Changes in the distribution of sardine eggs and larvae offPortugal, 1985–2000

Y. STRATOUDAKIS,1,* M. BERNAL,2

D. L. BORCHERS3 AND M. F. BORGES1

1Instituto de Investigacao das Pescas e do Mar (IPIMAR),Avenida de Brasilia, 1449-006, Lisboa, Portugal2Instituto Espanol de Oceanografıa (IEO), Puerto Pesquero s/n,29640 Fuengirola, Malaga, Spain3Research Unit on Wildlife Population Abundance (RUWPA),University of St Andrews, North Haugh, KY16 9SS, St

Andrews, UK

ABSTRACT

Generalized additive models (GAMs) were fitted tosardine (Sardina pilchardus) egg distribution data fromthree daily egg production method surveys. The resultsshowed that the area of egg cover off Portugaldecreased significantly from 11 800 km2 in 1988 to7000 km2 in 1997 and 7400 km2 in 1999. This isbecause of a significant reduction in sardine egg pres-ence off northern Portugal, GAM estimated areasbeing similar or higher in the late 1990s for south-western and southern Portugal. The distributional areacovered by larvae was not estimated for 1988 (larvaldistribution extended beyond the survey area),although it was probably higher than the 9600 km2 for1997 and 5500 km2 for 1999. In 1997 and 1999, theGulf of Cadiz was also sampled, indicating extensiveareas with sardine eggs and larvae (more than 50% ofthe total area of distribution off Portugal). Standard-ized data from 15 ichthyoplankton surveys between1985 and 2000 show a decline in the mean probabilityof egg presence within the Portuguese continentalshelf from the mid-1980s to the late-1990s, because ofa marked reduction in egg presence off northernPortugal. Sardine larval data from the same surveyssuggest that the reduction in mean probability ofpresence in the north is less marked than for eggs (al-though this comparison ignores the presence of sardinelarvae beyond the continental shelf in the 1980s).Similar changes off northern Portugal and western

Galicia are observed in commercial sardine catches andthe acoustically estimated area of fish distribution. It ispossible that the observed decline in spawning area offnorthwestern Iberia during the 1990s is indirectlyreflecting the prevalence of environmental conditionsdetrimental to sardine recruitment (northerly windsduring winter that favour coastal upwelling and off-shore transport), which have reduced the spawningcontribution of young fish in that area.

Key words: decadal changes, distribution, generalizedadditive models, Iberia, sardine

INTRODUCTION

Sardine (Sardina pilchardus) supports the largestcommercial fishery in the Atlantic waters of theIberian Peninsula, with annual catches generallyranging between 100 000 and 200 000 tonnes. Inrecent years, a dramatic decline in northern Iberianlandings, and the ensuing uncertainty in the state ofthe Atlanto-Iberian sardine stock, have intensifiedthe search for fisheries-independent information(ICES, 2000). The estimation of areas covered bysardine eggs and larvae using data from ichthyo-plankton surveys assists in constructing historicaltime series and exploring changes in the spawningdistribution of the stock. The use of �spawning� areainformation has for some time been advocated as aninexpensive means of crude evaluation of fisheriesresources (Mangel and Smith, 1990; Smith, 1993;Watanabe et al., 1997; Zenitani and Yamada, 2000).Smith (1990) suggested that estimates of the spawn-ing area of Pacific sardine (Sardinops sagax) cancomplement more reliable fisheries-independent esti-mates of stock size in years when the latter are notavailable; Deriso et al. (1996) included model-basedestimates of sardine egg and larval presence in acatch-at-age assessment model.

Augustin et al. (1996) and Borchers et al. (1997)demonstrated how presence/absence data could beused to model the distribution of wildlife empirically.In this study, we use generalized additive models(GAMs – Hastie and Tibshirani, 1990) to describethe spatial distribution of sardine eggs and larvae off

*Correspondence. e-mail: yorgos@ipimar.pt

Received 12 January 2001

Revised version accepted 12 May 2002

FISHERIES OCEANOGRAPHY Fish. Oceanogr. 12:1, 49–60, 2003

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the Portuguese coast and the Gulf of Cadiz. Thisallows us to estimate the area of egg and larval coverwith confidence intervals and to investigate statisti-cally significant changes in distributional cover amongsurveys. GAMs are fitted to sardine egg and larvalpresence/absence data from three surveys dedicated tothe application of the daily egg production method(DEPM) to Atlanto-Iberian sardine (ICES, 2002a).These surveys are the most reliable of those availableoff Portugal, as they cover the entire distribution areaof sardine eggs and follow identical sampling proto-cols. We then compare the GAM results with sum-mary statistics from all ichthyoplankton surveys (15surveys from November 1985 to March 2000) thatwere undertaken in Portuguese waters within thesardine-spawning season. Finally, we compare theichthyoplankton results with sardine information fromother sources (acoustic surveys and commercialcatches) to identify plausible hypotheses for theobserved changes in sardine spawning dynamics.

MATERIAL AND METHODS

Survey information

Table 1 lists the 15 ichthyoplankton surveys for whichsardine egg and larval (larvae defined here as all post-hatching sardine found in the plankton samples)information was made available for this study. Onlysurveys undertaken within the main spawning periodfor sardine in Portuguese waters (October to March –Re et al., 1990; Zwolinski et al., 2001) were considered.The most reliable are three surveys that directly

targeted sardine in March 1988, March 1997 andJanuary 1999. In these surveys, a dense grid of ich-thyoplankton stations was sampled to estimate sardineegg production as part of the DEPM applied to theAtlanto-Iberian stock of sardine (Fig. 1). More than150 stations were sampled within the continental shelfin each survey, with the total number of stationsexceeding 300 on each survey (Fig. 1). The length ofeach transect was modified adaptively (Cunha et al.,1992) to ensure, as far as possible, that the entire areaof sardine egg cover was sampled. The three DEPMsurveys followed the same sampling protocol (Cunhaet al., 1992; ICES, 2002a), with the only differencebeing the use of 200-lm net meshes, the exclusion ofthe Cadiz region in 1988, and the shift of the samplingmonth from March to January in 1999. The latterchange was adopted in view of recent biologicalinformation that January is closer to the peak ofsardine spawning off Portugal (Zwolinski et al., 2001).

The general aim of most of the remaining surveyswas to monitor ichthyoplankton along the Portuguesecoast (Lopes and Afonso, 1995). Exceptions were theMarch 1995 and February 1998 surveys that wereconducted as part of the triennial surveys for theestimation of mackerel (Scomber scombrus) and horsemackerel (Trachurus trachurus) annual egg production(ICES, 1999). These two surveys had the sparsestsampling grid within the continental shelf (19 and 24stations in 1995 and 1998, respectively) and sardinelarval data were not available. The number of samp-ling stations in the remaining surveys ranged between24 and 94 within the continental shelf and between 38

Table 1. Surveys used for the analysis of sardine egg and larval presence along the Portuguese coast. In surveys operated with adouble sampler, mesh size refers to the sampler used in this study. Surveys after 1995 include the Gulf of Cadiz.

Period Net type Mesh (lm) Stations Survey details

November 1985 Ring 500 72 Re et al. (1990)January 1986 Ring 500 127 Re et al. (1990)March 1986 Ring 500 127 Re et al. (1990)March 1988 CALVET 200 309 Cunha et al. (1992)October 1989 Bongo 500 66 P. Lopes (pers. comm.)November 1990 Bongo 500 86 Afonso and Lopes (1994)October 1991 Bongo 500 84 Lopes and Afonso (1995)October 1992 Bongo 335 39 Cardador (1995)February 1993 Bongo 500 87 Cardador (1995)March 1995 WP2 200 69 A. Farinha (pers. comm.)March 1997 CALVET 150 373 Cunha et al. (1997)February 1998 Bongo 335 71 ICES (1999)January 1999 CALVET 150 417 ICES (2000)November 1999 CALVET 150 124 P. Lopes (pers. comm.)March 2000 CALVET 150 121 P. Lopes (pers. comm.)

50 Y. Stratoudakis et al.

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and 127 overall. There were occasional gaps in spatialcoverage (e.g. in November 1985, October 1989 andOctober 1992) and inadequate delimitation of theoceanic boundaries of sardine egg distribution. In mostsurveys, flowmeter data were not readily available tostandardize observations per unit volume or area.Thus, for the purposes of this study it was not possibleto describe differences in the abundance of eggs/larvaeover time; hence, the analysis focused on presence/absence data and distributional area (where reasonableassumptions can be made to standardize observationsper unit area).

Spatial modelling

The aim of this analysis was to model the expectedprobability of sardine egg and larval presence in the

three DEPM surveys as a function of spatial and en-vironmental explanatory variables. For that, presence/absence data (assumed to have a binomial error dis-tribution) were used as the response variable in GAMsof the form:

EE½y� ¼ g�1 offset þ b0 þX

i

siðxiÞ !

ð1Þ

where the fitted expectation refers to the expectedprobability of sardine egg presence at a station and isdescribed by a vector of explanatory variablesX ¼ {X1,…,Xn} g(Æ) is a function linking the responseto the additive predictor, offset is a scaling parameterto standardize observations per unit of area sampled

Figure 1. Location of sampled stations for the three sardine DEPM surveys off Portugal. Surveys in the late-1990s include theGulf of Cadiz. Crosses refer to stations without sardine plankton (eggs or larvae), e to stations with sardine eggs only, l to stationswith sardine larvae only and open circles to stations with both. Thick lines indicate the borders for the designated areas:northern Portugal (OCN), southwestern Portugal (OCS), southern Portugal (ALG) and the Gulf of Cadiz (CAD).

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Sardine eggs and larvae off Portugal 51

and si(Æ) are univariate smoothing functions (smooth-ing splines in this case).

The offset variable was introduced to account fordifferences in sampling intensity among stations. Whenthe plankton net is towed vertically, the effective area(a) of the sampler is the opening of the mouth of the net(0.05 m2 for CALVET, 0.28 m2 for Bongo and 0.50 m2

for the ring net). However, when towing departs fromthe vertical, the effective area increases, as a largervolume of water is sampled for the given depth (in allcases sampled volume is reduced to equivalent areabecause it is assumed that no eggs or larvae are founddeeper than the sampling depth). To account fordepartures from the standard sampling area, the area ofthe mouth of the net was divided by the cosine of thetowing angle (measured from the vertical) at each sta-tion, and the natural logarithm of the effective area wasused as the offset variable [i.e. offset ¼ ln(a)].

Although the canonical link for binomial models isthe logit, here we used the complementary log–log link(McCullagh and Nelder, 1989) to allow for the offsetvariable to be additive at the predictor scale. Assumingthat the number of sampled eggs or larvae n(x, a) at astation follows a Poisson distribution with mean l(x)a,where l(x) is the expected density given the set ofcovariates x, and a is the sampled area, then the prob-ability of sampling at least one egg or larva p(x, a) is

pðx;aÞ¼P½nðx;aÞ�1�¼1�P½nðx;aÞ¼0�¼1�e�lðxÞa

ð2Þ

Assuming also that the expected density is relatedto the covariates through:

lðxÞ ¼ eb0þP

i

siðxiÞð3Þ

then the additive predictor for the complementarylog–log of the probability of presence is

g½pðx; aÞ� ¼ lnðaÞ þ b0 þX

i

siðxiÞ ð4Þ

thus providing a parameterization that allows theoffset variable to be incorporated in the fitted model asan additive term.

The following explanatory variables were consid-ered as the set of covariates X in the binomial modelsof egg and larval presence (with the abbreviation usedin the rest of the text in italics):latitude (Lat – decimal degrees);longitude (Long – decimal degrees);distance along the coastline (Along – km);

closest distance to the coastline (From – km);bottom depth (Depth – m).

The above set of covariates includes five parti-ally correlated spatial variables. Given that the aim ofmodel fitting is to provide a precise estimate of spawningarea, neither the correlation among variables nor theabsence of a biologically intuitive interpretation forsome of the partial effects prevents their use. Latitudeand longitude are natural candidates for describing thespatial distribution of survey observations. However,the shape of the Portuguese coast causes axes rotationfor these two variables (at Cape of St Vincente), sodistances along and from the coastline were also con-sidered. Distances along the coastline were calculatedwith respect to a fixed point at 42�N (slightly to thenorth of the northern Portuguese border). Bottom depth(natural logarithm to reduce the skewness of observa-tions) was also included because sardine are foundalmost exclusively within the continental shelf. As themain aim of the study is to compare predictions fromdifferent years on a common spatial grid, values for theexplanatory variables need to be known at all points onthe prediction grid. In this case, this precludes the use ofenvironmental covariates such as sea temperature andplankton volume that were only measured at the sam-pled locations and for which remotely sensed informa-tion was not readily available.

Model selection was based on a backward stepwiseprocedure starting from a model that included smoothfunctions (4 degrees of freedom, d.f.) for the fiveexplanatory variables listed above. Model reductionwas based on Akaike’s information criterion, onlyallowing each term to be included as a 4 d.f. smootheror a linear term. Residual plots for models consistingexclusively of main effects revealed adequate fits, sofirst-order interactions with multiplicative interactionterms were not considered worth pursuing for thepurposes of this study.

Estimation of area of egg/larval cover

The selected model from each survey was used topredict the probability of sardine egg or larval presenceon a dense grid of equidistant points along the Por-tuguese coast (36�–41�50¢N, 5�30¢–11�W). For pre-diction purposes, each point was considered as thecentre of a unit rectangle or �pixel� within the studyarea. Ideally, the size of the pixels on the predictiongrid should be very small so that summation over unitareas would approximate integration. However, theminimum dimensions of the pixels depended onthe finest resolution at which reliable depth data forthe Iberian coast could be obtained. Depth data were

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52 Y. Stratoudakis et al.

obtained from Ingrid.ldgo.columbia.edu/sources/worldbath/, where they were available at a 5¢ · 5¢ resolution.This led to the selection of 2246 points 6.88 km aparton a given latitude and 9.26 km apart on a givenlongitude (pixel area 63.71 km2). For pixels near thecoast, pixel area was corrected to avoid extrapolationover land. Within each pixel, the probability of egg/larval presence was considered uniform. Multiplyingthe fitted probability by the pixel area, and summingalong the coast, provided an estimate of the total areaof sardine egg or larval cover during the survey period.Estimates were also obtained separately for eachregion, the finest spatial resolution at which sardinefisheries and acoustic survey data are available. Thecriteria for the delimitation of regions are shown inFig. 1. The northern region (OCN) contributes 57% ofthe total continental shelf within Portuguese waters(close to 9000 km2), while the shelf area in the Gulf ofCadiz (CAD) is similar in size to that of the south-western (OCS) and southern (ALG) regions com-bined (around 6800 km2).

Bootstrap estimation of variance

To estimate the variation of the estimated area ofcover, parametric bootstrap was used (Efron and Tib-shirani, 1993). The fitted probability of egg presence ateach station was assumed to be the mean of a binomialdistribution, and bootstrap resamples were obtained asBernouli realizations from that distribution. The ori-ginally selected model was refitted to each set ofbootstrap �realizations� and area of cover was calcula-ted as described in the previous section. The entireprocess was repeated several times and variance wasestimated as the sample variance of the vector ofbootstrap estimates. Upper and lower limits of the95% confidence intervals were estimated by the valuesat the 2.5 and 97.5 percentile of the ranked estimates.Preliminary tests with 100–1000 bootstrap resamplesindicated that after 400 resamples the difference inestimation was below the level of reporting (decimalthousand km2), thus 400 resamples were consideredadequate for variance estimation.

Standardization and comparison of observationsfrom all surveys

When a series of surveys is preformed following thesame sampling methodology, a useful statistic forcomparisons across surveys is the proportion of stationswith eggs or larvae present (Smith, 1990). However, tocompare observations from surveys that use differentsamplers (ring, Bongo and CALVET nets in this case),we have to account for differences in the probability ofcapture. We assumed that the observed density at each

station (egg or larval count divided by the effectivearea of sampler) provided an estimate of the expecteddensity at that station. We then used eqn 2 to estimatethe theoretical probability of sampling at least one eggor larva in that station by a CALVET net that wastowed vertically (a ¼ 0.05 m2). As the observedtowing angles for surveys with Bongo and ring netswere not available, we assumed a 45� towing anglethroughout, given that these nets are towed obliquely.The mean of the estimated probabilities for stationswithin the continental shelf in each survey was used asa statistic that could be compared across surveys.

The comparison of data obtained with differentplankton samplers can be hindered by differences inthe fraction of the population that is vulnerable to thesampling gear. Different mesh sizes (ranging from150 lm in CALVET to 500 lm in Bongo) can affectthe selectivity properties of the net, while differentinlet areas (ranging from 0.05 m2 for the CALVET to0.50 m2 for the ring) can affect the catchabilitythrough gear avoidance (Somarakis et al., 1998). Sar-dine eggs (typically 1.2–1.6 mm in diameter) andlarvae (typically >2 mm in length) are considerablylarger than the openings of the widest mesh used inthis study, and there is no reference in the literaturethat could indicate selectivity as a problem for thisanalysis. Catchability can clearly be a problem for theanalysis of larval data, but it is more likely to influencethe estimated length distribution and abundance thanpresence.

RESULTS

Estimation of area based on GAMs

Final models selected for the DEPM surveys are shownin Table 2. It was not possible to fit a model to larvalpresence in 1988, as the oceanic boundary of sardinelarval distribution was not adequately defined in thatsurvey. In March 1988, sardine larvae were distributedsignificantly deeper than eggs (Kolmogorov–Smirnovstatistic ¼ 0.326, P < 0.001) and the survey, which wasdesigned to cover the distribution of sardine eggs, didnot extend sufficiently offshore to cover the entire dis-tribution of sardine larvae, particularly in northernPortugal (Fig. 1). Similar problems were observed in the1999 data set from the Gulf of Cadiz, although theremoval of two offshore points with high leverageallowed an adequate definition of oceanic limits in thatcase.

Figures 2 and 3 show the fitted probability of sar-dine egg and larval presence, respectively, in the threeDEPM surveys and Table 3 shows the estimated areas

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Sardine eggs and larvae off Portugal 53

of egg and larval distributional cover. These resultsshow a significant difference in distribution between1988 and the two surveys in the late-1990s: in 1988,sardine eggs and larvae were present throughout thenorthern continental shelf and beyond (with larvae

extending further offshore than eggs), which clearlywas not the case in the late-1990s. In the later years,eggs in the north were constrained to a small inshorepatch (1997) or to scattered patches within thecontinental shelf (1999), whereas larvae were only

Table 2. Summary of selected binomial model for each DEPM survey.

Type Year Model Dev d.f. r2 r2

Eggs 1988 Lat + s(Long) + s(logDepth) + Along + s(From) 218 294 0.74 45.71997 Lat + Long + logDepth + s(Along) + s(From) 215 361 0.58 49.41999 s(Lat) + s(Long) + s(logDepth) + Along + s(From) 325 399 1.04 34.4

Larvae 1988 NA1997 Lat + s(Long) + s(logDepth) + Along + From 315 361 0.87 32.21999 Lat + s(Long) + s(logDepth) + Along + s(From) 275 400 0.69 38.7

Dev ¼ residual deviance; d.f. ¼ residual degrees of freedom; r2 ¼ dispersion parameter; r2 ¼ percent of explained deviance.Variables selected as smooth terms are indicated with s(Æ).Smoothed variables in bold refer to approximate significance of term at 1% and normal at 5%.

Figure 2. Fitted probability of sardine egg presence in the three DEPM surveys off Portugal. Surveys in the late-1990s includethe Gulf of Cadiz. Colour scale indicates level of fitted probability (from blue, probability of 0, to pink, probability of 1).

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54 Y. Stratoudakis et al.

distributed within the continental shelf (1997) or werepractically absent (1999). The situation is different inthe southwestern and southern regions, where egg andlarval cover is similar or marginally higher in the late-1990s than in 1988. This apparent north–south con-

trast is further supported by the large areas of sardineegg and larval cover in the Gulf of Cadiz during 1997and 1999. Estimates for the Gulf of Cadiz wereequivalent to 56 and 52% of the total Portuguese eggand larval cover, respectively, in 1997, and 61 and

Table 3. Estimates of areas (thousand km2) with sardine eggs and larvae by year and region.

Area

Eggs Larvae

1988 1997 1999 1997 1999

North (OCN) 7.7 [7.0–8.4] 1.6 [1.2–2.2] 3.0 [2.4–3.7] 3.3 [2.6–4.3] 0.3 [0.1–0.6]Southwest (OCS) 2.8 [2.2–3.4] 3.3 [2.7–4.0] 3.2 [2.5–3.8] 4.6 [3.9–5.4] 2.3 [1.7–2.3]South (ALG) 1.3 [0.7–1.5] 2.1 [1.5–2.3] 1.2 [0.7–1.5] 1.7 [1.2–2.0] 2.7 [1.8–3.1]Portugal (OCN + OCS + ALG) 11.8 [10.7–12.6] 7.0 [6.0–7.7] 7.4 [6.2–8.3] 9.6 [8.4–10.6] 5.3 [4.1–6.1]Cadiz (CAD) – 3.9 [3.4–4.5] 4.5 [4.0–5.1] 5.0 [4.4–5.9] 5.5 [4.9–6.5]

See Fig. 1 for definition of regions.Values in square brackets indicate 95% confidence interval estimated with parametric bootstrap.

Figure 3. Sardine larval presence in the 1988 DEPM survey and fitted probability of sardine larval presence in the 1997 and1999 surveys. Surveys in the late-1990s include the Gulf of Cadiz. Colour scale indicates level of fitted probability (from blue,probability of 0, to pink, probability of 1).

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Sardine eggs and larvae off Portugal 55

103%, respectively, in 1999. Unfortunately, it is notpossible to evaluate the relative importance of theCadiz area to sardine reproduction during 1988 (in theyear that northern Portugal was by far the mostimportant spawning area of sardine) because the 1988DEPM survey did not sample that region.

Mean probability of presence from standardizedobservations

The mean probability of presence from standardizedobservations during the study period (1985–2000) wasused to identify trends supporting the GAM results. Totest the efficiency of the selected statistic, we com-pared the percentage difference between 1988 andthe late-1990s in the area of egg cover estimated by theGAMs and the mean probability of egg presence in thethree DEPM surveys (Table 4). This comparison showsthat the relative differences in GAM-estimated areaand mean probability from standardized observationshave the same direction and similar magnitudes (apartfrom the southern region in the 1988/1997

comparison), suggesting that we can obtain sensiblecomparisons of sardine egg and larval cover based onthe mean probability of standardized observations.

Preliminary analysis of the mean probability of eggand larval presence over time did not reveal strongnon-linear patterns; hence, weighted linear regressionwas used to test for the significance of the observedtrends (Table 5). Figure 4 shows the mean probabilityof sardine egg and larval presence within the Portu-guese continental shelf based on standardized datafrom 15 ichthyoplankton surveys between 1985 and2000, superimposing the regression lines in caseswhere the slope was significant at the 10% level (seeTable 5). Off Portugal, the mean probability of eggpresence decreases from the mid-1980s to the late-1990s, although the mean rate of change is lessdramatic than that observed in the DEPM surveyscomparison. The decline is exclusively because of amarked reduction in the probability of egg presence offnorthern Portugal, where the mean probability morethan halved from the mid-1980s to the late-1990s(roughly from 0.6 to 0.3). The pattern is different offsouthwestern and southern Portugal, where slightlypositive (but non-significant) trends are observed.Similar regional differences are observed in the meanprobability of larval presence, although the decline inthe north is less marked than for eggs and the increaseoff southern Portugal is highly significant. As a result,there is no trend in the mean probability of larvalpresence off Portugal over time, but this might bemisleading because it does not account for the relat-ively high probability of offshore larval presence in the1980s (comparisons were restricted to the continentalshelf because most surveys in the 1990s did not extendbeyond it).

Comparison with independent sources of information

Ichthyoplankton results were compared with data fromPortuguese acoustic surveys and commercial sardinecatches off the Iberian Peninsula during the studyperiod. The regional delimitation for commercialcatches is slightly different to that used in the surveys,

Region

1988 versus 1997 1988 versus 1999

Area Probability Area Probability

North (OCN) 79 82 61 62Southwest (OCS) )18 )7 )14 )9South (ALG) )62 )26 8 9Portugal (OCN + OCS + ALG) 32 40 29 37

Estimates are provided by region (see Fig. 1) and for Portuguese waters overall.

Table 4. Percent difference between1988 and the late 1990s in area of eggcover estimated by GAMs (Area) and inthe mean probability of egg presenceestimated by standardized presence/absence data (Probability) in the threeDEPM surveys. Estimates are provided byregion (see Fig. 1) and for Portuguesewaters overall.

Table 5. Slopes (time effect), t values and level of signifi-cance (P values) for weighted regression lines fitted to themean probability of egg and larval presence in Portuguesewaters overall and separately by region (see Fig. 1) during thestudy period (1985–2000).

Variable Area Slope t P

Egg probability Portugal –0.008 –1.93 0.076North –0.030 –4.07 0.001Southwest 0.008 1.72 0.110South 0.016 1.77 0.105

Larval probability Portugal 0.023 0.33 0.748North –0.013 1.92 0.081Southwest 0.010 1.28 0.228South 0.025 3.11 0.010

Mean probability in each survey is weighed by the number ofobservations.Equations with significant slopes (P < 0.1, bold) are shownin Fig. 4.

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56 Y. Stratoudakis et al.

although this does not affect the general conclusions.Only acoustic surveys undertaken within the mainspawning season of sardine (October–March) wereused. Distribution refers to the acoustically estimatedarea of sardine presence, whereas abundance refers tonumbers of fish excluding new recruits (age 0), in acrude attempt to represent the spawning component ofthe population.

Table 6 shows the slope (time effect) and the levelof significance for linear regression models fitted toeach variable and area, respectively. There is a signi-ficant reduction in the area of distribution of sardineoff Portugal through the study period, which is ex-clusively because of a highly significant reduction offnorthern Portugal. Although the regressions fitted toacoustically estimated sardine abundance are non-significant, there is a large difference in the magnitudeof negative slope for northern Portugal and the other

two Portuguese regions. Finally, there is a very clearnegative trend in the Iberian sardine catches, oncemore with marked regional differences in the level ofsignificance and the magnitude of the negative slope.The rate of decline is highest off Galicia and northernPortugal, and lowest off southwestern and southernPortugal (the latter showing no significant change insardine catches over time).

Overall, the Portuguese acoustic and Iberian catchdata seem to support the results on sardine egg andlarval distribution off Portugal during the period 1985–2000, in showing that sardine dynamics in thenorthwestern Iberian has changed markedly from themid-1980s to the late-1990s. It is also worth notingthat most Portuguese acoustic surveys since March1997 extended to the Gulf of Cadiz, providing addi-tional evidence of a large area of distribution andhigh sardine abundance in that region. Both the

Figure 4. Mean probability of sardine egg (e) and larval (l) presence within the continental shelf of Portugal (a), northernPortugal (b), southwestern Portugal (c) and southern Portugal (d) in ichthyoplankton surveys during the period November 1985to March 2000. Plotted lines (solid for eggs, broken for larvae) correspond to regression lines for slopes significant at the 10%level (in Table 5). Points are plotted only when more than 10 observations were available for the estimation of the mean.

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ichthyoplankton and acoustic surveys in the late-1990s indicated that estimates for the Gulf of Cadizoften exceeded 50% of the total area occupied by fish,eggs and larvae off Portugal. Although in terms ofacoustically estimated sardine abundance the contri-bution by the Gulf of Cadiz is slightly lower, it is stillfar higher than its contribution to commercial catches(generally <10% of the total Portuguese catches),suggesting that the fishing pressure in that region isconsiderably lower than in the rest of the stock area.

DISCUSSION

This study used data from 15 ichthyoplankton surveysto describe the distribution of sardine eggs and larvaeoff Portugal during the period 1985–2000 using simplepresence/absence information. Binomial models fittedto the data from the three surveys that covered theentire distribution of sardine eggs (DEPM surveys)permitted estimation of the area of sardine egg andlarval cover with 95% confidence intervals and indi-cated statistically significant changes from 1988 to thelate-1990s. Global and regional changes depicted bythe GAM results were corroborated by the comparisonof standardized information from the 15 surveys thattook place within the sardine-spawning seasonbetween 1985 and 2000. The standardization of pres-ence/absence data minimized the problems ofcomparability among surveys that used differentsamplers and designs, conditioned on the assumptionof a Poisson distribution of egg density. Further, theconsideration of surveys from the early, mid and latespawning season during the mid-1980s and late-1990s

provided some evidence that the observed patternsreflect inter-annual trends rather than changes in theseasonality of sardine spawning. In principle, similarcomparisons could be performed on sardine daily eggproduction and, in support of this, background work iscurrently in progress (i.e. staging historical sardine eggsamples, estimation of sampled water volume and areafor each station, etc.).

The main findings of the present analysis are thegeneral decline in the area of sardine eggs off Portugalover the study period and the contrast between nor-thern Portugal and the regions further south. Theichthyoplankton results showed that the observedmoderate decline in the estimated area of cover and inthe mean probability of egg presence off Portugal overtime are exclusively because of a large reduction ofdistribution off northern Portugal that is compensatedfor partly by a marginal increase in southwestern andsouthern areas off Portugal. Acoustic data on sardinedistribution and commercial catch data support theabove findings, all demonstrating a reduction in thecontribution of the area off northern Portugal fromthe mid-1980s to the late-1990s. It is worth stressingthat over the same period, large changes in thespawning distribution, acoustically estimated area offish distribution, abundance and commercial landingsof sardine in northern Spain were observed (ICES,2000); the distribution area of sardine eggs and adultfish and fish abundance off the northern Spanish coasthave been reduced considerably between the late-1980s and late-1990s, while Spanish sardine landingshave reached a historical low in recent years (Spanishsardine catches in 2000 reached the lowest level to

Variable Area Slope t P

Area Portugal )0.196 )2.25 0.042North )0.173 )3.36 0.005Southwest )0.008 )2.49 0.8080South )0.017 )0.87 0.450

Abundance Portugal )0.721 )1.37 0.194North )0.130 )1.28 0.221Southwest )0.029 )0.57 0.578South )0.011 )0.54 0.597

Commercial catch Iberia )159.1 )7.68 < 0.001Northern Spain )97.4 )7.25 < 0.001

Cantabria )39.4 )5.46 < 0.001Galicia )57.9 )4.39 < 0.001

Portugal )63.9 )5.93 < 0.001North )44.0 )7.18 < 0.001Southwest )11.4 )2.76 0.016South )8.6 )1.87 0.084

Table 6. Slopes (time effect), t valuesand level of significance (P values) forregression lines fitted to acousticallyestimated distribution and abundance ofsardine in Portuguese waters overall andby regions (see Fig. 1), and commercialcatches of sardine in Iberian waters dur-ing the study period (1985–2000).

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58 Y. Stratoudakis et al.

date), forcing considerable restrictions to the localpurse-seine fisheries (ICES, 2002b).

It is possible that the observed reduction inspawning area off the northwestern Iberian coast(northern Portugal and western Galicia) during the1990s is indirectly reflecting changes towards recruit-ment-unfavourable environmental conditions.Northwestern Iberia traditionally formed the mainrecruitment area for the Atlanto-Iberian stock ofsardine (Alvarez and Alemany, 1997) and, accordingto the annual assessment of the stock, recruitment hasbeen weak for most of the 1990s (ICES, 2000).Assuming that most spawning activity in northwest-ern Iberia is by young fish (most sardine are mature atthe end of the first year of life), it is plausible that theweak recruitments of the 1990s have contributed tothe observed reduction of egg cover in that area, ra-ther than being a consequence of it. This hypothesis issupported by recent data that show a very extensivearea of egg cover in northern Portugal during the2001–2002 spawning season, following an unprece-dented strong recruitment in that area during the lastquarter of 2000 (ICES, 2002b).

Santos et al. (2001) suggested that the decreasingtrend in sardine recruitment during the 1990s wasassociated with an increased frequency of winterupwelling events off the western coast of Portugal,reversing previous beliefs that coastal upwelling was acharacteristic of the western Iberian coast duringsummer months only (Wooster et al., 1976). Althoughthe formation of a coastal poleward current (Frouin etal., 1990) off the western Iberian coast during wintermonths may complicate water circulation and theinterpretation of upwelling indices based on coastaltemperature deficits, Borges et al. (2003) support thefindings of Santos et al. (2001) by demonstrating asignificant negative correlation between a sardinerecruitment index and intensity of upwelling-favour-able northerly winds in winter months. Santos et al.(2001) proposed that the mechanism underlying theserelationships is offshore transport. Supporting thisproposition has been the result from a recent processstudy using in situ data (SURVIVAL project), whichidentified upwelling off northern Portugal duringFebruary 2000, when sardine eggs and larvae weremainly found on the edge of the continental shelf andbeyond (Santos, 2000).

AKCNOWLEDGEMENTS

We thank the personnel at IPIMAR who contributedto the collection of ichthyoplankton data in this study(in particular Placida Lopes, Alexandra Barbosa,

Anabela Farinha, Emilia Cunha, Isabel Meneses andHortence Afonso). We also thank colleagues VitorMarques and Alexandre Morais for providing acousticdata, Manuela Azevedo for making available the dis-aggregated catch at age data, Alvaro Peliz and MiguelSantos for useful comments and discussions, andAnthony Richardson for his very constructive criti-cism of the original manuscript. This work was sup-ported by the post-doctorate scholarship PRAXISXXI, BPD/16336/98 and by the Programme PELAGI-COS (PLE/13/00) funded by the Portuguese Ministryof Science.

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