A continuous, underway fish egg sampler 6... · 2015-04-29 · A continuous, underway ﬁsh egg...

A continuous, underway ®sh egg sampler

DAVID M. CHECKLEY, JR,1 PETERB. ORTNER,2 LAWRENCE R. SETTLE,3

AND SHAILER R. CUMMINGS2

1 Corresponding author. Marine Life Research Group, ScrippsInstitution of Oceanography, La Jolla, California, USA 92093±0218 (e-mail: [email protected])2 Atlantic Oceanographic and Meteorological Laboratory,NOAA, Miami, Florida, USA 331763 Beaufort Laboratory, National Marine Fisheries Service,NOAA, Beaufort, North Carolina, USA 28518±9722

ABSTRACT

We describe a method to sample the highly contagiousdistribution of pelagic ®sh eggs. CUFES, the contin-uous, underway ®sh egg sampler, consists of a sub-mersible pump, concentrator, electronics and samplecollector. This system operates continuously and undernearly all sea conditions, providing a real-time esti-mate of the volumetric abundance of pelagic ®sh eggsat pump depth, usually 3 m. CUFES-derived estimatesof volumetric abundance agree well with those fromnets towed at pump depth and with areal abundanceestimated from vertically integrated plankton tows.CUFES has been used successfully to sample the eggsof menhaden, pin®sh, sardine, and anchovy off thecoasts of the eastern and western United States andSouth Africa. Two large patches of eggs of the At-lantic menhaden were sampled off North Carolina inwinter 1993±94, had a linear scale of 5±10 km, andwere found in waters between the Gulf Stream andmid-shelf front. Spawning location may be related tobathymetry. CUFES is now being used to estimatespawner biomass by the daily egg production method.An optical plankton counter provided accurate esti-mates of the number of Atlantic menhaden eggssample by CUFES.

Key words: pelagic ®sh eggs, sampling, spawning,Brevoortia tyrannus, Engraulis mordax, Sardinops sagax,Gulf Stream, optical plankton counter

INTRODUCTION

Pelagic eggs of ®sh are highly aggregated in time andspace. Such aggregation affects both the ecology of ®shand our ability to study and manage them. In partic-ular, estimates of egg abundance in time and space areused to estimate the spawning biomass of populationsof pelagic ®sh and are thus needed to understand thestatus and dynamics of ®sh populations in order to bestmanage them.

Contagious distributions are dif®cult to sample.Conventional methods, nets towed at discrete stations,are limited in their accuracy, precision and sensitivity,and are labour intensive and hence costly. In addition,such methods require the dedicated use of a ship, arelimited by adverse conditions, and produce sampleswhich await analysis ashore. We therefore sought analternative method to sample ®sh eggs. We wished tosample continuously, underway, for nearly all condi-tions at sea, and with other operations able to beperformed simultaneously. We sought a real-time as-sessment of egg abundance, to facilitate adaptivesampling (Thompson, 1992) and minimize subsequentlaboratory work. Here we describe our system and itssuccessful sampling of the Atlantic menhaden, Bre-voortia tyrannus, pin®sh, Lagodon rhomboides, northernanchovy, Engraulis mordax, and the Paci®c sardine,Sardinops sagax.

The impetus to develop this system was a desire toinvestigate the hypothesis that the Atlantic men-haden spawns during storms at the western wall ofthe Gulf Stream (Checkley et al., 1988). Subsequentdevelopment occurred as part of the South AtlanticBight Recruitment Experiment, SABRE, to investi-gate recruitment variation in estuarine-dependent®sh, including the Atlantic menhaden. Most re-cently, CUFES has been used to assess spawningstocks of sardine and anchovy off California andSouth Africa.

Pelagic eggs of ®sh are often spawned at night byadults in schools, resulting in distributions of eggs

Received for publication 19 December 1996

Accepted for publication 18 March 1997

FISHERIES OCEANOGRAPHY Fish. Oceanogr. 6:2, 58±73, 1997

58 Ó 1997 Blackwell Science Ltd.

that are highly contagious. The fertilized eggs arebuoyant and typically hatch in 1±4 days. Althoughthe depth of spawning varies within and betweenspecies, the distribution of eggs appears to achieve asurface maximum early in the development of the egg(Ware and Lambert, 1985; Pommeranz and Moser,1987; Tanaka, 1992; Cambalik, 1993). Turbulencewill mix buoyant eggs downward but they will remainmost abundant at or near the surface (Pommeranzand Moser, 1987; Sundby, 1991; Tanaka, 1992;Cambalik, 1993). Hence, we felt it appropriate tosample near the surface to allow inference about arealabundance. We hypothesized that the concentrationof eggs at a single depth is signi®cantly related toareal abundance.

Initially, we tested an optical plankton counter(OPC, Herman, 1988) to sense eggs of Atlanticmenhaden in the ambient plankton. We hypothesizedthat pelagic ®sh eggs, due to their relatively large size,would, when abundant, constitute a statistically id-enti®able peak in the particle size spectrum assessedoptically by the OPC. It was discovered, however, thatmenhaden eggs are optically similar to other, numer-ically dominant plankters (copepods) of approximatelyhalf their diameter, owing to the relative transparencyof menhaden eggs compared with other plankters.Similar results have subsequently been reported for theeggs of Baltic cod, Gadus morhua (Wieland andKoÈester, 1996). Hence, we sought to increase the`signal-to-noise' ratio for sensing pelagic ®sh eggs byconcentrating them relative to physically smaller, al-though optically indistinguishable, particles. To thisend, we used a scaled-up version of the zooplanktonconcentrator of Herman et al. (1984).

We wished to sample as large a volume as reason-able so as to maximize our sensitivity to detect eggs inlow abundance, at the edge of a patch of recentlyspawned eggs. To do so, we used a high-volume, sub-mersible pump having a ¯ow rate comparable to thatof the towed, in situ OPC.

Our system, named the continuous, underway ®shegg sampler (CUFES) therefore consists of a high-volume, submersible pump ®xed rigidly to the ship'shull and, on deck, devices to concentrate egg-sizedparticles and to collect sequential samples of theseparticles on a mesh. Other, electronic instruments maybe used to analyse particles in the ¯ow between theconcentrator and the sample collector. Here, wepresent results from use of the OPC; video has beencombined with the OPC but will be discussed else-where. It is important to recognize that, to date, theroutine use of CUFES requires the visual examinationof collected samples. However, our OPC results indi-

cate that automated, electronic counting of eggs isfeasible.

Other systems are analogous to CUFES in part butnot entirely. Lenz et al. (1995) describe a video-re-cording system for in situ studies of ichthyoplankton.Miller and Judkins (1981) and Star and Mullin (1981)describe plankton pumping systems. Murdoch et al.(1990) provide a method of shipboard identi®cationand counting of pelagic ®sh eggs but it does not addresssample collection and requires the use of photographyand is thus not real-time. None of these contains aconcentrating mechanism nor means of real-timecounting of eggs.

Here we discuss deployment of our system in thewinter of 1993±94, on the NOAA ship Oregon II offNorth Carolina, and in spring 1996, on the NOAAship David Starr Jordan off Southern California. Ourgoals were twofold. First, to test CUFES, includingcomparisons with conventional methods. Second, tosurvey the regions of most probable spawning of theAtlantic menhaden, northern anchovy, and Paci®csardine in order to assess the distribution and abun-dance of their eggs. Our intent in this paper is not topresent comprehensive results of either egg surveys orpatch studies but, rather, to demonstrate the potentialfor using this method to attain these larger objectives.We describe our underway, egg sampling system;present results for the menhaden, sardine, and an-chovy; and discuss our system's ef®cacy for censusingthe pelagic eggs of ®sh. We conclude that our systemsamples ®sh eggs well and enables improved assess-ment of their distribution and abundance.

MATERIALS AND METHODS

CUFES

Our pumping system consists of three elements(Fig. 1): ®rst, an in situ, submersible pump ®xed to theship's hull; second, a device to concentrate large par-ticles, including ®sh eggs; and third, analysis devices,including a laboratory OPC, video system, and me-chanical sample collector (MSC). These elementsenable us to: (i) pump �0.5±1.0 m3 min)1 from anominal depth, 3 m; (ii) concentrate large particles ina ¯ow of 15±20 l min)1; and (iii) electronically senseand physically collect particles for real-time assess-ment of the concentration of the target particle type,e.g. eggs of the Atlantic menhaden or Paci®c sardine,under nearly all sea conditions.

Ship requirements include: (i) a location to mountthe submersible pump, preferably amidships; (ii) alaboratory or protected area for the concentrator and

Continuous, underway ®sh egg sampler 59

Ó 1997 Blackwell Science Ltd., Fish. Oceanogr., 6, 58±73.

analysis equipment, including associated hoses; and(iii) electrical power for the submersible pump. Thetotal weight of CUFES is �800 lbs (365 kg). CUFESinstallation requires �2 days and removal �1 day.

Our pump is a semi-vortex pump (Ebara model 80DVSU 62.22), a type previously shown to not greatlydamage zooplankters (Omori, 1985; Checkley et al.,1992). Electrical power is either 440 V AC and4.2 amp or 220 V AC and 8.4 amp. The pump ismounted on the lower end of a 6.4-m (21-foot) long,10-cm (4-inch) i.d., schedule 80 (0.85-cm (0.337-inch) wall thickness) steel pipe which is orientatedvertically and held by clamps secured by bolts or weldsto the ship's gunwale and hull just above the waterline. In addition, the vertical pipe is guyed from nearthe pump, underwater, to ship structures fore and afton deck. Water from the pump enters a ¯exible, PVC-reinforced, 7.6-cm (3-inch) i.d. pressure hose which,in turn, enters the vertical pipe near the pump and

exits through the upper end of the pipe and thence tothe concentrator. A 440 or 220 V AC power line isattached to the pipe and energizes the pump. The pipeis faired below the water line to reduce drag. The pipeand attached pump can swing between the verticaland horizontal positions, to enable maintenance andtransport out of the water when not in service. Thepump depth may be adjusted between the surface and3 m by raising and lowering the vertical pipe.

The concentrator consists of an oscillating Nitexnet (570 cm2 total area) submerged in a 50-litre vessel,and is adapted from a smaller device (Herman et al.,1984). Water enters the concentrator from the top andexits either as ®ltrate (�97% of ¯ow) through its side,after passing through the net, or as concentrate (�3%of ¯ow) at the bottom end of the net and vessel. TheNitex is sewn tightly within a metal frame. The framewith Nitex moves laterally over a 2.3-cm range at5.75 Hz. The mesh size of the Nitex is selected to

Figure 1. Continuous underway ®sh egg sampler, CUFES. System details may vary between installations but always includesubmersible pump, concentrator and mechanical sample collector. Pump depth is nominally at 3-m depth. See text for details.


60 D. M. Checkley, Jr et al.

maximize the ef®ciency of retention of eggs of thetarget species and simultaneously minimize retentionof optically similar, though physically smaller, parti-cles, and clogging. In general, we use a mesh size �1/3±2/3 the equivalent spherical diameter of the targetegg. For eggs of the Atlantic menhaden (sphere, �1.4±1.8 mm diameter), we use 1-mm Nitex; for eggs of thenorthern anchovy (spherical ellipsoid, 1.2±1.4 mmmajor axis, 0.65±0.82 mm minor axis) and co-occur-ring Paci®c sardine (sphere, 1.4±2.1 mm diameter), weuse 0.500 mm Nitex. The ®ltrate is directed overboardthrough ¯exible hoses, one of which has a ball valve(not shown in Fig. 1) to control water level in theconcentrator.

Water from the concentrator ¯ows by gravity at�20 l min)1 in 1.9-cm (0.75-inch) i.d. clear, ¯exibletubing to electronic sensors and ®nally into the me-chanical sample collector. Fish eggs may be distin-guished from other particles by use of the OPC, basedon optical size, and video, based on other character-istics (shape, dimensions). Particles, including eggs,are then collected in the MSC on a Nitex mesh. TheMSC is a solenoid-driven, computer-controlled devicewhich directs ¯ow from the 1.9-cm (0.75-inch) clear,¯exible tubing coming from the concentrator to oneside or the other of a knife-edge ¯ow separator andthence onto a removable, Nitex ®lter, analogous to thecod end of a plankton net. The ¯ow is redirected pe-riodically from one side, hence ®lter, to the other. The®ltrate is directed overboard while, upon completionof the sample, the retained material is immediatelyinspected, and the target eggs counted, under a dis-secting microscope and then ®xed and preserved in asmall bottle, e.g. scintillation vial of 20 ml, with buf-fered, 5% formalin for later analysis.

The concentrator net eventually becomes clogged.The pump and oscillator motor are then turned off,and the Nitex mesh in the concentrator is cleaned inplace using a brush and by spraying with water underpressure. The period between clogging depends onthe ¯ow into the concentrator, the concentratormesh size, and the particulate matter in the sampledwater. Our experience is that, with full ¯ow(�640 l min)1), the concentrator mesh must becleaned every 2 to 12 h. Cleaning time is �5±10 min. Occasionally, other, large particles (salps,drift kelp) enter the system and necessitate it beingshut down and cleaned.

Periodically, the system's mean ¯ow rate is mea-sured. The ¯ow from each discharge hose and theMSC is measured individually. These data are com-bined to estimate ¯ow into the concentrator and fromthe concentrator to the MSC.

Concurrent with pumping, data are logged period-ically for date, time, position, and variables such astemperature, salinity, and chlorophyll a ¯uorescence.The former three variables are from a GPS. The lattermeasurements are at times made using our pumped¯ow and, at other times, the ship's seawater ¯ow, theformer being preferred. In either case, we assume thesemeasurements are comparable to those of CUFES intime and location.

On the January 1994 cruise of the NOAA vesselOregon II, for which data are presented, a TurnerDesigns ¯uorometer was placed in line between theconcentrator and the MSC and its output voltage re-corded. This ¯uorometer was calibrated in the labo-ratory with pure chl a and the resulting factor used toestimate in vivo chl a concentration in the pump ¯ow.Temperature and salinity were measured in the ship'sseawater ¯ow using Seabird Electronics temperatureand conductivity sensors. Position data were from theship's GPS. Data reported here were recorded at theend of each CUFES sample interval, either 5, 10, or15 min.

Net comparisons

On several cruises, net collections were made simul-taneous to pumping to compare (a) retention of eggsby CUFES relative to nets towed at the same depthand (b) estimates of the concentration of eggs onvolumetric (eggs m)3 at 3 m, CUFES) and areal(eggs m)2, vertically towed net) bases.

Retention ef®ciency was studied by collectingplankton at pump depth with either a bongo net(McGowan and Brown, 1966), MOCNESS (Wiebeet al., 1976), or Tucker (1951) trawl. In the formercase, a 70-cm bongo with paired 333-lm-mesh netswas lowered rapidly to pump depth; a new CUFEScollection begun; after a known period, usually�5 min, sampling ended by rapid retrieval of the netand changing CUFES samples. In the latter cases, ei-ther a 1-m2 MOCNESS or 1-m2 Tucker trawl with333-lm-mesh nets was lowered to pump depth andsuccessive nets opened and closed at the same time asample was collected from CUFES. In all cases, ¯ow-meters were used to measure the volume of water ®l-tered. Ship speed varied from 0.2 to 1.5 m s)1 (1±3 kt(knots)) and tow duration 2±5 min.

Areal distribution comparisons were made with aCalVET net and standard protocols (Smith et al.,1985). The CalVET net was raised at 1 m s)1 from70 m or bottom, if less. CalVET and CUFES sampleswere taken simultaneously, on opposite sides of thevessel. The CUFES sampling period (�5 min) brack-eted the CalVET ascent (�1-min duration). Each pair



of collections was made at a different station andhence under different atmospheric and oceanographicconditions, although the latter were not monitored.

Laboratory analysis

Ashore, all eggs of the respective target species of ®shwere enumerated in each sample. Identi®cation keyswere Fahay (1983) for Atlantic menhaden and pin®sh,Moser and Ahlstrom (1985) for northern anchovy,and Ahlstrom (1943) for Paci®c sardine. Eggs of thePaci®c sardine were assigned to 11 developmentalstages (Lo et al., 1996). Data on eggs collected per unittime were combined with the pump ¯ow rate to esti-mate concentration (ECUFES (eggs m)3)). Data oneggs collected per net tow were combined with ¯owmeter data to calculate egg concentration (Enet (eggsm)3)).

Optical plankton counter

The OPC was used both at sea, off North Carolina,and in the laboratory. At sea, a laboratory OPC was inline between the concentrator and MSC (Fig. 1). Datawere acquired with a DOS computer with customsoftware and synchronized to GPS. In the laboratory,individual particles were introduced into the OPC¯ow. A captive population of Atlantic menhaden wasinduced to spawn (Hettler, 1981). The fertilized eggsand resultant larvae were maintained in ®ltered seawater at 18°C in a 12:12 light:dark cycle. Periodically,eggs and yolk-sac larvae were removed and passedthrough the OPC in the laboratory. In addition, wealso used live eggs made opaque by staining withmethylene blue, eggs preserved in a 5% solution offormalin in sea water, and plastic beads the size of eggs.

RESULTS

General operation

CUFES is a robust system. It has operated at shipspeeds to 12 kt (�6 m s)1). We have used it success-fully in all conditions encountered to date, rangingfrom calm to storms (22 m s)1 winds, 4-m seas). Inheavy seas on a rolling ship, the system draws in pulsesof bubbles from breaking waves. This does not affect®sh egg sampling but can affect particle detection byelectronic sensors. A bubble trap reduces the numberof bubbles passing through the OPC and other in-struments; subsequent ®ltering of the data duringanalysis largely eliminates this problem.

CUFES has operated successfully for four winters(1993±1997) off North Carolina in studies of theAtlantic menhaden, two springs (1996) off California

in studies of Paci®c sardine and northern anchovy, andin autumn 1996 off South Africa (not discussed here),sampling pilchard, Sardinops sagax. Sampling depthwas 3 m. The ¯ow rate into the concentrator variedbetween 610 and 680 l min)1, with a mean value of640 l min)1. This rate appears unaffected by cloggingof the concentrator net, its mesh size (0.5 or 1.0 mm),ship motion, or other conditions.

It is of interest to know the approximate regionsampled by the pump. At rest, water is drawn from avolume surrounding the pump intake (8-cm diameter).As the ship moves at rate S, the pump, intake forward,draws water (F, ¯ow rate) from a nominal cylinder thediameter (/) of which decreases with increasing speed.For F of 640 l min)1, the ship speed for which / andthe pump intake are the same diameter is 2.1 m s)1

(�4 kt). At 5 m s)1 (�10 kt), / is 5.2 cm. Eggs donot respond behaviourally to the ¯ow ®eld at the pumpintake and hence avoidance is not an issue. Otherzooplankters, e.g. copepods, are capable of avoidanceyet should be well sampled because their escape speeds(�10 body lengths s)1, 20 mm s)1 for a 2-mm longcopepod) are far less than the speed at the pump in-take.

Egg retention

Four sets of comparisons were made between CUFESand towed nets to investigate retention ef®ciency.Two hypotheses were tested. First, we used an ANOVA

to test whether towed nets and CUFES provideequivalent estimates of ®sh egg concentration. Sec-ond, to test the null hypothesis that ®sh egg abun-dances estimated by towed net and CUFES are notrelated, we used Pearson's correlation coef®cient, r,and parameter estimates for the linear regression be-tween these variables. These tests were made with eggconcentration (E, eggs m)3) both untransformed (E)and transformed (ln(E + 1)) to account for inhomo-geneity of variances.

To estimate retention ef®ciency, collections weremade from the NOAA ship Oregon II off North Car-olina in winter 1993±94. CUFES was equipped with1-mm-mesh Nitex in its concentrator, as the targetspecies was Atlantic menhaden (egg diameter�1.6 mm). The nets were of 333-lm-mesh Nitex. Inthe ®rst comparison, a patch of pin®sh was discoveredand sampled with CUFES and bongo nets. Estimates ofthe concentration of pin®sh eggs by CUFES and bongonets were highly correlated (Table 1 and Fig. 2), al-though an ANOVA indicated a signi®cant effect of geartype (F1,11 = 43.13, P < 0.001). In the second case, apatch of eggs of the Atlantic menhaden was sampledwith CUFES and a 1-m2 MOCNESS. Eight paired



collections were made. An ANOVA showed no signi®-cant effect of gear type on egg concentration(F1,14 = 2.64, P = 0.126). In the third case, twoMOCNESS collections were made between the sur-face and 5 m simultaneous with pump samples takenat 3 m. The ANOVA indicated no signi®cant effect ofgear type (F1,6 = 0.268, P = 0.623). In the fourth case,a patch of Atlantic menhaden eggs was sampled fourtimes using CUFES and a Tucker trawl. Once again,ANOVA indicated no effect of gear type (F1,6 = 1.29,P = 0.299). Data for Atlantic menhaden have beencombined in Table 1 and Fig. 2; net- and CUFES-derived estimates of egg abundance are highly corre-lated (r2 = 0.80 and 0.92 for untransformed and ln-transformed data, respectively). The slopes of thelinear regressions for the untransformed data indicate

Figure 2. Volumetric abundances of egg concentrationmeasured using CUFES and towed nets. Linear regression ofln-transformed, volume-based abundances from CUFES(ECUFES, eggs m)3) and towed nets (Enet, eggs m)3) shownfor eggs of the Atlantic menhaden and pin®sh. See text fordetails and Table 1 for regression statistics.

Tab

le1.

Ret

enti

on

of

eggs

of

pin

®sh

,L

agod

onrh

ombo

ides

,an

dA

tlan

tic

men

had

en,

Bre

voor

tia

tyra

nn

us,

by

CU

FE

San

dto

wed

net

sdep

loye

dat

3-m

dep

th.

Egg

sof

both

spec

ies

are

sph

eric

al.

Co

nce

ntr

atio

no

feg

gs(e

ggs

m)

3)

isfr

om

CU

FE

S(E

CU

FE

S)

and

tow

edn

et(E

net)

.S

eete

xt

for

det

ails

.V

alues

inpar

enth

eses

are

95%

con

®den

celi

mit

sof

par

amet

eres

tim

ates

.*

ind

icat

essl

op

esi

gni®

can

tly

dif

fere

nt

fro

mo

ne

and

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.a

slo

pe

no

tsi

gni®

can

tly

dif

fere

nt

fro

mo

ne

or

anin

terc

ept

not

sign

i®ca

ntl

ydif

fere

nt

from

zero

.N

um

ber

of

obse

rvat

ion

s1

0fo

rL

.rh

ombo

ides

and

13

for

B.

tyra

nn

us.

Lea

st-s

qu

ares

lin

ear

regr

essi

on

Egg

Mes

h(m

m)

Un

tran

sfo

rmed

Tra

nsf

orm

ed

Sp

ecie

sD

iam

eter

(mm

)N

etC

UF

ES

Eq

uat

ion

r2E

qu

atio

nr2

Lag

odon

�1.0

0.3

33

1.0

00

EC

UFE

S�

0.2

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+0

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(EC

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0.6

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et

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))

0.0

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ides

(0.1

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0.3

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8)

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.n

.s.

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voor

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�1.6

0.3

33

1.0

00

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0.7

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+0

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(EC

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(En

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1.7

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.n

.s.

*n

.s.



retention of eggs by CUFES relative to towed nets tohave been 0.76 � 0.25 (mean � SD(mean)) for theAtlantic menhaden and 0.25 � 0.09 for pin®sh.

CUFES±CalVET comparisons

Comparative collections were made using CUFES andCalVET nets during cruise JD9603 of the NOAA shipDavid Starr Jordan off Southern California in March1996 (Table 2, Fig. 3). We tested the same pair ofhypotheses and tests as in the previous section. Ournull hypothesis of no relation between volumetricconcentration of eggs estimated using the two methodswas rejected for both northern anchovy and Paci®csardine for both untransformed (F1,89 = 267,P < 0.0001, and F1,89 = 40.9, P < 0.0001, respective-ly) and transformed (ln([eggs] + 1)) data (F1,89 = 504,P < 0.0001, and F1,89 = 143, P < 0.0001). Arealabundance (eggs m)2) is 3.5 times the CalVET volu-

Tab

le2.

Abu

nd

ance

of

eggs

of

no

rth

ern

anch

ov

y,E

ngr

aulis

mor

dax,

and

Pac

i®c

sard

ine,

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din

ops

saga

x,es

tim

ated

usi

ng

CU

FE

San

dC

alV

ET

net

s.C

UFE

Ssa

mple

dat

3-m

dep

th.E

ggs

of

the

Pac

i®c

sard

ine

are

sph

eres

and

tho

seo

fth

en

ort

her

nan

cho

vy

are

ob

late

sph

ero

ids.

Co

nce

ntr

atio

no

feg

gs(e

ggs

m)

3)

isfr

om

CU

FE

S(E

CU

FE

S)

and

Cal

VE

Tn

et(E

CalV

ET

).S

eete

xt

for

det

ails

.V

alu

esin

par

enth

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are

95

%co

n®

den

celi

mit

so

fp

aram

eter

esti

mat

es.

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dic

ates

slope

or

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rcep

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gni®

can

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nt

from

zero

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.s.

ind

icat

esn

osu

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iffe

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ce.

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mb

ero

fo

bse

rvat

ion

sis

91

inea

chca

se.

In8

8o

fth

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the

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asto

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m7

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dan

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mes

vo

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un

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ce(e

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m)

3).

Lea

st-s

qu

ares

lin

ear

regr

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on

Egg

Mes

h(m

m)

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sfo

rmed

Tra

nsf

orm

ed

Sp

ecie

sD

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eter

or

maj

or

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rax

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m)

Cal

VE

TC

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ES

Eq

uat

ion

r2E

qu

atio

nr2

En

grau

lis�1

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Figure 3. Comparison of egg abundance from CUFES(ECUFES, eggs m)3) sampling at 3 m and vertically inte-grated haul of CalVET (eggs m)3) for northern anchovy andPaci®c sardine. See text for details and Table 3 for regressionstatistics.



metric abundance (Enet, eggs m)3) for most (88 of 91)of the collections in this study (those from 70 m to thesurface). For each developmental stage, the sum of eggscollected by CUFES was divided by the sum of eggscollected by CUFES and CalVET nets. This ratio wasunrelated to developmental stage (r2 = 0.09; Fig. 4).

Mapping

Data were collected on 15±20 January 1994, duringcruise 9308 of the NOAA ship Oregon II near the GulfStream in Onslow Bay (Fig. 5). Data for the distribu-tion and abundance of Atlantic menhaden eggs andwater temperature, salinity, and chl a concentration,are given in Fig. 6. The ship steamed at about 10 kt(�5 m s)1). The CUFES sample interval varied be-tween 5 and 15 min (mean, 11 min), corresponding to�1.5±9 km (mean, 3 km) and 21±63 m3 (mean,46 m3). A total of 545 samples was obtained over103 h and 1480 km.

The Gulf Stream Front (GSF, Checkley et al.,1988), with temperature 18±21°C and salinity �36.35,occurred from the SW to the NE, with cooler, lesssaline water to the west and north. A Gulf Stream®lament appeared to enclose a tongue of cooler andless saline shelf water which extended east. High sa-linity (³ � 36.35) and chl a-rich water occurred justnorth of the GSF and to the south of the cold tongue.

Chl a was also maximal to the north-east. Atlanticmenhaden eggs occurred in two distinct patches(Fig. 6), each of 5±10 km scale. The ®rst was at theGSF and the second in slightly cooler water to thewest. Both patches were at locations near CapeLookout with a bottom depth of 20±30 m. The num-ber of eggs in a sample ranged from 0 (n = 461) to 595in one 5- min collection.

The concentration of menhaden eggs has beensummed within bins of temperature, salinity, and chl aand compared with sampling effort to indicate underwhat conditions eggs were most often collected(Fig. 7). The modal temperature for egg occurrencewas 17.5°C and range 15±21°C. The modal salinitywas 36.26 and range 36.10±36.45. Eggs were foundover a broad range of chl a concentrations but, ingeneral, not less than 0.1 lg chl a l)1.

Optical plankton counter

We sought to test our original hypothesis that eggs,when abundant and concentrated by CUFES, would bemanifest in the OPC size distribution. To this end, fortwo transects (cases A and B) through the westernmostpatch with abundant menhaden eggs, we compared thesize-frequency distribution of particles sensed by theOPC in the patch with that for a nearby control area,further along each transect, with few eggs (Fig. 8).OPC data and CUFES samples were acquired over20 min. The OPC data were binned by digital size andsize-frequency distributions constructed. For each bin,the control data were subtracted from the patch data. Apeak, corresponding to the menhaden eggs, is evidentin the differenced data in both cases. Integration be-neath these peaks and between their approximatelimits in digital size (22±59 digital size units, dsu) yieldsestimates of 534 and 1066 particles per 20 min for thetwo cases A and B, respectively. The numbers of eggscollected were 548 and 998, respectively. Hence, theOPC-derived estimate of egg-sized particles was 0.98and 1.1 times the true number of eggs collected for casesA and B. A Gaussian model was ®tted to the differ-enced histogram data for 22±59 dsu. The mean and SEwas 40 � 1 dsu for case A and 38 � 1 dsu for case B.

The response of the OPC to introduced particles isshown in Table 3. Digital size (dsu) for eggs of theAtlantic menhaden increased from 44, one day postfertilization (dpf), to nearly 81 at 3 dpf, immediatelyprior to hatching. OPC response declined uponhatching and increased thereafter during developmentof the yolk-sac larva. The equivalent spherical diam-eter (ESD), estimated from the regression of Hermanet al. (1991) for opaque particles, ranged from �0.7 to1.0 mm for eggs and yolk-sac larvae. Stained, live eggs

Figure 4. Comparison of CUFES and CalVET catches ofPaci®c sardine eggs of different developmental stage duringcruise JD9603. The ratio of the sum of eggs collected byCUFES to the sum of eggs collected by CUFES and CalVETnets is shown in relation to developmental stage of egg. Thesum of all eggs collected is shown in parentheses for eachstage. Stage one eggs (shaded) are not used in DEPM (Loet al., 1996).



and opaque, plastic beads the size of menhaden eggshad ESDs of 1.5±1.6 mm, while formalin-preservedeggs were of intermediate value.

DISCUSSION

CUFES has proven to be a reliable system with whichto sample pelagic eggs of ®sh. It provides shipboarddata on the distribution and abundance of target spe-cies of eggs under virtually all sea conditions in whichwe have deployed it thus far. Importantly, these in-clude conditions under which conventional samplers,including nets, may not be able to be used due to highwinds and heavy seas. CUFES attributes include thefollowing. (1) Sampling is continuous under nearly allsea conditions. This results in far more water sampledwhile at sea and no loss of samples in adverse condi-tions or `dead time' while in transit between stations.

(2) The rate at which water is sampled is constant. Inour use of CUFES reported here, the ®ltration a ratehas been �640 l min)1, independent of conditions,e.g. rate of ship movement and sea state. Flow rate mayvary between installations, depending on the hydraulichead (height from sea to concentrator) and wall fric-tion of the hose (distance from pump to concentrator).(3) Sampling can occur simultaneous with other shipactivities, underway or on station. For example,acoustic surveys of juvenile and adult ®sh can beconcurrent with sampling of eggs. (4) Fish eggs arequantitatively sampled. (5) CUFES samples are moreeasily analysed than those from conventional samplers,such as CalVET nets, owing to their concentration byrelatively large-mesh Nitex used in the concentratorand sample collector, and due to the action of theconcentrator. (6) Continuous sampling yields dataseries amenable to temporal and spatial analysis.

Figure 5. Site map, bathymetry, and cruise track from cruise 9308 of NOAA vessel Oregon II, January 1994. Cruise trackbegins at eastern edge and ends to the west. Shown are locations at end of each CUFES sample interval. See text for details.



The usefulness of data from CUFES depends on thedegree to which they compare with conventionalsamples. On both volumetric (Table 1) and areal(Table 2) bases, CUFES compares favourably withnets. Concentrations of eggs of pin®sh and Atlanticmenhaden at 3-m depth estimated from MOCNESS,Tucker, or bongo collections and CUFES were highlycorrelated (r2, 0.61±0.92). Pin®sh eggs are � 1.0 mm-diameter spheres and some extrusion was expectedthrough the 1-mm Nitex concentrator net and appearsto have occurred (Table 1); the slope of the linearregression of ECUFES on Enet was 0.25, signi®cantly lessthan unity, and the ANOVA indicated an effect ofsampling on egg abundance. Atlantic menhaden eggsare �1.6 mm-diameter spheres; the slope of the anal-ogous regression did not differ signi®cantly from unity,nor did an ANOVA indicate an effect of gear type onegg abundance. More data, hence statistical power,

may show CUFES, with a 1-mm concentrator mesh, toretain menhaden eggs with an ef®ciency less thanunity. Regardless, it is the consistency of this valuethat is important. CUFES has provided representativeestimates of volume-based egg abundance for bothspecies for which this comparison has been made.

Our data indicate that eggs 1.6 times the meshdimension are retained completely by CUFES,whereas eggs with a diameter equal to that of the meshdimension are retained with only a 26% ef®ciency.Lower retention of eggs by CUFES than nets may bedue to several processes. First, chance alone. Second,extrusion of eggs through the concentrator mesh.Third, disintegration due to mechanical damage. Theyolk in eggs of menhaden and sardine, which normallypossess a large perivitelline space early in develop-ment, is often dispersed through the entire egg volumeafter having passed through CUFES, as if the vitelline

Figure 6. CUFES and related data from cruise 9308 of NOAA vessel Oregon II, January 1994. All measurements are for 3 mdepth. See text for measurement details. Maps were made by using data at locations shown in Fig. 5 to construct a uniform grid,which was then colour contoured.



membrane were ruptured but the chorion remainedintact. Rarely, empty egg membranes are found. It isnot known at present where such damage arises, al-though we suspect it is in the mechanical samplecollector. Video recordings show eggs passing betweenthe concentrator and mechanical sample collector tobe in good condition, with yolk mass intact (Fig. 9).Effort is underway to correct this damage by use of amore gently-acting cod end with a large ®ltering sec-tion immersed in water. Even eggs with dispersed yolkare able to be assigned a stage of development, how-ever.

The correlation between the concentration of pe-lagic ®sh eggs estimated using CUFES sampling at 3 mand nets towed horizontally at 3 m (Table 1, Fig. 2)

and vertically over the range of eggs (Table 2, Fig. 3)is consistent with variability known for replicate col-lections of the plankton (Winsor and Clarke, 1940),including ®sh eggs (Silliman, 1946). Smith and Hewitt(1985) repeated collections of anchovy eggs with aCalVET net every 12 min for 84 min at 60 stations offsouthern California. Correlation coef®cients for col-lections 12 min apart increased from a median value of0.74 (range, W:0.25±0.93) for eggs 1 day old to 0.94(W:0.91±0.97) for eggs 3 days old. Correlation (r2) ofabundance (pteropods m)3) estimated from right andleft bongo nets in oblique hauls (n = 20) was 0.96 forLimacina in¯ata and 0.66 for Cavolinia in¯exa (calcu-lated from Table 3 of McGowan and Brown, 1966).Each collection device, including towed nets and

Figure 7. Histograms of frequency of occurrence of all samples (®lled circles in Fig. 5; open bars) and menhaden egg oc-currence (®lled bars), in relation to temperature, salinity, and chl a. All measured at 3 m.



CUFES, integrates over some volume of water andhence scale of patchiness, resulting in variable abun-dance estimates. Sources of variation in the horizontalinclude spawning in aggregations, and accumulation ofeggs in physical features such as fronts and Langmuirconvergences, and sources of variation in the verticalinclude depth of spawning, ascent rate of eggs, andphysical mixing and strati®cation. Ideally, one mightsample with CUFES at the `median depth' (sensu Wareand Lambert, 1985), whether directly measured (fromstrati®ed collections with a pump or nets), predictedfrom a model (Cambalik, 1993), or determined usingthe average of past measurements. The median depth

will vary (1±6 m for Atlantic mackerel, Ware andLambert, 1985; 3±9 m for the northern anchovy,Pommeranz and Moser, 1987; see also Sundby, 1991).We have opted to sample at a constant depth, usually3 m, most simple and robust logistically, and use theresults of a model (Cambalik, 1993) and empiricalcomparisions (Table 2, Fig. 3) using CUFES andCalVET, to infer areal abundance.

The use of CUFES to estimate the abundance ofeggs in a patch or area depends on the relation be-tween the volumetric abundance of eggs estimatedwith CUFES and the areal abundance estimated bynets towed vertically over the range of occurrence of

Figure 8. Optical plankton counter (OPC) data from CUFES. Two cases (A, B) are shown. For each, OPC data were collectedfor 20 min inside a patch (upper panels) and 20 min immediately outside a patch (middle panels) in a control region. Thedifference between the patch and control size-frequency distributions is shown in the lower panels. Note the peak, with mode� 38 digital size units, corresponding to menhaden eggs.



eggs. This, of course, depends on the vertical distri-bution of eggs and, in turn, the terminal velocity ofeggs and water-column mixing (Sundby, 1991; Cam-balik, 1993). One may assume, however, that pelagiceggs which, by de®nition, are positively buoyant, willmonotonically increase in concentration towards thesurface, as is the case for the Atlantic menhaden(Cambalik, 1993) and northern anchovy (Pommeranzand Moser, 1987). Cambalik (1993) used a one-di-mensional, time-dependent model of physical mixingwith laboratory-derived estimates of terminal ascentrate of Atlantic menhaden eggs to show they achievesuch a distribution within 12 h after spawning whenreleased as deep as 30 m. Hence, we hypothesized that

estimates of volume-based concentration at 3 m fromCUFES would be related to area-based estimates froma CalVET for northern anchovy and Paci®c sardine.This was the case for both species, with correlationcoef®cients for ln-transformed abundance of 0.85 and0.62 for anchovy and sardine, respectively. The slopeof the relation for both untransformed and ln-trans-formed data was greater for sardine than for anchovy.This may be due to the greater size, hence more ef®-cient retention, of the larger sardine egg but also todifferences in the vertical distributions of eggs of thesetwo species, for which comparative data are lacking. Arecent comparison of CUFES- and CalVET-derivedestimates of the concentration (eggs m)3) of pilchard,Sardinops sagax, eggs off the west coast of South Africayielded an r2 of 0.82 (n = 153) for untransformed data(C.D. van der Lingen and D.M. Checkley, Jr, unpub-lished data). We are now attempting to explain thevariance in the relation between volume- and area-based estimates of egg abundance by (a) measuring thevertical distribution of eggs and (b) predicting thisdistribution from their measured terminal ascent rate(Cambalik, 1993) and a mixing model forced by me-teorological and oceanographic variables able to bemeasured routinely at sea. To this end, a CTD shouldbe deployed with the CalVET net to measure physicalstructure of the water column. Such measurementswere not made during JD9603.

The average concentration of eggs in a large area orpopulation is needed at times, as for the daily eggproduction method (Lasker, 1985). This is done atpresent by taking CalVET collections at stations in apredetermined grid. The precision of the estimate of

Figure 9. Digitized images of menhaden eggs in CUFESacquired with OPC/video. Diameter of each egg is� 1.6 mm. (A) Early stage, < 24 h post fertilization; notelarge sphere of yolk and surrounding perivitelline space. (B)Late stage, > 48 h post fertilization; note curled embryo withsmall yolk sac.

Table 3. Response of optical plankton counter to individual particles. Age for eggs of Atlanticmenhaden, Brevoortia tyrannus, is days post fertilization (dpf). Hatching occurred at 3 dpf. ESDa isfrom semi-empirical equation of Herman et al. (1991).

Optical Plankton Counter Response

Particle type Digital size units (dsu)b ESD (mm)

Brevoortia tyrannusLive eggs, age 1 dpf 44 � 2 (15) �0.70Live eggs, age 2 dpf 53 � 1 (22) �0.78Live eggs, age 3 dpf 81 � 3 (32) �0.97Live larvae, age 3 dpf 47 � 3 (38) �0.73Live larvae, age 4 dpf 56 � 3 (37) �0.80Live larvae, age 5 dpf 60 � 3 (40) �0.82Stained, live eggs, age 3 dpf 186 � 2 (80) �1.5Formalin-®xed eggs, age 1 dpf 102 � 4 (36) �1.1

Polystyrene beads (opaque), 1.4±1.6 mm diameter 206 � 23 (96) �1.6

a Equivalent spherical diameter.b Data are mean � SE.



mean egg abundance depends on the number of sam-ples. CUFES may allow a signi®cant increase in pre-cision of this estimate for the following two reasons.

First, much more water potentially with eggs issampled when CUFES is deployed on and betweenstations. In JD9603, for example, 91 stations wereoccupied at �4 km spacing along transects. CalVETand CUFES samples were taken simultaneously ateach station. Between stations, CUFES samples wereacquired during 3±5 min intervals. A CalVET towfrom 70 m to the surface ®lters �3.5 m3 of water; in5 min, CUFES ®lters approximately the same volume(�3.2 m3) from 3-m depth. The total number ofCUFES samples in the 5.6-day cruise was 1396 and thetotal number of eggs collected was 10 120 for Paci®csardine and 1863 for northern anchovy. At the 91stations, CalVET collections yielded 518 sardine and85 anchovy eggs. The ratio of eggs collected byCUFES to those collected by CalVET is 20 and 22 forsardine and anchovy, respectively. The standard error,SD�x�, a measure of precision, depends on n, thenumber of samples: SD�x� � SD�x�= ��

np

. Hence, as-suming the SD�x� is similar between CUFES andCalVET and that SD�x� changes little from CalVET(n = 91) to CUFES (n = 1396), the standard error willdecrease by nCalVET=nCUFES� �1=2� 4:0. This was, infact, the case for anchovy (SD�x�, 0.33±0.078). Butthe decrease was less for sardine (0.93±0.68) due inlarge part to its higher sample variance. This, in turn,is due to the greater range of values from CUFES thanCalVET, indicating a highly contagious distribution.This decrease, however, does not take into accountthe increased autocovariance associated with CUFESsamples and hence may be an overestimate of the gainin precision (Thompson, 1992), an issue now underinvestigation (N. Lo, Southwest Fisheries ScienceCentre, NOAA, La Jolla, California, pers. comm.).

Second, analysis of CUFES samples at sea enablesadaptive sampling with consequent increases in theprecision of abundance estimates and survey ef®cien-cy. There was strong agreement (r2, 0.88±0.97) be-tween estimates of egg abundance made at sea at thetime of sampling and ashore with detailed microscopicanalysis of sardine and anchovy eggs from JD9603.Thus, sea counts are reliable indicators of egg abun-dance. Adaptive sampling will lead to a gain in pre-cision of the estimate of mean abundance if eggs arehighly aggregated, as is most often the case, and if theyoccur within a limited spatial area (Thompson, 1992).In the ®rst consideration, adaptive sampling will causethe survey pattern to include additional samples takenafter one meets a sample criterion, a critical number ofeggs per unit sample time or volume. In the second,

the survey pattern will be modi®ed to avoid prolongedsampling of waters not likely to contain eggs based onprior CUFES samples and other information, such asthe temperature dependence of egg abundance, AV-HRR SST, and 3-m temperature. Adaptive samplingusing CUFES may lead to signi®cant gain in precisionrelative to conventional sampling on a ®xed grid,leading to the more ef®cient use of ship time. In fact,when entering a patch of menhaden eggs in ourpresent investigations, eggs are ®rst detected visuallyon the video monitor and this information is used toinitiate more frequent sample collection.

For use of CUFES in the DEPM, eggs of all devel-opmental stages must be sampled with equal ef®ciency.This criterion, in turn, depends on the vertical dis-tribution of eggs of different stages of development.This distribution may vary between species and willdepend on depth of spawning and dependence of theascent rate on stage of development and environ-mental conditions. All developmental stages, save the®rst, of the Paci®c sardine appeared to have beensampled with equal ef®ciency by CUFES and CalVETnets in JD9603 (Fig. 4). Of the few (n = 34) stage-oneeggs collected, nearly all (n = 31) were caught by theCalVET net. This bias may have been due to chanceand/or the occurrence of stage-one eggs below theCUFES pump depth. Stage-one eggs are rarely col-lected by nets in DEPM surveys, presumably due totheir highly aggregated distribution, and thus are notused to estimate egg production or mortality (Lo et al.,1996). Comparison of CUFES and areal abundanceswith regard to stage of development will be necessarywhenever CUFES is to be used for stock assessmentusing the DEPM.

Few data exist for the distribution of eggs of theAtlantic menhaden off North Carolina, the primaryspawning region of this species (Judy and Lewis, 1983).Checkley et al. (1988) and Warlen (1994), based onthe collections of eggs and young larvae, indicatespawning to occur between the west wall of GulfStream and the mid-shelf front, a region delimited bysea surface temperatures of �21±15°C and salinity36.2±36.5. CUFES results presented here are consis-tent with this distribution. In addition, eggs tended tobe found in water with ³ 0.1 lg chl a l)1. Together,these data are consistent with spawning near thewestern wall of the Gulf Stream in recently upwelled,nutrient-rich water (Checkley et al., 1988). The dataare as yet too few to test the hypothesis that spawningoccurs during storms (ibid.), although CUFES facili-tates such a test due to its high ef®ciency (volumesampled / survey time) and ability to operate duringstorms. Data from 1994 to 1995 (not presented here)



show patches of menhaden eggs to have occurred inthe same geographical region as in 1993±94 (Fig. 6)and hence spawning may, in addition, be related tobathymetry. This may be evolutionarily advantageousowing to the placement of eggs in a region with pre-dictably favourable transport and development(Checkley et al., 1988; F. Werner, University of N.Carolina, Chapel Hill, pers. comm.). Sampling andmodelling studies are under way to address this idea.

At present, data on egg distributions from CUFESare obtained from the microscopic analysis of samples.We believe, however, that automation of the countingof target eggs in CUFES is feasible. Analysis of ourOPC data by differencing size-frequency distributionswithin and near patches of eggs clearly showed a peakattributable to menhaden eggs (Fig. 8). Integrationbeneath the peak yielded an estimate of menhadeneggs surprisingly similar to the actual number of eggsknown to have passed through the OPC and retainedby the MSC during these sampling periods. Finally,the mean and range for digital size of eggs in nature(Fig. 8) corresponded well to the digital size of eggsspawned and reared in the laboratory (Table 3), par-ticularly for early to mid-stage eggs, which dominatedthese patches. The increase in digital size of eggs andlarvae during development is most probably a functionof accumulated tissue, including melanophores, andorientation of the embryo and larva. Similar resultshave been reported for the Baltic cod (Wieland andKoÈester, 1996). Our comparison between the OPC andmicroscopic counts was made using samples of knownabundance of menhaden eggs, based on prior, micro-scopic analysis. We are developing real-time, video-based egg identi®cation and counting, either with orwithout use of the OPC. Images of early and late-stageeggs of the Atlantic menhaden (Fig. 9) are amenableto computer analysis and identi®cation. While mi-croscopic examination of net samples will always beneeded in conjunction with data from electronic de-vices, the use of the latter appears feasible in the nextseveral years. This would further enhance the ef®-ciency of CUFES and its use in the DEPM and basicscience studies.

CUFES has not only applied merit but is useful forbasic studies. The processes responsible for survivaland, conversely, mortality of the pelagic eggs of ®shoperate on scales from less than metres to greater thantens of kilometres. For example, eggs that accumulatein windrows of Langmuir circulations may be moresusceptible to predators (Matsushita, 1991). On alarger scale, eggs spawned in water upwelled at theGulf Stream Front during storms may exhibit optimaldevelopment and survival (Checkley et al., 1988).

CUFES affords the possibility of investigating thedistribution of eggs over this range of spatial scalessimultaneously.

ACKNOWLEDGEMENTS

Alex Herman contributed to the original design ofCUFES and provided valuable advice on use of theOPC. Jake Cooke, Bill Hettler, Woody Sutherland andnumerous other persons, including the captains andcrews of the NOAA vessels Albatross, Oregon II, andDavid Starr Jordan, contributed both at sea and ashore.John Hunter, Nancy Lo, Geof Moser, Rich Charter,and Paul Smith provided data for eggs of the northernanchovy and Paci®c sardine and Fig. 1. Trevor Cooperassisted in data analysis and presentation. Two anon-ymous reviewers provided constructive comments.This work is supported by the National ScienceFoundation (OCE-9296148 to DMC) and NOAACoastal Ocean Program's South Atlantic Bight Re-cruitment Experiment grants to DMC and PBO.

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A continuous, underway fish egg sampler 6... · 2015-04-29 · A continuous, underway ﬁsh egg...

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