© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Daily egg production of anchovy in European waters
a University of Patras, Department of Biology, Laboratory of Zoology 26500, Patra, Greece
b Departament de Recursos Marins Renovables, Institut de Ciències del Mar (CMIMA–CSIC) Passeig Marítim de la Barceloneta, 37–49, 08003 Barcelona, Spain
c Instituto Espanol de Oceanografia (IEO) Centro Oceanografico de Malaga, Puerto Pesquero s/n, 29640, Fuengirola, Malaga, Spain
d AZTIMAR–AZTI Marine Research Unit-Herrera kaia Portualdea z/g, 20110 Pasaia, Gipuzkoa, Basque Country, Spain
*Correspondence to S. Somarakis: tel: +30 2610 997521; fax: +30 2610 996100. e-mail: somarak{at}upatras.gr.
Since the late 1980s, the Daily Egg Production Method (DEPM) has been applied to several anchovy stocks in European waters. DEPM surveys in the Bay of Biscay were well standardized and focused on providing fisheries-independent information for stock assessment purposes. Those targeting Mediterranean stocks were largely experimental and often opportunistic, with the main aim of developing and testing the method, rather than providing estimates of spawning stock biomass (SSB) for stock assessment. Consequently, the DEPM has been applied once, twice, or a maximum of three times in certain Mediterranean areas with no among-area standardization. Different techniques for several aspects of the method have been used in the Mediterranean, and the parameters estimated vary greatly among stocks and year of application. Evidence is provided that variability in biological production among sub-basins and/or years, a characteristic of Mediterranean Sea, may directly affect anchovy egg production. The daily specific fecundity of anchovy stocks can vary greatly among years, areas, or seasons in response to changing environmental and trophic regimes. When the correlation between regression-derived estimates of daily egg production and associated estimates of daily specific fecundity for anchovy in the Mediterranean, the Bay of Biscay, and upwelling areas are compared, a significant isometric relationship emerges for the Mediterranean and the Bay of Biscay, implying density-dependent use of spawning habitat. In upwelling areas, estimates of daily egg production are relatively high for a narrow range of generally low daily specific fecundities. There is a strong linear relationship between anchovy SSB and spawning area in European waters that does not differ significantly between the Bay of Biscay and the Mediterranean Sea.
Keywords: anchovy, Bay of Biscay, Daily Egg Production Method, Engraulis encrasicolus, Mediterranean Sea
Received 9 March 2004; accepted 14 July 2004.
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Introduction |
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The spawning stock biomass (SSB) of an exploited species is an important variable in fisheries management. Egg production surveys provide a method of estimating it that is independent of any commercial catch data, and have become important because of heightened demands for fishery-independent information (Hunter and Lo, 1993).
The Daily Egg Production Method (DEPM) is an ichthyoplankton-based method for estimating the SSB of pelagic schooling fish such as anchovy and sardine. It is applicable to batch-spawning species with indeterminate annual fecundity, and was developed in the late 1970s at the Coastal Division of the Southwest Fisheries Science Center in La Jolla, California (Parker, 1980; Lasker, 1985). Since then, it has been applied to a variety of small pelagic stocks in different ecosystems around the world, as well as to Atlantic mackerel (Alheit, 1993; Hunter and Lo, 1993, 1997; Priede and Watson, 1993). Both number and type of application continue to increase. Besides biomass estimation, application of the DEPM provides regional time-series on important biological variables of fish stocks, which can lead to new insights into their reproductive biology, particularly when such variables can be compared among species and stocks, or habitats and seasons (Alheit, 1993).
The DEPM is based on the model
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Since the late 1980s, the DEPM has been applied to several European anchovy, Engraulis encrasicolus, stocks in the Mediterranean Sea and the Bay of Biscay (Table 1, Figure 1). Here we present a synthesis of these applications, contrast different methodologies, and highlight peculiarities of European anchovy habitats in respect of application of the DEPM. Finally, we examine the extent to which different DEPM parameters vary among stocks and/or years.
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Methods |
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DEPM application characteristics, and the relevant biology of European anchovy
Different DEPM estimates of SSB for European anchovy by area, month, and year are summarized in Table 1. Most of these estimates can be considered as total biomass, because the species matures on completion of its first year of life. In the Mediterranean, the length at first maturity is about 11 cm (Demir, 1965; Sinovcic, 1978; Giraldez and Abad, 1995; Basilone et al., 2003; Palomera et al., 2003). In the Bay of Biscay, all one-year-old anchovy >10 cm are sexually mature (Cort et al., 1976; Lucio and Uriarte, 1990). Therefore, during the peak spawning season, most recruits are mature (Motos, 1996; Somarakis, 1999).
Most DEPM surveys have been conducted in May and June (Table 1). The reproductive period of anchovy in the Mediterranean lasts from spring to autumn, usually from May to October, and rarely from March to December (Demir, 1965; Chavance, 1980; Palomera 1992; Somarakis, 1993; Regner, 1985, 1996; Giraldez and Abad, 1995; Garcia and Palomera 1996). Results of monthly egg surveys (Palomera, 1992; Somarakis, 1993) indicate that reproduction peaks during June in both the NW and NE Mediterranean. However, in most of the Mediterranean, the gonosomatic index (GSI) is high from May to July (Figure 2). Bay of Biscay anchovy appear to spawn earlier and for a shorter period, peaking in May and June (Motos, 1996), months also associated with spawning in GSI records (Figure 2: Sanz and Uriarte, 1989; Lucio and Uriarte, 1990).
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The timing of seasonal peak spawning and the location of the spawning grounds are generally associated with months/areas of high productivity, and specifically with conditions favourable for adult feeding (e.g. zooplankton maxima, riverine outflows, upwelling areas, fronts; Regner, 1985; Valencia et al., 1988; Palomera, 1992; Somarakis, 1993, 1999; Garcia and Palomera, 1996; Motos et al., 1996; Somarakis et al., 2000). In the Mediterranean, areas of increased productivity and conditions favourable for larval survival (Agostini and Bakun, 2002) are generally few, spatially restricted, and limited to northern areas. The main concentrations of anchovy in the Mediterranean are therefore located in the Catalan Sea/Gulf of Lions, in the Adriatic, and in the northern Aegean Sea, with most other areas inhabited by small and highly variable stocks (e.g. the Sicilian channel, Garcia-Lafuente et al., 2001; Quintanilla and Garcia, 2002). In the Bay of Biscay, spawning is triggered by the onset of thermocline formation caused by the relaxation of wind, and the warming of surface waters during spring. There, anchovy spawning appears to be associated with river plumes, shelf break fronts, and oceanic eddies (Koutsikopoulos and Le Cann, 1996; Motos et al., 1996).
Principal characteristics of the ichthyoplankton surveys in European anchovy DEPM applications are summarized in Table 2, and those of the corresponding adult surveys (which have generally been conducted concurrently with the respective egg surveys) in Table 3. DEPM applications in the Bay of Biscay have been carried out routinely for assessment purposes since 1987. In the Mediterranean, they were largely experimental, based on opportunistic funding, with the main aim of developing and testing the method, rather than to provide SSB estimates for stock assessment. Consequently, the method has been applied only once or twice in each Mediterranean area, though three successive attempts to apply it were made for Sicilian channel anchovy (Table 1). Although a standard protocol for implementation has been suggested for the DEPM (Lasker, 1985), a characteristic of its application to European anchovy has been that several aspects of the method have been modified in an effort to adapt to the specifics of target stocks and, on some occasions, in response to budget limitations.
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All applications have been based on the modification of Parker's model (Parker, 1980) by Stauffer and Picquelle (Stauffer and Picquelle, 1980), and the parameter-estimation procedures described in Picquelle and Stauffer (1985). The latter included: (i) the fitting of an exponential mortality model to the abundance of eggs on their age, to derive the daily egg production; (ii) stratification of survey area into negative and positive strata, when applicable; (iii) plankton station weighting proportional to the representative area; (iv) use of the ratio estimator for adult parameters and their variances (Equation 5 in Picquelle and Stauffer (1985)); (v) the fit of a linear model regressing batch fecundity on ovary-free weight; (vi) bias correction for spawning fractions when oversampling active spawning females.
Ideally, a DEPM application should include the entire spawning area, and be conducted during peak spawning (to increase precision in estimating the spawning fraction). Also, because it is the average fish that is of interest, sampling density should parallel fish density (Hewitt, 1985; Smith and Hewitt, 1985a). The CAT90, ADR94, and applications in the NE Aegean Sea (NAEe93, NAEe95) did not cover the entire spawning area of their respective stocks. Instead, they covered a particular (and distinct) spawning hotspot. Hence, the resultant SSB values (Table 1) are underestimates of the total SSB of the respective stocks. Moreover, adult sampling in the CAT90, the northern Aegean Sea (NAEe93, NAEw93, NAEe95, NAEw95), and the first two applications in the Bay of Biscay (BB87, BB88) was opportunistic, based on commercial rather than research samples. They were therefore representative of fishery catches, rather than the age structure and spatial distribution of the stocks. Adult fish were taken by observers at sea and preserved immediately after capture to fix the gonads.
The vertical distribution of anchovy eggs and larvae is generally restricted to the upper water column, concentrations peaking in the upper 20 m (Palomera, 1991; Motos et al., 1997; Conway et al., 1998; Olivar et al., 2001; Coombs et al., in press). However, subsurface peaks are often distinct, depending on local physical conditions (Motos and Coombs, 2000; Boyra et al., 2003). Plankton sampling in all DEPM applications included at least the 0–100 m layer. With the exception of the northern Aegean Sea (NAEe93, NAEw93, NAEe95, NAEw95), where bongo nets were used, all ichthyoplankton surveys utilized vertical tows of CalVET, PairoVET, or WP2 nets (Table 2).
Regression estimates of daily egg production
Estimating daily egg production (Table 4) generally involved the fitting of an exponential mortality model to a data set of egg abundance-at-age (Picquelle and Stauffer, 1985). Many applications used an automated procedure for the assignment of age to eggs (the STAGEAGE program of Lo (1985), as modified by Motos (1994)). The age was calculated on the basis of a temperature-dependent model of anchovy development rate (Motos, 1994), station surface temperature, peak spawning time, and time of tow.
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In areas of high surface temperature, such as the eastern Mediterranean, the duration of the egg stage is generally short, and eggs can also be easily grouped into "spawning nights" manually; the distribution of eggs over the different developmental stages form distinct groups (one or two), with unrepresented stages separating each group (Somarakis et al., 2002).
According to Motos (1994), the rate of development of E. encrasicolus eggs is slower than that of E. mordax (Lo, 1985), but similar to that of E. encrasicolus off southern Africa, a species formerly known as E. capensis (Valdés et al., 1987). In both the Atlantic and the Mediterranean, fish exhibit a diel spawning cycle (Regner, 1985; Somarakis, 1993, 1999; Motos, 1996, and references therein). Data from histological analysis of ovaries, as well as the presence of newly fertilized eggs in the plankton in relation to time of day, indicate that, during anchovy DEPM surveys, most spawning is between 22:00 and 02:00, peaking around midnight (Garcia et al., 1994; Motos, 1996; Somarakis, 1999; Quintanilla et al., 2000). Hence, in all applications here, peak spawning time was assumed to be midnight (00:00; Table 4).
When fitting an exponential mortality model for small, patchily distributed stocks and/or when egg incubation temperatures are high, there is usually a scarcity of positive egg data, resulting in the estimate of egg mortality being not significantly different from zero (Hunter and Lo, 1997; Somarakis et al., 2002). Problems with the fit of the mortality model become more serious when the number of plankton stations is inadequate, as was the case in the northern Aegean Sea (NAEe93, NAEw93, NAEe95, NAEw95). In the latter applications, the egg abundance-at-age data were considered insufficient for estimating egg mortality and daily egg production (Tsimenides et al., 1995; Somarakis and Tsimenides, 1997; Somarakis et al., 1997). Therefore, those estimates were revised (Somarakis, 1999, in press) using a method similar to the CAE99 and ION99 applications in the central Aegean and Ionian Seas (Somarakis et al., 2002). To increase the number of age categories for constructing mortality curves, Somarakis et al. (2002) assumed that the mortality rate was the same for eggs and yolk-sac larvae, and included both in single embryonic mortality curves. Regression parameter estimates are similar for the egg data set and the egg plus yolk-sac larva data set. However, in the latter case, the precision of the regression estimates is substantially higher (Somarakis et al., 2002).
Temperature-dependent duration curves exist for two stages of anchovy yolk-sac larvae (Somarakis et al., 2002), for YSI (larvae with unpigmented eyes), and for YSII (larvae with brown pigment traces or brownish eyes), calculated by Regner (1985) from laboratory experiments in the Adriatic Sea. These two stages of yolk-sac larvae are generally easily identified in plankton collections, because yolk-sac larvae rarely lose their eyes during sampling and preservation.
Spawning frequency estimation
In all DEPM applications, spawning frequency (S), the fraction of mature females spawning each night, was estimated histologically by the postovulatory follicle (POF) method (Hunter and Macewicz, 1985). Some studies used females with Day 1 POFs for estimating S (Table 3). Others used two daily classes of POF, either Day 1 and Day 2 (CAT94, SIC98, SIC99, SIC00, BB94–98), or Day 0 and Day 1 (NAEe93, NAEw93, NAEe95, NAEw95). Actively spawning anchovy (Day 0 females) are oversampled prior to or during the hours of spawning (Picquelle and Stauffer, 1985; Santiago and Sanz, 1989; Uriarte et al., 1999). Hence, the fraction of Day 0 females is not generally used for spawning frequency estimates. Its use in northern Aegean Sea applications was justified by the fact that the fractions of Day 0 females did not differ significantly from Day 1 females when samples were collected outside the daily spawning period (after 04:00; Somarakis, in press).
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Results |
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The estimated DEPM parameters for anchovy in European waters are summarized in Tables 4 and 5. They are characterized by high inter-regional and interannual differences, especially within the Mediterranean Sea. Estimates of daily egg production in the spawning area range from 8.88 to 110.40 eggs m–1 (Table 4), the spawning frequency from 0.06 to 0.36, the relative fecundity (the fraction F/W) from 226 to 646 eggs g–1 of mature female, and the daily specific fecundity (DSF = FSR/W) from 18 to 109 eggs g–1 of spawning stock (Table 5).
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In comparing the correlation between daily egg production in the spawning area and the corresponding daily specific fecundity in the Mediterranean and the Bay of Biscay, and for other anchovy species in upwelling areas (Table 6), an isometric relationship emerges for European anchovy (Figure 3). The relationships for the Mediterranean (log[P0] = 0.33 + 0.90 log[DSF]; r2 = 0.60, p = 0.001) and the Bay of Biscay (log[P0] = –0.77 + 1.20 log[DSF]; r2 = 0.30, p = 0.065) do not differ statistically (ANCOVA; slope F = 0.17, p = 0.680; intercepts F = 0.61, p = 0.442), and the pooled model has a slope that equals 1 (t-test, p > 0.05), explaining about 61% of the variation in the data. For the Bay of Biscay alone, the relationship is only marginally significant (p = 0.065), a finding that can be attributed to the low variability of the daily specific fecundity parameter in that area during peak spawning (Figure 3, Table 5). In upwelling areas, daily egg production is relatively higher for a narrow range of small DSF values.
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There is a strong relationship between the SSB and the spawning area (SA; positive strata) for anchovy (Figure 4) in both the Bay of Biscay and the Mediterranean Sea. The separate linear relationships for these two regions do not differ significantly (ANCOVA; slope F = 0.42, p = 0.523; intercepts F = 1.32, p = 0.263), and the intercept in both cases is not significantly different from zero (p > 0.05). The corresponding separate zero-forced models for the Mediterranean and the Atlantic are:
- Mediterranean; SSB = 1.18SA; r2 = 0.79, p < 0.001
- Bay of Biscay; SSB = 1.28SA; r2 = 0.83, p < 0.001
- Bay of Biscay; SSB = 1.28SA; r2 = 0.83, p < 0.001
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These results do not change if Mediterranean applications that did not cover the entire spawning grounds of the respective stocks (CAT90, ADR94, NAEe93, NAEe95) are excluded from the analysis.
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Discussion |
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TopIntroductionMethodsResultsDiscussionReferences |
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Methodology
DEPM surveys in the Bay of Biscay were well standardized and focused on providing information for stock assessment purposes, whereas those for Mediterranean stocks were largely experimental and often opportunistic. Different techniques, in several aspects of the method, have been used in the Mediterranean, and the parameters estimated vary greatly among stocks and year of application.
Adult sampling in certain Mediterranean applications, as well as in the first two applications in the Bay of Biscay, was based exclusively on commercial rather than research samples and, therefore, was representative of the commercial fishery catch rather than of the age structure and spatial distribution of the stocks. Indeed, purse-seine samples in the northern Aegean Sea were biased with regard to mean female weight, because fishers actively selected schools of bigger fish (in deeper water) because of the higher price bigger fish attract (Tsimenides et al., 1998). However, as pointed out by Motos and Uriarte (1991), the DEPM is quite insensitive to inadequate adult sampling, as long as there are no substantial differences in the W/F ratio, spawning frequency, and sex ratio among different age groups. For Bay of Biscay anchovy at least, no such differences exist during peak spawning (Motos, 1996), validating the adult sample protocol generally used in the area (and occasionally in certain Mediterranean applications), i.e. a composite of research vessel pelagic trawl samples plus opportunistic commercial purse-seine samples. In the northern Aegean, the linear regressions of batch fecundity on ovary-free weight had intercepts not significantly different from zero, indicating that relative fecundity (eggs g–1) did not change with fish size or age during the respective DEPM surveys (Maraveya et al., 2001). In contrast, adult parameters are age-dependent in northern anchovy, Engraulis mordax (Parrish et al., 1986). The dependence of relative batch fecundity and spawning fraction on size or age for different European anchovy stocks and different environments deserves further investigation, because it can have great impact on both parameter accuracy and population reproductive potential.
Early surveys in the northern Aegean were based on oblique rather than vertical plankton tows. Oblique bongo tows have been criticized in terms of their suitability for DEPM assessments (Somarakis and Tsimenides, 1997). However, in a recent comparison of replicate WP2 vertical (mouth area 0.255 m2, mesh size 0.200 mm) and bongo oblique (mouth diameter 0.6 m, mesh size 0.250 mm) tows, no significant between-gear differences were found in the mean abundance of anchovy eggs. Variance for the vertical tows was 7 times higher than for the oblique tows (Tzanatos et al., 2001). In Californian waters, Picquelle and Hewitt (1983) found that the CalVET net and the CalCOFI bongo net yielded consistent and compatible estimates of ichthyoplankton production.
The use of small-volume vertical plankton tows increases substantially the number of samples that can be collected for a given cost, reducing substantially the standard error of the regression estimates of daily egg production. In the Bay of Biscay, the vertical sampler was changed from a CalVET to a PairoVET net (two nets of twin CalVETs per tow; Smith et al., 1985) in 1994, because increasing the effective sampling area from 0.05 to 0.1 m2 reduced the sampling errors for 3-day-old anchovy eggs by about 33% (Uriarte and Motos, 1998).
In the eastern Mediterranean applications, both eggs and yolk-sac larvae were included in the mortality curves, to derive the daily egg production. It was assumed that the mortality rate was the same for eggs and yolk-sac larvae, as discussed in Hunter and Lo (1997) and Somarakis et al. (2002). The addition of yolk-sac larvae "anchors" the end of the mortality curve and substantially improves the precision of the estimate of daily egg production (Hunter and Lo, 1997). This allows efficient estimation of daily egg production and the rates of instantaneous mortality when egg stages are undersampled, i.e. if it is not possible to take adequate samples for budgetary reasons, or when the distribution of adults and their spawn are patchily distributed. The latter is the usual situation at low biomass (Lo et al., 1996).
In areas of high surface temperature (>20°C), the duration of the egg stage is generally very short (<2 days), and the eggs from previous nights' spawning at a station are clustered in one or two daily cohorts (Somarakis et al., 2002). The existence of only one or two cohorts of eggs in the samples greatly "reduces" available data points in the egg data set, which, in addition, consists mainly of patchily distributed <1-day-old eggs (Smith and Hewitt, 1985b; Hunter and Lo, 1997). The use of yolk-sac stages is therefore a useful option to increase the precision of estimates of daily egg production when sea temperatures are high.
All DEPM applications in European waters used the postovulatory follicle method to estimate spawning frequency. In general, the precision of the estimate of spawning frequency can be improved if more than one daily class of spawners can be identified in the samples, and subsequently combined to produce a composite estimate of spawning fraction (Uriarte et al., 1999; Quintanilla et al., 2000, Quintanilla and Garcia, 2001a, b, 2002; Ganias et al., 2003). A requisite of such combination is that different spawners' classes have the same statistical distributions (Ganias et al., 2003; Somarakis, in press).
The rate of POF degeneration has been described for Bay of Biscay anchovy, and has been calibrated experimentally in bait tanks (Motos, 1996). However, no such information is available for anchovy in the Mediterranean. The morphology of POFs should therefore be studied in detail in relation to time of collection, daily spawning period, and existing descriptions of POFs for other anchovy stocks or species. Interannual or regional differences in temperature regimes and their effect on the rate of POF degeneration should be addressed by analysing vertical profiles of temperature taken at the same time and in the same area (Ganias et al., 2003).
DEPM parameters
The most prominent characteristic of the estimated DEPM parameters for anchovy in European waters is their high inter-regional and interannual variability, especially in the Mediterranean Sea (Tables 4, 5, Figure 3). This variability can be attributed to the diversity of methodology applied, and standardization problems (Quintanilla and Garcia, 2001c), but most of it probably reflects natural variability in reproductive parameters. The latter can occasionally change within the same spawning season, as shown for the second of the two years of double surveys (1989–1990; Tables 4, 5) conducted experimentally in the Bay of Biscay (Motos and Uriarte, 1991).
Differences in biological production among sub-basins or among seasons/years, which are prominent at least in the Mediterranean (Stergiou et al., 1997; Agostini and Bakun, 2002), may directly influence anchovy egg production. Indeed, the trophic environment of reproducing stocks could directly impact anchovy reproductive effort, as shown by applications in the northern Aegean Sea. In comparing the DEPM parameters between 1993 and 1995 in relation to various environmental parameters and somatic condition, Somarakis (1999, in press) showed that adult food availability (mesozooplankton) was higher in 1993, when waters were significantly cooler and fresher, and, concurrently, female anchovy were in better condition, producing numerous eggs at a higher frequency (short interspawning interval; Figure 5). Those observations were consistent with a ration-related reproductive tactic of European anchovy (Somarakis, 1999, in press; Somarakis et al., 2000). Based on those findings and observations on interannual variations in the abundance of larvae of anchovy and mesopelagic species in the plankton (Somarakis, 1999; Somarakis et al., 2000; Somarakis and Maraveya 2001), short-lived planktivorous pelagic fish in the Mediterranean are classified as "income breeders" (sensu Stearns, 1992), spawning soon after energy for egg production becomes available. Income breeders might be characterized by substantial, ration-related variations in batch fecundity and spawning frequency, as observed for anchovy in the northern Aegean (Somarakis et al., 2000; Somarakis, in press).
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The energy allocated to multiple spawning in many small pelagic fish is derived primarily from feeding, rather than from energy reserves (Milton et al., 1994; Wang and Houde, 1994). In other cases, spawning is related both to dietary intake and the nutritional status of the fish (Milton et al., 1994). In Californian anchovy, Engraulis mordax, up to 70% of the energy stored in the previous feeding season is used for reproduction (Hunter and Leong, 1981). In eutrophic areas anchovy might find enough food to store energy for future use, in contrast to less productive or oligotrophic areas, where prey fields might not allow for significant surplus energy storage during winter, and fish can only allocate energy to reproduction during the period of maximum prey production.
Some marked inter-regional or interannual differences in anchovy reproductive parameters were observed in the more southern Mediterranean areas, such as the central Aegean and Ionian Seas (CAE99 and ION99), or the Sicilian channel (SIC98, SIC99, SIC00). These areas are inhabited by small stocks of anchovy with patchy distributions. They are largely oligotrophic, receiving the influence of only small rivers or wind-driven, but highly variable, upwelling. A remarkable difference in batch fecundity was found between the central Aegean and Ionian stocks (CAE99 and ION99, Table 5) in 1999. However, the interplay of fecundity and spawning frequency seemed eventually to condition reproductive effort, because the estimates of spawning frequency showed an opposing trend (Table 5), and resulting values for daily specific fecundity were almost equal for the two seas (about 18 eggs g–1 of reproducing stock).
In the Sicilian channel applications, the longest time-series in the Mediterranean (three years), the estimated SSB was relatively high in 1998 (13 224 t; Table 1), but it decreased to about 3000 t in 1999 and 2000. This decline was coupled with a contraction of the spawning area and a concomitant decline in daily egg production (Tables 2, 4). It seemed to be associated with a high interannual and short-term variability in the wind and upwelling regimes, and corresponding changes in the thermal and trophic environment in the area (Quintanilla and Garcia, 2002). In response to the decrease in daily egg production and SSB, the spawning stock almost doubled its daily specific fecundity (both relative fecundity and spawning frequency increased; Table 5) from 1998 to 2000. However, in all three years of the study, a high proportion of the adult females were in an atretic or inactive state (Quintanilla and Garcia, 2002), implying that only a fraction of the potential spawning stock produced eggs in this unstable, highly variable habitat.
Relationship between daily egg production and daily specific fecundity
An overall isometric relationship between daily egg production (P0) and daily specific fecundity (DSF) in European waters (Figure 3) implies density-dependent use of the spawning habitat by spawning anchovy. Indeed, there is a strong linear relationship between the size of the spawning stock (SSB) and the size of the spawning area (SA; Figure 4). In upwelling areas, the daily egg production is generally much higher for a narrow range of small DSF values (Figure 3). Presumably, the trophic condition and the carrying capacity of upwelling areas is much greater than the more oligotrophic European seas, supporting much higher fish biomass per unit sea surface area.
The relatively low and less variable DSF values in upwelling areas can be attributed to the lower variability in habitat conditions and the prolonged duration of pelagic fish spawning seasons in those areas (Alheit et al., 1984; Whitehead et al., 1988). In order to explain the high consistency of spawning fraction estimates for pelagic species in upwelling areas, Hunter and Lo (1997) introduced the "biorhythm hypothesis", which suggests that the frequency of spawning is relatively constant for females actively spawning, as soon as the habitat conditions (e.g. prey fields, temperature) remain about the same. In temperate European waters, the spawning season is shorter, coupled to seasonal temperatures and the short production cycle. Variability in habitat conditions seems to have a direct influence on anchovy reproductive parameters (see above).
The empirical relationships between P0 and DSF as well as SSB and SA found in the present study suggest that European anchovy tend to maintain an upper level of spawning stock density in European waters, one that is much lower than for upwelling areas. In the Bay of Biscay (Motos et al., 1996; Uriarte et al., 1996, 1999), in years of low stock abundance, eggs occur spatially restricted to the main spawning centres (i.e. productive waters of the southeastern coastal areas under the influence of river outflows, such as Garonne and Adour, and over shelf-edge fronts). In years of greater abundance, eggs occur over most of the Bay. It seems likely that when biomass per unit area of the stocks in the main spawning grounds exceeds a certain threshold (most likely related to the trophic capacity of European spawning grounds), fish tend to spread over a larger area, to avoid intra-specific interactions such as trophic competition and/or egg cannibalism. Indeed, egg cannibalism, which accounts for 20–30% of total egg mortality in upwelling areas (Alheit, 1993, and references therein), has never been observed in European anchovy (Tudela and Palomera, 1997; Plounevez and Champalbert, 1999, 2000).
According to the basin hypothesis of MacCall (1990), clupeoid populations represent optimal areas or basins for reproduction. In periods of low abundance, the distribution of stocks shrinks, and spawning is practically restricted to the more favourable spawning sites. In the Bay of Biscay, the spread of anchovy over a larger area appears to be led by the bigger/older anchovy, which consistently appear in deeper sea areas located far from the coast (Uriarte et al., 1996; Petitgas et al., 2003).
Based on the "ocean triad hypothesis", and the analysis of maritime weather reports and satellite-sensed ocean colour distributions, Agostini and Bakun (2002) suggested that suitable reproductive habitats and successful anchovy populations in the Mediterranean are likely to exist in the northern Aegean Sea, the Adriatic Sea, the Catalan Sea/Gulf of Lions, and the Alboran Sea. With the exception of the latter, which has a very narrow continental shelf, the other three areas support the largest anchovy fisheries. Furthermore, the Aegean, the Adriatic, and the western Mediterranean stocks differ substantially in genetic structure (Magoulas et al., 1996). These suitable anchovy spawning habitats are spatially restricted and separated from each other by deep, extremely oligotrophic basins, which would not be likely to support anchovy feeding and reproduction. For instance, in the Aegean Sea, there is a sharp contrast in productivity between its northern and southern basin, and anchovy schools are practically absent from the latter (Stergiou et al., 1997). Given the contrasting characteristics of adjacent Mediterranean basins, we believe that the expansion of spawning areas at high stock densities would not be beneficial for Mediterranean stocks. Migration of anchovy schools away from the traditional fishing/spawning grounds has seldom been reported by fishers, nor it has ever been proved by scientists. It is therefore probable that the Mediterranean anchovy stocks rarely reach spawning densities capable of triggering a significant expansion of the spawning areas.
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Acknowledgements |
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We thank Peter Witthames of CEFAS, UK, and an anonymous referee for useful comments on the manuscript.
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References |
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TopIntroductionMethodsResultsDiscussionReferences |
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