks were inserted through the
mouth of the bait fish with the tip exiting the ventral
surface (Fig. 1, A and B).

Baits were trolled at approximately 6 nm/hr (11.1 km/
hr) during daylight hours on 30-50 lb (13.6-22.7 kg)
class fishing tackle. As billfish approached the trolled
bait, anglers would typically decrease tension on the
line for periods of 4-10 s, “dropping back” the ballyhoo
bait to the feeding billfish, which provided time for the

Graves and Horodysky: Conservation benefits of circle hooks in multispecies recreational billfish fisheries

435

animal to ingest the bait before feeling tension on the
line (see Jolley, 1974; Mather et al., 1975; Prince et al.,
2007, for a description of this fishing method), although,
in some instances the fish attacked trolled baits before
an angler could reach the rod and drop back. The loca-
tion of the hook and the presence or absence of bleeding
(visible blood) was noted at the time of capture. Hooking
locations were classified as external when all or part of
the hook was visible outside of the fish’s mouth, includ-
ing fish that were foul hooked (hooked in areas away
from the fish’s mouth), and internal if no part of the
hook was visible when the fish’s mouth was closed.

Postrelease survival

PSATs were attached to 61 blue marlin caught in rec-
reational fisheries in the western Atlantic Ocean. Fish
were caught by using J hooks and circle hooks that were
rigged with natural baits consisting of ballyhoo or Span-
ish mackerel (Scomberomorous maculatus) . Baits were
rigged in a manner typical for the fishery. J hooks were
inserted inside the baits, which were fished in combina-
tion with a skirted artificial lure (e.g., Ilander [L & S
Bait Company, Largo, FL], chugger [Mold Craft Lures,
Pompano Beach, FL], or Seawitch [C & H Lures, Jack-
sonville, FL]) attached directly ahead of the bait (Fig.
1, C and D). Circle hooks were rigged externally on the
baits, either on top of the head or directly in front of the
bait. In some cases, a small artificial lure (chugger) was
placed between the circle hook and the bait.

Blue marlin were caught on 30-130 lb (13.6-59.1 kg)
class sportfishing tackle in waters off the United States
mid-Atlantic coast; St. Thomas, U.S. Virgin Islands;
Punta Cana, Dominican Republic; La Guaira, Venezuela;
and Porto Seguro, Brazil, between September 2007 and
October 2009 (Appendix 1). As is typical for the fishery,
the vessel was maneuvered by the captain to assist the
angler in the capture of the fish. Blue marlin were not
brought alongside the vessel until they were considered
to be sufficiently calm to allow accurate tag placement.

The first 61 fish available to us were tagged with a
Microwave Telemetry PTT 100 HR tag (Microwave Te-
lemetry, Inc., Columbia, MD), programmed for release
after 10 days. This tag model records temperature,
pressure (depth), and light levels approximately every
90-120 s. The tags were rigged as described in Graves
et al. (2002), and deployed as described in Horodysky
and Graves (2005). The location of the hook and pres-
ence or absence of bleeding was noted for each fish at
the time of tagging. If practical, the hook was removed
from the fish before its release. As is customary in this
fishery, blue marlin that were unable to maintain their
position upright in the water column were resuscitated
by using the forward motion of the vessel to facilitate
movement of water over the fish’s gills before release
(Appendix 1).

Survival of released blue marlin was inferred from
temperature and depth profiles following the protocols
of Horodysky and Graves (2005). Net displacement of
each fish was calculated as the minimum straight line

distance from the point of release to the point of tag
pop-up. Cochran-Mantel-Haenszel (CMH) or Fisher’s
exact tests were used to address the effect of the J
hooks and circle hooks on hooking location, hook-in-
duced trauma, and survival. A Yates correction for
small sample size was applied in conducting CMH tests
when expected cell values were less than 5 (Agresti,
1990). All statistical analyses were conducted in the
Statistical Analysis System, vers. 9.1 (SAS Institute,
Cary, NC). Bootstrapping simulations were performed
to determine the 95% confidence intervals of the esti-
mates of mortality after release by using the software
developed by Goodyear (2002).

Results

Hooking location

Hooking location and the presence or absence of bleeding
were noted for 123 blue marlin, 272 white marlin, and
132 sailfish caught on natural baits rigged with either J
hooks or circle hooks (Table 1). The incidence of internal
hooking with J hooks ranged from 19.1% (blue marlin)
to 44.4% (white marlin), and the frequency of internal
hooking locations for fish caught on circle hooks was
considerably lower, ranging from 1.8% (blue marlin)
to 6.2% (sailfish). For blue marlin, white marlin, and
sailfish, J hooks had a significantly higher probability
of internal hooking locations than circle hooks (P<0.007,
P<0.0001, P<0.001, respectively). The frequency of inter-
nal hooking locations for J hooks in blue marlin (19.1%)
was less than half the value observed for white marlin
and sailfish (44.4% and 41.2%, respectively), and the
difference between blue marlin versus white marlin and
sailfish combined was significant (P<0.0014).

The occurrence of trauma (bleeding) mirrored the pat-
tern observed for internal hooking locations between the
two hook types for each of the three billfishes. Across
the three species, over 81% of the instances of bleeding
(44/54) were associated with internal hooking loca-
tions (7/9 blue marlin, 20/24 white marlin, and 16/17
sailfish). Bleeding of fish caught on circle hooks ranged
from 0% in blue marlin to 2.5% in sailfish (Table 1). For
blue marlin, white marlin, and sailfish, J hooks had a
significantly higher probability of inducing bleeding
than circle hooks (P<0.0141, P<0.001, P<0.0001, re-
spectively). As with the occurrence of internal hooking
locations with J hooks among the three species, the
frequency of bleeding observed in blue marlin (13.2%)
was less than half that observed in white marlin and
sailfish (both 33.3%); blue marlin had significantly
lower rates of bleeding resulting from the use of J hooks
than white marlin and sailfish combined (P<0.027).

Postrelease survival

Sixty-one blue marlin were caught on natural baits
rigged with circle hooks (30) or on a combination of
artificial lure and natural bait rigged with J hooks (31),

436

Fishery Bulletin 108(4)

Table 1

Hooking location (frequency; 95% confidence interval) and presence or absence of trauma (bleeding, not bleeding) for observed
recreational catches of blue marlin (Makaira nigricans, zi = 123), white marlin (Kajikia albida, n-212), and sailfish (Istiophorus
platypterus, n = 132), caught on natural baits rigged with either J hooks or circle hooks in the western North Atlantic Ocean.

Hook location

Trauma

Species

Hook type

Internal

Externa]

Bleeding

Not bleeding

Blue marlin

Circle

1 (1.8%; 0-5.4%)

54 (98.2%; 90.0-99.9%)

0 (0%; 0-2.0%)

55 (100%; 93.5-100%)

“J”

13(19.1%; 10.6-28.5%)

55 (80.9%; 69.5-89.4%)

9 (13.2%; 6.2-23.6%)

59 (86.8%; 78.7-94.8%)

White marlin

Circle

4 (2.0%; 0. 6-5.0%)

196 (98.0%; 94.5-99.5%)

2 (1.0%; 0-2.4%)

198 (99.0%; 96.4-99.9%)

“J”

32 (44.4%; 32.7-56.6 %)

40 (55.6%; 43.4-67.3%)

24 (33.3% ; 22.4-44.2%)

48 (66.7%; 54.6-77.3%)

Sailfish

Circle

5 (6.2%; 2.0-13.8%)

76 (93.8%; 86.0-97.8%)

2 (2.5%; 0.3-8. 6%)

79 (97.5%; 91.4-99.7%)

“J”

21 (41.2%; 27.6-55.8%)

30 (58.8%; 44.3-72.4%)

17 (33.3%; 20.7-47.9%)

34(66.7%; 52.1-79.2%)

tagged with Microwave Telemetry PSATs, and released.
Three blue marlin were released off the U.S. mid-Atlan-
tic coast; 26 off St. Thomas, U.S. Virgin Islands; 2 off
Punta Cana, Dominican Republic; 21 off La Guaira,
Venezuela, and 9 off Porto Seguro, Brazil (Appendix 1).
Estimated fish weights ranged from 70 lb (31.8 kg) to
500 lb (227.3 kg) (mean=216.4 lb [98.2 kg]). Fight times
(including tag attachment) ranged from 4 to 85 minutes
(mean=19.4 minutes). After tag placement, eight fish
exhibited difficulty maintaining an upright orientation
alongside the boat and were resuscitated for periods
ranging from one to ten minutes before their release
(Appendix 1).

All 61 PSATs reported after detachment from the
fish. Two tags detached prematurely — both on the first
day of deployment — and were excluded from survival
analyses. The 59 tags that remained attached for the
ten-day deployment period successfully transmitted
between 18% and 96% (mean = 81%) of the archived
data. Most of these PSATs remained at sea during the
data transmission period which typically lasts about
30 days before the battery power is exhausted. How-
ever, six tags washed ashore during the period of data
transmission, resulting in reduced data reception from
these tags. Two tags were recovered by beachcombers
and returned to us, allowing recovery of 100% of the
archived data.

We inferred the survival of 57 of 59 fish (96.6%)
that carried the tags for the 10-day deployment from
analyses of pressure (depth) and temperature profiles
over the 10-day tagging period (Appendix 1). Surviv-
ing blue marlin exhibited multiple daily vertical move-
ments as evidenced by the temperature and pressure
(depth) profiles throughout the course of the ten-day
tagging period. Many animals demonstrated a distinct
diurnal patterning to their dives, remaining near the
surface at night and making deep dives during the day
(Fig. 2A). Net displacement ranged from 10 to 943 km
(mean=226.9 km).

The two mortalities inferred from the PSAT data
occurred among the 30 blue marlin caught on artifi-
cial lure and natural bait combinations rigged with
J-hooks. Both individuals were hooked internally
and bled profusely from the gill area at the time of
capture. The archived data indicated that these in-
dividuals sank to the bottom shortly after release
and remained there for 48-96 hr, after which time
a release mechanism was activated by the constant
depth data in each PSAT and initiated tag release
and data transmission (Fig. 2B). The two mortalities
of blue marlin caught on artificial lure and natural
bait combinations with J hooks resulted in an esti-
mated postrelease mortality rate of 6.7%. The results
of 10,000 bootstrap simulations at an underlying true
mortality of 6.7% indicated that the approximate 95%
confidence intervals (Cl) for the mortality estimates
of blue marlin caught on J hooks for an experiment
with 30 tags would range from 0% to 22% (with the
methods of Goodyear, 2002). None of the 29 blue mar-
lin caught on natural baits with circle hooks died
during the ten day period, resulting in a postrelease
mortality estimate of 0%, with corresponding 95%
Cl ranges from 0% to 12.5%. The difference between
the estimates of postrelease mortality for blue mar-
lin caught on J-hooks and circle hooks was not sta-
tistically significant (Fisher’s exact test: P=0.26).

Discussion

The goal of this study was to determine whether blue
marlin derive similar conservation benefits from the
use of circle hooks in the recreational fishery as has
been previously reported for other istiophorid billfishes.
A direct comparison of hooking locations with the use
of J hooks and circle hooks in natural baits rigged as
they are typically fished in the recreational fishery
indicates that the use of circle hooks results in sig-

Graves and Horodysky: Conservation benefits of circle hooks in multispecies recreational billfish fisheries

437

A

Q.

Q B

Figure 2

Depth plots derived from pop-up satellite archival tag pressure data
for two blue marlin ( Makaira nigricans ) caught in the western Atlantic
recreational fishery. (A) Blue marlin no. 49 was caught on a naked
ballyhoo bait with a circle hook. This fish survived for the ten day
tagging period and exhibited a strong diel pattern, diving during the
day and remaining in surface waters at night. (B) Blue marlin no. 41
was caught on an artificial lure (Ilander) and ballyhoo combination
bait with a J hook and was bleeding profusely from the gills at the
time of capture. This fish died and sank to the bottom shortly after
release. The release mechanism on the tag was activated by constant
depth measurements for 48 hours and the tag floated to the surface
and began transmitting data.

nificantly lower rates of internal hooking
locations for blue marlin, white marlin,
and sailfish. We observed incidences of
internal hooking locations with circle
hooks ranging from 1.8% (blue marlin) to
6.2% (sailfish). The value of 2.0% (;i=200)
observed for white marlin is comparable
to the value of 1.7% (n = 59) reported for
white marlin caught on natural baits
with circle hooks (Graves and Horodysky,

2008). The incidence of internal hook-
ing locations observed for circle hooks
in sailfish (6.2%) is slightly higher than
that reported by Prince et al. (2002) for
Pacific sailfish caught on trolled natu-
ral baits with circle hooks (1.7%) but is
within the range reported for circle hooks
in live baits for both Atlantic sailfish
(6-16%; Prince et al., 2007) and striped
marlin (5-7%; Domeier et al., 2003).

The use of J hooks in natural baits
resulted in incidences of internal hook-
ing ranging from 19.1% (blue marlin) to
44.4% (white marlin). The frequency of
internal hooking in white marlin caught
with natural baits rigged with J hooks
(44.4%) is similar to the value report-
ed for white marlin caught on J hooks
(50%) by Horodysky and Graves (2005).

Internal hooking locations for sailfish
caught on J hooks rigged with natural
baits (41.2%) are comparable to results
for Pacific sailfish caught on trolled dead
baits rigged with J hooks (46.8%), and
fall within the range reported for Atlan-
tic sailfish caught on live baits rigged
with J hooks using a variety of dropback
times (23-57%; Prince et al., 2007), as
well as striped marlin caught on live
baits with J hooks (28%; Domeier et al.,

2003). The use of J hooks resulted in
a tenfold increase in internal hooking
locations relative to circle hooks for blue
marlin and a twentyfold increase for
white marlin and sailfish — a trend also
noted in previous studies of istiophorid billfish (Prince
et al., 2002, 2007; Domeier et al., 2003; Horodysky and
Graves, 2005).

Although the frequency of internal hooking locations
was significantly higher for blue marlin, white marlin,
and sailfish caught on J hooks than on circle hooks, the
rate of internal hooking locations for blue marlin caught
on J hooks was less than half of the values observed
for white marlin and sailfish. In a study of postrelease
mortality in the recreational blue marlin fishery off
Bermuda, Graves et al. (2002) reported no internal
hooking locations for the nine blue marlin caught on
artificial lures or artificial lure and natural bait com-
binations rigged with J hooks. The lower incidence of
internal hooking locations for blue marlin caught on

natural baits rigged with J hooks than for white mar-
lin and sailfish caught on similar terminal tackle may
result from interspecific differences in feeding ecology.
Many billfishes follow trolled baits for a short time
before striking, giving alert anglers an opportunity to
pick up the rod and drop the bait back to the fish as it
attacks. Dropback times of 5-10 s are common in the
white marlin fishery (Mather et al., 1975; Jesien et al.,
2006), and can be considerably longer in the sailfish
live bait fisheries (Prince et al., 2007). By contrast,
blue marlin are typically more aggressive feeders, often
attacking the bait before anglers have an opportunity
to react. When dropbacks are possible for this species,
they are often of shorter duration than those for white
marlin and sailfish, allowing less time for the bait to

438

Fishery Bulletin 108(4)

be swallowed and hence for the hook to lodge in an
undesirable location (Prince et al., 2007).

In previous studies, internal or deep hooking loca-
tions have been associated with an increased incidence
of trauma in istiophorids and other large pelagic fishes
(Domeier et al. 2003; Horodysky and Graves, 2005;
Prince et al., 2007; Skomal, 2007). In the present study,
trauma, as evidenced by bleeding, was significantly
lower for blue marlin, white marlin, and sailfish caught
on circle hooks than for those caught on J hooks. The
low incidence of bleeding associated with natural baits
rigged with circle hooks for white marlin that we ob-
served (1.0%) concurs with the value of 1.7% reported
for white marlin by Graves and Horodysky (2008) and
the range reported for the congeneric striped marlin
caught on live baits with circle hooks (3-4%, Domeier et
al., 2003). The frequency of bleeding with circle hooks
observed for sailfish (2.5%) in this study is slightly low-
er than the values reported for Pacific sailfish caught
on natural baits (6%) and for Atlantic sailfish caught on
live baits with circle hooks (5-13%; Prince et al., 2002,
2007). We noted bleeding in 33% of the white marlin
and 33% of the sailfish caught on natural baits with J
hooks. This value is somewhat lower than those report-
ed for white marlin (45%) and Pacific sailfish (56.8%)
caught on trolled natural baits, and higher than those
reported for striped marlin (21%) and Atlantic sailfish
(21-25%) caught on live baits (Prince et al., 2002, 2007;
Domeier et al., 2003; Horodysky and Graves, 2005).
The incidence of bleeding in white marlin and sailfish
caught on J hooks was significantly higher than that
for blue marlin caught on the same terminal tackle and
is consistent with an increased incidence of internal
hooking rates in the former species observed in this and
previous studies (Prince et al., 2002; 2007; Domeier et
al., 2003; Horodysky and Graves, 2005).

To directly follow the fate of blue marlin caught on
trolled natural baits or on bait and lure combinations
rigged with either circle or J hooks and released, we
deployed 61 PSATs, of which 59 remained attached for
the ten-day tracking period. All 29 blue marlin caught
on circle hooks rigged with natural baits or bait and
lure combinations survived for ten days after release.
In a study of 59 white marlin caught on natural baits
rigged with circle hooks, Graves and Horodysky (2008)
reported a single mortality. Together, these studies
reveal a very low level of postrelease mortality for bill-
fishes caught on circle hooks in natural bait trolling
fisheries. In contrast, Domeier et al. (2003) reported
an adjusted rate of postrelease mortality of 17.4% for
striped marlin caught from stationary vessels on live
baits rigged with circle hooks. These results support the
contention of Cooke and Suski (2004) that the magni-
tude of the conservation benefits of circle hooks varies
among species, gear types, and fisheries.

PSAT depth records indicated that two of 30 blue
marlin caught on artificial lure and natural combina-
tions rigged with J hooks died after release, resulting in
an estimated postrelease mortality of 6.7%. This value
is approximately one-fifth of the postrelease mortality

reported by Horodysky and Graves (2005) for 20 white
marlin caught on natural baits rigged with J hooks
(35%) and less than one-fourth of the value of 29.4%
reported by Domeier et al. (2003) for 24 striped marlin
caught on live baits rigged with J hooks. The reduction
in postrelease mortality of blue marlin caught on natu-
ral baits with J hooks relative to postrelease mortality
of white marlin caught on the same terminal tackle
parallels the reductions observed in the frequency of
internal hooking locations and bleeding between these
species.

In this study, the use of circle hooks in natural baits
resulted in significantly reduced internal hooking and
bleeding for blue marlin, white marlin, and sailfish.
Because blue marlin caught on J hooks experienced
significantly lower incidences of internal hooking loca-
tions and trauma than white marlin and sailfish caught
on the same terminal tackle, the conservation benefit
resulting from the use of circle hooks for blue marlin
is less than that experienced by the other two species.
This asymmetry was also evident in the analysis of
postrelease survival. There was a trend for decreased
postrelease mortality of blue marlin caught on natu-
ral baits with circle hooks (0%) than for blue marlin
caught on artificial lures and natural baits with J hooks
(6.7%), but the difference was much smaller than that
previously reported for white marlin caught on natural
baits rigged with the two hook types (0% and 35%,
respectively; Horodysky and Graves, 2005). Although
these results provide support for recent management
measures implemented by NMFS that require the use of
non-offset circle hooks in natural baits for all Atlantic
billfish tournaments, it is important to realize that the
conservation benefits of this measure vary asymmetri-
cally among the different billfish species.

Acknowledgments

We thank Captains J. Grant, R. Cox and J. Ross for
compiling information on hook location and fish condi-
tion. B. DeGabrielle, J. Tierney, J. Thiel, K. Neill, D.
Dutton, J. Schratweiser, and many others provided assis-
tance in catching and tagging blue marlin. M. Domeier
and the International Game Fish Association provided
logistical support. Funding for this study was provided
by the Gulf States Marine Fisheries Commission (Bill-
fish-2005-11), the National Marine Fisheries Service
(NA07NMF4720295), and the Offield Family Foundation.
This article is VIMS contribution number 3107.

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440

Fishery Bulletin 108(4)

Appendix 1

Summary information for 61 blue marlin ( Makaira nigricans) caught on different types of terminal tackle in the western Atlantic
recreational fishery, tagged with pop-up satellite archival tags, and released. Fish were caught off Venezuela (VZ), the Domini-
can Republic (DR), Virginia (VA), North Carolina (NC), the U.S. Virgin Islands (VI), and Brazil (BR) on natural baits or combina-
tion baits consisting of an artificial lure (chugger [Chug], Ilander [I], or Sea Witch [Swi]), and natural bait rigged with J hooks
( J) or circle hooks (C). Hook locations were recorded as internal (I) or external (E). Fight time included the tagging process and,
where applicable, resuscitation (Rduratlon m minutes), ancj trauma (bleeding) at the time of release was noted as present (Y) or absent
(N). Also included are the percentage of archived data recovered, mean straight line displacement (MSLD) over the 10-day tag-
ging period, and fate of the blue marlin (coded as live [L], dead [D], or premature release [-]).

Fish

Date

Loca-

tion

Gear

(lb)

Established

weight

Hook

type

Hook

location

Fight

time

Trauma

Data

(%)

MSLD

(km)

Fate

1

9/7/07

VZ

30

200

Chug/J

I

55

N

82

172

L

2

3/17/08

VZ

50

175

I/J

E

28 R3

N

81

139

L

3

3/28/08

DR

50

125

I/J

E

15 R2

N

68

49

L

4

3/29/08

DR

50

100

C

E

30

N

85

86

L

5

5/15/08

VZ

30

165

C

E

18

N

84

30

L

6

5/15/08

VZ

30

100

Chug/C

E

5

N

85

10

L

7

5/16/08

VZ

50

160

I/J

E

5

Y

73

123

L

8

5/17/08

VZ

30

75

C

E

15

N

85

87

L

9

6/15/08

VA

50

400

I/J

E

56

N

85

546

L

10

6/22/08

NC

80

350

I/J

E

35

N

88

943

L

11

8/8/08

VI

50

450

I/J

E

18

N

90

502

L

12

8/10/8

VI

50

275

I/J

I

5

N

90

646

L

13

8/10/08

VI

50

350

Chug/C

E

8

N

92

349

L

14

8/11/08

VI

50

175

Chug/J

E

11

N

83

107

L

15

8/11/08

VI

50

175

Chug/C

E

4

N

88

343

L

16

8/12/08

VI

50

200

I/J

I

10

Y

93

488

L

17

8/12/08

VI

50

125

I/J

E

12

Y

87

328

L

18

8/17/08

NC

80

375

Swi/J

E

40

N

90

709

L

19

9/7/08

VI

50

160

I/J

E

20

N

91

191

L

20

9/7/08

VI

50

250

Chug/C

E

15

N

68

20

L

21

9/7/08

VI

50

235

C

E

22

N

92

319

L

22

9/8/08

VI

50

275

Chug/J

I

55

N

90

120

L

23

9/9/08

VI

50

125

I/J

I

14

N

93

238

L

24

9/10/08

VI

50

90

Chug/J

I

20 R10

Y

72

68

L

25

9/10/08

VI

50

90

Chug/J

E

13

N

88

264

L

26

9/11/08

VI

80

325

I/J

E

35

N

100

197

L

27

9/15/08

VI

50

100

Chug/C

E

12

N

92

234

L

28

9/25/08

VZ

30

70

C

E

5

N

90

13

L

29

11/1/08

BR

130

300

Chug/C

E

11 R2

N

85

119

L

30

11/2/08

VZ

30

150

Chug/C

E

21

N

84

336

L

31

11/3/08

VZ

30

290

C

E

85

N

94

171

L

32

11/4/08

BR

50

125

C

E

5

N

74

284

L

33

11/15/08

VZ

30

250

C

E

20

N

18

263

L

34

1 1/17/08

VZ

30

150

C

E

20

N

87

135

L

35

11/22/08

VZ

30

150

C

E

21

N

79

115

L

36

11/30/08

VZ

30

120

Chug/C

E

36 R4

N

86

83

L

37

12/2/08

BR

130

200

Chug/J

I

12

Y

93

47

D

38

12/2/08

BR

130

175

Chug/C

E

5

N

36

289

L

39

12/9/08

VZ

30

125

Chug/C

I

21

N

81

226

L

40

12/9/08

VZ

50

100

I/J

E

6

N

90

118

L

41

12/9/08

VZ

50

200

I/J

I

9

Y

61

109

D

continued

Graves and Horodysky: Conservation benefits of circle hooks in multispecies recreational billfish fisheries

441

Appendix 1 (continued)

Fish

Date

Loca-

tion

Gear

(lb)

Established

weight

Hook

type

Hook

location

Fight

time

Trauma

Data

(%)

MSLD

(km)

Fate

42

12/11/08

VZ

30

250

I/J

E

18

N

83

107

L

43

12/11/08

BR

130

450

Chug/C

E

10

N

85

218

L

44

12/12/08

BR

130

500

C

E

15

N

90

233

L

45

12/12/08

BR

50

400

C

E

12

N

91

216

L

46

1/2/09

BR

130

300

C

E

12

N

88

19

L

47

1/2/09

BR

130

400

Chug/C

E

10

N

94

329

L

48

2/7/09

VZ

80

145

Swi/J

E

10

N

26

124

L

49

4/18/09

VZ

80

115

C

E

14

N

85

96

L

50

5/6/09

VZ

50

265

I/J

E

34

N

57

88

L

51

5/9/09

VZ

50

110

C

E

10

N

100

90

L

52

7/6/09

VI

50

170

Chug/J

E

25 R3

N

85

70

—

53

7/6/9

VI

50

300

Chug/J

E

45 R1

N

80

196

L

54

7/9/09

VI

50

200

Chug/J

E

15

N

86

143

L

55

8/1/09

VI

50

250

Chug/C

E

15

N

38

109

L

56

8/8/09

VI

50

250

Chug/J

E

15

N

31

379

L

57

8/30/09

VI

50

175

C

E

20

N

93

80

—

58

9/2/09

VI

50

150

C

E

18

N

94

214

L

59

9/4/09

VI

50

350

C

E

16

N

96

463

L

60

9/30/09

VI

50

175

C

E

14

N

90

271

L

61

10/7/09

VI

50

200

I/J

E

40

N

92

385

L

442

Abstract — Settled juvenile blue rock-
fish ( Sebastes mystinus) were collected
from two kelp beds approximately 335
km apart off Mendocino in northern
California and Monterey in central
California. A total of 112 rockfish
were collected from both sites over
5 years (1993, 1994, 2001, 2002,
and 2003). Total age, settlement
date, age at settlement, and birth
date were determined from otolith
microstructure. Fish off Mendocino
settled mostly in June and fish off
Monterey settled mostly in May (aver-
age difference in settlement=23 days).
Although the difference in the timing
of settlement followed this same pat-
tern for both areas over the five years,
settlement occurred later in 2002 and
2003 than in the prior years of sam-
pling. The difference in the timing
of settlement was due primarily to
differences in birth dates for the
two areas. The time of settlement
was positively related to upwelling
and negatively related to sea level
anomaly for most of the months
before settlement. Knowledge of the
timing of settlement has implications
for design and placement of marine
protected areas because protection
of nursery grounds is frequently a
major objective of these protected
areas. The timing of settlement is
also an important consideration in the
planning of surveys of early recruits
because mistimed surveys (caused by
latitudinal differences in the timing
of settlement) could produce biased
estimates.

Manuscript submitted 4 May 2010.
Manuscript accepted 27 July 2010.
Fish. Bull. 108:442-449 (2010).

The views and opinions expressed
or implied in this article are those
of the author (or authors) and do not
necessarily reflect the position
of the National Marine Fisheries
Service, NOAA.

Influence of ocean conditions on the timing
of early life history events for blue rockfish
(Sebastes mystinus) off California

Thomas E. Laidig

Email address: tom.laidig@noaa.gov

Fisheries Ecology Division

Southwest Fisheries Science Center

National Marine Fisheries Service

National Oceanic and Atmospheric Administration

110 Shaffer Road

Santa Cruz, California 95060

Successful recruitment of fishes into
adult populations can have a major
influence on population biomass.
Within a species, recruitment events
can vary widely in magnitude both
temporally and spatially (Doherty and
Fowler, 1994; Ralston and Howard,
1995; Caley et al., 1996). Under-
standing this variability in recruit-
ment strength is a critical goal in
predicting adult population structure
(Doherty and Fowler, 1994; Hidalgo
et al., 2009). Knowledge of the spa-
tial and temporal variability in
recruitment of a population can lead
to enhanced management of the spe-
cies (e.g., to protection of important
nursery areas) (Grorud-Colvert and
Sponaugle, 2009).

Variation in recruitment strength
is influenced by multiple biotic and
abiotic factors, including the mag-
nitude of spawning biomass, preda-
tion, available habitat, available prey,
competition, temperature, upwelling,
turbulence, water quality, and ocean
currents (Peterman and Bradford,
1987; Ainley et al., 1993; Ralston
and Howard, 1995; Hobson et al.,
2001; Johnson et al., 2001; Sale et
al., 2005; Hidalgo et al., 2009). Re-
cruitment variability can occur from
large-scale (e.g., El Nino or La Nina
events, Pacific Decadal Oscillations)
(Carr, 1991; Field and Ralston, 2005;
Laidig et al., 2007) to small-scale pro-
cesses (e.g., localized patchiness of
suitable nursery habitats; fine-scale
oceanographic events) (Sale et al.,
2005; Johnson, 2006). Determining
the relative influence of these pro-

cesses on fish recruitment has been
a goal for many studies (Peterman
and Bradford, 1987; Yoklavich et al.,
1996; Laidig et al., 2007).

Annual recruitment of rockfishes
( Sebastes spp.) in the northeast Pa-
cific can vary by orders of magnitudes
between years (Ralston and Howard,
1995; Laidig et al., 2007). In addition
to temporal variability in recruitment,
latitudinal or spatial variability also
has been observed for several rockfish
species along the west coast (Sakuma
et al., 2006). Variable recruitment
leads to greater uncertainty in the
prediction of year-class strength.

Rockfishes give birth to larvae (par-
turition) that survive in the plankton
for several months before settling into
nursery or adult habitats (Carr, 1991;
Love et al., 2002; Ammann, 2004).
For several rockfish species, it has
been demonstrated that the strength
of the year class is determined during
this planktonic stage (Ralston and
Howard, 1995; Laidig et al., 2007;
Wilson et al., 2008) and that it can
be affected further by postsettlement
mortality from predation (Hobson et
al., 2001).

In this study, the recruitment of ju-
venile blue rockfish (S. mystinus) from
the pelagic environment to nearshore
kelp beds was examined in two geo-
graphic regions along the California
coast. Blue rockfish are an important
commercial and recreational species
in California ranging from at least
British Columbia to northern Baja
California (Love et al., 2002). Otolith
microstructure was used to estimate

Laidig: Influence of ocean conditions on the timing of early life events for Sebastes mystmus

443

Table 1

Location, year, sampling date, number of samples col-
lected, and size range of blue rockfish (Sebastes mystinus)
examined for settlement marks in otoliths.

Location

Year

Sample

date

Number

of

samples

Size range
(mm standard
length)

Mendocino

1993

2 Jun

11

37-48

Monterey

1993

3 Jun

11

38-48

Mendocino

1994

26 Jul

13

44-52

Monterey

1994

20 Jul

13

42-60

Mendocino

2001

11 Sep

10

48-70

Monterey

2001

5 Sep

10

53-68

Mendocino

2002

13 Aug

12

47-66

Monterey

2002

18 Jul

13

45-58

Mendocino

2003

4 Sep

10

58-73

Monterey

2003

1 Aug

9

47-59

the timing of settlement, birth dates, and length of
the pelagic larval and juvenile stages of blue rockfish.
Upwelling indices and sea level anomalies were used to
evaluate the influence of oceanographic conditions on
the timing of recruitment (settlement) for blue rockfish
in the two regions.

Materials and methods

Juvenile blue rockfish were collected in two areas,
approximately 335 km apart — one off northern Califor-
nia in Mendocino County (39°14'N lat., 123°46'W long.)
and the other off central California along the southern
edge of Monterey Bay in Monterey County (36°38'N lat.,
121°55'W long.; Fig. 1). Each area is typified by large
kelp beds that extend from shore to approximately 20
m depth. The Mendocino site is dominated by bull kelp
( Nereocystis luetkeana) and the Monterey site by giant
kelp ( Macrocystis pyrifera). These kelp-bed areas com-
prise high-relief bedrock interspersed with low-relief
cobble and sand areas. Both beds are exposed to open
ocean conditions, although the Monterey site is slightly
buffered from southerly seas by the tip of the Monterey
Peninsula.

Fish were collected throughout the kelp beds by div-
ers using small spears at depths of 5-20 m and were
frozen for later analysis. Fish were collected during late
spring and summer at both sites during five noncon-
secutive years (1993, 1994, 2001-2003). Years for data
analysis were selected on the basis of three criteria:
1) there were at least nine individuals collected from
each area; 2) sampling dates at each study site in a
particular year were reasonably close (approximately
one month or less apart); and 3) samples were collected
after 1 June to allow for complete settlement of the
juveniles (Table 1).

39°N

i Mendocino

Pt. Arena

V

38°N -

\

San Francisco •

Pacific

Ocean

37°N

XX

50

.km

Monterey

-124°N

-1 23°N

-122°N

Figure 1

Map of the two study areas along the California coast.
Black stars indicate areas where samples of blue rockfish
(Sebastes mystinus) were collected for otolith analysis to
determine the timing of early life history events.

Otolith data

Sagittal otoliths were removed and ages were deter-
mined visually by counting growth increments with a
compound microscope at 1000 x magnification (Laidig
et al., 1991), beginning at the first increment after the
extrusion check (a mark in the otolith formed when the
larvae were released from their mother). No validation
of the rate of deposition of these growth increments was
performed during this study, and none was available
from the literature. However, based on validation studies
for other co-occurring rockfish species, such as shortbelly
rockfish (S. jordani [Laidig et al., 1991]), bocaccio (S.
paucispinis) , chilipepper ( S . goodei ), widow rockfish (S.
entomelas), and yellowtail rockfish (S. flavidus [Wood-
bury and Ralston, 1991]), increments were assumed to
be deposited daily. Also, the calculated birth dates of the
blue rockfish in this study occurred within the months of
larval release for this species (Wyllie-Echeverria, 1987).

The duration of the pelagic larval and juvenile stages,
age at settlement (the total duration of pelagic larval
and juvenile stages), settlement date, and birth date
were calculated by identifying specific marks in the
otolith that indicate transitions from one life stage to

444

Fishery Bulletin 108(4)

Postsettleinent

increments

Pelagic increments

Settlement

mark

Figure 2

Growth increments in the otolith of a blue rockfish ( Sebastes
mystinus). The settlement mark and increments produced before
(pelagic) and after (post) settlement are indicated.

the next. Transformation from the larval to
the juvenile stage was ascertained by the oc-
currence of secondary growth primordia (areas
of new increment growth that form away from
the otolith core; Laidig et ah, 1991). This trans-
formation occurs during the planktonic stage
before settlement. Duration of the pelagic juve-
nile stage was estimated as the number of in-
crements occurring from the secondary growth
primordia to the settlement mark. Settlement
date was calculated by subtracting the number
of increments formed after the settlement mark
from the collection date, and birth date was
determined by subtracting the total number
of increments in the otolith from the collection
date. The otolith increments deposited during
the pelagic juvenile stage followed a regular
pattern, increasing in width with fish age (Fig.

2). The settlement mark was the increment
where a change in the depositional pattern of
the increments was observed after the pelagic
juvenile stage; typically the increment mark-
ing settlement is narrower than the preceding
increments (Amdur, 1991). To be considered
the settlement mark, this change in increment
width had to be visible from the settlement
mark to the outer edge of the otolith and not
just in one section. Often the settlement mark
was evident in the otolith as a dark ring of
numerous closely spaced increments. After the settle-
ment mark, increment widths followed no consistent
growth pattern.

Oceanographic data

Upwelling data were derived from monthly sea level pres-
sure fields provided by the U.S. Navy Fleet Numerical
Meteorology and Oceanography Center (data acquired
from NMFS, Environmental Research Division, South-
west Fisheries Science Center at http://www.pfeg.
noaa.gov, accessed July 2009) measured off Mendocino
(39°11'N lat., 123°58'W long.) and Monterey (36°47'N
lat., 122°24,W long.), California. Sea level anomaly data
(adjusted for local atmospheric conditions) were collected
from shore stations at Humboldt Bay (40°46'N lat.,
124°13'W long.) and Monterey (36°36'N lat., 121°53'W
long.), California, and monthly means were obtained
from the University of Hawaii Sea Level Center. These
data represent a measure of change in sea level height
over time and reflect water movement a positive anom-
aly was associated with poleward flow and a negative
anomaly was associated with equatorward flow.

Two-way analysis of variance was used to test the
hypotheses that mean settlement date, mean birth date,
mean duration of pelagic larval and juvenile stages, and
mean settlement age did not differ significantly between
the two study areas. Principal components analysis
(PCA) was used to evaluate the relationship among the
otolith data (settlement date, birth date, and settlement
age) and the oceanographic variables (monthly average

upwelling and sea level anomalies for January-June)
for both areas. Canonical correlation analysis (CCA)
of the oceanographic and otolith data was used to ex-
amine the possible causes of changes in interannual
settlement dates.

Resuits

A total of 112 otoliths were examined (56 otoliths each
from Mendocino and Monterey; Table 1). Sampling dates
ranged from 2 June to 11 September each year, vary-
ing from 1 to 34 days between the two study areas in
a particular year. Fish sizes ranged from 37 to 73 mm
standard length (SL) for Mendocino and from 38 to 68
mm SL for Monterey.

Average birth dates varied annually, with a differ-
ence of 7-30 days between locations and an average of
19 days difference over all years (Fig. 3). Birth dates of
Mendocino rockfish were always later in the year than
those of rockfish from Monterey (significantly different
in 1994, 2001, and 2002; P< 0.05). Birth dates ranged
from 4 January to 25 March for Mendocino fish (7 Feb-
ruary average) and from 22 December to 9 March for
Monterey fish (19 January average).

Average settlement dates were significantly different
(PcO.001) each year between the two locations, with
fish from Mendocino always settling later in the year
than fish from Monterey (23 days average; Fig. 4). The
difference in settlement between the two sites varied
from an average of 17 to 29 days. The earliest date of

Laidig: Influence of ocean conditions on the timing of early life events for Sebastes mystinus

445

settlement was 17 May 1993 for fish
off Mendocino and 23 April (occurring
in both 2001 and 1993) for fish from
Monterey; the latest settlement date
was 1 July 2002 for fish off Mendocino
and 4 June 2002 for fish off Monterey.
Settlement dates were later in 2002
and 2003 and earlier in 1993 than in
the other years.

The duration of the larval and pe-
lagic juvenile stages was not signifi-
cantly different between the two areas
in any particular year (Figs. 5 and
6). The average duration for the lar-
val stage was 69 days (range = 41-100
d) for fish off Mendocino and 68 days
(range = 47-90 d) for fish off Mon-
terey. The average duration for the
pelagic juvenile stage was 56 days
(range=26-90 d) for fish off Mendoci-
no and 52 days (range = 14-81 d) for
fish off Monterey. Duration of pelagic
larval and juvenile stages generally
was longer for fish born in the 2000s
than for fish born in the 1990s. Fish
settled at younger ages at both study
sites in the 1990s than in the 2000s
(Fig. 7). Age at settlement was signifi-
cantly different (P<0.05) between the
two locations only in 2003; fish from
Mendocino settled at an older age than
those from Monterey.

From the PCA, 56% of the variabili-
ty in otolith data was explained by the
first eigenvector for fish off Mendocino
and Monterey. This vector was char-
acterized by the inverse relationship
of birth date and settlement age, i.e.,
the earlier the birth date, the older
the settlement age. The second eigen-
vector explained 41% and 39% of the
variability in otolith data for fish off
Mendocino and Monterey, respectively;
this vector was characterized by later
settlement dates and birth dates. The
first eigenvector for oceanographic
data explained 60% of the variability
from Mendocino and 61% of the vari-
ability in data from Monterey; this
vector was associated with the inverse
relationship of upwelling and sea level
during the months of March through
June off Mendocino and May and June
off Monterey. The second eigenvector
in the oceanographic data was related
to the inverse relationship between
upwelling and sea level in April at
both sites and explained 30% and 28%
of the variability in data from Men-
docino and Monterey, respectively.

ii

March

Q1 -j

19

February

09

20

January

♦ Mendocino
■ Monterey

1993

1994

#

2001

2002

2003

Year

Figure 3

Average birth dates (in calendar days), back-calculated from otolith data,
for blue rockfish ( Sebastes mystinus) from two study areas in California.
Black stars indicate significant differences (P<0.05) between study areas
for a particular year. Dashed lines represent the 5-year average for each
site. Vertical bars represent one standard error. Horizontal lines on the
y axis separate months.

29 i

19

♦ Mendocino
■ Monterey

June

09

30

20

May

10

*

*

★

*

*

1993 1994

2001

Year

★

*

★

*

I

2002 2003

Figure 4

Average settlement dates (in calendar days), back-calculated from oto-
lith data, for blue rockfish (Sebastes mystinus ) from two study areas in
California. Black stars indicate significant differences (PcO.001). Dashed
lines represent the 5-year average for each site. Vertical bars represent
one standard error. Horizontal lines on the y axis separate months.

446

Fishery Bulletin 108(4)

78

76

♦ Mendocino
b Monterey

CO

>

03

C

o

03

TJ

"a3

>

Q)

CD

2

0

>

<

74

72

70

68

66

64

62 -

60 -I t

1993 1994

♦

♦

a-

Year

2001

2002 2003

Figure 5

Average larval duration, calculated from otolith data, for blue rockfish
(Sebastes mystinus) from two study areas off California. Dashed lines
represent the 5-year average for each site. Vertical bars represent one
standard error.

75.0

70.0

65.0

60.0
55 0

50.0

45.0

40.0

35.0

30.0

♦ Mendocino
■ Monterey

1993

1994

2001

Year

2002

2003

Figure 6

Average pelagic juvenile duration, calculated from otolith data, for blue
rockfish ( Sebastes mystinus) from two study areas off California. Dashed
lines represent the 5-year average for each site. Vertical bars represent
one standard error.

Results from the CCA were similar
for data from both study areas (Fig. 8).
For Mendocino, settlement dates later
in the year (later than the average date
for a particular year) were positively
related to upwelling in February, May,
and June, and inversely related to sea
level anomalies in February, March,
and May. For Monterey, later settlement
dates were positively related to upwell-
ing in all months, except April, and neg-
atively related to sea level anomalies in
all months, except April. There was an
inverse relationship between birth date
and settlement age for both sites, where-
by an early birth date corresponded with
an older settlement age.

Discussion

The timing of settlement of blue rockfish
was related primarily to the timing of
birth. Blue rockfish off Mendocino that
settled on average three weeks later than
fish off Monterey also were born, on aver-
age, about three weeks later than fish
off Monterey. The age at settlement did
not differ significantly between sites, nor
did the duration of the larval or pelagic
juvenile stages. Pasten et al. (2003) also
attributed differences in settling date to
time of parturition because early settlers
of Sebastes inermis to seagrass beds in
Japan were born earlier than late-set-
tling fish. These researchers concluded
that there was an ideal size for settle-
ment and for active migration. Sogard
et al. (2008) studied the maternal effects
of rockfishes on their progeny and postu-
lated that factors influencing the time of
parturition also influenced recruitment
success. It must be noted that parturi-
tion dates for blue rockfish in the present
study were calculated from surviving
juveniles. Those juveniles that did not
survive may have been born at a differ-
ent time and therefore would change the
average parturition date (Woodbury and
Ralston, 1991; Yoklavich et al., 1996).
However, because no estimate of early
larval or juvenile mortality exists for
blue rockfish, I could not adjust for this
effect.

Time of spawning and parturition
of many fish species vary by latitude.
Parturition dates for numerous east-
ern Pacific rockfish species occur later
in northern study areas off Washington
and Alaska than in areas off California

Laidig: Influence of ocean conditions on the timing of early life events for Sebastes mystmus

447

145.0 i

140.0 -

« 135.0 H

E 130.0 -
®

a>

Z 125.0 -

to

(1)

D)

120.0 -

> 1 15.0 H

<

110.0 H

105.0

♦ Mendocino
■ Monterey

1993 1994

#

2001 2002

2003

Year

Figure 7

Average age at settlement, calculated from otolith data, for blue rockfish
( Sebastes mystinus) from two study areas off California. Black stars indicate
significant differences (P<0.05). Dashed lines represent the 5-year average
for each site. Vertical bars represent one standard error.

(Wyllie-Echeverria, 1987). Plaza et
al. (2004) determined that parturi-
tion of S. inermis occurred later in
the season at the more northerly sites
in the western Pacific and suggested
that this difference may be related
to environmental cues. Vinagre et al.

(2008a, 2008b) reported a latitudi-
nal gradient in time of spawning for
European sea bass (Dicentrarchus
labrax ) and common sole ( Solea solea)
off Portugal and that spawning onset
occurs earlier in the south. These re-
searchers suggested that warm wa-
ter temperatures in winter at lower
latitudes or differences in photoperiod
may influence the onset of spawning.

The latitudinal difference in the
timing of settlement and parturition
in blue rockfish could be an adap-
tation by blue rockfish to oceanic
conditions. Bograd et al. (2009) cal-
culated the spring transition index
(i.e., the beginning of the upwelling
season) and found that upwelling be-
gan on average 20 days earlier off
Monterey than off Mendocino. This
difference is similar to the 23-day
average difference in settlement
timing between these two areas. It
is possible that blue rockfish have
adapted to this difference in the timing of upwelling.

Interannual variability in parturition dates has been
noted by researchers, but specific causes for this vari-
ability are still unknown. Woodbury and Ralston (1991)
observed variations in the timing of parturition for five
species of rockfishes over six years. Early parturition
dates have been related to increased maternal age and
size for some rockfish species (Bobko and Berkeley,
2004; Plaza et al., 2004; Sogard et al., 2008). Plaza et
al. (2004) proposed that the time of parturition could be
influenced by effects of temperature on gestation times.
Carr (1991) suggested that upwelling may influence the
time of parturition. Interestingly, positive upwelling in
January and February in this study was correlated with
settlement date and this finding strengthens Carr’s
speculation.

Interannual variability in settlement date was re-
lated to upwelling and sea level height in this study.
Settlement occurred later in years when upwelling
was stronger and sea level anomaly was negative (i.e.,
there was an equatorward flow of cold water). Stron-
ger upwelling may have transported juvenile rockfish
farther offshore, making their return to the nearshore
more difficult and causing successful recruitment to
occur later in the season (Ainley et al., 1993; Larson
et al., 1994; Sakuma et al., 2006; Wilson et al., 2008).
Years with reduced or negative upwelling should re-
sult in onshore transport and thus earlier settlement
to nearshore areas. Cold water produced by upwelling

or flow from the north may result in slow growth of
juvenile rockfishes (Boehlert and Yoklavich, 1983).
These slow-growing individuals may migrate slowly
to the nearshore environment. If prey are plentiful,
the fish may remain in these food-rich waters longer
or, if the quality of the prey items was low, the fish
may exhibit reduced growth rates (Boldt and Rooper,
2009). Both of these factors could lead to later settle-
ment of individuals.

Large-scale oceanographic processes (covering
100s of kilometers) can be important in determin-
ing recruitment strength over a broad area. Field
and Ralston (2005) concluded that the synchrony in
year-to-year recruitment for three rockfish species
along the west coast of North America was caused
by large-scale ocean processes (i.e., El Nino and Pa-
cific Decadal Oscillation). Ralston and Howard (1995)
reported similar recruitment strengths in blue and
yellowtail rockfishes from two areas off California
over a 10-year period and suggested large-scale ocean
processes that affect sea surface temperatures (such
as El Nino) are primarily responsible for the recruit-
ment variation. Laidig et al. (2003) estimated simi-
lar ages and growth curves for adult blue rockfish
from Mendocino and Monterey, which indicated that
the fish from these areas are influenced by similar
oceanographic conditions.

Understanding the causal relationship of biologic
and oceanographic factors on recruitment dynam-

448

Fishery Bulletin 108(4)

ics has implications for fisheries management. For
instance, the design and placement of marine pro-
tected areas can be augmented to include areas where
juvenile rockfishes are recruited and grow, increas-
ing the likelihood of sustained production for those
rockfish species. Recruitment dynamics also need to
be considered when conducting surveys of rockfish
populations early in their life. These surveys can lead
to enhanced recruitment predictions for the fishery.
However, without information on the spatial and tem-
poral occurrence of recruitment, surveys could be
mistimed in a particular region and lead to biased
estimates. Results of the present study indicate that
coastwide recruitment surveys should be conducted

from south to north to allow for later spawning times
with increased latitude.

Acknowledgments

The work of all the divers who helped over the five
years, especially T. Chess, T. Hobson, D. Howard, D.
VenTresca, A. Ammann, and K. Baltz is greatly appreci-
ated. M. Yoklavich and D. Watters offered helpful sug-
gestions during this study. I also thank A. Ammann,
S. Lonhart, K. Sakuma, B. Wells, M. Yoklavich, and
three anonymous reviewers for their helpful comments
of this manuscript.

1

0.75
0.5
0.25
0

-0.25

c -0.5
o

t -0.75

8 -1.25 -1 -0.75 -0.5 -0.25 0 0.25 0.5 0 75 1 1.25

o

§ 1.25

T3
C

O -I

o 1

0)

CO

0.75
0.5
0.25
0

-0.25
-0.5
-0.75
-1

-1 -0.75 -0.5 -0 25 0 0.25 0.5 0 75 1 1.25

First canonical correlation

Figure 8

Comparison of first and second canonical correlation coefficients from oceano-
graphic and otolith data at Monterey and Mendocino study sites. For each
combined acronym, U=upwelling anomaly, L = sea level anomaly, and month
is indicated. BD=birth date; SA=settlement age; SD = settlement date.

Mendocino

_

:

BD

_

UApril

UJanuary

UMarch

UMay

SD

: LMaLr&?bruary
■ LMay LJanuary

LJune

— i 1 1 — i 1 r-~ i —

LApril

i 1 1

UFebruary

UJune

SA

~ i 1 1 i 1 1

Monterey

-

SA

-

UMarch

LMay UApril

LJune

uFeW»

SD

LMarch . ,

LFebruary

LJanuary

LApril UJanuary

i i i i i i i i i

BD

— i — i i — |— i i r i i

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Vinagre, C., T. Ferreira, L. Matos, M. J. Costa, and H. N. Cabral.

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Woodbury, D., and S. Ralston.

1991. Interannual variation in growth rates and back-
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Wyllie-Echeverria, T.

1987. Thirty-four species of California rockfishes:
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Yoklavich, M. M., V. J. Loeb, M. Nishimoto, B. Daly.

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94:766-782.

450

Abundance and distribution of Atlantic sturgeon

(Acipenser oxyrinchus ) within

the Northwest Atlantic Ocean,

determined from five fishery-independent surveys

Email address for contact author: kdunton@notes.cc.sunysb.edu

1 School of Marine and Atmospheric Sciences
Stony Brook University

Stony Brook, New York 11794-5000

2 New York State Department of Environmental Conservation
Division of Fish, Wildlife and Marine Resources

Bureau of Marine Resources
205 North Belle Mead Road, Suite 1
East Setauket, New York 11733

Abstract — A lack of knowledge of how
oceanic habitat is used by juvenile
marine migrant Atlantic sturgeon
(Acipenser oxyrinchus ) is hindering
conservation measures directed at
restoring severely depleted popula-
tions. Identifying the spatial distribu-
tion of Atlantic sturgeon is necessary
to identify critical habitat and appro-
priate management actions. We used
five fishery-independent surveys to
assess habitat use and movement
of Atlantic sturgeon during their
marine life stage. The size distribu-
tion ranged from 56 to 269 cm total
length (mean = 108 cm). Ninety-eight
percent of all Atlantic sturgeon were
smaller than 197 cm — a size that indi-
cated the majority were immature.
The pattern of habitat use revealed
concentration areas and potential
migration pathways used for north-
erly summer and southerly winter
migrations. Atlantic sturgeon were
largely confined to water depths less
than 20 m and aggregations tended
to occur at the mouths of large bays
(Chesapeake and Delaware bays) or
estuaries (Hudson and Kennebec
rivers) during the fall and spring
and to disperse throughout the Mid-
Atlantic Bight during the winter. In
most surveys depth, temperature, and
salinity were significantly related to
the distribution of Atlantic sturgeon.
Knowledge of their habitat and move-
ments can be used to devise spatially
based conservation plans to minimize
bycatch and to enhance population
recovery.

Manuscript submitted 11 September 2009.
Manuscript accepted 28 July 2010.

Fish. Bull. 108:450-465 (2010).

The views and opinions expressed
or implied in this article are those
of the author (or authors) and do not
necessarily reflect the position
of the National Marine Fisheries
Service, NOAA.

Keith J. Dunton (contact author)1

Adrian Jordaan1

Kim A. McKown2

David O. Conover1

Michael G. Frisk1

The Atlantic sturgeon ( Acipenser oxy-
rinchus) is a long-lived anadromous
fish with a historic range from Ham-
ilton Inlet on the coast of Labrador
to the Saint Johns River in Florida
(Smith and Clugston, 1997). A major
commercial fishery once existed
throughout the historic range and
estimated U.S. landings peaked at
3.3 million kg in 1890 (Smith and
Clugston, 1997). Unable to support
such intensive fishing, Atlantic stur-
geon populations collapsed throughout
the eastern seaboard by 1901 (Secor
et al., 2002). During the late 1900s,
there was a brief re-emergence of the
Atlantic sturgeon fishery in New York
and New Jersey (Kahnle et al., 2007)
and landings peaked at 125,000 kg in
the late 1980s (Waldman et al., 1996;
Bain et al., 2000). In 1990 the Atlan-
tic States Marine Fisheries Commis-
sion (ASMFC) developed a fishery
management plan for the conservation
and restoration of Atlantic sturgeon in
order to restore population levels that
would support harvests at 10% of the
historical peak landings (ASMFC1).
With a continued decline in the popu-
lation, a 1998 ASMFC amendment
began a 40-year moratorium in order

to protect 20 year classes of spawning
females (ASMFC2). Currently, Atlan-
tic sturgeon are a candidate species
to be listed under the United States
Endangered Species Act.

Atlantic sturgeon use river, estua-
rine, coastal, and oceanic environ-
ments at different life stages but
spend the majority of their lives in
saltwater (Smith and Clugston, 1997).
However, information on oceanic habi-
tat use is lacking beyond evidence of
broad-scale marine migrations and
an exchange of populations among
river systems based on tag recaptures
(Dovel and Berggren, 1983) and com-
mercial fisheries bycatch data (Stein
et al., 2004a, 2004b). Fisheries-de-
pendent data indicate that most At-

1 Atlantic States Marine Fisheries Com-
mission (ASMFC). 1990. Fishery man-
agement plan for Atlantic sturgeon.
Fishery management report number 17,
85 p. ASMFC, Washington, D.C.

2 Atlantic States Marine Fisheries Com-
mission (ASMFC). 1998. Amendment 1 to
the interstate fishery management plan
for Atlantic sturgeon, Fishery Manage-
ment report 31, 59 p. ASMFC, Washing-
ton, D.C.

Dunton et at: Abundance and distribution of Aapenser oxyrinchus within the Northwest Atlantic Ocean

451

75°0'W 70°0'W 65°0'W

Figure 1

Coverage area of the Maine-New Hampshire inshore bottom trawl
survey (ME-NH), Massachusetts Division of Marine Fisheries
bottom trawl survey (MADMF), New York bottom trawl survey
(NYBTS), New Jersey Department of Environmental Protec-
tion finfish survey (NJDEP), and the National Marine Fisheries
Service bottom trawl surveys (NMFS). The area covered by the
NMFS survey is represented by horizontal stripes. All other
surveys are represented by shades of gray.

lantic sturgeon inhabit shallow in-
shore areas of the continental shelf
(Stein et al., 2004a, 2004b). More re-
cently, some long-term fishery-inde-
pendent data have revealed that juve-
nile Atlantic sturgeon use the inshore
waters of North Carolina during the
winter months (Laney et al., 2007).

Additionally, there are a handful of
reported cases of Atlantic sturgeon
captured in deeper offshore areas (Ti-
moshkin, 1968; Collins and Smith,

1997; Stein et al., 2004a, 2004b).

Still, more information is needed to
guide management towards the best
mechanisms to protect the remaining
Atlantic sturgeon.

One contributing factor to the con-
tinued decline of Atlantic sturgeon
populations is incidental capture of
juveniles in non-target marine fish-
eries (Collins et al., 1996; Stein et
al., 2004a). Most of the current by-
catch mortality occurs in gill and
drift net fisheries (Stein et al.,

2004a; ASSRT3). Discard mortality
from trawl fisheries is hard to esti-
mate because few direct mortalities
are observed. Mortality however may be
very high due to delayed effects on cap-
tured individuals (Davis, 2002; Broadhurst
et al., 2006). Because Atlantic sturgeon do
not reach maturity until 12-14 years of age
and reproductive output increases later in
life (Van Eenennaam and Doroshov, 1998),
reducing mortality on juveniles is key to
restoring depleted populations (Boreman,

1997).

In order to adequately protect both juvenile and adult
Atlantic sturgeon, marine distributional patterns must
be identified such that essential habitat may be pro-
tected. In this article we use data from five different
oceanic fishery-independent surveys to reveal the sea-
sonal distribution, abundance, and habitat use of Atlan-
tic sturgeon along the Northwest Atlantic continental
shelf from Cape Hatteras, NC, to the Gulf of Maine
(GOM) (Fig. 1).

Materials and methods

We analyzed data from five fishery-independent sur-
veys conducted by the following agencies: 1) National

3 Atlantic Sturgeon Status Review Team (ASSRT). 2007. Status
review of Atlantic sturgeon ( Acipenser oxyrinchus oxyrin-
chus), 174 p. Report to National Marine Fisheries Service,
Northeast Regional Office, Gloucester, MA, 23 Feb 2007.
National Oceanic and Atmospheric Science Administration,
Washington D.C.

Marine Fisheries Service (NMFS); 2) New Jersey
Department of Environmental Protection (NJDEP);
3) Maine Department of Marine Resources and the
New Hampshire Fish and Game Department (ME-
NH); 4), Massachusetts Division of Marine Fisheries
(MADMF); and 5) New York Bottom Trawl Survey
(NYBTS) (Fig. 1). Catch per unit of effort (CPUE) was
calculated (number of fish per tow) for each survey and
depth (m). Depth (m), temperature (°C), and salinity
(ppt) data were obtained from the NMFS, NJDEP, and
NYBTS databases to estimate environmental prefer-
ences. For all surveys, except the MADMF, depth was
calculated as the average between the maximum and
minimum values. Depth values used in the MADMF
analysis are the depth at which the tow started. For
all surveys, tows were analyzed for each season, which
are defined as winter (21 Dec-20 Mar), spring (21
Mar-20 Jun), summer (21 Jun-20 Sept), and fall (21
Sep-20 Dec). Specifics of each survey are discussed
in detail below.

Because male and female Atlantic sturgeon mature
at different size ranges (van Eenennaam and Doroshov,

452

Fishery Bulletin 108(4)

1998) and because we could not distinguish between
gender, we applied female size at maturation to all
individuals. Female maturation is reached at a total
length of 197 cm (van Eenennaam and Doroshov, 1998).

NMFS bottom trawl survey

These surveys were conducted primarily by the research
vessels Albatross IV and Delaware II where a Yankee
36 bottom trawl with a 1.27-cm mesh liner was towed
for 30 minutes at 3.79 knots. Sampling was conducted
during the day and night (Sosebee and Cadrin4). A total
of 300-400 trawls were executed each season from the
Gulf of Maine to just south of Cape Hatteras, NC (Fig.
1). Sampling for the NMFS fall survey began in 1963
and the waters of southern New England and the Gulf
of Maine were sampled before tows were expanded to
include inshore stations in 1973. The NMFS survey was
further expanded to include spring samples in 1973. We
also used some additional NMFS surveys that were con-
ducted during the winters of 1964-66, 1972, 1978, 1981,
and 1992-2007, and summers of 1977-81 and 1993-95.

NJDEP finfish survey

The NJDEP finfish survey began in 1988 and is con-
ducted five times per year in April, June, August, Octo-
ber, and January. A total of 186 tows are conducted each
year (39 stations per trip for spring-fall months and 30
stations per trip for winter months). Sampling occurred
from NY Harbor to the entrance of Delaware Bay, DE,
from 8 to 30 m depth (Fig. 1). A depth-stratified random
sampling design was used and a minimum of 10 tows
were completed per depth interval (0-10 m, 10-20 m,
and 20-30 m). The survey was conducted with a three-
to-one two-seam trawl (25-m headrope, 30.5-m footrope)
with 12-cm stretched mesh forward netting that tapered
down to 8-cm stretched mesh rear netting that was lined
with a 6.4-mm mesh codend liner. Tows were conducted
at a speed of 3-3.5 knots for a duration of 20 minutes
during daylight hours.

ME-NH inshore bottom trawl survey

This survey began in fall of 2000 and primarily covered
the inshore waters of Maine and New Hampshire and
a depth range of 9-150 m and distance up to 19.3 km
offshore (in accordance with the 12-mile territorial limit)
(Fig. 1). A total of 115 trawls were attempted each fall
and spring. 100 stations were selected on the basis of
a depth-stratified, random sampling design and of the
100 stations, 15 were fixed location stations. For this

4 Sosebee, K. A., and S. X. Cadrin.

2006. A historical perspective on the abundance and biomass
of northeast demersal complex stocks from NMFS and Mas-
sachusetts inshore bottom trawl surveys, 1963—2002. NEFSC
Ref. Doc. 06-05, 200 p. Northeast Fisheries Science Center,
National Marine Fisheries Service, Woods Hole Laboratory,
166 Water St., Woods Hole, MA 02543.

survey a 57-70 modified shrimp trawl (17.37-m head
rope, 21.34-m footrope) was used with 5.08-cm stretched
mesh and a 2.54-cm stretched mesh liner in the codend.
Tows were conducted for 20 minutes at 2. 2-2. 3 knots
during daylight hours.

MADMF bottom trawl survey

Conducted during the spring and fall from 1978-2007,
this bottom trawl survey encompassed the Massachu-
setts inshore waters up to 5.6 km from the boundaries
of New Hampshire and Rhode Island (Fig. 1). A % size
North Atlantic two-seam otter trawl (head rope 11.9 m,
footrope 15.5 m) with a 6.4-mm lined codend was towed
at 2.5 knots for 20 min during daylight hours. The
survey sampled 100 stations per year selected using a
depth-stratified, random sampling design.

New York bottom trawl surveys (NYBTS)

The NY surveys consisted of two surveys — the New
York young-of-the-year bluefish survey and the NY trawl
survey for subadult Atlantic sturgeon. The sampling
area encompassed the waters inshore of a depth of 30
m; the practical inshore limit was 8-10 m from Montauk
Point to the entrance of NY Harbor (Fig. 1). For this
survey a depth-stratified sampling design was used with
strata based on the depth intervals 0-10 m, 10-20 m,
and 20-30 m. Tows were randomly selected by using
a random number generator and were conducted for a
duration of 20 minutes at a tow speed of 3-3.5 knots
during daylight hours. The net was a three-to-one two-
seam trawl (25-m headrope, 30.6-m footrope) with for-
ward netting of 12-cm stretched mesh tapering down
to the rear netting of 8-cm stretched mesh and lined
with a 6.0-mm mesh liner within the codend. Because
exactly the same gear was used for the surveys, they
were combined for the purpose of this analysis. Further
differences between the two surveys are described below.

The NY young-of-the-year bluefish survey was ini-
tially restricted to the 10- and 20-m depth strata where
10 tows per depth stratum were completed for a total of
20 tows per cruise. Sampling took place June-October
in 2005 and August-September in 2006. The survey
was confined to the 10-m depth strata in September,
October, and November of 2007 when 25, 24, and 27
tows were completed, respectively.

For the NY trawl survey for subadult Atlantic stur-
geon, a total of 10 cruises were conducted from Octo-
ber 2005 through June 2007 with 30 tows per cruise
distributed within the 10-, 20-, and 30-m depth strata.
Sampling months were October, November, January,
April, May, and June. A total of 10 tows were completed
for each depth. In June 2007, 36 tows were confined to
the 10-m depth stratum.

Spatial analysis

Atlantic sturgeon captures were mapped by season with
ESRI® ArcGIS™, vers. 9.2 software (ESRI; Redlands,

Dunton et al.: Abundance and distribution of Acipenser oxyrinchus within the Northwest Atlantic Ocean

453

CA). Map base layers were obtained from
the United States Geological Survey Coastal
and Marine Geology Program GIS catalogue.
Atlantic sturgeon captures were plotted by
using graduated symbols in the following
categories: 1, 2, 3—4, 5—10, 11-14, and >15
Atlantic sturgeon per tow.

Habitat preferences

We estimated the habitat preference of Atlan-
tic sturgeon by using the catch-weighted
methods of Perry and Smith (1994) for cor-
recting bias that arises in stratified sur-
veys where sampling effort differs between
strata. With this method, a comparison of
a catch-weighted cumulative distribution of
available (all habitat sampled) and occupied
(habitat where Atlantic sturgeon were cap-
tured) habitat was made and a randomization
routine was used to estimate whether the
occupied habitat was significantly different
from available habitat. Habitat variables
analyzed included temperature, dissolved
oxygen, and salinity.

The cumulative distribution function (cdf)
of the environmental variable was calculated
with the following function:

0.35
0.30 -

I

fe °'25 -

Q.

= 0.20 -

'o

<5

| 0.15 -

c

LU 0.10 -

Z3

CL

O

0.05 -

0.00 T 1 1 T 1 1 1 1 1

NYBTS NJDEP ME-NH NMFS MADMF

Figure 2

Catch per unit of effort (CPUE) for Atlantic sturgeon ( Acipenser
oxyrinchus) during the New York bottom trawl survey (NYBTS),
New Jersey Department of Environmental Protection finfish survey
(NJDEP), Maine-New Hampshire inshore bottom trawl survey
(ME-NH), National Marine Fisheries Service bottom trawl surveys
(NMFS), and Massachusetts Division of Marine Fisheries bottom
trawl survey (MADMF).

, w

f(t)= X H—KXhO’ (1)

h , nh

where W,

n.

the proportion of the survey in stratum /z;
the number of tows in stratum h ;
the habitat variable in tow i and stratum
h; and

an indicator function where

| 1, if Hi^t

0, otherwise

(2)

The following function relates the catch weighted cdf
to the habitat variable:

*<*>=XX

nh yst

I(xlu),

(3)

Significance is determined by randomizing for 1000
trials the pairings of xhl and ( Wh/nh ) (yhi- yst)!yst ) and
by dividing the number of trials that are greater than
the test statistic by the total number of trials.

Results

The NYBTS had the highest CPUE (0.291 fish/tow),
followed by the NJDEP finfish survey (0.072 fish/tow),
ME-NH inshore bottom trawl survey (0.024 fish/tow),
NMFS bottom trawl survey (0.004 fish/tow), and the
MADMF bottom trawl survey (<0.001fish/tow), in the
latter of which only one Atlantic sturgeon has ever been
captured (Table 1; Fig. 2). The details of the CPUE by
depth (Fig. 3) and seasonal distribution and abundance
(Fig. 4-7) for each survey are reported in detail below.
Total length of Atlantic sturgeon captured within the
surveys ranged from 56 to 269 cm (mean=108 cm) (Table
2; Fig. 8).

where yhi = the number of fish captured in tow i in
stratum h ; and

yst = the stratified mean abundance.

The strength of the association is measured by the dif-
ference between the available and occupied cdf:

c|g(U-/'(U| =

max

XX—

h i nh

f — \

y -y ,

hi st

V st J

(4)

NMFS bottom trawl survey

A total of 107 Atlantic sturgeon were captured in 27,420
bottom trawls (Table 1). The depth distribution of com-
pleted tows ranged from 5 to 542 m deep, and 5214 peak
tows occurred between 20 and 40 m (Fig. 3A). CPUE of
Atlantic sturgeon was highest for the 10 -m depth stra-
tum (0.0273/tow) and decreased with each depth interval
(Fig. 3A). A total of 71.30% of the Atlantic sturgeon
were captured in 20 m or less and no individuals were
captured in water deeper than 30 m (Fig. 3A). Atlantic

454

Fishery Bulletin 108(4)

Table t

Summary of the surveys effort and Atlantic sturgeon ( Acipenser oxyrinchus ) captures for the New York bottom trawl survey
(NYBTS), New Jersey Department of Environmental Protection (NJDEP) finfish survey, National Marine Fisheries Service
(NMFS) bottom trawl survey, Maine Department of Marine Resources and New Hampshire Fish and Game (ME-NH) inshore
trawl survey, and Massachusetts Division of Marine Fisheries (MADMF) bottom trawl survey. Seasons are defined as winter (21
Dec-20 Mar), spring (21 Mar-20 Jun), summer (21 Jun-20 Sep), and fall (21 Sep-20 Dec).

Survey

Time period

Total number of
trawls completed

Total number of
Atlantic sturgeon captured

Catch per unit of effort

NYBTS

2005-07

512

149

0.291

fall

132

46

0.348

winter

59

4

0.068

spring

219

73

0.333

summer

102

26

0.255

NJDEP

1988-2007

3617

261

0.072

fall

769

74

0.096

winter

599

74

0.124

spring

1439

113

0.079

summer

810

0

0.000

NMFS

1973-2007

27,420

107

0.004

fall

11,919

26

0.002

winter

2563

12

0.005

spring

11,395

68

0.006

summer

1543

1

0.001

ME-NH

2000-06

1601

38

0.024

fall

773

31

0.040

spring

828

7

0.008

MADMF

1978-2007

5563

1

>0.001

spring

2874

1

>0.001

fall

2689

0

>0.001

Table 2

Mean, standard deviation, and range of total length (cm)
of Atlantic sturgeon ( Acipenser oxyrinchus ) captured in
the New York bottom trawl survey (NYBTS), New Jersey
Department of Environmental Protection (NJDEP) fin-
fish survey. National Marine Fisheries Service (NMFS)
bottom trawl survey, Maine Department of Marine
Resources and New Hampshire Fish and Game (ME-
NH) inshore trawl survey, and Massachusetts Division of
Marine Fisheries (MADMF) bottom trawl survey. Length
information includes all recorded lengths over the dura-
tion of the entire period of the above surveys.

Mean total
length ±standard

Survey deviation (cm) Range (cm)

NYBTS

112.01 ±27.75

72-215

NJDEP

103.89 ±32.13

52-248

NMFS

113.87 ±40.18

51-269

ME-NH

115.4 ±19.39

76-152

MADMF

78 ±0

—

sturgeon were captured during all seasons but were most
abundant during the spring, with an average CPUE of
0.006 fish/tow, followed by winter (0.005 fish/tow), fall
(0.002 fish/tow), and summer (0.001 fish/tow) (Table 1).

In the spring, 70.59% of Atlantic sturgeon were cap-
tured in Virginia (VA) and NC waters and 23.53% were
captured in NY and NJ. One Atlantic sturgeon was
captured south of Cape Hatteras and one was captured
offshore of northern MA. During winter months cap-
tures were evenly distributed from NJ to NC. A total
of 42.30% (11 fish) of fall captures occurred off Long
Island, NY, whereas 30.76% (8 fish) occurred in the
mouth of Delaware Bay, Delaware (DE). In addition
three fish were captured in NJ, one fish south of Cape
Hatteras, and one fish near Cape Cod, MA. Only one
Atlantic sturgeon was captured during this survey in
the summer months in NY waters off of Long Island.

NJDEP finfish survey

A total of 261 Atlantic sturgeon were captured within
3617 bottom trawls from 1988 through 2007 (Table 1) at
all depths sampled (Fig. 3B). Tow distribution ranged

Dunton et al.: Abundance and distribution of Acipenser oxyrinchus within the Northwest Atlantic Ocean

455

0.030

0.025

0.020

0.015

0.010

0.005

0.000

A (NMFS)

0.160

B (NIDEP) 0160

<

0.140

0.140

0.120

0.120

0.100

0.100

0.080

0.080

0.060

0.060

0.040

0.040

0.020

, 0.020

.-11 , , , , ,

- — . 0.000

— . — . — . — . — , — - — < o.ooo

0 50 1 00 1 50 200 250 300 350 400

0 50 100 150 200 250 300 350 400

(ME-NH)

.il.n.

0 50 1 00 1 50 200 250 300 350 400

Depth

>.

o

c

<D

c r
<D

0.0030

0.0025

0.0020

0.0015

0.0010

0.0005

0.0000

D (MADMF)

0 50 100 150 200 250 300 350 400

1.60 ~|
1.40 -
1.20 -
1.00 -
0.80 -
0.60 -
0.40 -
0.20 -
0.00 -

E (NYBTS)

50 100 150 200 250 300 350 400

Depth

Figure 3

Catch per unit of effort (CPUE) for Atlantic sturgeon ( Acipenser oxyrinchus) and frequency of tows conducted by depth
for the (A) National Marine Fisheries Service bottom trawl surveys (NMFS), (B) Maine-New Hampshire inshore bottom
trawl survey (ME-NH), (C) New Jersey Department of Environmental Protection finfish survey (NJDEP), (D) New York
bottom trawl survey (NYBTS), and (E) Massachusetts Division of Marine Fisheries bottom trawl survey (MADMF).

from 5 to 30 m and the majority of the tows occurred
within the 10-25 m range (Fig 3B). CPUE was highest
for the 10-15 m depth range (0.134 fish/tow) and lowest
for 20-30 m range (0.005 fish/tow) (Fig. 3B). A total of
94.78% of all captures occurred in depths less than 20
m (Fig. 3B). CPUE was highest for the winter months
(0.124 fish/tow) followed by fall (0.096 fish/tow) and
spring (0.079 fish/tow) (Table 1). No Atlantic sturgeon

were captured during the summer months (Table 1).
During the winter, 74 Atlantic sturgeon were captured
of which 67 were captured off northern NJ and of that
number, 59 were taken within a small area outside
Sandy Hook, NJ. Three fish were captured at 0—20 m
depth outside of Delaware Bay, DE. During the fall
season, 74 Atlantic sturgeon were captured of which 92%
(68 fish) were taken north of Little Egg Inlet, NJ. Of

456

Fishery Bulletin 108(4)

76°0'W

72°0'W

42°0'N

38°0'N -

- 42°0'N

0 50 100 200 km

1 i i i I

1 A

m

2

®

3-4

•

5- 10

•

11-14

2S_

>15

38°0'N

76°0'W

72°0'W

Figure 4

Number of captures of Atlantic sturgeon ( Acipenser oxyrinchus ) from all
surveys during spring months. Circle size corresponds to total number
of Atlantic sturgeon captured at a given location (insert A). Locations
of all tows can be seen in insert B.

the total Atlantic sturgeon captured, 64% (48 fish) were
captured off northern NJ. Captures within the spring
occurred along the entire coast of NJ and 44.2% of the
captures occurred in Sandy Hook, NJ.

ME-NH inshore bottom trawl survey

A total of 38 Atlantic sturgeon were captured in a total
of 1601 bottom trawls from 2001 through 2006 (Table
1). Sampling depths ranged from 10 to 200 m, and three
defined peaks in sampling effort occurred at 30 m, 65 m,
and 90 m (Fig. 3C). All Atlantic sturgeon were captured
between 15 and 90 m depth (Fig. 30 and 36 of the 38
Atlantic sturgeon were captured near the Kennebec
estuarine complex (Fig. 9A). Two additional Atlantic
sturgeon were captured south of the Kennebec River,
closer to the Saco River.

MADMF bottom trawl survey

Only one Atlantic sturgeon was captured in a total of
5563 bottom trawls (Table 1). Sampling depths ranged
from 4 to 86 m, and a peak in sampling effort occurred
at a depth of 20 m (Fig. 3D). The only Atlantic sturgeon

captured was collected during the spring at a depth of
41 m.

NYBTS

A total of 149 Atlantic sturgeon were captured in 512
random stratified tows (Table 1). Sampling depths ranged
from 5 to 35 m and a peak in sampling effort occurred
at a depth of 15 m (Fig. 3E). Atlantic sturgeon were cap-
tured within all months sampled; however, no Atlantic
sturgeon were captured deeper than 20 m. A total of 85%
of all Atlantic sturgeon were captured between 5 and 10
m with a mean CPUE of 1.34 (Fig. 3E). CPUE was high-
est during the fall (0.35 fish/tow) followed by spring (0.33
fish/tow) and summer (0.26 fish/tow) and was lowest
during the winter (0.07 fish/tow) (Table 1). Of the 149
Atlantic sturgeon captured, 51% were collected off the
western coast of Long Island, 30% were captured off cen-
tral Long Island, and only one was captured off the east
end of Long Island. During the spring, Atlantic sturgeon
were captured along the entire coast of Long Island,
NY, but 57% were captured off western Long Island,
specifically Rockaway, NY. The Rockaway region was
also an important area during the fall, accounting for

Dunton et al.: Abundance and distribution of Acipenser oxyrinchus within the Northwest Atlantic Ocean

457

76°0 W 72°0'W

Figure 5

Number of captures of Atlantic sturgeon ( Acipenser oxyrinchus) from all
surveys during winter months. Circle size corresponds to total number
of Atlantic sturgeon captured at a given location (insert A). Locations
of all tows can be seen in insert B.

70% of the catches occurring within this region. Twenty-
six Atlantic sturgeon were captured in the summer
months; 99% were captured in western-central Long
Island, NY, and only one was captured along the east
end of Long Island. During the winter, all Atlantic stur-
geon were captured off the western end of Long Island.

Habitat preferences

Hydrographic variables and distributions of Atlantic
sturgeon were compared only for the NMFS bottom
trawl survey, NJDEP finfish survey, and for NYBTS
for the spring and fall seasons because these contained
sufficient Atlantic sturgeon capture data to perform
the analyses. The depths (habitat) occupied by Atlantic
sturgeon was significantly different from the available
depths in the NMFS survey and NYBTS for both the
spring and fall surveys and the NJDEP spring survey
(Tables 3 and 4). Atlantic sturgeon occupied areas
with significantly different temperatures compared to
available habitat in the NYBTS spring and NMFS fall
survey, as well as areas of significantly different salini-
ties in the NMFS fall and spring surveys and NJDEP
spring survey (Table 3). Survey-specific cumulative
distribution functions for available and occupied habits

Table 3

P-values from the analysis of habitat preference of Atlan-
tic sturgeon (Acipenser oxyrinchus ) by season in the
northwestern Atlantic Ocean. The fish were captured in
the National Marine Fisheries Service (NMFS) bottom
trawl survey, New Jersey Department of Environmental
Protection (NJDEP) finfish survey, and New York bottom
trawl survey (NYBTS). Bold font indicates a significant
difference (P<0.01) between Atlantic sturgeon habitat
preference and the available habitat.

Season

Survey

Depth

Temperature

Salinity

fall

NMFS

<0.005

<0.005

<0.005

fall

NJDEP

0.129

0.173

0.273

fall

NYBTS

<0.005

0.518

0.530

spring

NMFS

<0.005

0.355

0.001

spring

NJDEP

<0.005

0.173

<0.005

spring

NYBTS

<0.005

0.001

0.084

with depth, salinity, and temperature profiles are shown
in Figure 10 and median values and 95% confidence
intervals are listed in Table 4. Where significant differ-

458

Fishery Bulletin 108(4)

76°0'W

72°0'W

42°0'N

38°0'N -

-42°0'N

- 38°0'N

76°0'W

72°0'W

Figure 6

Number of captures of Atlantic sturgeon ( Acipenser oxyrinchus) from all
surveys during fall months. Circle size corresponds to total number of
Atlantic sturgeon captured at a given location (insert A). Locations of
all tows can be seen in insert B.

ences in depth occurred, Atlantic sturgeon were always
found in shallower water than in potentially available
habitat (Table 4, Fig. 10). Salinities of occupied areas
were less than those of available habitat in all surveys,
although only the NMFS fall and spring survey and
NJDEP spring survey had significant differences (Table
4, Fig. 10). In two circumstances the temperature of
occupied habitat was significantly warmer than that
of available habitat, whereas temperature for the other
seasons and surveys showed no trend (Table 4, Fig. 10).

Discussion

A majority of the Atlantic sturgeon captured along the
continental shelf from ME to NC were juveniles aggre-
gating in specific locations around the mouths of estua-
rine complexes and along narrow dispersal corridors in
shallow water (<20 m) from Cape Hatteras (NC) to the
southern tip of Long Island (NY). The highest catches
occurred within the NY Bight in water 10-15 m deep,
particularly during the spring and fall. Few sturgeon
were captured north of MA. Little work has been done
to describe the marine habitat distribution and habi-
tat preference of Atlantic sturgeon, but similar coast-

wide, shallow (with respect to regional bathymetry)
marine distributions have been shown for green stur-
geon ( Acipenser medirostris) (Erickson and Hightower,
2007) and Gulf sturgeon ( Acipenser oxyrinchus desotoi)
(Edwards et al., 2007; Ross et al., 2009). The shallow,
coast-wide habitat identified within this study is also
consistent with Atlantic sturgeon bycatch data (Stein
et al., 2004a, 2004b). Our comprehensive analysis of
a coast-wide collection of surveys revealed the area
between the NY Bight to VA as a region of overwinter-
ing habitat for juvenile Atlantic sturgeon. This finding
agrees with that of Laney et al. (2007), who found the
coastal waters off NC and VA to be important overwin-
tering habitat for Atlantic sturgeon. Atlantic sturgeon
that originated from the Hudson River represented
43.5% of those in the NC overwintering habitat (Laney
et al., 2007) a percentage that agrees with Dovel and
Berggren’s (1983) tagging data that revealed a south-
erly movement of Atlantic sturgeon from the Hudson
River. In addition to Laney et al. (2007), there have
been further reports of Atlantic sturgeon in marine
waters off the coast of South Carolina during winter
months (Collins and Smith, 1997). The identification of
the NY Bight as an important overwintering area has
not been widely reported; therefore determining the

Dunton et al.: Abundance and distribution of Acipenser oxynnchus within the Northwest Atlantic Ocean

459

76°0'W 72°0'W

Figure 7

Number of captures of Atlantic sturgeon ( Acipenser oxyrinchus ) from all
surveys during summer months. Circle size corresponds to total number
of Atlantic sturgeon captured at a given location (insert A). Locations of
all tows can be seen in insert B.

genetic makeup of the sturgeon in this area
would add important information on Atlantic
sturgeon demographics and movements.

Atlantic sturgeon had a coast-wide distribu-
tion during the spring and fall, and southerly
and centrally located distributions during
the winter and summer, respectively. These
results corroborate tagging data that indi-
cate that Atlantic sturgeon undergo large-
scale southerly fall migrations and north-
erly spring migrations (Dovel and Berggren,
1983). Catches varied by season, but were
greatest during the fall and spring months.
Because of the strong seasonal movements
of Atlantic sturgeon, the timing of surveys
is critical for observing movement patterns.

Interaction of Atlantic sturgeon abundance
with temporal and spatial variability in
sampling effort

Some of the variation in distribution and
abundance of Atlantic sturgeon can be
explained by temporal and spatial differ-

Total length (cm)

Figure 8

Total length distribution for Atlantic sturgeon (Acipenser oxyrin-
chus) captured in all surveys combined.

460

Fishery Bulletin 108(4)

ences in sampling effort. Stein et al.

(2004a) reported that MA ports have one
of the highest cumulative catches of Atlan-
tic sturgeon. This high rate contrasts
with that for the MADMF bottom trawl
survey, during which virtually no Atlantic
sturgeon were captured. The discrepancy
between reports of Atlantic sturgeon in
MA waters likely comes from the timing of
sampling. Stein et al. (2004a) showed the
highest bycatch rates in June and Novem-
ber for bottom trawl fisheries, whereas the
MADMF survey took place during May
and September. Any aggregations and
dispersal of Atlantic sturgeon within MA
marine waters may occur at spatial and
temporal scales that are missed by the
survey. The absence of Atlantic sturgeon
during the MADMF survey does, however,
indicate lower abundance within the area
surveyed during comparable time frames
because Atlantic sturgeon are captured
at relatively high rates by other surveys
during this period. More work should be
done to monitor Atlantic sturgeon habitat
during other months not typically sampled
by the MADMF survey because it is pos-
sible that Atlantic sturgeon are present in
higher concentrations during months that
are not routinely sampled.

The NMFS survey missed critical ar-
eas for Atlantic sturgeon because inshore
areas in certain regions could not be
sampled. Such areas include important
overwintering habitat identified within
this study in NY waters and by Laney et
al. (2007) in VA and NC waters, in addi-
tion to critical habitat within the GOM.

The ME-NH inshore bottom trawl survey
was used to identify the Kennebec es-
tuarine complex as an important concentration
area for Atlantic sturgeon within the GOM re-
gion because shallower areas are sampled with
this survey. During additional inshore surveys,
such as the Northeast Fisheries Sciences Center
(NEFSC) industry-based surveys for cod ( Gadus
morhua) and yellowtail ( Limanda ferruginea),
Atlantic sturgeon have been captured between
the Saco and Kennebec rivers in fall, winter,
and spring (Fig. 9A; W. Kramer, personal com-
mun.5). Stein et al. (2004a, 2004b) also showed
that Atlantic sturgeon are captured as bycatch
within this region in sink gillnets. The depth
distribution of Atlantic sturgeon within the
GOM was deeper than that for the other coast-wide
captures, but similar to those reported for green

70°20'W

70°0'W

69°40'W

74°0'W

73°50'W

73°40'W

5 Kramer, William. 2009. NOAA Fisheries Service, Ecosystems
Survey Branch, 166 Water St., Woodshole, MA 02543.

Figure 9

Number of captures of Atlantic sturgeon ( Acipenser oxyrin-
clius) determined from (A) the Gulf of Maine from the Maine-
New Hampshire bottom trawl surveys (gray circles) and
from the Northeast Fisheries Science Center industry-based
surveys for cod (Gadus morhua) and yellowtail (Limanda
ferruginea) (black circles) and (B) Sandy Hook, NJ and
Rockaway NY, including all captures from the National
Marine Fisheries Service bottom trawl survey. New Jersey
Department of Environmental Protection finfish survey,
and New York bottom trawl survey. Dotted lines in both
panels represent suggested closed areas for habitat protec-
tion. Note different scales in figure.

sturgeon (Erickson and Hightower, 2007) in that both
species occupied areas of shallow depth in relation to
the bathymetric characteristics of the region. There
has not been sufficient inshore trawling conducted
during the winter and summer to validate whether
the GOM is important year-round habitat.

Dunton et al.: Abundance and distribution of Acipenser oxyrinchus within the Northwest Atlantic Ocean

461

Table 4

Median and 95% confidence intervals for available and occupied habitat of Atlantic sturgeon (Acipenser' oxyrinchus ) for depth,
temperature, and salinity for the fall and spring National Marine Fisheries Service bottom trawl survey (NMFS), New Jersey
Department of Environmental Protection finfish survey (NJDEP), and New York bottom trawl survey (NYBTS) where “available
habitat” represents all habitat sampled and “occupied habitat” represents habitat where Atlantic sturgeon were captured.

Season Parameter Survey

Median

95% confidence interval

Fall Depth (m) NMFS available habitat

76.0

15.5-260.5

NMFS occupied habitat

18.0

10.0-25.0

NJDEP available habitat

19.0

8.0-27.0

NJDEP occupied habitat

16.0

7.0-22.0

NYBTS available habitat

23.8

9.5-30.3

NYBTS occupied habitat

10.7

9.0-17.0

Temperature (°C) NMFS available habitat

10.6

5.9-22.5

NMFS occupied habitat

18.9

13.3-23.3

NJDEP available habitat

15.8

12.3-18.6

NJDEP occupied habitat

14.8

13.3-17.6

NYBTS available habitat

15.3

13.5-19.3

NYBTS occupied habitat

16.8

13.6-19.9

Salinity (ppt) NMFS available habitat

33.1

31.0-35.4

NMFS occupied habitat

31.6

29.3-32.0

NJDEP available habitat

32.0

29.6-33.5

NJDEP occupied habitat

31.5

29.5-33.1

NYBTS available habitat

31.4

30.1-32.9

NYBTS occupied habitat

31.3

29.4-31.8

Spring Depth (m) NMFS available habitat

76.0

16.0-259.0

NMFS occupied habitat

18.0

8.0-27.0

NJDEP available habitat

19.0

7.5-27.0

NJDEP occupied habitat

12.0

7.0-18.0

NYBTS available habitat

22.4

9.9-29.7

NYBTS occupied habitat

9.9

9.9-13.9

Temperature (°C) NMFS available habitat

6.0

3.4-12.5

NMFS occupied habitat

6.4

3.2-15.0

NJDEP available habitat

9.1

4.9-18.8

NJDEP occupied habitat

11.0

5.7-19.0

NYBTS available habitat

9.4

5.1-14.6

NYBTS occupied habitat

11.1

5.7-13.9

Salinity (ppt) NMFS available habitat

33.2

31.4-35.4

NMFS occupied habitat

32.0

27.0-32.8

NJDEP available habitat

32.0

30.0-34.0

NJDEP occupied habitat

30.0

28.8-35.0

NYBTS available habitat

31.6

30.2-33.1

NYBTS occupied habitat

30.9

29.9-32.3

Although the NMFS survey covered the entire conti-
nental shelf, no fish were captured deeper than 30 m.
However, Atlantic sturgeon of unknown size have been
captured in deeper waters (>100 m) on the continental
shelf as bycatch in gillnet fisheries (Stein et al. 2004b;
ASMFC6). Additionally, there have only been two re-
corded trawl captures of an Atlantic sturgeon in deep
waters; one mature Atlantic sturgeon (225 cm) was cap-
tured in the Hudson canyon in water 110 m deep off NY
and NJ and another was captured in Wilmington Can-

yon, 113 km southeast of Atlantic City, NJ (Timoshkin,
1968). The lack of trawl-caught fish on the continental
shelf may be a result of either a gap in timing of the
sampling and Atlantic sturgeon migrations on or off
the shelf, a function of gear selectivity towards smaller

6 ASMFC (Atlantic States Marine Fisheries Commission). 2007.
Estimation of Atlantic sturgeon bycatch in coastal Atlantic
commercial fisheries of New England and the Mid-Atlantic,
95 p. ASMFC, Washington D.C.

462

Fishery Bulletin 108(4)

A (NMFS)

B (NJDEP) C (NYBTS)

Depth (m)

Figure 10

Cumulative distribution functions for available habitat and habitat occupied by Atlantic stur-
geon ( Acipenser oxyrinchus) in the fall and spring surveys for (A) National Marine Fisheries
Service bottom trawl surveys (NMFS), (B) New Jersey Department of Environmental Protection
finfish survey (NJDEP), and (C) New York bottom trawl survey (NYBTS) for depth (m), salinity
(ppt), and temperature (°C). Solid lines indicate habitat occupied by A. oxyrinchus (gray=fall;
black=spring) and dashed lines indicate available habitat (dashed gray=fall; dashed black= spring).

fish, or simply a scarcity of Atlantic sturgeon. Either a
substantial increase in trawl survey effort or the use
of different gears, such as gillnets, may be required in
order to capture Atlantic sturgeon along the shelf.

Essential fish habitat

The Magnuson-Stevens Fishery Conservation and Man-
agement Act requires identification of Essential Fish
Habitat (EFH), defined as waters or substrate used
for spawning, breeding, feeding or growth to maturity,
in order to minimize adverse effects of fishing and to
promote conservation and enhancement of such habitat
for particular species. Unfortunately, EFH can only
be defined for federally managed species and does not

include species such as Atlantic sturgeon which are
managed by regional fishery management councils.
Atlantic sturgeon is a current candidate species for
listing under the US Endangered Species Act, and if
listed, the identification of critical habitat necessary to
recover the species will be required. The identification
of critical habitat for listed species is mandatory and
is defined as all areas essential to the conservation
of the species. Without EFH or critical habitat desig-
nation, habitat degradation and incidental mortality
within critical areas will continue to hinder population
recovery.

Our analysis of habitat preferences indicated that
depth was the primary environmental characteristic
defining the Atlantic sturgeon distribution. Thus, es-

Dunton et al.: Abundance and distribution of Acipenser oxyrmchus within the Northwest Atlantic Ocean

463

sential habitat for juvenile marine migrant Atlantic
sturgeon can broadly be defined as coastal waters <20
m depth, and it is concentrated in areas adjacent to es-
tuaries such as the Hudson River-NY Bight, Delaware
Bay, Chesapeake Bay, Cape Hatteras, and Kennebec
River. This narrow band of shallow water appears to
represent an important habitat corridor and potential
migration path. There are likely additional hotspots
along the migration corridor, but greater temporal and
spatial sampling effort is required to identify them.
Other authors have reported concentrations of Atlantic
sturgeon in Long Island Sound (Bain et al., 2000; Savoy
and Pacileo, 2003) and NC (Laney et al., 2007), and
Stein et al. (2004a) reported several concentrations of
Atlantic sturgeon in Massachusetts Bay, RI, NJ, and
DE. However, Stein et al. (2004a) used bycatch data in
areas where captures were lowest during the summer
months while the fishing rates were highest. However,
this change in fishing effort may influence the observed
distributions.

The reason(s) for aggregations of Atlantic sturgeon
migrants are not understood, nor are their movements
to and from aggregation areas. Concentrations identified
by Stein et al. (2004b) led the authors to suggest that
temperature, bathymetry, geomorphic formations, food
habits, and the sampling gear type used may contrib-
ute to observed movements and aggregation of Atlantic
sturgeon. Complex water circulation patterns are also
a potential reason for observed concentrations of At-
lantic sturgeon (Wilk and Silverman, 1976; Savoy and
Pacileo, 2003). Hatin et al. (2002) found that Atlantic
sturgeon concentrated within the St. Lawrence estu-
ary had large numbers of nematodes and oligochaetes
within their stomachs, which would indicate that these
habitats are feeding areas. Known seasonal migra-
tions often involve energetic demands related to food
availability, environmental factors, and reproductive
activity (Roff, 2002). Because the majority of captures
are juveniles, reproductive activity is not a likely cause
for movement, although causal mechanisms influencing
traits under selection are difficult to identify because
life-history stages are often linked through long-term
fitness (Taborsky, 2006). We hypothesize that migra-
tions are depth restricted and aggregations are related
to food availability, and that seasonal cues, temperature
in particular, drive movement.

Current and future management of Atlantic sturgeon

Current knowledge indicates that the majority of Atlan-
tic sturgeon populations have been extirpated and that
the Hudson River stock is one of the largest remaining
populations (Waldman et al., 1996; van Eenennaam et
al., 1998; Savoy and Pacileo, 2002; Secor et al., 2002).
Three fishery management tools commonly used to help
restore depleted populations are 1) minimum size limits,
2) temporary closures of the fishery, and 3) marine
reserves (Nowlis, 2000). Management of Atlantic stur-
geon has been accomplished by minimum size limits
since the early 1990s, followed directly by a 40-year

complete closure of the fishery beginning in 1998. Cur-
rently, after 10 years of the fishery closure, recruitment
within the Hudson River still remains at historic lows
(Kahnle et al., 2007).

Because previous Atlantic sturgeon management has
not resulted in significant improvements to popula-
tions, recovery efforts should now focus on establish-
ing marine reserves or implementing area closures
to protect essential habitat and to reduce fishing
mortality on juveniles (Collins et al., 2000). Specifi-
cally, Sandy Hook (NJ), Rockaway (NY), and Ken-
nebec (ME), which are hotspots of Atlantic sturgeon
captures, as identified by this study, should be pro-
tected. Although sturgeon are not as abundant in the
Kennebec region in ME as in NY and NJ waters, this
region represents a unique hotspot. It is of particular
importance because Atlantic sturgeon captured in ME
river systems have been shown to represent a separate
discrete population segment (Grunwald et al., 2008).
The genetic origins of the Atlantic sturgeon captured
within marine waters of ME are unknown, but they
are likely to originate from multiple stocks. Because
of the proximity of ME river systems, it is probable
that the majority of these Atlantic sturgeon are part of
this discrete population segment. If our recommended
habitat protection were to occur, the total amount of
closed area within these locations would be relatively
small — totaling 85.47 km2 within NJ (Fig. 9A), 106.19
km2 within NY (Fig. 9A), and 209.79 km2 within ME
(Fig. 9B). In addition, although Atlantic sturgeon are
highly migratory, primary juvenile habitat and migra-
tions are limited to narrow corridors in waters less
than 20 m deep. The presence of Atlantic sturgeon in
such narrow bands of water indicates a seasonal or
permanent closure to gillnet and trawl fisheries could
be successful. By focusing immediate efforts on the
protection of these hotspots and corridor pathways,
bycatch mortality will be reduced effectively through
protection of habitat. Further efforts should also be
made to protect important areas within other systems
and to conserve the several discrete population seg-
ments defined by ASSRT3 and Grunwald et al. (2008)
and to promote genetic diversity among Atlantic stur-
geon populations.

By understanding the time periods of localized ag-
gregations and movements of Atlantic sturgeon, plans
could be developed that minimize the extent and length
of closures that are concentrated within narrow cor-
ridors. Some states already restrict inshore trawling
which limits fishery interactions with Atlantic stur-
geon, such as NJ (3.22 km limit), MD (1.61 km limit),
DE (no trawling), and NY (various no trawl zones in
marine waters). Any spatial closures require proper
enforcement and substantial community-level support
for successful implementation (Sumaila et al.. 2000).
Although broad-scale movement patterns are becoming
clearer, work is required to understand the finer scale
movements of Atlantic sturgeon such that any spa-
tial management plans could be minimized while still
achieving adequate protection. Current plans toward

464

Fishery Bulletin 108(4)

understanding finer-scale movements are aided by co-
operative efforts such as those of the Atlantic Coopera-
tive Telemetry (ACT) network, which is a large scale
collaborative telemetry network of -30 groups from
Maine to South Carolina (D. Fox and T. Savoy, personal
commun.7'8). Such coordinated efforts are steps in the
right direction for species conservation. Once fine-scale
movements are understood, in particular for aggrega-
tion areas, fishery managers will be better informed
as to how to limit interactions between fisheries and
the near-endangered Atlantic sturgeon while minimiz-
ing economic impacts. Improving estimates of fishery
bycatch mortality would be of enormous value, in par-
ticular if these estimates included a spatial perspective.
Regardless of the outcome of the current consideration
of Atlantic sturgeon for listing under the endangered
species act, a coordinated effort among academic, fed-
eral, state, and local institutions will be required to
conserve this ancient species.

Acknowledgments

We would like to thank W. Kramer (National Oceanic
and Atmospheric Administration, National Marine Fish-
eries Service), D. Byrne (New Jersey Department of
Environmental Protection), J. Sowles (Maine Depart-
ment of Marine Resources), and J. King (Massachusetts
Division of Marine Fisheries) for providing the data
sets used in this study. We would like to thank M.
Wiggins for survey design and technical support and
Captain S. Cluett and the crew of the RV Seawolf for
helping collect data in New York waters. Funding for
the NY trawl surveys was provided by State Wildlife
Grant award no. 910245 and NOAA research grant no.
NA07NMF4550320. The Steven Berkeley Fellowship
award from the American Fisheries Society further
supported the research of K. Dunton.

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466

Day and night abundance, distribution,
and activity patterns of demersal fishes
on Heceta Bank, Oregon

Ted D. Hart'

Julia E. R. Clemons (contact author)2
W. Waldo Wakefield2
Selina S. Heppell'

Email address for contact author: Julia.Clemons@noaa.gov

1 Oregon State University
Department of Fisheries and Wildlife
104 Nash Hall

Corvallis, Oregon 97331

Present address for Ted D. Hart: Environmental Science and Management

Portland State University

1719 SW 10th Avenue, SB2 Room 218

Portland, Oregon 97201

2 Northwest Fisheries Science Center

Fishery Resource Analysis and Monitoring Division
National Marine Fisheries Service
National Oceanic and Atmospheric Administration
2032 SE OSU Drive
Newport, Oregon 97365

Abstract — Most shallow-dwelling
tropical marine fishes exhibit differ-
ent activity patterns during the day
and night but show similar transition
behavior among habitat sites despite
the dissimilar assemblages of the
species. However, changes in species
abundance, distribution, and activ-
ity patterns have only rarely been
examined in temperate deepwater
habitats during the day and night,
where day-to-night differences in light
intensity are extremely slight. Direct-
observation surveys were conducted
over several depths and habitat types
on Heceta Bank, the largest rocky
bank off the Oregon coast. Day and
night fish community composition,
relative density, and activity levels
were compared by using videotape
footage from a remotely operated
vehicle (ROV) operated along paired
transects. Habitat-specific abundance
and activity were determined for 31
taxa or groups. General patterns
observed were similar to shallow
temperate day and night studies,
with an overall increase in the abun-
dance and activity of fishes during
the day than at night, particularly
in shallower cobble, boulder, and
rock ridge habitats. Smaller school-
ing rockfishes ( Sebastes spp.) were
more abundant and active in day
than in night transects, and sharp-
chin (S. zacentrus ) and harlequin (S.
variegatus) rockfish were significantly
more abundant in night transects.
Most taxa, however, did not exhibit
distinct diurnal or nocturnal activ-
ity patterns. Rosethorn rockfish (S.
helvomaculatus) and hagfishes (Epta-
tretus spp.) showed the clearest diur-
nal and nocturnal activity patterns,
respectively. Because day and night
distributions and activity patterns in
demersal fishes are likely to influence
both catchability and observability in
bottom trawl and direct-count in situ
surveys, the patterns observed in the
current study should be considered
for survey design and interpretation.

Manuscript submitted 30 September 2009.
Manuscript accepted 24 August 2010.

Fish. Bull. 108:466-477 (2010).

The views and opinions expressed
or implied in this article are those
of the author (or authors) and do not
necessarily reflect the position
of the National Marine Fisheries
Service, NOAA.

For surveys of groundfish, swept-area
trawls are generally conducted and
direct-counts from video cameras
are recorded during daylight hours
(Gunderson, 1993; Adams et al., 1995;
Yoklavich et al., 2000; Wakefield et
al., 2005). If activity patterns vary
among species during the day versus
the night, conclusions about rela-
tive abundance, community composi-
tion, and habitat affiliations could be
incomplete or biased. It is not known
whether diel activity and abundance
patterns in fishes commonly found
in shallow temperate and tropical
areas are similar for fishes inhabit-
ing deeper temperate areas along the
west coast of North America, where
diel changes in light levels are subtle.
We used a repeat-transect (the tran-
sect was followed once during the day
and again at night) visual sampling
survey to examine differences in fish
abundance, distribution, and behavior
on Heceta Bank, a temperate reef and
ridge ecosystem off the central coast
of Oregon.

Diel distributions and activity pat-
terns in fishes have been well studied
in tropical areas, and these studies

have shown that most fishes exhibit
distinct diel behavioral patterns (Col-
lette and Talbot, 1972; Hobson, 1972;
Helfman, 1978). Generally, two-thirds
of fishes are diurnal, one-third are
nocturnal, and a marked change in
the vertical distribution of fishes oc-
curs between day and night (Helfman,
1978). Most fishes rigidly follow a di-
urnal or nocturnal activity pattern,
exhibiting very low activity in shel-
ter-providing areas and high activ-
ity during feeding. Rotation between
ecological niches at daytime and at
night, such as the broad replacement
of diurnal planktivores with preda-
tors during the night, proceeds in
predictable patterns (Hobson, 1972).
Some of the largest schools encoun-
tered by day in tropical waters are
nonfeeding, resting schools of noctur-
nal fishes, and many diurnal fishes
actively school in the water column
by day and then rest individually at
night (Hobson and Chess, 1973; Par-
rish, 1992).

Although not as well studied, diel
shifts in fish communities and be-
havioral patterns in shallow temper-
ate habitats are less distinct than

Hart et al.: Abundance, distribution, and activity patterns of demersal fishes on Hecate Bank, Oregon

467

those observed in warmer water regions (Hobson et
al., 1981). Deepwater habitats with low light penetra-
tion would therefore be expected to show only subtle
changes in species composition, densities, or activities
during night hours. Nevertheless, diel distributions
and activity patterns of some species of fish have been
observed in temperate areas at substantial depths. On
Stonewall Bank, Oregon, in situ direct observations in
shelf waters (41-70 m) revealed that species composition
changed little from day to night, but the abundance of
some fishes decreased dramatically (Hixon and Tissot1).
Specifically, juvenile rockfishes ( Sebastes spp. ) and ro-
sethorn rockfishes (S. helvomaculatus) showed much
greater abundance during the day, and spotted ratfish
( Hydrolagus colliei ) and widow rockfish (S. entome-
las ) were significantly more abundant at night. Within
Pribilof Canyon (181 to 240 m) in the Bering Sea, Pa-
cific ocean perch ( S . alutus) actively fed on euphausiids
just above sea-whip “forests” during the day and were
observed to be less active within the sea-whip habitat at
night (Brodeur, 2001). In deeper rocky bank areas with
lower levels of ambient light, it is not known whether
an overall change from high to low activity from day
to night exists, as is observed in shallow temperate
fish communities (Ebeling and Bray, 1976; Hobson and
Chess, 1976; Moulton, 1977).

We hypothesized there would be differences in the
day and night assemblages of fishes in deep temperate
waters, but that the patterns and changes in abundance
and activity would be less distinct than those observed
in tropical and shallow temperate fish communities.
Given its diverse range of habitats and water depths,
Heceta Bank is an ideal location for studying day-night
patterns of demersal fishes among different depths and
habitat types.

Materials and methods

Study area

Heceta Bank is one of the largest of all submarine,
rocky banks off the west coast of the United States,
located approximately 60 km off the central Oregon
coast, extending 50 km north to south (Fig. 1). The bank
has been a primary focus of direct-observation studies of
groundfishes, invertebrates, and habitat since the late
1980s (Pearcy et al., 1989; Stein et al., 1992; Wakefield
et al., 2005; Whitmire et al., 2007; Hixon and Tissot1;
Hixon et al.2). This bank comprises a wide range of

1 Hixon, M. A., and B. N. Tissot. 1992. Fish assemblages of
rocky banks of the Pacific Northwest. Final Report supple-
ment, OCS Study 91-0025, 128 p. U.S. Minerals Manage-
ment Service, Camarillo, CA 93010.

2 Hixon, M. A., B. N. Tissot, and W. G. Pearcy. 1991. Fish
assemblages of rocky banks of the Pacific northwest, Heceta,
Coquille, and Daisy Banks. OCS Study MMS 91-0052, 410 p.

U.S.D.I. Minerals Management Service, 770 Paseo Camarillo,
2nd Floor, Camarillo, CA 93010.

benthic habitats from rock ridge and boulder to sand,
and mud and extends from 70 m depth at the top of the
bank to >500 m in water depth on its flanks (Figs. 1 and
2). The bank has been generally characterized as having
three major habitat-depth profiles: 1) shallow rock ridge
and boulder habitat from 70 to 100 m; 2) boulder and
cobble habitat at mid-depth from 100 to 150 m; and 3)
mud habitat in greater than 150 m of water depth (Hixon
et al.2). Some portions of the bank show great habitat
variability (Hixon and Tissot1).

Light levels

Ambient light levels on Heceta Bank were measured
two weeks before the current study by the Plankton/
Bio-Optics group at Oregon State University during a
Global Ocean Ecosystems Dynamics (GLOBEC) study of
meso- and fine-scale physical and biological fields (Whit-
mire and Cowles, unpubl. data3). In order to characterize
the underwater light environment over the bank, the
OSU group used in situ total absorption coefficient data.
Absorption measurements (at[488 nm|) were collected
with a dual-path absorption and attenuation meter (ac-9;
WET Labs, Inc., Philomath, OR) that was mounted on
a SeaSOAR, a towed undulating vehicle used to deploy
a wide range of oceanographic monitoring equipment,
and towed in an undulating fashion along east to west
track lines over the bank during daylight hours on 5
and 6 June 2000. One percent light levels (in relation
to surface light values), a commonly used oceanographic
parameter for comparing light attenuation, were reached
at approximately 20 m in high chlorophyll coastal waters
(~3 to 6 mg/m), and at approximately 50 m in waters
at the western end of the east— west transects. This
empirical approach for light attenuation agreed well
with theoretical relationships between depth and light
attenuation as applied to coastal and offshore waters
within the California Current (Morel, 1988; Barnard
et al., 1999).

Survey transects

From 19 to 26 June 2000, an interdisciplinary group
of scientists used the remotely operated vehicle (ROV)
ROPOS (Remote Operated Platform for Ocean Science),
managed and operated by the Canadian Scientific Sub-
mersible Facility (CSSF), to revisit five stations on
Heceta Bank that were established in the 1980s (Figs.
1 and 2) (Pearcy et al., 1989; Stein et al., 1992; Hixon
and Tissot1; Hixon et al.2) and to explore new sites on the
bank. At each of five historical stations fish assemblages
were compared between day and night.

The ROV ROPOS is well suited for deepwater demer-
sal fish surveys. ROPOS is a 30-horsepower electro-
hydraulic ROV equipped with two video systems, a

3 Whitmire, A. L., and T. J. Cowles. 2008. College of Oceanic
and Atmospheric Sciences, Oregon State Univ., Corvallis,
OR 97331.

468

Fishery Bulletin 108(4)

125°0'W 124°52'W 125°0'W 124°30'W 124°0'W

Figure 1

Location and depth (in meters) of the study area, Heceta Bank off the Oregon coast, and the area mapped
with a multibeam sonar system in 1998 (MBARI 2201; modified from Whitmire et ah, 2008). The leftmost
panel shows the location of the ROV transects for areas surveyed during day and night periods for each
station (boxes) on Heceta Bank, Oregon. Global Ocean Ecosystem Dynamics (GLOBEC) track lines for light
levels (lines 3, 3a, 4, and 4a) are shown in white dashed lines and are labeled to the right of the map.
Depth contours are given in meters.

broadcast-quality Sony DXC 950 three-chip color video
camera (used for fish and habitat video analysis), a
wide-angle low light black and white video camera, an
obstacle avoidance sonar, a compass, three arc lights
(250 W), four halogen lights with adjustable intensity
(250 W), and a 10-hp cage with a separate light and
video system (Wallace and Shepherd, 2003). One pair of
scaling lasers (10-cm scale) mounted in parallel on the
color video camera provided scale in the field of view of
the video image for estimating the width of transects
and the size of fishes and features on the seafloor. The
distance surveyed was determined from smoothed navi-
gation of tracklines obtained from ultra-short baseline
tracking. Real-time audio commentary of habitat type
and fish identification was overlaid on the videotape.
The technical side of the ROV dive transects was man-
aged and conducted by two four-member CSSF teams
that worked in alternating 12-hour watches. Parallel
interdisciplinary science teams worked in tandem with

the ROV group to direct the scientific operations and
ensure consistency in sampling effort.

Day and night complements were completed outside
the two-hour twilight periods of dawn (0436 to 0636
PST) and dusk (2006 to 2206 PST) to avoid possible
biases due to changes in the behavior of fishes dur-
ing crepuscular periods (Yoklavich et al., 2000). Only
daytime fish transects that overlapped geographically
with, or were in close proximity to, corresponding night
fish transects (stations 2, 3, 4, 6, and 9) were used
in this analysis. Station 4 contained a night transect
located approximately 1 nautical mile (nmi) away from
the day transect but in a comparable depth range and
over similar habitat, and therefore it was included in
the analysis.

A total area of 5.5 hectares along a combined total
transect distance of 40.9 km was surveyed during 45.6
hours (Fig. 2). Stations varied in habitat composition and
depth (Fig. 2). Shallow areas (70-100 m) were dominated

Hart et al.: Abundance, distribution, and activity patterns of demersal fishes on Hecate Bank, Oregon

469

Station 4

Day I...,,

" I "1 n

R527

Night M

R528

o'o

0'5

TO

Station 9

Day

HI

R537

Night

R538

0.0

0.5

TO

Station 2

Day (HIT-

— iuuth

R531

Niaht

'I a

0.0

0.5

1.0

Station 3

Day L .1

rm

R532

Night fimm

R533

0.0

0.5

1.0

Station 6

Dav i

-fe«.vl

R534

Night L

11!

Area (ha)

Day

Night

11 Flat Rock

B Flat Rock

13 Rock ridge

□ Rock ridge

E] Boulder

H Boulder

□ Cobble

H Cobble

D Pebble

02 Pebble

□ Sand

D Sand

□ Mud

□ Mud

Figure 2

Bar graphs indicate the area and relative
composition (in hectares) of each primary
habitat surveyed along transects during
day and night periods for each station on
Heceta Bank, OR. ROV dives associated
with each station are identified by an “R”
followed by the dive number.

by rock ridge and boulder, mid-depth by cobble, and
deeper areas by mud habitat with isolated patches of
cobble and boulder. Rock ridge, boulder, cobble, and mud
composed the four most dominant primary habitat types.

Videotape analysis

Videotape collected along all transects was analyzed for
fish and habitat identification. Sunset, dawn, dusk, and
nautical twilight times (Pacific daylight savings time)
were derived from the U.S. Naval Observatory website
(http://www.usno.navy.mil/, accessed June 2000) and
calculated for the day of each dive by using the specific
longitude and latitude coordinates (degrees and minutes)
for each station.

Transects were subdivided into habitat patches, based
on primary habitat types observed on the videotapes.

Seafloor habitats were classified into seven standard-
ized categories (Hixon and Tissot1; Stein et al., 1992):
rock ridge (high relief where vertical rock was found
to be >3.0 m); flat rock (low relief where vertical rock
was found to be <3.0 m); boulder (300-25.6 cm rock);
cobble (25.6-6.4 cm rock); pebble (6. 4-0. 2 cm rock);
sand (2.0-0.06 mm); and mud (<0.06 mm). Only the pri-
mary habitat (>50% of the seafloor) in the field of view
was used in our analysis. The length of each habitat
patch was determined by using the geographic position
recorded at the start and end of each patch. With the
scaling lasers, the width of each transect was estimated
by selecting random frames every minute during each
transect, measuring the width of these lasers on the
video monitor, and extrapolating to the field of view.
Transect width ranged from 1.3 to 2.1 meters. The
area of each patch was determined by multiplying the
patch length by the average patch width. Each transect
consisted of a few to many habitat patches, depending
on the variability of substrate.

Videotape analysis was performed by two technicians
simultaneously in order to confirm fish identifications,
counts, and fish activity. All fishes were identified to
the lowest practical taxonomic unit (usually to species)
and total fish length was estimated to the nearest 5
cm. For fish that could be identified to a taxonomic
group, but not species, a generalized abbreviation was
used (e.g., FF for unidentified flatfish), and in cases
where the fish observed was one of two species, a new
abbreviation was created to accommodate this situa-
tion. Fish were counted at the point where they passed
through the level of the scaling lasers and were as-
signed a GMT time that became a permanent time and
geographic reference point in a database. A single ana-
tomical feature (eye) was used to determine whether or
not a fish was considered within the transect to prevent
underestimating transect width and overestimating
abundance. We restricted our analysis to 31 identified
species or taxonomic groups that were seen frequently
enough to represent >0.1% of the total day and night
fish density (number of fish per hectare). Exceptions to
this rule were the inclusion of three rarely seen species:
darkblotched rockfish (S. crameri), because this is an
important commercial species; kelp greenling (Hexa-
grammos decagrammus ); and bigfin eelpout ( Lycodes
cortezianus), because the day-night activity patterns of
the latter two have been studied in shallow temperate
areas (Moulton, 1977). Some categories of multiple taxa
were created, such as “pygmy-Puget Sound rockfish
complex” {S. wilsoni and S. emphaeus), where it was
impossible to identify every individual in aggregations.
Another common category was “unidentified rockfish,”
where it was not possible to classify a rockfish to spe-
cies conclusively. “Unidentified juvenile rockfish” (ab-
breviation RRF) were categorized by size (<10 cm long),
not by morphological features, because video resolu-
tion and inherent difficulty of in situ identification of
young-of-the-year rockfishes precludes determinations
at the level of species. Hagfishes (Eptatretus spp. ) were
not identified to species, but on the basis of depth of

470

Fishery Bulletin 108(4)

occurrence, the species observed was probably the Pa-
cific hagfish (Eptatretus stoutii) (Barss, 1993).

All fish in the videotapes were counted and assigned
an activity category (“active” or “inactive”). The two cat-
egories were developed in order to analyze the videotape
efficiently and quantitatively, and all fishes were placed
into one of the two categories. Active fish were off the
bottom (or temporarily in contact with the substrate),
and inactive fish were in contact with the substrate
(e.g., in contact with the seafloor or were occupying
crevices). All flatfish were excluded from the activity
analysis because of our definition of “activity.” We as-
sumed that fish were counted only once and that the
submersible did not influence the activity of fishes.
When the ROV clearly affected the behavior of a fish,
the activity of the fish observed before the ROV inter-
ruption was used in analyses.

Data analysis

Relative abundance was determined for each taxon on
a broad scale over all stations (2, 3, 4, 6, and 9) and all
habitat types, and on a finer scale within each of the
four primary habitat types (rock ridge, boulder, cobble,
and mud) over all stations. Fish abundance was first
normalized by dividing the abundance for a given taxon
in a habitat patch by the area swept in that habitat
patch. Relative abundance in a daytime habitat patch
was matched up with a relative abundance in a night-
time habitat patch of closest geographic proximity for a
given taxon. These pairs were used to create the ranks
in a Wilcoxon signed-rank test. For all taxa, 402 habitat
patches were included in the analysis, and an average of
59 habitat patches were compared for each taxon (many
taxa were in the same habitat patch). This enabled us to
estimate if relative abundance trends were consistent at
both scales. For the finer scale, some habitat types (e.g.,
flat rock) did not contain sufficient relative abundance
for analysis.

The Wilcoxon signed-rank test was performed with
S-Plus, vers. 3.2 software (TIBCO Software Inc., Palo
Alto, CA) to determine significant differences in the ac-
tivity of fishes during day and night (Ramsey and Scha-
fer, 2002). This test involved estimating the percentage
of fish active and inactive within each habitat patch for
each taxon (raw abundance was used). These day and
night pairs (percentage of fish active and percentage of
fish inactive) were used to create the ranks in the test
for a given taxon over primary habitat types. A total of
398 habitat patches were analyzed for all taxa, with an
average of 64 habitat patches compared for each taxon.

We also used nonmetric multidimensional scaling
(NMS) to examine associations between day and night
fish abundance with depth and with primary habitat
(McCune and Grace, 2002). PC-ORD software, vers.
5.0 (MjM Software, Gleneden Beach, OR), was used
with a Monte Carlo test and Sprensen distance mea-
sure, starting with random configurations (Mather,
1976). We restricted the NMS to taxa that showed
significantly greater abundance during day or night in

the Wilcoxon signed-rank test (P<0.05), and to those
that showed a strong correlation (Pearson and Kendall
correlation) with depth (P<-0.5 or >0.5 on the second
axis) during trial NMS runs with all 31 taxa. A total
of 11 taxa met these criteria. The final species (taxa)
matrix included columns of log-transformed abundance
and rows of sample units grouped by primary habitat
for each dive during day and night (e.g., boulder-night -
R534). All primary habitat types were used because
the NMS determines correlation strength along an
environmental gradient and does not require paired
plots as in the Wilcoxon signed-rank test. The final
environmental matrix included two quantitative vari-
able columns: primary habitat types (flat rock, rock
ridge, boulder, cobble, pebble, sand, and mud) and
average depth (meters). Sample units greater than 3.0
standard deviations were excluded from analysis. The
final ordination had 166 iterations and 15 runs. This
test enabled us to determine if marked differences in
fish abundance were associated with depth and pri-
mary habitat, and whether taxa showing significantly
greater abundance during day or night were distrib-
uted similarly on the bank.

Results

A total of 29,787 individual fish were counted on the
ROV transect videotapes. During the day, we observed
an average of 207 fishes per hectare, and at night we
observed a lower average of 141 fishes per hectare.
Fish taxa in greatest abundance were from the genus
Sebastes. Dominant taxa (pygmy and Puget Sound rock-
fish, and unidentified juvenile rockfish) showed the
largest differences in relative abundance between day
and night (Fig. 3). Across all stations and primary
habitat types, and within at least one primary habitat
type, eight taxa showed significantly greater abundance
during the day (P<0.05) and five taxa exhibited sig-
nificantly greater abundance during the night (P<0.05,
Table 1 , Fig. 3). Three taxa were found to be signifi-
cantly greater in abundance during day (kelp greenling
and unidentified mottled poacher [Agonidae]) and night
(redstripe rockfish [S. proriger ] ) only in specific primary
habitat types (Table 1). Several taxa showed apparent
differences in abundance, but sample sizes were too
small for statistical significance in the paired Wilcoxon
signed rank test (e.g., kelp greenling). Harlequin rock-
fish ( S . variegatus) was the only species we regularly
encountered exclusively at night (darkblotched rockfish
were rare but were also seen only at night), whereas
kelp greenling were encountered only during the day
at shallow depths.

NMS analysis of distribution

The NMS analysis showed significant correlations
(P=0.03) among taxa, depth, primary habitat, and day
and night (Fig. 4). The ordination explained 78% of the
variation with an acceptable stress value (a lower value

Hart et al.: Abundance, distribution, and activity patterns of demersal fishes on Hecate Bank, Oregon

471

"Pygmy rockfish [
"Puget Sound rockfish [
‘Pygmy-Puget Sound complex [
"Unident, juvenile rockfish [
"Rosethorn rockfish [
"Sharpchin rockfish [
Unident adult rockfish [
Yellowtail rockfish f
Greenstriped rockfish j
Redstripe rockfish [
"Harlequin rockfish
Widow rockfish
Yelloweye rockfish
Canary rockfish
Darkblotched rockfish
Shortspine thornyhead || ~ | ,
Dover sole
Unident, flatfish
‘Rex sole
"Unident, sculpin
"Unident, mottled sculpin
Threadfin sculpin
Icelinus spp
Kelp greenling
Lingcod
‘Eptatretus sp.
"Spotted ratfish
Sablefish
Unident, mottled poacher

‘Unident, ronquil br.--”r'T
Bigfin eelpout |

1

33

=11

Ha 11

3*111

3*

□ Day
O Night

:a±-

IV

=Bh

10 100

Number of fish/hectare

1000

10,000

Figure 3

Total abundance (number of fish per hectare) of fish taxa as determined from the ROV during
night and daytime transects over all habitat types. Wilcoxon signed-rank test was used to
compare day and night abundance across stations and primary habitat types (*P<0.05, **
PcO.Ol). Arabic numerals indicate the most dominant taxa during day, and Roman numer-
als indicate the most dominant taxa during night. Error bars indicate standard error of the
abundance for each taxon. White bars represent day abundance and gray bars represent
night abundance for the following species groups: Sebastes, Sebastolobus, flatfishes, Cottidae,
and other fish. Scientific names for all taxa include from top to bottom: pygmy rockfish (S.
wilsoni ), Puget Sound rockfish (S. emphaeus ), unidentified juvenile rockfish less than 10 cm
long (Sebastes spp.), rosethorn rockfish (S. helvomaculatus), sharpchin rockfish (S. zacentrus),
unidentified adult rockfish (Sebastes spp.), yellowtail rockfish (S. flavidus), greenstriped
rockfish (S. elongatus), redstripe rockfish (S. proriger), harlequin rockfish (S. variegatus),
widow rockfish (S. entomelas ), yelloweye rockfish (S. ruberrimus), canary rockfish (S. pin-
niger ), darkblotched rockfish (S. crameri), shortspine thornyhead (S. alascanus ), Dover sole
(Microstomus pacificus), unidentified flatfish (Pleuronectidae), rex sole (Glyptocephalus zaclii-
rus ), unidentified sculpin (Cottidae), unidentified mottled sculpin (Cottidae), threadfin sculpin
(Icelinus filamentosus), Icelinus spp., kelp greenling (Hexagrammos decagrammus ), lingcod
( Ophiodon elongatus), unidentified hagfishes (Eptatretus spp.), spotted ratfish (Hydrolagus
colliei), sablefish (Anoplopoma fimbria), unidentified mottled poacher (Agonidae), unidentified
ronquil (Bathymasteridae), and bigfin eelpout (Lycodes cortezianus) . Alternate shading of the
background represents general taxonomic groups.

472

Fishery Bulletin 108(4)

Table t

Fish taxa exhibiting significantly greater relative abundance (number of fish per hectare) across all stations over primary habi-
tat types at Heceta Bank, OR, (rock ridge, boulder, cobble, and mud) during daytime or nighttime. Wilcoxon signed-rank test was
used (*P<0.05, **P<0.01) to compare day and night relative abundance between habitat patches in closest geographic proximity
within primary habitat types over all stations. Taxa are listed in order of relative abundance from top to bottom; primary habitat
is listed in decreasing order of size from left to right, and numbers in parentheses are relative abundance during day or night.

Taxon

Rock ridge

Boulder

Cobble

Mud

Significantly more abundant during day

unidentified juvenile rockfish ( Sebastes spp.)

(1498)**

(2123)*

(632)**

(150)*

Puget Sound rockfish (S. emphaeus )

(2235)**

(421)**

pygmy rockfish (S. wilsoni )

(4878)**

(46)*

(634)**

pygmy-Puget Sound complex (S. wilsoni and S', emphaeus )

(3240)*

rosethorn rockfish (S. helvomaculatus)

(249)**

(291)*

(124)*

unidentified ronquil (Bathymasteridae)

(16)**

(43)*

unidentified mottled sculpin (Cottidae)

(30)**

unidentified sculpin (Cottidae)

(12)*

(28)**

unidentified mottled poacher (Agonidae)

(12)*

kelp greenling ( Hexagrammos decagrammus )

(6)*

Significantly more abundant during night

sharpchin rockfish (S. zacentrus )

(460)**

(1134)*

(5603)*

(1656)*

redstripe rockfish (S. proriger )

(90)*

harlequin rockfish (S. variegatus)

(103)**

spotted ratfish (Hydrolagus colliei)

(75)*

(56)*

unidentified hagfishes ( Eptatretus spp.)

(45)*

(64)*

rex sole (Glyptocephalus zachirus)

(69)*

denotes a better “fit” of data) of 20.5 for three axes.
After a +115° rotation, the first axis showed correlation
with day (right side) and night (left side) sample units,
explaining 22% of the variation in the data and revealed
a mean stress of 49.8. The second axis explained an
additional 30% of the variation in the data and showed
a negative correlation with depth (Pearson’s r=0.141)
and a mean stress of 29.1. The second axis also showed
a positive correlation with substrate, and larger-size
primary habitat was found in the first and second quad-
rants of the graph and smaller-size primary habitat in
the third and fourth quadrant. The third axis improved
the cumulative coefficient of determination, r2, to 0.777
with little additional stress; this axis enabled us to
rotate the ordination in three dimensions to distinguish
habitat and species and showed good correlations with
the day-night and habitat-depth axes, but is not easily
plotted. Higher dimensions showed little improvement
in model fit.

Taxa more abundant during the day (rosethorn rock-
fish, pygmy rockfish, pygmy-Puget Sound rockfish com-
plex, kelp greenling, and unidentified juvenile rockfish)
showed a positive correlation along axes one and two
and appear in the upper right quadrant of Figure 4.
Puget Sound rockfish showed a correlation with the
day-night axis, but this species was associated with
greater depth and smaller-size substrate as primary
habitat when compared to the other taxa that were
more abundant during the day; this taxon appears in

the lower right quadrant. Thus, this dominant day
assemblage was observed mainly at shallow- to mid-
depths over medium to large-size substrata. Taxa show-
ing greater abundance during the night (spotted ratfish
[Hydrolagus colliei], hagfishes, rex sole [Glyptocephalus
zachirus], sharpchin rockfish [S. zacentrus], and harle-
quin rockfish) showed a negative correlation along axes
one and two. Thus, the dominant night assemblage was
generally over deeper areas of medium- to small-size
substrata of cobble and mud.

Day and night species assemblages

During the day within all stations, large densities of
mostly small-size rockfish taxa were primarily found
over shallow rock ridge, boulder, and cobble substrata
(Table 1, Figs. 3 and 4). The four most dominant day
taxa (both active and inactive) were pygmy rockfish,
Puget Sound rockfish, pygmy-Puget Sound rockfish
complex, and unidentified juvenile rockfish. Yellowtail
rockfish (S. flavidus) were also an important component
of the daytime assemblage, albeit less abundant and less
dominant during night. Many of these taxa showed sig-
nificantly greater abundance and activity over medium-
to large-size habitat (cobble, boulder, and rock ridge)
(Tables 1 and 2). Rosethorn rockfish showed the clearest
diurnal pattern of all species (Table 2). Small rockfishes
and yellowtail rockfish were more active during the day
but did not exhibit clear inactivity during the night.

Hart et al.: Abundance, distribution, and activity patterns of demersal fishes on Hecate Bank, Oregon

473

Larger

A

CD

n

C/5

.2

ro

to

-Q

D

co

A Day—
Y Night
X Day-
+ Night
O Day—

♦ Night
O Day—'

• Night
□ Day—
a Night
A Day—
A Night
x Day-

mud
—mud
sand
— sand
pebble
pebble
cobble
—cobble
boulder
—boulder
rock ridge
rock ridge
flat rock

▼

Smaller

Night <-

' » PR

° A

s JV*

A “> A "*•

® „ • RA

• ;* \HF

R$\ 9

RT o ° ° CKG

, & ■ % A A

SH

HR

S 4.

A o c

PRC

RRF

PSR

O

Shallow

A

Axis 1

T

Deep

-> Day

Figure 4

Nonmetric multidimensional scaling (NMS) ordination showing association between 11 taxa and habitat patches
(different symbols) from all stations (2, 3, 4, 6, and 9). Taxa codes are: HF (hagfishes, Eptatretus spp.), HR
(harlequin rockfish, S’. variegatus), KG (kelp greenling, Hexagrammos decagrammus), PR (pygmy rockfish, S.
wilsoni), PRC (pygmy-Puget Sound complex, S’. wilsoni and S. emphaeus), PSR (Puget Sound rockfish, S. empha-
eus), RA (spotted ratfish, Hydrolagus colliei), RS (rex sole, Glyptocephalus zachirus), RT (rosethorn rockfish, S.
helvomaculatus), RRF (unidentified juvenile rockfish, Sebastes spp.), and SH (sharpchin rockfish, S. zacentrus ).
Environmental variables include the quantitative variable of depth (increasing depth from top to bottom), and
the categorical variables (shape of symbols) of day, night, and habitat.

When compared to the dominant day assemblage,
the night assemblage exhibited lower overall densities
and consisted of less active, larger-size fish of fewer
taxa, many of which were also seen during the daylight
hours (Tables 1 and 2, Fig. 3). Dominant night taxa
were sharpchin rockfish, yellowtail rockfish, Dover sole
(Microstomus pacificus), and greenstriped rockfish (S.
elongatus). Of the dominant night assemblage, sharp-
chin rockfish comprised over half of the fish encoun-
tered at night (Fig. 3) and was one of the only taxa
that showed significantly greater abundance during the
night (P<0.05) in most primary habitat types (Table 1).
Hagfishes and spotted ratfish were significantly greater
in abundance and activity during the night (P<0.05),
and widow rockfish showed significantly greater activity
during the night (P<0.05), despite being rarely observed
(Table 2). Hagfishes were the only taxa that exhibited
a distinct nocturnal activity pattern (P<0.05).

Discussion

The relative composition of fish taxa over all depths
and habitat types on Heceta Bank did not show a broad
replacement from day to night, as observed in shallow
tropical areas. However, there were consistent patterns
of abundance and activity that were species-, depth-,
and habitat-specific. There was a considerable day-
night change in the abundance of the four most domi-
nant day taxa (pygmy rockfish, Puget Sound rockfish,
pygmy-Puget Sound rockfish complex, and unidentified
juvenile rockfish) over shallower areas of rock ridge
and boulder habitat. Active, small- to medium-size fish
taxa tended to aggregate around shallow medium- to
large-size habitat features during the day, and larger-
size night taxa (sharpchin rockfish, yellowtail rockfish,
Dover sole, and greenstriped rockfish) tended to aggre-
gate around these features at night. Rosethorn rockfish

474

Fishery Bulletin 108(4)

Table 2

Fish taxa (raw count s) exhibiting a significant difference in the percentage of fish found to be active and inactive during day and
night within similar primary habitat types (rock ridge, boulder, cobble, and mud) over all stations at Heceta Bank, OR. Values
represent the percentage of fish found to be active or inactive over each substrate type, and values in parentheses indicate n for
each comparison. Wilcoxon signed-rank test was used (*P<0.05, **P<0.01, not significant [ns], P>0.05). Taxa are listed in order
of highest abundance (number of fish per hectare) within each category.

Taxon

Primary

habitat

Day

active fish

Day

inactive fish

Night
active fish

Night

inactive fish

Diurnal

rosethorn rockfish (S. helvomaculatus)

rock ridge

76% (246)**

ns

boulder

74% (243)**

85% (123)**

cobble

66% (405)*

92% (143)**

mud

ns

93% (47)**

Nocturnal

Eptatretus spp.

cobble

87% (23)*

69% (29)*

Significantly more active during day

unidentified juvenile rockfish

rock ridge

99% (855)**

( Sebastes spp.)

boulder

98% (1214)**

cobble

96% (876)**

mud

91% (54)**

Puget Sound rockfish (S. emphaeus)

boulder

71% (367)**

cobble

73% (2501)**

mud

87% (126)**

pygmy rockfish (S. wilsotii)

rock ridge

99% (855)**

cobble

99% (235)**

mud

94% (34)**

yellowtail rockfish (S. flavidus)

rock ridge

95% (259)**

boulder

96% (260)**

Significantly more active during night

spotted ratfish (Hydrolagus colliei )

boulder

87% (16)*

mud

92% (87)*

widow rockfish (S. entomelas)

boulder

96% (45)*

and hagfishes exhibited distinct diurnal and nocturnal
activity, respectively. These day and night patterns were
similar to those observed during day-time surveys from
manned submersibles on Heceta bank (Pearcy et al.,
1989; Stein et al., 1992; Hixon et al.2), day and night
surveys on Stonewall Bank (Hixon and Tissot1), and are
generally consistent with most patterns found in other
shallow temperate day and night studies, but were much
less distinct than those for fishes inhabiting tropical
fish communities (Helfman, 1978). The overall marked
decrease in abundance and activity of smaller-size taxa
at night was similar to the decrease that Ebeling and
Bray (1976) and Moulton (1977) observed, but our study
did not provide evidence of a pronounced replacement
of diurnally active taxa by exclusively nocturnal spe-
cies as observed at Santa Catalina Island (Hobson and
Chess, 1973; Hobson et al., 1981), Hawaiian tropical
reefs (Hobson, 1972), and reefs in the Virgin Islands
(Colette and Talbot, 1972).

It is possible that light illumination at the top of
Heceta Bank during the day contributed to the higher
abundance and activity of the three most dominant

day taxa (pygmy rockfish, pygmy-Puget Sound rockfish
complex, and unidentified juvenile rockfish), as found in
similar studies on temperate species. Fishes found at
the top of Heceta Bank likely perceive and use the faint
sun illumination during the day (Boehlert, 1979). On
Heceta Bank, the photic zone generally extends down
to approximately 50 m water depth and it is generally
accepted that sun illumination affects behavior of fishes
down to these depths (L. Britt, personal commun.4).
This was confirmed by the GLOBEC survey, which mea-
sured one percent of surface light at 50 m, just above
the shallowest fish survey depths (70 m) where most of
the unidentified juvenile rockfish were present. Light il-
lumination may be aiding the dominant day assemblage
because these taxa stay close (perhaps within visual
distance) to large features that provide refuge from
larger, active piscivorous predators. In Puget Sound

4 Britt, Lyle L. 2007. Alaska Fisheries Science Center,
National Marine Fisheries Service, National Oceanic and
Atmospheric Administration, 7600 Sand Point Way N.E.,
Seattle, WA 98115.

Hart et al.: Abundance, distribution, and activity patterns of demersal fishes on Hecate Bank, Oregon

475

(Moulton, 1977), on rocky kelp forests off Santa Bar-
bara, California (Ebeling and Bray, 1976), and on Santa
Catalina Island, California (Hobson and Chess, 1976;
Hobson et al., 1981), the small-size adult and juvenile
rockfish that remain exposed from refuge during the
night stay close to the seafloor.

Only two taxa showed distinct day and night activity
patterns (diurnal: rosethorn rockfish and nocturnal:
hagfish), indicating that marked differences in day
and night activity are not as prevalent as those found
in shallow tropical coral reef and temperate fish com-
munities (Table 2) (Hobson, 1972; Helfman, 1978). The
diurnal activity pattern exhibited by rosethorn rockfish
was independent of habitat, indicating that habitat type
may not be a significant factor in determining differ-
ences between day and night activities for this species
(Tables 1 and 2). The nocturnal activity pattern that
hagfishes exhibited was similar to that observed by
Ooka-Souda et al. (1985) of another hagfish species
(Eptatretus burgeri ), in the laboratory. During the day
on Heceta Bank, most hagfish were observed coiled up
over mud or sand, or around cobble, whereas during
the night fish of this taxon was observed swimming
above bottom or moving in contact with the bottom
in a twisted manner. Like silver hake ( Merluccius bi-
linearis) which use sand waves (transverse ridges of
sand) for refuge during the day (Auster et al., 2003)
and that forage during the night (Bowman and Bow-
man, 1980; Auster et al., 1995), hagfishes on Heceta
Bank may use mid-depth cobble and mud habitats for
resting during the day and may forage at night. Not
all rosethorn rockfish and hagfishes strictly followed a
diurnal or nocturnal activity pattern; however, the fish
activity measure we used was not sensitive enough to
detect subtle differences in behavior, such as resting
individuals found hovering close to but not in contact
with the seafloor.

Potential bias exists in observing and attempting
to quantify activity in fishes when using video survey
methods (Uzmann et al., 1977; Sale and Douglas, 1981;
Wakefield and Smith, 1990). Our inability to identify
many of the rockfishes to species is potentially problem-
atic, and illustrates a limitation of this survey method.
The majority of historical studies show that very few
fishes exhibit changes in activity with the presence of
an ROV or submersible, although a handful of taxa do
show behavioral responses (High, 1980; Carlson and
Straty, 1981; Pearcy et al., 1989). SCUBA-based video
surveys of fish abundance and behavior indicate that
although the majority of fishes show no noticeable reac-
tion, some species may avoid or be attracted to divers
outside the camera’s field of visibility and may even
follow divers (Moulton, 1977). It has been argued that
SCUBA surveys do not significantly affect counts be-
cause most fishes that follow divers remain behind the
field of view of the camera (Powles and Barans, 1980).
In our study, anecdotal evidence indicated that the
ROV had limited effect on fish behavior, except in cases
where the ROV came in contact with the substrata.
Further investigation is needed, however, to fully grasp

the impacts of observational vehicles on fish responses
(Stoner et al., 2008).

Implications for groundfish surveys

Day and night activity patterns in demersal fishes have
been shown to dramatically change the catchability of
some species on the West Coast (Hannah et al., 2005),
in the Northwest Atlantic (Bowman and Bowman, 1980),
in Newfoundland (Casey and Myers, 1998), and in the
North Sea (Petrakis et al., 2001). In this study, we
found that daytime surveys could underestimate the
abundance of certain species that are more abundant
or active at night, such as sharpchin rockfish. Highly
significant differences in day and night abundance
of schooling rockfishes found in this study indicate
that daytime trawl surveys over small- to medium-size
habitat features may be biased for some fish species.
Migration of fishes into the overlying water column, hori-
zontally off the bank, or into hiding among medium- to
large-size features is likely the most common day and
night behaviors that would decrease the availability of
fishes to the ROV. Specifically, Puget Sound rockfish may
be more available over deeper, smaller-size rock struc-
tures, whereas other dominant day taxa (pygmy rockfish,
pygmy-Puget Sound rockfish complex, and unidentified
juvenile rockfish) and sharpchin rockfish are likely less
available to trawl surveys over large-size features in
shallower portions of the bank. We speculate that the
reduction in abundance of the four most dominant day
taxa is due to fish seeking refuge around medium- to
larger-size structures because of the potential presence
of large piscivores (Wilkins, 1986; Adams, 1987), rather
than to schooling in the water column.

Acknowledgments

We would especially like to thank the following col-
leagues who contributed to this study: B. Barss, B.
Embley, G. Hendler, M. Hixon, D. Markle, B. McCune, S.
Merle, B. Tissot, M. Yoklavich, and K. York. A. Whitmire
and T. Cowles generously contributed information on
ambient light levels. L. Britt, C. Whitmire, and L. Cian-
nelli provided constructive reviews of the manuscript.
This portion of the Heceta Bank project was funded by
the West Coast and Polar Regions Undersea Research
Center of the National Oceanographic and Atmospheric
Administration’s (NOAA) National Undersea Research
Program, the Northwest and Southwest Fisheries Sci-
ence Centers, NOAA’s Pacific Marine Environmental
Laboratory, and the Cooperative Institute for Marine
Resources Studies at Oregon State University. We would
like to thank the professional personnel who operated
the ROV ROPOS and the NOAA RV Ronald Brown. T.
Hart was supported through the Oregon Agricultural
Experiment Station project ORE00102, the H. Richard
Carlson Scholarship, the Collaborative Marine Fisher-
ies Fellowship and the Bill Wick Award through Oregon
State University.

476

Fishery Bulletin 108(4)

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2008. Evaluating the role of fish behavior in surveys
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2005. Fish habitat studies: combining high-resolution geo-

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478

Abstract — Ichthyoplankton surveys
were conducted in shelf and slope
waters of the northern Gulf of Mexico
during the months of May— September
in 2005 and 2006 to investigate the
potential role of this region as spawn-
ing and nursery habitat of sailfish
( Istiophorus platypterus). During the
two-year study, 2426 sailfish larvae
were collected, ranging in size from
2.0 to 24.3 mm standard length. Mean
density for all neuston net collections
(n= 288) combined was 1.5 sailfish per
1000 m2, and maximum density was
observed within frontal features cre-
ated by hydrodynamic convergence
(2.3 sailfish per 1000 m2). Sagittal
otoliths were extracted from 1330
larvae, and otolith microstructure
analysis indicated that the sailfish
ranged in age from 4 to 24 days after
hatching (mean=10.5 d, standard de-
viation [SD] = 3.2 d). Instantaneous
growth coefficients ( g ) among survey
periods (n = 5) ranged from 0.113 to
0.127, and growth peaked during
July 2005 collections when density
within frontal features was high-
est. Daily instantaneous mortality
rates ( Z ) ranged from 0.228 to 0.381,
and Z was indexed to instantaneous
weight-specific growth (G) to assess
stage-specific production potential
of larval cohorts. Ratios of G to Z
were greater than 1.0 for all but one
cohort examined, indicating that
cohorts were gaining biomass during
the majority of months investigated.
Stage-specific production potential,
in combination with catch rates and
densities of larvae, indicates that
the Gulf of Mexico likely represents
important spawning and nursery
habitat for sailfish.

Manuscript submitted 4 March 2010.
Manuscript accepted 28 July 2010.
Fish. Bull. 108:478-490 (2010).

The views and opinions expressed
or implied in this article are those
of the author (or authors) and do not
necessarily reflect the position
of the National Marine Fisheries
Service, NOAA.

Distribution, growth, and mortality
of sailfish (Istiophorus platypterus ) larvae
in the northern Gulf of Mexico

Jeffrey R. Simms1 (contact author)

Jay R. Rooker1
Scott A. Holt2
G. Joan Holt2
Jessica Bangma3

Email address for contact author: jsimms@entrix.com

1 Department of Marine Biology
Texas A&M University at Galveston
P.O. Box 1675

Galveston, Texas 77553

2 University of Texas Marine Science Institute
University of Texas at Austin

750 Channel View Dr.

Port Aransas, Texas 78383

3 Department of Zoology
University of British Columbia
6270 University Boulevard
Vancouver, BC, Canada V6T 1Z4.

Declining populations of Atlantic
sailfish (Istiophorus platypterus)
(ICCAT, 2001) emphasize the need
for a better understanding of their
biology, especially processes affect-
ing growth and mortality during
early life because these mechanisms
often regulate recruitment (Fuiman,
2002). To date, studies on sailfish
biology during the early life interval
are limited; however, recent research
conducted in the Straits of Florida
indicates that sailfish grow rapidly
and experience high mortality during
early life (Luthy et al., 2005; Rich-
ardson et al., 2009a). Although our
understanding of the early life ecol-
ogy of sailfish has improved in recent
years, work to date has been limited
in geographic scope and basic life his-
tory data on sailfish are limited or
not available for other regions of the
Atlantic that may represent essential
spawning and nursery habitat of sail-
fish. In particular, bycatch data from
pelagic longline fisheries in the Gulf
of Mexico indicate that catch rates
for sailfish are twofold higher in the
Gulf than in other areas of the North
Atlantic during the presumed spawn-
ing season (May-September; de Sylva

and Breder, 1997; NMFS1). Because
spawning stock biomass appears high
in this region, a better understand-
ing of the role of the Gulf of Mexico
as spawning and early life habitat of
Atlantic sailfish is essential.

The Gulf of Mexico supports one
of the most productive fisheries in
the world (Chesney et al., 2000), and
oceanographic features within the
Gulf are influenced by inflow from
the Mississippi River and large-scale
oceanographic features, such as the
Loop Current and associated warm
and cold core eddies (Govoni and
Grimes, 1992; Sturges and Leben,
2000). Physicochemical conditions
and primary production vary mark-
edly within and across these features
(Grimes and Finucane, 1991; Biggs,
1992), and have been shown to af-
fect the distribution and growth of
pelagic larvae in the Gulf (Govoni et
al., 1989; de Vries et al., 1990; Lang
et al., 1994). Namely, higher densities

1 NMFS (National Marine Fisheries Ser-

vice. 2008. NMFS Pelagic Longline
Logbook data, (http://www.sefsc.noaa.
gov/flslandingsdata.jsp, accessed Decem-

ber 2008).

Simms et al.: Distribution, growth, and mortality of larval Istiophorus plcitypterus in the northern Gulf of Mexico

479

and increased growth have been observed for larvae
within frontal features created by riverine discharge
and hydrodynamic convergence (Lang et ah, 1994; Hoff-
meyer et ah, 2007). It is likely that oceanographic fea-
tures also influence the early life ecology and population
dynamics of sailfish in this region, and therefore an
improved understanding of the effects of these features
on distribution, growth, and survival will aid in deter-
mining the value of the Gulf as spawning and nursery
habitat for sailfish.

The objectives of this research were threefold: 1) to
characterize spatial and temporal patterns of abun-
dance of sailfish larvae in the northern Gulf of Mexico;
2) to relate spatial variation in distribution and growth
to oceanographic features to determine the causal fac-
tors responsible for recruitment variability; and 3) to
estimate demographic parameters within and across
years to determine whether these traits varied tempo-
rally. Estimates of growth (G) and mortality (Z) were
combined ( G:Z ) to determine indices of stage-specific
production potential and to assess the functional role
of the Gulf as spawning and nursery habitat of this
species.

Materials and methods
Field collections

Five ichthyoplankton surveys were conducted in shelf
and slope waters of the northern Gulf during spring
and summer of 2005 (May, July, and September) and
summer of 2006 (June and August). Surveys were con-
ducted in an area bounded by 27° to 28°N latitude and
88 to 94°W longitude. This sampling area was selected
because bycatch rates of adult sailfish by U.S. longliners
were high in this region during the presumed spawning
period of Atlantic sailfish (NMFS1). Istiophorid larvae
were collected with paired neuston nets (2-m widthxl-m
height frame) with two mesh sizes (500 pm and 1200 pm)
to account for potential differences in capture success
between mesh sizes. Nets were towed through the top
meter of the water column at approximately 2.0 knots for
10 minutes. Paired tows were taken at 60 to 70 sampling
stations spaced approximately 15 kilometers (km) apart
during each survey. Sampling was conducted at 15-km
intervals to allow coverage of a large area encompassing
multiple oceanographic features. The September 2005
survey was shortened (39 stations sampled) because of
inclement weather.

At each station, sea surface temperature (°C), salin-
ity (ppt), and dissolved oxygen (mg/L) were recorded
by using a Sonde 6920 Environmental Monitoring Sys-
tem (Yellow Springs Instruments Inc., Yellow Springs,
OH). A probe malfunctioned during sampling in August
2006, preventing dissolved oxygen measurements. Sea
surface height (cm) for each station was determined
from archived satellite altimetry data provided by the
Colorado Center for Astrodynamics Research (CCAR)
Real-Time Altimetry Project (argo.colorado.edu; R. Leb-

en, personal commun.2). Flowmeters (General Oceanics,
model 2030R, Miami, FL) placed within each net were
used to determine the surface area sampled by each
net. A formula provided by the manufacturer was used
to determine distance towed during each collection
which was multiplied by net width to determine surface
area sampled during each collection (m2): surface area
sampled (m2) = distance sampled (m) x 2 m (net width).

Fish larvae and associated biota were preserved on-
board in 95% ethanol and istiophorids were sorted from
each sample in the laboratory with the use of a Leica
MZ stereomicroscope and stored in 70% ethanol. Istio-
phorid larvae were photographed and standard length
(SL) was measured to the nearest 0.1 mm. Istiophorids
do not have a full complement of fin rays until reaching
20 mm SL (Richards, 1974), and 99.8% of specimens col-
lected in the Gulf were less than 20 mm. Even though
a small number of our largest specimens were over 20
mm and may be considered early juveniles in- 3), for the
purposes of this study, all sailfish collected are referred
to as larvae.

Genetic identification

A percentage of istiophorid larvae (22.2%) were iden-
tified to the species level by following the protocol of
Bangma (2006). The protocol was subsequently modi-
fied and the remaining istiophorid larvae (77.8%) were
identified according to the protocol of J. Magnussen and
M. Shivji (personal commun.3). Briefly, a single eyeball
was removed from each larva and DNA was extracted by
using a QIAGEN DNeasy blood and tissue kit (QIAGEN
#69506, Valencia, CA). A multiplex polymerase chain
reaction (PCR) was performed by using an Eppendorf
mastercycler gradient, QIAGEN Hot Star Taq DNA
Polymerase (QIAGEN #203203), and PCR grade dNTP
mix (QIAGEN #201901). Four primer pairs were used
in each PCR reaction: a universal billfish primer set,
and species-specific primers for sailfish, white marlin,
( Kajikia albida), and blue marlin ( Makaira nigricans).
PCR reactions were examined by means of gel electro-
phoresis with 1% agarose gels containing ethidium bro-
mide and species identification was based on gel banding
patterns. This multiplex assay was employed to identify
sailfish larvae as follows. For samples consisting of less
than 10 individuals, all specimens were assayed. For
samples with 10-50 istiophorid larvae, 40—60% of larvae
were processed. For samples with >50 istiophorid larvae,
25% of larvae were processed. If all larvae in a particu-
lar subsample were identified as conspecific, remaining
larvae from the sample were assigned to that species.
If more than one istiophorid species was detected in a
subsample, all remaining larvae from the sample were
identified genetically.

2 Leben, Robert. 2008. Colorado Center for Astrodynamics
Research, Univ. Colordao, Boulder, CO.

3 Shivji, Mahmood. 2007. Guy Harvey Research Institute,
Nova Southeastern Univ., Ft. Lauderdale, FL.

480

Fishery Bulletin 108(4)

Density and catch rate

The total number of sailfish caught at each sampling
station was divided by the surface area sampled to
determine the density of larvae in number of individuals
per 1000 m2. Mean density did not vary between the two
mesh sizes (500 pm and 1200 pm) in any survey (paired
t-test, all P>0.05), indicating no difference in capture
success between net sizes. However, mean standard
length was smaller in the 500-pm net gear (5.2 mm vs.
5.6 mm; Fa 3116)=21.3, PcO.Ol), indicating that a larger
fraction of small larvae were retained by the finer mesh.
Frequency of occurrence was calculated for each survey
as the number of collection stations which produced at
least one sailfish larva by using the equation

Frequency of occurrence =

( number of stations with

>1 larva / total number of (1)

stations during survey) x 100.

In order to compare catch rates with those from other
ichthyoplankton studies, catch per unit of effort (CPUE)
of sailfish larvae was estimated with the equation

CPUE (larvae per hour) =
number of larvae collected /

([ number of towsxtow length (min) x (2)

2 ( number of nets towed)] / 60).

Oceanographic features

Remotely sensed sea surface height (SSH) data were
used to delineate oceanographic features into one of
four categories (Leben et ah, 2002). Briefly, stations
with a SSH greater than 17 cm were considered to be
within the core of the Loop Current or an associated
eddy system and classified as “anticyclones” (warm core
eddies) (Leben et ah, 2002). Further, the core of adjacent
“cyclones” (cold core eddies) were identified by a SSH of
less than -10 cm. Frontal features associated with the
Loop Current and anticyclones have been reported to
extend up to 60 km from the 17-cm contour. Therefore,
stations between 17 cm and -10 cm SSH and within 60
km of the 17 cm SSH contour were classified as being
in a “front” (Tidwell, 2008). Remaining stations were
classified as “open ocean.”

Analysis of otolith microstructure

Sagittal otoliths were extracted, cleaned of tissue in
immersion oil, and preserved in mounting media (Flo-
texx, Fisher Scientific #14-390-4, Pittsburgh, PA) for
a subset of sailfish larvae. Mounted otoliths were pho-
tographed under high magnification (400x) with an
Olympus BX41 light microscope, and daily growth
increments were enumerated with the use of Image-
Pro Plus software (vers. 4.5, Media Cybernetics Inc.,
Bethesda, MD) by counting the first visible incre-
ment beyond the hatch check as day one (Luthy et al.

2005). Inner increments of large otoliths are occasion-
ally difficult to enumerate; therefore a regression of
growth increment radius on age was used to predict
the number of increments at various distances from
the core (Rooker et al., 1999). The number of incre-
ments within unclear regions was estimated with this
regression and added to the increment count for the
enumerated section to produce final age estimates.
Less than 25% of age estimates were corrected with
this method, and if the unclear region comprised more
than 33% of the final age estimate, the otolith was not
used for age and growth assessments. Two independent
readings of daily increments were conducted by a single
reader for each otolith. When two readings were within
10% variance of each other, one reading was randomly
selected for analysis. If readings differed by >10%, a
third reading was performed. If the third reading was
within 10% variance of one of the former readings,
one of the two similar readings was randomly selected
for analysis. If each reading differed from the others
by >10%, the otolith was not used for further analysis
(n = 94, 7.1%).

Growth, mortality and hatch dates

Growth rates were determined by using otolith-derived
age estimates (n = 1236) and standard length data.
Because ages varied among surveys, growth rates were
based on a limited age range (<17 days or the oldest
larva in May 2005 collections) to minimize any effect
of variable age ranges on growth analyses (Rilling and
Houde, 1999). Daily instantaneous growth coefficients
(g) were calculated from an exponential model:

Lt = L0esf, (3)

where Lt = length (mm SL) at time t;

L0 = estimated length at hatching;
g = instantaneous growth coefficient (d); and
t - otolith-derived age (days after hatching).

Ages of sailfish without an otolith-derived age were
predicted by using age-length relationships (n=1118). A
small number of sailfish larvae were damaged (n=72),
and therefore length and age estimates could not be
determined for these larvae.

Daily mortality was estimated for each survey from
regressions of the decline in log,, {abundances 1) on age.
In order to minimize the influence of gear avoidance by
larger larvae (Houde, 1987), mortality estimates were
determined over a short time interval (10 days), and
thus for a limited size range of larvae (<10 mm). Mor-
tality was calculated for several time intervals rang-
ing from 5 to 10 days and differences were negligible,
indicating that the 10-day duration was appropriate
for the target life stage. The age of peak abundance for
each cohort was used as the initial point for catch-curve
analysis and ranged from 9 to 11 days after hatching.
Daily instantaneous mortality rates (Z) were calculated
from the exponential model

Simms et al.: Distribution, growth, and mortality of larval Istiophorus platypterus in the northern Gulf of Mexico

481

Table 1

Mean environmental conditions (± standard deviation [SD] ) by oceanographic feature for ichthyoplankton collections in the
northern Gulf of Mexico in 2005 and 2006. Environmental parameters were recorded at the surface at each sampling station.

Feature

Temperature (°C)

Salinity (ppt)

Dissolved oxygen (mg/L)

Anticyclone

29.1 (1.6)

36.1 (0.4)

6.8 (0.8)

Front

28.9(1.4)

36.1 (0.4)

6.6 (0.5)

Open ocean

29.3 (1.6)

35.5(1.2)

6.7 (0.8)

Cyclone

28.2 (2.0)

35.6(0.6)

7.2 (1.3)

Nt = N0e-Zt, (4)

where Nt - abundance at time t\

N0 = estimated abundance at hatching;

Z = instantaneous mortality coefficient (d); and
t = otolith-derived age.

Dry weight (mg) was calculated for all larvae with a
measured length by using the length-weight relationship
for sailfish larvae by Luthy et al. (2005): weight (mg) =
0.002(SL[mm] )3012. Weight-at-age data were fitted with
exponential growth models to determine instantaneous
weight-specific growth coefficients (G) for each survey
by using the equation

Wt = W0eGt, (5)

where Wt = dry weight (mg) at time t ;

W0 = estimated weight at hatching;

G = instantaneous weight-specific growth coef-
ficient (d); and
t - otolith-derived age.

Indices of stage-specific production potential were
assessed for each cohort by examining the ratio of
instantaneous weight-specific growth to daily mortal-
ity ( G:Z ). This ratio incorporates growth and mortality
and was used as an index of stage-specific production
of larval cohorts (Rilling and Houde, 1999; Rooker et
al., 1999; Wells et al., 2008). A cohort with a G.Z>1.0
was considered to be gaining biomass, which indicates
that individuals had increased survival and production
potential (Houde and Zastrow, 1993; Wells et al., 2008).

Hatch dates for larvae were determined by sub-
tracting age from date of collection. Otolith-derived
ages were used when available, and remaining ages
were predicted by applying cohort-specific age-length
keys. Given that larger, older larvae in our collections
hatched earlier and experienced greater cumulative
mortality than larvae that hatched later, adjustments
for mortality were made to more effectively represent
the hatch dates of survivors in our collections by using
the equation

N0 = Nt / e~Zt, (Powell et al., 2004), (6)

where N0 = estimated number of larvae at hatching;

Nt = number of larvae at time t (Nt= 1 because N0 was
calculated for each individual larva);

Z = cohort-specific daily instantaneous mortality
rate; and

t = age of larva in days.

Data analysis

Spatial and temporal variation in environmental condi-
tions and density of sailfish larvae was examined with a
two-way analysis of variance (ANOVA) (factors: oceano-
graphic feature and survey). Because of uneven repli-
cates in 2005 and 2006, separate one-way ANOVAs were
conducted to assess inter- and intra-annual variation in
length and age of sailfish with year or survey as a fixed
factor. In order to minimize heteroscedasticity, estimates
of density were log^+1 transformed, whereas standard
length and age data were loge transformed. In cases
where variances were unequal, nonparametric analyses
(Brown-Forsythe F-Test; Brown and Forsythe, 1974) were
performed; however, results were consistent with para-
metric tests (ANOVA) and thus only parametric analyses
are presented. Post-hoc differences among levels of the
main effect) s) were examined with Tukey’s honestly
significant difference (HSD) test when variances were
equal and with a Dunnett’s T3 test when variances were
unequal (Zar, 1996). Analysis of covariance (ANCOVA)
was used to test for spatial and temporal variations in
growth and mortality (covariate: age) with models to
determine if the slopes of the regression lines differed
(slopes test). All data analyses were performed with
SPSS, vers. 15.0 (SPSS Inc., Chicago, IL) with a=0.05.

Results

Environmental conditions

Spatial and temporal variations in environmen-
tal conditions were observed during Gulf collections.
Temperatures were not significantly different among
oceanographic features (ANOVA, F(3 270)= 2.2, P=0.09),
albeit temperature was lowest within cyclones (28.2°C)
compared with other oceanographic features (28.9-
29.3°C) (Table 1). Mean temperature was 28.8°C and
29.4°C in 2005 and 2006, respectively, and varied signifi-
cantly among the five surveys (ANOVA, F{4 270)=354.0,

482

Fishery Bulletin 108(4)

Table 2

Mean environmental conditions (± standard deviation [SD]) for ichthyoplankton surveys in the northern Gulf of Mexico in
2005 and 2006. Environmental parameters were recorded at the surface for each sampling station. Dissolved oxygen is
not reported for the August 2006 survey because of a probe malfunction (NA).

Year

Survey

Date

Temperature (°C)

Salinity (ppt)

Dissolved oxygen (mg/L)

2005

May

17-22

26.4(0.9)

35.5 (0.7)

7.1 (0.7)

July

23-28

30.4(0.7)

35.2(1.3)

6.8 (1.2)

September

16-19

29.8(0.6)

36.5 (0.6)

6.3 (0.4)

All surveys

28.8(2.0)

35.6 (1.1)

6.8 (1.0)

2006

June

15-20

28.7 (0.5)

35.8 (0.4)

6.6 (0.1)

August

31 July- 5 Aug

30.1 (0.3)

36.2(0.4)

NA

All surveys

29.4(0.8)

36.0 (0.5)

NA

Table 3

Total catch, frequency of occurrence, and density (± standard deviation [SD] ) of sailfish ( Istiophorus platypterus ) larvae collected
from the northern Gulf of Mexico in 2005 and 2006 arranged by survey. Number of stations during each survey (n) shown. Per-
cent frequency of occurrence was based on collection stations during each survey that yielded 1 or more larvae.

Survey

n

Sailfish

catch

Frequency of
occurrence

Density

(± SD) (no. /1000m2)

Maximum

density

Larvae/hour

May 2005

60

212

26.7

0.6 (1.8)

10.5

10.6

July 2005

62

755

56.5

2.1 (7.5)

51.4

36.5

Sept 2005

39

134

46.2

0.6 (1.3)

4.5

10.3

June 2006

62

691

48.4

2.0 (4.7)

22.1

33.4

Aug 2006

65

634

47.0

1.7 (3.0)

10.2

25.4

Total

288

2426

45.0

1.5 (4.5)

24.4

PcO.Ol) (Table 2). Spatial variation in salinity was
detected among oceanographic features (ANOVA, Pl3
270)=16.8, PcO.Ol), and lowest salinity observed within
open ocean and cyclonic features (35.5 ppt and 35.6 ppt,
respectively) and higher salinity in anticyclonic and fron-
tal features (36.1 ppt and 36.1 ppt, respectively) (Table
1). Mean salinity was 35.6 ppt and 36.0 ppt in 2005
and 2006, respectively, and significant variation was
observed among the five surveys (ANOVA, P(4 270) =11.1,
PcO.Ol) (Table 2). Dissolved oxygen (DO) varied sig-
nificantly among oceanographic features (ANOVA, P(3
270)=2.7, P=0.048) and surveys (ANOVA, P(4 270)=38.9,
PcO.Ol) (Table 2). Lower DO levels were observed within
anticyclones, fronts, and the open ocean (6.8 mg/L, 6.6
mg/L, and 6.7 mg/L, respectively) compared to those
within cyclonic features (7.2 mg/L) (Table 1).

Spatial and temporal patterns of abundance

A significant interaction effect between oceanographic
feature and survey on the density of sailfish was detected
(ANOVA, F(10 271)=2.1, P=0.02), and highest densities
were observed within frontal features in three of five
surveys and in the open ocean during the remaining
surveys (Fig. 1). No individual effect of oceanographic

feature or survey on density was observed (feature
P=0.06, survey P=0.11), although density was lowest
within cyclones during all surveys. When data from all
surveys were combined, significant spatial variation
in the density of sailfish among oceanographic features
was observed (ANOVA, P(3 285)=3.3, P=0.02); density
within cyclones was lower than that within other fea-
tures (P<0.05).

Frequency of occurrence and relative abundances
were highest in June (48.4%), July (56.5%), and August
(47.0%) surveys and lowest during the May 2005 survey
(26.7%) (Table 3). The overall density of sailfish was 1.5
larvae per 1000 m2; lowest densities were observed in
May and September 2005 surveys (0.6 larvae per 1000
m2 and 0.6 larvae per 1000 m2, respectively) and higher
densities during July 2005 (2.1 larvae per 1000 m2),
June 2006 (2.0 larvae per 1000 m2), and August 2006
(1.7 larvae per 1000 m2) (Table 3). Catches peaked in
July 2005 and June 2006 when maximum densities of
51.4 larvae per 1000 m2 and 22.1 larvae per 1000 m2
were observed, respectively (Table 3). The overall catch
per unit of effort (CPUE) for sailfish in the northern
Gulf was 24.4 larvae per hour, and highest CPUEs
were reported for July 2005 (36.5), June 2006 (33.4),
and August 2006 (25.4) (Table 3).

Simms et al.: Distribution, growth, and mortality of larval Istiophorus platypterus in the northern Gulf of Mexico

483

Table 4

Exponential growth models arranged by survey
and oceanographic feature for sailfish (Istiopho-
rus platypterus) larvae collected from the northern
Gulf of Mexico in 2005 and 2006. Number of larvae
collected within each feature is given ( n ). Cyclones
excluded from analysis because of low sample sizes
within this type of feature. * indicates significant
growth difference among features.

Survey

Feature

n

Growth model

July 2005

Anticyclone

135

1.289e0128(ase)

Front

45

1.458e° 122(agc)

Open ocean

108

1.331e0124(age)

June 2006

Anticyclone

21

1 7i3e°

Front

108

1.415e° 120<a^e)

Open ocean

118

1.526e0112(a^>

August

Anticyclone

131

1.682e0105(a^e,*

2006

Front

166

1.480e° u4(a«e)

Open ocean

149

1.442e° 117(a^e)*

Sailfish length and age distributions

No significant difference in mean standard lengths
of sailfish was observed between 2005 (5.1 mm,
standard deviation [SD]=2.1) and 2006 (4.9 mm,
SD=2.0) (ANOVA, F(1 2352)= 3.3, P-0.07) (Fig. 2).
Sailfish were most abundant in the 3-6 mm size
range, with 70.4% and 65.9% of the catch in this
size range in 2005 and 2006, respectively. Intra-
annual differences in mean lengths of sailfish were
observed in 2005 (ANOVA, F(2 1034)=62.6, PcO.Ol)
and 2006 (ANOVA, F(1 1315)=75.8, PcO.Ol); small-
est mean lengths were observed in May 2005 (4.1
mm, SD-1.6) and June 2006 (4.5 mm, SD-1.6),
and larger larvae were collected in July 2005 (5.4
mm, SD-2.2) and August 2006 (5.4 mm, SD-2.3).

Mean ages were statistically similar between
2005 (10.1 days, SD-3.1 days) and 2006 (10.5
days, SD-3.2) (ANOVA, F(1 1234)=2.7, P-0.10)

(Fig. 2). Sailfish larvae were most abundant in
the 7-11 day range, with 60.7% and 53.9% of
the catch in this age range in 2005 and 2006,
respectively. Significant intra-annual variation
in sailfish mean ages was observed in 2005
(ANOVA, P(2 521)=51.6, PcO.Ol) and 2006 (ANOVA,
F(\ 7ioi=47.9, P<0.01), when youngest mean age was ob-
served in May 2005 (8.0 days, SD-2.3) and June 2006
(9.4 days, SD-3.1), and older larvae were observed in
July 2005 (11.0 days, SD-3.3) and August 2006 (11.0
days, SD-3.1).

Spatial and temporal patterns of growth

Spatial variation in growth was analyzed across oceano-
graphic features (anticyclone, front, and open ocean) for
three of the five surveys, and significant differences in

100 -i

□

Anticyclone

■

Open ocean

0

Front

□

Cyclone

May 2005 July 2005 September June 2006 August

surveys

2005

2006

100

w 2

03 to
CO CD

2 ^
o a

<D

75

50

25

& 2

B

i

M

May 2005 July 2005 September June 2006 August All
2005 2006

surveys

2005

2006

Figure t

(A) Percentage of sample collections of sailfish (Istiophorus
platypterus) conducted within each oceanographic feature
during ichthyoplankton surveys the northern Gulf of Mexico
in 2005 and 2006. (B) Percentage of sailfish larvae collected
within each oceanographic feature. (C) Mean density of sail-
fish larvae within each feature. Error bars represent one
standard deviation (SD).

growth were observed during August 2006 collections
(Table 4). Cyclones were excluded from our analysis
because of low sample sizes within this type of feature.
During the August 2006 survey, daily instantaneous
growth rates (g) of larvae collected within anticyclones
(g= 0.105) was significantly slower than growth of larvae
collected in the open ocean (g=0.117) (ANCOVA, slopes,
F(2 44o>=3-4’ P-0.03) (Table 4). In contrast, growth did
not differ significantly among the three features in July
2005 (anticyclones g=0.128, fronts g=0.122, and open
ocean g= 0.124) and June 2006 (anticyclones g-0.101,
fronts g-0.120, and open ocean g-0.112) (ANCOVA,

484

Fishery Bulletin 108(4)

slopes, F{ 2 282)=®-^’ F=0.67 and ANCOVA, slopes, F(2
241)=2.5, P=0.09, respectively).

Interannual differences in daily instantaneous growth
rates of sailfish were detected between 2005 {g= 0.123)
and 2006 (g=0.114) (ANCOVA, slopes, F(1 i205)=21.4,
P<0.01) (Fig. 3). Further, significant intra-annual varia-
tion in growth was observed in 2005 (ANCOVA, slopes,
F[2 507) = 5.1, P=0.01); larvae collected in September
(g- 0.113) displayed slower growth than larvae collected
in July (g=0.127) (Fig. 4). In contrast, growth was sta-
tistically similar between surveys in 2006 (ANCOVA,
slopes, F(1 692)=0-7, P=0.39).

Temporal variation in mortality

Estimates of daily instantaneous mortality (Z) did not
differ significantly between 2005 (Z=0.288) and 2006

(Z=0.394) (ANCOVA, slopes, P(1 46)=1.0, P=0.33) (Fig.
5, Table 5). Mortality rates ranged from 0.228 to 0.345
among survey periods in 2005, but rates were statisti-
cally similar (ANCOVA, slopes, P(2 24)=2.1, P=0.15)
(Fig. 6). Further, mortality rates were not significantly
different between survey periods in 2006, ranging from
0.344 in June to 0.381 in August (ANCOVA, slopes, F(1
16)=0.5, P=0.48).

Production potential (G.Z)

Instantaneous weight-specific growth coefficients ( G )
were 0.371 in 2005 and 0.347 in 2006, and G was indexed
to daily instantaneous mortality (Z) to assess stage-
specific production potential, G.Z (Table 5). Annual
estimates of G.Z were 1.29 in 2005 and 0.88 in 2006.
Production potential was highest in May 2005 (1.30) and
July 2005 (1.66). In contrast, G.Z ratios of
the September 2005 (1.01), June 2006 (1.02),
and August 2006 (0.91) surveys were lower.

400

300

200

ioo-

2005

10

120

100

- 80

- 60

- 40

25

400

300

200

ioo-

2006

120

- 80

60

- 40

- 20

0 5 10 15 20 25

Standard length (mm)/age (days)

Figure 2

Standard length and age-frequency distributions of sailfish ( Istiopho -
rus platypterus) larvae collected from the northern Gulf of Mexico
in 2005 and 2006. Standard length distributions are shown in dark
bars (n = 1037 and n = 1317 in 2005 and 2006, respectively). Age
distributions are shown in light bars (n = 524 and n=712 in 2005
and 2006, respectively). Note: 72 larvae indicated in Table 2 were
damaged and no length measurements were taken for these larvae.

Hatch-date distribution

Age-based estimates of hatch date indicated
that sailfish in our collections were spawned
from May to September (Fig. 7). Hatching of
sailfish peaked in mid-July, and the majority
of larvae hatched in July: 56.1% according to
back-calculated estimates, 73.4% according
to mortality adjusted estimates. The percent-
age of total catch from July for mortality-
adjusted hatch dates was 52.1% in 2005,
and 77.1% in 2006. Because the majority of
sailfish were <20 days of age and sampling
was conducted bimonthly, hatch-date dis-
tributions comprised multiple cohorts from
separate spawning events throughout the
spawning season.

Discussion

The relative abundance of sailfish larvae
collected in the present study was compa-
rable to or higher than values reported from
other putative spawning grounds of sailfish.
Llopiz and Cowen (2008), collected 7.3 sail-
fish larvae per hour in neuston tows over a
two-year period in waters of the Straits of
Florida; their catch rate was lower than the
catch rate of 27.4 sailfish larvae per hour
reported by Post et al. (1997) in the same
region. Further, Richardson et al. (2009b),
during a single week, reported a catch
rate of 298 sailfish larvae per hour in the
Straits of Florida; this catch rate indicates
that very high, but ephemeral, abundances
occur in this region. Catch rates of istio-
phorid billfishes (sailfish, white marlin,
and blue marlin) reported in other areas,

Simms et at: Distribution, growth, and mortality of larval Istiophorus platypterus in the northern Gulf of Mexico

485

including the Bahamas (Serafy et al., 2003) and
the Dominican Republic (Prince et al., 2005),
were less than 10 istiophorid larvae per hour,
which is markedly lower than rates reported in
our study for the Gulf of Mexico (24.4 sailfish
larvae per hour). Sailfish frequency of occur-
rence from the Gulf (45.0%) also corresponds
closely to the 41.1% occurrence reported in the
Straits of Florida and Bahamas by Luthy (2004),
which included all Atlantic billfishes. Although
CPUE was standardized for tow length, sampling
gear, and number of tows, variations in towing
methods as well as in the timing of sampling
may have affected differences in catch rates of
larvae. However, the relatively high catch rate of
sailfish larvae reported in our study supports the
premise that this region is an important spawn-
ing and nursery ground of sailfish — a contention
supported by high bycatch rates of adult sailfish
during summer months (NMFS1).

The highest density of larvae was reported
within mesoscale frontal features and highest
catch rates were observed from June through
August. Lowest densities of sailfish larvae were
observed in cold core features during all surveys;
however, as with other pelagic species (Richards
et al., 1993, Hoffmeyer et al., 2007), catches were
higher within fronts and anticyclones associated
with the western margin of the Loop Current.

In fact, highest densities were observed within
frontal features during three of five surveys and
over the course of all surveys combined. Higher
catches of marine fish larvae have been reported
at frontal features created by riverine discharge
or converging oceanic currents in both temper-
ate and tropical oceans (Hoffmeyer et al., 2007;
Richardson et al., 2009b). The accumulation of
larvae near or within fronts may simply be due
to hydrodynamic convergence which has been
shown to aggregate marine larvae in the Gulf
and other regions (Govoni and Grimes, 1992; Bakun,
2006). Alternatively, elevated primary and secondary
production within frontal features often increases the
availability of planktonic prey (Govoni et al., 1989;
Grimes and Finucane, 1991) and therefore may effect
higher survival for larvae within these oceanographic
features (Grimes and Finucane, 1991; Biggs, 1992).
In a recent study in the Straits of Florida, larval
sailfish density was observed to peak at eddy frontal
zones where there was a corresponding increase in
density of common sailfish prey items (Llopiz and
Cowen, 2008; Richardson et al., 2009b). This finding
supports the premise that larvae are more abundant
at fronts because of the increased availability of prey.
As with spatial trends in sailfish density, temporal
patterns in Gulf collections were comparable to those
in the Straits of Florida; sailfish larvae were more
abundant during spring and summer months (Post et
al., 1997; Luthy, 2004). Elevated catches of sailfish in
the summer correspond to peak spawning activity of

sailfish in the North Atlantic (de Sylva and Breder,
1997; Richardson, 2007).

Spatial variation in growth of sailfish was limited
despite elevated densities of sailfish larvae within
fronts. The general lack of growth variation in sailfish
among oceanographic features is somewhat unexpected
given that cyclonic and frontal features often display
increased primary productivity relative to anticyclones
(Grimes and Finucane, 1991; Biggs, 1992) and that
growth variation during early life is influenced by pri-
mary productivity and prey availability (de Vries et
al., 1990; Wexler et al., 2007). The lack of variation
in growth among oceanographic features may be at-
tributed to the fact that larvae in the northern Gulf
likely spend time in multiple oceanographic features
during early life. Oceanographic currents in this re-
gion have been observed to have speeds up to 0.8 me-
ters per second (69.1 kilometers per day) (Govoni and
Grimes, 1992), and higher velocity currents have been
recorded within the Loop Current (1.0 meters per sec-

486

Fishery Bulletin 108(4)

Figure 4

Size-at-age relationships of sailfish ( Istiophorus platypterus ) larvae collected from the
northern Gulf of Mexico in 2005 and 2006 arranged by survey. Age in days was determined
from otolith microstructure analysis. Exponential equations are given.

Table 5

Instantaneous weight-specific growth ( G ) and mortality ( Z ) coefficients of sailfish ( Istiophorus platypterus ) larvae collected from
the northern Gulf of Mexico in 2005 and 2006. Percentage per day was calculated from instantaneous growth and mortality coef-
ficients. The G:Z index of stage-specific production potential is also shown.

Year

Survey

G

%/d ay

Z

%/day

G:Z

2005

May

0.371

44.9

0.285

24.8

1.30

July

0.378

45.9

0.228

20.4

1.66

September

0.347

41.5

0.345

29.2

1.01

All surveys

0.371

44.9

0.288

25.0

1.29

2006

June

0.351

42.0

0.344

29.1

1.02

August

0.347

41.5

0.381

31.7

0.91

All surveys

0.347

41.5

0.394

32.6

0.88

Simms et al.: Distribution, growth, and mortality of larval Istiophorus platypterus in the northern Gulf of Mexico

487

2005 (n=524)

LogeN, = 7.131 -0.288 (age)
r2 = 0.94

o 0

10

15

20

2006 (n =71 2)

Loge N, = 9.1 24 - 0.394(age)
r2 = 0.95

10

Age (days)

15

Figure 5

Regression plots of loge (abundances 1) on age for ten-day cohorts
of sailfish ( Istiophorus platypterus) larvae collected from the
northern Gulf of Mexico in 2005 and 2006. Regression equations
and plots are arranged by year.

ond; Vukovich and Maul, 1985), which indicate
that planktonic larvae may encounter multiple
oceanographic features during their planktonic
larval duration. Further, pelagic larvae from
broad oceanic areas have been reported to ac-
cumulate within frontal zones (Richards et al.,

1993; Bakun, 2006), making it difficult to de-
termine where individuals spend the majority
of their lives and therefore, in which feature(s)
most of their early growth occurs.

Estimated growth of sailfish in the Gulf
(g=0.113 to 0.127) varied temporally and rates
were comparable to or slightly slower than
those reported for sailfish in the Straits of
Florida (g=0.130 to 0.146; Luthy et al., 2005;
Richardson, 2007; Richardson et al., 2009a)
and blue marlin from the Bahamas (g= 0.098
to 0.125; Serafy et al., 2003; Sponaugle et al.,

2005) and the Straits of Florida (g=0.089 to
0.114; Sponaugle et al., 2005; Richardson,

2007). Observed differences in growth among
studies are minor and similarities are not un-
expected because the timing of collections and
environmental conditions between the regions
were comparable. Sampling in the Straits
of Florida was conducted between April and
September in waters ranging from 26.1°C to
30.6°C (Luthy et al., 2005; Richardson, 2007).

This range of temperatures is similar to tem-
peratures present in the Gulf during our May
to September sampling period (26.4-30.4 °C).
Moreover, observed ranges in salinity were
nearly the same between the Straits of Flor-
ida (34.0-36.7 ppt) and Gulf (35.2-36.5 ppt).
Temporal variations in growth of marine lar-
vae have been shown to be correlated with
temperature (Rilling and Houde, 1999), and the most
rapid growth of sailfish larvae was observed during
July 2005 when the warmest mean temperature was
reported. Nevertheless, the second fastest growth rate
for sailfish was observed during May 2005 when the
lowest mean temperature was reported. Thus, other
factors known to affect growth, such as density of con-
specifics or prey availability (Jenkins et al., 1991; Lang
et al., 1994; Wexler et al., 2007), may be responsible
for observed variations in growth of sailfish larvae.

Although intra-annual differences in mortality were
limited, losses were substantial throughout the early
life interval examined (Z = 0.23 to 0.38). Daily instan-
taneous mortality rates reported in our study are
10-45% lower than mortality rates for sailfish and
blue marlin larvae from the Straits of Florida and
Exuma Sound, Bahamas (Richardson et al., 2009a).
However, the losses reported in our study are compa-
rable to those of other pelagic larvae, such as bluefin
tuna ( Thunnus thynnus ) (Z=0.20; Rooker et al., 2007),
yellowfin tuna ( Thunnus albacares) (Z= 0.33; Lang et
al., 1994), and members of the suborder Scombroidei,
which includes tunas, billfishes, and the barracuda
Sphyraena barracuda (Z = 0.34; Houde and Zastrow,

1993). Predation has been observed to be a major
cause of mortality during the early life interval of pe-
lagic species (Leggett and Deblois, 1994; Houde, 2002)
and it may be responsible for high losses of sailfish
larvae. Recent studies indicate that istiophorids are
preyed upon by conspecifics and congeners (Llopiz and
Cowen, 2008; Tidwell, 2008) and, if so, cannibalism or
predation pressure by other istiophorids may represent
an important source of mortality for sailfish during
early life.

Observed G:Z ratios were greater than 1.0 during
all but the August 2006 survey, indicating conditions
were likely favorable for production during the life
stage examined. Houde and Zastrow (1993) reported a
mean G:Z ratio of 0.89 for marine fish larvae (pooled
across several taxa), which is lower than the range
reported in our study for sailfish (0.91-1.66). However,
indices reported for individual species or taxonomic
groups ranged from 0.26 to 2.42 for larvae abundant
in upwelling and shelf zones, indicating wide-ranging
stage-specific production potential for pelagic fishes.
Collection of larvae peaked in July and it is possible
that increased G:Z coincided with increased temper-
ature or prey availability, both of which have been

488

Fishery Bulletin 108(4)

August 2006 (n=459)

Loge A/, = 8.645 - 0.381 (age)
r2 = 0.94
Ns

o o

n

10 12 14 16 18 20

Age (days)

Figure 6

Regression plots of logp {abundance + 1 ) on age for ten-day cohorts of sailfish (Istiopho-
rus platypterus) larvae collected from the northern Gulf of Mexico in 2005 and 2006.
Regression equations and plots arranged by survey.

shown to increase stage-specific production potential
(Rilling and Houde, 1999).

Hatch dates of sailfish larvae collected in this study
indicate that spawning is protracted in the northern
Gulf and peak activity occurs during July. To date,
sailfish spawning has not been documented in the
northern Gulf, but sailfish are known to have pro-
tracted spawning in other regions of the Atlantic and
Pacific oceans (de Sylva and Breder, 1997; Chiang et
al., 2006; Richardson, 2007). Although the timing of
sampling likely influences hatch-date distributions of
sailfish in the Gulf, resulting in a multimodal distri-
bution, spawning has been shown to occur from May
to September in the western North Atlantic Ocean
(de Sylva and Breder, 1997) and from April to Sep-
tember in the eastern Pacific (Chiang et ah, 2006),
corresponding to the spawning range observed in this

study. Additionally, data from studies indicate that
peak spawning occurs in mid to late summer because
increased frequencies of mature ovaries have been ob-
served in sailfish landed in July and August (de Sylva
and Breder, 1997; Chiang et ah, 2006; Richardson et
al., 2009a).

Questions remain regarding the specific factors regu-
lating observed variations in distribution, growth, and
mortality of sailfish, as well as the extent of spawn-
ing in the northern Gulf. Regardless, high densities
and broad distributions of larvae combined with rapid
growth and high production potential indicate that
sailfish larvae spawned or hatched in the northern Gulf
potentially contribute to Atlantic sailfish populations.
This study provides strong evidence that the northern
Gulf serves as an important spawning and nursery
habitat for Atlantic sailfish.

Simms et al.: Distribution, growth, and mortality of larval Istiophorus platypterus in the northern Gulf of Mexico

489

-10.0

“0
CD
O
<D

5T

CO
CD
O

-5.0 £

<
a»

CD
zr
Q3_

o

IT
<D
Cl

— - 0.0
Oct. 1

Hatch date (month/day)

Figure 7

Hatch-date distribution of sailfish (Istiophorus platypterus ) larvae collected
from the northern Gulf of Mexico in 2005 (n=1037) and 2006 Cm. = 1317 ) (gray
bars). Larvae were pooled and arranged by month and day. Hatch dates were
determined by subtracting age from catch date. Otolith-derived ages were used
when available; remaining ages were predicted by applying age-length key. The
mortality-adjusted hatch-date distribution as a percentage of hatching events
per day (solid line) is also shown.

Acknowledgments

This work was supported by the McDaniel Charitable
Foundation, the National Oceanic and Atmospheric
Administration, and the Oceanic Conservation Organiza-
tion. We thank J. Alvarado Bremer, T. Potter, C. Pratt,
B. Saxton, T. Tidwell, and others for assistance in the
field and in the laboratory. J. Magnussen and M. Shivji
of Nova Southeastern University provided the genetic
identification protocol, and J. Graves and J. McDowell
of the Virginia Institute of Marine Science provided
training in identification of larvae. This work would not
have been possible without the support of J. Heldt who
provided the boat time. A. Anis, A. Armitage, and D.
Wells provided comments on the manuscript.

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491

Acknowledgment of reviewers

The editorial staff of Fishery Bulletin would like to acknowledge the scientists
who reviewed articles published in 2009-2010. Their contributions have helped
ensure the publication of quality science.

Joel Anderson
Roland Anderson
Francisco Arreguin-Sanchez
Peter J. Auster
Toby D. Auth

Jay Barlow

Gretchen Bath-Martin
David A. Beauchamp
Hugues P. Benoit
Barbara Block
Andre M. Boustany
Matt K. Broadhurst
John L. Butler

Jennifer Cahalan
Michael Cappo
Francois Chapleau
Yuk W. Cheng
David M. Clausen
Christina Conrath
Daniel W. Cooper

Dimitrios Damalas
Joseph T. DeAlteris
Edward E. DeMartini
Alejandro De Robertis
William B. Driggers III
Jennifer M. Dupont

Daniel L. Erickson

Elizabeth Fairchild
Rui Faria
Petter Fossum
Matt Friedman
Michael Frisk
Robert J. Fryer

Sarah K. Gaichas
Yongwen Gao
Graciela Garcia
Vladlena Gertseva
Anita Gilles
Christopher W. Glass

Joseph Godlewski
Humberto Gomez Hazin
John J. Govoni
Raymond E. Grizzle
Thomas Grothues
Angel Guerra

Robert W. Hannah
Christopher G. Hayes
Eliza Heery
Jon Heifetz
Ryan J. Heise
Scott A. Heppell
Alistair J. Hobday
Aleta A. Hohn
Scott A. Holt
Edward D. Houde
Carrie Hubard

Kevin H. Kelly
Jeff Kneebone

Thomas E. Laidig
Robert D. Lauth
R. Wilson Laney
Milton S. Love
Stuart Ludsin
Joanne Lyczkowski-Shultz

James A. MacDonald
John Martell
Richard S. McBride
Susanne McDermott
Richard D. Methot
Scott Meyer
Russell B. Millar
Jessica Miller
Henry Milliken
Adam Moles
Barbara A. Muhling
Keith D. Mullin
Thomas A. Munroe

Atsushi Nanami

Robert J. Olson
Olav A. Ormseth

Heather M. Patterson
William F. Patterson, III
Pierre Pepin
Mark S. Peterson
Alejandro D. Pettovello
Beth Phelan
Susan Picquelle
Kevin Piner
Arthur N. Popper
Michael H. Prager
Andre E. Punt

Chet F. Rakocinski
Pierre Richard
Marie-Joelle Rochet
Gregg Rosencranz
Rodney A. Rountree

Toshihiko Saito
Jason J. Schaffler
Joseph E. Serafy
Frank R. Shaw
Richard Shaw
Gregory B. Skomal
Steve J. Smith
Su Sponaugle
David Sterling
Molly Sturdevant
Chi-lu Sun

John F. Thedinga
Brian N. Tissot
Verena M. Trenkel

Terence I. Walker
Benjamin Walther
T. Mark Willette
Mark Wuenschel

Yimin Ye

492

Fishery Bulletin 108(4)

Fishery Bulletin index

Volume 108(1-4), 2010
List of titles

108(1)

1 A modeling approach to identify optimal habitat
and suitable fishing grounds for neon flying squid
( Ommastrephes bartramii) in the Northwest Pacific
Ocean, by Xinjun Chen, Siquan Tian, Yong Chen, and
Bilin Liu

15 Statistical inference about the relative efficiency of
a new survey protocol, based on paired-tow survey
calibration data, by Noel G. Cadigan and Jeff J.
Dowden

30 Effects of trawling for ocean shrimp (Pandalus jor-
dani) on macroinvertebrate abundance and diversity
at four sites near Nehalem Bank, Oregon, by Robert
W. Hannah, Stephen A. Jones, William Miller, and
Jayme S. Knight

39 Evaluation of the capture efficiency and size selec-
tivity of four pot types in the prospective fishery for
North Pacific giant octopus ( Enteroctopus dofleini),
by Patrick D. Barry, Sherry L. Tamone, and David A.
Tallmon

45 Larval development of the spotfin tonguefish (Sym-
phurus oligomerus Mahadeva and Munroe, 1990)
(Pleuronectiformes: Cynoglossidae) from the Gulf of
California, Mexico, by Ricardo J. Saldierna-Martinez,
Gerardo Aceves-Medina, and Enrique A. Gonzalez-
Navarro

56 Feeding ecology of Atlantic bluefin tuna ( Thunnus
thynnus ) in North Carolina: diet, daily ration, and
consumption of Atlantic menhaden ( Brevoortia
tyrannus ), by Christopher M. Butler, Paul J. Ruder-
shausen, and Jeffrey A. Buckel

70 Maturity and growth of female dusky rockfish
( Sebastes variabilis) in the central Gulf of Alaska,
by Elizabeth A. Chilton

79 Environmental characterization of seasonal trends
and foraging habitat of bottlenose dolphins (Tursiops
truncatus ) in northern Gulf of Mexico bays, by Cara
E. Miller and Donald M. Baltz

87 A molecular genetic investigation of the population
structure of Atlantic menhaden (Brevoortia tyran-
nus ), by Abigail J. Lynch, Jan R. McDowell, and John
E. Graves

98 Variation in the isotopic signatures of juvenile gray
snapper (Lutjanus griseus ) from five southern Flor-
ida regions, by Trika Gerard and Barbara Muhling

106 Assessing trends in the density of Atlantic croaker
(Micropogonias undulatus): a comparison of passive
acoustic and trawl methods, by Damon P. Gannon
and Janet G. Gannon

108(2)

1 19 Age and growth of spiny dogfish ( Squalus acanthias)
in the Gulf of Alaska: analysis of alternative growth
models, by Cindy A. Tribuzio, Gordon H. Kruse, and
Jeffrey T. Fujioka

136 Effective herding of flatfish by cables with minimal
seafloor contact, by Craig S. Rose, Carwyn F. Ham-
mond, and John R. Gauvin

145 Flatfish herding behavior in response to trawl
sweeps: a comparison of diel responses to conven-
tional sweeps and elevated sweeps, by Clifford H.
Ryer, Craig S. Rose, and Paul J. Iseri

155 Spatial and temporal variation in otolith chemistry
for tautog (Tautoga onitis) in Narragansett Bay and
Rhode Island coastal ponds, by Ivan Mateo, Edward
G. Durbin, David A. Bengtson, Richard Kingsley,
Peter K. Swart, and Daisy Durant

162 Fish assemblages associated with three types of
artificial reefs: density of assemblages and pos-
sible impacts on adjacent fish abundance, by Reiji
Masuda, Masami Shiba, Yoh Yamashita, Masahiro
Ueno, Yoshiaki Kai, Asami Nakanishi, Masaru Tor-
ikoshi, and Masaru Tanaka

174 Biomass and reproduction of Pacific sardine
(Sardinops sagax ) off the Pacific northwestern
United States, 2003-2005, by Nancy C. H. Lo, Bev-
erly J. Macewicz, and David A. Griffiths

193 Seasonal variability in ichthyoplankton abundance
and assemblage composition in the northern Gulf of
Mexico off Alabama, by Frank J. Hernandez Jr., Sean
P. Powers, and William M. Graham

208 Observer-reported skate bycatch in the commercial
groundfish fisheries of Alaska, by Duane E. Steven-
son and Kristy A. Lewis

218 Effects of starvation on energy density of juvenile
chum salmon (Oncorhynehus keta) captured in
marine waters of Southeastern Alaska, by Emily A.
Fergusson, Molly V. Sturdevant, and Joseph A. Orsi

List of titles

493

226 Accuracy of sex determination for northeastern
Pacific Ocean thornyheads ( Sebastolobus altivelis
and S. alascanus ), by Erica L. Fruh, Aimee Keller,
Jessica Trantham, and Victor Simon

233 Measurement errors in body size of sea scallops
( Placopecten magellanicus) and their effect on stock
assessment models, by Larry D. Jacobson, Kevin D. E.
Stokesbury, Melissa A. Allard, Antonie Chute, Brad-
ley P. Harris, Deborah Hart, Tom Jaffarian, Michael
C. Marino II, Jacob I. Nogueira, and Paul Rago

108(3)

251 Abundance of harbor porpoise ( Phocoena phocoena )
in three Alaskan regions, corrected for observer
errors due to perception bias and species misidenti-
fication, and corrected for animals submerged from
view, by Roderick C. Hobbs and Janice M. Waite

268 Effects of lunar cycle and fishing operations on
longline-caught pelagic fish: fishing performance,
capture time, and survival of fish, by Francois
Poisson, Jean-Claude Gaertner, Marc Taquet, Jean-
Pierre Durbec, and Keith Bigelow

282 Using experiments and expert judgment to model
catchability of Pacific rockfish in trawl surveys, with
application to bocaccio ( Sebastes paucispinis ) off
British Columbia, by Murdoch K. McAllister, Rich-
ard D. Stanley, and Paul Starr

305 Using productivity and susceptibility indices to
assess the vulnerability of United States fish stocks
to overfishing, by Wesley S. Patrick, Paul Spen-
cer, Jason Link, Jason Cope, John Field, Donald
Kobayashi, Peter Lawson, Todd Gedamke, Enric
Cortes, Olav Ormseth, Keith Bigelow, and William
Overholtz

323 Distribution and life history of two diminutive flat-
fishes, Citharichthys gymnorhinus and C. cornutus
(Pleuronectiformes: Paralichthyidae), in the western
NorthAtlantic,byThomasA.MunroeandSteveW.Ross

346 Age validation of great hammerhead shark (Sphyrna
mokarran ), determined by bomb radiocarbon analy-
sis, by Michelle S. Passerotti, John K. Carlson,
Andrew N. Piercy, and Steven E. Campana

352 Use of stereo camera systems for assessment of
rockfish abundance in untrawlable areas and for
recording pollock behavior during midwater trawls,
by Kresimir Williams, Christopher N. Rooper, and
Rick Towler

108(4)

365 Species compositions of elasmobranchs caught by three
different commercial fishing methods off southwestern
Australia, and biological data for four abundant bycatch
species, by Ashlee A. Jones, Norman G. Hall, and Ian C.
Potter

382 Ontogenetic patterns and temperature-dependent growth
rates in early life stages of Pacific cod ( Gadus macrocepha-
lus ), by Thomas P. Hurst, Benjamin J. Laurel, and Lorenzo
Ciannelli

393 Feeding ecology of juvenile Pacific salmon ( Oncorhynchus
spp.) in a northeast Pacific fjord: diet, availability of zoo-
plankton, selectivity for prey, and potential competition for
prey resources, by Stephen M. Bollens, Rian vanden Hooff,
Mari Butler, Jeffrey R. Cordell, and Bruce W. Frost

408 Movement patterns of winter flounder ( Pseudopleuronectes

americanus) in the southern Gulf of Maine: observations
with the use of passive acoustic telemetry, by Gregory R.
DeCelles and Steven X. Cadrin

420 Demographic characteristics of exploited tropical lutjanids:
a comparative analysis, by Michelle R. Heupel, Ashley J.
Williams, David J. Welch, Campbell R. Davies, Ann Penny,
Jacob P. Kritzer, Ross J. Marriott, and Bruce D. Mapstone

433 Asymmetric conservation benefits of circle hooks in mul-
tispecies billfish recreational fisheries: a synthesis of hook
performance and analysis of blue marlin (Makaira nigri-
cans) postrelease survival, by John E. Graves and Andrij
Z. Horodysky

442 Influence of ocean conditions on the timing of early life
history events for blue rockfish (Sebastes mystinus ) off
California, by Thomas E. Laidig

450 Abundance and distribution of Atlantic sturgeon ( Acipenser

oxyrinchus ) within the Northwest Atlantic Ocean, deter-
mined from five fishery-independent surveys, by Keith
J. Dunton, Adrian Jordaan, Kim A. McKown, David O.
Conover, and Michael G. Frisk

466 Day and night abundance, distribution, and activity pat-
terns of demersal fishes on Heceta Bank, Oregon, by Ted D.
Hart, Julia E. R. Clemons, W. Waldo Wakefield, and Selina
S. Heppell

478 Distribution, growth, and mortality of sailfish ( Istiophorus
platypterus) larvae in the northern Gulf of Mexico, by Jef-
frey R. Simms, Jay R. Rooker, Scott A. Holt, G. Joan Holt,
and Jessica Bangma

494

Fishery Bulletin 108(4)

Fishery Bulletin Index

Volume 108 (1-4), 2010
List of authors

Aceves-Medina, Gerardo 45
Allard, Melissa A. 233

Baltz, Donald M. 79
Bangma, J. 478
Barry, Patrick D. 39
Bengtson, David A. 155
Bigelow, Keith 268, 305
Bollens, Stephen M. 393
Buckel, Jeffrey A. 56
Butler, Christopher M. 56
Butler, Mari 393

Cadigan, Noel G. 15
Cadrin, Steven X. 408
Campana, Steven E. 346
Carlson, John K. 346
Chen, Xinjun 1
Chen, Yong 1
Chilton, Elizabeth A. 70
Chute, Antonie 233
Ciannelli, Lorenzo 382
Clemons, Julia E. R. 466
Conover, David O. 450
Cope, Jason 305
Cordell, Jeffrey R. 393
Cortes, Enric 305

Davies, Campbell R. 420
DeCelles, Gregory R. 408
Dowden, Jeff J. 15
Durant, Daisy 155
Durbec, Jean-Pierre 268
Dunton, Keith J. 450
Durbin, Edward G. 155

Fergusson, Emily A. 218
Field, John 305
Frisk, Michael G. 450
Frost, Bruce W. 393
Fruh, Erica L. 226
Fujioka, Jeffrey T. 119

Gaertner, Jean-Claude 268
Gannon, Damon P. 106
Gannon, Janet G. 106
Gauvin, John R. 136
Gedamke, Todd 305
Gerard, Trika 98
Gonzalez-Navarro, Enrique A. 45
Graham, William M. 193
Graves, John E. 87

Griffiths, David A. 174
Graves, John E. 433
Hall, Norman G. 365
Hammond, Carwyn F. 136
Hannah, Robert W. 30
Harris, Bradley P. 233
Hart, Deborah 233
Hart, Ted D. 466
Heppell, Selina S. 466
Hernandez, Frank J., Jr. 193
Heupel, Michelle R. 420
Hobbs, Roderick C. 251
Holt, G. Joan 478
Holt, Scott A. 478
Horodysky, Andrij Z. 433
Hurst, Thomas P. 382

Iseri, Paul J. 145

Jacobson, Larry D. 233
Jaffarian, Tom 233
Jones, Ashlee A. 365
Jones, Stephen A. 30
Jordaan, Adrian 450

Kai, Yoshiaki 162
Keller, Aimee 226
Kingsley, Richard 155
Knight, Jayme S. 30
Kobayashi, Donald 305
Kritzer, Jacob P. 420
Kruse, Gordon H. 119

Laidig, Thomas E. 442
Laurel, Benjamin J. 382
Lawson, Peter 305
Lewis, Kristy A. 208
Link, Jason 305
Liu, Bilin 1
Lo, Nancy C. H. 174
Lynch, Abigail J. 87

Macewicz, Beverly J. 174
Mapstone, Bruce D. 420
Marino, Michael C., II 233
Marriott, Ross J. 420
Masuda, Reiji 162
Mateo, Ivan 155
McAllister, Murdoch K. 282
McDowell, Jan R. 87
McKown, Kim A. 450
Miller, Cara E. 79

Miller, William 30
Muhling, Barbara 98
Munroe, Thomas A. 323

Nakanishi, Asami 162
Nogueira, Jacob I. 233

Ormseth, Olav 305
Orsi, Joseph A. 218
Overholtz, William 305

Passerotti, Michelle S. 346
Patrick, Wesley S. 305
Penny, Ann 420
Piercy, Andrew N. 346
Poisson, Francois 268
Potter, Ian C. 365
Powers, Sean P. 193

Rago, Paul 233
Rooker, Jay R. 478
Rooper, Christopher N. 352
Rose, Craig S. 136, 145
Ross, Steve W. 323
Rudershausen, Paul J. 56
Ryer, Clifford H. 145

Saldierna-Martinez, Ricardo J. 45

Shiba, Masami 162

Simms, Jeffrey R. 478

Simon, Victor 226

Spencer, Paul 305

Stanley, Richard D. 282

Starr, Paul 282

Stevenson, Duane E. 208

Stokesbury, Kevin D. E. 233

Sturdevant, Molly V. 218

Swart, Peter K. 155

Tallmon, David A. 39
Tamone, Sherry L. 39
Tanaka, Masaru 162
Taquet, Marc 268
Tian, Siquan 1
Torikoshi, Masaru 162
Towler, Rick 352
Trantham, Jessica 226
Tribuzio, Cindy A. 119

Ueno, Masahiro 162

vanden Hooff, Rian 393

Waite, Janice M. 251
Wakefield, W. Waldo 466
Welch, David J. 420
Williams, Ashley J. 420
Williams, Kresimir 352
Yamashita, Yoh 162

495

Fishery Bulletin Index

Volume 108(1-4), 2010
List of subjects

Abundance 478
Atlantic croaker 106
harbor porpoise 251
Acipenser oxyrinchus - see sturgeon,
Atlantic

Acoustic surveys, passive 106
Age 478

Age validation 346
Ages, daily 442

Aggregations (Atlantic sturgeon) 450
Alabama 193
Alaska 39, 251
southeast 218
Aleutian Islands 208
management, area-based 450
Australia 365, 420

Bayesian statistics 282
Behavior
fish 352
groundfish 466
pollock 352
Bering Sea 208
Bias, perception 251
Billfishes 433
Bioacoustics 106
Biomass, estimates
daily egg production method 174
rockfish 352
swept-area method 174
Bocaccio 282
Body size 233

Bomb radiocarbon (aging) 346
Brevoortia

patronus - see menhaden, Gulf
tyrannus - see menhaden,

Atlantic
Bycatch 145
elasmobranchs 365
invertebrate 30
skates 208

California 442
Capture efficiency 39, 145
Catch per unit of effort (CPUE) 106
Catchability, trawl (rockfish) 282
Catch-and-release 433
Census, underwater visual 162
Chemical lightstick (effect on
swordfish CPUE) 268
Chesapeake Bay
(Atlantic menhaden) 87

China 1
Circle hooks 433
Citharichthys cornutus — see whiff,
horned

Citharichthys gymnorhinus -
see whiff, anglefin

Climate change (diminutive flatfishes)
323

Cod, Pacific 382
Condition index 218
Conservation (elasmobranchs) 365
Continental slope 226
Coral reef fishes 420
Croaker, Atlantic 106
Cryptomeria japonica - see Japanese
cedar

Cumulative prey curves 56

Cynoglossidae 45

Cytochrome c oxidase subunit I 87

Daily ration (Atlantic bluefin tuna)
56

Demersal fish 466

Diel, activity patterns (groundfish)

466

Diet

Atlantic bluefin tuna 56
juvenile salmon 393
Distribution 478

latitudinal (diminutive flatfishes)
323

Dogfish, spiny 119
Dolphin, bottlenose 79

Early life history 478
rockfish 442
Effects
mixed 15
random 15

Electivity (feeding) 393
Energy density 218
Enteroctopus dofleini — see octopus,
North Pacific giant
Error, measurement 233
Estuarine (salmonid feeding ecology)
393

Exterilium larvae 45

Feeding ecology (juvenile salmonids)
393
Fish

assemblage 162

behavior 145
larvae (seasonality) 193
length 233
measurement 233
Fishery

demersal 365
groundfish 208
Lutjanidae 420
octopus 39
recreational 433
Fishing

commercial longline 268
effort (neon flying squid) 1
grounds, identification of 1
swordfish 268
Flatfish 136
diminutive 323
Florida Bay (gray snapper) 98
Flounder, winter 478
Food limitation 218
Foraging, cetacean 79

Gadus macrocephalus — see cod,
Pacific

Gastric evacuation (Atlantic bluefin
tuna) 56

Gear modification (trawl) 136
Gear performance 145
Great Barrier Reef 420
Groundfish 466
fishery 208
Growth 478
dusky rockfish 70
elasmobranchs 119
rate 382
Growth model
fit 119

Gompertz 119
logistic 119
von Bertalanffy 119
Gulf of Alaska 70, 119, 208
Gulf of California, spotfin tonguefish
45

Gulf of Maine 408
Gulf of Mexico 193,478
bottlenose dolphin 79
Gulf menhaden 87

Habitat
analysis 442
cetacean 79
complexity 162
flatfish 136

nursery (gray snapper) 98
spawning (Pacific sardine) 174
spawning (winter flounder) 408
suitability index (HSI) 1
Heceta Bank 466
Herding, flatfish 136, 145
Hooking time (swordfish) 268

496

Fishery Bulletin 108(4)

Ichthyoplankton 478
survey 193
Istiophoridae 433
Istiophor'us platypterus — see sailfish

Japanese cedar 162
Juvenile

Pacific cod 382
settlement (rockfish) 442

Kajikia albida - see marlin, Atlantic
white

Larvae (Pacific cod) 382
Lengths at maturity (elasmobranchs)
365

Life history

diminutive flatfishes 323
Lutjanidae 420
strategies 305
Louisiana

Barataria Basin 79
bottlenose dolphin 79
Lunar index (swordfish CPUE) 268
Lutjanidae 420

Lutjanus griseus — see snapper, gray

Makaira nigricans - see marlin, blue
Marine

salmonid feeding ecology 393
protected areas 442
Marlin

Atlantic white 433
blue 433

Mass spectrometry (otolith) 98
Maturity (dusky rockfish) 70
Menhaden
Atlantic 56, 87
Gulf 87
Mexico 45

Microchemistry, otolith 98
Micropogonias undulatus - see
croaker, Atlantic
Microsatellites 87
Migration
corridors 450
winter flounder 408
Model

assessment 233

habitat suitability index (HSI) 1

Narragansett Bay 155
Natural tags 155
Nehalem Bank 30
Neuse River (Atlantic croaker) 106
North Carolina (Atlantic bluefin tuna)
56

Nursery 155

Octopus, North Pacific giant 39
Ommastrephes bartramii - see squid,
neon flying

Oncorhynchus keta - see salmon, chum
Oncorhynchus spp. 393
Ontogeny 382
Oregon 30
Otolith 442
chemistry 155
isotopic signatures 98
microstructure 478
Over-dispersion 15
Overfishing 305
Overlap (resource) 393

Pacific Ocean

northeastern 226
northwest 1

Pacific salmon, juvenile 393
Pandalus jordani - see shrimp, ocean
Phocoena phocoena - see porpoise,
harbor

Plaeopecten magellanicus — see
scallop, sea

Population, structure (menhaden)

87

Porpoise, harbor 251
Pot selectivity 39
Predator-prey relationship 56
Priors (prior probability distributions)
282

Productivity (fishery) 305
PSAT - see tag, pop-up satellite
archival

Pseudopleuronectes americanus -
see flounder, winter

Rajidae 208
Reef, artificial 162
Regression
binomial 15
logistic 15

Remotely operated vehicle (ROV) 466
Reproduction, dusky rockfish 70
Reunion Island 268
Rhode Island 155
Risk assessment 305
Rockfish 226
blue 442
dusky 70

Sailfish 478,478
Salmon, chum 218
Salmonid 393
Sardine, Pacific 174
Sardinops sagax — see sardine,

Pacific

Scallop, sea 233

SCUBA 233
Sea of Japan 162
Seafloor
habitat 30
mud 30
Sebastes

mystinus - see blue rockfish
paucispinis - see bocaccio
spp. 282

variabilis - see rockfish, dusky
Sebastolobus

alascanus — see thornyhead,
shortspine

altivelis - see thornyhead, longspine
spp. 226

Selectivity, gear (elasmobranchs) 365

Sex determination (thornyhead) 226

Shark, great hammerhead 346

Shrimp, ocean 30

Skates 208

Snapper, gray 98

Spatial

distributions 450
variation 15

Spawning habitat (winter flounder)
408

Species

compositions 365
misidentification 251
Sphyrna mokarran - see shark, great
hammerhead

Squalus acanthias - see dogfish, spiny

Squid, neon flying 1

Stable isotopes 155

Starvation 218

Stereo-camera 352

Stock

assessment (methods) 15
assessment (rockfish) 282
assessment (sea scallop) 233
data-poor 305
structure (menhaden) 87
Sturgeon, Atlantic 450
Survey
aerial 251

calibration (for stock assessments)
15

dredge (sea scallop) 233
fishery independent 450
ichthyoplankton 193
stereo-camera 352
techniques 352

underwater video (sea scallop) 233
untrawlable habitat 352
video 352
Survival
postrelease 433
rates (swordfish) 268

List of subjects

497

Susceptibility (fishery) 305
Sustainability (fish stock) 305
Swordfish 268
Symphurus oligomerus — see
tonguefish, spotfin

Tag, pop-up satellite archival 433
Tautog 155

Tautoga onitis — see tautog
Telemetry, acoustic 408
Temperature 382
Thornyhead
longspine 226
shortspine 226

Thunnus thynnus — see tuna, Atlantic
bluefin

Tide index (swordfish CPUE) 268
Tonguefish
larval 45
spotfin 45
Trawl

otter 136
survey 174, 282
Trawling 136, 145, 365
impacts 30

Tuna, Atlantic bluefin 56
7 \irsiops truncatus — see dolphin,
bottlenose

Variables, environmental 79
Vertebral band counts 346
Vision 145

Vulnerability (fishery) 305
Whiff

anglefin 323
horned 323
Winter flounder 408

Xiphias gladius - see swordfish

Zooplankton 393

498

Fishery Bulletin

Guidelines for authors

Manuscript Preparation

Contributions published in Fishery Bulletin describe
original research in marine fishery science, fishery
engineering and economics, as well as the areas of
marine environmental and ecological sciences (including
modeling). Preference will be given to manuscripts that
examine processes and underlying patterns. Descriptive
reports, surveys, and observational papers may occa-
sionally be published but should appeal to an audience
outside the locale in which the study was conducted.
Although all contributions are subject to peer review,
responsibility for the contents of papers rests upon the
authors and not on the editor or publisher. Submission
of an article implies that the article is original and is not
being considered for publication elsewhere. Articles may
range from relatively short contributions (10-15 typed,
double-spaced pages, tables and figures not included)
to extensive contributions (20-30 typed pages). Manu-
scripts must be written in English; authors whose native
language is not English are strongly advised to have
their manuscripts checked by English-speaking col-
leagues before submission.

Title page should include authors’ full names and
mailing addresses and the senior author’s telephone,
fax number, and e-mail address, and a list of key words
to describe the contents of the manuscript. Abstract
should be limited to 200 words (one-half typed page),
state the main scope of the research, and emphasize
the author’s conclusions and relevant findings. Do not
review the methods of the study or list the contents of
the paper. Because abstracts are circulated by abstract-
ing agencies, it is important that they represent the
research clearly and concisely. Text must be typed in
12 point Times New Roman font throughout. A brief
introduction should convey the broad significance of
the paper; the remainder of the paper should be divided
into the following sections: Materials and methods,
Results, Discussion (or Conclusions), and Acknowl-
edgments. Headings within each section must be short,
reflect a logical sequence, and follow the rules of multi-
ple subdivision (i.e., there can be no subdivision without
at least two items). The entire text should be intelligible
to interdisciplinary readers; therefore, all acronyms,
abbreviations, and technical terms should be written
out in full the first time they are mentioned. Include
FAO common names for species in the list of keywords
and in the introduction. Regional common names may
be used throughout the rest of the text if they are dif-
ferent from FAO common names which can be found at
http://www.fishbase.org/search.html. Follow the U.S.
Government Printing Office Style Manual (2000 ed.)
and Scientific Style and Format: the CSE Manual for
Authors, Editors, and Publishers (7th ed.) for editorial

style; for fish nomenclature follow the most current
issue of the American Fisheries Society’s Common and
Scientific Names of Fishes from the United States,
Canada, and Mexico, 6th ed. Dates should be written
as follows: 11 November 2000. Measurements should
be expressed in metric units, e.g., 58 metric tons (t); if
other units of measurement are used, please make this
fact explicit to the reader. Write out the numbers zero
through nine unless they form part of measurement
units (e.g., nine fish but 9 mm). Refrain from using
the shorthand slash (/), an ambiguous symbol, in the
general text.

Literature cited comprises published works and
those accepted for publication in peer-reviewed litera-
ture (in press). Follow the name and year system for
citation format in the “Literature cited” section (that
is say, citations should be listed alphabetically by the
authors’ last names, and then by year if there is more
than one citation with the same authorship). If there is
a sequence of citations in the text, list chronologically:
(Smith, 1932; Green, 1947; Smith and Jones, 1985).
Abbreviations of serials should conform to abbreviations
given in Cambridge Scientific Abstracts (http://www.csa.
com/ids70/serials_source_list.php?ab=biolclast-set-c).
Authors are responsible for the accuracy and complete-
ness of all citations. Literature citation format: Author
(last name, followed by first-name initials). Year. Title
of report or manuscript. Abbreviated title of the series
to which it belongs. Always include number of pages.
Cite all software and special equipment or chemical
solutions used in the study, not in a footnote but within
parentheses in the text (e.g., SAS, vers. 6.03, SAS Inst.,
Inc., Cary, NC).

Tables are often overused in scientific papers; it
is seldom necessary or even desirable to present all
the data associated with a study. Tables should not
be excessive in size and must be cited in numerical
order in the text. Headings should be short but ample
enough to allow the table to be intelligible on its own.
All unusual symbols must be explained in the table
legend. Other incidental comments may be footnoted
with italic numeral footnote markers. Use asterisks to
indicate significance in statistical data. Do not type
table legends on a separate page; place them above the
table data. Do not submit tables in photo mode.

Figures include line illustrations, photographs (or
slides), and computer-generated graphs and must be
cited in numerical order in the text. Graphics should
aid in the comprehension of the text, but they should
be limited to presenting patterns rather than raw data.
Figures should not exceed one figure for every four
pages of text. Figures must be labeled with author’s
name and number of the figure. Avoid placing labels
vertically (except for y axis). Figure legends should
explain all symbols and abbreviations and should be
double-spaced on a separate page at the end of the
manuscript. Color is allowed in figures to show morpho-
logical differences among species (for species identifica-
tion), to show stain reactions, and to show gradations in
temperature contours within maps. Color is discouraged

Fishery Bulletin 108(4)

499

in graphs, and for the few instances where color may
be allowed, the use of color will be determined by the
Managing Editor.

• Zeros should precede all decimal points for values
less than one.

• Sample size, n, should be italicized.

• Capitalize the first letter of the first word in all labels
within figures.

• Do not use overly large font sizes in maps and for units
of measurements along axes in figures.

• Do not use bold fonts or bold lines in figures.

• Do not place outline rules around graphs.

• Use a comma in numbers of five digits or more (e.g.
13,000 but 3000).

• Maps require a North arrow and degrees latitude-
longitude (e.g., 170°E).

Failure to follow these guidelines
and failure to correspond with editors
in a timely manner will delay
publication of a manuscript.

Copyright law does not apply to Fishery Bulletin,
which falls within the public domain. However, if an

author reproduces any part of an article from Fishery
Bulletin in his or her work, reference to source is consid-
ered correct form (e.g., Source: Fish. Bull. 97:105).

Submission

Submit manuscript online at http://mc.manuscriptcental.
com/fisherybulletin. Commerce Department personnel
should submit papers under a completed NOAA Form
25-700. For further details on electronic submission,
please contact the Scientific Editorial Office directly at

julie.scheurer@noaa.gov

Once the manuscript has been accepted for publication,
you will be asked to submit a final electronic copy of your
manuscript. When requested, the text and tables should
be submitted in Word format. Figures should be sent as
PDF files, Windows metafiles, tiff files, or EPS files. Send
a copy of figures in the original software if conversion to
any of these formats yields a degraded version.

Questions? If you have questions regarding these
guidelines, please contact the Managing Editor, Sharyn
Matriotti, at

Sharyn.Matriotti@noaa.gov

Questions regarding manuscripts under review should
be addressed to Julie Scheurer, Associate Editor.

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