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Full text of "Fishery bulletin"

U.S. Department 
of Commerce 

Volume 92 
Number 1 
January 1994 




U.S. Department 
of Commerce 

Ronald H. Brown 
Secretary 

National Oceanic 
and Atmospheric 
Administration 

D. James Baker 
Under Secretary for 
Oceans and Atmosphere 

National Marine 
Fisheries Service 

Rolland A. Schmitten 
Assistant Administrator 
for Fisheries 




Scientific Editor 

Dr. Ronald W. Hardy 

Northwest Fisheries Science Center 
National Marine Fisheries Service, NOAA 
2725 Montlake Boulevard East 
Seattle, Washington 981 12-2097 




Editorial Committee 

Dr. Andrew E. Dizon National Marine Fisheries Service 
Dr. Linda L. Jones National Marine Fisheries Service 
Dr. Richard D. Methot National Marine Fisheries Service 
Dr. Theodore W. Pietsch University of Washington 
Dr. Joseph E. Powers National Marine Fisheries Service 
Dr. Tim D. Smith National Marine Fisheries Service 



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The Fishery Bulletin carries original research reports and technical notes on investiga- 
tions in fishery science, engineering, and economics. The Bulletin of the United States 
Fish Commission was begun in 1881; it became the Bulletin of the Bureau of Fisheries 
in 1904 and the Fishery Bulletin of the Fish and Wildlife Service in 1941. Separates 
were issued as documents through volume 46; the last document was No. 1 103. Begin- 
ning with volume 47 in 1931 and continuing through volume 62 in 1963, each separate 
appeared as a numbered bulletin. A new system began in 1963 with volume 63 in 
which papers are bound together in a single issue of the bulletin. Beginning with 
volume 70, number 1, January 1972, the Fishery Bulletin became a periodical, issued 
quarterly. In this form, it is available by subscription from the Superintendent of 
Documents, U.S. Government Printing Office, Washington, DC 20402. It is also 
available free in limited numbers to libraries, research institutions, State and Federal 
agencies, and in exchange for other scientific publications. 



U.S. Department 
of Commerce 

Seattle, Washington 

Volume 92 
Number 1 
January 1994 



Fishery 
Bulletin 



Biological laboratory/ 
Je Oceancgraphic Instituuo,, 
Library 

B 2 3 1994 



Contents 



Woods Hole, MA 02543 



1 Barbieri, Luiz R., Mark E. Chittenden Jr., and 

Cynthia M. Jones 

Age, growth, and mortality of Atlantic croaker, Micropogonias 
undulatus, in the Chesapeake Bay region, with a discussion of 
apparent geographic changes in population dynamics 

1 3 Bigelow, Keith A. 

Age and growth of the oceanic squid Onychoteuthis 
borealyaponica in the North Pacific 

26 Burke, Vincent J., Stephen J. Morreale, and 

Edward A. Standora 

Diet of the Kemp's ridley sea turtle, Lepidochelys kempu, 
in New York waters 

33 Ditty, James G., and Richard F. Shaw 

Larval development of tripletail, Lobotes sunnamensis (Pisces: 
Lobotidae), and their spatial and temporal distribution in the 
northern Gulf of Mexico 

46 Ferreira, Beatrice Padovani, and 

Garry R. Russ 

Age validation and estimation of growth rate of the coral trout, 
Plectropomus leopardus. (Lacepede 1 802) from Lizard Island, 
Northern Great Barrier Reef 

58 Gold, John R., and Linda R. Richardson 

Genetic distinctness of red drum [Sciaenops ocellatus) from 
Mosquito Lagoon, east-central Florida 

67 Incze, Lewis S., and Terri Ainaire 

Distribution and abundance of copepod naupln and other small 
(40-300 (im) zooplankton during spring in Shelikof Strait, Alaska 



Fishery Bulletin 92(1), 1994 



79 Jaenicke, Herbert W., and Adrian G. Celewycz 

Marine distribution and size of juvenile Pacific salmon in Southeast Alaska and northern 
British Columbia 

91 Johnson, Allyn G., William A. Fable Jr., Churchill B. Grimes, Lee Trent, 

and Javier Vasconcelos Perez 

Evidence for distinct stocks of king mackerel, Scomberomorus cavalla, in the Gulf of Mexico 

102 Milton, David A., Stephen J. M. Blaber, and Nicholas J. F. Rawlinson 

Reproductive biology and egg production of three species of Clupeidae from Kiribati, tropical 
central Pacific 

122 Perryman, Wayne L., and Morgan S. Lynn 

Examination of stock and school structure of striped dolphin [Stenella coeruleoalba) in the eastern 
Pacific from aerial photogrammetry 

132 Punsly, Richard G., Patrick K. Tomlinson, and Ashley J. Mullen 

Potential tuna catches in the eastern Pacific Ocean from schools not associated with dolphins 

144 Sinclair, Elizabeth, Thomas Loughlin, and William Pearcy 

Prey selection by northern fur seals (Callorhinus ursinus) in the eastern Bering Sea 

157 Stone, Heath H., and Brian M. Jessop 

Feeding habits of anadromous alewives, Alosa pseudoharengus, off the Atlantic Coast of Nova Scotia 

171 Stoner, Allan W, and Kirsten C. Schwarte 

Queen conch, Strombus gigas, reproductive stocks in the central Bahamas: distribution and 
probable sources 

180 Wilber, Dara H. 

The influence of Apalachicola River flows on blue crab, Callinectes sapidus. in north Florida 

189 Fargo, Jeff, and Albert V. Tyler 

Oocyte maturation in Hecate Strait English sole (Pleuronectes vetulus) 

203 Polovina, Jeffrey J., and Gary T. Mitchum 

Spiny lobster recruitment and sea level results of a 1990 forecast 

206 List of recent NOAA Technical Reports NMFS 



Abstract. — Atlantic croaker, 
Micropogonias undulatus, col- 
lected from commercial catches in 
Chesapeake Bay and in Virginia 
and North Carolina coastal waters 
during 1988-1991 (n = l,967) were 
aged from transverse otolith sec- 
tions. Ages 1-8 were recorded, but 
eight-year-old fish were rare. Mar- 
ginal increment analysis showed 
that for ages 1-7, annuli are 
formed once a year during the pe- 
riod April-May. Otolith age read- 
ings were precise: >99% agree- 
ment within and between readers. 
Observed lengths-at-age were 
highly variable and growth rate 
decreased after the first year. De- 
spite the high variability in sizes- 
at-age, observed lengths for ages 
1-7 fit the von Bertalanffy growth 
model (r 2 =0.99; n=753) well. No 
differences in growth were found 
between sexes. Total annual in- 
stantaneous mortality (Z) esti- 
mated from maximum age and 
from a catch curve of Chesapeake 
Bay commercial catches ranged 
from 0.55 to 0.63. Our results do 
not indicate the existence of a 
group of larger, older Atlantic 
croaker in Chesapeake Bay com- 
pared with more southern waters 
and suggest that the hypothesis of 
a basically different population 
dynamics pattern for this species 
north and south of Cape Hatteras, 
North Carolina, should be reevalu- 
ated. 



Age, growth, and mortality of 
Atlantic croaker, Micropogonias 
undulatus, in the Chesapeake Bay 
region, with a discussion of 
apparent geographic changes \n 
population dynamics* 

Luiz R. Barbieri 

College of William and Mary, Virginia Institute of Marine Science 
Gloucester Point. Virginia 23062 

Present address: University of Georgia Marine Institute 

Sapelo Island. Georgia 31327 

Mark E. Chittenden Jr. 

College of William and Mary, Virginia Institute of Marine Science 
Gloucester Point, Virginia 23062 

Cynthia M. Jones 

Old Dominion University. Applied Marine Research LaPoratory 
Norfolk, Virginia 23529 



Manuscript accepted 12 August 1993 
Fishery Bulletin 92:1-12 (1994) 



The Atlantic croaker, Micropo- 
gonias undulatus (Linnaeus), is 
one of the most abundant inshore 
demersal fishes along the Atlantic 
and Gulf of Mexico coasts of the 
United States (Joseph, 1972). Al- 
though recent commercial and rec- 
reational catches have come prima- 
rily from the South Atlantic Bight 
and the Gulf of Mexico, Atlantic 
croaker still support important 
fisheries along the Mid-Atlantic 
coast, especially from Maryland to 
North Carolina (Wilk, 1981). In 
Chesapeake Bay, they are caught 
by commercial and recreational 
fishermen during late spring and 
early fall migrations and, to a 
lesser extent, during the summer. 
In winter, Atlantic croaker leave 
the Bay to overwinter off the coast 
of Virginia and North Carolina, 
where they are caught by otter 
trawl and gillnet fisheries (Haven, 
1959). 

Little is known about age, 
growth, and mortality of Atlantic 



croaker in the Middle Atlantic and 
Chesapeake Bay regions. Studies 
based on length frequencies (Ha- 
ven, 1957; Chao and Musick, 1977) 
require considerable subjective in- 
terpretation given the extended 
spawning period of Atlantic croaker 
(Morse, 1980; Warlen, 1982; Bar- 
bieri et al., unpubl. ms.) and the 
difficulty in distinguishing modal 
groups at older ages (White and 
Chittenden, 1977; Jearld, 1983). Al- 
though scale-ageing has also been 
used (Welsh and Breder, 1923; 
Wallace, 1940; Ross 1988), prob- 
lems in applying this method to 
Atlantic croaker have been widely 
reported (Roithmayr, 1965; Joseph, 
1972; Barger and Johnson, 1980; 
Barbieri, 1993). 

In this study we provide informa- 
tion on age, growth, and mortality 
of Atlantic croaker in the Chesa- 



* Contribution No. 1806 from the College of 
William and Mary, School of Marine Sci- 
ence/Virginia Institute of Marine Science, 
Gloucester Point, Virginia 23062 



Fishery Bulletin 92(1). 1994 



peake Bay region using a validated otolith-ageing 
method. We also evaluate the relationship between 
otolith size and fish size and age, and discuss the 
implications of using otoliths for ageing Atlantic 
croaker. Finally, based on current information on 
growth, and size and age compositions in Chesa- 
peake Bay, we discuss the hypothesis of White and 
Chittenden (1977) and Ross (1988) regarding the 
existence of a basically different population dynam- 
ics pattern for Atlantic croaker north and south of 
Cape Hatteras, North Carolina. 



Methods 

Atlantic croaker were collected between June 1988 
and June 1991 from commercial pound-net, haul- 
seine, and gillnet fisheries which operate from early 
spring to early fall in Chesapeake Bay. Local fish 
processing houses and seafood dealers were con- 
tacted weekly or fortnightly, and one 22.7-kg (50-lb) 
box of fish of each available market grade (small, 
medium, or large) was purchased. Although boxes 
of fish were not randomly selected, Chittenden 
(1989) found only minor among-box differences in 
Atlantic croaker length compositions in pound-net 
and haul-seine catches. Because nearly all variation 
in size compositions was captured by the within-box 
variation, box selection did not present a problem. 

Since Atlantic croaker migrate from Chesapeake 
Bay in early fall to overwinter offshore (Haven, 
1959), samples for the period November-March 
were obtained from commercial trawlers which op- 
erate in Virginia and North Carolina shelf waters. 
Young of the year (90-114 mm total length, TL) used 
to validate the first annulus on otoliths were ob- 
tained from the Virginia Institute of Marine Science 
juvenile bottom trawl survey. 

Fish were measured for total length (TL, ±1.0 
mm), weighed for total weight (TW, ±1.0 g), sexed, 
and both sagittal otoliths removed and stored dry. 
The left otolith was transversely sectioned through 
the core with the diamond blade of a Buehler low- 
speed Isomet saw. Sections 350-500 urn thick were 
mounted on glass slides with Flo-texx clear mount- 
ing medium and read under a dissecting microscope 
(6-12x) with transmitted light and bright field, with 
the exception of samples from the period April-May, 
when sections were also read with reflected light 
and dark field to help identify the last annulus. 

Ages were assigned based on annulus counts; 
January 1 was taken as an arbitrary average 
birthdate when fish from one age class were as- 
signed to the next oldest (Jearld, 1983). Although 
the average spawning date (average biological 



birthdate) of Atlantic croaker in the Chesapeake Bay 
region occurs in September (Barbieri et al., unpubl. 
ms.), we chose, for ageing purposes, to use January 
1 as the average birthdate because annuli are 
formed during the period April-May (see Age deter- 
mination below). To assess ageing precision, all 
otolith sections (n- 1,967) were read twice by each 
of two readers, and agreement between readings and 
readers evaluated by percent agreement. All dis- 
agreements were resolved by a third reading with 
both readers. 

Annuli were validated by the marginal increment 
method (Bagenal and Tesch, 1978). For each age, the 
translucent margin outside the proximal end of the 
last annulus was measured along the ventral side 
of the otolith sulcal groove (Fig. 1). Measurements 
(±0.02 mm) were taken with an ocular micrometer 
at 25x. 

To evaluate growth, observed lengths at ages 
1-7 were fit to the von Bertalanffy model (Ricker, 
1975) by using nonlinear regression (Marquardt 
method). Model parameters were the following: L m , 
the mean asymptotic length; K, the Brody growth 
coefficient; and t () , the hypothetical age at which a 
fish would have zero length (Ricker, 1975). To cor- 
rect for growth after the time of annulus formation, 
only data for September, the peak spawning and 
thus average biological birthdate for Atlantic 
croaker in the Chesapeake Bay region (Barbieri et 
al., unpubl. ms.), were used for growth analysis. 

To evaluate changes in otolith size relative to fish 
length and age, 30 randomly selected otoliths per 
age, for ages 1-7 ( 198^100 mm TL), were measured 
for maximum length (OL, ±0.05 mm) and maximum 
thickness (OT, ±0.05 mm), and weighed (OW, 
± 0.001 g). After sectioning, otoliths were measured 
for otolith radius (OR, ±0.02 mm), defined as the dis- 
tance between the center of the core and the otolith 
outer edge along the ventral side of the sulcal groove 
(Fig. 1). Relationships between otolith measure- 
ments and fish TL were evaluated by regression 
analysis. The effect offish age on these relationships 
was evaluated by analysis of covariance (ANCOVA). 

Linear regression was used to determine a length- 
weight relationship for fish ranging from 152 to 400 
mm TL (36.3 to 967.0 g TW). Difference between 
sexes was tested by ANCOVA. The hypothesis of 
isometric growth (Ricker, 1975) was tested by t-test. 

Instantaneous total annual mortality rates, Z, 
were estimated from maximum age by using 
Hoenig's pooled regression equation (Hoenig, 1983), 
by calculating a theoretical total mortality for the 
entire lifespan following the reasoning of Royce 
(1972), and by the regression method with a catch 
curve of combined pound-net, haul-seine, and gillnet. 



Barbieri et al.: Age, growth, and mortality of Micropogonias undulatus 



Proximal 



Ventra 




Figure 1 

Transverse otolith section of an 8-year-old Atlantic croaker caught in Sep- 
tember 1988 in Chesapeake Bay. Arrows indicate annuli. The translu- 
cent zone beyond the last annulus represents additional growth after the 
annulus was formed during April-May. SG =sulcal groove, a = artifact 
of preparation. Ventral and proximal indicate axes of orientation. 



data for all recruited ages having five or more fish 
(Chapman and Robson, 1960). To avoid sampling 
bias associated with individual gears, we considered 
the age-frequency distribution obtained from data 
from combined gears as the best estimate of Atlan- 
tic croaker age composition in Chesapeake Bay 
(Ricker, 19751. Commercial trawl collections were 
not used in this analysis because they had different 
length compositions than the other gears and could 
be biased towards small fish. Because in catch curve 
analysis the age group represented by the apex of 
the catch curve may or may not be fully recruited 
to the gears (Everhart and Youngs, 1981), mortal- 
ity estimates were based on ages 3-7 only. Data 
from 1988 to 1991 were combined to minimize the 
effect of variation in year-class strength (Robson and 
Chapman, 1961). The right tail of the catch curve 
(Ricker, 1975) was tested for deviation from linear- 
ity by analysis of variance (ANOVA). Values of Z 
were converted to total annual mortality rates, A, 
by using the relationship A = 1 - e - z { Ricker, 1975). 
All statistical analyses were performed by using 
the Statistical Analysis System (SAS, 1988). Rejec- 
tion of the null hypothesis in statistical tests was 
based on a=0.05. F-tests in ANCOVA were based on 
Type III sums of squares (Freund and Littell, 1986). 



Assumptions of linear models were checked by re- 
sidual plots as described in Draper and Smith 
( 1981). For the OL-TL, OW-TL, and TW-TL relation- 
ships, and for all ANCOVA and ANOVA analyses, 
data were log 10 -transformed to correct for non-lin- 
earity and heterogeneous variances. For the catch 
curve analysis, log e -transformed numbers at age 
were regressed on age. Unless otherwise indicated, 
back-transformed data and regression equations are 
presented in the results. 



Results 

Age determination 

Transverse otolith sections of Atlantic croaker show 
very clear, easily identified marks that can be used 
for ageing. Typical sections have an opaque core 
surrounded by a blurred opaque band composed of 
fine opaque and translucent zones (Fig. 1). This 
band represents the first annulus. The width of this 
annulus varies among fish, from a very narrow band 
that is almost continuous with the core, to a wide, 
well-defined band clearly separated from the core. 
Because of this variation in width and proximity to 



Fishery Bulletin 92(1). 1994 



the core, the first annulus is sometimes difficult to 
identify. Subsequent annuli are represented by eas- 
ily identified, narrow, opaque bands that alternate 
with wider translucent bands outside the proximal 
margin of the first annulus (Fig. 1). 

Annuli are formed on otoliths once a year in the 
period April-May. For ages 1-7, mean monthly 
marginal increment plots show only one minima 



during the year, indicating that only one annulus is 
formed each year (Fig. 2). The trough starts abruptly 
in April, a period when there is, in general, maxi- 
mum variation in the mean marginal increment, 
suggesting that some fish have begun to form the 
annulus while others have not. Lowest marginal 
increment values occurred in May, the most inten- 
sive period of annulus formation. Marginal incre- 



E 
E 



c 

CD 

E 

CD 
CJ 

c 

~co 
c 

en 

ca 



18 •' ,6 

ft* 



Age 1 



jsJ 



Age 2 



) I! 

1 



9 

rfj 


12 

rfi 


"1 17 


^rfl 


30 




IB 

i 


14 


12 



6 


I r 


5 


Age 3 

12 

snfin 


39 


12 

1 


9 


25 



1 

T 


4 
I 


Age 4 

7 

1 T 

| 1 : 23 |* 

10 '» 1*1 

: . ,. -if II 


27 




a 


10 



JFMAMJ JASOND 





3 


e 


Age 5 

21 


13 


7 


4 



* 




s 


4 
r5- 


Age 6 

32 


11 


8 


1 


1 



Age 7 



nnn 



Age 8 



H 



JFMAMJJASOND 



Months 

Figure 2 

Mean monthly marginal increment for Atlantic croaker ages 1-8 from the Chesa- 
peake Bay region, 1988-91. Vertical bars are ±1 standard error. Numbers above 
the bars are sample sizes. 



Barbien et al Age, growth, and mortality of Micropogonias undulatus 



ment values progressively rise to a somewhat stable 
maximum from October through March or April, 
indicating a period of little or no otolith growth. 
Because only two age-8 fish were collected, it was 
not possible to validate annuli beyond age 7. 

To confirm our interpretation that the blurred 
opaque band around the otolith core represents the 
first annulus, (i.e., that fish hatched in the fall form 
a mark during their first spring), otolith sections of 
young of the year (94-114 mm) collected during the 
period March-June were examined. All those col- 
lected in March-April were developing fine opaque 
marks around the core, and all those in May-June 
had an opaque mark already formed (Fig. 3). 

Otolith age readings were very precise, both 
within and between readers. Percent agreement was 




Figure 3 

Transverse otolith section of a young-of-the-year Atlan- 
tic croaker ( 114 mm TL) collected in June 1990 in Chesa- 
peake Bay. The arrow indicates the outer edge of the first 
annulus formed during the period April-May. SG=sulcal 
groove; Ve=ventral; Pr=proximal; a=artifact of preparation. 



99.5% for reader 1, 99.3% for reader 2, and 99.2% 
between readers. In all cases of disagreement, the 
difference never exceeded 1 year. Only one of the 
1,967 left otoliths sectioned was crystallized and 
could not be read. In that case, the right otolith was 
read. Difficulty in ageing Atlantic croaker from 
otolith sections did not increase with increasing age. 
However, proper identification of the first annulus 
was very important. All disagreements, independent 
of age, were due to problems in identifying the first 
annulus. 

Otolith size relative to fish size and age 

Changes in otolith size relative to fish size were not 
constant along all axes (Fig. 4). Otolith maximum 
length was the only axis that showed a linear, 
isometric increase with fish length. Otolith ra- 
dius, the axis along which annuli were read in 
transverse sections, showed a non-linear rela- 
tionship with fish length, and had the small- 
est r 2 of all variables (Fig. 4). The curvilinear 
relationship suggests that otolith growth rela- 
tive to fish growth slows down along this axis 
as fish get bigger. 

Despite its poor relationship with fish length, 
otolith radius showed a very strong linear re- 
lationship with fish age. An ANCOVA model 
showing length, age, and their interaction ex- 
plained 97% of the variation in otolith radius 
(Table 1). All factors in the model were highly 
significant (P<0.01). Similar models for otolith 
maximum length, maximum thickness, and 
weight were also highly significant and had 
high coefficients of determination (r 2 >0.85). 
However, significance for these models was due 
to fish length only, neither age nor the inter- 
action factor was significant. 

Growth 

Observed lengths varied greatly within ages 
(Fig. 5). Atlantic croaker showed a rapid in- 
crease in size during the first year, but annual 
growth rate greatly decreased during the sec- 
ond year, remaining comparatively low there- 
after (Fig. 5). On average, 64% of the cumula- 
tive total observed growth in length occurred 
in the first year and 84% was completed after 
two years. 

No differences in mean lengths at age were 
found between sexes (Mest at each age; P>0.05 
for all ages). Mean observed total lengths for 
pooled sexes were 201, 263, 274, 285, 290, 307, 
309, and 313 mm, for ages 1-8, respectively. 



Fishery Bulletin 92(1). 1994 



A B 


6 


OR = -3 90 + 03 TL - 001 TL 2 ^10- 


OT = -2.73 + 0.04 TL - 0.0004 TL 2 




r 2 = 43, P = 0001 £ 


r 2 = 65; P = 0001 


Radius (mm) 

O CO 


<D 

■■J^rr o 5 

•••-.?•••*.. "F 

M- E . 

X 

m q 


r 


) 250 500 250 500 


C D 


-201 

E 
p 


1 4 - 

OL = 1 91 + 04 TL 
r 2 = 80. P = 0001 


OW = -2  10 7 TL 262 
r 2 = 0.77; P = 0001 


length (r 
o 


■. •.:♦..- 


s 


aximum 


5 


0- 


5 


o.oJ 






c 


250 500 ° 250 500 


Total length (mm) 


Figure 4 


Scatter plots and fitted regression lines of different otolith measurements versus At- 


lantic croaker total length: (A) otolith radius (OR); (B) otolith maximum thickness 


(OT); (C) otolith maximum length (OL); and (D) otolith weight (OW). Sample size in 
each plot is 210. 



500 



E 
E 



c 

0) 

o 



250- 



145 72 



46 



143 



170 



168 



Age (years) 

Figure 5 

Observed lengths at age and fitted von Bertalanffy 
regression line for Atlantic croaker from the Chesa- 
peake Bay region (September, 1988-91). Numbers 
above data points are sample sizes at each age. 



Despite the high variability in sizes at age, observed 
lengths at ages 1-7 showed a very good fit to the 
von Bertalanffy growth model (^=0.99; n=753). Esti- 
mated model parameters, asymptotic standard errors, 
and 95% confidence intervals are given in Table 2. 

No difference in the length-weight relationship 
was found between sexes (ANCOVA; 7^=2.46; 
df=3,005; P=0.15). The equation for pooled sexes 
(Fig. 6) was 

TW = 2.41 x lO^TL 3 ' 30 (r 2 = 0.97; n = 3,006;P< 0.01). 

The slope of the regression line (6=3.30; SE=0.0141) 
was significantly different from 3.00 (Mest; r=7.26; 
P<0.01), indicating allometric growth. 



Size and age compositions 

Length-frequency distributions of Atlantic croaker 
samples obtained from different fishing gears were 
similar (Fig. 7), with the exception of commercial 
trawl data which were dominated by fish smaller 
than 275 mm. The smallest Atlantic croaker cap- 



Barbien et al Age, growth, and mortality of Micropogonias undulatus 



Table 1 

Summary of ANCOVA to evaluate the effect of 
Atlantic croaker (Micropogonias undulatus) total 
length (TL) and age on otolith maximum thickness 
(OT), maximum length (OL), weight (OW), and ra- 
dius (OR), n = 210 for each analysis; a = 0.05. 



Otolith 
relation 



Source of 
variation 



P-value 



OT 



OL 



OW 



OR 



age 



model 
TL 
age 
TL x 

model 
TL 
age 
TL x age 

model 
TL 
age 
TL x age 

model 
TL 
age 
TL x age 



0.85 



I) s.s 



0.90 



0.97 



0.0001 
0.0001 
0.3263 
0.6214 

0.0001 
0.0001 
0.9780 
0.7907 

0.0001 
0.0001 
0.0863 
0.1402 

0.0001 
0.0001 
0.0001 
0.0008 



tured by each gear was approximately 200 mm, al- 
though these data represent only market foodfish 
grades (small, medium, or large) and did not include 
smaller fish sold as scrap. The maximum length 
recorded was 400 mm, from a pound-net catch in 
1988. However, for all gears 99% of the Atlantic 
croaker collected were <345 mm. 

Age compositions from different gears were not as 
similar as length frequencies suggest (Fig. 7). Haul- 
seines, gill nets, and commercial trawls caught a 
large proportion offish at ages 1 and 2, and had age 
2 as the first age fully recruited. Pound nets cap- 
tured a comparatively larger proportion of fish at 
ages 4-7, and had age 3 as the first age fully re- 
cruited. Age-1 fish were not fully recruited to any 
of the gears sampled, but this may reflect, in part, 
the exclusion of scrap fish from our collections. 

The maximum age sampled was 8 years. Despite 
the large sample size and the variety of gears used, 
only two eight-year-old fish were collected, one from 
a pound net in September 1988 (334 mm) and one 
from a gill net in September 1990 (293 mm). 

Mortality 

Instantaneous total annual mortality rates (Z) 
ranged from 0.55 to 0.63. Estimates obtained for a 



Table 2 




Parameter estimates, standard errors, and 95% 
confidence intervals for the von Bertalanffy 
growth model for Atlantic croaker {Micropogonias 
unpulatus) in the Chesapeake Bay region ( 1988-90). 


Standard 
Parameter Estimate error 


95% confidence 

intervals 


Lower tipper 


L„ 312.43 7.44 
K 0.36 0.08 
t -3.26 0.84 


297.82 327.04 

0.20 0.52 

-491 -1.61 



maximum age of 8 years were 0.55 (A=42%) by us- 
ing Hoenig's (1983) method, and 0.58 (A=43%) by 
using Royce's ( 1972) method. A regression estimate 
obtained from the slope of the catch curve (Fig. 8) 
was 0.63 (A=47%); confidence intervals were 0.36 
(A=30%) and 0.90 (A=59%). The regression line did 
not deviate significantly from linearity (ANOVA; 
^=1.15: P=0.40). 



Discussion 

Age determination 

Our criteria for ageing Atlantic croaker from otolith 
sections differ from those of Barger (1985), in that 
we considered the first annulus to be the blurred 
opaque band surrounding the otolith core. However, 
evidence from both studies seems to support our 
interpretation. Barger (1985) reported 58% of the 
otoliths in his samples had marks that were too thin 
or discontinuous and too close to the core to be con- 
sidered annuli. By examining otoliths of young of the 
year during the period of annulus formation, we 
were able to validate this mark as the first annu- 
lus, formed during their first spring in the estuary. 
Because spawning of Atlantic croaker in the Chesa- 
peake Bay area extends from late July to Decem- 
ber (Barbieri et al., unpubl. ms.) and the first an- 
nulus is formed during their first spring after hatch- 
ing, fish forming the first annulus could range from 
5 to 10 months of age. As marginal increment plots 
indicated, all subsequent annuli formed at yearly 
intervals. 

Variation in the width of the first annulus also 
seems to reflect the protracted spawning period of 
Atlantic croaker. Early hatched fish (July-August) 
would probably be large enough by April or May to 
have this annulus close to, but not continuous with, 
the otolith core. In contrast, late-hatched fish (No- 
vember-December) would be small in the spring and 



Fishery Bulletin 92(1), 1994 



a 


1000n 


N = 3,006 '/ 


5 

05 


fi = 0.97; P<0.01 t/i? 


| 500 


.jjfi 


Total 


j— i^B • B 





■*** 


I ' I ' I 


200 300 400 


Total length (mm) 


Figure 6 


Length-weight relationship of Atlantic croaker in 


the Chesapeake Bay region, 1988-91. 



would probably show the first mark and the core 
virtually fused together. Since Atlantic croaker also 
spawn over a long period in the Gulf of Mexico 
(White and Chittenden, 1977), this might explain 
why the first annulus was apparent in only a por- 
tion of Barger's (1985) fish. 

Our interpretation of the first annulus is also con- 
sistent with evidence from another ageing method. 
Ross (1988) reported that some Atlantic croaker 
from North Carolina showed an early, age-0 scale 
mark, apparently formed during their first winter. 
However, they were not counted as annuli. 

The high precision of repeated age readings and 
validation of annuli almost to the maximum ob- 
served age indicate that otolith sections represent 
a very reliable method for ageing Atlantic croaker. 
Identifying the first annulus may require some prac- 
tice, but all other annuli are extremely clear and 
easy to identify. Otolith sections do not have the 
problems scales reportedly do, such as the occur- 
rence of double marks (White and Chittenden, 1977; 
Music and Pafford, 1984; Ross, 1988; Barbieri, 
1993), or marks that are poorly defined and difficult 
to distinguish (Joseph, 1972; Barger and Johnson, 
1980; Barbieri, 1993). 

The pattern of otolith growth relative to fish 
growth also indicated the high reliability of trans- 
verse otolith sections for ageing Atlantic croaker. 
Although otolith radius, the axis we used to read 
annuli, showed a poor correlation with fish length, 
the strong linear relationship between otolith radius 



and age indicates that otolith growth along this axis 
seems to be continuous with age, independent offish 
growth. This supports previous suggestions 
(Mosegaard et al., 1988; Wright, 1991) that a pro- 
cess other than somatic growth governs the rate of 
otolith accretion. Because otoliths grow at a faster 
rate than the body during slow somatic growth, they 
are excellent structures for recording the seasonal 
cycle and age in slow-growing and old fish, especially 
those approaching asymptotic length (Casselman, 
1990). The high correlation we found between otolith 
radius and age for Atlantic croaker seems to confirm 
this pattern. 

Growth and mortality 

High variability of observed lengths at age indicates 
that length is a very poor predictor of age for Atlan- 
tic croaker, especially beyond age 2. The wide range 
in lengths at age can be attributed to a combination 
of two factors: 1) most of Atlantic croaker's growth 
occurs during the first two years, becoming asymp- 
totic after age 2; and 2) fish are born at different 
times during the extended spawning season and 
display different growth rates. Warlen (1982) re- 
ported that Atlantic croaker larvae caught later in 
the spawning season had slower growth rates than 
those taken during peak spawning. Since growth 
decreases sharply after their first year, such differ- 
ences in growth rates among young of the year is 
likely to cause a large variation in lengths at age. 

Growth parameter estimates reported here do not 
agree with previous reports for Atlantic croaker. 
However, comparisons with previous studies are 
difficult because other estimates were based on dif- 
ferent ageing methods (White and Chittenden, 1977; 
Ross, 1988), different otolith-ageing criteria (Barger, 
1985; Hales and Reitz, 1992), or a period before any 
significant fishery for Atlantic croaker occurred 
(Hales and Reitz, 1992). Methods used to estimate 
length-at-age data or to fit the von Bertalanffy 
model also varied. Previous studies on Atlantic 
croaker growth generally used back-calculated 
rather than observed lengths at age. Although back- 
calculation has been widely used and represents 
standard methodology in age and growth studies 
(Bagenal and Tesch, 1978; Jearld, 1983), recent evi- 
dence indicates that it may generate biased results 
(Campana, 1990; Ricker, 1992). By basing our 
growth parameter estimates on observed lengths at 
age of fish collected in September — the average 
spawning period of Atlantic croaker in the Chesa- 
peake Bay area — we avoided problems related to 
back-calculation procedures or seasonal growth effects. 

Our total mortality estimates are the lowest ever 



Barbien et al Age, growth, and mortality of Micropogonias undulatus 



o 

c 

CD 
13 
CX 
CD 



50 



25 



Pound net 



D^ 



50 



25 



2 4 6 8 



Haul seine 



20 



50 



25 



Gill net 



On 



50 i ?i 



25 



Trawl 



Oji: 



Age (years) 



15 



10 



Pound net 
N = 1 061 



o V 




i i t — t 

150 200 250 300 350 400 



Haul seme 
N = 332 




I I I | 

150 200 250 300 350 400 



5 


Gill net 




N = 317 





iL 


5 



JilL^ 


i i i i 1* i 



150 200 250 300 350 400 



Trawl 
N = 257 




I I 

150 200 250 300 350 400 



Total length (mm) 



Figure 7 

Age frequency (left panels) and length frequency (right panels) distributions by 
fishing gear for Atlantic croaker in the Chesapeake Bay region, 1988-91. Num- 
bers above bars are sample sizes by age. 



reported for Atlantic croaker. However, the close 
agreement we found between estimates obtained 
from maximum age and from the catch curve indi- 
cates our values are probably realistic, at least for 
the Chesapeake Bay area. Comparisons with previ- 



ous studies are difficult because other estimates 
were based on different ageing methods (scales and 
length frequencies), and on collections from a single 
sampling gear and different geographical areas 
(White and Chittenden, 1977; Ross, 1988). 



Fishery Bulletin 92(1). 1994 



10 



CD 
-Q 

E 

3 



o 



Log e Number = 6.86 - 0.63 Age 
N= 1,027; r2 = 0.93; (P<0.05) 



12 3 4 5 6 
Age (years) 



7 8 



Figure 8 

Catch curve for Atlantic croaker collected from pound- 
net, haul-seine and gillnet commercial catches in 
Chesapeake Bay, 1988-91. Ages 1, 2, and 8 (triangles) 
were not used in calculating the regression line. 



Geographic comparisons 

The possible existence of two groups of Atlantic 
croaker, exhibiting different life history and popu- 
lation dynamics attributes north and south of Cape 
Hatteras, North Carolina, has been extensively dis- 
cussed in the scientific literature (Chittenden, 1977; 
White and Chittenden, 1977; Ross, 1988). Ross 
(1988) hypothesized that these groups may overlap 
and mix in North Carolina and stated that, if the 
Atlantic croaker designated in his study as "north- 
ern" were fish migrating south from the Chesapeake 
and Delaware Bay areas, their larger sizes (350-520 
mm TL) and older ages (5-7 years, as aged by 
scales) would be consistent with the proposed north- 
ern group life history pattern. However, our results 
do not support the hypothesis of a group of larger, 
older Atlantic croaker in Chesapeake Bay, at least 
in recent years. 

Maximum length and size ranges reported here 
are consistent with recent data from North Carolina, 
both for inshore waters as well as for the offshore 
trawl fishery. Since 1982, Atlantic croaker trawl 
catches in North Carolina have been dominated by 
small fish. Fish larger than 300 mm TL and older 
than 3 years have represented less than 1% of the 
recent catches (Ross, 1991). Although records of 
large fish do exist, Atlantic croaker as large as those 
reported by Ross ( 1988) have never been common in 
commercial catches from the Chesapeake Bay re- 
gion. Even in the early 1930's, when the winter 
trawl fishery had just been established off the coasts 



of Virginia and North Carolina and catches of At- 
lantic croaker were dominated by large fish, most 
fish measured 260-360 mm TL (Pearson, 1932). 
Length frequencies of Atlantic croaker sampled from 
commercial pound nets in the lower Chesapeake Bay 
in 1922 (Hildebrand and Schroeder, 1928) and dur- 
ing 1950-1958 (Massmann and Pacheco, 1960), as 
well as from pound nets and haul-seines in Pamlico 
and Core sounds, North Carolina (Higgins and 
Pearson, 1928), show the same pattern. 

Recreational catch records also indicate that the 
large Atlantic croaker reported by Ross ( 1988) have 
not been common in the Chesapeake and Delaware 
Bay areas. Between 1960 and 1970 the minimum 
citation weight for Atlantic croaker in the Virginia 
Saltwater Fishing Tournament ranged from 0.91 to 
1.36 kg. Although 741 citations were issued during 
this period, only 1.9% were for Atlantic croaker 
>1.82 kg. Between 1977 and 1982, however, al- 
though the minimum citation weight was raised to 
1.82 kg, 599 citations were issued, including 47 
entries for Atlantic croaker >2.27 kg (483-610 mm 
TL). The largest number of citations occurred in 
1979 and 1980, coinciding with Ross's (1988) sam- 
pling period in North Carolina. Records from the 
Delaware State Fishing Tournament show the same 
pattern as that from Virginia. The number of cita- 
tions was very small during the early 1970's, 
reached a peak in 1980, and decreased rapidly there- 
after. Although complete information covering their 
entire range is not available, state records of Atlan- 
tic croaker along the east coast of the United States 
show the same pattern. Records from Georgia to 
New Jersey were broken during the period 1977-82, 
indicating that 1) unusually large fish occurred 
during this period and have not occurred since; and 
2) their occurrence was not limited to areas north 
of North Carolina. 

In conclusion, recent size and age composition 
data do not indicate the existence of a group of 
larger, older Atlantic croaker in the Chesapeake Bay 
region compared with more southern waters. His- 
toric information agrees well with our results and 
indicates that fish >400 mm TL have not repre- 
sented a large proportion of Atlantic croaker in this 
area. The abundance of unusually large fish during 
the period 1977-82 apparently constituted an un- 
usual event and may reflect passage through the 
fishery of a few strong year classes that seemingly 
disappeared after 1982. Similar episodes — the occur- 
rence of larger fish for a few years — have been pre- 
viously reported for Atlantic croaker in Chesapeake 
Bay (Hildebrand and Schroeder, 1928; Massmann 
and Pacheco, 1960), suggesting the phenomenon 
happens periodically. An increase in survivorship of 



Barbien et al.: Age, growth, and mortality of Micropogonias undulatus 



1 I 



early spawned fish, combined with higher mortal- 
ity of late-spawned fish as a result of low winter 
temperatures in estuarine nursery areas (Mass- 
mann and Pacheco, 1960; Joseph, 1972; Warlen and 
Burke, 1991) could account for an increase in the 
proportion of larger fish in certain years and explain 
the episodic occurrence of large Atlantic croaker in 
this area. 

Our results for Chesapeake Bay, together with 
records of large fish south of North Carolina during 
1977-82, suggest that the hypothesis of a basically 
different life history and population dynamics pat- 
tern for Atlantic croaker north and south of Cape 
Hatteras, North Carolina, should be reevaluated. 
However, sampling programs over time describing 
size and age compositions of Atlantic croaker 
throughout their range are still necessary to fully 
evaluate this question. 

Acknowledgments 

We would like to thank the Chesapeake Bay com- 
mercial fishermen and James Owens (VIMS) for 
helping us obtain samples. Sue Lowerre-Barbieri 
helped with fish processing and with otolith section- 
ing and reading. Claude Bain (Virginia Saltwater 
Fishing Tournament) and Jessie Anglin (Delaware 
Department of Natural Resources) provided infor- 
mation on Atlantic croaker recreational citation 
records. Ronald Hardy, Joe Loesch, Sue Lowerre- 
Barbieri, Jack Musick, Rogerio Teixeira, and two 
anonymous reviewers made helpful suggestions to 
improve the manuscript. Financial support was pro- 
vided by the College of William and Mary, Virginia 
Institute of Marine Science, by Old Dominion Uni- 
versity, Applied Marine Research Laboratory, and by 
a Wallop/Breaux Program Grant for Sport Fish Res- 
toration from the U.S. Fish and Wildlife Service 
through the Virginia Marine Resources Commission, 
Project No. F-88-R3. Luiz R. Barbieri was partially 
supported by a scholarship from CNPq, Ministry of 
Science and Technology, Brazil (process No. 203581/ 
86-OC). 

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Barger, L. E. 

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Barger, L. E., and A. G. Johnson. 

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Campana, S. E. 

1990. How reliable are growth back-calculations 
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1960. The analysis of a catch curve. Biometrics 
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1977. Simulations of the effects of fishing on the 
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pound-net and haul-seine catch compositions. N. 
Am. J. Fish. Mgmt. 5:86-90. 
Draper, N. R., and H. Smith. 

1981. Applied regression analysis, 2nd ed. John 
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Everhart, W. H., and W. D. Youngs. 

1981. Principles of fishery science, 2nd ed. Cornell 
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Freund, R. J., and R. Littell. 

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ciformes: Sciaenidae). J. Archaeol. Sci. 19:73-99. 
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venile croaker, Micropogon undulatus, in Vir- 
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1959. Migration of the croaker, Micropogon 
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erence to the destruction of undersized fish and 
the protection of the gray trout, Cynoscion 
regalis. Rep. U.S. Comm. Fish. 2:29-65. 
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1928. The fishes of Chesapeake Bay. Bull. U.S. 
Bur. Fish. 43:1-388. 



12 



Fishery Bulletin 92(1), 1994 



Hoenig, J. M. 

1983. Empirical use of longevity data to estimate 
mortality rates. Fish. Bull. 82:898-902. 
Jearld, A., Jr. 

1983. Age determination. In L. A. Nielsen and D. 
L. Johnson (eds.), Fisheries techniques, p. 301- 
324. Am. Fish. Soc, Bethesda, MD. 

Joseph, E. B. 

1972. The status of the sciaenid stocks of the mid- 
dle Atlantic coast. Chesapeake Sci. 13:87-100. 
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1960. Disappearance of young Atlantic croakers 
from the York River, Virginia. Trans. Am. Fish. 
Soc, 89:154-159. 

Morse, W. W. 

1980. Maturity, spawning and fecundity of Atlan- 
tic croaker, Micropogonias undulatus, occurring 
north of Cape Hatteras, North Carolina. Fish. 
Bull. 78:190-195. 

Mosegaard, H., H. Svendang, and K. Taberman. 

1988. Uncoupling of somatic and otolith growth 
rates in Arctic char (Salvelinus alpinus) as an ef- 
fect of differences in temperature response. Can. 
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Music, J. L., Jr., and J. M. Pafford. 

1984. Population dynamics and life history aspects 
of major marine sportfishes in Georgia's coastal 
waters. Georgia Dep. Nat. Res., Coast. Res. Div., 
Contr. Ser. No. 38, Brunswick, 382 p. 

Pearson, J. C. 

1932. Winter trawl fishery off the Virginia and 
North Carolina coasts. U.S. Bur. Fish., Invest. 
Rep. No. 10, Washington, 31 p. 
Ricker, W. E. 

1975. Computation and interpretation of biological 
statistics of fish populations. Bull. Fish. Res. 
Board Can. 191, 382 p. 
1992. Back-calculation offish lengths based on pro- 
portionality between scale and length 
increments. Can. J. Fish. Aquat. Sci. 49:1018- 
1026. 
Robson, D. S., and D. G. Chapman. 

1961. Catch curves and mortality rates. Trans. 
Am. Fish. Soc. 90:181-189. 

Roithmayr, C. M. 

1965. Review of industrial bottomfish fishery in 
northern Gulf of Mexico, 1959-62. Comm. Fish. 
Rev., U.S. 27:1-6. 



Ross, J. L. 

1991. Assessment of the North Carolina winter 
trawl fishery, September 1985-April 1988. North 
Carolina Dep. Environ. Health Nat. Res., Div. Mar. 
Fish., Spec. Sci. Rep. No. 54, 80 p. 
Ross, S. W. 

1988. Age, growth, and mortality of Atlantic 
croaker in North Carolina, with comments on 
population dynamics. Trans. Am. Fish. Soc. 
117:461-473. 
Royce, W. F. 

1972. Introduction to the fisheries 
sciences. Academic Press, NY, 351 p. 
SAS. 1988. 

SAS/STAT user's guide. Release 6.03 edition. SAS 
Institute Inc., Cary, NC, 1028 p. 
Wallace, D. H. 

1940. Sexual development of the croaker, 
Micropogon undulatus, and distribution of the 
early stages in Chesapeake Bay. Trans. Am. Fish. 
Soc. 70:475-482. 
Warlen, S. M. 

1982. Age and growth of larvae and spawning time 
of Atlantic croaker in North Carolina. Proc. Ann. 
Conf. S.E. Assoc. Fish and Wildl. Agencies 34:204- 
214. 
Warlen, S. M., and J. S. Burke. 

1991. Immigration of larvae of fall/winter spawn- 
ing marine fishes into a North Carolina 
estuary. Estuaries 13:453-461. 
Welsh, W. W., and C. M. Breder. 

1923. Contributions to the life histories of 
Sciaenidae of the eastern United States 
coast. Bull. U.S. Bur. Fish. 39:141-201. 
White, M. L., and M. E. Chittenden Jr. 

1977. Age determination, reproduction, and popu- 
lation dynamics of the Atlantic croaker, 
Micropogonias undulatus. Fish. Bull. 75:109- 
123. 
Wilk, S. J. 

1981. The fisheries for Atlantic croaker, spot, and 
weakfish. In H. Clepper (ed.) Proceedings of the 
6th annual marine recreational fisheries sympo- 
sium, p. 5-27. Sport Fish. Inst., Washington. 
Wright, P. J. 

1991. The influence of metabolic rate on otolith in- 
crement width in Atlantic salmon parr, Salmo 
salar L. J. Fish Biol. 38:929-933. 



Abstract. Statolith micro- 
structural analysis was applied to 
126 specimens of the oceanic bo- 
real clubhook squid, Onychoteuthis 
borealijaponica, for estimation of 
age and growth rates. Specimens 
were captured from the western, 
central, and eastern North Pacific 
between approximately lat. 38° N 
and 47°N by driftnet fishing, 
trawling, and jigging in the sum- 
mers of 1990 and 1991. Results 
suggest that increments were de- 
posited at a rate of one per day. 
Both sexes live approximately one 
year; males mature at smaller 
sizes and younger ages than fe- 
males. Exponential growth models 
suggest that growth in length was 
similar for males and females 
(0.80% ML/day) in the central 
North Pacific, while growth in 
weight was higher for females 
( 1.90% WT/day) than males (1.40% 
WT/day). Females in the western 
North Pacific exhibited faster 
growth rates than individuals 
from the central North Pacific. O. 
borealijaponica were estimated to 
have hatched year round based on 
back calculation of statolith incre- 
ments from the time of capture. 
Post-recruit individuals exploited 
in the O. borealijaponica jig fish- 
ery and Ommastrephes bartramii 
driftnet fishery typically hatched 
from late summer to early winter. 



Age and growth of the oceanic 
squid Onychoteuthis borealijaponica 
in the North Pacific 

Keith A. Bigelow 

Honolulu Laboratory, Southwest Fisheries Science Center 
National Marine Fisheries Service. NOAA 
2570 Dole Street, Honolulu, HI 96822-2396 



The oceanic boreal clubhook squid 
Onychoteuthis borealijaponica 
Okada, 1927 is common in subarc- 
tic waters of the North Pacific. This 
species ranges from the western 
coast of the United States and 
Canada to the eastern coast of 
Hokkaido, Japan, and the Kurile 
Islands, but does not occur in the 
Sea of Okhotsk or Bering Sea 
(Young, 1972; Murata et al., 1976; 
Naito et al., 1977a; Fiscus and 
Mercer, 1982; and Kubodera et al., 
1983). Onychoteuthis borealijapon- 
ica has commercial value through- 
out its range. Between 1971 and 
1979, commercial landings aver- 
aged 1,171 metric tons (t) per year 
from a jig fishery in oceanic waters 
east of Hokkaido, Japan (Okutani 
and Murata, 1983), and approxi- 
mately 254 and 2,705 t of O. bor- 
ealijaponica were caught in 1990 
and 1991, respectively, by Japan, 
Korea, and Taiwan in the Ommas- 
trephes bartramii highseas driftnet 
fishery (DiNardo and Kwok, in re- 
view 1 ). Based on exploratory fish- 
ing, Fiscus and Mercer (1982) sug- 
gested that O. borealijaponica 
could be commercially exploited by 
a jig fishery from the Gulf of Alaska 
westward to the Aleutian Islands, 
and Murata (in Okutani, 1977) in- 
dicated that the potential fishery 
yield of O. borealijaponica may be 
50,000-200,000 t in an area west of 



Manuscript accepted 26 July 1993 
Fishery Bulletin 92:13-25 (1994) 



1 DiNardo, G. T., and W. Kwok. In review. 
Estimates offish and cephalopod catch in 
the North Pacific high-seas driftnet fish- 
eries, 1990-91. 



long. 152°E and lat. 40-45°N. If a 
commercial fishery does develop, 
accurate life-history information is 
essential for management purposes. 

The general biology and feeding 
ecology of Onychoteuthis borealija- 
ponica have been investigated 
(Naito et al., 1977b; Okutani and 
Murata, 1983); however, little in- 
formation is available on age and 
growth. Average growth rates have 
been inferred from length-fre- 
quency distributions of sequential 
jigging samples (Murata and Ishii, 
1977). This study suggested that 
the lifespan for boreal clubhook 
squid is approximately one year; 
females grow faster and attain a 
larger size (370 mm mantle length 
(ML)) than males (270 mm ML). 
Growth estimates from driftnet 
studies (Kubodera et al., 1983; 
Kubodera, 1986) were inconclusive 
because length-frequency modes 
were impossible to detect, possibly 
because of protracted spawning 
seasons or variable individual 
growth rates within a population. 

The accuracy and precision of 
cephalopod growth estimates have 
been greatly enhanced through the 
use of daily increments within sta- 
toliths (Natsukari et al., 1991). 
Ageing by counting statolith incre- 
ments allows the estimation of size 
at age and may provide informa- 
tion on individual age and growth 
rates. Hatchdates can be estimated 
by back calculation of daily incre- 
ments. Age and growth estimates 
derived from statolith analysis 



13 



14 



Fishery Bulletin 92(1), 1994 



have been obtained from a variety of neritic squid 
species (see review by Rodhouse and Hatfield, 1990a). 
The objectives of this study were to 1) estimate 
the age and growth of O. borealijaponica from sta- 
tolith microstructural analysis, 2) determine the 
periodicity of increment formation, 3) statistically 
compare appropriate growth models fit to the age- 
ing data, 4) determine the distribution of back-cal- 
culated hatching dates of O. borealijaponica and 
draw inferences about spawning locations, and 5) 
determine the relationship between age and matu- 
rity stages. 



Materials and methods 

Taxonomic clarifications 

At least five onychoteuthid species are found in the 
North Pacific: O. borealijaponica from subarctic 
waters; an undescribed species occupying the North 
Pacific transition zone (-29— 40"N, Bigelow, unpubl. 
data); and three subtropical species of the O. banksii 
complex (Young and Harman, 1987). Juvenile, sub- 
adult, and adult O. borealijaponica (69-343 mm ML) 
were separated from other onychoteuthid species 
based on the number of tentacular hooks (n =25-29) 
on each club. Identification of O. borealijaponica 
paralarvae (11.5 to 35 mm ML) was based on mantle 
chromatophore patterns (Bigelow, unpubl. data). 

Data collection 

Subadults, adults During July-September 1990, 
O. borealijaponica specimens were collected on vari- 
ous research cruises in the North Pacific. Most squid 
specimens were captured by research drift net ( mesh 
size=48-220 mm stretch mesh) in the western and 
central North Pacific, but squid jigs were also used 
to capture specimens from the central and eastern 
North Pacific (Fig. 1, Table 1). Squid samples were 
frozen (-20°C) upon capture and returned to the 
laboratory for analysis. 

Paralarvae, juveniles From 5 to 24 August 1991, 
39 tows with a modified Cobb trawl were made 
along meridian 179°30'W between 36°56'N and 
46°00'N, and along meridian 174°30'W between 
39°00'N and 45°00'N. The trawl was dual warp, with 
a mouth area of approximately 140 m 2 when fish- 
ing and a cod-end liner constructed of 3.2 mm 
knotless nylon delta mesh ( Wyllie Echeverria et al., 
1990; Lenarz et al., 1991). Thirty-one oblique night 
tows (0-150 m) and eight oblique day tows (0-750 
m> were conducted. O. borealijaponica specimens 
from eight tows (Fig. 1, Table 1) were sorted on 



board and immediately frozen (-20°C, juveniles) or 
fixed in 95% ethyl alcohol (paralarvae). 

Laboratory analysis 

Dorsal mantle length measurements were made to 
the nearest millimeter (mm) on thawed specimens. 
Squids less than 0.5 g were blotted dry and weighed 
to the nearest 0.001 g, whereas larger specimens 
were weighed to the nearest 0.1 g. No correction was 
made for shrinkage of paralarvae from fixation in 
ethanol, because the species possesses a strong 
gladius and exhibited minimal shrinkage (<2%). 
Specimens were sexed and assigned a maturity 
stage (I: juvenile; II: immature; III: preparatory; 
IV: maturing; V: mature) based on the appearance 
and relative size of the gonads and accessory repro- 
ductive organs (Lipinski, 1979). Statoliths were dis- 
sected from the specimens and stored in 95% ethyl 
alcohol. 

Statolith preparation and microstructural 
analysis One statolith of the pair was mounted on 
a microscope slide in Eukitt resin (Calibrated In- 
struments Inc. 200 Saw Mill Rd., Hawthorne, NY 
10532) with the concave side (anterior) facing up. 
The transparency of paralarval statoliths allowed 
their examination without further preparation (Fig. 
2). The thickening of statoliths from larger squid 
(>35 mm ML) required that they be ground with 
fine-grained (1200-grade) carborundum paper and 
polished with 0.3-|am alumina-silica powder prior to 
microstructural examination. 

Increments were counted beginning at the first 
visible increment outside the nucleus (Fig. 3A), and 
continued to the margin of the dorsal dome (Fig. 3B). 
The diameter of the circular nucleus averaged 28.0 
urn (SD=2.4 |im, n-37). The precision of increment 
counts was assessed by using the coefficient of varia- 
tion (Chang, 1982). Two nonconsecutive blind incre- 
ment counts were made on each statolith with trans- 
mitted light at a magnification of 1500x. The mean 
of the two increment counts was accepted if the co- 
efficient of variation was <7.0%, otherwise a third 
count was conducted. With this criteria, two incre- 
ment counts were acceptable for 115 statoliths, 
whereas three increment counts were required for 
11 statoliths. Hatching dates were computed by 
subtracting the mean increment count from the date 
of capture and were pooled into monthly periods. 
Increment counts were assumed to represent the 
individuals' age in days, based on the following re- 
sults (periodicity of increment deposition) which 
provided support for the hypothesis that one incre- 
ment is deposited per day. 



Bigelow Age and growth of Onychoteuthis boreahjaponica 



15 




Figure 1 

Location of stations in the North Pacific sampled for Onychoteuthis boreahjaponica: Western North Pacific 1990 
(open circles), central North Pacific 1990 (closed circles), central North Pacific 1991 (closed triangles), and east- 
ern North Pacific 1990 (open squares). 



Periodicity of increment deposition Three sub- 
adult squid caught by jig or trawl in the central 
North Pacific were placed for two hours in 20 L of 
seawater containing 250 mg/L oxytetracycline hy- 
drochloride (OTC). After OTC exposure, squid were 
maintained in a 20-L tank with flowthrough sea- 
water under ambient photoperiod and temperature 
conditions. Freshly captured live saury (Cololabis 
saira) were introduced as prey, but no feeding was 
noted or observed. Squids survived up to 61.5 hours 
in captivity. Statoliths were prepared as above and 
illuminated with ultraviolet (Fig. 4) and natural 
light. Under fluorescent light, an ocular marker was 
aligned with the inner edge of the OTC band. The 
statolith was then examined under natural light, 
but increments peripheral to the band were difficult 
to count. Therefore, to determine the periodicity of 
increment deposition, statolith growth following 
OTC exposure was related to the average increment 
width prior to exposure. The distance from the in- 
ner edge of the OTC band to the statolith perimeter 
was divided by the mean width of increments prior 
to the OTC band. Three estimates of statolith 
growth after OTC exposure were made, and the 



average increment width calculated for 15 incre- 
ments prior to the OTC band. 

Statistical procedures 

Mantle length-weight relationships Mantle 
length-weight regressions were fit to the data by 
using the model 

WT(g) = a*ML(mm) b (D 

Separate ML-weight equations were developed for 
both sexes, and a single equation was used for squid 
of unknown sex (<60 mm ML). 

Fitting of size-at-age data Researchers have used 
a variety of different models to describe cephalopod 
growth (e.g., linear, logistic, von Bertalanffy), al- 
though the rationale for using a given model is usu- 
ally not stated. Schnute ( 1981 ) proposed a flexible four- 
parameter model to describe growth which includes 
most growth models historically used in fisheries re- 
search as special cases. The model takes the form 



Y(t): 



V, +(Vi 



v ): 



1-e-""-' 1 ' 



-.j U,-r, ) 



l/i 



(2) 



16 



Fishery Bulletin 92(1), 1994 









Table 1 












Data on samples 


of Onychoteuthis borealijaponica 


collected for 


age analysis 




















Mantle 










Depth 


Temperature 




length 


Date 


Lat. 


Long. 


Gear 


(m) 


CO 


n 


(mm) 


Western North Pacific 














24 Jul. 1990 


42 - 00'N 


158°58'E 


Driftnet 


0-10 


14.9 


5 


197-316 


25 Jul. 1990 


43'03'N 


158'59'E 


Driftnet 


0-10 


15.5 


12 


203-311 


26 Jul. 1990 


44'02'N 


158 a 56E 


Driftnet 


0-10 


16.1 


14 


214-343 


28 Jul. 1990 


44'00'N 


160"00'E 


Driftnet 


0-10 


16.5 


15 


206-339 


29 Jul. 1990 


43'16'N 


159'58'E 


Driftnet 


0-10 


15.7 


8 


204-233 


06 Aug. 1990 


43'30'N 


161"02'E 


Driftnet 


0-10 


16.0 


2 


275-288 


20 Sep. 1990 


44"45'N 


160 = 03'E 


Driftnet 


0-10 


15.7 

Total 


1 
57 


182 


Central North Pacific 














SAMPLE A 
















08 Jul. 1990 


42'30'N 


172°32'W 


Driftnet 


0-8.5 


14.8 


2 


165-195 


04 Aug. 1990 


46"30'N 


152 U 30W 


Driftnet 


0-8.5 


12.1 


4 


147-180 


10 Aug. 1990 


46'30'N 


157'30'W 


Driftnet 


0-8.5 


11.8 


7 


191-313 


12 Aug. 1990 


43'29'N 


157'27'W 


Driftnet 


0-8.5 


14.3 


1 


343 


SAMPLE B 
















06 Aug.1991 


37"59'N 


179'28'W 


Cobb 


0-154 


11.7-24.1 


5 


11.5-32 


06 Aug.1991 


37'55'N 


179 - 26'W 


Cobb 


0-158 


11.7-24.1 


H 


24-35 


09 Aug.1991 


41°08'N 


179"30'W 


Cobb 


0-130 


11.0-20.3 


1 


42 


12 Aug.1991 


43°12'N 


179"30'W 


Cobb 


0-775 


3.5-16.4 


1 


58 


12 Aug.1991 


43°04'N 


179"30'W 


Cobb 


0-156 


8.6-15.9 





69-83 


15 Aug.1991 


44"59'N 


179°27'W 


Jig 


0-5 


12.6 


7 


119-190 


18 Aug.1991 


45°00'N 


174 31'W 


Cobb 


0-162 


6.8-13.2 


4 


75-82 


20 Aug.1991 


43'00'N 


174°30'W 


Cobb 


0-142 


8.8-16.5 


2 


72-78 


22 Aug.1991 


41'14'N 


174"29'W 


Cobb 


0-730 


5.6-21.1 

Total 


1 
49 


66 


Eastern North Pacific 














18 Aug. 1990 


42°47'N 


125°25'W 


Jig 


II 100 


15.1 


5 


214-251 


19 Aug. 1990 


44'12'N 


124"54'W 


Jig 


0-100 


15.9 


2 


229-236 


04 Sep. 1990 


44°23'N 


124'44'W 


Jig 


0-75 


16.4 

Total 


13 
20 


218-312 



where Y(t) is the estimated length or weight at age 
t, andy 1 and v., represent size at two ages t x and t.„ 
which are typically the youngest and oldest indi- 
viduals in the sample. The estimated parameters a 
and b describe how the model connects y ; and y 2 . 
Values of a and b and their 95% confidence inter- 
vals lead to the selection of other submodels. 

The Schnute model (written in Microsoft 
Quickbasic) was fit to the size-at-age data (Fig. 5) 
by nonlinear regression on an IBM-compatable mi- 
crocomputer. Growth modelling was restricted to 
individuals from the central North Pacific samples, 
because of inadequate age representation from the 
western and eastern North Pacific samples. 
Paralarval size-at-age estimates were included in 
the growth models for males and females, because 



size-at-age results were similar for juvenile (66-83 
mm ML) males and females. 

Model comparison If we assume that the Schnute 
model exactly predicts the size of an individual, then 
the residual sum of squares (RSS) of this full model 
is an estimate of measurement error. To ascertain 
if a reduced model with fewer parameters (e.g., 2- 
parameter exponential) adequately describes the 
data, the RSS's from the reduced model and full 
model were compared using an F test statistic: 

( RSS R - RSS F )/( DF h - DF F ) 
RSS f /DF F 



f- 






with DF R - DF F ,DF F degrees of freedom. 



Bigelow Age and growth of Onychoteuthis borealijaponica 



17 




Figure 2 

Onychoteuthis borealijaponica. Light micrograph of a transverse section of a sta- 
tolith from a 11.5-mm mantle length paralarva. Duplicate increment counts were 
61 and 63. 



40 



im 



40 urn 








'" 







Figure 3 

Onychoteuthis borealijaponica. Light micrographs of a ground statolith. (A) Increment deposition within early 
life history. Arrow indicates edge of nucleus. (B) Statolith microstructure within dorsal dome region. 



Fishery Bulletin 92(1). 1994 




Figure 4 

Onychoteuthis borealijaponica. UV micrograph of a ground 
statolith stained with tetracycline. 



where RSS,, is the RSS from the full 
(Schnute) model, RSS R is the RSS from the 
reduced (exponential) model, DF F is the 
number of degrees of freedom from the full 
model, and DF R is the number of degrees 
of freedom from the reduced model (Neter 
et al., 1985). 

Differences in the slopes of the ML- 
weight and size-at-age relationships by sex 
and geographical location were compared 
with analysis of covariance (ANCOVA) and 
F-tests (Sokal and Rolff, 1981). Data were 
initially In-transformed, and ANCOVA was 
used to test for differences in slopes of the 
linearized equations. Elevations of the lin- 
earized equations were compared with F- 
tests. Analyses were performed on central 
North Pacific male and female growth data 
and western North Pacific female data 
with the assumption that females in the 
western North Pacific exhibited a similar 
type of growth as individuals in the central 
North Pacific. There were too few individu- 
als to test for differences in growth rates 



300 -i 500 -| 


250 - 


Males 

400 - 


Males 


200 - 


300 - 




150 - 






100 - 


200 - 




E 

E 50 - 


100 - 




X 


- 




Z 50 100 150 200 250 300 350 400 450 t 50 100 150 200 250 300 350 400 450 

J o 

£ 400 -, 1000 n 


| 350 - 


Females 


Females 


300 - 


750 - 




250 - 






200 - 


500 - 




150 - 






100 - 


250 - 




50 - 












50 100 150 200 250 300 350 400 450 50 100 150 200 250 300 350 400 450 


AGE (days) AGE (days) 


Figure 5 


Relation between age (determined by number of increments within statoliths) and 


mantle length (mm) and weight (g) for male and female Onychoteuthis 


borealijaponica. Western North Pacific 1990 (open circles), central North Pacific 1990 


(closed circles), central North Pacific 1991 (closed triangles = juveniles-subadults, 


open triangles = unknown sex), and eastern North Pacific 1990 (open squares). 



Bigelow Age and growth of Onychoteuthis borealijaponica 



of western North Pacific males or eastern North Pa- 
cific males and females. 



Results 

Statolith analysis 

Statolith microstructural analysis was applied to 
131 squid from the western, central, and eastern 
North Pacific. Five statoliths (3.8%) were broken or 
poorly sectioned and excluded from further analy- 
sis. The coefficient of variation about the mean for 
the aged samples (n = 126) averaged 3.7% based on 
2-3 increment counts for each statolith. No obvious 
trend existed in the coefficient of variation with the 
increment count or body size. 

Periodicity of increment formation 

A fluorescent OTC band was evident in the sta- 
toliths of the three squid exposed to oxytetracycline. 
While increments peripheral to the inner edge of the 
OTC band could not be reliably counted, the rela- 
tion between the growth of the statolith, rearing 
period, and the width of increments prior to the OTC 
band suggested that increments were deposited 
daily (Table 2). Statolith growth in the dorsal dome 
region ranged from 1.4 to 4.3 urn over the rearing 
period (26-61.5 hr). The average number of incre- 
ments deposited per day after oxytetracycline expo- 
sure was 1.30 (range 1.08-1.52) for the three squid. 

Mantle length-weight relationships 

The ML-weight relationship for paralarval O. 
borealijaponica from the central North Pacific is 
represented by the equation 



WT = 2.484 x 10" 5 ML 3015 ;fl 2 = 0.99(n = 36). 



(4) 



The ML-weight relationships for juvenile-adult O. 
borealijaponica from the western, central, and east- 
ern North Pacific are represented by the following 
equations: 

males: 

WT = 1 .873 x lO^ 4 ML 2596 ;J? 2 = 0.96(n = 43) (5) 
females: 

WT = 3.521 x \0- ML 2SX5 ;R 2 = 0.99(n = 68) (6) 

The slopes of the ML-weight regressions for male 
and female O. borealijaponica were significantly 
different (P<0.001). 

Growth 

A good relationship existed between the number of 
increments within statoliths and squid size for in- 
dividuals in the central North Pacific (Fig. 5). An 
exponential model (Table 3, Equation 7) was appro- 
priate to describe the ML-at-age relationship 
(f-1.82, F=2A9) for females (paralarvae-subadult) in 
the central North Pacific. A logistic model was ap- 
propriate to describe the ML-at-age relationship 
(f=1.85, f=2.93) for males (paralarvae-adult) in the 
central North Pacific. However, the oldest individual 
(394 days, 245 mm ML) was a mature male (stage 
V) which influenced the type of model selected. 
Omitting that individual resulted in the selection of 
an exponential model (f=2A9, F=2.55) over a logis- 
tic model (/"=4.73, F=2.94) to describe paralarval- 
subadult growth (Table 3, Equation 8). Exponential 
models were also fit to weight-at-age data for 
paralarval-subadult males and females (Table 3, 
Equations 9 and 10). 

Growth in length (% increase in length per day) 
was similar for males and females (0.80% ML/day) 
in the central North Pacific, while growth in weight 
was faster for females (1.90% WT/day) than males 
(1.40% WT/day). By using the exponential models, 
mantle length, weight-at-age, and absolute growth 







Table 2 








Age validation information for Onychoteu 


this b 


orealijaponica with 


oxytetracycline (OTC) tech 


nique. Width of 


oxytetracycline band is the distance observed between the fluorescent band and the margin 


of the statolith. 


Mean increment width is that of the outer 15 


increments formed 


prior 


to the OTC band. 








Width of 






Estimated 


Rearing 




oxytetracycline 




Mean increment 


increments 


No. ML Imm) period (hr) 




band (pm) 




width (|im) 


per day 


1 162 26 




1 1 




1.19 


1.08 


2 166 61.5 




4.3 




1.10 


1.52 


3 175 44 




L'K 




1.16 


1.32 



20 



Fishery Bulletin 92(1), 1994 



Exponential e 
Pacific Ocean 


quati 


ons for growth of 


ma 


e and fe 


Table 3 

male Onychoteuthis borea 


lijaponica from the 


central North 


Variable 




Age interval (d) 




n 




Equation 




r 2 


Equation no. 


Length (F) 
Length (M) 
Weight (F) 
Weight (M) 




62-376 
62-314 
62-376 
62-314 




36 

27 
36 

27 




mm = I8.41e 000785t 
mm = I7.17e 000798t 
g = 0.74e 00188t 
g = 2.19e 001381 




0.97 
0.89 
0.92 
0.82 


7 

8 

9 

10 



rates (AGR, mm/day or g/day) were predicted for the 
initial 365 days (Table 4). 

The slopes of the size-at-age regression equations 
for females from the western North Pacific were 
significantly different from those for both central 
North Pacific males and females (Fig. 6, Table 5). 
Comparisons of regression slopes between central 
North Pacific males and females revealed no signifi- 
cant differences in length or weight-at-age relation- 
ships (P=0.424, P=0.307). Testing of elevations from 
the central North Pacific male and female data iden- 
tified a significant difference (P<0.001, Table 5); 
therefore, males and females in the central North 
Pacific grow in length and weight at a similar rate, 
but females display a significantly greater size at 
age than males (Table 4). 

Back-calculated hatching dates 

Backcalculation of hatching dates demonstrated 
that O. borealijaponica hatched in all months except 



March (Fig. 7). The distribution of hatching dates 
was not necessarily related to spawning intensity, 
as more subadult squid were available for age analy- 
sis than paralarvae and juveniles. Subadult and 
adult squid captured from July to September in the 
North Pacific had similar hatch dates as samples 
collected from the western (August-February), cen- 
tral (July-February), and eastern North Pacific (Au- 
gust-November). Paralarval and early juvenile 
squid captured in the central North Pacific during 
August 1991 were estimated to have hatched be- 
tween February and June, 1991. 

Maturity stage-age relationships 

Maturity stages were closely related to squid size for 
all three sampling areas; males, however, matured 
at a smaller size than females (Fig. 8). Females and 
males recruit to the driftnet fishery after attaining 
maturity stages III and IV, respectively. No mature 
females (stage V) were captured by any sampling 















Table 


4 












Growth of cen 


tral North Pacific 


Onychoteuth 


is borealijapor 


ica pred 


cted by the exponential 


equations 


based 


on statolith analysis 


Ab 


solute 


grow 


th rates 


(AGR) are given in mm or g per day. 








Estimated age 










Mi 


les 








Females 






Mantle length 




Weight 






Mantle length 




Weight 




(days) 






(mm) 




AGR L 


(g) 




AGR W 


(mm) 


AGR, 


(g) 


AGR W 


50 






25.6 




0.20 


4.4 




0.06 


27.3 


0.21 


1.9 


0.04 


75 






31.2 




0.25 


6.1 




0.09 


33.2 


0.26 


3.0 


0.06 


100 






38.1 




0.31 


8 7 




0.12 


40.3 


0.32 


4.8 


0.09 


125 






46.5 




0.37 


12.2 




0.17 


49.1 


0.39 


7.7 


0.15 


150 






56.8 




0.46 


17.3 




0.24 


59.7 


0.47 


12.4 


0.24 


175 






69.4 




0.56 


24.3 




0.34 


72.7 


0.57 


19.8 


0.38 


200 






84.7 




0.68 


34.3 




0.48 


88.4 


0.70 


31.7 


0.60 


225 






103.4 




0.83 


48.5 




0.67 


107.5 


0.85 


50.8 


0.96 


250 






126.2 




1.01 


68.4 




0.95 


130.8 


1.03 


81.3 


1.54 


275 






154.1 




1.23 


96.5 




1.34 


159.2 


1.25 


130.0 


2.47 


300 






188.1 




151 


136.1 




1.89 


193.7 


1.53 


■J IIS II 


3.95 


325 






229.6 




1.84 


192.1 




2.66 


235.7 


1.86 


332.8 


6.31 


350 






280.3 




2.24 


271.0 




3.75 


286.7 


2.26 


532.5 


1(1 K) 


365 






316.0 




2.57 


337.3 




4.66 


323.2 


2.51 


706.9 


13.42 



Bigelow: Age and growth of Onychoteuthis borealijaponica 





8 " 


Males - Central North Pacific 




E , 


Females - Centra] North Pacific 




E 7 " 


Females - Western North Pacific 




I 






H 6- 


, ..-5 ' 




o 


.-- — ■" *- 




z 


S^' 




3 s - 


^S 




UJ 


ST 




J 


jS 




H «- 


s' 




Z 


^0< 




< 


^^ 




2 3- 


^ 




_c 






8 - 






7 - 






— 6 - 


--"'"'*"/ ' 




M 












H 5 " 






= 4- 
O 












nj 3 - 


// 




* :- 






c 

— i - 






- 

-1 - 


/ 






) 50 100 150 200 250 300 350 400 450 




AGE (days) 




Figure 6 


Log-lin 


ear growth models for male and female Ony- 


choteut 


his borealijaponica . 



method. There was some evidence that males (stage 
IV-V) and females (stage III— IV) in the western 
North Pacific were younger than similar stage in- 
dividuals from the central and eastern North Pacific. 



Discussion 

The data presented provide support for the one-in- 
crement-deposited-per-day hypothesis within the 
statoliths of Onychoteuthis borealijaponica although 
further work is required to rigorously test the hy- 
pothesis. Tetracycline was incorporated into the sta- 
tolith, but the animals did not feed and survival was 
not sufficiently long enough (2-3 days) to provide a 
rigorous test on the rate of increment deposition. 
Validation of the daily increment hypothesis has 
come from tetracycline labeled statolith experiments 
with several neritic squid species (Illex illecebrosus, 
Dawe et al., 1985, Alloteuthis subulata, Lipinski, 
1986, Todarodes pacificus, Nakamura and Sakurai, 
1991). Future statolith validation experiments with 















20 - 


Western North Pacific suhadults/adulls 






15 - 








10 - 








5 - 








^^ 






Central North Pacific 


0! 15 - 

m 

S io- 

Z 5- 
- 
20 - 


^ — subadults/adulls 

■1- 


□- 


- paralarvae/j uve rules 






Eastern North Pacific subadulisyadulls 


15 - 






10 - 


M 




5 - 


_^Hb 




JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC 


MONTH OF HATCHING 


Figure 7 


Estimated hatch-date distributions by month for Ony- 


choteuthis borealijaponica. 



Table 


5 




Comparisons of Onychote 


uthis 


borealijaponica 


growth equations based on 


analysis of covariance. 




Slope 


Elevation 




(F) 


(F) P 


Length-at-age comparisons 




Central North Pacific, 






male vs. female 


0.647 


0.424 
1002.4 <0.001 


Western North Pacific 






female vs. central 






Pacific female 


62.9 


<0.001 


Western North Pacific 






female vs. central 






Pacific male 


62.2 


<0.001 


Weight-at-age comparisons 




Central North Pacific, 






male vs. female 


1.063 


0.307 
1121.1 <0.001 


Western North Pacific 






female vs. central 






Pacific female 


65.9 


<0.001 


Western North Pacific 






female vs. central 






Pacific male 


66.6 


<0.001 



22 



Fishery Bulletin 92(1), 1994 



V 


Males 






B 


IV 


t* 


111 


• 


II 


• 












1 


, 


i ' i  i 



Males 



H3— 
-B- 



100 



Females 



200 



Mil) 



Females 



200 



did 



Kill 



500 



100 200 300 

MANTLE LENGTH (mm) 



)(i( i 



200 300 
AGE (days) 



Figure 8 

Relationship between mantle length and number of increments in sta- 
toliths and male and female maturity stage: western North Pacific (open 
circles), central North Pacific (closed circles), and eastern North Pacific 
(open squares). Ranges are represented by horizontal bars. 



active oceanic squids (e.g., Onychoteuthidae, 
Ommastrephidae) may require substantial mainte- 
nance facilities to support long-term survival. 

Although the rate of increment deposition derived 
by the statolith marking experiment should be con- 
sidered preliminary, indirect evidence was obtained 
to suggest that increments were formed daily. The 
hypothesis that the lifespan is 1 year (Murata and 
Ishii, 1977; Naito et al., 1977b) was supported by the 
present data where only 4 of the 126 individuals 
aged had more than 365 increments within the sta- 
tolith. In addition, back-calculated hatch dates 
(July-February) of post-recruit individuals exploited 
in the O. borealijaponica jig and Ommastrephes 
bartramii squid driftnet fishery were consistent with 
information on spawning (fall-winter) reported in 
the literature (Murata et al., 1976; Murata and Ishii, 
1977; Naito et al., 1977b). This study suggests that 
spawning for O. borealijaponica occurs year round. 
While subadult O. borealijaponica are distributed in 
subarctic waters, evidence from the distribution of 
paralarvae, juveniles, and sexually mature females 
suggests that spawning may occur to the south of 
the subarctic boundary in the North Pacific transi- 
tion zone (30^42°N, terminology after Roden, 1991). 
In the central and eastern North Pacific, O. 
borealijaponica paralarvae and juveniles have been 
recorded from this study (38°N, 179°30'W°) and the 



coast of California (~33°N, Young, 
1972), respectively. In the western 
North Pacific, spawning may oc- 
cur in waters of the Kuroshio Cur- 
rent and Kuroshio Countercurrent 
(Murata and Ishii, 1977; Naito et 
al., 1977a) or between the Kuro- 
shio and Oyashio fronts. Onycho- 
teuthid paralarvae have been cap- 
tured from both the Kuroshio Cur- 
rent and Kuroshio Countercurrent 
(Okutani, 1968, 1969, 1975); how- 
ever, distributional evidence is in- 
conclusive because of the taxo- 
nomic uncertainties of the speci- 
mens captured. Spawning may 
occur in the transitional area be- 
tween the Kuroshio and Oyashio 
fronts, as sexually mature and 
copulated females have been cap- 
tured off Hokkaido, Japan (42°30TSJ, 
150°40'E and 42°15'N, 144°25'E, 
Murata et al., 1981). 

The ML-weight relationships 
obtained in this study for the 
western, central, and eastern 
North Pacific were similar to the 
values previously given for O. borealijaponica cap- 
tured off Japan (Murata and Ishii, 1977). Slope val- 
ues obtained for the ML-weight relationships 
(males=2.596, females=2.915) were similar to other 
active oceanic squids having thick muscular mantle 
walls. Paralarval O. borealijaponica had a higher 
slope value (3.015) than older males and females, 
consistent with previous results for loliginid squids 
and benthic octopods (Forsythe and Van Heukelem, 
1987). 

There is no clear consensus on the type of model 
which best describes cephalopod growth, although 
several studies argue against the use of asymptotic 
models, such as Gompertz or von Bertalanffy 
(Forsythe and Van Heukelem, 1987; Saville, 1987). 
Exponential models have been typically used to 
describe the growth of field caught and laboratory 
reared paralarval squid (Yang et al., 1986; Balch et 
al., 1988; Forsythe and Hanlon, 1989; Bigelow, 1992, 
1993). For growth estimates derived from statolith 
analysis, a linear model is frequently used because 
growth is analyzed over a short segment of the 
cephalopod's life history, such as post recruitment 
to a fishery (Rosenberg et al., 1980; Radtke, 1983; 
Rodhouse and Hatfield, 1990b) or habitat (Jackson 
and Choat, 1992). 

Since the Schnute model encompasses a wide 
range of growth models, it can be used to system- 



Bigelow Age and growth of Onychoteuthis borealijaponica 



23 



atically assess the type of growth model which best 
describes the data. A statistical comparison of sev- 
eral growth models found that growth in O. 
borealijaponica from the paralarval to subadult size 
range could be sufficiently described with an expo- 
nential model, though there was weak evidence that 
a logistic model may be sufficient to describe growth 
in males from the paralarval to adult size range. The 
most appropriate growth model (exponential or lo- 
gistic) for the entire life cycle of O. borealijaponica 
will emerge when sexually mature males and fe- 
males are aged. 

Estimated growth rates from this study were 
higher than estimates derived from length-fre- 
quency analysis of fisheries data (Murata and Ishii, 
1977). Growth estimates based on length-frequency 
analysis with time often provide evidence of de- 
creased growth rate, which is usually described by 
an asymptotic model (Patterson, 1988). Length-fre- 
quency analysis may be inappropriate for estimat- 
ing growth in cephalopods (Jackson and Choat, 
1992), either because 1) cohorts are difficult to de- 
tect because spawning occurs throughout the year, 
2) variable individual growth rates produce Lee's 
phenomenon (Ricker, 1975), or 3) samples of a mi- 
grating population are taken at a point along the 
migration route, which results in overestimating 
growth in young squid and underestimating growth 
in older squid. 

Growth data presented for O. borealijaponica from 
the central North Pacific provide a useful compari- 
son of growth between males and females. The ex- 
ponential models predict that males and females 
grow in length at similar rates (0.80% ML/day), but 
females grow faster in weight (1.90% WT/day) than 
do males (1.40% WT/day). These rates correspond 
closely with the average growth rates of similar 
sized squids from temperate waters (e.g., Illex 
illecebrosus, O'Dor, 1983; /. argentinus, Rodhouse 
and Hatfield, 1990b). 

The most significant advantage of using statolith 
ageing techniques is the ability to produce indi- 
vidual rather than population statistics. Using sta- 
tolith analysis, spatial variations in size at age, 
growth parameters, and maturity stage at age were 
observed between O. borealijaponica individuals 
from the western and central North Pacific. Little 
is known concerning genetic variation and stock 
structure of O. borealijaponica in the North Pacific; 
however, female squid in the western North Pacific 
were found to grow faster than both male and fe- 
male squid in the central North Pacific and were 
younger at maturity stages III and IV than central 
North Pacific females. Apparent growth rate and 
maturity stage differences may be related to water 



temperatures or food availability during the 
paralarval stage. Forsythe and Hanlon (1989) 
showed that temperature had a pronounced effect 
on the increase in length and weight of the squid 
Loligo forbesi. In their laboratory study, a tempera- 
ture increase of 1°C increased the growth in length 
and weight of paralarval squid 0.5% and 2.0% per 
day, respectively. Subadults in the western Pacific 
may have hatched in the warm Kuroshio Current 
or in productive transition waters between the 
Kuroshio and Oyashio fronts. Paralarvae hatched in 
the western North Pacific may therefore experience 
higher temperatures or a greater abundance of prey 
species, or both, than paralarvae hatched in the 
central North Pacific, which could explain the ob- 
served spatial differences in growth. 



Acknowledgments 

I gratefully acknowledge the help of the officers and 
crew of the research vessels Hai Kung, and Shoyu 
Maru and the help of the officers, crew, and scien- 
tific field party of the NOAA ship Townsend Crom- 
well cruise 91-06. 1 would like to thank C. H. Fiscus 
who kindly provided the statolith samples from the 
eastern North Pacific and D. R. Kobayashi for assis- 
tance in fitting the Schnute model. This paper 
benefitted from comments by G. T. DiNardo, E. E. 
DeMartini, C. H. Fiscus, and anonymous reviewers. 



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AbStfclCt. A review of previ- 
ous studies on Kemp's ridley sea 
turtle (Lepidochelys kempii) diet 
was combined with information on 
the diet of the species in the 
coastal waters of New York State. 
Juvenile Kemp's ridleys occupy 
coastal Long Island, New York 
waters during the summer and 
early autumn months. Both fecal 
and intestinal samples collected 
between 1985 and 1989 were ana- 
lyzed to obtain information on the 
diet of this endangered species. 
Fecal and intestinal sample analy- 
sis, as well as information from 
previous studies, indicated that 
juvenile Kemp's ridleys primarily 
consume crabs. Walking crabs of 
the genera Libinia and Cancer 
appear to be the primary food 
sources for the species in New 
York waters. 



Diet of the Kemp's ridley sea turtle, 
Lepidochelys kempii, in New York 
waters 

Vincent J. Burke 

Savannah River Ecology Laboratory and Department of Zoology 
University of Georgia, Drawer E 
Aiken. SC 29802 

Stephen J. Morreale 

Center for the Environment, Room 200, Rice Hall 
Cornell University, Ithaca, NY 14853-5601 

v. 

Edward A. Standora 

Department of Biology, State University College at Buffalo 
1 300 Elmwood Avenue, Buffalo, NY 1 4222 



Manuscript accepted 29 September 1993 
Fishery Bulletin 92:26-32 (1994) 



The Kemp's ridley sea turtle, 
Lepidochelys kempii, was placed on 
the United States endangered spe- 
cies list in December 1970 and was 
listed as one of the twelve most 
endangered species in the world by 
the International Union for the 
Conservation of Nature and Natu- 
ral Resources in 1986 (Federal Reg- 
ister, 1989; Marine Turtle Newslet- 
ter, 1989). Despite a recent in- 
crease in research on the Kemp's 
ridley, little attention has been fo- 
cused on its feeding habits. An un- 
derstanding of the dietary require- 
ments and available food resources 
for the Kemp's ridley is a critical com- 
ponent in the future management and 
protection of this species' habitats. 

While occasional glimpses into 
the composition of Kemp's ridley 
diets have been obtained, detailed 
quantified examinations of the spe- 
cies' diet have only rarely been 
undertaken (Table 1). In one of the 
earliest accounts of the diet of 
Kemp's ridleys, De Sola and 
Abrams (1933) dissected "two foot 
specimens" from the Georgia coast 
and described the main dietary 
component as Platyonichus ocel- 
latus, later renamed the spotted 



lady crab, Ovalipes stephensonii 
(Williams, 1984). 

Two decades later, the first pub- 
lished record describing the diet of 
the Kemp's ridley in the Gulf of 
Mexico was produced (Liner, 1954). 
In that study, gastrointestinal con- 
tents of eight L. kempii ranging in 
size from 3.2 kg to 26.6 kg were 
examined. All the turtles had con- 
sumed portunid crabs iCallinectes 
sp.) and occasional barnacles. 
Dobie et al. (1961), elaborating on 
the findings of Liner (1954), re- 
ported that small molluscs, plant 
parts, and mud were also contained 
in the gastrointestinal tracts of two 
of Liner's turtles. The molluscs in- 
cluded gastropods (Nassarius sp.) 
and bivalves of the genera Nuculana, 
Corbula, and probably Mulinia. 

In Virginia, Hardy (1962) dis- 
sected a single specimen and found 
that the digestive tract contained 
95% Callinectes sp. and one 
swimmerette was identified as that 
of the blue crab, C. sapidus. Re- 
search conducted in the waters of 
Chesapeake Bay, Virginia, by 
Lutcavage (1981) indicated that 
three Kemp's ridley carcasses had 
both blue crabs and Atlantic rock 



26 



Burke et al.: Diet of Lepidochelys kempii 



27 









Table 


1 






Compilation of available 


diet stud 


ies of Kemp's ridley 


sea turtles (Lepidochelys kempii) 


publ 


shed from 1933 


to 1991. The studies are 


ord 


?red from north to south and 


east to west. Marquez (1973) is 


cited from Pritchard 


and Marquez (1973). 
















Author! s) 






Location 




Diet components 




Life stage 


Hardy (1962) 






Chesapeake Bay 




Blue crabs 




Juvenile 


Lutcavage (1981) 






Chesapeake Bay 




Blue crabs 




Juvenile 


Belmund et al. (1987) 






Chesapeake Bay 




Rock and blue crabs 




Juvenile 


DeSola and Abrams (1933) 






Coastal Georgia 




Crabs [Ovalipes spp.) 




Not given 


Carr (1942) 






Florida 




Calico crabs 




Juvenile 


Liner (1954) 






Louisiana 




Blue crabs 




Juvenile 


Dobie et al. (1961) 






Louisiana 




Crabs, whelks, clams 




Juvenile 


Shaver (1991) 






Texas 




Various crab species 




Juvenile 


Marquez (1973) 






Tampico, Mexico 




Crustaceans, fish, molluscs 




Adult 



crabs (Cancer irroratus) in their digestive tracts. 

Recently, Shaver (1991) found that Kemp's ridleys 
in coastal Texas waters preyed mainly on crabs. The 
most commonly ingested species was the speckled 
crab (Arenaeus cribrarius). Many other crab species 
were recorded by Shaver, including purse crabs 
(Persephonia sp.), spider crabs (Libinia sp.), and 
blue crabs (Callinectes sp.). 

During the past decade, the role of the northeast- 
ern coast of the United States in the life cycle of 
Kemp's ridleys has received considerable attention 
(Carr, 1980; Morreale and Standora, 1990 '; Burke 
et al., 1991). The northeastern coast includes the 
New York area which contains over 300 km of shore- 
line, mainly the coastline of Long Island. Long Is- 
land has a variety of marine habitats, including the 
shallow, enclosed waters of the Peconic and south- 
ern bays, the deeper waters of Long Island Sound, 
and the Atlantic Ocean (Fig. 1). Each year Kemp's 
ridleys begin inhabiting the Long Island area dur- 
ing July (Morreale and Standora, 1989 2 ; Morreale 
and Standora, 1990 1 ). To date, all Kemp's ridleys 
encountered in Long Island have been juveniles 
(straight-line carapace length from 22 cm to 42 cm 
x=29.8 cm, SD=3.7 cm [Morreale and Standora, 
1989 2 , 1990 1 ]). This size class of turtles represents 
a range of ages from 3 to 7 years (Zug and Kalb, 1989). 

Between July and early October these young 
Kemp's ridleys are active within the estuarine wa- 
ters (Long Island Sound and the Peconic Bays) and 
the southern bays. Kemp's ridley growth rates as 



1 Morreale, S. J., and E. A. Standora. 1990. Occurrence, move- 
ment and behavior of Kemp's ridley and other sea turtles in 
New York waters. Annual report to the New York State, Dep. 
Environmental Conservation, April 1989-April 1990. 

2 Morreale, S. J., and E. A. Standora. 1989. Occurrence move- 
ment and behavior of the Kemp's ridley and other sea turtles 
in New York waters. Annual report to the New York State, Dep. 
Environmental Conservation, April 1988-April 1989. 



high as 25% body weight per month indicate that 
waters around Long Island, New York, provide 
abundant food resources for the maintenance and 
growth of the juvenile turtles (Standora et al., 1989; 
Burke, 1990). During October the turtles begin 
moving out of the estuaries and into the ocean. Long 
distance recaptures of Kemp's ridley, green 
(Chelonia mydas), and loggerhead (Caretta caretta) 
sea turtles tagged near Long Island indicate that 
some turtles emigrate to the southeastern United 
States (Morreale and Standora, 1989 2 ; Burke, 1990; 
Morreale and Standora, 1990 1 ). Kemp's ridleys that 
do not emigrate by late November are likely to be- 
come cold-stunned (Burke et al., 1991). Cold-stun- 
ning, or severe hypothermia, occurs when ambient 
water temperatures fall below 10°C (Schwartz, 
1978). Cold-stunning causes turtles to become tor- 
pid and buoyant, and eventually results in death. 
In Long Island, declining water temperatures usu- 
ally reach 10°C during early December. 

The cold-stunning phenomenon, other types of 
strandings, and live captures of sea turtles during 
commercial fishing operations can be utilized as 
sources of turtles for dietary studies. The goal of the 
current study is to provide a quantitative descrip- 
tion of the diet of Kemp's ridleys in the northeast- 
ern United States based on gut contents from car- 
casses, previously preserved dietary samples, and 
feces from live turtles. 

Materials and methods 

The dietary components of the Kemp's ridley were 
assessed by using two separate approaches. First, 
fecal samples were collected from live turtles and 
examined for their constituents. Second, complete 
gastrointestinal contents were removed from dead 
turtles and identified. Samples were obtained from 



28 



Fishery Bulletin 92(1), 1994 




Figure 1 

The waters from which Kemp's ridley sea turtles, Lepidochelys kempii, were obtained for this study can be di- 
vided into four habitats: Long Island Sound, where most of the stranded turtles were recovered; the Atlantic Ocean, 
which was the habitat of two turtles in the study; the southern bays, where one live capture and one boat-hit 
turtle were recovered; and the Peconic Bay system, where most of the turtles for the fecal analysis and several 
turtles for the digestive tract analysis wree recovered. 



turtles encountered in New York waters from 1985 
through 1989. 

Nineteen fecal samples were obtained. Fourteen 
were collected during 1989, three during 1988, and 
two during 1987. Of these fecal samples, 17 were 
obtained from live turtles captured during warmer 
months (June to October) and two samples were 
retrieved from revived, cold-stunned turtles in late 
November. Captured turtles were obtained from lo- 
cal commercial fishermen who were asked to retain 
turtles caught incidentally in fishing gear (predomi- 
nantly pound nets). After the fishermen docked, they 
called a 24-hour number to reach a biologist, who 
generally picked up the turtle while the fishermen 
were still unloading their catch. All noncold-stunned 
Kemp's ridleys received from commercial fisheries 
in Long Island were alive and apparently healthy. 

All turtles were weighed and measured upon re- 
turn to the laboratory. Each turtle was then allowed 
to swim freely in an individual 2100-liter tank and 
was offered either squid or clam meat. Most Kemp's 
ridleys accepted the food offerings, but many fed 
only after the food was dangled in front of them for 



as long as 2-3 hours. Feeding often induced defeca- 
tion within a relatively short time. 

Tanks were checked at least three times a day for 
the appearance of feces. Filter intakes in the tanks 
were elevated and covered, except for small holes, 
to insure against sample loss. When feces were ob- 
served, they were immediately removed and placed 
in individual sample jars. If a turtle did not defecate 
within 24 hours of being placed in captivity, it was 
given an enema of dioctyl sodium sulfosuccinate 
(Disposaject brand, Pitman-Moore Inc.). If a fecal 
sample was still not obtained after another 24 hours, 
the turtle was released. 

The rate of food passage was examined during this 
study to insure that samples were not polluted with 
prey items eaten while the turtles were in the 
fishermen's nets. Gut passage rates were deter- 
mined for two Kemp's ridleys by feeding them 
declawed lobsters (Homarus americanus). Lobster 
was used as a tracer because it has never been re- 
ported as a prey item and is consumed relatively 
readily by the turtles. By monitoring fecal output, 
the amount of time between ingestion of the lobster 



Burke et al.: Diet of Lepidochelys kempii 



29 



and its first appearance in the feces was determined. 

All fecal samples collected for dietary analysis 
were immediately placed in preservative. For fecal 
samples obtained during 1989, animal components 
were preserved as described by Zinn ( 1984) and al- 
gae were preserved in Transeau's solution ( 10 parts 
formalin/30 parts ethanol/60 parts distilled H. 2 0/25 
mg CuS0 4 /L). Feces obtained prior to 1989 were pre- 
served in 10% formalin. 

Analysis of the fecal samples was conducted in 
January 1990, after all the samples were collected. 
The samples were removed from the preservative 
and air dried for 24 hours on wire mesh in an en- 
closed hood. The samples were then placed in a U.S. 
standard number-5 mesh (4 mm) sieve and pieces 
smaller than 4 mm were separated out by shaking 
the sample in a Tyler RO-TAP testing sieve shaker 
for three minutes. Pieces smaller than 4 mm were 
not identified because of the difficulty of assigning 
them to a meaningful category. The amount of 
sample lost because of this constraint was never 
greater than 5% for any given sample. 

Each fecal sample was examined under a dissect- 
ing microscope and each fragment of the sample was 
identified to the lowest taxon possible. Fragments 
belonging to the same taxonomic level were grouped. 
A list of components (e.g., one species of crab is one 
component) was compiled for each sample and the 
data were analyzed to determine the percentage of 
turtles in which each component occurred. Less than 
1% of the fragments could not be assigned to a taxo- 
nomic category. 

For the 1989 samples only, the relative amount of 
each dietary component was determined by oven 
drying each component from each sample for 48 
hours at 60°C and weighing it. The dry weights were 
then used to determine the relative importance of 
the different dietary components in each turtle's 
fecal sample. Dry weight analysis was conducted by 
finding the percentage of each sample weight rep- 
resented by each component and then determining 
the mean for that component. This technique of 
analyzing dry weights as a percentage eliminated 
over- or under-representation of large or small fe- 
cal samples. 

A second method of determining dietary compo- 
nents was analysis of gastrointestinal contents from 
stranded, dead turtles. Stranded Kemp's ridleys died 
from a number of causes: cold-stunning, boat colli- 
sions, entanglement in a gill net, and natural and 
unknown causes. Whenever possible, each stranded 
turtle was weighed, measured (straight-line cara- 
pace length) and dissected. Following removal, in- 
testinal contents were placed in 95% ethanol (1985), 
10% formalin (1986-1988), or treated in the same 



manner as the fecal samples (1989). Identification 
of intestinal tract contents was performed during 
1990. All components of each sample were identified 
to the lowest taxon possible, generally to species. 
These data were used to determine the percentage 
of turtles in which the components occurred. 

Results 

The food passage rate analysis indicated that lob- 
ster was retained within the digestive tracts of the 
two Kemp's ridleys for seven and eight days. Be- 
cause fecal samples were obtained within 48 hours 
of receiving a turtle from a fisherman, we believe 
the possibility of samples having been "contami- 
nated" by items eaten while the turtles were in the 
fishermen's nets is minimal. 

Mean straight-line carapace length for the 19 
turtles in the fecal analysis study was 32.3 cm 
(range=24.7 to 42.7 cm, SD=4.87). Eighteen of the 
19 turtles consumed crabs (Fig. 2). Mollusc species 
were found in 26% of the fecal samples and algae 
were found in 11%> of the Kemp's ridley feces. Natu- 
ral and synthetic debris were present in 21% and 
11% of the feces respectively. 

Crab species that were identified included nine- 
spined spider crabs, Atlantic rock crabs, and lady 
crabs (Ovalipes ocellatus). Further examination of 
only the crab portion of the feces revealed that 58% 
of the turtles had consumed spider crabs, 36% had 
eaten rock crabs, and 16% had consumed lady crabs. 



100 



60 



w 40 
O 



















- 






n = 19 












m 


'.'.'. 








i 







CRAB MOLLUSK ALGAE NATURAL SYNTHETIC 

DEBRIS DEBRIS 

Figure 2 

Percent occurrence of various prey items identified 
in the feces of 19 Kemp's ridley sea turtles 
(Lepidochelys kempii) that were live-captured in 
Long Island waters. Each bar indicates the percent 
of turtles in which the prey items occurred. 



30 



Fishery Bulletin 92(1). 1994 




a. 
z 
< 



CRAB MOLLUSK ALGAE NATURAL SYNTHETIC 

DEBRIS DEBRIS 

Figure 3 

Mean percent of the fecal dry weight of general 
catergories of Kemp's ridley sea turtles 
(Lepidochelys kempii) prey items. Each area repre- 
sents the mean percent of dry weight for that com- 
ponent of the feces (n=14). Crabs composed the pre- 
dominant portion of the feces. 



o 
\- 

z 















70 - 








60 - 






50 - 




n = 18 


40 








30 - 








20 










10 - 














- 


.-. 






i 







CRAB 



MOLLUSK 



NATURAL 
DEBRIS 



Figure 4 

The percent of Kemp's ridley sea turtles 
(Lepidochelys kempii) from the digestive tract analy- 
sis that had consumed various types of ingesta. 
Most of the turtles had consumed crabs. Synthet- 
ics and algae were not present in the digestive 
tracts. 



Included in three fecal samples were crab parts from 
which the fragments could not be identified to genus. 

Mollusc species in the samples included blue 
mussels (Mytilus edulis) and bay scallops 
(Argopectin irradians). Two Kemp's ridley fecal 
samples contained mollusc fragments that could not 
be identified beyond phylum. Algal species in the 
samples included Sargassum natans, Fucus sp., and 
Ulua sp. A few turtles had small pieces of the mac- 
rophyte Zostera marina as well. Natural debris in- 
cluded such things as pebbles, small rocks, and bird 
feathers. Synthetic debris included only small pieces 
of polystyrene and latex. 

Analysis of fecal components with dry weights 
(mean of percent per sample) revealed that crabs 
were the predominant component of all but one of 
the 14 fecal samples from 1989. The mean percent 
of crab dry weight for the samples was 80% (Fig. 3). 
The mean percent dry weight for each crab species 
revealed that spider crabs composed 60% of the 
identifiable crab parts. The remainder was com- 
posed of 22% rock crabs and 18% lady crabs. Thus, 
most of the Kemp's ridleys had consumed spider 
crabs, which represented a large portion of the bulk. 
Although more turtles consumed rock crabs than 
lady crabs, Kemp's ridleys that consumed lady crabs 
had feces composed exclusively of them. 

For the period 1985 througn 1989, 87 dead Kemp's 
ridleys were recovered from Long Island's waters. 
Gastrointestinal tracts were removed from 40 of the 



87 turtles. Eighteen of the 40 stranded Kemp's rid- 
leys contained identifiable diet components in the 
gut. All 18 turtles were juveniles. Mean straight-line 
carapace length for the 18 stranded turtles was 30.5 
cm (range=24.8 cm to 39.7 cm, SD=3.5 cm). Thirteen 
of the 18 gastrointestinal tracks contained crab 
parts and seven contained mollusc shells (Fig. 4). 

The most frequently encountered crabs in the gut 
content samples were spider crabs and rock crabs. 
Spider crab fragments were found in five of the 18 
samples; rock crabs were found in four of the 18 
samples. Lady crabs were found in two of the 
samples and the blue crab (C. sapidus) was found 
in the digestive tract of one Kemp's ridley. Two of 
the turtles had crab parts in their digestive tracts 
that could not be assigned reliably to any genus. 

An additional 14 of the 40 Kemp's ridleys that 
were dissected had completely empty digestive 
tracts. All of these turtles had stranded from cold- 
stunning. Upon further review of necropsy data 
sheets from all of the Kemp's ridleys that had 
stranded during the study period, but from which 
samples were not preserved, it was noted that al- 
most all of the cold-stunned individuals had empty 
or almost empty gastrointestinal tracts. 

The remaining eight turtles had been collected in 
1985 and 1986, and gut contents were unidentifiable 
because of improper preservation. These samples 
had been preserved for as long as five years prior 
to examination. 



Burke et al.: Diet of Lepidochelys kempn 



Discussion 

The analysis of fecal samples from live turtles and 
of gut contents from dead specimens strongly sug- 
gests that crabs are the main dietary component for 
Kemp's ridleys in New York waters. Crab parts were 
present in 18 of the 19 turtles from which fecal 
samples were obtained and were the predominant 
food item by dry weight analysis. The analysis of 
fecal material, however, may be biased because it 
examines only that material which has not been 
fully digested. This could cause overrepresentation 
of less digestible components. 

The gastrointestinal tract results (which are less 
susceptible to such bias) support the results of the 
fecal sample analysis. Of the 18 stranded turtles 
which contained identifiable food items, 13 con- 
tained crab parts in their guts. Gut contents can 
potentially be biased because of differential diges- 
tion. However, from our qualitative observation of 
the condition of the intestinal contents during dis- 
section, we believe the components described herein 
are representative of the diet. 

One difference between the fecal and intestinal 
samples was the source of the turtles. Most fecal 
samples were obtained from turtles captured in the 
Peconic Bays, but most stranded turtles were recov- 
ered on beaches adjacent to Long Island Sound. 
Presumably the dietary samples reflect feeding ac- 
tivities near the location of capture (or stranding). 
Thus, the observation of spider and rock crabs as the 
predominant components in the diets of both live- 
captured and stranded turtles emphasizes their 
importance as food items. 

The dietary components observed during the 
study may be related to the relative abundance of 
the prey species in the environment. Of the four 
species of crab that were identified, the spider crab 
was both the most frequently encountered fecal com- 
ponent and the predominant crab identified in the 
gut contents of dead turtles. During the course of 
our studies we have noted that the nine-spined spi- 
der crab was one of the most common crabs in the 
waters where the turtles occurred. We have observed 
local commercial fishermen retrieving thousands of 
spider crabs while hauling in their nets. The Atlan- 
tic rock crab was also frequently encountered in the 
feces and gut contents of the turtles. The rock crab 
is also abundant in many of the areas in which the 
turtles occur. 

Not all of the dietary make-up observed in this 
study can be explained by prey abundance. The 
green crab (Carcinus maenus) is very common in 
many of Long Island's estuaries but was not present 
in any of the turtles examined. This species usually 



inhabits shallower, rocky intertidal and subtidal 
habitats (Ropes, 1968; Williams, 1984), and our re- 
search on turtle behavior indicates that the Kemp's 
ridleys typically forage in deeper waters (Standora 
et al., 1990). 

While we have commonly encountered lady crabs 
in the waters where turtles forage, this species was 
represented in only a few samples. Also rare in the 
samples was the locally and commercially harvested 
blue crab. Both the lady crab and the blue crab are 
portunid crabs, capable of swimming very quickly. 
This characteristic differentiates the portunids from 
the slower walking crabs, such as the spider and 
rock crabs. 

The only molluscs consumed by turtles examined 
during this study included a few fragments of rela- 
tively thin-shelled blue mussels (Mytilus edulis) and 
bay scallops (Argopectin irradians), and entire shells 
of the small three-lined mud snail (Nassarius 
trivitattus). These mud snails are scavengers and 
can be found locally in association with dead fish 
and crabs (Long Island Shell Club, 1988). Their oc- 
currence in four turtles, all of which had been cold- 
stunned, may indicate that the turtles were scaveng- 
ing during periods of low water temperature. 

Because sea turtles were obtained from different 
sources in New York waters, it was possible to ob- 
tain dietary information on a larger number of 
Kemp's ridleys. In many of the previous studies 
presented in Table 1, portunid crabs were indicated 
as a main dietary component for Kemp's ridleys. 
Although this crab family was observed in some 
New York turtles, it was of secondary importance to 
the walking crabs. 

In terms of the overall life cycle of Kemp's ridleys, 
it appears that post-pelagic juveniles exploit the 
benthic environments of Long Island's estuaries, 
preying mainly on walking crabs. Data from our 
ongoing research indicate that sea turtles emigrat- 
ing from New York inshore waters travel to south- 
ern coastal areas. Kemp's ridleys exhibiting this 
behavior may join the more southerly portion of the 
Atlantic population. Therefore, management plans 
for Kemp's ridleys should consider factors that af- 
fect benthic fauna, especially the abundant crab 
populations in the northeastern region. Such im- 
pacts could have far-reaching effects on a critical 
stage in the lives of these endangered sea turtles. 

Acknowledgments 

This study was supported by a grant from the Na- 
tional Marine Fisheries Service under contract num- 
ber 40AANF902823. We thank Phil Williams for his 
encouragement and support. Long-term support for 



32 



Fishery Bulletin 92(1), 1994 



sea turtle studies in New York was provided by the 
N.Y. State Dept. "Conservation's Return a Gift to 
Wildlife" program. Manuscript preparation was 
aided by contract DE-AC09-76SROO-819 between 
the University of Georgia and the U.S. Department 
of Energy. Workspace was provided by the State 
University College at Buffalo and the Okeanos 
Foundation. Turtle collection could not have been 
accomplished without the help of hundreds of vol- 
unteers and the commercial fishermen of Long Is- 
land, New York. We thank Anne Meylan for main- 
taining intestine samples and records from the years 
1985 and 1986. For their efforts in collecting turtles, 
we thank C. Coogan, P. Logan, S. Sadove, and R. 
Yellin. The Long Island Shell Club donated mollusc 
voucher specimens. William Zitek graciously pro- 
vided necropsy facilities during 1985 and 1986, and 
veterinary advice during 1989 that allowed us to 
increase the number of fecal samples obtained. 



Literature cited 

Bellmund, S. A., J. A. Musick, R. C. Klinger, R. A. 
Byles, J. A. Keinath, and D. E. Barnard. 

1987. Ecology of sea turtles in Virginia. Spec. Sci. 
Rep. No. 19, Virginia Institute of Marine Science, 
Coll. of William and Mary, Gloucester Point, Virginia. 

Burke, V. J. 

1990. Seasonal ecology of Kemp's ridley 
(Lepidochelys kempi) and loggerhead (Caretta 
caretta ) sea turtles in the waters of Long Island, 
New York. Master's thesis, State University of 
New York, College at Buffalo, NY. 

Burke, V. J., E. A. Standora, and S. J. Morreale. 

1991. Factors affecting strandings of cold-stunned 
Kemp's ridley and loggerhead sea turtles in Long 
Island, New York. Copeia 1991:1136-1138. 

Carr, A. 

1942. Notes on sea turtles. Proc. New England 

Zoological Club 21:1-16. 
1980. Some problems of sea turtle ecology. Am. 
Zool. 20:489-498. 
DeSola, C. R., and F. Abrams. 

1933. Testudinata from southeastern Georgia, in- 
cluding the Okefinokee swamp. Copeia 1:10-12. 
Dobie, J. L., L. H. Ogren, and J. F. Fitzpartick Jr. 

1961. Food notes and records of the Atlantic ridley 
turtle (Lepidochelys kempii) from Louisi- 
ana. Copeia. 1961:109-110. 

Federal Register. 

1989. Endangered and threatened wildlife and 
plants. 50 CFR 17.11 and 17.12. 
Hardy, J. D. 

1962. Comments on the Atlantic ridley turtle, 
Lepidochelys olivacea kempi, in the Chesapeake 
Bay. Chesapeake Science 3:217-220. 



Liner, E. A. 

1954. The herpetofauna of Lafayette, Terrebonne 
and Vermilion Parishes, Louisiana. Proc. Louisi- 
ana Academy of Sciences. 17:65-85. 

Long Island Shell Club. 

1988. Seashells of Long Island, New York. Long 
Island Shell Club, Inc., Long Island, NY. 

Lutcavage, M. 

1981. The status of marine turtles in Chesapeake 
Bay and Virginia coastal waters. Master's thesis, 
College of William and Mary, VA. 

Marine Turtle Newsletter. 

1989. IUCN resolution urges maximum size limits, 
protection of habitat, TED's. Mar. Turtle News- 
letter. 44:1-3. 

Pritchard, P. C. H., and R. Marquez. 

1973. Kemp's ridley turtle or Atlantic ridley. 
International Union for the Conservation of Na- 
ture and Natural Resources Monograph No. 2, 
Marine Turtle Series. Morges, Switzerland. 

Ropes, J. W. 

1968. The feeding habits of the green crab, 
Carcinus maenas (L.). Fish. Bull. 67:183-200. 

Schwartz, F. J. 

1978. Behavioral and tolerance responses to cold 
water temperatures by three species of sea turtles 
(Reptilia, Cheloniidae) in North Carolina. Florida 
Marine Research Pub. 33:16-18. 

Shaver, D. J. 

1991. Feeding ecology of wild and head-started 
Kemp's ridley in South Texas waters. J. Herpetol. 
25:327-334. 

Standora, E. A, S. J. Morreale, E. Estes, R. Thomp- 
son, and M. Hilburger. 

1989. Growth rates of Juvenile Kemp's ridleys and 
their movement in New York waters. Proceedings 
of the Ninth Annual Workshop on Sea Turtle Con- 
servation and Biology, p. 175-177. 

Standora, E. A., S. J. Morreale, R. D. Thompson, 
and V. J. Burke. 

1990. Telemetric monitoring of diving behavior and 
movements of juvenile Kemp's ridleys. Pro- 
ceedings of the Tenth Annual Workshop on Sea 
Turtle Conservation and Biology, 133 p. 

Williams, A. B. 

1984. Shrimps, lobsters, and crabs of the Atlantic 
coast of the eastern United States, Maine to Flori- 
da. Smithsonian Institution Press, Washington, D.C. 
Zinn, D. J. 

1984. Marine mollusks of Cape Cod. Cape Cod 
Museum of Natural History, Brewster, Massachu- 
setts, 78 p. 
Zug, G. R., and H. J. Kalb. 

1989. Skeletochronological age estimates for juve- 
nile Lepidochelys kempi from Atlantic coast of 
North America. Proceedings of the Ninth Annual 
Workshop on Sea Turtle. 



Abstract. The tripletail, 

Lobotes surinamensis, is the only 
member of the family Lobotidae in 
the western Atlantic Ocean, and 
its life history is poorly under- 
stood. We describe development of 
tripletail larvae, clarify the litera- 
ture on their identification, and 
discuss their temporal and spatial 
distribution in the northern Gulf 
of Mexico. Larval tripletail are 
characterized by 1) a vaulted, me- 
dian supraoccipital crest with 
spines along the leading edge; 2) 
precocious, heavily pigmented pel- 
vic fins; and 3) large preopercular 
spines. In addition, the surface of 
the frontal and supraoccipital 
bones have a reticulated pattern of 
depressions or "waffled" appear- 
ance. Transition to juvenile stage 
begins at about 9.0-9.5 mm stan- 
dard length. Tripletail have three 
supraneurals, six branchiostegal 
rays, 11 + 13 vertebrae, 27 dorsal 
rays (XII, 15), and 14-15 anal rays 
(III, 11-12). Overall, 75% of trip- 
letail larvae were found in waters 
>28.8°C, >30.3 ppt, and at stations 
>70 m deep. Larval tripletail were 
collected primarily from July 
through September and almost 
exclusively in surface tows. Triple- 
tail spawn offshore. Juveniles, al- 
though sporadic, are apparently 
not uncommon in Gulf of Mexico 
estuaries during summer. 



Larval development of tripletail, 
Lobotes surinamensis (Pisces: 
Lobotidae), and their spatial and 
temporal distribution in the 
northern Gulf of Mexico* 

James G. Ditty 

Center for Coastal, Energy, and Environmental Resources 
Coastal Fisheries Institute, Louisiana State University 
Baton Rouge, LA 70803 

Richard F. Shaw 

Center for Coastal, Energy, and Environmental Resources 
Coastal Fisheries Institute, Louisiana State University 
Baton Rouge, LA 70803 



Manuscript accepted 4 October 1993 
Fishery Bulletin 92:33-45 (1994) 



The percoid family Lobotidae is 
usually considered to comprise two 
genera with about four species 
(Nelson, 1984), although Johnson 
( 1984) only included Lobotes, ques- 
tioning the affinity of Datnioides. 
The tripletail, Lobotes surinamen- 
sis, is cosmopolitan and found in all 
warm seas (Fischer, 1978); one 
adult was recorded as far north as 
St. Margarets Bay, Nova Scotia 
(44°37'N, 64°03'W (Gilhen and 
McAllister, 1985). Lobotes surina- 
mensis is the only member of the 
family in the Gulf of Mexico (Gulf) 
(Hoese and Moore, 1977). Tripletail 
generally occur along the Gulf 
coast from April through early Oc- 
tober (Baughman, 1941) and mi- 
grate south during fall and winter 
(Merriner and Foster, 1974). Al- 
though apparently abundant no- 
where, adult and juvenile tripletail 
are not uncommon in bays, sounds, 
and estuaries along the north-cen- 
tral Gulf coast during summer 
(Baughman, 1941; Benson, 1982). 
Tripletail up to 18.6 kg and 89 cm 
standard length (SL) have been 
caught, but most average between 
1 and 7 kg (Gudger, 1931; Baugh- 
man, 1941). Tripletail often are in- 



cluded as a category in Gulf fishing 
rodeos (Benson, 1982) because of 
their reputation as "a bold biter" 
and strong fighter (Gudger, 1931; 
Baughman, 1941). Tripletail enter 
the commercial catch on the east 
and west coasts of Florida and a 
few tons are taken annually 
(Fischer, 1978). 

The development of tripletail lar- 
vae and their spatial and temporal 
distribution is poorly understood. 
Hardy ( 1978) compiled information 
on tripletail life history. Uchida et 
al. (1958) and Konishi (1988) pro- 
vide limited information and illus- 
trations of tripletail larvae off Ja- 
pan; however, Konishi's 5.1-mm 
larva is misidentified. Johnson 
(1984) commented on cranial mor- 
phology. Our objectives were to de- 
scribe the development of tripletail 
larvae, to clarify the literature on 
their identification, and to discuss 
the spatial and temporal distribu- 
tion of larval tripletail in the north- 
ern Gulf of Mexico. 



* Louisiana State University Coastal Fish- 
eries Institute Contribution No. LSU- 
CFI-92-8. 



33 



34 



Fishery Bulletin 92(1). 1994 



Materials and methods 

Tripletail larvae were obtained from museum collec- 
tions throughout the Gulf of Mexico to determine 
their spatial and temporal distribution. These in- 
clude collections from the Southeast Area Monitor- 
ing and Assessment Program's (SEAMAP) ichthy- 
oplankton surveys of the Gulf from 1982 through 
1986 (SEAMAP 1983-1987 1 ); National Marine Fish- 
eries Service (NMFS, Panama City, Florida) and 
Louisiana State University (LSU) collections from 
within riverine and oceanic frontal zones off the 
Mississippi River delta; and collections made by the 
Gulf Coast Research Lab (GCRL), Ocean Springs, 
Mississippi, and by Freeport-McMoRan Inc., New 
Orleans (Appendix Tables 1 and 2). 

SEAMAP collections from 1982 to 1986 represent 
the first time-interval for which a complete set of 
data were available. Standard ichthyoplankton 
survey techniques as outlined by Smith and 
Richardson (1977) were employed in data collection. 
SEAMAP stations sampled by NMFS vessels were 
arranged in a systematic grid of about 55-km inter- 
vals. NMFS vessels primarily sampled waters >10 
m deep. Each cooperating state had its own sam- 
pling grid and primarily sampled their coastal wa- 
ters. Latitude 26°00'N was the southern boundary 
of the survey area. Hauls were continuous and made 
with a 60-cm bongo net (0.333-mm mesh) towed 
obliquely from within 5 m of the bottom or from a 
maximum depth of 200 m. A flowmeter was mounted 
in the mouth of each net to estimate volume of wa- 
ter filtered. Ship speed was about 0.75 m/sec; net 
retrieval was 20 m/min. At stations <95 m deep, tow 
retrieval was modified to extend a minimum of 10 
minutes in clear water or 5 minutes in turbid wa- 
ter. Tows were made during both day and night 
depending on when the ship occupied the station. 
Overall, 1,823 bongo-net tows were collected and 
processed during these years. The SEAMAP effort 
from 1982 to 1984 also involved the collection and 
processing of 814 neuston samples taken with an 
unmetered 1x2 m net (0.947-mm mesh) towed at 
the surface for 10 minutes at each station. SEAMAP 
sampling during April and May was primarily be- 
yond the continental shelf, whereas that during 
March and from June through December was over 
or immediately adjacent to the shelf at stations <180 
m deep. No samples were taken during January and 
February Additional information on the temporal 
and spatial coverage of SEAMAP plankton surveys 



1 SEAMAP. 1983-1987. (plankton). ASCII characters. Data for 
1982-1986. Fisheries-independent survey data. National Ma- 
rine Fisheries Service, Southeast Fisheries Center: Gulf States 
Marine Fish. Comm., Ocean Springs, unpubl. data. 



is found in Stuntz et al. ( 1985), Thompson and Bane 
(1986, a and b), Thompson et al. (1988), and Sand- 
ers et al. (1990). 

Collections from frontal zones off the Mississippi 
River delta include 311 surface-towed 1x2 m neus- 
ton net samples (0.333-mm mesh) made by NMFS. 
NMFS samples were collected during May, August, 
September, and December (1986 to 1989), although 
not all four months were sampled each year (Appen- 
dix Table 1). We also examined 63 surface-towed 
1-m 2 Tucker trawl samples (0.363-mm mesh) taken 
at seven stations during July 1987, and 45 surface- 
towed multiple opening/closing net and environmen- 
tal sensing system (MOCNESS) (Wiebe et al., 1976) 
samples (0.363-mm mesh) collected at five stations 
during April 1988. These samples were from LSU 
collections. In addition, we examined 17 samples 
from stations taken by LSU inside the 100-0m 
isobath during October 1990. The sampling area 
during October 1990 extended 140 km west from 
Southwest Pass of the Mississippi River delta along 
the inner-to mid-shelf. Samples were collected with 
a 60— cm bongo net (0.333-mm mesh) towed ob- 
liquely to the surface from 5 m of the bottom or from 
a maximum depth of 50 m (Appendix Tables 1 and 2). 

Museum collections from GCRL and Freeport- 
McMoRan, Inc. were primarily taken off Mississippi 
Sound and within the Barataria Bay system of Loui- 
siana, respectively. Gear type and most environmen- 
tal data were not available from these two institu- 
tions (Appendix Table 2). 

Temperature and salinity data were from the sea 
surface. Hydrographic data from stations where lar- 
vae were taken were multiplied by the total num- 
ber of larvae collected at each station to derive 
median and mean hydrographic values. This method 
gives weight to distribution of larvae rather than to 
distribution of stations. We used percent cumulative 
frequency for defining the relationship between dis- 
tribution of larval tripletail and water temperature, 
salinity, and station depth. Percent frequency indi- 
cates the range of hydrographic conditions most of- 
ten associated with occurrences of tripletail larvae. 
Median, mean, and percent cumulative frequency 
statistics were calculated (SAS Institute, 1985). 

An examination of tripletail larvae was made to 
describe developmental morphology. Body measure- 
ments were made on 21 tripletail between 2.2 and 
23.0 mm SL (Table 1) according to the methods of 
Hubbs and Lagler (1958) and Richardson and 
Laroche (1979). Measurements were made to the 
nearest 0.1 mm with an ocular micrometer in a dis- 
secting microscope. We follow Leis and Trnski's 
(1989) criteria for defining length of preopercular 
spines, body depth, head length, eye diameter, and 



Ditty and Shaw: Larval development and distribution of Lobotes sunnamensis 



35 











Table 


1 








Morphometries 


of larval triplet 


ail [Lobotes 


sunnamensis 


) from the 


northern Gulf 


of Mexico. Measurements 


are expres 


sed as % standard length (SL). 
















Preanal 


Head 


Snout 


Orbit 


Greatest 


Upper jaw 


Prepelvic 


SL 


n 


length 


lengt h 


length 


diameter 


body depth 


length 


distance 


2.2-2.4 


2 


60.5-66.0 


29.0-29.5 


6.5-7.0 


12.5-13.5 


25.0-27.5 


11.5-14.5 




4.0-5.9 


3 


60.0-70.0 


37.5-40.0 


7.5-10.0 


14.0-14.5 


40.0-53.5 


20.0-20.0 


37.5-55.0 


6.0-7.9 


4 


69.5-79.5 


38.0-43.0 


6.5-9.5 


14.0-16.0 


51.0-59.5 


15.5-17.5 


38.0-57.0 


8.0-9.9 


4 


68.0-77.5 


34.5-38.5 


5.5-6.5 


14.0-15.5 


58.0-59.0 


14.0-15.5 


39.0-48.0 


10.0-11.9 


2 


68.5-74.0 


38.0-39.0 


6.0-6.5 


14.5-15.0 


54.0-56.5 


14.0-14.5 


39.0-40.0 


13.0-14.9 


2 


71.5-72.5 


35.5-37.0 


6.5-7.0 


13.0-14.0 


55.0-57.5 


13.5-14.0 


40.0-44.5 


15.0-16.9 


2 


72.5-77.5 


34.5-35.5 


6.0-6.5 


12.5-13.0 


56.5-58.0 


12.5-13.0 


42.0-47.5 


21.0-23.0 


2 


74.0-76.5 


39.5-41.5 


7.0-8.0 


12.0-13.0 


54.5-58.0 


13.0-14.0 


46.5-52.0 



eye diameter/head length ratio. We consider noto- 
chord length in preflexion and flexion larvae synony- 
mous with SL in postflexion larvae and report all 
lengths as SL unless otherwise noted. Specimens 
were fixed in 10% formalin and later transferred to 
70% ethyl alcohol. Representative specimens were 
illustrated with the aid of a camera lucida. Because 
of the paucity of material, only two specimens were 
cleared with trypsin and stained with alizarin to 
examine head spines. We examined the surface of 
the occipital and frontal bones with a scanning elec- 
tron microscope (SEM) after the epithelium was par- 
tially digested with trypsin. Soft rays of the dorsal and 
anal fins were counted when their pterygiophores were 
visible, and spines were counted when present. 

Results 

Larval morphometries and pigmentation 

Ninety-eight larval or juvenile tripletail were exam- 
ined during this study (Appendix Table 2): 7 were 
preflexion or flexion (<5.0 mm), 34 were postflexion 
(5.1 to 9.5 mm), and 57 were transforming or juve- 
nile (>9.5 mm). Body depth increased rapidly dur- 
ing preflexion and flexion with depth >50% SL by 
5.0 mm. The gut was straight. Larvae had 24 
myomeres which became obscured by pigment in 
postflexion larvae. Preanal length was 60-65% SL 
in preflexion larvae and increased to 70-75% SL in 
larvae >5.0 mm. Head length averaged 29% SL dur- 
ing preflexion and increased to about 40% SL in 
juveniles. The head became increasingly steep, and 
the upper profile of the forehead was concave by 20.0 
mm. The eye was large and had an orbit diameter 
usually from 35 to 40% head length ( 12.5 to 15.0% 
SL) by 4.0 mm. The upper jaw reached about mid- 
eye. Pelvic fins were precocious, heavily pigmented, 
and inserted behind the pectoral fins near mid-body, 



usually about 40-50% SL (Table 1). The pelvic fins 
extended past the anus by 4.0 mm. 

Early preflexion larvae of 2.2-2.4 mm were 
sparsely pigmented; pigment was primarily re- 
stricted to the head and abdomen. On the head, 
external pigment was present on the posterior sur- 
face of the midbrain, posteriorly at the base of the 
supraoccipital crest, on the nape, and immediately 
anterior to the cleithral symphysis (Fig. 1). By early 
flexion (4.0 mm), pigment was added between the 
fore- and mid-brain and on the preopercle above the 
dorsal-most preopercular spine (Fig. 1). Pigment 
occurred at the tip of the upper and lower jaws and 
at the angle of the preopercle near the base of the 
angle spine by 5.0 mm. The head became heavily 
pigmented during postflexion. By 10.0 mm, a band 
of pigment extended diagonally across the head from 
the nape to the orbit and from below the orbit to the 
angle of the preopercle (Fig. 1). The eye was at the 
apex of this chevron-shaped band of pigment. Two 
parallel stripes of pigment were present between the 
orbits by 14.0-15.0 mm, extending from the nares 
to the anterior margin of the supraoccipital crest. 
These pigment stripes became better formed as lar- 
vae developed. On the abdomen, melanophores were 
distributed dorsally over the air bladder, and dor- 
sally and ventrally along the visceral mass and 
hindgut of early larvae (Fig. 1). By early flexion, 
pigment also was present on the pectoral axilla, 
posteriorly over the visceral mass and hindgut, and 
was scattered laterally over the body above the vis- 
ceral mass. Body pigmentation increased rapidly 
during early postflexion and extended posteriorly to 
the caudal peduncle by 6.0 mm (Fig. 1). Blotches or 
mottled areas of pigment formed over the body by 
8.0-9.0 mm, becoming more evident as larvae devel- 
oped (Fig. 1). 

Pigment along the ventral midline between the 
anus and notochord tip was restricted to four to five 



36 



Fishery Bulletin 92(1), 1994 



melanophores in early larvae. 
By early flexion, only one or 
two postanal melanophores 
were present along the ventral 
midline and these were located 
on the caudal peduncle and at 
the posterior margin of the 
hypural bones (Fig. 1). Pigment 
was also present on the devel- 
oping pelvic fins by early flex- 
ion. Melanophores were distrib- 
uted over the dorsal and anal 
spines by 6.0 mm and over the 
anterior-most dorsal and anal 
rays by 8.5-9.5 mm. Pigment 
covered all but the distal tips of 
the dorsal and anal rays by 
15.0 mm. Only the base of the 
caudal- and pectoral-fin rays 
were pigmented by 13.0-14.0 
mm (Fig. 1) and pigment cov- 
ered about 50% of the caudal 
fin in a 23.0-mm larva. Pigment 
occurred only over the proximal 
portion of the dorsal-most pec- 
toral-fin rays in the 23.0-mm 
larva. 

Head spination and fin 
development 

Tripletail larvae were charac- 
terized by a vaulted, median 
supraoccipital crest, which 
originated above mid-eye, and 
by numerous spines and ridges 
on the head. Larvae of 2.2-2.4 
mm had five to six spines along 
the leading edge of the supra- 
occipital crest and one spine on 
the posterior edge (Fig. 1). Usu- 
ally eight spines occurred along 
the leading edge of the crest by 
4.0 mm, giving the crest a ser- 
rate appearance. Length of the 
crest and its spines decreased 
as larvae grew (Fig. 1); and the 
entire supraoccipital crest was 
resorbed by 15.0-16.0 mm. The 
surface of the supraoccipital 
and frontal bones had a reticu- 
lated pattern of depressions or "waffled" appearance 
(Fig. 2). Because so few preflexion larvae were col- 
lected, we were unable to determine when this char- 
acter first appeared. A large, laterally projecting 





Figure 1 

Larval development of tripletail iLobotes surinamensis) from the north- 
ern Gulf of Mexico. (A) 2.2 mm, (B) 4.0 mm, (C) 6.3 mm, (D) 8.5 mm, (E) 
10.8 mm, (F) 13.7 mm. All measurements are standard length (SL). 



supraorbital ridge with a single spine was present 
above the eye of tripletail larvae by 4.0 mm. Both 
the supraorbital spine and ridge were resorbed by 
19.0 mm. Single, simple spines were present on the 



Ditty and Shaw: Larval development and distribution of Lobotes surinamensis 



37 



posttemporal and supraclei- 
thrum by 4.5 mm; a low, simple 
ridge occurred along the 
pterotic at about 5.0 mm (Fig. 
1). The posttemporal and 
supracleithral spines were par- 
tially covered by epithelium 
but both they and the pterotic 
ridge were visible on the larg- 
est specimen examined. 

Tripletail larvae developed 
two series of preopercular 
spines, one along the outer 
shelf and the other along the 
inner shelf. Both outer and in- 
ner shelves have dorsal and 
ventral limbs. Three spines oc- 
curred along the posterior mar- 
gin of the outer shelf of 2.2-2.4 
mm larvae, the longest at its 
angle (Fig. 1). A fourth spine 
was forming but was small at 
2.2 mm. Fifth and sixth spines 
were added by 6.0 mm; a sev- 
enth spine, by 7.0 mm. One to 
two small additional spines 
were added as larvae grew. By 
15.5 mm, three to five spines 
were visible along the dorsal 
margin of the outer preopercular 
shelf, one at the angle, and usu- 
ally three along the ventral 
margin; the anterior-most 
spine along the ventral margin 
was short and blunt (Fig. 1). All 
spines along the outer shelf 
were present in the largest 
specimen examined (i.e., 26.0 
mm). Along the inner preop- 
ercular shelf, one spine was 
present in 2.2-2.4 mm larvae 
and three to four spines by 5.0 
mm (Fig. 1). Spines along the 
inner shelf were short and 
blunt and covered by epithe- 
lium. A spine occurred along 
the posterior margin of the 
subopercle by 6.0-6.5 mm, near 
but dorsal to the angle spine of 
the outer preopercular shelf. The 
subopercular spine was resorbed 
by 20.0 mm. A small, flexible spine was present dor- 
sally on the opercle by 10.0 mm. This spine was diffi- 
cult to locate on unstained larvae because it was cov- 
ered by integument. 




A continuous median finfold extended posteriorly 
around the body from the nape to the anus of early 
larvae. Pelvic fins were precocious and elongate 
(usually >25% SL) and had a full complement of 



38 



Fishery Bulletin 92(1), 1994 










Figure 2 
Scanning electron micrograph of the supraoccipital and frontal bones of a 6.3-mm standard length 
tripletail, Lobotes surinamensis, from the northern Gulf of Mexico. Magnification: 280x. 



elements (I, 5) by 5.0 mm (Table 2). We were unable 
to determine when the pelvic-fin buds formed or 
flexion began because of a lack of specimens between 
2.4 and 4.0 mm. Development of the hypural com- 
plex (by 4.0 mm) coincided with that of the 
pterygiophores of the dorsal and anal fins. Anlagen 
of caudal-fin rays formed obliquely in the caudal 
finfold. The central-most caudal-fin rays formed first 
and development proceeded outward from mid-base. 
Notochord flexion was complete by 5.0 mm. The 



adult complement of 9+8 principal caudal rays were 
present by 7.0 mm, as were all procurrent caudal 
rays by 9.0-9.5 mm. All dorsal- and anal-fin ptery- 
giophores were present by 4.5-5.0 mm and both 
dorsal and anal spines developed before their rays 
in each fin. Dorsal and anal spines began to develop 
anteriorly and proceeded posteriorly to a full comple- 
ment of elements in each fin by 6.5 mm. Pectoral 
rays began to form at 5.5-6.0 mm and a full comple- 
ment (16 rays) was present by 7.0 mm (Table 2). A 



Fin ray counts of larval tripletail (Lobotes 
are in standard length (SL). 


Table 

surinamensis 


2 
i 


from 


th 


e northern 


Gulf of Mexico. 


Measurements 


Size 
(mm SL) n Dorsal 


Anal 








Pectoral 




Pelvic 


Caudal 


4.0 1 Finbase 
4.5 1 II, Anlagen 

5.0 1 VII, Anlagen 
6.3 1 XII. 15 

7.1 1 XII, 15 
10.2 1 XII, 15 


Finbase 
I, Anlagen 
I. Anlagen 

II, 12 
III, 12 

III. 11 








Anlagen 
Anlagen 

13 

16 

16 




3 

I, 5 
I, 5 
I, 5 
I. 5 
I, 5 


4 + 3 

6 + 6 

7 + 7 
3-9+8-2 
4-9+8-4 



Ditty and Shaw: Larval development and distribution of Lobotes surinamensis 



39 



cleared-and-stained 10.2-mm specimen had three 
supraneurals, six branchiostegal rays, four upper 
and four lower procurrent caudal rays, 11+13 ver- 
tebrae, 27 dorsal rays (XII, 15), and 14-15 anal rays 
(III, 11-12). Scales first appeared at 9.0-9.5 mm and 
marked the beginning of transition to the juvenile 
stage. 

Spatial and temporal distribution 

Overall, 75% of tripletail larvae in this study (Ap- 
pendix Table 2) occurred at surface water tempera- 
tures >28.8°C (median=28.9°C, range=27.6-31.0°C), 
at salinities >30.3 ppt (median = 31.3 ppt, 
range=22. 0-36.0 ppt), and at stations >70 m deep 
(median=205 m, range=l-2707 m) (Figs. 3 and 4). 
Larvae <5.0 mm were collected only at stations >110 
m deep. The two smallest larvae (2.2 and 2.4 mm) 
were taken on 28 July 1987 in a Tucker trawl 



sample at a station 110 m deep off Southwest Pass 
of the Mississippi River (Appendix Table 2). Other 
life stages were collected throughout the study area 
(Fig. 5, Appendix Table 2). 

Tripletail larvae were taken almost exclusively 
from July through September. Two specimens were 
collected in neuston nets outside this time period, 
one taken on 21 May 1983 (7.0 mm) and the other 
by GCRL on 9 October 1968 (10.2 mm) (Appendix 
Table 2). Salinity (36.5 ppt) and station depth (2,707 
m) for the May specimen were the maximums re- 
corded for a station where larvae were collected 
during this study (Appendix Table 2). 

Larval tripletail were collected primarily near the 
surface. Only 2 of 528 oblique bongo-net collections 
between July and September yielded tripletail lar- 
vae («=6, 6.0-9.0 mm, 18 September 1985). Of 537 
total surface net tows taken during this same time 
period, only 31 tows (5.8%) collected tripletail lar- 



67% 



N = 77 




28 29 30 31 
TEMPERATURE (C) 




22 26 27 28 29 30 31 32 33 34 35 36 
SALINITY (PPT) 



<5 5-50 51-180 >180 

DEPTH (M) 



Figure 3 

Summary of hydrographic data from positive catch stations for larval tripletail (Lobotes surinamensis) in 
the northern Gulf of Mexico. Percent catch is sum of larvae by interval divided by total number of tripletail 
larvae collected overall. Discrepancies in n (number of larvae), among parameters, are the result of missing 
hydrographic data. Depth is station depth. 



40 



Fishery Bulletin 92(1), 1994 













' 1 MS 


AL \ _, f 


l \ GA f 






LA A^, 






30- 


TX A^ 


-a, ^? ::|^C\V/A \ 






\ Yt*' ' ' '  


\ tovj&i/ ° xK* \ \ 






wu^'° ' * * * : ' 








ybr* ' i^-*~~* — *"" * ' 


! '. .*}?$.. o \ A . / \ 




LATITUDE 

to M 


V — " V 


 


 +  


vr^ . ' A. A .fo FL \ 






JULY-SEPTEMBER 


V / 40 M 
1B0 M 




2-4-| — 

95 


i i 
90 85 80 




LONGITUDE 




Figure 4 


Distribution of larval tripletail (Lobotes 


surinamensis) in the northern Gulf of Mexico. Plus ( + ) signs 


are stations sampled; open diamonds arc 


> positive catch stations. Data are for collections between July 


and September 1966-89. 





vae («=79) (Appendix Tables 1 and 2). Larvae from 
GCRL and Freeport-McMoRan collections also oc- 
curred primarily between July and September, but 
collection data are not available (e.g., total number 
of stations sampled and extent of sampling area). 



Discussion 

The developmental morphology of tripletail larvae 
from the Gulf generally agrees with limited infor- 
mation provided by Uchida et al. ( 1958) and Johnson 
(1984). Larval tripletail are characterized by Da 
vaulted, median supraoccipital crest with spines 
along the leading edge; 2) precocious, heavily pig- 
mented pelvic fins; and 3) large preopercular spines 
(Uchida et al., 1958; Johnson, 1984; this study). The 
supraoccipital crest is resorbed by 15.0-16.0 mm SL 
in Gulf specimens (this study) and by 17.5 mm TL 
(probably about 16.0 mm SL) off Japan (Uchida et 
al., 1958). Johnson (1984) described the surface of 
the frontal and supraoccipital bones of tripletail 
larvae as rugose. We would characterize these bones 



as having a "waffled" appearance rather than an 
elevated one, as implied by rugose (Fig. 2). Regard- 
less, this modification is found in relatively few 
other taxa (Johnson, 1984). Sequence of fin comple- 
tion in larval tripletail is Pg-Dj-Dg-A-Pj and is 
unlike the six patterns described by Johnson (1984). 
The third anal spine is the last dorsal- or anal-fin 
element to form. The dark band of pigment extend- 
ing backward from above and below the orbit in 
10.0-mm larvae is present at 8.3 mm SL (10.6 mm 
TL) off Japan (Uchida et al., 1958) and in juveniles 
and adults (Gudger, 1931; Breder, 1949). We did not 
find the nasal spine noted by Uchida et al. (1958). 
The 5.1-mm TL specimen listed as L. surinamensis 
by Konishi (1988) lacks a supraoccipital crest and 
precocious pelvics, and it has a small, multi-serrate 
supraorbital ridge rather than the single supraor- 
bital spine we found. Thus, we believe that Konishi's 
5.1-mm TL specimen is not L. surinamensis. 

Because tripletail have a cosmopolitan distribu- 
tion, their larvae may be confused with many taxa. 
Larval tripletail resemble larvae of caproids, some 
carangids, cepolids, drepaneids, ephippids, leiog- 



Ditty and Shaw. Larval development and distribution of Lobotes surinamensis 



41 



nathids, lethrinids, priacanthids, and Hap- 
alogenys sp. These taxa generally have a 
median supraoccipital crest, an elongate 
spine at the preopercular angle, and about 
24 myomeres (except cepolids which have 
28+ myomeres). In addition, cepolids are 
lightly to moderately pigmented and have 
fewer dorsal spines and more soft dorsal- 
fin rays than tripletail (Leis and Trnski, 
1989). Species of other families may have 
a median supraoccipital crest during devel- 
opment, but most have pelvic fins inserted 
anterior to pectorals. Also, larvae of other 
percoid families are usually not as deep- 
bodied and as heavily pigmented as triple- 
tail by early postflexion, and few possess 
an elongate preopercular spine and low 
myomere count. Of the aforementioned 
taxa, only caproids, carangids, ephippids, 
and priacanthids occur in the Gulf of 
Mexico. Larvae of the caproid genus 
Antigonia are most similar to tripletail but 
have a serrate frontal crest and lower jaw, 
a very long and serrate preopercular angle 
spine, and more than 39 dorsal and 26 anal 
elements (Tighe and Keene, 1984; Leis and 
Trnski, 1989). In carangids, the two ante- 
rior-most anal spines are separated from 
the third by a distinct gap and most spe- 
cies have a low, median supraoccipital crest 
with dorsal serrations; other carangids lack 
a supraoccipital crest entirely. Some car- 
angids also have a precocious dorsal fin 
with elongate anterior spines or rays, or a 
serrated preopercular angle spine. 
Drepaneids have pigment on the pectoral 
fins and multiple barbels along the lower 
jaw. Both larval drepaneids and ephippids 
are rotund and have pelvic fins inserted 
anterior to the pectorals. In addition, the 
Gulf ephippid Chaetodipterus faber has a 
supraoccipital crest with a single spine 
dorsally rather than the vaulted, serrate 
supraoccipital crest found in tripletail. Atlantic spa- 
defish also have more anal fin elements (tripletail: 
A. Ill, 11-12; Atlantic spadefish: A. Ill, 17-18). Lar- 
val leiognathids and lethrinids have a supraoccipital 
crest that originates above the anterior margin of 
the eye and both taxa are lightly pigmented (Leis 
and Trnski, 1989). Also, lethrinids have higher anal 
fin counts and serrations along the lower jaw (Leis 
and Rennis, 1983), and leiognathids have a distinc- 
tive pattern of pigment ventrally on the tail (Leis 
and Trnski, 1989). Priacanthids have serrate dorsal, 
anal, and pelvic spines and other serrate ridges and 




DEPTH ZONE 



LENGTH (SL) 
<5 LZZI 5-50 KX] 



51-180 rV^ 



Figure 5 

Distribution of larval tripletail iLobotes surinamensis) in the 
northern Gulf of Mexico with respect to station depth (m). 
Length classes are combined as follows: 2 mm = 1.0-2.9 mm, 
4 mm = 3.0-4.9 mm, 6 mm = 5.0-6.9 mm, etc. All measurements 
are standard length (SL). Numbers above bars are number of 
larvae in each length category. 



spines on the head that tripletail lack (Johnson, 
1984). Hapalogenys sp. larvae are extremely simi- 
lar to tripletail but Hapalogenys sp. apparently lack 
pigmented pelvic fins, have a serrate supraorbital 
ridge, have a lacrimal spine, and have pterotic 
spines or a ridge (Johnson, 1984). 

Collections of early larvae (this study) and gravid 
females (Baughman, 1941; Merriner and Foster, 
1974) suggest that tripletail spawn primarily dur- 
ing summer along both the U. S. Gulf and Atlantic 
coasts. In the Gulf, spawning begins in May, based 
on the collection of a 7.0-mm larva, and extends 
through September with peak spawning during July 



42 



Fishery Bulletin 92(1). 1994 



and August (Appendix Table 2). These findings sup- 
port Baughman's (1941) observation that eggs in 
gravid females are largest during July and August 
and small or absent thereafter. Larvae are collected 
primarily during August and September off Japan 
(Uchida et al., 1958). 

Tripletail spawn offshore. This hypothesis of off- 
shore spawning is supported by the collection of all 
larvae <5.0 mm at stations on the outer shelf and 
in oceanic waters. We found no published informa- 
tion on larval distribution as related to water tem- 
perature, salinity, or station depth of capture. 

Larval and juvenile tripletail are collected prima- 
rily in surface tows (Uchida et al., 1958; this study). 
Juveniles are often collected with drifting sea weeds, 
including Sargassum, and near floating objects 
(Baughman, 1943; Breder, 1949; Uchida et al., 1958; 
Dooley, 1972; Benson, 1982) as they float on their 
side (Gudger, 1931; Breder, 1949). The size at which 
tripletail become associated with drifting sea weeds 
is poorly known, but Uchida et al. (1958) collected 
juveniles between 10.0 and 20.0 mm TL in seaweeds. 

Adult tripletail occur primarily in gulf waters, but 
enter passes, inlets, and bays near river mouths 
(Gudger, 1931; Baughman, 1941). The degree to 
which tripletail utilize estuaries during their life 
history is unknown. Juveniles are apparently not 
uncommon (although they may be sporadic) in Gulf 
coast estuaries during the summer. We examined 
eight specimens (14.5-26.0 mm) collected at the 
surface in waters <3 m deep (Fig. 5). Modde and 
Ross (1981) collected 236 juvenile tripletail (size 
range not given) during 1976 in the surf zone of 
Horn Island, Mississippi, but only one during 1975 
and five during 1977. Juveniles also occur in shal- 
low waters (1-3 m) within the Barataria Bay sys- 
tem of Louisiana. 2 In contrast, juvenile and adult 
tripletail in the Indian River lagoon off the east 
coast of Florida occupy areas which average 30—31 
ppt. The lagoon typically goes hypersaline, to 40 ppt, 
during spring when most tripletails first appear in 
the lagoon. Tripletail have not been observed or 
captured in extensive collections of oligohaline ar- 
eas of the St. Lucie River and Sebastian Creek. 3 

Adult tripletail generally occur along the Gulf 
coast from April through early October (Baughman, 
1941) and are caught in great numbers in Mobile 
Bay, Alabama, and along the Mississippi coast dur- 
ing summer (Baughman, 1941). Greatest concentra- 
tions of adults are found along the northern Gulf 
from St. Marks, Florida, to the St. Bernard River, 



2 Leroy Kennair, Freeport-McMoRan, Inc., New Orleans, LA., 
pers. commun. 1993. 

3 R. Grant Gilmore, Harbor Branch Oceanographic Institution, 
Fort Pierce, FL, pers. commun. 1993. 



Texas (Baughman, 1941). Seasonality of adults sug- 
gests that tripletail migrate south during fall and 
winter and return in spring (Merriner and Foster, 
1974). Tripletail congregate around sea buoys, bea- 
cons, pilings, and other objects (Gudger, 1931) but 
have been collected in a wide variety of habitats 
including rocky and coral reef areas in deeper wa- 
ter (Baughman, 1941). 



Acknowledgments 

This study was supported by the Marine Fisheries 
Initiative (MARFIN) Program (contract numbers: 
NA90AA-H-MF111 and NA90AA-H-MF727). We 
thank SEAMAP and the Gulf States Marine Fish- 
eries Commission for providing specimens and en- 
vironmental data, and the Louisiana Board of Re- 
gents and the LaSER (Louisiana Stimulus for Ex- 
cellence in Research, contract number 86-LUM(D- 
083/13) program for support during July 1987, April 
1988, and October 1990 ichthyoplankton cruises. We 
also thank those who loaned us specimens or pro- 
vided data: Churchill Grimes, NMFS, Southeast 
Fisheries Center, Panama City, FL; Wayne Forman 
and Leroy Kennair, Freeport-McMoRan, New Or- 
leans, LA.; Stuart Poss, Gulf Coast Research Lab, 
Ocean Springs, MS. Thanks also to Cathy Grouchy 
for illustrating larvae, to Joseph S. Cope for computer 
assistance, and to Laura Younger for providing scan- 
ning electromicrographs of the frontal and occipital 
bones. Finally, we thank the reviewers for their com- 
ments in substantially improving the mansucript. 

Literature cited 

Baughman, J. L. 

1941. On the occurrence in the Gulf coast waters 
of the United States of the triple tail, Lobotes 
surinamensis, with notes on its natural 
history. Am. Nat. 75:569-579. 

1943. Additional notes on the occurrence and natu- 
ral history of the triple tail, Lobotes 
surinamensis. Am. Midi. Nat. 29(2):365-370. 
Benson, N. G. (ed.). 

1982. Life history requirements of selected finfish 
and shellfish in Mississippi Sound and adjacent 
areas. U.S. Fish and Wildl. Serv., Office Biol. 
Serv., Washington, D.C., FWS/OBS-81/51, 97 p. 
Breder, C. M., Jr. 

1949. On the behavior of young Lobotes surinam- 
ensis. Copeia 1949(4):237-242. 
Dooley, J. K. 

1972. Fishes associated with the pelagic sargassum 
complex, with a discussion of the sargassum 
community. Contrib. Mar. Sci., Univ. Texas 16:1-32. 



Ditty and Shaw: Larval development and distribution of Lobotes surinamensis 



43 



Fischer, W., (ed.). 

1978. FAO species identification sheets for fishery 
purposes. Western Central Atlantic (Fishing Area 
31), Vol. 3. FAO, Rome. 
Gilhen, J., and D. E. McAllister. 

1985. The tripletail, Lobotes surinamensis, new to 
the fish fauna of the Atlantic coast of Nova Scotia 
and Canada. Can. Field-Natur. 99(1):116-118. 
Gudger, E. W. 

1931. The tripletail, Lobotes surinamensis, its 
names, occurrence on our coasts and its natural 
history. Am. Nat. 65: 49-69. 
Hardy, J. D., Jr. 

1978. Development of fishes of the Mid-Atlantic 
Bight: an atlas of egg, larval and juvenile stages. 
Vol. Ill: Aphredoderidae through Rachycentridae. 
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78/12. 
Hoese, H. D., and R. H. Moore. 

1977. Fishes of the Gulf of Mexico: Texas, Louisi- 
ana, and adjacent waters. Texas A&M Univ. 
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Hubbs, C. L., and K. F. Lagler. 

1958. The fishes of the Great Lakes region. Univ. 
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Johnson, G. D. 

1984. Percoidei: development and relationships. 
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1988. Lobotidae. In M. Okiyama (ed.), An atlas of 
the early stage fishes in Japan. Tokai Univ. 
Press, Tokyo, 1,154 p. (In Japanese.) 

Leis, J. M., and D. S. Rennis. 

1983. The larvae of Indo-Pacific coral reef 
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Leis, J. M., and T. Trnski. 

1989. The larvae of Indo-Pacific shorefishes. Univ. 
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Merriner, J. V., and W. A. Foster. 

1974. Life history aspects of the tripletail, Lobotes 

surinamensis (Chordata-Pisces-Lobotidae), in 

North Carolina waters. J. Elisha Mitchell Sci. 

Soc. 90<4):121-124. 
Modde, T., and S. T. Ross. 

1981. Seasonality of fishes occupying a surf zone 

habitat in the northern Gulf of Mexico. Fish. 

Bull. 78(41:911-922. 
Nelson, J. S. 

1984. Fishes of the World. 1984, 2nd ed. John 
Wiley & Sons, NY, 523 p. 



Richardson, S. L., and W. A. Laroche. 

1979. Development and occurrence of larvae and 
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77(11:1-46. 

Sanders, N., Jr., T. Van Devender, and P. A. 
Thompson. 

1990. SEAMAP environmental and biological atlas 
of the Gulf of Mexico, 1986. Gulf States Marine 
Fish. Comm., Ocean Springs, MS, No. 20, 328 p. 
SAS Institute, Inc. 

1985. SAS user's guide: statistics, 1985 ed. SAS 
Institute, Cary, NC, 584 p. 
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100 p. 
Stuntz, W. E., C. E. Bryan, K. Savastano, R. S. 
Waller, and P. A. Thompson. 

1985. SEAMAP environmental and biologcial atlas 
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Fish. Comm., Ocean Springs, MS, No. 12, 145 p. 
Thompson, P. A., and N. Bane. 

1986a. SEAMAP environmental and biological at- 
las of the Gulf of Mexico, 1983. Gulf States Marine 
Fish. Comm., Ocean Springs, MS, No. 13, 179 p. 
1986b. SEAMAP environmental and biological at- 
las of the Gulf of Mexico, 1984. Gulf States Marine 
Fish. Comm., Ocean Springs, MS, No. 15, 171 p. 
Thompson, P. A., T. Van Devender, and N. J. 
Sanders, Jr. 

1988. SEAMAP environmental and biological atlas 
of the Gulf of Mexico, 1985. Gulf States Marine 
Fish. Comm., Ocean Springs, MS, No. 17, 338 p. 
Tighe, K. A., and M. J. Keene. 

1984. Zeiformes: development and relationships, p. 
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fishes. Am. Soc. Ichthy. Herp., Spec. Publ. No. 1. 
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Shojima, T. Senta, M. Tahuka, and Y. Dotsu. 
1958. Studies on the eggs, larvae, and juveniles of 
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1976. A multiple opening/closing net and environ- 
mental sensing system for sampling zoo- 
plankton. J. Mar. Res. 34(3):313-326. 



44 



Fishery Bulletin 92(1), 1994 



Appendix Table 1 

Summary of total number of bongo-net/neuston-net stations examined for tripletail larvae (Loboten surina- 
mensis) in the Gulf of Mexico. Acronyms are as follows: SEAMAP = Southeast Area Monitoring and Assess- 
ment Program; NMFS = National Marine Fisheries Service, Panama City, Florida; LSU = Louisiana State 
University. NS means no samples. 





MAR 


APR 


MAY 


JUN 


JUL 


AUG 


SEP 


OCT 


NOV 


DEC 


SEAMAP 






















1982 


77 J /0 2 


69/68 


71/73 


102/100 


26/24 


NS 


NS 


3/8 


29/3 


NS 


1983 


15/13 


27/27 


84/84 


55/45 


44/42 


NS 


NS 


39/26 


NS 


24/23 


1984 


23/0 


44/0 


46/0 


55/54 


20/26 


155/162 


NS 


24/0 


6/0 


36/36 


1985 


29/0 


NS 


NS 


85/0 


39/0 


69/0 


20/0 


4/0 


2/0 


24/0 


1986 


NS 


24/0 


90/0 


57/0 


10/0 


NS 


145/0 


43/0 


73/0 


24/0 


TOTAL 


144/13 


164/95 


291/157 


354/199 


139/92 


224/162 


165/0 


113/34 


110/3 


108/59 


NMFS 2 






















1986 














46 








1987 














68 








1988 






55 






71 








36 


1989 














35 








LSU 






















1987 3 










63 












1988'' 




45 


















1990' 
















17 







1 60-cm bongo net, 0.333-mm mesh, oblique-tow from depth. 

- 1 x 2 m neuston net, 0.947-mm mesh, 10 mill, surface-tow, unmetered. 

3 lm 2 Tucker trawl, 0.947-mm mesh, 3 min. surface-tow each net, nine net collections per station, 

4 lm 2 MOCNESS, nine nets of 0.333-mm mesh, 3-min. surface-tow each net, five total stations. 



ieven total stations. 



Ditty and Shaw: Larval development and distribution of Lobotes surinamensis 



45 













Appendix 


Table 2 










Positive catch station data for tripletail (Lobotes surinamensis) larvae from noi 


•thern Gulf 


of Mexi 


co waters. 


Gear codes are: B=bongo 


net, N= 


:Neuston net, T=Tucker trawl, U= 


unknown. 








Station 




Date 


Gear 


Latitude 


Longitude 


Station 
depth (m) 


*C 


PPT 


n 


Length 
(mm SL) 


SEAMAP 2 






















1420 




5-21-83 


N 


26*30 


88*00 


2707 


27.6 


36.5 




7.0 


3235 




7-17-84 


N 


28*15 


90*30 


70 


29.4 


25.9 




8.8 


3238 




7-17-84 


N 


28*30 


90*30 


38 


29.4 


25.8 




7.0 


3259 




7-22-84 


N 


29*00 


87*00 


1251 


28.9 


32.8 




12.3 


2511 




8-03-84 


N 


29*00 


88*15 


1013 


27.6 


32.4 




7.1-18.5 


2523 




8-03-84 


N 


29*15 


88*30 


82 


28.0 


26.0 




7.9 


2548 




8-05-84 


N 


29*00 


88*45 


249 


27.6 


28.7 




16.8 


4231 




8-05-84 


N 


29*28 


87*00 


486 


28.9 


30.3 


16 


6.8-13.0 


4201 




8-01-85 


N 


28*00 


84*52 


205 


29.6 


30.8 


10 


10.3-15.9 


4204 




8-01-85 


N 


28*00 


85*02 


265 


28.8 


32.6 


5 


9.0-16.5 


4210 




8-02-85 


N 


28*21 


86*00 


457 


28.8 


32.1 


4 


6.8-10.0 


4216 




8-03-85 


N 


28*53 


86*16 


335 


29.1 


31.3 


2 


9.0 


4219 




8-03-85 


N 


28*40 


86*30 


457 


28.9 


33.6 


1 


9.9 


4320 




8-24-85 


N 


27*38 


94*00 


455 


28.0 


— 


1 


4.0 


4326 




8-25-85 


N 


27*40 


93*00 


265 


29.7 


36.0 


1 


7.8 


4332 




8-26-85 


N 


27*46 


92*00 


457 


30.0 


35.4 


1 


9.1 


4484 




9-18-85 


B 


29*07 


89*44 


20 


27.8 


29.5 


2 


6.0 


4490 




9-18-85 


B 


28*37 


90*26 


27 


27.8 


32.6 


4 


6.4-9.0 


LSU 2 






















137 




7-28-87 


T 


28*42 


89*29 


110 


29.5 


22.0 


2 


2.2-2.4 


145 




7-28-87 


T 


28*35 


89*22 


182 


29.6 


32.5 


2 


5.0 


163 




7-30-87 


T 


28 2 t 


89*14 


640 


31.0 


33.6 


2 


6.3 


168 




7-30-87 


T 


28*24 


89*14 


640 


31.0 


33.6 


2 


6.3 


175 




7-30-87 


T 


28*27 


89*16 


410 


29.8 


35.3 


2 


— 


177 




7-30-87 


T 


28*27 


89*16 


410 


29.8 


35.3 


2 


4.5 


GCRL 5 






















Station 6 




7-13-67 


N 


29*15 


88*11 


182 


— 


— 


1 


12.5 


T-108-7- 


-02 


8-25-71 


U 


29*10 


88*45 


55 


— 


— 


1 


8.7 


T-108-3- 


114 


8-27-71 


U 


29*50 


88*05 


'J 7 


— 


— 


1 


11.7 


T-208-4- 


■01 


8-23-72 


I' 


29*40 


88*14 


38 


— 


— 


2 


7.2-7.3 


T- 109-6- 


■02 


9-21-71 


V 


29*20 


88*21 


55 


— 


— 


1 


15.4 


T- 109-5- 


03 


9-22-71 


u 


29*30 


88*24 


46 


— 


— 


1 


8.6 


T-209-2- 


ill 


9-15-72 


u 


30*00 


88*14 


27 


— 


— 


2 


7.7-10.7 


Station 5 




10-09-68 


N 


29*19 


88*14 


73 


— 


— 


1 


10.2 


Freeport-McMoRan'' 


















2 




8-24-71 


u 


29*16 


89*57 


1 


— 


— 


1 


14.5 


3 




8-10-71 


u 


29*22 


89*48 


3 


— 


— 


2 


16.5-18.5 


4 




8-23-73 


u 


29*16 


89*57 


1 


— 


— 


1 


26.0 


5 




8-15-66 


u 


29*16 


89 57 


3 


— 


— 


4 


11.5-21.5 


NMFS 5 






















53 




8-28-88 


N 


29*00 


88*53 


149 


30.3 


27.5 


1 


10.8 


58 




8-29-88 


N 


29*07 


88*49 


8 J 


29.5 


29.0 


1 


13.7 


5 




9-03-87 


N 


29*12 


88 43 


71 


29.3 


32.8 


1 


23.0 


23 




9-25-86 


N 


28*50 


89*05 


195 


29.4 


34.0 


2 


7.3-13.2 


32 




9-06-89 


N 


28*49 


89*16 


410 


29.8 


35.3 


1 


18.7 


42 




9-26-86 


N 


29*09 


88 40 


77 


29.3 


— 


1 


8.6 


43 




9-05-87 


N 


28*46 


89*29 


104 


29.2 


32.1 


1 


7.5 


; Southeast Area Monitoring and Assessment Program. 

2 Louisiana State University, Coastal Fisheries Institute, Baton Rouge. 

3 Gulf Coast Research Lab. Ocean Springs, Mississippi. 

4 Freeport-McMoRan. Inc., New Orleans, Louisiana. 

5 National Marine Fisheries Service, Panama City Lab, Florida. 



Abstract. — Otoliths were 
used to determine the age and 
growth of the coral trout Plectro- 
pomus leopardus from Lizard Is- 
land area, Northern Great Barrier 
Reef, Australia. An alternating 
pattern of opaque (annulus) and 
translucent zones was visible in 
whole and sectioned otoliths. How- 
ever, compared to sectioned 
otoliths, whole readings tended to 
underestimate age of older fish. 
Otoliths of mark-recaptured fishes 
treated with tetracycline showed 
that one annulus is formed per 
year during the winter and spring. 
The oldest individual examined 
was 14 years of age. Schnute's 
growth formula was used to deter- 
mine the best model to describe 
the growth of the coral trout. The 
von Bertalanffy model for fork 
length (FL) fitted the data well 
and the resulting model was 
L t = 52.2(1 -e -0.354U + 0.766)). 
Line-fishing usually does not cap- 
ture fishes smaller than 25 cm FL, 
thereby excluding most 0+ and 1+ 
year old fish and probably the 
slower growing 2+ year old fish. 
These first three years of life rep- 
resent the period of fastest growth, 
so, if the growth curve is fitted 
only to the line fishing data, the 
growth rate of the population is 
underestimated. Multiple regres- 
sion was used to predict age from 
otolith weight and fish length and 
weight. Otolith weight was the 
best predictor of age in the linear 
model and explained as much 
variation in age as fish size in the 
von Bertalanffy model. 



Age validation and estimation of 
growth rate of the coral trout, 
Plectropomus leopardus, 
(Lacepede 1802) from 
Lizard Island, Northern 
Great Barrier Reef 



Beatrice Padovani Ferreira* 
Garry R. Russ 

Department of Marine Biology, James Cook University of North Queensland 
Townsville Q481 1, Australia 

*Present address: CEPENE-IBAMA. R Samuel Hardman s/n° Tamandare. 
Pernambuco. Cep. 55578-000. Brazil 



Manuscript accepted 8 September 1993 
Fishery Bulletin 92:46-57 (1994) 



The coral trouts of the genus Plec- 
tropomus Oken are members of the 
serranid subfamily Epinephelinae, 
commonly known as groupers. 
These fishes occur in shallow tropi- 
cal and subtropical seas of the 
Indo-Pacific region (Randall and 
Hoese, 1986) where they usually 
are at the top of food chains and 
thus play a major role in the struc- 
ture of coral reef communities 
(Randall, 1987). 

Groupers typically represent an 
important fishery resource 
throughout the tropical and sub- 
tropical regions of the world 
(Ralston, 1987). On the Great Bar- 
rier Reef, the common coral trout 
Plectropomus leopardus (Lacepede 
1802) is the most abundant species 
of the genus (Randall and Hoese, 
1986) and usually the primary tar- 
get of recreational and commercial 
fishermen. The Queensland com- 
mercial line-fishing fleet takes a 
total annual catch of about 4,000 
metric tons (t) of reef and pelagic 
species. The coral trout composes 
the largest single component of this 
catch (over 30%) with around 1200 
t caught annually (Trainor, 1991). 
The recreational sector of this fish- 
ery is estimated to catch two to 
three times the commercial catch of 
reef fish (Craik, 1989 1 ). 



Worldwide studies on age and 
growth of Epinephelinae indicate 
that they are long lived, slow grow- 
ing, and have relatively low rates of 
natural mortality (Manooch, 1987). 
Fishes with these characteristics are 
susceptible to overfishing. Only by 
obtaining validated estimates of 
growth is it possible to determine 
population dynamics, estimate po- 
tential yield, monitor the responses 
of populations to fishing pressure, 
and properly manage the fishery. 

Some information on age, 
growth, and longevity is available 
for the common coral trout. On the 
Great Barrier Reef, Goeden (1978) 
estimated the growth rate of this 
species at Heron Island from 
length-frequency data. Mcpherson 
et al. (1988), determined age and 
growth of the common coral trout 
in the Cairns region by counts of 
annuli in whole otoliths. Loubens 
(1980) estimated age and growth 
for P. leopardus from New Cale- 
donia from counts of annuli in bro- 
ken and burnt otoliths. The period- 
icity of formation of annual rings in 
the latter two studies was verified 
through observation of marginal 



1 Craik, G. J. S. 1989. Management of rec- 
reational fishing in the Great Barrier Reef 
Marine Park Tech. Memo. GBRMPA-TM- 
23, 35p. 



46 



Ferreira and Russ: Age-validation and growth rate of Plectropomus leopardus 



47 



increments in otoliths. Direct validation of age has 
not yet been attempted for P. leopardus. 

Fish population models usually require a general 
description of the growth process by means of an ap- 
propriate mathematical function. The von 
Bertalanffy (1938) growth model is the most stud- 
ied and the most frequently used, since its applica- 
tion by Beverton and Holt (1957) to the yield-per- 
recruit problem (Kimura, 1980; Gallucci and Quinn, 
1979). Many alternative growth curves have been 
proposed (see Moreau, 1987) as well as the use of 
polynomial functions (Chen et al., 1992). In this 
work, Schnute's (1981) formula was used to find the 
model that best described the growth of P. leopardus. 

For several species of fishes, otolith growth has 
been found to continue with age, independent offish 
size (Boehlert, 1985; Casselman, 1990; Beckman et 
al., 1991). Boehlert (1985) suggested the use of 
otolith weight as a non-subjective, cost-effective 
methodology for age determination that would de- 
crease variability among age estimates. 

The aims of this study were to obtain direct vali- 
dation of age-at-length information and to find the 
model that best described the growth of the common 
coral trout from Lizard Island, Northern Great Bar- 
rier Reef, Australia. In addition, the relationship 
between otolith weight, body size, and age of the 
coral trout was studied to understand the mode of 
growth of the otolith and to assess the usefulness 
of otolith dimensions in predicting age. 

Materials and methods 

Coral trout (t?=310) were sampled in the Lizard Is- 
land area (lat. 14° 40' S, long. 154° 28' E) from March 
1990 to February 1992. Fishes were caught by rec- 
reational and commercial fishermen using hook and 
line (77 = 184) and by recreational spearfishermen 
(n=94). Individuals smaller than 20-cm total length 
are usually not vulnerable to line fishing, so they 
were caught around Lizard Island by scuba divers 
using fence nets (77=32). Fork length (FL, cm), stan- 
dard length (SL, cm) and total weight (TW, g) were 
measured for each fish. FL is defined as the length 
from the front of the snout to the caudal fork, and 
SL is defined as the length from the front of the 
upper lip to the posterior end of the vertebral col- 
umn. A simple linear regression of the form FL= a 
+ 6*SL was used to describe the relationship be- 
tween FL and SL. To describe the relationship be- 
tween FL and TW the variables were logarithmically 
transformed and the linearized version of the power 
function TW(g)= a*FL(cm)b was fitted to the data. 
In the coral trout, the sagittae are the largest of 
the three pairs of otoliths and were used for read- 
ings. Sagittae were removed, cleaned, weighed, and 



stored dry. Left and right sagittae, when intact, were 
weighed to the nearest milligram. Otoliths were 
prepared and read as described by Ferreira and 
Russ (1992). To increase contrast between bands, 
whole otoliths were burned lightly on a hot plate at 
180°C (Christensen, 1964). Both right and left 
sagitta were read whole under reflected light with 
a dissecting microscope at 16x magnification. The 
otoliths, with the concave side up, were placed in a 
black container filled with immersion oil. Subse- 
quently, the left sagittae was prepared for reading 
by embedding in epoxy resin (Spurr, 1969) and sec- 
tioning transversely through the core with a Buehler 
Isomet low-speed saw. Sections were mounted on 
glass slides with Crystal Bond 509 adhesive, ground 
on 600- and 1200-grade sand paper, polished with 
0.3— u alumina micropolish and then examined un- 
der a dissecting microscope at 40x magnification 
with reflected light and a black background (Fig. 1). 
Annuli were counted from the nucleus to the proxi- 
mal surface of the sagitta along the ventral margin 
of the sulcus acousticus. 

Terminology for otolith readings followed defini- 
tions of Wilson et al. (1987). Two experienced read- 
ers independently counted opaque zones (annuli) in 
each whole and sectioned otolith of a random 
subsample (77 = 136) to assess the precision and ac- 
curacy of countings obtained by the two methods. 
The precision of age estimates was calculated with 
the Index of Average Percent Error (IAPE), (Bea- 
mish and Fournier, 1981). Results obtained from 
whole and sectioned otoliths were compared by plot- 
ting the difference between readings obtained from 
whole and sectioned otoliths (Section Age- Whole 
age) against Section Age. The results of this com- 
parison indicated that whole otolith readings tended 
to be lower than readings from sectioned otoliths 
when more than six rings occurred in the otolith. 
Therefore, remaining otoliths were read whole first 
and, if the number of rings was higher than six or 
the whole otolith was considered unreadable, the 
otolith was sectioned and counts were repeated. The 
results were accepted and used in the analysis when 
the counts of the two readers agreed. If the counts 
differed, the readings were repeated once and if the 
counts still differed, the fish was excluded from the 
analysis. 

Ages were assigned based on annulus counts and 
knowledge of spawning season. The periodicity of 
annulus formation was determined with the use of 
tetracycline labelling. From August 1990 to Febru- 
ary 1992, 80 fishes were caught in a trapping pro- 
gram at Lizard Island fringing reeflDavis, 1992 2 ), 

2 C. Davies. 1992. James Cook University, Townsville, Q4811, 
Australia, unpubl. data. 



48 



Fishery Bulletin 92(1), 1994 





Figure 1 

Whole (A) and sectioned (B) otolith of an 11-year-old coral trout, P. Icopardus, under 
reflected light with a black background showing alternating pattern of translucent and 
opaque bands; a = anterior, p = posterior, d = dorsal, v = ventral, di = distal, pr = proxi- 
mal, ds = dorsal sulcus, vs = ventral sulcus. Scale bar = 1 mm 



tagged with T-bar anchor tags and injected with 
tetracycline hydrochloride before being released. The 
fish were injected in the coelomic cavity under the 
pelvic fin with a dosage of 50 mg of tetracycline per 
kg offish (McFarlane and Beamish, 1987), in a con- 
centration of 50 mg per mL of sterile saline solution. 



Five fish were recaptured after periods of at least 
one year at large. Two of those fish were reinjected 
at the time of recapture and kept in captivity for 
periods of three to four months. 

To determine the time of formation of the first 
annulus, five young of the year were captured with 



Ferreira and Russ: Age-validation and growth rate of Plectropomus leopardus 



49 



fence nets. Three of these fishes were injected with 
tetracycline at the time of capture, and all five fish 
were kept in captivity for periods of 3 to 17 months. 
The otoliths of the fishes treated with tetracycline 
were removed, sectioned, and observed under fluo- 
rescent light. To determine time of formation of the 
translucent and opaque zones, the distances be- 
tween events for which time of occurrence was 
known (i.e., between two tetracycline bands or be- 
tween a tetracycline band and the margin of the 
otolith) were measured on otolith sections and plot- 
ted against the corresponding time interval. The 
relative positions of the translucent and opaque 
zones to these marks were then measured and plot- 
ted on the same scale. While this method does not 
provide real distances, it standardizes the measure- 
ments allowing for comparison between fish of dif- 
ferent ages. 

The relation between otolith weight, fish size 
(length and weight), and age was analyzed. Otolith 
weight was plotted against FL for each age class 
separately. A multiple linear regression model was 
fitted in a step-wise manner to predict age from 
otolith weight and fish size and to predict otolith 
weight from age and fish size. The inclusion level 
for the independent variables was set at P=0.10. The 
assumptions of normality and homoscedasticity 
were tested by plotting the residuals from the re- 
gression models. 

The growth models were fitted to the data and 
their coefficients and standard errors estimated by 
means of standard non-linear optimization methods 
(Wilkinson, 1989). As the plot of the length-at-age 
data indicated, some form of asymptotic growth, 
Schnute's (1981) reformulation of the von Bert- 
alanffy growth equation for length in which a*0 was 
fitted to the data: 



,-aU-t\) 



L,=y\ h +(y2 b -yl b ) 



where L f is length at age; tl and t2 are ages fixed 
as 1 and 14 respectively ; yl and y2 are estimated 
sizes at these ages; and a and b are the parameters 
which indicate if the appropriate growth curve lies 
closer to a three or two parameter sub-model. By 
limiting parameter values, the data were used di- 
rectly in selecting the appropriate sub-model, 
namely the generalized von Bertalanffy, Richards, 
Gompertz, Logistic, or Linear growth models. Sub- 
sequently, the original von Bertalanffy (1938) 



-KU -to) 



To evaluate the effects of gear selectivity (and 
consequently varying size and age composition) on 
the estimates of growth parameters, the von 
Bertalanffy growth equation was fitted first to data 
collected by line and spear fishing only and then to 
the same data combined with the fence-net sample 
composed of younger fish. 



Results 

Otolith reading 

In the coral trout, the sagittae presented a pattern 
of alternating translucent zones and wide opaque 
zones (annuli) with no sharp contrast between zones 
(Fig. 1). The first two annuli were notably wider and 
less well defined than the subsequent ones in sec- 
tioned otoliths. Whole sagittae were used to confirm 
the presence of these first annuli. 

In whole otoliths, annuli were clearly distinguish- 
able and easy to count along the dorsal side of the 
otolith, where up to 12 rings were counted in some 
otoliths. However, readings from whole otoliths 
tended to be lower than readings from sectioned 
otoliths when more than six rings were present, and 
this tendency increased with the mean number of 
rings, particularly after ten rings. (Fig. 2 ). Tetra- 
cycline-labelled otoliths validated the periodicity of 
annuli in sectioned otoliths, indicating that whole 
otolith readings tend to underestimate age of > 10- 
year-old fishes. A comparison between results of 



)was 



growth equation for length L ( = L^d-e 
fitted to the data. V is length at age; L x is the as- 
ymptotic length, K is the growth coefficient, t is age, 
and t o is the hypothetical age at which length is zero. 















£, 4 

< 


,1 




5 3 
o 

c 

5 2 






i 

<u 1 


,1 






Section Ag 

) — o 


?, . in' i 








2 4 6 8 10121416 


Section Age 


Figure 2 


Average difference between counts obtained from 


sectioned and whole otoliths (Section Age-Whole 


Age) of coral trout, P. Leopardus, plotted against 
Section Age. Error bars show standard error. 



50 



Fishery Bulletin 92(1). 1994 



countings performed on whole and sectioned otoliths 
showed that, in the sub-sample analysed, the Index 
Average Percent Error (IAPE) of Beamish and 
Fournier (1981), was lower for counts performed on 
whole (6.7%) than for counts performed on sectioned 
otoliths (12.1%). For the total sample, where read- 
ings from whole and sectioned otoliths were inte- 
grated, the IAPE was reduced to 5.1%. 

Otolith growth 

Otolith weight was directly related to age and an 
exponential function offish length (Fig. 3). Within 
each age class, otolith weight was positively corre- 
lated with fork length for most classes (Table 1), 
indicating a tendency for larger fish to have larger 



100 




10 20 30 40 50 60 70 

Fork Length (cm) 



E 



5 



I0U 




Figure 3 

Relation between otolith weight and Fork Length 
(FL) and otolith weight and age for coral trout, 
P. leopardus. 



otoliths than smaller fish of the same age. The 
weight of the otolith was a good predictor of age and 
accounted alone for 89%> of the variability in age of 
the coral trout (r^O.889, P<0.0001), with fork length 
accounting for 1.5% (partial r 2 = 0.015). Otolith 
weight was a function of age and fish size, as indi- 
cated by the results of the multiple regression fit- 
ting. The interaction between age and fork length 
alone accounted for 89% of the variability (r-^0.892, 
P<0.0001) 



Validation of annulus formation 

All fishes treated with tetracycline displayed clear 
fluorescent marks in their otoliths (Fig. 4). The re- 
sults obtained for recaptured and captive fish, rang- 
ing in age from one to eight years, showed that 
annuli are formed once per year (Fig. 5). The first 
annulus is formed in the otoliths of the juvenile coral 
trout during their first year of life (Fig. 6). The rela- 
tive positions of the fluorescent bands, in relation 
to the otolith margin and the translucent and 
opaque zones (annuli), indicated that the formation 
of the annulus occurred mainly during winter and 
early spring (Figs. 5 and 6). 

Growth model 

The samples obtained from line-fishing and spear- 
fishing were selective towards individuals larger than 
25 cm FL. Consequently, the 0+ age class was not rep- 
resented in this sample and the age-1 year class was 
represented by only four individuals (Fig. 7). The 
sample collected with fence nets, composed of indi- 
viduals from the smaller size classes, consisted to- 
tally of individuals of the 0+ and 1+ year classes 
(Fig. 7). Table 2 shows the results obtained when 
fitting the growth model to the data including all 
age classes and to the data including only age >2+. 







Table 1 






Correlation between otolith weight (mg) and fork 


length (cm) 


for each age class of the 


coral trout 


P. leopardus. 








Age r- 


P< 


df 


Age 


r 2 


P< df 


0.826 


0.0001 


18 


8 


0.481 


0.0001 19 


1 0.972 


0.0001 


10 


9 


0.405 


0.0001 12 


2 0.829 


0.0001 


27 


10 


0.120 


no sig. 8 


3 0.747 


0.0001 


19 


11 


0.937 


0.0001 7 


4 0.652 


0.0001 


18 


12 


0.526 


no sig. 3 


5 0.650 


0.0001 


30 


13 


0.993 


0.05 2 


6 0.489 


0.0001 


43 


14 


0.049 


no sig. 2 


7 0.514 


0.0001 


30 









Ferreira and Russ: Age-validation and growth rate of Plectropomus leopardus 




Figure 4 

Sectioned otolith of a recaptured individual coral trout, P. leopardus In" 0057) 
rescent band. Scale Bar = 0.25 mm 



showing fluo- 



When fitting Schnute's model to both sets of data, 
the value of the parameter b was very close to 1. In 
the boundary where 6 = 1, the curve was reduced 
to a three parameter model that corresponds to the 
von Bertalanffy curve for length (Schnute, 1981). 
The resulting growth model for all age classes, in 
the form of a von Bertalanffy model, was 

L, =52.2 (1-e- 0.354(^ + 0.766)) r = 0.895 (Fig. 8). 



Table 2 

Von Bertalanffy growth parameters V.B. and re- 
spective standard errors (SE), correlation coeffi- 
cients (r 2 ) and degrees of freedom (df) for the 
growth curve fitted to all data and to the data for 
coral trout, P. Leopardus, >2 year old only. 



(SE) 



K 

(SE) 



(SE) 



df 



V.B. 
all ages 

V.B. 
age >2+ 



52.20 
(0.768) 



0.354 
(0.0241 



61.29 0.132 
(3.483) (0.030) 



-0.766 
(0.097) 



-4.660 
(1.024) 



0.895 310 



622 272 



The results obtained when fitting the growth curve 
to all data and to the data for fish >2+ years old only 
were quite different (Table 2). From age-2 onwards, 
the growth rate is much slower than the one esti- 
mated by using all age classes, as indicated by the 
growth coefficient K. Consequently, the estimated L m 
is larger and the estimated t o is a very large, nega- 
tive value. The resulting growth model was 

L, =61.29 (l-e-0.132(f + 4.66)) r = 0.622 (Fig. 9). 

No systematic trend in the residuals was observed 
(normality test P>0.1) (Figs. 8 and 9). 

The relation between fork length (FL) and the 
standard length (SL) was 

SL = -0.308 + 0.852 * FL, r 2 = 0.994, 

and the relationship between FL and Total Weight 
(TW) was 



TW = 0.0079 *FL 



3 157 



0.967. 



Discussion 

While some comparisons between readings of whole 
and sectioned otoliths have indicated good agree- 



52 



Fishery Bulletin 92(1), 1994 



WSSAWSSAW 



Tag No AUG 90 



0085 r 




|H FEB 92 


NOV 90 


age = 5 | 




H NOV 91 




NOV 90 


NOV 91 


3862 1 
ago = 7 | 




| FEB 92 




MAR 90 


MAR 91 


WW  1 

age I 



 Fluorescent 
| Translucent 
^ Opaque 



YY Winter § Summer 

^ Spnng /\ Autumn 



Figure 5 

Diagrammatic representation of otoliths of mark- 
released-recaptured coral trout, P. leopardus, 
treated with tetracycline showing relative positions 
of the fluorescent bands, otolith margin, translucent 
and opaque zones. Bars represent only the distal 
part of the radius of the otolith section, measured 
from the nucleus to the proximal surface of the 
sagitta along the ventral margin of the sulcus 
acousticus. The dates on the top of the bars indi- 
cate time of tetracycline treatment and the dates on 
the end of the bars indicate time of recapture. 



ment (Boehlert, 1985; Maceina and Betsill, 1987), 
others have suggested that reading whole otoliths 
underestimates true age and that this problem be- 
comes worse with fish age (Boehlert, 1985; Hoyer et 
al., 1985). This is mainly due to the fact that in 
many species, sagittae growth is asymmetrical (Irie, 
1960). Growth appears to be linear only up to a cer- 
tain age or size, after which additions occur mainly 
on the interior proximal surface, along the sulcus 
region (Boehlert, 1985; Brothers, 1987; Beamish and 
McFarlane, 1987). That seems to be the case for the 
coral trout, as comparison of results of whole and 
sectioned otoliths indicated that lateral views did 
not reveal many of the annual growth zones in older 
individuals. However, whole otoliths require much 
less time for analysis than sectioned ones and seem 
to provide more precise readings. Therefore, it is use- 
ful to know the limit of reliability of whole readings 
and to define the conditions appropriate for its use. 

Like the inshore coral trout Plectropomus 
macula tits (Ferreira and Russ, 1992), the common 
coral trout P. leopardus is a relatively long-lived, 
slow-growing species. The results on growth and 



longevity obtained here differ somewhat from those 
of previous studies. Goeden (1978), using the 
Petersen method, identified age cohorts up to age 
5+ for P. leopardus. However, the limitations of the 
use of length-frequency data to estimate age of long- 
lived fish are well known (Manooch, 1987; Ferreira 
and Vooren, 1991). Mcpherson et al. (1988), using 
counts of annuli in whole otoliths, were able to age 
fish up to seven years old. Longevity was probably 
underestimated in their study as counts were per- 
formed only on whole otoliths. More recently. Brown 
et al. (1992) 3 analyzed whole and sectioned otoliths 
of coral trout from the same area as Mcpherson et 
al. (1988) and were able to count up to 14 rings. 
Loubens ( 1980) counted annuli from burnt and bro- 
ken otoliths and estimated a maximum longevity for 



3 Brown, I. W., L. C. Squire, and L. Mikula. 1992. Effect of zon- 
ing changes on the fish populations of unexploited reefs. Stage 
1: pre-opening assessment. Draft interim report to the Great Bar- 
rier Reef Marine Park Authority, Townsville, Australia, 27 p. 



SAWSSAWSS 




age = 2 



| Fluorescent 
| Translucent 
^] Opaque 



yry Winter ^ Sumrr 

^ Spnng J\ Auturr 



Figure 6 

Diagrammatic representation of otoliths of young- 
of-the year coral trout, P. leopardus, kept in captiv- 
ity, showing relative positions of the fluorescent 
bands, otolith margin, translucent, and opaque 
zones. Bars represent the whole radius of the otolith 
section, measured from the nucleus to the proximal 
surface of the sagitta along the ventral margin of 
the sulcus acousticus. The dates on the top of the 
bars indicate time of tetracycline treatment or cap- 
ture and the dates on the end of the bars indicate 
time of death. 



Ferreira and Russ: Age-validation and growth rate of Plectropomus leopardus 



53 



so 

B 
<u 

-J 
_<: 
C 



P leopardus of 19 years in New Caledonia. 
These higher estimates of longevity suggest 
that coral trout at Lizard Island could also 
attain older ages. In this case, the absence 
of fishes older than 14 years of age in the 
sample collected at Lizard Island could be 
related to local levels of fishing pressure. 

In the present work, the results of tet- 
racycline labelling indicated that in the 
otoliths of P. leopardus the opaque zone 
(annulus) was formed during the winter 
and spring months whereas the translu- 
cent zone was formed during summer and 
autumn. Though the physiological basis for 
the formation of optically distinct zones in 
calcified structures has not been directly 
established, their presence has been com- 
monly associated with varying growth 
rates, influenced by temperature, photo- 
period, feeding rate, or reproductive cycle 
(see Casselman, 1983, and Longhurst and 
Pauly, 1987, for review). On a daily basis, 
it has been demonstrated that the trans- 
lucent zone, or accretion zone, is formed 
during the phase of more active otolith 
growth, and the opaque or discontinuous 
zone is formed during growth stagnation (Mugiya et 
al., 1981; Watabe et al., 1982). Mosegaard et al. 
(1988) examined the effect of temperature, fish size, 
and somatic growth rate on otolith growth rate and 
suggested that metabolic activity, not necessarily so- 
matic growth rate, governs otolith growth. Thus, if 
the formation of the opaque zone in the coral trout 
otoliths is associated with a period of reduced meta- 
bolic activity, an external determining factor could 
be temperature, as the lowest values for water tem- 
perature around Lizard Island are observed during 
winter and early spring. 4 Annulus formation oc- 
curred in otoliths of juveniles and adults of coral 
trout during the same period, suggesting that repro- 
duction is not a determining factor. 

The growth of the otolith was continuous with age 
but apparently related to somatic growth. A simi- 
lar pattern has been observed for other species of 
fish (Beckman et al., 1991). Otolith weight was the 
best predictor of age in the linear model, explain- 
ing as much variation in age as fork length in the 
von Bertalanffy model. 

The main criteria for choosing a growth curve are 
quality of fit and convenience, differing according to 
whether the need is for a mathematical description 
of a detailed physiological growth process or for fish- 
ery managem ent (Moreau, 1987). The results ob- 

4 Lizard Island Research Station. 1992. LIRS, PMB 37, Cairns, 
Queensland 4870, Australia. Unpubl. data. 



70 



60 



50 



- 40 



30 - 



20 - 



10 



+  

 I 



!!!! 



  

! i I i J ' « 



 


Hook & Line 


+ 


Spear 


o 


Fence Net 



Age-at 
Island 



2 2 4 6 8 10 12 14 16 

Age (years) 

Figure 7 

•length data for coral trout, P. leopardus, from Lizard 
captured by each sampling gear used in this study. 



tained here indicated clearly that the von 
Bertalanffy model adequately described the growth 
of the coral trout. Schnute's model was useful because 
of its flexibility and the stability of its parameters. 

As most fishing gears are selective towards a cer- 
tain size (Ricker, 1969), and smaller sizes are not 
usually available, it is common that growth curves 
are fitted to truncated data representing only part 
of the population. For the coral trout, because of 
gear selectivity and legal size restrictions (legal 
minimum=35 cm TL), only fish of 2+ years were 
captured by line- and spear-fishing. However, the 
first three years of life represent the period of fast- 
est growth, after which the growth pattern changes 
considerably. As a result, much slower growth rates 
were obtained when the growth curve was fitted 
only to the age classes recruited to the fishery. The 
effects of different age ranges on estimated von 
Bertalanffy growth parameters have been recog- 
nized for many years (Knight, 1968; Hirschhorn, 
1974) and greatly compromise comparisons of 
growth rates between populations (Mulligan and 
Leaman, 1992). 

Furthermore, one effect of size-dependent mortal- 
ity is the selective removal of fast-growing individu- 
als (Ricker, 1969; Miranda et al., 1987). Thus, it is 
likely that the average size of the youngest age 
groups recruited to the fishery will be biased to- 
wards the largest, fast-growing individuals. This 



54 



Fishery Bulletin 92(1), 1994 




20 



10 



3 
— 



DS 



-10 



-20 



B     

'■'Ii! ::■■■ 



-2 



10 



13 



16 



Age (years) 



Figure 8 

Von Bertalanffy growth curve fitted to length-at-age 
data of all age classes of coral trout, P. leopardus, 
and plot of residuals. 



seems to be the case for age class 2+, the length of 
which is underestimated by the model including all 
data (Fig. 8). Exclusion of younger ages under these 
circumstances would further enhance the underes- 
timation of K, as well as overestimation of L^ 
(Mulligan and Leaman, 1992). 

Recent research has suggested the possibility of 
different growth processes within a population with 
associated selective fishing mortality (Parma and 
Deriso, 1990) and natural mortality (Mulligan and 



70 






    


60 


 




 ■"■■■■ _JL — 




•   1 1 ^-8 


g 50 

o 

J3 


.: 


  
1 1 


w 


«, «° 








 


c 










u 

M 30 


A-- 


o 




a. 




20 




10 








-2 1 4 7 10 13 16 


Age (years) 


20 


r 




u 





. -   : 




 . . -   


Residual 

o 


Ii. 


 1   

1 1 1 • 

■;.«= : 


10 


 . i 




 


-2 1 4 7 10 13 16 


Age (years) 


Figure 9 


Von Bertalanffy growth curve fitted to length-at-age 


data of >2+ years old coral trout, P. leopardus, and 


plot of residuals. 



Leaman, 1992). The large variability in size at a 
given age observed for the coral trout suggests the 
occurrence of individual variability in growth. The 
reliability of methods of growth estimation like 
length-frequency analysis and growth increments 
from marking-recapture techniques, is greatly af- 
fected by this kind of variation (Sainsbury, 1980), 
further enhancing the importance of obtaining vali- 
dated length-at-age estimates for exploited fish 
populations. The results of selective mortality are 
a direct effect of growth variability on the dynam- 
ics of abundance, and failure to consider the effects 



Ferreira and Russ: Age-validation and growth rate of Plectropomus leopardus 



55 



of different growth potentials can result in gross 
overestimation of optimal fishing levels (Parma and 
Deriso, 1990). 

The absence of marked seasonal changes in low 
latitudes has led to the general belief that tropical 
fishes do not form annual rings in their calcified 
structures (Pannella, 1974). Consequently, most of 
the studies of age determination of tropical fishes 
have concentrated on examination of daily rings. 
This technique, however, is time consuming and lim- 
ited to younger ages (see Longhurst and Pauly, 1987, 
and Beamish and McFarlane, 1987, for review). The 
presence of annual marks in otoliths has been vali- 
dated for an increasing number of species of tropi- 
cal fishes (Samuel et al., 1987; Fowler, 1990; Fer- 
reira and Russ, 1992; Lou, 1992) showing the poten- 
tial of this technique to be used routinely in tropi- 
cal fishery management. 

Acknowledgments 

We would like to thank P. Laycock for his assistance 
with the otolith readings. Many thanks to Owen 
Roberts, who kindly gave us access to his commer- 
cial fishing samples. We thank M. Maida, P. 
Laycock, C. Davies, M. and L. Pearce, L. Vail, A. 
Hogget, J. St. John, and D. Zeller for help in the 
field and in collecting the samples. We are grateful 
to C. Davies for allowing us to use his trapping and 
mark-recapture program to validate this study. This 
work was supported by grants from the Brazilian 
Ministry of Education (CAPES), Australian Re- 
search Council (ARC), Fishing Industry Research 
and Development Council (FIRDC), and the Great 
Barrier Reef Marine Park Authority (Augmentative). 



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1981. A method for comparing the precision of a set 
of age determinations. Can. J. Fish. Aquat. Sci. 
38:982-983. 
Beamish, R. J., and G. A. McFarlane. 

1987. Current trends in age determination 
methodology. In R. C. Summerfelt and G. E. Hall 
(eds.), Age and growth offish, p. 15-42. Iowa 
State Univ. Press, Ames. 
Beckman, D. W., A. L. Stanley, J. H. Render, and 
C. A Wilson. 

1991. Age and growth-rate estimation of sheeps- 
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Beverton, R. J. H., and S. J. Holt. 

1957. On the dynamics of exploited fish popula- 
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Boehlert, G. W. 

1985. Using objective criteria and multiple regres- 
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Brothers, E. B. 

1987. Methodological approaches to the examina- 
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Summerfelt and G. E. Hall (eds.), Age and growth 
offish, p. 319-330. Iowa State Univ. Press, Ames. 
Casselman, J. M. 

1983. Age and growth assessment of fish from their 
calcified structures: techniques and tools. U.S. 
Dep. Commer., NOAA Tech. Rep. NMFS 8, 
p. 1-17. 

1990. Growth and relative size of calcified structures 
of fish. Trans. Am. Fish. Soc. 119:673-688. 

Chen, Y., D. A. Jackson, and H. H. Harvey. 

1992. A comparison of von Bertalanffy and polyno- 
mial functions in modelling fish growth data. 
Can. J. Fish. Aquat. Sci. 49:1228-1235. 
Christensen, J. M. 

1964. Burning of otoliths, a technique for age de- 
termination of soles and other fish. J. Cons, 
perm. int. Explor. Mer. 29:73-81. 
Ferreira, B. P., and C. M. Vooren. 

1991. Age, growth and structure of vertebra in the 
school shark Galeorhinus galeus (Linnaeus, 1758) 
from Southern Brazil. Fish. Bull. 89 (1):19-31. 

Ferreira, B. P., and G. R. Russ. 

1992. Age, growth and mortality of the inshore coral 
trout Plectropomus maculatus (Pisces: Serranidae) 
from the Central Great Barrier Reef, Aus- 
tralia. Aust. J. Mar. Freshwater Res. 43:1301-1312. 

Fowler, A. J. 

1990. Validation of annual growth increments in 
the otoliths of a small, tropical coral reef 
fish. Mar. Ecol. Prog. Ser. 64:25-38. 
Gallucci, V. F., and T. J. Quinn. 

1979. Reparameterizing, fitting and testing a 
simple growth model. Trans. Am. Fish. Soc. 
108:14-25. 
Goeden, G. B. 

1978. A monograph of the coral trout Plectropomus 
leopardus (Lacepede). Qld. Fish. Serv, Res. Bull. 
(l):l-42. 
Hirschhorn, G. 

1974. The effect of different age ranges on esti- 
mated Bertalanffy growth parameters in three 
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13-27. Unwin Bros., Surrey, England. 
Hoyer, M. V., J. V. Shireman, and M. J. Maceina. 
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Irie, T. 

1960. The growth of the fish otolith. J. Fac. Fish. 
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56 



Fishery Bulletin 92[ I), 1994 



Kimura, D. K. 

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Abstract. Red drum, 

Sciaenops ocellatus, from Mosquito 
Lagoon, east-central Florida, were 
examined for variation in products 
of nine polymorphic nuclear-gene 
(allozyme) loci and in mitochon- 
drial (mt)DNA restriction sites. 
Genetic data from Mosquito La- 
goon fish were compared to simi- 
lar data from red drum sampled 
from the northeastern Gulf of 
Mexico (Gulf) and the Carolina 
coast of the southeastern United 
States. Significant heterogeneity 
among red drum from the three 
areas was found in the frequencies 
of inferred alleles at two to three 
allozyme loci and in the frequen- 
cies of six mtDNA haplotypes. Red 
drum from Mosquito Lagoon were 
as differentiated genetically from 
red drum in the northeastern Gulf 
and Carolina coast as the latter 
two were from each other. Genetic 
data are consistent with the hy- 
pothesis that red drum in Mos- 
quito Lagoon are self-contained 
and at least partially isolated from 
red drum in other U.S. waters. 



Genetic distinctness of red drum 
(Sciaenops ocellatus) from 
Mosquito Lagoon, 
east-central Florida* 

John R. Gold 

Department of Wildlife and Fisheries Science 
Texas A&M University, College Station. Texas 77843 

Linda R. Richardson 

Department of Wildlife and Fisheries Science 
Texas A&M University. College Station, Texas 77843 



Manuscript accepted 17 August 1993 
Fishery Bulletin: 92:58-66 (1994) 



Over the past five years, our labo- 
ratory has carried out studies of 
spatial and temporal genetic varia- 
tion among red drum (Sciaenops 
ocellatus) from the northern Gulf of 
Mexico (Gulf) and the Carolina 
coast of the southeastern United 
States (Bohlmeyer and Gold, 1991; 
Gold and Richardson, 1991; Gold et 
al., 1993, in press). Red drum cur- 
rently support important recre- 
ational fisheries in both the north- 
ern Gulf and U.S. Atlantic (Mat- 
lock, 1984; Mercer, 1984), and both 
fisheries are now regulated to re- 
duce growth and recruitment over- 
fishing (Swingle et al., 1984 1 ; 
Goodyear, 1989 2 ). Collectively, our 
genetic data have indicated that 
red drum in U.S. waters are sub- 
divided with weakly differentiated 
subpopulations in the northern 
Gulf and along the Carolina coast. 
No genetic heterogeneity has been 
found among red drum from differ- 
ent localities within either the 
northern Gulf or Carolina coast 
(Gold et al., 1993, in press). The ge- 
netic data are consistent with sev- 
eral aspects of red drum biology 
and life history that suggest red 
drum dispersal and gene flow 
among contiguous bays and estuar- 
ies could be extensive. These in- 
clude 1) transport of eggs, larvae, 
or juveniles from spawning locali- 
ties near the mouths of bays or es- 



tuaries to adjacent bays or estuar- 
ies by oceanic currents (Lyczkoski- 
Schultz et al., 1988 3 ), 2) movement 
of sexually-mature adults from bay 
or estuarine juvenile nurseries into 
deeper, offshore waters prior to 
spawning (Matlock, 1984), and 3) 
formation of large, offshore schools 
that can migrate extensively 
(Overstreet, 1983; Matlock, 1984; 
Swingle et al., 1984 1 ). 

In this study, data on allozyme 
and mitochondrial (mt)DNA varia- 
tion among red drum sampled from 
Mosquito Lagoon on the east coast 
of Florida are presented and com- 
pared to data from previous stud- 
ies. The goal of the study was to 



* Contribution No. 24 of the Center for Bio- 
systematics and Biodiversity, Texas A&M 
University. 

1 Swingle, W., T. Leary, D. Davis, V. Blomo, 
W. Tatum, M. Murphy, R. Taylor, G. 
Adkins, T Mcllwain, and G. Matlock. 
1984. Fishery profile of red drum. Gulf of 
Mexico Fish. Mngmt. Council and Gulf 
States Mar. Fish. Comm., Lincoln Cntr, 
Suite 331, 5401 West Kennedy Blvd., 
Tampa, FL. 

2 Goodyear, C. P. 1989. Status of red drum 
stocks of the Gulf of Mexico: report for 
1989. Contrib. CRD 88/89-14, Southeast 
Fish. Cntr, Miami Lab., Coast. Res. Div., 
75 Virginia Beach Drive, Miami, FL. 

■' Lyczkowski-Schultz, J., J. P. Steen Jr., 
and B. H. Comyns. 1988. Early life history 
of red drum (Sciaenops ocellatus) in the 
northcentral Gulf of Mexico. Mississippi- 
Alabama Sea Grant Consortium (Project 
No. R/LR-12). Gulf Coast Res. Lab., P.O. 
Box 7000, Ocean Springs, unpubl. ms. 



58 



Gold and Richardson: Sciaenops ocellatus from Mosquito Lagoon 



59 



test the hypothesis that red drum from Mos- 
quito Lagoon and other U.S. waters are geneti- 
cally homogeneous. Red drum in Mosquito 
Lagoon are of particular interest because they 
may represent a self-contained, at least par- 
tially isolated subpopulation. Evidence for the 
latter includes documentation within the sys- 
tem of both post-spawning females and red 
drum eggs (Murphy and Taylor, 1990; Johnson 
and Funicelli, 1991). In addition, physical ac- 
cess to the Atlantic from the lagoon is limited. 
In brief, Mosquito Lagoon (Fig. 1) is long and 
narrow (54 km x 4 km) and is separated from 
the Atlantic by a barrier beach. The lagoon 
represents the northern part of the Indian 
River lagoonal system and has two narrow 
outlets: one, Ponce de Leon Inlet, is a natural 
pass to the Atlantic located at the northern end 
of the lagoon; the other, Haulover Canal, is a 
man-made passageway at the southern end of 
the lagoon that leads into the Indian River. 
Access to or from the Atlantic through Ponce 
de Leon Inlet is restricted because of a series 
of islands and small passageways in the north- 
ern part of the lagoon. Access to or from the 
Atlantic through Haulover Canal (completed in 
1929) would only be recent, and the nearest 
outlet to the Atlantic south from Haulover ca- 
nal is roughly 90-100 km. We also were inter- 
ested in studying red drum from Mosquito 
Lagoon because our earlier work (Gold et al., 
1993, in press) did not include red drum from 
the east coast of Florida, an area of potential 
importance to tests of hypotheses regarding ge- 
netic subdivision between red drum from the 
northern Gulf and the U.S. Atlantic (Gold et 
al., in press). Finally, adult red drum from Mos- 
quito Lagoon form a large part of the 
broodstock used by the Florida Department of 
Natural Resources (FDNR) to supplement and 
enhance the red drum fishery in Florida wa- 
ters. The genetic composition of Mosquito La- 
goon red drum is thus important to research 
in stocking hatchery-raised fish. 

Materials and methods 

Red drum were collected from Mosquito Lagoon 
during fall 1988, spring 1990, and spring 1991. 
Fish were captured with trammel nets. Tissues 
(heart, spleen, and muscle) were removed and 
placed in liquid nitrogen for transport to Texas A&M 
University where they were stored at -80°C. Ages 
of all but yearling (age zero) individuals (i.e., speci- 
mens less than 300 mm total length) were deter- 



Ponce de Leon Inlet 




10km 




Figure 1 

Mosquito Lagoon, east-central Florida, showing Ponce de 
Leon Inlet and Haulover Canal. 



mined from annuli on otoliths by using methods 
described in Bumguardner (1991). 

Individuals sampled in 1988 (41 total) were sur- 
veyed for variation at nine polymorphic allozyme 



60 



Fishery Bulletin 92(1), 1994 



loci: ACP-2* (acid phosphatase); ADA* (adenosine 
deaminase); ADH* (alcohol dehydrogenase); sAAT-1* 
(aspartate aminotransferase); EST-1* (esterase); 
GPI-B* (glucose phosphate isomerase); and PEPB' , 
PEPD * , and PEPS' (peptidases). Techniques for ver- 
tical starch gel electrophoresis, details of grinding 
and running buffers, starch composition of gels, 
protein staining, and interpretation of banding pat- 
terns may be found in Bohlmeyer (1989) and 
Bohlmeyer and Gold (1991). Designation of allelic 
variants was based on relative mobility to the most 
common allele (Allele * 100). 

All individuals collected (109 total) were assayed 
for 104 mtDNA restriction sites with 13 restriction 
enzymes: BamKl, Bell, EcoRV, Hindlll, Ncol, Nsil, 
PstI, Pvull, Seal, Spel, Stul,Xbal, and Xmnl. Meth- 
ods used to assay mtDNAs of individual fish may 
be found in Gold and Richardson (1991). Homology 
of fragments from single digestions was tested by 
multiple, side-by-side comparisons. Variant patterns 
exhibiting only a single band of greater than 15 kb 
were tested for homology by using double digestions 
with BawHI as described in Gold and Richardson 
(1991). 

Red drum from Mosquito Lagoon were initially 
subdivided into year classes and tested for hetero- 
geneity in both allozyme and mtDNA haplotype fre- 
quencies. Year classes (number of individuals) were 
1985 (17), 1986 (25), 1987 (11), 1988 (7), and 1989 
(49). No significant heterogeneity (P>0.05) in 
allozyme or mtDNA haplotype frequencies was 
found among year classes. Subsequent data analy- 
ses employed three test groups: 1) red drum from 
Mosquito Lagoon; 2) red drum from the northeast- 
ern Gulf; and 3) red drum from the Carolina coast. 
Data for the latter two were taken from Gold et al. 
(1993, 1994) and represent red drum from the fol- 
lowing localities: northeastern Gulf — Apalachicola 
Bay, Riviera Bay, and Sarasota Bay (west coast of 
Florida); and Carolina coast — Calibogue Sound, 
Charleston Bay, and North Inlet (South Carolina), 
and the Pamlico River and Oregon Inlet (North 
Carolina). A map showing these localities may be 
found in Bohlmeyer and Gold ( 1991 ). A summary of 
allele frequencies at the nine polymorphic allozyme 
loci and the distribution of mtDNA haplotypes in 
each test group are given in Appendix Tables 1 and 
2, respectively. 

For allozyme data, tests of Hardy-Weinberg equi- 
librium expectations and generation of Nei's (1978) 
unbiased genetic distance were accomplished by 
using BIOSYS-1 (Swofford and Selander, 1981). 
Deviations from Hardy-Weinberg expectations were 
tested by using pooled genotypes and the chi-square 
statistic with one degree of freedom. Significance 



testing of allele-frequency differences among test 
groups was accomplished by using 1) the G-statis- 
tic (Sokal and Rohlf, 1969) on contingency tables of 
allele counts and the BIOM-PC program (Rohlf, 
1983), and 2) the ^-statistic (DeSalle et al., 1987) 
on arcsin, square-root transformed allele frequen- 
cies. For mtDNA data, significance testing of 
mtDNA-haplotype frequency differences was carried 
out by using the G- and V-statistics as described 
above and a Monte Carlo randomization procedure 
(Roff and Bentzen, 1989). Nucleon diversities and 
intra- and inter-populational nucleotide sequence 
diversities were estimated by using equations in Nei 
and Tajima (1981). Analysis of mtDNA data was 
facilitated by the Restriction Enzyme Analysis Pack- 
age (REAP) of McElroy et al. (1992). Significance 
levels for multiple tests performed simultaneously 
were adjusted after Cooper (1968). 



Results 

No significant deviations from Hardy Weinberg equi- 
librium expectations at any of the nine polymorphic 
allozyme loci were found following corrections for 
multiple tests. Two significant deviations were found 
in uncorrected tests: at GPI-B* (P=0.015) and PEPS' 
(P=0.012) in the northeastern Gulf. Both deviations 
appeared to be due to rare homozygotes for low fre- 
quency alleles. One new allele (Allele * 110 at EST- 
l') was found among Mosquito Lagoon fish at a fre- 
quency of 1.2 percent (Appendix Table 1). 

Estimates of allozyme variation (Table 1) indicate 
that red drum from Mosquito Lagoon have fewer 







Table 1 




Allozyme 


variation in 


red drum (S 


iaenops ocel- 


latus). 
















Mean 


Mean 






Mean 


number of 


hetero- 


Test 




sample 


alleles/locus 


zygosity/ 


group 




size/locus 


<± SE) 


locus' (±SE) 


Northeastern 








Gulf of 










Mexico 




246 


3.9 + 0.9 


0.225 ± 0.076 


Mosquito 










Lagoon, 










Florida 




41 


2.9 ± 0.6 


0.206 ± 0.081 


U.S. Carol 


id. i 








Coast 




176 


3.9 ± 0.9 


0.213 ± 0.074 


1 Direct-cou 


nt estimate. 







Gold and Richardson: Sciaenops ocellatus from Mosquito Lagoon 



61 



alleles per locus or lower estimates of mean het- 
erozygosity, or both, than do red drum from the 
northeastern Gulf and Carolina coast. The differ- 
ences in genetic variation, however, are non-random 
across loci. Heterozygosity per locus values among 
Mosquito Lagoon fish at loci (e.g., ACP-2* , ADA*, 
ADH*, sAAT-1*, and EST-1*) where alternate alleles 
occurred at frequencies of five percent or greater 
were equivalent to values among fish from the 
northeastern Gulf and Carolina coast (data not 
shown). Differences in heterozygosity per locus val- 
ues were observed at loci (e.g., GPI-B *, PEPB* , and 
PEPD* ) where alleles occurring in a frequency of one 
to three percent in northeastern Gulf or Carolina coast 
fish, or both, were not found among Mosquito Lagoon 
fish (Appendix Table 1). 

Significant heterogeneity (P<0.05) in allele fre- 
quencies among test groups was found by using the 
G-test at ADA* (G=33.92, df=22, P=0.004) and sAAT- 
1* (G=13.59, df=6, P=0.036). Additional G-tests were 
carried out after pooling alleles whose frequency in 
any sample was less than 10%. Significant hetero- 
geneity was again found at ADA* (G=9.62, df=4, 
P=0.048) and also at PEPB* (G=6.86, df=2, PM3.034). 
Examination of allele frequencies at ADA*, sAAT-1, 
and PEPB* did not reveal any striking differences 
among test groups, suggesting that heterogeneity 
was due to accumulation of small differences in fre- 
quencies of rare alleles. At ADA*, for example, the 
frequency of Allele *115 was higher among Mosquito 
Lagoon fish and lower among Carolina coast fish; 
whereas the frequencies of Alleles *90 and *85 were 
higher among northeastern Gulf fish (Appendix 
Table 1). At sAAT-1* and PEPB*, slight frequency dif- 
ferences were apparent for Allele * 110 (higher in 
Mosquito Lagoon fish) and Allele 115 (higher in 
northeastern Gulf fish and absent 
from Mosquito Lagoon fish), re- 
spectively (Appendix Table 1). The 
observation that G-test heteroge- 
neity was due to small, cumula- 
tive frequency differences was cor- 
roborated by V-tests where no sig- 
nificant heterogeneity (P>0.05) in 
allele frequencies was found at 
any locus following corrections for 
multiple tests. 

MtDNA fragment patterns from 
single digestions with 13 restric- 
tion enzymes generated 36 com- 
posite mtDNA haplotypes among 
fish from Mosquito Lagoon, eleven 
of which (numbers 114, 134-143) 
have been found only in Mosquito 
Lagoon red drum (Appendix Table 



2). Estimates of mtDNA variation (Table 2) indi- 
cated that nucleon diversity (the probability of any 
two individuals differing in mtDNA haplotype) was 
highest in red drum from the northeastern Gulf and 
lowest in red drum from the Carolina coast; whereas 
intrapopulational nucleotide sequence diversity (the 
genetic difference between any two individuals) was 
greatest among Mosquito Lagoon fish. These esti- 
mates of mtDNA variation are among the highest 
reported to date for a non-clupeid, marine fish spe- 
cies (Richardson and Gold, 1993). 

Highly significant heterogeneity in mtDNA- 
haplotype frequencies among test groups and be- 
tween pairwise comparisons of test groups were 
found in both G-tests and Monte Carlo 
bootstrapping (Table 3). These results indicate that 
all three test groups differ significantly from each 
other. V-tests, carried out on haplotypes found in ten 
or more individuals (12 haplotypes total), identified 
six haplotypes (Table 4) that differed significantly 
among test groups. Genetic distances based on 
allozymes and mtDNAs (Table 5) indicate that red 
drum from Mosquito Lagoon are at least as diver- 
gent genetically from red drum in the northeastern 
Gulf and Carolina coast as the latter two are from 
each other. 



Discussion 

Tests of heterogeneity clearly indicate that red drum 
from Mosquito Lagoon differ genetically from red 
drum in the northeastern Gulf and along the Caro- 
lina coast and that at least three subpopulations of 
red drum occur in U.S. waters. That the genetic 
differences appear more pronounced in mtDNA than 









Table 2 






MtDNA 


variation in 


red drum (Sciaenops ocellatus). 












Nucleotide 






Number 


Number 




sequence 


Test 




of 


of 


Nucleon 


diversity 


group 




individuals 


haplotypes 


diversity 


(± SD)' 


Northeastern 












Gulf of Mexico 




247 


49 


0.947 


0.557 ± 0.298 


Mosquito Lagoon, 












Florida 




109 


36 


0.912 


0.597 ± 0.321 


U.S. Carolina 












Coast 




174 


43 


0.904 


0.560 ± 0.351 


1 Values are in percent 


Standard d 


eviations are used 


instead of standard errors be- 


cause of the large 


number of pairwise comparisons used to generate 


mean values. 



62 



Fishery Bulletin 92(1), 1994 





Table 


3 




Results of tests for heterogeneity in 
among red drum (Sciaenops ocellatu 
Mexico, Mosquito Lagoon, Florida, a 


mtDNA haplotype frequencies 
s) from the northeastern Gulf of 
nd the U.S. Carolina coast. 


Test group 


Results of G-tests 


P-value from 

Monte Carlo 

randomizations 


G-score 


P-value 


Northeastern Gulf vs. 
Mosquito Lagoon vs. 
Carolina Coast 


159.5 


<0.001' 


<0.001 


Northeastern Gulf vs. 
Mosquito Lagoon 


73.9 


<0.001 2 


<0.00T 


Northeastern Gulf vs. 
Carolina Coast 


76.2 


<0.001 3 


<0.001 


Mosquito Lagoon vs. 
Carolina Coast 


66.2 


<0.001 4 


0.006 


Degrees of freedom in G-tests: 48' 


18 2 , 19 3 , and 27 J . 











Table 4 






Frequency 7 of six 


sign 


ificantly he 


terogeneous mtDNA 


haplotypes of red drum {Sciaenops ocellatus) in 


the northeast- 


era Gulf of Mexico, 


Mosq 


uito Lagoon, 


Florida, 


and the U.S. 


Carolina 


coast. 












Northeastern 


Mosquito 


Carolina 


Probability 


Haplo- 


Gulf 




Lagoon 


Coast 


value from 


type 


(rc=247) 




(rc=109) 


(n = 174) 


V-test 2 


8 


13.3 




23.8 


10.3 


=0.010 


9 


7.7 




13.8 


26.4 


<0.001 


11 


9.3 




1.8 


7.5 


=0.019 


12 


0.0 




7.3 


3.4 


<0.001 


21 


4.4 




i) i) 


ii 6 


=0.004 


29 


1 () 




ii i) 


1.7 


=0.021 


' Values are in percent. 

2 After DeSalle et al. (1987). 



in (presumed) nuclear-coding genes is not surpris- 
ing, given that mtDNA is expected to be at least four 
times more sensitive to population substructuring 
(Birky et al., 1983; Templeton, 1987). Because pre- 
vious studies (Gold et al., 1993, in press) found no 
evidence of genetic heterogeneity among red drum 
from eleven estuaries or bays in the northern Gulf 
or among red drum from five estuaries or bays along 
the Carolina coast, red drum from Mosquito Lagoon 
are unusual in representing a genetically distinct 
red drum subpopulation existing within a single bay 
or estuary. 



Campton (1992) 4 examined red 
drum from Mosquito Lagoon for 
allelic variation at several 
allozyme loci and found genetic 
homogeneity among red drum 
from Mosquito Lagoon, the north- 
ern Gulf, and the Carolina coast. 
He suggested that our initial 
study (Bohlmeyer and Gold, 1991) 
of allozyme variation among 
northern Gulf and Carolina coast 
red drum did not account for tem- 
poral variation among samples 
within localities. Our subsequent 
studies (and this one), however, 
have included temporal sampling 
of variation in both allozymes and 
mtDNA and have demonstrated 
that weak (but significant) genetic 
heterogeneity exists (Gold et al., 
1993, in press). Sampling error 
associated with specimen procure- 
ment in varying time and space 
may account for the different results ob- 
tained in Campton's (1992) 4 study and 
this one. However, in Campton's (1992) 4 
study, the total G-statistic, obtained by 
summing individual G-values and their 
associated degrees of freedom, was signifi- 
cant at the 0.01 level. This suggests the 
existence of spatial or temporal genetic 
heterogeneity, or both, among the locali- 
ties sampled. 

Genetic differentiation of red drum in 
Mosquito Lagoon is consistent with the 
hypothesis that red drum in Mosquito 
Lagoon represent a self-contained, at 
least partially isolated subpopulation. 
Three lines of evidence support this hy- 
pothesis. First, genetic differences be- 
tween red drum from Mosquito Lagoon 
and red drum sampled elsewhere involve 
frequencies of alleles at two or three pu- 
tative nuclear-gene loci and frequencies of at least 
six mtDNA haplotypes. Differentiation of several, 
presumably independent and selectively-neutral, 
genetic markers suggests a genome-wide effect re- 
lated to at least partial isolation and reduced gene 
flow (Wright, 1978; Hartl and Clark, 1989). Second, 
inferred nuclear-gene alleles present in low fre- 
quency in red drum sampled outside of Mosquito 



Campton, D. E. 1992. Gene flow estimation and population struc- 
ture of red drum iSaaenops ocellatus) in Florida. Final Rep. Coop. 
Agrmt. No. 14-16-009-1522, U.S. Fish & Wildl. Serv, Natl. Fish. 
Res. Cntr., 7920 N.W. 71st St., Gainesville, FL. 



Gold and Richardson: Sciaenops ocellatus from Mosquito Lagoon 



63 



Table 5 

Matrix of Nei's (1978) unbiased genetic distance 
based on allozymes (upper diagonal) and Nei and 
Tajima's (1981) corrected interpopulational nucle- 
otide sequence divergence based on mtDNAs 
(lower diagonal) among red drum (Sciaenops 
ocellatus) from the northeastern Gulf of Mexico, 
Mosquito Lagoon, Florida, and the U.S. Carolina 
coast. Interpopulational nucleotide sequence di- 
vergence values are in percent. 

Northeastern Mosquito Carolina 
Gulf Lagoon Coast 

Northeastern Gulf 0.000 0.001 

Mosquito Lagoon 0.006 0.002 

Carolina Coast 0.006 0.009 



Lagoon were not found in red drum from Mosquito 
Lagoon; whereas one inferred allele and eleven 
mtDNA haplotypes were unique to red drum from 
Mosquito Lagoon. The distribution of low frequency 
nuclear-gene alleles and mtDNA haplotypes is con- 
sistent with reduced gene flow concomitant with 
allele-frequency drift expected in isolated subpopu- 
lations. Finally, both females with ovaries contain- 
ing postovulatory follicles and spawned red drum 
eggs have been documented in Mosquito Lagoon 
(Murphy and Taylor, 1990; Johnson and Funicelli, 
1991), clearly indicating that red drum spawn 
within the system. 

Assuming red drum in Mosquito Lagoon represent 
a partially isolated, self-contained subpopulation, 
one question of interest is how long the subpopula- 
tion has been semi-isolated. Geological evidence 
(Mehta and Brooks, 1973, cited from Johnson and 
Funicelli, 1991) indicates that several tidal inlets 
once connected Mosquito Lagoon to the Atlantic, the 
last of which is estimated to have closed about 1,500 
years ago. Assuming some variation in the geologi- 
cal estimate, this date does not differ substantially 
from an estimate of 2,900 ± 1,550 (SD) years based 
on 1) a corrected interpopulational nucleotide se- 
quence divergence (between red drum in Mosquito 
Lagoon and red drum elsewhere) of 0.0058 ± 0.0031 
(SD) percent, and 2) an evolutionary rate for verte- 
brate mtDNA of 0.01 substitutions/bp/lineage/Myr 
(Brown et al., 1979; Wilson et al., 1985). Given on- 
going debates about molecular clocks, the correspon- 
dence between the two temporal estimates is note- 
worthy. 

Because the genetic distinctness of Mosquito La- 
goon red drum appears to stem largely from physi- 
cal isolation, the biological reasons for subdivision 



between red drum in the northern Gulf and those 
along the Carolina coast remain unknown. Possible 
reasons for this subdivision could include 1) current 
patterns between the Gulf and U.S. Atlantic, 2) 
absence of suitable near-shore habitats along the 
southeastern coast of Florida, or 3) differences in 
biogeographic provinces (Gold et al., 1993, in press). 
Similar genetic discontinuities between U.S. Atlan- 
tic and Gulf coast fauna have been described by 
Avise and co-workers (reviewed in Avise, 1992). 
Their hypothesis is that the concordant 
phylogeographic patterns provide evidence of simi- 
lar vicariant histories that are tentatively related to 
episodic changes in environmental conditions dur- 
ing the Pleistocene (Avise, 1992). The relative inac- 
cessibility of Mosquito Lagoon suggests that sam- 
pling red drum from north or south of Mosquito 
Lagoon may be more informative for testing hypoth- 
eses regarding phylogeographic subdivision between 
the northern Gulf and the U.S. Atlantic. 

A last point to consider is the use of Mosquito 
Lagoon red drum as broodstock for stock enhance- 
ment programs. It could be argued that red drum 
from Mosquito Lagoon differ genetically from red 
drum sampled elsewhere (e.g., the northeastern 
Gulf) and should be used only for stock enhancement 
at localities where no genetic differences exist. Al- 
ternatively, it could be argued that the genetic dis- 
tinctiveness of red drum in Mosquito Lagoon is rela- 
tively small and possibly inconsequential. This fol- 
lows from the observation that the documented ge- 
netic difference between red drum in Mosquito La- 
goon and red drum sampled elsewhere is consider- 
ably less than that, on average, among races of man 
(Cann et al., 1987). One other consideration might 
be to cross red drum from Mosquito Lagoon with red 
drum from elsewhere (e.g., the northeastern Gulf) 
in order to increase performance from potential 
heterotic effects. 



Acknowledgments 

Assistance in procuring red drum specimens from 
Mosquito Lagoon was provided by J. Burch, J. 
Camper, B. Denis, C. Furman, M. Murphy, G. 
Ramos, and D. Roberts. Their assistance is grate- 
fully acknowledged. Special thanks are extended to 
C. Amemiya and D. Roberts for providing no-cost 
lodging during field trips. We also thank B. Colura 
and B. Bumguardner for carrying out age determi- 
nations from otoliths, D. Bohlmeyer and C. Furman 
for assistance in the laboratory, R. Taylor for pro- 
viding historical information on the construction of 
Haulover Canal, and M. Murphy for providing criti- 



64 



Fishery Bulletin 92(1). 1994 



cal comments on a draft of the manuscript. Work 
was supported by the Texas A&M University Sea 
Grant College Program (grants NA85AA-D-SG128 
and NA89AA-D-SG139), by the MARFIN Program 
of the U.S. Department of Commerce (grants NA89- 
WC-H-MF025 and NA90AA-H-MF107), and by the 
Texas Agricultural Experiment Station (Project H- 
6703). This paper represents number XI in the se- 
ries "Genetic Studies in Marine Fishes." 



Literature cited 

Avise, J. C. 

1992. Molecular population structure and the bio- 
geographic history of a regional fauna: a case his- 
tory with lessons for conservation biology. Oikos 
63:62-76. 

Birky Jr., C. W., T. Maruyama, and P. Fuerst. 

1983. Mitochondrial DNAs and phylogenetic 
relationships. In S. K. Dutta (ed.), DNA system- 
atics, p. 107-137. CRC Press, Boca Raton, FL. 
Bohlmeyer, D. A. 

1989. A protein electrophoretic analysis of popula- 
tion structure in the red drum (Sciaenops 
ocellatus). M.S. thesis, Texas A&M University, 
College Station, TX. 
Bohlmeyer, D. A., and J. R. Gold. 

1991. Genetic studies in marine fishes. II: A pro- 
tein electrophoretic analysis of population struc- 
ture in the red drum Sciaenops ocellatus. Mar. 
Biol. 108:197-206. 
Brown, W. M., M. George Jr., and A. C. Wilson. 

1979. Rapid evolution of animal mitochondrial 
DNA. Proc. Natl. Academy Sci. (USA) 76:1967- 
1971. 
Bumguardner, B. W. 

1991. Marking subadult red drums with 
oxytetracycline. Trans. Am. Fish. Soc. 120:537-540. 
Cann, R. L., M. Stoneking, and A. C. Wilson. 

1987. Mitochondrial DNA and human evolution. 
Nature 325:31-36. 
Cooper, D. W. 

1968. The significance level in multiple tests made 
simultaneously. Heredity 23:614-617. 
DeSalle, R., A. Templeton, I. Mori, S. Pletscher, 
and J. S. Johnston. 

1987. Temporal and spatial heterogeneity of 
mtDNA polymorphisms in natural populations of 
Drosophila mercatorum. Genetics 116:215-233. 
Gold, J. R., and L. R. Richardson. 

1991. Genetic studies in marine fishes. IV: An 
analysis of population structure in the red drum 
(Sciaenops ocellatus) using mitochondrial 
DNA. Fish. Res. 12:213-241. 
Gold, J. R., L. R. Richardson, C. Furman, and T. 
L. King. 

1993. Mitochondrial DNA differentiation and popu- 
lation structure in red drum (Sciaenops ocellatus) 



from the Gulf of Mexico and Atlantic Ocean. Mar. 
Biol. (In press.) 
Gold, J. R., T. L. King, L. R. Richardson, D. A. 
Bohlmeyer, and G. C. Matlock. 

In press. Genetic studies in marine fishes. VII: 
Allozyme differentiation within and between red 
drum (Sciaenops ocellatus) from the Gulf of Mexico 
and Atlantic Ocean. J. Fish Biol. 116:175-185. 
Hartl, D. L., and A. G. Clark. 

1989. Principles of population genetics, 2nd 
ed. Sinauer Assoc, Inc., Sunderland, MA. 

Johnson, D. R., and N. A. Funicelli. 

1991. Spawning of the red drum in Mosquito La- 
goon, east-central Florida. Estuaries 14:74-79. 

Matlock, G. C. 

1984. A basis for the development of a management 
plan for red drum in Texas. Ph.D. diss., Texas 
A&M University, College Station, TX. 
McElroy, D., P. Moran, E. Bermingham, and I. 
Kornfield. 

1992. REAP-The Restriction Enzyme Analysis 
Package. J. Hered. 83:157-158. 

Mehta, A. J., and H. K. Brooks. 

1973. Mosquito Lagoon barrier beach study. Shore 
and Beach 41:27-34. 
Mercer, L. 

1984. A biological and fisheries profile of red drum, 
Sciaenops ocellatus. Spec. Sci. Rep. 41, North 
Carolina Dep. Nat. Resour. Community Dev, Div. 
Mar. Fish., Raleigh, NC. 
Murphy, M. D., and R. G. Taylor. 

1990. Reproduction, growth, and mortality of red 
drum, Sciaenops ocellatus, in Florida. Fish. Bull. 
88:531-542. 

Nei, M. 

1978. Estimation of average heterozygosity and ge- 
netic distance from a small number of indi- 
viduals. Genetics 89:583-590. 
Nei, M., and F. Tajima. 

1981. DNA polymorphism detectable by restriction 
endonucleases. Genetics 97:145-163. 
Overstreet, R. M. 

1983. Aspects of the biology of the red drum, 
Sciaenops ocellatus, in Mississippi. Gulf Res. 
Rep. (Suppl.) 1:45-68 
Richardson, L. R., and J. R. Gold. 

1993. Mitochondrial DNA variation in red grouper 
(Epinephelus morio) and greater amberjack 
(Seriola dumerili) from the Gulf of Mexico. ICES 
J. Mar. Sci. 50:53-62. 

Roff, D. A., and P. Bentzen. 

1989. The statistical analysis of mitochondrial poly- 
morphisms: chi-square and the problem of small 
samples. Mol. Biol. Evol. 6:539-545. 
Rohlf, F. J. 

1983. BIOM-PC: a package of statistical programs 
to accompany the text BIOMETRY. W. H. Free- 
man & Co., San Francisco, CA. 
Sokal, R. R., and F. J. Rohlf. 

1969. Biometry. The principles and practice of sta- 



Gold and Richardson: Saaenops ocellatus from Mosquito Lagoon 



65 



tistics in biological research. W. H. Freeman & 
Co., San Francisco, CA. 
Swofford, D. L., and R. B. Selander. 

1981. BIOSYS-1: a FORTRAN program for the 
comprehensive analysis of electrophoretic data in 
population genetics and systematics. J. Hered. 
72:281-283. 
Templeton, A. R. 

1987. Genetic systems and evolutionary rates. In K 
F. S. Campbell and M. F. Day (eds.), Rates of evolu- 
tion, p. 218-234. Australian Acad. Sci., Canberra. 



Wilson, A. C, R. L. Cann, S. M. Carr, M. George 
Jr., U. B. Gyllensten, K. M. Helm-Bychowski, R. 
G. Higuchi, S. R. Palumbi, E. M. Prager, R. D. 
Sage, and M. Stoneking. 

1985. Mitochondrial DNA and two perspectives on 
evolutionary genetics. Biol. J. Linnaean Soc. 
26:375-400. 

Wright, S. 

1978. Evolution and the genetics of popu- 
lations. Univ. Chicago Press, Chicago, IL. 



Appendix Table 1 

Allele frequencies at nine polymorphic loci among red drum iSciaenops ocellatus) from the northeastern Gulf 
of Mexico, Mosquito Lagoon, Florida, and the U.S. Carolina coast. 





Northeastern 


Mosquito 


U.S. 




Northeastern 


Mosquito 


U.S. 


Locus 


Gulf of 


Lagoon, 


Carolina 


Locus 


Gulf of 


Lagoon, 


Carolina 


allele 


Mexico' 


Florida 


coast 7 


allele 


Mexico' 


Florida 


coast' 


ACP-2' 
















'125 


0.002 


0.012 


0.000 


EST-f 








'115 


0.087 


0.073 


0.063 


'110 


0.000 


0.012 


0.000 


'100 


0.911 


0.915 


0.937 


'100 


0.911 


0.915 


0.898 


(n) 


(246) 


(41) 


(175) 


"95 


0.089 


0.073 


0.102 










in) 


(246) 


(41) 


(176) 


ADA' 
















'150 


0.000 


0.012 


0.003 


GPI-B' 








'130 


0.036 


0.024 


0.028 


'-110 


0.004 


0.000 


0.003 


'125 


0.315 


0.354 


0.372 


'-100 


0.976 


1.000 


0.971 


'118 


0.006 


0.000 


0.003 


'-50 


0.020 


0.000 


0.026 


'115 


0.081 


0.122 


0.028 


in) 


(247) 


(41) 


(176) 


'113 


0.002 


0.000 


0.003 










'110 


0.061 


0.012 


0.060 


PEPB' 








'100 


0.443 


0.452 


0.469 


'115 


0.022 


0.000 


0.006 


'90 


0.010 


0.000 


0.003 


'100 


0.974 


1.000 


0.991 


'85 


0.024 


0.000 


0.003 


'85 


0.004 


0.000 


0.003 


'78 


0.000 


0.000 


0.000 


M 


(247) 


(41) 


(176) 


'75 


0.018 


0.024 


0.028 










'65 


0.004 


0.000 


0.000 


PEPD' 








in) 


(247) 


(41) 


(176) 


'115 


0.002 


0.012 


0.009 










'100 


0.968 


0.988 


0.968 


ADH' 








'85 


0.030 


0.000 


0.020 


'-100 


0.508 


0.451 


0.566 


'75 


0.000 


0.000 


0.003 


'-75 


0.458 


0.525 


0.391 


in) 


(247) 


(41) 


(176) 


'-50 


0.028 


0.012 


0.020 










'-20 


0.006 


0.012 


0.023 


PEPS' 








in) 


(246) 


(41) 


(175) 


'105 


0.040 


0.024 


0.023 










'100 


0.958 


0.976 


0.977 


sAAT-1' 








'95 


0.002 


0.000 


0.000 


'120 
'110 


0.000 
0.134 


0.012 

0.171 


0.017 
0.120 


in) 


(247) 


(41) 


(176) 










'100 


0.856 


0.817 


0.854 


' Data are from Gold et al. (in press). 






'90 


0.010 


0.000 


0.009 










in) 


(242) 


(41) 


(175) 











66 



Fishery Bulletin 92(1), 1994 



Appendix Table 2 

Distribution of mtDNA haplotypes among red drum iSciaenops ocellatus) from the northeastern Gulf of Mexico, 
Mosquito Lagoon, Florida, and the U.S. Carolina coast. 





Composite 


North- 








Composite 


North- 








mtDNA 


eastern 


Mosquito 


U.S. 




mtDNA 


eastern 


Mosquito 


U.S. 


Haplo 


digestion 


Gulf of 


Lagoon, 


Carolina 


Haplo- 


digestion 


Gulf of 


Lagoon, 


Carolina 


type 


pattern' 


Mexico- 


Florida 


coast- 


type 


pattern' 


Mexico 1 ' 


Florida 


coast- 


1 


ABAAAAAAAAAAA 


Ill 


4 


10 


56 


AGAAAAAAAAAAA 








1 


2 


ABCCAAAAAAAAA 


in 


6 


3 


57 


AAAAAABAAAEAA 


— 


— 


1 


3 


ABBACAAAAAAAA 


11 


1 


10 


58 


BBAAAFAAAAAAA 


3 


— 


— 


4 


EAAAAABAAAAAA 


1 


— 


— 


60 


FBBAAAAAAACAA 


— 


— 


1 


5 


BAAAACBAAAAAA 


1 


— 


— 


61 


AAAAAAAADAAAA 


— 


— 


1 


6 


CBAAAAAAAAAAA 


2 


1 


1 


62 


BBBAAAAAAAAAA 


— 


— 


1 


7 


AAABAAAAAAAAA 


7 


1 


— 


64 


AAAEAABAAAAAA 


5 


— 


— 


8 


AAAAAABAAAAAA 


33 


26 


18 


66 


BBADAAAAAAAAA 


— 


— 


1 


9 


BAAAAAAAAAAAA 


19 


15 


46 


68 


BBAEAAAAAAAAA 


1 


— 


— 


10 


BBAAAAAAAAAAA 


9 


2 


4 


69 


AFAAAABAAAAAA 


4 


— 


— 


11 


AAAAAAAAAAAAA 


23 


2 


13 


70 


ACAAAAAACAAAA 


1 


— 


— 


12 


CBAAAABAAAAAA 


— 


8 


6 


76 


BAAAAAAAABAAA 


2 


— 


— 


13 


ABCAAACAAAAAA 


1 


— 


4 


77 


AB AAAG FAAAAAA 


1 


— 


— 


14 


BBFAAAAAAABAB 


— 


— 


4 


82 


ABAAAAFAAAAAA 


4 


— 


— 


15 


AAAAAABACAAAA 


— 


1 


2 


89 


BIAAAAAAAAAAA 


— 


— 


1 


16 


ACAAAAAAAAAAA 


6 


2 


4 


90 


BAAAAAGAEAAAA 


— 


1 


1 


18 


ABAACAAAAAAAA 


5 


2 


1 


91 


AAAAAAABAAAAA 


— 


— 


1 


L9 


BBAAADAAAAAAA 


— 


2 


5 


92 


ABBAFAAAAACAA 


— 


— 


1 


20 


ABBAAAAAAACAA 


— 


3 


2 


93 


AAAFGAAAEAAAA 




— 


— 


21 


BABAAAAAAAAAA 


1 1 


— 


1 


94 


AAAAAABAAAADA 




— 


— 


22 


BAAAAABAAAAAA 


4 


1 


2 


95 


BAAAAHAAAAAAC 


2 


— 


— 


23 


AAAABAAAAAAAA 


17 


6 


8 


96 


BCAAAAAAAAAAA 




— 


— 


24 


AAAAAAAAAAAAC 


5 


2 


1 


97 


H B AAAAAAAAAAA 




— 


— 


25 


ADCCAAAAAAAAA 


2 


— 


1 


98 


BAAABAAAAAAAA 




— 


— 


26 


BABABAAAAAAAA 


3 


1 


1 


99 


B B B AAAAAAAFAA 




— 


— 


27 


AACCAAAAAAAAA 


— 


5 


1 


100 


AAIAAABAAAAAA 




— 


— 


28 


ABAADAAAAAAAA 


— 


2 


2 


101 


ABCCAAFAAAAAA 




— 


— 


29 


AAAAABABAAAAA 


10 


— 


3 


106 


AAAAIAAAAAAAC 




— 


— 


31 


DBCAAAAAAAAAA 


1 


— 


— 


107 


BAAAABABAAAAA 


2 


— 


— 


35 


AB B AAAAAAAAAA 


— 


2 


4 


114 


AC B AAAAAAAAAA 


— 


1 


— 


36 


ABADAAAAAAAAA 


1 


— 


1 


121 


ABADAAAADAAAA 


1 


— 


— 


45 


BABAAABAAAAAA 


2 


— 


— 


134 


AAAAGABAAAAAA 


— 




— 


46 


ABEAAAAAAAAAA 


1 


1 


— 


135 


BBJAADAAAAAAA 


— 




— 


47 


BBAAAFAAEAAAA 


2 


— 


— 


136 


BBADAAABAAAAA 


— 




— 


48 


AAEAAAAAAAAAA 


1 


— 


— 


137 


BBAAAAACAABAA 


— 




— 


VJ 


CBBAAAAAAAAAA 


3 


— 


— 


138 


BBAAAAAAAABAB 


— 




— 


50 


BBHAAAAAAABAB 


— 


— 




139 


AAACAAAAAAAAA 


— 




— 


51 


ABCAAAAAAAAAA 


— 


1 




140 


ABACAAAAAAAAA 


— 




— 


52 


BBAAAAACAABAB 


— 


— 




141 


AACABAAAAAAAA 


— 




— 


53 


ABBAAAAAAAFAA 


2 


— 




142 


AACAAABAAAAAA 


— 




— 


54 


B.AAEAAAAAAAAA 


— 


— 




143 


ABAACAAAAAAAA 


— 




— 


55 


AHCCAAAAAAAAA 


— 


— 















' Letters (from left to right! are digestion patterns for: Nco\, Sc/I, Seal, Pvull, Spel, Xbal, Xmnl, HindlU, Stul, BamHl, EcoRV, Pstl, and 

Nsil Details regarding fragment sizes of individual digestion patterns are available upon request. 
2 Data are from Gold et al (1993). 



AbStfclCt. Microzooplankton 

retained by a 41-um mesh was 
sampled along a 50-km transect in 
the Shelikof Strait between 
Kodiak Island and the Alaska Pen- 
insula. We sampled once each year 
during spring (April-May) 1985- 
1989 using Niskin bottles closed at 
10-m depth intervals. Sampling 
was conducted near the time and 
place of peak hatching of walleye 
pollock (Theragra chalcogramma) 
larvae. We examined horizontal 
and vertical patterns of abundance 
of potential prey organisms, espe- 
cially copepod nauplii, and de- 
scribed these patterns with respect 
to the oceanography of the Strait. 
Hydrography, nutrients, chloro- 
phyll-a and net zooplankton data 
also were collected and were used 
to help interpret the microzoo- 
plankton patterns. Copepod nau- 
plii composed from 46 to 82% of all 
organisms in the formalin-pre- 
served samples. Eggs (3-35%), ro- 
tifers (up to 14%) and loricate 
tintinnids (up to 11%) were the 
next most abundant taxa. The 
abundance of microzooplankton 
varied greatly across the Strait 
and, for copepod nauplii, had 
maxima associated with the 
Alaska Coastal Current. A meso- 
scale feature in the coastal current 
appeared to influence the distribu- 
tion of microzooplankton and may 
affect feeding conditions for larval 
walleye pollock. Significant differ- 
ences in abundance of copepod 
eggs and nauplii were detected 
between some transects. The inte- 
grated, 0-60 m depth, across-strait 
average abundance of copepod 
nauplii varied from a low of 5.8 x 
10 3 nr 2 (sampled in 1985) to a 
high of 17.6 x 10 3 nr 2 (1987). The 
maximum concentration found in 
these same transects varied from 
18 to 144 L' 1 , respectively. Be- 
tween 60 and 70% of the nauplii 
sampled were of a size (>125 urn 
total length) composing approxi- 
mately 98% of the naupliar diet of 
larval walleye pollock in spring. 



Distribution and abundance of 
copepod nauplii and other small 
(40-300 jim) zooplankton during 
spring \n Shelikof Strait, Alaska* 



Lewis S. Incze 

Bigelow Laboratory for Ocean Sciences 
West Boothbay Harbor. ME 04575 

Terri Ainaire 

Bigelow Laboratory for Ocean Sciences 
West Boothbay Harbor, ME 04575 



Manuscript accepted 17 September 1993 
Fishery Bulletin 92:67-78 (1994) 



The high mortality rate of marine 
fish larvae is attributed to high 
rates of predation (Moller, 1984; 
Bailey and Houde, 1989), sensitiv- 
ity to feeding conditions (Thei- 
lacker and Watanabe, 1989) and 
interactions between these factors 
(Houde, 1987; Purcell and Grover, 
1990). The larvae of temperate 
fishes often occur during spring, 
when planktonic production is in 
early stages of its annual cycle and 
is easily disrupted or delayed by 
adverse conditions. Also, larvae 
have small search volumes and 
generally small energy reserves 
(Bailey and Houde, 1989). Thus, a 
spatial or temporal "match" or 
"mismatch" between the demand 
for larval food and its availability 
seems intuitively likely and has 
been the subject of much research 
(e.g., Lasker, 1981; Buckley and 
Lough, 1987; Cushing, 1990). The 
quest to quantify feeding relation- 
ships has led to continuing efforts 
to reduce container effects in ex- 
perimental studies (Gamble and 
Fuiman, 1987; McKenzie et al., 
1990), to improve the sensitivity of 
physiological measurements (e.g., 
Buckley et al., 1990), to understand 
the small-scale distribution of prey 
in the field (Owen, 1989), and to 
understand the role of mixing in 
enhancing or retarding interactions 



between predator and prey 
(Rothschild and Osborne, 1988; 
Davis et al., 1991). In the ocean, 
feeding takes place in a complex 
spatial array of biological and 
physical conditions. Any study of 
rate-influencing processes that af- 
fect larvae must take into account 
the distribution of these conditions 
in order to understand effects at 
the population level. 

In this paper we examine the 
springtime community of small 
zooplankton, primarily copepod 
nauplii, that may be prey for larval 
walleye pollock, Theragra chal- 
cogramma, in Shelikof Strait, 
Alaska (Fig. 1), and we report on 
the distribution and abundance of 
these organisms with respect to 
oceanographic conditions. A large 
population of walleye pollock 
spawns in the Strait in late March 
and early April, forming dense ag- 
gregations of planktonic eggs in the 
deepest part of the sea valley be- 
tween Kodiak Island and the 
Alaska Peninsula. Hatching occurs 
from middle or late April through 
early May (Kendall et al., 1987; 
Incze et al., 1989; Yoklavitch and 
Bailey, 1990). While the eggs re- 
main mostly below 150 m, larvae 

* Bigelow Laboratory Contribution No. 93- 
006. Fisheries Oceanography Coordinated 
Investigations Contribution No. 0186. 



6 7 



6 3 



Fishery Bulletin 92(1). 1994 



160° 150° 140° 

. i 



-60 N 




156° 



154° 



152 c 




156° 



154° 



Figure 1 

Top panel shows location of the study area and a 
generalized scheme of the surface circulation. 
Middle and bottom panels show Shelikof Strait and 
the sampling transect. Stations are numbered con- 
secutively beginning with 55 near the Kodiak Island 
shore; only the end and middle stations are labeled. 



are found primarily in the upper 50 m (Kendall et 
al., 1993 1 ) and have been shown to prey heavily on 
copepod nauplii during the first several weeks of 
development (Dagg et al., 1984; Kendall et al., 1987; 
Canino et al., 1991). 

The upper water column of Shelikof Strait con- 
sists of at least three distinct water types (Reed and 

1 A. W. Kendall Jr., L. S. Incze, P. B. Ortner. S. R. Cummings, 
and P. K. Brown. 1993. The vertical distribution of eggs and 
larvae of walleye pollock in Shelikof Strait, Gulf of Alaska. Sub- 
mitted to Fish. Bull. 



Schumacher, 1989). A cold, slightly freshened, tur- 
bid coastal water band of narrow width (<10 km) 
remains near the Alaska Peninsula (northern) side 
of the Strait. This water receives its signature from 
glacial melt-waters draining into Cook Inlet at the 
northern end of the Strait and thus varies season- 
ally in volume. A second water type is encompassed 
in the Alaska Coastal Current (ACC), part of a 
baroclinic current running more or less continuously 
along 1000 km of the Alaskan south coast. The ACC 
flows from northeast to southwest in a band approxi- 
mately 20 km wide through the middle portion of 
the Strait, but it has a highly variable current struc- 
ture marked by numerous baroclinic instabilities 
(Mysak et al., 1981; Vastano et al., 1992). In the 
vertical, the southward flow of the ACC induces an 
opposite bottom flow of more saline, nutrient rich 
water that enters the sea valley at the shelf edge 
south of the study area (Fig. 1; see Reed et al., 1987). 
A third water type is made up of waters from a 
mixture of sources, including outer shelf and oceanic 
intrusions. Most of this water enters from the north 
and flows the length of the Strait along Kodiak Is- 
land, but current meter measurements and satellite 
imagery show that water sometimes enters from the 
south (Schumacher, 199 1 2 ). 

The work reported here was undertaken as part 
of a multi-disciplinary program (Fisheries Oceanog- 
raphy Coordinated Investigations: FOCI) aimed at 
understanding the influence of environmental fac- 
tors on the early life history of walleye pollock 
spawned in the Strait (Schumacher and Kendall, 
1991). An extensive grid of sampling stations occu- 
pied in early May 1985, the first year of the pro- 
gram, showed that the spring bloom of large diatoms 
did not occur homogeneously throughout the Strait. 
Rather, in that year, large diatoms bloomed first in 
a band which occupied the longitudinal mid-portion 
of the Strait (Incze, unpubl. observ.). Hydrographic 
data show that this feature was in the ACC, which 
had at that time a shallower upper mixed layer than 
elsewhere in the Strait. It seemed likely, therefore, 
that conditions affecting the feeding and growth of 
larval walleye pollock would be subject to dynam- 
ics of the ACC and would differ across the Strait as 
well as through time. As part of the research pro- 
gram, a standard across-strait transect was estab- 
lished near the southern end of the Strait proper 
(about halfway up the sea valley: Fig. 1). This 
transect has been sampled with a CTD (Conductiv- 
ity, Temperature, Depth) as often as ship and re- 
search schedules have permitted. Biological sam- 



2 J. Schumacher. 1991. Pacific Marine Environmental Labora- 
tory, Seattle, WA, unpubl. data. 



Incze and Ainaire: Distribution and abundance of copepod naupln 



69 



pling begins along this transect near the time of 
larval hatching each spring and proceeds down-cur- 
rent (westward) over time. In this paper we report 
on across-shelf patterns of abundance and vertical 
distribution of copepod nauplii and other small zoop- 
lankton from 1985 through 1989 and relate these 
patterns to hydrographic conditions, chlorophyll 
concentrations, and distributions of selected taxa of 
adult female copepods. 



Materials and methods 

For convenience, we use the term microzooplankton 
to refer to small zooplankton captured and pre- 
served by methods described below. Hydrography, 
nutrients, and microzooplankton were sampled with 
a CTD and rosette sampler along a transect of sta- 
tions across Shelikof Strait, Alaska, during spring 
from 1985 through 1989 (Fig. 1) (sampling dates are 
listed in Table 2). Hydrographic (CTD) data were 
obtained near bottom at 7 stations at 7-km inter- 
vals and were processed to give 1-m averaged data 
of salinity, temperature and density. Nutrients were 
sampled at five or more stations on the transect by 
removing water samples from 10-L Niskin bottles 
tripped at standard depths of 10, 20, 30, 50, 75, and 
100 m; below this depth we sampled with lower reso- 
lution, generally at 50-m intervals, plus a sample 
near bottom. Nutrient concentrations were deter- 
mined after the cruise by using standard 
autoanalyzer techniques on frozen samples 
(Whitledge et al., 1981 3 ). Chlorophyll data were 
obtained from nutrient sampling depths in the up- 
per 100 m in 1988 and 1989. Analyses were con- 
ducted on board the vessel following methods of 
Yentsch and Menzel (1963) as modified by Phinney 
and Yentsch (1985) with 0.45-|im Millipore HA ac- 
etate filters. Microzooplankton was sampled from 
Niskin bottles were tripped at 10-m intervals from 
to 60 m in 1985 and from 10 to 60 m in other years. 
We used the same bottles as for nutrient and chloro- 
phyll samples for those depths which were common to 
all. The number of stations sampled varied over the 
years, beginning in 1985 with stations 55, 58, and 61. 
In 1986 and 1987 we included station 60. In 1988 we 
sampled all seven stations along the transect, and in 
1989 we sampled all except station 57. 

Niskin bottles were sampled for nutrients and 
chlorophyll when called for; the remaining contents 
of the bottles were filtered through small (6 x 18 cm) 



3 Whitledge, T. E., S. C. Molloy, C. J. Patton, and C. D. Wirick. 
1981. Automated nutrient analyses in seawater. Tech Rep. No. 
BNL-51398, Brookhaven Natl. Lab., Upton, NY. 



conical nets made of 41-um mesh nylon netting. 
Material retained on the netting was flushed into 
4— ounce (120 mL) glass jars by using 0.45-um fil- 
tered seawater and was preserved in a final solu- 
tion of 5% formalin:seawater. Larger zooplankton 
was sampled at all seven stations by using 60-cm 
diameter bongo samplers equipped with 333-um 
mesh nets and towed in double-oblique fashion from 
the surface to about 10 m off bottom. From 1986 
onward, a 20-cm bongo sampler with 150-um mesh 
nets was attached to the towing wire 1 m above the 
larger sampler to try to improve on the sampling of 
smaller copepods. Properties of each tow were moni- 
tored by time, wire angle from the towing block, 
mechanical flowmeters mounted across the mouth 
of each net, and a bathykymograph attached to the 
bridle of the large bongo. 

In the laboratory, each microzooplankton sample 
was filtered onto a 41-um mesh sieve, stained over- 
night in Rose Bengal, transferred to a 10-mL scin- 
tillation vial and examined in approximately 2-mL 
aliquots. Microzooplankton was analyzed by using 
a stereo dissecting microscope equipped with an 
image analysis system consisting of a high-resolu- 
tion video camera and computer software to make 
measurements and record data (Incze et al., 1990). 
The microscopist made identifications, placing each 
organism into one of thirteen categories (Table 1), 
and directed the orientation of measurements. Cope- 
pod nauplii were measured for total length (TL) and 
maximum width. Total length was the carapace 
length ("prosome"), plus the abdomen ("urosome") 
when present. The latter section often was curled 
beneath the carapace, necessitating measurement 
along a curved line. We measured the diameter of 
eggs and only the total body length of all other or- 
ganisms. In most cases the entire sample was ana- 
lyzed, but 25% of the original sample sometimes pro- 
vided adequate counts, which we established as at 
least 50 nauplii per sample. Subsampling was done 
by increasing the stored sample volume to 200 mL, 
dividing as necessary, then recondensing the mate- 
rial for examination. Subsampling was checked for 
accuracy by completely analyzing both half-portions 
from 30 samples. Final counts of microzooplankton 
were corrected for the subsampling fraction and for 
differences in the original volume of water filtered 
and are presented as number of organisms per li- 
ter. Integrated abundances (No. m~ 2 ) were estimated 
for the upper 60 m of the water column by using a 
trapezoidal algorithm. 

Vertical and horizontal patterns of micro- 
zooplankton distribution were plotted by using an 
inverse distance gridding technique ("Surfer", 
Golden Software, Inc., Golden, CO) with a grid size 



70 



Fishery Bulletin 92(1). 1994 



Table 1 

(A) Composition of microzooplankton in Shelikof 
Strait during spring, expressed as a percent of 
total organisms counted. Hyphens indicate values 
greater than zero but less than 2%; non-zero val- 
ues shown are rounded to nearest whole number. 
Shed ovisacs are from Oithona spp.; "Other" in- 
cludes infrequent and unidentified organisms. (B) 
Vertically integrated abundances of organisms are 
averaged across Shelikof Strait for each year; "All 
other" refers here to all categories from (A) com- 
bined except for those specifically listed. 

A Percent composition 



( 'ategory 



1985 1986 1987 1988 1989 



Copepod nauplii 

Other nauplii 

Invertebrate eggs 

Ovisacs 

Copepods 

Euphausiids 

Rotifers 

Tinitinnids 

Larvaceans 

Polychaetes 

Echinoderms 

Foraminifera 

Other 



50 



46 54 82 76 



25 
3 
9 



35 

2 


7 



L3 



14 

11 





B Average integrated abundance (1000s m -2 ) 
from 0-60 m 



Copepod nauplii 
Invertebrate 

eggs 
All other 
Total 



5.8 13.9 17.6 9.4 9.6 



3.0 10.4 

4.6 5.7 

13.3 30.0 



3.6 0.4 0.6 

8.6 1.9 2.6 

29.8 11.8 12.8 



set at 25 units in both the X and Y directions. The 
same technique was used for contouring CTD and 
nutrient data. A subset of contours from all three 
data types was compared by inspection to the origi- 
nal input data to look for artifacts caused by the 
contouring software. Integrated abundances of nau- 
plii across the Strait were compared for the four 
years which had late April-early May sampling 
(1985, '86, '88, '89). Data were taken from those sta- 
tions (#55, 58, 61) sampled every year in the series 
and were compared by using a non-parametric two- 
way analysis of variance (ANOVA) on ranks (also 
referred to as the Quade test: Conover, 1971). A 
multiple comparison based on ranks (Conover, 1971) 
was applied when the ANOVA showed statistically 
significant differences. 

We used the estimated abundances of adult fe- 
male copepods (No. m" 2 ) from the oblique bongo tows 



to consider possible sources of planktonic eggs and 
nauplii sampled in our study. Data are from a da- 
tabase being used to describe spatial and 
interannual patterns of major zooplankton taxa 
(FOCI Database, National Marine Fisheries Service, 
Seattle); subsampling and counting followed stan- 
dard procedures and are detailed in a series of five 
reports (e.g., Siefert and Incze, 1991 4 ). The relative 
contribution of each taxon to the standing stock of 
planktonic copepod eggs and early nauplii was esti- 
mated by using egg production rates reported in the 
literature or from unpublished data. This is simplis- 
tic, because it ignores changes in egg and naupliar 
concentrations as a function of birth rate, develop- 
ment time, and mortality, all of which may vary 
considerably. However, the calculations provide a 
rough evaluation of potential sources of nauplii in 
Shelikof Strait. Sizes of eggs and early nauplii (e.g., 
Nauplius I [NI]) were used when reports were found. 
We used the following information: Calanus 
marshallae (eggs 175-185 |im, fecundity 12 eggs 
d : [Runge, 1990 5 1; Calanus pacificus (eggs ca. 160 
urn, fecundity 38 eggs d" 1 [Runge, 19841; NI ca. 220 
Urn CL [Fulton 19721); Metridia pacifica (eggs 150 
urn [Runge, 1990 6 1; fecundity 2.5 eggs d" 1 
[Batchelder and Miller, 1989)); Pseudocalanus spp. 
(eggs ca. 110-130 urn retained in ovisacs [Frost, 
1987]; fecundity 4 eggs d" 1 [Dagg et al., 1984; Paul 
et al., 1990]; NI ca. 180 pirn CL [Fulton, 1972]). 
Jeffry Napp 7 and Kenric Osgood 8 both have found 
that Metridia pacifica held in the laboratory may 
produce eggs at higher rates, and they suggest that 
the population average at times may be several 
times greater than the rate given above. 

Results 

In this section we designate different transects by the 
year in which they were sampled but do not mean to 
imply that the differences necessarily were interannual. 
We address this distinction in the discussion section. 

Nitrate concentrations in bottom waters were 
highest in 1985, 1988, and 1989 (>25 ug-at L" 1 com- 



4 Siefert, D. L. W., and L. S. Incze. 1991. Zooplankton of Shelikof 
Strait, Alaska, April and May 1989: data from Fisheries Ocean- 
ography Coordinated Investigations (FOCI) cruises. Alaska 
Fish. Sci. Center, NOAA, Seattle, WA, 119 p. 

5 J. Runge. 1990. Insti. Maurice Lamontagne, Mont-Joli, Que- 
bec, Canada, pers. commun. 1990. 

6 J. Runge. 1993. Inst. Maurice Lamontagne, Mont-Joli, Quebec, 
Canada, unpubl. data. 

7 Jeffry Napp. Nat. Mar. Fish. Serv., Alaska Fishereis Science 
Center, Seattle, WA, pers. commun. 1993. 

8 Kenric Osgood, Dep. Oceanography, Univ. Washington, Seattle, 
WA, pers. commun. 1993. 



Incze and Ainaire: Distribution and abundance of copepod nauplii 



71 



pared to <20 ug-at L : in the other years); in sur- 
face waters they were lowest in 1987 (mostly <2 ug- 
at L" 1 ), followed by 1986 (<4 ug-at L M and 1989 (<5 



Ug-at L _1 ) (Fig. 2). Surface nitrate distributions gen- 
erally reflected density structure. Isopleths of den- 
sity (Fig. 2), salinity, and temperature show larger 



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72 



Fishery Bulletin 92(1). 1994 



volumes of high density (high salinity) bottom wa- 
ter in 1985, 1986, and 1989 compared with other 
years. The upper mixed layer generally was deep- 
est on the northern end of the transect, near the 
Alaska Peninsula, with a steeply sloping density 
gradient near the middle. The exception, in 1988, is 
discussed later. Averaged across the Strait, the up- 
per mixed layer was deepest in 1985 and shallow- 
est in 1986 and 1987. 

Observations of phytoplankton clogging sampling 
nets during the cruises showed that the spring 
bloom of large diatoms occurred latest in 1985. By 
this approximation, what probably was the major 
spring bloom in the Strait began after the first week 
of May in 1985, whereas it already was well under- 
way when we began sampling in early May 1986 
and 1989 and late April 1988. A grid of sampling 
stations that extended to the northern end of the 
Strait in 1985 showed that the bloom in that year 
formed first in a band along the middle of the Strait 
for virtually its full length of 300 km. Our grid in- 
terval was not sufficiently fine to resolve the width 
of the bloom feature, but our findings are consistent 
with a diameter <25 km. 

Our samples were dominated numerically by cope- 
pod nauplii, which composed from 46 to 827c of all 
organisms sampled along the transect over the five- 
year period (Table 1), followed in most years by cope- 
pods eggs, from 3.5 to 35 f /r. Of the remaining taxo- 
nomic categories, only a few ever contributed more 
than 57c of the total organism count: small copep- 
ods (including copepodid stages), tintinnids, rotifers, 



Nauplii 
Late April - Early May 



1.8 x 10 6 



o 1.2 x 10 6 



<d 6 x 1 o b 

E 



1 x 10 s 




Kt 



57 58 59 

1985-1989 



60 61 

7 Km 



Figure 3 

Across-strait patterns of integrated abundance (No. m' 2 ) and 
average concentration mo. L ' ) of copepod nauplii from surface 
to 60-m depth during spring at the primary time-series sta- 
tions, marked with asterisks. Upper and lower lines describe 
the maximum and minimum values observed, 1985-89. 



and polvchaete larvae. None of these ever exceeded 
15'7r of the total count. 

The integrated (0-60 m depth) abundance of 
microzooplankton at the primary sampling stations 
increased across the Strait from south to north (see 
Fig. 3 for copepod nauplii). Average abundances of 
nauplii, eggs, and all other organisms were highest 
in 1986 and 1987. For copepod nauplii, abundance 
was lowest in 1985 and intermediate in 1988 and 
1989 (Table 1). In 1985, near-surface concentrations 
averaged 869}- of those at 10-m depth. Therefore, the 
assumption of uniform concentration of organisms 
in the upper 10 m may have introduced a small 
upward bias in the integrations from 1986 onward. 
The 7-km resolution of microzooplankton obtained 
across the Strait in 1988 (Fig. 4) shows a more com- 
plex pattern of distribution than suggested by other 
transects. Specifically, comparatively large numbers 
of nauplii and other microzooplankton were found 
at stations 56 and 57, nearly equivalent to popula- 
tions at the two northern stations. Both groups of 
stations were marked by waters of lower surface 
nitrate concentration (Fig. 2) associated with flow 
around a dynamic high in the middle of the Strait 
(Fig. 5). The two groups of stations differed from 
each other in the composition of planktonic eggs 
(greater concentrations at stations 60, 61) and other 
microzooplankton (greater at 56 and 57) and in tem- 
perature and salinity. The southern "limb" of the 
anticylconic feature was about 0.1 C warmer and 
0.05 g kg~ ! more saline than the northern limb. 
Chlorophyll data show high chlorophyll-a concentra- 
tions (up to 6 ug Lr x ) and high integrated 
chlorophyll-a (140-180 mg m" 2 , 0-100 m) 
in the two limbs of the ACC surrounding 
the anticyclonic feature; the lowest chlo- 
rophyll-a (10 mg m -2 ) was found in the 
middle. 

Copepod nauplii were found mostly in 
the upper 30 m, though they extended 
deeper at some stations in 1985 and 1988 
(Fig. 6). Naupliar concentrations were 
greater in the northern half of the 
transect in 1985, 1986, and 1987; they 
were distinctly bipolar in 1988; and in 
1989 maximum concentrations of both 
nauplii (Fig. 6) and chlorophyll-a (Fig. 7) 
occurred in the center of the Strait. Maxi- 
mum naupliar concentrations encoun- 
tered at any depth across the Strait per 
transect ranged from 18 L "' in 1985 to 144 
L ' in 1987, both at 20 m depth at station 
60. Planktonic copepod eggs also occurred 
mostly in the upper 30 m but exhibited a 
variety of across-shelf patterns that were 



30 



20 E 



Incze and Ainaire: Distribution and abundance of copepod nauplii 



73 



not always the same as those found for nau- 
plii. Maximum egg concentrations ranged 
from 2.2 L" 1 in 1988 (at 30 m depth) to 
45 L" 1 in 1986 (10 m depth), both at station 
59. Most eggs and nauplii were in the up- 
per mixed layer. Since sampling in 1987 oc- 
curred in late May, the relatively high abun- 
dance of nauplii may be attributed to time 
of year. Consequently, a statistical compari- 
son between transects focussed on the other 
four years, which were sampled the last 
week of April and first week of May. This 
time period is close to the time of peak lar- 
val hatching. Abundance was statistically 
different among transects (Quade test 0.025 
< P < 0.05). The lowest (1985) and highest 
(1986) concentrations were significantly dif- 
ferent at a = 0.05; the intermediate concen- 
trations of 1988 and 1989 differed from 
those in 1985 (but not 1986) at a = 0.10 
(Multiple comparisons of ranks). 

The lengths of sampled nauplii showed 
positively skewed frequency distributions 
with peak abundance between 100 and 150 
urn TL in all years and nearly identical cu- 
mulative distribution functions (Fig. 8). 
Median size differed by less than 15 urn 
among years and averaged 140 urn during 
the five-year period. The average length: 
width ratio of nauplii measured in this study 
was 2.2, with a standard deviation of 0.1 
(rc = 1500). Consequently, our mesh, 41 urn on 
a side and 58 urn on the diagonal, should 
have retained some nauplii >90 urn long and 
all nauplii >128 urn. Our data showed a 
steep decline in frequency of nauplii with 
length <110 um, between the above esti- 
mates, and width <50 um, corresponding to 
the relationship 110/2.2 = 50. Most of the 
nauplii did not have urosomal segments, so 
total length and maximum width are equiva- 
lent to prosome length and width for most 
of our data. 

The abundance and size distribution of 
eggs differed substantially between years 
(Fig. 8). The greatest number (and smallest median 
size [ca. 75-um diameter]) of planktonic eggs was 
present in 1986; the fewest eggs occurred in 1988, 
when median size was the largest (ca. 165 urn). 

Abundances of potentially significant contributors 
to the standing stocks of copepod eggs and nauplii 
are given in Table 2. Among the taxa of interest, 
Calanus pacificus had low adult female numbers 
because most individuals were in copepodid stage 5 
(C5) during spring. Other adult female copepods 



Chl-a (mg m 2 ) 





20 


177 


10 


142 




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Figure 4 

Mean number of nauplii and total microzooplankton per li- 
ter in the upper 60 m across the study transect in April 1988 
(top panel), viewed looking westward. Numbers at the top 
of the panel show integrated (0-100 m) chlorophyll-a con- 
centrations (mg m -2 ). Temperature (°C) and salinity (g kg -1 ) 
are shown in the middle and bottom panels, respectively. 
Data can be compared with nutrient distributions (Fig. 2), 
dynamic topography (Fig. 5), and depth distributions of 
nauplii (Fig. 6). 



were broadly distributed across the Strait, but the 
maximum concentration of each taxon occurred in 
the northern half (among stations 58-61) in all but 
one instance. The across-Strait patterns of low and 
high abundances within species were similar from 
year to year and statistically significant (Spearman 
rank correlation test, P<0.05). The shift in mesh 
sizes for Pseudocalanus spp. collections limits the 
between-transect comparisons that can be made. 
(Note that there are interspecific differences within 



74 



Fishery Bulletin 92[ I). 1994 



57°30 



;-»T llll 



Alaska 
Peninsula 




155°30' 



154 D 30 



Longitude ( W ) 



Figure 5 

Contours of 0-150 m dynamic height in western Shelikof 
Strait during April 1988. Solid circles show locations of CTD 
stations. The study transect is the farthest northeast sec- 
tion. Open circles denote those transect stations with the 
highest microzooplankton standing stocks (cf. Figs. 4, 6). A 
dynamic high (H) and low (L) are labelled; arrows show 
inferred flow. 



the genus that prohibit any simple correction for 
different mesh collections: see Frost, 1987.) Within 
these limitations, data for 1985 and 1986 (333 pm) 
were statistically different (Wilcoxon signed rank 
test, P=0.076), whereas the multi-year comparison 
for early spring samplings (1986, 1988, 1989: 150 
pm mesh) showed no statistically significant differ- 
ences (Quade test, a= 0.05). Among early spring 
values, there were no statistically significant differ- 
ences in abundance of Metridia spp.. 

Discussion 

The method of sampling and preservation used in 
this study under-represented smaller components of 
the microzooplankton (James, 1991) but was ad- 
equate to capture the majority of prey items of lar- 
val walleye pollock based on prey sizes reported 
from earlier studies of Clarke (1984: Bering Sea), 
Nishiyama and Hirano (1983, 1985: Bering Sea), 
Dagg et al. (1984: Bering Sea); and Kendall et al. 
(1987: Shelikof Strait). For small larvae of 5-10 mm 
standard length (SL) in those studies, copepod nau- 
plii composed the majority of items found in larval 
stomachs. They also made up the bulk of estimated 



volume or carbon content of prey when these 
values were calculated (Incze et al., 1984; 
Nishiyama and Hirano, 1983). The 10-m 
vertical resolution of our sampling method 
almost certainly failed to detect the highest 
concentrations of prey available to larval 
walleye pollock under some conditions, such 
as in small patches (Owen, 1989), but prob- 
ably reflects adequately the average abun- 
dances found at different depths in the wa- 
ter column, in different sections across the 
Strait and in different transects. 

Size-frequency distributions of sampled 
nauplii and dimensions of the sampling 
mesh suggest that there was virtually com- 
plete retention of nauplii with total length 
> 125 pm. In most cases these measure- 
ments were carapace ("prosome") lengths. 
Unpublished data from stomach content 
studies (Canino, 1992 9 ) show that ca. 98% 
of the nauplii consumed by larval walleye 
pollock collected during our cruise in May 
1989 had carapace length > 125 pm. Be- 
tween 60 and 70% of the nauplii in our 
samples were of this size (Fig. 8). 

Concentrations and integrated abun- 
dances of nauplii differed across Shelikof 
Strait in patterns that appear to be related 
to circulation features. Our data indicated 
that standing stocks and maximum concen- 
trations of copepod nauplii in spring were greatest 
in the ACC, which is also where greatest chloro- 
phyll-o concentrations occurred (latter data for 1988, 
1989; cf. Figs. 4, 6, 7). The lowest naupliar concen- 
trations of the early spring samplings occurred in 
1985, which had the weakest stratification. In gen- 
eral, nauplii were most abundant at 20-m depth 
except in 1988, when maximum concentrations oc- 
curred at 30-m depth in the deeper mixed perimeter 
of the anticyclonic feature. The lowest standing 
stock of nauplii coincided with the latest apparent 
phytoplankton bloom in 1985, but we cannot deter- 
mine if lower individual copepod egg production 
rates or lower standing stocks of copepods were re- 
sponsible because we lack adequate collections ( 150— 
pm mesh) of Pseudocalanus spp. in 1985. Alterna- 
tively, the low naupliar standing stocks could have 
been due to higher predation, but our data show 
that springtime populations of predators were gen- 
erally low and were similar among years. 

Our data suggest that the distribution of copepod 
nauplii and some other microzooplankton across 



9 M. Canino. 1992. Natl. Mar. Fish. Serv., Alaska Fisheries Sci- 
ence Center, Seattle, WA, unpubl. data. 



Incze and Ainaire: Distribution and abundance of copepod nauplii 



75 



naupui (So. r 1 ) 
1985 (R=0-18;CI=2) 

Distance (km) 




1986 (R=1-56;CI=4) 

3 y \0 JO ' 




1987 (R=1-144;CI=10) 




1988 (R=0-26; Cl=2) 

10 » 




Figure 6 

Contour plots of naupliar concentrations (no. Lr 1 ) 
across Shelikof Strait during spring. Numbers in 
parentheses after the year (upper left of each plot) 
show the range (R) of data and the contour inter- 
val (CI) used in plotting. Transects are viewed look- 
ing westward. 



Shelikof Strait were subject to the influence of 
baroclinic instabilities. The timing and rotational 
sense of these instabilities therefore may have a 
large influence not only on the distribution of wall- 
eye pollock larvae themselves (Reed et al., 1989; 
Incze et al., 1990; Vastano et al., 1992), but also on 
the feeding conditions they experience. For example, 
the feature sampled in 1988 covered a substantial 



Chlorophyll - a (ug I 1 ) 

Distance (km) 

20 JO 

T" 




Figure 7 

Chlorophyll-a distributions across Shelikof Strait, 
May 1989, looking westward (data may be compared 
with nutrient and hydrographic structure in Fig. 2 
and naupliar concentrations in Fig. 6). 



portion of the main spawning and hatching area. 
Although we do not have extended observations of 
this feature, Vastano et al. (1992) showed that eddy- 
like features may remain near the hatching area for 
as long as two weeks, a substantial portion of the 
hatching period (Yoklavitch and Bailey, 1990). If 
walleye pollock larvae migrate vertically into the 
center of a dynamic high after hatching, then the 
amount of time that passes before they are advected 
into better feeding conditions (in this case at the 
periphery of the high ) may be important to early 
larval feeding and growth. 

The average integrated abundance of copepod 
nauplii across the Strait was different for the vari- 
ous transects. The maximum values that were seen 
in 1987 probably can be attributed to the compara- 
tively late sampling of that year. However, among 
the four years with similar timing of transect sam- 
pling, there remained statistically significant differ- 
ences that may have been important to hatching 
walleye pollock larvae (see Canino et al., 1991, for 
feeding conditions and larval RNA/DNA ratios). 
Since hatching takes place over a relatively short 
time period (Yoklavitch and Bailey, 1990), the phas- 
ing of hatching and upper layer conditions may play 
an important role in establishing the larval year 
class. Unfortunately, we do not know how long the 
observed conditions persisted in each year relative 
to the population hatching time or to other require- 
ments of the early feeding period in larval develop- 
ment. Advection (Incze et al., 1989) and short-term 
fluctuations in mesoscale circulation (Vastano et al., 
1992) may cause conditions in the Strait to change 
quickly, requiring more frequent sampling and im- 
proved techniques to rapidly assess prey distributions. 

Nauplii that were most abundant in the diet of 
larval pollock must have come from copepods large 
enough to be retained by mesh sizes used on the 



76 



Fishery Bulletin 92(1), 1994 



1986 
nauplii 




500— 

>> 
U 

g 400-| 

3 
ST 300 

1*1 200— 



100— 





1986 



rn-i-! — -^ 



50 100 150 200 260 300 



Size ((im) 



C.D.F. 



1.0 






1985 


0.8 






y£^\% 


0.6 




// 


nauplii 


0.4 


- 


/'" 




0.2 


- 






0.0 


1 


y s 


i i i 



i 

l 

14- 

13- 

12 

11 

10- 



5 
4 
3 
2 
1 





50 100 160 200 260 300 



1988 
eggs 



JL 



60 100 160 200 260 300 

Size (um) 



Figure 8 

Size-frequency distribution of nauplii and eggs. Graph in upper left shows size frequency 
of nauplii from 1985. Graph in upper right shows the full range of size distributions of 
nauplii by comparing the cumulative distribution functions (CDF) for the two extremes, 
1985 and 1986. Size distributions of eggs are shown in the two lower graphs for years 
with the smallest (1986) and largest (1988) eggs. Note changes in frequencies shown on 
the various ordinates. 



bongo samplers (Table 2). Based on the average 
abundance and fecundity (see Methods) of adult fe- 
male copepods, the approximate contribution of each 
species to the daily production of NI would be: 
Pseudocalanus spp., >75% ; Metridia pacifica, 18%; 
Calanus marshallae, 49r; and Calanus pacificus, 
<1%. These percentages are useful only for the rela- 
tive scaling they permit; many factors may influence 
copepod reproduction rates, and rates of develop- 
ment and mortality will influence further the total 
standing stock of nauplii contributed by each spe- 
cies. These results agree with those of Dagg et al. 
(1984) with respect to the importance of Pseudo- 
calanus spp. naupliar production for larval walleye 
pollock feeding. Our results differ in the greater 
inferred role of Metridia spp., probably because of 
the deep waters of the Shelikof sea valley compared 



with the Bering Sea shelf where Dagg and his co- 
authors worked. The numerous small nauplii <120 
(im that we sampled are from unknown sources. The 
abundance and fecundity of M. pacifica suggest that 
they were significant contributors to populations of 
planktonic eggs and that Calanus marshallae plays 
a lesser role. A large number of small planktonic 
eggs <150-um diameter are not accounted for by the 
adult female copepods retained by our nets. 

Acknowledgments 

This research was supported by the U.S. National 
Oceanic and Atmospheric Administration through 
the FOCI program. We thank J. Schumacher for 
providing CTD data, M. Canino for sharing unpub- 
lished data on larval walleye pollock diet, K. 



Incze and Ainaire: Distribution and abundance of copepod nauplii 



77 









Table 2 








Abundance (no. m~ 2 ) of adult female copepods on a transect across western Shelikof Strait during spring. 
Data are listed vertically showing mean, (standard deviation) and range. Metridia pacifica is Metridia pacifical 
M. lucens; unidentified Metridia spp. are not included in this tally. Hyphens indicate absence of data. 


Taxon and mesh size 








Year and day 






1985 
(3 May) 


1986 

(3 May) 


1987 
(19 May) 


1988 
(27 Apr) 


1989 
(10 May) 


Pseudocalanus spp. 
150 |im 




— 


14,183 

(6,523) 

6,758-18,994 


41,058 

(25,527) 

6,108-78,976 


13,634 

(4,128) 
7,846-20,316 


8,450 

(4,026) 

2,870-12,563 


Pseudocalanus spp. 
333 pm 




9,119 

(4,767) 

2,509-16,110 


16,232 

(8,295) 
7,848-30,573 


33,098 

(19,398) 

6,273-51,729 






Calanus marshallae 
333 pm 




130 
(146) 
0-431 


82 
(72) 
0-211 


610 
(532) 
0-1,343 


125 
(93) 
0-238 


618* 

(786) 

0-2,196 


Metridia pacifica 
333 pm 




5,082 

(4,128) 

68-11,899 


3,168 

(1,956) 

24-6,340 


9,537 

(5,570) 

288-5,715 


3,211 

(1,626) 

288-5,715 


2,713 
(2,549) 
0-6,945 


Calanus pacificus 
333 pm 




15 
(27) 
0-73 


2 

(4) 
0-9 





28 
(61) 
0-164 


133 
(228) 
0-521 



McCauley for early work with microzooplankton 
sorting, D. Siefert for processing net zooplankton 
samples and our many sea-going colleagues for their 
help in the field. Our work benefitted from discus- 
sions with A. Kendall, K. Bailey, J. Schumacher, and 
J. Runge, and our manuscript from comments by M. 
Mullin, J. Napp, and an anonymous reviewer. 

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Fishery Bulletin 92(1), 1994 



Gamble, J. C, and L. A. Fuiman. 

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Owen, R. W. 

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Abstract. Distribution and 

size during their first summer at 
sea were determined for juvenile 
salmon (Oncorhynchus spp.) 
caught in oceanic waters off north- 
ern British Columbia and South- 
east Alaska, and in marine waters 
within the Alexander Archipelago 
of Southeast Alaska. More than 
10,000 juvenile salmon were 
caught in 252 purse-seine sets 
during August 1983, July 1984, 
and August 1984. Distribution was 
patchy; juvenile salmon were 
highly aggregated, rather than 
dispersed randomly. Distribution 
and size of pink salmon 
(O. gorbuscha), sockeye salmon (O. 
nerha), and chum salmon (O. keta) 
were similar but differed from 
coho salmon (O. kisutch). Chinook 
salmon (O. tshawytscha) were ex- 
cluded from most analyses because 
few were caught. Sizes were con- 
sistent with the concept that juve- 
nile salmon in more northern and 
seaward locations had been at sea 
longer than those in more south- 
ern and inshore locations. Juvenile 
salmon migration up the Pacific 
coast did not peak in abundance 
off Southeast Alaska until August; 
movement from inside to outside 
waters was not complete by the 
end of August. The migration band 
of juvenile salmon in outside wa- 
ters of Southeast Alaska extended 
beyond the continental shelf to at 
least 74 km offshore, twice the dis- 
tance previously reported. 



Marine distribution and size of 
juvenile Pacific salmon in 
Southeast Alaska and 
northern British Columbia 

Herbert W. Jaenicke 

Adrian G. Celewycz 

Auke Bay Laboratory, Alaska Fisheries Science Center 

National Marine Fisheries Service. NOAA 

1 1305 Glacier Highway. Juneau. Alaska 99801-8626 



Manuscript accepted 28 September 1993 
Fishery Bulletin 92:79-90 (1994) 



The general migratory movements 
of Pacific salmon (Oncorhynchus 
spp.) during their first year at sea 
have been described (Hartt and 
Dell, 1986), but little information is 
available on the seaward migration 
of juvenile salmon from the inside 
waters of Southeast Alaska into the 
Gulf of Alaska. Salmon moving sea- 
ward from streams inside South- 
east Alaska pass first through the 
complex waterways of the 
Alexander Archipelago, the "inside 
waters" of Southeast Alaska. Upon 
entering the Gulf, these salmon 
either occupy outer coast inlets or 
move into exposed outside waters. 
Salmon entering exposed outside 
waters either migrate north along 
the coast or move progressively far- 
ther offshore (Hartt and Dell, 
1986). Determining when and at 
what size juvenile salmon from 
Southeast Alaska utilize different 
habitats during their seaward mi- 
gration to the Gulf may facilitate 
understanding the high mortality 
during their first few months at sea 
(Parker, 1968; Bax, 1983; Furnell 
and Brett, 1986). 

Our goal was to ascertain the 
distribution and migration of juve- 
nile Pacific salmon during their 
first summer at sea after they 
leave nearshore estuarine habitats. 



Specific objectives were 1) to deter- 
mine relative distribution, abun- 
dance, and size of juvenile salmon in 
exposed outside waters, in protected 
waters adjacent to the outer coast, 
and in the inside waters of Southeast 
Alaska, and 2) to compare abun- 
dance and size of juvenile salmon in 
outside waters of Southeast Alaska 
and northern British Columbia. 



Methods 

Study area and time 

The study area extended from 
Lituya Bay, Southeast Alaska, to 
the northern end of Vancouver Is- 
land, British Columbia (Fig. 1). 
Three major habitats were 
sampled: 1) outside waters (the 
North Pacific Ocean and Gulf of 
Alaska adjacent to the outer coast 
of Southeast Alaska and British 
Columbia); 2) outer coast inlets 
(protected waters along the outer 
coast of Southeast Alaska); and 3) 
inside waters (marine waters 
within the Alexander Archipelago). 
Southeast Alaska was further di- 
vided at lat. 56°N into a northern 
and southern region for some 
analyses. Fishing effort was con- 
centrated in the northern region of 
Southeast Alaska (Fig. 1). 



79 



80 



Fishery Bulletin 92(1), 1994 




Figure 1 

Locations seined in Southeast Alaska and British Columbia 
in 1983 and 1984. The delineation between northern and 
southern Southeast Alaska is indicated by the dotted line 
(running along 56°N lat.). 



We sampled in Southeast Alaska during three 
periods: 6 August-3 September 1983 (hereafter des- 
ignated August 1983), 9-24 July 1984, and 1-30 
August 1984. Sampling in British Columbia was 
conducted 1-6 July 1984. 

Survey stations in outside waters were located 
along transects perpendicular to shore (Fig. 1). The 
nearshore station of each transect was as close to 
land as net depth and safety permitted. Stations 
were usually sampled progressively offshore at 5.6 
km (3 nautical miles [nmi]) intervals in 1983 and 
at 9.3 km (5 nmi) intervals in 1984. Sampling gen- 
erally did not extend beyond 37 km offshore except 
in Southeast Alaska in August 1984, when transects 



extended as far as 74 km offshore. Distances 
are rounded to the nearest 1 km in the text. 
In large passages in the inside waters, sets 
were often made along transects near the en- 
trance to outside waters (Fig. 1). Multiple sets 
were also made in clusters in the larger inlets. 

Gear 

Stations were sampled with table and 
drum seines as described by Browning 
(1980). The 28-m NOAA RV John N. Cobb 
fished a table seine in August 1983 and 
August 1984; the 24-m FV Bering Sea 
fished a drum seine in July 1984. Sets were 
made at predetermined locations without 
reference to visual or instrument sightings 
of fish. All sets were round hauls: the net 
was set in a semi-circle, held open 3—5 
minutes, closed, pursed, and retrieved by 
means of a hydraulic power block (table 
seine) or a hydraulic roller (drum seine). 
Only catches from effective seine sets are 
listed (Table 1). 

Although the seines differed in size, 
mesh, and area enclosed, the two nets were 
assumed to be comparable in their ability 
to capture juvenile salmon. The table seine 
was 455 m long; depth tapered from 37 m 
in the wing to 11 m in the bunt; web sizes 
(stretch mesh) were 89 mm and 57 mm in 
the wing, and 25 mm in the bunt. The 
drum seine was 503 m long, 46 m deep, and 
had 32-mm mesh in the wing, and 25 mm 
in the bunt. Depths fished were assumed 
to be adequate for sampling juvenile pink 
(O. gorbuscha), chum (O. keta), sockeye (O. 
nerka), and coho (O. kisutch) salmon, which 
usually occupy the upper 10 m of the wa- 
ter (Manzer, 1964; Godfrey et al., 1975; 
Hartt, 1975). To compensate for the larger 
surface area enclosed by the drum seine 
(20,150 m 2 ) compared to the table seine (16,467 m 2 ), 
drum seine catches (July 1984) were reduced during 
analyses by 18.3% to standardize the catch per unit 
of effort (CPUE). This standardization caused the July 
1984 catches reported to be sometimes less than the 
number of fish measured for size that period. 



Catch processing and analysis 

The catch was processed aboard ship and in the 
Auke Bay Laboratory. The number of juvenile 
salmon captured in each set was counted if the catch 
was small (i.e., <100 fish) or estimated gravimetri- 
cally if the catch was large. Up to 100 salmon from 
each set were preserved in 10% formalin in seawater 



Jaenicke and Celewycz: Marine distribution and size of juvenile Pacific salmon 











Table 1 












Number of 


uvenile salmonid 


s caught by species 


, period, and hg 


bitat. All 


seining occurred in 


Southeast Alaska 


(SE AK) except in July 1984 


when the 


outside 


waters of Briti 


sh Colum 


bia (B.C.) were alsc 


sampl 


ed. 












Number of fish caught 












dumber 






























Period 


Habitat 


of sets 


Pink' 


Churn 1 ' 


Sockeye 1 ' 


Coho J 


Chinook 5 


All species 


August 1983 


Inside waters 


54 


2,011 


385 


178 


201 


3 




2,778 




Outer coast inlet 


27 


680 


85 





23 


1 




789 




Outside waters 


8 


20 


2 


9 


27 







58 




Subtotal 


89 


2,711 


472 


187 


251 


4 




3,625 


July 1984 


Inside waters 


18 


91 


16 


17 


197 


19 




340 




Outer coast inlet 


14 


10 


2 





24 







36 




Outside waters 




















B.C. 


21 


573 


189 


581 


33 


5 




1,381 




SE AK 


33 


181 


34 


109 


28 


1 




353 




Subtotal 


86 


855 


241 


707 


282 


25 




2,110 


August 1984 


Inside waters 


37 


1,850 


163 


23 


375 


23 




2,434 




Outer coast inlet 


4 





12 





3 


i) 




15 




Outside waters 




















<37 km seaward 


26 


866 


152 


171 


128 


5 




1,322 




>37 km seaward 


l(i 


522 


63 


119 


26 







730 




Subtotal 


77 


3,238 


390 


313 


532 


28 




4,501 


All 


Inside waters 


109 


3,952 


564 


218 


77.3 


45 




5,552 




Outer coast inlet 


45 


690 


99 





50 


1 




840 




Outside waters 


98 


2,162 


440 


989 


242 


11 




3,844 




Total 


252 


6,804 


1,103 


1,207 


1,065 


57 




10,236 


; Oncorhynchus gorbuscha. 


















2 0. kela. 




















3 0. nerka. 




















4 0. kisutch. 




















5 0. tshawytsc 


ha 



















for later species identification and size measure- 
ments (fork length [FL] to nearest mm). If more 
than 100 juvenile salmon were captured in a set, the 
excess fish were released alive. 

Graphs (Chambers et al., 1983) and exploratory 
data analysis (Tukey, 1977) were used to present 
catch data because the data had a nonnormal dis- 
tribution with values clumped at zero (many seine 
sets did not capture juvenile salmon). Transforma- 
tions of catch data were ineffective in making the 
distribution more symmetrical. Quantile plots 
(Chambers et al., 1983), which show individual 
catches from smallest to largest, were used to de- 
scribe the statistical distribution of catches of each 
species. Chinook salmon (O. tshawytscha) were ex- 
cluded from the remaining analyses because few 
were caught. Morisita's Index of Aggregation 
(Morisita, 1959; Poole, 1974) was used to test 
whether each salmon species was randomly dis- 
persed or aggregated in marine waters of Southeast 
Alaska. 



Morisita's index is defined as 



N 



£«,(«,-!> 



i l 



rc(n-l) 



N, 



where N is the number of samples, n { is the num- 
ber of individuals in the z'th sample, and n is the 
total number of individuals in all samples. The sig- 
nificance of I & is tested with the Ftest described by 
Poole (1974). Spearman's rho (p) correlation test 
(Daniel, 1978) was used to measure association be- 
tween each possible pairing of the four main species 
caught (pink, chum, sockeye, and coho salmon). 

For comparisons, catch data were split into cells 
by 1) species, 2) habitat (outside waters, outer coast 
inlets, and inside waters), 3) region (northern South- 
east Alaska, southern Southeast Alaska, and Brit- 
ish Columbia), and 4) time period (August 1983, 
July 1984, and August 1984). CPUE was used as an 
index of abundance; frequency of occurrence (FO) 



82 



Fishery Bulletin 92(1), 1994 



was used as a measure of presence of juvenile 
salmon. 

Five null hypotheses were tested during fish 
length analyses of the four species. The first four 
hypotheses stated that size of a species did not dif- 
fer for fish from 1) outside and inside waters, 2) 
outside waters >37 km offshore and <37 km offshore, 
3) northern and southern waters, and 4) July and 
August of 1984. The alternate hypotheses stated 
that fish were larger in 1) outside than inside wa- 
ters, 2) outside waters >37 km offshore than outside 
waters <37 km offshore, 3) northern than southern 
waters, and 4) August than July of 1984. The fifth 
hypothesis stated that length did not differ among 
species caught within each period. 

A number of one-tailed, two-sample ^-tests were 
conducted under null hypotheses 1-4. Only cells 
that varied in one dimension were directly com- 
pared. (For example, under the hypothesis that 
mean sizes of fish from northern and southern wa- 
ters did not differ, the mean lengths of pink salmon 
in the inside waters of northern and southern South- 
east Alaska in August 1983 could be compared be- 
cause the difference between these two cells was in 
only one dimension — north versus south. ) Each pos- 
sible pairwise comparison under one of the hypoth- 
eses was treated as a separate, single, and indepen- 
dent test, and all comparisons were equally weighted. 
No ^-tests could be conducted if one cell had only one 
fish length. For the overall probability statement, the 
following statistic was used (Winer, 1971): 



22>" 



where it, 



lnP. 



Under the hypothesis that the observed probabili- 
ties were a random sample from a population of 
probabilities having a mean of 0.50, the % 2 statistic 
has a sampling distribution which is approximated 
by the x 2 distribution having 2k degrees of freedom, 
where k is the number of comparisons (Winer, 1971). 
For size hypothesis 5 (no difference in mean fork 
length among salmon species), ANOVA was applied 
by pooling observations for each species from all 
habitats and regions. In effect, the pooled species 
length distribution is a weighted sum of the compo- 
nent distributions represented by the individual 
samples. Mean lengths of different species were 
compared separately for each period. If the overall 
F-test was significant, all possible species compari- 
sons within a period were tested with two-tailed t- 
tests. Experimentwise error was controlled at a = 
0.05 by adjusting the critical value for each t-test 
to a = 0.0085, by using the Dunn-Sidak method 
(Sokal and Rohlf, 1981). 



Results 

Total catch 

Over 10,000 juvenile Pacific salmon were captured 
in 252 seine sets during the three sampling periods 
(Table 1). The catch consisted of 66% pink salmon, 
11% chum salmon, 12%' sockeye salmon, 10% coho 
salmon, and 1%> chinook salmon. Pink salmon were 
the most abundant species (CPUE=27), with 6,804 
caught. Chinook salmon were the least abundant 
species (CPUE=0.23), with only 57 caught. 

Statistical distribution of catch 

Catch distribution of juvenile salmon was extremely 
patchy. None were caught in 22% of the sets; more 
than half were captured in 5% of the sets. Plotting 
catch abundance against quantiles illustrated that 
the underlying statistical distribution for each spe- 
cies was clustered around zero (Fig. 2). Chinook 
salmon had the lowest FO in catches ( 12%), followed 
by sockeye salmon (32%), chum salmon (397/ ), pink 
salmon (45%), and coho salmon (54%). Coho salmon 
(median catch=l) was the only species with a me- 
dian catch >0. 

Juvenile salmon had highly aggregated distribu- 
tions. Morisita's Index of Aggregation (I & ) was sig- 
nificantly (P<0.001) greater than 1, indicating all 
species had aggregated distributions in each habi- 
tat and for all habitats pooled (Table 2). 

Species associations 

Pink, chum, and sockeye salmon catches were 
closely associated with each other. Catches of pink, 
chum, and sockeye salmon were positively and sig- 
nificantly (P<0.05) correlated (Table 3). In contrast, 
coho salmon abundance was not correlated with that 
of other salmon (Table 3). 

Abundance 

By habitat In Southeast Alaska and British Co- 
lumbia combined, pink salmon were the most abun- 
dant species in each habitat (Table 1). The total pink 
salmon catch exceeded the catch of each of the other 
species by six times or more. 

In Southeast Alaska, the CPUE of juvenile pink, 
chum, coho, and chinook salmon was greater in in- 
side waters than in outside waters (Fig. 3), whereas 
sockeye salmon were more abundant in outside 
waters than inside waters (Fig. 3). For each species, 
the lowest CPUE and FO were in the outer coast 
inlets; sockeye salmon were never captured in an 
outer coast inlet (Fig. 3). The FO of pink, chum, and 
sockeye salmon was higher in outside than inside 
waters; the opposite was true for coho salmon (Fig. 3). 



Jaenicke and Celewycz: Marine distribution and size of juvenile Pacific salmon 



83 









1500 - 


,.i 






1000 - 


Pink talmon 






500 - 


..---"'" , _J 






100 - 


Chum talmon ...-■"""' 




~ 50- 

£ 
B 

O 400 - 


| . — r^ 








fe 


Sockeya talmon 






a 








E 200- 

3 

c 


...-•'""* 






£ 

O J 

n ioo - 


1 _, J 




.A 





Coho talmon 




50 - 


,- '■ , _J 




10 - 








5 - 


Chinook salmon 

, • . J 






° 6 0.2 0.4 I 0.6 08 1 


median 


Fraction of ordered data 


Figure 2 


Quantile plots of abundance of the five species of 


juvenile Pacific salmon (pink, Oncorhynchus 


gorbuscha; chum, O. keta; sockeye, 0. nerka; coho, 


0. kisutch; chinook, 0. tshawytscha) caught in 252 


purse-seine sets in Southeast Alaska in 1983 and 


1984 and in British Columbia in 1984. The ranked 


catches are from the smallest (0) to largest (1) on 


the X axis. A theoretical normal distribution is in- 


dicated by the dotted lines. 



By distance offshore in outside waters Dis- 
tribution of juvenile salmon varied by distance off- 
shore. Substantial numbers offish were captured up 
to the maximum distance fished offshore (74 km, 
Fig. 4A). At intervals offshore, abundance and pres- 
ence of each species is shown by the 3RSSH 
smoothed (Tukey, 1977) natural logarithms (In) of 
CPUE (Fig. 4B) and smoothed FO (Fig. 4C) respec- 
tively. Highest In CPUE of pink and chum salmon 
was near the center of the distance fished offshore 
(Fig. 4B). The transformed CPUE of sockeye salmon, 
the least abundant species nearshore (Fig. 4B), was 
greatest 37-74 km offshore, indicating they may 
have been abundant beyond 74 km. The In CPUE 
of coho salmon suggests it was the least abundant 
species beyond 56 km (Fig. 4B). 



Table 2 
Morisita's Index of Aggregation (J 8 ) and the asso- 
ciated F-value for seine catches of juvenile pink, 
chum, sockeye, and coho salmon taken in indi- 
vidual habitats (inside waters, outer coast inlets, 
outside waters I and all these habitats pooled in 
Southeast Alaska in August 1983, July and Au- 
gust 1984. Dashes indicate no fish captured. 



Salmon 








species 


Habitat 


h 


F 


Pink' 


Inside waters 


20.0 


695.7* 




Outer coast inlet 


10.7 


153.0* 




Outside waters 


3.6 


54.9* 




All habitats pooled 


18.5 


474.5* 


Chum 2 


Inside waters 


13.6 


66.6' 




Outer coast inlet 


9.0 


18.7* 




Outside waters 


5.4 


15.3* 




All habitats pooled 


12.7 


47.6* 



Sockeye 3 Inside waters 

Outer coast inlets 



Coho-' 



11.8 



22.7* 



Outside waters 


15.1 


23.2 


All habitats pooled 


9.5 


24.2 


Inside waters 


4.4 


25.1 


Outer coast inlets 


2.9 


3.1 


Outside waters 


7.8 


19.5 


All habitats pooled 


6.2 


24.3 



F-value is significant for P < 0.001. 
7 Oncorhynchus gorbuscha. 

2 0. keta 

3 O. nerka. 

4 O. kisutch. 







Table 


3 




Spearman's rank cc 


rrelati 


on coefficient (p) test of 


pair rankings 


of juvenile 


salmon species catches 


taken during 


252 


separate 


sets in Southeast 


Alaska and British Columbia 




Comparison of 








Correlation between 


species of 








species pair rankings 


salmon 








(pi 


Pink'/Chum 2 








+0.75* 


Pink/Sockeye' 








+0.68* 


Pink/Coho 4 








+0.14 


Chum/Sockeye 








+0.55* 


Chum/Coho 








+0.13 


Sockeye/Coho 








+0.11 


Significant association at P < 


0.05 


. with rejection criteria 


adjusted for mu 


tiple comparisons. 




1 Oncorhynchus gorbusc 


ha. 






- keta. 










 7 0. nerka. 










' O kisutch 











84 



Fishery Bulletin 92(1). 1994 



40 



30 



Outside waters 
Outer coast inlets 
Inside waters 




Pink 



Coho 



Chum Sockeye 

Salmon species 

Figure 3 

Catch per unit of effort (CPUE) and frequency of occurrence of 
juvenile salmonids (pink, Oncorhynchus gorbuscha; chum, O. keta; 
sockeye, O. nerka; coho, O. kisutch; in outside waters (77 sets), 
outer coast inlets (45 sets), and inside waters ( 109 sets) in South- 
east Alaska in 1983 and 1984 combined. 



Pink and chum salmon FO was lowest nearshore, 
then increased and stabilized mid-distance offshore, 
around 37 km (Fig. 4C). Pink salmon were caught 
in all sets beyond 37 km and had the highest FO of 
all species; sockeye salmon FO remained constant 
2-74 km offshore. Coho salmon FO was the highest 
nearshore (2 km) of all species, then the FO stabi- 
lized at 37 km and beyond (Fig. 4C). 

By sampling period Abundance of juvenile salmon 
in Southeast Alaska increased from July (CPUE=11) 
to August (CPUE=58) 1984 for all species. Summed 
over all habitats, pink, chum, sockeye, and coho 
salmon had higher FO's and abundance in August 
than in July. In outside waters, CPUE of each spe- 
cies increased two to seven times from July to Au- 
gust 1984, with juvenile pink salmon showing the 



largest increase (Fig. 5). In inside wa- 
ters, CPUE of pink and chum salmon 
increased 10 and 5 times respectively 
from July to August, whereas CPUE's 
of sockeye and coho salmon remained 
constant (Fig. 5). For all four species, 
FO increased in outside waters but de- 
creased in inside waters from July to 
August 1984 (Fig. 5). The low number 
of sets (four) made in outer coast inlets 
of Southeast Alaska in August 1984 
precluded seasonal comparisons of 
CPUE or FO for this habitat. 

Size 



Juvenile salmon were larger in outside 
waters than in inside waters. Thirteen 
matched pairs of size samples could be 
compared under the hypothesis that 
size did not vary between outside and 
inside waters; the fish were larger in 
the outside water in all comparisons 
(Table 4, x 2 =133.66, df=26, P<0.005) 
and the null hypothesis was rejected. 
Juvenile salmon in outside waters 
were larger farther seaward. Of the 
eight possible matched pairs of samples 
compared under the hypothesis that 
size was not different between outside 
waters >37 km offshore and <37 km 
offshore, the juvenile salmon were 
larger >37 km seaward in all compari- 
sons (Table 4, x 2 = 67.44, df=16, 
P<0.005). 

Juvenile salmon in northern waters 

were larger than those in southern 

waters. The fish were larger in the 

northward locations than southward locations in 18 

of 23 possible paired size comparisons (Table 4, 

X 2 =214.76, df=46, P<0.005). 

Juvenile salmon were larger in August than in 
July. Of the matched size samples compared under 
the hypothesis that size was not different between 
August and July of 1984, fish in August were larger 
than in July in 10 of 12 comparisons (Table 4, 
X 2 =145.36, df=24, P<0.005). 

The sizes between the different species of juvenile 
Pacific salmon differed significantly (P<0.05) (Table 
5). Coho salmon juveniles were significantly larger 
than other species in each sampling period; mean 
length of coho salmon was always at least 40% 
greater than in other species, whereas pink, chum, 
and sockeye salmon were within 9% of each other. 
Juvenile sockeye salmon were significantly larger 



Jaenicke and Celewycz: Marine distribution and size of juvenile Pacific salmon 



than pink salmon in each sampling 
period and were significantly larger 
than chum salmon in 1984. In both 
July and August 1984, pink and chum 
salmon did not differ in size, and in 
August 1983 chum and sockeye salmon 
did not differ in size. 



Discussion 



Fish distribution 

Each species of juvenile salmon was 
highly aggregated rather than dis- 
persed randomly. In contrast to our 
results, Hartt and Dell (1986) seldom 
observed zero catches and therefore 
concluded that juvenile salmon in the 
ocean were evenly dispersed. Several 
differences between our study and 
theirs may explain the differing conclu- 
sions. Seines used by Hartt and Dell 
were longer than ours and were held 
open for 30 minutes instead of 3-5 
minutes. Our catches may be more of 
a point estimate or instantaneous pic- 
ture of fish abundance, whereas their 
seines were more likely to intercept at 
least part of a juvenile salmon school. 
More importantly, Hartt and Dell did 
not separate juvenile salmon by species 
when considering their distribution. 



Species associations 

Juvenile pink, chum 




(4) 



(3) 



(5) (4) 

(2) 

L I  1 1 1 , I  i  




65 



74 



and sockeye 
salmon were generally closely associ- 
ated with each other in their distribu- 
tion. The distribution of these species, 
however, differed from the distribution 
of coho salmon, a result consistent with the conclu- 
sions of Hartt and Dell (1986) and Waddell et al. 
(1989). In the inside waters and outer coast inlets, 
we found that pink, chum, and sockeye salmon had 
a lower FO than coho salmon, indicating that those 
species were more highly aggregated and sparsely 
distributed than coho salmon. Paszkowski and Olla 
( 1985) found that behavior patterns of juvenile coho 
salmon promoted dispersion, not aggregation. The 
utilization of similar areas in this study by juvenile 
pink, chum, and sockeye salmon correlates with the 
high degree of diet overlap observed between these 
species; in contrast, juvenile coho salmon showed 



28 37 46 

Distance offshore (km) 

Figure 4 

Abundance of juvenile salmonids (pink, Oncorhynchus gorbuscha; 
chum, O. keta; sockeye, O. nerka; coho, O. kisutch ) by distance off- 
shore in the outside waters of Southeast Alaska in August 1984 
(36 sets). Abundance is shown in terms of (A) catch per unit of 
effort (CPUE), (B) the smoothed natural logarithm of CPUE. and 
(C) the smoothed frequency of occurrence of the catches; number 
of sets is in parentheses. All distances are rounded to the nearest 
kilometer. Actual distance between intervals (except the first) 
is 9.3 km. 



little diet overlap with the other species. 1 Healey 
( 1991) reported that juvenile pink, chum, and sockeye 
salmon in British Columbia were also aggregated. 

Migration 

The migration of juvenile salmon off Southeast Alaska 
(Hartt and Dell, 1986) consists of two components: 1) 
fish migrating north from the Pacific Northwest and 
British Columbia, and 2) fish from Southeast Alaska 
migrating from inside to outside waters. 



J. H. Landingham, Auke Bay Laboratory. 11305 Glacier High- 
way, Juneau, AK 99801-8626, pens, commun. Jan. 1992. 



86 



Fishery Bulletin 92(1), 1994 













1 Outside 
I waters 


X ?■ 


Outer coast 
inlets 




Inside 
waters 













July 1984 



August 1984 



UJ 
Z> 
0. 

o 



o 

C 
ID 
i_ 
i- 
3 
O 
O 
O 



>- 

o 

c 

ID 

3 
O" 
0> 




100 



Pink Chum Sockeye Coho 



Pink Chum Sockeye Coho 



Salmon species 

Figure 5 

Catch per unit of effort (CPUE) and frequency of occurrence of 
juvenile salmonids (pink, Oncorhynchus gorbuscha; chum, O. keta; 
sockeye, O. nerka; coho, O. kisutch) in the outside waters (69 sets), 
outer coast inlets (18 sets), and inside waters (55 sets) in South- 
east Alaska in July and August 1984. Note change in scale of 
CPUE from July to August 1984. 



Juvenile salmon migrations along the Pacific coast 
in 1984 did not peak off Southeast Alaska until, at 
earliest, August. In July, CPUE's were much higher 
in the outside waters of British Columbia than in 
Southeast Alaska. By August, CPUE of juvenile 
salmon in outside waters of Southeast Alaska had 
increased fivefold, and FO had increased for each 
species. Hartt and Dell (1986) observed that juve- 
nile salmon abundance peaked in August in outside 
waters of Southeast Alaska. 

In Southeast Alaska, juvenile sockeye salmon 
probably begin their ocean migration to the Gulf of 
Alaska before juvenile pink and chum salmon, based 
on two observations from our study. First, the sock- 
eye salmon did not occur in protected waters along 
the outer coast of Southeast Alaska like the other 
species: no sockeye salmon were captured in an 



outer coast inlet. Second, sockeye 
salmon was the only species with a 
higher CPUE in outside waters than in 
inside waters. This higher abundance 
outside, coupled with low abundance in 
inside waters in July and August, is 
consistent with the conclusion that 
sockeye salmon commence their ocean 
migration before pink or chum salmon 
(Straty, 1981; Healey, 1982). 

The migration of pink salmon from 
the inside waters of Southeast Alaska 
lasts until at least September. Martin 
(1966) concluded that late July and 
early August were the peak periods of 
juvenile pink salmon migration from 
the inside waters. However, our data 
show that pink salmon abundance in 
inside waters increased from July to 
August and that pink salmon were 
more abundant in inside waters than 
outside waters in August, thus indicat- 
ing that migration out of the inside 
waters was not complete in August. 
The seasonal migration of juvenile 
chum salmon out of Southeast Alaska 
could not be determined from the abun- 
dance data of this study. The migration 
of juvenile pink, chum, and sockeye 
salmon out of the inside waters in Sep- 
tember and later has not been studied. 
The offshore migration of coho 
salmon in Southeast Alaska is more 
complex. CPUE and FO of coho salmon 
in inside waters remained relatively 
constant for July and August. Coho 
salmon was the only species with both 
a higher CPUE and FO in inside wa- 
ters than in outside waters in August. These data 
suggest extensive residency in inside waters for a 
substantial portion of coho salmon juveniles in 
Southeast Alaska. Other researchers have found 
that some juvenile coho salmon remain in the east- 
ern Pacific Ocean inside waters until late fall 
(Healey, 1984; Hartt and Dell, 1986; Orsi et al., 
1987). Winter residency of juvenile coho in inside 
waters of Southeast Alaska is apparently rare. 2 
Hartt and Dell ( 1986) and Pearcy and Fisher ( 1990) 
also found coho salmon offshore as early as May or 
June; Hartt and Dell ( 1986) noted that juvenile coho 
salmon migrated seaward earlier than the other 
salmon species, presumably because of their larger 



2 J. A. Orsi, Auke Bay Laboratory, L1305 Glacier Highway, Ju- 
neau, AK 99801-8628. pers. commun. Jan. 1992. 



Jaenicke and Celewycz: Marine distribution and size of juvenile Pacific salmon 



87 









Table 4 






Fork length (FL) of juvenile salmonids sampled by period, habitat, north (N) or south (S) region, and dis- 
tances offshore in outside waters of Southeast Alaska in 1983 and 1984 and outside waters of British Colum- 
bia (B.C.) in 1984. Values are mean ± standard error, with number of samples in parenthesis. In brackets 
under the values are the specific paired size comparisons used in the null hypothesis testing of sizes by: 
northern vs. southern waters (Al, A2, ..., A23); outside vs. inside waters (Bl, B2, ..., B13); August vs. July 
1984 (CI, C2, ..., C12); and outside waters >37 km offshore vs. outside waters <37 km offshore (Dl, D2, ..., 
D8). Dashes indicate no fish caught. 


Period 


Habitat (region) 




FL of salmon (mm) 




Pink' 


Chum 2 


Sockeye- 3 


Coho" 


Aug 83 


Inside (N) 


169 ± 0.8 (890) 
[All 


180 ± 1.8 (199) 
[A2] 


163 ± 2.7 (74) 


233 ± 1.8 (136) 
[A3] 




Inside (S) 


121 ± 1.9 (10) 
[Al, Bl] 


139 ± 4.6 (18) 
[A2, B2] 


— 


227 ± 11.9 (5) 
[A3, B3] 




Outer coast inlet (N) 


— 


166 ± 4.9 (4) 
[A4] 


— 


221 ± 6.3 (11) 
[A5] 




Outer coast inlet (S) 


124 ± 0.5 (404) 


133 ± 1.5 (76) 
[A4] 


— 


217 ± 7.9 (11) 
[A5] 




Outside (S) 


153 ± 3.6 (19) 
[Bl] 


141 ± 13.5 (2) 
[B2] 


152 ± 2.6 (9) 


234 ± 3.6 (25) 
[B3] 


July 84 


Inside (N) 


121 ± 1.7 (94) 
[A6, B4, CI] 


112 ± 5.2 (19) 
[B5, C2] 


136 ± 5.9 (20) 
[B6, C3] 


193 ± 2.0 (206) 
[A7, B7, C4] 




Inside (S) 


132 ± 1.2 (3) 
[A6, B8] 


135 ± (1) 


— 


202 ± 7.8 (3) 
[A7, B9] 




Outer coast inlet (N) 


105 ± 10.9 (4) 


139 + (1) 


— 


177 ± 3.6 (27) 




Outside (N) 


135 ± 0.8 (207) 
[A8, A9, B4, C5] 


133 ± 2.3 (38) 
[A10, All, B5, C6] 


151 ± 2.1 (111) 
[A12, A13, B6, C7] 


220 ± 4.5 (26) 
[A14, A15, B7, C8] 




Outside (S) 


134 ± 4.6 (10) 
[A8, A16, B8, C9] 


161 ± 18.5 (2) 
[A10, A17, C10] 


157 ± 2.6 (19) 
[A12, A18, Cll] 


224 ± 7.5 (8) 
[A14, A19, B9, C12] 




Outside (B.C.) 


128 ± 1.0 (126) 
[A9, A16] 


132 ± 1.5 (46) 
[All, A17] 


128 ± 0.9 (197) 
[A13, A18] 


129 ± 10.3 (7) 
[A15, A19] 


Aug 84 


Inside (N) 


143 ± 1.0 (358) 
[B10, CI] 


125 ± 1.2 (118) 
[Bll, C2] 


157 ± 2.1 (18) 
[B12, C3] 


234 ± 1.9 (168) 
[B13, C4] 




Outer coast inlet (S) 


— 


132 ± 6.1 (12) 


— 


246 ± 12.2 (3) 




Outside (N) 


144 ± 0.6 (730) 
[A20, B10, C5] 


160 ± 2.0 (93) 
[A21, Bll, C6] 


159 ± 1.5 (75) 
[A22, B12, C7] 


267 ± 5.6 (33) 
[A23, B13, C8] 




<37 km 


143 ± 0.8 (457) 
[Dl] 


157 ± 2.2 (73) 
[D2] 


156 ± 1.7 (52) 
[D3] 


266 ± 6.5 (28) 
[D4] 




>37 km 


146 ± 1.0 (273) 
[Dl] 


169 ± 4.1 (20) 
[D2] 


165 ± 2.8 (23) 
[D3] 


274 ± 2.3 (5) 
[D4] 




Outside (S) 


139 ± 1.0 (373) 
[A20, C9] 


144 ± 2.1 (66) 
[A21, C10] 


149 + 0.9 (141) 
[A22, Cll] 


265 ± 3.3 (37) 
[A23, C12] 




<37 km 


135 + 1.2 (243) 
[D5] 


144 ± 2.7 (38) 
[D6] 


148 ± 1.0 (103) 
[D7] 


263 ± 3.3 (35) 
[D8] 




>37 km 


144 ± 1.4 (130) 
[D5] 


145 ± 3.5 (28) 
[D6] 


152 ± 1.5 (38) 
[D7] 


291 ± 15.0 (2) 
[D8] 


; Oncorhynchus gorbuscha. 

2 0. keta. 

3 O. nerka, 

4 O. kisulch. 



88 



Fishery Bulletin 92(1). 1994 



size. An early component of coho salmon juveniles 
could have moved offshore in June, prior to our sam- 
pling effort. More extensive sampling from late 
spring through fall is required to define the timing 
of migrations of coho salmon in the waters of South- 
east Alaska. 

The sizes of juvenile salmon we captured support 
the findings of Hartt and Dell (1986) that fish in 
more northern locations have been at sea longer 
than those in southern locations. Hartt and Dell 
(1986) observed a general increase in mean length 
of juvenile salmon from south to north in the out- 
side waters from Washington to Southeast Alaska. 
In the coastal waters off Oregon and Washington, 
larger, presumably older, juvenile coho salmon were 
found farther north (Pearcy and Fisher, 1988). As- 
suming they were similar in size on entering the sea, 
the smaller fish in the southerly locations are recent 
arrivals from nearby production areas, whereas the 
larger fish in the northerly locations have been at 
sea longer and probably migrated from more south- 
erly production areas (Hartt and Dell, 1986). Our 
studies also reveal juvenile salmon in Southeast 
Alaska were larger in the outside waters than in- 
side waters and farther offshore in the outside wa- 
ters than closer to shore. The progression of juve- 
nile salmon migrations over a season may be size- 
dependent (Healey, 1982, 1984), and certain phases 
of migration may depend on fish reaching a thresh- 
old size. According to Hartt and Dell ( 1986), the off- 
shore migration into the Gulf of Alaska of juvenile 



Table 5 

Comparison of mean fork lengths (FL) of juvenile salmonids caught in 
the marine waters (all habitats pooled) of Southeast Alaska and north- 
ern British Columbia in 1983-84. Sample size = n; standard deviation 
of the size in mm = s. The hypothesis was that there were no size dif- 
ferences between species during the same period. The rejection crite- 
ria were adjusted for multiple comparisons so that experimental error 
did not exceed a = 0.05. Species having the same letter in a column were 
not significantly different by size. 



August 1983 



July 1984 



Salmon 
species 



mean FL 

Immi 



n 



mean FL 
(mm) 



n 



Pink' 1,323 

Chum 2 299 

Sockeye'* 83 

Coho'' 188 



155 c 
165 6 
162'' 
232° 



29 
31 

23 

22 



444 
108 
347 

277 



130' 
129 r 
138'' 
193 



1 1 
17 
20 

30 



1,461 
289 
234 
241 



Oncorhynchus gorbuscha. 
b O. keta. 
c O. nerka. 
d O. kisutch. 



pink, chum, and sockeye salmon does not begin until 
September or October when fish are 180-230 mm 
or greater in mean FL. However, our findings show 
that these species are found offshore earlier (in 
August) and at a much smaller size (145-170 mm 
mean FL). 

Width of migration band 

Juvenile Pacific salmon typically migrate in 
nearshore waters during their first few months at 
sea (Straty, 1981); however, the width of this migra- 
tion band varies regionally (Straty and Jaenicke, 
1984; Hartt and Dell, 1986). Juvenile salmon con- 
centrated within 37 km of shore along the broad 
continental shelf (<183 m deep) off Oregon and 
Washington (Miller et al., 1983; Pearcy and Fisher, 
1990). Hartt and Dell (1986) concluded that the 
band of juvenile salmon was within 37 km of shore 
off Southeast Alaska where the continental shelf is 
narrow, but that the band widened in the northern 
Gulf of Alaska where the shelf is wider. 

Our results indicate that the coastal band of mi- 
grating juveniles can be much wider than 37 km and 
that the offshore migration beyond 37 km may be- 
gin as early as August. Catches of juvenile salmon 
74 km offshore — the maximum distance we fished 
offshore — and the catch distributions indicate that 
some juvenile salmon (pink, chum, and sockeye) may 
have been abundant even farther seaward. Two- 
thirds of the juvenile salmon captured in outside wa- 
ters in August 1984 were beyond the continental shelf. 
The width of the migration band is probably in- 
fluenced by the Alaska Coastal 
Current — a dominant feature 
in the circulation of Gulf of 
Alaska coastal waters. This 
freshwater-driven current be- 
gins along the British Colum- 
bia coast and flows north then 
west within 20 km of shore into 
the Bering Sea (Royer, 1984). 
The strength of this current is 
affected by local precipitation, 
wind, air temperature, and 
other meteorological condi- 
tions. Millions of juvenile 
salmon migrate through the cur- 
rent every year en route to 
more oceanic waters. Cooney 
(1984) theorized that the cur- 
rent represents a critical early- 
feeding habitat in the summer 
and early fall. In modeling the 
early-ocean limitations of Pa- 
cific salmon production, Wal- 



August 1984 



mean FL 
(mmi 



142'' 
141 r 
153'' 
253° 



18 
22 
12 
20 



Jaenicke and Celewycz: Marine distribution and size of juvenile Pacific salmon 



89 



ters et al. (1978) noted that production predictions 
were critically sensitive to the width of the coastal 
band within which salmon migrate during their first 
summer at sea. We recommend additional sampling 
be conducted from June through September to bet- 
ter document 1) the width of the coastal band of ju- 
venile salmon migrations through the summer and 
2) the timing of offshore migrations beyond 37 km 
from the outer coast. 

Acknowledgments 

We thank the biologists and technicians who helped 
in the field and laboratory. We also thank the crew 
on the NOAA RV John N. Cobb and FV Bering Sea 
for their cooperation during seining operations. The 
FV Bering Sea cruise was part of a cooperative 
coastwide survey from California to Southeast 
Alaska with W Pearcy, Oregon State University. 

We especially acknowledge the review of the 
manuscript by A. Wertheimer. 

Literature cited 

Bax, N. J. 

1983. Early marine mortality of marked juvenile 
chum salmon (Oncorhynchus keta) released into 
Hood Canal, Puget Sound, Washington, in 
1980. Can. J. Fish. Aquat. Sci. 40:426-435. 
Browning, R. J. 

1980. Fisheries of the North Pacific: history, spe- 
cies, gear and processes. Alaska Northwest Publ., 
Anchorage, 423 p. 
Chambers, J. M., W. S. Cleveland, B. Kleiner, and 
P. A. Tukey. 

1983. Graphical methods for data analysis. 
Duxbury Press, Boston, 395 p. 

Cooney, R. T. 

1984. Some thoughts on the Alaska Coastal Cur- 
rent as a feeding habitat for juvenile salmon. //; 
W. G. Pearcy (ed.), The influence of ocean condi- 
tions in the production of salmonids in the North 
Pacific, p. 256-268. Oregon State Univ. Sea 
Grant College Program Rep. ORESU-W-83-001. 

Daniel, W. W. 

1978. Applied nonparametric statistics. Houghton 
Mifflin, Boston, 503 p. 
Furnell, D. J., and J. R. Brett. 

1986. Model of monthly marine growth and natu- 
ral mortality for Babine Lake sockeye salmon 
(Oncorhynchus nerka). Can. J. Fish. Aquat. Sci. 
43:999-1004. 
Godfrey, H., K. A. Henry, and S. Machidori. 

1975. Distribution and abundance of coho salmon 
in offshore waters of the North Pacific Ocean. Int. 
North Pac. Fish. Comm. Bull. 31, 80 p. 
Hartt, A. C. 

1975. Problems in sampling Pacific salmon at 
sea. In Symposium on evaluation of methods of 



estimating the abundance and biological attributes 
of salmon on the high seas, p. 165-231. Int. 
North Pac. Fish. Comm. Bull. 32. 
Hartt, A. C, and M. B. Dell. 

1986. Early oceanic migrations and growth of ju- 
venile Pacific salmon and steelhead trout. Int. 
North Pac. Fish. Comm. Bull. 46:1-105. 

Healey, M. C. 

1982. The distribution and residency of juvenile Pa- 
cific salmon in the Strait of Georgia, British Colum- 
bia, in relation to foraging success. In B. R. Melteff 
and R. A. Neve (eds.), Proceedings of the North Pa- 
cific aquaculture symposium, p. 61-69. Alaska Sea 
Grant Rep. 82-2. Univ. Alaska, Fairbanks. 

1984. The ecology of juvenile salmon in Georgia 
Strait, British Columbia. In W. J. McNeil and D. 
C. Himsworth (eds.), Salmonid ecosystems of the 
North Pacific, p. 203-229. Oregon State Univ. 
Press, Corvallis. 

1991. Diets and feeding rates of juvenile pink, 
chum, and sockeye salmon in Hecate Strait, Brit- 
ish Columbia. Trans. Am. Fish. Soc. 120:303-318. 
Manzer, J. I. 

1964. Preliminary observations on the vertical dis- 
tribution of Pacific salmon (Genus Oncorhynchus) 
in the Gulf of Alaska. J. Fish. Res. Board Can. 
21:891-903. 
Martin, J. W. 

1966. Early sea life of pink salmon. In W. L. 
Sheridan (ed.). Proceedings of the 1966 Northeast 
Pacific pink salmon workshop, p. 111-125. Alaska 
Dep. Fish Game, Info. Leafl. 87, Juneau. 
Miller, D. R., J. G. Williams, and C. W. Sims. 

1983. Distribution, abundance and growth of juve- 
nile salmonids off the coast of Oregon and Wash- 
ington, summer 1980. Fish. Res. 2:1-17. 

Morisita, M. 

1959. Measuring the dispersion of individuals and 
analysis of the distributional patterns. Mem. 
Fac. Sci. Kyushu Univ. Ser. E. (Biol) 2:215-235. 
Orsi, J. A., A. G. Celewycz, D. G. Mortensen, and 
K. A. Herndon. 

1987. Sampling juvenile chinook salmon 
(Oncorhynchus tshawytscha) and coho salmon (O. 
kisutch) by small trolling gear in the northern and 
central regions of southeastern Alaska, 
1985. U.S. Dep. Commer., NOAA Tech. Memo. 
NMFS F/NWC-115, 47 p. 

Parker, R. R. 

1968. Marine mortality schedules of pink salmon 
of the Bella Coola River, central British 
Columbia. J. Fish. Res. Board Can. 25:757-794. 
Paszkowski, C.A., and B. L. Olla. 

1985. Social interactions of coho salmon 
(Oncorhynchus kisutch ) smolts in seawater. Can. 
J. Zool. 63:2401-2407. 

Pearcy, W. G., and J. P. Fisher. 

1988. Migrations of coho salmon, Oncorhynchus 
kisutch, during their first summer in the 
ocean. Fish. Bull. 86:173-195. 



90 



Fishery Bulletin 92(1), 1994 



1990. Distribution and abundance of juvenile 
salmonids off Oregon and Washington, 1981- 
1985. U.S. Dep. Commer., NOAA Tech. Rep. 
NMFS 93, 83 p. 

Poole, R. W. 

1974. An introduction to quantitative ecology. 
McGraw-Hill, NY, 532 p. 

Royer, T. C. 

1984. Annual and interannual variability of tem- 
perature and salinity in the Gulf of Alaska with 
emphasis on the coastal waters. In W. G. Pearcy 
(ed.), The influence of ocean conditions in the pro- 
duction of salmonids in the North Pacific, p. 244- 
255. Oregon State Univ. Sea Grant College Pro- 
gram Rep. ORESU-W-83-001. 

Sokal, R. R., and F. J. Rohlf. 

1981. Biometry, the principles and practices of sta- 
tistics in biological research. W. H. Freeman & 
Co., NY, 859 p. 

Straty, R. R. 

1981. Trans-shelf movements of Pacific salmon. In 
D. W. Hood and J. A. Calder (eds.), The eastern 
Bering Sea shelf: oceanography and resources 



1:575-595. U.S. Dep. Commer., NOAA, Off. Mar. 
Pollut. Assess., Juneau, AK. 

Straty, R. R., and H. W. Jaenicke. 

1984. Estuarine influence of salinity, temperature, 
and food on the behavior, growth, and dynamics 
of Bristol Bay sockeye salmon. In W. J. McNeil 
and D. C. Himsworth (eds.), Salmonid ecosystems 
of the North Pacific, p. 247-265. Oregon State 
Univ. Press, Corvallis. 

Tukey, J. W. 

1977. Exploratory data analysis. Addison-Wesley 
Publishing, Reading, MA, 506 p. 

Waddell, B. J., M. C. Healey, and J. F. T. Morris. 
1989. Data analysis of 1986 and 1987 Hecate Strait 
juvenile salmon surveys. Can. Tech. Rep. Fish. 
Aquat. Sci. 1719, 76 p. 
Walters, C. J., R. Hilborn, R. M. Peterman, and M. 
J. Staley. 

1978. Model for examining early ocean limitation 
of Pacific salmon production. J. Fish. Res. Board 
Can. 35:1303-1315. 

Winer, B. J. 

1971. Statistical principles in experimental 
design. McGraw-Hill, NY, 907 p. 



Abstract. Evidence support- 
ing a two stock hypothesis for king 
mackerel, Scomberomorus cavalla, 
in the Gulf of Mexico was devel- 
oped principally from the results of 
electrophoretic patterns of one 
polymorphic dipeptidase locus and 
supporting evidence from mark- 
recapture, charterboat catch, and 
spawning studies. 

There are two identifiable stocks 
of king mackerel in the Gulf of 
Mexico: a western stock and an 
eastern stock. The western stock 
migrates northward along the 
Mexico-Texas coast during the 
spring and early summer from its 
winter grounds in Mexico (Yucatan 
Peninsula). This stock has a high 
frequency of the dipeptidase 
PEPA-2*a allele. The eastern stock 
migrates at the same time north- 
ward along the eastern coast of the 
Gulf of Mexico from its winter 
grounds in south Florida (Gulf of 
Mexico and Atlantic coast). This 
stock has a high frequency of the 
dipeptidase PEPA-2*b allele. Both 
stocks migrate simultaneously into 
the northern Gulf of Mexico and 
mix at varying degrees in the 
northern summering grounds 
(Texas to northwest Florida). 



Evidence for distinct stocks of 
king mackerel, 
Scomberomorus cavalla, 
in the Gulf of Mexico 



Allyn G. Johnson 

William A. Fable Jr. 

Churchill B. Grimes 

Lee Trent 

Southeast Fisheries Science Center 
National Marine Fisheries Service. NOAA 
3500 Delwood Beach Road 
Panama City. Florida 32408 

Javier Vasconcelos Perez 

Instituto Nacional de la Pesca 
Mexico City. Mexico 



Manuscript accepted 17 August 1993 
Fishery Bulletin 92:91-101 (1994) 



The king mackerel, Scomber- 
omorus cavalla, is a widely distrib- 
uted, coastal pelagic species in the 
western Atlantic Ocean. This 
scombrid is found from the Gulf of 
Maine to Rio de Janiero, Brazil, in- 
cluding the Gulf of Mexico and 
Caribbean Sea (Rivas, 1951; 
Collette and Nauen, 1983). It is a 
valuable resource that supports 
fisheries throughout most of its 
range (Manooch et al., 1978). 

The U.S. and Mexico have been 
major exploiters of king mackerel 
resources. U.S. commercial land- 
ings have been reported since 1888. 
Landings have ranged from 2,213 
metric tons (t) (1972) to 4,746 t 
(1974). U.S. recreational catches 
are estimated to be two to ten 
times larger than the commercial 
catches (Deuel and Clark, 1968; 
Deuel, 1973; Manooch, 1979; U.S. 
Dep. Commer., 1984, 1986, 1987). In 
Mexican waters, commercial land- 
ings for king mackerel from 1968 to 
1988 have ranged from 784 t ( 1968) 
to 6,133 t (Collins and Trent, 1982 1 ). 

Because king mackerel are pres- 
ently managed in the southeastern 
U.S. (represented by more than 



eight states and two regional fish- 
ery management council jurisdic- 
tions) and support both recre- 
ational and mixed gear commercial 
fisheries, the identities of compo- 
nent stocks are important. Current 
management of king mackerel fish- 
eries assumes two migratory stocks 
with overlapping ranges, one in the 
U.S. Atlantic Ocean and one in the 
Gulf of Mexico (Gulf of Mexico and 
South Atlantic Fishery Manage- 
ment Councils, 1985). This separa- 
tion is based on mark-recapture 
results (Sutherland and Fable, 
1980; Williams and Godcharles, 
1984 2 ; Sutter et al., 1991). 

The concept of a stock is one of 
the most fundamental to fishery 
management. A stock is variously 
defined, ranging from the strict 
definition of a single interbreeding 
population to a unit capable of in- 



1 L. A. Collins and L. Trent, Natl. Mar. 
Fish. Serv., Panama City, FL, pers. 
commun. 1992. 

2 Williams. R. O., and M. F. Godcharles. 
1984. Completion report, king mackerel 
tagging and stock assessment. Project 2- 
341-R. Fla. Dep. Natl. Resour. Unpubl. 
Rep., 45 p. 



9 1 



92 



Fishery Bulletin 92(1). 1994 



dependent exploitation or management and contain- 
ing as much of an interbreeding unit or as few re- 
productively isolated units as possible (Royce, 1972). 
An additional term that has been used to define the 
stock concept used in fishery management is "unit 
stock" which was referred to by Kutkuhn (1981) as 
"one consisting of randomly interbreeding members 
whose genetic integrity persists whether they re- 
main spatially and temporally isolated as a group, 
or whether they alternately segregate for breeding 
and otherwise mix freely with members of other unit 
stocks of the same species." This term is more func- 
tional for application to many marine resources 
which have identifiable components but for which 
reproductive isolation has not been demonstrated. 
We consider stock and unit stock to be identical with 
regard to king mackerel resources at the present 
time. 

Using Kutkuhn's (1981) definition, this report 
presents evidence of two stocks of king mackerel 
existing in the Gulf of Mexico (the Gulf), an east- 
ern and a western stock which winter off south 
Florida and off the Yucatan peninsula (Mexico), re- 
spectively. In the spring these fish migrate along 
their respective coasts to summer areas in the 
northern Gulf. The concept of two Gulf of Mexico 
stocks was first presented by Baughman ( 1941). He 
based his hypothesis on observations by fishermen 
of simultaneous migrations along the eastern and 
western sides of the Gulf. More recently, May 
(1983) 3 reported electrophoretic differences in king 
mackerel between the eastern and western Gulf. 
Using more recent tagging data and electrophoretic 
information, Grimes et al. (1987) reintroduced the 
hypothesis. 

Additional evidence for a two-stock hypothesis is 
the following: 

1 Fish movements along the coast, as indicated by 
mark-recapture studies (Fable et al., 1990 4 ). 

2 The simultaneous migration along the eastern 
and western coasts of the Gulf in spring and 
early summer as detected by analysis of 
charterboat CPU data (Trent et al., 1987b). 

3 The difference in spawning times of king mack- 
erel in the northern and southern areas of the 
Gulf (Grimes et al., 1990). 



3 May, B. 1983. Genetic variation in king mackerel 
(Scomberomorus cavalla). Final Rep. Fla. Dep. Natl. Resour. 
Contract C-14-34, 20 p. 

4 Fable, Jr., W.A., J. Vasconcelos P., K. M. Burns, H. R. Osburn, 
L. Schultz R., and S. Sanchez G. (1990). King mackerel, 
Scomberomorus cavalla, movements and migrations in the Gulf 
of Mexico. Natl. Mar. Fish. Serv., Panama City Lab., Panama 
City, FL (unpubl. ms.l. 



We report the results from electrophoretic inves- 
tigations and summarize current information from 
tagging, migration, and spawning time studies. We 
also propose a possible mechanism to explain the 
observed results with regard to the water circula- 
tion of the area. 



Methods and materials 

Samples of muscle tissue, along with fork length 
(mm) and sex, were collected during 1985 through 
1990 from fish obtained in recreational and commer- 
cial fisheries from North Carolina to Yucatan 
(Table 1). The samples were frozen as soon as pos- 
sible in the field and then shipped frozen to the Na- 
tional Marine Fisheries Service's Panama City Labo- 
ratory. Muscle tissue (about 10 grams) was excised 
from each sample and stored in a freezer (in 1985 at 
-5° to -10°C and from 1986 through 1990 at -100°C). 

Tissue extracts were prepared by mixing equal 
volumes of muscle tissue and distilled water and 
grinding with glass rods to uniform pastes. Extracts 
were centrifuged at 3,400 rpm (1,000 x G) for five 
minutes, then supernatants were drawn onto 4 mm 
x 8 mm filter paper inserts (Whatman 1). 

Starch gel electrophoretic separation of the ex- 
tracts was performed following the methods of 
Kristjansson (1963). Electrophoretic buffers were 
those of A) Markert and Faulhaber (1965), and B) 
N-(3-aminopropyl)-morpholine-citrate (pH 6.1) 
buffer of Clayton and Tretiak (1972). The gel con- 
sisted of 35 g of starch (Sigma Chemical Co. lots 
123F-0591, 35K-0383, and 94F-0536) plus 250 mL 
of buffer. Amperage during electrophoresis was kept 
below 50 MA, and voltage varied between 100 and 
400 V, depending on the buffer. Temperature was 
maintained at 2°C by using a refrigerated cooling 
system (see Aebersold et al., 1987, for description). 
After electrophoresis, the gels were sliced into four 
horizontal sections and stained for dipeptidase (EN 
3.4.-.-). In 1985 (1,223 fish) and 1988 (879 fish), 27 
additional enzymes were examined. Methods fol- 
lowed May (1983) 3 and Aebersold et al. (1987). 

We conducted statistical analyses using Biosys-1 
(Swofford and Selander, 1981) to test for conform- 
ance to Hardy-Weinberg expectations and spatially 
related differences in allele frequencies compared to 
distance and physical feature subdivisions. The 
Kolmogorov-Smirnov goodness-of-fit test was used 
for comparing allele distributions by size of fish 
(100-mm-FL intervals), while the chi-square contin- 
gency test was used for comparing allele distribu- 
tions by sex (see Sokol and Rohlf (1981) for proce- 
dures i. 



Johnson et al.: Evidence for distinct stocks of Scomberomorus cavalla 



93 



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Johnson et al.: Evidence for distinct stocks of Scomberomorus cavalla 



95 



Results 

Of the 50 loci surveyed in 1985, 30% were variable. 
In 1988, the 50 loci were again surveyed (879 fish 
from 10 locations) and 24% of the loci were found 
to have variants. Variations other than dipeptidase 
(EN 3.4.-.-) PEPA-2 were found in low frequency 
(uncommon allele 0.000 to 0.063) in 18 polymorphic 
systems. Occurrence of these variants differed be- 
tween locations and years. Electrophoretic variants 
were found for loci including aspartate aminotrans- 
ferase (EN 2.6.1.1) sAAT ", acid phosphatase (EN 
3.1.3.2) ACP-2*, adenosine deaminase (EN 3.5.4.4) 
ADA , adenylate kinase (EN 2.7.4.3) AK-1* and AK- 
2' , alanine aminotransferase (EN 2.6.1.2) ALAT-1 
and ALAT-2', esterase-D (EN 3.1.-.-) ESTD-2' and 
ESTD-3 , fructose-bis-phosphate aldolase (EN 
4.1.2.13) FBALD-2 \ glucose-6-phosphate isomerase 
(EN 5.3.1.9) GPI-1* and GPI-2\ isocitrate dehydro- 
genase (NADP + ) (EN 1.1.1.42) sIDHP , malic en- 
zyme (NADP + ) (EN 1.1.1.38) ME-2' , mannose-6- 
phosphate isomerase (EN 5.3.1.8) MPf, dipeptidase 
(EN 3.4.-.-) PEPA-1 , phosphogluconate dehydroge- 
nase (EN 1.1.1.44) PGDH*, and phosphoglucomutase 
(EN5.4.2. 2) PGM-2*. 

Use of very low-frequency variations for stock 
identification of king mackerel was impractical, be- 
cause sufficient sample sizes (numbers of fish) for 
detection during short time periods (one month or 
less) were unavailable. Tagging studies (Fable et al., 
1990 4 ) indicated that discrete geographic population 
units were not available during the time intervals 
required to obtain sufficient samples. Only dipepti- 
dase (glycyl-leucine substrate) 5 consistently varied 
between locations. In 1985 (1,223 fish), 1986 (1,537 
fish), 1987 (2,120 fish), 1988 (1,631 fish), 1989(1,502 
fish), and 1990 (963 fish), muscle tissues were ex- 
amined for the dipeptidase variation. This enzyme 
developed on electropherograms as two zones of 
activity, and showed the pattern of a two allele ("a 
and b) polymorphism in the most anodal zone 
{PEPA-2\ in most collections, as described by May 
[1983]). We refer to May's 1 and 2 alleles (electro- 
morphs) as a and *b, respectively (Fig. 1). A third 
allele (*c) which is anodal of the a allele was found 
in 1988 and 1989 collections from Veracruz, Mexico 
to Alabama. 6 Only one homozygote (*c*c) and 20 
heterozygotes Cc'a) were found from 3,487 fish. 



5 Enzyme is also active with valyl-leucine and leucyl-tyrosine as 
substrates. 

6 The genetic nomenclature for this polymorphic system accord- 
ing to the recommendations of Shaklee, et al. (1990), is dipep- 
tidase 3A.-APEPA-2') with three variant alleles '//(). '105, and 
'100. These alleles are represented in this report as *c, *a, and 
'b, respectively. 



PEPA-2 
PEPA-1 



■Tit ••!••.— IV'Ii T 



(D 



'a'a a'b Vb 



(2) 



I 



 • 



^(3) 




Figure I 

King mackerel iScomberomorus cavalla) dipeptidase 
(PEPA-P and PEPA-2*): (1) schematic of gel with 
25 samples (PEPA-2* a is 0.700), (2) schematic of en- 
largement of section of PEPA-2 on gel showing 
three phenotypes ( a a, ab, b 6), and (3) photo- 
graph of actual gel section used for schematic (2). 



Because of the rareness of this allele Cc), it was 
combined with allele a for analysis. 

Allele frequencies and phenotypic distributions 
varied extensively within and between areas from 
1985 to 1990 (Table 1). The majority of monthly 
collections conformed to the Hardy-Weinberg expec- 
tation; however, many of the yearly collections did 
not conform. In general, higher *a allele frequencies 
were found west of Florida than in Florida and along 
the Atlantic coast. 

The phenotypic distributions of the dipeptidase 
polymorphism were not significantly correlated with 
body length, with few exceptions. When the pheno- 
typic distribution was compared by 100-mm-FL size 
intervals for five geographic locations (Atlantic 
coast, Alabama-Mississippi, Louisiana, east Texas, 
and south Texas) by year, only seven of the 78 com- 
parisons were significantly different (Kolmogorov- 
Smirnov goodness-of-fit test, P<0.05). Four of these 



96 



Fishery Bulletin 92(1). 1994 



deviant collections occurred in the northern Gulf 
(east Texas and Alabama-Mississippi). The other 
three (1988— *a*a phenotype on Atlantic coast; 1989- 
*b*b, and 1990-*a*a phenotypes in northwest 
Florida) are believed to have resulted from sampling 
inadequacies (in 1988, only 9 *a*a were collected on 
the Atlantic coast, and in 1989 northwest Florida 
had 136 of the 275 *b*b in the <600-mm-FL cell, 
which represented 167 of the 344 fish; and in 1990, 
northwest Florida had 12 *a*a of the 17 *a*a in the 
900, 1,000, and >1,100 mm cells). 

When allele distributions were compared by sex 
at seven locations for each year in which sufficient 
data were available, eight of the 23 allele compari- 
sons deviated significantly (chi-square contingency 
test, P<0.05). Six deviant collections occurred in the 
northern Gulf (Texas-Mississippi 1985-1989) and 
were from collections that did not conform to Hardy- 
Weinberg expectations with regard to their pheno- 
typic distributions. Two others occurred in Veracruz, 
Mexico (1988 and 1990). The total allele-sex (1985- 
90) comparisons for the seven locations did not de- 
viate significantly, except for Veracruz, Mexico. 
Veracruz collections were dominated by small fish 
(<600 mm FL) of which sex determination was dif- 
ficult, especially early in the year (Jan. -July) be- 
cause of undeveloped gonads. Sex could only be de- 
termined for 68% of the fish tested from this area. 

The geographic pattern of dipeptidase (PEPA-2*) 
(1985-90) indicated that western Gulf differed from 
eastern Gulf and Atlantic coast king mackerel. In 
all years except 1985, comparison of allele counts 
(Table 1) of the various geographic groupings of the 
Gulf varied significantly (P<0.05) both within the 
Gulf and between the Gulf and the Atlantic coast. 
On the Atlantic coast (north of Florida vs. Florida), 
the variation was found not significant (except in 
1990). The trend in these comparisons was for ex- 
cess *a allele in the western Gulf and for excess *b 
allele in the eastern Gulf and the Atlantic coast. 



Discussion 

Comparisons of subdivisions (Table 2) show a con- 
sistently higher level of PEPA-2*a in western Gulf 
king mackerel and a deficit of this allele in king 
mackerel in the eastern Gulf and along the Atlan- 
tic coast. 

Electrophoretic data (ours and that of May ( 1983 ) 3 
indicating high dipeptidase PEPA-2* a frequency in 
the western Gulf and low *a frequency in the east- 
ern Gulf and along the Atlantic coast supports a two 
stock hypothesis for king mackerel in the Gulf. Sup- 



porting information can be obtained from other in- 
vestigations: mark-recapture (Fable et al., 1990 4 ), 
charterboat catches (Trent et al., 1987b) and spawn- 
ing date analysis (Grimes et al., 1990). Fish move- 
ments indicated by mark-recapture are consistent 
with the two stock hypothesis. The charterboat in- 
formation provides evidence of simultaneous north- 
ward migration on both sides of the Gulf, while the 
spawning date information offers evidence for repro- 
ductive isolation. 

The king mackerel dipeptidase (PEPA-2") varia- 
tion found in 1985-90 was similar to the variation 
first reported by May (1983) 3 . His data showed 
higher dipeptidase *a allele frequencies for Louisiana 
(0.618) and Texas (0.736) than were found eastward. 

Temporal variations in the PEPA-2* allele frequen- 
cies are difficult to interpret without taking into 
consideration the migratory behavior. The variation 
was extreme at some locations, giving the impres- 
sion that the samples were collected from different 
or mixed schools from different origins. For example, 
in east Texas (Galveston-Freeport area) (1986), five 
discrete collections (5 July-28 August) of 27 to 56 
fish each (204 total) were sampled. The PEPA-2* a 
frequencies were 0.933, 0.769, 0.202, 0.839, and 
0.037 (in collection order). In other collection peri- 
ods, variations in frequencies indicated that we had 
sampled the same school of fish. For example, in 
Louisiana (1987) three collections 7 days apart (21 
Aug.^1 Sept.) were obtained. Their PEPA-2* a fre- 
quencies were 0.590 (50 fish), 0.580 (50 fish), and 
0.594 (48 fish). In view of the extreme variability of 
PEPA-2* frequencies, numerous deviations from 
Hardy- Weinberg expectations, and sampling difficul- 
ties (one or more schools per collection), proper spa- 
tial subdivision and grouping of collections for test- 
ing specific hypotheses is arduous. The expanse of 
the sampling area (Virginia to Yucatan) can be di- 
vided into various subdivisions representing dis- 
tance or physical features (Table 2). Examples of 
subdivisions by distance are the following: Missis- 
sippi westward vs. Alabama eastward, Alabama to 
Florida Keys, Florida vs. Atlantic coast, and Florida 
east vs. Georgia northward. Examples of physical 
subdivisions are the following: Florida peninsula 
(Florida east coast versus Florida west coast), east- 
ern Gulf and Atlantic coast (Alabama to Florida 
Keys versus Atlantic coast), and northern and west- 
ern Gulf (Louisiana-Mississippi versus Texas versus 
Mexican sector of the Gulf) (See also Collard and 
Ogren, 1990). 

Caution should be applied to interpreting electro- 
phoretic results in which variation has not been 
proven to be of genetic origin by the use of breed- 
ing analysis (i.e., crossing of phenotypes and analy- 



Johnson et al.: Evidence for distinct stocks of Scomberomorus cavalla 



97 



sis of offspring). Deviation from 
Hardy- Weinberg expectations 
can result from stock mixing, 
natural selection, or drift in 
small populations (Smith, 
1990). While we favor the inter- 
pretation that these king mack- 
erel data suggest stock mixing, 
consideration should be given 
to natural selection as the ul- 
timate maintenance factor of 
PEPA-2* frequencies as sug- 
gested for dipeptidase (PEPA- 
LT*) and other variations found 
in Menidia beryllina (Johnson, 
1974). 

Electrophoretic data suggest 
that two stocks of king mack- 
erel occur in the Gulf, a west- 
ern stock with high frequency 
of the *a allele and an eastern 
stock with a low frequency of 
the *a allele. The northern Gulf 
appears to be a zone of mixing 
of these two stocks during the 
summer. Our electrophoretic 
information does not distin- 
guish the eastern Gulf fish 
from those along the Atlantic 
coast. 

Historical tagging data 
showed migration between 
south Florida and the north 
and northwest Gulf. Williams 
and Godcharles (1984) 2 (and 
Sutter et al.'s later analysis 
(1991) of Williams and 
Godcharles' data) can be exam- 
ined in light of the two stock 
hypothesis. Williams and 
Godcharles tagged approxi- 
mately 12,000 king mackerel 
off south and southeast 
Florida, primarily in winter 
months. Forty-nine tags were 
recovered in the northeast Gulf 
and another 49 tags were re- 
turned from the northwest 
Gulf. Almost all tagged fish 
were recaptured in the warmer 
months of the year, supporting 
the hypothesis of migration 
from wintering grounds in 
southeast Florida waters to 
northern Gulf of Mexico waters 







Table 2 






Comparisions o 


f geographic groupings 


of a 


llele counts of dipeptidase (PEPA- 


2*) in king mac 


terel. {Scomberomorus 


cava 


lla), 1985- 


-90. 


Location' Year 


Alleles 


X 2 


df 


P 


Remarks 


MS westward vs. AL eastward (distance) 2 






1985 


1,620 


297.3417 




<0.001 


Deficient *b in MS 
westward 


1986 


1,676 


340.9499 




<0.001 


Devidient *6 in MS 
westward 


1986 


3,976 


283.7311 




<0.001 


Deficient *b in MS 
westward 


1988 


2,468 


812.6335 




<0.001 


Excess *b east of Al 
Deficient *a east of AL 


1990 


1,926 


793.5280 




<0.001 


Excess *b east of AL 
Deficient *a east of AL 


Key West, FL westward 


vs. Atlantic coast (physical) 




1985 


2,630 


329.0983 




<0.001 


Excess *a in Gulf 


1986 


2,662 


879.2843 




<0.001 


Excess *a in Gulf 


1987 


3,865 


271.3356 




<0.001 


Excess *a in Gulf 


1988 


3,084 


643.4390 




<0.001 


Excess *b in Atl. coast 
Deficient *a in Gulf 


1989 


3,004 


657.913 




<0.000 


Excess *b in Atl. Coast 
Deficient *a in Atl. Coast 


1990 


1,926 


339.2062 




<0.001 


Excess *b in Atl. coast 
Deficient *a in Atl. coast 


AL to Key West, 


FL vs. Atlantic coast (distance) 




1985 


1.518 


0.0040 




>0.90 




1986 


1,258 


33.1770 




<0.001 


Excess *a in Gulf 


1987 


1,550 


64.6325 




<0.001 


Deficient *a in Atl. coast 


1988 


1,022 


10.4639 




<0.001 


Excess *a in Atl. coast 
Deficient *a in Gulf 


1989 


1,406 


6,2033 




>0.01 


Excess *a in Gulf 
Deficient *a in Atl. Coast 


1990 


864 


22.0855 




<0.001 


Excess *a in AL to 

Key West, FL 
Deficient *a in Atl. coast 


Within northerr 


and western Gulf (LA-MS, 


TX, MX) (physical) 


1985 


1,110 


7.9835 


2 


>0.01 




1986 


1,410 


135.5281 


3 


<0.001 


Excess *b in LA-MS 
Excess *a in MX 


1987 


2,416 


71.5602 


2 


<0.001 


Excess *b in LA-MS 
Excess *a in MX 


1988 


2.062 


40.1994 


2 


<0.001 


Excess *b in LA-MS 
Deficient *b in TX 


1989 


1,598 


70.2421 


2 


<0.001 


Excess *b in LA-MS 
Deficient *a in LA-MS 


1990 


1,062 


120.9159 


2 


<0.001 


Excess *b in LA-MS 
Deficient in *a in LA-MS 
Deficient in *b in MS 


Within Atlantic 


coast (N of FL vs. FL) (distance) 




1985 


1,008 


0.0738 


1 


>0.70 




1986 


992 


1.8493 


1 


>0.10 




1987 


336 


0.1133 


1 


>0.70 




1988 


616 


0.9336 


1 


>0.30 




1990 


388 


6.0278 


1 


>0.01 


Excess *a in FL 


' Abbreviations are 


used for 


states: AL=Alabama; Fl 


^Florida, LA=Louisiana; MS=Mississippi. 


TX=Texas; MX=M 


>XlCO 










: ' In parentheses { ) 


general ci 


assification of range subc 


lvisions. See 


text 



98 



Fishery Bulletin 92(1), 1994 



in the summer. These authors also tagged fish off 
North and South Carolina, but none were recovered 
in the Gulf. 

According to Fable et al. (1990), 4 king mackerel 
tagged in northwest Florida have been recovered in 
south Florida. Typically, these are the smallest and 
youngest tagged in the southeast United States. 
Sutherland and Fable ( 1980) showed that northeast 
Gulf fish migrated to south Florida. However, addi- 
tional tagging (Fable et al., 1990 4 ) showed that 
northeast Gulf fish eventually moved westward to 
Louisiana, Texas, and Mexico waters when they had 
been free for a sufficient time and grown to a larger 
size. 

Tagging off Louisiana from 1983 to 1985 (Fable 
et al., 1987) indicated that the northwest Gulf may 
have year round residental large king mackerel that 
mix in the warm months with smaller migrants 
from south Florida and Mexico. Recent tagging data 
(Fable et al., 1990 4 ) from this region have provided 
additional recoveries from both south Florida and 
Mexico, strengthening this interpretation. Addi- 
tional support is provided by the occurrence in Loui- 
siana of a year-round king mackerel fishery, whereas 
elsewhere the fishery is seasonal. 

In contrast to historical reports, recent tagging 
(Fable et al., 1990 4 ) showed movements between 
Texas and Mexico. Fish tagged in Texas waters mi- 
grate to both Florida and Mexico. Additionally, fish 
movements between Texas and eastward (as far as 
Panama City, FL) were documented. 

Mark-recapture data (Fable et al., 1990 4 ) from 
tagging in Mexican waters suggest that the states 
of Campeche and Yucatan are wintering areas for 
king mackerel in the western Gulf. Fish tagged in 
warmer months (April-July) in Texas, Tamaulipas, 
and Veracruz were found in Campeche and Yucatan 
in the winter. Tagging efforts (Fable et al., 1990 4 ) 
in Veracruz have provided evidence of northward mi- 
grations to Tamaulipas and Texas in spring and sum- 
mer, and movement to the Yucatan peninsula in winter. 

Additional evidence supporting two Gulf stocks 
can be found in catch-effort data of king mackerel. 
Although the data are complicated by different fish- 
ing strategies depending on the type of fishery (rec- 
reational or commercial) and regulatory closures, 
detailed analysis of catch data from the southeast- 
ern United States charterboat fishery indicated that 
in spring and early summer some stocks of fish si- 
multaneously migrated northward along the west- 
ern and eastern coasts of the Gulf (Trent et al., 
1987b). They also developed the ". . . idea that part 
of the population of large fish remains in the Loui- 
siana area year-round and that the abundance of 
these fish is greatest during cold months." 



The fishery for king mackerel in Louisiana is 
unique among the fisheries in the northern Gulf of 
Mexico in that it is year-round; elsewhere it takes 
place mainly from late spring to late fall. The win- 
ter fishery (commercial hook-and-line) in Louisiana 
began in 1981-82. Distinctive differences character- 
ized winter and spring-fall seasons: 1) the smallest 
fish (both males and females) were caught April to 
October whereas the largest fish were caught be- 
tween November and March; 2) females were more 
abundant in the winter fishery than at other times 
of the year (Trent et al, 1987a). 

For two or more populations to maintain separate 
identities they must be isolated, either physically or 
reproductively (Hartl, 1980). In the case of Gulf king 
mackerel, there is evidence for reproductive isola- 
tion. Grimes et al. (1990) presented a detailed ex- 
amination of the distribution and occurrence of lar- 
val and juvenile king mackerel in the Gulf (based 
on published reports, neuston sampling, and Mexi- 
can trap net and trawl collections). The spawning 
season in the northern Gulf (U.S. waters), as indicated 
by the seasonal occurrence of larvae, is May to Octo- 
ber. Larval collections off Mexico were sparse and of- 
fered little information on spawning seasonality. 

The summer spawning period in the northern 
Gulf was also indicated by seasonal gonadal devel- 
opment of king mackerel (Finucane et al., 1986). 
They reported that reproductive activity occurred 
from May through September; a few fish were re- 
productively active as early as April and as late as 
October. However, spawning dates of January 
through August for Mexican juveniles estimated 
from otolith data showed a bimodal distribution, 
which suggests that spawning seasons in Mexican 
waters are different from those in the northern Gulf 
(Grimes et al., 1990). 

Two of the four collections of juvenile king mack- 
erel in Mexico used by Grimes et al. ( 1990) had tis- 
sue samples (Tampico, July 1986, and Playa Norte, 
Sept. 1986), and we analyzed these samples for 
PEPA-2* variation. Spawning dates of fish in the 
Tampico collection ranged from mid-February to 
mid-April and PEPA-2' a frequency was 0.896. The 
Playa Norte collection's spawning dates ranged from 
mid-April to mid-July and PEPA-2* a frequency was 
0.600 (Table 1). 

Water circulation data for the Gulf of Mexico 
(Salsman and Tolbert, 1963 7 ) and information from 
Trent et al. (1987b), Grimes et al. (1990), Fable et 
al. 1990, 4 along with our data on king mackerel, sug- 



7 Salsman, G. G., and W. H. Tolbert. 1963. Surface currents in 
the northeastern Gulf of Mexico. U.S. Navy Mine Defense 
Laboratory, Panama City, FL, Res. and Dev. Rep. 209, 43 p. 



Johnson et al.: Evidence for distinct stocks of Scomberomorus cavalla 



99 



gest one plausible scenario with regard to king 
mackerel stocks in the Gulf of Mexico. A western 
population exists that winters and spawns in the 
Gulf of Campeche. The Mexican Current serves as 
an entrainment system for its young. As these young 
become older and larger, they are able to cross the 
region of offshore advection and utilize the north- 
ern Gulf area (Texas to Florida) for summer feed- 
ing. This stock of fish has a high PEPA-2*a fre- 
quency and spawns earlier in the year than fish in 
the northern and eastern Gulf of Mexico. No infor- 
mation (tagging, electrophoretic, or reproductive) is 
available on fish of the Yucatan Straits area and the 
Caribbean Sea to evaluate their relation to the west- 
ern Gulf of Mexico fish. An eastern population of 
king mackerel uses the eastern and northern Gulf 
of Mexico area as entrainment systems for its young 
and the northern Gulf (Florida-Texas) as summer 
feeding grounds. The spawning area extends from 
Texas to northwest Florida between April and Oc- 
tober; the majority of spawning probably occurs in 
the northwest Florida-Louisiana area. Tagging stud- 
ies suggest that this stock uses south Florida and the 
southeast coast of Florida as its wintering grounds. 

The Louisiana area is somewhat of an enigma. 
Tagging studies indicate that the area is used by fish 
from both sides of the Gulf, fish are in the area year- 
round, PEPA-2'a frequencies are between the ex- 
tremes of the east and west Gulf, and tag recover- 
ies from winter tagging in Louisiana have been from 
Louisiana and westward, whereas recoveries from 
summer tagging were both east and west of Louisi- 
ana. Additionally, Finucane et al. (1986) suggested 
an earlier distinct peak in gonadal development 
(May) for Louisiana-Mississippi than in northwest 
Florida (August) and in Texas (August). The ques- 
tion still remains: Does the Louisiana area have an 
independent spawning population that utilizes the 
northern Gulf currents for its life cycle? The exist- 
ing evidence (especially tagging) suggests the area 
is not independent; however, information comes 
from larger fish. Thus, the area may be occupied by 
individuals from both sides of the Gulf which may 
or may not reproduce in the area. Further investi- 
gation especially on the younger life stages using other 
methods of analyses may answer this question. 

Another group (stock) of king mackerel that im- 
pinges upon the Gulf of Mexico resources (officially 
recognized by Fishery Management Councils) is the 
Atlantic Migratory Group. This group has a vary- 
ing range from Virginia to southwest Florida de- 
pending on the time of the year (Gulf of Mexico and 
South Atlantic Fishery Management Councils, 
1985). The stock is considered to winter in South 
Florida and ranges along the Atlantic coast to North 



Carolina and South Carolina during the summer. 
The fish probably spawn from May to October with 
a peak in July (Finucane et al., 1986). These fish are 
currently regulated as a group with seasonal south- 
ern boundaries of lat. 25°48'N (the Collier/Monroe 
County line, FL) from 1 April to 31 October and lat. 
29° 25'N (the Volusia/Flagler County line, FL) from 
1 November to 31 March. Tagging information sup- 
ports this separation (Gulf of Mexico and South 
Atlantic Fishery Management Councils, 1985). 

PEPA-2' a allele frequencies are generally low 
(0.00-0.10) along the Atlantic coast as in the east- 
ern Gulf of Mexico. The higher PEPA-2*a values 
(>0.10) occasionally encountered may be the result 
of fish entrapped in water masses coming up the 
coast from outside the east coast of Florida. This 
possibility is suggested by the recovery along this 
coast of drift bottles that were released in the 
Yucatan Straits area (Salsman and Tolbert, 1963 7 ). 

All these stocks need to be further investigated in 
order to be elevated to the status of genetic stocks 
(i.e., completely isolated reproductive populations of 
the same species). 

Conclusion 

Four lines of evidence for a two stock hypothesis for 
the Gulf of Mexico king mackerel have been pre- 
sented. The two stock hypothesis states that the 
Gulf contains a western stock of king mackerel, 
which winters in Mexico and migrates in spring and 
early summer to the northern Gulf (Texas-Alabama), 
and an eastern Gulf stock which winters in south 
Florida and migrates in spring and early summer 
to the northern Gulf. The two stocks mix in the 
northern Gulf during the summer. 

The four lines of evidence are the following: 

1 Dipeptidase (PEPA-2' ) data showing western 
Gulf fish high in *a allele and eastern fish low 
in *a allele. 

2 Mark-recapture data showing movement along 
both sides of the Gulf from south to north. 

3 Catch data indicating simultaneous migrations 
northward on each side of the Gulf in early 
spring and summer. 

4 Estimates of spawning dates suggesting pos- 
sible temporal and spatial differences between 
the northern and southern Gulf. 



Acknowledgments 

Especially helpful in collecting specimens and data 
were staff members of the following organizations: 



100 



Fishery Bulletin 92(1). 1994 



Florida Department of Natural Resources (Tallahas- 
see, FL); Gulf Coast Research Laboratory (Ocean 
Springs, MS); Institute Nacional de la Pesca (Mexico 
City, Mexico); Louisiana State University (Baton 
Rouge, LA); Mote Marine Laboratory (Sarasota, FL); 
North Carolina Division of Marine Fisheries 
(Morehead City, NO; Savannah State College (Sa- 
vannah, GA); Texas Parks and Wildlife (Austin, TX); 
Virginia Institute of Marine Sciences (Gloucester 
Point, VA); and the various laboratories of the Na- 
tional Marine Fisheries Service, Southeast Fisher- 
ies Center (Miami, FL). Special thanks go to B. May, 
Cornell University (Ithaca, NY) for sharing his ex- 
perience with king mackerel with us, to K. M. 
Burns, Mote Marine Laboratory (Sarasota, FL) for 
coordinating field work and obtaining specimens in 
Mexico, and to P. Ramsey, Louisiana Technical Uni- 
versity (Ruston, LA), and to J. Shaklee, Washing- 
ton State Department of Fisheries (Olympia, WA) for 
their helpful suggestions and efforts on our behalf. 



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Abstract. — The spawning 
seasonality, fecundity, and daily 
egg production of three species of 
short-lived clupeids, the sardine 
Amblygaster sirm, the herring 
Herklotsichthys quadrimaculatus, 
and the sprat Spratelloides 
delicatulus were examined in 
Kiribati to assess whether vari- 
able recruitment was related to 
egg production. All species were 
multiple spawners, reproducing 
throughout the year. Periods of 
increased spawning activity were 
not related to seasonal changes in 
the physical environment. Spawn- 
ing activity and fish fecundity 
were related to available energy 
reserves and, hence, food supply. 
The batch fecundity of A. sirm and 
S. delicatulus also varied inversely 
with hydrated oocyte weight. 

The maximum reproductive life 
span of each species was less than 
nine months and averaged two to 
three months. Each species had a 
similar spawning frequency of 
three to five days, but this varied 
more in A. sirm and S. delica- 
tulus. Amblygaster sirm had the 
highest fecundity and potential 
lifetime egg production, but the 
number of eggs produced per ki- 
logram of fish was highest in the 
small sprat S. delicatulus. 

Monthly estimates of the daily 
egg production of each species 
varied with the proportion of the 
population that was spawning. 
Estimates of egg production 
showed little similarity to the fre- 
quency distribution of birthdates 
back-calculated from length-fre- 
quency samples. The distribution 
of back-calculated birthdates con- 
firmed that fish spawned in all 
months, but the proportion born 
each month varied widely from 
species to species and year to year. 
The reproductive strategy of these 
species ensures that successful 
spawning is likely, and so the 
level of recruitment is more de- 
pendent on post-hatching survival 
rates than on egg production. 



Reproductive biology and 
egg production of three species of 
Clupeidae from Kiribati, 
tropical central Pacific 

David A. Milton 
Stephen J. M. Blaber 
Nicholas J. F. Rawlinson 

CSIRO Division of Fisheries. Marine Laboratories, 
RO. Box 1 20, Cleveland, Queensland 4 1 63, Australia 



Manuscript accepted 24 September 1993 
Fishery Bulletin 92:102-121 (1994) 



The sprat Spratelloides delicatulus, 
the herring Herklotsichthys quadri- 
maculatus, and the sardine Ambly- 
gaster sirm are the dominant tuna 
baitfish species in the Republic of 
Kiribati (Rawlinson et al., 1992). 
All three species inhabit coral reef 
lagoons and adjacent waters. 
Sprats school in shallow water 
around reefs and adjacent seagrass 
during the day. Herring also form 
dense schools in shallow water 
along the shoreline and among 
reefs during the day (Williams and 
Clarke, 1983). Unlike the other 
species, sardines school near the 
bottom of the lagoon during the day 
(Conand, 1988). All species disperse 
into the mid and upper waters of 
the lagoon during the night to feed 
and become available to the com- 
mercial fishery. 

A major source of lost fishing 
time by pole-and-line vessels in 
Kiribati has been irregular baitfish 
catches (Maclnnes, 1990). These 
important tuna baitfish species 
have shown large seasonal and 
interannual fluctuations in abun- 
dance since they were first re- 
corded during the 1940s (McCar- 
thy, 1985 1 ; Rawlinson et al., 1992). 
Both A. sirm and H. quadrima- 
culatus disappear from baitfish 
catches for variable periods and 
can be absent for months or years 
(Kiribati Fisheries Division, 1989 2 ). 



Changes in abundance may be 
related to variable or irregular re- 
cruitment, because many clupeoids 
(especially clupeids and engraulids) 
have little capacity to compensate 
for environmental variation during 
the period of peak spawning and egg 
production (Cushing, 1967, 1971). 

Most clupeids, including some 
tropical species, are multiple 
spawners (Alheit, 1989). Multiple 
spawning should be advantageous 
for short-lived species because it 
enables them to maintain rela- 
tively stable population sizes in 
unpredictable environments 
(Armstrong and Shelton, 1990). 
Multiple spawning has been estab- 
lished for few tropical clupeids 
(e.g., Sardinella brasiliensis; Isaac- 
Nahum et al., 1988). Of the three 
major baitfish species in Kiribati, 
only S. delicatulus has been shown 
to be a multiple-spawner (Milton 
and Blaber, 1991). All three species 
are subject to high natural mortal- 
ity in Kiribati (Rawlinson et al., 
1992), thus lifetime egg production 



1 McCarthy, D. 1985. Fishery dynamics and 
biology of the major wild baitfish species 
particulary Spratelloides delicatulus, from 
Tarawa, Kiribati. Kiribati Fisheries Div., 
Tarawa, Kiribati, 53 p. 

2 Kiribati Fisheries Division. 1989. Fisher- 
ies Division 1989 Annual Rep., Ministry 
of Natural Resources Development, 
Tarawa, Kiribati, 38 p. 



102 



Milton et al.: Reproductive biology and egg production of three species of Clupeidae 



103 



may be increased if they spawned multiple batches 
of eggs. 

Egg production of multiple spawning species de- 
pends on reproductive life span, the time between 
spawnings, and the age structure of the population 
(Parrish et al., 1986). Batch fecundity of S. delica- 
tulus varies widely between sites, both within and 
between countries (Milton et al., 1990). In a short- 
lived species such as S. delicatulus (<5 months; 
Milton et al., 1991), reproductive life span may have 
an important influence on potential lifetime egg 
production. 

Batch fecundity of H. quadrimaculatus does not 
appear to vary throughout its distribution, and 
ranges from 4,000 to 10,000 eggs (Marichamy, 1971; 
Hida and Uchiyama, 1977; Williams and Clarke, 
1983; Moussac and Poupon, 1986; Conand, 1988). 
Fish mature at about 90 mm in length at six months 
of age (Williams and Clarke, 1983), and they sur- 
vive for at least one year (Milton et al., 1993). Little 
is known of fecundity and egg production of A. sirm. 
Fecundity of the species is related to length and 
weight, with a mean of 20,000 eggs per batch, and 
individuals probably spawn more than one batch of 
eggs (Conand, 1988). 

Temperate clupeids vary widely in life-history 
parameters (e.g., Clupea spp., Jennings and 
Beverton, 1991). Food availability and environmen- 
tal conditions affect the size and number of eggs of 
Pacific herring (Clupea pallasi) (Hay and Brett, 
1988). Results of studies of temperate clupeoids 
suggest that they do not spawn during periods of 
high food abundance, but store energy as fat for 
later reproductive activity (Hunter and Leong, 1981; 
lies, 1984). There are no similar studies of tropical 
clupeids. Encrasicholina heterolobus, a tropical 
engraulid, does not deplete energy reserves in the 
liver or soma during spawning (Wright, 1990). Fish 
with higher condition factor (K) also had higher 
fecundity. 

Stored energy or fish condition that may influence 
both spawning frequency and batch fecundity have 
a marked influence on egg production and, hence, 
affect subsequent recruitment (Ricker, 1954; 
Beverton and Holt, 1957). Adult reproductive varia- 
tion should strongly influence recruitment in short- 
lived tropical species that have short larval phases 
and rapid growth. An example is S. delicatulus 
which, in the Solomon Islands, live a maximum of 
five months and mature at about two months of age 
(Milton and Blaber, 1991; Milton et al., 1991). 
Amblygaster sirm and H. quadrimaculatus live less 
than two years (Milton et al., 1993) and mature in 
6-12 months (Williams and Clarke, 1983; Conand, 
1988). 



In this study, we examined the variability in re- 
productive biology of the three major baitfishes in 
Kiribati to determine the influence of adult repro- 
ductive variability on subsequent recruitment. Our 
objective was to test the hypothesis that reproduc- 
tive biology of short-lived clupeids is adapted to 
maintaining relatively stable population sizes. We 
determined potential life-time egg production and 
whether estimated egg production is related to the 
frequency distribution of back-calculated birthdates. 



Methods and materials 

Study areas 

The Republic of Kiribati covers an area of 3 x 10 6 
km 2 in the central Pacific ocean and comprises three 
main island groups (Gilbert, Phoenix, and Line Is- 
lands) (see Inset Fig. 1). The Gilbert Island group 
is the most populated, consisting of 16 coral reef 
islands. All islands in the group have a typical ocean 
platform coral reef structure and have been built up 
by scleractinian corals and coralline algae on a sub- 
merged mountain (Gilmour and Colman, 1990 3 ). 
Most atolls consist of small islets lying on the east- 
ern side of a lagoon with an open western side due 
to the prevailing easterly winds. Most typically have 
passages between the islets through which water is 
exchanged. 

The four study sites (Abaiang, Butaritari, Tarawa, 
and Abemema) were typical of islands in the Gilbert 
Island group; all had narrow islets on their south- 
ern and eastern sides, except Abaiang (Fig. 1). La- 
goons were mainly shallow (20-30 m deep), often 
with large areas of intertidal seagrass or sand on 
their eastern sides. Bottom topography of the deeper 
parts of the lagoon was generally smooth, with some 
coral outcrops. Our study sites were similar to those 
described by Hobson and Chess (1978) in the 
Marshall Islands. 

Environmental parameters 

On each sampling occasion, we measured the time 
of collection, sea surface temperature (°C), cloud 
cover (okters), wind direction and speed, and moon 
phase because these factors may be related to 
spawning or recruitment (Dalzell, 1985, 1987; 
Peterman and Bradford, 1987; Milton and Blaber, 
1991). For each site, monthly rainfall data for 1989 



Gilmour, A. J., and R. Colman. 1990. Report on a consultancy 
on a pilot environmental study of the outer island development 
program. Republic of Kiribati. Graduate School of the Environ- 
ment, Macquarie Univ., Australia, 151 p. 



104 



Fishery Bulletin 92(1), 1994 



173°E 



I 
175°E 



177°E 



Butaritari 



Abaiang 
> Tarawa 



Gilbert Is 



2°N- 



(D 



.Abemama 



$><0 



o°- 




<%> <^ 



100 



kms 



1S0°E 



Gilbe rt Is 



,-, < *.r ^Solomon 



Australia 

N 




^Tuvalu 



Fiii 



% 



Figure 1 

Map of Gilbert Islands, Kiribati showing the four study sites 
(Butaritari, Abaiang, Tarawa, and Abemama). Inset shows the ter- 
ritorial boundary of Kiribati, the Gilbert Islands, and their posi- 
tion in the Pacific. 



and 1990 were obtained from the Kiribati Govern- 
ment Meteorological Division. 

Sampling 

Fifty to 1,000 Amblygaster sirm, Herklotsichthys 
quadrimaculatus, and Spratelloides delicatulus were 
collected monthly at one or more of four sites in 
Kiribati (Butaritari, Abaiang, Tarawa, and 
Abemama; Fig. 1) between August 1989 and May 
1991. Additional samples of A. sirm and H. 
quadrimaculatus were collected in November 1988 



and January 1989 from Tarawa. Fish 
were caught by several methods at 
each site. Most samples were collected 
from the commercial tuna baitfish 
catches each month at each site. 
Supplementary samples were ob- 
tained by beach-seining (H. 
quadrimaculatus and S. delicatulus), 
cast-netting (H. quadrimaculatus) in 
shallow water during the day, or gill- 
netting (25- and 38-mm stretched 
mesh) at night near baitfishing opera- 
tions. All fish were preserved in 70% 
ethanol. 

Reproductive biology 

Laboratory studies All fish collected 
from commercial baitfish sampling 
were measured (standard length in 
millimetres), and a subsample of 20 to 
60 specimens weighed (±0.005 g). Go- 
nads, otoliths, liver, and viscera were 
removed and the amount of visible fat 
subjectively estimated. Both ovaries 
from the first 20 females of each spe- 
cies at each site for each month were 
dried of surface moisture, weighed 
(±0.001 g) and stored in 4% formalin- 
seawater for histology. Testes, ovaries 
of other fish, liver, and the soma were 
dried at 60°C to a constant weight. 
Otoliths were used to estimate the 
age (in days) of each fish by methods 
outlined in Milton et al. ( 1993). Addi- 
tional samples offish caught by other 
methods were treated separately, but 
in a similar way. We report only on 
results of studies offish collected from 
commercial samples unless otherwise 
stated. 

For histological preparations, go- 
nads were embedded in paraffin, sec- 
tioned at 9 mm, and stained with Ehrlich's 
haemotoxylin and eosin (McManus and Mowry, 
1964). Gonad maturation stages were defined follow- 
ing Cyrus and Blaber (1984) and Hunter and 
Goldberg (1980), and were similar to those of 
Moussac and Poupon (1986) for H. quadrimaculatus 
from the Seychelles. We staged each gonad accord- 
ing to the relative numbers of cells at each develop- 
mental stage (Young et al., 1987; Table 1), and the 
presence of any post-ovulatory follicles was noted. 
The percentage of each histological section that cor- 
responded to each developmental stage was subjec- 



2°S- 



Milton et al.: Reproductive biology and egg production of three species of Clupeidae 105 





Table 1 


Criteria used for 


staging female gonads of tropi- 


cal clupeids stained with haematoxylin and eosin. 


Stage 


Histology 


(1) Immature 


Chromatin nucleolar stage — 




prefollicle cells surround each 




oocyte 


(2) Developing/resting Perinucleolar stage — 




uniform staining cytoplasm 


(3) Maturing 


Yolk vesicle formation; some 




non-staining yolk (lipid) 


(4) Ripe 


Vitellogenic stage — red- 




staining yolk; developed 




chorion 


(5) Running ripe 


Globular red-staining yolk; 


(spawning) 


oocytes hydrated; develop- 




ment complete 


(6) Spent 


Presence of post-ovulatory 




follicles; cortical alveoli 




present and/or atresian of 




remaining ripe oocytes 



tively estimated. Post-ovulatory follicles were aged 
according to stages found in other multiple-spawning 
clupeoids (Hunter and Goldberg, 1980; Goldberg et al., 
1984; Isaac-Nahum et al., 1988). Gonosomatic indices 
(GSI) were calculated as the ratio of wet gonad weight 
to somatic weight (total weight minus gonad weight), 
expressed as a percentage. Similarly, we calculated a 
hepatosomatic index (HSI) as the ratio of liver dry 
weight to somatic dry weight (total weight minus en- 
tire viscera), expressed as a percentage. 

Length and age at sexual maturity were defined 
as the minimum size and age at which fish had ripe 
oocytes (Stage 4), determined by histological exami- 
nation. Fish that had running-ripe oocytes (Stage 5) 
were recorded as in spawning condition. We defined 
the length and age at first spawning as the small- 
est size where the proportion of running-ripe oocytes 
in the section exceeded 85% for more than 50% of 
the fish of that length or age. We chose this crite- 
rion after examining large numbers of histological 
sections with running-ripe oocytes. In these sections 
they always represented more than 85% of the sec- 
tion area. Our results were similar to that found in 
other tropical clupeoids (Milton and Blaber, 1991). 
The reproductive life span of the population of each 
species at each site each month was determined 
from the oldest fish (Milton et al., 1993) in each 
sample minus the age at first spawning. 

We estimated batch fecundity for each species 
from fish that had been examined histologically and 
had oocytes that were starting to hydrate ( ripe-early 
running ripe; Stages 4-5; Table 1), but we did not 



examine the fecundity of fish with any empty fol- 
licles. An advanced modal size group of oocytes could 
be distinguished in ripe fish. We separated a 
subsample of between half (A. sirm) and all (S. 
delicatulus) of the ovary and weighed it. The num- 
ber of eggs in the advanced mode was counted and 
the fecundity was estimated by multiplying the 
number of eggs in the subsample by the ratio of total 
gonad weight to subsample weight. Fecundity esti- 
mates were made within three to four days after the 
ovary was removed from the fish to minimize the 
potential bias of differential absorption of fixative 
by oocytes and surrounding somatic tissue. 

We used hydrated oocytes from fish caught be- 
tween 2000 and 2330 hours to estimate egg weight. 
Oocyte weights were estimated from hydrated oo- 
cytes in ovaries that were almost ready to spawn 
(late Stage 5; Table 1). We measured oocyte dry 
weight by counting 10 samples of 10 oocytes from 
each ovary, drying the oocytes at 50° C to a constant 
mass and weighing each subsample separately. 

We scored visceral fat on a five-point scale. If a 
fish had less than 25% of the intestine covered in 
fat deposits, it was scored as (1); 25-50%, (2); 50- 
75%, (3); and 75-100%, (4). A fish scored (5) when 
all intestine was covered with fat and deposits were 
also present around the stomach (Nikolsky, 1963). 

The proportion of females examined histologically 
each month that had post-ovulatory follicles (POF; 
Stage 6) was used to evaluate reproductive season- 
ality. We determined that these fish had spawned 
within the previous 15-48 hours, because these 
structures decompose and cannot be recognised af- 
ter that time (Hunter and Goldberg, 1980; Clarke, 
1989). In samples where no fish had POF's, we used 
the proportion of fish in the histological subsample 
whose sections had greater than 85% running-ripe 
oocytes (Milton and Blaber, 1991). We used this 
proportion to calculate monthly estimates of mean 
daily oocyte production and the number of batches of 
oocytes spawned each month (Parrish et al., 1986). 

We estimated daily oocyte production (n/kg of 
adults; egg production index) for samples collected 
from commercial baitfishing, because these samples 
were assumed to be most representative of the popu- 
lation. Our methods were similar to those of Parker 
(1980, 1985), which have been used to estimate the 
spawning biomass of a number of multiple spawn- 
ers (Armstrong et al., 1988; Pauly and Palomeres, 
1989; Somerton, 1990). However, our methods dif- 
fered because we used commercial catch per unit of 
effort (CPUE) as an index of adult abundance. 



Egg production 
index 



^(fiPF.SR^^WiYcPUE (1) 



106 



Fishery Bulletin 92(1). 1994 



where f- is the proportion of females in the ith 
length class, p is the proportion of the sample 
spawning, F is the fecundity of a fish of that length 
taken from the fecundity-length regression, SR t is 
the sex-ratio of the ith length class and W i is the 
total weight of fish in the ith sample. CPUE was 
estimated from the monthly catch returns of the 
commercial fleet. We chose this method of estimat- 
ing egg production because S. delicatulus have de- 
mersal eggs (Leis and Trnski, 1989) and the eggs of 
A. sirm and H. quadrimaculatus are difficult to 
sample adequately in the large areas of suitable 
habitat in each lagoon. 

For comparison with adult spawning data, we 
back-calculated the distribution of birthdates offish 
collected in each length-frequency sample by using 
the growth equations of Milton et al. (1993). Fre- 
quencies in each age class were adjusted for mor- 
tality by using the estimates of Rawlinson et al. 
(1992). The distribution of birthdates was also back- 
calculated for H. quadrimaculatus and S. delica- 
tulus length-frequency samples from previous stud- 
ies at one site (Tarawa) January 1976 to February 
1977 (R. Cross, 1978 4 ) and May 1983 to April 1984 
(McCarthy, 1985 1 ). We used age distribution in these 
earlier studies and those of the present study to ex- 
amine seasonal, annual, and site-related differences 
in the reproductive life span of each species. 

Statistical analyses Inter- and intra-specific differ- 
ences in fat index, HSI and K were examined with 
Fisher's r-tests to account for unequal sample sizes. 
Seasonal and site-related differences in fecundity 
(expressed as oocytes per gram) were examined by 
analysis of covariance with weight as the covariate. 
Hydrated oocyte weight and reproductive life span 
were examined by one-way analysis of variance. 

We examined the relative influence of exogenous 
and endogenous factors on the fecundity of each 
species at each site by stepwise regression (Sokal 
and Rohlf, 1981). We included the following: length, 
weight, age, sea-surface temperature (°C), wind 
speed (in knots), moon phase (expressed by fitting 
a sin/cosin curve to the number of days since the last 
full moon before the sample was taken divided by 
the number of days in a lunar month (29.5) (Milton 
and Blaber, 1991), fish condition (K: weight/length 3 ), 
fat, and HSIC7r ). We retained only those variables 
that significantly improved the fit of the model 
(P<0.05). Because several of these variables were 
correlated, we did a partial-correlation analysis be- 
tween these variables and fecundity, and the results 



4 Cross, R. 1978. Fisheries research notes. Fisheries Division, 
Ministry of Commerce and Inductry, Tarawa, Kiribati, 58 p. 



of the two approaches were compared. If the variable 
most related to fecundity in the stepwise regression 
was not the one most related to fecundity in the par- 
tial-correlation analysis, the stepwise regression model 
was discarded and no relationship was assumed. 

In order to estimate egg production (Eq. 1), we 
estimated the proportion of females in each 5-mm 
length class from the total sample of each species. 
The variance of these estimates was calculated by 
using the normal approximation to the binomial dis- 
tribution (Walpole, 1974). We assessed whether the 
monthly percentage of annual egg production was 
related to the proportion of annual recruitment in 
the same month by rank-correlations (Conover, 
1980). 

The average age of the potential spawning popu- 
lation in each sample was compared by a nested 
analysis of variance with month of sampling nested 
within year. Significant differences between treat- 
ments were identified from comparison of the least- 
squares means of each treatment, as sample sizes 
differed between cells (Sokal and Rohlf, 1981). 



Results 

Environmental parameters 

Sea-surface temperature in Kiribati varied little 
throughout the year. During the study period, tem- 
peratures varied between 29°C and 32°C (Table 2). 
Rainfall varied along the Gilbert Island group; rain- 
fall was higher in Butaritari than at the other sites. 
Some rain fell throughout the study period but was 
more intense during 1990 at all sites. Rainfall dur- 
ing 1989 was below the long-term average at all 
sites and was 16-50% that of 1990. The highest 
rainfall fell during the north-east monsoon (Decem- 
ber-April) at all sites. Winds were mostly light, and 
varied in direction seasonally, blowing from the east 
during the monsoon, but from the south-south-west 
for the rest of the year (Table 2). 

Reproductive biology 

Maturation The length and age at first maturity 
of A. sirm varied between sites (Table 3). Ambly- 
gaster sirm matured younger and smaller in Kiribati 
than elsewhere. Length and age at first spawning 
were much greater than the length or age when fish 
reached sexual maturity, but this size was similar 
to that of fish from northern Australia (Table 3). 
Herklotsichthys quadrimaculatus matured and were 
capable of spawning at 70 mm length and 4 months 
of age (Table 3). The relative size and age at which 
fish matured (as a proportion of maximum size and 



Milton et al.: Reproductive biology and egg production of three species of Clupeidae 107 



age) did not differ among fish 
from the four sites. In Kiribati, 
S. delicatulus become sexually 
mature at 40 mm and two 
months of age and spawn 
shortly afterwards. Compared 
to the other species, the length 
and age at maturity and first 
spawning varied less among 
sites (Table 3). The three spe- 
cies differed in the length and 
age at sexual maturity and 
first spawning. However, as a 
proportion of their maxima, the 
three species were similiar Cu- 
test; P>0.1). All matured and 
spawned at about 70% of maxi- 
mum size and 50% of maxi- 
mum age (Table 3). 



Timing of spawning We iden- 
tified recent spawning by the presence of post-ovu- 
latory follicles in the ovaries. In A. sirm, follicles 
were detected in samples collected between 0100 to 
1630 hours, and new post-ovulatory follicles (iden- 
tified as day-0 [<24 hr]; Hunter and Goldberg, 1980; 
Goldberg et al., 1984) were observed in fish collected 
between 0100 and 0510 hours. Female H. 
quadrimaculatus with post-ovulatory follicles were 
collected between 2130 and 1630 hours and day-0 
follicles were found in samples collected between 
2130 to 0300 hours. In female H. quadrimaculatus 
caught after 0300 hours, follicles could not be dis- 
tinguished from day-1 type POF's, as the follicles de- 
generated rapidly. Similarly, we detected post-ovu- 
latory follicles in female S. delicatulus collected from 
2210 to 1930 hours, and follicles of all females col- 
lected earlier than 0845 hours were identified as 
day-0. Those in females of the single sample col- 
lected later in the day ( 1930) were assigned as day-1. 

Spawning season There was protracted spawning 
in A. sirm with periods of intense spawning activ- 
ity (Fig. 2). During both 1989 and 1990, fish 
spawned August to October and also during May- 
June in 1990. Condition, fat index, and HSI were 
less during spawning periods and reached a peak in 
March-April 1990, i.e., before spawning (Fig. 2). We 
found less fat deposits in spent fish and the fish 
were in poorer condition than fish with gonads in 
other stages of development (P<0.05; Table 4). We 
noted no significant differences in HSI among fish 
with gonads at the same stage of development. 

Herklotsichthys quadrimaculatus spawned 
throughout the study period: 20 to 50%> of the popu- 







Table 2 








Mean water temperature (°C) 


, wind speed (kn), clou 


d cover, and monthly 


rainfall (mm) at four sites 


in 


Kiribati from November 1988 to 


May 1991. 


Parameter 




Butaritari 


Abaiang 


Tarawa 


Abemama 


Water temperature (°C) 




30.2 ± 0.3 


30.2 ± 0.4 


29.5 ± 0.1 


29.9 ± 0.2 


Range 




28-32 


27-33 


29-30 


29-31 


Wind speed (kn) 




2.2 ± 0.6 


4.2 ± 0.9 


5.4 ± 1.2 


2.2 ± 0.2 


Range 




0-7 


0-10 


1-15 


1-5 


Prevailing direction 




East 


East 


East 


East 


Cloud cover (okters) 




2 ± 0.6 


5 ± 0.6 


3 ± 0.5 


1 ± 0.4 


Range 




0-6 


1-7 


0-7 


0-4 


Monthly rainfall (mm) (1945- 


-88 


263 ± 35 


181 + 35 


165 ± 35 


128 ± 33 


Range 




7-908 


0-761 


0-824 


0-728 


Monthly rainfall 1989 (mm) 




184 ± 29 


42 ± 10 


77 ± 23 


36 ± 10 


Range 




51-351 


0-108 


6-235 


3-102 


Monthly rainfall 1990 (mm) 




404 ± 37 


- 


298 ± 51 


202 ± 31 


Range 




195-614 


- 


19-643 


93-402 


Months sampled 




14 


12 


18 


13 



lation spawned each month (Fig. 3). Female condi- 
tion, fat index, and HSI all followed a similar pat- 
tern during the study but did not appear to be di- 
rectly related to spawning activity. Fish in spawn- 
ing condition had the highest HSI, fat, and condi- 
tion values, but these were only significantly greater 
than those of spent fish (P<0.05; Table 4). 

Spratelloides delicatulus spawned almost continu- 
ously throughout the study period but spawning 
varied in intensity (Fig. 4). Peak spawning occurred 
during different periods in each of the years 
sampled. Female HSI and fat index showed a simi- 
lar pattern during the study but monthly changes 
in these parameters or fish condition did not follow 
the spawning cycle. We found no significant differ- 
ences in HSI or fat index for females with ovaries 
in different stages of development (P>0.1; Table 4). 
Fish condition was lower among spent fish than in 
ripe or spawning fish (P<0.05; Table 4). Females 
with ripe ovaries had higher mean HSI, fat, and 
condition than those in other stages of development, 
but these differences were not significant (Table 4). 

Fecundity The relative fecundity of A. sirm and H. 
quadrimaculatus did not differ among sites or sea- 
sonally within sites in Kiribati (ANCOVA with 
weight as covariate; overall P>0.07; Table 5). How- 
ever, the relative fecundity of H. quadrimaculatus 
was significantly different between fish from Tarawa 
and Abemama (<-test; P<0.05). Batch fecundity of both 
species did not differ among sites in Kiribati. Within 
their respective species groups, both species had simi- 
lar batch fecundities to the other species listed, al- 
though their relative fecundities were lower (Table 5). 



108 



Fishery Bulletin 92(1), 1994 



Table 3 

Length and age at sexual maturity and first spawning of Amblygaster sirm, Herklotsichthys quadrimaculatus, 
and Spratelloides delicatulus from various populations throughout their range. (L t = length at maturity, 
L & . = length at first spawning, L max = maximum size, T mal = age at maturity, T f = age at first spawning, 
maximum age, K = Kiribati, I = India, SI = Solomon Islands). 



2 







Length at 


Length at first 




Age at first 








maturity (mm) 


spawning (mm) 


Age at maturity(d) 


spawning (d) 




Species 


Site 


«w/*w> 


a-fip/LmaJ 


(T IT 

mat 1 max) 


^ fsp IT max ) 


Source' 


A. sirm 


Kiribati 


110 (0.50) 


180 (0.80) 


150 (0.29) 


330 (0.65) 


(1) 




New Caledonia 


132 (0.72) 


— 


295 (0.40) 


— 


(2) 




N. Australia 


174 (0.79) 


193 (0.88) 


— 


— 


(3) 




Sri Lanka 


166 (0.88) 


— 


-330 (0.80) 


— 


(4) 


Mean 




146 (0.72) 


— 


— 






H. quadrimaculatu 


8 Hawaii 


80 (0.63) 


90 (0.70) 


160 (0.53) 


190 (0.63) 


(5) 




Marshall Is. 


90 (0.82) 


— 


190 (0.72) 


— 


(6) 




Fiji 


95 (0.78) 


98 (0.80) 


275 (— ) 


294 (— ) 


(7), (8) 




Butaritari (K) 


65 (0.68) 


70 (0.74) 


125 (0.50) 


135 (0.53) 


(1) 




Abaiang (K) 


70 (0.74) 


70 (0.74) 


125 (0.37) 


125 (0.37) 


(1) 




Tarawa (K) 


69 (0.72) 


70 (0.73) 


138 (0.45) 


150 (0.48) 


(1) 




Abemama (K) 


70 (0.64) 


72 (0.65) 


140 (0.34) 


150 (0.36) 


(1) 




New Caledonia 


91 (0.64) 


— 


244 ( — ) 


— 


(9) 




Andaman Is. (I) 


99 (0.81) 


104 (0.85) 


— 


— 


(10) 




Seychelles 


97 (0.71) 


— 


150 (0.30) 


— 


(11) 


Mean 




83 (0.72) 


82 (0.74) 


172 (0.46) 


174 (0.47) 




S. delicatulus 


Fiji 


35 (0.56) 


39 (0.63) 


52 (0.43) 


61 (0.51) 


(7). (8) 




Butaritari (K) 


40 (0.68) 


40 (0.68) 


65 (0.51) 


68 (0.54) 


(1) 




Abaiang (K) 


45 (0.75) 


53 (0.88) 


62 (0.51) 


80 (0.64) 


(1) 




Tarawa (K) 


45 (0.68) 


50 (0.76) 


77 (0.50) 


90 (0.57) 


(1) 




Munda (SI) 


37 (0.58) 


37 (0.58) 


72 (0.47) 


78 (0.51) 


(12), (13) 




Vona Vona (SI) 


37 (0.66) 


37 (0.66) 


68 (0.53) 


72 (0.56) 


(12), (13) 




Tulagi (SI) 


38 (0.60) 


38 (0.60) 


73 (0.55) 


75 (0.57) 


(12), (13) 




Maldives 


38 (0.69) 


40 (0.73) 


90 (0.60) 


97 (0.65) 


(13), (14) 




India 


42 (0.71) 


— 


— 


— 


(15) 


Mean 




40 (0.66) 


42 (0.69) 


70 (0.51) 


78 (0.57) 





' Sources: (1) present study. (2) Conand (1991). (3) Okera (1982), (4) Dayaratne and Gjosaeter (1986). (5) Williams and Clarke (1983), (6) 
Hida and Uchiyama (1977), (7) Lewis et al. (1983), (8) Dalzell et al. (1987), (9) Conand (1988), (10) Marichamy (1971), (11) Moussac anf 
Poupon (1986), (12) Milton and Blaber 11991), (13) Milton et al. (1991), (14) Milton et al. (1990), (15) Mohan and Kunhikoya (1986). 



Using stepwise linear regression, we found that 
fecundity was related to weight in all species (Table 
6; Fig. 5). Fecundity of A. sirm was significantly 
correlated with HSI and fish condition. Fish condi- 
tion, HSI, and fat index were all correlated with 
fecundity in H. quadrimaculatus (Table 6). Fecun- 
dity was significantly correlated with weight and 
condition at two of the four sites. Although, when 
data from all sites were combined, weight and fat 
index were the only significant correlates. 

Fecundity of S. delicatulus varied widely among 
sites, both within Kiribati and among countries 
(Table 5). In Kiribati, relative fecundity was higher 
at Butaritari than at Abaiang (P<0.05), but differed 
less than among sites in the Solomon Islands. Fe- 
cundity did not vary seasonally at any site. Relative 



fecundity of S. delicatulus was highest in New 
Caledonia — significantly higher than at all other 
sites except Butaritari in Kiribati (Table 5). How- 
ever, the relative fecundity of S. delicatulus was 
lower than its congeners, S. gracilis and S. lewisi, 
at sites where they co-occurred (Table 5). 

We found that the fecundity of S. delicatulus cor- 
related strongly with fish weight (Fig. 5). The only 
other factor related to fecundity in S. delicatulus 
was HSI. There was a significant relationship be- 
tween fecundity and HSI at Butaritari and Tarawa 
and when all data were combined. Spawning fish 
had a higher HSI at Butaritari than at other sites 
(2.24 ± 0.13 vs. 1.41 ± 0.08; P<0.001). 

The HSI of male S. delicatulus that had a GSI 
similar to that of spawning females (>5%) was also 



Milton et al.: Reproductive biology and egg production of three species of Clupeidae 



109 



o 

o 



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4 

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j'f'm'a'm'j'j'a's'o'n'd 

1989 



j'F m a'm'j'j'a's'o' 

1990 



Figure 2 

Monthly variation (±95% confidence limits) in (A) 
condition, (B) visceral fat index, (C) hepatosomatic 
index and (D) proportion spawning of female 
Amblygaster sirm from Kiribati between January 
1989 and October 1990. 



5-i 



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Figure 3 

Monthly variation (±95% confidence limits) in (A) 
condition, (B) visceral fat index, (C) hepatosomatic 
index and (D) proportion spawning of female 
Herklotsichthys quadrimaculatus from Kiribati be- 
tween November 1988 and April 1991. 



higher at Butaritari (1.41 ± 0.06; N=57) than at 
other sites (Abaiang HSI=1.07 ± 0.11; N=7; Tarawa 
HSI=0.81 ± 0.09; A/=14). The proportion of male S. 
delicatulus that had GSI greater than 5% was also 
higher at Butaritari (36%) than at other sites 
(Abaiang 17.5%; Tarawa 20%). 

Oocyte weights of A. sirm and S. delicatulus dif- 
fered significantly from site to site (Table 7). In S. 
delicatulus, we found the greatest oocyte weight at 
Abemama and Abaiang — significantly higher than 
at Butaritari and Tarawa (P<0.01). Oocyte weights 
in A. sirm were also higher at Abaiang (P<0.001; 



Table 7). We found no significant differences among 
sites for oocyte weights of H. quadrimaculatus. 

Sex ratio The sex-ratio of A. sirm, H. quadrima- 
culatus, and S. delicatulus changed as fish grew but 
only among the largest length classes of each spe- 
cies were there significant deviations from a ratio 
of 1:1. In all three species, females dominate the 
largest length classes (Fig. 6). In our samples, we 
found significantly more female A. sirm and S. 
delicatulus among fish larger than the length at first 
spawning (180 and 45 mm respectively). With H. 



10 



Fishery Bulletin 92(1), 1994 



Table 4 

Mean hepatosomatic index (HSI: %), visceral fat index (Fat) and condi- 
tion (K: dry weight/length 3 ) of Amblygaster sirm, Herklotsichthys 
uadrimaculatus and Spratelloides delicatulus at different stages of gonadal 
development (SE = standard error ± N = number of females examined). 



Species 



Stage 



HSI ± SE 



Fat ± SE tf(xlO-6)+SE N 



A. sirm 



maturing 0.38 ± 0.06 

ripe 0.43 ± 0.04 

spawning 0.39 ± 0.06 

spent 0.42 ± 0.05 



H. quadrimaculatus 



maturing 
ripe 

spawning 
spent 



0.87 ± 0.08 
0.96 ± 0.06 
1.04 ± 0.07 
0.69 ± 0.04 



S. delicatulus 



maturing 1.41 ± 0.19 

ripe 1.98 + 0.10 

spawning 1.84 ± 0.15 

spent 1.46 ± 0.10 



3.4 ± 0.6 

3.2 ± 0.3 

2.6 ± 0.4 

1.7 ± 0.2 

1.4 ± 0.1 

1.6 ± 0.1 

1.8 ± 0.1 

1.7 ± 0.1 

1.3 ± 0.2 
1.6 ± 0.1 
1 3 • n 1 
1.2 ± 0.1 



4.05 ± 0.25 
4.14 ± 0.07 
4.03 ± 0.13 
2.77 ± 0.13 



;!ii 

16 

6 



3.89 ± 0.05 45 

3.81 + 0.05 127 

3.91 ± 0.05 95 

3.53 ± 0.06 40 



2.36 ± 0.06 
2.51 ± 0.04 
2.46 ± 0.04 
2.28 ± 0.04 



15 
41 
35 
55 



higher lifetime egg production 
at all sites than did co-occur- 
ring S. delicatulus. The num- 
ber of days between successive 
spawnings influenced esti- 
mates of lifetime egg produc- 
tion. Although longer in A. 
sirm, the difference was not 
significant (Table 8). 



quadrimaculatus, females dominated among fish 
over 80 mm (Fig. 6). 

Egg production The number of spawnings per 
month and the daily egg production of all species 
generally followed the pattern of the proportion 
spawning (Fig. 7). We found lower daily egg produc- 
tion in A. sirm than in the other species. During the 
period of maximum spawning activity, A. sirm and 
H. quadrimaculatus spawned up to 20 times per 
month (Fig. 7), and S. delicatulus spawned daily. 

Reproductive life span The reproductive life span 
of A. sirm was significantly longer in Tarawa (60.1 
+ 15.4 days) than at the other sites during 1989-90 
(P<0.01; Table 8). Similarly, we found H. 
quadrimaculatus had a longer reproductive life span 
at Abemama (141.8 ± 30.9 days) than at other sites 
during 1989-91 (P<0.01; Table 8). During the same 
period, the reproductive life span of S. delicatulus 
was similar at all sites (57.5 ± 4.6 days). However, 
the reproductive life span of S. delicatulus at 
Tarawa varied significantly between years; fish 
caught during 1990-91 were not as old as those in 
previous j'ears (P<0.05; Table 8). No corresponding 
pattern was observed in H. quadrimaculatus from 
Tarawa. Herklotsichthys quadrimaculatus and S. 
delicatulus lived significantly longer after maturity 
than A. sirm (P<0.01). 

Our estimates of maximum lifetime egg produc- 
tion of A. sirm were similar at the two sites (Abaiang 
and Tarawa). Herklotsichthys quadrimaculatus had 



Recruitment Amblygaster 
sirm recruited from a single 
protracted period in Kiribati 
during 1989 (March to October; 
Fig. 8). We found a greater pro- 
portion of survivors had been 
born between March and July 
than in all other months except 
September (P<0.05). There 
were insufficient data to com- 
pare monthly egg production 
with recruitment, but the pe- 
riod of highest recruitment corresponded with the 
times of greatest spawning activity. However, this 
did not appear to be directly related to the absolute 
number of oocytes produced (Fig. 7). 

The proportion of H. quadrimaculatus born each 
month differed over the four years (P<0.05; Fig. 9). 
In 1976, the greater proportion were born from 
November to March, while in 1983 over 40% were 
born during July. Fish caught during 1989-90 
showed a different pattern. The highest proportion 
in 1989 were born in May, whereas in 1990 the high- 
est proportion were born in January. Over all 4 
years' data, December ( 15.4% ) and July ( 13.7% ) had 
the greatest mean proportion of births (P<0.05), but 
the July value may be biased by the large value in 
1983 (Fig. 10). Where data were comparable, we 
found no relationship between proportion of annual 
recruitment and monthly egg production (r.=0.70, 
P<0.10, N=6 in 1989; r s =-0.15, P>0.5, N=U in 
1990). 

The proportion of S. delicatulus born each month 
varied considerably among the four years examined 
(Fig. 10). December had the highest proportion of 
births in 1976. In 1983, most fish were born between 
May and August, and a similar pattern was found 
in 1989. By comparison, the distribution of 
birthdates was more evenly spread in 1990 (Fig. 10). 
The months with the largest mean proportion across 
the four years were May (11.2%), June (14.9%), July 
(15.8%), and December (11.9%). We found a nega- 
tive relationship between the proportion of births 
and egg production in 1990 (r s =-0.58; P<0.05, 
7V=10). 



Milton et al.: Reproductive biology and egg production of three species of Clupeidae 



I 1 



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1989 




1990 



Figure 4 

Monthly variation (±95% confidence limits) in (A) 
condition, (B) visceral fat index, (C) hepatosomatic 
index and (D) proportion spawning of female 
Spratelloides delicatulus from Kiribati between 
November 1988 and May 1991. 



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O Ocf 










<4/"o o 


1000 - 




„ooe 





o 


- 











Figure 5 

The relationship between batch fecundity and 
fish weight for (A) Amblygaster sirm, (B) 
Herklotsichthys quadrimaculatus and (C) 
Spratelloides delicatulus from Kiribati. 



Discussion 

The reproductive cycles of A. sirm, H. quadrima- 
culatus, and S. delicatulus in Kiribati are similar to 
that reported for temperate multiple-spawning 
clupeoids (Hunter and Goldberg, 1980; Gil and Lee, 
1986; Shelton, 1987; Alheit, 1989). Most studies on 
multiple spawning clupeoids have been on 
engraulids; these species spawn many batches of 
eggs each year and have variable batch fecundity 
(Alheit, 1989). Our results for H. quadrimaculatus 



and S. delicatulus from Kiribati agree with previ- 
ous reproductive studies of these species in tropical 
areas (McCarthy, 1985 1 ; Moussac and Poupon, 1986; 
Milton and Blaber, 1991). In the tropics, both spe- 
cies spawn throughout the year, but have periods 
when spawning activity is greater. In more temper- 
ate parts of their range, the reproductive season of 
both H. quadrimaculatus and S. delicatulus is 
shorter and coincides with increases in water tem- 
perature in early summer (Williams and Clarke, 
1983; Lewis et al., 1983; Conand, 1988). 



1 12 



Fishery Bulletin 92|l), 1994 









Table 5 










Mean length (mm), age (y 


ears), fecundity, relative fecundity (eggs g ') of Amblyg 


aster sirm, Herklot 


sichthys 


quadrimaculatus, and 


Spratelloides delicatulus and 


other tropical and subtropical clupeids ( 


sardines, her- 


rings, and sprats) (K = 


Ki 


ribati, SI = Solomon Island 


3, I = India, 


P.N.G. = Papua 


New Guinea 


UK = 


= United 


Kingdom, SU = Soviet Un 


ion, G = Germany 


). 


















Length 


Age 


Fecundity 


Rel. fecundity 






Species 




Site 


± SE 


± SE 


± SE 


± SE 


N 


Source 


Sardines 


















Amblygaster sirm 




Abaiang (Kl 


189 ± 5 


0.97 ± 0.03 


18789 ± 2757 


187.1 ± 25.3 


7 


(1) 






Tarawa (K) 


194 ± 1 


1.04 ± 0.03 


20327 ± 1391 


192.0 ± 12.0 


25 


(1) 






New Caledonia 


139-177 


0.90-2.2 


8000-27780 


300.0 ± 16.9 


24 


(2), (3) 


Sardinella brasiliensis 




Brazil 


162 ± 2 


— 


23318 ± 2065 


356 ± 37 


23 


(4) 


S. marquesensis 




Marquesas Is. 


109 ± 6 


— 


4150 + 1000 


— 


6 


(5) 


S. zunasi 




Korea 


75-142 


1-3 


8800-58800 


— 


31 


(6) 


Herrings 


















Herklotsich thys 


















uadnmaculatus 




Hawaii 


80-121 


— 


1155-6296 


160-311 


46 


(7) 






Marshall Is. 


100 + 2 


0.59 ± 0.02 


4755 ± 380 


— 


7 


(8) 






Butaritari (K) 


75 ± 1 


0.45 ± 0.01 


1844 ± 108 


295.5 ± 12.1 


44 


(1) 






Abaiang (K) 


75 ± 1 


0.45 ± 0.02 


1975 ± 133 


317.4 ± 19.3 


27 


(1) 






Tarawa (K) 


76 ± 1 


0.44 ± 0.02 


2353 ± 110 


344.1 ± 10.2 


63 


(1) 






Abemama (K) 


84 ± 2 


0.61 ± 0.04 


3008 ± 207 


319.1 ± 22.7 


33 


(1) 






Andaman Is. (I) 


95-115 


— 


8353 ± - 


— 


19 


(9) 






Seychelles 


88-127 


— 


4500-8000 


— 


24 


(10) 


Opisthonema 


















libertate 




Mexico 


142 ± 1 


— 


57125 + 1850 


553 ± 14 


115 


(11) 


Sprats 


















Spratelloides dehcatul 


us 


Butaritari ( K) 


52 ± 2 


0.27 ± 0.01 


1359 ± 143 


867 ± 55 


1') 


(1) 






Abaiang (K) 


52 ± 1 


0.21 ± 0.02 


973 ± 43 


667 + 35 


7 


(1) 






Tarawa (K) 


54 ± 1 


0.29 ± 0.01 


1255 ± 54 


735 ± 25 


49 


(1) 






Abemama (K) 


41 ± 1 


0.20 ± 0.02 


524 + 95 


702 ± 75 


12 


(1) 






Munda (SI) 


48 ± 1 


0.26 ± 0.01 


799 ± 45 


554 ± 25 


57 


(12) 






Vona Vona (SI) 


49 ± 1 


0.26 ± 0.01 


925 ± 102 


717 ± 45 


28 


(12) 






Tulagi (SI) 


46 ± 1 


0.21 ± 0.01 


926 ± 93 


567 ± 49 


28 


(12) 






New Caledonia 


45 


— 


710 


883 ± 14 


20 


(2) 






India 


40 ± 3 


— 


608 ± 54 


— 


15 


(13) 


S. gracilis 




Munda (SI) 


50 


0.19 


514 


504 


1 


(14) 






Vona Vona (SI) 


37 ± 1 


0.15 + 0.01 


505 ± 51 


882 ± 68 


13 


(12) 






P.N.G. 


53 ± 2 


— 


2592 ± 313 


1690 ± 96 


18 


(15) 






Maldives 


59 ± 1 


0.29 ± 0.02 


1998 ± 137 


1073 ± 54 


33 


(12) 






India 


40 + 5 


— 


790 ± 71 


962 ± 53 


If. 


(13) 


S. lewisi 




Munda (SI) 


44 ± 1 


0.18 + 0.01 


887 + 20 


925 ± 16 


219 


(14) 






Vona Vona (SI) 


42 ± 1 


0.14 ± 0.01 


930 ± 51 


1032 + 36 


62 


(14) 






Tulagi (SI) 


49 ± 1 


0.28 ± 0.02 


1290 ± 84 


1230 ± 69 


29 


(14) 


Sprattus sprattus 




Scotland (UK) 


108 


3 


2729 


187 


64 


(16) 






Baltic Sea (SU) 


121 


1.9 


2174 


232 


46 


(17) 






North Sea (G) 


— 


2 


— 


413 


— 


(17) 


Sources: (li present study, (21 Conand (1988), (3) Conar 


d (1991), (4i Isaac-Nahum 


et al. (1988). (5) Nakamura and Wilson (19701, (6) Gil 


and Lee (19861. (7) Williams 


and Clarke (1983), (8) Hid 


a and Uchiyama (1977), (9) Manchamy (1971), 


(10) Moussac ar 


d Poupon (1986), 


(11) Torres-Villegas and Perezgomez (1988), (121 Miltor 


et al. (1990). (13i Mohan 


and Kunhikoya (1986), (14) Milton unpubl. 


data. 1 15i 


Dalzell (19851, (16) De Silva 


(1973), (17i Alheit (1988). 















Although we found A. sirm also had an extended 
spawning season in Kiribati, the species may not 
spawn throughout the year. Our result differs from 
previous studies that found the spawning season 



lasted two to five months during early summer 
(Conand, 1991) or the monsoon period (Rosa and 
Laevastu, 1960; Dayaratne and Gjosaeter, 1986). 
Neither temperature nor rainfall appear to be the 



Milton et al.: Reproductive biology and egg production of three species of Clupeidae 



I 13 



proximate stimuli for spawning 
of A. sirm in Kiribati. Tempera- 
ture was constant throughout 
the year and rainfall was 
higher at all sites in Kiribati 
between December and April, 
when spawning activity was 
lowest. Most spawning activity 
in this species occurred during 
the second half of the year 
when the prevailing wind di- 
rection changed from east to 
west, associated with the north- 
west monsoon that starts at 
this time (Burgess, 1987 5 ). Our 
limited wind and rainfall data 
did not indicate that increased 
spawning activity in A. sirm 
was related to the shift in 
weather pattern. 

Gonad maturation and 
spawning were also linked to 
changes in fish liver-weight 
(HSI), visceral fat, and condi- 
tion of each species. Either HSI 
or fat index and condition were 
all significantly reduced in 
postspawning fish. Amblygas- 
ter sirm stores energy in the 
viscera rather than in the liver. 
Other multiple-spawning clup- 
eoids also transfer energy from 
stored fat to reproductive tis- 
sue (Dahlberg, 1969; Okera, 
1974; Hunter and Leong, 1981). 
In contrast, spent H. quadrimaculatus and S. 
delieatulus had reduced HSI, which suggests that 
the liver is the energy store utilized during repro- 
duction (Diana and MacKay, 1979; Smith et al., 
1990). Energy stored in this organ would be readily 
available for rapid assimilation; hence, fish could 
spawn multiple batches of eggs rapidly. 

Studies of temperate herring, Clupea harengus, 
have shown that gonad maturation is linked to food 
availability and fat storage (Linko et al., 1985; 
Henderson and Almatar, 1989; Rajasilta, 1992). 
Ovaries of all three species in Kiribati and of S. 
delieatulus in the Solomon Islands (Milton and 
Blaber, 1991) vary in a similar way to herring. 
Milton and Blaber (1991) did not find a direct rela- 
tion between spawning and prey availability. This 
suggests that while gonad maturation in these clu- 

5 Burgess, S. M. 1987. The climate of western Kiribati. New 
Zealand Meterological Service, Wellington, NZ. Miscellaneous 
publ. 188, part 7. 





Table 6 










Stepwise regression of the re 


lationship 


between 


various endogenous 


factors and fish fecundity from sites in 


Kiribati. 


<cv; = 

•efficein 


partial 




correlation coefficient; r 2 = overall corre 


lation cc 


t; P = signifi- 


cance level; N = sample size; 


HSI = hepatosoma 


tic index; All = 


data 


from each site combined). 












Species Site 


Factor 


r 2 
p 


r 2 


P 


N 


Amblygaster sirm Tarawa 


Weight 
HSI 


0.24 
0.20 


0.44 


<0.05 


25 


All 


Weight 
Condition 


0.38 
0.28 


0.64 


<0.001 


32 


Herklotsiehthys Butaritari 


Weight 


0.36 


0.43 


<0.001 


44 


quadrimaculatus 


Condition 


0.07 








Abaiang 


Weight 
HSI 


0.28 
0.11 


0.39 


<0.01 


27 


Tarawa 


Length 

Condition 

Age 


0.58 
0.03 
0.02 


0.63 


<0.001 


63 


Abemama 


Weight 
Fat 


0.62 
0.10 


0.72 


<0.001 


33 


All 


Weight 
Fat 


0.54 
0.03 


0.57 


<0.001 


167 


Spratelloides Butaritari 


Weight 


0.70 


0.76 


<0.001 


19 


delieatulus 


HSI 


0.06 








Abaiang 


no factor 








7 


Tarawa 


Weight 
HSI 


0.37 
0.15 


0.52 


<0.001 


49 


Abemama 


Weight 


0.87 


0.87 


<0.001 


12 


All 


Weight 
HSI 


0.59 
0.07 


0.66 


<0.001 


87 



Table 7 






Mean hydra ted oocyte dry weight of Amblygaster 


sirm, Herklotsiehthys qua 


drimaculatus, and 


Spratelloides delieatulus 


from four sites 


in 


Kiribati (TV = number of fern 


ales examined). 






Hydrated oocyte 






weight ± SE 




Species Site 


(x 10- 4 g) 


N 


A. sirm Abaiang 


4.4 ± 0.5 


1 


Tarawa 


1.5 ± 0.1 


16 


H. quadrimaculatus Butaritari 


2.0 ± 0.2 


36 


Abaiang 


l.S-lll 


12 


Tarawa 


1.6 ± 0.2 


19 


Abemama 


1.9 + 0.2 


26 


S. delieatulus Butaritari 


0.7 ± 0.1 


11 


Abaiang 


1.4 ± 0.2 


12 


Tarawa 


0.8 ± 0.04 


27 


Abemama 


2.2 ± 0.2 


10 



1 14 



Fishery Bulletin 92(1), 1994 




100 110 120 130 140 150 160 170 180 190 200 >200 

Length (mm) 



100 




<30 40 50 60 70 80 90 >90 
Length (mm) 



100 
BO 
60 - 

40 

20 - 

C 




<30 35 40 45 50 55 60 >60 
Length (mm) 

Figure 6 

Ontogenetic change in the proportion female of (A) 
Amblygaster sirm , (B) Herklotsichthys quad- 
rimaculatus and (C) Spratelloides delicatulus (±95"7r 
confidence limits) from Kiribati. 



peids is probably linked to cycles in prey abundance, 
fat storage may reduce the effects of short-term fluc- 
tuations in prey abundance on reproduction. 

Diel timing of spawning events was similar for all 
species. We found new post-ovulatory follicles (day- 
0) in females collected from 2130 hours onwards 
with the greatest proportion detected after 0100. 
This indicates that these species spawn during the 
early part of the night, probably prior to midnight. 
Our results are consistent with previous studies that 
found high densities of A. sirm eggs in the plank- 
ton after midnight (Delsman, 1926; Lazarus, 1987). 
Studies of other sardines (Goldberg et al., 1984; 
Isaac-Nahum et al., 1988; Re et al., 1988) and tropi- 



<o~ 5-, 
o 

.* 4 

c 
o 

D) 
O) 

O , 

_>. 
TO 

Q 



j'f'm'a'm'j'j'a's'o'n'd 



1989 



Avr 



j'f'm'a'm'jjVs'o' 



1990 



Time 




o n c i 

ND J FMAMJ J ASOND J FMAMJ J ASONCJj FMAM 



1989 



1990 



1991 



Time 




t"| i i i i i i i i i i i i n i i i i i n i I i i i ii 

ND J FMAMJ J ASOND J FMAMJ J ASOND J FMAM 



1989 



1990 



1991 



Time 



Figure 7 

Monthly estimates of daily egg production of (A) 
Amblygaster sirm, (B) Herklotsichthys quadrima- 
culatus and (C) Spratelloides delicatulus from 
Kiribati during the study period. 



cal clupeoids (Clarke, 1987) also showed that spawn- 
ing peaked before midnight. 

Length and age at sexual maturity of A. sirm and 
H. quadrimaculatus in Kiribati differed from those 



Milton et al.: Reproductive biology and egg production of three species of Clupeidae 



1 15 







Tab 


e 8 










Mean reproductive life spa 


n (in days) and days between spawning 


of Amblygaster sirm, Herklotsichthys 


quadrimaculatus, and Spra 


telloides delicatulus from four sites 


in Kiribati (TV = number of length- 


frequency 


samples; No. = number of months examined). 






















Days 


Max. lifetime 






Reproductive 






between 


egg 


production 


Species Site 


Year 


life span ± SE 


Range 


N 


spawning Range No. 




(> 10 4 l 


A. sirm Abaiang 


1989-1990 


19.0 + 6.4 


0-66 


L2 






20.0 


Tarawa 


1989-1990 


60.1 ± 15.4 


0-127 


7 






41.6 


Abemama 


1989-1990 


3.2 + 3.1 


0-19 


6 








Overall 1989-1990 


26.7 ± 6.8 


0-127 


25 


6.2 ± 2 


3 1.5-25.9 10 38/ 






H. quadrimaculatus Butaritari 


1989-1991 


47.3 + 15.0 


0-201 


14 






11.9 


Abaiang 


1989-1991 


73.9 + 15.6 


0-201 


17 






12.8 


Tarawa 


1976/83/89-91 


84.1 + 7.8 


0-254 


64 






19.3 


Abemama 


1989-1991 


141.8 + 30.9 


0-286 


12 






27.7 


Overall 


1989-1991 


80.6 ± 8.6 


0-286 


74 


3.1 ± 0.3 1.3-4.7 15 




21.1 


S. delicatulus Butaritari 


1989-1991 


53.6 + 4.6 


24-74 


15 






1.9 


Abaiang 


1989-1991 


49.2 ± 5.1 


21-80 


11 






1.5 


Tarawa 


1989-1991 


66.9 + 10.6 


0-144 


16 






3.5 


Tarawa 


1976 


76.6 ± 10.5 


45-129 


7 






3.1 


Tarawa 


1983/84 


84.3 ± 9.5 


34-152 


16 






3.7 


all 


1989 


90.0 + 13.4 


53-144 


7 






3.2 


all 


1990/91 


51.0 ± 4.1 


0-109 


35 






2.5 


Overall 


1989-1991 


57.5 ± 4.6 


0-144 


42 


5.2 ± 1.8 1-30 16 




3.2 



20 






1989 

(n = 717) 

III  


(%) 


c 


Recruitme 
o 


I III 





l.llllllll.l 


J FMAMJ JASOND 


Time 


Figure 8 


The proportion of Amblygaster sirm (±95% 


confidence limits 1 sampled between August 


1989 and July 1990 born each month in 1989, 


backcalculated from length-frequency samples. 



in other parts of their range (Table 3). We found few 
differences within Kiribati, but both species became 
sexually mature and spawned at much shorter body 
lengths than at other locations. Herklotsichthys 
quadrimaculatus did not grow as large in Kiribati 
as elsewhere (Milton et al., 1993). but the propor- 
tion of maximum size at which this species matured 
was similar throughout its range. Milton and Blaber 
( 1991) found regional differences in length at sexual 
maturity in other small tropical clupeoids; they sug- 



gested these differences were consistent with the 
hypothesis of Longhurst and Pauly (1987) that fish 
of any species living in cooler water will grow to and 
mature at a larger size through the interaction of 
oxygen supply and demand. Our data on H. 
quadrimaculatus is consistent with this hypothesis 
— the other studies were all at sites at higher lati- 
tudes than Kiribati, where the water temperature 
is lower. Also, the proportion of maximum size at 
which fish matured was similar at all locations, 
despite the absolute differences in size at maturity 
in Kiribati. 

By comparison, A. sirm matured at a smaller size 
and grew to a larger size in Kiribati than at other 
locations (Milton et al., 1993). The proportion of 
maximum size at which fish matured was also lower 
than found in previous studies and was less than the 
proportion common to a wide range of clupeoids 
(70%; Beverton, 1963). In response to severe fishing 
pressure, the size and age at sexual maturity of 
several sardine species have been found to decline 
(Murphy, 1977). Presumably, this is because any 
density-dependent effects are reduced during early 
growth (Beverton and Holt. 1957; Ware, 1980). 
Amblygaster sirm can have high or variable adult 
mortality in Kiribati (Rawlinson et al., 1992), 
favouring early maturation (Stearns and Crandall, 
1984). 

Length at first spawning was a similar proportion 
of maximum size for the three species and was con- 



] 16 



Fishery Bulletin 92(1), 1994 



50 


1976 


40 


(n = 13131) 


30 




20 


-| 


10 



■■■■-■■..■II 


50 | 1983 


40 


(n= 1705) 

 


30 




? 20 


 


b 10 

1 ° 


ll_«j 


5 50 


1989 


o 
£40 


(n = 4745) 


30 




20 


m 


10 


___ll...llll 


50 1990 


40 


(n = 2747) 


30 




20 


 


: 


laHlll-l. 


J FMAMJ JASOND 


Time 


Figure 9 


The proportion of Herklotsichthys quad- 


rimaculatus born each month in 1976, 1983, 


1989, and 1990, back-calculated from length- 


frequency samples (95'/ confidence limits of 


all proportions are all less than 1.5%). 



30 


1976 


• 


(n = 3002) 


20 




10 



..lllll — ll 


30 | 1983 


 


(n = 9198) 


20 


I- 


lent (%) 

o o 


l...lll. .1 


fc 
5 30 


_ 1989 




(n = 2014) 


01 20 


l| 


10 


 III 





 ■■lllll— 


30 -i 1990 




(n = 16419) 


20 




10 

o- 


.llllllllll. 


J FMAMJ JASOND 


Time 


Figure 10 


The proportion of Spratelloides delicatulus 


born each month in 1976, 1983, 1989, and 


1990, back-calculated from length-frequency 


samples I95'i confidence limits of all propor- 


tions are all less than 1.59f ). 



sistent with the close relation with maximum size 
found by Blaxter and Hunter (1982) for other 
clupeoids. These authors also noted a latitudinal 
effect; fish from lower latitudes spawned at a 
smaller proportion of maximum size. 

Temperate clupeids (especially herrings, Clupea 
spp.) show a great plasticity in the number and size 
of eggs produced; many species show seasonal, and 
inter-annual, as well as geographic, variation in 
their reproductive outputs (Alheit, 1989; Jennings 
and Beverton, 1991) reflecting energetic resources 
and environmental conditions (Hay and Brett, 1988; 
Henderson and Almatar, 1989). By comparison, the 
tropical herring, H. quadrimaculatus, spawned 
throughout the year and showed negligible tempo- 
ral or spatial variation in fecundity, egg weight, or 
inter-spawning interval. This indicates that egg 
production was almost constant throughout the 



study period and suggests that adult food resources 
and larval survival are predictable or relatively con- 
stant (Sibly and Calow, 1983). 

In comparison to other species, S. delicatulus had 
a higher relative fecundity that was also correlated 
with HSI. Females in spawning condition also had 
a higher HSI at Butaritari. Commercial CPUE was 
highest at this site (Rawlinson et al., 1992) and S. 
delicatulus spawned more, smaller eggs than at 
other sites where relative fecundity was lower. 
These data suggest that the fecundity of S. 
delicatulus may be influenced by the amount of 
energy stored in the liver. This energy store would 
be important in a small multiple-spawning species; 
it would enable the fish to continue spawning dur- 
ing short periods of reduced food supply (Hay and 
Brett, 1988). The length of the inter-spawning in- 
terval has been shown experimentally to be related 



Milton et al.: Reproductive biology and egg production of three species of Clupeidae 



I / 



to food supply in other fish species (Townshend and 
Wootton, 1984). Fish at Butaritari may experience 
a more predictable environment that enables them 
to produce more eggs of smaller size than fish in 
more variable environments. 

In contrast, A. sirm delayed spawning beyond the 
size and age at sexual maturity and did not spawn 
until one year old. As fecundity was related to 
weight, delayed spawning enabled A. sirm to grow 
faster than the other species (Milton et al., 1993) 
and have a higher batch fecundity when spawning 
started. Murphy (1968) hypothesized that delayed 
spawning and longer reproductive life span would 
evolve in response to variable reproductive success. 
However, Armstrong and Shelton (1990) demon- 
strated that, even with a short reproductive life 
span, multiple spawners had a high probability of 
successful reproduction when subject to random 
environmental fluctuations over time. Thus, delay- 
ing spawning would be of adaptive advantage if 
mortality was low (Roff, 1984) because batch fecun- 
dity and lifetime egg production would be increased. 

Our estimates of the reproductive lifespan of A. 
sirm indicate that this species spawns fewer times 
in their lifetime than other species and thus would 
also have less chance of successful spawning than 
other species. Given that this is the longest-lived of 
the species examined, our estimate of overall mean 
lifespan may be biased by the small number of 
months sampled. Large fish may be under-repre- 
sented in small catches and may contribute to un- 
derestimating the reproductive potential of A. sirm. 

Herklotsichthys quadrimaculatus had a longer 
reproductive life span and spawned more frequently 
than did the other species. Reproductive life span 
varied little among sites (except Abemama) and 
there was no significant temporal variation, which 
suggests that survival rates of large adult H. 
quadrimaculatus are fairly constant in Kiribati. 
This is reflected in their life-history parameters, 
which varied little among sites or over time. In con- 
trast, the frequency distribution of back-calculated 
birthdates indicated that overall survival was vari- 
able both between and within years, and was not 
related to monthly egg production. We have no es- 
timates of adult abundance during the study period, 
and so population egg production could not be as- 
sessed. However, the annual CPUE and abundance 
of H. quadrimaculatus in the baitfishery were simi- 
lar in the three years for which both data sets were 
available (Rawlinson et al., 1992). This suggests that 
population size was relatively constant during this 
period. If so, then variation in post-hatching survival 
probably has an important influence on recruitment 
in this species (Smith, 1985). 



The reproductive life span of the smallest species, 
S. delicatulus, was intermediate between the other 
species and varied little among sites during 1989 
and 1990. Unlike H. quadrimaculatus, the reproduc- 
tive life span of S. delicatulus varied between years, 
which suggests that survival rates are not as con- 
stant or as predictable as those of H. 
quadrimaculatus. Potential lifetime egg production 
of each female was only one tenth that of other spe- 
cies, but, because of the larger number of females, 
monthly estimates of daily egg production were 
higher. The distribution of back-calculated 
birthdates varied between years, but a greater pro- 
portion of births fell in May-August, irrespective of 
che pattern of egg production. Annual CPUE of S. 
delicatulus (Rawlinson et al., 1992) was similar in 

1989 and 1990, which suggests that fishing mortal- 
ity had not contributed to the increased mortality 
that reduced the reproductive life span in 1990. 

The reproduction and abundance of S. delicatulus 
may be more directly influenced by its environment 
than are the other species. Adult survival is vari- 
able and low (Tiroba et al., 1990); egg production 
varies, probably in response to food supply, and sur- 
vival to recruitment is unpredictable. Yet the poten- 
tial for successful reproduction with this strategy 
may still be relatively high (Armstrong and Shelton, 
1990). In contrast, H. quadrimaculatus appears to 
be able to offset environmental variability to produce 
a relatively constant supply of eggs. 

The distribution pattern of back-calculated 
birthdates of each species was not consistent among 
species. Months when a higher proportion survived 
differed for each species during all years; months 
with highest mean survival were not the same for 
any species. This suggests that the effects of envi- 
ronmental conditions such as seasonal food avail- 
ability or favorable physical conditions are not the 
same for each species. Alternatively, other factors 
such as predation (Rawlinson et al., 1992) may have 
greater influence on survival to recruitment. Egg 
production by S. delicatulus was positively corre- 
lated to survival rates in 1989 and negatively cor- 
related in 1990. This seems unrelated to fish abun- 
dance as catch rates were higher in 1989 than in 

1990 (Rawlinson et al., 1992). 

Large variations in recruitment, reflected in catch 
rates of the main baitfishes do not appear to be di- 
rectly linked with variations in egg production. All 
spawn in the lagoon for most of the year, and dis- 
tribution of birthdates indicated recruitment in most 
months. Although the absolute level of recruitment 
varied throughout the year, multiple spawning re- 
duces fluctuations in population size due to environ- 
mental variability and should ensure that relatively 



18 



Fishery Bulletin 92(1), 1994 



stable population sizes are maintained. Earlier stud- 
ies of A. sirm and H. quadrimaculatus in Tarawa 
lagoon suggested that these species spend at least 
part of their life outside the lagoon (R. Cross, 1978 4 ; 
McCarthy, 1985 1 ). If this is the case, fluctuations in 
the relative abundances of these species may be re- 
lated to migrations; a better understanding of the fac- 
tors causing large-scale movements is necessary 
before predicting the potential yield of this fishery. 



Acknowledgments 

We thank staff of the Kiribati Fisheries Division for 
assistance with fieldwork during the project. Peter 
Crocos and Jock Young and three anonymous re- 
viewers made constructive comments on earlier 
drafts. This work formed part of the baitfish re- 
search project PN 9003 funded by the Australian 
Centre for International Agricultural Research. 



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Abstract. Determination of 

stock structure for striped dol- 
phins (Stenella coeruleoalba) in 
the eastern Pacific has been prob- 
lematic, because very few speci- 
mens have been available for 
study. We compared length data 
obtained from vertical aerial pho- 
tographs of 28 schools of striped 
dolphins from the northern and 
southern regions of the eastern 
tropical Pacific and found no sig- 
nificant differences in average 
length for adult animals (> 180cm) 
or for adult females, defined here 
as dolphins closely accompanied 
by a calf. Analyses of back-pro- 
jected birth dates for dolphins 
>155cm revealed a broad pulse in 
reproduction extending from the 
fall through the spring; however, 
sample size was inadequate to 
compare timing of reproduction 
between the two areas. Striped 
dolphins measured from aerial 
photographs were longer on aver- 
age than those killed incidentally 
in fishing operations. We found a 
pattern of segregation by size be- 
tween schools that is analogous to 
the separate schools of juveniles 
and adults that are found in the 
western Pacific. We hypothesized 
that the specimen data base may 
be biased because tuna purse- 
seine fishermen in the eastern 
tropical Pacific may selectively set 
on schools composed of younger, 
smaller dolphins. 



Examination of stock and school 
structure of striped dolphin 
(Stenella coeruleoalba) in 
the eastern Pacific from 
aerial photogrammetry 

Wayne L. Perryman 

Morgan S. Lynn 

Southwest Fisheries Science Center 

National Marine Fisheries Service. NOAA 

8604 La Jolla Shores Drive. La Jolla. Calif 92037 



Manuscript accepted 20 September 1993 
Fishery Bulletin 92:122-131 (1994) 



Because striped dolphins, Stenella 
coeruleoalba, are killed incidentally 
in purse-seine fishing for yellowfin 
tuna in the eastern tropical Pacific 
(ETP), the National Marine Fisher- 
ies Service (NMFS) is required by 
the Marine Mammal Protection Act 
(as amended in 1988) to monitor 
trends in their abundance (Holt 
and Sexton, 1989; Wade and 
Gerrodette, in press). To satisfy 
this congressional mandate, infor- 
mation on stock structure is re- 
quired. The determination of stock 
structure for striped dolphins in 
the ETP has been particularly dif- 
ficult because of the small number 
of animals killed in the tuna fish- 
ery and, therefore, small number of 
specimens available for study 
(DeMaster et al., 1992). In the ab- 
sence of morphological, life history, 
or genetic data to provide evidence 
of reproductive isolation, stocks of 
striped dolphins have been identi- 
fied provisionally based on 
discontinuities in distribution. 
With more sighting data from ob- 
servers aboard fishing vessels and 
research cruises, the number of 
proposed stocks has decreased from 
five or six (Smith, 1979 1 ; Holt and 
Powers, 1982) to one (Dizon et al., 
in press) pending availability of 
additional data. 

For this report, we examined 
length data to help clarify the issue 
of stock structure. These data were 



extracted from vertical aerial pho- 
tographs collected during line 
transect surveys and are thus pre- 
sumably free of any "sampling" bi- 
ases associated with the fishery. 
Here, we compare length samples 
from aerial photographs of animals 
from the northern and southern 
stock regions proposed by Perrin et 
al. (1985) for evidence of differences 
in average length or timing of re- 
production. Data were then com- 
pared with measurements avail- 
able from specimens killed inciden- 
tally in purse-seine fishing. We also 
examined the frequency distribu- 
tion of lengths within individual 
schools. These data were used to 
test for size-age segregation, as 
reported for dolphins taken in the 
drive fishery on the Pacific coast of 
Japan (Miyazaki, 1977; Miyazaki 
and Nishiwaki, 1978). 

Methods 

Length measurements were made 
on vertical aerial photographs of 28 
schools of striped dolphins (Fig. 1). 
We photographed the schools with 
a KA-45A military reconnaissance 



1 Smith, T. D. (ed). 1979. Report of the sta- 
tus of porpoise stocks workshop; 27-31 
August, La Jolla, California. U.S. Dep. 
Commer., NOAA, Natl. Mar. Fish. Serv., 
Southwest Fish. Sci. Cent, P.O. Box 271, 
La Jolla, CA 92038. Admin Rep., L.l-79- 
41, 120 p. 



122 



Perryman and Lynn: Stock and school structure of Stenella coeruleoalba 



123 



30' 



20' 



10' 



10' 




20' 



160° W 



150° 



120° 



1 10" 



90» 



80° W 



Figure 1 

Distribution of schools of striped dolphin, Stenella coeruleoalba, (dark circles), from which data were taken for 
this report. Boundaries for northern and southern stocks were taken from Perrin et al. 1985. 



camera mounted below the fuselage of a Hughes 
500D helicopter that was launched from the NOAA 
Ship David Starr Jordan. This photographic sam- 
pling was part of a long-term research effort con- 
ducted by NMFS to monitor trends in abundance of 
dolphin populations in the ETP (Holt and Sexton, 
1989; Wade and Gerrodette, in press). 

The reconnaissance camera was equipped with a 
very fast, medium focal length lens (152 mm) and a 
forward image motion compensation system that 
eliminated the blur normally found in images taken 
from a low altitude, high-speed platform. We used 
Kodak Plus-X Aerecon II (thin-base) film, exposed 
through a medium yellow filter, throughout the experi- 
ment. This filter significantly reduced the amount of 
blue light reaching the film, thus enhancing both the 
contrast and resolution of our photographs. 

The observer sitting in the right front seat of the 
helicopter triggered the camera, controlled cycle rate 
and shutter speed, and adjusted the forward motion 
compensation system. As each firing pulse was sent 
to the camera, a data acquisition system recorded 



the time that the image was captured and an alti- 
tude reading from the helicopter's radar altimeter. 
To check for accuracy in our recorded altitude data 
(A J, we photographed calibration target arrays and 
compared altitude calculated from measurements of 
these known distances with recorded altitude (see 
Perryman and Lynn, 1993). 

We found a consistent bias in A r and used the lin- 
ear regression equation shown below to calculate a 
corrected altitude (AJ for each photograph used in 
this report. 

A c = (A r ) 1.013 - 33.755 (r 2 = 0.993) . 

Length determination 

We reviewed the images of 88 schools of striped 
dolphins photographed from 1987 through 1990 and 
selected the images of 28 schools that provided the 
best combination of image clarity and water pen- 
etration. From this sample, we selected the photo- 
graphic pass over each school that captured the larg- 
est number of dolphins swimming parallel to and 



124 



Fishery Bulletin 92(1), 1994 



very near the surface. Dolphins were not measured 
if either the rostrum or tail flukes were not clearly 
visible or if they were surfacing, diving, or jumping, 
which would make them appear shorter when 
viewed from above. Because there was from 80 to 
90% overlap between adjacent photographs, the 
same dolphin could often be measured in two to four 
photographs. If more than one length was available 
for a dolphin, the largest length was selected, as- 
suming it was the best determination of true length. 
This helped to minimize the reduction in apparent 
length caused by the normal swimming movements 
of the dolphins (Scott and Perryman, 1991; 
Perryman and Lynn, 1993). 

We measured each dolphin from the tip of the 
rostrum to the trailing edge of the tail flukes (Fig. 
2). These points were selected because the fluke 
notch that is used to determine standard length 
(Norris, 1961) was very difficult to see in most of the 
images. For adult specimens, this measurement 
should exceed standard length by 2-2.5 cm (Chivers, 
1993 2 ). The measurements were made on sections 
of the original black and white negatives that we 
captured with a high-resolution video camera and 
transferred to a Macintosh Ilci computer. Image 
enhancement and length measurements were made 
with the aid of the digital image processing and 
analysis program, Image (version 1.37), which was 
developed by the National Institute of Health (W. 
Rasband, Research Services, Bethesda, Maryland). 
The length of each dolphin was determined by mul- 
tiplying its length on the image by the scale of the 
photograph ( scale= A/lens focal length ). 

Data analysis 

Perrin et al. (1985) compared the mean lengths of 
physiologically adult male and female dolphins from 



2 S. Chivers. 1993. Southwest Fisheries Science Center, La Jolla, 
California 92037. unpubl. data. 



■Photo Length- 




putative geographic stocks of several species to pro- 
vide supporting morphological evidence for repro- 
ductive isolation. For our analyses, we used length 
as the criteria for eliminating the youngest dolphins 
from our sample. Based on the length data for adult 
striped dolphins in Perrin et al. (1985) and a review 
of our length sample, we estimated that the mini- 
mum length for adult female striped dolphins in the 
eastern Pacific is about 180 cm. We used this length 
as our first cut-off point, and tested for differences 
U-test) between the means of our length samples 
(<180 cm) from the northern and southern regions 
(Fig. 1). Since the selection of this value was some- 
what arbitrary, we repeated the tests on data sets 
with minimum values of 185 and 190 cm. 

Based on behavioral arguments reviewed in Per- 
ryman and Lynn ( 1993), we assumed that the larger 
dolphin swimming closely alongside a calf was an 
adult female. Since this determination was based on 
behavior and not on examination of sexual charac- 
ters, we qualify the term in quotation marks, "adult 
female," whenever we are referring to a length 
sample based on this assumption. A <-test was used 
to compare the mean lengths of "adult females" from 
the northern and southern regions. We also per- 
formed a power analysis to determine what range 
of differences between means we could expect to 
detect (probability of type II error < 0.10) for this 
analysis and the ones described in the paragraph 
above. 

Calf birth dates 

We examined the length data from striped dolphins 
estimated to be one year old or less for evidence of 
pulses in reproduction (see Barlow 1 1984], for spot- 
ted and spinner dolphins; Perryman and Lynn 
(1993], for common dolphins). Ninety centimeters 
was used as the best estimate of average length at 
birth and 155 cm for average length at one year for 
striped dolphins in the eastern Pacific (Gurevich and 
Stewart, 1979 ;i ). We as- 
sumed postnatal growth was 
linear during the first year 
and back-projected the birth 
dates for all dolphins <155 
cm in length. Our goal here 
was not to determine the ex- 



Photo 



Length 



■Standard Length- 



Figure 2 

Illustration of the difference between points used to determine standard 
length and length as measured from our vertical photographs. 



1 Gurevich, V. S., and B. S. Stewart. 
1979. A study of growth and re- 
production of the striped dolphin 
iStenella coeruleoalba). U.S. Dep. 
Commer., NOAA, Natl. Mar. Fish. 
Serv., Southwest Fish. Sci. Cent., 
P.O. Box 271, La Jolla, CA 92038. 
Final Rep to NOAA, SWFC Con- 
tract 03-78-D27-1079, 29 p. 



Perryman and Lynn: Stock and school structure of Stenella coeruleoalba 



125 



act date of birth for each dolphin but rather to exam- 
ine the distribution of birth dates, based on the same 
assumptions, from the two regions. We used 
Kupier's modification of Kolmogorov's test for com- 
parisons of circular distributions (Batschelet, 1965) 
to compare the calculated distribution of birth dates 
with a uniform distribution. 

Comparisons with specimen data 

We conducted four tests to compare the sample of 
photogrammetric lengths with data collected from 
striped dolphins killed incidentally in purse-seine 
fishing in the ETP (Perrin et al., 1976). The data 
from specimens included the information published 
by Perrin et al. ( 1985) and a small set of data from 
dolphins killed since 1985. T-tests were used to com- 
pare the mean length of "adult females" with the 
mean length of adult female specimens and with the 
mean length of lactating adult female specimens. We 
also compared the mean (f-test) and shape 
(Kolmogorov-Smirnov test) of the photogrammet- 
rically determined length distribution of striped 
dolphins > 180 cm with data from specimens > 180 
cm in length. 

School structure 

Examination of the structure of schools of striped 
dolphins captured in the drive fishery in Japan has 
revealed a distinct pattern of segregation based on 
sex, maturity, and length (Miyazaki, 1977, 1984; 
Miyazaki and Nishiwaki, 1978). Researchers have 
categorized these schools as adult, juvenile, or mixed 
depending on the proportion of juvenile dolphins 
(excluding calves) captured. In these studies, length 
(<174 cm) or age (<1.5 years) was used as the crite- 
rion for eliminating nursing calves from the sample; 
the remainder of the dolphins was determined to be 
juvenile or adult by direct examination of the go- 
nads. 

We examined the length distributions for the pho- 
tographed schools to see if an analogous pattern of 
segregation in schools from the eastern Pacific was 
detectable. We divided our samples into two length 
categories which we labeled juvenile or adult. The 
minimum length for the juvenile category was set 
at 165 cm to eliminate nursing calves as described 
above. We selected this minimum value because 1) 
length at birth for striped dolphins from the ETP is 
apparently about 10 cm shorter than that reported 
from the western Pacific (Miyazaki, 1977; Gurevich 
and Stewart, 1979 3 ), and we assumed that the dif- 
ference in the average length at weaning was ap- 
proximately the same; 2) dolphins larger than 165- 



170 cm in length were very rarely found swimming 
in the characteristic cow/calf configuration we see 
in our photographs. 

We selected 195 cm as the upper bound for the 
juvenile category because this appears to be about 
the minimum size for adult male striped dolphins 
that have been killed in the ETP tuna purse-seine 
fishery (Perrin et al., 1985). This value was keyed 
to male length data because the studies of school 
structure from Japan indicated that a disproportion- 
ate number of the dolphins captured in juvenile 
schools were males (Miyazaki and Nishiwaki, 1978). 
Thus dolphins in each school were categorized as 
juvenile if they were between 165 and 195 cm in 
length and as adult if they were > 195 cm in length. 
The goal in this classification scheme was to create 
one category that would be composed of mostly ju- 
venile and young adult dolphins and another that 
would include mostly adult animals. 

We used chi-square analysis to test the hypoth- 
esis that the number of dolphins in the two catego- 
ries in our schools was independent of school. For 
this analysis, we eliminated schools from which we 
had measured less than 20% of the school or fewer 
than 17 dolphins. The second criterion was estab- 
lished to minimize the number of predicted values 
in the chi-square analysis that were less than five. 
Application of these criteria reduced our sample to 
21 schools for this test. Because the selection of 195 
cm for the cut-off between the two size categories 
probably includes more adult females in the juve- 
nile category than males, we decreased the limit to 
190 cm and repeated the chi-square test. We also 
conducted a regression analysis to determine 
whether the proportion of the measured sample in 
the juvenile category was related to school size. 

With the exception of the power analyses and 
birth date comparison which were done by hand, all 
tests presented in this report were performed with 
the program StatView developed by Abacus Con- 
cepts (Berkeley, CA). Unless noted otherwise, tests 
were considered significant for P values < 0.05. 



Results 

Regional comparisons 

We compared the average length of striped dolphins 
from the northern and southern regions and found 
no significant differences between the samples 
(Table 1; Fig. 3). In tests for differences in mean 
lengths of "adult females" (Fig. 4), no differences 
were found between the regions. Although none of 
the differences was significant, means of the 



126 



Fishery Bulletin 92(1), 1994 



samples from the northern region were generally a 
few centimeters smaller than those from the south, 
a pattern reported by Perrin et al. (1985). This level 
of difference was less than we could detect given the 
available sample and the variability of our data 



Table 1 

Results of r-tests for differences between means 
of length samples from striped dolhin, Stenella 
coerueoalba, from the northern (Nor) and south- 
ern (So) regions. 


Sub-sample (cm) 


n 
Nor/So 


mean (cm) 
Nor/So 


P 

(2-tailed) 


>180 
>185 
>190 
"Adult females" 


160/251 

154/484 

140/450 

19/63 


205.1/205.9 
206.07207. 7 
207.9/209.2 
200.2/204.0 


0.476 
0.138 
0.230 
0.201 



30 
25 • 
20 • 



S 15 H 

o 



10 - 



Northern Region 
n = 202 



I I i I I 



M 



tk 



80 100 120 140 160 180 200 220 240 260 
Length (cm) 



80 
70 
60 
50 

40 
30 
20 
10 

o 



Southern Region 
n = 616 



': 



m 



n p-i r-f 



^=^ 



1 40 



160 180 200 
Length (cm) 



Figure 3 

Distribution of lengths of striped dolphins, Stella 
coeruleoalba, measured from the northern and 
southern regions. 



(Table 2). With this length sample, it appears that 
we can expect to detect differences between means 
that differ by at least 4 cm. 





Table 


2 




Minimum detectable diffe 


rences 


between means 


for ^-tests for 


samples from striped dolphins, 


Stenella coerureoalba, from the 


northern (Nor) 


and Southern (So) regions. 


Beta error set at 0.10. 








Minimum 


Variance 






detectable 


Sub-sample (cm) 


Nor/So 


lvalue 


difference (cm) 


>180 


164.99 
190.11 


1.963 


4.01 


>185 


148.23 
162.59 


1.964 


3.82 


>190 


122.21 
141.94 


1.964 


3.72 


"Adult females" 


53.61 

147.57 


1.292 


9.63 



8 


"Adult Females" - 
n = 19 


— Northern Region 






7 - 










b 










5 












- 


4 - 














3 - 














2 




















1 

n 





















140 150 160 



180 190 200 
Length (cm) 



210 220 230 240 



"Adult Females" 
n = 63 



- Southern Region 



140 150 160 170 180 190 200 210 220 230 240 
Length (cm) 

Figure 4 

Distribution of lengths of "adult females", defined 
here as stroped dolphins, Stenella coeruleoalba, 
closely associated with a calf, measured from the 
northern and southern regions. 



Perryman and Lynn: Stock and school structure of Stenella coeruleoalba 



127 



The sample from the northern region 
was too small to test for a seasonal pat- 
tern in reproduction, but the distribution 
of back-projected births from the south- 
ern region differed significantly from the 
uniform distribution (P<0.01; Figs. 5 and 
6). Reproduction for striped dolphins 
from the southern region appears to be 
broadly pulsed in the fall through spring 
period. 

Photogrammetric and specimen 
data 

Since significant differences between 
length samples from the northern and 
southern regions could not be detected, 
we pooled length data from the two re- 
gions in the tests that follow. We found 
that "adult females" were significantly 
longer (4.8 cm) on average than adult 
females from the specimen data base. 
When the test was repeated by using 
length data for lactating females from 
the specimen data base, the two samples 
no longer differed significantly (Table 3). 
Striped dolphins > 180 cm in length from 
the photogrammetric sample were sig- 
nificantly longer on average than the 
sample based on the same length crite- 
ria from specimen data. We also per- 
formed a Kolmogorov-Smironov test to 
compare the two distributions (Fig. 7) 
and found that they differed signifi- 
cantly (P<0.01). 



Northern Region 



6 - 

5 



R . R 



fl . H , . R fl 






Southern Region 



1 



m 




i 



i! 






lis. 



o 
=1 
< 



Northern and Southern Region 







,fl, .B RTOlfc 



i 



Figure 5 

Distribution of back-projected birth dates for striped dolphins, 
Stenella coeruleoalba, from the northern and southern regions 
and for the two regions combined. 





Table 3 


Results of comparisons between means of length 


data for striped dolphins, 


Stenella coerueoalba, 


taken from specimens (spec) and aerial photo- 


graphs (photo) (f-tests), and the distribution of 


lengths >180cm 


(Kolmogorov-Smirnov \k and si 


test) from these two sources. 




n 


Mean (cml P 


Comparison 


spec/photo 


spec/photo (2-tailed) 


Adult females 






specimen/photo 


50/82 


198.2/203.0 0.007 


Lactating 






specimens/ 






"adult females" 


23/82 


199.8.203.0 0.202 


> 180cm f-test 


256/681 


199.19/205.73 0.0001 


>180cm h and s 


256/681 


Z=3.378 0.0007 



School size and structure 

We performed a chi-square test to determine whe- 
ther the number of dolphins in our two size catego- 
ries were distributed randomly between schools (Fig. 
8) and the hypothesis was significantly rejected 
when the maximum length for the juvenile category 
was 195 or 190 cm (P<0.001). With a maximum 
value of 190 cm, four expected values generated by 
the test were lower than five. When these schools 
were deleted from the test or lumped with adjacent 
schools to eliminate these low expected values, the 
test results remained highly significant. 

When school size was regressed against propor- 
tion in the juvenile category, the slope of the regres- 
sion was not significantly different from zero. Thus, 
in our sample, the proportion of small dolphins in a 
school was not related to school size. 



128 



Fishery Bulletin 92(1). 1994 





100% r 




90% 




80% 








70% \ 


qj 




13 

ST 


60% \ 






LL 


50% 1 


> 




TO 


40% 


3 




3 


30% 


O 






20% 




10% - 




0% ? 




Birth Months 
Figure 6 

Cumulative distribution of back-projected striped dolphin, Stenella 
coeruleoalba, birth dates (solid squares) and those predicted by a uni- 
form distribution of births (open squares). 




D □ 



Length (cm) 

Figure 7 

Length-frequency distributions for specimens of striped dolphin 
Stenuella coeruleoalba, (> 180 cm) taken incidentally in purse-seine 
fishing in the eastern tropical Pacific and striped dolphins sampled 
photogrammetrically that are > 180 cm. Samples from northern and 
southern regions are combined in this figure. 



Discussion 

We found no significant differences in our length 
samples of striped dolphins from the northern and 
southern regions to support a recommendation that 
they be managed as separate stocks. This must be 
tempered by the fact that length differences of a 



scale not detectable in our 
sample, i.e. < 4 cm, could exist. 
The case for two stocks is also 
weakened by the distribution of 
sightings of this species from re- 
cent research vessel surveys 
(Wade and Gerrodette, in press). 
These data indicate that, al- 
though a hiatus in striped dolphin 
distribution exists in the typically 
tropical (high temperature, low 
salinity) inshore habitat centered 
around lat. 15° N, there appears 
to be a broad avenue for movement 
between the northern and southern 
regions in the upwelling modified 
habitat east of long. 110° West (Au 
and Perryman, 1985; Reilly, 1990). 
When we compared our sample 
of lengths for "adult females" and 
dolphins > 180 cm with data from 
specimens killed incidentally in 
purse-seine fishing, we found that 
the means from the photogram- 
metric sample were significantly 
larger (by about 3-6 cm). This 
does not seem unreasonable at 
first glance because our measure- 
ments to the trailing edge of the 
flukes rather than to the fluke 
notch introduces a positive bias in 
the photogrammetric data of 
about 2-2.5 cm. Also, the "adult 
female" category probably in- 
cludes only those females who 
have carried and given birth to a 
live calf, thus eliminating the 
younger, presumably smaller, fe- 
males who are physiologically 
adult but have not yet had a suc- 
cessful pregnancy. However, these 
results for adult females are con- 
trary to previous comparisons of 
photographic and specimen data 
for northern and central common 
dolphins (Perryman and Lynn, 
1993) and eastern spinner dol- 
phins (Perryman, unpubl. data). 
Since the photogrammetric data for all of these taxa 
were collected in the same manner, it seems likely 
that the difference between the two striped dolphin 
samples reflects some form of selectivity in either 
or both sampling systems. 

The schools of striped dolphins that we photo- 
graphed showed a pattern of segregation by length 



Perryman and Lynn: Stock and school structure of Stenella coeruleoalba 



129 



> 
O 

z 

LU 

o 

in 
rr 



35 
30 
25 
20 
15 
10 

5 


35 
30 
25 
20 
15  
10 

5 


35 
30 
25 
20 
15 
10 

5 


35 
30 
25 
20 
15 
10 

5 


35 
JO 
25 
20 
15 - 

10 

5 


35 
30 
25 
20 
15 

10 

5 


35 
30 
25 
20 ' 
15 
10 

5 





SCHOOL 1 

School Size - 79 
No. Measured - 26 



J3- 



M, 



" i 



XL 



SCHOOL 2 

School Size - 222 
No. Measured = 46 



-E3- 




SCHOOL 3 

School Size - 73 
No Measured - 30 

n 




SCHOOL 4 

School Size - 1 73 
No Measured - 16 

1 l , P. 


. 








-^ 





SCHOOL 5 

School Size - 87 
No. Measured = 33 



rrm n i 



IT 



SCHOOL 6 

School Size = 1 S1 
No. Measured ■= 42 


m* 



SCHOOL 7 

School Size - 25 
No Measured = 9 



1 



" n 



100 120 140 160 18 



200 220 240 



SCHOOL 8 

School Size - 56 
No Measured - 29 



SCHOOL 9 

School Size - 86 
No. Measured - 54 

. rv r^V t 



Length 
cated le 



LENGTH (CM) 

Figure 

frequencies for each school of striped dolphi 
ngths of dolphins that were included in the 



SCHOOL 10 

School Size = 23 
No Measured = 1 7 



SCHOOL 11 

School Size = 100 
No. Measured - 10 



SCHOOL 12 

School Size - 54 
No Measured = 29 



la 



SCHOOL 14 

School Size - 46 
No Measured « 30 



ra , n , 




Jfl 






W 




SCHOOL 13 

School Size- 124 


fh .*.m 




im» 




& 



m_ 



100 120 140 



180 200 220 240 



LENGTH (CM) 
8 

ns, Stenella coeruleoalba. Shaded bars indi 
juvenile categeory. 



that is very similar to that reported from the west- 
ern Pacific (Miyazaki, 1977; Miyazaki and 
Nishiwaki, 1978). It also appears that the propor- 
tion of smaller dolphins in our sample of schools is 
not related to school size. Possibly this segregation 



is the explanation for differences between specimen 
and photogrammetric data sets. 

Tuna fishermen select dolphin schools for encircle- 
ment based mainly on the amount of tuna associ- 
ated with the school. Schools of younger/smaller 



130 



Fishery Bulletin 92(1), 1994 



> 
o 

z 

LU 

ZD 

o 

UJ 

rr 

LL 



35 

30 

25 

20 

15 

10 

5 



15 

30 

25 

20 

15 

10 

5 



35 

30 

25 

20 

15 

10 

5 



35 

30 

25 

20 

15 

10 

5 



35 

30 

25 

20 

15 

10 

5 



35 

30 

25 

20 

15 

10 

5 



35 
30 
25 
20 
15 
10 
5 




SCHOOL 15 

School Size- 125 
No Measured  60 




SCHOOL 16 

School Size - 59 
No. Measured = 1 4 



ll 



 .■■ I'll 



SCHOOL 17 

School Size. 100 

No Measured. 51 P 

I 

(71 fT-n MyPI^H 1 


In 



SCHOOL 18 

School Size - 95 
No Measured - 25 



■itti 



1 



SCHOOL 19 

School Size - 88 
No Measuied - 55 


it 



SCHOOL 20 

School Size = 10 
No Measured • 5 






SCHOOL 21 

School Size = 30 
No Measured - 9 




140 160 180 200 220 240 



LENGTH (CM) 



35 

30 

25 

20 

15 

10 

5 



35 

30 

25 

20 

15 

10 

5 



35 

30 

25 

20 

15 

10 

5 



35 

30 

25 

20 

15 

10 

5 



35 

JO 

25 

20 

15 

10 

5 



35 

30 

25 

20 

15 

10 

5 



35 

30 

25 

20 

15 

10 

5 





SCHOOL 22 

School Size - 40 
No Measured - 10 



SCHOOL 23 

School Size- 175 
No Measured - 66 



t>.cwx 



SCHOOL 24 

School Size - 58 
No Measured - 16 



Jl 



l j 



SCHOOL 25 

School Size - 76 R 
No. Measured = 36 

mi m~ 


~ 


h 



SCHOOL 26 

School Size - 48 
No Measured - 30 



XI 



J3L 



im 



SCHOOL 27 

School Size - 23 
No Measured . 9 

S i 



HI 



SCHOOL 28 

School Size - 44 
No Measured = 21 



JGL 




100 120 140 160 180 200 220 240 

LENGTH (CM) 



Figure 8 (Continued) 



striped dolphins might carry more tuna and be cap- 
tured more frequently than schools composed of 
adult animals. If the bond between yellowfin tuna 
and dolphins is related to size and hydrodynamics 
as suggested by Edwards i 1992) then it may be that 
the smaller striped dolphins are hydrodynamically 



more suitable for this association. Juvenile schools 
of striped dolphins are made up of animals that are 
about the same length as schools of spotted or spin- 
ner dolphins for which the tuna-dolphin association 
appears to be the strongest. 



Perryman and Lynn: Stock and school structure of Stenella coeruleoalba 



131 



Acknowledgments 

A. E. Dizon, D. P. DeMaster, W. F. Perrin, and two 
anonymous reviewers read the manuscript and pro- 
vided very useful suggestions. Valuable assistance 
and specimen data were provided by S. Chivers. Sev- 
eral of the photographs for this analysis were taken 
by J. Gilpatrick and R. Westlake. This work would 
have not been possible without the field support of 
the Officers and Crew of the NOAA Ship David 
Starr Jordan and the pilots and mechanics of 
NOAA's Aircraft Operations Center. 



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(eds.), Dolphin societies-discoveries and puzzles, p. 
227-241. Univ. California Press, Berkeley. 

Wade, P. R., and T. Gerrodette. 

In press. Estimates of cetacean abundance and 
distribution in the eastern tropical Pacific. Rep. 
Int. Whaling Comm. 43. 



Abstract. — The eastern Pa- 
cific purse-seine tuna fishery has 
historically been very productive, 
yielding up to 400,000 metric tons 
(t) per year of primarily yellowfin, 
Thunnus albacares, and skipjack, 
Katsuwonus pelamis. However, ef- 
forts to minimize dolphin (prima- 
rily spotted dolphin, Stenella 
attenuata, spinner dolphin, S. 
longirostris, and common dolphin, 
Delphinus delphis) mortality inci- 
dental to tuna seining in the east- 
ern Pacific ocean have been in- 
creasing. Therefore, predictions of 
what the tuna catches will be in 
the future, if there is a ban or 
moratorium on catching dolphin- 
associated tuna, are useful. Based 
on recruitment levels, age-specific 
catchability coefficients for yellow- 
fin tuna caught without dolphins, 
and average fishing effort ob- 
served during 1980-88, we pre- 
dicted that yellowfin catches 
would be reduced by an average of 
about 25%. These results were 
verified by Monte Carlo simula- 
tions, by using average effort and 
randomly selected yellowfin re- 
cruitment and catchability coeffi- 
cients from 1980 to 1988, which 
predicted a mean annual decrease 
of 55,563 t or 24.7% of yellowfin 
catch. The actual reduction in yel- 
lowfin catch might be greater be- 
cause 1) fishing effort will prob- 
ably decline, 2) the range of the 
fishery might be reduced to the 
traditional inshore non-dolphin 
regions, and 3) yellowfin recruit- 
ment could be reduced by the 
change in age structure and popu- 
lation size likely to result from a 
moratorium. Because skipjack sel- 
dom associate with dolphins, redi- 
rection of fishing effort to schools 
of tuna not associated with dol- 
phins would probably result in in- 
creased skipjack catch rates. How- 
ever, the magnitude of the in- 
crease is difficult to estimate, be- 
cause the population dynamics of 
skipjack are poorly understood. 
Finally, this study predicted that 
the catches in the first years after 
a moratorium on dolphin sets 
would not necessarily reflect long- 
term catches. 



Potential tuna catches in the eastern 
Pacific Ocean from schools not 
associated with dolphins 



Richard G. Punsly 
Patrick K. Tomlinson 
Ashley J. Mullen 

Inter-American Tropical Tuna Commission 
8604 La Jolla Shores Dr. La Jolla. CA 92037 



Manuscript accepted 22 July 1993 
Fishery Bulletin 92:132-143 (1994) 



Since the late 1950's, purse-seine 
fishermen in the eastern Pacific 
Ocean (EPO), knowing that schools 
of yellowfin tuna (Thunnus alba- 
cares) often associate with dolphins 
(primarily spotted dolphins, Sten- 
ella attenuata, spinner dolphins, S. 
longirostris, and common dolphins, 
Delphinus delphis), have used the 
dolphins to help locate and capture 
yellowfin. Dolphins are relatively 
easy to detect, being larger and 
closer to the surface than yellowfin. 
In fact, the most efficient means of 
catching the 2- and 3-year-old yel- 
lowfin, which comprise the largest 
component of the tuna catch in the 
EPO, is purse-seine fishing for dol- 
phin associated schools (Punsly 
and Deriso, 1991). Yellowfin remain 
associated with dolphins while the 
net is being set around the dolphin 
herds. The fishermen attempt to 
release all of the dolphins from the 
net; however, incidental mortality 
sometimes occurs through entang- 
lement. 

As a result of increasing public 
pressure to prevent mortality of 
dolphins incidental to tuna purse 
seining, elimination of setting on 
dolphin-associated tunas is being 
considered. Therefore, fishermen, 
biologists, and managers need to 
know the extent to which tuna 
catch in the EPO might be reduced 
by the elimination of sets on dol- 
phin-associated fish. The objective 
of this study was to estimate this 
potential reduction in the catch. No 



such estimates have been pub- 
lished previously. 

Tuna catches could be affected by 
a ban or moratorium on dolphin 
sets in six ways: 

1 The overall catchability of yel- 
lowfin by purse seiners could be 
reduced. 

2 The yield per recruit of yellow- 
fin could decline because non- 
dolphin-associated yellowfin 
caught by purse seiners are 
mostly composed of fish younger 
than the optimum age of entry 
(Calkins, 1965; Allen, 1981). 

3 The average age of yellowfin and 
mean biomass may be reduced 
by fishing on younger age 
groups. This might not only re- 
duce the catch in weight, but 
also reduce the spawning poten- 
tial and possibly the resulting 
recruitment. 

4 Since the offshore EPO purse- 
seine fishery is directed prima- 
rily at dolphin-associated fish 
(Fig. 1, A and B), a moratorium 
on setting on dolphin herds 
could result in a contraction of 
the range of the fishery into in- 
shore regions. The number of 
fish recruited to this new 
smaller area might be lower 
than the number recruited to the 
entire area. Lower effective re- 
cruitment would also result in 
lower catches. 

5 If a moratorium on catching dol- 
phin-associated tuna occurs, 



132 



Punsly et al.: Potential non-dolphin-associated tuna catches in the eastern Pacific Ocean 133 



some purse-seine fishermen 
may decide to move to other 
oceans or retire, which would 
reduce total fishing effort and 
hence the catch. 
6 Since skipjack tuna (Katsuwo- 
nus pelamis), the only other 
primary target species in the 
fishery, seldom associate with 
dolphins, their catch may in- 
crease if effort remains at 
1980-88 levels and is directed 
only toward tuna schools not 
associated with dolphins. 

Because no relation between 
spawners and recruitment of yel- 
lowfin has been established 
(Bayliff, 1992, p. 62), the possible 
effects of reduced recruitment 
were not addressed in this study. 
Also, since the authors cannot 
predict how many seiners would 
leave the EPO, or how much the 
fishery would contract, these two 
factors were not considered. In 
other words, this study only at- 
tempted to estimate how much 
tuna catches might change due to 
changes in yellowfin catchability, 
yield per recruit, total biomass, 
and age structure. 

To measure the possible effects 
of changing the mode of fishing 
from being directed toward prima- 
rily dolphin-associated schools of 
tuna ("dolphin sets," Allen, 1981) 
to one directed at exclusively free- 
swimming schools ("school sets") 
and floating-object-associated 
schools ("log sets," Greenblatt, 
1979), we first estimated what the 
tuna catches would have been in 
previous years if dolphin sets had 
been replaced by non-dolphin 
sets. Then the estimates were 
compared with actual catches. 
Our method used non-dolphin-set 
catchability coefficients and total 
effort to estimate what the 
catches would have been during 
1980-88 if there had been a mora- 
torium on dolphin sets beginning 
in 1980. Other works in which 
catches were estimated for alter- 




Figure 1 

(A) Geographic distribution of average yellowfin tuna (Thunnus 
albacares) catch by purse seiners, during 1980-88, from schools associ- 
ated with dolphins (Delphinidae). Catches are expressed in metric tons 
by 2.5-degree quadrangles. (B) Geographic distribution of average yel- 
lowfin catch by purse seiners, during 1980-88, from schools not associ- 
ated with dolphins. Catches are expressed in metric tons by 2.5-degree 
quadrangles. 



134 



Fishery Bulletin 92(1), 1994 





1 -10 Boat-Days 
CD 11 -50 Boat-Days 
J\ 51 - 100 Boat-Days 

101 -200 Boat-Days 

201 - 500 Boat-Days 

Greater than 500 Boat-Days 



Figure 2 

(A) Geographic distribution of total purse-seiner fishing effort during 
1980-88 which lead to dolphin (Delphinidae) sets. Effort levels are ex- 
pressed in boat-days of fishing by 2.5-degree quadrangles. (B) Geo- 
graphic distribution of total purse-seiner fishing effort during 1980-88 
which lead to non-dolphin sets. Effort levels are expressed in boat-days 
of fishing by 2.5-degree quadrangles. 



native catchability coefficients 
include Holt ( 1958), Jones ( 196 1 ), 
and Bartoo and Coan (1978). 

Materials and methods 
Data 

The Inter-American Tropical Tuna 
Commission's (IATTC) logbook 
and length-frequency data bases 
were used in this study. The log- 
book data base, described in Or- 
ange and Calkins (1981), Punsly 
(1983; with emphasis on set 
types), and Punsly (1987; with 
emphasis on yellowfin catch 
rates), contains information on 
the fishing activities of about 90^ 
of the purse seiners in the EPO. 
Total catches were estimated by 
multiplying the logbook catches 
by the ratio of the sum of the un- 
loading weights to the sum of the 
logbook catches. Geographic dis- 
tributions of the logbook data on 
catch and effort, during 1980-88, 
for both dolphin-associated and 
unassociated schools are shown in 
Figures 1 and 2. The length-fre- 
quency data base, described by 
Hennemuth (1957). Punsly and 
Deriso (1991), and Tomlinson et 
al. (1992), has information from 
samples of about 12-15^ of the 
catch. Age-specific yellowfin abun- 
dances from cohort analysis 
(Pope, 1972; also called sequential 
computation of stock size in 
Ricker, 1975; and virtual popula- 
tion analysis in Gulland. 1965) 
were taken from Bayliff ( 1990). 

Data from 1980 to 19S8 were 
used in this study. Data before 
1980 were not used because of the 
difficulty in modeling the closed 
seasons for yellowfin (Cole, 1980). 
Data after 1988 were not used be- 
cause cohort analysis cannot pro- 
duce accurate abundance esti- 
mates for cohorts which have not 
been in the fishery for a sufficient 
period of time. 

Semi-annual age groups used in 
this study were described in detail 



Punsly et al.: Potential non-dolphm-associated tuna catches in the eastern Pacific Ocean 



135 



in Bayliff (1992, p. 52). Monthly age compositions 
were estimated by combining 1-cm length-interval 
data into semi-annual age groups by fitting 
multinormal distributions to the data with the aid 
of the computer program NORMSEP, (Abramson, 
1971), and constraining the fit to the growth param- 
eters of Wild (1986). "X" and "Y" cohorts were de- 
fined as those fish reaching 30 cm, which correspond 
to the approximate age of first recruitment, during 
the fourth and second quarters of the year, respec- 
tively. Age groups in our study, 0.5 to 5.5 in 0.5 year 
increments, correspond to the Y0, XI, Yl ... Y5 co- 
horts, respectively, in Table 21 of Bayliff (1992). 

Estimates of fishing effort 

The total monthly effort by purse seiners was esti- 
mated as 

E = f Y l\ 

om J om om I .' om ' 

where o, refers to the observed mixture of set types, 
Y is the yellowfin catch unloaded by purse sein- 
ers in month (m),y om is the yellowfin catch reported 
in the IATTC logbooks and f is the effort, in boat- 
days of fishing, reported in the logbooks. Effort on non- 
dolphin sets for all purse seiners was estimated by 



^nm / , / .lnmcs^omcs/y 






v„ 



where f nmcs is the fishing effort which lead to non- 
dolphin (n) sets by monitored vessels of size (s) from 
country (c), Y omcs is the total catch of yellowfin from 
unloadings by size (s) vessels from country (c), and 
y is the total yellowfin catch by monitored ves- 

J omcs J "* 

sels. These estimates were stratified by country and 
size of vessel because the proportion of dolphin sets 
is affected by these two factors. 



Estimation of yellowfin catches if all effort 
were non-dolphin 

This method used age-specific, monthly catchability 
coefficients by fishing mode and allowed the future 
population structure to be affected by previous 
catches. First, age-specific catchability coefficients 
for non- dolphin sets in) in each month (m) were 
estimated for each semi-annual age group (/'): 



Qnmj ~ ^nmj y^nm^ mj J i 



where C are the monthly, total, non-dolphin 
purse-seine catches (in numbers of fish) of semi- 
annual age group (j) and N mj are the age-specific, 
monthly, average abundances estimated by the co- 
hort analysis (Bayliff, 1990). Beginning with the 
population structure in January 1980, obtained from 
cohort analysis, we estimated what the catch in each 
month of each semi-annual age group would have 
been without dolphin sets; i.e., 



pmj 



(N mj q nmj E om )/(q nm] E om + Mj ) 



where Mj is the age-specific, instantaneous, monthly 
natural mortality (Bayliff, 1992, p. 52). Yield in 
weight was estimated by 

Y =W (i)C , 

1 pmj m y J ' pmj ' 

where W(j) is the estimated mean weight of age (j) 
yellowfin in month m caught during 1980-88. The 
subsequent month's abundance of semi-annual age 
group (j) was estimated to be 



Estimates of skipjack catches if all effort 
were non-dolphin 

Skipjack are suspected to be mostly transient in the 
EPO (Joseph and Calkins, 1969), so we assumed 
that depletion is probably unimportant. Thus, the 
ratio of the total effort to the non-dolphin effort was 
used to estimate skipjack catches: 



Y pm (SJ): 



Y nm (SJ)E om /E nn 



where Y m (SJ) is the potential (p) non-dolphin, skip- 
jack catch and Y nm (SJ) is the actual non-dolphin-set, 
skipjack catch. In essence, skipjack catches were 
estimated to be linear extrapolations of catch rates 
to higher levels of effort. 



£*m+Xj mj 



-iq nm .E om+ M,) 



except for the months of recruitment (May and 
January), when N JAN2 and N MA y, 3 were set e Q ual to 
the historical recruitment previously estimated for 
that time period by cohort analysis. Yellowfin form 
the first semi-annual age group (those fish hatched 
in the middle of the current year) were not included 
in the analysis because they were not recruited until 
the next year, when they became semi-annual age 
group 3. Each January, the semi-annual age groups 
were graduated as follows: 



N JANJ+2 =N 



DEC. J 



iaDEi ' 



 +M, 



136 



Fishery Bulletin 92(1). 1994 



Monte Carlo simulation 

The age-structure method produced catches specific 
to the observed time-series of recruitment and age- 
specific catchability coefficients during 1980- 88. 
Additional information can be gained by estimating 
what the trend in catches would be if the recruit- 
ment and catchability trends were different. In or- 
der to explore the range of resulting catches which 
might have occurred under various conditions, a 
Monte Carlo simulation was used. Paired simula- 
tions were performed for both the observed mixed- 
mode fishery and a fishery in which all effort was 
directed toward non-dolphin-associated tuna. Fre- 
quency distributions of differences between catches 
from the two simulated fisheries provide a more 
comprehensive estimate of future expectations. 

The simulations used quarterly time steps and 
1,000 replicates. At each quarter of each year in each 
replicate, a year between 1980 and 1988 was ran- 
domly selected with replacement (i.e., each year 
could be selected more than once). Pairs of quarterly 
catchability coefficients (one from the observed mix- 
ture of fishing modes and one for the non-dolphin 
sets only) estimated for the corresponding year, were 
used in the calculations during the time steps. Quar- 
terly coefficients were calculated with the same 
equation as that for the monthly coefficients with 
months replaced by quarters. Quarterly fishing ef- 
forts were set to the 1980-88 averages. The same 
average total effort was applied to both the observed 
and non-dolphin fishing-mode models. 

Recruitment was simulated to occur in the second 
and fourth quarter. For each year in each simula- 
tion, a randomly selected year was chosen. Recruit- 
ment pairs (X and Y) from the randomly selected 
year were used for both fishery models. Initial popu- 
lation sizes and age structures were also set to the 
1980-88 averages. 

One thousand differences between the simulated 
catches for the mixed- mode and non-dolphin only 
scenarios were generated for a time series of nine 
years. The 95% confidence intervals corresponded to 
the 50th and 950th highest differences from the 
1,000 simulations. Because yellowfin usually live for 
less than 5 years (Fig. 3), results for the last (9th) 
year were unaffected by the initial age structure. 

Results 

Deterministic approach 

If trends in total effort, recruitment, and non-dol- 
phin-set catchability coefficients had been the same 
as during 1980-88, with all effort directed at non- 
dolphin sets, yellowfin catches (Table 1, column 



Table 1 

Estimated annual tuna (Scombridae) catches by 
purse seiners in the eastern Pacific ocean, in 
thousands of metric tons. 



Year 


OYF 


NYF 


QYF 


OSJ 


NSJ 


OT 


QT 


NT 


1980 


170 


129 


158 


131 


155 


301 


313 


284 


1981 


190 


152 


146 


120 


151 


310 


297 


303 


1982 


134 


111 


120 


99 


129 


233 


249 


240 


1983 


104 


96 


98 


58 


73 


162 


171 


169 


1984 


155 


103 


125 


HI 


90 


215 


215 


193 


1985 


227 


132 


169 


49 


99 


276 


268 


231 


1986 


286 


193 


168 


64 


113 


350 


281 


305 


1987 


285 


243 


195 


62 


120 


347 


314 


363 


1988 


303 


266 


229 


85 


123 


388 


352 


389 


Mean 


206 


158 


156 


81 


117 


286 


274 


275 



OYF 
NYF 



yellowfin tuna iThunnus albacares) - observed mixture 
of set types. 

yellowfin tuna - all effort directed at non-dolphin 
( Delphimdae) sets, using the observed monthly 
catchability coefficients for non-dolphin sets. 

QYF = yellowfin tuna - all effort directed at non-dolphin sets, 
using the average, observed, quarterly catchability co- 
efficients for non-dolphin sets. 

OSJ = skipjack tuna {Katsuwonus pelamis) - observed mixture 
of set types. 

skipjack tuna - all effort directed at non-dolphin sets, 
yellowfin plus skipjack tuna - observed mixture of set 
types. 

yellowfin plus skipjack tuna - effort directed at non-dol- 
phin sets, using quarterly average catchability coeffi- 
cients. 

yellowfin plus skipjack tuna - all effort directed at non- 
dolphin sets, using monthly catchability coefficients. 



NSJ = 
OT = 

QT = 



NT 



NYF) were estimated to have averaged 77% of the 
observed catch (Table 1, column OYF). The range 
was from 58% in 1985 when dolphin-associated tuna 
fishing was good to 93% in 1983 when dolphin-as- 
sociated tuna fishing was poor. The reasons why the 
ratio of estimated catch without dolphin sets to the 
observed catch varied annually can be seen in Fig- 
ures 3-7. For example, the high estimated bio- 
masses of 1.5-year-old yellowfin in 1988 (Fig. 4), 
coupled with their high non-dolphin-set catchability 
coefficients (Fig. 5), produced an estimated catch of 
266,000 t for all effort directed at non-dolphin sets, 
which was almost as high as the 303,000 t catch 
estimated from the catchability coefficients for the 
observed mixture of set types (Fig. 6). Catchabilities 
could have increased in 1988 for a variety of reasons, 
including the use of deeper nets, the use of "bird 
radar" (relatively new radar used for detecting birds 
which commonly have tuna beneath them) or envi- 
ronmental factors, such as a shoaling of the ther- 
mocline (Green, 1967). For a given level of effort, 
catches depended on the age-specific abundances 
(Figs. 3 and 4) and catchability coefficients (Figs. 5 
and 6). Consequently, the estimated catches if all 
effort were directed at non-dolphin sets approached 



Punsly et al.: Potential non-dolphin-associated tuna catches in the eastern Pacific Ocean 



137 



1 

- 



y 
Vi 
< 

Z 

21 



1 — i — r 


- 1 — i — i — i t i i i 


'■rff 


Rtk  


\aL 


~K_ ; 


'■■All 


TK : 


: -^z 


TK '■ 


'■ H~ 


Ht^ 


r-| 






-n-n-^ : 


-r^TTTTT^_ 



1982 
1981 

1980 




Figure 3 

Estimated average annual biomasses (t) of yellowfin tuna (Thunnus albacares) 
by semi-annual age group for the observed mixture of set types. In the left panel, 
biomasses are summarized by age within year. In the right panel, biomasses 
are summarized by year within age group. Age refers to the age in years at the 
middle of the year. 



-nSl 



- 
 



V) 

-T. 

< 
z 



rrrihTh-w 



JH 



r-TTfl ITr-^- 



r^TTTl^. 




1988 



1986 



1984 

1983 
1982 
1981 
1980 



VI 

< 

Z 

3 




-1 1 T 1 1 - 



: rrr^r4~m 



: rr>^rn HI 



r^m 



nrrrrrj 



I I I I 1 I I 



- AGE 5.5 



AGE 5 . C 
AGE 4 . 5 
AGE 4 . C 

AGE 3.5 



AGE 1 . 
AGE 0.5 



Figure 4 

Estimated average annual biomasses (t) of yellowfin tuna (Thunnus albacares) 
by semi-annual age group for all effort directed at non-dolphin (Delphinidae) 
sets. In the left panel, biomasses are summarized by age within year. In the 
right panel, biomasses are summarized by year within age group. Age refers to 
the age in years at the middle of the year. 



Fishery Bulletin 92(1), 1994 



J 




0. 



JTw-lhTr 



- 1987 




^-TTH rTfTH^ : 



r^Vn-rr-ITln 




^TH^rrT~r-^l 



' rT^-r^-fT^l 



1980 



_□=. 



rm-vj 



rThmT> 



TTT 




1:JJlHJJ1l. 



rT-mll-r 



n,^ 



.□L 



AGE 5 . 5 

AGE 5 . 

AGE 4 . 5 
AGE 4 . 
AGE 3 . 5 



Figure 5 

Average annual non-dolphin-set yellowfin tuna (Thunnus albacares) 
catchability coefficients (q in boat-days - ^) by semi-annual age group. In the 
left panel, coefficients are summarized by age within year. In the right panel, 
coefficients are summarized by year within age group. Annual catchability 
coefficients are estimated as the mean of the monthly coefficients. Age re- 
fers to the age in years at the middle of the year. 



=r£ 



^^fn-u 



-mW^ 




■j-ri~H—i 



1983 
1982 
1981 

1980 



JZL 



oiEt£^d 



rffl 



FT-fTM I rh : 



-■■i  '' I ' I 



AGE 5 . 5 
AGE 5 . C 



AGE 3 . 
AGE 2 . 5 
AGE 2 . 
AGE 1 . 5 
AGE 1 . 
AGE . 5 



Figure 6 

Average annual observed yellowfin tuna (Thunnus albacares) catchability coef- 
ficients (<? in boat-days -1 ) by semi-annual age group. In the left panel, coeffi- 
cients are summarized by age within year. In the right panel, coefficients are 
summarized by year within age group. Annual catchability coefficients are es- 
timated as the mean of the monthly coefficients. Age refers to the age in years 
at the middle of the year. 



Punsly et al.: Potential non -dolphin-associated tuna catches in the eastern Pacific Ocean 



39 



< 1 — i — i — i — i — i — i — r 


pJU i i 


■• , — r-r 


I — | 


: : r-r 


~L : 


^ ^rfK : 




-i  


? rT 


"V 


> rfff 


Ti  


n i ^-T -1 — ' — ' 


h - 


>•— 1 — i — i ' l ' l ' l ' J l 


Ctbi 



. 1988 

1987 
1986 

1985 

1984 

1983 

1982 
1981 
1980 



— i — i — i — i — r- 

IZI B- 



I ! T I 



n^Tr-r^ 



o. 



Oil 



□£l 



TI 



- AGE 4 . 



r^ 



OZL 



TTT-rL 



J~ r— r 



~1 1 1 I~~I 1 1 ! T- 



AGE 5.5 



AGE 5.0 



AGE 3.5 

AGE 3 . 
AGE 2.5 
AGE 2 . 
AGE 1 . 5 
AGE 1.0 
AGE . 5 



Figure 7 

Average annual differences between the observed and non-dolphin (Delphinidae) 
catchability coefficients (boat-days -1 ). In the left panel, differences are summa- 
rized by age within year. In the right panel, differences are summarized by year 
within age group. Age refers to the age in years at the middle of the year. Nega- 
tive values (those pointing down) indicate that those non-dolphin-set catchability 
coefficients were greater than the observed coefficients. 



the observed levels when the non-dolphin-set 
catchability coefficients were greater than or equal 
to the observed overall catchability coefficients 
(Fig. 7, negative values) for the age groups of the 
greatest biomass (Figs. 3 and 4). Estimated total yel- 
lowfin plus skipjack catches, if all effort were di- 
rected at non-dolphin sets, ranged from 84% during 
1985 to 104% in 1983. 

Estimates (Table 1, column QYF) of what the 
catches would have been without dolphin sets, us- 
ing the quarterly average (over years) non-dolphin- 
set catchability coefficients for 1980-88, indicate 
that yellowfin catchabilities on non-dolphin sets 
increased in the late 1980's. Average quarterly 
catchability coefficients produced noticeably higher 
catches than the observed non-dolphin-set monthly 
coefficients in 1983-85 when the observed coeffi- 
cients on small fish were low. On the other hand, 
average quarterly catchability coefficients produced 
lower catches during 1986-88, when the observed 
non-dolphin-set coefficients were high. 

Monte Carlo simulation 

The Monte Carlo simulations (Table 2) predicted 
that, if total effort, recruitment, and non-dolphin-set 



catchability coefficients had varied randomly 
throughout their 1980-88 distributions, and current 
levels of effort and recruitment had been main- 
tained, changing to a fishery with all effort directed 
toward non-dolphin sets would have resulted in an 
average reduction of 55,563 t (24.7%) of yellowfin 
catch per year. The 95% confidence interval, based 
on the 50th and 950th highest simulated differences 
was 24,000 to 91,000 t (10%-42%). The entire fre- 
quency distribution of the differences between the 
two fishing-mode models in the 9th year is shown 
in Figure 8. Simulated recruitment estimates were 
selected from the observed values during 1980-88. 
Thus, average recruitment used in the simulations 
was higher than the mean actual recruitment to the 
initial 1980 population structure, which was partly 
a result of the poor recruitment during 1978 and 
1979. Consequently, simulated catches were higher 
for both the observed mixed mode fishery (229,000 
t per year) and the non-dolphin-set only fishery 
(175,000 t). 

Yield per recruit 

Estimated yellowfin catches from both the determin- 
istic approach (Table 1) and the Monte Carlo simu- 



140 



Fishery Bulletin 92(1), 1994 



■j. 



a. 
Oj 

IX 

o 
o 
o 

r-i 

E 

c 



>> 
u 

c 

OJ 
3 
CT 
U 

L- 



250 



200 



150 



100 



50 




50 60 70 80 90 100 110 
Yellowfin Catch Retained (%) 

Figure 8 

Frequency distribution of the percent of the yel- 
lowfin tuna (Thunnus albacares) catch in weight 
retained in the ninth year of a ban on dolphin 
(Delphinidae) sets, from 1,000 Monte Carlo simu- 
lated replicates. The percent of catch retained is 
calculated as 100x (the catch if all effort were 
directed at non-dolphin sets) / (the catch from the 
observed mixture of set types). 











Table 


2 










Monte-Carlo 


simulated annual yellowfin tu 


na (Th 


/ n n u s 


albacares) 


catch 


es, in 


thousands of tons, from 1980- 


-88, quarter 


y, average 


catchability coefficien 


ts. 














YEAR 


OYFM 


OYFL 


OYFU 


NYFM 


NYFL 


NYFU 


PCM 


PCL 


PCU 


1 


202 


184 


229 


150 


121 


186 


72 


ill 


S3 


2 


215 


183 


247 


164 


127 


205 


76 


62 


89 


3 


227 


183 


276 


170 


129 


217 


76 


59 


91 


4 


229 


183 


283 


175 


131 


223 


71) 


68 


ss 


5 


236 


188 


2H6 


181 


139 


230 


76 


r,!i 


91 


6 


245 


195 


302 


187 


138 


241 


76 


ill 


91 


7 


237 


ISO 


294 


180 


138 


229 


75 


59 


90 


8 


231 


182 


281 


176 


134 


228 


76 


58 


91 


9 


229 


1S1 


279 


174 


131 


222 


75 


58 


90 


OYFM 


= mean veilowfin tuna catch 


*or the observed mix 


;ure of se 


t tvpes. 






OYFL 


= OYFM Iowei 959! 


confidence interval. 












OYFU 


= OYFM 


upper 959! 


confidence interval 












NYFM 


= mean yellowfin tuna catch using total 


effort and 


non-dolphin catchability 


coeffi- 




cients. 


















NYFL 


= NYFM lower 95% 


confidence interval 












NYFU 


= NYFM 


upper 959c 


confidence interval 












PCM 


= mean 


percent of c 


atch retained 1 100 x 


NYFM/OYF: 








PCX 


= PCM 1 


awer 95% confidence 


interval. 












PCU 


= PCM l 


pper 95% confidence 


interval. 













lations (Table 2) were heavily influenced by the re- 
cruitment and fishing effort levels used. Recruit- 
ment in the future may be different from that of 
past, because of changes in population size, age 
structure, and environmental factors. Therefore, 
actual future catches could be different from what 
we estimated. For these reasons, results in terms of 
reduction in yield per recruit are of interest. We 
estimated that the change to non-dolphin sets only 
would result in the reduction of the yield per recruit 
of yellowfin from the observed value of 2.8 kg per 
recruit to 2.1 kg as shown in Figure 9. In addition, 
effort levels could change in the future, perhaps as 
a reaction to the moratorium. Therefore, estimates 
of yield per recruit for various levels of effort might 
be useful. If effort levels change in the future, the 
multipliers on the X-axis in Fig. 9 could be used to 
estimate the potential yellowfin catch. 



Discussion 

In order to predict what the tuna catches might be 
in the future if there were a moratorium on dolphin 
sets, we estimated what the tuna catches would 
have been during 1980-88, had there been a mora- 
torium on dolphin sets beginning in 1980. Using 
these estimates to predict future catches required 
the following assumptions: 



1 Age-specific, non-dolphin 
catchability coefficients will 
be the same in the future 
as during 1980-88. 

2 Fishing effort will remain 
at 1980-88 levels. 

3 The geographic distribution 
of effort will be the same as 
during 1980-1988 (Fig. 2, A 
and B combined). 

4 Recruitment will be at 
1980-88 levels. 

5 Natural mortality will not 
change in the future. 

6 Skipjack abundance will 
not significantly change. 

Significant deviations from 
these assumptions could make 
our estimates less valid. There- 
fore, the potential ramifications 
of deviations from the assump- 
tions are discussed in detail below. 

Major changes in the vulner- 
ability of non-dolphin-associ- 



Punsly et al.: Potential non-dolphin-associated tuna catches in the eastern Pacific Ocean 



141 



*: 



8 

OC 1.5 

S 

a. 
■o 

O 1.0 



ated yellowfin to purse seiners could 
result in significantly different catches 
than we estimated. Allen and Punsly 
(1984) showed that both environmental 
and vessel efficiency factors affect the 
catchability of yellowfin by purse sein- 
ers in the EPO. Improvements in vessel 
efficiency could increase future 
catchability coefficients; whereas, envi- 
ronmental factors could produce either 
higher or lower catchability coefficients 
than those observed during 1980-88. 
Environmental factors affecting 
catchability could conceivably mask the 
effects of a moratorium on dolphin sets 
for several years. For example, if a 
moratorium on dolphin sets had been 
imposed at the beginning of 1983, the 
low catch in 1983 would have made it 
appear that the decline resulted from 
the moratorium. However, we predicted 
that a moratorium would have had the 
smallest effect in 1983 (Table 1). Fish- 
ermen, biologists, and managers should 
be aware that catches during the first year after a 
moratorium starts may not be indicative of long- 
term averages. However, since 9 years of data were 
used, our long-term average estimates should only 
be affected by long-term changes in catchability. 

An assumption that effort will be lower in the 
future may be more realistic than our assumption 
that effort will remain at 1980-88 levels. However, 
we could not predict the extent to which effort might 
be reduced because it is affected by ex-vessel tuna 
prices at canneries all over the world, the prices of 
other foods, and the cost of fuel. Nevertheless, if we 
could estimate what the effort reductions would be 
in the future, the effort multipliers in the the yield- 
per-recruit estimates in Fig. 9 could still be used. 

If the fishery contracted into the traditional in- 
shore school- and log-set areas after a moratorium 
on dolphin sets, then catches may be lower than we 
estimated them to be. For example, if the area fished 
were smaller, and mixing between the fish inside 
and outside the area were incomplete, then the new 
fishing area would encompass fewer fish than the 
total area. Therefore, all of the population sizes of 
yellowfin used in the equations in the methods sec- 
tion would be overestimated. Recruitment estimates, 
which are estimates of the number of 30-cm yellow- 
fin, would also be overestimated. In addition, if fish- 
ing effort remained high, but the range contracted, 
then a gear- competition effect might lower the catch 
of both yellowfin and skipjack. However, since effort 
levels are expected to decline after a moratorium, 




j I l I I I i 



Observed Mixture 
of Fishing Modes 

No Dolphin Sets 



1 I I I L 



0.2 0.4 O.e 0.8 1.0 1.2 1.4 1.6 1.8 2.0 2.2 2.4 2.6 2.8 3.0 

Effort Multiplier 

Figure 9 

Yield per recruit of yellowfin tuna (Thunnus albacares) (kg) for 
the observed 1980-88 fishery (solid line) and a fishery with all 
effort directed at non-dolphin (Delphinidae) sets (dashed line). 
An effort multiplier of 1.0 refers to the 1980-88 average effort. 



localized depletion of tuna due to a contracted fish- 
ery is unlikely. 

We assumed that yellowfin recruitment in the 
future would not be affected by the changes in popu- 
lation size and age structure which might result 
from re-directing effort toward smaller fish, because 
a relationship between yellowfin spawning biomass 
and recruitment has not yet been demonstrated. 
However, a spawner-recruit relationship for yellow- 
fin may be discovered in the future, because better 
estimates of yellowfin fecundity by size offish, sea- 
son, and area are currently being developed at 
IATTC. When this work is completed we may be able 
to predict recruitment levels and their resulting 
catches more accurately in the future. If future re- 
cruitment levels could be estimated, the future catches 
could be derived by multiplying the recruitment esti- 
mates by the yield per recruit shown in Figure 9. 

Environmental factors have long been suspected 
of having significant effects on yellowfin recruit- 
ment. For example, favorable conditions in the late 
1980's may have contributed to the large number of 
recruits (Bayliff, 1992). In 1987, the number of re- 
cruits was so large that the effect of a moratorium 
in 1988 would have been masked by a high catch of 
1.5 year old yellowfin, first recruited during 1987. 
In 1988, the high abundance of 1.5 year old fish (Fig. 
4) coupled with their high catchability for non-dol- 
phin sets (Fig. 5) caused the estimated yellowfin 
catch if all effort were directed at non-dolphin sets 
to be almost as high as the estimated actual catch. 



142 



Fishery Bulletin 92(1). 1994 



In order to predict future recruitment, the IATTC 
is currently studying the relationship between the 
environment and yellowfin recruitment. If they are 
successful the yield-per-recruit estimates in Figure 
9 could be multiplied by the recruitment estimates 
to better predict future yellowfin catches. 

Little is known about the rate of natural mortal- 
ity of yellowfin. However, there is no reason to be- 
lieve this rate will change. But, if it does change, a 
reasonable assumption would be that if natural 
mortality goes up, catch will go down and vice versa. 
Little is known about skipjack population dynam- 
ics. We assumed that local depletion is negligible for 
skipjack. However, since skipjack are primarily 
caught in association with floating objects, if the 
amount of effort per floating object increases as a 
result of effort being re-directed from dolphin-asso- 
ciated tunas to floating objects, then the chances of 
depletion is certainly possible. If this occurs, our 
estimates of skipjack catch rates will be too high. 
This effect could be compounded during years in 
which floating objects are scarce, because the num- 
ber of sets per floating object would increase. Since 
the skipjack catches have been increasing in the west- 
ern Pacific Ocean, their abundance and catch in the 
eastern Pacific could be lower than our estimates. 

A moratorium on dolphin sets is likely to result 
in reduced catchability, yield per recruit, average 
age, and total biomass of yellowfin. The catch of 
yellowfin, based on these factors only, was predicted 
to decline by approximately 55,600 t (25%). On the 
other hand, skipjack catches could increase, making 
the reduction in total tuna catches much smaller 
(4%). The effects of reductions in fishing effort, the 
range of the fishery, and recruitment were not ana- 
lyzed in this study because they are currently un- 
predictable; however, all three would result in an 
additional decrease in total tuna catches. If better 
predictions of effort levels and yellowfin recruitment 
are made, the yield-per-recruit estimates in Figure 
9 could be used in conjunction with them to better 
predict yellowfin catches. The results of our analy- 
sis indicate that catches in the first years after a 
moratorium begins may not be indicative of the long- 
term catches. Fishermen, biologists, and managers 
should not consider these first-year catches as indices 
of future catches, because recruitment and catchability 
vary annually. On the other hand, our estimates of 
future average catches should be useful unless there 
are long-term changes in catchability or recruitment. 

Acknowledgments 

We would like to thank James Joseph, director of 
investigations of the Inter- American Tropical Tuna 



Commission for suggesting the need for this re- 
search, Richard B. Deriso for his many methodologi- 
cal suggestions, Alejandro Anganuzzi for his reviews 
and for sharing his knowledge about about dolphins, 
and William H. Bayliff for his extensive editorial re- 
views of this manuscript. 



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Allen, R. L. 

1981. Dolphins and the purse-seine fishery for yel- 
lowfin tuna. I.A.T.T.C. Int. Rep. 16, 23 p. 

Allen, R. L., and R. G. Punsly. 

1984. Catch rates as indices of abundance of yellow- 
fin tuna, Thunnus albacares, in the eastern Pacific 
Ocean. I.A.T.T.C. Bull. 18(4):301-379. 

Bartoo, N. W., and A. L. Coan. 

1978. Changes in yield per recruit of yellowfin tuna 

(Thunnus albacares) under the ICCAT minimum 

size regulation. I.C.C.A.T Col. Vol. Sci. Pap. 

8(D:120-183. 
Bayliff, W. H. (ed.) 

1990. Annual report of the Inter-American Tropical 

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Tuna Commission 1991, 271 p. 

Calkins, T. P. 

1965. Variation in size of yellowfin tuna within in- 
dividual purse-seine sets. I.A.T.T.C. Bull. 
10(8):463-524. 

Cole, J. S. 

1980. Synopsis of biological data on the yellowfin 
tuna, Thunnus albacares (Bonnaterre, 1788), in the 
Pacific Ocean. I.A.T.T.C. Special Rep. 2:71-150. 
Green, R. E. 

1967. Relationship of the thermocline to success of 
purse seining for tuna. Am. Fish. Soc, Trans. 
96(2):126-130. 

Greenblatt, P. R. 

1979. Association of tuna with flotsam in the east- 
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Gulland, J. A. 

1965. Estimation of mortality rates. Annex to Rep. 
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Sea CM. 1965(3), 9 p. 

Hennemuth, R. C. 

1957. Analysis of methods of sampling to determine 
the size composition of commercial landings of yel- 
lowfin tuna (Neothunnus rnacropterus) and skip- 
jack (Katsuwonus pelamis). I.A.T.T.C. Bull. 
2(5):174-243. 



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Holt, S. J. 

1958. A note on the simple assessment of a pro- 
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1961. The assesment of the long term effects of 
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Joseph, J., and T. P. Calkins. 

1969. Population dynamics of the skipjack tuna 
(Katsuwonis pelamis) of the eastern Pacific Ocean. 
I.A.T.T.C. Bull. 13(1), 273 p. 
Orange, C. J., and T. P. Calkins. 

1981. Geographical distribution of yellowfin and 
skipjack tuna catches in the eastern Pacific Ocean, 
and fleet and total catch statistics 1975- 
1978. I.A.T.T.C. Bull. 18(1):1-120. 
Pope, J. G. 

1972. An investigation of the accuracy of virtual 
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Punsly, R. G. 

1983. Estimation of the number of purse-seiner sets 
on tuna associated with dolphins in the eastern 



Pacific Ocean during 1959-1980. 
18(3):227-299. 



I.A.T.T.C. Bull. 



1987. Estimation of the relative annual abundance 
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1991. Estimation of the abundance of yellowfin 
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Bull. 20(2):98-131. 

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1975. Computation and interpretation of biological 
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Tomlinson, P. K., S. Tsuji, and T. P. Calkins. 

1992. Length frequency estimation for yellowfin 
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1986. Growth of yellowfin tuna, Thunnus albacares, 
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increments. I.A.T.T.C. Bull. 18(61:423^182. 



Abstract. Gastrointestinal 

tract contents were evaluated from 
73 female and juvenile male north- 
ern fur seals (Callorhinus ursinus) 
for analysis of their diet in the 
Bering Sea. Fur seals were col- 
lected from August to October of 
1981, 1982, and 1985. Juvenile 
walleye pollock (Theragra chalco- 
gramma) and gonatid squid were 
the primary prey. Pacific herring 
(Clupea pallasi) and capelin 
(Mallotus villosus), considered im- 
portant fur seal prey in previous 
reports, were absent from the diet. 
Prey species and size varied 
among years and between near- 
shore and pelagic sample loca- 
tions. Interannual variation in the 
importance of pollock in the diet of 
fur seals was positively related to 
year-class strength of pollock. 
Midwater (n=23) and bottom 
(rc=116) trawls were conducted at 
the location of fur seal collections 
to determine availability of fish 
and squid relative to prey species 
eaten by fur seals. The species and 
size composition of prey taken by 
fur seals was similar to midwater 
trawl collections, but differed from 
bottom trawl catches. Contrary to 
earlier conclusions that northern 
fur seals are opportunistic in their 
feeding habits, we conclude that 
fur seals are size-selective mid- 
water feeders during the summer 
and fall in the eastern Bering Sea. 



Prey selection by northern fur seals 
(Callorhinus ursinus) in the eastern 
Bering Sea 

Elizabeth Sinclair 

Thomas Loughlin 

National Marine Mammal Laboratory, Alaska Fisheries Science Center, 

National Marine Fisheries Service, NOAA 

7600 Sand Point Way, N.E., Seattle, Washington 98 11 5 

William Pearcy 

College of Oceanography, Oregon State University 
Oceanography Administration Building 1 04 
Corvallis, Oregon 97331 



Manuscript accepted 19 August 1993 
Fishery Bulletin: 92:144-156 (1994) 



The Pribilof Island population (St. 
George and St. Paul Islands) of 
northern fur seals (Callorhinus 
ursinus) represents approximately 
75% of the total species breeding 
population. Between 1975 and 
1981, the Pribilof Island population 
declined from 1.2 million to an es- 
timated 800,000 animals (York and 
Hartley, 1981; Fowler, 1985). Abun- 
dance levels on St. Paul Island ap- 
pear to have stabilized (York and 
Kozloff, 1987) at a level 60-70% 
below estimates of the 1940s and 
1950's, and at one-half the esti- 
mated carrying capacity (Fowler 
and Siniff, 1992). The number of 
animals continues to decline on St. 
George Island (York, 1990). 

The objectives of this study were 
to determine the species and size of 
prey eaten by northern fur seals in 
the eastern Bering Sea, to compare 
the seals' present diet with that 
prior to the population decline, and 
to examine the seals' consumption 
of prey relative to prey availability. 
Previous studies on the feeding 
habits of northern fur seals in the 
eastern Bering Sea (Scheffer, 
1950a; Wilke and Kenyon, 1952; 
Wilke and Kenyon, 1957; North 
Pacific Fur Seal Commission Re- 
ports 1962, ' 1975, 2 and 1980 3 ; 
Fiscus et al., 1964; Fiscus et al., 
1965; Fiscus and Kajimura, 1965) 



were conducted prior to the 1975- 
81 population decline and prior to 
the 1970s development of a com- 
mercial walleye pollock (Theragra 
chalcogramma) fishery in the 
Bering Sea. Neither the size of fur 
seal prey, nor fur seal selection of 
prey relative to real-time availabil- 
ity have been previously examined 
in detail. 

Methods 

Northern fur seals were collected 
from 17 to 28 October 1981; from 
24 September through 6 October 



1 North Pacific Fur Seal Commission Re- 
port on Investigations from 1958 to 1961: 
Presented to the North Pacific Fur Seal 
Commission by the Standing Scientific 
Committee on 26 November 1962, 183 p. 
Available: Alaska Fish. Sci. Cent., NOAA, 
NMFS, 7600 Sand Point Way NE., 
BinC15700, Seattle, WA 98115-0070. 

- North Pacific Fur Seal Commission Re- 
port on Investigations from 1967 through 
1972: Issued from the headquarters of the 
Commission, Washington, D.C., June 
1975, 212 p. Available: Alaska Fish. Sci. 
Cent., NOAA, NMFS, 7600 Sand Point 
Way NE., BinC15700, Seattle, WA 
98115-0070. 

3 North Pacific Fur Seal Commission Re- 
port on Investigations during 1973-76: 
Issued from the headquarters of the Com- 
mission, Washington, D.C., February 
1980, 197 p. Available: Alaska Fish. Sci. 
Cent., NOAA, NMFS, 7600 Sand Point 
Way NE., BinC 15700, Seattle, WA 
98115-0070. 



144 



Sinclair et al.: Prey selection by Callorhinus ursmus 



45 



59° N 



• Seal samples (all years) 
D Marinovich midwater trawls 
A Diamond midwater trawls 



Middle Shelf Domain 




Figure 1 

The study area with midwater trawl locations and northern fur seal collection positions. All 
midwater trawls were conducted in 1985. Seal numbers 1-17 were collected in 1981, 18-40 were 
collected in 1982, and 41-83 were collected in 1985. 



1982; and from 6 to 16 August 1985. Collections 
were made within 185 km of the Pribilof Islands 
over the continental shelf, continental slope, and 
oceanic domain of the eastern Bering Sea (Fig. 1). 
Seals were shot from a small craft and returned 
to the NOAA ship Miller Freeman (65-m stern 
trawler) for examination within 1.5 hours of collec- 
tion. The esophagus of each seal was checked for 
food as an indication of regurgitation, and the gas- 
trointestinal (GI) tract was removed and frozen. 
Gastrointestinal tract contents were later thawed 
and gently rinsed through a series of graded sieves 
(0.71, 1.00 or 1.40, and 4.75 mm in 1981 and 1982; 
0.50, 1.00, 1.40, and 4.75 mm in 1985). Fleshy re- 
mains were preserved in 10% formalin. Fish otoliths 
and bones were stored dry. Cephalopod rostra and 



statoliths were preserved in 70% isopropyl alcohol. 
Prey identification was based on all remains, in- 
cluding otoliths. Otoliths were not used for fish iden- 
tification in earlier fur seal diet studies because 
stomach samples were stored in formalin, which 
dissolves otoliths. Techniques and references for the 
identification of prey based on otoliths include Fitch 
and Brownell (1968), Morrow (1979), Frost and 
Lowry (1981), and otolith reference collections (see 
Acknowledgments). References for cephalopod beak 
and statolith identification include Clarke (1962), 
Young (1972), Roper and Young (1975), Clarke 
(1986), and beak and statolith reference collections 
(see Acknowledgments). A tooth was collected from 
each fur seal that was shot and ages were derived 
from direct readings of canine tooth sections follow- 



146 



Fishery Bulletin 92(1), 1994 



ing Scheffer (1950b). In the analysis of data, males 
and females of all ages were treated as one group 
because of small sample sizes. 

The highest number of either upper or lower 
cephalopod beaks and left or right otoliths was re- 
corded as the maximum number of each species 
present. If deterioration made some left and right 
otoliths of a species indistinguishable, they were 
counted and the total was divided by 2. The fre- 
quency of occurrence and number of individuals 
from each prey taxon was calculated for each seal. 

The fork length (FL) of pollock and dorsal mantle 
length (DML) of squid was measured directly when 
whole prey were present in the stomachs. In the 
absence of whole prey, body size was estimated by 
measurement of otoliths and beaks. The maximum 
length of pollock otoliths and lower rostral length 
(LRL) of gonatid squid beaks were measured to the 
nearest 0.05 mm with vernier calipers. Squid DML's 
were estimated by comparison of LRL measure- 
ments to the LRL/DML relationship of 51 gonatid 
squid caught in trawls conducted in the vicinity of 
seal collections. Walleye pollock fork lengths were 
estimated by regression against otolith length (Frost 
and Lowry, 1981). For otoliths measuring: 

> 10.0mm,(FL) Y = 3. 175X - 9.770 ( R = 0.968) 
< 10.0mm, (FL) Y = 2.246X- 0.5 10 (/? = 0.981). 

Walleye pollock ages were estimated from these 
lengths based on length-age relation described by 
Smith (1981) and Walline (1983) for walleye pollock 
from the Bering Sea. 

Otoliths may dissolve or erode to varying degrees 
depending on their size and duration in fur seal 
stomachs. We evaluated the bias introduced in FL 
estimates due to eroded otoliths by assigning 
otoliths to four condition categories (excellent, good, 
fair, and poor) based on amount of wear. After qual- 
ity categorization, the maximum lengths of otoliths 
(except those in "poor" condition) were measured for 
estimation of body length by regression, and length 
frequencies of each category were determined inde- 
pendently. 

Cephalopod beaks are more resistant to digestion 
than otoliths and were typically identifiable. Beaks 
with chipped, worn, or broken rostra were rare and 
were not measured. Cephalopod beaks were identi- 
fied to species when possible, but most were catego- 
rized into two groups referred to as Gonatopsis bo- 
realis-Berryteuthis magister or Gonatus madokai- 
Gonatus middendorffi . The two individual species 
within each group can be separated based on their 
external morphology and statolith structure, but 



cannot presently be separated based on beak struc- 
ture alone (Clarke, 1986). 



Trawl collections of potential seal prey 

Trawls were conducted throughout the study area 
from the Miller Freeman between 1900 and 0600 
hours within the vicinity of seal collections (Fig. 1). 
Both bottom and midwater trawls were conducted 
to provide a relative measure of the availability and 
size of potential fur seal prey species. Bottom trawls 
were made at 52-498 m (.v=139 m) depths with an 
83/112 Eastern bottom trawl (17-m width, 2.3-m 
height mouth opening; 3.2-cm codend liner mesh; 
360-mesh circumference; 200-mesh depth; 30-m 
bridle). Thirty-nine bottom trawls were conducted 
in 1981 (14 October-4 November), 51 in 1982 (24 
September-8 October), and 26 in 1985 (5 August- 
22 August). Seven 1985 trawls were made beyond 
maximum recorded dive depths of adult female seals 
(257 m; Ponganis et al., 1992). They were included 
in analyses because the species and size offish and 
squid caught were consistent with those caught by 
bottom trawl within seal dive depths. 

Collection and sorting methods and calculation of 
bottom trawl catch per unit of effort (CPUE) values 
followed Smith and Bakkala (1982). The total bot- 
tom trawl catch was randomly split into a sample 
of about 2500 kg. Individual species of fishes were 
identified and weighed (wet) and CPUE (no./ha) was 
estimated based on distance trawled. In 1981 and 
1982, cephalopods were classified as squid or octo- 
pus and discarded. In 1985, all cephalopods were 
identified, sexed, weighed, and frozen whole. Beaks 
were extracted and stored in 70% isopropyl alcohol. 

Sex and age determination and body length mea- 
surements were made on a subsample of up to 200 
walleye pollock from each trawl. Fork lengths were 
measured to the nearest centimeter. Saccular 
otoliths were collected for age determination (Smith 
and Bakkala, 1982) and stored in 70% isopropyl 
alcohol. Walleye pollock CPUE was calculated by age 
and body length. For purposes of this study, age- 
length frequencies for male and female walleye pol- 
lock were combined for each of the three years. 

Midwater trawls were made in 1985 with a Dia- 
mond midwater net (n=8) ( 10-16 fm mouth opening; 
3.2-cm codend liner mesh; 354-mesh circumference; 
and 160-mesh depth with 2-m bridles) and a 
Marinovich herring trawl (rc = 15) (6.1-m width, 6.1- 
m height mouth opening; 1-cm codend liner mesh; 
150-mesh circumference; and 350-mesh depth with 
10-m bridles). Specific trawling positions were cho- 
sen within the vicinity of northern fur seal collec- 
tion areas based on the presence of fish or squid as 



Sinclair et al.: Prey selection by Callorhinus ursinus 



147 



indicated on 38 kHz echosounders and a chromoscope. 
Midwater towing depths measured by an attached 
transducer ranged from 22 to 340 m (x=143 m). 

All species of fish and cephalopods collected in 
midwater trawls were identified and counted. The 
CPUE and frequency of occurrence of each species, 
LRL and sex of gonatid squid, and walleye pollock 
frequency of occurrence by age and length were cal- 
culated separately for each trawl type. 

Comparison of seal diet and trawl collections 

The Odds Ratio (Fleiss, 1981) was used to compare 
prey availability (as determined by midwater and 
bottom trawls) with selection of prey by fur seals for 
each sample year: 



= 



pV 



where pi = % of diet comprised by a given prey 
taxon, 
ql = % of diet comprised by all other prey 

taxon, 
p2 = % of food complex in environment com- 
prised by a taxa, and 
q2 = %> of food complex in environment com- 
prised by all other taxa. 
Values were calculated for number of each prey 
species and percent frequency of occurrence among 
seals, and CPUE values (no./ha) for each trawl type. 
Values for p2 and ql were also calculated for the 
trawl types combined in order to provide a compre- 
hensive description of the water column. The natu- 
ral log of the calculated Odds Ratio represents ei- 
ther positive or negative selection- The Odds Ratio 
was chosen because, unlike other electivity indices, 
the significance of the distance of calculated values 
from zero (null hypothesis that prey were consumed 
non-selectively) can be tested with the Z-statistic 
(Gabriel, 1978). 

In order to quantify the degree of overlap in the 
composition of bottom trawls, midwater trawls and 
fur seal GI contents, percent similarity (PS) values 
(Langton, 1982) were calculated: 



PS =100-0.5^a -b, 



where a = %> number of a given prey for seals, and 
b = % number of the same prey for trawls. 

Results 

Fur seal diet 

Eighty-three fur seals were collected. Ten of the 17 
GI tracts collected in 1981 were empty and were 



excluded from the analysis. Of the 73 animals in- 
cluded in the analysis, 13 were juvenile males, 3 
were juvenile females and 57 were adult females. 
Most fur seals were collected over depths less than 
200 m within the outer shelf domain (Fig. 1). 

Fish represented 89% and cephalopods 11% of 
prey numbers for all three sample years combined. 
One-hundred percent of the GI tracts had fish re- 
mains and 82% of all samples contained walleye 
pollock. A total of 2,658 walleye pollock otoliths were 
measured. In all years combined, juvenile walleye 
pollock (3-20 cm FL) were the most numerous and 
frequently occurring prey species. Sixty-five percent 
of prey walleye pollock were from the 0-age group 
(3-13 cm FL) and 31% were from age group 1 (13- 
20 cm FL). Only 4% of prey pollock were from age 
group 2 (20 + cm FL) and older. 

Gonatid squids occurred in 36% of the samples, 
but in comparison with pollock, they were not con- 
sumed in large numbers (Fig. 2). Gonatus madokai- 
G. middendorffi and Gonatopsis borealis-Berry- 
teuthis magister were the second most frequently 
occurring prey in all years combined. Seventy-nine 
percent of the 389 beaks measured were from squid 
5-12 cm DML. 

Northern smoothtongue (Leuroglossus schmidti), 
a bathylagid deepsea smelt, was the second most 
numerous fish prey overall (Fig. 2) even though it 
was found only in 1985 (Table 1). Northern smooth- 
tongue composed a higher percentage of the total 
number offish than walleye pollock >2 years old for 
all sample years combined. Atka mackerel 
(Pleurogrammus monopterygius) composed 23.9% of 
the 1981 prey sample and was present in five of 
seven stomachs collected in 1981 that had prey re- 
mains, but the species was identified from the prey 
remains of only one other individual among the six 
collected in the same area in 1982 (Table 1). 

Although walleye pollock were eaten by fur seals 
in all 3 years, marked differences in age and body 
size were found between years (Table 1; Fig. 3). In 
1981, the few walleye pollock otoliths found were 
from fish 3-4 years of age. Fur seal GI tracts con- 
tained primarily age-0 pollock in 1982 and age-1 
pollock in 1985. Exclusion of otoliths that were in 
fair condition caused a downward shift in modal FL 
frequencies of 1 to 2 cm, but did not change our es- 
timation of the age categories of pollock eaten by 
fur seals. 

The species of forage fishes and squids consumed 
by fur seals varied between samples taken on and 
off the continental shelf (200 m) (Fig. 4). The GI 
tracts of fur seals collected over oceanic and conti- 
nental slope regions contained primarily northern 
smoothtongue and squids, especially Gonatopsis 



148 



Fishery Bulletin 92f 1). 1994 



10 20 



Percent number/frequency 
30 40 50 60 70 



walleye pollock 
(Theragra chalcogramma) 

gonatid squid 

(Gonatidae) 

Atka mackerel 

(Pleurogrammus monopterygius) 

northern smoothtongue 
(Leuroglossus schmidti) 

Salmoniformes 
fOsmendae) 





Percent of total number of 
prey, all years 

Percent frequency of 
occurrence of prey, all years 



Figure 2 

Percent of total number and frequency of occurrence of primary prey in northern fur seal 
(Callorhinus ursinus) gastrointestinal tracts for sample years 1981, 1982, and 1985 combined. 
Species shown include the top three prey from each sample year. 



borealis-Berryteuthis magister. Seals collected over 
the continental shelf contained the remains of wall- 
eye pollock of all ages and squids, especially Gonatus 
madokai-G. middendorffi. Adult walleye pollock, 
although rare in stomach contents, were found in 
greatest frequency in fur seals collected from the 
outer domain of the continental shelf. Juvenile wall- 
eye pollock were consumed primarily over the 
midshelf and outer domain. Atka mackerel was 
found only in samples collected over the outer shelf 
domain north of Unimak Island. 

Comparisons with trawl samples 

Of the five top-ranked species collected in bottom 
trawls, only walleye pollock was found in fur seal 
GI contents (Figs. 2 and 5). Walleye pollock from 
bottom trawls ranged from 1 to over 12 years of age 
and had mean body lengths of 38.9 cm (3-4 years 
old) in 1981, 39.7 cm (4-5 years old) in 1982, and 
44 cm (5-6 years old) in 1985 (Fig. 6). All but four 
of the cephalopods caught in 1985 bottom trawls 
were Berryteuthis magister ranging from 17.5 to 31.2 
cm DML ( x = 2 1.6). As in the seal samples, B. 
magister was collected in trawls conducted over the 
outer continental shelf domain along the 200-m 
contour, or over the continental slope between 200 
and 1000 m. Otherwise, the bottom trawl catch for 
all three years was so dissimilar to the midwater 
trawl catch (Figs. 5 and 6) and fur seal GI contents 
(Fig. 2) that electivity computations were not mean- 
ingful (Odds Ratio=0). 



Calculation of the Odds Ratio and Z-statistic on 
1985 data with midwater and bottom trawl catch 
combined showed statistically significant positive 
selection by fur seals for age-0 pollock (P=0.0002), 
age-1 pollock (P<0.0001), northern smoothtongue 
(P<0.0001), and gonatid squid (P=0.02). Negative 
selection for adult walleye pollock was suggested but 
was not statistically significant (P=0.13). 

A similarity index of 81% was calculated for spe- 
cies composition and prey size in the 1985 GI 
samples and midwater trawls. Fur seals fed on three 
of the four top-ranked species caught in midwater 
trawls (Figs. 2 and 5). Midwater trawls and seals 
caught predominantly juvenile walleye pollock. 
Gonatid squids (Gonatus madokai, G. middendorffi, 
and Gonatopsis borealis) had low CPUE values but 
were second in frequency of occurrence in both fur 
seal GI tracts and midwater trawls. The modal 
length of walleye pollock and gonatid squids was 5- 
20 cm in both midwater trawl and GI samples in 
1985. Few adult walleye pollock and no large squid 
were collected in midwater trawls or seal GI samples. 

Seals and midwater trawls caught the same prey 
species at the same general locations on and off the 
continental shelf (Fig. 4). As in GI contents, age-0 
and age-1 walleye pollock were collected in 
midwater trawls made on the middle and outer shelf 
and near the continental slope. Gonatopsis borealis 
were found on the continental slope and near-slope. 
Gonatus madokai and G. middendorffi were found 
throughout the sampling area, but primarily on the 
outer continental shelf and near-slope sampling areas. 



Sinclair et al.: Prey selection by Callorhinus ursinus 



149 







Table 1 










Gastrointestinal contents of 73 northern fur seals (Callorh 


nus ursinus) collected from the Bering 


Sea in 1981 


(n=7), 1982 (n=23), and 1985 (n=43). 


Tentative 


identifications are 


designated as (t). 






Prey species 


% number in each 


year 


% frequency occurrence 


1981 


1982 


1985 


1981 


1982 


1985 


Fish 














Clupea pallasi 


— 


0.1 


— 


— 


4.4 


— 


Osmeridae (t) 


8.7 


— 


— 


42.9 


— 


— 


Salmonidae 


5.4 


— 


— 


42.9 


— 


— 


Leuroglossus schmidti 


— 


— 


12.7 


— 


— 


9.3 


Gadus macrocephalus (t) 


— 


— 


0.1 


— 


— 


7.0 


Theragra chalcogramma 


54.4 


87.3 


74.1 


100 


95.7 


72.1 


3-5cm fork length 


— 


(8.8) 


(5.7) 








5-10cm fork length 


(4.3) 


(63.9) 


(2.3) 








10-20cm fork length 


— 


— 


(55.6) 








>20cm fork length 


(38.0) 


(1.4) 


(1.7) 








T. chalcogramma (t) 


— 


0.1 


0.1 


— 


8.7 


4.7 


unidentified Gadidae 


— 


— 


0.9 


— 


— 


20.9 


Lycodes sp. 


1.1 


— 


0.5 


14.3 


— 


— 


Pleurogrammus monopterygius 


23.9 


0.1 


— 


71.4 


4.4 


— 


P. monopterygius (t) 


— 


0.1 


— 


— 


4.4 


— 


unidentified percoid 


1.1 


— 


— 


14.3 


— 


— 


unidentified fish 


5.4 


0.4 


0.5 


14.3 


13.0 


25.6 


Squid 














Gonatus berryi 


— 


— 


0.1 


— 


— 


2.3 


G. pyros 


— 


— 


0.1 


— 


— 


2.3 


G. tinro 


— 


— 


0.1 


— 


— 


2.3 


G. tinro (t) 


— 


— 


0.1 


— 


— 


2.3 


Gonatus madokai-middendorffi 


— 


0.1 


4.8 


— 


4.4 


34.9 


Gonatus sp. 


— 


— 


0.1 


— 


— 


2.3 


Berryteuthis magister 


— 


0.6 


— 


— 


8.7 


— 


Gonatopsis borealis-B. magister 


— 


10.2 


6.4 


— 


17.4 


20.9 


unidentified Gonatidae 


— 


— 


0.1 


— 


— 


7.0 


unidentified squid 


— 


1 


— 


— 


34.8 


— 


Total number prey 


92 


1638 


2189 








Total number fish 


92 


1445 


1936 


100 


100 


100 


Total number squid 





193 


253 





52.2 


46.5 



Discussion 

The modal size distribution of walleye pollock in GI 
contents of female and juvenile male fur seals re- 
flected year-class strength projections of walleye 
pollock (Fig. 7). Walleye pollock have highly variable 
recruitment rates (Smith, 1981), and year-class 
strength varied five-fold between 1977 and 1982 
(Bakkala et al., 1987). Population estimates based 
on bottom trawl and midwater acoustic surveys in 
the eastern Bering Sea indicated that the 1980 year 
class (age 1 in 1981) was about half the average 
year-class size; the 1981 year class (age in 1981) 
was the weakest observed prior to 1983; and the 
1978 year class (age 3 in 1981) was the strongest 
observed. The 1982 and 1984 year classes were 



strong and the 1985 year class was considered av- 
erage (Bakkala et al., 1987). Similarly, walleye pol- 
lock as prey in 1981 were primarily adults 3 and 4 
years of age (from the 1977 and 1978 year class); in 
1982, seals ate age-0 pollock exclusively; and in 
1985, prey pollock were primarily from the 1984 
year class. The concordance of pollock recruitment 
and fur seal GI content analysis indicates that the 
variable recruitment of walleye pollock affects prey 
consumption by northern fur seals. 

The three basic dive patterns described for adult 
females in the Bering Sea are shallow, pelagic night- 
time diving (most commonly to 50—60 m); deep day- 
and-night diving over the continental shelf (most 
commonly to 175 m); and some combination of both, 
including shallow diving over the continental shelf 



50 



Fishery Bulletin 92(1). 1994 




 


1981 
n.39 


' □ 


1982 
n-1191 




1985 
n-1428 



Figure 3 

Age-length frequencies of walleye pollock (Ther 
chalcogramma) based on otoliths in northern fur 
[Callorhinus ursinus) gastrointestinal tracts by year. 



agra 
seal 



and both shallow and deep diving along the conti- 
nental slope. Dive pattern information is based on 
time-depth recordings (Gentry et al., 1986; Loughlin 
et al., 1987; Goebel et al., 1991), radio telemetry 
(Loughlin et al., 1987), stomach volume estimates 
(Mead, 1953; Taylor et al., 1955'; Spalding, 1964; 
Wada, 1971; Kajimura, 1984), and stomach clear- 
ance studies (Miller, 1978 5 ; Bigg, 1981 6 ; Bigg and 
Fawcett, 1985; Murie and Lavigne, 1985). 



Based on fur seal and trawl collections in 
this study and on distributional information 
of prey (Smith, 1981; Dunn, 1983; Kubodera 
and Jefferts, 1984; Lynde, 1984), shallow 
diving fur seals over the continental shelf 
concentrated on juvenile walleye pollock and 
juvenile gonatid squid (Gonatus madokai-G. 
middendorffi), while shallow divers off-shelf 
targeted juvenile gonatid squid (Berryteuthis 
magister-Gonalopsis borealis) and bathy- 
lagid smelt. Daytime deep diving over the 
continental shelf would be advantageous to 
seals concentrating on prey (i.e., adult wall- 
eye pollock) that tend to school at depth 
during daytime hours and disperse as they 
rise in the water column at night. Adult 
gonatid squid probably occur in schools at 
the bottom on the continental shelf and re- 
main deep along the shelf edge during both 
day and night. The location and degree of 
concentration of prey may be closely associ- 
ated with the hydrography of the foraging 
region. The hydrography of the foraging re- 
gion may have the most direct influence on 
the diving patterns of fur seals. 

Hydrographic characteristics of the Bering 
Sea continental shelf, include a two-layered 
midshelf and a three-layered outer shelf 
domain that may stratify and concentrate 
prey by species and age in a vertical plane. 
Nishiyama et al. (1986) proposed that ver- 
tical stratification within the eastern Bering 
Sea shelf serves as a "nursery layer" to con- 
fine young-of-the-year pollock in the upper 
40 m of the water column within the bound- 
ary region between the upper and lower lay- 
ers. Copepod nauplii are also concentrated 
in this area, providing a ready source of food 
for larval walleye pollock (Bailey et al., 
1986). Wada ( 1971) determined that primary 
foods of fur seals off the Sanriku Coast in Japan 
consisted of migrating species closely related to 
boundary regions, especially transition zone regions. 
The horizontal temperature and salinity structures 
that occur on either side of frontal regions within 
our study area (Kinder and Schumacher, 1981 ) may 



4 Taylor. F II (' , M. Fuginaga, and F. Wilke. 1955. Distribu- 
tion and food habits of the fur seals of the North Pacific Ocean 
Rept. of Coop. Invest by the Govts, of Can., Japan, and the 
U.S.A. Feb. -July, 86 p Available Alaska Fish. Sci. Cent.. 
NOAA, NMFS, 7600 Sand Point Waj \K , BinC 15700, Seattle, 
WA 98115-0070. 



' Miller, L. K. 1978. Energetics of the northern fur seal in rela- 
tion to climate and food resources of the Bering Sea. Final Rep. 
to U S. Mar. Mamm. Comm. MMC-75/08, 27p. 

K Bigg. M. A. 1981. Digestion rates of herring (Clupea harengus 
pallasi i and squid iLali^o npalfsri-nsi in northern fur seals. 
Submitted to the 24th Annual Meeting of the Standing Sci. 
Comm., N. Pac. Fur Seal Comm., 6-10 April, Tokyo, Japan. 
Available: Alaska Fish. Sci. Cent.. 7600 Sand Point Way NE., 
BmC15700, Seattle, WA 98115-0070. 



Sinclair et al.: Prey selection by Callorhmus ursinus 



151 



Percent number 



100 90 80 70 60 50 40 30 20 10 



10 20 30 40 50 60 70 80 90 100 



northern smoothtongue 

(Leurogkxsus Schmidt) 



gonatid squid 

(Gonatopsis borealis/ 
Berryteu&tts magister) 

gonatid squid 
(Gonatus madokairmiddendotlrl) 



walleye pollock (all ages) 
(Theragra chalcogramma) 



Oceanic domain/Continental slope 



seals 



midwater trawls 



Continental shell (<200m) 



seals 



midwater trawls 



Figure 4 

Primary species identified in fur seal (Callorhinus ursinus) gastrointestinal tracts and midwater trawls col- 
lected on and off the eastern Bering Sea continental shelf in 1985. 



walleye pollock 
(Themgra chalcogramma) 



lanternfish 
(Myaophxlae) 



northern smoothtongue 
(Leuroglossus schmidti) 



gonatid squid 
(Gonatidae) 




40 



60 



80 



100 






Q Marinovich midwater trawl 
 Diamond midwater trawl 



50 
I 



100 



150 



200 



walleye pollock 
(Theragra chalcogramma) 



yellowfin sole I 

jronectes asper) iMmnmu 



(Pleuronectes asper) 



rock sole 
(Lepidopsena bilineala) I 



Pacific cod 
(Gadus macrocephalus) 



Bottom trawls 
 1981 
^ 1982 
□ 1985 



Mean CPUE values (no. /ha) 



Figure 5 

Catch per unit of effort (CPUE) number/hectare (no. /ha) values for species caught in 1985 
midwater trawls and bottom trawls in 1981, 1982, and 1985. 



152 



Fishery Bulletin 92(1), 1994 



400 



300- 



1 

1 200 

$ 

E 



100- 



1985 Trawls 



| Midwater 
□ Bottom 



N-4140 



Jll^l 



10 




20 25 30 
Fork length (cm) 

J I 



45 



_L_L 



50 



2 3 

Age (years) 



6 7 



Figure 6 

Age-length frequencies of walleye pollock (Therag 
chalcogramma) collected in bottom and midwater trawls 

19H5. 



also form boundaries that concentrate prey. Diving 
depths of 175 m coincide with the depth break of the 
outer continental shelf. Diving depths of 50-60 m 
coincide with the depth break of the frontal systems 
between the midshelf and inner shelf. 

Previous analyses of fur seal diet in the eastern 
Bering Sea were based primarily on a sample of 
3,530 stomachs collected pelagically in 1960, 1962- 
64, 1968, 1973, and 1974 (North Pacific Fur Seal 
Commission Reports 1962, ' 1975, 2 and 1980 3 ; Fiscus 
et al. 1 D64; Fiscus et al. 1965; Fiscus and Kajimura 
1965;. i:tviews of the pelagic data cite walleye pol- 
lock (Kajimura, 1985; Perez and Bigg, 1986), Pacific 
herring (Clupea pallasi), capelin (Mallotus villosus), 
Atka mackerel, gonatid squids (Gonatus spp., 
Berryteuthis magister and Gonatopsis borealis), and 
intermittently, northern smoothtongue (Kajimura, 
1984) as principal fur seal prey in the eastern 
Bering Sea. Published reports and reviews of fur 
seal feeding habits prior to the pelagic collections 
(1892-1950's) also described walleye pollock, cape- 
lin, gonatid squid, and bathylagid smelt as primary 
prey in seal spewings or stomachs (Scheffer, 1950a; 
Wilke and Kenyon, 1952; Wilke and Kenyon, 1957). 



In terms of prey species composition, the 
summer diet of female and juvenile male 
northern fur seals does not appear to have 
changed dramatically since the turn of the 
century. Pollock and gonatid squid are still 
the predominant prey of northern fur seals 
in the eastern Bering Sea. More subtle 
changes, such as a decrease in pollock size 
may have occurred (Smith, 1981; Swartz- 
man and Haar, 1983) and could play a criti- 
cal role in foraging success of northern fur 
seals. Unfortunately, records of prey size 
in historical fur seal diet studies are incom- 
plete. 

It should be noted that Pacific herring 
and capelin were absent from fur seal di- 
ets in this study, despite collections in ar- 
eas where they occurred as important prey 
in the past. Fluctuation in the population 
status of Pacific herring and capelin in the 
Bering Sea has been attributed to the spo- 
radic and localized nature of their abun- 
dance (Turner, 1886; Meek, 1916; Favorite 
et al. 1977 7 ; Lowe 1991 8 ), overharvesting 
and displacement by walleye pollock 
(Wespestad and Barton, 1981; Swartzman 
and Haar, 1983; Wespestad and Fried, 
1983; Bakkala et al., 1987), and/or environ- 
mental change such as the pronounced 
warming in the Gulf of Alaska and Bering 
Sea over the past decade (Royer, 1989). The 
absence of these previously important prey may be 
critical to seals during successive years of weak 
walleye pollock year-class abundance. 

Fur seals select juvenile walleye pollock as prey 
despite a wide availability of other prey types within 
their dive range. Fur seals may select their prey by 
size and schooling behavior, whether the prey are 
myctophids in oceanic waters off Japan (Wada, 
1971); Pacific herring, capelin, market squid iLoligo 
opalescens) and Pacific whiting (=Pacific hake, 
Merluccius productus) in the eastern North Pacific 
(Kajimura, 1984; Perez and Bigg, 1986); or walleye 
pollock in the eastern Bering Sea (Kajimura, 1984). 
The most consistent prey characteristic between 
feeding studies across the northern fur seal range 



7 Favorite, F., T. Laevastu, and R. R. Straty. 1977. Oceanogra- 
phy of the northeastern Pacific Ocean and eastern Bering Sea, 
and relations to various living marine resources. NWAFC Proc. 
Rep. 280p. Alaska Fish. Sci. Cent., NMFS, NOAA, 7600 Sand 
Point Way NE., Bin C 15700, Seattle, WA 98115-0070, 280p. 

R Lowe, S. A. 1991. Atka mackerel. In Stock assessment and fish- 
ery evaluation report for the groundfish resources of the Bering 
Sea/ Aleutian Islands region as projected for 1992, p. 11-2 to 
11-40. North Pacific Fishery Management Council, P.O. Box 
103136, Anchorage, AK 99510. 



Sinclair et al.: Prey selection by Callorhmus ursinus 



53 



B * 

C l/i 

IB C 

£: O 



ra E 
a> = 

>• c 

SI 

o « 

°- g. 

o 

CL 



90 - 
80 - 
70- 
60 - 
50 - 
40- 
30 - 
20 - 
10- 
- 

100 




1978 1979 1980 1981 1982 1983 1984 1985 

Pollock year class 



80 



70 - 



2 50 



 1981 
□ 1985 




1978 1979 1980 1981 1982 1983 1984 1985 



Pollock year class 

Figure 7 

Estimates of walleye pollock iTheragra 
chalcogramma) year-class strength 1978- 
85 (Bakkala et al., 1987), and the relative 
abundance of specific year classes in 
northern fur seal gastrointestinal tracts. 



is size and the tendency to form dense schools. In 
this sense, a "juvenation" of walleye pollock in the 
Bering Sea (Swartzman and Haar, 1983) may have 
provided fur seals with a newly abundant but un- 
stable resource, due to large fluctuations in the 
annual year-class strength of walleye pollock and 
due to potential displacement of other prey species 
(Pacific herring and capelin). During years of low 
pollock recruitment, fur seals may switch to other 
prey such as capelin and Pacific herring, and expe- 
rience food limitation only if these alternate prey 
resources have been displaced or depleted. Histori- 



cal records of northern fur seal diet are inadequate 
to either support or refute an "alternate prey" ar- 
gument. However, we suggest that when juvenile 
walleye pollock are unavailable, such as in our 1981 
sampling season, female and juvenile fur seals se- 
lect other specific prey of the same size and eat adult 
walleye pollock only if these other preferred prey are 
not available. 

During their summer breeding season, northern 
fur seals consume the most abundant and available 
fish and squid in the eastern Bering Sea. Walleye 
pollock make up an estimated 50% of the ground- 
fish biomass in the eastern Bering Sea and Aleutian 
Islands area (Walters et al., 1988) and dense aggre- 
gations of 0-age pollock occur off the Pribilof Islands 
June through mid-August (Smith, 1981). Kubodera 
and Jefferts (1984) suggested gonatids are the ma- 
jor pelagic cephalopod group in the Bering Sea, 
where large increases in abundances of larval and 
postlarval gonatid squid occur in early June. Among 
Bering Sea gonatids, Gonatopsis borealis and 
Berryteuthis magister are considered to be among 
the most numerically dominant (Jefferts, 1983; 
Kubodera and Jefferts, 1984). 

Selection by northern fur seals of a wide variety 
of numerically dominant prey species throughout 
their migratory range has led to the general conclu- 
sion that they are non-specific, opportunistic feed- 
ers (Kajimura, 1985). Northern fur seals are flexible 
in their feeding habits, as indicated by the variation 
in GI contents of seals collected between California 
and Alaska. Nonetheless, fur seals concentrate on 
an average of three primary species within each 
oceanographic subregion (Perez and Bigg, 1986). In 
addition, fur seal consumption of walleye pollock, 
gonatid squid, and bathylagid smelt in the eastern 
Bering Sea is consistent throughout historical 
records, despite the wide variety of prey available 
to fur seals within their diving range. Based on this 
study, we conclude that female and young male fur 
seals select juvenile and small-sized fish and squid, 
despite the availability of larger prey types within 
their diving range. This study demonstrates that 
female and young male fur seals are size-selective 
midwater shelf and mesopelagic feeders, at least 
during the breeding and haul-out season in the east- 
ern Bering Sea. 



Acknowledgments 

Otolith identifications for the 1981 samples were 
made by the late J. Fitch. Otolith identifications for 
1982 and 1985 were based on the otolith reference 
collections at the National Marine Mammal Labo- 



54 



Fishery Bulletin 92(1). 1994 



ratory (NMML) and Los Angeles County Museum 
(LACM). Cephalopod identifications were based on 
the reference collections of the NMML and Oregon 
State University (OSU). Voucher specimens of prey 
material (statoliths, beaks, otoliths, teeth, and 
bones) are archived at the NMML. Identifications of 
squid and squid beaks were confirmed by C. Fiscus 
(NMML, retired), K. Jefferts (OSU), and W. Walker 
(LACM). Identification of fish otoliths and bones 
were confirmed by G. Antonelis Jr. (NMML) and J. 
Dunn (University of Washington) respectively. 
Voucher samples of juvenile pollock otoliths were 
confirmed by A. Brown (Alaska Fisheries Science 
Center [AFSC]), K. Frost (Alaska Department of 
Fish and Game [ADF&G], and L. Lowry [ADF&G]). 
Gary Walters (AFSC) helped interpret bottom trawl 
values, and W Carlson and C. Leap of the AFSC 
Graphics Unit helped produce the figures. 

The following individuals contributed to the qual- 
ity and content of this manuscript: G. Antonelis Jr., 
J. Baker, L. Fritz, R. Gentry, P. Livingston, and two 
anonymous reviewers. These data were first pre- 
sented in part as a Northwest and Alaska Fisher- 
ies Center Processed Report (Hacker and Antonelis, 
1986 9 ) and in full as a Masters Thesis from Oregon 
State University (Sinclair, 1988). 



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Abstract. — The stomach con- 
tents of 1,215 anadromous ale- 
wives collected during winter and 
summer groundfish research sur- 
veys (1990-91) off Nova Scotia 
were examined to 1) describe the 
diet by season, area, bottom depth 
(<101 m, 101-200 m, >200 m), 
time of day and fish size (<151 
mm, 151-200 mm, 201-250 mm, 
>250 mm FL), 2) evaluate diel 
feeding periodicity, and 3) estimate 
daily ration. Euphausiids, particu- 
larly Meganyctiphanes norvegica, 
were the most important prey and 
represented more than 82% by vol- 
ume of total stomach contents sea- 
sonally and geographically. Contri- 
butions by other prey groups 
(hyperiid amphipods, calanoid 
copepods, crustacean larvae, poly- 
chaetes, chaetognaths, mysids, 
pteropods, and fish larvae) were 
small and varied temporally and 
spatially. The proportion of eu- 
phausiids in the diet of alewives 
from the Scotian Shelf (winter) 
and Bay of Fundy (summer) 
tended to increase with increasing 
depth. Day and night differences 
in diet composition indicate that 
alewives may particulate-feed on 
macrozooplankton when prey vis- 
ibility is high and filter-feed on 
microzooplankton when prey vis- 
ibility is low. Diet composition was 
relatively homogenous among ale- 
wife size groups with euphausiids 
composing most of the total food 
volume. Alewives of different size 
groups ate similarly sized M. 
norvegica, generally the largest M. 
norvegica available. Diel feeding 
activity (stomach fullness) peaked 
at mid-day (summer collections) 
and mid-afternoon (winter collec- 
tions); feeding activity was re- 
duced at night. In all areas, feed- 
ing activity and the proportion of 
feeding fish was highest in regions 
where bottom depths exceeded 200 
m. Mean stomach fullness was 
highest during summer in the Bay 
of Fundy and during winter on the 
Scotian Shelf; these regions are 
seasonally important foraging ar- 
eas for alewives off Nova Scotia. 
Daily ration was 1.2% of body 
weight during winter and 1.9% 
during summer. 



Manuscript accepted 17 August 1993 
Fishery Bulletin 92:157-170 (1994) 



Feeding habits of anadromous 
alewives, Alosa pseudoharengus, 
off the Atlantic Coast of Nova Scotia 



Heath H. Stone 

Department of Fisheries and Oceans, Biological Sciences Branch 
PO. Box 550, Halifax. Nova Scotia B3J 2S7 CANADA 

Present address: Biological Station, Department of Fisheries and Oceans 

St. Andrews, New Brunswick, EOG 2XO CANADA 

Brian M. Jessop 

Department of Fisheries and Oceans, Biological Sciences Branch, 
RO. Box 550, Halifax, Nova Scotia, B3J 2S7 CANADA 



The anadromous alewife, Alosa pseu- 
doharengus, is a clupeiform fish 
whose range extends from New- 
foundland to North Carolina 
(Bigelow and Schroeder, 1953). Off 
Nova Scotia, alewives occur through- 
out the year in regions characterized 
by strong tidal mixing and up- 
welling in the Bay of Fundy-east- 
ern Gulf of Maine and are abun- 
dant during spring in the warmer, 
deeper waters of the central 
Scotian Shelf and areas of warm 
slope water intrusion along the 
Scotian Slope and the edges of 
Georges Bank (Stone and Jessop, 
1992). In the Maritime provinces of 
Canada and Atlantic coastal 
United States, alewives and 
blueback herring, A. aestivalis, are 
fished commercially during their 
spring spawning migrations and 
are often marketed together as 
gaspereau or river herring. Little is 
known about the importance of ale- 
wives as predators in the marine 
environment or about their feeding 
habits and food consumption rates. 
Alewives are generally classified 
as size-selective, particulate and 
filter-feeding microphagists and 
can actively feed on individual 
zooplankton or passively feed by 
filtering the water with their gill 
rakers (Janssen, 1976; Durbin, 
1979; James, 1988). Feeding mode 



depends on prey density, size, and 
visibility, and on predator size 
(Janssen, 1976, 1978a, 1978b; 
Durbin, 1979). The ability to switch 
feeding modes enables alewives to 
consume a wide size range of prey 
in a variety of environmental con- 
ditions. Size-selective predation by 
juvenile and nonanadromous fresh- 
water alewives can shift the species 
and size composition of zooplank- 
ton communities towards smaller 
forms (Brooks and Dodson, 1965; 
Brooks, 1968; Wells, 1970; Wars- 
haw, 1972; Vigerstad and Cobb, 
1978). No information is available 
on size-selective predation in the 
ocean; however, in Minas Basin, a 
turbid macrotidal estuary, alewives 
were generally particulate feeders 
of larger, benthic prey rather than 
smaller pelagic prey (Stone and 
Daborn, 1987). 

Information on the feeding hab- 
its of anadromous alewives in the 
ocean is limited to qualitative as- 
sessments but is better known for 
freshwater juveniles (Vigerstad 
and Cobb, 1978; Gregory et al., 
1983; Jessop, 1990) and estuarine 
resident subadults during summer 
(Stone and Daborn, 1987). Eu- 
phausiids, calanoid copepods and, 
to a lesser extent, hyperiid amphi- 
pods, chaetognaths, mysids, ptero- 
pods, decapod larvae, and salps 



157 



58 



Fishery Bulletin 92|1|. 1994 



have been identified as prey for alewives in conti- 
nental shelf waters from North Carolina to Nova 
Scotia (Holland and Yelverton, 1973; Edwards and 
Bowman, 1979; Neves, 1981; Vinogradov, 1984; Bow- 
man, 1986). However, none of these studies were 
comprehensive. 

We examined the stomach contents of anadromous 
alewives obtained from winter and summer ground- 
fish research surveys on the Scotian Shelf, Georges 
Bank, and in the Bay of Fundy to determine the 
importance of these regions as foraging areas for 
these fish. Seasonal, spatial, diel and size-related vari- 
ability in feeding are examined. Daily ration is esti- 
mated from information on diel feeding periodicity. 



Materials and methods 

Data collection 

Alewives were collected from seven groundfish re- 
search surveys conducted by the Canadian Depart- 
ment of Fisheries and Oceans in three regions 
(Georges Bank, central Scotian Shelf, and outer Bay 
of Fundy) during winter (February-March) and 
summer (July) over a two-year period (1990-91) 
(Table 1). All surveys used a Western IIA bottom 
trawl with a 10-mm stretched-mesh liner in the cod 
end. Thirty-minute tows at each sampling station 
were conducted throughout the 24-hour day. Up to 
40 fish of representative size range from each set 
were frozen for later analysis. Bottom water tem- 
perature CO, time of tow deployment, latitude, lon- 
gitude, and bottom depth (m) were recorded for each 
set. Stomach content data were grouped by season 
and sample location: Winter-Fundy, Winter-Shelf, 
Winter-Georges, and Summer-Fundy (Fig. 1). Stone 



and Jessop (1992) provide additional details of the 
survey area and procedures, and seasonal distribu- 
tion of fish. 

Fork length (mm), weight (g), sex and species (de- 
termined by peritoneal colour (Leim and Scott, 
1966)) were recorded for each fish. Whole digestive 
tracts, individually identified, were preserved in 4% 
buffered formalin. 

Diet analysis 

Stomachs were weighed (±0.01 g) and the contents 
ranked subjectively using a fullness code (0=empty, 
1 = 12% full, 2=25% full, 3=50% full, 4=75% full, 
5=100% full) and a digestion code ( l=finely digested, 
nothing recognizable; 2=medium digestion, some 
recognizable parts; 3=some digested, some undi- 
gested material; 4=undigested whole animals). The 
stomach content weight was obtained by subtract- 
ing the weight of the empty stomach from the total 
stomach weight. Stomach content weight, as a per- 
centage offish body weight C#BW), was used as an 
index of fullness to evaluate feeding activity and 
estimate daily ration. Stomach contents were iden- 
tified (to species where possible), enumerated, and 
the volume of each food type estimated by means of 
a points system (Swynnerton and Worthington, 
1940; Stone and Daborn, 1987). 

For diet analysis, prey taxa (Table 2) were 
grouped into nine categories based on taxonomy and 
ecology: 1) euphausiids (Meganyctiphanes norvegica 
and some Thysanoessa spp.); 2) hyperiid amphipods 
(Parathemisto gaudichaudiy, 3) calanoid copepods 
(Calanus spp., Centrophoges spp. and Metridia spp.); 
4) polychaetes (Nereis spp. and unidentifiable spe- 
cies); 5) fish larvae (Ammodytes dubius and uniden- 
tifiable species); 6) mysids {Neomysis americana); 1) 







Table 1 
















Stomach and fork length statistics, by season and geographic area, 
tained from groundfish research surveys conducted off Nova Scotia 


for al 
(1990 


ewives, 
-1991). 


Al 


osa pseudoharengus. ob- 


Season and area 


Collection date 




Number 










Fork length 


(mm) 


1990 1991 


Sets 


Stomach 




Stomachs 
with prey 


Mean ± SD 


Range 


Winter-Fundy 


2-10 Feb 


:i 


112 






58 




201.9 ± 5.38 


100-303 


Winter-Georges 


28 Feb-Mar 7 Feb 16-26 


29 


438 






147 




193.6 ± 1.83 


118-305 


Winter-Shelf 


13-19 Mar Mar 15-18 


29 


489 






322 




223.8 ± 2.82 


95-302 


Summer-Fundy 


6-10 Jul Jul 05-09 


15 


176 






141 




242.6 + 2.48 


142-302 


Total 




82 


1,215 






668 




213.6 ± 1.86 


95-305 



Stone and Jessop: Feeding habits of Alosa pseudoharengus 



159 



40°N 




70°W 



Figure 1 

Set locations for alewives, Alosa pseudoharengus, obtained from groundfish re- 
search surveys off the Atlantic coast of Nova Scotia (1990-91) grouped by season 
and geographic area. Offshore banks are delineated by the 100-m depth contour; 
the outer edge of the continental shelf is delineated by the 200-m depth contour. 



chaetognaths; 8) crustacean larvae (furciliae of 
Thysanoessa spp. and some decapod larvae); and 9) 
pteropods. The percent frequency of occurrence 
(%FO), percent of total stomach content number 
(%N), and percent of total stomach content volume 
(%V) of prey categories were estimated for stomachs 
containing recognizable food (digestion code >2). The 
Index of Relative Importance (IRI=(%N+%V) x <7rFO) 
was calculated for each prey category (Pinkas et al., 
1971) and used for various diet comparisons. Diets 
were analyzed by season and geographic area (Win- 
ter-Fundy, Winter-Georges, Winter-Shelf, Suramer- 
Fundy), as well as by depth range within season and 
area, to compare food items from shallow regions 
and offshore banks <<100 m), mid-depths (101-200 
m) and the shelf edge or deep basins (>200 m). Diel 
differences in diet composition (day and night, based 
on time of gear deployment) were examined for the 
entire data set. Ontogenetic differences in diet 
within season/area were examined by grouping fish 
lengths into four size classes (<151, 151-200, 201- 
250 and >250 mm FL), which were assumed suffi- 
cient for detecting shifts in prey composition. Data 
from 1990 and 1991 were combined for all compari- 



sons because the ranks of IRI values for all prey 
categories between years were highly correlated 
(Spearman rank correlation coefficient (r s )=0.67; 
P<0.05; n=9). 



Predator-prey size analysis 

Total lengths (±1 mm, tip of rostrum to end of tel- 
son) of undigested, whole M. norvegica in the stom- 
achs of 55 alewives (>200 mm FL, since most intact 
prey occurred only in larger fish) from Winter- 
Georges, Winter-Shelf, and Summer-Fundy cruises 
were compared with predator size. Thysanoessa spp. 
were not measured because of poor condition. 
Lengths of M. norvegica from Emerald Basin col- 
lected in June 1991, by Sameoto et al. (1993) using 
the Bedford Institute of Oceanography Net and 
Environmental Sensing System (BIGNESS) were 
compared with euphausiid length frequencies from 
stomach contents to estimate the proportion of the 
available size range of M. norvegica consumed by 
alewives. The BIONESS is not considered to be size- 
selective for euphausiids (Sameoto et al., 1980). 



160 



Fishery Bulletin 92(1). 1994 



Diel feeding periodicity and daily ration 
estimate 

Diel feeding periodicity and daily ration were exam- 
ined separately for winter (Bay of Fundy, Scotian 
Shelf, and Georges Bank combined) and summer 
(Bay of Fundy) collections because of seasonal dif- 
ferences in photoperiod. Stomach fullness data from 
tows within each successive 3-hour (winter cruises) 
and 4-hour (summer cruises) interval were grouped 
and assigned to the midpoint of the time period. 
Small sample sizes precluded grouping of summer 
collections into 3-hour intervals. 

Daily ration (DR) of alewives during winter and 
summer and by size class during winter (<151 mm, 
151-200 mm, 201-250 mm, >250 mm) was esti- 
mated in terms of % body weight from the model of 
Elliott and Persson (1978): 

c _ (*-*■-) a . 



1-e 



■Rt 



where the consumption of food (C t ) during the time 
interval t to t t is calculated from the average 
amount of food in the stomach at time t (S„), the 
amount in the stomach at time t t (S,) and the instan- 
taneous evacuation rate R. The estimates of C t cal- 
culated for each time interval are then summed to 
give the total daily ration (DR). Feeding is assumed 
constant within each time interval. R is assumed 
exponential and temperature dependent (Elliott, 
1972), as 



R = ae hT . 

The slope (6) may be fairly constant for different 
prey types and fish species (mean=0.115), but the 
intercept (a) changes with prey type and can be 
estimated from gastric evacuation experiments 
(Durbin et al., 1983). Gastric evacuation rate data 
are unavailable for anadromous alewives; therefore, 
an intercept (a=0.0406) was obtained from Durbin 
et al. based on values for a variety of small 

invertebrates fed to several freshwater and marine 
fishes. High fat levels in the prey may retard evacu- 
ation (Durbin et al., 1983) but the principal food 
item in this study (M. norvegica) has a low lipid 
content (Ackman et al., 1970). Average bottom tem- 
peratures for winter (mean=7.16°C) and summer 
(mean=7.43°C) collections were used to estimate R. 

Statistical analysis 

Differences in the rankings of IRI values for prey 
categories (n =8 1 between three or more groups were 
tested for significance with the Kendall coefficient 



of concordance (w) (Siegel, 1956); for paired groups, 
the Spearman rank correlation coefficient (rj was 
used (Fritz, 1974). Euphausiids, which consistently 
ranked highest in importance in all comparisons, 
were excluded from correlation analysis to reduce 
bias and emphasize correlations among remaining 
prey groups. 

One-way ANOVA was used to examine feeding 
activity, represented by the index of fullness (arc- 
sine Vp transformed) by season and geographic area, 
by depth range within season and geographic area 
and by diel sampling period (winter and summer 
collections) and to compare total lengths of eu- 
phausiid prey. Paired means, adjusted for unequal 
sample sizes, were compared with the Tukey- 
Kramer test (Sokal and Rohlf, 1981). The relation 
between predator fork length and mean prey length 
was examined by linear regression for alewives with 
three or more M . norvegica present in their stomachs. 

Results 

Alewives examined for stomach contents measured 
95 to 305 mm FL (mean=213.6 mm, n=l,215); fish 
from summer cruises in the Bay of Fundy were 
larger on average than those from other collections 
(Table 1). Capture depths ranged from 36 to 269 m, 
although most (75%) specimens were obtained from 
regions 101 to 200 m deep. 

Recognizable prey from over 20 different taxa oc- 
curred in 55% (668 of 1,215) of stomachs examined 
(Table 2). Over 95% of the total prey number, vol- 
ume, and frequency of occurrence were crustaceans 
(Table 2). Euphausiids were the most prevalent (91% 
by volume); Meganyctiphan.es norvegica were domi- 
nant by volume (61%) and furcilia larvae of 
Thysanoessa spp. were dominant numerically (32%). 
Other prey, including hyperiid amphipods, calanoid 
copepods, crustacean larvae, mysids, polychaetes, 
chaetognaths, pteropods, and fish larvae contributed 
little and varied temporally and spatially in relative 
importance. 

Diet composition by season and area 

Euphausiids were the most important food of ale- 
wives during winter and summer for all areas (Fig. 
2). During winter, alewives from the outer Bay of 
Fundy and Georges Bank fed almost exclusively on 
euphausiids (99% and 95% of total volume, respec- 
tively). On Georges Bank, small (%V<3) proportions 
of calanoid copepods, hyperiid amphipods, and ptero- 
pods were also consumed. Prey diversity was great- 
est for alewives from the Scotian Shelf; euphausi- 
ids dominated by volume (82%) but were numeri- 



Stone and Jessop: Feeding habits of Alosa pseudoharengus 



161 









Table 2 








Prey items found in the stomachs 


of alewives, Alosa 


pseudoharengus , collected from 


groundfi 


sh research 


surveys off Nova Scotia, 1990 


-91. %FO = 


percent frequency of occurrence, %N = percent by number, 


%V = 


percent by volume. 
















Prey item 


%FO 


%N 


%V 


Prey item 


%FO 


%N 


%v 


Crustacea 


97.6 


95.0 


97.3 


Decapoda 


0.5 


0.1 


<0.1 


Euphausiacea 


91.3 


72.4 


91.0 


Zoea 


0.2 


<0.1 


<0.1 


Meganyctiphanes norvegica 


37.7 


29.4 


60.9 


Megalopa 


0.3 


0.1 


<0.1 


Thysanoessa spp 


6.9 


4.5 


6.0 


Cirripedia Cypris larvae 


0.2 


<0.1 


<0.1 


Thysanoessa spp furcillia 
Unidentified Euphausiacea 


3.7 
40.1 


32.1 
6.3 


1.2 
23.0 


Insecta Hymenoptera 


0.5 


<0.1 


<0.1 


Amphipoda 


15.9 


4.7 


4.8 


Polychaeta 
Nereis spp 


1.8 
1.1 


0.1 
0.1 


0.5 
0.4 


Hyperiidea 

Parathemisto gaudichaudi 
Unidentified Hyperiidea 


15.6 
9.9 

5.7 


4.2 
3.1 
1.0 


4.4 
2.9 
1.5 


Unidentified Polychaeta 
Chaetognatha 


0.8 
1.1 


<0.1 
3.6 


0.1 

<0.5 


Gammaridea 
Caprellidea 


0.3 
0.2 


0.5 
<0.1 


0.4 
<0.1 


Hydrozoa 


0.3 


— 


<0.1 










Gastropoda Pteropoda (Limacina) 5.1 


0.8 


0.3 


Copepoda 
Calanoidea 


8.2 


17.4 


1.2 


Teleost larvae 


3.9 


0.5 


1.4 


Centrophages spp 
Calanus spp 


3.1 
0.5 


1.3 
0.7 


0.2 
<0.1 


Ammodytes dubius 
Unidentified fish larvae 


2.7 
1.2 


0.5 
<0.1 


1.0 
0.4 


Metridia spp 
Unidentified calanoids 


2.0 
6.9 


1.1 
14.3 


<0.1 
0.9 


Algae 

Organic material 


1.2 
0.6 


— 


0.2 
<0.1 


Mysidacea 








Unidentified remains 


6.6 


— 


0.8 


Neomysis americana 


0.2 


0.4 


0.2 


Total stomachs with food 
Total prey number 


668 
14,752 






Cumacea 


0.3 


<0.1 


<0.1 


Total prey volume (points) 


25,232 







cally less than in other areas. Hyperiid amphipods, 
(Parathemisto gaudichaudi), ranked second in im- 
portance (%V=10), followed by crustacean larvae 
(furciliae), calanoid copepods, and fish larvae, 
(Ammodytes dubius). During summer in the Bay of 
Fundy, alewives fed heavily on euphausiids (%V=95) 
but also consumed chaetognaths, mysids, and poly- 
chaetes (second, third, and fourth in importance). 

Rankings of IRI values (excluding euphausiids) for 
Winter-Georges, Winter-Shelf, and Summer-Fundy 
samples were not significantly correlated (u^O.22, 
P=0.701), indicating seasonal and geographic differ- 
ences in the dietary importance of these lesser prey 
categories. Winter-Fundy samples contained too few 
prey categories to be analyzed. 

Diet composition by depth range 

For Winter-Shelf and Summer-Fundy collections, 
the proportion of euphausiids in the diet increased 
with increasing depth (Fig. 3). At bottom depths less 
than 101 m on the Scotian Shelf, euphausiids com- 
posed 64% of total volume and 22% of total number; 
at 101 to 200 m, %V = 83 and %N = 23 and at depths 



greater than 200 m, %V = 96 and %N = 95. During 
summer in the Bay of Fundy, euphausiid consump- 
tion increased with depth such that at less than 101 
m, %V = 82 and %N = 35; at 101 to 200 m, %V = 97 
and %N = 97; while at depths greater than 200 m, 
both %V and %N = 100. Other prey categories gen- 
erally decreased in number with increasing depth 
as did their relative proportion. For both Winter- 
Shelf and Summer-Fundy collections, prey diversity 
and abundance were greatest where bottom depths 
were less than 101 m. 

Multiple correlations of IRI values for prey cat- 
egories (excluding euphausiids) between the three 
bottom-depth interval groups were not significant 
(u>=0.54, P=0.12) for Scotian Shelf collections and 
reflect the decreasing number of prey categories 
with increasing depth. For Summer-Fundy samples, 
the Spearman rank correlation of IRI values for the 
two shallower depth-intervals was not significant 
(r s =-0.35, P>0.05) and euphausiids were the only 
prey at depths greater than 200 m. 

Depth-related differences did not occur in the 
euphausiid-dominated diet of alewives from the 
Winter-Fundy and Winter-Georges collections at 



162 



Fishery Bulletin 92(1), 1994 



Winter-Fundy 

(n = 58) 



Winter-Georges 

(n = 147) 




%N 



%v 



1UU- 






60- 






20- 




j^L 


20- 






60- 






100^ 


I I I I 


I I 1 1 



Winter-Shelf 



%N 



%v 





n = 322) 








100- 




60- 














20- 






y 


20- 






60- 






100 i 


I I I I 


I 




I I 



%N 



%v 



Summer-Fundy 




(n - 141) 
OO-i 


Legend 








Eup 


60- 






Cop 
Pter 








Amp 


20- 




I 


CruLar 


20- 






=1 Chaet 

M Mys 








1 Poly 


60- 








00- 


1 1 1 1 


1 




H- l=J 


!0% FO 





t— I = 20% FO 

Figure 2 

Relative importance of prey categories in the diet of alewives, Alosa 
pseudoharengus, collected from groundfish research surveys off 
Nova Scotia (1990-91), ranked from highest Index of Relative Im- 
portance (left to right) by season and area, n = number of stom- 
achs with prey; '#FO = % frequency of occurrence; %N = % of total 
prey number; %V = % of total prey volume; Eup = euphausiids; Cop 
= calanoid copepods; Pter = pteropods; Amp = hyperiid amphipods; 
CruLar = crustacean larvae; FishLar = fish larvae; Chaet = cha- 
etognaths; Mys = mysids; Poly = polychaetes. 



bottom depths exceeding 101 m (no fish were ob- 
tained at bottom depths less than 101 ml. IRI 
rankings of" prey categories between depth groups 
r Georg nk collections were highly correlated 

• .=0 !9, P fi.01 ' / prey i igorie n 

present for analysis of Winter-Fundy collections. In 

both winter and summer, most euphausiids con- 

med at depths less than 101 m were Thysanoessa 

pp. v than M. m vegica a) 

f, r shallower regions < (Table 3). 

el vari< t 

t h ou gh i 



numbers and volumes were ingested 
during the day (7rN=74, %V=92) than 
at night ( r /rN=16, %V=85) (Fig. 4). IRI 
values for day and night collections 
were not significantly correlated 
(r s =0.26, P>0.05) reflecting the 
greater consumption of hyperiid am- 
phipods during the day and copepods, 
crustacean larvae and fish larvae at 
night. 

Diet composition by size class 

Diet composition was relatively homo- 
geneous among alewife size groups 
(<151 mm, 151-200 mm, 201-250 
mm, >250 mm) with euphausiids com- 
posing most of the total food volume 
(Fig. 5). Multiple correlations of IRI 
values for prey categories (excluding 
euphausiids) by fish length group 
were significant for both the Scotian 
Shelf (u;=0. 58, P=0.024) and Georges 
Bank (w=0.65, P=0.011). For Sum- 
mer-Fundy collections, diets of the 
two largest size groups were nearly 
identical; IRI values were not signifi- 
cantly correlated (r s =0.38, P>0.05) 
due to slight differences in the 
rankings of minor prey categories 
(i.e., amphipods, mysids, polychaetes, 
chaetognaths). 

Prey size composition 

Alewives ingested similar sizes of M. 
norvegica during winter (Georges 
Bank, Scotian Shelf) and summer 
(Bay of Fundy) (Fig. 6). Modal peaks 
in euphausiid size appeared at 25-27 
mm and 30 mm on the Scotian Shelf and at 30-35 
mm for Georges Bank and the Bay of Fundy. In com- 
parison, M. norvegica from Emerald Basin 
BIONESS collections in June 1991 were bimodally 
ibut( it 25-27 mm and 34 mm. Euphausiids 
larger than 29 mm were proportionately less fre- 
quent than in stomach contents. 

Mean lengths of M. norvegica consumed by ale- 
vives varied by season/area group (F._, 7II| =65.5, 
P<0.001), although differences between means were 
small (Winter-Georges: mean=32.1±3.13; Winter- 
Shelf: mean=28.7±3.72; Summer-Fundy: mean 
ll.2±3.64). The average size of euphausiids con- 
d did not differ (F, 50 =3.31, P =0.075) with ale- 



wife stum;. I tion -ize i ran<i;.>: 225-300 mm FL). 



Stone and Jessop: Feeding habits of Alosa pseudoharengus 



163 



Feeding activity 

Feeding activity, as indicated by 
mean stomach fullness index 
values, varied by season/geo- 
graphic area (F 3 1910 =46.20, P< 
0.001). Mean stomach fullness 
was highest for Summer-Fundy 
and Winter-Shelf collections and 
lowest for Winter-Fundy and 
Winter-Georges collections (Ta- 
ble 4). The proportion of feeding 
fish was highest during summer 
in the Bay of Fundy (80.6%) and 
lowest during winter on Georges 
Bank (33.6%). Stomach fullness 
was significantly higher at bot- 
tom depths greater than 200 m 
for all but the Winter-Shelf col- 
lections, where mean fullness 
did not differ among depth 
groups (Table 4). Similarly, the 
proportion of feeding fish was 
highest in areas exceeding 200 m 
deep for all collections. 

Alewife feeding activity varied 
throughout the diel period dur- 
ing winter (F 1 1(m =24.97, P< 
0.001) and summer (F 5 196 = 7.98, 
P<0.001) with maximum full- 



%N 



%V 



Winter-Shelf 

100-| < 101 m (n = 49) 

60 



20- 



20- 



60 



100 



Summer-Fundy 

100-1 < 101 m (n = 33) 




Chaot 



%N 



%v 



60 



20- 



20" 



60 



100 



Jzj_P" 



%N 



%v 



100- 


101-200 


m (n = 262) 


60- 






fl 








j 


L 












20" 




60- 
























1 1 1 


I 


I 1 


i i 



%N 



%V 



100- 


101-200 


m 


<n 


= 72) 


60 - 










20- 








Amp 


20" 








Cop | 


60- 






















I I I 




I 


1 1 1 1 



Legend 

Eup 



Cop 

Pter 

Amp 

CruLar 

FIshLar 

Chaet 

Mys 

Poly 



%N 



%V 



ness in both seasons occurring 
near mid-day (Fig. 7). In winter, 
feeding activity was extremely 
variable: mean fullness was high 
during early morning (0001- 
0430 hours), declined until dawn 
(0730), increased sharply until 
early afternoon (1330), declined 
again in late afternoon (1630) 
and then increased after sunset 
before falling off again prior to 
midnight. During summer, diel 
feeding activity was much more 
constant, although sample sizes were smaller and 
stomach fullness more variable. Feeding activity in- 
creased gradually after sum ise, peaked by mid-mo 71- 
ing ( 1000), then declined throughout the afternoon and 
evening until just prior to midnight (2200). Although 
alewives fed actively at night during winter, peak feed- 
ing generally occurred during the day in winter and 
summer. 

Daily ration 

Daily consumption of alewives in the field was about 
1.22% BW at 7.16°C during winter and 1.88% BW 



100- 


> 200 m (n = 


11) 


60- 






20- 




M 






20" 






60- 






- 






100- 


I I I I 


i i i 



%N 



%V 





> 200 m (n = 36) 


60- 






20- 






20-1 






60- 








1 'III 


1 1 1 



i = 20% FO 



i = 20% FO 



Figure 3 

Relative importance of prey categories in the diet of alewives, Alosa 
pseudoharengus, obtained from groundfish research surveys off Nova 
Scotia (1990-91), ranked from highest Index of Relative Importance (left 
to right), by depth range, for Scotian Shelf (winter) and Bay of Fundy 
(summer) collections. (Symbols as in Fis;. 2). 



at 7.43°C during summer (Table 5). The winter daily 
ration of alewives generally decreased from 1.95% 
BW for fish less than 151 mm FL to 1.13% BW at 
151-200 mm FL, 1.19% BW at 201-200 mm FL and 
1.00% BW at larger than 250 mm FL. 



Discussion 

Our study clearly indicates that alewives off Nova 
Scotia feed primarily on euphausiids, particularly 
Meganyctiphanes norvegica; much smaller contribu- 
tions are made by other prey. Alewives from the 



164 



Fishery Bulletin 92(1), 1994 







Table 3 












Mean number 


of Meganyctiphanes norvegi 


:a and 


Thysanoessa spp. 


in 


the stomachs 


of alewives 


, Alosa 


pseudoh 


irengus 


, by depth interval 


within season 


and geogra 


phic area 


from groundfi 


sh researc 


h surveys 


off Nova Scotia (1990-91). 


n = nx. 


mber of s 


tomach 


s with 


prey. 






Depth 


M 


in 


i vegica 




Thysanoessa spp 


. 


















Season and area 


(mi 


Mean 


t 


SD 


n 


Mean 


+ 


SD 


n 


Winter-Fundy 


101-200 


11.3 


+ 


7.36 


3 


5.4 


+ 


0.81 


5 




>200 


10.2 


+ 


2.20 


9 


2.5 


i 


1.50 


2 


Winter-Georges 


101-200 


5.9 


± 


0.81 


26 


11.8 


* 


6.55 


6 




>200 


20.3 


+ 


1.68 


28 


— 




— 


— 


Winter-Shelf 


<101 


— 




— 


— 


32.0 


+ 


14.63 


10 




101-200 


14.7 


+ 


1.41 


89 


9.6 


± 


3.79 


20 




>200 


5.8 


1 


3.47 


1 


— 




— 


— 


Summer-Fundv 


<101 


18.9 


+ 


3.47 


14 


12.0 


± 


2.00 


2 




101-200 


21.9 


- 


2.67 


48 


— 




— 


— 




>200 


27.5 


± 


2.39 


31 


23.0 




— 


1 



100-1 



%N 



%v 




100 



Night 
(n = 290) 



%N 



%V 



Legend 

Eup 



100 




100 



"i — i — i — r 
i = 20% FO 



Figure 4 

Relative importance of prey categories in the diet of alewives, Alosa 
pseudoharengus, obtained from groundfish research surveys off Nova 
Scotia ( 1990-91), ranked from highest Index of Relative Importance 
(left to right) for day and night collections (Symbols as in Fig. 2). 



Atlantic seaboard of the United States consumed 
relatively fewer euphausiids 137-56% by weight) 
(Edwards and Bowman, 1979; Vinogradov, 1984) 
than off Nova Scotia (82-99% by volume). 

Euphausiids represent a large component of the 
marine zooplankton community and are abundant 
in the Bay of Fundy (Kulka et al., 1982; Locke and 
Corey, 1988), Gulf of Maine (Bigelow, 1926), the deep 
basins of the Scotian Shelf (Herman et al., 1991) and 
the outer shelf and shelf slope (Sameoto, 1982). 
Given their two-year life cycle (Hollingshead and 
Corey, 1974; Berkes, 1976), the availability and rela- 
tive abundance of euphausiids is more seasonally 



stable than for other prey spe- 
cies (i.e., chaetognaths, 
hyperiid amphipods, calanoid 
copepods, mysids), most of 
which undergo fluctuations in 
abundance progressing from a 
spring low to a summer high 
before declining in fall and win- 
ter (Evans, 1968; Sherman and 
Schaner, 1968; Corey, 1988; 
McLaren et al., 1989). 

Small seasonal differences in 
diet composition reflect the op- 
portunistic foraging behaviour 
of alewives and the availability 
of food types from offshore re- 
gions during winter as com- 
pared with the Bay of Fundy in 
summer. During winter, the 
diet diversity of alewives was 
greatest on the Scotian Shelf 
probably because the late win- 
ter (mid-March) sampling period co- 
incides with the hatching and occur- 
rence of the larval forms of Thy- 
sanoessa spp. (Berkes, 1976) and 
Ammodytes dubius (Scott, 1972), 
both of which occurred only in the 
diet of alewives from the Scotian 
Shelf. In the Bay of Fundy, alewife 
consumption of chaetognaths and 
mysids in the summer reflects their 
increased abundance and availabil- 
ity (Sherman and Schaner, 1968; 
Corey, 1988). 

The increased proportion of eu- 
phausiids in the diet of alewives 
from the Scotian Shelf (winter) and 
the Bay of Fundy (summer) coin- 
cides with an increased relative 
abundance of euphausiids with in- 
creasing depth. In the Scotian Shelf 
Basins, M. norvegica occur between 170 m and the 
bottom with highest concentrations generally below 
200 m (Sameoto et al., 1993). In the Bay of Fundy, 
M. norvegica is most abundant where bottom depths 
are between 165 and 200 m, while Thysanoessa 
inermis occur between 95 and 155 m (Kulka et al., 
1982). The greater proportion and number of other 
prey categories at depths less than 101 m on the 
Scotian Shelf and in the Bay of Fundy likely result 
from decreased euphausiid abundance (thereby in- 
creasing the relative contribution of other prey) 
rather than an absolute increase in the abundance 
of other zooplankters. Depth-related variation in 



Stone and Jessop: Feeding habits of Alosa pseudoharengus 



165 



euphausiid species composition in the 
diet of alewives from all regions 
matches differences in the bottom 
depth preferences of M. norvegicci 
(>150 m) and Thysanoessa spp. (100- 
150 m) (Berkes, 1976; Kulka et al., 
1982; Sameoto et al., 1993). 

Diel differences in the diet of ale- 
wives may reflect the influence of vary- 
ing light intensity on prey availability 
and on their relative success in locat- 
ing and capturing prey. Consumption of 
microzooplankters (crustacean larvae, 
calanoid copepods) was greater at night 
perhaps because of increased filter- 
feeding activity (Janssen, 1978b). Con- 
versely, ingestion of macrozooplankters 
(euphausiids, hyperiid amphipods) may 
be highest during the day because visual 
cues favour a particulate-feeding mode. 

Large size, darkly pigmented eyes, 
and a habit of forming large concentra- 
tions (Mauchline and Fisher, 1969) 
may make M. norvegica easily detect- 
able by alewives during daylight 
whereas at night, photophores along 
the abdomen of M. norvegica may as- 
sist detection. Most euphausiid species 
migrate vertically over the diel period, 
rising from deep water (150-200 m) 
towards the surface at dusk, remaining 
near surface throughout the 
night, and then migrating to 
the depths at dawn (Mauch- 
line, 1984). Alewives also have 
a diel pattern of vertical migra- 
tion in the marine environment 
(Neves, 1981; Stone and 
Jessop, 1992) and may encoun- 
ter sufficient light higher in the 
water column at night to par- 
ticulate feed on euphausiids. 

Ontogenetic differences in 
diet composition were not ap- 
parent; euphausiids dominated 
the diet of alewives ranging in 
length from 95 to 305 mm. Ale- 
wives switch from feeding pri- 
marily on microzooplankton to 
macrozooplankton at some 
point during their marine de- 
velopment and like other simi- 
larly sized clupeids, concentrate 
their feeding at intermediate 
trophic levels (James, 1988). 



Winter- 
Shelf 



100 



E 

O 

> 
CD 

1) 
u 

n. 



80 



GO 



40 



20 



 35 


12 


141 


134 






.;;:;' 









Winter- 
Georges 

13 65 34 3S 



Summer- 
Fundy 






66 


S3 









Legend 

Eup 



Cop 

Ptar 

Amp 

CruLar 

FIshLar 

Chaet 

Mys 

Poly 



B C 



C D 

Predator length group 



c D 



Figure 5 

Percentage of total volume of prey categories in the diet of ale- 
wives, Alosa pseudoharengus, for different size classes (mm FL) 
obtained from groundfish research surveys off Nova Scotia (1990- 
91). Euphausiids were the only prey category in Winter-Fundy 
cruises. A: <151 mm; B: 151-200 mm; C: 201-250 mm; D: >250 
mm; Eup = euphausiids; Cop = calanoid copepods; Pter = ptero- 
pods; Amp = hyperiid amphipods; CruLar = crustacean larvae; 
FishLar = fish larvae; Chaet = chaetognaths; Mys = mysids; Poly 
= polychaetes; n = number of stomachs with food. 



Winter-Georges 
Winter-Shelf 
Summer-Fundy 
BIONESS 




(n = 257) 
(n - 269) 
(n = 178) 
(n = 785; 



25 30 35 

Total length (mm) 



45 



Figure 6 

Size frequency distributions of M. norvegica consumed by alewives, Alosa 
pseudoharengus, obtained from winter (Georges Bank. Scotian Shelf) and 
summer (Bay of Fundy) groundfish surveys off Nova Scotia (1990-91) and 
from BIONESS samples in Emerald Basin (Spring, 1991 ). n = sample size. 



166 



Fishery Bulletin 92(1), 1994 







Table 4 










Mean stomach fullness index (arcsine Vp transformed) by season and 


geographic area and by 


depth 


interva 


for 


al 


ewives, Alosa 


pseudoharengus, 


obtained from groundfish research surveys 


off Nova 


Scotia (1990-91) 


Mean fullness inde 


x values 


lacking 


a letter in com- 


mon are significantly differe 


nt (Tukey HSD, 


P<0.05). 


n = number of 


stomachs examined (including empty 


stomach 


s). 
















Full 


ness index 


(%BW) 








% with 










Season and area 


Depth (m) 


n 


food 


Mean 


i 


SD 


Maximum 


Winter-Fundy 


all 


112 


51.8 


2.3z 


i 


0.25 


9.9 


Winter-Georges 


all 


438 


33.6 


2.1z 


± 


0.13 


9.9 


Winter-Shelf 


all 


489 


65.0 


3.8y 


± 


0.10 


10.0 


Summer-Fundy 


all 


175 


80.6 


3.9y 


+ 


0.21 


10.0 


Winter-Fundy 


101-200 


60 


28.3 


1.5z 


t 


0.29 


9.4 




>200 


52 


78.8 


3.7y 


+ 


0.32 


9.9 


Winter-Georges 


<101 


7 


28.6 


2.1z 


i 


0.87 


5.9 




101-200 


376 


28.7 


1.7z 


t 


0.12 


9.9 




>200 


55 


67.3 


4.6y 


* 


0.46 


9.9 


Winter-Shelf 


<101 


92 


55.3 


3.4z 


i 


0.16 


7.4 




101-200 


385 


68.1 


3.9z 


+ 


0.12 


10.0 




>200 


12 


91.7 


3.4z 


+ 


0.46 


8.0 


Summer-Fundy 


<101 


48 


liS s 


3.5z 


+ 


0.33 


8.8 




101-200 


87 


82.8 


3.6z 


+ 


0.30 


10.0 




>200 


40 


90.1 


5.0y 


t 


0.51 


9.8 



Gilmurray (1980) found mainly microplanktonic 
prey (e.g., calanoid copepods, cypris larvae, insects) 
in the diet of alewives less than 80 mm FL obtained 
from tidal creeks in the upper Bay of Fundy. The 
shift towards consumption of macrozooplankton 
likely occurs at fish sizes smaller than those examined 
in the present study (i.e., <95 mm FL). 

Diel feeding activity during winter and summer, 
as indicated by the mean fullness index, reached a 
maximum near mid-day and is typical of size-selec- 
tive predators which rely on visual cues (Eggers, 
1977). Summer resident subadult alewives in Minas 
Basin display a similar feeding pattern, although 
peak feeding occurred later in the afternoon (1500 
hours), coincident with the time of high tide when 
turbidity was lowest and prey visibility highest 
(Stone, 1985). Summer feeding activity by juvenile 
anadromous alewives in freshwater also peaks dur- 
ing the day but ceases or declines overnight ( Jessop, 
1990). Nocturnal feeding by alewives was more ap- 
parent during winter than summer; the significance 
of this seasonal difference in feeding activity is un- 
clear. Alewives can and do feed efficiently at night 
using both particulate (Janssen and Brandt, 1978) 



and filter-feeding (Janssen, 
1978b) modes. 

Alewives greater than 200 
mm FL generally consumed the 
largest Meganyctiphanes avail- 
able. Length-frequency distri- 
butions of M. norvegica, which 
has a life span of about two 
years, are typically bimodal 
(Hollingshead and Corey, 1974; 
Berkes, 1976). Alewives selec- 
tively favor larger prey (Brooks 
and Dodson, 1965; Brooks, 
1968; Wells, 1970) and likely 
use a particulate feeding strat- 
egy in doing so. Slight seasonal 
and geographic differences in 
the average size of M. 
norvegica ingested likely reflect 
size differences in euphausiid 
populations rather than selec- 
tion by the predator. 

Daily ration calculations 
were based on the model of El- 
liott and Persson (1978) which 
was originally intended for 
field samples collected within a 
given area from the same popu- 
lation over time. Our stomach 
fullness data for alewives from 
the Bay of Fundy, Georges 
Bank, and the Scotian Shelf covered a wide area 
geographically and may involve more than one popu- 
lation. The broad temporal and spatial coverage 
reduces the effect of day-to-day and regional varia- 
tions in diet which would arise from more restricted 
sampling. Calculated daily ration levels for alewives 
off Nova Scotia were similar to those reported for 
other teleosts (Fange and Grove, 1979). Lower esti- 
mates were obtained during winter (1.22% BW at 
7.16°C) than for summer ( 1.88% BW at 7.43°C) since 
temperature is related to metabolic requirements 
and to the evacuation rate of stomach contents 
(Durbin et al., 1983). Both estimates are well above 
maintenance ration levels for temperatures in the 
7-8°C range and are sufficient for positive growth 
(Brett and Groves, 1979). Alewife daily ration de- 
clined with increasing fish size; small fish, includ- 
ing marine species such as North Sea cod, Gadus 
morhua (Daan, 1973), winter flounder, Pseudo- 
pleuronectes arnericanus (Huebner and Langton, 
1982) and silver hake, Merluccius bilinnearis 
(Durbin et al., 1983), generally consume proportion- 
ally more food per unit weight than large fish 
(Windell, 1978). Overall, our estimates of daily 



Stone and Jessop: Feeding habits of Alosa pseudoharengus 



167 











Table 5 












Mean amount of food (%BW) in the stomachs of alewives, Alosa pseudoharengus , 


obtained from 


groundfish 


surveys off Nova 


Scotia 


(1990-91), 


with estimates of food consumption (C.) 


and daily ration {DR 


= XCJ, by 


season and size c 


lass, n 


= number of stomachs examined (including 


empty 


stomachs. For winter collections, 


R = 0.0925, temperature = 7.16°C; 


'or summer collections, R = 


0.0954, tern 


perature = 7.43°C. 












Stomac 


h 
















contents (%BWl 








Season 

(size class) 




Time period 
(hr) 












c, 

(%BW) 


DR 




n 


Mean 


+ 


SD 




(%BW) 


Winter (all) 




2400-0300 


84 


0.75 


+ 


0.100 






1.216 






0300-0600 


184 


0.65 


* 


0.053 




0.098 








0600-0900 


97 


0.23 


± 


0.038 




-0.308 








0900-1200 


122 


0.52 


+ 


0.079 




0.401 








1200-1500 


96 


1.09 


i 


0.104 




0.792 








1500-1800 


150 


0.20 


( 


0.032 




-0.709 








1800-2100 


177 


0.52 


± 


0.043 




0.421 








2100-2400 


189 


0.42 


i- 


0.053 




0.033 

0.488 




Summer (all) 




2400-0400 


11 


0.22 


i 


0.041 






1.880 






0400-0800 


5 


0.58 


+ 


0.198 




0.515 








0800-1200 


61 


2.32 


± 


0.161 




2.316 








1200-1600 


74 


1.32 


• 


0.190 




-0.320 








1600-2000 


19 


0.48 


i 


0.249 




-0.508 








2000-2400 


5 


0.03 


+ 


0.031 




-0.357 
0.234 




Winter 




2400-0400 


29 


0.95 


.i 


0.233 






1.949 


(<151 mm FL) 




0400-0800 


31 


1.13 


± 


0.146 




0.563 








0800-1200 


4 


0.90 


+ 


0.382 




0.143 








1200-1600 


3 


1.32 


+ 


0.439 




0.842 








1600-2000 


13 


0.42 


± 


0.110 




-0.593 








2000-2400 


87 


0.55 


i 


0.103 




0.311 




Winter 




2400-0300 


22 


1.10 


+ 


0.199 






1.126 


(151-200 mm FL) 




0300-0600 


IS 


0.61 


+ 


0.095 




-0.253 








0600-0900 


26 


0.12 


+ 


0.048 




-0.396 








0900-1200 


29 


0.22 


i 


0.063 




0.151 








1200-1500 


9 


0.84 


± 


0.532 




0.765 








1500-1800 


119 


0.14 


t 


0.039 




-0.565 








1800-2100 


26 


0.74 


t 


0.153 




0.719 








2100-2400 


25 


0.16 


* 


0.053 




-0.457 




Winter 




2400-0300 


30 


0.52 


± 


0.094 






1.189 


(201-250 mm FL) 




0300-0600 


60 


0.62 


i 


0.093 




0.256 








0600-0900 


23 


0.27 


+ 


0.062 




-0.222 








0900-1200 


:.] 


0.53 


* 


0.123 




0.372 








1200-1500 


27 


0.93 


i 


0.192 




0.600 








1500-1800 


56 


0.31 


+ 


0.065 




-0.453 








1800-2100 


42 


0.61 


+ 


0.075 




0.434 








2100-2400 


36 


0.50 


+ 


0.093 




0.046 
0.156 




Winter 




2400-0300 


14 


0.24 


t 


0.052 






1.000 


O250 mm FL) 




0300-0600 


34 


0.32 


+ 


0.042 




0.161 








0600-0900 


17 


0.27 


t 


0.067 




0.029 








0900-1200 


39 


0.68 


+ 


0.173 




0.545 








1200-1500 


57 


1.19 


± 


0.124 




0.772 








1500-1800 


22 


0.11 


I 


0.032 




-0.902 








1800-2100 


39 


0.31 


t 


0.076 




0.257 








2100-2400 


11 


0.50 


* 


0.141 




0.302 





168 



Fishery Bulletin 92(1], 1994 



x 

•a 

c 

</) 
w 

0) 

c 



7, 

6 

5. 

4. 

3 

2 

1 



Winter 



J 96 

i i A 

J— -Jim / \ r 

I M \ / \ 1,17 

V 1 \V t 18 

I 97 V 

1 J150 



l •  I 

3 6 



12 15 18 21 24 



7 

6 

5. 

4_ 

3. 

2. 

1 

0. 



Summer 



Jl61 



; r s 



\ 



^^v< 



4 8 12 16 20 24 

Time (h) 

Figure 7 

Diel feeding chronology of alewives, Alosa 
pseudoharengus , from winter and summer 
groundfish research surveys off Nova Scotia 
(1990-91), as determined from changes in 
fullness index values. Data are means (arc- 
sine \'p transformed with 95% confidence in- 
tervals) placed at the midpoint of each 3-hour 
(winter) and 4— hour (summer) interval. Aster- 
isk denotes mean significantly different (P<0.05) 
from that of previous time interval. Sample size 
is adjacent to each symbol. Open and solid por- 
s of horizontal bars represent light and dark 
hours during winter and summer. 



ration may be on the low side because of possible 
weight loss in M. norvegica due to the effects of for- 
malin preservation (Steedman, 1976). However, 
weight loss in euphausiids preserved for up to one 
year would likely be less than 10% because of their 
large size and low lipid content (Sameoto, 1993 1 ). 



1 D. Sameoto, Bedford Institute of Oceanography, Dartmouth, 
Nova Scotia B2Y 4A2, pers. commun. July 1993. 



The higher mean stomach fullness indices during 
summer in the Bay of Fundy and winter on the 
Scotian Shelf indicate that these regions are season- 
ally important foraging areas for alewives. Off Nova 
Scotia, alewives fed most actively (judged by the 
proportion of feeding fish and their stomach full- 
ness) where oceanic conditions, particularly depth 
(>200 m) and temperature, were suitable for M. 
norvegica (Kulka et al., 1982; Sameoto et al., 1993). 
Alewives prefer bottom temperatures of 7— 11°C off- 
shore at mid-depths in spring ( 101-183 m), in shal- 
lower nearshore waters in summer (46-82 m) and 
in deeper offshore waters in fall ( 119-192 m) (Stone 
and Jessop, 1992). During winter, Meganyctiphanes 
seeks deeper, warmer water rather than the cold 
upper layers (Bigelow, 1926; Hollingshead and 
Corey, 1974). While the seasonal pattern of move- 
ment by alewives (inshore and northward during 
spring and offshore and southward during fall) is 
partially linked with spawning migrations, it is 
apparent that their marine distribution is also in- 
fluenced by the distribution, availability, and abun- 
dance of their main prey, M. norvegica. 



Acknowledgments 

We thank D. Sameoto and R. Cutting for critically 
reviewing earlier drafts of the manuscript. We also 
wish to thank M. Strong, P. Fanning, and J. Martell 
for collecting the alewives used in our analyses, S. 
Wilson and J. Tremblay for taxonomic assistance, 
and D. Ingraham for helping with laboratory work. 



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estuary. Env. Biol. Fish. 19:55-67. 
Stone, H. H., and B. M. Jessop. 

1992. Seasonal distribution of river herring Alosa 
pseudoharengus and A. aestivalis off the Atlantic 
coast of Nova Scotia. Fish. Bull. 90:376-389. 
Swynnerton, G. H., and E. B. Worthington. 

1940. Notes on the food of fish in Haweswater 
(Westmoorland). J. Anim. Ecol. 9:183-187. 
Vigerstad, T. J., and J. S. Cobb. 

1978. Effects of predation by sea-run juvenile ale- 
wives ( Alosa pseudoharengus) on the zooplankton 
community at Hamilton Reservoir, Rhode 
Island. Estuaries 1:36-45. 
Vinogradov, V. I. 

1984. Food of silver hake, red hake and other fishes 
on Georges Bank and adjacent waters, 1968- 
74. NAFO Sci. Counc. Studies 7:87-94. 
Warshaw, S. J. 

1972. Effects of alewives (Alosa pseudoharengus) on 
the zooplankton of Lake Warskopmic, Con- 
necticut. Limnol. Oceanogr. 17:816-825. 
Wells, L. 

1970. The effects of alewife predation on zooplankton 
in Lake Michigan. Limnol. Oceanogr. 15:556-565. 
Windell, J. T. 

1978. Digestion and the daily ration of fishes. In 
T Bagenal (ed.), Fish production in fresh waters, 
p. 227-254. Blackwell Scientific Pubis., London, 
365 p. 



Abstract. A survey of queen 

conch [Strombus gigas) popula- 
tions near Lee Stocking Island, 
Exuma Cays, Bahamas, showed 
that 74% of all adults were on the 
narrow island shelf adjacent to the 
Exuma Sound, in 10-18 m of wa- 
ter. None were found deeper than 
25 m, and relatively few adults 
were found shallower than 10 m. 
Numbers of juveniles were great- 
est on the Great Bahama Bank 
and decreased with increasing 
depth on the island shelf. No juve- 
niles were found in shelf regions 
greater than 15 m in depth. Pat- 
terns of shell morphology, which 
were related to growth rates in 
juveniles, suggest that adults that 
mature on the Great Bahama 
Bank rarely move to deep water, 
and that the most important 
sources for deep-water stocks are 
small, nearshore nurseries on the 
island shelf. The mostly unfished 
deep-water populations are prob- 
ably now the primary source of 
larvae for queen conch in the 
Exuma Cays. Because virtually all 
of the conch are within the limits 
of SCUBA diving, it will be impor- 
tant to identify and to protect criti- 
cal nursery habitats for reproduc- 
tive stocks. 



Queen conch, Strombus gigas, 
reproductive stocks in the central 
Bahamas: distribution and 
probable sources 

Allan W. Stoner 
Kirsten C. Schwarte 

Caribbean Marine Research Center. 805 E 46th Place 
Vera Beach, Florida 32963 



Manuscript accept 8 September 1993 
Fishery Bulletin 92:171-179 (1994) 



Queen conch (Strombus gigas), 
once abundant throughout the Car- 
ibbean region, have been fished to 
near extinction or to a level at 
which there is no longer a viable 
fishery in many localities (Appel- 
doorn et al., 1987; Berg and Olsen, 
1989). This is particularly true in 
nations where the fishery has been 
open to SCUBA divers. Stock 
depletion resulted in at least tem- 
porary closures of the conch fishery 
in Bermuda, Florida, Cuba, Bon- 
aire, and the U.S. Virgin Islands. 
Regulations including size limits, 
catch quotas, gear restrictions, and 
closed areas have been instituted 
in other countries. 

This study was conducted in an 
attempt to understand reasons for 
the rapid depletion of queen conch 
populations in the Caribbean re- 
gion, and to evaluate the signifi- 
cance of deep-water conch stocks. 
Several authors have suggested 
that these deep-water conch, living 
beyond the normal range of free 
divers, are the primary source of 
larvae for shall-water populations 
and the fishery (Berg and Olsen, 
1989; Wicklund et al., 1991; Stoner 
et al., 1992; Stoner and Sandt, 
1992). Therefore, we surveyed the 
density and age structure of queen 
conch in the vicinity of Lee Stock- 
ing Island in the central Bahamas. 
Differences in shell morphology 
and growth rate between conch 
found on Great Bahama Bank and 



on the windward island shelf adja- 
cent to Exuma Sound were used as 
indicators of geographic source for 
reproductive stocks. The impor- 
tance of deep-water populations is 
discussed in terms of fisheries 
management. 



Methods and materials 

Study site 

An assessment of the adult conch 
population was conducted between 
1989 and 1991 in a 12-km long sec- 
tion of the Exuma Cays, central 
Bahamas, adjacent to Lee Stocking 
Island (Fig. 1). To the west and 
south of the Cays lies the Great 
Bahama Bank, a shallow, sand- 
and seagrass-covered platform that 
extends to the Tongue of the Ocean. 
To the east and north is a narrow 
(1-2 km) island shelf, a steep shelf- 
break beginning at an approxi- 
mately 30-m depth, and the deep 
Exuma Sound. 

Great Bahama Bank in the re- 
gion of the study site is character- 
ized by strong tidal currents that 
carry oceanic water from Exuma 
Sound onto the bank through chan- 
nels between the islands. Approxi- 
mately 909r of the bank area is less 
than 3.5 m deep; the remainder is 
tidal channels with depths to 8 m 
near the inlets and between the 
Brigantine Cays. For this study the 



I 71 



172 



Fishery Bulletin 92(1). 1994 




Figure 1 

Map of the survey area near Lee Stocking Island, Exuma Cays, Bahamas. Flood tidal cur- 
rents (arrows) and the locations of queen conch, Strombus gigas, nursery habitats (cross- 
hatched) are shown. Dashed lines separate the inner and outer bank regions and delineate 
the study site. Areas south and west of the Brigantine Cays were not surveyed. 



bank was divided into an inner section from the 
Brigantine Cays to a line mid-way between the Brig- 
antines and Lee Stocking Island, and an outer sec- 
tion from the mid-line to the cays at the eastern side 
of the bank (Fig. 1). Each section is approximately 
5 km wide. The rationale for this division was that 
the outer section of the bank is flushed with oceanic 
water on every tide, while the inner bank is flushed 
only on extreme tides. Virtually all queen conch nurs- 
eries in the Exuma Cays are found within the outer 
5.0 km of the bank (Stoner et al., in press.) (Fig. 1). 
The eastern shores of the Exuma Cays are char- 
acterized primarily by steep aeolianite cliffs and 
beach rock interspersed with a few high-energy 
sandy beaches in coves, particularly on Lee Stock- 
ing Island and Children's Bay Cay. The seagrass 
Thalassia testudinum is found on shallow, soft-sedi- 
ment platforms extending a short distance off the 
sandy beaches. Most of the shallow nearshore, how- 
ever, is hard-bottom covered with a short turf of the 
green alga Cladophoropsis sp. The hard-bottom 
habitat, interspersed with small patches of sand and 
hard corals, is characteristic to 10-m depth. From 



10 to 20 m the bottom comprises mixed hard-bottom 
and bare sand. Off Lee Stocking Island, corals form 
a 2-km long steep ledge from 10 to about 18 m, but 
a gradual slope to 25 m is typical of most of the 
study area. Patchy sand, coral, and hard-bottom are 
found between 20 and 30 m. 

Detailed hydrographic charts are not available for 
the Exuma Cays; therefore, shelf bathymetry was 
mapped with 540 electronic depth-sounder points, 
corrected for tidal state, and positions acquired with 
Global Positioning System (GPS) from the RV Chal- 
lenger during summer 1991. GPS positions taken at 
close intervals along the eastern shores of the is- 
lands were used as zero-depth data points. Three- 
dimensional plotting features of Systat 5.0 software 
were used to provide a bathymetric chart for the 
shelf region with 0, 2.5, 5, 10, 15, 20, 25 and 30 m 
contours for depth at mean low tide. Total surface 
area for each of the seven depth intervals was cal- 
culated with a digitizing board and SigmaScan 3.9 
software. The surface area of the inner and outer 
bank regions was determined in a similar way with 
the aid of topographic maps. 



Stoner and Schwarte: Distribution of Strombus gigas 



173 



Survey methods 

The shelf region was surveyed in each of seven 
depth zones between 2.5 and 30 m (described above) 
along nine transects (perpendicular from the Cays 
into Exuma Sound) placed at approximately 1.0-km 
intervals. At each of the 63 shelf stations, divers 
swam parallel to the isobaths for a distance mea- 
sured with a calibrated General Oceanics flow meter 
equipped with a large propeller for low velocity 
flows. Calibration was performed by towing the 
meter repeatedly (n>6) through calm water at the 
side of a small boat over a pre-measured distance 
of 100 m. Precision was ±2%. Current velocity on the 
shelf adjacent to Lee Stocking Island is generally 
low (<3 cm/sec) and to the northwest, parallel to the 
isobaths (Smith, 1992 1 ). Recognizing the potential 
effect of current on the calculated distance, each dive 
included two legs, one up-current and one down- 
current in parallel lines of equal length separated 
by approximately 20 m. 

Two dives were made at most stations for density 
determinations and shell measurements (described 
below). For density, all queen conch were counted 
in an 8-m wide path defined by a line held between 
two divers. The average swim distance was 380 m, 
resulting in coverage of just over 3000 m 2 . Conch 
density was calculated by using only those conch in 
the 8-m band. Shell measurements were made for 
animals outside the 8-m band in areas with low 
conch densities. Underwater visibility was usually 
high and the area of bottom searched was actually 
much larger than the swim path alone. Conse- 
quently, all conch within approximately 30 m could 
be collected for measurement. In areas where conch 
densities were high, one dive was made to collect 
density data and another to collect only measure- 
ment data. An attempt was made to measure at 
least 100 adults from each depth zone, but this was 
not possible in the 0-5, 5-10, and 25-30 m zones 
because of low densities in these zones. Statistical 
differences in density among the survey zones were 
evaluated with the non-parametric Kruskal-Wallis 
test (Sokal and Rohlf, 1969) with stations used as 
replicates (n-9). 

The shallowest depth zone (0-2.5 m) was limited 
primarily to sandy coves on the major islands of the 
survey area. Adult queen conch were few in these 
areas, and juveniles were distributed unevenly; 
therefore, the important seagrass areas of the shal- 
low coves were thoroughly searched. Density mea- 
sures were not made but all conch encountered were 
measured (as described below). 



1 N. P. Smith, Harbor Branch Oceanography Inst., Fort Pierce. 
FL, pers. commun. 1992. 



Sparse distribution of adult conch and the large 
surface area of the Great Bahama Bank required the 
use of different survey methods from those applied 
on the shelf. Because the bank waters are shallow 
and conch were easily seen, large areas were sur- 
veyed by towing a diver at the surface in continu- 
ous lines. The bank region was divided into 95 — 1 
x 1 km squares oriented along lines of latitude. 
Then, in a systematic grid of lines running diago- 
nally through the squares, every square was crossed 
at least once during the survey. Additional tows were 
made in areas already known to have concentrations 
of adults, i.e., near nurseries previously mapped 
(Fig. 1; Stoner et al., in press.). Divers were towed 
a total distance of 126 km. 

Although water clarity on the bank was not as 
high as that on the island shelf, the towed diver 
could usually see at least 2.5 m on either side of the 
transect line. Surveys were not conducted on a few 
days when visibility was restricted. While being 
towed at approximately 50 cm/sec, the diver signaled 
numbers of adult queen conch to the boat operator, 
who recorded position. Positions for the ends of all 
straight line transects were determined with GPS, 
tow distance was estimated by chart, and conch 
density was calculated on the basis of the 5-m wide 
path examined. During the bank survey, 472 adults 
were gathered and measured. Presence of juveniles 
on the bank was noted but not quantified in this 
study. For comparison with shelf sites, a random 
collection of 322 juvenile conch was made from a 
nursery west of Lee Stocking Island during August 
1991. These conch were measured for shell length. 

The total number of adult queen conch was esti- 
mated crudely for each bank and shelf area by ex- 
trapolating the average density of conch for an in- 
dividual zone over the total surface area for the 
same zone. Because variances in the density data 
were large, confidence intervals for the extrapolated 
numbers of conch were not calculated. 



Shell measurements 

Queen conch reach sexual maturity between 3.5 and 
4 years of age, a few months after the shell edge has 
formed a broadly flared lip (Appeldoorn, 1988). Af- 
ter the lip flares, queen conch stop growing in length 
but continue to deposit shell material on the inside 
of the lip (Egan, 1985; Appeldoorn, 1988). Therefore, 
with certain limitations, thickness of the shell lip is 
an indicator of approximate age (Stoner and Sandt, 
1992). In this study, shell-lip thickness was mea- 
sured with calipers in the area of greatest thickness, 
about two-thirds of the distance posterior from the 



174 



Fishery Bulletin 92(1), 1994 



siphonal groove and 35 mm in from the edge of the 
shell, according to the methods of Appeldoorn (1988) 
and Stoner and Sandt (1992). Shell length was 
measured from the tip of the spire to the end of the 
siphonal canal in both adults and juveniles. Re- 
peated measures made by different persons showed 
that both length and lip thickness measurements 
were made to ±1 mm. Differences in length-fre- 
quency and thickness-frequency distributions 
were tested with the non-parametric Kolmogorov- 
Smirnov test. 

Morphological differences between bank and shelf 
populations were tested with canonical discriminant 
function analysis from shell length and lip thickness 
data. This multivariate technique is well suited for 
differentiating two types where individual charac- 
teristics do not separate the types. The analysis 
computes a third variable Z, which is a linear func- 
tion of both variables (length and thickness, in this 
case) such that the equation for the new line maxi- 
mizes the distance between the two types ( Sokal and 
Rohlf, 1969). The significance of the discriminant 
function Z was determined with the Hotelling- 
Lawley trace test statistic (Morrison, 1976). Results 
of the canonical analysis were then examined to 
determine what percentage of the individuals were 
correctly classified according to collection site. 

Observations were also made on general shell 
thickness (particularly in juveniles), length of api- 
cal spines and resultant shell diameter, and num- 
ber of spines per whorl. None of these characteris- 
tics were quantified systematically. 

Shell growth experiment 

Early observations suggested that shell phenotypes 
were different between shelf and bank conch. Adults 
from the shelf appeared to be longer and to have 
thicker shell lips than those from the bank. Juve- 
niles from the shelf were more narrow, thin-lipped, 
and had shorter apical spines than those on the 
bank (Martin-Mora, 1992). To examine the potential 
relation between shell morphology and growth rates, 
juveniles were tagged in two different nursery sites: 
in the well-studied nursery west of Children's Bay 
Cay and in seagrass areas off Charlie's Beach in the 
northeast cove of Lee Stocking Island (Fig. 1). Ju- 
veniles were individually marked with spaghetti 
tags (Floy Tag & Manufacturing Co.) tied around the 
spire and measured to the nearest millimeter with 
calipers. Charlie's Beach conch between 108 and 150 
mm (mean=137 mm, n=281) were measured and 
released in the last week of August 1990. Children's 
Bay Cay conch, somewhat smaller than the Charlie's 
Beach conch (106 to 133 mm, mean=118 mm. 



n=292), were tagged and released in early Septem- 
ber 1990. Conch from both populations were 
remeasured for shell length five months later, at the 
end of February 1991. Forty-eight conch were recov- 
ered at Charlie's Beach and 135 were recovered at 
the Children's Bay Cay site. Daily growth rate was 
calculated for individuals by dividing increase in 
length by the number of days between measure- 
ments. Differences in growth rate between the two 
sites were evaluated by using the Mann-Whitney U- 
test. 



Results 

Conch densities and abundance 

Densities of adult queen conch in the survey area 
were highest between 15 and 20 m depth on the 
island shelf (Table 1) with nearly 88 conch/ha 
(Fig. 2). Density was also high between the 10- and 
15-m isobaths. In both of these depth zones densi- 
ties of adults were highly variable, but there was no 
apparent pattern across transect lines. There was 
a highly significant difference in the density of adult 
conch in the survey zones (Kruskal-Wallis test, 
H adj =36.195, P<0.001KFig. 2). No conch were found 
deeper than 25 m, despite an abundance of appar- 
ently suitable habitat of sand and algae-covered 
hard-bottom. Adults were most sparsely distributed 



50 



20 • 



10  



o 
c 



If) 
c; 
v 
Q 



U 

C 

o 
O 



120  
100  

80 
60 
40 

20 




r+-. 



Eh 



Inner Outer 



Bank 



•- «- CN 



^ Depth 

in (Meters) 



Shelf 



Figure 2 

Density of queen conch, Strombus gigas, on the 
Great Bahama Bank and in six different depth 
zones of the island shelf hear Lee Stocking Island, 
Bahamas. Values are ± mean standard error of the 



Stoner and Schwarte: Distribution of Strombus gigas 



175 











Table 1 




Estimated total 


number o 


f adu 


It queen conch, Strombus gigas, in a 12- 


km section o 


fth 


e Exuma 


Cays 


, Bahamas, between 


Adderly Rocks and 


Rat Cay. 




















Density (no. /ha) 




Region 


Total area (h 


a) 


(mean ± SE of mean) 


Total no. of conch 


Bank 












Inner 




4,979 




0.19 ± 0.14 


946 


Outer 




3,997 




3.16 ± 1.69 


12,631 


Bank total 




8,976 






13,577 


Shelf 












0-2.5 m 




161 




Low — not qualified 


Negligible 


2.5-5 m 




198 




2.24 ± 1.70 


444 


5-10 m 




465 




7.21 ± 4.11 


3,353 


10-15 m 




429 




60.1 ± 46.8 


25,800 


15-20 m 




454 




87.9 ± 31.5 


39,902 


20-25 m 




320 




18.3 ± 9.1 


5,843 


25-30 m 




151 




± 





Shelf total 




3,687 






75,342 


Grand Total 




12,663 






88,919 



in the inner section of the Great Bahama Bank with 
only 0.19 conch/ha (SD=0.15, n=28). Density of adult 
conch in the outer (seaward) section of the bank was 
close to the value for the 2.5-5 m depth zone on the 
shelf. Although not quantified, numbers of adults 
in the nearshore (0-2.5 m) zone of the shelf were 
negligible. 

Few juvenile conch were observed on the shelf 
between 2.5-and 15-m depth (Fig. 2). A total of 372 
juveniles were found in densely aggregated patches 
on seagrass beds off the eastern beaches of Lee 
Stocking Island. On the Great Bahama Bank, most 
juveniles were aggregated in specific nursery loca- 
tions documented previously (Stoner et al., in 
press.). None was found deeper than 15 m. 

The area between 10 and 20 m depth on the is- 
land shelf was a particularly important habitat for 
adult queen conch (Table 1). Approximately 74% of 
all conch in the 12-km long survey area reside in 
this narrow depth zone. It is also clear that large 
expanses of shallow bank habitat support a rela- 
tively small proportion (15.2%) of the adult popula- 
tion. Mating conch and demersal egg masses were 
very abundant during summer months at shelf 
sites deeper than 10 m, but none were observed on 
the bank. 

Shell morphology 

The shelf sites were characterized by large adult 
queen conch, primarily between 200 and 260 mm 
(mean=227, SD=23, n=572), whereas most adult 



conch on Great Bahama Bank 
were between 170 and 210 mm 
shell length (mean=187, 
SD=16, n=472). Pooling all 
adults measured, there was a 
highly significant difference in 
the length-frequency distribu- 
tion of conch on the shelf and 
on the bank (Kolmogorov- 
Smirnov test, P<0.001). The 
distributions (Fig. 3) show 
clearly the separation in size of 
adults between bank and shelf 
sites, particularly when com- 
paring nearshore (0-5 m) shelf 
zones with those from the 
bank. The distributions show a 
decrease in shell length be- 
tween the nearshore shelf and 
deeper zones, while those be- 
tween 5 and 25 m are obviously 
similar. 

Bank conch had thin shell 
lips (mean=10, SD=6); conch 
from nearshore (2.5-5 m) regions of the shelf were 
intermediate in lip thickness (mean=18, SD=5); and 
deep-shelf (5-25 m) conch had the thickest shell lips 
(mean=30, SD=7)(Fig. 4). All three of these groups 
were significantly different from one another in 
terms of lip thickness distribution (Kolmogorov- 
Smirnov tests, P<0.01). There was obvious similar- 
ity in the thickness distributions of shells in depth 
zones between 5 and 25 m; therefore, these four 
depth categories were pooled. 

Distinctness of the morphs collected on the bank 
and shelf is further suggested by a plot of shell 
length and lip thickness for 250 randomly chosen 
individuals from each of the two regions (Fig. 5). 
Also, when length and lip thickness data for all 
1,029 conch measured in the survey were used in 
canonical discriminant function analysis, a highly 
significant separation was found between conch col- 
lected in the two different regions (Hotelling-Lawley 
Trace, F= 1,854, P<0.001). Less than 5% of the conch 
in the survey were not collected in the region pre- 
dicted by the multivariate equation. Bank conch 
were small and had thin shell lips, whereas conch 
from the island shelf were large and had thick shell 
lips. Results of the analysis, however, do not rule out 
the possibility that the smallest adult conch from 
the shelf region, particularly apparent in the 5-10 
m depth zone, could be older animals from the bank. 
Length-frequency distributions of juvenile queen 
conch were different on the Great Bahama Bank and 
island shelf (Fig. 6). Both the bank and nearshore 



176 



Fishery Bulletin 92(1). 1994 









40 


N - 472 Boik 




30 






20 






10 






40 


n . m Shelf 0-5 m 




30 


 




C 20 


j_ 




O 10 


Jl 




_l 1 


- -■■ 




o « 


N .57 Shelf 5-10 m 




D x 






Q_ 20 






o l0 

CL 






v, «o 


N . 22» Shelf 1 0- 1 5 m 




O 30 






-1 — ' 20 


J 




rcen 

o o o 


-- ^. 




:, , ,50 Shelf 15-20 m 




CL) 






0- 20 


I 




10 


^m 




40 


. N _ loo Shelf 20-25 m 




JO 






20 






10 






100 120 140 160 180 200 220 240 260 280 300 


She!! Length (mm) 


Figure 3 


Length-frequency distributions for adult 


queen conch, Strombus gigas, on the Great 


Bahamas Bank and in five different depth 


zones of the island shelf near Lee Stocking 


Island, Bahamas. 











40 


N - 472 Bonk 






30 








20 


A 






10 


JL 






to 


N . j6 Shelf 0-5 m 






30 


 




c 


10 


J_ 




o 


10 


Jl 




1 , 




40 


. JHH 




o 


K ,i, Shelf 5-10 m 




13 


so 






CL 


20 






O 

CL 


10 


.^4. 




^_ 


40 


N . 2 29 Shelf 10-15 m 




o 


30 
20 






c 

CD 

(J 


10 


4 


_jL 




n. iso Shelf 15-20 m 




CD 


30 






CL 


20 


1 






10 


^jjL 






40 


n . ioo Shelf 20-25 m 






30 








20 


J 






10 


_jB_ 






100 120 140 160 180 200 220 240 260 280 300 




Shell Length (mm) 




Figure 4 


Distribution of shell lip-thickness for adult 


queen 


conch, Strombus gigas, on the Great 


Bahama Bank and in five different depth 


zones 


of the island shelf near Lee Stocking 


Island 


Bahamas. 



(0-2.5 m) shelf had juveniles less than 100 mm in 
shell length; however, these were rare in the shelf 
environment, and few juveniles less than 160 mm 
were found on the shelf between 2.5- and 15-m 
depth. None of the juveniles on the bank were near 
the 227-mm average length of adults on the shelf, 



but many juveniles collected in deeper water were 
close to adult size. 

Other differences were observed in the shells of 
queen conch from bank and shelf regions. Juvenile 
conch from the bank differed from shelf juveniles 
because of thicker shells and longer lateral spines 



Stoner and Schwarte: Distribution of Strombus gigas 



177 



w 

c 

-XL 



Q. 



50 

40 
30 
20 
10 




° Bonk 
• Shelf 



- ^i t • • 

v Jn 



♦. 400. 




10 15 20 25 

Shell Length (cm) 



30 



Figure 5 

Scatterplot of shell lip-thickness vs. shell length for 
adult queen conch, Strombus gigas, collected from the 
Great Bahama Bank and from the Lee Stocking Island 
shelf. Two-hundred and fifty randomly chosen points 
were plotted for each site. 



(5—6 spines/whorl vs. 7-9 spines/whorl in shelf ju- 
veniles). Bank conch had a maximum shell diameter 
between 80 and 90% of shell length at 100 mm 
length, whereas juveniles from the shelf had diam- 
eters between 50 and 60% of shell length. These 
characteristics persisted to adult stages with bank 
conch having longer spines. The outer whorls of 
shelf adults, even young individuals, were often 
nearly smooth. 

Growth rates 

Juvenile queen conch on the island shelf at Charlie's 
Beach grew in length at a rate approximately 2.4 
times the rate observed at the Children's Bay Cay 
site. Conch recovered at Charlie's Beach grew 0.139 
mm/day (SD=0.025, n=135). At Children's Bay Cay, 
mean growth rate was 0.058 mm/day (SD=0.021, 
n=48). The differences in growth rate between bank 
and shelf juveniles were highly significant (Mann- 
Whitney [/-test, P<0.001). 



Discussion 

The rapid increase in adult queen conch density at 
depths greater than 10 m is probably a direct func- 
tion of fishing, which is limited to free-diving on the 
bank and shallow nearshore shelf areas around Lee 
Stocking Island. This conclusion is substantiated by 
observations of conch depth distribution in other 
localities. In unfished areas of Islas Los Roques, 
Venezuela, Weil and Laughlin (1984) found that 




60 B0 100 120 140 160 180 200 220 240 260 280 



Shell Length (mm) 

Figure 6 

Length-frequency distribution for juve- 
nile queen conch, Strombus gigas, from 
the Great Bahama Bank and from two 
depth zones on the island shelf near Lee 
Stocking Island, Bahamas. 



density of queen conch was highest in 4.0 m of wa- 
ter and density decreased with depth to 18 m. This 
may represent the natural distribution of queen 
conch. In comparable 4-m deep habitats not pro- 
tected from fishing, densities were 5 times less than 
those in the protected area. Similarly, in the Exuma 
Land and Sea Park, a 500-km 2 fishery reserve 90 
km north of Lee Stocking Island, there are large 
numbers (unquantified) of adult conch at 2-4 m 
depth, and many of these shallow-water conch have 
been observed laying eggs (Stoner, pers. observ.); 
whereas adults are uncommon in shallow water 
near Lee Stocking Island and spawning has never 
been observed at less than 5 m depth. Similar to the 
pattern reported in this study for Lee Stocking Is- 
land, Torres-Rosado ( 1987) found maximum density 
of adult queen conch between 10 and 20 m in Puerto 
Rico, where fishing is heavy in shallower waters. 

It is recognized that queen conch move to greater 
depths with age and size (Randall, 1964; Weil and 
Laughlin, 1984); this has been confirmed in the Lee 
Stocking Island area by the recovery of individuals 
that were tagged as juveniles at Charlie's Beach and 
subsequently found in deeper offshore waters 



Fishery Bulletin 92(1). 1994 



(Stoner, unpubl. data). However, our morphological 
analyses of conch suggest that very few conch us- 
ing the bank for a nursery actually reach the off- 
shore spawning sites. Furthermore, similarities in 
length frequency and shell morphology between ju- 
veniles found immediately off the east (windward) 
side of the Cays on isolated seagrass beds and adults 
in deep water suggest that the small aggregations 
of juveniles found on the shelf serve as the primary 
source for the offshore reproductive stocks. Given 
that mating and egg-laying are rare on the Great 
Bahama Bank, it is likely that recruitment to bank 
nurseries is sustained by deep-water reproductive 
populations (Wicklund et al., 1991; Stoner et al., 
1992; Stoner and Sandt, 1992). 

Differences in shell morphology between bank and 
shelf conch are not well understood but appear to 
be related to growth rate. Alcolado (1976) reported 
that large, thin shells and short spines in queen 
conch in Cuba were associated with rapid growth. 
A similar phenomenon may explain the shell differ- 
ences observed in this study. Juveniles in the 
nearshore shelf environment of Charlies' Beach 
grew rapidly and had the large, thin-shelled, short- 
spined morphotype typical of the shelf adults. The 
small, thick-shelled, long-spined conch on the bank 
had growth rates less than half of those on the shelf. 
A recent transplant experiment at Lee Stocking Is- 
land demonstrated that shell form and spination in 
juvenile conch is an environmentally mediated char- 
acteristic associated with habitat type and indi- 
vidual growth rate (Martin-Mora, 1992). 

The large size of the deep-water reproductive 
stock may explain high productivity of queen conch 
in the Exuma Cays. It is likely, however, that abun- 
dance of conch in the region is now dependent upon 
the small, isolated pockets of fast-growing juveniles 
that inhabit the nearshore shelf habitat during the 
first two or more years of life then recruit to deep- 
water reproductive populations. Stoner and Sandt 
(1992) found that the adult population at an 18-m 
deep site off Lee Stocking Island was relatively 
stable between 1988 and 1991, but most individu- 
als were old and thick-lipped. The predominance of 
old conch in deep water may or may not be a func- 
tion of low recruitment rates from shallow water in 
recent years, and the significance of shallow-water 
spawning to conch abundance is unknown. 

In an comparison of data from Glazer and Berg 
(in press.), densities of queen conch in the Exuma 
Cays are 10 to 100 times higher than those reported 
for many other localities in the Caribbean region. 
This may be related to geographic differences in 
habitat quality, recruitment processes, and fishing 
methods. The Exuma Cays probably represent a 



particularly efficient system for retaining conch lar- 
vae because of unique geographic and oceanographic 
conditions such as an alongshore current and nu- 
merous tidal inlets leading to nursery grounds 
(Stoner et al., in press), but fishing methods can play 
a large role in the population structure of queen 
conch. Fishing in the Bahamas is restricted to free- 
diving and limited diving with surface-supply air for 
adults with flared shell lips; therefore, conch deeper 
than 10 m are rarely exploited. Depth distribution 
of queen conch near Lee Stocking Island suggests 
that virtually every conch in the Exuma Cays is 
within the range of SCUBA divers and that popu- 
lations of S. gigas could be decimated quickly if the 
fishery were opened to this latter gear. On the other 
hand, if the source of deep-water conch is shallow- 
water nurseries, protection of deep-water reproduc- 
tive stocks only delays the effects of overfishing, and 
certain nurseries should be protected as well. Analy- 
sis of larval transport and recruitment processes will 
be crucial to the sound management of this already 
threatened commercial species. 



Acknowledgments 

This research was supported by a grant from the 
Undersea Research Program of NOAA, U.S. De- 
partment of Commerce. We thank P. Bergman, G. 
Donnly, R. Gomez, J. Lally, D. Mansfield, M. Ray, 
V. Sandt, D. Wicklund, and E. Wishinski for assis- 
tance in the field work. R. I. Wicklund prompted us 
to examine the important juvenile stocks off the 
windward beaches. The manuscript was improved 
with helpful criticism by R. Appeldoorn, R. Hardy, 
E. Martin, M. Ray, and an anonymous reviewer. 



Literature cited 

Alcolado, P. M. 

1976. Crecimiento, variaciones morfologicas de la 
concha y algunos datos biologicos del cobo 
Strombus gigas L. (Mollusca, Mesogas- 
tropoda). Acad. Ciencias de Cuba, Inst, de 
Oceanol. No. 34, 36 p. 
Appeldoorn, R. S. 

1988. Age determination, growth, mortality, and 
age of first reproduction in adult queen conch, 
Strombus gigas L., off Puerto Rico. Fish. Res. 
6:363-378. 
Appeldoorn, R. S., G. D. Dennis, and O. 
Monterrosa-Lopez. 

1987. Review of shared demersal resources of Puerto 
Rico and the lesser Antilles region. In R. Mahon 
(ed.), Report and proceedings of the expert consul- 



Stoner and Schwarte: Distribution of Strombus gigas 



179 



tation on shared fishery resources of the lesser 
Antilles region. FAO Fish. Rep. 383:36-106. 
Berg Jr., C. J., and D. A. Olsen. 

1989. Conservation and management of queen 
conch (Strombus gigas) fisheries in the 
Caribbean. In J. F. Caddy (ed.), Marine inverte- 
brate fisheries: their assessment and 
management. Wiley & Sons, NY, p. 421-442. 
Egan, B. D. 

1985. Aspects of the reproductive biology of 
Strombus gigas. M.S. thesis, Univ. British Co- 
lumbia, Vancouver, Canada, 147 p. 
Glazer, R. A., and C. J. Berg Jr. 

In press. Current and future queen conch, 
Strombus gigas, research in Florida. In R. S. 
Appeldoorn and B. Rodriguez (eds.), The biology, 
fisheries, mariculture, and management of the 
queen conch. Fundacion Cientifica Los Roques, 
Caracas, Venezuela. 
Martin-Mora, E. 

1992. Developmental plasticity in the shell of the 
queen conch, Strombus gigas. M.S. thesis, 
Florida State Univ., Tallahassee, 52 p. 
Morrison, D. F. 

1976. Multivariate statistical methods. McGraw- 
Hill, New York. 
Randall, J. E. 

1964. Contributions to the biology of the queen conch, 
Strombus gigas. Bull. Mar. Sci. 14:246-295. 
Sokal, R. R., and F. J. Rohlf. 

1969. Biometry. W. H. Freeman, San Francisco, 
776 p. 
Stoner, A. W., and V. J. Sandt. 

1992. Population structure, seasonal movements. 



and feeding of queen conch, Strombus gigas, in 
deep-water habitats of the Bahamas. Bull. Mar. 
Sci. 51:287-300. 
Stoner, A. W., V. J. Sandt, and I. F. Boidron- 
Metairon. 

1992. Seasonality in reproductive activity and lar- 
val abundance of the queen conch, Strombus 
gigas. Fish. Bull. 90:161-170. 
Stoner, A. W., M. D. Hanisak, N. P. Smith, and R. 
A. Armstrong. 

In press. Large-scale distribution of queen conch 
biology, fisheries, and mariculture: implications for 
stock enhancement. In R. S. Appeldoorn and B. 
Rodriguez (eds.), The biology, fisheries, maricul- 
ture, and management of the queen 
conch. Fundacion Cientifica Los Roques, Cara- 
cas, Venezuela. 
Torres-Rosado, Z. A. 

1987. Distribution of two mesogastropods, the 
queen conch, Strombus gigas Linnaeus, and the 
milk conch, Strombus costatus Gmelin, in La 
Parguera, Lajas, Puerto Rico. M.S. thesis, Univ. 
Puerto Rico, Mayaguez, 37 p. 
Weil, E., and R. Laughlin. 

1984. Biology, population dynamics, and reproduc- 
tion of the queen conch, Strombus gigas Linne, in 
the Archipielago de Los Roques National Park. J. 
Shellfish Res. 4:45-62. 

Wicklund, R. I., L. J. Hepp, and G. A. Wenz. 

1991. Preliminary studies on the early life history 
of the queen conch, Strombus gigas, in the Exuma 
Cays, Bahamas. Proc. Gulf Caribb. Fish. Inst. 
40:283-298. 



Abstract. — Regression and 
time series analyses were used to 
investigate the relation between 
Apalachicola River flows and blue 
crab, Callinectes sapidus, harvests 
in and around Apalachicola Bay, 
Florida. Apalachicola River flows 
in one year were positively corre- 
lated with Franklin County blue 
crab landings during the next year 
(r 2 =0.32, P<0.001, 1952-90), and 
the strength of the correlation in- 
creased when only more recent 
years were examined (r 2 =0.49, 
P=0.001, 1973-90). In this area, 
blue crabs mature to a harvestable 
size by one year of age. Apala- 
chicola River flows were also cor- 
related with neighboring Wakulla 
County blue crab landings with a 
one-year time lag (r 2 =0.52, 
P=0.001, n=l7), but were not asso- 
ciated with blue crab landings for 
the remaining west coast of 
Florida. The mean monthly flow 
from September to May, termed 
the growout period, was the pa- 
rameter most highly correlated 
with the following year's blue crab 
landings. Of five north Florida riv- 
ers examined, the Apalachicola 
River was most highly correlated 
with Franklin and Wakulla 
County blue crab landings. 

Results of this study further 
document the influence of Apal- 
achicola River flows on estuarine 
productivity. The positive relation 
between flows and blue crab har- 
vests a year later suggests that 
low flow conditions in the estuary 
during the growout period nega- 
tively affect juveniles. Although 
the underlying causes of the corre- 
lations are not known, the effect of 
inflows on estuarine salinity is one 
of several possible mechanisms 
that warrants further investigation. 



The influence of Apalachicola River 
flows on blue crab, Callinectes 
sapidus, in north Florida 



Dara H. Wilber 

1 640 Oak Ridge Road. Vicksburg. MS 39 1 80 



Manuscript accepted 20 July 1993 
Fishery Bulletin 92:180-188 1 1994) 



River flow affects many character- 
istics of estuaries, including salin- 
ity, turbidity, and nutrient and de- 
trital concentrations. Changes in 
flow, therefore, may significantly 
affect estuarine biota, the extent to 
which may be inferred by examin- 
ing historical relations between 
flow and productivity. Apalachicola 
Bay, Florida, like many estuaries, 
is subject to changes in freshwater 
inflow related to factors such as 
rainfall and upstream demands for 
agricultural, municipal, and indus- 
trial uses. Plans to reallocate fresh- 
water resources (U.S. Army Corps 
of Engineers, 1989 1 ) have renewed 
interest in the question of how 
freshwater inflows are related to 
productivity in the Apalachicola 
River and Bay system. This study 
examined the historical relation- 
ship between Apalachicola River 
flows and estuarine productivity. 

One method of characterizing the 
importance of freshwater inflow to 
estuarine productivity is to corre- 
late historical flow data with the 
commercial catch (landings) of es- 
tuarine-dependent species (Fun- 
icelli, 1984). Commercial landings 
are used to estimate estuarine pro- 
ductivity because they are often 
the only available long-term 
records from which species abun- 
dance can be inferred. Long-term 
records are available for several 
commercially important species in 
Apalachicola Bay, including oysters 
and blue crabs, which have differ- 
ent trophic requirements and es- 
tuarine residency patterns. By ex- 
amining associations between 



these species and Apalachicola 
River flows, effects of freshwater 
delivery upon estuarine productiv- 
ity can be evaluated. Associations 
between freshwater inflows and 
Apalachicola oyster harvests have 
been previously addressed (Wilber, 
1992). The present study examines 
the influence of Apalachicola River 
flows on local and regional commer- 
cial blue crab, Callinectes sapidus, 
landings. Other north Florida riv- 
ers were also examined to estimate 
the relative importance of the 
Apalachicola River to blue crab 
landings with respect to these 
drainages. 

Blue crabs in the Gulf of Mexico 
reach a harvestable size within a 
year of age (Perry, 1984) and com- 
prise a significant portion of the 
commercial landings by 18-months 
of age (Steele, 1992 2 ). Blue crabs 
enter the Apalachicola estuary as 
megalopae and young juveniles, 
reaching peak juvenile abundances 
in the winter (Livingston, 1983). 
Young crabs concentrate in the less 
saline portions of the bay, whereas 
egg-bearing females remain in the 
higher-salinity gulf waters where 
they spawn. It has been proposed 
that adult female blue crabs along 
the Florida gulf coast migrate to 



1 U.S. Army Corps of Engineers, Mobile 
District. 1989. Draft Post Authorization 
Change Notification Report for the Real- 
location of Storage from Hydropower to 
Water Supply at Lake Lanier, Georgia, 
320 p. 

2 P. Steele, Florida Marine Research Inst., 
108th Ave. SE, St. Petersburg, FL 33701, 
pers. commun. 1992. 



180 



Wilber: Influence of Apalachicola River flows on Callinectes sapidus 



181 



gulf waters near Apalachicola Bay to spawn and 
that the larvae are distributed to the south by loop 
currents (Oesterling and Evink, 1977). Evidence 
supporting this hypothesis was examined in this 
study. 



Methods 

Fisheries data 

Several aspects of the blue crab fishery may lead to 
inaccurate fishery representation of adult stock 
abundance. For example, unreported landings from 
the recreational fishery and crab bycatch from the 
shrimp fishery are potential sources of bias in blue 
crab landings statistics (Perry, 1984). Although these 
sources of error cannot be controlled, if they are 
independent of river flow and account for a rela- 
tively constant proportion of the total landings over 
time, a valid, although perhaps conservative, rep- 
resentation of environmental effects on the species 
can be obtained. 

The Florida Department of Natural Resources 
(FDNR) provided monthly landing data for blue 
crabs from Franklin and Wakulla Counties for 1979- 
90, monthly effort data (number of trips) for 1987- 
90, annual landing data from Wakulla County from 
1973 to 1990 (excluding 1977), and annual landing 
data from the Florida west coast from 1960-1990. 
Franklin County annual landing data from 1952 to 
1979 were also obtained (Herbert et al., 1988 3 ). Sta- 
tistical analyses (Wilkinson, 1990) were conducted 
by using the full 39-year Franklin County dataset, 
as well as a shorter (1973-90) dataset, which al- 
lowed comparisons between Franklin and Wakulla 
Counties that were not confounded by differences in 
time periods. The limited amount of effort data pre- 
cluded analyses of catch per unit of effort. 

Flow and rainfall data 

The Apalachicola River begins at the Florida state 
line by the confluence of the Chattahoochee and 
Flint Rivers. Apalachicola flow data were collected 
at the United States Geological Service gauge at 
Blountstown, Florida, which is the closest station to 
the estuary (105 km upstream) with an adequate 
period of record. This station is not immediately 
adjacent to the estuary, therefore fresh water from 
local inputs and storm events are not included. The 
drainage area downstream from the Blountstown 
gauge is less than 9% of the total area drained by 



the Apalachicola-Chattahoochee-Flint River system 
(Leitman et al., 1983 4 ). 

Parameters examined included the highest and 
lowest average flows for 7 and 120-consecutive days 
each year (referred to as the 7- and 120-day maxi- 
mum and minimum flows). Monthly minimum, 
mean, and maximum values, and the mean monthly 
flow during the growout period (September-May) 
were also examined. By using these flow durations, 
associations between landings and seasonal high 
and low flows could be examined, which was not 
possible when analyses included only mean annual 
flow. The growout-flow time period was adapted 
from a similar study correlating blue crab landings 
in Georgia with river discharges (Rogers et al., 
1990 5 ). 

Sufficient historical flow data were also available 
for the Suwannee, Econfina, St. Marks, and 
Ochlockonee Rivers (Fig. 1), thus permitting a re- 
gional analysis of associations between flows and 
blue crab landings. For each river, the annual one- 
day minimum, one-day maximum, and annual mean 
flows were used. One-day high and low flow magni- 
tudes were used because of their availability and 
because preliminary analyses which substituted 
other flow durations (annual minimums and maxi- 
mums) on the Apalachicola River did not change 
results considerably. 

Statistical analyses 

Blue crab landings and flow data were tested for 
monthly, seasonal, and inter-annual dependencies 
through autocorrelations. Data were adjusted to 
remove dependencies when autocorrelations were 
significant. If autocorrelations between successive 
months were present, data were replaced by the 
difference between each month and the preceding 
month. If seasonal autocorrelations were present, 
the effects were removed by dividing each value by 
a seasonal factor. For instance, if landings exhibited 
a significant autocorrelation with a 12-month time 
lag, which reflected a similarity in catches for the 
same month among years, each monthly value was 
divided by the month's mean value and replaced by 
the quotient. Similar analyses were conducted with 
seasonal (three-month averages) landings and flow 
data following adjustments to remove significant 
autocorrelations. Flow data were log 10 transformed. 



3 Herbert, T. A., and Associates. 1988. The Franklin County 
Fisheries Options Report, 164 p. 



4 Leitman, H. M., J. E. Sohm, and M. A. Franklin. 1983. Wet- 
land hydrology and tree distribution of the Apalachicola River 
flood plain, Florida. U.S. Geological Survey Water-Supply Pa- 
per 2196, 52 p. 

5 Rogers, S. G., J. D. Arrendondo, and S. N. Latham. 1990. As- 
sessment of the effects of the environment on the Georgia blue 
crab stock. Final Rep. Georgia Dep. Natl. Resources, 69 p. 



182 



Fishery Bulletin 92(1), 1994 



. . A .Jl A .£ A _M_A_ 




A- Apalachicola R. 
O Ocklockonee R. 
SM- St. Marks R. 

E- Econfina R. 

S- Suwannee R. 



" EST ^..-•'^•° °° 



Figure 1 

Percentage of total Florida west coast blue crab (Callinectes sapidus) landings 
caught by area (Steele, 1982). The five rivers used in the multivariate regres- 
sion analyses (Apalachicola, Ochlockonee, St. Marks, Econfina, and Suwannee) 
are depicted. 



Autoregressive order 1 (ARIMA) models were con- 
ducted on the Franklin and Wakulla County blue 
crab annual data and the residuals from these 
analyses were correlated with flow. This approach 
provided statistically rigorous estimates of P-values 
for the flow/landings relationships that were inde- 
pendent of any effects resulting from the one-year 
autocorrelations in landings. Analyses that used the 
ARIMA residuals and those that used unadjusted 
blue crab landings data were reported because both 
methods impart useful information. Correlations 
that used unadjusted annual blue crab data, i.e., 
significant autocorrelations were not removed, were 
biologically relevant because feedback mechanisms 
inherent to these autocorrelations (such as reproduc- 
tion and recruitment) may also be associated with 
flow. Results of analyses that used unadjusted data 
are also more readily compared to results of other 
studies. Use of ARIMA models statistically validated 



the significant relations between blue crab landings 
and flow data, but may have removed some biologi- 
cally relevant information. This paper primarily 
refers to unadjusted regression results. 

Regression analyses incorporating a one-year time 
lag between flows and landings were conducted to 
examine the effects of flow on early blue crab life 
history stages. Contemporaneous analyses were con- 
ducted to assess the effect of flow on adults. 

Univariate and stepwise multivariate regression 
analyses were conducted to estimate the amount of 
variability in blue crab landings accounted for by 
five major rivers on Florida's northern gulf coast. 
The criterion for admitting a flow variable into the 
stepwise regression models was an F-statistic 
greater than 4.0 for its partial correlation with land- 
ings. Data on blue crab landings for the west coast 
of Florida were used as a dependent variable in 
some analyses. To more specifically examine 



Wilber: Influence of Apalachicola River flows on Callinectes sapidus 



183 



whether there was evidence that the Apalachicola 
River affects blue crab landings on a regional basis, 
Franklin and Wakulla landings were removed from 
the west coast dataset. Regression analyses were 
conducted to test whether Apalachicola flows and 
the remaining west coast landings were significantly 
related. 



Results 

Annual landings 

Blue crab landings varied nearly 10-fold over the 
period of record examined in each county (Fig. 2). 
Significant autocorrelations between consecutive 
years were present in both Franklin (r 2 =0.19, 
P=0.006) and Wakulla (r 2 =0.37, P=0.016) County 
landings. Annual flow parameters did not exhibit 
any significant autocorrelations. 

Annual Franklin County blue crab landings were 
most highly correlated with Apalachicola River flows 
of the previous year and these correlations were 
positive (Table I). The growout flow with a one-year 
time lag accounted for the greatest amount of varia- 
tion in blue crab landings (r 2 =0.32, P<0.001; Fig. 
3A). The regression analysis of ARIMA residuals 
(autocorrelation in blue crab landings removed) and 
growout flows of the previous year was also signifi- 
cant (r 2 =0.21; P=0.004). Wakulla County landings 



ANNUAL BLUE CRAB LANDINGS 



1.5 



O.S 



0.0 



WAKULLA 
FRANKLIN 




—i — i — i — [ — i — i — i — i — | — i — i — i — i — [ — r 
1950 1960 1970 1980 

YEAR 



1990 



Figure 2 

Annual blue crab (Callinectes sapidus) landings for 
Franklin (closed squares) and Wakulla (open 
squares) Counties in millions of kilograms. 





Table 1 




R 2 values from 


regression analyses 


for Franklin 


(n=39) and Wakulla (n = 17) Coun 


ty blue crab 


(Callinectes sap 


idus) landings and 


Apalachicola 


River flows. All 


correlations were positive. 


Flow parameter 


Franklin 


Wakulla 


no lag period 






7-day low 


0.16* 


0.12 


120-day low 


0.14* 


0.18 


7-day high 


0.04 


0.07 


120-day high 


<0.01 


<0.01 


growout 


0.08 


0.10 


one-year lag 






7— day low 


0.25** 


0.29* 


120-day low 


0.21** 


0.21 


7-day high 


0.18* 


0.17 


120-day high 


0.21** 


0.31* 


growout 


0.32*** 


0.52*** 


* = P < 0.05. 






** = P < 0.01. 






*** = P < 0.001. 







were significantly correlated only with Apalachicola 
flows of the previous year, with the growout flow 
also accounting for the greatest amount of variation 
in annual blue crab landings (r 2 =0.52, P=0.001; Fig. 
3B). The regression analysis of ARIMA residuals 
and growout flows one year previous was significant 
(r 2 =0.35, P=0.02). The shorter (1973-90) data record 
for Franklin County landings was more strongly 
correlated with growout flows with a one-year time 
lag (r 2 =0.49, P=0.001; Fig 3C) than was the full 39- 
year dataset. 

Monthly and seasonal landings 

As expected, the monthly Franklin and Wakulla 
County blue crab landings (1979-90) exhibited sig- 
nificant autocorrelations for 1- and 12-month time 
lags. All monthly river flow parameters (minimum, 
mean, and maximum) also exhibited significant cor- 
relations between successive months and with 12- 
month lags. Correlations between monthly landings 
and flow parameters (without any adjustments for 
significant autocorrelations) were positive for time 
lags of 3, 4, and 5 months. Significant negative cor- 
relations were present for flows that lagged 2-4 
months behind landings. Correlations that used 
landings and flow data with the 1- and 12-month 
autocorrelation effects removed were not significant 
for either county. 

Peak harvests generally occurred between May 
and September in both counties. There were also no 
significant correlations between the seasonal (three- 



184 



Fishery Bulletin 92(1), 1994 



ONE-YEAR TIME LAG 
FRANKLIN COUNTY (1952-1990) 



ONE-YEAR TIME LAQ 
WAKULLA COUNTY (1873-1990) 




2.0 -i 



O 1.6 



1.0 



2 

° 0.6 



0.0 



r - 0.62 



B 



300 



500 



700 



800 1100 



300 



500 



700 



000 



1100 



QROWOUT FLOW (lnT/SEC) 



QROWOUT FLOW (M /SEC) 



ONE-YEAR TIME LAQ 
FRANKLIN COUNTY (1973-1990) 



1.0 



0.8 



o 

j 0.6 



I 

Q 



< 

cr 
o 



0.4 - 



0.2 - 



0.0 




T~ 

300 500 700 900 

QROWOUT FLOW (M^SEC) 



1100 



Figure 3 

Apalachicola River growout (flows m 3 /sec, mean flow from September through May) plotted against the following 
year's (A) Franklin County blue crab landings (1952-90), (B) Wakulla County blue crab landings (1973-90 ex- 
cluding 1977), and (C) Franklin County blue crab landings (1973-90). Flow data were log transformed in the 
statistical analyses. 



Wilber: Influence of Apalachicola River flows on Callinectes sapidus 



185 



Apalachicola 


1.00 


Ochlockonee 


0.59** 


St. Marks 


0.32 


Econfina 


0.50* 


Suwannee 


0.60** 


* = P < 0.01. 




** = P < 0.001. 





month average) flow and land- 
ings data with autocorrelations 
removed. The timing of peak 
monthly harvests was not re- 
lated to the magnitude of the 
annual harvests. 

Regional analysis 

Given the close geographical 
proximity of the five rivers ( Fig. 
1) used in the multiple regres- 
sion analyses, significant corre- 
lations between annual flow pa- 
rameters may be expected 
among the rivers. Apalachicola River an- 
nual mean flows, although significantly 
correlated with other river flows (except 
the St. Marks), had the lowest correla- 
tions with the other drainages (Table 2). 

Significant correlations with blue crab 
landings were more common for 
Apalachicola River flows than for any 
other north Florida river tested (Table 3). 
Franklin County landings were correlated 
only with Apalachicola flows, whereas 
Wakulla County and west coast landings 
were also correlated with Suwannee and 
Ochlockonee flows, respectively (Table 3). 
These significant univariate correlations 
incorporated a one-year time lag. 

The Franklin County multivariate re- 
gression model included Apalachicola and 
Ochlockonee minimum flows of the previ- 
ous year (r 2 =0.45, P<0.001; Table 4). The 
Wakulla multivariate model accounted for the most 
variation in blue crab landings (r 2 =0.64; Table 4) 
and included Apalachicola mean and Ochlockonee 
minimum flows of the previous year. The west coast 
multivariate model with a one-year time lag in- 
cluded Apalachicola maximum and Ochlockonee 
minimum and mean flows (r 2 =0.53; Table 4). 

The only significant multivariate model that in- 
cluded parameters with and without time lags was for 
west coast landings, which used both no-lag Suwannee 
minimum flows and Apalachicola maximum flows of 
the previous year (r 2 =0.49). Analyses that examined 
associations between Apalachicola River flow and 
west coast landings with Franklin and Wakulla 
County landings removed were not significant. 

Discussion 

Several consistent results appeared in the correla- 
tions of annual blue crab landings with Apalachicola 



Table 2 

Pearson correlation matrix of annual mean river flows for all possible 
combinations of five north Florida rivers. 

Apalachicola Ochlockonee St. Marks Econfina Suwannee 



1.00 
0.77* 
0.76* 
0.93* 



1.00 
0.64** 

0.77** 



1.00 
0.79* 



1.00 



Table 3 








Univariate correlations between Wakulla, Franklin, an 


d west 


coast blue crab (Callinectes sapidus 


) landings 


and th 


a river 


flows from five north Florida drainages (Suwannee, Econfina, 


St. Marks, Ochlockonee, and Apalachicola) wi 


th a one-year 


time lag. Signs of the correlations are given in 


parentheses. 


Region Correlation 


r 2 


P 


Franklin Apalachicola minimum 


( + ) 


0.31 


0.001 


Apalachicola mean 


( + ) 


0.25 


0.004 


Apalachicola maximum 


( + ) 


0.14 


0.039 


Wakulla Apalachicola minimum 


(+) 


0.29 


0.031 


Apalachicola mean 


( + ) 


0.38 


0.010 


Suwannee minimum 


( + ) 


0.30 


0.028 


West Coast Apalachicola mean 


( + ) 


0.15 


0.035 


Apalachicola maximum 


( + ) 


0.26 


0.004 


Ochlockonee minimum 


(-) 


0.22 


0.009 



Table 4 

Multiple regression results for Franklin, Wakulla, 
and west coast landings of blue crabs (Callinectes 
sapidus) with a one-year time lag incorporated 
into the analyses. The independent variables are 
the five river drainages listed in Table 3. Listed 
below are the signs of the correlations in paren- 
theses, Student's ^-statistics, and associated P- 
values. 



Region 



Variable 



Franklin 



Wakulla 



West Coast 



Apal. min ( + ) 
Och. min. (-) 

Apal. mean ( + ) 
Och. min. (-) 

Apal. max. ( + ) 
Och. mean ( + ) 
Och. min. (-) 



4.38 
-2.68 

4.57 
-3.05 

2.99 
3.12 
-2.61 



<0.001 
0.012 

0.001 
0.009 

0.006 
0.004 
0.015 



0.45 



(I 64 



0.53 



186 



Fishery Bulletin 92(1), 1994 



River flows. Statistically significant correlations 
were positive and primarily restricted to a time lag 
of one year, indicating higher flows were associated 
with higher blue crab landings the following year 
and lower flows with poorer landings the next year. 
The mean flow during the growout period (Septem- 
ber through May) of the previous year was the most 
highly correlated flow parameter with blue crab 
landings in both counties. 

A number of explanations are consistent with the 
observation that more fresh water (within a certain 
range) was associated with higher blue crab land- 
ings the following year. Greater freshwater inflows 
reduce estuarine salinities, thereby increasing the 
area of suitable habitat in the middle, and perhaps 
lower, estuary where juvenile blue crabs can forage 
and develop (Livingston et al., 1976; Perry, 1984). 
Increases in low salinity habitat may reduce preda- 
tion by marine species on juvenile blue crabs. 
Greater freshwater flows may also broaden an 
estuary's signal to offshore female migrants and/or 
megalopae, thus increasing the potential recruit- 
ment population base (Perry and Stuck, 1982; 
Mense and Wenner, 1989). In addition, higher in- 
flows carry more detrital and nutrient matter 
(Mattraw and Elder, 1982), which may either di- 
rectly or indirectly enhance food availability. 

In both Franklin and Wakulla counties, flows be- 
low approximately 600 m 3 /sec appear more closely 
related to the following year's landings than higher 
growout flows, i.e., the regression equation fits the 
data better at the low end of the flow spectrum (Fig. 
3). Several factors may explain this phenomenon. 
Food availability may limit blue crab production at 
flows below a certain level but may not be limiting 
at flows above this level and, therefore, crab produc- 
tivity is not influenced by further increases in flow. 
Prey limitation at low flows may also lead to canni- 
balism, further limiting blue crab population size 
(Lipcius and Van Engel, 1990). 

The finding that more recent years produce a 
stronger correlation between blue crab landings and 
river flows was also observed in Georgia (Rogers et 
al., 1990 5 ). Total discharges from September to May 
(growout period) of five Georgia rivers were posi- 
tively correlated with landings (r 2 >0.8). Shorter time 
periods (the most recent 14 and 19 years of land- 
ings statistics) produced better correlations with 
flow than the full period of record (37 years). The 
authors concluded increased fishing pressure in 
more recent years resulted in only one year class 
being fished, and, thus, environmental effects were 
more obvious on a single year class in the shorter 
dataset. Similarly, that more recent landings for 
Franklin County were more highly correlated with 



Apalachicola River flows than landings for the 
longer 39-year period may reflect a trend toward 
harvesting a single year class. 

The significant 1- and 12-month time lags in 
Franklin and Wakulla County reflect similarities in 
catches between successive months and a seasonal 
component, respectively. The 12-month auto- 
correlation indicates that trends in landings occur 
at the same time of year (e.g., summer peaks) and 
should not be confused with an annual auto- 
correlation, which is indicative of a similarity in 
harvests between entire years. The positive corre- 
lations between unadjusted monthly flow and land- 
ings data correspond to the summer peak in blue 
crab landings following 3-5 months after the spring 
peak in flows, and low winter landings following low 
late-summer and fall flows. The negative correla- 
tions with 2-4 month time lags reflect fall low flows 
following peak summer harvests and high spring 
flows occurring after low winter harvests. The ab- 
sence of significant correlations between monthly 
landings and flows, once these data were adjusted 
to remove seasonal autocorrelations, indicates that 
residual (non-seasonal) variation in monthly flows 
is unrelated to the non-seasonal variation in mon- 
thly landings. 

Livingston (1991) found a positive contemporane- 
ous correlation between monthly Apalachicola River 
flows and blue crab abundances in trawl surveys 
conducted from 1972 to 1985. This finding corre- 
sponds to high juvenile abundances during high-flow 
months. The positive correlation in the present 
study between monthly flows and blue crab landings 
3-5 months later may reflect the maturation of ju- 
veniles into adults in the summer, and thus the 
observed time lag in the correlation. 

The majority of the Apalachicola-Chattahoochee- 
Flint basin is in Georgia and is subject to different 
climatic conditions than are the other north Florida 
rivers examined, which may explain the relatively 
small correlations between Apalachicola River flows 
and flows on these other rivers. Georgia rainfall is 
more strongly correlated with Apalachicola River 
flows than Florida rainfall (Meeter et al., 1979). A 
consistent and important finding of the multivari- 
ate regression analyses was that Apalachicola flows 
were more highly correlated with Franklin, Wakulla, 
and Florida west coast landings of the next year 
than any other river drainage tested. Regressions 
comparing Apalachicola flows to west coast landings, 
after Franklin and Wakulla County landings were 
removed, were not significant, suggesting the influ- 
ence of the Apalachicola drainage is restricted pri- 
marily to Franklin and neighboring Wakulla County. 
Thus, there was no evidence supporting the hypoth- 



Wilber: Influence of Apalachicola River flows on Callmectes sapidus 



187 



esis of mass blue crab spawning near Apalachicola 
Bay and larval transport down the gulf coast of Flor- 
ida via the loop current (Oesterling and Evink, 1977). 

Several studies have addressed factors that influ- 
ence interannual variation in blue crab abundance, 
primarily concentrating on larval and post-larval 
recruitment (reviewed in Lipcius and Van Engel, 
1990). Lipcius and Van Engel (1990) found high 
interannual, seasonal, and spatial variation in blue 
crab abundances in a 17-year fishery-independent 
dataset collected in the Chesapeake Bay. They ob- 
served that years with high blue crab abundances 
appeared to be dominated by the previous year class 
because peak catches occurred in the summer. Years 
with low abundances had peak abundances in the 
fall, suggesting the dominance of the new year class. 
This observation supports the contention that varia- 
tion in recruitment plays a major role in determin- 
ing interannual fluctuations. No interaction between 
annual abundance and seasonal peak catch was 
apparent for the Franklin or Wakulla County blue 
crab landings, which may indicate either the true 
absence of such a relation, the inadequacies of us- 
ing fishery statistics, or a difference in growth rates 
between the two regions that invalidates the use of 
the same analysis. Interestingly, the fishery-inde- 
pendent trawl data from the Chesapeake were sig- 
nificantly (r 2 =0.33) correlated with the commercial 
landings data. 

The influence of physical factors on blue crab 
abundances has been documented in other areas, 
such as a positive relationship between blue crab 
landings and freshwater inflows in Georgia (Rogers 
et al., 1990 5 ), an inverse relation between salinity 
and juvenile blue crab abundances on the Texas 
coast (More, 1969), and a positive relation between 
blue crab productivity and vegetated area in the 
Gulf of Mexico (Orth and van Montfrans, 1990). The 
positive correlation between blue crab landings and 
Apalachicola River flows of the previous year pro- 
vides additional evidence of the importance of fresh- 
water inflows to juvenile blue crabs. 

Apalachicola River flows have a significant impact 
on estuarine productivity, as indicated by commer- 
cial harvests of oysters (Wilber, 1992) and blue 
crabs. Although statistical correlations do not indi- 
cate the causal mechanisms underlying these asso- 
ciations, the river's influence on estuarine salinities 
as a mediating factor is deserving of further exami- 
nation. Undoubtedly, the Apalachicola River affects 
estuarine biota via mechanisms other than salinity 
(Livingston, 1991). Factors such as the transport of 
nutrients and organic matter, however, are unlikely 
to result in a significant correlation between low 
flows and oyster harvests two years later, unless 



food limitation is only measurably important for 
newly settled oyster spat. In addition, the majority 
of nutrient and detrital transport from the river 
occurs during high flow periods in the spring 
(Mattraw and Elder, 1982). There was no evidence 
that above-average flows were associated with either 
oyster or blue crab productivity. In both fisheries, 
flows on the low end of the spectrum were most sig- 
nificantly associated with landings. These signifi- 
cant correlations were positive and incorporated 
time lags, suggesting estuarine conditions during 
low minimum flow periods were not favorable for 
juveniles of either species. 



Acknowledgments 

The careful reviews of R. Hardy, G. Lewis, D. 
Meeter, R. Lipcius, P. Steele, and R Wilber are grate- 
fully acknowledged, as well as the technical support 
of J. Bennett, J. McKenna, G. Miller, and D. 
Tonsmeire. This work was supported by the North- 
west Florida Water Management District and the 
State of Florida's Surface Water Improvement and 
Management (SWIM) Program. 



Literature cited 

Funicelli, N. A. 

1984. Assessing and managing effects of reduced 

freshwater inflow to two Texas estuaries. In V. S. 

Kennedy (ed. ), The estuary as a filter, p. 435-446. 
Lipcius, R. N., and W. A. Van Engel. 

1990. Blue crab population dynamics in Chesa- 
peake Bay: variation in abundance (York River, 
1972-1988) and stock-recruit functions. Bull. 
Mar. Sci. 46:180-194. 

Livingston, R. J. 

1983. Resource atlas of the Apalachicola 
estuary. Florida Sea Grant College Publication 
No. 55, 64 p. 

1991. Historical relationships between research 
and resource management in the Apalachicola 
River-estuary. Ecological Applications 1(4):361- 
382. 

Livingston, R. J., G. J. Kobylinski, F. G. Lewis HI, 
and P. F. Sheridan. 

1976. Long-term fluctuations of epibenthic fish and 
invertebrate populations in Apalachicola Bay, 
Florida. Fish. Bull. 74(2):311-321. 
Mattraw, H. C, and J. F. Elder. 

1982. Nutrient and detritus transport in the 
Apalachicola River, Florida. U.S. Geol. Surv. 
Water-Supply Pap. 2196-C. 
Meeter, D. A, R. J. Livingston, and G. C. 
Woodsum. 

1979. Long-term climatological cycles and popula- 



188 



Fishery Bulletin 92(1). 1994 



tion changes in a river-dominated estuarine 
system. In R. J. Livingston (ed.), Ecological pro- 
cesses in coastal and marine systems. Marine 
Science 10:315-338. 
Mense, D. J., and E. L. Wen nor. 

1989. Distribution and abundance of early life his- 
tory stages of the blue crab, Callinectes sapidus, 
in tidal marsh creeks near Charleston, South 
Carolina. Estuaries 12:157-168. 

More, W. R. 

1969. A contribution to the biology of the blue crab 
(Callinectes sapidus Rathbun) in Texas, with a 
description of the fishery. Texas Parks Wildl. 
Dep. Tech. Ser. 1:1-31. 

Oesterling, M. L., and G. L. Evink. 

1977. Relationship between Florida's blue crab 
population and Apalachicola Bay. In R. J. 
Livingston and E. A. Joyce (eds.), Proceedings of 
the conference on the Apalachicola drainage sys- 
tem; 23-24 April 1976, Gainesville, Florida. FL 
Mar. Res. Pub. 26:101-121. 

Orth, R. J., and J. van Montfrans. 

1990. Utilization of marsh and seagrass habitats by 
early stages of Callinectes sapidus: a latitudinal 
perspective. Bull. Mar. Sci. 46:126-144. 



Perry, H. M. 

1984. A profile of the blue crab fishery of the Gulf 
of Mexico. Gulf State Mar. Fish. Comm. No. 9, 
80 p. 

Perry, H. M., and K. C. Stuck. 

1982. The life history of the blue crab in Mississippi 
with notes on larval distribution: proc. blue crab 
colloquium; 18-19 October 1979, Biloxi, 
Mississippi. Gulf States Mar. Fish. Comm. 
7:17-22. 

Steele, P. 

1982. A synopsis of the biology of the blue crab 
Callinectes sapidus Rathbun in Florida: proc. blue 
crab colloquium; 18-19 October 1979, Biloxi, 
Mississippi. Gulf States Mar. Fish. Comm. 
7:29-35. 
Wilber, D. H. 

1992. Associations between freshwater inflows and 
oyster productivity in Apalachicola Bay, 
Florida. Estuarine, Coastal and Shelf Sciences 
35:179-190. 

Wilkinson, L. 

1990. SYSTAT: the system for statistics. SYSTAT, 
Inc. Evanston, IL, 676 p. 



Oocyte maturation in Hecate Strait 
English sole [Pleuronectes vetulus) 

Jeff Fargo 

Department of Fisheries and Oceans, Pacific Biological Station 
Biological Sciences Branch. Nanaimo, British Columbia V9R 5V6 

Albert V. Tyler 

School of Fisheries and Oceans 

University of Alaska, Fairbanks, Alaska 99775 



English sole, Pleuronectes vetulus, 
is an important component of the 
bottom trawl fishery in Hecate 
Strait, British Columbia, Canada. 
It is a small-mouthed flounder 
that feeds on sedentary inverte- 
brates associated with sandy sub- 
strate and is most common at 
depths of 80-150 m (Hart, 1973). 
The species is characterized by 
moderate growth (&=0.22), mortal- 
ity (M=0.20) and longevity (20 
years) (Fargo, 1993). It recruits to 
the fishery at an age of four years, 
which is roughly equivalent to the 
age of sexual maturity (Ketchen, 
1956; Tyler et al., 1987 1 ). Most of 
the exploited population is under 
12 years of age (30-45 cm in 
length) (Fargo, 1993). Results 
from tagging studies (Ketchen, 
1956; Fargo et al., 1984) and 
analysis of landing statistics and 
age composition data (Fargo, 
1993) indicate that a single stock 
exists in Hecate Strait. 

Since 1955, abundance for this 
stock has fluctuated, primarily be- 
cause of changes in recruitment 
(Fargo, 1993). Factors influencing 
recruitment for this stock are 
poorly understood. Ocean tem- 
perature and circulation have 



1 Tyler, A. V., J. Fargo, R. P. Foucher, and 
J. B. Lucas. 1987. Studies on the repro- 
ductive biology of Pacific cod and En- 
glish sole in Hecate Strait from the 
cruise of the FR/V W.E. Ricker, Novem- 
ber 25-29, 1986. Can MS. Rep. Fish. 
Aquat. Sci. 1937, 43 p. 



been found to influence spawning 
time and oocyte maturation for 
the stock off the Oregon coast 
(Kruse and Tyler, 1989). These 
authors postulated that 1) the 
rate of gonadal development for 
English sole was inversely related 
to summer bottom temperatures 
in the same manner as is somatic 
growth, and 2) spawning was de- 
layed by rapid increases in bottom 
temperature caused by upwelling. 
In Hecate Strait, where Ekman 
transport is weak, these tempera- 
ture changes may be brought 
about by the fall transition when 
strong winds from the south cause 
mixing of the warm surface wa- 
ters to depths of 150 metres 
(Dodimead, 1980 2 ). Relatively 
little information exists on spawn- 
ing time and egg development for 
the Hecate Strait stock. We inves- 
tigated oocyte growth and devel- 
opment to examine the length of 
the oocyte maturation period and 
the time and duration of spawn- 
ing for the English sole stock in 
Hecate Strait. 



Materials and methods 

Samples of English sole ovaries 
were obtained from research 



cruises and at ports-of-landing 
from commercial vessels between 
November 1987 and November 
1990. The fish were caught with 
bottom trawls at five locations 
throughout Hecate Strait (PMFC 
Areas 5C-D, Table 1, Fig. 1). 
Length-stratified samples were 
collected to ensure that ovaries 
were obtained throughout the size 
range of fish collected. For each 
collection we attempted to sample 
fifteen sexually mature fish from 
each 5-cm length interval over a 
range of 30-50 cm, though this 
was not always possible. The 
minimum size fish (30 cm) from 
which an ovary was dissected cor- 
responds to the length at first 
maturity for this stock (Ketchen, 
1956; Tyler et al., 1987 1 ). Total 
length and the condition of matu- 
rity for each fish sampled was re- 
corded. The right ovary was then 
removed and preserved in a buff- 
ered formalin-saline solution 
(Foucher et al., 1987 3 ). Sampling 
methods have been described in 
previous reports (Foucher et al., 
1987 3 ; Tyler et al., 1987 1 ). A list 
of ovary samples examined is 
given by sample type and month 
in Table 1. 

Preserved ovaries were pre- 
pared for histological examination 
by soaking in Davidson's fixative 
for approximately 24 hours. Sub- 
sequently, tissue sections were 
dissected from the anterior por- 
tion of the ovary (which contained 
the greatest amount of eggs), em- 
bedded in paraffin wax, sectioned 
at 5 u, stained with haematoxylin 
and counterstained with eosin 
(Yasutake and Wales, 1983). 

Oocyte diameter was measured 
with a light microscope calibrated 



2 Dodimead, A. J. 1980. A general review 
of the oceanography of the Queen Char- 
lotte Sound-Hecate Strait-Dixon En- 
trance region. Can. MS. Rep. Fish. 
Aquat. Sci. 1574, 248 p. 



3 Foucher, R. P., J. Fargo, and J.B. Lucas. 
1987. Cruise of the FV Nucleus. Janu- 
ary 5-17, 1987 to Hecate Strait to study 
reproductive biology of Pacific cod and 
English sole. Can. MS Rep. Fish. Aquat. 
Sci. 1941, 25 p. 

Manuscript accepted 8 October 1993. 
Fishery Bulletin 92:189-197 (1994) 



189 



190 



Fishery Bulletin 92(1), 1994 




Figure 1 

Location of trawling grounds in the study area, Hecate Strait, British 
Columbia, Canada. 



to the nearest 5 p, or with a projection microscope 
calibrated to the nearest 4 u. Three hundred oocytes 
were measured from at least one fish for every cm 
length interval for each sample (Table 1). Measure- 
ment of 300 oocytes per fish was necessary to pro- 
vide complete information on the size composition 
of developing oocytes. Only oocytes that had been 
sectioned through the nucleus, close to the center of 
the oocyte, were measured. Mean diameter was es- 
timated as the mean of the minimum and maximum 
diameters for each oocyte (Foucher and Beamish, 
1980). For smaller oocytes (10-20 p), precision of the 
measurement was lower because of distortion of the 
oocyte by surrounding maturing oocytes (Dunn, 
1970). A description of the histological stage of oo- 



cyte development (Fargo and Sex- 
ton, 1991 4 ) was also recorded. 

We were unable to obtain oocyte 
measurements from ovaries col- 
lected from ripe fish in October 
and November 1990. These 
samples were taken from com- 
mercial vessels at ports of land- 
ing. Ovaries from these samples 
had combinations of hydrated and 
non-hydrated oocytes with many 
burst cells. These fish had been 
held in chilled seawater for sev- 
eral days prior to sampling, prob- 
ably exacerbating the state of hy- 
drated oocytes and causing them 
to burst. Since oocyte diameter 
data for these samples would 
have been biased (because most 
measurable oocytes would not 
have reached the hydrated state) 
the slides from these samples 
were used only to assess the his- 
tological stage of the oocytes. This 
problem did not occur with the 
November 1987 sample collected 
at sea on a research vessel. 

Prior to statistical testing of the 
data, we tested oocyte size distri- 
butions for normality using the 
Shapiro-Wilk test. We applied two 
sample £-tests to test for differ- 
ences in the mean diameter of 
previtellogenic and vitellogenic 
oocytes between months within 
years and among years. We used 
linear regression to investigate 
the relation 1) between fish 
length and mean oocyte diameter 
within months and 2) between 

fish length and mean oocyte diameter at the time of 

spawning. 

Results 

Oocyte development 

Ovaries were examined from 174 fish (Table 1) 
caught at five locations in Hecate Strait (Fig. 1). The 
sampling period encompassed seven different 
months over three years. Descriptions and micro- 



4 Fargo, J., and T. Sexton. 1991. A quide to the ovarian histol- 
ogy of English sole iParophrys vetulus). Can. MS. Rep. Fish. 
Aquat. Sci. 2133, 19 p. 



NOTE Fargo and Tyler: Oocyte maturation in Pleuronectes vetulus 



191 



graphs of the stages of matura- 
tion for English sole oocytes 
have been summarized by 
Fargo and Sexton (1991). 4 Ex- 
amples of oocyte size distribu- 
tions for fish of different 
lengths sampled during the 
same period, August 1988, are 
presented in Figure 2. For all 
sizes of English sole collected, 
we observed the simultaneous 
presence of only two modes in 
the oocyte size distributions. 
The smaller mode (10-150 u> 
consisted of previtellogenic oo- 
cytes and the larger mode 
(150-500 u) of vitellogenic oo- 
cytes. No previtellogenic oo- 
ctyes >150 u were observed. 
The size modes for previtel- 
logenic oocytes were similar 
among fish ranging in size from 
33 to 46 cm. The mode for 
vitellogenic oocytes shifted to 
the right (increased) with in- 
creasing fish length. 

Vitellogenic oocytes in- 
creased in size from early sum- 
mer until they became hy- 
drated prior to spawning in the 
fall (Fig. 3). We observed no 
trend in the size composition of 
previtellogenic oocytes over the 
same period. As the month of 
spawning was approached a 
complete separation between 
the two modes became appar- 
ent. The irregular shape of the 
modal distribution for vitel- 
logenic oocytes in Figure 3 is 
caused by combining data for 
fish of different lengths and de- 
veloping at different rates. The 
more normal distribution for 
this mode during the month of 
spawning is due to two factors. 
First, the size range of fish for 
this sample was smaller than 
for other samples and, second, 
egg diameter at the time of 
spawning was similar for fish 
of different length. Fargo and 
Sexton (1991) 4 described the 
events of oocyte maturation for 
English sole in detail. Briefly, 





Table 1 






A summary of ovary 


samples examined 


in the study of oocyte matura- 


tion in Hecate Strait English sole (Pleu 


ronectes vetulus) 








Length class (cm) 








(No. ovaries 


Date 


Sample type 


Location 


examined) 


7-13 January 1987 


Research cruise 


Two Peaks 


30-34 (2) 






White Rocks 


35-39 (6) 
40-44 (5) 
45-49 (5) 
50-54 (4) 
55-59 ( 1 ) 






Total 


(23) 


19 January 1988 


Port sample 


White Rocks 


30-34 ( 1 ) 
35-39 (1) 
40-44 ( 1 ) 






Total 


(3) 


17 March 1987 


Research cruise 


Horseshoe 


30-34 (2) 
35-39 (2) 
40-44 (3) 
45-49 (2) 
50-54 (1) 






Total 


(10) 


16 March 1988 


Port sample 


Horseshoe 


30-34 ( 1 ) 
35-39 (4) 
40-44 (2) 
45-49 (1) 






Total 


(8) 


May 5 1988 


Port Sample 


Horseshoe- 


30-34 ( 1 ) 






White Rocks 


35-39 (1) 
40-44 (2) 
45-49 (6) 






Total 


(10) 


6 June 1987 


Research cruise 


Horseshoe- 


30-34 ( 1 i 






Bonilla 


35-39 ( 3 1 
40-44 (3) 
45-49 (3) 
50-54 (3) 






Total 


(12) 


2 June 1988 


Port sample 


Horseshoe 


30-34 ( 1 ) 
35-39 (3) 
40-44 (3) 
45-49 (3) 
50-54 (2) 






Total 


(12) 


27 August 1987 


Research cruise 


Horseshoe 


30-34 (1) 
34-39 ( 7 ) 
40-44 (5) 
50-54 1 1 ) 






Total 


(14) 



192 



Fishery Bulletin 92(1). 1994 





Table 1 


(continued) 












Length class (cm) 










(No. ovaries 


Date 


Sample type 




Location 


examined) 


22 August 1988 


Port sample 




Horseshoe 

Total 


30-34 (2) 
34-39 (5) 
40-44 (8) 
45-49 (6) 
50-54 (1) 
(22) 


28 August 1990 


Port sample 




Two Peaks 

Total 


35-39 (4) 
40-44 (4) 
45-49 (4) 
50-54 (1) 
(13) 


27 January 1988 


Port sample 




Two Peaks- 
Butterworth 

Total 


30-34 (4) 
35-39 (2) 
40-44 (3) 
45-49 (1) 
50-54 (1) 
(11) 


19 January 1990 


Port sample 




Horseshoe 

Tota 


30-34 (1) 
35-39 (6) 
40-44 (8) 
45-49 (1) 

(16) 


5-6 November 1987 


Research cruise 


Horseshoe- 


30-34 (5) 








Butterworth- 


35-39 (7) 








White Rocks 


40-44 (4) 
45-49 (2) 
50-54 (1) 


3 November 1990 


Port sample 




Butterworth 

Total 


30-34 (D 
35-39 (ll 
40-44 (2) 
45-49 (1) 
50-54 (1) 
(6) 



vitellogenesis occurred when oocytes reached a di- 
ameter of about 150 p. Vacuolization occurred in 
oocytes ranging from 180 u to 250 p Deposition of 
yolk in the outer cortex occurred in oocytes ranging 
in size from 200 p to 430 p, and hydra ted oocytes 
ranged in size from 375 (i to 550 p. 

We began our investigation of the timing and 
duration of oocyte maturation by examining the size 
composition and histological stage of oocytes col- 
lected from fish sampled between January and No- 
vember. Ovaries examined from 68 of 72 fish col- 
lected during winter and spring (January 1987-88 
and March 1987-88) contained mainly pre- 
vitellogenic oocytes. The fish examined from the 
January samples contained previtellogenic oocytes 



only. Four of 22 fish examined 
from samples collected during 
the month of March contained 
vitellogenic oocytes. Three of 
these (36-40 cm in length) con- 
tained vitellogenic oocytes that 
were hydrated and translucent 
(405-429 p mean diameter). 
The fourth fish (46 cm in 
length) contained oocytes that 
had recently undergone vitello- 
genesis (mean diameter=230 p). 
Vitellogenesis for most fish 
occurred in the early summer. 
In May 1988, we observed 
vitellogenic oocytes in six of 
nine fish examined, ranging 
from 40 to 49 cm in length. All 
of these oocytes were in the 
early stages of development, 
prior to vacuolization, with 
mean diameters ranging from 
174 to 263 p. Smaller fish 
(length range 33-42 cm) con- 
tained previtellogenic oocytes 
only . In June (1987, 1988) vi- 
tellogenic oocytes, ranging in 
mean diameter from 178 p to 
269 p, were present in 23 of 24 
fish examined (length range 
36-52 cm). Vitellogenic oocytes 
in one fish of 52 cm were at an 
advanced stage of development 
(mean diameter=252 p), with 
yolk granules formed in the 
outer cortex. The relation be- 
tween mean diameter of vitel- 
logenic oocytes and fish length 
was not significant for the 
months of May ( 1988) and June 
(1987, 1988) (linear regression, P>0.1 for all three, 
n=6, 11, 12) 

By August the oocytes in some of the larger fish 
(45-50 cm) were nearing hydration. Mean diameters 
for vitellogenic oocytes from fish sampled in August 
(1987, 1988, 1990) ranged from 226 p to 429 p. 
There were significant, positive linear relationships 
between fish length and mean oocyte diameter for all 
of these samples (Table 2, Fig. 4). 

The size distributions for previtellogenic and 
vitellogenic oocytes did not differ significantly 
(Shapiro- Wilk test, P<0.05) from that of the normal 
distribution for any of the following cases. There was 
no significant difference in mean diameter of 
previtellogenic oocytes for the same months across 



NOTE Fargo and Tyler: Oocyte maturation in Pleuronectes vetulus 



193 



33 cm 



prevHellogenlc 




60 110 160 210 260 310 360 410 460 
Oocyte diameter (microns) 



42 cm 



prevHellogenlc 




60 110 160 210 260 310 360 410 460 
Oocyte diameter (microns) 



38 cm 




10 60 110 160 210 260 310 360 410 460 
Oocyte diameter (microns) 



46 cm 




| vltellogenlc 
prevHellogenlc 



10 60 110 160 210 260 310 360 410 460 
Oocyte diameter (microns) 



Figure 2 

Oocyte size compositions determined from ovary samples collected from Hecate Strait English sole 
{Pleuronectes vetulus) in August 1988. 



the two years (Table 3). However, there were signifi- 
cant differences in mean diameter for previtellogenic 
oocytes among months within both years (Table 4). 
No obvious trend in mean diameter over time was 
apparent for previtellogenic oocytes. There were sig- 
nificant differences in the rate of oocyte development 
between 1987 and 1988 (Table 3). The mean diam- 
eter of vitellogenic oocytes in June and August of 
1987 was significantly larger than for the same 
months in 1988, suggesting that vitellogenesis oc- 
curred earlier in 1987 than in 1988. There were also 
significant differences in the mean diameter of 
vitellogenic oocytes among months within years 
(Table 5). The mean diameter of vitellogenic oocytes 
increased significantly, coinciding with advancing 
oocyte development, between June-November in 
1987 and June-October in 1988. 

Spawning 

Ovaries obtained from spawning fish (October 1988, 
1990 and November 1987, 1990) were examined to 
investigate 1) size-dependent spawning and 2) the 



relation between fish length and egg diameter at the 
time of spawning. For the October 1988 sample, we 
observed the presence of vitellogenic oocytes only in 
fish smaller than 40 cm. The mean diameter of 
vitellogenic oocytes in these fish ranged from 287 to 
408 p. Fish ranging in length from 43 to 52 cm con- 
tained spent ovaries with previtellogenic oocytes 
only. Thus, we concluded that the larger fish had 
spawned prior to the time of the sample collection. 
In the October 1990 sample, taken two weeks ear- 
lier than the 1988 sample, some of the fish larger 
than 40 cm contained hydrated oocytes while oth- 
ers had spent ovaries with resorbing oocytes, sug- 
gesting that they were spawning in early October. 
Oocytes examined from samples collected in Novem- 
ber (1987, 1990) also indicated that larger fish had 
spawned previous to this time. Fish larger than 42 
cm contained only pre-vitellogenic oocytes and there 
was no sign of resorbing oocytes. Most smaller fish 
were in spawning condition during this month. 
Vitellogenic oocytes were present in fish ranging 
from 30 to 42 cm. Mean diameter ranged from 373 
to 483 p and these oocytes were hydrated and trans- 



194 



Fishery Bulletin 92(1). 1994 



January 




n=1001 



10 60 110 160 210 260 310 360 410 460 
Oocyte diameter (micron*) 



May 



previtellogenic 



vltellogenk; 




10 60 110 160 210 260 310 360 410 460 
Oocyte diameter (microns) 



June 

prevttellooenlc 



1/ n=676 

^ vttellogenlc 

Ik 

10 60 110 160 210 260 310 360 410 460 
Oocyte diameter (microns) 



600 
— 500 
J.400 
?300 

V 

I 200 

"- 100 





August 
prevttellooenlc 
1/ 



n= )564 




vltellogenlc 

/ 



10 60 110 160210260310360410460 
Oocyte diameter (microns) 



October 

(spawning) 




prevttellogenlc 



n=377 
vttellogenlc 

A 



10 60 110 160 210 260 310 360 410 460 
Oocyte diameter (microns) 



Figure 3 

Oocyte size composition determined from ovary samples collected from Hecate Strait English sole iPleuronectes 
vetulus) during January-October in 1988 (samples combined). 



lucent. We then combined all the 
data on mean egg diameter for 
spawning fish and there was no 
relationship between mean egg di- 
ameter at the time of spawning 
(hydrated and translucent) and 
fish length (linear regression, 
P>0.1, rc = 19). 

Discussion 

Oocyte development 

Dunn and Tyler ( 1969) and Dunn 
(1970) determined the length of 
time required for oocyte matura- 
tion in winter flounder iPleuronectes americanus). 
They observed two size modes of previtellogenic 
oocytes at any particular time. They documented the 
rate of increase in size for these modes for three 
consecutive years and concluded that the oocyte 
maturation period for this species was three years. 
We observed only a single mode for both 
previtellogenic and vitellogenic oocytes in fish 
sampled during all the months examined in our 
study. Johnson et al. ( 1991) reported similar results 
in their study of Puget Sound English sole. If oocytes 









Table 2 










Linear regression statistics for the relationship 


bet 


ween vitell 


ogenic 


oocyt 


e mean diameter and fis 


h length 


"or Engl 


sh 


sole (Pleuronectes 


vetul 


us) for the 


month of August 1987 


1988, and 1990. 






Degrees o 


f 












Year 


freedom 


F-statistic 


P 


Regression 


equation' 


r 


1987 


13 


10.72 


0.007 


Y = 


122 


+ 5.93X 


0.687 


1988 


20 


20.93 


- n iiiiiii 


Y = 


-93 


+ 9.44X 


0.910 


1990 


12 


44.01 


. I) 1)001 


Y = - 


237 


+ 12. 6X 


0.724 


' Y = 


oocyte mean 


diameter (a.). 












X = 


total length 


of fish (cm ) 













produced in year i were spawned in year i+1, we 
would expect to see two size classes of immature 
oocytes in year i+1, corresponding to those oocytes 
that were produced in year i (large immatures) to 
be spawned in year i+1 and those that were pro- 
duced in year i+1 (small immatures) to be spawned 
in year i+2. The fact that there were no significant 
differences in the mean diameter of previtellogenic 
oocytes for the same months in consecutive years 
(1987-88) suggests that the oocyte maturation pe- 
riod for Hecate Strait English sole is probably one year. 



NOTE Fargo and Tyler: Oocyte maturation in Pleuronectes vetulus 



195 



500 
450 
400 
350 
300 
250 
200 
150 
100 
50 




500 
450 

T 40 ° 
I 350 \ 

4 300 

| 250 

-I 200 

§ 100 
50 





30 



500 

450 

1" 400 

§ 350 

4 300 

I 250 

-1 200 

-£. 150 

<§ 100 

50 





30 



Aub-37 



° g ° 6 o o ° o; 



o provttolloflonlc 
• vltsllogenic 
— regression 



30 35 40 45 50 

Total length (cm) 



55 



Aug-88 




oggooe °86 oo 



35 



40 45 

Total length (cm) 



50 



55 



Aug-90 



• • 



OO OOq nOO 



35 



40 45 

Total length (cm) 



50 



55 



Figure 4 

Mean oocyte diameter vs fish length determined 
from ovary samples collected from Hecate Strait 
English sole {Pleuronectes vetulus) during the 
month of August, 1987. 1988, and 1990. 



We also found no trend in the mean size of 
previtellogenic oocytes among months within years, 
contrary to results reported by Dunn and Tyler 
(1969). One explanation for this is that the recruit- 
ment of small immature (previtellogenic) oocytes 
from the germinal epithelium is a continual process 
for Hecate Strait English sole. Alternatively, there 
may be a short time period, following spawning for 
example, during which previtellogenic oocytes recruit 
and quickly grow to a size of around 80 p. Additional 
work is needed to resolve these possibilities. 





Table 


3 






Results of two sample r-tests of mean diameters 
of previtellogenic and vitellogenic oocytes for 
English sole (Pleuronectes vetulus) determined 
from samples collected during the same month in 
1987 and 1988. 


Month and year 


n 


mean diameter 

(microns) P 


previtellogenic 










January 1987 
January 1988 


6,264 
1,001 




69.0 
69.4 


>0.1 


March 1987 
March 1988 


1,603 
1,737 




59.2 
59.8 


>0.1 


June 1987 
June 1988 


1,389 
1,132 




72.4 
72.9 


>0.1 


August 1987 
August 1988 


1,812 
2,071 




66.7 
65.8 


>0.1 


vitellogenic 










June 1988 
June 1988 


953 
1,029 




219.1 
203.3 


<0.0001 


August 1987 
August 1988 


1,774 
3,584 




362.1 
318.1 


<0.0001 



Spawning 

In general larger fish produced yolk earlier and 
spawned earlier than smaller fish. Most of the 
spawning fish were obtained from samples collected 
in October and November but there was also evi- 
dence of spring (March) spawning for smaller fish. 
Egg size at the time of spawning did not appear to 
be dependent on fish length. However, there is some 
evidence from this study to suggest a possible mini- 
mum size limit for eggs at the time of spawning. 
That is, the difference in the mean diameter of 
vitellogenic oocytes between smaller and larger fish 
decreased over time until there was no apparent 
difference at the time of spawning. Observations 
made during this study indicate that atresia was not 
as prevalent for Hecate Strait English sole as that 
reported for English sole in Puget Sound by Johnson 
et al. (1991). 

Marine fish species show wide variability in the 
reproductive process, which enables them to miti- 
gate the uncertain conditions in the marine environ- 
ment (Murphy, 1968; Roff, 1981). English sole dem- 
onstrate considerable phenotypic plasticity with 
regard to spawning. In Hecate Strait the spawning 
season extends from early fall through the follow- 



196 



Fishery Bulletin 92|1), 1994 



Table 4 






Results of two sample t-tests of the mean diameter ( 


|i ) of previtellogenic 


oocytes in English sole (Pleuronectes vetulus) among 


months for samples 


collected in 1987 and 1988. 






Year and Month January March June 


August 


November 


1987 






January P<0.0001 P<0.0001 P=0.0004 


P<0.0001 


(n=6264, 7=69. Out 






March P<0.0001 P<0.0001 


P<0.0001 


<n = 1603, 7=59. 2u) 






June P<0.0001 


P<0.0001 


<n = 1389, 7=72. 4u) 






August 


— 


P<0.0001 


(n = 1812, 7=66. 7u) 






November — 


— 


— 


(n=4205, 7=63. Ou I 






Year and Month January March May June 


August 


October 


1988 






January — P=0.0009 P<0.0001 P=0.0009 


P<0.0001 


P<0.0001 


(7i = 1001,7=69.4ul 






March P<0.0001 P<0.0001 


P<0.0001 


P<0.0001 


(7i = 1737, 7=59.8u) 






May P=0.003 


P<0.0001 


P<0.0001 


(ti = 1609, 7=76. 2u> 






June 


P<0.0001 


P<0.0001 


(/i = 1132, 7=72. 9u) 






August 


— 


P<0.0001 


(/i = 2071, 7=65. 8u) 






October 


— 


— 


(o = 1500, 7=56.9u) 







Table 5 






Results of two sample r-tests of the mean diameter (u) of vitellogenic oocytes in E 


riglish sole (Pleuronectes 


vetulus) among months for samples collected in 1987 and 1988. 






Year and month June August November 


Year and month May 


June August 


October 


1987 


1988 






June — <0.0001 <0.0001 


May 


>0.1 <0.0001 


<0.0001 


(n= 953, 7=219.1u) 


(n=191, .7=201. 4u I 








June 


— <0.0001 


<0.0001 


August <0.0001 


(/i = 1029. 7=203. 3u) 






(re=1774, 7=362. lu) 


August 

(7i=3584, 7=318. In) 


<0.0001 


<0.0001 


November — — — 


October 


— — 


— 


(n= 488, i=413.7m 


(71=710, 7=342. lu) 







ing spring. Johnson et al. (1991) reported a similar 
spawning period for Puget Sound English sole as did 
Kruse and Tyler ( 1989) in their study of English sole 
off the Oregon coast. This reproductive strategy may 
increase the probability of encountering favorable 
conditions for larval survival by spreading the re- 
productive effort over the longest possible time span. 



Based on our results it is unlikely that cohort-spe- 
cific spawning occurs as in Pacific herring, Clupea 
pallasi (Ware and Tanasichuk, 1989), and Norwe- 
gian Atlantic herring, Clupea harengus (Lambert, 
1990). However, in view of the relation between 
oocyte maturation and fish length and the duration 
of the spawning period, it is possible that first time 



NOTE Fargo and Tyler: Oocyte maturation in Pleuronectes vetulus 



197 



spawners spawn at a different time than the rest of 
the stock. We can suggest no mechanism to account 
for this and more data are required to corroborate 
these results. 

There is also evidence of interannual variability 
in oocyte maturation and this process appears to be 
size-related. Smaller fish matured later and 
spawned later than larger fish. Our results indicate 
that the time of peak spawning and the duration of 
the spawning season are variable from year to year. 
The results from this study provide baseline infor- 
mation for an investigation of the recruitment biol- 
ogy of this stock. 

Acknowledgments 

We wish to acknowledge John Bagshaw, Serge 
Villeneuve, Tammy Laberge, Christina Horvath, 
Tracy Sexton, and Corinne Kikegawa for their aid 
in preparing the slides for histological examinations 
and photography of specimens. Ron Tanasichuk and 
Doug Hay reviewed the manuscript and provided 
advice regarding the spawning characteristics for 
the species. The scientific editor and three anony- 
mous reviewers provided a number of suggestions 
which improved the paper. 

Literature cited 

Dunn, R. S. 

1970. Further evidence for a three year oocyte 
maturation time in the winter flounder (Pseu- 
dopleuronectes americanus). J. Fish. Res. Board 
Canada. 27:957-960 

Dunn, R. S., and A. V. Tyler. 

1969. Aspects of the anatomy of the winter floun- 
der (Pseudopleuronectes americanus) with hypoth- 
eses on oocyte maturation time. J. Fish. Res. 
Board Canada 26:1943-1947. 

Fargo, J. 

1993. Flatfish. In B. M. Leaman and M. Stocker 
(ed.), Groundfish stock assessments for the west 
coast of Canada in 1992 and recommended yield 
options for 1993. Can. Tech. Rep. Fish. Aquat. 
Sci. 1919:95-131. 



Fargo, J, R. P. Foucher, S. C. Schields, and 
D. Ross. 

1984. English sole tagging in Hecate Strait, R/V 
G.B. REED, June 6-24, 1983. Can. Data Rep. 
Fish. Aquat. Sci. 427, 49 p. 
Foucher, R. P., and R. J. Beamish. 

1980. Production of nonviable oocytes by Pacific 
hake (Merluccius productus). Can. J. Fish. Aquat. 
Sci. 37:41-47. 

Hart, J. L. 

1973. Pacific fishes of Canada. Fish. Res. Board 
Can. Bull. 180, 740 p. 
Johnson, L. L, E. Casillas, M. S. Myers, 
L. D. Rhodes and O. P. Olson. 

1991. Patterns of oocyte development and related 
changes in plasma 17-B estradiol, vitellogenin and 
plasma chemistry in English sole Parophrys 
vetulus Girard. J. Exp. Mar. Biol. Ecol. 152: 
161-185. 
Ketchen, K. S. 

1956. Factors influencing the survival of the lemon 
sole (Parophrys vetulus) in Hecate Strait, British 
Columbia. J. Fish. Res. Board Canada, 13(5): 
647-694. 
Kruse, G. H., and A. V. Tyler. 

1989. Exploratory simulation of English Sole 
(Parophrys vetulus) recruitment mechanisms. 
Trans. Am. Fish. Soc. 118:101-118. 

Lambert, T. C. 

1990. The effect of population structure on recruit- 
ment in herring. J. Cons. int. Explor. Mer 
47:249-255. 

Murphy, G. I. 

1968. Pattern in life history and the 
environment. Am. Nat. 102:391-403. 
Roff, D. A. 

1981. Reproductive uncertainty and the evolution 
of iteroparity: why don't flatfish put all their eggs 
in one basket? Can. J. Fish. Aquat. Sci. 38:968- 
977. 

Ware, D. M., and R. Tanasichuk. 

1989. Biological basis of maturation and spawning 
waves in Pacific herring (Clupea harengus 
pallasi). Can. J. Fish. Aquat. Sci. 46(101:1776- 
1784. 
Yasutake, W. T., and J. H. Wales. 

1983. Microscopic anatomy of salmonids: an 
atlas. Fish. Wild. Ser. U.S. Dep. Int. Res. Pub. 
150, 189 p. 



Estimation of weight-length 
relationships from group 
measurements 



William H. Lenarz 

Tiburon Fisheries Laboratory 

National Marine Fisheries Service, NOAA 

3 1 50 Paradise Drive. Tiburon, CA 94920 



Catch sampling provides data 
that are basic to fisheries re- 
search and is often an important 
component of research budgets. 
Samplers typically select fish ran- 
domly, measure length, remove 
ageing structures, and determine 
sex for each individual. In many 
schemes for sampling commercial 
(e.g., Sen, 1986; Tomlinson, 1971) 
and survey catches (e.g., Gun- 
derson and Sample, 1980), sample 
weight is needed to expand the 
sample results to the total catch. 
Individual weights are usually 
not needed to satisfy the main 
objectives. Often only the aggre- 
gate weight of the sample is taken 
to save time, and if at sea, to 
avoid difficult logistics. While 
sampling costs are easily justified 
by program objectives, scientists 
frequently use the data for addi- 
tional research. 

Investigators often use weight- 
length relations to study possible 
correlations between condition of 
fish and environmental factors or 
population density (e.g., Pat- 
terson, 1992). A literature search 
revealed only two previous devel- 
opments of methods of estimating 
weight-length relations from 
samples of individual lengths and 
aggregate weights (WLRAW). 
Cammen (1980) used a general 
nonlinear regression program 
from the BMDP package (Dixon, 
1983) as a WLRAW method. He 
tested the method with simulated 
data and compared the results of 
regression using unweighted ob- 
servations to using observations 
weighted by the inverse of sample 



weights, and with various esti- 
mates made when individual 
weights were known. Since the 
data were simulated, assuming a 
multiplicative error term, it would 
have been more appropriate to 
use the inverse of sample weight 
squared for weighting. The non- 
linear method produced good fits 
to the simulated data, and 
weighted parameter estimates 
were closer to the true values 
than unweighted estimates. 
Damm ( 1987) developed two non- 
linear WLRAW methods. One 
method is a biased approxima- 
tion, and his report indicated that 
the other method did not always 
produce estimates of the param- 
eters. 

In this note I describe a new 
WLRAW method, compare it with 
Cammen's method, explore error 
term characteristics, and describe 
bootstrap estimates of confidence 
limits of estimates. The methods 
of Damm (1987) were not studied 
because his biased approximation 
method requires as much calcula- 
tion as my new method and his other 
method does not always work. 

Methods 

The relation between expected 
weight and length of an indi- 
vidual fish is usually assumed to 
be the power equation, 



E(W l ) = alf l 

Where V^ = weight of fish i, 
a - parameter. 



(1) 



L, = length of fish i, 

p = parameter. 
For the new WLRAW method I 
modeled the weight-length rela- 
tionship as 



W, 



flK) 



+ £, 



(2) 



J i=i 



where W = 



L. = 



e. = 



T = 



average weight of 
fish in sample j, 
number of fish in 
sample j, 
length of fish i in 
sample j, 
error term for 
sample j, 
1,  • • , T, 
number of 
samples. 



I assumed that error was additive 
because under field conditions 
much of the error was due to lim- 
its to the accuracy in measure- 
ment of sample weights. Because 
the dependent variable in Equa- 
tion 2 was a sample average, its 
variance should contain a compo- 
nent which is proportional to the 
inverse of n . Thus in the new es- 
timation procedure, I weight each 
observation by n to stabilize the 
variance. I made the assumption 
that, after weighting by sample 
size, error was random and inde- 
pendent of,/. 

The new method treated esti- 
mation of parameters of (Eq. 2) as 
a separable least-squares problem 
(Seber and Wild, 1989). For a trial 
value of (3 (P'l, y was calculated 
for each sample, 



/,=<2X>/», 



(3) 



With the new notation, Equation 
2 becomes 



W- = a y ; + e 



j~ 



(4) 



Manuscript accepted 16 August 1993 
Fishery Bulletin 92:198-202 (1994) 



198 



NOTE Lenarz: Estimation of weight-length relations from group measurements 



199 



I then obtained an estimate of a (a') corresponding 
to p" by using the standard least squares linear re- 
gression with zero intercept method. I used a non- 
linear least squares procedure to obtain the estimate 
of (3 ( B )■ This procedure was analogous to finding 
the transformation, Lf, that minimized the sum of 
squares about the linear regression (Eq. 4). Using 
this procedure, I estimated brackets for ensuring 
that the searching range included P with the proce- 
dure MNBRAK (Press et al., 1989). Then I used the 
iterative procedure BRENT (Press et al., 1989) to 
obtain the final estimate. BRENT uses parabolic 
interpolation to minimize the sum of squares as a 
function of (3'. Convergence is assumed when the 
procedure does not change the value of P' more than 
a tolerance specified by the user. As previously 
stated, observations were weighted by n to stabilize 
the variance. I implemented the WLRAW method in 
double precision using Sun FORTRAN for a Sun 
SPARC2 work station. 

Bootstrap approximations of confidence intervals 
about the line were calculated for the new method. 
The literature contains a variety of bootstrap meth- 
ods proposed to approximate confidence intervals 
(e.g., DiCiccio et al., 1992). I used the nonparamet- 
eric BC method of Efron (1987) because it often 

a 

produces good results and is relatively easy to use. 
BC a stands for accelerated bias corrected boot- 
strap confidence intervals. Efron (1987) showed that, 
in the parametric case, the method is approximately 
correct if a transformation to a normally distributed 
variable exists. The transformation does not need to 
be known and the variance does not need to be con- 
stant. While the correctness of the BC has not been 

a 

mathematically proven for nonparametric cases, such 
as the WLRAW, Efron (1987) stated, "...empirical re- 
sults look promising." The BC a confidence limits of an 
estimate of parameter 8, 0, are 



IBS(N(z[a]))<6<IBS(Nlz[l-a])) 



(5) 



IBS(P) is the value of 6 that corresponds to the per- 
centile P of the cumulative bootstrap frequency dis- 
tribution. N(Z) is the percentile of the cumulative 
normal probability distribution that corresponds to 
the standard deviate Z. z[a] is given by Efron 
(1987) as 



z[a] = z n + 



Zn+Z 



l-a(z 0+ z"») 



(6) 



z ,al is the standard deviate that corresponds to the 
a percentile of the normal cumulative distribution. 



2 is the standard deviate of the normal cumulative 
distribution that corresponds to the percentile that 
corresponds to in the cumulative bootstrap fre- 
quency distribution. Efron (1987) called z Q the bias 
constant. Efron called a the acceleration constant. It 
is related to the skewness of the bootstrap frequency 
distribution. Efron gave the following approximation 
for a: 



a ~ 



<2>J 



;=i 



(7) 



where U , 



3(A) 






ef ] -e 

A 
estimate of 6 whenyth sample has 
a very small amount of extra 
weighting (A). 



If a and z are zero, then Equation 7 becomes the 
percentile method that is the most frequently used 
bootstrap method in the fisheries literature (e.g., 
Sigler and Fujioka, 1988). 

I chose to approximate 90% confidence bands 
rather than 95% or 99% bands because 90% non- 
parametric bootstrap intervals tend to perform bet- 
ter than intervals that cover a wider portion of the 
distribution (Efron, 1988). Following the advice of 
Efron, I used 1,000 bootstrap replicates. 

Cammen (1980) used the general nonlinear re- 
gression program of BMDP to estimate the param- 
eters of Equation 2, except that he assumed that the 
error term is multiplicative and used total sample 
weight instead of average weight as the dependent 
variable. The BMDP program uses the Gauss-New- 
ton algorithm. I used the same algorithm in the 
nonlinear regression program of the SAS package 
(SAS Institute Inc., 1989) on a Sun SPARC2 to com- 
pare parameter estimates and execution times with 
the new method. Since the correct error model is not 
known, I also estimated the parameters using 
no _weighting__and weight set to 1/W ,1/W, 2 , 
n l IW r and n ] I W", and compared asymptotic stan- 
dard errors of the parameter estimates. The new es- 
timation procedure is simpler than the Gauss-New- 
ton approach because it searches for the least 
squares by iteratively changing the value of one 
parameter instead of two. 

I used data collected on chilipepper rockfish 
{Sebastes goodei) by a cooperative landing sampling 
program of the California Department of Fish and 



200 



Fishery Bulletin 92|1). 1994 



Game and National Marine Fisheries Service to 
examine utility of the WLRAW method. Samplers 
collected two groups of fish from each sampled land- 
ing. For each group a container that holds 22.7 kg 
of fish was filled with fish regardless of species. 
Then the sampler obtained total group weights to 
the nearest lb (0.45 kg) for each species and the total 
length of each fish was measured to the nearest mm. 
I converted weights to kg. I changed lengths to deci- 
meters to minimize potential scaling problems in the 
computations. Before using the WLRAW method, I 
combined groups within a landing because they may 
not be independent. 

I first used data for all months during 1991 from 
all ports between Morro Bay and Crescent City, 
California, to develop, test, and time the software. 
Results of the test runs are described briefly in the 
Results and Discussion section. More detailed re- 
sults are presented for a more typical application of 
the method. Investigators are more likely interested 
in results from a smaller number of samples taken 
from more restrictive scales of time and area than 
from data sets like the one used in the preceding 
example. I used data for chilipepper rockfish taken 
during July and August 1991 from Morro Bay to 
illustrate use of the method. 

Results and discussion 

The data from all ports consisted of measurements 
from 7,687 fish taken in 186 samples. The procedure 
required 1.6 seconds, compared with 18.8 seconds for 
the Gauss-Newton method. The Gauss-Newton and 
new methods produced parameter estimates that 
were identical to six decimal places. Predicted 
weights were very close to the results of Phillips 
(1964), who used data from individually measured 
fish. Sums of squares plotted against P' indicated 
that there were no local minima. Residuals were not 
related to weight, indicating that the additive error 
assumption is correct. Sometimes transformation of 
(3' to ln(P') when estimating parameters of power 
equations avoids problems due to curvature (Rat- 
kowsky, 1983). Transformation was tried and pa- 
rameter estimates were identical to the results when 
P' was not transformed. When P' was transformed, 
the procedure required more time to complete, so the 
transformation was not used. 

Data were available for 583 fish taken from 13 
samples taken in Morro Bay, during July and Au- 
gust 1991. There were no strong trends between the 
residual and expected weight (Fig. 1). There was a 
tendency for absolute values of residuals to be nega- 
tively correlated with the number offish in a sample 
(Fig. 2A). The tendency was reduced when residu- 



004 










D 




0.02 














Residual (kg) 

8 o 






B o 






D 






D 
D 
D D 




n 




-0.04 














-0.06 








D 







04 0.5 06 07 0.8 0.9 1 

Expected Weight (kg) 

Figure 1 

Residual of average weight (kg) as a function of 
expected weight (kg) for chilipepper rockfish 
(Sebastes goodei) collected in samples taken from 
Morro Bay during July and August 1991. 



als were multiplied by sn , as expected under the 
assumption that variance is proportional to the in- 
verse of sample size (Fig. 2B). Also, n produced the 
lowest asymptotic standard errors of the parameter 
estimates of the six weighting factors explored 
(Table 1). The results shown in Table 1 and Figures 
1 and 2 indicated that the additive error model with 
weighting by n was appropriate for these data. 
Bootstrap estimates of standard error using the new 
method were higher than asymptotic estimates us- 
ing the Gauss-Newton method. The bootstrap and 
asymptotic normal confidence intervals were narrow 
and similar within the range of most observed av- 
erage weights but diverged when expected weight 
was greater than 0.75 kg even though individual 
fish of larger size occurred in many of the samples 
(Table 2). The bootstrap confidence intervals were 
skewed at the larger sizes. However, the bootstrap 
estimates of absolute bias were less than 0.01 kg 
except they were -0.01 kg for 450-mm fish and -0.02 
kg for 500-mm fish. All estimates of the absolute 
value of a were about 0.015, which indicated that a 
could have been ignored for this set of data. 

The new WLRAW method performed well. Good 
fits to the data were obtained and the residuals 
agreed with the assumptions. Approximate confi- 
dence limits indicated that precise estimates of ex- 
pected weight are obtained with a small number of 
samples under field conditions for sizes of fish 
within the range of most observed average weights. 
The method is fast when used on a work station or 
on a modern personal computer. The new method is 
10 times faster than using the Gauss-Newton ap- 



NOTE Lenarz: Estimation of weight-length relations from group measurements 



201 



0.04 




A 


D 










0.02 



•0.02 






a 




D 


a 


D 






n 


o 


O 
D 




a 


■0 04 
















■0.08 
-0.08 






D 

1 


1 




i 


 



40 60 

Sample Size 



0.2 


B 






a 










fo, 

CO 

* o 








o 




n 


L> 


D 


to 

D 

■o 

i-o.t 

ir 






o 




D 


o 

D 




O 


-0.2 


















-0.3 




D 


_l 




1 






- 1 



40 60 

Sample Size 



Figure 2 

(A) Residual of average weight (kg) as a function of 
sample size for chilipepper rockfish (Sebastes 
goodei ) collected in samples taken from Morro Bay 
during July and August 1991. (B) Residual multi- 
plied by yrij as a function of sample size. 



proach with a standard statistical package. Some of 
the difference is probably due to the overhead in- 
volved with using the statistical package. When 
computationally intensive methods such as 
bootstrapping are used, time saved by using the new 
method is significant. 

The widening confidence limits for expected 
weights beyond the range of most observed average 
weights indicated use of expected weights beyond 
the observed range is extrapolation and should not 
be done. This also applies to comparison of param- 
eter estimates from different sets of data. If the 
range of observed average weights differ much 
among the data sets, comparison of parameter esti- 
mates is not meaningful. Estimates of the two pa- 



Table 1 

Estimates of standard errors of parameter esti- 
mates of weight-length model for chilipepper rock- 
fish iSebasted goodei) collected from Morro Bay 
during July and August 1991. The Gauss-New- 
ton method was used with observations weighted 
by six factors to estimate the parameters, and the 
new method with rij as the weighting factor. As- 
ymptotic standard errors are shown for the Gauss- 
Newton method and bootstrap standard errors for 
the new method. Coefficients of variation of the pa- 
rameter estimates are shown in parentheses. 



Standard error 



Weighting 
factor 



Gauss-Newton method 

none 0.0028 (0.30) 

n, _ 0.0019 (0.21) 

raj/Wj 0.0020 (0.20) 

n/W, 2 0.0022 (0.20) 

1/W, 0.00.30 (0.29) 



1/W, : 



New method 



0.0032 (0.28) 



0.0046 (0.50) 



0.2159 (0.07) 
0.1489 (0.05) 
0.1528 (0.05) 
0.1547 (0.05) 
0.2129 (0.07) 
0.2069 (0.07) 



0.2211 (0.07) 







Table 2 






Expecte 


d weigh 


ts for 


chilipepper roc 


kfish 


iSebastes 


goodei ) 


collected from 


Morro Bay dur- 


ing July 


and August 1991, and 


909t confidence 


about th 


3 line. C 


onfidence limits were approxi- 


mated us 


\>iv, 1 he 


bootstrap BC 


(bootstrap 


) and 


the asymptotic normal 


method 


3 ( normal ) 


. Ex- 


pected weights were ca 


culatec 


from the 


esti- 


mated weight- 


ength 


relation (0.0091819 


Length 3 L 


758673 , 
















Confidence limits 




Normal 


Bootstrap 


Total 


Expected 


















length 


weight 


Lower 


Uppei 


Lower 


Jpper 


(dm) 


(kg) 


(kg) 


(kg) 


(kg) 


(kg) 


3.00 


0.30 


0.28 


0.32 


0.28 


0.33 


3.50 


0.49 


0.47 


0.51 


0.47 


0.50 


3.75 


0.61 


0.60 


0.62 


0.60 


0.62 


4.00 


0.75 


0.74 


0.76 


0.73 


0.76 


4.50 


1.09 


1.04 


1.14 


0.99 


1.12 


5.00 


1.52 


1.42 


1.63 


131 


1.61 



rameters of the weight-length relation are highly 
correlated even when individuals are weighed and 
standard linear regression is used (Lenarz, 1974). 
Thus, regardless of the type of data or statistical 



202 



Fishery Bulletin 92(1). 1994 



procedure, I recommend comparison of weight- 
length relations among data sets by comparison of 
expected weights of fish at sizes within the range 
of observed average weights common to all data sets 
of interest. 

The results of this study suggest that an additive 
error term is more appropriate than a multiplica- 
tive error term for modeling weight-length relations. 
Most previous studies have assumed multiplicative 
error, which is implied when the log-log transforma- 
tion is used to estimate parameters of the model 
from individually measured fish by linear regres- 
sion. The multiplicative error assumption has not 
been demonstrated correct even when data are 
available from fish weighed individually. While good 
fits to data are usually obtained under the multi- 
plicative assumption, if the assumption is not valid, 
statistical inferences may be erroneous. Pienaar and 
Thomson (1969) assumed that the error term was 
additive for their data and discussed statistical as- 
pects of the assumption. Further examination of the 
error term form would be interesting. 

Copies of the FORTRAN code used in this study 
are available from the author. 



Acknowledgments 

I thank James Bence for considerable statistical 
advice, particularly on the bootstrap procedure. 
James Bence, Alec MacCall, and Steve Ralston con- 
structively reviewed drafts of the note. I also thank 
David Woodbury for his assistance during an early 
stage of this study and Dale Roberts for his help 
with the use of SAS. 



Literature cited 

Cammen, L. M. 

1980. Estimation of biological power functions from 
group measurements. Can. J. Fish. Aquat. Sci. 
37:716-719. 
Damm, U. 

1987. The estimation of weight at length from the 
total weight and the length distribution of a 
sample. ICES CM 1987/D:16, 9 p. 
DiCiccio, T. J., M. A. Martin, and G. A. Young. 

1992. Fast and accurate approximate double boot- 
strap confidence intervals. Biometrika 79(2): 
285-95. 



Dixon, W. J. 

1983. BMDP statistical software. Univ. California 
Press, Berkeley, 733 p. 
Efron, B. 

1987. Better bootstrap confidence intervals. J. 
Am. Statist. Assoc. 82(3971:171-185. 

1988. Bootstrap confidence intervals: good or 
bad? Psychol. Bull. 104(2):293-6. 

Gunderson, D. R., and T. M. Sample. 

1980. Distribution and abundance of rockfish off 
Washington, Oregon, and California during 
1977. Mar. Fish. Rev. 42 (3-41:2-16. 
Lenarz, W. H. 

1974. Length-weight relations for five eastern 
tropical Atlantic scombrids. Fish. Bull. 72:848- 
851. 
Patterson, K. R. 

1992. An improved method for studying the condi- 
tion offish, with an example using Pacific sardine 
Sardinops sagax (Jenyns). J. Fish Biol. 40: 
821-831. 
Phillips, J. B. 

1964. Life history studies on ten species of rockfish 
(genus Sebastodes). Calif. Dep. Fish Game Fish 
Bull. 126, 70 p. 
Pienarr, L. V., and J. A. Thomson. 

1969. Allometric weight-length regression 
model. J. Fish. Res. Board Canada 26:123-131. 
Press, W. H., B. P. Flannery, S. A. Teukolsky and 
W. T. Vetterling. 

1989. Numerical recipes the art of scientific com- 
puting (FORTRAN version). Cambridge Univ. 
Press, Cambridge, 702 p. 
Ratkowsky, D. A. 

1983. Nonlinear regression modeling. Marcel 
Dekker, NY, 276 p. 
SAS Institute Inc. 

1989. SAS/STAT® User's guide, version 6, 4th edi- 
tion, Vol. 2. SAS Institute Inc., Cary, NC, 846 p. 
Seber, G. A., and C. J. Wild. 

1989. Nonlinear regression. J. Wiley & Sons, NY, 
768 p. 
Sen, A. R. 

1986. Methodological problems in sampling com- 
mercial rockfish landings. Fish. Bull. 84:409- 
421. 
Sigler, M. F., and J. T. Fujioka. 

1988. Evaluation of variability in sablefish, 
Anoplopoma fimbria, abundance indices in the 
Gulf of Alaska using the bootstrap method. Fish. 
Bull. 86:445-452. 
Tomlinson, P. K. 

1971. Some sampling problems in fishery work. 
Biometrics 27:631-41. 



Spiny lobster recruitment and sea 
level: results of a 1 990 forecast 



Jeffrey J. Polovina 

Honolulu Laboratory, Southwest Fisheries Science Center 

National Marine Fisheries Service, NOAA 

2570 Dole Street, Honolulu, Hawaii 96822-2396 

Joint Institute for Marine and Atmospheric Research (JIMAR) 
University of Hawaii, Honolulu. Hawaii 96822 

Department of Oceanography, School of Ocean and 

Earth Science and Technology 
University of Hawaii, Honolulu, Hawaii 96822 

Gary T. Mitchum 

Joint Institute for Marine and Atmospheric Research LIIMAR) 
University of Hawaii, Honolulu, Hawaii 96822 

Department of Oceanography, School of Ocean and 

Earth Science and Technology 
University of Hawaii, Honolulu. Hawaii 96822 



A relation between recruitment to 
the fishery and sea level for the 
spiny lobster Panulirus mar- 
ginatus, in the Northwestern Ha- 
waiian Islands, was supported by 
data from 1985 through 1990 
(Polovina and Mitchum, 1992). A 
forecast of future recruitment was 
made based on projected sea lev- 
els (Polovina and Mitchum, 1992). 
This note updates that forecast 
with two more years of data. 

Fishery data from 1985 to 1990 
indicated considerable inter- 
annual variation in recruitment 
strength of spiny lobster, Pan- 
ulirus marginatus, between the 
two principal fishing grounds 
(Necker Island and Maro Reef), 
although separated by about 700 
km (Fig. 1; Polovina and 
Mitchum, 1992). Recruitment 
strength variation between the 
two fishing areas was measured 
as the ratio of the commercial 
landings from Maro Reef divided 
by the combined commercial land- 
ings from Necker Island and Maro 
Reef. A strong correlation was ob- 



served between this measure of 
recruitment strength at Maro 
Reef and the sea level gradient 
along the Northwestern Hawaiian 
Islands, advanced by four years 
(Polovina and Mitchum, 1992). 
The sea level gradient was mea- 
sured as the difference in sea 
level between tide gauges at 
French Frigate Shoals, southeast 
of Maro Reef, and Midway Island, 
northwest of Maro Reef. A high 
proportion of the commercial 
landings came from Maro Reef 
following a steep gradient, while 
relatively few spiny lobsters were 
caught at Maro Reef following a 
flat gradient. The four-year lag is 
based on the minimum legal har- 
vest size which, for the spiny lob- 
ster is about three years old, af- 
ter benthic settlement. Prior to 
benthic settlement, the larvae are 
planktonic for about one year. 

Since sea level gradient appears 
to lead recruitment to the fishery 
by four years, the relation can 
provide up to a four-year forecast. 
Based on data through 1990, it 



was forecast that in 1991 recruit- 
ment to the fishery at Maro Reef 
would be weak but would recover 
in 1992 relative to recruitment at 
Necker Island (Fig. 2). The 1991 
and 1992 fishery data show this 
forecast correct (Fig. 2), although 
the fishery for the entire North- 
western Hawaiian Islands was 
relatively weak in 1992. Thus, 
while sea level gradient index 
does forecast the relative strength 
of recruitment at Maro Reef, it is 
not, by itself, an index of absolute 
recruitment strength. 

It has been argued that sea 
level gradient measures the 
strength of the Subtropical 
Counter Current, which appears 
to intersect the Hawaiian ridge as 
three narrow eastward flowing 
bands at 20, 24, and 26 degrees 
north latitude (Polovina and 
Mitchum, 1992; White and 
Walker, 1985). Recent studies of P. 
marginatus larval distribution 
find a relatively high abundance 
of late stage larvae consistently 
present near lat. 26°N, and tracks 
from Argos drifter buoys drogued 
at 30 m indicate buoy entrap- 
ment along lat. 26'N. 1 These re- 
sults provide some additional sup- 
port to our original hypothesis 
that a positive relationship exists 
between the strength of the Sub- 
tropical Counter Current and lo- 
cal larval survival, retention, and 
recruitment to the fishery at Maro 
Reef (Polovina and Mitchum, 
1992). 

Literature cited 

Polovina, J. J., and G. T. 
Mitchum. 

1992. Variability in spiny lob- 
ster Panulirus marginatus re- 



1 Polovina, J.J.. and R.B. Moffitt. In re- 
view. The spatial and temporal distribu- 
tion of the larvae of the spiny lobster 
{Panulirus marginatus) in the North- 
western Hawaiian Islands. 

Manuscript accepted 11 August 1993 
Fishery Bulletin 92:203-205 (1994) 



203 



204 



Fishery Bulletin 92(1), 1994 




Figure 1 

The Hawaiian Archipelago. 



o 

3 



a 

3 



.s 

<S1 



0.9- 



0.8- 




o catch ratio 
• sea level 



  



120 
90 

60 

30 



•30 



■60 S 



-90 * 



120 to 
150 



180 



1234123412341234123412341234123412341234123412341234 

1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 

Year 

Figure 2 

Three-quarter moving average of the ratio of quarterly landings of spiny lobster, 
Panulirus marginatus, at Maro Reef to quarterly landings at Maro Reef and Necker 
Island (bold line), 1984-92. Solid dots are values of the catch ratio since the 1990 
forecast. Overlayed is the 3-quarter moving average of French Frigate Shoals (FFS)- 
Midway sea level deviation advanced by four years (dashed line), 1980-92. 



NOTE Polovina and Mitchum: Panulirus marginatus recruitment and sea level 205 



cruitment and sea level in the Northwestern Ha- 
waiian Islands. Fish. Bull. 90:483^193. 
White, W. B., and A. E. Walker. 

1985. The influence of the Hawaiian Archipelago 
upon the wind-driven subtropical gyre in the West- 
ern North Pacific. J. Geophys. Res. 90 C4:7061- 
7074. 



us. Department Recent publications in the 

of Commerce r 

Seattle Washington NOAA Technical Report NMFS Series 



1 13 Maturation of nineteen species of finfish off 
the northeast coast of the United States, 
1985-1990 

Loretta O'Brien. Jay Burnett, and Ralph K. Mayo, June 1993, 
66 p. 



1 14 Structure and historical changes in the 

groundfish complex of the eastern Bering Sea 

Richard G Bakkala, July 1993, 91 p. 



1 1 5 Conservation biology of elasmobranchs 

Steven Branstetter (editor), SeptemPer 1993, 99 p 



1 1 6 Description of early larvae of four northern 

California species of rockfishes (Scorpaenidae: 
Sebastes ) from rearing studies 

Guillermo Moreno, NovemPer 1993, 18 p. 



Some NOAA publications are available b> 
purchase from the Superintendent of 
Documents. U.S. Government Printing 
Office, Washington, DC 20402. 



206 



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U.S. Department 
of Commerce 

Volume 92 
Number 2 
April 1994 




Fishery 
Bulletin 






AP^ ^94 



Woods Hole. M/> 




U.S. Department 
of Commerce 

Ronald H. Brown 
Secretary 

National Oceanic 
and Atmospheric 
Administration 

D. James Baker 
Under Secretary for 
Oceans and Atmosphere 

National Marine 
Fisheries Service 

Rolland A. Schmitten 
Assistant Administrator 
for Fisheries 



=/ 


l 


D 


![ 




Scientific Editor 

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Northwest Fisheries Science Center 
National Marine Fisheries Service, NOAA 
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appeared as a numbered bulletin. A new system began in 1963 with volume 63 in 
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agencies, and in exchange for other scientific publications. 



U.S. Department 
of Commerce 

Seattle, Washington 

Volume 92 
Number 2 
April 1994 



Fishery 
Bulletin 



Contents 



iii Errata 



207 



223 



236 



254 



262 



275 



292 



APR 2 8 1994 



Woods Hole, MA 02543 



Blood, Deborah M., Ann C. Matarese, and 
Mary M. Yoklavich 

Embryonic development of walleye pollock, Theragra 
chalcogramma, from Shelikof Strait, Gulf of Alaksa 

Brodeur, Richard D., and William C. Rugen 

Diel vertical distribution of ichthyoplankton in the northern 
Gulf of Alaska 

Clark, Malcolm R., and Dianne M. Tracey 

Changes in a population of orange roughy, Hoplostethus 
atlanticus, with commercial exploitation on the 
Challenger Plateau, New Zealand 

Daniel, Louis B., Ill, and John E. Graves 

Morphometry and genetic identification of eggs of 
spring-spawning sciaenids in lower Chesapeake Bay 

Ditty, James G., Richard F. Shaw, and 
Joseph S. Cope 

A re-description of Atlantic spadefish larvae, Chaetodipterus 
faber (family: Ephippidae), and their distribution, abundance, 
and seasonal occurrence in the northern Gulf of Mexico 

Ditty, James G., Richard F. Shaw, 
Churchill B. Grimes, and Joseph S. Cope 

Larval development, distribution, and abundance of common 
dolphin, Coryphaena hippurus, and pompano dolphin, 
C. equiselis (family: Coryphaenidae), in the northern 
Gulf of Mexico 

Kastelle, Craig R., Daniel K. Kimura, 
Ahmad E. Nevissi, and Donald R. Gunderson 

Using Pb-2 1 0/Ra-226 diseguilibria for sablefish, 
Anoplopoma fimbria, age validation 



Fishery Bulletin 92(2). 1994 



302 Moltschaniwskyj, Natalie A., and Peter J. Doherty 

Distribution and abundance of two juvenile tropical Photololigo 
species (Cephalopoda: Loliginidae) in the central Great Barrier 
Reef Lagoon 

313 Murie, Debra J., Daryl C. Parkyn, Bruce G. Clapp, and Geoffrey G. Krause 

Observations on the distribution and activities of rockfish, Sebastes spp., in Saanich Inlet, 
British Columbia, from the Pisces IV submersible 

324 Perrin, William F, Gary D. Schnell, Daniel J. Hough, James W. Gilpatrick Jr., 
and Jerry V. Kashiwada 

Reexamination of geographic variation in cranial morphology of the pantropical spotted dolphin, 
Stenella attenuata, in the eastern Pacific 

347 Powell, Eric N., John M. Klinck, Eileen E. Hofmann, and Sammy M. Ray 

Modeling oyster populations. IV: Rates of mortality, population crashes, and management 

374 Prager, Michael H. 

A suite of extensions to a nonequilibrium surplus-production model 

390 Stoner, Allan W., and Megan Davis 

Experimental outplanting of juvenile queen conch, Strombus gigas. comparison of wild and 
hatchery-reared stocks 

412 Taylor, David M., Paul G. O'Keefe, and Charles Fitzpatrick 

A snow crab, Chionoecetes opilio (Decapoda, Majidae), fishery collapse in Newfoundland 

420 Warlen, Stanley M. 

Spawning time and recruitment dynamics of larval Atlantic menhaden, Brevoortia tyrannus, into a 
North Carolina estuary 

434 Reilly, Stephen B., and Paul C. Fiedler 

Interannual variability of dolphin habitats in the eastern uupical Pacific. I: Research vessel surveys, 
1986-1990 

451 Fiedler, Paul C, and Stephen B. Reilly 

Interannual variability of dolphin habitats in the eastern tropical Pacific. II: Effects on abundances 
estimated from tuna vessel sightings, 1 975-1 990 



Notes 

464 Aurioles-Gamboa, David, Maria Isabel Castro-Gonzalez, and 
Ricardo Perez-Flores 

Annual mass strandings of pelagic red crabs, Pleuroncodes planipes (Crustacea: Anomura 
Galatheidae), in Bahia Magdalena, Baja California Sur, Mexico 

471 Ennevor, Bridget C. 

Mass marking coho salmon, Oncorhynchus kisutch, fry with lanthanum and cerium 

474 Hazin, Fabio H. V, Clara E. Boeckman, Elizabeth C. Leal, Rosangela R T. Lessa, 
Kohei Kihara, and Kazuyuki Otsuka 

Distribution and relative abundance of the blue shark, Prionace glauca. in the southwestern 
equatorial Atlantic Ocean 



Errata 

(i) 

Bigelow, Keith A. 

Age and growth of the oceanic squid Onychoteuthis 
borealijaponica in the North Pacific 
Fish. Bull. 92(l):13-25 
Figure 5 should read as shown below. 



— 



300 
250 
200 
150 
100 
50 



400 
350 
300 
250 
200 
150 
100 
50 




Males 



• • 



- 1 1 1 1 i i 1 1 1 

50 100 150 200 250 300 350 400 450 





Males 




400 - 
300 - 




°^ D# 


200 - 




o o Jr 


100 - 
- 


A n. 


~+t-^ — , — , — , — , 



50 100 150 200 250 300 350 400 450 



Females 






• 


V? 




1 1 I 1 1 1 


1 1 1 



X 
£ 

S: 1000 -, 



Females 






o H .-, » _ <*u 



50 100 150 200 250 300 350 400 450 

AGE (days) 



50 100 150 200 250 300 350 400 450 
AGE (days) 



Figure 5 

Relation between age (determined by number of increments within statoliths) and 
mantle length (mm) and weight (g) for male and female Onyclwteuthis 
borealijaponica. Western North Pacific 1990 (open circles), central North Pacific 1990 
(closed circles), central North Pacific 1991 (closed triangles = juveniles-subadults, 
open triangles = unknown sex), and eastern North Pacific 1990 (open squares). 



(2) 

Perryman, Wayne L., and Morgan S. Lynn 

Examination of stock and school structure of 
striped dolphin {Stenella coeruleoalba) in the 
eastern Pacific from aerial photogrammetry 
Fish. Bull. 92(1):122-131 



Figures 3, 4, and 7, and Tables 1, 2, and 3 show an 
incorrectly typeset species name for striped dol- 
phin. The correct name should read striped dol- 
phin, Stenella coeruleoalba. 



The National Marine Fisheries Service (NMFS) does not approve, recommend, 
or endorse any proprietary product or proprietary material mentioned in this 
publication. No references shall be made to NMFS, or to this publication fur- 
nished by NMFS, in any advertising or sales promotion which would indicate 
or imply that NMFS approves, recommends or endorses any proprietary pro- 
duct 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 pur- 
chased because of this NMFS publication. 



Abstract. Eggs of walleye 

pollock, Theragra chalcogramma, 
from Shelikof Strait, Alaska, were 
reared at three temperatures: 3.8°, 
5.7°, and 7.7°C. Development was 
divided into 21 stages. A piece- 
wise regression model with mid- 
points of each stage describes the 
relation between time to each 
stage of development and tempera- 
ture. Preserved eggs of each stage 
are described, illustrated, and pho- 
tographed. Midpoint of hatch was 
393 hours at 3.8°C, 303 hours at 
5.7°C, and 234 hours at 7.7°C. 
Mean length of larvae at hatch in- 
creased linearly with temperature. 
We compared rate of develop- 
ment, time to 50% hatch, and mor- 
phological development with other 
studies of walleye pollock eggs. 
Rate of development and time to 
50% hatch were similar among 
populations of eastern North Pa- 
cific walleye pollock. Western 
North Pacific walleye pollock re- 
quired longer incubation times 
than eastern North Pacific walleye 
pollock. Morphological develop- 
ment of Shelikof Strait eggs differs 
from development of western 
North Pacific walleye pollock eggs: 
optic vesicles, myomeres, eye 
lenses, heart, and otic capsules 
appear earlier than in Shelikof 
Strait eggs, and eye pigment ap- 
pears later. The differences in de- 
velopment may be exacerbated by 
the condition of the eggs in which 
they were examined (e.g. pre- 
served vs. live). Developmental 
differences between stocks are dis- 
cussed with the conclusion that 
model components for egg mortal- 
ity and spawning biomass must be 
based on specimens collected in 
the area of interest. 



Embryonic development of 

walleye pollock, 

Theragra chalcogramma, 

from Shelikof Strait, Gulf of Alaska* 

Deborah M. Blood 
Ann C. Matarese 
Mary M. Yoklavich** 

Alaska Fisheries Science Center, National Marine Fisheries Service. NOAA 
7600 Sand Point Way N.E., Seattle, WA 981 15-0070 



Walleye pollock, Theragra chalco- 
gramma, is the most abundant 
member of the family Gadidae in 
the subarctic Pacific Ocean and 
Bering Sea, supporting the largest 
single-species commercial fishery 
in the world (Megrey, 1991). In 
the Gulf of Alaska, Shelikof Strait 
is the principal spawning area 
(Kendall and Picquelle, 1990) and 
has been the site of intensive re- 
search to understand processes 
leading to recruitment variability 
of walleye pollock (Schumacher and 
Kendall, 1991). 

Age determination of fertilized 
eggs is a basis for investigating 
biotic and abiotic impacts on the 
earliest life-history stage and thus 
for understanding interannual 
variability in walleye pollock re- 
cruitment. Age of walleye pollock 
eggs has been crucial to several 
studies. Egg mortality and spawn- 
ing biomass are estimated by mod- 
eling age-specific egg abundance 
over time (Picquelle and Megrey, 
1993; Bates 1 ). Patterns in horizon- 
tal or vertical distribution and 
abundance of walleye pollock eggs 
in the western Gulf of Alaska have 
been described by grouping devel- 



opmental stages into broad age 
groups (Kendall and Kim, 1989; 
Kendall and Picquelle, 1990). 

Egg age is an independent vari- 
able in the models used to estimate 
egg production and mortality. 
Therefore, increasing the accuracy 
in measuring egg ages should im- 
prove estimates of these values. In 
past studies, walleye pollock eggs 
have been incubated in the labora- 
tory to develop temperature-spe- 
cific equations that estimate dura- 
tion of development or age of the 
eggs, to describe morphological de- 
velopment, to observe effects of 
light on egg buoyancy and hatching 
rate, and to obtain larvae for ex- 
periments (Table 1). Although 
these incubation studies provide 
pertinent data on ontogeny of wall- 
eye pollock, none can be used with 
accuracy to determine age of eggs 



Bates, R. D. 1987. Estimation of egg pro- 
duction, spawner biomass, and egg mor- 
tality for walleye pollock, Theragra 
chalcogramma, in Shelikof Strait from 
ichthyoplankton surveys during 1981. 
U.S. Dep. Commer., NOAA, Nat. Mar. 
Fish. Serv., Northwest Alaska Fish. Cent., 
7600 Sand Point Way N.E., Bin C15700, 
Bldg. 4, Seattle, WA 98115-0070. Proc. 
Rep. 87-20, 192 p. 



Manuscript accepted 3 November 1993 
Fishery Bulletin 92: 207-222 (1994) 



* Contribution 0148 of the Fisheries Oceanography Coordinated Investigations, NOAA, 

Seattle. 
** Present address: Southwest Fisheries Science Center, Pacific Fisheries Environmen- 
tal group. National Marine Fisheries Service, NOAA, P.O. Box 831, Monterey, CA 93942 



207 



208 



Fishery Bulletin 92(2). 1994 









Table 1 














Summary of Theragra chalcogramma egg incubation 


stuc 


ies. 






Reference 


Temperature 

(°C) 


Source and 
region 


Stages' 


Regression 
equation 


Morphological 
description 


Illustrations 


Photographs 


Gorbunova, 
1954 


3.4, 8.2 
(means) 


western 
Pacific 
Ocean 


N ii n i • 


No 


Yes 






Yes 


No 


Yusa, 1954 


6.0-7.0 


Ishikan Bay, 
Japan 


27 2 


No 


Yes 






Yes 


Yes 


Hamai et al., 
1971 


2.4-2.5, 
6.5-6.7, 
9.9-10.1, 

( means) 


Funka Bay, 
Japan 


4 


Stage-specific 
equation to 

predict age (d) 
at any stage 


No 






No 


No 


Hamai et al., 
1974 


5.0 (mean) 


Funka Bay, 
Japan 


6 


No 


No 






No 


No 


Matarese 1983 
unpubl.'' 


5.0 


N. Gulf of 
Alaska 


21 


Stage-specific 

equation to 
predict age (h) 
at any stage'' 


Nn 






No 


No 


Haynes and 
Ignell, 1983 


2.0, 5.0, 
6.0, 8.0, 11.0 


Stephens 

Passage, SE 

Alaska 


7 


General equation 

to predict age (h) 

at any stage 


No 






No 


No 


Nakatani and 
Maeda. 1984 


-1.0, 0.0, 2.0, 
4.0, 7.0, 
10.0, 13.0 


Funka Bay, 
Japan 


5 


To 507r hatch 


No 






No 


No 


Paul, 1984, 
unpubl. 1 


5.0 


N. Gulf of 
Alaska 


21 


No 


No 






No 


No 


Bailey and 
Stehr, 1986 


5.6, 8.5 


Puget Sound, 
Washington 


None 


No 


No 






No 


No 


Olla and 
Davis, 1993 


6.0 


Shelikof Strait, 
Alaska 


Nunc 


Nil 


No 






No 


No 


; Prior to hatch. 

2 Reported as intervals of time. 

3 A. C. Matarese, Alaska Fisheries Science Center, National Marine Fisheries Service, 7600 Sand Poin 

4 In Bates 1987 (Footnote 1). 

1 A J. Paul, University of Alaska Fairbanks, Institute of Marine Science, Seward Marine Center Lab, 


t Way 
P.O. B 


NE., Seattle 
ox 730, Sewa 


WA 98115. 
rd, AK 99664. 



from Shelikof Strait. Eggs need to be obtained from 
the study area and incubated at a range of tempera- 
tures occurring in the area. Categorizing the con- 
tinuous process of egg development into a large 
number of stages should increase the precision of the 
egg-age estimate 

The first objective of our study was to incubate 
Shelikof Strait walleye pollock eggs at the mean 
water temperature for Shelikof Strait, bracketing 
that temperature to include upper and lower ex- 
tremes. Egg development times were used to pro- 



duce a stage duration table and a regression model 
to estimate egg age based on water temperature and 
developmental stage. Morphological development is 
described for 21 developmental stages. These de- 
scriptions are accompanied by illustrations and 
photographs to facilitate identification of body struc- 
tures and stage hallmarks. 

The second objective was to compare our rates of 
egg development to other walleye pollock incubation 
studies. Morphological development is included in 
this comparison. 



Blood et al.. Embryonic development of Theragra chalcogramma 



209 



Methods 

Incubation 

Adult walleye pollock were collected with a rope 
trawl off Cape Kekurnoi (57°42.5'N, 155°16.2'W) in 
Shelikof Strait, Alaska, on 7 April 1989 from the 
NOAA research vessel Miller Freeman. Eggs from 
one female and milt from three or four males were 
hand stripped into glass petri dishes, gently mixed, 
and left undisturbed for one minute. Eggs were then 
rinsed, transferred to 3°C (surface water tempera- 
ture) seawater in glass jars (3.8 L), and held two 
hours. Floating eggs with a perivitelline space were 
assumed to be fertilized (Blaxter, 1969; Alderdice, 
1988). Viable eggs were poured into eighteen 0.5-L 
jars filled with 3°C seawater. Eggs were not counted 
but apportioned similarly among the jars at a con- 
centration of about one egg/mL. Six capped jars were 
held in each of three water bath incubators onboard 
the Miller Freeman. Initial incubation temperatures 
were set to include the range of temperatures in the 
area. Mean water temperature at depths of 150-200 
m in Shelikof Strait, where most eggs are found 
(March-May) (Kendall and Kim, 1989), is 5°C; ex- 
tremes of 3.6° and 5.9°C have been reported (Reed 
and Schumacher, 1989). Incubators were sealed to 
minimize light and movement and placed in sepa- 
rate refrigerators adjusted to 3°, 5°, and 7 C. One- 
half of the water in the jars was replaced every day 
with seawater of the same temperature. Eggs were 
preserved in phosphate buffered formalin (5%) 2 or 
Stockard's solution 3 (Velsen, 1980). Stockard's solu- 
tion cleared the chorion and darkened embryonic 
tissue, easing examination of embryonic develop- 
ment. Phosphate buffered formalin did not darken 
embryonic tissue as much as Stockard's solution, 
yielding better definition of some structures like 
somites and otic capsules. Live, newly hatched lar- 
vae were measured (standard length in millimeters) 
and preserved (5% buffered formalin). Detailed exami- 
nation and morphological description of embryos were 
completed after eggs were returned to the laboratory. 
During the first 24 hours after fertilization, eggs 
were sampled at 2-3 hour intervals. After 24 hours, 
intervals were increased to about 6 hours. When an 
interval was less or greater than 6 hours, the sub- 
sequent sampling time was adjusted to return to the 
original 6-hour schedule. Data were not recorded for 
three sampling times late in development because 



intervals were inadvertently extended to 12 hours 
(236, 258, and 282 hours). 

At each interval, 10 to 50 eggs were sampled from 
one jar per incubator; only one jar was sampled to 
ensure there would be enough eggs and larvae left 
to sample near the end of the incubation period. Jars 
were sampled in rotation throughout the duration 
of the experiment until no eggs remained. When 
eggs began to hatch, all jars were checked and newly 
hatched larvae were removed in addition to eggs 
scheduled to be sampled. Dead eggs were removed 
from the designated sample jar at each interval. 
Water bath temperatures were recorded for every 
sampling interval. Frequent opening of refrigerators 
during the initial short sampling intervals increased 
temperatures in the refrigerators despite thermostat 
adjustments. Water bath temperatures stabilized 
after 48 hours to 3.8°, 5.7°, and 7.7°C. 

Morphological descriptions 

Eggs were examined with the aid of a dissecting 
microscope (6-50x magnification) and described ac- 
cording to a 21-stage scheme adapted from Naplin 
and Obenchain (1980) (Table 2). Morphological 
terms follow Trinkaus ( 1951) with one exception: the 
term "blastodisc," in this paper, includes the germi- 
nal area from the time of cytoplasm polarization 
until embryonic shield formation (Markle and 



Table 2 

Stages of embryonic development of Theragra 
chalcogramma (adapted from Naplin and 
Obenchain, 1980). 



Stage 



Developmental stage 



2 50 mL 37% formaldehyde, 4.0 g sodium phosphate monobasic, 
6.5 g sodium phosphate dibasic, made up to 1 L with distilled 
water. 

3 50 mL 371 formaldehyde, 40 mL glacial acetic acid, 60 mL 
glycerin, and 850 mL distilled water. 



1 


Precell 


2 


2 cell 


3 


4 cell 


t 


8 cell 


5 


16 cell 


6 


32+ cell 


7 


Blastodermal cap 


8 


Early germ ring 


9 


Germ ring 1/4 down yolk 


10 


Germ ring 1/2 down yolk 


11 


Germ ring 3/4 down yolk 


12 


Late germ ring 


L3 


Early middle (blastopore closure) 


14 


Middle middle (appearance of pigment 


15 


Late middle (tail bud thickens) 


\h 


Early late (tail bud lifts from yolk) 


17 


Tail 5/8 around yolk 


18 


Tail 3/4 around yolk 


19 


Tail 7/8 around yolk 


20 


Full circle around yolk 


21 


Tail 1-1/8 around yolk 



210 



Fishery Bulletin 92(2). 1994 



Waiwood, 1985, in part). Eggs preserved in 
Stockard's solution were photographed with a Nikon 
F2 camera fitted with a PB6 200-mm bellows exten- 
sion and a 24-mm 1:2.8 reverse-mounted lens. This 
configuration produced a 47x magnification. Re- 
flected light was supplied by two synchronized flash 
units. Other photographs (stages 5 and 6) were 
taken with a single-lens reflex adapter (0.32x) on a 
Wild M-8 dissecting microscope with transmitted 
light. At 50x, the phototube and adapter increased 
magnification to 66x. 

Analysis 

Endpoint, midpoint, and duration of stage (in hours) 
were estimated for eggs incubated at each tempera- 
ture. For stages 1-20, stage endpoint was deter- 
mined by the presence of two stages during a sam- 
pling time; if stages n and n + \ were present, the 
time at which the eggs were sampled was consid- 
ered a transition and therefore the endpoint for 
stage n. If there was no transition, the endpoint for 
stage n was the midpoint between the last sampling 
time during which stage-rc eggs were present and 
the first time stage-« + l eggs were observed. Dura- 
tion and midpoint of stage n were determined as 

Duration Stage n = Endpoint Stage (n) - 
Endpoint Stage in - 1); 



Midpoint Stage n = Endpoint Stage (n 
Duration Stage n 



li 



Endpoint of stage 21 was the sampling interval 
when the last embryo had hatched. With the mid- 
points and time of 50% hatch, a piece-wise least- 
squares linear regression model (SAS, 1985) was 
derived to estimate age (hours) of eggs at a specific 
stage incubated at any temperature within the lim- 
its of this experiment. 

Differences in mean lengths of larvae hatched 
from the three temperature groups were analyzed 
by a Student-Newman-Keuls test. Lengths of larvae 
hatching at stages 20 and 21 were analyzed by a 
two-way analysis of variance (ANOVA) by using 
stage and temperature. 

We chose five representative developmental stages 
and compared time to midpoint of each stage among 
incubation studies. Comparison with Hamai et al. 
(1971, 1974) was possible for only three stages. We 
grouped data on time to 509f hatch into western and 
eastern North Pacific studies and performed a log- 
transformed analysis of covariance to test for differ- 



ences in time to 50% hatch between these two ar- 
eas with incubation temperature as the covariate. 



Results 

Incubation rates 

Temperatures of the three water baths increased at 
the beginning of sampling (Fig. 1). Temperature 
spikes that occurred after 288 hours in the 5.7°C jars 
and after 396 hours in the 3.8°C jars, were associ- 
ated with the appearance of large numbers of lar- 
vae; water baths may have warmed when refrigera- 
tors were opened frequently to measure larvae. 

Eggs developed at similar rates among incubation 
temperatures for the first 36 hours through stage 6 
(Fig. 2). After stage 6, at about 36 hours, when tem- 
peratures had stabilized, development rates began 
to diverge. Duration of stages 7-21 was variable 
(Table 3). Usually the duration of a stage was longer 
at cooler temperatures. However, this was not al- 
ways the case, and stages 12 and 20 required simi- 
lar amounts of time regardless of temperature. At 
all temperatures, hatching began during stage 20; 
the percentage of eggs hatched by the beginning of 
stage 21 was 35% at 3.8°, 40% at 5.7°, and 8.1% at 
1.1'C Four larvae from the 7.7°C group hatched 
after 192 hours; another 18 hours elapsed before 
other larvae hatched at this temperature. These 
early larvae were not included in this analysis be- 
cause we assumed that the hiatus in hatching times 
indicated that early hatching was anomalous, i.e. 
hatching may have been mechanically induced. Af- 
ter hatching began, time required for 50% hatch 
decreased as temperature increased: 48, 36, and 24 
hours at 3.8°, 5.7 , and 7.7°C. The elapsed time be- 
tween hatching of the first and last larvae was 72 
hours at 3.8°C and 60 hours at both 5.7 and 7.7°C. 

Eggs developed normally at 5.7° and 7.7°C; how- 
ever, curvature of the spine was observed in some 
late-stage embryos incubated at 3.8C These abnor- 
mal eggs hatched, but most larvae were not mea- 
sured because of curvature. Mean length at hatch 
of all larvae increased with incubation temperature: 
4.15 (SD 0.380, n = 100), 4.29 (SD 0.272, rc=192), and 
4.55 mm (SD 0.303, rc=84> at 3.8°, 5.7°, and 7.7'C 
(Fig. 3). Mean lengths of larvae from the three tem- 
perature groups were significantly different 
(P<0.05). In addition, larval lengths increased as the 
hatching period progressed at all temperatures. 
Length of larvae hatching at stages 20 and 21 was 
significantly different at all temperatures (P<0.01); 
larvae that hatched at stage 21 were 9-13% longer 
than larvae that hatched at stage 20. 



Blood et al.: Embryonic development of Theragra chalcogramma 



21 1 



O 



/ 



J& * 



**.^*^w**** **•**.*** * ********* *.. ; 




3.8 C -+- 5.7 C * 7.7 C 



I 1 1 1 1 I : 1 1 1 1 1 1 1 1 1 1 

24 48 72 96 120 144 168 192 216 240 264 288 312 336 360 384 408 

Incubation time (h) 

Figure 1 

Temperatures recorded in water baths during incubation of Theragra chalcogramma eggs. 



o> 
CO 

*-■ 
CO 

c 
CD 

E 

Q. 

o 

CD 

> 
CD 

Q 







24 48 72 96 120 144 168 192 216 240 264 288 312 336 360 384 408 

Incubation time (h) 

Figure 2 

Development of Theragra chalcogramma eggs incubated at 3.8°, 5.7°, and 7.7°C. Points represent occurrence of 
stages at scheduled sampling times. 



The piece-wise regression model (SAS, 1985) has 
two separate components and is discontinuous be- 
tween stages 6 and 7 (Fig. 4). This type of model was 
necessary because of the rapid divergence of devel- 
opmental rates at all temperatures after stage 6; it 
was not possible to fit one equation to the entire 
incubation time. The two components are described 
by the following equations: 



component 1: stages 1-6 

Age = 3.27 - 0.13 (stage) (temperature) 
+ 0.47 (stage 2 ); 

component 2: stages 7-21 

Age = 17.82 + 7.05(stage) - 0.656 (stage) 

(temperature) + 0.043(stage 3 ) - 0.0032 

(temperature) (stage 3 ), 



212 



Fishery Bulletin 92(2). 1994 









Table 3 










Endpoint, midpoint, and duration in hours (h) of stage of deve 


opment of Theragra chalcogramma 


eggs incu- 


bated at 3.8°, 5.7°, and 7.7°C 
















3.8'C 




5.7"C 






7.7°C 




Stage Endpoint (h) 


Midpoint (h) 


Duration (h) 


Endpoint (h) Midpoint (h) 


Duration (h) 


Endpoint (h) 


Midpoint (h) 


Duration (h) 


1 4.00 


2.00 


4.00 


4.00 2.00 


4.00 


3.50 


1.75 


3.50 


2 6.00 


5.00 


2.00 


6.00 5.00 


2.00 


4.00 


3.75 


0.50 


3 8.00 


7.00 


2.00 


7.00 6.50 


1.00 


5.00 


4.50 


1.00 


4 10.25 


9.12 


2.25 


9.00 8.00 


2.00 


7.00 


6.00 


2.00 


5 12.50 


11.37 


2.25 


10.25 9.62 


1.25 


10.25 


8.62 


3.25 


6 22.50 


17.50 


10.00 


22.50 16.37 


12.25 


19.50 


14.87 


9.25 


7 64.00 


43.25 


41.50 


51.00 36.75 


28.50 


40.00 


29.75 


20.50 


8 78.00 


71.00 


14.00 


68.00 59.50 


17.00 


48.00 


44.00 


8.00 


9 90.00 


84.00 


12.00 


75.00 71.50 


7.00 


54.00 


51.00 


6.00 


10 105.00 


97.50 


15.00 


87.00 81.00 


12.00 


57.00 


55.50 


3.00 


11 120.00 


112.50 


15.00 


93.00 90.00 


6.00 


68.00 


62.50 


11.00 


12 138.00 


129.00 


18.00 


108.00 100.50 


15.00 


84.00 


76.00 


16.00 


13 153.00 


145.50 


15.00 


114.00 111.00 


6.00 


87.00 


85.50 


3.00 


14 180.00 


166.50 


27.00 


135.00 124.50 


21.00 


102.00 


94.50 


15.00 


15 195.00 


187.50 


15.00 


164.00 149.50 


29.00 


111.00 


106.50 


9.00 


16 219.00 


207.00 


24.00 


174.00 169.00 


10.00 


117.00 


114.00 


6.00 


17 252.00 


235.50 


33.00 


189.00 181.50 


15.00 


132.00 


124.50 


15.00 


18 312.00 


282.00 


60.00 


219.00 204.00 


30.00 


144.00 


138.00 


12.00 


19 336.00 


324.00 


24.00 


258.00 238.50 


39.00 


180.00 


162.00 


36.00 


20 378.00 


357.00 


42.00 


300.00 279.00 


42.00 


219.00 


199.50 


39.00 


21 414.00 


393.00' 


36.00 


330.00 303.00' 


30.00 


270.00 


234.00' 


51.00 


' 50% hatch. 



where age of the egg is expressed in hours. The 
value of R 2 is 0.96 for component 1 and 0.99 for 
component 2. 

We compared our rates of egg development to 
other walleye pollock incubation studies in the 5- 
7°C range (Table 4). There was a significant differ- 
ence between regression equations of incubation 
time to 50% hatch and temperature for western 
versus eastern North Pacific studies (P<0.01), but 
the slopes were not different (P=0.18). Based on the 
95% confidence interval about the parameter esti- 
mates, time to 50% hatch of western North Pacific 
walleye pollock tended to be 1.2 to 1.3 times longer 
on average than that of the eastern North Pacific 
fish at a specific temperature. 

Morphological descriptions 

Walleye pollock eggs are pelagic and have a smooth, 
clear chorion and homogeneous yolk. No oil globules 
are present. Preserved eggs range from 1.2 to 1.8 
mm in diameter, although most are 1.35-1.45 mm 
(Matarese et al., 1989). Appearance of the egg var- 
ies with type of preservative. There was little or no 
shrinkage of yolk material in Stockard's solution, 



whereas yolk of formalin-preserved eggs decreased 
in volume and the yolk membrane frequently col- 
lapsed. This effect of formalin preservation was 
helpful in determining how much of the tail had 
lifted away from the yolk in late-stage embryos. 

Development of walleye pollock eggs and embryos, 
from fertilization to just before hatching, was di- 
vided into the following 21 stages (Table 2): 

Precell (stage 1) Cytoplasm at the animal pole 
forms a blastodisc; bands of cytoplasm extend from 
below the equator to the blastodisc (Fig. 5A), which 
is without distinct margins (Fig. 6A). When intact, 
the yolk membrane almost touches the inner wall 
of the chorion. The perivitelline space is most vis- 
ible over the blastodisc. 

2 cells (stage 2) The first cell division of the 
blastodisc is in the horizontal plane. Cell material 
may not be equally divided (Figs. 5B and 6B). 

4 cells (stage 3) The second cleavage is perpen- 
dicular to, and in the same plane as, the first. Cells 
are roughly equal in size and form a square (Figs. 
5C and 6C). 

8 cells (stage 4) The third cleavage is perpen- 
dicular to the second cleavage (parallel to first cleav- 
age). Each cell divides in half in the horizontal 



Blood et al.: Embryonic development of Theragra chalcogramma 



213 



E 
E 



O) 

c 

9 

C 
CO 
9 

s 



5.5 



5.0 



4.5 



4.0 



3.5 



"T 




O 7./C 
D 6.7°C 
A 3.8° C 




3.0 
204 



248 



292 



336 



380 



424 



Total incubation time (h) 



Figure 3 

Mean hatch lengths at each sampling interval during the hatching period of 
Theragra chalcogramma larvae incubated at 3.8°, 5.7°, and 7.7°C. Stage of de- 
velopment at hatch is also shown. Shaded circle indicates overall mean length 
for each temperature. Vertical bars are standard deviations; numbers indicate 
sample size. 



plane. Cells form a rectangle with the four cells in 
the center smaller than those at the corners of the 
rectangle (Figs. 5D and 6D). 

16 cells (stage 5) The fourth cleavage is perpen- 
dicular to the third; this is the last stage in which 
cell division is restricted to the horizontal plane. 
Most eggs have a square or rectangular block of cells 
with four cells on each side; all cells are in contact 
with yolk through this stage (Figs. 5E and 6E). 

32 cells (stage 6) Initially, the single layer of 
cells has a flat, irregular square or rectangular 
shape. Cell division continues in horizontal and 
vertical planes, transforming the blastodisc into a 
hollow cap of cells on the yolk resembling a rasp- 
berry (Figs. 5F and 6F). Cells increase in number 
but the size of the blastodisc remains constant. The 
perivitelline space widens between yolk and chorion. 

Blastodermal cap (stage 7) The blastodisc 
progresses through two steps: at first, cell size de- 
creases from continued cleavage; cell material ap- 
pears granular and the blastodisc resembles a flat- 
tened dome on the yolk surface. Then, the base of 
the cell mass sinks below the yolk surface; the 
periblast extends beyond the equator of the blasto- 
disc, giving the appearance of a "flying saucer" in 



lateral view (Figs. 5G and 
6G). 

Early germ ring (stage 

8) The center of the blasto- 
disc flattens and the periph- 
ery (germ ring) thickens in 
preparation to overgrow the 
yolk (epiboly). The blasto- 
coel, visible on one side of 
the blastodisc, appears 
grainy and pale (Fig. 5H). 
The margin between blasto- 
coel and blastodisc is indis- 
tinct (Fig. 6H). 

Germ ring 1/4 around 
yolk (stage 9) The blasto- 
disc, now the embryonic 
shield, expands as the germ 
ring begins to overgrow the 
yolk. The margin of the fu- 
ture anterior end of the em- 
bryo is slightly curved and 
sharply defined. Cell mate- 
rial covering the blastocoel 
appears less grainy than in 
the previous stage. After 
preservation, this thin cellu- 
lar layer appears concave in 
lateral view. The germ ring 
margin is thin and flattened, 
extending 1/4 around yolk (Figs. 51 and 61). 

Germ ring 1/2 around yolk (stage 10) The 
germ ring envelopes half the yolk and the anterior 
margin of the embryonic shield is sharply curved 
and thick (Figs. 5J and 6J). The beginning of neu- 
ral development is visible; a neural keel extends 
from the anterior margin of the embryonic shield to 
2/3 its length (Fig. 5K). 

Germ ring 3/4 around yolk (stage 11) Head 
and upper body region begin to differentiate but no 
distinct brain lobes are apparent. Optic vesicles 
develop. Prospective head and body mesoderm out- 
lines the hour-glass shape of the developing embryo 
(Fig. 7A). The notochord is visible ventrally. The germ 
ring has progressed 3/4 down the yolk (Fig. 6K). 

Late germ ring (stage 12) Myomere differen- 
tiation begins; separate myomeres are not visible. 
The midbody expands dorsoventrally; prospective 
head and body mesoderm forms a narrow outline of 
the embryo. The blastopore is open and the germ 
ring envelopes more than 7/8 of the yolk (Figs. 7B 
and 8A). 

Early middle stage (stage 13) The blastopore 
is closed. The notochord and 7-12 incomplete 
myomeres are visible. Tail margin is indistinct and 



214 



Fishery Bulletin 92(2). 1994 



a> 



c 

o 
a. 
■o 

E 

o 



0) 

E 

i- 



flat; the medial portion of 
the tail bud is thicker (Figs. 
7C and 8B). The body of the 
embryo appears flattened. 
Although not distinguish- 
able in preserved specimens, 
Kupffer's vesicle is visible in 
the live egg. 

Middle middle stage 
(stage 14) Embryos have 
14-16 myomeres. Differen- 
tiation begins in eyes and 
mid- and hindbrain. Fore- 
brain very small and under- 
developed. The tail bud mar- 
gin is defined but still flat- 
tened (Fig. 8C). The entire 
length of the body is thicker. 
Small melanophores are 
scattered along the dorsum 
between the hindbrain and 
4/5 of body length (Fig. 7D). 

Late middle stage (stage 
15) About 20-25 myomeres 
are visible. Eye lenses are 
formed. The liver appears as 
a slight bulge in the body 
wall, and the gut area is de- 
lineated. The tail bud is thick and appears lifted 
from the yolk surface with the margin attached (Fig. 
7E). Pigment is darker than in the previous stage 
and dendritic, extending from midbrain to tip of tail 
bud and confined mostly to the dorsum. Nares, mid- 
and hindbrain, and pectoral bud anlagen are visible 
dorsally (Fig. 8D). 



450 
400 
350 
300 
250 
200 
150 
100 
50 




n — i — i — i — i — i — i — i — i — i — i r 



n — i — i — i — i — i — i — r 



-B-- 


3.a°c 


-e- 


 

9.7 C 


▲ 


7.7 °C 




I I I I I I I I L 



J I L 



1 2 3 



S 7 8 10 11 12 13 14 18 Ifl 17 18 10 20 BOM 



Developmental stage 

Figure 4 

Time (h) to midpoint of stage of Theragra chalcogramma eggs incubated at 3.8°, 
5.7°, and 7.7°C. Fitted lines are results of regression model; symbols are observed 
values. 



Early late stage (stage 16) Heart tissue begins 
to expand when the embryo has about 24-36 myo- 
meres. Forebrain differentiates from midbrain. The 
tail bud lifts from the yolk surface (Figs. 7F and 8E) 
and pigment forms two parallel rows dorsoposteriorly. 

Tail 5/8 around yolk (stage 17) The embryo 
has 27-36 myomeres. More of the tail lifts from the 



Table 4 

Comparison of time (h) to estimated midpoint of five developmental milestones of Theragra chalcogramma 
embryos incubated at 5-7°C. 





Eastern 


North Pacific 


incubation stuc 


ies 


Western North Pacific incubation 


studies 




Matarese, 


Paul, 1984, 


Haynes and 


This 


Hamai et al., 


Yusa, 


Nakatani and 


Hamai et al., 




1983, unpubl. 


unpubl. - 


Ignell, 1983' 


study 


1971* 


1954 


Maeda, 1984 5 


1974 


Stage 


15.0-C) 


15.0 C) 


16.0 C) 


(5.7'C) 


(6.5-6.7'C) 


(6.0-7.0 Cl 


(7.0"C) 


(5.0 Cl 


Blastodermal cap 


37.5 


39.5 


35 


36.8 




28.5 


31 




Blastopore closure 114 


UK 


105 


108 


100 


102 


Its 


139 


Tail 3/4 


211.7 


217 


li,l 


204 




234 


192 




Tail full circle 


274.5 


264 


250 


279 


250 


270 


216 


330 


Vi<, hatch 


349 


320 


285 


303 


345 


288+ 


298 


411 



A C Matarese. Alaska Fisheries Science Center, National Marine Fisheries Service, 7600 Sand Point Way N.E., Seattle, WA 98115. 
2 A .1 Paul, University of Alaska Fairbanks. Institue of Marine Science, Seward Marine Center Lab, P.O. Box 730, Seward, AK 99664. 

Values except for hatch estimated from Table 3 in Haynes and Ignell (1983). 50% hatch from Table 7. 
1 Values except fur hatch estimated from Fig. 3 in Hamai et al. (1971). 
' Values except for hatch estimated from Fig 5 in Nakatani and Maeda (1984). 



Blood et al.: Embryonic development of Theragra chalcogramma 



215 



cytoplasm 




- blastodtsc 



perivitelline 
space 







E 



periblast 




germ ring 




blastocoel 






neural keel 



Figure 5 

Illustrations of preserved Theragra chalcogramma eggs. (Al Stage 1 (precell); (B) Stage 2 (2 cell); (C) Stage 
3 (4 cell); (D) Stage 4 (8 cell); (E) Stage 5 (16 cell); (F) Stage 6 (32 cell); (G) Stage 7 (blastodermal cap); (H) 
Stage 8 (early germ ring); (I) Stage 9 (germ ring 1/4, lateral view); (J) Stage 10 (germ ring 1/2, lateral view); 
(K) Stage 10 (dorsal view). 



216 



Fishery Bulletin 92(2), 1994 







E 






II 










Figure 6 

Photographs of preserved Theragra chalcogramma eggs. (A) Stage 1 (precell); (Bi Stage 2 (2 cell); (C) Stage 3 
(4 cell); (D) Stage 4 (8 cell); (E) Stage 5 (16 cell); (F) Stage 6 (32 cell); (G) Stage 7 (blastodermal cap); (H) Stage 
8 (early germ ring); (I) Stage 9 (germ ring 1/4); (J) Stage 10 (germ ring 1/2); (K) Stage 11 (germ ring 3/4). 



Blood et al.: Embryonic development of Theragra chalcogramma 



217 



optrc vesicle 




prospective 
head and body 
mesoderm 



optic vesicle 



myomeres 






blastopore 



lens 




E 



otic capsule 




H 





hatching 
gland: 




hatching 
glands 



J K L 

Figure 7 

Illustrations of preserved Theragra chalcogramma eggs. (A) Stage 11 (germ ring 3/4); (B) Stage 12 (blastopore 
almost closed); (C) Stage 13 (early middle); (D) Stage 14 (middle middle); (E) Stage 15 (late middle); (F) Stage 16 
(early late); (G) Stage 17 (tail 5/8 circle); (H) Stage 18 (tail 3/4 circle); (I) Stage 19 (tail 7/8 circle); (J) Stage 20 
(tail full circle, lateral view); (K) Stage 20 (dorsal view); (L) Stage 21 (tail 1-1/8 circle). 



218 



Fishery Bulletin 92(2). 1994 








Figure 8 

Photographs of preserved Thcragra chaleogramma eggs. (A) Stage 12 (blastopore almost closed); (B) 
Stage 13 (early middle); (C) Stage 14 (middle middle); (D) Stage 15 (late middle); (E) Stage 16 (early 
late); (F) Stage 17 (tail 5/8 circle); (G) Stage 18 (tail 3/4 circle); (H) Stage 19 (tail 7/8 circle); (I) Stage 
20 (tail full circle); (J) Stage 21 (tail 1-1/8 circle). 



Blood et al.: Embryonic development of Theragra chalcogramma 



219 




3.5 mm SL 



Figure 9 

Illustration of preserved Theragra chalcogramma yolk-sac larva 
(Matarese et al., 1989). 



yolk surface (Fig. 8F). The dorsal finfold is formed 
on the posterior 1/3 of the body and pigment on the 
head extends at least to the posterior margin of the 
eye (Fig. 7G). The liver is prominent and the heart is 
beating in the live egg. 

Tail 3/4 around yolk (stage 18) The embryo 
has 36-41 myomeres. The tip of the tail is tapered 
and curves away from the longitudinal axis of the 
embryo (Fig. 7H). The dorsal finfold extends to 
midbody and pectoral fin buds are prominent. Otic 
capsules are formed. Large stellate melanophores 
are scattered over the dorsum, extending just to the 
midlateral surface; posterior to the anus, two rows 
of melanophores are seen dorsally and a few are 
found along the ventral midline (Fig. 8G). The tip 
of the tail is unpigmented. 

Tail 7/8 around yolk (stage 19) When the 
embryo has 44-48 myomeres, the dorsal finfold ex- 
tends anteriorly 2/3 body length, inserting just pos- 
terior to the pectoral fin buds and centered over the 
liver (Figs. 71 and 8H). Pigment on the head extends 
to the middle of the eye. At midbody, pigment is scat- 
tered on either side of the dorsal midline, extend- 
ing to just above the lateral midline. Postanal pigment 
migrates toward the dorsal and ventral midlines. 

Tail full circle around yolk (stage 20) The 
embryo has 48—49 myomeres and the pancreas is 
visible adjacent to the liver (Fig. 7J). The embryo 
now encircles the yolk and the tail tip may reach 
from near the snout to as far back as the posterior 
margin of the eye (Fig. 81). Hatching glands, simi- 
lar to those of other teleosts (Yamagami, 1988), are 
discernible on the surface of the snout and may 
extend over the dorsal surface of the eye (Figs. 7 J 
and 7K). The posterior portion of the eye is pig- 
mented. Postanal pigment migrates and begins to 
form the postanal bars found in yolk-sac larvae 
(Matarese et al., 1989) (Fig. 9). 

Tail 1 1/8 times around yolk (stage 21) The 
embryo has 49-50 myomeres and the tail tip elon- 



gates, extending beyond the posterior 
margin of the eye (Fig. 8J). The urinary 
bladder is visible posterior to the anus 
(1/3 body length; not shown on figure) 
and the dorsal finfold extends to mid- 
brain. Head pigment extends to the 
anterior margin of the eye (Fig. 7L). 
The dorsal half of the eye is pigmented. 
Most body pigment coalesces to three ar- 
eas: dorsally, on gut; a bar at 1/2 body 
length; and a bar at 3/4 body length. In 
the postanal bars, most pigment is along 
dorsal and ventral midlines; some pig- 
ment extends onto the lateral body. Pig- 
ment is scattered on the preanal body. 



Discussion 

Time from first hatch to 50% hatch was inversely 
related to temperature. Hatch times reflected the 
effects of temperature described by Yamagami 
(1988), who demonstrated that the hatching enzyme 
secreted by the embryo solubilizes the chorion more 
rapidly at higher temperatures. The first larvae to 
hatch were stage 20. Early hatching may have been 
an artifact of rearing conditions. However, hatching 
glands were present at this stage, which, with the 
appearance of eye pigment, may correspond to a 
level of development that would enable these larvae 
to survive. Early hatching may occur naturally with 
some frequency. Within batches of walleye pollock 
larvae from Puget Sound that had been incubated 
in the laboratory, larvae hatching early grew to an 
equivalent size as larvae hatching later (larvae 
hatched on day 1 were the same length at day 3 as 
larvae hatched on day 3). Those early hatched lar- 
vae also began to feed at the same time as larvae 
hatched later. 4 

Rate of development and time to 50% hatch were 
similar among studies of walleye pollock from the 
eastern North Pacific, specifically the Gulf of Alaska 
(Matarese, unpubl. data; Haynes and Ignell, 1983; 
and this study; Paul 5 ). From data on time (days) to 
50% hatch for all temperatures reported in all in- 
cubation studies (Fig. 10), incubation times of west- 
ern North Pacific walleye pollock are longer than 
eastern North Pacific walleye pollock. 

This finding appears to conflict with Haynes and 
Ignell's (1983) comparison with Yusa's (1954) study 
in which they report similar rates of development 

4 Olla, B. Mark O. Hatfield Marine Science Center, Oregon State 

University, 2030 Marine Science Drive, Newport, OR 97365- 

5297. Pers. commun. 18 August 1992. 
s Paul, A. J. University of Alaska Fairbanks, Institute of Marine 

Science, Seward Marine Center Lab, P.O. Box 730, Seward, AK 

99664. Unpubl. data. 



220 



Fishery Bulletin 92(2). 1994 



for eastern and western stocks. However, their com- 
parison was made with midpoints of stages calcu- 
lated from a regression model instead of observed 
midpoints. Also, Yusa (1954) reported a temperature 
range of 6— 7"C instead of a mean; our interpreta- 
tion of Haynes and Ignell's (1983) classification and 
calculation of Yusa's (1954) data suggests incubation 
temperatures were always above 6.5°C (see their 
Table 6 and our Table 4). Finally, Haynes and Ignell 
(1983) monitored midpoints of stages more closely 
than midpoint of hatch and did not specifically re- 
fer to 50% hatch. 6 We assumed the values reported 
as observed midpoints of hatch (their Table 7) were 
close to 50% hatch. Yusa's (1954) study could not be 
compared with ours with regard to time to 50% hatch. 

Time of hatch is often a result of how eggs are 
treated during incubation and may vary with differ- 
ent batches. 7 However, walleye pollock eggs from 
Japanese waters are larger than those from the Gulf 
of Alaska (mean=1.4— 1.6 mm and 1.3—1.4 mm, re- 
spectively; Bailey and Stehr, 1986). At similar tem- 
peratures, larger eggs take longer to develop (Pepin, 
1991). The difference in incubation time emphasizes 
the need to collect data from fish specific to the area 
of interest. This will reduce the 
sources of variation in develop- 
ment time for laboratory- 
reared eggs; failure to identify 
and improve these sources 
would compromise the useful- 
ness of models predicting 
egg age based on water tem- 
perature. 

Development is a continuous 
process. The sampling intervals 
and arbitrary designation of 
stage endpoints break develop- 
ment into subjective units. Us- 
ing the 21-stage scheme, we did 
not see a clear decrease in each 
stage duration with an increase 
in temperature. However, this 
will not affect the usefulness of 
our results. When stages are 
grouped to encompass a greater 
degree of morphological devel- 
opment, as in Haynes and 



Ignell (1983) and Picquelle and Megrey (1993), de- 
velopment time is inversely related to temperature. 
A greater number of stages within a group increases 
the accuracy of prediction of egg age. A large num- 
ber of stages also allows others greater flexibility in 
grouping those stages. 

Our regression model predicts temperature-spe- 
cific development time for purposes of computing 
rates of egg production and egg mortality. There is 
no biological basis upon which the regression is 
predicated because stages that are assigned to the 
eggs are arbitrary; stages are ordinal data that are 
based on morphological criteria without consider- 
ation for development time. An alternative method 
to estimate development time from temperature is 
to fit a separate regression for each stage. The dis- 
advantage of this alternative method is that many 
parameters are fitted with few data points. 

Two studies describing morphological develop- 
ment, Gorbunova (1954) and Yusa (1954), have been 
published. Gorbunova ( 1954) was not comparable to 
our study. We compared our descriptions of morpho- 
logical development with Yusa (1954). We assigned 
stages to descriptions of hourly morphological devel- 



6 Haynes, E., National Marine Fisher- 
ies Service, Auke Bay Laboratory, 
11305 Glacier Highway, Juneau, AK 
99801-8626. Pers. commun. April 
1991. 

7 Paul, A. J., University of Alaska 
Fairbanks, Institute of Marine Sci- 
ence, Box 730, Seward, AK 99664. 
Pers. commun. 17 March 1992. 



O 
-*- 
CO 



o 



CO 
Q 



30 



25 



20 



15 



10 



-&- Matarese 1 983 (see caption) 
—8- Paul 1 984 (see caption) 
— This study 
-B- Haynes and Ignell 1983 



— Hamaietal. 1974 
-A- Hamai et al. 1971 
O Nakatani and Maeda 1 984 




Western North Pacific 
ncubation Studies 



Eastern North Pacific 
Incubation Studies 



4 6 8 

Incubation temperature (°C) 



10 



12 



Figure 10 

Days to 50% hatch for Theragra chalcogramma eggs at various temperatures 
of incubation. (A. C. Matarese, unpubl. data, Alaska Fisheries Science Cen- 
ter, National Marine Fisheries Service, 7600 Sand Point Way N.E., Seattle, 
WA 98115. A. J. Paul, unpubl. data, University of Alaska Fairbanks, Insti- 
tute of Marine Science, Seward Marine Center Lab, P.O. Box 730, Seward, 
AK 99664.) 



Blood et al.: Embryonic development of Theragra chalcogramma 



221 



opment of walleye pollock embryos incubated at 6.0— 
7.0°C (Yusa, 1954) for comparison with morphologi- 
cal characteristics of eggs reared at 5.7°C in this 
study We used hallmarks of each stage (e.g. num- 
ber of cells, germ ring advancement, number of 
myomeres, tail growth around yolk) to distribute 
Yusa's (1954) descriptions into 21 stages. Yusa's 
(1954) descriptions were similar to ours up to stage 
11. Beginning with stage 11, Yusa (1954) described 
the development of some structures occurring one 
or more stages earlier than this study: myomeres 
and nares were sighted one stage earlier; brain dif- 
ferentiation and eye lenses, two stages earlier; the 
heart, three stages earlier; and the otic capsules, five 
stages earlier (Table 5). Otoliths sighted by Yusa 
( 1954) were not visible in our specimens. Conversely, 
eye pigment was observed in our study one stage 
earlier than that observed by Yusa (1954). Other 
structures appeared at the same stage in each study: 
optic vesicles, Kupffer's vesicle, liver, gut, and pec- 
toral-fin anlagen. Also, after stage 13, similar num- 
bers of myomeres were visible at like stages in both 
studies as was the beating of the heart. 

Differences between the two studies may be the 
result of egg condition when examined: Yusa (1954) 
described live eggs, whereas most of our descriptions 
were of preserved eggs. Formalin preservation may 
obscure myomeres or destroy structures such as 
embryonic otoliths (McMahon and Tash, 1979). 
Stockard's solution darkens embryonic tissue and 
obscures fine details. Also, morphological develop- 
ment may differ between western and eastern North 



Pacific walleye pollock, further emphasizing the 
need to restrict data collection to specific areas of 
interest to increase accuracy of interpretation. 



Acknowledgments 

We thank the following people whose combined ef- 
forts helped us accomplish our research and produce 
this paper: William Rugen assisted with shipboard 
experiments; Kevin Bailey, Gail Theilacker, and 
Steve Porter helped us interpret the morphology of 
late-stage eggs and yolk-sac larvae; Trish Brown 
provided statistical analyses; Morgan Busby photo- 
graphed the eggs; and Beverly Vinter illustrated 
eggs and helped interpret many morphological struc- 
tures. We thank Art Kendall, A. J. Paul, Kevin 
Bailey, Susan Picquelle, and Bori 011a for prelimi- 
nary reviews of the manuscript. Gail Theilacker and 
Richard Brodeur helped refine later versions. We 
also thank the members of FOCI who assisted with 
field collections. 



Literature cited 

Alderdice, D. F. 

1988. Osmotic and ionic regulation in teleost eggs 
and larvae. In W. S. Hoar and D. J. Randall 
(eds.), Fish physiology, Vol. XI, Part A, p. 163-251. 
Academic Press, Inc., San Diego. 





Table 


5 


Descri 
(1954) 


ptions of morphological development of Theragra c 
and this study. 


halcogramma embryos at comparable stages by Yusa 


Stage 


Yusa 
(6.0-7.CTC) 


This study 
(5.7"C) 


11 


medullary plate and optic vesicles visible 


optic vesicles visible 


12 


5-7 myomeres; 3 sections of brain visible 


myomeres begin to differentiate 


13 


9-13 myomeres; heart, otic capsules, otoliths, 
eye lenses, and Kupffer's vesicle visible 


7-12 myomeres; Kupffer's vesicle visible 


14 


16-17 myomeres; nares and pigment along 
dorsum visible 


14-16 myomeres; pigment along dorsum visible; mid- 
and hindbrain differentiation 


15 


18-30 myomeres; liver, gut, and pectoral anlagen 
visible; 3 sections of brain formed 


20-25 myomeres; eye lens, nares, pectoral anlagen, 
liver, and gut visible 


16 


35 myomeres 


24-36 myomeres; heart visible; 3 sections of brain formed 


17 


37 myomeres; heart beating 


27-36 myomeres; heart beating 


18 


40 myomeres 


36-41 myomeres; otic capsules visible 


19 




44-48 myomeres 


20 




48-49 myomeres; eye pigment appears 


21 


eye pigment appears 





222 



Fishery Bulletin 92(2). 1994 



Bailey, K. M., and C. L. Stehr. 

1986. Laboratory studies on the early life history 
of the walleye pollock, Theragra chalcogramma 
(Pallas). J. Exp. Mar. Biol. Ecol. 99:233-246. 

Blaxter, J. H. S. 

1969. Development: eggs and larvae. In W. S. 
Hoar and D. J. Randall (eds.), Fish physiology, Vol. 
Ill, p. 177-252. Academic Press, New York. 

Gorbunova, N. N. 

1954. Reproduction and development of the wall- 
eye pollock, Theragra chalcogramma (Pallas). Tr. 
Inst. Okeanol. Akad. Nauk. SSSR 11:132-195. (In 
Russian, transl. by S. Pearson, 1972, Natl. Mar. 
Mammal Lab., NMFS, 7600 Sand Point Way N.E., 
Seattle, WA 98115-0070.) 

Hamai, I., K. Kyushin, and T. Kinoshita. 

1971. Effect of temperature on the body form and 
mortality in the development and early larval 
stages of the Alaska pollock, Theragra chalco- 
gramma (Pallas). Bull. Fac. Fish. Hokkaido Univ. 
22:11-29. 

Hamai, I., K. Kyushin, and T. Kinoshita. 

1974. On the early larval growth, survival, and 
variation of body form in the walleye pollock, 
Theragra chalcogramma (Pallas), in rearing ex- 
periment feeding the different diets. Bull. Fac. 
Fish. Hokkaido Univ. 25:20-35. 

Haynes, E. B., and S. E. Ignell. 

1983. Effect of temperature on rate of embryonic 
development of walleye pollock, Theragra 
chalcogramma. Fish. Bull. 81:890-894. 

Kendall, A. W., Jr., and S. Kim. 

1989. Buoyancy of walleye pollock (Theragra 
chalcogramma) eggs in relation to water proper- 
ties and movement in Shelikof Strait, Gulf of 
Alaska. In R. J. Beamish and G. A. McFarlane 
(eds.), Effects of ocean variability on recruitment 
and an evaluation of parameters used in stock 
assessment models, p. 169-180. Can. Spec. Publ. 
Fish. Aquat. Sci. 108. 

Kendall, A. W., Jr., and S. J. Picquelle. 

1990. Egg and larval distributions of walleye pol- 
lock Theragra chalcogramma in Shelikof Strait, 
Gulf of Alaska. Fish. Bull. 88:133-154. 

Markle, D. F., and K. G. Waiwood. 

1985. Fertilization failure in gadids: aspects of its 
measurement. J. Northw. Atl. Fish. Sci. 6:87-93. 
Matarese, A. C., A. W. Kendall Jr., D. M. Blood, 
and B. M. Vinter. 

1989. Laboratory guide to early life history stages 
of Northeast Pacific fishes. U.S. Dep. Commer., 
NOAA Tech. Rep. NMFS 80, 652 p. 
McMahon, T. E., and J. C. Tash. 

1979. Effects of formalin (buffered and unbuffered) 
and hydrochloric acid on fish otoliths. Copeia 
1979:155-156. 



Megrey, B. A. 

1991. Population dynamics and management of 
walleye pollock (Theragra chalcogramma) in the 
Gulf of Alaska, 1976-1986. Fish. Res. 11:321- 
354. 

Nakatani, T., and T. Maeda. 

1984. Thermal effect on the development of wall- 
eye pollock eggs and their upward speed to the 
surface. Bull. Jpn. Soc. Sci. Fish. 50:937-942. 

Naplin, N. A., and C. L. Obenchain. 

1980. A description of eggs and larvae of the snake 
eel, Pisodonophis cruentifer (Ophichthidae). Bull. 
Mar. Sci. 30:413-423. 
Olla, B. L., and M. W. Davis. 

1993. The influence of light on egg buoyancy and 
hatching rate of the walleye pollock, Theragra 
chalcogramma (Pallas). J. Fish. Biol. 42:693-698. 
Pepin, P. 

1991. Effect of temperature and size on develop- 
ment, mortality, and survival rates of the pelagic 
early life history stages of marine fish. Can. J. 
Fish. Aquat. Sci. 48:503-518. 
Picquelle, S. J., and B. A. Megrey. 

1993. A preliminary spawning biomass estimate of 
walleye pollock, Theragra chalcogramma, in the 
Shelikof Strait, Alaska, based on the annual egg 
production method. Bull. Mar. Sci. 53:728-749. 
Reed, R. K., and J. D. Schumacher. 

1989. Transport and physical properties in central 
Shelikof Strait, Alaska. Cont. Shelf Res. 9:261-268. 
SAS Institute, Inc. 

1985. SAS® user's guide: basics, version-5 edition. 
SAS Institute, Inc., Cary, NC, 1290 p. 

Schumacher, J. D., and A. W. Kendall Jr. 

1991. Some interactions between young walleye 
pollock and their environment in the western Gulf 
of Alaska. Calif. Coop. Oceanic Fish. Invest. Rep. 
32:22-40. 
Trinkaus, J. P. 

1951. A study of the mechanism of epiboly in the 
egg of Fundulus heteroclitus. J. Exp. Zool. 
118:269-319. 
Velsen, F. P. J. 

1980. Embryonic development in eggs of sockeye 
salmon, Oncorhynchus nerka. Can. Spec. Pub. 
Fish. Aquat. Sci. 49, 19 p. 
Yamagami, K. 

1988. Mechanisms of hatching in fish. In W. S. Hoar 
and D. J. Randall (eds.), Fish physiology, Vol. XI, Part 
A, p. 447^99. Academic Press, Inc., San Diego. 

Yusa, T. 

1954. On the normal development of the fish, 
Theragra chalcogramma (Pallas), Alaska 
pollock. Bull. Hokkaido Reg. Fish. Res. Lab. 
10:1-15. 



Abstract. — The diel vertical 
distribution patterns of several 
abundant ichthyoplankton taxa 
were examined from depth-strati- 
fied tows off Kodiak Island in the 
western Gulf of Alaska during 
1986 and 1987. Most larvae were 
found in the upper 45 m of the 
water column throughout the diel 
period but were concentrated in 
higher densities near the surface 
(0-15 m) in daylight hours and at 
greater depths at night. Four of 
the five dominant taxa examined 
in detail showed significantly 
greater weighted mean depths 
during the night than during the 
day. This pattern was the opposite 
to that previously reported for the 
numerically dominant taxa (Ther- 
agra chalcogramma) in this area. 
Since there was no clear relation 
between the diel vertical distribu- 
tion of these taxa and the vertical 
distribution of water temperature 
and density or copepod nauplii 
prey, we hypothesize that this re- 
verse migration is either a strat- 
egy to minimize spatial overlap 
with predators that follow a nor- 
mal diel migration pattern or one 
to optimize light levels for feeding. 



Diel vertical distribution of 
ichthyoplankton in the northern 
Gulf of Alaska* 

Richard D. Brodeur 
William C. Rugen 

Alaska Fisheries Science Center, National Marine Fisheries Service, NOAA 
7600 Sand Point Way NE, Seattle, WA 98 1 1 5 



Planktonic eggs and larvae of ma- 
rine fishes exist in three dimen- 
sions in the open ocean. Unfortu- 
nately, traditional ichthyoplankton 
surveys, which use non-closing 
sampling gear, provide information 
only on two dimensions, integrat- 
ing the vertical indirectly into the 
horizontal dimensions. It is well 
known that vertical current shear 
can be substantial over short dis- 
tances and that light, temperature, 
hydrostatic pressure and food show 
much stronger gradients in the ver- 
tical relative to the horizontal di- 
mensions in the water column 
(Laprise and Dodson, 1993). Thus, 
a larva can often change not only 
its geographic position, but also its 
immediate environment by altering 
its vertical position in the water 
column. 

Diel vertical migration is well 
documented for larval, juvenile, 
and adult life history stages of ma- 
rine fishes (see review by Neilson 
and Perry, 1990). The adaptive sig- 
nificance of these migrations is 
presently in dispute, but it has 
been attributed to position mainte- 
nance, bioenergetic optimization, 
thermoregulation, and predator 
avoidance (Kerfoot, 1985; Lampert, 
1989). In addition, the degree of 
migration and amplitude of depths 
over which a species vertically mi- 
grates often changes during ontoge- 
netic development (Brewer and 



Kleppel, 1986; de Lafontaine and 
Gascon, 1989). 

Knowledge of vertical distribu- 
tion patterns of marine fish larvae 
is crucial not only in understand- 
ing ecological processes but also 
has practical implications in the 
assessment of abundance. Sam- 
pling just the upper depths of a 
species range can lead to substan- 
tial underestimates of abundance, 
whereas sampling the entire water 
column for surface-dwelling taxa 
may waste limited ship time. De- 
spite the importance of the larval 
phase in recruitment of marine 
fishes, relatively little is known 
about larval vertical distribution 
patterns off the continental shelf in 
the North Pacific Ocean. With the 
exception of walleye pollock, Ther- 
agra chalcogramma, which has 
been fairly well studied through 
much of its geographic range 
(Kamba, 1977; Kendall et al., 1987; 
Pritchett and Haldorson, 1989; 
Kendall et al. 1 ), the only compre- 
hensive studies on vertical distri- 
bution of coastal ichthyoplankton 
in the northeast Pacific Ocean are 
from the California Current region 
(Ahlstrom, 1959; Boehlert et al., 
1985; Brewer and Kleppel, 1986; 
Lenarz et al., 1991). This paper 
presents information on the verti- 
cal distribution of five abundant 
ichthyoplankton taxa (other than 
walleye pollock) collected in the 



Manuscript accepted 18 October 1993 
Fishery Bulletin 92:223-235 (1994) 



"Contribution No. 0181 of the Fisheries Oceanography Coordinated Investigations. 



223 



224 



Fishery Bulletin 92|2), 1994 



coastal waters of Alaska during 
spring and examines diel differences 
in these patterns in relation to en- 
vironmental and biotic factors. 



Materials and methods 

Samples examined were collected 
from two cruises of the NOAA ship 
Miller Freeman in the area south- 
west of Kodiak Island in the north- 
ern Gulf of Alaska (Fig. 1). During 
May 1986 and 1987, 22 depth-strati- 
fied tows were made with a 1-m 2 
Multiple Opening/Closing Net and 
Environmental Sensing System 
(MOCNESS) (Wiebe et al., 1976) 
equipped with 153-um mesh. The 
net was towed obliquely and nets 
were opened sequentially at the de- 
sired depth strata. The primary pur- 
pose of the sampling was to collect 
information on the vertical distribu- 
tion of walleye pollock larvae, which 
are generally found in the upper 50 m 
(Kendall et al. 1 ), and their prey. 
Therefore, the emphasis during the 
sampling was on the upper part of 
the water column. The nets sampled 
the following nominal depths: 0-15, 
15-30, 30-45, 45-60, 60-80, 80-100, 
and >100 m. Maximum sampling 
depth varied (range 150-252 m) depending on the 
depth of the water column at a particular station. 
There were eight depth strata sampled at most sta- 
tions but the cutoff depth between the seventh and 
eighth net was variable. Therefore, we pooled the 
catches from these two nets into a single depth stra- 
tum (>100 m) for analysis. The actual sampling 
depths are given in Table 1. More complete station 
and catch information is given in Siefert et al. 2,3 





-i 1 1 1 1 " 1- 




cX S j 


/ { Kodiak 
i y Island 






A) / + 


4 


/ FJ 


-57 00 




<^y <-, 


;• c 






\ / 


-£> 






+5 > 








C^> +9 ' 

Sutwik 1. I , 


/?Ck. 




r ~ ' 


(/ Trinity Is. 






+7 ' / 

i f 
















Semidi Is. ^ / 








0-6 > 

N + - " Chirikof 1. 




-56 00 




;- 4 


/ 






1 






V 


/ 






' , 


s 






* 




00 


TL , . 1 . 

157 00W 156 00 


1 ' (■ 

1 55 00 1 54 


Figure 1 




Location of MOCNESS sampling series in Shelikof Strait used to de- 


termine vertical distribution of larvae in 


1986 and 1987. 



1 Kendall, A. W., Jr., L. S. Incze, P. B. Ortner, S. R. Cummings, 
and P. K. Brown. In review. The vertical distribution of eggs 
and larvae of walleye pollock {Theragra chalcogramma i in 
Shelikof Strait, Gulf of Alaska. Submitted to Fish. Bull. 

2 Siefert, D. L. W., L. S. Incze, and P. B. Ortner. 1988. Vertical 
distribution of zooplankton, including ichthyoplankton, in 
Shelikof Strait, Alaska: data from Fisheries Oceanography 
Coordinated Investigations (FOCI) cruise in May 1986. 
NWAFC Processed Rep. 88-28, 232 p. 

1 Siefert, D. L. W., L. S. Incze, and P. B. Ortner. 1990. Vertical 
distribution of zooplankton, including ichthyoplankton, in 
Shelikof Strait, Alaska: data from Fisheries Oceanography 
Coordinated Investigations (FOCI) cruise in May 1987. 
NWAFC Processed Rep. 90-05, 129 p. 



The 22 tows were grouped into five collection se- 
ries (Table 1) based upon date and location of sam- 
pling (see Kendall et al. 1 ) and included two complete 
diel series. The first diel series (Series 4) attempted 
to sample the same body of water over a four day 
period during 1986 by following a radar-tracked 
drifter drogued at 35 m (Incze et al., 1990). The 
second diel series (Series 9) sampled the same loca- 
tion on three successive days during 1987. Other 
collections (Series 5, 6, and 7) were taken at vari- 
ous times of the day but in the same general area 
as these two series (Fig. 1, Table 1). 

Retrieved nets were thoroughly washed and con- 
tents were preserved in 5% buffered formalin. 
Samples were sorted to the lowest possible taxon 
and life history stage at the Polish Sorting Center 
in Szczecin, Poland. The volume filtered was esti- 
mated from a mechanical flowmeter mounted on the 
MOCNESS frame and abundances were converted to 
number per 1000 m 3 . Up to 50 preserved larvae of each 
taxon from each net were measured to the nearest 0. 1 
mm standard length. Net depth, temperature, and 



Brodeur and Rugen: Vertical distribution of ichthyoplankton in the northern Gulf of Alaska 



225 

















Table 1 




























Station 


and tow data for collection subset 


used in the diel series ordered by 


time 


of day. 


































Net depths (m) 




















Bottom 


Local 


Time 


























































Series 


Tow 


Year 


Date 


depth (m) 


time 


period 




1 


2 


3 


4 


5 




6 


7 


4 


5 


1986 


10 May 


293 


0745 


Dawn 


2- 


-15 


15- 


-30 


29- 


45 


46- 


-58 


59 


-78 


79- 


-99 


101- 


-229 


4 


1 


1986 


8 


May 


220 


0746 


Dawn 


1- 


15 


15- 


-31 


35- 


45 


45- 


-61 


61- 


-80 


80- 


-100 


101- 


-200 


9 


4 


1987 


23 


May 


201 


0747 


Dawn 


0- 


15 


15- 


-30 


30- 


-45 


45- 


-60 


60- 


-80 


80- 


-100 


100- 


-150 


9 


8 


1987 


24 


May 


190 


0800 


Dawn 


0- 


15 


15 


30 


30 


-45 


45 


■60 


60- 


-80 


80- 


-100 


100- 


-150 


6 


2 


1986 


L5 


May 


223 


0940 


Day 


2- 


-14 


15- 


29 


30 


44 


45 


-60 


61 


-80 


80- 


-100 


100- 


-175 


5 


1 


1986 


13 


May 


210 


1010 


Day 


2- 


15 


16 


-30 


30- 


-45 


45- 


-61 


61 


-80 


80 


-100 


101- 


-152 


4 


6 


1986 


111 


May 


296 


1341 


Day 


2- 


14 






30- 


45 










77- 


-99 


99- 


-214 


5 


2 


1986 


13 


May 


210 


1351 


Day 


2- 


-14 


15 


-29 


30- 


4 4 


45- 


-59 


59- 


-78 


80- 


-99 


100- 


-176 


4 


2 


1986 


8 


May 


227 


1356 


Day 


2- 


-14 


15- 


-30 


30- 


-47 










79- 


-99 


99- 


-200 


9 


5 


1987 


23 


May 


179 


1422 


Day 


0- 


15 


15- 


-30 


30- 


-45 


45 


-60 


60- 


80 


80- 


-100 


100- 


-150 


9 


9 


1987 


24 


May 


191) 


1543 


Day 


0- 


15 


15 


-30 


30- 


-45 


45 


-60 


60 


-80 


80- 


-100 


100- 


-150 


7 


2 


1986 


18 


May 


123 


1911 


Dusk 


2 


15 


15 


30 


30 


45 


45 


-59 


60 


-79 


so 


-100 






4 


3 


1986 


9 


May 


235 


2006 


Dusk 


2- 


-13 


13- 


28 


29- 


-45 


46 


59 


60- 


-79 






100- 


-200 


4 


7 


1986 


11 


May 


293 


2011 


Dusk 


3- 


-14 


14 


-30 


31- 


44 


43- 


-59 


60- 


-78 


78 


-97 


98- 


-252 


9 


6 


1987 


24 


May 


179 


2107 


Dusk 


0- 


-15 


15 


-30 


30- 


-45 


45 


-60 


60 


-80 


80- 


-100 


100- 


-150 


9 


Hi 


1987 


25 


May 


196 


2122 


Dusk 


0- 


-15 


15- 


-30 


30- 


-45 


45 


-60 


60 


-80 


80- 


-100 


100- 


-150 


5 


3 


1986 


14 


May 


210 


2200 


Night 


2- 


-14 


14- 


-30 


30 


45 


46 


-60 


60 


-80 


81- 


-101 


100- 


-163 


7 


1 


1986 


17 May 


126 


2416 


Night 


1 


15 


16 


30 


31- 


45 


45- 


-59 


60 


-80 


80 


-99 






4 


4 


1986 


9 May 


242 


0135 


Night 


2- 


-15 


15- 


30 


30- 


-58 






59- 


-80 


80- 


-100 


100- 


-202 


9 


11 


1987 


25 May 


198 


0218 


Night 


0- 


-15 


15 


30 


30- 


45 


45 


-60 


60 


-80 


80- 


-100 


100- 


-150 


9 


7 


1987 


24 


May 


195 


0219 


Night 


0- 


15 


15 


30 


30- 


45 


45- 


60 


60- 


-80 


80- 


-100 


100- 


-150 


6 


1 


1986 


15 


May 


229 


0353 


Night 


2- 


-15 


15- 


29 


30 


-44 


45- 


-60 


60 


80 


80 


-100 


100- 


-172 



salinity were measured continuously in real time dur- 
ing the tow and stored for later analysis. 

To examine diel variations in density and size of 
larvae with depth, collections from the 22 tows were 
grouped into one of four time periods (hours): dawn 
(0530-0830), day (0830-1830), dusk (1830-2130), 
and night (2130-0530). Diel-depth variation in den- 
sity of eggs and larvae at each depth was examined 
by using a two-way ANOVA on log-transformed data. 
The log (X+l) transformation was used to achieve 
homogeneous variances (Bartlett's Test, all P>0.05). 
In addition, a weighted mean depth of occurrence 
of eggs or larvae of the dominant species for each 
time interval was calculated as follows: 



IIXa,, 



A- 






m 



where n ( = number of tows in time interval t , 

N = number of larvae in net j in tow i in 



'.it 



time interval t, 



D = midpoint depth of net j in tow i in time 



interval t with a variance equal to 



Var(D t ) = 



( "' ] 


w=i ; 



2>2(Z) a -A> 2 , 



K-i) 



& 



where N (/ = number of larvae in tow i in time 

interval t. 
Differences in the weighted mean depths over the 
four time periods were tested with ANOVA, and 
Tukey multiple-comparison tests were conducted 
when significant differences were observed. 
Untransformed larval lengths for the three most 
abundant species were entered as dependent vari- 
ables in two-way ANOVAs, with time of day and 
depth as factors. 



Results 

Species composition 

Eggs and larvae of species other than walleye pol- 
lock were found in 134 of the 145 samples collected 



226 



Fishery Bulletin 92(2). 1994 



during the 1986 and 1987 cruises. Flathead sole 
(Hippoglossoides elassodon) eggs were the only pe- 
lagic eggs other than walleye pollock collected and 
were found in 28.4% of the samples. This species 
had a mean density of 62.99 eggs/1000 m 3 
(SD=179.66) and comprised 74.9% of the total egg 
abundance in the 22 tows. 

A total of 33 larval taxa were identified but only 
a few taxa occurred in more than 10% of the samples 
(Table 2). Larvae other than walleye pollock oc- 
curred in 92.4% of the collections but made up only 
26.3% of the overall total abundance of larvae (to- 
tal mean density=143.61 larvae/1000 m 3 ; 
SD=257.03). Larvae of three taxa (H. elassodon , Am- 
modytes hexapterus, and Bathymaster spp. 4 ) were 



found at sufficient densities to enable examination 
of their vertical abundance and length distribution 
patterns in detail for the four time periods. Two 
other species (Gadus macrocephalus and Pleuro- 
nectes bilineatus) were found at relatively high den- 
sities during day and night but at low densities 
during the twilight periods; hence, these taxa were 
examined only for day-night differences. 

Vertical distribution 

The distribution of//, elassodon eggs showed little 
variation in weighted mean depth by time of day 
(F=3.10, P>0.05); the highest abundances were 



4 Larvae of three Bathymaster species known to occur in the 
study area are presently not identifiable to species. Based on 



the abundance and distribution patterns of the adults, most of 
the larvae present in our collections are probably B. signatus. 
(A. Matarese, Alaska Fisheries Science Center, Seattle, WA 
98115. Pers. commun. 1992). 





Table 2 








Summary of all larvae 


including walleye pollock collected 


in the 1986-87 


vertical distribution study. 






Percent 


Mean 


Length 






occurrence 


density 


range 


Scientific name 


Common name 


(n=145) 


(no./1000m :i ) 


(mm) 


Osmerus mordax 


rainbow smelt 


0.69 


0.25 


21 


Leuroglossus schmidti 


northern smoothtongue 


0.69 


0.02 


9-15 


Stenobraehius leueopsarus 


northern lampfish 


4.14 


3.05 


4-7 


Protomyctophum thompsoni 


bigeye lanternfish 


0.69 


0.04 


10 


Myctophidae 


unidentified myctophid 


0.69 


0.06 


3 


Gadus macrocephalus 


Pacific cod 


15.86 


27.51 


3-11 


Theragra chalcogramma 


walleye pollock 


93.79 


402.71 


3-8 


Gadidae 


unidentified gadid 


2.76 


0.36 


4 


Sebastes spp. 


unidentified rockfish 


1.38 


0.17 


4-5 


Hexagrammos decagrammus 


kelp greenling 


1.38 


0.05 


8-11 


Dasycottus setiger 


spinyhead sculpin 


0.69 


0.07 


8 


Gymnocanthus spp. 


unidentified sculpin 


0.69 


0.07 


7-8 


Hemilepidotus hemilepidotus 


red Irish lord 


1.38 


0.13 


11-13 


Icelinus spp. 


unidentified sculpin 


7.59 


0.65 


4-5 


Malacocottus zonurus 


darkfin sculpin 


0.69 


0.05 


6-7 


Radulinus asprellus 


slim sculpin 


1.38 


0.10 


4-5 


Ruscarius meanyi 


Puget Sound sculpin 


0.69 


0.04 


4 


Agonidae 


unidentified poacher 


10.34 


0.84 


5-10 


Nectoliparis pelagicus 


tadpole sculpin 


0.69 


0.07 


4-8 


Cyclopteridae 


unidentified snailfish 


2.07 


0.19 


4-5 


Bathymaster spp. 


unidentified ronquil 


13.10 


30.67 


4-7 


Anoplarchus spp. 


unidentified prickleback 


2.07 


0.26 


8-10 


Lumpenella longirostris 


longsnout prickleback 


1.38 


0.05 


10-11 


Lumpenus maculatus 


daubed shanny 


6.21 


0.64 


12-23 


Poroclinus rothrocki 


whitebarred prickleback 


4.83 


0.97 


10-15 


Cryptacanthodes aleutensis 


dwarf wrymouth 


1.38 


0.19 


14 


Pholis spp. 


unidentified gunnel 


0.69 


0.04 


13-17 


Zaprora silenus 


prowfish 


3.45 


0.40 


12-14 


Ammodytes hexapterus 


Pacific sand lance 


40.69 


12.76 


6-19 


Hippoglossoides elassodon 


flathead sole 


17.93 


59.81 


4-19 


Pleuronectes bilineatus 


rock sole 


13.10 


3.71 


3-10 


Pleuronectes vetulus 


English sole 


0.69 


0.13 


8 


Psettichthys melanostictus 


sand sole 


0.69 


0.14 


4-5 


Pleuronectidae 


unidentified flounder 


0.69 


0.10 


4 



Brodeur and Rugen: Vertical distribution of ichthyoplankton in the northern Gulf of Alaska 



227 



found in the surface layer (0-15 m) during all four 
time periods (Fig. 2). Although there were signifi- 
cant (P=0.005) differences in density by depth 
strata, neither the diel density differences alone 
(P=0.838) nor the interaction between time and 
depth (P=0.996) was significant. 

The majority of larvae, excluding pollock larvae, 
from all collections combined were collected from the 
upper three depth strata (Fig. 3). The maximum 
density overall occurred at the second depth stra- 
tum ( 15-30 m), below which larval density declined 
with depth. However, this overall vertical distribu- 
tion pattern was apparently confounded by higher 
larval densities found during the night when the 
larvae were mainly caught in the 15-30 m stratum; 



Dawn 



Day 



ro 



CD 

c 



Q. 

<D 
O 









0-15 - 


















15-30  












30-45 - 
45-60 - 
60-80 
80-100 
> 100 - 









0-16 
15-30 



30-45 
45-60 
60-80 
80-100 
> 100- 



} 



100 200 300 
No/1000 m 3 



100 200 300 400 
No/1000 m 3 



Dusk 



Night 





-15 
■30 
•45 



























15 






30 






45 


-60 - 


I 


60 


-80 - 


I 


80- 


100 
100 - 

































15-30 














30-45 


} 




45-60 




60-80 


^ 


80-100 


) 


> 100 





100 200 300 400 
NO./1000 m' 



100 200 300 400 
No/1000 m 3 



Figure 2 

Diel vertical distribution of Hippoglossoides elassodon eggs. Bars are 
mean abundances per 1000 m 3 at each depth interval and error bars 
are ± one standard deviation about the mean abundance. 



during the other three time periods the highest den- 
sities were in surface waters (Fig. 4). The weighted 
mean depth of larvae overall was significantly 
(P<0.05) greater at night than during the other 
three time periods (Table 3) and the interaction 
between time and depth was marginally significant 
(P=0.05; Table 4), suggesting that there were diel 
differences in overall larval depth distribution. 

Four of the five most abundant larval taxa showed 
the greatest weighted mean depths (Table 3) and the 
lowest surface densities (Fig. 4) at night. This gen- 
eral pattern was also evident in the two time peri- 
ods examined for the fifth species, G. macro- 
cephalus, but the diel differences were not signifi- 
cant (Table 3). Only A. hexapterus and G. macro- 
cephalus showed significant diel dif- 
ferences in larval density, with high- 
est densities occurring at night 
(Table 4). None of the dominant 
taxa, however, showed a significant 
interaction between time and depth 
strata. 

Length distributions 

The distribution of larval lengths by 
time of day and depth showed no 
consistent pattern among the three 
most abundant species (Fig. 5). Al- 
though time and time-depth interac- 
tions were significant (all P<0.03) 
factors in explaining the variation in 
mean length of H. elassodon and 
Bathymaster spp., none of the fac- 
tors was significant for A. hexap- 
terus. Examining only the strata 
where more than two lengths were 
available, we found that the small- 
est larvae of both Bathymaster spp. 
and A. hexapterus were caught in 
the surface stratum at night but in 
deeper strata during daylight hours 
(Fig. 5). However, H. elassodon 
showed an increase in mean length 
with depth during daylight hours 
and the reverse pattern at night 
(Fig. 5). Hippoglossoides elassodon 
was the only taxon to show a signifi- 
cant difference in length distribu- 
tions between night and day collec- 
tions (Kolmogorov-Smirnov Test; 
Z=3.881; P=0.001). Although the 
lack of larger larvae in daytime col- 
lections might suggest some daytime 
gear avoidance by this species 



228 



Fishery Bulletin 92(2). 1994 



(Fig. 6), there were few small larvae caught at night, 
which cannot be explained by gear avoidance. Since 
the majority (>95%) of these lengths were from lar- 











0-15 




I 


I 




r 


I 












15-30 






I 




i 










E 

— 30-45 

N 








I 






n 






| 45-60 


3 


.c 




cj 60-80 - 
a 


80-100 


> 100 





100 200 300 400 500 600 
NO./1000 m J 

Figure 3 

Vertical distribution of all larvae ex- 
cluding walleye pollock (Theragra 
chalcogramma) combined over all time 
periods. Bars are mean abundances 
per 1000 m 3 at each depth interval and 
error bars are ± one standard deviation 
about the mean abundance. 



vae collected from the same location (Series 9), sam- 
pling variability cannot be invoked as an explana- 
tion for this pattern. 



Discussion 

Our results indicate that the vast majority (>99%) 
of pelagic eggs and larvae (excluding walleye pol- 
lock) are distributed in the upper 100 m of the wa- 
ter column during the spring months. Therefore, 
sampling to this depth should be sufficient to char- 
acterize the horizontal distribution patterns of these 
species. Of the common taxa we examined, all but 
H. elassodon have demersal eggs (Matarese et al., 
1989). The transit time to surface waters following 
hatching from demersal eggs is apparently of such 
short duration that even newly hatched larvae were 
rarely collected below 100 m. However, this does not 
appear to be the case for walleye pollock, which 
spawn at depths greater than 200 m in Shelikof 
Strait, with mean depths of eggs and yolk-sac lar- 
vae generally greater than 100 m (Kendall and Kim, 
1989; Kendall et al. 1 ). 

The diel vertical distribution pattern that we ob- 
served for several taxa is not the pattern typically 
observed for most ichthyoplankton and for zooplank- 
ton in general. The more common pattern, termed 
a 'Type F migration (Neilson and Perry, 1990), in- 
volves a nocturnal ascent into surface waters and 
is undertaken by larvae of a diversity offish species. 







Table 


3 






Weighted mean depths (m) and standard deviations of the mean depths (in parentheses) for each taxon and 
for all larvae excluding walleye pollock by time of day and overall depth for all times combined. Also given 
are the results of the ANOVAs testing for diel differences in weighted mean depth and the significant 
(P< 0.05) Tukey multiple-comparison tests between time periods. 


Dawn Day 


Dusk 


Night 


Overall 


F-value 


Tukey test 


All Larvae (excluding walleye pollock) 

16.59(2.72) 17.46(1.52) 15.45(2.25) 


25.74 (1.52) 


21.75 (1.87) 


33. 17**' 


Night>Day=Dawn=Dusk 


Hippoglossoides elassodon 

14.82(0.63) 16.94(2.73) 


10.80 (0.42) 


20.10 (0.05) 


18.06 (1.33) 


3] 89 


Nigh t > Day = Da wn> Dusk 


Ammodytes hexapterus 

31.21(11.45) 27.67 (4.59) 


22.67 (2.38) 


37.51 (4.45) 


32.85 (3.39) 


6 05" ' 


Night>Dusk = Day 


Bathymaster spp. 

8.21 (0.11) 11.25 (0.08) 


11.28 (1.08) 


37.95 i2.84) 


18.12 (6.05) 


441.48*** 


Nigh t>Dusk= Day > Dawn 


Pleuronectes bilineatus 

19.75 (1.83) 




30.73 (1.63) 


25.47 (4.64) 


128.36*** 


Night>Day 


Gadus macrocephalus 

20.36(10.35) 





24.92 (0.12) 


22.12 (6.56) 


1.14 n.s. 




P<0.001, 

" P<0.01; 
n.s. P>0.05. 



Brodeur and Rugen: Vertical distribution of ichthyoplankton in the northern Gulf of Alaska 



229 



However, the reverse pattern ('Type II' migration), 
although less frequently documented, has been ob- 
served for larvae of several fish species, including 
many of the taxa we examined. For example, 
Boehlert et al. (1985) observed larval G. 
macrocephalus at lower depths at night than dur- 
ing the day off the Oregon coast. Walline 5 found that 
Bathymaster spp. in the Bering Sea generally mi- 
grated downward at night. Larvae of A. hexapterus 
collected in bays around Kodiak Island were concen- 
trated from 10 to 30 m during the day but were 
found at lower depths at night (Rogers et al. 6 ), and 
larvae of a congener (A. personatus) collected off Ja- 
pan also exhibited reverse migration (Yamashita et 
al., 1985). Rogers et al. 6 and Pritchett and Haldor- 





Table 4 








Results of two-way ANOVAs 


testing for differences 


in density of larvae 


by depth and time of day. 












Sum of 


Mean 






Source of variation df 


squares 


square 


F-ratio 


P-value 


All larvae (excluding walley 


B pollock) 








Time 3 


14.60 


4.86 


9.85 


0.00 


Depth 6 


51.63 


8.61 


17.40 


0.00 


Time x depth 18 


14.11 


0.78 


1.58 


0.05 


Error 4868 


2406.73 


0.49 






Hippoglossoides elassodon 










Time 3 


4.97 


1.66 


0.48 


0.69 


Depth 6 


93.59 


15.60 


4.54 


0.00 


Time x depth 18 


15.49 


0.86 


0.25 


0.99 


Error 116 


398.59 


3.44 






Ammodytes hexapterus 










Time 3 


55.08 


18.36 


11.70 


0.00 


Depth 6 


94.13 


15.69 


9.99 


0.00 


Time x depth 18 


34.27 


1.90 


1.21 


0.26 


Error 116 


182.03 


1.57 






Bathymaster spp. 










Time 3 


8.84 


2.95 


1.24 


0.30 


Depth 6 


44.33 


7.39 


3.10 


0.01 


Time x depth 18 


21.35 


1.19 


0.49 


0.96 


Error 116 


276.73 


2.39 






Pleuronectes bilineatus 










Time 1 


1.68 


1.68 


1.35 


0.25 


Depth 6 


19.01 


3.17 


2.55 


0.03 


Time x depth 6 


3.47 


0.58 


0.47 


0.83 


Error 69 


85.78 


1.24 






Gadus macrocephalus 










Time 1 


9.12 


9.12 


4.09 


0.05 


Depth 6 


22.46 


3.74 


1.68 


0.14 


Time x depth 6 


7.06 


1.18 


0.53 


0.79 


Error 69 


153.81 


2.23 







son (1989) found that rock sole (P. bilineatus), as 
well as larvae of several other taxa, showed reverse 
diel migrations during the spring. 

We believe that sampling bias could not have re- 
sulted in the observed reverse distributions. Eggs of 
H. elassodon, as expected, showed no differences by 
time of day in our study and walleye pollock larvae 
in these same collections exhibited a normal diel mi- 
gration pattern (Type I), occurring mainly in the 30- 
45 m range during daytime and above 30 m at night 
(Kendall et al. 1 ; see also Kendall et al., 1987). Net 
avoidance, although suggested by the higher night 
catches overall as well as the larger mean size of 
larvae collected at night, is not a plausible expla- 
nation for the observed diel pattern. Light-aided 
daytime avoidance would be ex- 
pected to influence the catch of lar- 
vae in the surface strata more than 
those in deeper strata, thus leading 
to underestimates of near-surface 
daytime abundances and the mag- 
nitude of reverse migration. 

The prevalence of the reverse 
diel migration pattern in our 
study suggests an adaptive role 
for this behavior. Temperature 
gradients are relatively minor 
(<1°C) over the upper 50-60 m 
where most of the migration oc- 
curs (Fig. 7), and the majority of 
the larvae appear to be above the 
seasonal thermocline at all times 
of the day. Thus, we see no possi- 
bility of temperature-mediated 
energetic advantage related to 
migration at any time of the day. 
Similarly, observed density gradi- 
ents are not pronounced (<0.5 o t 
units) within this surface layer 
(Fig. 7; Kendall et al. 1 ) and there 
appears to be no physical mecha- 
nism that would aggregate either 



5 Walline, P. D. 1981. Hatching dates of 
walleye pollock (Theragra ehalco- 
gramma) and vertical distribution of 
ichthyoplankton from the eastern 
Bering Sea, June-July 1979. NWAFC 
Processed Rep. 81-05, 22 p. 

6 Rogers, D. E., D. J. Rabin, B. J. Rogers, 
K. J. Garrison, and M. E. Wangerin. 
1979. Seasonal composition and food 
web relationships of marine organisms 
in the nearshore zone of Kodiak Island 
including ichthyoplankton, mero- 
plankton (shellfish), zooplankton and 
fish. Univ. Washington, Fish. Res. Inst. 
Rep. FRI-UW-7925, 291 p. 



230 



Fishery Bulletin 92(2). 1994 



DAWN 



DAY 



DUSK 



NIGHT 



All non-Pollock 
larvae 



0-15 
15-30 
30-45 1 
45-60 
60-80 J 
80-100 
> 100 



3- 



i 



40 



80 120 50 100 150 200 40 80 120 



Hippoglossoides 
elassodon 



0-15 
15-30 
30-45 
45-60 
60-80 
80-100 
> 100 



' 



• 



50 100 150 200 100 200 300 40 80 120 160 




Bathymaster spp. 



0-15 


I 


I 


*—* 15-30 
t 30-45 




>m^ 




45-60 

CO 

— 60-80 
J~ 80-100 




*- > 100 





} 



I 4. 



200 400 600 800 



3- 



i 



10 20 30 40 50 



100 200 300 40 80 120 160 20 40 60 80 



Ammodytes 
hexapterus 



C 0-15 


I 


I 








15-30 
+- 30-45 

© 45 " 6 ° 
p| 60-80 

80-100 

> 100 


| 


I 







4. 



Gadus 
macrocephalus 



Pleuronectes 
bilineatus 




* 



T 



3- 



10 20 30 10 20 30 40 50 20 40 60 80 100 



10 20 30 40 



3- 




12 



8 10 



8 12 




5 10 15 20 10 20 30 40 50 



Density (no. /1 000m 3 ) 

Figure 4 

Diel changes in the vertical distribution of all larvae (excluding walleye pollock), and Hippoglossoides 
elassodon, Bathymaster spp., Ammodytes hexapterus, Gadus macrocephalus, and Pleuronectes bilineatus 
larvae. Bars are mean abundances per 1000 m 3 at each depth interval and error bars are ± one standard 
deviation about the mean abundance. 



Brodeur and Rugen: Vertical distribution of ichthyoplankton in the northern Gulf of Alaska 



231 





DAWN 




DAY 




DUSK 




NIGHT 




0-15 
15-30 
30-45 

Hippoglossoides ^ 45-60 
elassodon £ 60-80 

80-100 
CO » 100 


~-, 




-^ 








^^ 




• • 


co < 


5 6 7 8 9 10 <■ 


56789 10 456789 10 456789 10 


> 0-15 
1- 15-30 
® 30-45 

Bathymaster tT 45-60 

S PP- •- 60-80 
80-100 

-*- > 100 






 




. — . — , 










^^ 




Q. 


15 6/ 


i 


5 6 


r t 


5 6 7 4 


5 6 7 


0) 0-15 
Q 15-30 

Ammodytes 30-45 
hexapterus 45 . 60 

60-80 

80-100 

' 100 


• 




* 




^_ 




— — 


• 


, . , 




• 


4 8 12 16 20 4 8 12 16 20 4 8 12 16 20 4 8 12 16 20 

Length (mm) 

Figure 5 

Diel vertical distribution of larval lengths of Hippoglossoides elassodon, Bathymaster spp., and Ammodytes 
hexapterus. Circles are mean length at each depth interval and error bars are ± one standard deviation 
about the mean length. The plus signs indicate actual lengths measured when less than three lengths were 
available from a particular depth stratum. 



0.30 
0.25 

0.20 

c 
o 

£ 0.15 

a. 
o 

£ 0.10 
0.05 
0.00 



! 



UDay □ Night 



2 



6 7 8 

Length (mm) 



10 



Figure 6 

Day versus night proportional length distribu- 
tions of Hippoglossoides elassodon larvae. 



larvae or their prey at certain depths or inhibit them 
from migrating to different depths. 

The fact that walleye pollock larvae, which are the 
dominant fish larvae in this area representing 70- 
80% of the larvae present in Shelikof Strait in the 
spring (Rugen 7 ; this study), show a normal migra- 
tion pattern (Kendall et al., 1987) suggests one po- 
tential explanation for reverse migration patterns 
of other larvae. If other larvae feed on the same 
microzooplankton prey as larval walleye pollock and 
these prey resources were limiting, then the pres- 
ence of these other larvae in surface waters at dif- 
ferent times of the day than those of walleye pol- 
lock would reduce competition with the numerically 
dominant taxon. Copepod nauplii, an important 



7 Rugen, W. C. 1990. Spatial and temporal distribution of lar- 
val fish in the Western Gulf of Alaska, with emphasis on the 
period of peak abundance of walleye pollock tTheragra 
chalcogramma) larvae. NWAFC Processed Rep. 90-01, 162 p. 



232 



Fishery Bulletin 92(2), 1994 



Water temperature and density 



DAWN 



NIGHT 



DAY DUSK 

Sigma-t 

2S 2 253 254 26.5 266 25.2 25 3 254 25 5 25 6 25 1 25 2 253 25 4 25 5 25.2 25.3 254 25 5 25 6 



E 


20 


-— - 




-C 




•*—• 




a. 




a> 


60 


Q 






BO 



sigma-t 



temp 








3 4 6 60 30 4 5 6 30 4 5 6 3.0 4 5 6 



Temperature (°C) 



Figure 7 

Diel vertical profiles of temperature and density (o t ). Data are means of at least four casts within 
each time interval and were collected at 1 m depth intervals. 



component of the diet of many larval fishes includ- 
ing walleye pollock (Kendall et al., 1987), were the 
most abundant microzooplankton category found in 
Shelikof Strait, mostly in the upper 30 m during 
May 1986 and 1987 (Incze and Ainaire 8 ). During diel 
Series 4, copepod nauplii had overall mean depths 
between 20 and 34 m but showed no obvious diel 
pattern in depth distribution (Kendall et al. 1 ). Al- 
though feeding at a different time of day from wall- 
eye pollock might reduce interference competition 
(i.e. behavioral interactions) with the dominant spe- 
cies, it is highly unlikely, based on typical larval fish 
and copepod naupliar densities, that prey resources 
could ever be depleted by larval fish (Cushing, 1983; 
MacKenzie et al., 1990). Moreover, if food were lim- 
iting, then it would be advantageous for all larvae 
to stay in the layer of maximum food concentration 
throughout the diel period to maximize total intake. 
Thus, we do not see a trophic benefit accruing from 
a reverse migration pattern for these larvae. 

If feeding by these larvae is periodic and depen- 
dent on some minimum light level, then the verti- 
cal distribution pattern can be partially explained 
by larval feeding response. Assuming light levels 
were limiting feeding at depths below 30 m, then it 
would be necessary for larvae to ascend to a shal- 
lower depth during the daytime when light is at a 
maximum. Following the cessation of feeding at 
dusk, larvae would be expected to become inactive 



and passively sink to deeper levels at night. Such a 
mechanism has been postulated for Japanese sand 
lance (A. personatus) by Yamashita et al. ( 1985) who 
demonstrated a nocturnal cessation of feeding in 
this species. Although we lack data on the diel feed- 
ing chronology of any of the taxa examined here, it 
is possible that feeding occurs mainly in the crep- 
uscular periods, with a temporary cessation of in- 
gestion occuring during midday as observed in the 
field for larval walleye pollock (Canino and Bailey 9 ). 
The shallowest mean depth occurs at either dawn 
or dusk for the three common species that were ex- 
amined over the four time periods with slightly 
greater depths occurring during midday. If larvae 
were not feeding during the middle of the day, it 
would be advantageous to cease swimming alto- 
gether and sink through the water column to avoid 
being sensed by mechanoreceptive or visual preda- 
tors. Following a particular isolume would produce 
a similar daytime pattern but could not account for 
the deeper distribution at night that we observed. 
Larval walleye pollock in the laboratory have been 
shown to avoid high light levels (Olla and Davis, 
1990) but they also require relatively low light lev- 
els to initiate feeding (Paul, 1983). Unfortunately, 
we have no data available on the light levels neces- 
sary for feeding in the taxa we examined with which 
we can evaluate this hypothesis. 



8 Incze, L. S., and T. Ainaire. In review. Zooplankton of Shelikof 
Strait, Alaska. I. Micro-zooplankton prey of larval pollock, 
Theragra chalcogramma. Submitted to Fish. Bull. 



9 Canino, M. F., and K. M. Bailey. In review. Gastric evacuation 
of walleye pollock, Theragra chalcogramma (Pallas), larvae in 
response to feeding. Submitted to Journal of Fish Biology. 



Brodeur and Rugen: Vertical distribution of ichthyoplankton in the northern Gulf of Alaska 



233 



A potential disadvantage to a diurnal ascent is 
increased susceptibility to visually feeding 
planktivorous fishes. However, acoustic and trawl 
survey data suggest that epipelagic fish predators 
are rare during the spring in this area and the 
majority of the nekton biomass is found in midwater 
or near the bottom (Brodeur et al., 1991), well be- 
low the depth of most larvae. On the other hand, 
euphausiids, which are possibly the major inverte- 
brate predator on walleye pollock yolk-sac larvae, 
undergo a nocturnal ascent to surface water and 
descend to greater depths during the day in Shelikof 
Strait (Bailey et al., 1993). If euphausiids were also 
predators on non-pollock larvae and feed only in the 
surface layer above the nightime depths of these lar- 
vae, then a distinct advantage would be conferred 
upon individuals adopting a reverse diel migration 
pattern, as has been postulated for copepods (Ohman 
et al., 1983; Ohman, 1990). Based on field and experi- 
mental results, it has become increasingly apparent 
that predators can alter the diel vertical distribution 
patterns of invertebrate prey (Ohman et al., 1983; 
Gliwicz, 1986; Bollens and Frost, 1989; Levy, 1990; 
Neill, 1990; Frost and Bollens, 1992), but evidence for 
this effect on larval fish as prey is presently lacking. 

Although a variation in depth by time of day was 
apparent for all species and consistent among spe- 
cies, it was not substantial enough to be statistically 
significant in all cases (e.g. G . macrocephalus). This 
may be due in part to the lack of resolution of our 
sampling intervals. The smallest average migration 
that we could detect is -15 m; thus, diel vertical 
migrations less than that were not likely to be de- 
tected. Although a daily ambit of 30 m is not excep- 
tional for larger larvae, it may be excessive for newly 
hatched individuals. For a study specifically exam- 
ining the diel vertical distribution of the species 
considered here, we recommend sampling with a 
multiple net system every 5 m over the upper 40 m 
of the water column. Some bias may have also re- 
sulted from combining tows from different years, 
weeks, or geographic areas into our four time peri- 
ods, which was necessitated by the relatively low oc- 
currence rate and densities of these taxa. However, 
the remarkably strong and consistent diel differ- 
ences among the different taxa, despite this intro- 
duced sampling variability, lend credence to our 
findings. 

If there was differential migration by size classes 
of larvae, this condition might also obscure some of 
our results. The vertical distribution of larval 
lengths of the dominant species did not show any 
consistent patterns by time of day. The mean length 
by depth varied significantly for H. elassodon; 
smaller larvae were found at greater depths during 



the daytime and at the surface at night. This can- 
not be explained by visual gear avoidance alone 
since the nighttime pattern would then be expected 
to be random rather than exhibit the increasing 
mean length with depth that we observed. A possible 
explanation for this pattern might be that larger 
larvae may migrate a greater distance than smaller 
larvae, a pattern frequently observed in other fish 
larvae (Neilson and Perry, 1990). It is also possible 
that the migration of different size classes is asyn- 
chronous (Pearre, 1979). However, the available size 
ranges of the dominant species in our data was not 
extensive enough to examine diel migration patterns 
of different size classes. Moreover, caution should be 
exercised in examining larval length data in mul- 
tiple net systems. Since larvae shrink upon death 
(Theilacker, 1980; Hay, 1981) and the likelihood of 
death may be related to time in net, we may assume 
that larvae caught in the first (deepest) net may 
have undergone more shrinkage than those in the 
last (surface) net. 

In conclusion, this study shows that all the com- 
mon larvae exhibit a reverse vertical migration pat- 
tern, opposite to that of the overall dominant spe- 
cies, walleye pollock. In Auke Bay, an inland 
embayment in Southeast Alaska (58°22' N) on the 
eastern side of the Gulf of Alaska, Haldorson et al. 
( 1993) found a Type I migration for the numerically 
dominant osmerid larvae in their sampling and a 
Type II migration for the five next most abundant 
taxa {T. chalcogramma, H. elassodon, P. bilineatus, 
Leuroglossus schmidti, and Agonidae). These au- 
thors attribute this diel-depth distribution pattern 
to temperature preferences by each species, al- 
though their vertical temperature gradients were 
more pronounced than what we observed in our 
study. Since most abiotic variables (other than light 
intensity) and food resources varied little over the 
depths through which much of the migration oc- 
curred in Shelikof Strait, we hypothesize that the 
reverse migration pattern that we documented was 
either a predator-avoidance mechanism or else an 
optimization of light levels for feeding. The preva- 
lence of reverse migration in this and other studies 
suggests that it may be more common than previ- 
ously suspected, especially in higher latitude ecosys- 
tems, and the factors contributing to this phenom- 
enon merit further investigation. 



Acknowledgments 

The MOCNESS tow collections used in this study 
were made available by Lew Incze (Bigelow Labo- 
ratory) and Peter Ortner (Atlantic Oceanographic 



234 



Fishery Bulletin 92(2). 1994 



and Meteorological Laboratories, NOAA). Field as- 
sistance was provided by Shailer Cummings 
(AOML) and the crew of the NOAA ship Miller Free- 
man. Susan Picquelle and Patricia Brown (Alaska 
Fisheries Science Center) assisted in statistical 
analysis. Art Kendall, Gary Stauffer, JeffNapp, Bori 
Olla, Susan Sogard, and Michael Davis (AFSC), R. 
Ian Perry (Pacific Biological Station), Steven Bollens 
(Woods Hole Oceanographic Institution), and two 
anonymous reviewers provided valuable comments 
on earlier versions of the manuscript. 

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Abstract. — The commercial 
fishery for orange roughy on the 
Challenger Plateau developed in 
1981, increased markedly through- 
out the mid-1980s, and then de- 
clined rapidly by 1990. Data from 
research trawl surveys and com- 
mercial fishing returns over the 
period are examined, and changes 
in the population are described. 

The distribution of orange 
roughy changed over the period 
examined; there was a contraction 
of the areas of high density and 
apparent fishing-out of aggrega- 
tions on relatively fiat bottom. Ag- 
gregations are now largely con- 
fined to pinnacles. Biomass of or- 
ange roughy, measured by bottom 
trawl survey indices and commer- 
cial catch per unit of effort, de- 
clined substantially and is cur- 
rently estimated to be about 20% 
of virgin levels. Most other inci- 
dental species in the trawl surveys 
have also declined in abundance, 
and there are no indications of 
'species replacement.' 

Data on size, reproductive stage, 
size at maturity, and feeding have 
also been examined. Size structure 
of the population has not changed 
over time. Time of spawning (July) 
and the pattern of gonad develop- 
ment have been consistent over 
the years. Diet composition has 
also remained similar; dominant 
prey groups are natant decapod 
crustaceans and small fish. 

It is suggested that biological 
changes have not been apparent 
because orange roughy are a long- 
lived, slow-growing species, with 
low productivity. There could be a 
long response time to fishing pres- 
sure, yet orange roughy popula- 
tions can be quickly reduced to low 
levels by commercial fishing. 



Changes in a population of 

orange roughy, 

Hoplostethus atlanticus, 

with commercial exploitation on the 

Challenger Plateau, New Zealand 

Malcolm R. Clark 
Dianne M. Tracey 

MAF Fisheries Greta Point. PO. Box 297 

295 Evans Bay Parade, Wellington, New Zealand 



Manuscript accepted 4 November L993 
Fishery Bulletin 92:236-253 (1994) 



Orange roughy (Hoplostethus 
atlanticus Collett) has a worldwide 
distribution on the continental 
slope at depths of 700 to 1,500 m. 
However, it is fished commercially 
only off New Zealand, Australia, 
and in the northeastern Atlantic 
Ocean. The New Zealand fishery is 
the most established, having 
started in 1978; the others date 
from 1988 and 1991, respectively. 
Orange roughy is one of the most 
valuable commercial species in 
New Zealand waters, with annual 
landings of 40-50,000 metric tons 
(t) and export earnings of NZ $100- 
150 million (Robertson, 1991). 

The New Zealand fishery for or- 
ange roughy occurs in a number of 
areas (Fig. 1), including the Chal- 
lenger Plateau, a broad submarine 
plateau off the west coast of New 
Zealand. The commercial fishery on 
the Plateau developed in late 1981 
and rapidly expanded into one of 
the most important orange roughy 
fisheries in New Zealand waters, 
with annual catches up to approxi- 
mately 16,000 t (Table 1). The fish- 
ery operates primarily during win- 
ter (June-August), when the fish 
form large spawning aggregations at 
depths of 850-900 m (Clark, 1991a). 

The fishery has been managed by 
a Total Allowable Catch (TAC) sys- 
tem since 1982. Tracey et al. (1990) 



and Clark (1991a) discussed details 
of this management regime. Ini- 
tially, catches were limited to 7,000 
t by the TAC for all areas of the 
New Zealand Exclusive Economic 
Zone (EEZ), outside the established 
fishing grounds on the east coast. 
A TAC of 4,950 t was set for 1983- 
84 and 1984-85 (October-Septem- 
ber fishing year) on the Challenger 
Plateau and west coast of the 
South Island. This was raised to 
6,190 t specifically for the Chal- 
lenger fishery in 1985-86 based on 
biomass estimates from a trawl 
survey in winter 1984. The quota 
was raised to 10,000 t in 1986-87, 
and further to 12,000 t in 1987-88, 
in order to assess the effects of 
heavier fishing on the population 
dynamics of orange roughy ("adap- 
tive management"). In the follow- 
ing fishing year only 8,200 t of 
quota were allocated, the rest with- 
held because of signs that the or- 
ange roughy population was declin- 
ing rapidly. During 1989-90 the 
TAC was reduced to 2,500 t after 
new stock assessments showed the 
population was overexploited and 
had declined to low levels (Clark 
and Francis, 1990). The TAC was 
further reduced for 1990-91 to pro- 
mote rebuilding of the population. 
These changes occurred against 
a background of increasing infor- 



236 



Clark and Tracey: Population changes of Hoplostethus atlanticus on the Challenger Plateau 



237 



/175°W 



* EEZ boundary 




Figure 1 

Map of New Zealand and offshore waters of the Exclusive Economic Zone 
(EEZ), showing the location of the Challenger Plateau and other major 
fishing areas for orange roughy (Hoplostethus atlanticus). 





Table 1 






Reported catch 


es (t) of orange roughy (Hop- 


lostethus atlanti 


cus) from the Challenger Plateau 


(ORH 7A and outside EEZ) (from Clark 1992; to- 


tal estimated catch includes allowance for re- 


search survey 


catches an 


d a correction for 


15-30% under-estimation of true catch in reported 


catch figures because of bu 


rst trawls. 


fish dis- 


cards, and incorrect official 


conversion 


factor). 




Total 


Total 




Fishing year 


reported 


estimated 




(Oct-Sept) 


catch 


catch 


TAC 


1980/81 


33 


43 




1981/82 


4,248 


5,522 




1982/83 


11,839 


15,409 




1983/84 


9,527 


12,514 


4,950 


1984/85 


5,117 


6,707 


4,950 


1985/86 


7,753 


10,251 


6,190 


1986/87 


11,492 


15,750 


10,000 


1987/88 


12,181 


15,830 


12,000 


1988/89 


10,241 


12,627 


12,000' 


1989/90 


4,309 


5,171 


2,500 


1990/91 


1,357 


1,560 


1,900 


' 8,219 t allocated. 



mation on orange roughy. It has 
only recently been realized that 
orange roughy is very slow-growing 
and long-lived. Mace et al. (1990) 
recorded a growth rate of about 
three cm per year for the first four 
years of life (validated ages), and 
an estimated age at maturity of 24 
years and maximum age over 50 
years. They estimated natural mor- 
tality to be low (less than 0-1 yr -1 ) 
and concluded that sustainable 
yields of orange roughy would be 
relatively low and show slow recov- 
ery from over-fishing. Recent esti- 
mates of the maximum age of or- 
ange roughy from Australian wa- 
ters approach 150 years (Fenton et 
al., 1991). 

Quotas for orange roughy har- 
vest from New Zealand have been 
reduced in recent years on the ba- 
sis of information which suggests 
much lower productivity than origi- 
nally assumed. However, the Chal- 
lenger Plateau population had al- 
ready declined markedly and pro- 
vides some insight into the effects 
of heavy fishing pressure on orange 
roughy population dynamics. 
There is an extensive literature on general re- 
sponses offish populations to exploitation, covering 
lake ecosystems (e.g. Regier and Loftus, 1972; 
Spangler et al., 1977), coral reef fisheries (e.g. Russ 
and Alcala, 1989), and relatively shallow-water 
marine environments (e.g. Hempel, 1978; Pauly, 
1979; Grosslein et al. 1980). There have been few 
studies on deep-water or long-lived species such as 
orange roughy. The closest is probably Pacific ocean 
perch (Sebastes alutus) which is found at depths to 
600 m in the North Pacific Ocean and has a maxi- 
mum age of 90 years (e.g. Gunderson, 1977; Lea- 
man, 1991). 

There are a number of general population re- 
sponses to exploitation, which include 

1 Decline in abundance of fished species. 

2 Contraction of distribution or areas of high density. 

3 Change in age structure or size structure, or both, 
with fewer old, large fish and the population 
dominated by new recruits. 

4 Increase in growth rate of individuals, with a 
decrease in age for a given length. 

5 Lower age at maturity or size at maturity, or 
both. 



238 



Fishery Bulletin 92(2), 1994 



6 Possible change in species composition over time 
('species replacement'). 

Such responses are often observed in short-lived, 
fast-growing species (e.g. Pauly, 1979; Grosslein et 
al., 1980). Some have also been noted with Sebastes 
alutus (Gunderson, 1977; Leaman, 1991), but it is 
not clear whether these changes would occur in such 
a long-lived species as orange roughy, or over what 
time period such changes would become apparent. 
Orange roughy on the Challenger Plateau have been 
exploited for only 10 years, and hence it seems un- 
likely that marked changes in biological character- 
istics could occur over such a relatively short time 
period in relation to the longevity of the species. 
Therefore, we might expect to observe changes in 
biomass and distribution, as well as age and size struc- 
ture of the population, but not changes in growth rate 
or reproductive potential. 

In this paper, we summarize some of the available 
data on distribution, abundance, and biology of or- 
ange roughy on the Challenger Plateau, primarily 
over the period 1984-90. This period covers the 
early years of the developing fishery, to maximum 
levels of exploitation, and subsequent decline of the 
population. We describe the reduction in size and 
distribution of the stock and investigate associated 
changes in size structure, aspects of reproduction, 
and feeding. 



Methods 

Research trawl surveys 

Trawl surveys have been carried out in the winter 
(June-July) of each year from 1984 to 1990. The 
vessel used, area covered, intensity of trawling, and 
survey design differed between 
years, and all are not directly 
comparable (Table 2). Surveys 
from 1987 to 1989 were treated as 
fully comparable, but only se- 
lected data have been used from 
other surveys: distribution from 
1984 and 1990, and biology (size, 
reproductive, and feeding data) 
from 1984, 1985, 1986, and 1990. 
The general survey design was 
two-phase stratified random (af- 
ter Francis, 1984). The survey 
area was divided into a number of 
strata based on depth and certain 
bottom features (e.g. pinnacles). 
General stratification is shown in 



Figure 2. The depth range covered was 800 to 1,200 
m. New, random station positions within strata were 
selected each year, except in strata 10 and 11 on 
pinnacles where a random tow direction was ad- 
justed to avoid untrawlable ground, and these 
trawls were repeated each year. A similar net de- 
sign and gear set up was used for each survey. Tow 
length was standardized where possible at 1.5 nau- 
tical miles (nmi). Trawling speed was 3.0-3.5 knots. 
Biomass indices were calculated by the area swept 
method as described by Francis ( 1981). Biomass and 
its standard error were calculated from the follow- 
ing formulae: 



and 



B=^(X,a,)/cb 



S B = J^sfaf/c 2 b 2 



where B is biomass (t), X is the mean catch rate 
(kg-km -1 ) in stratum i, a i is the area of stratum i 
(km 2 ), b is the width swept by the gear (defined as 
doorspread (m) by MAF Fisheries), c is the catch- 
ability coefficient (an estimate of the proportion of 
fish available to be caught by the net), S B is the 
standard error of the biomass, s ( is the standard 
error of X t 

The catchability coefficient was assigned a value 
of 0.27, which represents the wingend spread di- 
vided by the doorspread, because orange roughy 
form schools which are not believed to be herded 
substantially by doors or sweeps. 1 

Approximate 95% confidence limits (CD were 
calculated as 

CL = B±2S B . 



1 Orange Roughy Working Group, MAF Fisheries, Greta Point, 
P.O. Box 297, Wellington, New Zealand, pers. commun. 1991. 









Table 


2 






Trawl surveys carried out 


on the Cha 


lenger 


Plateau for 


orange roughy 


(Hoplostethus a 


'In 


nticus). 


















Area 


Number 




Vessel 




Year 


Date 


(km 2 ) 


of trawls 


Survey design 


Arrow 




1984 


3/7-18/7 


11,956 


118 


2 phase SRTS' 


Arrow 




1985 


4/7-20/7 


209 


16 


1 phase SRTS 


Arrow 




1986 


4/7-17/7 


94 


10 


transect grid 


Amaltal Explorer 




1987 


18/6-13/7 


8,270 


129 


2 phase SRTS 


Amaltal Explorer 




1988 


4/7-24/7 


8,270 


85 


2 phase SRTS 


Amaltal Explorer 




1989 


8/7-30/7 


8,270 


160 


2 phase SRTS 


Will Watch 




1990 


7/7-29/7 


8,270 


141 


2 phase SRTS 


' Stratified random 


tra 


wl survey 











Clark and Tracey: Population changes of Hoplostethus atlanticus on the Challenger Plateau 



239 



EEZ boundary 




Figure 2 

The Challenger Plateau survey area, showing bathymetry (depth contour in 
m) and details of survey stratification. 



ment of the fishery through 
to maximum exploitation. 
It is felt that the fishery 
was not constrained much 
by the TAC over this time. 
CPUE in winter months 
from 1983 to 1991. This in- 
cludes data from 1990 and 
1991, following a substantial 
reduction in TAC and effort. 
CPUE in non-winter months 
from 1983 to 1991. 
Trawl survey indices from 
1987 to 1989. These sur- 
veys covered the same area, 
had the same design, and 
used the same vessel. 
Trawl survey indices from 
1984 and 1987 to 1990. 
This series incorporated 
data from a smaller area 
surveyed in 1984 and from 
the 1990 survey, both of 
which used a different ves- 
sel from 1987 to 89. 



The coefficient of variation (CV) is a measure of 
the precision of the biomass estimate, and was cal- 
culated by 

CV = 5 B /Bxl00. 

Stock reduction analysis 

A stock reduction technique was used to estimate 
virgin biomass based on the method of Francis 
(1990, 1992). This incorporated a complete catch 
history for the stock, a time series of abundance 
indices, and life history parameters used in a deter- 
ministic age-structured population model (see 
Clark, 1992). The latter were the von Bertalanffy 
growth parameters (L m =39.5 cm, &=0.059yr _1 , t = 
-0.3 yr), natural mortality=0.04yr _1 , weight-length 
parameters (a=0.0963, 6=2.68), age at maturity (24 
yr), age at entry to the fishery (24 yr), and Beverton- 
Holt recruitment steepness of 0.75. 

Five sets of abundance indices were used from 
trawl surveys between 1984 and 1990, and commer- 
cial catch per unit of effort (CPUE) data (unstand- 
ardized mean catch per tow by monthly groupings): 

1 CPUE in winter months (June-September) from 
1983 to 1989. This covered the period of develop- 



The maximum likelihood 
method was used to estimate 
virgin biomass. Ninety-five 
percent confidence intervals 
were estimated by using bootstrapping techniques 
with the coefficient of variation fixed at 20%. The 
best estimate of virgin biomass was then used in an 
age-structured model (detailed in Francis, 1992) to es- 
timate current biomass. 



Biological data 

Standard procedure during trawl surveys was to 
take a random sample of about 200 fish from each 
tow. These were measured (standard length rounded 
down to the nearest whole cm [standard MAF Fish- 
eries procedure]) and sexed. Twenty of these fish 
were randomly selected, their otoliths extracted, and 
more detailed data collected: standard length (rounded 
down to the nearest whole mm), weight (rounded down 
to the nearest gm), sex, stage of gonad maturity (see 
below), gonad weight (rounded down to the nearest 
gm), fullness of stomach, state of digestion of contents, 
and stomach contents (to species level where possible). 

Size Length-frequency distributions have been con- 
structed to represent the total population where 
possible. In the years 1984 and 1987-90, data have 



240 



Fishery Bulletin 92(2). 1994 



been scaled by percentage sampled to represent each 
catch and further scaled by stratum biomass to ap- 
proximate the population. Samples in 1985 and 1986 
were scaled to represent solely the catch, as survey 
design was inadequate for biomass estimation. 

Length-frequency data are difficult to compare 
statistically and, for the purposes of this study, have 
not been attempted. However, to enable a general 
comparison, a single distribution was constructed 
combining length-frequency data from all years 
weighted by the number of tows each year. This 
distribution is plotted together with those from each 
year separately. 

Mean size by sex was calculated separately for 
three main regions of spawning within the survey 
area (strata 1, 4; 10; 9, 11) as it was unlikely these 
areas had been fished equally (see later 'Commer- 
cial Fishery' section). The sample sizes used in cal- 
culating the standard error were number of tows, 
not number of fish. Orange roughy can associate in 
size groups; between-tow variance was greater than 
within-'tow variance. Variance is represented by ±2.0 
standard errors for all years except 1986, when ±2.2 
standard errors was arbitrarily used because there 
were only 10 trawls. 

Reproduction Macroscopic staging of reproductive 
condition followed Pankhurst et al. (1987): 



Stage 



Female 



Male 



1 

2 
3 


Immature/resting 
Early maturation 
Maturation 


Immature/resting 
Early maturation 
Maturation 


5 
6 


Ripe 
Running ripe 

Spent 


Ripe/running ripe 
Spent 



Relative frequency of gonad stages was examined. 
Analyses were based on the samples taken. They 
were not scaled in any way, as there were no appar- 
ent differences between the length frequencies of the 
samples and the distribution of the total population. 
Only data from females are presented, as their 
macroscopic gonad stages can be determined more 
accurately than those from males. 

Size at maturity was determined from samples 
taken over the total survey area using a 'probit 
analysis' approach (after Pearson and Hartley, 
1976). It was assumed that length at maturity is 
normally distributed in the population. The regres- 
sion part of the analysis was repeated 10 times to 
ensure convergence of the estimate. 2 A standard lin- 



2 Francis, C, MAF Fisheries, pers. commun. 1991 



ear regression analysis was carried out on results 
to investigate trends over time by using the SAS sta- 
tistical package (SAS, 1988). 

Feeding Data on frequency of occurrence were 
available from all surveys. Frequency of occurrence 
was defined as the number of stomachs in which a 
food item occurs, expressed as a proportion of the 
total number of stomachs containing food. Only 
stomachs with part-full or full classifications, and 
with fresh or partly digested contents, were included 
in analyses. 



Commercial fishing data 

Data on the catch and position of each tow and the 
start and finish times have been collected since 
1980. However, catch and effort information is dif- 
ficult to standardize and interpret for orange roughy. 
Fish can be highly aggregated at various times of 
the year, and 'windows' or escape panels in the net 
are frequently used to reduce catch size and mini- 
mise damage to nets. Fishing performance varies 
with experience of skipper and crew, and technol- 
ogy has advanced considerably in recent years (in 
particular, development of Global Positioning Sys- 
tem navigation, which enabled improved accuracy 
when fishing pinnacles). Fishing logbooks often do 
not have accurate information on length of tow on 
the bottom. Fishing for orange roughy on the Chal- 
lenger Plateau occurs on a variety of bottom terrain: 
on flat bottom, in troughs and steep slope, and on 
the tops and sides of pinnacles. In each case, the 
effective fishing time and fishing technique differ 
greatly, and they are almost separate types of fish- 
eries. In order to gain an indication of trends in 
catch rates, data were examined on the basis of 
mean catch per tow for two size classes of vessel (20— 
60 m, generally domestic fresh fish boats; and 60- 
90 m, domestic factory trawlers). Catch per unit of 
effort (CPUE) values were similar for both classes, 
and so data here are combined. Monthly data were 
amalgamated into two time periods: first, 'winter' 
(June, July, August) which covers the spawning 
period; second, 'out of season' (all other months). 
This division represents two distinct phases of or- 
ange roughy distribution, as well as differences in 
the mode of fishing (Clark, 1992). The former period 
is characterized by the formation of relatively stable, 
dense aggregations of fish, whereas in the latter 
period the orange roughy are more dispersed and 
widely distributed (Clark, 1991a). Fishing in win- 
ter generally involves shorter tows, often with 
smaller nets, than does out-of-season fishing. 



Clark and Tracey: Population changes of Hoplostethus atlanticus on the Challenger Plateau 24 1 



In the following text, three colloquial area names 
have been used. These are given below with specific 
strata numbers (see Fig. 2): 



Central Flat 
Pinnacles 
Westpac Bank 



strata 1, 4 
stratum 10 
strata 9, 11 



Results 

Distribution 

Trawl surveys The distribution of orange roughy in 
the survey area changed substantially between 
years (Fig. 3). In 1984 high catch rates were ob- 
served across much of the Central Flat area. (No 
trawls were made on the Pinnacles although heavy 
marks were observed on the echosounder; the sur- 
vey did not cover the Westpac Bank area.) In 1987 
fish were still widely distributed in the Central Flat; 



















-36' 


1984 








>48' 










•40°S 






Catch rate kg.knrr 1 
100 


j-s^ii 




-12' 






^P 10 000 




12' 24' 


36' 48' 168° E 12' 24' 






















-36' 


1987 




>36' 


1988 






-48<P 


'^~> 




■48'----.. 


[®j 






-40°S 






-40°S 


r-'iS 






-12' 






 12' 








12' 24' 


36' 48' 168° E 12' 24' 




1 2' 24' 


36' 48' 168° E 12' 24' 




















36' 


1989 




- 3IV 


1990 






■48' ; <3 ; 


.---. 




- € 


''--. S; 






■40°S 


r-<5/ 




■40°S 


■0 






■12' 






- 12' 








1 2' 24' 


36' 48' 168° E 12' 24' 




12' 24' 


36' 48' 168° E 12' 24' 






Figure 3 




Contours of trawl survey catch rates (kg-km l ) of orange roughy (Hoplostethus 
atlanticus) in 1984 and 1987-90. 



there were two main schools and further concentra- 
tions around the Pinnacles and the Westpac Bank. 
In 1988 there was a marked contraction in the area 
of high catch rates; a single small aggregation was 
observed on the Central Flat, and by 1989 there 
were no aggregations in the Central Flat region. High 
catch rates still occurred on the Pinnacles and Westpac 
Bank in 1989, and these actually increased in 1990, 
after the TAC and fishing effort were greatly reduced. 

Commercial fishery The commercial fishery has 
been centered mainly inside the EEZ, targeting ag- 
gregations of orange roughy on the Central Flat and 
Pinnacles. Distribution of effort (number of tows) 
and catch between these two areas has changed over 
time (Table 3). In the period 1982-87, over 80% of 
the catch from the two areas was taken from the 
Central Flat with over 75% of the number of tows. 
In 1988 there was a marked increase in the propor- 
tion of catch and effort on the Pinnacles, and a corre- 
sponding reduction on the Cen- 
tral Flat. This shift continued 
in 1989 and 1990, during which 
the Pinnacles accounted for 
65-70% of the catch. These 
changes reflect the change in 
distribution observed in the re- 
search trawl surveys. 

Relative abundance 

Trawl surveys Biomass indi- 
ces (estimates of relative bio- 
mass) from trawl surveys in 
1987, 1988, and 1989 are 
given in Table 4. The indices 
indicate a marked decline in 
biomass over the period. The 
distribution of biomass among 
strata changed over the years 
1987-90 (Table 5). In 1987 
and 1988 over 60% of the bio- 
mass was in the Central Flat 
area, but only 30% in 1989 
and 1990. Over this period, 
there was an increase in the 
proportion on the Pinnacles, 
especially between 1989 and 
1990. Biomass levels in the 
surrounding areas have fluc- 
tuated but were particularly 
high in 1989. The proportion 
of biomass on the Westpac 
Bank has remained compara- 
tively constant. 



242 



Fishery Bulletin 92(2), 1994 



Commercial fishery Mean catch per tow for all 
New Zealand vessels in the fishery from 1983 to 
1991 is given in Table 6. Catch rates in winter, when 
the fish are aggregated for spawning, are generally 
higher than in other months. Although aggregations 
occur at other times, presumably for feeding, they 
are not as large or as stable as in winter. Catch rates 
in both periods declined steadily from 1983 to 1989 
to between about 15% and 20% of original levels. 
The trend is slightly different in the two periods; 
winter catch rates declined more sharply to 1988, 
whereas in the other months the largest decrease 
was between 1983 and 1984. Catch rates increased 
in 1990, following a reduction of the TAC, when there 
were less vessels and fewer trawls on the grounds. 

Individual trawl catch rates for orange roughy can 
be highly variable, consisting of 'hits' and 'misses.' 
Therefore it is not useful to describe the variance 
around these mean catch rates, beyond commenting 
that there is wide variation. It should be stressed 
that the changes in catch rates presented here may 
give an indication of changes in stock size but should 
be treated with caution. Difficulties in interpreta- 
tion of such data for orange roughy are described in 
the 'Methods' section, and the form of relationship 
between mean catch per tow and stock abundance 
is uncertain. 

Stock reduction results 

Abundance indices used in, and estimates of virgin 
biomass from, the stock reduction analyses are given 
in Table 7. Point estimates of B Q range from 95,000 t 
to 278,000 t. The best fits of data to the model (those 
with the lowest CV) are from the winter CPUE se- 
ries. Results from trawl survey data have higher 
CVs but confirm that an estimate of the order of 
100,000 t is reasonable. 

The 1987-89 trawl survey series gave the lowest 
virgin biomass estimate. It was not considered reli- 
able because there were only three indices, and high 







Table 3 






Distribution of commercial catch (% of total catch 


taken 


tn the two 


areas) and effort (% of number 


of tows) for orange roughy (Hoplostethus 


atlan- 


ticus) for the Central Flat and Pinnacles ( 


winter 


period 


June to August). 






Year 


Central Flat 


Pinnae 


les 


% catch 


% tows 


% catch 


% tows 


1982 


97.2 


95.6 


2.8 


4.4 


1983 


97.0 


94.7 


3.0 


5.3 


1984 


95.2 


93.6 


4.8 


6.4 


1985 


87.7 


78.0 


12.3 


22.0 


1986 


87.3 


83.2 


12.7 


16.8 


1987 


84.4 


77.3 


15.6 


22.7 


1988 


52.9 


56.0 


47.1 


44.0 


1989 


34.0 


43.3 


66.0 


56.7 


1990 


30.2 


45.0 


69.8 


55.0 



Biomass indices 
tethus atlanticus) 
from 1987 to 1989 


Table 4 

(t) of orange roughy (Hoplos- 
from trawl surveys, conducted 
. (CV = coefficient of variation.) 


Year 


Biomass (t) 


CV 


1987 
1988 
1989 


78,661 
30,946 
11,746 


26 
27 
11 



fishing mortality rates were required to support the 
catch history. A maximum F of 1.0 is regarded as 
realistic for orange roughy (Francis et al., 1992). 
This constrains the virgin biomass to a minimum 
value of 94,000 t. 

The estimate from non-winter CPUE is compara- 
tively high. It has a large CV and is based on rela- 
tively low numbers of trawls (because most fishing 
effort is in winter). Such a biomass level would also 



Comparison of biomass estimates (t) o] 


'orange 


Table 5 

roughy (Hopl 


ostethus 


atlanticus) by 


region 


from 1987 to 1990. 


1987 




1988 




1989 




1990 


Region Biomass (t) 


'; 


Biomass (t) 


', 


Biomass (tl 


', 


Biomass <t) % 


Central Flat 56,636 
Pinnacles 7,794 
Surrounding background 10,717 
Westpac Bank 3,514 

Total 78,661 


72.0 
9.9 

13.6 

4.5 

100.0 


21,051 

5,215 

2,878 
1,802 

30,946 


68.0 

16.9 

9.3 

5.8 

100.0 


3,275 

2,821 

5,088 

563 

11,747 


27.9 

24.0 

43.3 

4.8 

100.0 


4,228 30.8 

5,508 40.1 

3,208 23.3 

794 5.8 

13,738 100.0 



Clark and Tracey: Population changes of Hoplostethus atlanticus on the Challenger Plateau 



243 









Table 6 






Catch 


per 


unit of effort (mean 


catch (t) 


per trawl) 


of ora 


nge 


roughy (.Hoplostethus atla 


iticus) for 


New Zealand fish 


ing vessels. 






Calend 




Winter 


Other months 












year 




CPUE 


No. trawls 


CPUE 


No. trawls 


1983 




16.2 


222 


9.2 


307 


1984 




15.3 


54 


5.2 


515 


1985 




13.3 


87 


4.6 


530 


1986 




10.5 


512 


3.3 


486 


1987 




10.2 


681 


2.4 


255 


1988 




5.9 


1,269 


2.7 


99 


1989 




3.7 


1,094 


13 


81 


1990 




6.6 


325 


7.3 


25 


1991 




4.1 


264 


0.1 


4 



suggest low values of F in recent years, which seems 
unlikely given the substantial effort in the fishery 
yet catches being less than the TAC. 

There is considerable uncertainty in all the data 
sets. However, assuming a virgin biomass of 110,000 t 
(as an approximation of the trawl survey and win- 
ter CPUE values), the decline in mid-year biomass 
of the population was rapid and the level in 1991 
was about 20% of the virgin level (Table 8). 

Other species 

Biomass indices of the 12 main bycatch species caught 
in the trawl surveys from 1987 to 1989 are presented 
in Table 9. The coefficients of variation of these mean 



values range from 11% to 69% and differ between 
years and species, which limits their comparability. 

However, there were no strong indications of in- 
creasing abundance of any species relative to abun- 
dance in 1987. There was little apparent change in 
abundance of ribaldo (Mora moro), leafscaled gulper 
shark (Centrophorus squamosus), widenosed chi- 
maera (Rhinochimaera pacifica), spiky oreo (Neoc- 
yttus rhomboidalis), Owston's spiny dogfish (Centro- 
scymnus owstoni), or white rattail (Trachyrinchus 
sp.). Declining abundance was suggested for big 
scaled brown slickhead (Alepocephalus sp.), basket- 
work eel (Diastobranchus capensis), Johnson's cod 
(Halargyreus johnsoni), smallscaled brown slickhead 
[Alepocephalus australis), shovelnosed spiny dogfish 
(Deania calcea), and seal shark (Dalatias licha). The 
biomass of species relative to orange roughy has 
generally increased for all species except seal shark. 
This change is strongest for ribaldo, Owston's dog- 
fish, widenosed chimaera, leafscaled gulper shark, 
and white rattail. 

Size structure 

Length-frequency distributions of orange roughy 
from the entire survey area were similar in all years 
with no marked differences from the overall 
weighted length frequency (Fig. 4). There was a 
strong unimodal distribution with the peak at 32- 
33 cm standard length. Fish ranged in standard 
length from 9 cm to 44 cm. 

Sex ratios varied between years, but were gener- 
ally about 1:1. However, females always dominated 
the size distribution above about 35 cm. The mean 











Table 7 








Summary o 


f biomass indices 


for orange roughy 


(Hoplostethus a 


tlanticus) 


used in stock rt 


duction analyses, 


and estimates of virgin biomass (B ) (mean 


and 95% confidence 


interval), 


and coefficients 


of variation (CV). 




CPUE 


CPUE 




CPUE 




Trawl survey 


Trawl survey 


Year 


(winter) 


(winter) 




(other month 


SI 


(full area) 


(reduced area) 


1983 


16.2 


16.2 




9.2 








1984 


15.3 


15.3 




5.2 






143,500 


1985 


13.3 


13.3 




4 6 








1986 


10.5 


10.5 




3.3 








1987 


10.2 


10.2 




2.4 




78,600 


75.000 


1988 


5.9 


5.9 




2.7 




30.900 


28,900 


1989 


3.7 


3.7 




1.3 




11,700 


11,000 


1990 




6. is 




7 3 






12,900 


1991 




1.1 




01 








Parameter estimates 














B (t) 


100,000 


122,000 




278,000 




83,000 


95,000 


B (95% CI) 


94,000-156,000 


94,000-224,000 


216,000-500,000 


94,000-181,000 


94,000-194,000 


CV (%) 


8 


22 




76 




27 


37 



244 



Fishery Bulletin 92(2). 1994 



Table 8 




Estimated biomass values by year 


(mid-year bio- 


mass, rounded to nearest 100 t) for 


orange roughy 


(Hoplostethus atlanticus). 




Year Biomass (t) 


Year 


Biomass (t) 


1980 110,000 


1986 


67,000 


1981 110,000 


1987 


54,900 


1982 107,000 


1988 


40,500 


1983 96,500 


1989 


28,400 


1984 83,200 


1990 


22,300 


1985 74,600 


1991 


21,400 



size of females was significantly greater than that 
of males «-test, P<0.05). Size data were also exam- 
ined by the following subareas: Central Flat, Pin- 
nacles, and Westpac Bank. Length frequencies by 
sex were generally similar to those for the total 
survey area and are not presented here. However, 
the distributions were approximately normal in 
shape and could be described by their means and 
standard errors to provide a simpler comparison 
between areas and between years (Fig. 5). There 
were no apparent differences between years or be- 
tween areas «-test, P<0.05), and no consistent trend 
in size over time. 



Reproduction 

All trawl surveys occurred during the months of 
June— July. There was considerable variation evident 
in the overall proportions of fish of different repro- 
ductive stage between years and areas (Table 10). 
To a large extent this reflected the timing of the 
survey (e.g. 1987 was earlier than the others) and 
showed a high proportion of maturing fish. However, 
in all years the majority of fish sampled were ma- 
ture and were involved in that year's spawning 
(stages 3-6). 

The Central Flat and Pinnacle regions were typi- 
cally dominated by mature fish in or near spawn- 
ing condition. In 1987 on the Westpac Bank there 
was a high proportion of fish that were in very early 
stages of maturation and hence unlikely to spawn 
in that year. From 1988 to 1990 the proportion of 
actively spawning fish increased. However, levels of 
nonspawning fish have consistently been higher 
here than in the Central Flat and Pinnacle areas. 

Timing of spawning 

The progression of gonad stages appeared consistent 
between years for which data spanning several 
weeks in July exist (Fig. 6). A pattern of maturing 
fish declining to low levels was observed early in 













Table 9 
















Biomass (t) of the 
(Hoplostethus atla 


main bycatch species in the trawl surveys, their proportion of that 
nticus) biomass (ref ORH), and their proportion of their biomass in 


year's orange roughy 
1987 (ref 1987). 






1987 






1988 








1989 




Biomass (CV) 


Ref 

1987 


Ref 
ORH 


Biomass 


(CV) 


Ref 
1987 


Ref 
ORH 


Biomass (CV) 


Ref 

1987 


Ref 
ORH 


Ribaldo 


295 


(14) 


1 (i 


0.004 


378 


(16) 


1.3 


0.012 


317 


llll 


1.1 


0.027 


Owston's dogfish 


567 


(32) 


1 


0.007 


358 


(31) 


0.6 


0.011 


400 


(20) 


0.7 


0.034 


Leafscaled gulper 
shark 


160 


(32) 


1 


0.002 


167 


(52) 


1.0 


0.005 


208 


(40) 


1.3 


0.018 


Spiky oreo 


75 


(38) 


1 (1 


0.001 


156 


(36) 


2.1 


0.005 


68 


(28) 


i) 9 


0.006 


Bigscaled brown 
slickhead 


1,345 


(20) 


L.O 


0.017 


486 


(21) 


(i 4 


0.016 


314 


(20) 


ii 2 


0.026 


Basketwork eel 


332 


(19) 


1 


0.004 


153 


(37) 


0.5 


0.005 


57 


(39) 


ii -1 


0.005 


Johnson's cod 


145 


(17) 


1 


0.002 


ill 


(36) 


0.4 


0.002 


M 


(16) 


ii 3 


0.004 


White rattail 


467 


(23i 


1 


0.006 


345 


(29) 


0.7 


0.011 


610 


(17) 


1.3 


0.052 


Smallscaled brown 
slickhead 


1,197 


(39) 


1 1) 


0.015 


285 


(22) 


0.2 


0.009 


610 


(13) 


ii S 


0.052 


Widenosed 
chimaera 


274 


(21) 


1 (1 


0.003 


662 


(20) 


2 1 


0.021 


283 


(16) 


in 


0.024 


Shovelnosed 
dogfish 


277 


(23) 


1 I) 


0.003 


218 


(41) 


0.8 


0.007 


73 


(31) 


0.3 


0.006 


Seal shark 


467 


(32) 


1.(1 


0.006 


H7 


(69) 


i) 2 


0.003 


17 


(39) 


0.1 


0.004 



Clark and Tracey: Population changes of Hoplostethus atlanticus on the Challenger Plateau 



245 



1984 



nfm) 5020 
n(t)68 



I II II I I i r i i i i i i i i \ i frr ft 



ttfl ll II 





1986 






IS  


n(m) 1865 
n(l) 10 


: 




10- 




r 


1 


5 - 
0- 




1 1 mil rnf 


— : m 1 1 1 1 



01 

fcl 20 

01 





1988 




5 - 


n(m) 12 665 
n(t) 81 






[. 




0^ 


 






j - 


- - 


5- 
0- 


-j 


"rrii 1 1 1 1 1 





1990 




15- 


nlm) 12 881 
n(t) 130 


10- 


, L 


| 


0- 


Jf 


- 

: muni 



1985 

n(m) 2609 
n(t) 18 



& 

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 r n 1 1 Fri 



rfl i n i 



1987 



n(m) 18 981 
n(t) 124 



J 

1 1 1 1 1 1 1 1 1 ii 1 1 1 1 1 1 n 1 1 1 T n 1 1 1 



: krrr 



1989 



n(m)20 148 
n(t) 158 



l l 1 1 1 ll 1 1 1 1 1 1 I r ftf I I - 



trh 1 1 1 1 



i m 1 1 1 1 1 1 

5 10 15 20 25 30 35 40 45 



Standard length (cm) 



5 10 15 20 25 30 35 40 45 

Standard length (cm) 



Figure 4 

Length-frequency distribution of the orange roughy {Hoplostethus atlanticus) popu- 
lation by year (stipple=male, clear=female, dashed line=weighted length frequency 
for all years combined, n(m)=number offish measured, nU)=number of trawls from 
which samples were taken, data are scaled by stratum areas to represent total popu- 
lation-size distribution). 



July; ripe fish dominated through mid-July; and the 
proportion of spent fish increased progressively from 
low levels during the first two weeks in July to peak 
in the third or fourth week. 



Data are insufficient to examine regional varia- 
tion in this pattern, but there may be some differ- 
ences between areas; fish appear to spawn slightly 
later on the Westpac Bank than those on the Central 



246 



Fishery Bulletin 92(2). 1994 



Central flat area 



Males 



MIm 



i { 



Females 



\ H H i * 



1984 1965 1986 1967 1986 1989 1990 



Pinnacles 



1 



I 



1 



1 1 1 1 1 1 1 

1984 1985 1986 1987 1988 1989 1990 



it** 



i r - 



36 


Westpac Bank 






J6 - 






34 






32- 










30 








28- 







— I 1 1 1 

1987 1988 1989 1990 



Year 



Figure 5 

Mean length (±2 standard errors) of orange roughy (Hoplostethus atlanticus) by year 
in the three main spawning areas: Central Flat, Pinnacles, and Westpac Bank. 



Flat and Pinnacles. The increase in ripe fish towards 
the end of the 1990 survey was due largely to sam- 
pling the Westpac Bank at this time. 

The onset of spawning, defined as the first date 
on which 20% of fish sampled were spent (after 
Pankhurst, 1988), has been relatively consistent 
over the years (Table 11). Actual dates based on fe- 
males have ranged from 9 July to 16 July. 

Size at maturity 

Mean lengths at maturity for males and females by 
year are given in Table 12. There is a significant 
trend of decreasing mean size for males (linear re- 
gression F-test, P<0.05), but there is no consistent 
trend for females. 

Feeding 

Data on frequency of occurrence of broad taxonomic 
prey groups from 1984 to 1990 showed the most 



common prey were natant decapod crustaceans and 
fish (Table 13). 

The main groups that could be identified were 
macrourids (small species of Coelorinchus and 
Coryphaenoides) and myctophids (species of 
Lampanyctus and Lampanyctodes). Natant decapod 
crustacean prey were mainly species in the genera 
Pasiphaea, Sergestes, Oplophorus, and Acan- 
thephyra. Squids and amphipods were also frequent 
prey. 



Discussion 

Orange roughy on the Challenger Plateau were over- 
exploited in the late 1980s. Research trawl survey 
and commercial catch and effort data show similar 
changes in distribution and abundance. There was 
a marked contraction in the area of high catch rates, 



Clark and Tracey: Population changes of Hoplostethus atlanticus on the Challenger Plateau 247 







Table 10 








Gonad stage 


proportions of femal 


i orange roughy 


(Hoplostethus 


atlanticus 


) by area by 


year ( 


n = sample 


size; 1 = immature/resting, 


2 = early matura 


tion, 


3 = maturation, 4 


= ripe 


5 = running ripe, 


6 = spent). 


Area and year 






Gonad stage 






1 


2 


3 


4 


5 


6 


n 


Central Flat 
















1987 





2.8 


81.9 


14.7 





0.6 


531 


1988 





1.2 


3.4 


20.3 


17.1 


58.0 


438 


1989 


0.3 


1.2 


20.5 


46.5 


12.4 


19.1 


591 


1990 


0.4 


2.0 


13.3 


41.1 


10.0 


33.2 


460 


Pinnacles 
















1987 


ill 


8.5 


74.4 


15.9 





0.8 


246 


1988 





5.0 


9.9 


31.5 


14.0 


39.6 


222 


1989 


(i 


1.6 


17.6 


43.4 


7.3 


30.1 


426 


1990 


0.3 


1.6 


10.8 


34.9 


9.0 


43.4 


378 


Westpac Bank 
















1987 





45.6 


50.9 








3.5 


57 


1988 


i) 


33.7 


16.3 


32.6 


2.3 


15.1 


86 


1989 





21.4 


19.1 


35.7 


9.5 


14.3 


84 


1990 


3.9 


15.1 


17.5 


35.9 


8.7 


18.9 


206 









Table 1 1 




Date at 


whi 


ch 


20% of orange 


roughy (Hoplo- 


stethus o 


tlan 


ticus) sampled were spent. 


Year 






Male 


Female 


1984 






13 July 


12 July 


1985 






8 July 


9 July 


1986 






after 16 July 


10 July 


1987 






before 12 July 


10 July 


1988 






10 July 


16 July 


1989 






20 July 


15 July 


1990 






11 July 


9 July 









Table 12 






Mean 


length (cm) 


at maturity 


and two sta 


ndard 


errors 


(SE), 


of orange roughy (Hoplosteth 


us at- 


lanticus) by 


sex and year. 






Year 






Male 


Femal 


e 


length 


2 SE 


Length 


2 SE 


1984 




27.1 


0.54 


25.7 


0.68 


1987 




24.4 


0.80 


24.3 


1.02 


1988 




23.2 


1.12 


22.7 


1.56 


1989 




23.6 


1.16 


23.4 


1.38 


1990 




22.3 


1.10 


24.5 


1.00 



a reduction in the number of spawning schools, 
and a marked decline in biomass. Stock reduction 
analyses have estimated virgin biomass to be 
about 110,000 t. The stock had declined to about 
20% of this by 1991, well below the optimal long- 
term biomass of 30% of virgin levels predicted by 
computer modelling under an F 1 fishing strat- 
egy (Clark, 1992). 

It is clear that the Challenger Plateau spawn- 
ing population declined rapidly and substantially 
with commercial fishing in the 1980s. However, 
it is uncertain exactly how much of the change 
was directly attributable to the fishery. There are 
no data on size of the stock prior to its exploita- 
tion, so the level of any natural fluctuations in 
population size and distribution is unknown. It 
is possible that stock size might have decreased 
in the absence of any fishing, but it seems very 
unlikely, given the longevity of orange roughy, 
that such changes would occur as rapidly as we 
observed. There could also have been a progres- 
sive change in the availability of fish in the area 
covered by the trawl surveys or bulk of the com- 
mercial fleet. Adult orange roughy do not neces- 
sarily spawn each year (e.g. Bell et al., 1992; 
authors' unpubl. data) and hence may not migrate 
to the general spawning area. In the early years 
of the fishery, large catches were taken over much 
of the year, but the period of large catches became 
progressively reduced to the winter months (Clark, 
1991a). This suggests that initially there were resi- 
dent fish on the grounds, with a migratory compo- 
nent which used the area for spawning only. If this 
latter group had a variable number of spawners 
each year, this could have affected how well trawl 
survey or CPUE data reflected true biomass. How- 
ever, if this occurred, greater variation in abundance 
indices between years than observed would be ex- 
pected. There could also have been other spawning 
grounds that fish from the 'Challenger stock' used. 
However, there were no indications of this from ei- 
ther commercial or research survey trawling beyond 
the main grounds. A further alternative explanation 
for the observed decline in abundance could be a 
change in vulnerability to the trawl gear, either by 
fish residing above the bottom in midwater, or by 
heavy fishing pressure disrupting existing aggrega- 
tions or preventing their formation. There is no in- 
formation on the former (although no fish marks 
were noted on the echosounder above the bottom 
during the last two research surveys), but the lat- 
ter is likely to have occurred (Clark and Tracey, 
1991). The effects of fishing on school stability could 
have resulted in a greater decline in catch rates 
than true abundance, but reduced stability of schools 



248 



Fishery Bulletin 92(2), 1994 



00- 


1984 


Male 


80- 






60- 






40- 






20- 


X 


^/C*--~^ 


0- 




r * •   i ' * • * i  ' * • i  '  • i 



1987 



1988 



1989 



was not observed prior to 
1988, and so does not ex- 
plain the consistent 
downward trend in CPUE 
indices. Hence, although 
alternative hypotheses 
cannot be discounted, 
fishing is most likely to 
have been the major fac- 
tor in the observed deple- 
tion of the stock. 

Most other 'bycatch' 
species also declined in 
abundance, although 
changes were relatively 
minor compared with 
that of orange roughy. 
There was no strong in- 
dication of any 'species 
replacement' of orange 
roughy. The fishery on 
the Challenger Plateau 
targets specifically or- 
ange roughy, and other 
species are not caught in 
large quantities. In the 
trawl surveys, orange 
roughy have generally 
accounted for over 95% 
of the biomass. The com- 
mercial fishery would 
probably take even less 
bycatch than the surveys 
because it focuses on the 
aggregations which are 
usually almost exclu- 
sively orange roughy. In- 
tuitively, some compen- 
satory increase in other 
components of the Chal- 
lenger Plateau commu- 
nity is to be expected 
because of the extent of 
orange roughy depletion, 
but there is no informa- 
tion on biomass, trophic 
interactions, and produc- 
tivity of other fish or in- 
vertebrate species. In 

addition, even if most of the other finfish species 
have higher fecundity and faster growth rates than 
orange roughy, there could be a relatively long re- 
sponse time to changes in species dominance. 

There has been no apparent change in the size 
structure of the orange roughy population. With 



Female 





1990 





July date 

Figure 6 

Relative proportions of maturing, ripe, and spent gonads of orange roughy 
iHoplostethus atlanticus) by day during research surveys in 1984 and 1987-90 (5 
day running mean; maturing=dashed line, ripe=solid line, spent=dotted line; 
maturing=stage-3 male, stage-3 female; ripe=stage-4 male, stages 4 and 5 female; 
spent=stage-5 male, stage-6 female). 



heavy exploitation, a truncation of the length fre- 
quency distribution and a reduction in the mean size 
of fish in the population might have been expected, 
as larger fish were removed and new recruits en- 
tered the population. Such changes in size structure 
of exploited populations are well documented (e.g. 



Clark and Tracey: Population changes of Hoplostethus atlanticus on the Challenger Plateau 



249 











Table 


13 










Frequency of occurrence 


of 


major prey groups of orange roughy (Hoplosteth 


is atlant 


cus) by year. 










1984 


1985 


1986 


1987 


1988 


1989 


1990 


Crustacea 




















Amphipoda 






13.5 


7.6 





6.3 


8.0 


19.1 


5.9 


Decapoda/Natantia 






53.8 


56.1 


22.8 


44.5 


43.0 


23.5 


34.5 


Euphausiacea/Mysidacea 






4.3 


0.7 


13.6 


7.7 


8.0 


2.8 


2.3 


Crustacean remains/other 


groups 


6.4 


5.3 


9.1 


13.5 


9.3 


10.0 


9.3 


Mollusca 




















Cephalopoda 






14.5 


9.1 


13.6 


10.4 


10.6 


9.5 


7.7 


Thaliacea 




















Salpidae 






— 






— 


0.3 


0.4 


0.7 


Teleosts 






45.7 


29.5 


40.9 


33.1 


30.1 


36.3 


36.6 



Smith, 1968; Gulland 1971; Edwards and Bowman, 
1979; Grosslein et al., 1980; Rowling, 1990), al- 
though none of these studies have dealt with a spe- 
cies as long-lived or slow-growing as orange roughy. 
The length frequency distribution of spawning or- 
ange roughy consists largely of 25^10 cm fish. These 
sizes are probably fully vulnerable to trawl gear 
with 100 mm mesh size (legal minimum). Hence, 
there could be relatively constant fishing mortality 
across all size groups. There have been no indica- 
tions of large numbers of new recruits in the length 
frequency data. This may suggest low levels of re- 
cruitment, or at least no entry of any strong year 
class since 1984 that would reduce mean size. 

Interpretation of changes in size structure is also 
limited by the lack of age data for adult orange 
roughy. Available ageing data (Mace et al., 1990; 
MAF Fisheries 3 ) for orange roughy suggest a wide 
range of ages for a given length, and it is possible 
that age structure may change more rapidly than 
size structure. Smith et al. ( 1991) reported a reduc- 
tion in genetic diversity of orange roughy from sev- 
eral New Zealand areas, including the Challenger 
Plateau, and suggested this was due to higher mor- 
tality of older fish that may remain longer on the 
spawning grounds than that of younger fish. 

Size at maturity showed a significant decline in 
males, but not in females. It is possible that one sex 
could be more vulnerable to fishing, but there are 
no indications of unbalanced sex ratios in commer- 
cial catches (authors' unpubl. data). Macroscopic 
examination of gonads for identification of gonad 
stage is more reliable in females, where criteria 
based on colour and size of oocytes are clearer than 
the presence of milt in male gonads. However, the 
data may not be representative of true size at ma- 



MAF Fisheries, unpubl. data, 1993. 



turity in the total population. It is possible that the 
size at maturity measured here is lower than the 
true population value because fish that migrate to 
the spawning grounds are primarily those that are 
mature, and the relative proportions of immature and 
mature small fish are not accurately represented. 

The apparent lack of change in size at maturity 
is not surprising in view of the stability of the total 
population length frequency. An increase in growth 
rate, with a corresponding reduction in the age at 
maturity, of individuals in an exploited population 
is well documented (e.g. Pitt, 1975; Spangler et al., 
1977; Borisov, 1978; Hempel, 1978; Leaman, 1991). 
However, Pitt (plaice, Hippoglossoides platessoides, 
on the Grand Banks) and Leaman (Sebastes spp. in 
the north Pacific Ocean) noted that whereas age at 
first maturity decreased with exploitation, size at 
maturity remained the same. Orange roughy are 
estimated to be about 24 years of age at maturity 
(Mace et al., 1990), and hence such functional 
changes in growth rate or maturity may not be ob- 
vious after 10 years of fishing, despite a major re- 
duction in population size. 

Orange roughy on the Challenger Plateau have 
consistently spawned in the same general area at 
the same time of year from 1984 to 1990. The go- 
nad-stage pattern observed in trawl surveys has 
been similar each year. However, there is evidence 
of some regional variability in the proportion of fish 
spawning. The Central Flat and Pinnacles have con- 
sistently sustained levels of spawning fish over 90%. 
On the Westpac Bank this proportion has been 
lower, and the percentage spawning has progres- 
sively increased from 1987 (54%) to 1990 (81%). 
Reasons for this are not clear. Sample sizes from the 
Westpac Bank are smaller than those from the other 
areas but still come from at least six trawls, which 
should give a representative sample. In 1987 no 



250 



Fishery Bulletin 92(2), 1994 



actively spawning fish were caught, perhaps because 
the survey had been taken in June/early July and 
peak spawning on the Westpac Bank could have 
occurred slightly later than in the other two areas 
(Clark, 1991b). Originally it was thought that fish 
on the Westpac Bank migrated east to the Central 
Flat and Pinnacles for spawning (Clark and Tracey, 
1988). However, in subsequent years ripe and run- 
ning-ripe fish were found. Nevertheless, in 1987 
there was a large proportion of fish that were not 
spawning that year. It is possible that the Westpac 
Bank has only developed as a spawning ground 
since 1987, but if so, whether heavy fishing on the 
other grounds was a factor is unknown. The bio- 
mass index on the Westpac Bank has declined since 
1987, so it is unlikely that there has been a major 
shift of fish from the Central Flat or Pinnacles. 

The time of spawning (defined by 20% spent) has 
consistently been in the second and third weeks of 
July. Pankhurst (1988) reported that day length was 
a critical factor in synchronizing the reproductive 
cycle of orange roughy. The changes in dates of 20% 
spent between years do not correlate exactly with 
annual changes in the shortest day, but day length 
could nevertheless be an important general cue. 
Gonadal development has remained consistent de- 
spite major changes in the size of the population and 
the spawning school structure. There are indications 
that heavy fishing pressure may disrupt the stabil- 
ity of schools of orange roughy (Clark and Tracey, 
1991). In 1989 when fishing effort was at its peak, 
a comparatively high proportion of the biomass was 
in 'background' areas, outside the three main re- 
gions of spawning activity. Catch rates in the spawn- 
ing areas were lower than in other years. It is pos- 
sible that fishing pressure was affecting the forma- 
tion of aggregations, but nevertheless reproductive 
development still occurred normally. However, the 
success of spawning could have been reduced be- 
cause the fish were more dispersed. 

The diet of orange roughy, and the relative fre- 
quency of occurrence of prey groups, were similar 
over the period examined. Natant decapod crusta- 
ceans and fish remains have dominated the diet. 
This diet composition concurs with other accounts 
of orange roughy feeding habits in New Zealand 
waters (e.g. Liwoch and Linkowski 1986; Rosecchi 
et al., 1988) and is similar to diet composition of 
orange roughy in the North Atlantic Ocean (e.g. 
Mauchline and Gordon, 1984; Gordon and Duncan, 
1987), Indian Ocean (Kotlyar and Lipskaya, 1981), 
and off southeastern Australia (Bulman and Koslow, 
1992). The trophic effects of the decline in orange 
roughy biomass are unknown. There is little infor- 
mation on predator-prey relationships within com- 



munities containing orange roughy. Published feed- 
ing studies and observations from research cruises 
at different times during the year (authors' unpubl. 
data) indicate that orange roughy do not prey on 
eggs or larvae of other fish species. The only pub- 
lished data on predation of orange roughy record 
them in stomachs of seal shark on the Challenger 
Plateau (Clark and Tracey, 1988). Sperm whales 
(Physeter catodon) are often observed in orange 
roughy spawning areas, and although they can dive 
to depths of over 1000 m. It is uncertain whether 
they feed on orange roughy. 

Orange roughy are slow-growing and long-lived 
with low productivity, making them highly suscep- 
tible to the effects of overfishing. Long-term sustain- 
able yield for the Challenger Plateau stock is esti- 
mated at 1.6% of virgin biomass (Clark, 1992). In 
the early years of a developing fishery catch levels 
are likely to be high. The schooling behavior of or- 
ange roughy for spawning or feeding means that 
large catches can be taken in a short time, and high 
catch rates may be maintained despite decreasing 
biomass. CPUE declined on the Challenger Plateau 
but not as consistently on the Chatham Rise where 
the population was also reduced by heavy fishing 
(Francis et al., 1992), although there was a progres- 
sive shortening of the period over which high catch 
rates occurred (Coburn and Doonan, in press). 

In 1986, the TAC on the Challenger Plateau was 
increased from 6,000 to 10,000 t in order to assess 
the impact of heavier fishing and to learn more 
about the productivity of orange roughy. At that 
stage there was little understanding of stock size, 
or age and growth characteristics of the species. 
Hence the intention was to increase catch suffi- 
ciently to provide a contrast in abundance indices 
and give information on the resilience of the stock. 
However, there were several problems with this 
'adaptive management' strategy as applied to Chal- 
lenger Plateau orange roughy. The first was that it 
began without good data on the abundance of the 
stock against which to measure any change. It would 
have been preferable to have had at least two years 
of abundance data before increasing fishing pres- 
sure. At the time, CPUE had not been examined, 
and trawl survey results were inadequate to esti- 
mate biomass. A new time series of trawl surveys 
began in 1987, and although the 1988 survey 
showed a large decrease, with only two survey re- 
sults we could not be confident about interpreting 
the differences as a strong decline in stock size. A 
further difficulty with such management is that 
with a slow-growing species like orange roughy, 
potential effects of any changes in spawning stock 
size on recruitment will not be evident for 20-25 



Clark and Tracey: Population changes of Hoplostethus atlanticus on the Challenger Plateau 



251 



years when the results of that year's spawning re- 
cruit to the fishery. Hence, until that time the fish- 
ery will be removing only accumulated adult stock 
and low levels of virgin stock recruitment. A third 
important feature of adaptive management is the 
understanding that it can involve high risk to a 
species like orange roughy. Changes in biomass 
could occur rapidly and any quota system and in- 
dustry response must be flexible, so catch levels can 
be reduced rapidly. 

The recovery of orange roughy from heavy fish- 
ing may be slow. Their fecundity is low at 20,000- 
30,000 eggskg -1 body weight (Pankhurst and 
Conroy, 1987; Clark and Tracey, 1991). There is no 
evidence of a marked change in fecundity of Chal- 
lenger Plateau fish over the period 1987-90 (au- 
thors' unpubl. data), but Leaman (1991) reported 
reduced fecundity in exploited stocks of Sebastes 
alutus, rather than an increase which might have 
been expected. In addition, Leaman and Beamish 
(1984) suggested a possible correlation between lon- 
gevity of a species and the period between strong 
year classes. Brown et al. ( 1983) noted that a reduc- 
tion in population size of several species in the 
Georges Bank region to low levels ( 10-20% of peak 
abundance) was followed by less frequent occurrence 
of strong year classes. 

High vulnerability to fishing and possible slow 
recovery from over-fishing are important for man- 
agement of orange roughy fisheries. Data over a 
comparatively long time period are required to pro- 
vide a basis for sound management of long-lived 
species (Leaman, 1991). It is clear with orange 
roughy on the Challenger Plateau that such species 
can be overfished in a much shorter time than that 
required for the desired data collection. Hence, de- 
velopment of an orange roughy fishery needs care- 
ful control from the outset. It is important that re- 
search occurs in advance of substantial fishing, so 
that baseline data on distribution, abundance, and 
biology are collected. The most commonly used tech- 
niques for stock assessment of orange roughy (trawl 
survey, acoustic survey, CPUE analysis) provide 
relative abundance indices, and therefore require 
several surveys before absolute biomass can be de- 
termined. Results of surveys in other areas, where 
the relation between survey indices and true biom- 
ass has been established, may be useful, but only if 
gear, bottom type, and fish distribution are similar. 
Egg production surveys have been carried out in 
both New Zealand and Australia, and may enable 
more rapid assessment in some localized areas. 
'Adaptive management,' as discussed above, may be 
appropriate as an aid to estimate biomass by stock 
reduction methods, but it must be carried out with 



flexibility in order to change catch levels quickly. If 
development of the fishery is carefully regulated in 
the first few years while such data are collected, 
later management problems such as too many ves- 
sels involved in the fishery and the need to quickly 
and substantially decrease quota levels could be 
avoided. 



Acknowledgments 

The authors thank those too numerous to name, who 
have participated in research cruises over the years 
which provided the basic data for this study. We also 
thank Chris Francis and Ian Doonan for statistical 
advice, Ralph Coburn for some of the commercial 
data extracts, and Kevin Sullivan and John Annala 
(all MAF Fisheries) as well as two anonymous jour- 
nal referees for constructive comments on the manu- 
script. 



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Sebastes stocks. Env. Biol. Fish. 30:253-271. 

Leaman, B. M., and R. J. Beamish. 

1984. Ecological and management implications of 
longevity in some Northeast Pacific 
groundfishes. Int. North Pac. Fish. Comm. Bull. 
42:85-97. 

Liwoch, M., and T. B. Linkowski. 

1986. Some biological features of orange roughy 
Hoplostethus atlanticus (Trachichthyidae) from 
New Zealand waters. Pr. morsk. Inst. ryb. Gdyni 
21:27-41. 

Mace, P. M., J. M. Fenaughty, R. P. Coburn, and I. 
J. Doonan. 

1990. Growth and productivity of orange roughy 
(Hoplostethus atlanticus) on the north Chatham 
Rise. N.Z. J. Mar. Freshwater Res. 24:105-119. 
Mauchline, J., and J. D. M. Gordon. 

1984. Occurrence and feeding of berycomorphid 
and percomorphid teleost fish in the Rockall 
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Pankhurst, N. W. 

1988. Spawning dynamics of orange roughy, 
Hoplostethus atlanticus, in mid-slope waters of 
New Zealand. Env. Biol. Fish. 21:101-116. 
Pankhurst, N. W., and A. M. Conroy. 

1987. Size-fecundity relationships in the orange 
roughy, Hoplostethus atlanticus. N.Z. J. Mar. 
Freshwater Res. 21:295-300. 

Pankhurst, N. W., P. J. McMillan, and D. M. Tracey. 
1987. Seasonal reproductive cycles in three com- 
mercially exploited fishes from the slope waters off 
New Zealand. J. Fish Biol. 30:193-212. 
Pauly, D. 

1979. Theory and management of tropical multi- 



Clark and Tracey. Population changes of Hoplostethus atlanticus on the Challenger Plateau 253 



species stocks. A review, with emphasis on the 
Southeast Asian demersal fisheries. ICLARM 
Stud. Rev. 1. 
Pearson, E. S., and H. O. Hartley (eds.). 

1976. Biometrika tables for statisticians. 2 
vols. Cambridge Univ. Press, Cambridge. 
Pitt, T. K. 

1975. Changes in abundance and certain biological 
characteriplatessoides. sties of Grand Bank Ameri- 
can plaice, Hippoglossoides platessoides. J. Fish. 
Res. Board Can. 32:1383-1398. 
Regier, H. A., and K. H. Loftus. 

1972. Effects of fisheries exploitation on salmonid 
communities in oligotrophic lakes. J. Fish. Res. 
Board Can. 29:959-968. 
Robertson, D. A. 

1991. The New Zealand orange roughy fishery: an 
overview. In K. Abel, M. Williams, and P. Smith 
(eds.), Australian and New Zealand southern trawl 
fisheries conference. Aust. Bureau of Rural Re- 
sources Proc. 10:38-48. 
Rosecchi, E., D. M. Tracey, and W. R. Webber. 

1988. Diet of orange roughy, Hoplostethus atlanticus 
(Pisces: Trachichthyidae) on the Challenger Plateau, 
New Zealand. Mar. Biol. 99:293-306. 
Rowling, K. R. 

1990. Changes in the stock composition and abun- 



dance of spawning gemfish Rexea solandri f Cuvier), 
Gempylidae, in southeastern Australian 
waters. Aust. J. Mar. Freshwater Res. 41:145-163. 
Russ, G. R., and A. C. Alcala. 

1989. Effects of intense fishing pressure on an as- 
semblage of coral reef fishes. Mar. Ecol. Prog. 
Ser. 56:13-27. 

SAS. 

1988. SAS/STAT Users Guide, Release 6.03 ed. 
SAS Institute, Cary, NC. 
Smith, P. J., R. I. C. C. Francis, and M. McVeagh. 
1991. Loss of genetic diversity due to fishing pres- 
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Smith, S. H. 

1968. Species succession and fishery exploitation in 
the Great Lakes. J. Fish. Res. Board Can. 
25:667-693. 
Spangler, G. R., N. R. Payne, J. E. Thorpe, J. M. 
Byrne, H. A. Regier, and W. J. Christie. 

1977. Responses of percids to exploitation. J. Fish. 
Res. Board Can. 34:1983-1988. 
Tracey, D. M., P. J. McMillan, J. H. Armstrong, 
and D. A. Banks. 

1990. Orange roughy trawl survey: Challenger Pla- 
teau and west coast South Island, 1983. N.Z. 
Fish. Tech. Rep. 22, 34 p. 



Abstract. — Restriction-fragment 
length polymorphism (RFLP) 
analysis of mitochondrial mtDNA 
was used to identify morphologi- 
cally similar eggs of spring spawn- 
ing sciaenids in lower Chesapeake 
Bay. During spring 1990 and 1991, 
ichthyoplankton surveys were con- 
ducted in lower Chesapeake Bay 
to estimate seasonal egg produc- 
tion and population biomass of 
black drum, Pogonias cromis. 
Rearing experiments indicated 
that at least three species of 
sciaenid (silver perch, Bairdiella 
chrysoura; weakfish, Cynoscion 
regalis and P. cromis) were spawn- 
ing in the survey area during both 
years. Specific identification of 
eggs based on previously pub- 
lished ranges of outside egg diam- 
eter (OED) were not reliable be- 
cause of considerable overlap in di- 
ameter distributions. However, 
analysis of weekly OED frequen- 
cies revealed the presence of three 
modes which differed in temporal 
occurrence, suggesting the prod- 
ucts of three species. Genetic typ- 
ing of eggs using RFLP analysis of 
mtDNA confirmed the presence of 
three species, but demonstrated 
that eggs of certain size classes 
represented two species. These 
results illustrate that reliance on 
previously published ranges of egg 
diameter for specific identification 
of spring-spawning sciaenids may 
overestimate the spawning bio- 
mass of black drum in Chesapeake 
Bay by as much as 50% owing to 
misidentification of weakfish eggs. 



Morphometric and genetic 
identification of eggs of 
spring-spawning sciaenids in 
lower Chesapeake Bay* 



Louis B. Daniel III 

John E. Graves** 

School of Marine Science 
Virginia Institute of Marine Science 
The College of William and Mary 
Gloucester Point, Virginia 23062 



At least five species of the family 
Sciaenidae (silver perch, Bairdiella 
chrysoura; spotted seatrout, 
Cynoscion nebulosus; weakfish, C. 
regalis; northern kingfish, Menti- 
cirrhus saxatilis; and black drum, 
Pogonias cromis) are purported to 
spawn during the spring in lower 
Chesapeake Bay (Joseph et al., 
1964; Lippson and Moran, 1974; 
Johnson, 1978; Brown, 1981; Olney, 
1983; Cowan et al., 1992). The eggs 
of spring-spawning sciaenids in 
lower Chesapeake Bay are morpho- 
logically similar, ranging in outside 
egg diameter (OED) from 0.66 to 
1.18 mm, and having single or 
multiple oil globules of varying 
sizes (Johnson, 1978; Olney, 1983). 
As a result, specific identification of 
eggs based on morphological crite- 
ria is problematic. Holt et al. ( 1988) 
suggested that it may not be pos- 
sible to determine the specific iden- 
tity of sciaenid eggs from morpho- 
logical criteria; Joseph et al. (1964) 
reported that positive identification 
could only be achieved with supple- 
mental hatching studies. 

Hatching studies have tradition- 
ally been used to identify morpho- 
logically similar eggs, including 
those of sciaenids. Joseph et al. 
(1964) cultured eggs of several sci- 
aenids collected at a single station 



in southern Chesapeake Bay (16 
May 1962) and raised larvae to an 
identifiable size (5-7 mm). The 
smallest eggs (0.630-0.777 mm) 
were found to be B. chrysoura, 
whereas the larger eggs (0.814- 
1.110 mm) developed into P. cromis. 
Culture of eggs (0.777-0.950 mm) 
collected during early June pro- 
duced no P. cromis but did result in 
larvae of B. chrysoura and C. 
regalis. In contrast, Olney (1983) 
suggested that eggs of P. cromis, C. 
regalis, B. chrysoura, and Ment- 
icirrhus spp. were included in a 
size-frequency distribution of mor- 
phologically similar eggs collected 
from May through August in lower 
Chesapeake Bay, but that identifi- 
cations based on diameter were 
ambiguous because of the high de- 
gree of overlap in diameter distri- 
butions (Table 1). Confounding this 
problem is the observation that egg 
size may change with varying sa- 
linity or as the spawning season 
progresses (Johnson, 1978). 

Because many species of Sci- 
aenidae in lower Chesapeake Bay 
spawn concurrently and have mor- 
phologically similar eggs, most 
studies have relied either on previ- 
ously published egg size distribu- 
tions or rearing for identification 
(Holt et al., 1985, 1988; Comyns et 



Manuscript accepted 10 November 1993 
Fishery Bulletin 92:254-261 (1994) 



"Contribution No. 1818 of the Virginia Institute of Marine Science. 
**To whom reprint requests and correspondence should be sent. 



254 



Daniel and Graves: Morphometry and genetic identification of sciaenid eggs 



255 







Table 1 




Reported range 


of outside egg diameter (OED) and study location for 


spring-spawning sciaenids. 


Species 


OED (mm) 


Location 


Author! s) 


Bairdiella chrysoura 


0.62-0.78 


Chesapeake Bay 


Joseph et al., 1964 




0.59-0.82 


NW Gulf of Mexico 


Holt et al., 1988 


Cynoseion nebulosus 


0.60-0.85 


NW Gulf of Mexico 


Holt et al., 1988 




0.70-0.85 


NW Gulf of Mexico 


Fable et al., 1978 


Cynoscion regalis 


0.68-1.18 


Long Island Sound 


Merriman and Sclar, 1952 




0.70-1.17 


Chesapeake Bay 


Pearson, 1929 




0.84-0.96 


Delaware Bay 


Wisner, 1965 


Menticirrhus saxatilis 


0.80-0.85 


New Jersey 


Welsh and Breeder, 1923 


Menticirrhus spp. 


0.63-0.87 


NW Gulf of Mexico 


Holt et al., 1988 


Pogonias cromis 


0.82-1.02 


Chesapeake Bay 


Joseph et al., 1964 




0.90-1.20 


NW Gulf of Mexico 


Holt et al., 1988 



al., 1991; Saucier and Baltz, 1992; Saucier et al., 
1992). However, the misidentifications that can result 
from overlapping egg-diameter distributions and the 
time-consuming nature of culture experiments make 
methods based on other characters desirable. 

The application of biochemical genetics has pro- 
vided an alternative to culture for positive identifi- 
cation of morphologically similar eggs. Electrophore- 
sis of water-soluble proteins (allozyme analysis) has 
been used to distinguish between larvae and juve- 
niles of morphologically similar species of marine 
fishes (eg. Morgan, 1975; Smith and Benson, 1980; 
Graves et al., 1988). Similarly, restriction fragment 
length polymorphism (RFLP) analysis of mitochon- 
drial DNA has been employed to discriminate be- 
tween the eggs of three congeneric serranids that 
could not be unambiguously identified with a single 
allozyme locus (Graves et al., 1990). More recently, 
direct sequencing and RFLP analysis of DNA am- 
plified by the polymerase chain reaction (PCR) have 
been used to identify morphologically similar larvae 
of invertebrates (Olson et al., 1991; Silberman and 
Walsh, 1992). 

In this paper we report that identification of eggs 
of sciaenids in lower Chesapeake Bay during spring 
based on published morphological criteria, rearing 
experiments, and genetic analysis are inconsistent. 
These results indicate that it is not possible to iden- 
tify sciaenid eggs accurately by using diameter as 
the sole criteria. In addition, we present the results 
of weekly plots of egg size-frequency distributions 
and a RFLP analysis of mtDNA to determine the 



specific composition of eggs of sciaenids that may be 
present in lower Chesapeake Bay during spring. 

Material and methods 

Weekly zooplankton surveys of the lower Chesa- 
peake Bay were conducted during April and May 
1990 and 1991 to determine the distribution and 
abundance of eggs of black drum for an estimate of 
seasonal egg production. Samples of eggs were ob- 
tained with an in situ silhouette photography sys- 
tem consisting of paired 60-cm diameter, 335-u nets 
fitted to a rigid frame (see Olney and Houde, 1993, 
for a detailed gear description). All deployments 
were 5-minute, stepped-oblique tows and yielded a 
standard plankton sample and a replicate film record. 
Plankton samples were preserved in 5—8% buffered 
formalin and sciaenid eggs were identified by using the 
criteria of Lippson and Moran (1974) and measured 
to the nearest 0.025 mm with a Zeiss Stemi SR stere- 
omicroscope. Ten subsamples of eggs (rc=75-100) 
sorted from preserved plankton samples were 
remeasured to assess measurement error. 

During several cruises in May 1990 and 1991, eggs 
were collected in an area off the city of Cape Charles, 
Virginia, with a 0.5-m Hansen net fitted with 202-u 
mesh to seed 1-liter Imhoff settling cones for hatch- 
ing experiments. Eggs were originally separated as 
Type I (<0.80 mm) and Type II (>0.85 mm) based on 
the morphological criteria of Joseph et al. ( 1964). Rear- 
ing chambers were returned to the laboratory and held 
for 3 to 14 days. In these, larvae were periodically sac- 



256 



Fishery Bulletin 92(2). 1994 



rificed and preserved in 5-8% buffered formalin. Iden- 
tifications of preserved sciaenid larvae from pigment 
characters were based on Ditty (1989). 

Sciaenid eggs collected in the same area during 
spring 1991, 1992, and 1993 were sorted from fresh 
plankton samples. To avoid contamination by the 
morphologically similar eggs of the cynoglossid 
Symphurus plagiusa and the soleid Trinectes macula- 
tus that contain several oil globules and are abundant 
in lower Chesapeake Bay during the spring, all eggs 
with >3 oil globules were omitted from the samples. 
Although eggs of most spring-spawning sciaenids gen- 
erally possess three or fewer oil globules (usually two) 
those of Menticirrhus saxatilis may contain from 1 
to 16 oil globules (Johnson, 1978). After sorting, eggs 
were measured, placed in scintillation vials with 26 
ppt seawater, and frozen at -70°C for genetic analy- 
sis. Individual eggs were thawed and remeasured prior 
to homogenization to assess shrinkage. 

Sciaenid eggs were genetically typed by compar- 
ing mtDNA restriction fragment patterns of indi- 
vidual eggs with those of known adults. To obtain 
patterns of known adults, mature female sciaenids 
(B.chrysoura, C. nebulosus, C. regalis, M. saxatilis, 
and P. cromis) were collected by pound net, trawls, 
and hook and line in April and May 1990 and 1991. 
Ovarian tissue was excised and frozen at -70°C. 
MtDNA was purified from ovarian tissue by cesium 
chloride equilibrium density gradient ultracentrifu- 
gation following the protocols of Lansman et al. 
(1981). To determine a restriction enzyme that un- 
ambiguously identified the different sciaenid spe- 
cies, aliquots of mtDNA were individually digested 
with the following restriction enzymes: Apal, Aval, 
Banl, Banll, Hindlll used according to manu- 
facturer's instructions. The resulting fragments 
were separated electrophoretically on 1.0% agarose 
mini-gels run at 5 V/cm for four hours and visual- 
ized with ethidium bromide. 

MtDNA-enriched genomic DNA was isolated from 
individual eggs following the protocols of Graves et 
al. (1990). Entire DNA samples were digested with 
a single discriminating restriction endonuclease, 
separated electrophoretically, and transferred to a 
nylon filter (Southern transfer) following standard 
protocols (Sambrook et al., 1989). Filters were hy- 
bridized with highly purified black drum mtDNA, 
nick-translated with biotin-7-dATP, washed, blocked 
and visualized following the methods of Graves et al. 
(1990). 

Results 

A total of 10,803 sciaenid eggs was sorted from 
samples collected in 1990 and 1991. Outside egg 



diameter of all specimens ranged from 0.650 to 1.12 
mm. Successive blind readings of samples of 75 to 
100 eggs were used to assess measurement error. No 
differences were found in the size-frequency distri- 
butions indicating good agreement within the 0.025- 
mm size classes (two-sample <-test, P<0.05, n=79). 

Qualitative analysis of culture experiments using 
the two egg types of Joseph et al. (1964) revealed 
the presence of three species. Cultures containing 
eggs designated Type I (<0.80 mm) resulted in lar- 
vae of B. chrysoura, whereas cultures of eggs desig- 
nated Type II (>0.85 mm) resulted in larvae of C. 
regalis and P. cromis. 

Analysis of preserved ichthyoplankton samples 
from 1990 and 1991 revealed the presence of larvae 
of B. chrysoura, C. regalis, and P. cromis. No early 
life history stages of other sciaenids were identified; 
however, yolk-sac larvae could not be identified to 
species. Because rearing studies and analysis of 
field-caught plankton samples revealed the presence 
of more than two species, we could not rely on the 
criteria of Joseph et al. (1964) for specific identifi- 
cation. We therefore examined weekly frequency of 
occurrence of all sciaenid eggs during 1990 (Fig. 1) 
and 1991 (Fig. 2). Based on temporal occurrence and 
size frequency we identified three modes. The larg- 
est eggs (>0.975 mm), Type C, were most abundant 
during the period 23 April through 9 May. Type-C 
eggs declined in abundance throughout May in both 
years. Mid-sized eggs (0.850-0.950 mm), designated 
Type B, generally appeared later than Types A and 
C. Type-B eggs did not exceed 5% of the total fre- 
quency of sciaenid eggs until 15 May 1990 and 9 
May 1991. Type-B eggs increased in abundance from 
mid-May until the end of sampling. The smallest 
eggs (<0.850 mm), designated Type A, co-occurred 
with Type-C eggs; however, they did not exceed 5% 
of the total sciaenid eggs until 8 May 1990 and 9 
May 1991. In 1990, Type-A eggs peaked in abun- 
dance on 15 May and gradually declined through- 
out the sampling period. In 1991, Type-A eggs were 
most abundant during the last sample on 28 May. 

To test the hypothesis that eggs designated Types 
A, B, and C were separate species assemblages, the 
mtDNA restriction fragment patterns of known 
adult sciaenids were compared with those of fresh 
egg samples separated into Types A, B, and C. Re- 
striction fragment length polymorphism analysis of 
mtDNA, purified from adult B. chrysoura, C. 
nebulosus, C. regalis, Menticirrhus saxatilis, and P. 
cromis, revealed species-specific restriction fragment 
patterns for each of the five enzymes. Of the five en- 
zymes, Hindlll showed the greatest differences be- 
tween species, facilitating visualization with the 
Southern blotting procedure (Table 2). 



Daniel and Graves: Morphometry and genetic identification of sciaenid eggs 



257 



> 
o 

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LU 

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23 April 1990 



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15 May 1990 



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0.65 0.75 85 95 1 05 115 



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0.65 0.75 0.85 95 105 1 15 



OUTSIDE EGG DIAMETER (mm) 

Figure 1 

Frequency distributions of outside egg diameters of sciaenid eggs collected 
over six weeks during spring 1990 in lower Chesapeake Bay. 



mm and larger (n=32), all pos- 
sessed the restriction fragment 
pattern diagnostic for P. cromis. 



Discussion 



A total of 62 eggs, representing all sciaenid egg 
size classes collected in lower Chesapeake Bay, was 
identified with diagnostic Hi n dill restriction frag- 
ment patterns. Bairdiella chrysoura, C. regalis, and 
P. cromis were the only species of sciaenids identi- 
fied; no other restriction fragment patterns were 
observed. Genetic identification of eggs designated 
Type A (<0.850 mm, n=12) resulted in 11 individu- 
als of B. chrysoura and one specimen (0.825-mm 
OED size class) of C. regalis (Fig. 3). Cynoscion 
regalis composed the majority of type-B eggs (0.850- 
0.975 mm, rc = 18) analyzed, but seven of the 10 larg- 
est type-B eggs (0.975-mm OED size class) were 
identified as black drum. Type-C eggs, those 1.00 



Identifications of eggs of sci- 
aenids are often based on pub- 
lished diameter distributions or 
hatching experiments, or both. 
Results of hatching experiments 
and genetic analysis in this 
study indicate that samples of 
eggs of a single size class may 
represent the products of two or 
more species. For example, eggs 
designated Type I (<0.80 mm) 
and identified as silver perch by 
Joseph et al. (1964) were shown 
with genetic analysis to contain 
eggs of both weakfish and silver 
perch. Similarly, eggs designated 
Type II (>0.85 mm) and identi- 
fied as black drum by Joseph et 
al. (1964) were shown with rear- 
ing and genetic analysis to con- 
tain eggs of both weakfish and 
black drum. 

During the present study, nei- 
ther hatching experiments nor 
genetic analysis identified eggs 
as black drum that were smaller 
than 0.975 mm OED. While tem- 
porally limited, the results of 
this study suggest that the 
range in size for eggs of black 
drum (0.975-1.125 mm) in lower 
Chesapeake Bay may be more 
restricted than those previously 
reported. 
The ranges of egg diameter overlapped for silver 
perch and weakfish. Eggs genetically identified as 
silver perch ranged in size from 0.650 to 0.825 mm, 
in agreement with previously reported size ranges 
for silver perch in the northwestern Gulf of Mexico 
(0.59-0.82 mm, Holt et al., 1988) and Chesapeake 
Bay (0.625-0.775 mm, Joseph et al., 1964). Although 
Holt et al. (1988) identified eggs of silver perch as 
small as 0.590 mm, no sciaenid eggs smaller than 
0.650 mm OED were collected in the present study. 
Sizes of eggs genetically identified as weakfish were 
found to range from 0.825 to 0.975 mm in diameter. 
These values are comparable with those reported by 
Wisner ( 1965, 0.84-0.96 mm) but are narrower than 



258 



Fishery Bulletin 92(2), 1994 



30 



20 



10 



I I Type A 
 TypeB 
W TypeC 



o 

z 

LU 

o 
cc 



LU 

o 

a: 

LU 
Q. 



20 



15 



the range (0.68-1.18 mm) given 
by Merriman and Sclar (1952) 
for Block Island Sound, New 
York. While the range in sizes 
for silver perch and weakfish re- 
ported in this study agree with 
past research, overlaps in these 
ranges preclude the sole use of 
egg size for identification. 

Neither Joseph et al. (1964), 
Olney (1983), nor the present 
study identified eggs of C. nebu- 
losus or M. saxatilis in samples 
collected in lower Chesapeake 
Bay. Fable et al. (1978) described 
laboratory-spawned eggs of C. 
nebulosus from a single female 
and reported a mean diameter of 
0.77 mm (range 0.70-0.85 mm). 
Although based upon a limited 
sample size, Fable et al.'s data 
indicate that eggs of C. nebu- 
losus could be confused with 
eggs of B. chrysoura; however, no 
eggs in our limited sample of 
this size range (n=12) were ge- 
netically identified as C. nebu- 
losus. A possible explanation for 
the lack of eggs of C. nebulosus 
in the present study may be the 
tendency for adults to spawn in 
or around vegetated areas 
(Brown, 1981). The absence of 
eggs of Menticirrhus spp. in this 
genetic analysis may be ex- 
plained by our exclusion of eggs 
with greater than three oil glob- 
ules. Additionally, Menticirrhus 
saxatilis reportedly spawns off 
front beaches and possibly off- 
shore (deSylva et al., 1962); con- 
sequently, circulation in the bay may prevent eggs 
of this species from entering the survey area or they 
may be transported to areas that were not sampled 
in our study. 

The identification of species-specific restriction 
fragment patterns for spring-spawning sciaenids is 
based on the assumption that there is limited in- 
traspecific variation of the diagnostic restriction 
fragment patterns. Recent studies of the population 
genetics of spotted seatrout, black drum, and weak- 
fish (Graves et al., 1992; Gold et al., 1993) indicate 
that these species exhibit low intraspecific mtDNA 
variability. Furthermore, no variation of the Hi n dill 
fragment pattern was found in a survey of mtDNA 



23 APR 1991 



19 MAY 1991 




20 



10 


















I 


I 




n# 


II 


n 


I, 


IWr- 



65 0.75 0.85 0.95 1.05 1.15 



29 APR 1991 



0.65 75 085 95 1.05 1.15 



22 MAY 1991 




30 



25 



10 























JjlLl. 


I 




}l, .1^1.. 



65 75 85 95 1 05 1 15 



9 May 1991 



065 0.75 085 0.95 1 05 1.15 



28 MAY 1991 













n 


l 


|| 


, PP Ulfl.U, 


ll 


I -I 



20 



15 













I 








I 




p 


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:, 


,<}■,', =m^h 


a- 



65 75 85 95 1.05 1.15 



065 0.75 0.85 0.95 1.05 1.15 



OUTSIDE EGG DIAMETER (mm) 



Figure 2 

Frequency distributions of outside egg diameters of sciaenid eggs collected 
over six weeks during spring 1991 in lower Chesapeake Bay. 



isolated from 25 adult B. chrysoura (L. Daniel, 
unpubl. data). Consequently, the common restriction 
fragment patterns used to distinguish species in this 
study were deemed suitable for use in identifications. 

Variability in egg-size distributions with changing 
salinity and over the spawning season were not exam- 
ined in this study. Consequently, exact size groupings 
may only be applicable to the particular salinity re- 
gime (19-25 ppt) that we sampled. However, samples 
were taken throughout peak spawning for black drum 
and silver perch and may encompass the ranges that 
occur for these species in lower Chesapeake Bay. 

Results of our genetic analysis suggest that iden- 
tifications of eggs of spring-spawning Sciaenidae in 



Daniel and Graves: Morphometry and genetic identification of sciaenid eggs 



259 



Table 2 

Common fragment sizes produced by restriction endonuclease {Hindlll) 
digestion of mtDNA purified from ovarian tissue of spring spawning 
sciaenids. 


Species 




Fragment sizes (Kbi 




Bairdiella chrysoura 5.0 
Cynoscion nebulosus 8.5 
Cynoscion regalis 5.6 
Menticirrhus saxatilis 5.4 
Pogonias cromis 3.3 


3.9 
4.5 
4.3 
3 2 
2.9 


2.8 1.9 

3.8' 

4.1 2.9 

2.4 2.0 

2.7 2.5 


1.7 

1.9 

2.1 


1.7 1.3 

1.8 

1.3 1.0 


' J. Gold, Texas A&M, College Station, TX, 


pers. commun. 1993. 








07 0.7250750775 08 08250.850875 09 09250950975 1 1025105107511 1125 



Outside Egg Diameter (mm) 



B. chrysoura | | C. regalis 



P. cromis 



Figure 3 

Size distributions of all eggs morphologically typed as sciaenids and identi- 
fied using genetic techniques. 



wise, measures of spawning stock 
biomass will be similarly over-es- 
timated, results that could signifi- 
cantly impact management deci- 
sions. Comparable biases in esti- 
mates of egg production and 
spawning stock biomass of weak- 
fish could result from egg mis- 
identifications. However, the more 
protracted spawning season and 
greater area of spawning for 
weakfish in Chesapeake Bay 
(Olney, 1983) would make these 
impacts much less severe. 

Biochemical techniques are 
an important tool for the fur- 
ther study of eggs of sciae- 
nids. Genetic analysis has the 
potential to produce reliable 
results and permit the stor- 
age of samples for later analy- 
sis. Additional studies are 
needed to survey genetic 
identifications over the entire 
spawning season and area to 
determine if egg sizes change 
over time or are influenced by 
seasonal changes in hydrog- 
raphy or by age structure of 
the spawning stock. Finally, 
the use of genetic techniques, 
coupled with an extensive ex- 
amination of morphology 
could lead to the delineation 
of other characters that may 
be useful in separating the 
eggs of these species. 



Acknowledgments 



lower Chesapeake Bay based on OED are subject to 
error. These findings are particularly timely in light 
of the increased use of fishery-independent assess- 
ments of stock size that require precise estimates 
of egg abundance (egg production method). Because 
eggs of black drum and weakfish are spatio-tempo- 
rally coincident and OEDs overlap, estimates of egg 
production by black drum in lower Chesapeake Bay 
may be over-estimated by 50% or greater if identi- 
fication criteria are based solely on egg size. Like- 



J. McGovern, M. Cavaluzzi, 
J. Field, C. Baldwin, and K. 
Kavanaugh kindly assisted 
with sample collection. P. Crewe patiently processed 
plankton samples at sea and in the laboratory, and 
J. McDowell provided valuable technical assistance 
with mtDNA analyses. J. Olney helped in the de- 
sign and implementation of the sampling program 
and provided comments on the manuscript. Addi- 
tional reviews were provided by J. Musick, J. 
Cowan, and E. Heist. This study was funded in part 
by the Virginia Marine Resources Commission un- 
der U.S. Fish and Wildlife Contract F-95-R. 



260 



Fishery Bulletin 92(2). 1994 



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Abstract. — The Atlantic spa- 
defish (Chaetodipterus faber) is the 
only member of the family 
Ephippidae in the western Atlan- 
tic Ocean and its life history is 
poorly understood. We redescribe 
Atlantic spadefish larvae, discuss 
their relationship to known larvae 
of other ephippid genera, and dis- 
cuss the distribution, abundance, 
and seasonal occurrence of Atlan- 
tic spadefish in the northern Gulf 
of Mexico. Larval Atlantic spade- 
fish are characterized by a small, 
peak-like, median supraoccipital 
crest with a single, dorsally di- 
rected spine; large preopercle 
spines, numerous serrate ridges, 
and other spines on the head; a 
deep, robust body which becomes 
laterally compressed; heavy body 
pigmentation; and early develop- 
ment of specialized spinous scales 
or "prescales" (at about 5.5-mm 
standard length [SL]). Transition 
to juvenile stage begins about 8.0- 
8.5 mm SL. Developmental mor- 
phology and head spination of At- 
lantic spadefish is similar to that 
of Pacific spadefish, Chaetodipter- 
us zonatus. Sequence of fin com- 
pletion is pelvics — dorsal and 
anal soft rays — dorsal spines- 
pectorals. Overall, >85% of Atlan- 
tic spadefish larvae were found in 
waters >28.0°C and between 26.7 
and 31.3 ppt. Larvae occur prima- 
rily in coastal waters, except near 
the Mississippi River delta, an 
area with a narrow shelf and rap- 
idly increasing water depths. 
Delta waters may offer additional 
habitat suitable to Atlantic spade- 
fish larvae because of lower salini- 
ties. Larvae are primarily collected 
between June and August and in 
the north-central Gulf of Mexico. 
Larval Atlantic spadefish are ap- 
parently rare in the eastern Gulf 
off Florida. Catch rates near the 
Mississippi River delta during 
August were higher than else- 
where in the north-central Gulf 
and suggest a possible association 
with riverine frontal areas which 
requires further study. 



A re-description of Atlantic spadefish 
larvae, Chaetodipterus faber (family: 
Ephippidae), and their distribution, 
abundance, and seasonal occurrence 
in the northern Gulf of Mexico 



James G. Ditty 
Richard F. Shaw 
Joseph S. Cope 

Coastal Fisheries Institute, Center for Coastal, Energy, and Environmental Resources 
Louisiana State University, Baton Rouge, LA 70803 



The percoid family Ephippidae is 
usually considered to comprise five 
genera and 17 species (Nelson, 
1984). The Atlantic spadefish (Chae- 
todipterus faber) is the only mem- 
ber of this family in the western 
Atlantic Ocean. Rare north of 
Chesapeake Bay, Atlantic spadefish 
inhabit coastal waters which ex- 
tend southward to Brazil (Johnson, 
1978). Historically, Atlantic spade- 
fish represented a relatively minor 
portion of recreational fisheries. 
Nevertheless, fishing tournaments 
are currently being used to stimu- 
late interest in their fisheries 
(Schmied and Burgess, 1987). 
Ryder (1887) described eggs and 
yolk-sac larvae of Atlantic spade- 
fish, but Johnson (1978) questioned 
the identity of these specimens. 
Larvae >2.5 mm standard length 
(SL) are described and illustrated 
by Hildebrand and Cable (1938), 
but this study is insufficient to ex- 
amine important developmental 
details and is based on the static 
rather than dynamic approach to 
larval description (Berry and 
Richards, 1973). Finucane et al. 1 
illustrated 5.1- and 6.4-mm SL At- 
lantic spadefish. Johnson (1984) 
commented on cranial morphology 



and provided insight on the value 
of larval characters in resolving the 
relations among ephippids and 
their relation to other families. 
Aspects of juvenile and adult life 
history are discussed for Atlantic 
spadefish from South Carolina wa- 
ters (Hayse, 1990), but the distri- 
bution, abundance, and seasonal 
occurrence of Atlantic spadefish 
larvae are poorly understood. Our 
objectives are to redescribe the de- 
velopment of Atlantic spadefish lar- 
vae, discuss their relation to known 
larvae of other ephippid genera, 
and to describe the distribution, 
abundance, and seasonal occurrence 
of Atlantic spadefish larvae in the 
northern Gulf of Mexico (Gulf). 



Materials and methods 

The distribution, abundance, and 
seasonal occurrence of larval Atian- 



Finucane. J. H., L. A. Collins, L. E. 
Barger, and J. D. McEachran. 1979. 
Ichthyoplankton/mackerel eggs and lar- 
vae. Environmental studies of the south 
Texas outer continental shelf, 1977. Final 
Rep. to Bur. Land Manage., Wash., DC, 
Southeast Fish. Cent., Natl. Mar. Fish. 
Serv. NOAA, Galveston, TX 77550, 504 p. 



Manuscript accepted 19 August 1993 
Fishery Bulletin 92:262-274 (1994) 



Contribution No. LSU-CFI-92-7 of Louisiana State University Coastal Fisheries 
Institute. 



262 



Ditty et al.: A redescription of Chaetodipterus faber larvae 



263 



tic spadefish were determined from collections taken 
primarily during Southeast Area Monitoring and 
Assessment Program (SEAMAP) ichthyoplankton 
surveys of the Gulf between 1982 and 1986 
(SEAMAP 2 ). These years represent the first time 
interval for which a complete set of data were cur- 
rently available. Latitude 24°30' N was the south- 
ern boundary of our study area in the eastern Gulf, 
a cutoff which approximates the continental shelf 
break off the southern tip of Florida. Latitude 26°00' 
N was the southern boundary of the central and 
western Gulf. These coordinates approximate the 
U.S. Exclusive Economic Zone (EEZ (/Fishery Con- 
servation Zone (FCZ). 

Standard ichthyoplankton survey techniques as 
outlined by Smith and Richardson (1977) were em- 
ployed in data collection. Stations sampled by Na- 
tional Marine Fisheries Service (NMFS) vessels 
were arranged in a systematic grid of about 55-km 
intervals. NMFS vessels primarily sampled waters 
>10 m deep. Each cooperating state had its own 
sampling grid and primarily sampled their coastal 
waters. Hauls were continuous and made with a 60- 
cm bongo net (0.333-mm mesh) towed obliquely 
from within 5 m of the bottom or from a maximum 
depth of 200 m. A flowmeter was mounted in the 
mouth of each net to estimate volume of water fil- 
tered. Ship speed was about 0.75 m/sec; net retrieval 
was 20 m/min. At stations <95 m deep, tow retrieval 
was modified to extend a minimum of 10 minutes 
in clear water or 5 minutes in turbid water. Tows 
were made during both day and night depending on 
when the ship occupied the station. Overall, 1,823 



2 SEAMAP. 1983-1987. (plankton). ASCII characters. Data for 
1982-1986. Fisheries-independent survey data/National Ma- 
rine Fisheries Service, Southeast Fisheries Center: Gulf States 
Marine Fisheries Commission, Ocean Springs, MS (producer). 



bongo net tows were made between 1982 and 1986. 
The SEAMAP effort between 1982 and 1984 also 
involved the collection and processing of 814 neus- 
ton samples taken with an unmetered 1x2 m net 
(0.947-mm mesh) towed at the surface for 10 min- 
utes at each station. SEAMAP sampling during 
April and May was conducted primarily off the con- 
tinental shelf; sampling during March, and from 
June through December, was conducted primarily 
over the shelf at stations <180 m deep. Additional 
information on the spatial and temporal coverage of 
SEAMAP plankton surveys is found in Stuntz et al. 
(1985), Thompson and Bane (1986, a and b), Thomp- 
son et al. (1988), and Sanders et al. (1990). Atlantic 
spadefish larvae were also obtained from surface- 
towed 1x2 m neuston net collections (0.947-mm 
mesh, 71 samples) made by the National Marine 
Fisheries Service (NMFS, Panama City, Florida) 
during August 1988. These NMFS collections were 
associated with riverine/oceanic frontal zones off the 
Mississippi River delta. Frontal zones near the delta 
were not sampled during either June or July. 

A detailed examination of Atlantic spadefish lar- 
vae was made to describe developmental morphol- 
ogy. Body measurements were made on 21 Atlantic 
spadefish larvae between 1.9 and 12.5 mm (Table 1) 
and follow Hubbs and Lagler (1958) and Richardson 
and Laroche (1979). Measurements were made to 
the nearest 0.1 mm with an ocular micrometer in a 
dissecting microscope. We follow Leis and Trnski's 
(1989) criteria for defining length of preopercular 
spines, body depth, head length, eye diameter, and 
the eye diameter/head length ratio. We consider 
notochord length in preflexion and flexion larvae 
synonymous with SL in postflexion larvae and re- 
port all lengths as SL unless otherwise noted. Speci- 
mens were field-fixed in 10% formalin and later 
transferred to 70% ethyl alcohol. Terminology for 















Table 1 












Morphometries of larval Atlan 
surements are expressed as % 


tic spadefish (Chaetodipterus faber) from the northern Gulf 
standard length (SL) and rounded to the nearest whole num 


of M 
ber 


sxico. Mea- 


SL 




N 


Preanal 
length 




Head 

length 


Snout 
length 




Orbit 

diameter 


Body depth 
pectoral 




Prepelvic 

distance 


1.8-2.9 




3 


42-55 




21-31 


3-8 




13-15 


34-44 




— 


3.0-4.9 




3 


54-65 




35-43 


5-7 




15-17 


50-60 




30-36 


5.0-6.9 




1 


60-61 




30-42 


5-6 




15-18 


56-63 




30-35 


7.0-8.9 




4 


61-64 




35-39 


7-9 




11 


55-64 




27-37 


9.0-10.9 




4 


59-61 




34-35 


6-8 




13-14 


60-65 




27-34 


11.0-11.9 




2 


54-56 




34-35 


7-9 




11 


60-65 




27 


12.5 




1 


60 




36 


K 




1 l 


68 




36 



264 



Fishery Bulletin 92|2). 1994 



location of head spines followed Gregory (1933). One 
larva was cleared with trypsin then stained with 
alizarin in each millimeter (mm) length interval to 
examine small serrate ridges around the orbit (i.e. 
circumorbital bones), and spines and ridges on the 
head. We examined spines on the occipital and fron- 
tal bones with a scanning electron microscope 
(SEM), and specialized spinous scales with a com- 
pound microscope. Fin rays were counted when first 
segmented and spines when present. Representative 
specimens were illustrated with the aid of a cam- 
era lucida. 

Estimates of larval density (number of larvae/ 
100m 3 of water) and catch (number of larvae/10 tow) 
were calculated by month. Months were combined 
across years because not all months were sampled 
every year (Appendix Table). Densities for stations 
where larvae were collected (i.e. positive catch sta- 
tions) were calculated by dividing sum of larvae 
collected in bongo net tows by total positive catch 
station volume of water filtered (VWF) and multi- 
plying the result by 100. In addition, an overall (i.e. 
grand) density estimate was calculated by dividing 
sum of larvae by total VWF for all stations sampled 
that month and multiplying the result by 100. Over- 
all density more closely reflects the density of lar- 
vae throughout the area by including the total vol- 
ume of water filtered in calculations. Estimates of 
larval catch in neuston nets were calculated by di- 
viding sum of larvae by number of positive catch 
neuston stations or by total number of neuston sta- 
tions sampled and multiplying the result by 10. 
Estimates of larval density and catch included sta- 
tions at long. >88°00' W because only one Atlantic 
spadefish larva was collected east of Mobile Bay, 
Alabama. Similarly, estimates were calculated only 
for June through August because May and Septem- 
ber had but one positive catch station each. 

Temperature and salinity data were gathered 
from the sea surface. Positive catch station hydro- 
graphic data were multiplied by total number of 
larvae collected at each station to obtain a monthly 
median and mean. Hydrographic data were also 
combined across months to obtain an overall (i.e. 
grand) median and mean. This method gives weight 
to distribution of larvae rather than to distribution 
of stations. We used a percent cumulative frequency 
of >85%> for defining the relation between distribu- 
tion of Atlantic spadefish larvae and water tempera- 
ture, salinity, and station depth. Percent frequency 
indicates the range of hydrographic conditions most 
often associated with occurrences of larvae. Proc 
Univariate was used to calculate median, mean, and 
percent cumulative frequency statistics (SAS Insti- 
tute, 1985). 



Results 

Morphometries and pigmentation 

Early larvae were rotund and deep-bodied; body 
depth was >50% SL by 3.5 mm and >60% by 9 mm 
(Table 1). Atlantic spadefish became increasingly 
deep-bodied and laterally compressed after noto- 
chord flexion. There were 24 myomeres but these 
became obscured by pigment in postflexion larvae. 
The head was large and averaged about 35% SL in 
larvae >3.0 mm. Head profile became steep and in- 
creasingly deeper than long. The mouth was termi- 
nal and the upper jaw reached to about mid-eye. 
Eyes were round and large, ranging from 36 to 43% 
of head length in larvae >3.5 mm (i.e. about 14-15% 
SL). The gut was tightly coiled in a single loop and 
the anus was slightly beyond mid-body (usually 
55-60% SL). 

Pigment was largely restricted to the anterior-half 
of the body in early preflexion larvae of Atlantic 
spadefish. On the head of a 1.8-mm larva, external 
pigment was scattered over the mid- and hindbrain, 
nape, opercle, branchiostegal membrane, and along 
the isthmus and quadrate. Internally, pigment was 
present along and above the anterior portion of the 
notochord, and a single median patch was observed 
on the roof of the mouth. On the abdomen, there was 
a patch of pigment on the visceral mass immediately 
anterior to and below the pectoral-fin base. In ad- 
dition, melanophores were scattered over the pecto- 
ral fin base and its finfold and were distributed lat- 
erally over the visceral mass and hindgut. A row of 
about 20-25 small, closely spaced melanophores 
were visible along the ventral midline of the tail in 
early larvae. Number of melanophores along the 
ventral midline of the tail decreased as larvae grew. 
Melanophores on the nape, opercle, pectoral-fin 
base, and visceral mass formed a "swath" of pigment 
over the anterior 55-60% of the body by 2.5-3.0 mm 
(Fig. 1). By 3.0—3.5 mm, internal melanophores were 
visible anteriorly on the forebrain and laterally on 
the midbrain above the eye. Melanophores were also 
scattered both internally and externally over the 
hindbrain both anterior to and posterior to the base 
of the supraoccipital crest. By early postflexion (i.e. 
5.0 mm), the head and abdomen were densely pig- 
mented but the posterior portion of the body was 
sparsely pigmented. Pigmentation increased on the 
posterior-half of the body as larvae grew, and by 10.0 
mm the entire body was pigmented (Fig. 1). Consoli- 
dation of pigment into bands began on the head of 
Atlantic spadefish larvae with one band visible 
above the eye by 10.0-11.0 mm. This band of pig- 
ment was enclosed by indefinite, pale crossbars. The 



Ditty et al.: A redescription of Chaetodipterus faber larvae 



265 



anterior pale crossbar was situated above the middle 
of the eye and the posterior crossbar was behind the 
eye, extending mid-way down the preopercle. Lar- 
vae <12.5 mm had only one band of pigment (Fig. 1). 
The pelvics were the first fins to have pigment. 
Pelvic fin buds were pigmented by 4.0 mm; the 
pelvics were densely pigmented thereafter. Pigment 






Figure 1 

Larval development of Atlantic spadefish, Chaetodipterus faber, from the 
northern Gulf of Mexico. (All. 8 mm; (Bl 3.5 mm; (C) 5.0 mm; (D) 7.0 mm; 
(E) 11.6 mm. All measurements are standard length (SL). 



appeared on the pectoral fin along the proximal 
portion of the rays at about 4.0-4.5 mm. Melano- 
phores were lightly scattered over the pectoral fin 
in the largest specimen examined (Fig. 1). Melano- 
phores were scattered over the membrane covering 
the anterior-most dorsal spines by about 6.0 mm and 
the anal spines by about 8.0 mm. Melanophores 
were added along the dorsal and 
anal fins as larvae developed, cov- 
ering the proximal-third of each 
soft ray in the largest specimen 
examined. Pigment was present 
along the proximal portion of the 
central rays of the caudal fin by 
11.0 mm (Fig. 1). 

Head and body spination 

Atlantic spadefish larvae develop 
two series of preopercular spines, 
one along the posterior margin of 
the outer shelf and the other 
along the inner shelf. Both the 
outer and inner shelf have dorsal 
and ventral limbs. Three pre- 
opercular spines were present 
along the outer shelf of a 1.8-mm 
larva, the largest of which was 
present at its preopercular angle 
(Fig. 1). A fourth and a fifth spine 
were added by 3.5 mm, one dor- 
sal and one ventral to the angle 
of the preopercle. A sixth preop- 
ercular spine, smaller than the 
others and often difficult to locate, 
was present by 5.0 mm. This sixth 
spine was the anterior-most spine 
along the ventral limb of the ex- 
terior shelf and was resorbed by 
11.0-12.0 mm in some specimens. 
One larva we examined had seven 
preopercular spines along the 
outer shelf but most had two 
spines along the dorsal limb, one 
at the angle, and three along the 
ventral limb (Fig. 2). Spines along 
the outer shelf were simple. Two 
to three spines were also present 
along the inner shelf of the 
preopercle by 3.5 mm. Number of 
spines along the inner shelf in- 
creased as larvae grew, resulting 
in a serrate margin (Fig. 2). A 
small, poorly developed opercle 



266 



Fishery Bulletin 92|2). 1994 



spine was forming by 5.0 mm and 
was difficult to locate on larvae 
not cleared and stained. A spine 
also was present along the poste- 
rior margin of the interopercle 
near its junction with the 
subopercle by 6.0 mm (Fig. 2). The 
interopercular spine often was 
hidden by the large spine at the 
preopercular angle but was more 
easily located as the preopercular 
angle spine regressed. 

Atlantic spadefish larvae have 
numerous spines and ridges scat- 
tered over the head. A thickened 
ridge was visible dorsally along 
the supraoccipital of 2.0-mm lar- 
vae. This thickened ridge became 
a small, peak-like, median supra- 
occipital crest with a single, dor- 
sally directed spine by 2.5 mm. 
The supraoccipital spine began to 
regress by 5.0 mm and was re- 
sorbed by 10.0-10.5 mm. A su- 
praorbital ridge was present by 
3.5 mm. This ridge became ser- 
rate by 4.0 mm. Small serrate 
ridges were visible along the dor- 
sal margin of both the lacrimal 
and jugal bones (i.e. first and sec- 
ond suborbitals; Gregory, 1933) 
and third suborbital bone by 5.0 
mm. Spines or spinous ridges 
were also visible along the fourth 
and fifth suborbitals, dermo- 
sphenotic (i.e. sixth suborbital), 
posttemporal, pterotic, tabular, 
and supracleithral bones by 6.0 
mm. The ventral margin of the 
jugal bone near the posterior margin of the maxil- 
lary had a single, ventrally directed spine by 7.0 mm 
(Fig. 2). Individual spines were also scattered over 
the frontal and occipital bones of young Atlantic 
spadefish. The bases of these spines were covered 
by integument so that only a portion of each spine 
was visible (Fig. 3). All head spines and spinous 
ridges were present in the largest specimen exam- 
ined (12.5 mm) but were difficult to locate on lar- 
vae not cleared and stained because of heavy body 
pigment. 

Teeth in Atlantic spadefish were placed in an in- 
ner and outer band. Teeth first appeared in a single 
band on the premaxillary and anteriorly on the 
dentary at about 2.5 mm. Teeth were pointed and 
closely spaced. A second band of teeth formed along 





Figure 1 (Continued) 



the upper and lower jaws by 4.0 mm; the outer band 
was slightly larger than the inner band. Teeth were 
added along the upper and lower jaws as larvae de- 
veloped (Figs. 1 and 2). 

Specialized spinous scales or "pre-scales" began to 
develop at about 5.5 mm. Pre-scales were character- 
ized by a single, elevated, posteriorly directed spine 
that was positioned near the center of the scale. Pre- 
scales developed first on the head and later ap- 
peared anteriorly along the lateral midline. Pre- 
scales were added outward toward the dorsal and 
ventral midlines and proceeded in a posterior direc- 
tion, covering the body by 10.0 mm. 

The first bones to ossify were the preopercular 
spines, supraoccipital crest, premaxillary, dentary, 
and cleithrum. Three predorsal bones (i.e. supra- 



Ditty et al.: A redescription of Chaetodipterus faber larvae 



267 



SUPRAOCCIRTAL 



SUPRAORBITAL 




POSTTEMPORAL 

TABULAR 
SUPRACLEITHRAL 
OPERCLE 

CIRCUMORBITALS 

INTEROPERCLE 
INNER PREOPERCLE 
OUTER PREOPERCLE 



Figure 2 

Location of head spines on a 7.0-mm SL larva 
of Atlantic spadefish, Chaetodipterus faber, 
from the northern Gulf of Mexico. 



neurals) were ossifying by 6.0 mm. The anteriormost 
precaudal vertebrae and dorsal- and anal-fin 
pterygiophores ossified first; ossification proceeded 
posteriorly. All caudal bones were ossifying by 8.0 
mm. Six branchiostegal rays and 10+14 vertebrae 
were present in all cleared and stained specimens. 

Fin development 

A continuous median finfold extended around the 
body from the nape to the anus of early larvae. Fin 
ray anlagen began forming obliquely downward in 
the caudal finfold during flexion (usually 3.5-4.5 
mm). Caudal-fin ray development proceeded out- 
ward from mid-base as the hypural complex shifted 
to a terminal position, with the adult complement 
of 9+8 principal rays attained at about 6.0 mm 
(Table 2). Development of the dorsal- and anal-fin 
bases coincided with notochord flexion. Both fin 
bases and their ray anlagen began to differentiate 
near mid-fin; development proceeded outward from 
mid-fin. All dorsal and anal soft rays were present 
by about 7.0 mm. Soft dorsal and anal fin ray 
complements were present before their spines (Table 
2); dorsal and anal spines developed in an anterior 




Figure 3 

Scanning electromicrograph of the frontal and occipital spines of a 7.0-mm SL Atlantic spade- 
fish, Chaetodipterus faber. Epithelium was partially digested with trypsin to enhance visibility 
of frontal and occipital spines. Magnification: 140x. 



268 



Fishery Bulletin 92(2). 1994 



to posterior direction. Pelvic fins 
were precocious and heavily pig- 
mented. Pelvic buds were visible 
by 4.0 mm; pelvics had a full 
complement of elements (I, 5) by 
6.0 mm. Pectoral rays began to 
develop by 5.0 mm and a full 
complement (17) was present by 
8.0 mm. Sequence of fin comple- 
tion was pelvics - soft dorsal and 
anal rays - dorsal spines - pecto- 
rals. A full complement of elements 
in all fins by 8.0-8.5 mm marked 
the beginning of transition to the 
juvenile stage (Table 2). 







Table 2 






Fin-ray counts of larval Atlantic spade 


fish (Chaetodipterus 


faber) from 


the northern Gulf of Mexico 










Length 












(mm SD' 


Dorsal 


Anal 


Pectoral 


Pelvic 


Caudal 


4.3 


III, Anlagen 


8 


Anlagen 


Anlagen 


0-7+7-0 


5.0 


III, 14 


11 


7 


4 


0-6+6-0 


6.1 


VII, 24 


II, 17 


13 


I, 5 


3-9+8-3 


7.0 


VII, 23 


II, 18 


1(1 


I, 5 


4-9+8-5 


8.3 


IX, 21 


III, 17 


17 


I, 5 


4-9+8-4 


9.3 


IX, 21 


III, 18 


17 


I, 5 


5-9+8-4 


10.0 


VIII, 23 


III, 18 


17 


I, 5 


5-9+8-5 


; One larva 


of each length. 











Temporal and spatial 
distribution 



Alantic spadefish larvae were col- 
lected from May through Septem- 
ber primarily in the north-central 
Gulf. Larvae were usually col- 
lected between June and August, 
density being highest during June 
and catch highest during August 
(Table 3). Larval Atlantic spade- 
fish were especially abundant 
near the Mississippi River delta 
during August 1988, when 19 of 
72 neuston tows (26%) associated 
with riverine frontal zones col- 
lected larvae. During August 
1984, however, <5% of neuston 
tows (rc = 162) from other areas of 
the north-central and western 
Gulf not associated with the delta 
captured larvae. Only one Atlan- 
tic spadefish larva was collected 
east of Mobile Bay, Alabama (long. 
88°00' W). This 4.0-mm specimen 
was found off Apalachicola Bay 
(Florida) during August 1984 at a 
station 13 m deep (Fig. 4). Salin- 
ity at this station (34.2 ppt) was the highest re- 
corded with a positive catch during the study. The 
largest specimen collected in surface-towed nets was 
12.5 mm; this observation may indicate that larvae 
move out of surface waters by this size. 

Overall, >85% of Atlantic spadefish larvae were 
collected in surface waters >28.0°C (median: 28.TC, 
mean: 28.7°C, range: 25.0°-32.2 <, C), at salinities be- 
tween 26.7 and 31.3 ppt (median: 28.8 ppt, mean: 
28.4 ppt, range: 11.8-34.2 ppt), and at station depths 
<238 m (median: 83 m, mean: 139 m, range: 9-470 m) 



Table 3 

Density (number of larvae/100 m 3 ) and catch (number of larvae/10 neus- 
ton tows) of Atlantic spadefish larvae (Chaetodipterus faber) from the 
northern Gulf of Mexico. Months are combined across years (1982-1986, 
and August 1988). Not all months were sampled each year. Numbers 
in parentheses are positive catch stations over total stations sampled 
by month. Monthly density estimates were calculated by dividing sum 
of larvae by either sum of volume water filtered (VWF) overall, or sum 
of positive station VWF. Monthly catch estimates were calculated by di- 
viding sum of larvae by number of stations sampled overall or by num- 
ber of positive catch stations. 



Gear 


June 


July 


August 


Bongo 

Overall density 
Positive density 

Neuston 

Overall catch 
Positive catch 


0.3' 

6.2 (19/341) 

4.0 
42.6 (19/201) 


<0.l 2 - 3 
1.3 (4/134) 

0.4 
13.3 (3/92) 


<0.\ 4S 

1.5 (4/221) 

17.0 
131.6 (32/248) 



' Total VWF - 43,730 m 3 , positive catch station VWF - 1,799 m 3 , number of larvae col- 
lected was 111. 

2 0.02/100 m 3 . 

3 Total VWF - 22,207 m 3 , positive catch station VWF - 381 m 3 , number of larvae collected 
was 5. 

4 0.03/100 m 3 . 

5 Total VWF - 35,174 m 3 , positive catch station VWF - 796 m 3 . number of larvae collected 
was 12. 



(Fig. 5). However, distribution of larvae versus sta- 
tion depth was strongly influenced by two very large 
neuston-net collections of 192 and 64 larvae during 
August 1985 which represented 40% of all larval 
Atlantic spadefish taken. These two stations were 
located in waters near the shelf edge, 50 and 75 km 
east of the Mississippi River delta (28.1°C, 30.1 ppt, 
235 m deep; 27.9°C, 28.1 ppt, 238 m deep, respec- 
tively). Other stations had 27 or fewer larvae. Dis- 
tribution of larvae versus station depth without the 
two large collections shifted median station depth 



Ditty et al.: A redescription of Chaetodipterus faber larvae 



269 



shoreward from 83 to 26 m; larvae may, therefore, 
primarily inhabit coastal waters. This shoreward 




LONGITUDE 



Figure 4 

Distribution of Atlantic spadefish larvae (Chaetodipterus 
faber) in the northern Gulf of Mexico by month. Months are 
combined across years ( 1982-1986, and August 1988). Not all 
months sampled each year. Plus ( + ) signs are total stations 
sampled and squares are positive catch stations. Distribution 
of stations are for both bongo and neuston net tows. 



shift in median station depth was reinforced by dis- 
tribution of larvae in bongo net tows and by distri- 
bution of larvae during June and July (Fig. 
4, Table 4). About 86% of all Atlantic spade- 
fish larvae collected in bongo net tows (rc=128) 
were from waters <25 m deep. In addition, 
distribution of larvae during June and July 
was shoreward of that during August. Simi- 
larly, 51% of all stations where larvae were 
collected (i.e. 41 of 81) were inside 25 m; 64% 
were inside 50 m. Only 14% of positive catch 
stations were located beyond the 100 m 
isobath; most of these stations were near the 
Mississippi River delta, an area with a nar- 
row shelf and rapidly increasing water 
depths. 



Discussion 

Our observations on the morphological devel- 
opment of Atlantic spadefish larvae generally 
agree with Hildebrand and Cable (1938). 
These authors, however, do not discuss pig- 
ment on the roof of the mouth. The presence 
of a single, median patch of pigment on the 
roof of the mouth is helpful in identifying 
early Atlantic spadefish larvae before the 
supraoccipital crest is clearly visible. 
Hildebrand and Cable (1938) do not discuss 
small spines or ridges along the circumorbital 
bones (i.e. supraorbital, suborbitals, and 
dermosphenotic) or tabular bone (Fig. 2) but 
do illustrate serrate ridges above the eye and 
in the pterotic region (Hildebrand and Cable, 
1938, their Figs. 26 and 27). Spination on the 
circumorbital bones has generally been found 
only in those larval percoids with cranial or- 
namentation (Johnson, 1984). Most of these 
larval percoids also have other specializa- 
tions, such as spinous scales and an elongate 
spine at the angle of the preopercle, among 
other characters (Johnson, 1984). Neither 
Hildebrand and Cable (1938) nor Johnson 
(1984) mention the supracleithral spines we 
found on Atlantic spadefish larvae (Fig. 2) and 
in larvae of Pacific spadefish, Chaetodipterus 
zonatus (Martinez-Pecero et al., 1990). The 
"short, hair-like spines on the upper surface 
of the head" noted by Hildebrand and Cable 
(1938) on 9.0-mm Atlantic spadefish larvae 
may be the same spines we found scattered 
over the frontal and occipital bones (Fig. 3). 
These frontal and occipital spines are difficult 
to see under a dissecting microscope because 



270 



Fishery Bulletin 92(2). 1994 



• larvae (6) = 123 

• larvae (N) - 478 




GEAR TYPE Hi BONGO tXS NtuSTON 




25 27 26 29 30 31 32 



Temperature (°C) 



12 IS 16 17 19 20 23 24 25 26 27 2B 29 X 31 32 33 34 

Salinity (ppt) 




Depth (m) 



Figure 5 

Summary of positive catch station hydrographic data for larval Atlantic spadefish (Chaetodipterus faber) from 
the northern Gulf of Mexico. Percent catch is sum of larvae by interval and gear divided by total number of At- 
lantic spadefish larvae collected overall. Discrepancies in number of larvae by month among parameters are the 
result of missing hydrographic data. 



Table 4 

Summary of hydrographic data by month for Atlantic spadefish [Chaetodipterus faber) larvae from the northern 
Gulf of Mexico. Data are from the surface and for positive catch bongo and neuston net stations only. Station 
hydrographic data are multiplied by total number of larvae collected at each station to obtain monthly mean 
and median values.' W is the number of larvae used to obtain mean and median values. Discrepancies in W 
by month among parameters resulted from missing hydrographic data. 







Water temperature 


CO 




Sal 


nity (ppt) 






Station depth (m 


) 




N 


Mean 


Median 


Range 


N 


Mean 


Median 


Range 


N 


Mean 


Median 


Range 


June 
July 
August 


160 

9 

433 


29.0 
29.4 
28.1 


29.3 
29.8 
28.6 


25.0-30.5 
29.3-30.5 
27.6-32.2 


143 

9 

433 


27.6 

27.6 
28.8 


27.6 
27.6 
29.4 


12.1-33.9 
25.4-28.6 
11.8-34.2 


192 

9 

433 


17.3 
27.3 
194 


16 

21 

235 


9-90 
16-70 
11-470 



This method gives weight to distribution of larvae rather than distribution of stations. 



they are largely covered by integument. The 
supraoccipital crest was resorbed by about 10.0-10.5 
mm in Gulf larvae but still present on a 11.5-mm 
specimen from the U. S. Atlantic coast (Hildebrand 
and Cable, 1938). 

The identity of Ryder's (1887) yolk-sac Atlantic 
spadefish larvae is uncertain (Johnson, 1978). 
Ryder's 3.5-mm and 4.0-mm larvae lack a supra- 



occipital crest and preopercular spines, both of 
which Hildebrand and Cable (1938) and we found 
by 2.5 mm in Atlantic spadefish larvae. Ryder's 
4.0-mm larva also has an oil globule in the yolk sac 
and the gut does not have the single, tightly coiled 
loop we found in preflexion Atlantic spadefish. Nei- 
ther Hildebrand and Cable (1938) nor we found an 
oil globule in Atlantic spadefish larvae of 2.0 mm or 



Ditty et al.: A redescription of Chaetodipterus faber larvae 



271 



2.5 mm, respectively. Differences between Ryder's 
and our study do not support identification of 
Ryder's larvae <4.0 mm as Atlantic spadefish even 
if we allow for specimen shrinkage (also noted by 
Johnson, 1978) and for slower development times 
due to cooler waters of Chesapeake Bay during the 
summer when Atlantic spadefish spawn. 

Johnson (1984) characterized the sequence of fin 
completion in larval Atlantic spadefish as pattern A: 
dorsal and anal soft rays - spinous dorsal - pelvics 
- pectorals. We cleared and stained seven larvae and 
found the sequence of fin completion more closely 
resembles Johnson's (1984) pattern F with all ele- 
ments of the pelvic fin present before dorsal and 
anal soft rays. This difference in fin completion pat- 
tern, however, may be due to differences in how we 
and Johnson interpreted spine formation and fin 
completion. We counted rays when first segmented 
and spines when present; Johnson may have 
counted pterygiophores. Pattern F is found in Hapa- 
logenys, Monodactylidae, and Pempherididae 
(Johnson, 1984). 

Larvae of Atlantic spadefish are characterized by 
early development of specialized spinous scales or 
"prescales" (at about 5.5 mm, this study) that even- 
tually transform into adult ctenoid scales. Spinous 
larval scales are present to about 15.0 mm (Johnson, 
1984). Ctenoid scales are well developed by 18.0 mm 
(Hildebrand and Cable, 1938). 

Developmental morphology and head spination of 
Atlantic spadefish is generally similar to that of 
Pacific spadefish ( Martinez-Pecero et al., 1990). Both 
species are deep-bodied (usually 55-60% SL) and 
preanal length is about 60% SL. Pigmentation and 
standard length at which fins develop also are simi- 
lar; a full complement of rays is present in all fins 
by 8.0-9.0 mm in both species (Hildebrand and 
Cable, 1938; Martinez-Pecero et al., 1990; this 
study). However, consolidation of pigment into lat- 
eral bands, resorption of the supraoccipital crest, 
and the beginning of transition to the juvenile stage 
occur earlier in Pacific spadefish than in Atlantic 
spadefish. Larvae of ephippids from the Indo-Pacific 
region differ from Chaetodipterus from the western 
Atlantic and Pacific Oceans in extent of head 
spination (Leis and Trnski, 1989; Martinez-Pecero 
et al., 1990; this study). Larvae of Platax from the 
Indo-Pacific have a median supraoccipital crest with 
a serrate leading edge (Leis and Trnski, 1989) but 
do not have the circumorbital series of spinous 
ridges, nor spines on the jugal, tabular, pterotic, or 
supracleithral bones found in Chaetodipterus 
(Martinez-Pecero et al., 1990; this study). Head 
spination in Ephippus larvae from the Indo-Pacific 
is similar to that of Chaetodipterus and these two 



genera are probably more closely related than either 
is to Platax. Other species-specific head spination 
found in Chaetodipterus larvae from the western 
Atlantic and Pacific Oceans, and in Ephippus orbis, 
Platax batavianus, and three Platax species from 
the Indo-Pacific region include a posttemporal spine 
which may be reduced to a ridge in some species, a 
supraorbital ridge that varies in size among species, 
and one or two subopercular spines (Leis and Trnski, 
1989; Martinez-Pecero et al., 1990; this study). 

Early larvae of Atlantic spadefish could be con- 
fused with priacanthids, lobotids, some carangids 
and stromateoids, the wreckfish — Polyprion amer- 
icanus, and Menticirrhus spp. because of similari- 
ties in head spination or in body pigmentation. 
Priacanthids have an elongate, serrate, median 
supraoccipital crest that extends posteriorly over the 
mid- and hindbrain; serrations along the lower jaw 
and frontal bone; and the angle preopercular spine 
is elongate and serrate as is the pelvic spine. Trip- 
letail, Lobotes surinamensis, have a vaulted, serrate 
supraoccipital crest in early larvae, the pelvics are 
inserted behind the pectoral fins, and have fewer 
anal fin elements than Atlantic spadefish (Atlantic 
spadefish: A. Ill, 17-18, tripletail: A. Ill, 11-12). In 
carangids, the two anteriormost anal spines are 
separated from the third by a distinct gap and most 
species have a low, median supraoccipital crest that 
has serrations along the dorsal edge; other carangids 
lack a supraoccipital crest entirely. Some carangids 
also have a precocious dorsal fin with anterior 
spines or rays elongate, or with serrations along the 
angle preopercular spine. Some stromateoids (e.g. 
Ariommus spp., Nomeus gronovii) resemble Atlan- 
tic spadefish in early body pigmentation, body 
shape, and by having precocious pelvics, but 
stromateoids lack a median supraoccipital crest, a 
large preopercular angle spine, and all but 
Hyperoglyphe have >30 myomeres. Polyprion 
americanus larvae have a small, peak-like median 
supraoccipital crest, but with serrations along the 
leading edge, and lack a serrate pterotic ridge and 
spines on the tabular bone (Johnson, 1984). 
Wreckfish also have 27 myomeres, fewer dorsal (22- 
24) and anal fin (11-13) elements, and the mouth 
is larger than in Atlantic spadefish. Larval Atlantic 
spadefish differ from early larvae of Menticirrhus 
spp. by lack of both preopercular spines and the 
median supraoccipital crest in the latter. 

We recently examined specimens reported by 
Dawson (1971) as larval black driftfish, Hypero- 
glyphe bythites. These specimens had a supra- 
occipital crest, pterotic ridge, spine on the inter- 
opercle, other head spination, and a pigmentation 
pattern identical to Atlantic spadefish. Vertebral, 



272 



Fishery Bulletin 92(2). 1994 



dorsal, and anal fin counts overlap between black 
driftfish and Atlantic spadefish, but teeth are found 
in a single band on the dentary in black driftfish 
(Ginsburg, 1954) and in two bands in Atlantic spa- 
defish (Hildebrand and Cable, 1938; this study). 
Dawson's 5.7-7.9 mm specimens had teeth in two 
bands along the dentary. Because it is unlikely that 
black driftfish larvae have the same suite of char- 
acters as Atlantic spadefish, Dawson's specimens 
should be assigned to Atlantic spadefish. 

Atlantic spadefish spawn from May through Sep- 
tember based on seasonal abundance of Atlantic 
spadefish larvae in the northern Gulf; peak spawn- 
ing occurs between June and August (Ditty et al., 
1988; this study). Density estimates were highest 
during June in this study (Table 3), during July in 
a previous study of coastal waters off central Loui- 
siana (Ditty, 1986), and during July and August off 
Mississippi Sound (Stuck and Perry, 1982). Neuston 
net collections were greatest during August (Table 
3). Gonad maturity data off South Carolina support 
peak spawning of Atlantic spadefish during summer 
(Hayse, 1990). 

Spatial distribution data indicate that Atlantic 
spadefish larvae are apparently rare in the eastern 
Gulf. Only one larva was collected east of Mobile 
Bay (Alabama) during this study, and one larva by 
Houde et al. 3 in a survey of Gulf waters off Florida. 
In addition, distribution of both larvae and station 
depths where larvae were collected indicates that 
Atlantic spadefish occur primarily in coastal waters 
(Ditty and Truesdale, 1984; this study), except near 
the Mississippi River delta where waters may offer 
additional habitat suitable to larvae because of 
lower salinities. The relatively high number of posi- 
tive stations (26%) near the delta during August 
1988 sampling of frontal zones suggests that fron- 
tal zones may concentrate larvae. Frontal zone wa- 
ters may also provide a richer environment for feed- 
ing and growth of larvae because of higher phy- 
toplankton and zooplankton biomass (Govoni et al., 
1989; Grimes and Finucane, 1991). However, Powell 
et al. (1990) were unable to demonstrate consis- 
tently that larvae have a nutritional advantage 
when associated with the Mississippi River plume. 
A possible association of Atlantic spadefish larvae 
with riverine frontal areas requires further study. 

In conclusion, understanding the biology, life his- 
tory, and relations of Atlantic spadefish requires a 
knowledge of the morphology, distribution, and ecol- 
ogy of their larvae. Larval characters (e.g. degree of 



3 Houde, E. D., J. C. Leak, C. E. Dowd, S. A. Berkeley, and W. 
J. Richards. 1979. Ichthyoplankton abundance and diversity 
in the eastern Gulf of Mexico. Univ. Miami Report BLM Con- 
tract No. AA550-CT7-28, Miami, FL 33149, 546 p. 



head spination) may also provide insight into the 
interrelationships among the Ephippidae and their 
relationship to other families. The potential use of 
larval characters in defining these relationships, 
however, cannot be clearly understood until larval 
development within the family is more fully docu- 
mented (Watson and Walker, 1992). 



Acknowledgments 

This study was supported by the Marine Fisheries 
Initiative (MARFIN) Program (contract numbers: 
NA90AA-H-MF111 and NA90AA-H-MF727). The 
authors would like to thank the Southeast Area 
Monitoring and Assessment Program (SEAMAP) 
and Gulf States Marine Fisheries Commission for 
providing specimens and environmental data; 
Churchill Grimes (NMFS, Panama City Lab, 
Florida) for access to neuston net collections off the 
Mississippi River delta during August 1988; and 
John Lamkin (NMFS, Pascagoula, MS) for provid- 
ing specimens of the reported black driftfish for 
examination. We also thank Laura Younger for pro- 
viding scanning electromicrographs of the head 
spines of Atlantic spadefish larvae. Finally, we thank 
the reviewers for their comments in substantially 
improving the manuscript. Jack Javech (NMFS, 
Miami, FL) illustrated the larvae. 



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