Growth and feeding patterns of European anchovy (Engraulis encrasicolus) early life stages in the Aegean Sea (NE Mediterranean)

Estuarine, Coastal and Shelf Science 86 (2010) 299–312

Contents lists available at ScienceDirect

Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss

Growth and feeding patterns of European anchovy (Engraulis encrasicolus) early life stages in the Aegean Sea (NE Mediterranean) Ignacio A. Catala´n a, *, Arild Folkvord b, Isabel Palomera c, Gemma Quı´lez-Badı´a c,1, Fotini Kallianoti d, Anastasios Tselepides e, Argyris Kallianotis d a

Institut Mediterrani d’Estudis Avançats (IMEDEA, CSIC/UIB), C/Miquel Marque´s 21, CP 07190, Esporles, Balearic Islands, Spain Department of Biology, University of Bergen, 5020 Bergen, Norway Institut de Cie`ncies del Mar (ICM-CSIC), Passeig Maritim de la Barceloneta, 37-49 CP 08003, Barcelona, Spain d National Agricultural Research Foundation-Fisheries Research Institute (NAGREF-FRI) N. Peramos, 640 07 Kavala, Greece e University of Piraeus, Department of Maritime Studies, Karaoli & Dimitriou 40, Piraeus 185 32, Greece b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 22 July 2009 Accepted 26 November 2009 Available online 4 December 2009

The objective of this work was to describe inter- and intra-annual variations in the environmental characteristics of the North-eastern Aegean Sea and to relate these changes to the egg and larval distributions, growth and feeding of larval anchovy (Engraulis encrasicolus). Four cruises, two in July and two in September in 2003 and 2004 were performed. The distributions of eggs and larvae were associated with i) salinity fronts related to the Black Sea Water and ii) shallow areas of high productivity over the continental shelf, some of them with high riverine influence. The first published description of the anchovy larval diet in the Eastern Mediterranean was conducted in individuals ranging from 2.2 to 17 mm standard length. The number of non-empty guts was relatively high (between 20% and 30%), and the diet was described through 15 main items. The mean size of the prey increased with larval size, and was generally dominated by prey widths smaller than 80 mm (mainly the nauplii and copepodite stages of copepods). Small larvae positively selected copepod nauplii. As larvae grew, they shifted to larger copepod stages. At all sizes, larvae rejected abundant taxa like cladocerans. The average trophic level calculated for anchovy of all size ranges was 2.98  0.16 (SE). Growth rates varied from 0.41 to 0.75 mm d 1, with the highest growth rates generally observed in September. Variability in the Black Sea Water influence and the recorded inter- and intra-annual changes in primary and secondary production, combined with marked changes in temperature over the first 20 m depth, are used to frame the discussion regarding the observed significant differences in growth rates in terms of both length and weight. Ó 2009 Elsevier Ltd. All rights reserved.

Keywords: Engraulis encrasicolus feeding fish larvae growth Mediterranean Aegean Sea

1. Introduction The European anchovy Engraulis encrasicolus is one of the most important pelagic fish species in the Mediterranean in economic terms (Lleonart and Maynou, 2003). Together with the NW Mediterranean and Adriatic stocks, the North Aegean stock is one of the largest exploited anchovy stocks in the Mediterranean (Stergiou et al., 1997) as a result of the conjunction of favourable environmental factors falling into the ‘‘Ocean triad’’ hypothesis, including

* Corresponding author. E-mail addresses: [email protected] (I.A. Catala´n), Arild.Folkvord@bio. uib.no (A. Folkvord), [email protected] (I. Palomera), [email protected] (A. Tselepides), [email protected] (A. Kallianotis). 1 Present address: Smithsonian Environmental Research Center, USA. E-mail: [email protected]. 0272-7714/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2009.11.033

enrichment, concentration and retention (Agostini and Bakun, 2002). The literature on the early life history of anchovies in the North Aegean Sea is relatively recent (Somarakis et al., 1997; Somarakis et al., 2002; Somarakis and Nikolioudakis, 2007; Isari et al., 2008) compared to the knowledge on other Mediterranean areas. In terms of environmental change, alterations in water properties and fluxes through straits may affect the ecosystems in nearby areas such as the North-eastern Aegean Sea (NEA) in the mid- to long-term. Therefore, there is a clear need to describe these systems. Although data on growth, mortality and distribution exist for this species and this area, data on feeding are absent, and the temporal resolution of the existing works tends to exclude withinyear variation (Somarakis and Nikolioudakis, 2007; Isari et al., 2008). The NEA includes the region where Black Sea water (BSW) flows into the North Aegean Sea (Fig. 1). Oceanographic literature on the region indicates that the area is characterised by a strong

300

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

Fig. 1. Study area and sampling stations for each survey. Symbols indicate both bongo sampling and CTD casts (þ) or only CTD casts ($). Numbers are station codes. Capital letters in the first graph indicate the main topographic features: E, Evros river; N, Nestos river; T, Thassos Island; I, Imvros Island; L, Lemnos Island; S, Samothraki Island. Small letters indicate stations for which otolith (O) or feeding analyses (F) were conducted. Microzooplankton casts were collected in most stations. Isobaths are shown in the top-right graph.

thermohaline front in the vicinity of Lemnos island (Zodiatis and Baloupoulos, 1993) (Fig. 1). The position of the front varies seasonally, possibly advected by the dominant wind stress (Zervakis and Georgopoulos, 2002). In summer, the etesian winds (dry northerly winds dominating the Aegean from mid-May to midSeptember) tend to push part of the thermohaline front to move south of Lemnos. In winter, the front is situated between the islands of Lemnos and Imvros, and the surface BSWs are carried on a north-westward track towards the shelf of the Sea of Thrace, thus fertilising the area. The general circulation in the region is also characterised by the presence of a permanent anticyclone around the island of Samothraki (and possibly Imvros, Fig. 1); the ‘‘Samothraki gyre’’ recirculates the surface BSW and increases its residence time in the region (Zervakis and Georgopoulos, 2002), affecting the distributions of fish larvae and mesozooplankton (Isari et al., 2008). The Samothraki gyre is thought to provoke a quasipermanent mechanism for larval retention (Somarakis and Nikolioudakis, 2007), possibly contributing to the importance of this area for anchovy populations. The objectives of the present work were to analyse the feeding ecology of larval anchovy in the area, to widen the variability scale in growth analyses by analysing two seasons (July and September) in two consecutive years and to analyse these processes with regard to environmental variability. Geographically, the aim was to cover the main area affected by the BSW outflow, including stations south of Lemnos Island.

2. Materials and methods 2.1. Sampling area and collection methods The four surveys analysed herein comprise a physical and biological grid over the NEA (Fig. 1). The surveys were conducted during July 2003 (days 4–15), September 2003 (days 5–15), July 2004 (days 9–19) and September 2004 (days 17–20) onboard the R/Vs ‘‘Aegaeo’’ and ‘‘Philia’’. Data from several mesozooplankton groups and the basic physical and biological sampling plan have been described elsewhere (Isari et al., 2008). Basically, a grid of 51 physical and 42 biological stations including ichthyoplankton hauls (bongo 60 cm diameter equipped with 250-mm mesh and flow meters General Oceanics 230) were sampled during the first three surveys. For the last survey, the grid was reduced for logistic reasons (Fig. 1). CTD water column profiles (temperature,  C, salinity, and fluorescence, Volts) were taken at all stations, using a Seabird SBE 9 profiler equipped with a fluorometer. Seawater samples were collected at four depths (2, 5, 10, 20 m) at 26 stations on the grid using a 5 L ‘‘Universal Water Sampler’’ (Hydrobios, Kiel). Water samples were analysed for nutrient determination following Parsons et al. (1984). Water samples for Chlorophyll-a (Chla, mg L1) analysis were transported in 1 L polyethylene containers and filtered through Millipore GF filters, which were kept frozen in darkness at 22  C until further analysis. Chla concentrations were determined fluorometrically (Lorenzen and Jeffrey, 1980; Yentsch

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

and Menzel, 1963) using a Turner TD-700 fluorometer. Microzooplankton (MZ, mg m3) was collected at most stations and time points, with the exception of September 2004, using vertical tows and a vertical WP-2 type net of 40 cm diameter and 63-mm mesh. Samples were collected from the bottom (maximum of 150 m) to the surface. Most of the sample was preserved and stored in 4% formalin buffered with borax, and 30 ml of each sample were kept at 22  C for biomass determination. In the lab, the sample was filtered through a 200-mm mesh to obtain the 63–200 mm fraction. This fraction was forced through a pre-weighed 47-mm GF/C Whatman filter, and the dry weight (DW, mg) was obtained (precision of 0.1 mg) after drying at 70  C for 24 h. For selected stations, the taxonomic composition was determined for the main groups to analyse larval feeding preferences. Bongo hauls for anchovy eggs and larvae were performed during daylight hours and samples were preserved in 4% phosphate-buffered formalin. These specimens were used for distribution/dynamics analyses and for feeding analyses. For growth analyses, larvae from selected stations (12 stations in July 2003, 10 stations in September 2003 and 18 stations in July 2004), including some repeated hauls, were preserved in 96% ethanol (Fig. 1, Table 1).

301

2.2. Distributions and dynamics of eggs and larvae Eggs and larval abundances were standardised to ind. 10 m2 (Smith and Richardson, 1977), and a random sample from each station (at least 30 larvae when possible: Table 1) was used for standard length (SL, mm) determination using a binocular microscope to the nearest 0.01 mm. Comparisons of length distributions were performed using a nested ANOVA design via GLM (Statistica v7.0, Statsoft Inc.), where the factors were year, survey and a prioridefined regions (nested). The definition of regions is explained in section 2.5. 2.3. Feeding analysis In all, 651 larvae from selected stations were analysed via a compromise of sampling enough individuals (by statistical standards) from comparable length ranges within a reasonable spatial coverage (Fig. 1, Table 1). Larval length was corrected using a factor of 1.03 for formalin shrinkage (Theilacker, 1980). Larvae were measured to the nearest 0.01 mm using an eyepiece micrometer under a binocular microscope, and their digestive tracts were then removed and longitudinally dissected with a blade. The gut

Table 1 Number of anchovy larvae used for length (NL), growth (NG) or feeding (NF) studies. Station

Jul 03 NL

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 Total

19 1 5 72 27 11 41 63 173 277 36 115 161 155 332 75 107 0 124 141 277 93 138 126 149 11 34 48 8 16 104 71 29 45 110 123 113 49 1 190 216 81 3967

Sep 03 NG

NF

NL

Jul 04 NG

NF

48 3 5 31 1

21 18 17 16 23 14 19

40

68 43

15 18

17

43 38 15 21 45 49 214

324

17 19 25 52 8 57 128 144 162 52 4 19 76 175 171 30 107 34 112 39 77 116 64 6 2 82 47 96 159 49 13 3 28 21 17 2299

15

15 32

25 24

26

32

18

17

9 30

14 22 42 249

130

NL 1 81 15 33 2 84 80 22 64 100 23 100 23 137 66 121 1 89 25 9 80 75 16 8 67 47 11 4 1 20 10 8 90 16 82 39 2 63 40 14 1769

Sep 04 NG

NF

NL

NG

2 1 17 15 2 16

8 3 2

8 2

19 14

1 24

14 61 37 18 5 14

17 4 15 50 1

4 2 4 4

1

2 2 20 13 20

17 18

23

18 2

14 11

24 57

191

197

164

16

NF

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

302

contents were identified to the lowest possible taxonomic level, and the lengths and widths of food items were recorded under a microscope to the nearest 1 mm. The feeding incidence (% of larvae with food in their gut) was analysed for each survey at 2 mm SL classes. The lack of a sufficient number of feeding larvae precluded their analysis at a level more in depth than by survey. The diet composition was described for each prey type and larval size interval through i) the percentage of positive stomachs containing a given prey type (% F) and ii) the numerical representation of a given prey type with respect to all prey (% N). The relationship between prey width (PW), prey type and larval length was studied using both 2-mm SL classes and 0.2-mm SL classes. The former division was used to study the changes in prey size of the main prey types through larval size class, whereas the second method was adopted to quantify total changes in PW with larval length. Following the statistical considerations of several authors (Pearre, 1986; Pepin and Penney, 1997), Log10transformed PW values were regressed against larval 0.2 mm SL ranges using the number of prey per larval size class as weights. The niche breadth was conceptualised as the relationship between the standard deviation of Log10-transformed PW and larval SL classes. Therefore, large standard deviations imply increased size ranges of prey. The possible change in the trophic level of anchovy larvae from different size classes was calculated through the Troph value, which expresses the position of organisms within the food webs of aquatic ecosystems. The definition of Troph for any consumer species (i) is:

Trophi ¼ 1 þ

G X

DCij *Trophj

j¼1

where Trophj is the fractional trophic level of prey j, DCij represents the fraction of j in the diet of i and G is the total number of prey species (or groups). In aquatic consumers the Troph varies between 2.0, for herbivorous/detritivorous, and 5.0, for piscivorous/carnivorous organisms (Pauly et al., 1998). The Troph value was calculated using the ‘‘quantitative aproach’’ from TrophLab software (Pauly et al., 2000). This approach uses the weight or volume contribution and the trophic level of each prey species to the diet to estimate the Troph and its standard error (SE). We used the default Troph values for various prey (based on data in FishBase; Froese and Pauly, 2000). For converting our length measures into dry weights (DW mg), we used published length–weight conversions. For copepods, we used data from Van der Lingen (2002) (eggs), Uye (1982) (copepodites/adults) and Berggreen et al. (1988) (nauplii). Other sources included Catala´n et al. (2007) for Evadne sp., Ikeda (1992) for ostracods, Menden-Deuer and Lessard (2000) for phytoplankton and other protist, Holland et al. (1975) for gastropod larvae and Madin et al. (1981) for gelatinous plankton. A 40% carbon in DW measures was assumed if necessary.

2.4. Growth analyses Typically, 15 randomly selected larvae were analysed for age determination from each station. Standard length was measured to the nearest 0.1 mm using the free Image J software, and no shrinkage due to ethanol preservation was assumed (Theilacker, 1980). The DW (mg) of each larva (except for July 2003 larvae and stations 15, 19, 27 and 34 in September 2003) was recorded to the nearest 1 mg after drying for 24 h at 60  C. Both sagittae otoliths were extracted under a Leica dissection microscope (Wild Heerburg) equipped with polarising filters and mounted in CrystalbondÔ 509 on labelled glass slides. The otolith growth analysis

was undertaken at a 1000 magnification under transmitted light with a microscope (Olympus BX60) coupled to a digital camera. Otolith radius (OR), first check and increment width (IW) (mm) were measured to the nearest 0.1 mm using Image-Pro Plus 5.0.2. The increments were measured along the longest radius, from the middle of one D-zone to the middle of the next D-zone (as the first check is a D-zone). The same overall quality scale used by Somarakis and Nikolioudakis (2007) was used in addition to the quality scale for each increment. Increments were assumed to be daily (DI) from the first check, which usually contained up to five finer increments from the core. All otoliths were read twice, and the readings were accepted only if they differed by less than 2 DI, choosing the sagitta that presented the best picture quality. The daily length increment (DLI, mm d1) was calculated using the equation DLI ¼ (SLSL0) DI1, where SL ¼ the observed standard length, SL0 ¼ 3.2 mm and DI ¼ the number of daily increments. The value for SL0 was chosen because this was the smallest value of larva materials from the same population. Palomera et al. (1988) found yolk sac larvae up to a length of 3.5 mm, but larvae with functional mouths were found from 3.2 mm. The time from hatching to the presence of functional jaws and yolk sac absorption was found to be 2 d. This value was not added to the DI in the results. 2.5. Relationships among growth, feeding and environment Surface temperature, salinity and egg and larval distributions were mapped using optimal interpolation methods from ODV v4.0.0.e (Schlitzer, 2008). A general environmental characterisation of the first three surveys, for which more data were available, was first performed using Principal Component Analysis (PCA) on a correlation matrix of six selected variables (Depth (D, m), MZ, and mean values in the first 20 m of temperature (T20), salinity (S20), oxygen (O20, mg O2 L1) and Chlorophyll a (Chla20)). The depth of 20 m was selected as the integration depth for comparative analyses as in other areas it includes most eggs and a large proportion of small-sized larvae (Olivar et al., 2001). Further, values of selected  3 nutrients (N–NHþ 4 , N–NO3 , P–PO4 , SiO2), expressed in mM, were correlated with the main PCA axes to explore possible mechanisms for the observed resulting patterns. They were not originally included in the PCA design due to the lower number of data points, and only nutrients at the surface (5 m) were used, as they were highly correlated with values at other depths. Only PCA axes with eigenvalues close to or greater than 1 (Kaiser criterion) were used for interpretation. Further, bivariate relationships were explored using non-parametric Spearman correlations (Rs). For the September 2004 survey, only T20 and S20 data were available. Thus, we used weekly composites of surface Chla (mg m3, Modis Aqua, NASA, 0.05 ) and SST ( C, AVHRRv5, NOAA, 0.05 ) to help in the interpretation of results, which were calculated over the area determined by the sampling grid. This resolution (around 800 effecive pixels) was considered adequate for non-quantitative interpretations. To help in the explanation of the results, the stations within each survey were qualitatively classified into five main regions that included specific features such as river outflows or the BSW-LW front. The resulting regions included the following: I (inshore, St. 1-6); N-C (North-Central, St. 7-25, excluding St. 11); S-C (South-Central, St. 26-34); N-E (North-East, St. 35-39) and S (South, St. 40-42) (Figs. 1 and 2). Whereas larval length variability was analysed at a full factorial level (see section 2.2), feeding and growth had to be aggregated at the survey level. The diet of larval anchovy was compared to the microzooplankton species composition collected in the same stations for which feeding data were available. Comparisons of growth patterns were conducted using ANCOVA and ANOVA with

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

303

Fig. 2. Surface (5 m) temperature (T,  C) and salinity (S) horizontal distribution. In the top left graph the geographic divisions used for explanations in the text are shown, where I ¼ inshore; N-E ¼ North-East; N-C ¼ North-central; S-C ¼ South-central; S ¼ South. Means and standard deviations are also shown.

304

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

GLM (see section 2.2). The relationships between environmental patterns and daily length increments at the individual level were analysed using correlation techniques on data from all surveys and regions. 3. Results 3.1. Environmental context In July 2003, surface temperature (21.6  C–25.8  C) showed the highest contrasts between the central and the southern regions (Fig. 2). Surface salinity (31.9–38.1) followed a pattern opposite to that of temperature. The signs of the BSW were evident in the first 20 m and occupied all of the horizontal transect between the

islands of Thassos and Samothraki (Fig. 3). Over 74% of the environmental variability within the first 20 m was explained from the first two Principal Components (PCs, Table 2). The first PC (54% of the variance) accounted for the inverse relationship between T20 and S20 that occurred at relatively deep (central) areas. Chla20 and MZ were directly inter-related and positively correlated with Chla at other depths (Table 2). Chla20 and MZ were basically associated with shallow depths and high salinity values (Table 2, Fig. 4), observed at area I and around Lemnos Island. In general, nutrient levels correlated poorly with the main PCs but tended to appear at shallow depths (possibly influenced by rivers) or in areas influenced by BSW (PC1, Fig. 2). In September 2003, the surface temperature ranged from 20.3  C to 25.2  C. The thermohaline front was clearly apparent to

Fig. 3. Vertical profiles of temperature (shaded) and salinity (contours) for the cruises along a horizontal section indicated in the top left graph (see Fig. 1). For temperature, divisions are 1  C resolution.

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

305

Table 2 Factor loadings for the PCA performed on 6 selected environmental variables for the three main surveys. D, depth (m); Chla, mean Chlorophyll-a (mg L1); MZ, mean microzooplankton concentration (mg DW m3); O2, mean oxygen concentration (mg L1); PC, principal component; S, mean salinity; T, mean temperature ( C). Variables not used in the PCA but with potential explanatory value (nutrients etc.) were correlated with each PC and are shown in the table. The subscript ‘‘20’’ indicates values averaged over the first 20 m, excluding the first 2 m. Used for PCA PC Jul-03

Sep-03

Jul-04

1 2 3 1 2 3 1 2 3

Not used for PCA

T20

S20

O20

Chla20

MZ

D

0.895 0.301 0.214 0.908 0.148 0.217 0.678 0.635 0.121

0.835 0.389 0.273 0.888 0.290 0.054 0.111 0.962 0.067

0.850 0.172 0.241 0.804 0.003 0.408 0.793 0.540 0.055

0.644 0.509 0.374 0.867 0.170 0.089 0.659 0.667 0.007

0.501 0.664 0.528 0.477 0.636 0.561 0.671 0.131 0.707

0.776 0.102 0.307 0.279 0.835 0.387 0.757 0.295 0.444

NH4þ (5 m)

NO 3 (5 m)

PO3 4 (5 m)

SiO2 (5 m)

Chla (5 m)

Max Chla (0–50 m)

Eigen.

% Total variance

0.381 0.032 0.178 0.047 0.087 0.109 0.064 0.481 0.209

0.075 0.212 0.045 0.233 0.039 0.172 0.279 0.127 0.053

0.041 0.042 0.036 0.136 0.136 0.195 0.029 0.033 0.447

0.207 0.128 0.036 0.302 0.167 0.143 0.404 0.604 0.020

0.621 0.039 0.139 0.681 0.317 0.069 0.589 0.260 0.244

0.210 0.010 0.258 0.591 0.310 0.041 0.513 0.314 0.361

3.49 0.98 0.69 3.31 1.24 0.69 2.56 2.17 0.71

58.2 16.4 11.5 55.3 20.6 11.5 42.7 36.2 12.0

Stations N-C

I 1

3

5

7

9

S-C

N-E

S

11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41

0.25

Jul 03

25

MICROZOOPL. 0.20

CHLA

10m

20

0.15 15 0.10

100m

10

0.05

5

1000m 0

0.00

N-C NC

I 1

3

5

7

9

SC S-C

N E N-E

S

11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41

0.25

Sep 03

25

0.20

10m

20

0.15 15 0.10 10

100m

0.05

5

1000m I

0 1

3

5

0.00

N-C 7

9

S-C

N-E

S

11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41

30

0.25

Jul 04

25

0 20 0.20

10m 0.15

15 10

100m

0.05

5 0

0.10

Chla (µg l-1)

20

Chla (µg l-11)

Microzoop plankton (mg m -3)

30

Microzooplankton (mg m -3)

Chla (µg l-1)

Microzooplankton (mg m -3)

30

1000m

0.00

Fig. 4. Microzooplankton and Chla values (0–20 m) at each station superimposed on the depth profile. The scale for the depth is in log10 units, at the inside of the left axis. The geographic divisions in the top axis are explained in section 2.5.

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

the south, and the average salinity was slightly higher than in the previous survey (Fig. 2), ranging from 33.8 to 39.2. The BSW signal was deeper and occupied the entire horizontal transect (Fig. 3), suggesting a ‘‘relaxed mode’’ of the Samothraki gyre, which extended over the northern part of the surveyed area (Figs. 2 and 3). Over 76% of the variance was explained by the first two PCs (Table 2). The first PC accounted basically for the BSW-influenced waters, whereas the second axis showed the opposing trends of depth and production (Table 2, Fig. 4). In July 2004, the surface temperature (20.2  C–24.7  C) was slightly lower than in July 2003 (Fig. 2). Surface salinity ranged from 32.0 to 36.9. The surface temperature and salinity patterns showed an easterly displaced BSW with respect to the previous surveys which, together with the lifting isohalines around station 19 (Fig. 3), suggested that there was a cyclonic circulation that was more confined to the Samothraki island; this was also evident from geostrophic calculations (not shown). The PCA showed that the first two axes explained ca. 79% of the variance. The PC1 showed that the high temperatures observed over deep stations were not characterised by low salinity, but showed low production (Table 2). In contrast, PC2 showed that the stations highly influenced by BSW were more coastal and more productive than the previous surveys in areas I and N-C (Fig. 4). Nutrient levels were also higher at lower depths, particularly in the case of SiO2. In September 2004, the number of stations was reduced, and no production or nutrient data were collected. Temperature ranged from 21.5  C to 23.2  C and salinity from 34.4 to 35.3. The vertical profile of the transect indicated that the gyre was confined to the vicinity of Samothraki island, as in July 2004. Satellite-derived images showed that the average SST was higher in 2003 than in 2004 during the entire larval season (May–October, Fig. 5A),

26

surveySep03

surveyJul04

Monthly T 2003 surveyJul03 Monthly T 2004 Weekly T difference (2003-2004)

surveySep04

24

T (°C)

22 20

The horizontal distribution of eggs and larvae were relatively constant among surveys (Fig. 6). In both years, the abundance of eggs peaked in July, with a maximum of 7496 eggs 10 m2 in July 2003 and a maximum of 6684 eggs 10 m2 in July 2004. The peak of eggs in September was only 1691 eggs 10 m2 in 2003 and 276 eggs 10 m2 in 2004. The distribution of eggs was concentrated in shallow productive areas (Fig. 6), and remarkably, at the edge of the gyre in 2004 (Figs. 2, 6). The abundance of larvae was higher in 2003, with peaks of 8471 larvae 10 m2 in September and 4464 larvae 10 m2 in July. September 2004 showed the lowest abundances. In general, the distribution of larvae was skewed towards relatively shallow areas, including the S and S-C areas around Lemnos Island, where high microzooplankton occurred (Table 2, Fig. 4) and where the influence of BSW was evident. A balanced GLM analysis on SL using larvae from the three coincident regions for each survey (N-C, N-E and I, constituting between 78% and 100% of all measured larvae) showed that interregion differences in SL existed (effect: region (year*month); F8,7976 ¼ 64.3, p < 0.0001), and only between-year effects were significant (effect: year; F1,7976 ¼ 107.5, p < 0.001). Larvae from 2004 tended to be larger than in 2003, except for few larvae in southern stations in September 2003 (Table 3). During 2003, there was generally a north-to-south increasing gradient in mean

B

1.4 4 3

1.2

2

10 1.0

1 0

18 -1 16

Monthly Chla 2003 (mg m-3) Monthly Chla 2004 (mg m-3) Weekly Chla difference (2003-2004)

0.6

0.8

0.4

0.2

0.0

0.6 -0.2 0.4

-2

14

J

F M A

J

M

J A

S

0

5

10

15

20

25

30

J

O N D

10

Lat C

35

40

-0.4

0.2

-3

12

40.9 40.7 40.6 40.4 40.3 40.1 40 39.8 39.7 40.9 40.7 40.6 40.4 40.3 40.1 40 39.8 39.7

3.2. Distributions and dynamics of eggs and larvae

Chla (mg m-3)

A

Difference ((2003-2004)

28

whereas surface Chla values were comparable and were at their lowest values during the surveys (Fig. 5B). Spatially, it was clear that the northern part usually showed higher temperatures and Chla values (Figs. 5C and D). In September 2004, the Chla in the northern region tended to be slightly higher than the same month in 2003 (Fig. 5D).

Difference (2003-2004)

306

F M A M

0.0

-4 45

0

T (°C)

D

5

10

15

J 20

S

J A 25

30

O 35

N D 40

-0.6 45

Log Chla

27

0.7

25

0.5

23 21

2003

19

0.3

2003

01 0.1 -0.1

17

2004 5

15

-0.3

13

-0.5

11

-0.7

9 10

15

20

25

30

Week number

35

40

45

7

2004 5

-0.9 10

15

20

25

30

35

40

45

-1.1

Week number

Fig. 5. Area-averaged monthly SST (AVHRR) and suface Chla (ModisAqua), and interannual weekly differences (A, B). Latitudinal differences in weekly SST and Chla in the surveyed area (C, D). The position of the surveys is indicated by a vertical dashed arrow.

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

307

Fig. 6. Eggs and larval relative abundances during the surveys. Environmental areas used for length distribution analyses are depicted in the top right-hand graph (see Fig. 4).

length (Table 3), suggesting a recent spawning activity at the northern-central stations, as supported by Fig. 6. In September 2004, evidence of relatively recent spawning was overruled by mean SL values consistently larger than in September 2003 (Table 3).

3.3. Feeding ecology Information on prey composition in the guts was obtained for larvae measuring between 2.3 and 11.8 mm SL. From 651 larvae, 167 larvae had food in their guts. The mean feeding incidence varied

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

308

Table 3 Mean standard length (mm) and 95% confidence intervals for larval groups from each survey, region and year. Regions as in Fig. 4. Region

Jul 03

Sep 03

Jul 04

Sep 04

I N-C N-E S-C S

2.9  0.17 3.6  0.05 2.9  0.08 4.4  0.15 3.9  0.17

3.1  0.15 3.6  0.06 3.1  0.11 4.1  0.15 6.9  0.51

2.8  0.08 5.0  0.13 5.5  0.17 3.7  0.22 3.9  0.31

4.4  1.43 4.3  0.31 4.9  0.85 – –

from 21% to 30% among years (Table 4). Due to the relatively low number of larvae with food in their guts, a full factorial analysis was considered inappropriate. The number of prey items per positive gut varied between 1 and 7 (av. ¼ 1.7, SD ¼ 1.41). Of 290 prey items found, 77% were identified and, from these, 80% corresponded to copepod nauplii and copepodite stages. These were the only items that appeared more than once in a given gut. The maximum mean number of nauplii/gut was detected in larvae <7.9 mm SL, whereas the mean number of copepodites/gut was >1 in all larval size classes but the smallest one. As the mean number of prey per stomach was relatively low, both % F and % N did not differ greatly for a given prey type and larval size class. Copepod nauplii made up over 40% of the diet in terms of both % F and % N, followed by copepodites and adult copepods (22%) (Table 4). Besides these prey, copepod eggs and pollen were the only items yielding percentages over 5%. The vast majority of copepods belonged to the Order Calanoidea, although a few individuals from Harpacticoid (Microsetella sp., Euterpina sp.) and Poecilostomatoida (Corycaeidae) were found. Diet composition varied with larval SL, shifting from a naupliidominated diet to an increasingly significant fraction of larger copepod stages (Table 4). This implied a progressive incorporation of larger-sized prey as the anchovy larvae grew that resulted in a slight but significant increase in average prey width (Fig. 7A, C). The standard deviation of the Log10-transformed prey widths also

increased significantly with larval development, indicating a widening of the niche breadth (Fig. 7B). When comparing the diets of the larvae at each survey with the relative abundances of the ingested prey at the stations where the larvae were collected, a clear pattern emerged. Larvae tended to capture copepod nauplii at levels that were much higher than (July 2003) or similar to (September 2003) their relative abundance in the water column (Fig. 7D). An opposite trend was observed for cladocerans. The proportion of copepods and copepodites was also higher in the guts than in the environment, at least in September 2003 and July 2004. Ostracods and dinoflagelates were not detected in the guts at the rates expected from their abundances in the wild (Fig. 7D). As expected, the increased prey size with larval length (Fig. 7A, C), together with the increase in niche breadth (Fig. 7B) were translated into a shift in the selection of copepods over nauplii in the larger larvae analysed from September 2003 and July 2004; this was coupled to a larger mean size of the larvae analysed in those surveys (Fig. 7D). Average Trophs were close to 3 in larvae under 10 mm and almost 4 in larvae over 10 mm (Table 4). The high Troph value in the last size-class was due to the inclusion of a gelatinous plankton item and the low number of fish larvae. The average Troph for all larval sizes was 3.33  0.2, but it went down to 2.98  0.16 when this gelatinous item was excluded. 3.4. Growth patterns In all cruises, the average otolith daily increment width varied between approximately 1 mm d1 at the first increments up to an average of 5 mm d1. The larval populations from the September surveys showed the fastest increase in IW (Fig. 8A). Inter-cruise comparisons were made for several variables using only coincident length or age ranges. In the otolith size/larval size relationships, all regressions were significant (p < 0.0001). The otolith radius (OR) increased

Table 4 Feeding incidence and mean diet composition of anchovy larvae in the NEA during 2003 and 2004. NF ¼ number of larvae (and percentage with respect to analysed larvae) with non-empty guts for each year and size-class; % F, frequency of occurrence; % N, numeric frequency. The mean Trophs and the standard errors are indicated. Larval SL class (mm)

Feeding inc.

NF NF NF NF

Jul-03 Sep-03 Jul-04 TOT

Copepod eggs Copepod nauplii Copepodites/copepods Ostracod nauplii Cladocerans Acantharia Radiolaria Dinoflagellates Diatoms Pollen Salpidae Gastropod larvae Eneropneuste larvae Polychaete larvae Parasite Unidentified crustacean Unidentified prey Troph *

2–3.9

4–5.9

6–7.9

8–9.9

‡ 10

Pooled

34 (24.6%) 1 (5.3%) 1 (2.6%) 36 (18.4%) N. prey ¼ 68 %F %N 19.4 10.3 58.3 52.9 0.0 0.0 2.8 1.5 – 2.8 1.5 2.8 0.0 8.3 4.4 – 2.8 1.5 – 2.8 1.5 – – 2.8 1.5 – 16.7 23.5 3.04  0.29

37 (34.3%) 15 (25.8%) 17 (27.8%) 69 (30.4%) N. prey ¼ 112 %F %N 2.9 1.8 59.4 54.4 23.2 18.8 4.3 2.7 1.4 0.9 – 1.4 0.9 1.4 0.9 – 2.9 1.9 – – 1.4 0.9 1.4 0.9 1.4 0.9 1.4 0.9 14.5 15.2 2.99  0.15

20 (32.8%) 7 (21.2%) 19 (28.3%) 46 (28.6%) N. prey ¼ 84 %F %N 2.2 1.2 34.8 40.5 30.4 38.1 2.2 2.4 – 2.2 1.2 – – 2.2 1.2 6.5 3.6 – – – 2.2 1.2 2.2 1.2 2.2 1.2 10.9 9.5 3.15  0.31

4 (33.3%) 0 4 (22.2%) 8 20.5%) N. prey ¼ 16 %F %N – 12.5 6.3 50.0 50.0 – 12.5 6.3 – – – – 25.0 12.5 12.5 6.3 –

2 (40%) 4 (36.3%) 2 (15.3%) 8 (27.6%) N. prey ¼ 10 %F %N – 12.5 10.0 25.0 30.0 12.5 10.0

97 (30%) 27 (20.7%) 43 (21.8%) 167 (25.7%) N. prey ¼ 290 %F %N 6.0 3.4 47.9 45.6 21.6 21.9 3.6 2.4 1.2 0.7 1.2 0.7 0.6 0.3 3.0 1.8 0.6 0.3 5.4 3.1 1.2 0.7 0.6 0.3 1.8 1.0 0.6 0.3 1.8 1.0 1.2 0.7 14.4 15.8 2.98*  0.16

The gelatinous item was excluded, see text.

12.5

– – – 18.8 2.92  0.03

– – – – 12.5 12.5 –

10.0 10.0

– – – 25.0 30.0 3.91  0.28

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

A

B

2.2

SD Log 10 prey width (µm)

2 1.8 1.6 1.4 1.2 1

0.35 0.30 0.25 0.20 0.15 0.10

2.2 2.8 3.4 4.0 4.6 5.2 5.8 6.4 7.0 7.6 8.2 8.8 9.4 10.0 10.6 11.2 11.8 12.4

0.00

SL (mm)

C

260 240 220 200 180 160 140 120 100 80 60 40 20 0

Copepod eggs Nauplii Copepodites Others

n=56 9

26

µm >120 81-120 41-80 <40

n=91

1

n=54 4 31

n=18 11

n=10

33

10

20

48 30 66

50

39

43 7

SL (mm)

D Larval SL (mm)

Prey width (µm)

Y=0.1379+0.008x, r2= 0.04,p<0.01

0.05

2.2 2.8 3.4 4.0 4.6 5.2 5.8 6.4 7.0 7.6 8.2 8.8 9.4 10.0 10.6 11.2 11.8 12.4

Log 10 prey width (µm)

0.40

Y=1 .6367+0.0188x, r2 =0.18, p<0.0001

2.4

Prey width(%)

309

14

16

40

2-3.9 4-5.9 6-7.9 8-9.9 > 10 Larval SL class (mm)

9 7 5 3

0. 5

1

1. 5

2

2. 5

3

3. 5

100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0%

DIN OS CL C N July-03 Sep-03 July-04 Survey

Fig. 7. Weighted regression results for prey width vs. larval size (A) and niche breadth (B). In both graphs, means (A) and SD (B) for each 0.2 mm SL class are represented by slashes. Only larval classes with 3 or more prey are used for regressions. The prey width of each prey category along anchovy length is shown in (C) with the median, interquartilic range and outliers in the upper graph. The percentage composition by prey width ranges for each larval size class is shown in the lower part of graph C, where n ¼ number of prey. The comparison among the relative proportions of some of the numerically most important prey found in the anchovy guts (Gut) with respect to that proportion at the water column (Envir.) is shown in (D). In D, note the increasing larval size in the upper sub-graph. DIN, dinoflagellates; OS, ostracod nauplii; CL, cladocerans; C, copepodites; N, copepod nauplii.

exponentially with SL up to around 10–11 mm SL in all surveys. Above that length, the rates of increase slowed down, but only data for one survey was available, and it was not further analysed. There were no differences in the rates of increase of OR (ln-transformed) vs. SL, nor among the OR means, and the common otolith growth equation was described by Ln OR ¼ 1.638 (0.018) þ 0.13 (0.003) SL (r2 ¼ 0.78, n ¼ 513, p < 0.0001). The OR vs. dry weight relationship was allometric, and there were no significant differences in slopes or means between surveys in the linearised equations. The common equation was thus described by Ln OR ¼ 0.625 (0.036) þ 0.48 (0.009) Ln DW (r2 ¼ 0.89, n ¼ 336, p < 0.0001). For the DW (ln-transformed) vs. SL relationship, only larvae between 4 and 10 mm SL were used to ensure coincident data. No significant differences in slopes existed between groups, but clear significant differences in the means were evident (F2480 ¼ 67.78, p < 0.0001). Post-hoc comparisons (not shown) revealed that only July 2004 (Ln DW ¼ 1.13 (0.123) þ 0.51 (0.021) SL, r2 ¼ 0.81, n ¼ 134, p < 0.0001) showed a significantly higher average DW with respect to the other seasons (common

regression for the rest: Ln DW ¼ 0.867 (0.069) þ 0.50 (0.011) SL, r2 ¼ 0.92, n ¼ 182, p < 0.0001). Individual mean daily length increments ranged from 0.1 to 0.9 mm d1. The average estimated length growth rate ranged from 0.41 to 0.75 mm d1 (Fig. 8B, linear fit yielded similar r2 values to exponential fit; all significant, p < 0.0001). Comparisons for coinciding age ranges (10 DI) showed that there were significant differences in slopes between surveys (F3,502 ¼ 4.03, p < 0.01). Posthoc comparisons (not shown) showed that only the July surveys were not significantly different between them. Therefore, the growth rates in September were higher than in July (Fig. 8B). The pooled linear model for coinciding ages was SL ¼ 2.590 (0.097) þ 0.45 (0.016) DI (r2 ¼ 0.60, n ¼ 509, p < 0.0001). The mean DW increased between 24% and 39% d1 (Fig. 8C), and larvae from September 2004 also grew at a significantly higher rate than the rest (F2,286 ¼ 4.27, p < 0.001). With regard to environmental variables, inter-regional analyses could not be done due to unequal sample representation. To explore the possible effect of the environment on recent growth, individual DLI data from all surveys

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

310

Increment width (µm)

A

6

Jul 03 Sep 03 Jul 04 Sep 04

5 4 3 2 1 0

B

0

2

4

6

8

10

12

14

16

18

20

22

16 14

SL (mm)

12 10 8 6 4

Jul 03 Sep 03 Jul 04 Sep 04

2 0

C

0

2

4

6

8

10

12

y = 2.502 + 0.41x r2 = 0.69 y = 2.592 + 0.53x r2 = 0.72 y = 2.597 + 0.43x r2 = 0.68 y = 1.851 + 0.75x r2 = 0.79

14

16

18

20

22

8 7

Ln DW (µg)

6 5 4 3 Sep 03 y = 2.357+ 0.24x r2 = 0.77 Jul 04 y = 2.235+ 0.25x r2 = 0.77 Sep 04 y = 1.544 + 0.39x r2 = 0.79

2 1

0

2

4

6

8

10

12

14

16

18

20

22

Daily growth increments Fig. 8. Comparison of the otolith increment width (A) body standard length (B) and body dry weight (C) vs. daily increments of anchovy larvae during the cruises. In A, means, standard error (inner spread) and standard deviation (outer spread) are shown. In C, July 2003 was not included due to the low sample size.

were used and correlated against environmental variables at the corresponding station of collection. DLI varied between 0.15 and 0.72 mm d1. As DLI was found to be largely related to larval length (both ln-transformed) (r2 ¼ 0.41, p < 0.001), residuals from a regression on transformed values vs. mean environmental variables (averaged over the first 20 m) were analysed. From all variables, significant correlations were only found with increasing T20 (Rs ¼ 0.20, n ¼ 431) and Chla20 (Rs ¼ 0.19, n ¼ 225) and decreasing S20 (Rs ¼ 0.15, n ¼ 431). 4. Discussion The hydrographic conditions in 2003–2004 followed the known patterns in the area (Zervakis and Georgopoulos, 2002), and have

been partially described previously (Isari et al., 2008). The presence of a retention area around Samothraki Island and the annual cycles of surface temperature and chlorophyll support the suitability of the area for anchovy spawning and larval development. This together with the low salinity BSW and the river-associated nutrient input, conforms to the requirements of the ocean triad hypothesis (Agostini and Bakun, 2002), which favours the persistence of anchovy populations in the Thracian Sea (Somarakis et al., 2002; Somarakis and Nikolioudakis, 2007). The multivariate environmental characterisation showed that relatively shallow areas influenced by BSW or nearby rivers tend to exhibit high Chla and MZ values. These areas are related to high mesozooplankton abundances and to the abundance of epipelagic species (Isari et al., 2007; Isari et al., 2008). We observed that the spawning area was largely influenced by BSW-associated structures. In 2003, the BSW extended over a wide zone, and spawning occupied a relatively wide zone in July (Fig. 6). In contrast, in 2004 the gyre was displaced to the East and spawning was associated with the edges of the gyre. The association of BSW-related structures (the Samothraki gyre), and particularly its frontal zone, with anchovy spawning areas has been documented (Somarakis and Nikolioudakis, 2007; Isari et al., 2008). As it underlies the distribution of fish eggs and larvae, the adult distribution plays an important role and has been found to be associated to anticyclones in the area (Giannoulaki et al., 2005). The vast majority of the collected individuals for length analyses were under 6 mm (Table 3). The mean length of larvae tended to be higher in 2004, except for September 2003 at stations south of Lemnos (Table 3, Figs. 1, 5). This makes sense, as the extension of the Samothraki gyre was narrower in 2004, creating a strong retention zone in the area that would favour larval concentration close to suitable nursery grounds related to coastal rivers in the area, as described in Somarakis and Nikolioudakis (2007). However, these data are not conclusive, as the size range is small and retention effects are thus barely traceable through advection. It was clear, however, that the preferred spawning sites were located at I and N-C areas, as confirmed by the north-to-south gradient observed in mean length. This is the first work describing the feeding of larval anchovy in the Aegean Sea, and the data on the species and sizes composing the diet is highly relevant from an ecophysiological standpoint. Indeed, an increasing number of works devoted to the implementation of individual-based models of European anchovy claim to provide species-specific data on feeding and growth (Oguz et al., 2008; Uritzberea et al., 2008). The feeding incidence increased with larval size when the largest group was excluded due to the low larval numbers. This trend is common in larval anchovies (Islam and Tanaka, 2008) and may be due to i) the reduced tow-induced defecation, ii) the lower feeding incidence of smaller individuals with a narrowed window for prey selection or iii) to our inability to detect small prey items leaving few hard structures that may actually be important constituents of the larval fish diet (Hunt von Herbing et al., 2001). The feeding incidence was comparatively high with respect to other Mediterranean areas where larvae were captured with bongo nets (Tudela et al., 2002), but lower than for samples captured with LHPR (Conway et al., 1998). Allowing for sampling technique, our data derive only from day-collected larvae, which may imply an overestimation of feeding incidence. Further, food extrusion at fishing time is a well-known phenomenon in larvae with straight guts (Conway et al., 1998). Feeding incidence values are thus probably not useful for comparative purposes, but serve as an indication of how representative the feeding analysis was. With regard to prey composition and prey size vs. larval size, it is assumed that the food items found in the gut are present in a proportional manner to larval feeding preferences for prey size

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

and prey types. Anchovy larvae are unusual feeders in comparison to other larvae (Last, 1980) in the sense that their gut is rapidly emptied (Conway et al., 1998). Therefore, the observed gut contents (allowing for artificial evacuation, etc.) are probably representative of the actual prey field at the moment of capture. In this respect, the food composition and relative proportion in the guts are similar to other distant areas of the Mediterranean (Regner, 1985; Conway et al., 1998; Tudela et al., 2002). Some prey types may also have not been detected due to their small size and soft tissues, whilst others may have been overestimated due to their hard parts. Although an electivity index could not be calculated due to the relatively low number of prey per larval size class and year, the comparison of prey in the guts vs. prey in the field performed at selected stations suggested that copepods were positively selected in September 2003 and July 2004, whereas nauplii were positively selected in July 2003. These patterns probably arise from the lower mean size of the larvae in July 2003 and agree with Chesson’s derived data for anchovy larvae in other areas (Morote and Olivar, pers comm). Overall, the mean Trophs for the different size classes reflected a diet based on planktonic copepods in various phases, and did not reflect the change in prey size. These values are similar to the troph of adult anchovies (Coll et al., 2008), and in the lower range of generic Troph values calculated for fish larvae (Froese and Pauly, 2000). Probably, the gelatinous items found in the largest larval length group were overestimated in length and so were the derived DW for those larvae. Primary producers were found in most small larvae, which partly explains the low Troph values. Despite their initial preference for microzooplankton, it is well known that anchovies can change from particulate to filter feeding depending on the available prey fields, which makes them highly flexible feeders (eg. Borme et al. (2009) and references therein). This suggests that the use of Trophs might be of use in order to detect significant differences in local feeding conditions. Our length growth rates are in the range of those calculated for several areas in the Mediterranean (See Somarakis and Nikolioudakis (2007) and references therein), although they varied greatly between seasons. The surveys in September (particularly 2004) tended to show higher growth rates (in SL and DW) than the July surveys. Interpretation of surface Chla patterns from satellitederived images was the only way to cross-compare all surveys for this variable. Generally, Chla was slightly higher in the July than in September surveys (Fig. 5B, D). A plausible explanation for the higher growth, particularly in September 2004, was the dominance of relatively low temperatures in the northern shelf zone and around Samothraki Island (Fig. 2) coupled with levels of Chla that were higher than in September 2003 and similar to the July months at this collection site (Fig. 5D). Despite the lack of essential microzooplankton data for September 2004, literature data show that the effect of high temperatures coupled to low food availability are highly detrimental to larval growth (Folkvord, 2005), which may be a common situation in oligotrophic areas like the NEA. Therefore, increasing temperature trends in this area might not necessarily have a positive effect on anchovy populations. Further field evidence comes from Garcı´a et al. (1998), who found faster growth rates and better conditions of European anchovy larvae in colder areas characterised by a richer feeding environment. Similar trends were found by Catala´n et al. (2006) in larval European pilchard at a mesoscale level within a given cruise. Additionally, the effect of parental stock on the higher quality of eggs in September 2004 cannot be discarded. Actually, the Chla values in the northern part of the NEA were higher in 2004 than in 2003 (Fig. 5D), and this might have affected the egg quality in that season. The reason for the higher DW values for a given length in July 2004 is difficult to determine, but might be related to the combination of higher potential food abundance at lower temperatures. Although in situ

311

data for microzooplankton were not particularly plentiful in July 2004, values for in situ Chla were (Fig. 4). On the other hand, data on mesozooplankton abundance for that area and period showed that values from the first 50 m were much higher in July 2004 than in any 2003 season (Isari et al., 2008). The high observed growth rates in September 2004 might be explained in terms of relatively low temperature coupled to high prey abundance. This might have affected the residuals of the individually calculated DLI, which correlated positively with T20 and Chla20, but negatively with S20, further supporting the link between anchovy larval growth rates and BSW-related features. In conclusion, besides the effect of BSW and shelf-associated effects on eggs and larval distribution, we observed inter-annual growth variability that might be associated to combinations of potential food availability and temperature. Larval feeding ecology is firstly described for this area. Feeding intensity was relatively high compared to other Mediterranean areas and comparable in terms of diet composition through larval size. Data suggests positive feeding selection for nauplii and later developmental stages of copepods, but higher temporal and spatial resolution data is needed in order to fully understand trophic connections in larval anchovy and how growth is affected by changing combinations of prey fields and the physical environment in the NEA. Acknowledgements The present study was supported by the EU project ANREC (QLRT-2001-01216). The authors thank the captain, the crew and the scientific teams involved in all the cruises conducted onboard R/V AEGAEO and R/V PHILIA. Thanks also go to all people that contributed with technical assistance (special thanks go to Turid Solbakken and Martı´ Galı´) in the preparation and analysis of biological and physical data. The first author was partially funded by the EU project SESAME (FP6: 036949-2). References Agostini, V.N., Bakun, A., 2002. ‘Ocean triads’ in the Mediterranean Sea: physical mechanisms potentially structuring reproductive habitat suitability (with example application to European anchovy, Engraulis encrasicolus). Fisheries Oceanography 11, 129–142. Berggreen, U., Hansen, B., Kiørboe, T., 1988. Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implication for determination of copepod production. Marine Biology 99 341–352. Borme, D., Tirelli, V., Brandt, S.B., Fonda Umani, S., Arneri, E., 2009. Diet of Engraulis encrasicolus in the northern Adriatic Sea (Mediterranean): ontogenetic changes and feeding selectivity. Marine Ecology Progress Series 392, 193–209. Catala´n, I.A., Alemany, F., Morillas, A., Morales-Nin, B., 2007. Diet of larval albacore Thunnus alalunga (Bonnaterre, 1788) off Mallorca Island (NW Mediterranean). Scientia Marina 71, 347–354. Catala´n, I.A., Olivar, M.P., Palomera, I., Berdalet, E., 2006. Link between environmental anomalies, growth and condition of pilchard Sardina pilchardus (Walbaum) larvae in the NW Mediterranean. Marine Ecology Progress Series 307, 219–231. Coll, M., Palomera, I., Tudela, S., Dowd, M., 2008. Food-web dynamics in the South Catalan Sea ecosystem (NW Mediterranean) for 1978–2003. Ecological Modelling 217, 95–116. Conway, D.V.P., Coombs, S.H., Smith, C., 1998. Feeding of anchovy Engraulis encrasicolus larvae in the northwestern Adriatic Sea in response to changing hydrobiological conditions. Marine Ecology Progress Series 175, 35–49. Folkvord, A., 2005. Comparison of size-at-age of larval Atlantic cod (Gadus morhua) from different populations based on size- and temperature-dependent growth models. Canadian Journal of Fisheries And Aquatic Sciences 62, 1037–1052. Froese, R., Pauly, R., 2000. FishBase 2000: Concepts, Design and Data Sources. ˜ os, Laguna, Philippines, pp. 344. ICLARM, Los Ban Garcı´a, A., Cortes, D., Ramirez, T., 1998. Daily larval growth and RNA and DNA content of the NW Mediterranean anchovy Engraulis encrasicolus and their relations to the environment. Marine Ecology-Progress Series 166, 237–245. Giannoulaki, M., Machias, A., Somarakis, S., Tsimenides, N., 2005. The spatial distribution of anchovy and sardine in the northern Aegean Sea in relation to hydrographic regimes. Belgian Journal of Zoology 135, 151–156. Holland, R., Tantanasiriwong, R., Hannant, P.J., 1975. Biochemical Composition and Energy Reserves in the Larvae and Adults of the Four British Periwinkles

312

I.A. Catala´n et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312

Littorina littorea, L. fittoralis, L. saxatilis and L. neritoides. Marine Biology 33, 235–239. Hunt von Herbing, I., Gallager, S.M., Halteman, W., 2001. Metabolic costs of pursuit and attack in early larval Atlantic cod. Marine Ecology Progress Series 216, 201–212. Ikeda, T., 1992. Laboratory observations on spawning, fecundityand early development of a mesopelagic ostracod, Conchoecia pseudodiscophora, from the Japan Sea. Marine Biology 112, 313–318. Isari, S., Fragopoulu, N., Somarakis, S., 2008. Interanual variability in horizontal patterns of larval fish assemblages in the northeastern Aegean Sea (eastern Mediterranean) during early summer. Estuarine, Coastal and Shelf Science 79, 607–619. Isari, S., Psarra, S., Pitta, P., Mara, P., Tomprou, M.O., Ramfos, A., Somarakis, S., Tselepides, A., Koutsikopoulos, C., Fragopoulu, N., 2007. Differential patterns of mesozooplankters’ distribution in relation to physical and biological variables of the northeastern Aegean Sea (eastern Mediterranean). Marine Biology 151, 1035–1050. Islam, M.S., Tanaka, M., 2008. Diet and prey selection in larval and juvenile Japanese anchovy Engraulis japonicus in Ariake Bay, Japan. Aquatic Ecology. doi:10.1007/ s10452-008-9207-6. Last, J.M., 1980. The food of twenty species of fish larvae in the west-central North Sea. Fisheries Research Technical Report 60. MAFF Directorate of Fisheries Research, Lowestoft. Lorenzen, C., Jeffrey, J., 1980. Determination of chlorophyll in seawater. UNESCO Technical paper. Marine Sciences 35, 1–20. Lleonart, J., Maynou, F., 2003. Fish stocks assessments in the Mediterranean: state of the art. Scientia Marina 67, 37–49. Madin, L.P., Cetta, C.M., McAlister, V.L., 1981. Elemental and biochemical composition of salps (Tunicata, Thaliacea). Marine Biology 63, 217–226. Menden-Deuer, S., Lessard, E.J., 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45, 569–579. Oguz, T., Salihoglu, B., Fach, B.A., 2008. A coupled plankton-anchovy population dynamics model assessing nonlinear controls of anchovy stock and anchovy-gelatinous regime shift in the Black Sea. Marine Ecology Progress Series 369, 229–256. Olivar, M.P., Salat, J., Palomera, I., 2001. Comparative study of spatial distribution patterns of the early stages of anchovy and pilchard in the NW Mediterranean Sea. Marine Ecology Progress Series 217, 111–120. Palomera, I., Morales-Nin, B., Lleonart, J., 1988. Larval growth of anchovy, Engraulis encrasicolus, in the Western Mediterranean Sea. Marine Biology 99, 283–291. Parsons, T.R., Maita, Y., Lalli, C., 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford, pp. 173. Pauly, D., Trites, A., Capuli, E., Christensen, V., 1998. Diet composition and trophic levels of marine mammals. ICES Journal of Marine Sciences 55, 467–481. Pauly, D., Froese, R., Sa-a, P., Palomares, M.L., Christensen, V., Rius, J., 2000. TrophLab in MS Access 2000. Electronic homepage http://www.fishbase.org/download/ TrophLab2K.zip.

Pearre, S., 1986. Ratio-based trophic niche breadths of fish, the Sheldon spectrum, and the size-efficiency hypothesis. Marine Ecology Progress Series 27, 299–314. Pepin, P., Penney, R.W., 1997. Patterns of prey size and taxonomic composition in larval fish: are there general size-dependent models? Journal of Fish Biology 51, 84–100. Regner, S., 1985. Ecology of planktonic stages of the anchovy, Engraulis encrasicolus (Linnaeus, 1758), in the central Adriatic. Acta Adriatica 26 (1, Series Monographiae, 1), 1–113. Schlitzer, R., 2008. Ocean Data View, http://odv.awi.de. Smith, P.E., Richardson, S.L., 1977. Standard techniques for pelagic fish egg and larva surveys. FAO Fisheries Technical Paper, 175. FAO, Rome, pp. 100. Somarakis, S., Drakopoulos, P., Filippou, V., 2002. Distribution and abundance of larval fish in the northern Aegean Sea–eastern Mediterranean–in relation to early summer oceanographic conditions. Journal of Plankton Research 24, 339– 358. Somarakis, S., Kostikas, I., Tsimenides, N., 1997. Fluctuating asymmetry in the otoliths of larval fish as an indicator of condition: conceptual and methodological aspects. Journal of Fish Biology 51, 30–38. Somarakis, S., Nikolioudakis, N., 2007. Oceanographic habitat, growth and mortality of larval anchovy (Engraulis encrasicolus) in the northern Aegean Sea (eastern Mediterranean). Marine Biology 152, 1143–1158. Stergiou, K.I., Christou, E.D., Georgopoulos, D., Zenetos, A., Souvermezoglou, C., 1997. The Hellenic Seas: physics, chemistry, biology and fisheries. Oceanography and Marine Biology: an Annual Review 35, 415–538. Theilacker, G.H., 1980. Changes in body measurements of larval northern anchovy, Engraulis mordax, and other fishes due to handling and preservation. Fishery Bulletin 78, 685–692. Tudela, S., Palomera, I., Quı´lez, G., 2002. Feeding of anchovy Engraulis encrasicolus larvae in the north-west Mediterranean. Journal of the Marine Biological Association of the United Kingdom 82, 349–350. Uritzberea, A., Fiksen, Ø., Folkvord, A., Irigoien, X., 2008. Modelling growth of larval anchovies including diel feeding patterns, temperature and body size. Journal of Plankton Research 30, 1369–1383. Uye, S., 1982. Length-weight relationships of important zooplankton from the Inland Sea of Japan. Journal of the Oceanographical Society of Japan 38, 149– 158. Van der Lingen, C.D., 2002. Diet of sardine Sardinops sagax in the southern Benguela upwelling ecosystem. South African Journal of Marine Science 24, 301–316. Yentsch, C.S., Menzel, D.W., 1963. A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep Sea Research 10, 221–231. Zervakis, V., Georgopoulos, D., 2002. Hydrology and circulation in the North Aegean (eastern Mediterranean) throughout 1997 and 1998. Mediterranean Marine Science 3, 5–19. Zodiatis, G., Baloupoulos, E., 1993. Structure and characteristics of fronts in the north Aegean Sea. Bolletino Oceanologia Teorica ed Aplicata 11, 113–124.