56 (2006) 294–304www.elsevier.com/locate/seares

Journal of Sea Research

Fine-scale distribution of sardine (Sardina pilchardus) eggs andadults during a spawning event

Juan Zwolinski ⁎, Evan Mason, Paulo B. Oliveira, Yorgos Stratoudakis

IPIMAR, Av. Brasilia s/n, 1449–006 Lisboa, Portugal

Received 4 August 2005; accepted 24 May 2006Available online 6 July 2006

Abstract

High-resolution acoustic and ichtyoplankton sampling with a ‘continuous under-way fish egg sampler (CUFES)’ was performedin two regions of approximately 100 square nautical miles off southern Iberian Peninsula, with the aim of studying the small scaledistribution of sardine (Sardina pilchardus) adults and eggs during a spawning event. Very dense patches (246 eggs m−3) ofrecently spawned eggs with dimensions (up to 3 nautical miles wide) significantly larger than daytime sardine schools were presentin both regions. Egg staging and ageing showed very little intra-sample variation, indicating a synchronous spawning period atdusk. The internal structure of the patches evaluated by variography showed very low internal variability, as if they consisted of asingle unit. This hypothesis is confirmed by the acoustic finding of large sardine shoals with similar dimensions to those of thepatches after sunset and throughout the night. During that period, adults were found near or in contact with the bottom, suggestingthat spawning occurred at depth. A distinct patch of older eggs was found in both areas, but with a few nautical miles of horizontalseparation. Their characteristics (a larger area, lower egg densities and a more irregular shape) indicate that these patches wereexposed to dispersion and ‘stirring’ by physical forces, reshaping their initial appearance, while mesoscale water circulation couldhave displaced the core of the patches away by several kilometres within a day.© 2006 Elsevier B.V. All rights reserved.

Keywords: Sardina pilchardus; CUFES; Acoustics; Fish distribution; Dispersion; Daily egg production

1. Introduction

Schooling behaviour is a salient characteristic ofsmall pelagic fish contributing to complex spatio-temporal organisation and dynamics at scales rangingfrom 10 s of metres to 100 s of kilometres and fromminutes to weeks or months (Mackinson et al., 1999;Petitgas et al., 2001; Haugland and Misund, 2004).Habitat occupation by schools and school clusters ispatchy and frequently reshaped to minimise predation

⁎ Corresponding author.E-mail address: juan@ipimar.pt (J. Zwolinski).

1385-1101/$ - see front matter © 2006 Elsevier B.V. All rights reserved.doi:10.1016/j.seares.2006.05.004

risk and maximise feeding potential (Pitcher et al., 1996;Misund et al., 1998; Haugland and Misund, 2004).Schooling behaviour follows the diel pattern of ambientlight levels (Fréon et al., 1996; Beare et al., 2002), withlooser aggregations and upward migration oftenreported during the night (Giannoulaki et al., 1999;Orlowski, 2005). In the case of clupeoids laying pelagiceggs (especially anchovies and sardines) the diel patternof schooling may become more complex during thereproductive season, when ephemeral spawning aggre-gations are created by ripe females joining male-dominated formations (Hunter and Goldberg, 1980;Alheit, 1993; Ganias et al., 2003; Stratoudakis et al.,

Fig. 1. Acoustic survey day transects extending from the Gulf of Cadiz(Spain, to the east of the Guadiana River) to the western part of theAlgarve in Portugal (west of the Guadiana River) and small samplingevents. Crosses correspond to 1 nm EDSU during day sampling, thetwo clusters of circles correspond to 1 nm CUFES and EDSU duringthe small-scale survey. In both cases, small-scale sampling wasconducted from the east to the west starting roughly at 18:00 andlasting for approximately 12 hours.

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2006). The early distribution of eggs is thought to reflectthe spatial organisation of spawning adults (Smith,1973; Curtis, 2004) but it becomes progressivelyreshaped by physical forcing in the upper layers of thewater column (Fletcher et al., 1996; Stabeno et al., 1996;Lynn, 2003).

The spatial dynamics of pelagic fish and eggs need tobe taken into account in the design and estimation ofacoustic (Barange and Hampton, 1997; Petitgas et al.,2001) and ichthyoplankton (Uriarte and Motos, 1998;Fletcher and Sumner, 1999; Lo et al., 2001) surveys thatare extensively used worldwide to support stockassessment and management decisions for manycommercially important clupeoid stocks. In the case ofthe daily egg production method (DEPM), adequateknowledge of spawning dynamics is required to obtainunbiased and precise estimates of egg production anddaily fecundity (ICES, 2004). Here, we study the fine-scale spatial distribution of sardine Sardina pilchardusand its eggs during two spawning events off thesouthern Iberian Peninsula using combined acoustic,ichthyoplankton and environmental sampling. Theresults provide new insight into the spawning behaviourof sardine and the hydrological influences on eggdistribution at the spatial scale of individual spawningevents that usually remain unresolved during routineDEPM surveys.

2. Material and methods

2.1. Egg and acoustic sampling

During the Portuguese acoustic survey for sardine inNovember 2001, intensive acoustic, ichthyoplanktonand environmental sampling took place in two locationsoff the southern Iberian Peninsula. Each location wassampled over a single night. Both sites covered an areaof approximately 100 square nautical miles (nm) andwere placed in areas where sampling during daytimeindicated large concentrations of pelagic fish andsardine eggs. The first location was situated in theGulf of Cadiz, southwest of the Guadalquivir Rivermouth in Spain, centred at 36.8′N, 6.85°W (Fig. 1). Thisarea was surveyed from late afternoon on 12 Novemberto the morning of 13 November (12 h of sampling) and atrawl station was performed at 15:00 on 12 November,yielding 1365 fish, of which 860 were sardine. Thesecond location was south of Lagos in southern Portugal(Algarve), centred at 37.0°N, 8.65°W (Fig. 1) and wassampled from late afternoon of 17 November to earlymorning on 18 November. Three trawl stations wereperformed in the latter area during the day of 18

November with a total number of 154, 272 and 1422 fishof which 154, 258, 1351, respectively, were sardine.

In each site, sampling took place on a regular gridalong 11 parallel transects with an inter-transect distanceof 1 nm. Ichthyoplankton sampling was performed withan externally mounted CUFES (Checkley et al., 1997)sampler. This device enabled us to continuously samplethe sub-superficial (3 m) layer of water for plankton invery fine detail, simultaneously obtaining physical andbiological parameters. Egg samples were taken every6 min along the transects, corresponding to 1 nm of eggintegration at a cruising speed of 10 knots. Geographicalposition, time, filtered water volume, and mean salinity,fluorescence and temperature were recorded for eachsample. Egg samples were kept in a 4% formalin/saltwater solution for later analysis. Acoustic data obtainedwith a Simrad EK500 scientific echo-sounder at 38 kHzwere digitally recorded with the MOVIES software(Weill et al., 1993) for depth and adult fish analysis. Forthe Lagos site, additional information from the standarddaytime acoustic survey taken on 18 November was also

Fig. 2. Sea surface temperature map of 14 November 2001 for Cadiz(top) and Lagos (bottom). The dots represent the CUFES samples andarrows indicate the displacements of thermal structures observedbetween successive images from 13 and 14 November.

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analysed, since three of these transects were within thearea sampled during the previous night. In this case,CUFES samples were taken at 18 min intervals(approximately 3 nm) and the elementary distancesampling unit (EDSU) for acoustics was set at 1 nm, theusual spatial resolution of sampling during acousticsurveys in the Iberian Peninsula.

In the laboratory, with the aid of a binocularstereoscope, sardine eggs were staged according toICES (2004) and their age was calculated by the stage/age temperature-dependent relation obtained by Mir-anda et al. (1990).

2.2. Data analysis

Egg counts were standardised by volume and therewere no attempts to obtain overall abundance estimatesfor the whole water column. The area occupied by eachdaily egg cohort was estimated as the total sampled areatimes the proportion of positive stations. Severalsemivariogram models (gaussian, power and spherical)were fitted to empirical semivariograms (Chilés andDelfiner, 1999) calculated from egg concentrations, inorder to establish the degree of correlation at small lags.Semivariogram calculation and fitting was performedwith the package geoR (Ribeiro and Diggle, 2001)being the sample semivariogram calculated by therobust estimator of Cressie (1991) to just half thedistance between the two outermost transects. Fitting ofthe theoretical model was performed by weighted leastsquares and the best fit was decided by residual analysis.Contouring of egg density data and environmentalvariables was performed by kriging.

Fish backscatter with volume backscattering strength(Sv) higher than −60 dB (lower threshold for sardinesurveys off the Iberian Peninsula) was integrated forevery CUFES sample. The resulting nautical areascattering coefficient (NASC) for each sample waspartitioned according to Nakken and Dommasnes(1975) based on the nearest trawl catch composition.

2.3. Oceanographic features

For a large-scale consideration of the main oceano-graphic features during the sampling period, sea surfacetemperature (SST) images were obtained from theEUMETSAT Ocean and Sea Ice Satellite ApplicationFacility (O&SI SAF) led by Météo France. The datawere extracted from the ‘Regional SST’ product,‘CANA’ zone, available from the O&SI SAF server instereopolar projection at 2-km resolution. These datarefer to the subskin SST, comparable to in situ (buoy)

measurements at night, computed according to theprocedures described by Brisson et al. (2001). Twosuccessive high-quality, cloud-free images wereobtained for 13 and 14 November 2001. From theseimages, two smaller areas centred at the location of therespective CUFES surveys were extracted to allow adetailed analysis of the small-scale structures andestimation of their advection velocities. These velocitieswere estimated by measurement of the displacement ofidentifiable structures that occurred between the twodaily images (Fig. 2). A generally eastward flow patternis evident at both locations with velocities ranging from4.5 to 10 nm d−1.

The wind evolution at Cadiz and Lagos was alsotaken into consideration through data obtained from theNational Centers for Environmental Prediction (NCEP)web-site, which provided a 6-hourly derived windproduct at 2.5° resolution. During the survey, windswere from a northerly direction and did not exceed 4 m

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s−1, corresponding to maximum displacements of lessthan 1 nm over a 12 h period. These estimates werebased on Vek= t/(r.df) to compute the Ekman layervelocity Vek, where t is the NCEP wind stress, airdensity r=1.22 kg m−3, Ekman layer depth d=15 mand f the Coriolis parameter.

3. Results

The CUFES and acoustic data from the two small-scale surveys were able to capture spawning events ofconsiderable dimensions, with eggs, adults and oceano-graphic data gathered simultaneously within a relativelyshort period of time. Cross-shelf CUFES transectsextended beyond the limits of sardine egg and fishdistribution in both sampling sites. Egg presence wasrestricted to the mid-shelf (40–105 m in Cadiz and 35–95 m in Lagos), with a symmetric distribution of eggdensities along this depth range (Fig. 3). Along-shelfspatial delimitation was less clear, particularly in the

Fig. 3. Egg distribution in space and depth in the two sampling regions. Circleeggs m−3) which was obtained in Lagos and ‘x’ represents CUFES samples

eastern boundary of Cadiz and the western boundary ofLagos. Sardine egg densities were high in both sites,with higher values in Lagos (mean of 23.4 eggs m−3

against 15.5 eggs m−3 in Cadiz). In Lagos, CUFES eggdensities were at the level of the highest records from theregular acoustic surveys in Portuguese waters over theperiod from 2000 to 2005.

SSTs were slightly above 18 °C in both areas, whichin sardines leads to hatching of larvae approximatelytwo days after spawning. Egg staging and ageingrevealed that the samples were composed of two dailycohorts: Day-0 and Day-1, the former consisting ofyoung eggs spawned during the night the sampling tookplace and the latter of older eggs spawned the nightbefore. The homogeneity of stages within each sampleand the progression of stages over sampling timeindicated a spawning synchronism around dusk forboth daily cohorts. The spatial distribution of the twocohorts revealed that, at each site, what initiallyappeared to be a continuous egg patch (Fig. 3), consisted

diameters are proportional to the absolute maximum observation (259with no eggs.

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in fact in two structures with little spatial overlap anddistinct shape and extension (Fig. 4). The observationsfor each cohort in the two sites provided structuredsemivariograms with similar shape and very smallnugget effects (Fig. 5), indicating that each cohortconsisted of a smooth and single patch with nosignificant components of variation at spatial scalesbelow that of sampling.

Day-0 patches were more compact and had sharpermargins than Day-1 patches in both sites (Fig. 4). Eggdensity at the centre of the Day-0 patches reached 141and 246 eggs m−3 in Cadiz and Lagos, respectively,approximately an order of magnitude larger than themean density in each site. Day-0 eggs were found in55% of the samples in each site, while Day-1 eggs had aconsiderably wider distribution (79% and 78% in Cadizand Lagos, respectively). In the Day-1 cohorts, eggdensities were also lower than their youngest counter-part, reaching 67 eggs m−3 in Cadiz and 184 eggs m−3

in Lagos. Although sampling deficiencies (incompletehorizontal delimitation and insufficient vertical integra-

Fig. 4. Egg-density contour separated by daily cohorts superimposed

tion) do not allow the estimation of daily production andmortality from these data, the observed cohort distribu-tions and densities indicate that diffusion must haveinteracted with mortality to increase the distancebetween eggs, lower their density and increase theirdistribution area.

Together with the egg patches, Fig. 4 shows waterdensity anomaly (sea-water density in kg m−3-1000)contours, computed from CUFES temperature andsalinity data. The Lagos site features a marked densityfront running east-west across the southern part of theplot; at Cadiz the isopycnals are more complex,revealing a southern area of lighter water intrudinginto the denser water to the north. The Cadiz Day-0patch is well resolved with the highest egg concentra-tions in the centre. The core of the patch (measuredwithin the 30 eggs m−3 contour line) has a meandiameter of almost 3 nm and lies within the 25.98isopycnal. At Lagos, although the main Day-0 patch wasonly partially sampled in the along-shore direction, asharp radial concentration gradient, lying over the

on water-density anomaly calculated from in situ CUFES data.

Fig. 5. Sample semivariograms of egg data with fitted model. All models are Gaussian semivariograms, apart from Day-0 in Cadiz, which is a powermodel.

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density front between the 26.16 and the 26.28isopycnals, is visible at the western limit, suggestingthat this patch is similar in shape and size to the CadizDay-0 patch.

The Cadiz Day-1 egg distribution (Fig. 4) iscomplex: there are two centres of rather low (incomparison with Day-0 values) egg concentrations atthe bottom right of the plot; the first of these centres isat the head of a tongue of denser water — a ‘wake’ oflow egg concentrations extends westward from itscentre, following the 25.98 isopycnal; the secondcentre of concentration lies to the right of the first, andis located over a region of lighter water. In contrast toCadiz, the Lagos Day-1 patch is still a highly coherentbody, with high egg concentrations. To the west of thispatch a similar ‘wake’ of low egg concentrations isalso visible. Both the patch and wake lie over thesurface density front, between the 26.16 and 26.26isopycnals. Although not very clear for the Cadiz Day-1, in Lagos the Day-1 patch core diameter in theNorth-South direction is 1 nm larger than that of theDay-0 cohort.

The eastward surface flow estimates inferred fromthe satellite images (Fig. 2) matches with the distanceand relative position of the cohorts, indicating that ineach region the two daily cohorts were spawned roughlyin the same location although neither the in situoceanographic and biological data (temperature, salinityand fluorescence) nor the satellite images revealed anymarked difference between the presumed spawning

location and the surrounding waters. The ‘wake’ of eggs‘behind’ the centre of the Day-1 patches is another proofof the eastward movement of the patches that may berelevant to the analysis of CUFES data taken with alower resolution on the following day at Lagos (Fig. 6).Fig. 6 shows the Day-0 egg distribution in threetransects about 15 h after the night sampling. Theoverall picture is quite different, with absence of eggs inareas where they were previously found and with thepresence of two high-density samples at the centre of thefigure to the east, suggesting that the whole Day-0structure has shifted eastwards. Also, quite noticeable isthe lack of perception of the patch as the sampling gridgets coarser. This was verified by variography applied toCUFES egg data across the daytime transects of thewhole survey region (Fig. 1), which showed a great lossin spatial structure resulting in a flat semivariogram.

Fig. 6 also shows the presence of important echotraces at the Lagos site during the night, confirmed tobe mainly (90% of the acoustic energy) maturesardines. The night echo traces were mostly presentin the western part of the survey to depths of up to60 m, which is slightly lower than the depths whereeggs were found. The spatial distribution of sardines atnight matched the distribution of sardine echoes of thefollowing day, showing the same decreasing trendtowards the west. In general, higher NASC valueswere obtained during the night, with the maximum(14,817 m2 nm−2) being more than twice the daytimehighest value (6370 m2 nm−2). In Cadiz, fish were

Fig. 6. Comparison of day and night sampling of eggs (left) and sardine echoes (right) in Lagos. In the egg plot, circles represent the Day-0 cohortduring the night (open circles) and on the following day (full grey circles). ‘X’ indicates the samples with no eggs during the day and the dots show thenil samples during the night. In the NASC plot, empty circles represent night sardine NASC and full gray circles day-time sardine NASC. ‘X’represents EDSU with no sardine energy and the dots their night counterparts. Circle diameters are proportional to maximum local values.

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present only in the shallow part of the survey area(Fig. 7), slightly inshore of the centre of the Day-0patch. NASC values were also high, with a maximumof 12,400 m2 nm−2, but the partition of the total echo-integral based on the nearest trawl haul yielded only48% of the energy for sardine. As in Lagos, thedaytime acoustic sampling also showed lower NASCvalues.

Differences in sardine schooling behaviour betweenday and night were also found. In Lagos, from the onsetof sampling (18:40, more than 1 h after sunset) andthroughout the night, sardines were found formingextensive demersal shoals in a continuum that reachedmore than 2 EDSU (Fig. 8) along transects. Some of theshoals were probably more than 2 nm in the along-shelf

Fig. 7. Sardine NASC data in Cadiz during the night (empty circles)with Day-0 egg cohort in full grey circles. Circle diameters areproportional to maximum local values.

direction, hence only slightly lower dimensions thanthose of the egg patches. These aggregations wereattached to the bottom, with heights ranging from 10 s ofcm up to 10 m above the seabed. No significant echotraces were found in the upper half of the water column,and even in the more shallow waters fish shoals weredemersal. This seems to corroborate previous anecdotalevidence that sardine spawning off Portugal occurs nearthe bottom. This makes possible that a part of the Day-0patch in Lagos could have been lost during the earlynight sampling due to their unavailability for CUFESsampling at the surface, in particular in the east andmiddle part of this site. In Cadiz, extensive sardineshoals were also found during the night but they weregenerally not in close contact with the bottom, butinstead holding their position 5 to 10 m above theseabed. During dawn and early morning (Fig. 8) thesardine schools reorganised. In Lagos, some of thelarger schools were now clearly pelagic, separated fromthe substrate, but more than 80% of the day EDSUs withsardine presence still had schools in the proximity or incontact with the bottom. In Cadiz, sardine schools werefound to be in mid-water, with almost 80% of theEDSUs containing only pelagic schools. In both areas,school values of Sv, were 10 to 20 dB higher duringdaytime, meaning an increase in volumetric fish densityof 10 to 100 times.

4. Discussion

CUFES has proved to be a valuable tool for small-scale studies, as it provides a quasi-synoptic view overa large area with less time and effort than conventional

Fig. 8. Daily pattern of sardine schooling from selected echograms in the Lagos site at 20:30 (top) and 9:30 (bottom). Vertical lines indicate 1 nm.Sunrise and sunset occurred at 7:09 and 17:23, respectively.

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net samplers of the water column. Also, the ability tocouple CUFES with acoustics and oceanographic datais of major importance for ecological and behaviouralstudies such as the present study. Compared to similarstudies on Sardinops sagax (Curtis, 2004; Fletcher andSumner, 1999, van der Lingen et al., 1998), the eggdensities observed in this study are highest, meaningthat sampling was performed in areas of intensespawning. At a cruising speed of 10 knots, CUFESwas able to sample around 100 nm2 with 1 nmresolution in less than 12 h. As a result, the areasampled was large enough for the purpose of the studyand with sampling duration sufficiently constrained toavoid large changes in oceanographic conditions, andin the distribution of the eggs and adults. However, theincrease in the two-dimensional resolution of eggpatches comes at a price: there is no information on thevertical distribution of the eggs in the water column,thus precluding inference of total abundance and eggmortality rates from this study.

The Cadiz Day-0 and Lagos Day-1 cohorts showed astructured body resembling a bell-shaped distribution,suggesting a pulsed source from a single origin (Largier,2003). The finding of such patches with diameters of upto 3 nm is a novelty in comparison with other clupeoidssuch as the Pacific sardine (S. sagax), where eggs arereported to be spawned in a mosaic pattern of fish schoolproportions (Smith, 1973), or anchovy, where the largeregg patches are in the order of hundreds of metres long

(Smith et al., 1985; Hunter and Lo, 1997). It is unlikelythat the egg patches we sampled were composed ofsmaller units such as those referred above for otherspecies, because such a spatial organisation would havebeen detected in the form of a nugget effect in thevariogram analysis.

The analysis of the adult distribution from thebeginning of sampling and throughout the night showedthat fish were organised in large shoals with dimensionscomparable to that of the Day-0 patches, establishing thelink between adults and eggs and showing that the scaleof sardine egg patches may be larger than the commonschool dimensions observed during daytime (Muiño etal., 2003). While larger in size, night shoals showedinternal concentrations 10 to 100 times lower thanduring the day. This fact appears contradictory to what iscommonly perceived to be a school of spawning fish.However, a study on Sardinops melanosticus off Japan(Shiraishi et al., 1996) revealed that this species spawnsin pairs rather than in swarms, explaining how thesardines could be loosely occupying a wide area and yetbeing able to mate.

The dynamics of sardine spawning and early eggdistribution observed in this study provide informationthat is relevant for understanding processes that affectDEPM sampling and estimation but occur at spatio-temporal scales unaccounted for during routinesampling. The disaggregation of sardine schools andthe formation of large shoals with reduced density

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around dusk, which is the period of peak sardinespawning (Zwolinski et al., 2001; ICES, 2004),indicates that sardine spawning can occur at a spatialscale considerably larger than that of the school. Atboth sites, the presence of a continuous shoal duringthe night over an area similar to that occupied byyoung eggs (in the case of Lagos reaching severalnm2) indicates that during spawning and the firsthours thereafter, active spawners are in close proxi-mity to non-spawning fish. This allows us to interpretthe existence of large variation in biological properties(sex ratio and spawning fraction) over repeated haulsin the same location during and after dusk (Stratou-dakis et al., 2006). The size, patchiness and degree ofsegregation of active spawners within the shoal remainunknown, but the limited vertical extension of theshoal precludes vertical segregation as the reason forthe frequent observation of male-dominated adultsamples together with hydrated females around thedaily spawning peak of several sardine and anchovyDEPM applications worldwide (Hunter and Goldberg,1980; Alheit et al., 1984; Ganias et al., 2003).

The close association of the observed shoals to thebottom around dusk also indicates that sardinespawning takes place in the bottom third of thewater column, and that it takes at least a few hours foreggs to ascend to the upper part of the column andattain vertical stability (Coombs et al., 2004). As aresult, CUFES (which is often used as a secondarysampler in DEPM surveys (Lo et al., 2001; ICES,2004) may be an unreliable sampler of young eggs inthe first hours after spawning, thus preventing theresults of the present study from being used to explorethe impact of dispersion on the estimated eggmortality. Despite this deficiency, the CUFES dataare able to show that, once at the surface, eggdistribution is constantly reshaped by local oceano-graphic events. A consequence of this is the contrastobserved between the Day-1 patches in both regions.In Lagos, the zonal density front favours a stable,eastward advection resulting in a westerly wake ofeggs behind the patch as the result of the meaneastwards flow (Fig. 4). For this reason, the Day-1 eggpatch remains a single coherent structure where anapparent bell-shaped distribution is maintained,although it is expected to be significantly displacedfrom its origin by the mean flow. The lower maximumegg concentration in this cohort relative to the Day-0patch is an expected consequence of the diffusionprocesses, which also appears as an increase in theoverall area. By contrast, the water density structure inCadiz is more complex, and so is the patch structure.

Small-scale eddies appear to have broken the originalpatch into two close, but separate, centres in a‘stirring’ rather than a mixing process (Siegel et al.,2003). The resultant area increase again indicates thepresence of a diffusive process, so that egg concentra-tions are substantially decreased within the patch area.

The common feature of both regions is that, givena certain amount of time (between 24 and 36 h) theoriginal egg distribution can be significantly re-shapedand advected. Hence, it appears that the observedevolution in the distribution of daily egg cohortsresulting from the physical processes can explain thelow levels of precision observed in the estimation ofdaily egg production for DEPM purposes (coefficientof variation in the order of 30% or higher). Althoughspatial modelling techniques have recently allowedsome improvement in the precision of estimates(Borchers et al., 1997; ICES, 2004), these modelscan only accommodate large-scale spatial differencesin mean production. Hence, the small-scale spatialvariation resulting from the accumulated effect ofhydrography on a daily egg cohort (from the time ofattaining vertical stability to hatching) is unlikely to becaptured by any modelling procedure and makes acase for the use of larger samplers, even in the case ofsardines and anchovies (where the CalVET net hasbeen introduced to reduce laboratory time in sortingand staging of large samples; Smith and Hewit, 1985).

Acknowledgements

The work of Juan Zwolinski is funded by thePortuguese Ministry of Science through a PhD grant.Evan Mason was funded by the project PELAGICOS(FCT PLE/13/00). The authors are grateful to ‘ProgramaPELAGICOS’ funded by the Portuguese Ministry ofScience and to ‘Plano Nacional de AmostragemBiológica for funding IPIMAR's acoustic survey.Acoustic day-time echogram scrutiny and trawl proces-sing data were provided by Vitor Marques andAlexandre Morais at IPIMAR. NCEP Reanalysis datawere provided by the NOAA-CIRES Climate Diagnos-tics Center, Boulder, Colorado, USA, from their Website at http://www.cdc.noaa.gov/. Thanks to the Institu-tions that distributed satellite data: Goddard EarthSciences Distributed Active Archive Center (GES-DAAC) for MODIS/Terra Ocean Color Derived Pro-ducts, EUMETSAT Ocean and Sea Ice SatelliteApplication Facility at Météo France for the SSTmaps. We would also like to thank an anonymousreferee for the comments that improved the originalmanuscript.

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