Estuarine, Coastal and Shelf Science 86 (2010) 299–312
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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. Catalán a, *, Arild Folkvord b, Isabel Palomera c, Gemma Quı́lez-Badı́a c,1, Fotini Kallianoti d,
Anastasios Tselepides e, Argyris Kallianotis d
a
Institut Mediterrani d’Estudis Avançats (IMEDEA, CSIC/UIB), C/Miquel Marqués 21, CP 07190, Esporles, Balearic Islands, Spain
Department of Biology, University of Bergen, 5020 Bergen, Norway
Institut de Ciències 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. Catalán), 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. Catalán 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. Catalán 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
302
I.A. Catalán et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312
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 Catalán 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. Catalán 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. Catalán 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. Catalán 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. Catalán 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. Catalán 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
308
I.A. Catalán et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312
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. Catalán 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
310
I.A. Catalán et al. / Estuarine, Coastal and Shelf Science 86 (2010) 299–312
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. Catalán 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 Garcı́a 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 Catalán 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 Martı́ Galı́) in the preparation and analysis of biological and physical data. The first author was partially funded by
the EU project SESAME (FP6: 036949-2).
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