ICES Journal of

Marine Science
ICES Journal of Marine Science (2012), 69(8), 1394–1402. doi:10.1093/icesjms/fss117

Is juvenile anchovy a feeding resource for the demersal

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community in the Bay of Biscay? On the availability of pelagic
prey to demersal predators
Lucı́a López-López 1,2 *†, Izaskun Preciado 2, Begoña Villamor 2, Francisco Velasco 2,
Magdalena Iglesias 3, Enrique Nogueira 4, Jose Luis Gutierrez-Zabala2, and Ignacio Olaso2
1
GEOMAR- Helmholtz Zentrum für Ozeanforschung Kiel, Düsternbrooker Weg 20, 24105 Kiel, Germany
2
IEO Centro Oceanográfico de Santander, Promontorio San Martı́n s/n, PO Box 240, 39080 Santander, Spain
3
IEO Centro Oceanográfico de Baleares, Moll de Ponent s/n, Apdo 291, 07015 Palma de Mallorca, Spain
4
IEO Centro Oceanográfico de Gijón, Avenida Prı́ncipe de Asturias 70 bis, 33212 Gijón, Spain
*Corresponding author: tel: +34 942 291 716; fax: +34 942 275 072; e-mail: lucia.lopezlopez@st.ieo.es
†Present Address: IEO Centro Oceanográfico de Santander, Promontorio San Martı́n s/n, PO Box 240, 39080 Santander, Spain

López-López, L., Preciado, I., Villamor, B., Velasco, F., Iglesias, M., Nogueira, E. Gutierrez-Zabala, J. L., and Olaso, I. 2012. Is juvenile anchovy a
feeding resource for the demersal community in the Bay of Biscay? On the availability of pelagic prey to demersal predators. – ICES
Journal of Marine Science, 69: 1394 – 1402.
Received 9 December 2011; accepted 30 May 2012; advance access publication 12 July 2012.

The role that juvenile anchovy (Engraulis encrasicolus) play as a food resource for the demersal community in the southern Bay of
Biscay is assessed using 21 years of anchovy abundance data and demersal predator diets. During the study period, a total of 26
fish and elasmobranch species preyed on anchovy either frequently or occasionally. Predators with a crustacean-based diet targeted
the smaller anchovy individuals. The size range of anchovy juveniles (centred at 7.5– 8.9 cm) was comparable to that of the largest
nektonic– benthic crustaceans, but generally smaller than other demersal and pelagic fish prey. Hake (Merluccius merluccius) and
megrim (Lepidorhombus whiffiagonis) were the predators that consumed the highest number of anchovy, one of the main prey
items driving the variability of their diets. Anchovy consumption conformed only partially to the abundance of anchovy in the south-
ern Bay of Biscay, suggesting that factors other than abundance might condition its availability to demersal predators. Prey size could
be one of them, as the size of the anchovy preyed on proved to be significantly smaller than the individuals collected with bottom
trawls. However, other factors, such as the vertical position of the shoals of anchovy juveniles, could also constrain anchovy availability
to demersal predators.
Keywords: anchovy, Bay of Biscay, demersal predator, diet variability, hake, megrim, prey availability.

Introduction the interactions, and thus the adaptability of the foodweb to chan-
Much effort has been devoted during recent decades to under- ging conditions, since they are based either on a snapshot of the
standing how trophic interactions shape population dynamics. interactions at particular moments or on integrations over certain
Cascading effects in marine ecosystems following the collapse of time-periods (Moloney et al., 2011).
large predators are well documented (Frank et al., 2005; Casini In coastal environments, small pelagic fish play a fundamental
et al., 2009; Baum and Worm, 2009), and the bottom –up effect role in the benthic –pelagic coupling since they link plankton pro-
that fluctuations in mid-trophic fish can exert in the top predator duction and demersal predators (Palomera et al., 2007). Anchovy
guilds has also been proven (Frederiksen et al., 2006; Luczak et al., species are recognized keystone species in upwelling regions
2011). However, most foodweb studies obviate the dynamism of (Libralato et al., 2006) and in highly productive temperate seas

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Is juvenile anchovy a feeding resource for demersal predators? 1395

(Somarakis and Nikolioudakis, 2007). Their key role is achieved Methods

through their importance as a food resource for a great variety Data sources
of organisms, from seabirds (Okes et al., 2009; Luczak et al.,
Bottom trawl surveys for the assessment of demersal and benthic
2011) to large pelagic fish (Lezama-Ochoa et al., 2010), demersal
stocks (“Demersales” surveys) were conducted every autumn
fish (Preciado et al., 2008; Byron and Link, 2010), and jellyfish
from mid- September to October between 1990 and 2010 on
(Sabates et al., 2010), which feed on different anchovy life stages.
soft bottoms of the Cantabrian Sea continental shelf, between 1
In the Bay of Biscay, the European anchovy (Engraulis encrasi-
and 98W (Figure 1). Trawling operations were carried out
colus) not only plays an important role as a forage fish in structur-
during the daytime using a “Baka” 44/60 net with 20 mm mesh
ing the ecosystem, but also constitutes an important fishery
in the codend. The tows lasted for ca. 30 min at a constant

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resource. Recent years have seen fluctuations of the stock,
speed of 3 knots. The survey design followed a stratified random
related to both changes in environmental variables and fishing
sampling scheme covering the depth range 70 –500 m. For this
pressure (Borja et al., 2008). The anchovy fishery remained
work, we focused on the depth strata 70 –120 m and 120–
closed between 2006 and 2009 due to the low biomass level and
200 m, where anchovies are normally found. A few special tows
the failure of the fishery (ICES, 2010). However, there is high vari-
were also performed at shallower depths (,70 m) and considered
ability in the annual anchovy stock biomass due to natural recruit-
in this study. After each haul, the catch was separated into species.
ment variability (Uriarte et al., 1996).
Anchovy specimens were measured (total length to the lower
The distribution of European anchovy in the Bay of Biscay
centimetre), and the total weight of the anchovy catch was
spans from shelf to oceanic areas. The southern part of the Bay
recorded. From each potential predator species, a maximum of
is characterized by a narrow continental shelf and marked environ-
ten specimens were randomly selected from each haul and set
mental gradients. It has been suggested that the complex oceanog-
aside for extended biological sampling. The sampling effort was
raphy of the region favours anchovy recruitment success through a
higher for Merluccius merluccius, Lepidorhombus whiffiagonis,
spatial loophole, where early stages are advected off the shelf, thus
and L. boscii, from which a maximum of ten individuals per size
avoiding high predation pressure, while juveniles return to the
category were sampled (categories comprised size ranges of 5 cm).
shelf during autumn, withstanding countercurrents, once they
As part of the extended biological sampling, quantitative diet
have achieved a sufficient size (Uriarte et al., 2001; Irigoien
estimates were obtained by measuring the stomach contents
et al., 2007). During this cross-shelf migration, young-of-the-year
using a trophometer (Olaso, 1990), which consists of a set of grad-
anchovy might be exposed to demersal predators living on the
uated half-cylinders of different diameters for measuring the
continental shelf. The degree to which juvenile anchovy contribute
volume of the stomach pellet. For each stomach, prey were sepa-
to the diet of the demersal fish community in the Bay of Biscay is,
rated, identified to the lowest taxonomic level, and measured (to
however, still unclear (Olaso, 1990; Velasco and Olaso, 1998;
the lower millimetre) whenever possible. In the case of partly-
Preciado et al., 2008).
digested prey, hard structures, such as exoskeletons for crusta-
In this study, we focus on young-of-the-year European anchovy
ceans, or otoliths for fish, were used for identification; however,
in the southern Bay of Biscay (Cantabrian Sea) aiming to deter-
some specimens had to be grouped as unidentified fish (UNID
mine their role as forage fish for the demersal fish community,
,10% of the total prey). The volume percentage occupied by
and whether the strong anchovy fluctuations in recent decades
each prey item in the total stomach content volume was visually
have had an effect on the diet of demersal predators. To this
estimated. All dissections and identification of stomach contents
end, we investigate the relationship between anchovy abundance
were carried out on board. Fresh prey or any items presumably
and its availability to the demersal community, hypothesizing on
consumed in the net were excluded from the analysis.
possible factors affecting this relationship.

Figure 1. Location of the study site. The locations of bottom trawls are marked with crosses (“Demersales” survey), while the vertical lines
indicate the position of the acoustic transects (“Pelacus10” surveys).
1396 L. López-López et al.

The one-year-old anchovy abundance and recruitment series relative abundance was lower than 0.01% in all years or which oc-
were obtained from the analytical assessment of the total stock curred only during one year were eliminated. The number of
(anchovy of the Bay of Biscay) for the period 1991–2011 (ICES, dimensions of the prey assemblage was further reduced by apply-
2011). Additionally, acoustic surveys were carried out on board ing a principal component analysis, from which only the two first
R/V “Thalassa” in the Bay of Biscay (between 58W and 28W) components were retained. Species contributing more than 0.05
every autumn (September–October) between 2006 and 2009 (in absolute values) to the loadings were identified as the main
to estimate the biomass of small pelagic fish, with anchovy drivers of diet variability.
(young-of-the-year plus adults) as the target species A total fullness index was computed for Lepidorhombus whiffia-
(“Pelacus10” surveys). Acoustic transects were run perpendicular gonis and Merluccius merluccius to investigate the possible effect of

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to the coast between 30 and 2000 m depth, with an intertransect anchovy consumption. This fullness index was calculated using the
distance of 15 nautical miles. Pelagic trawls were conducted in following formula:
those areas where singular echotraces were recorded using a
“Pelágico” 72/76 net with 20 mm mesh in the codend. These  Vj
fishing operations aimed to identify the species composition and Wj
size structure of the observed shoals in order to divide the recorded FI = (1)
N
acoustic energy for the biomass assessment of the pelagic fish com-
munity. The catch was sorted by species, weighed, and all speci- where Vj represents the volume of the stomach pellet of the preda-
mens were measured to the lower 0.5 cm (total length). tor j and Wj the weight of the predator j. The number of predators
Age–length keys estimated from these surveys (Demersales and with food in their stomach in a given year is represented by N. This
Pelacus10) were applied to anchovy length distributions and index was calculated annually for all ontogenetic groups of the pre-
stomach contents to obtain age distributions (data not shown). dators in which anchovy constituted one of the main food
Similar information to Pelacus10 for autumn (September) of resources, in order to account for differences in diet. Pearson’s cor-
2003–2005 and 2010 was obtained from the reports of the acoustic relation was used to investigate the relationship between the full-
Juvena surveys, which aimed to estimate the biomass of anchovy ness indexes of the main anchovy predators in the historical series.
(young-of-the-year plus adults) (Boyra et al., 2005, 2006, 2007, The relationship between consumed anchovy and the abun-
2008). dance of anchovy juveniles was assessed using the total abundance
of spring recruits in the Bay of Biscay, the abundance of juveniles
Statistical analysis estimated from the bottom trawls, and the anchovy consumption
We determined the number of anchovy consumed per predator by the demersal community. We also computed, using the Pearson
and year to obtain a clear picture of the changes in anchovy con- correlation test, the relationship between anchovy in the diet of de-
sumed during the study period (1990–2010). Differences in the mersal predators and the abundance of anchovy in hauls at each
size of consumed anchovy between piscivorous predators and pre- sampling station from the bottom trawl survey.
dators with a crustacean-based diet were assessed using a Kruskal As anchovy in the southern Bay of Biscay show high abundance
Wallis test. To identify changes in the predation on anchovy during variability along a zonal gradient in the Cantabrian Sea (Uriarte
the predators’ lifespans, we used predator size ranges from the lit- et al., 2001), we analysed the interannual variation and the accu-
erature (Velasco, 2007) and ontogenetic dietary shifts previously mulated frequency of anchovy consumption for the entire study
determined by clustering predator lengths based on their diet. period along this zonal gradient. Since the size of juvenile
Preliminary analysis showed that predator diet was not density- anchovy could influence its availability as prey for the demersal
dependent, specifically regarding predation on anchovy, and community, we computed the zonal differences in the size of ju-
thus we did not account for predator density in our analyses. venile anchovy using data from the acoustic surveys (2003–
The size distribution of the items in the diet was calculated per 2010), the demersal trawling (1990– 2010), and the fish diet ana-
predator and ontogenetic group in order to compare it with the lysis (1990– 2010) along the zonal gradient in the Cantabrian Sea.
size of anchovy juveniles. Using the first and third quartiles of All statistical analysis was performed with the software R for
the anchovy size distribution, we identified those prey items mathematical and statistical computing R 2.13.2 (R Development
with similar size that could occupy the same trophic guild as Core Team, 2011).
anchovy, and thus act as anchovy surrogates. The habitats for
these species were extracted from the online databases Results
SeaLifeBase (SeaLifeBase, 2011) and FishBase (FishBase, 2011), A total of 26 fish and elasmobranch predators consumed anchovy
while their maximum recorded lengths were obtained from the either frequently or occasionally during the study period
bottom trawl “Demersales” surveys database. (Figure 2). Nevertheless, its importance as a food resource for de-
To assess the role of anchovy in triggering shifts in the predator mersal predators showed remarkable annual variability, with high
diets, years were classified by their prey assemblage for the species consumption in 1991–1992, 1996– 1998, and 2000, and excep-
with a higher consumption of anchovy (Lepidorhombus whiffiago- tionally high consumption in 2010. The proportion of predators
nis and Merluccius merluccius). As prey volume is highly depend- that consumed anchovy also increased during these periods.
ent on predator size, we standardized the volume of each prey Hake (Merluccius merluccius) and megrim (Lepidorhombus whif-
species by predator weight (partial fullness index), thus eliminat- fiagonis) consumed the highest number of anchovy (Figure 2).
ing the overrepresentation of the larger fish diet in the prey matrix. Anchovy consumption in the diet of these two main predators
Subsequently, this standardized volume was annually averaged by took place across ontogenetic categories, with the exception of ju-
the number of predators (with no zero repletion), to eliminate the venile megrim (,16 cm in length) that did not consume anchovy.
effect of annual differences in predator abundance. In order to The relative importance of juvenile anchovy in hake juveniles
eliminate noise in the prey matrix, those prey species whose (,18 cm), medium hake (18– 35 cm), and large hake (.35 cm)
Is juvenile anchovy a feeding resource for demersal predators? 1397

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Figure 2. Annual and decadal consumption of anchovy (number of specimens) by demersal predators.

than the average size of other prey items (Figure 3). Only the
group of large megrim adults (≥35 cm) consumed other prey
items in a size range similar to the size range of anchovy juveniles.
On the other hand, hake juveniles (,18 cm) generally consumed
prey smaller than anchovy, while in the two categories of larger
hake (≥18 cm), anchovy juveniles taken as prey were generally
smaller than other prey items consumed (Figure 3). On expanding
this size analysis to the entire predator community, piscivorous
predators (i.e. M. merluccius, L. whiffiagonis, Zeus faber) consumed
larger anchovy juveniles than the predators that generally fed on crus-
taceans (i.e. Lepidorhombus boscii, Raja montagui, Chelidonichthys
Figure 3. Size distribution of all prey items consumed by the cuculus), with an average difference of 5 cm (d.f. ¼ 159.212;
different ontogenetic groups of the main anchovy predators p , 0.01).
(Lepidorhombus whiffiagonis and Merluccius merluccius). The size of Only a limited number of prey in the demersal community had
the young-of-the-year anchovy preyed upon is represented as a grey a size range overlapping the size range of anchovy juveniles,
band in the background of the plots; the light grey band indicates making them a suitable substitute in the absence of anchovy.
the total range of the consumed anchovy size, and the dark grey They consisted mostly of small demersal fish, such as Argentina
indicates the area between the first and third quartiles in this sphyraena, Callionymus spp., Gaidropsaurus macrophthalmus, and
anchovy size distribution. small pelagic fish, such as Gadiculus argenteus or small Trachurus
trachurus. The size distribution of the largest demersal shrimp,
was 34.15, 7.49, and 21.03%, respectively. In the case of megrim, such as Solenocera membranacea or Chlorotocus crassicornis, also
the importance of anchovy in the different ontogenetic categories overlapped with the size of anchovy juveniles. Most of the fish
was 15.88 (16 –23 cm), 30.57 (24–36 cm), and 34.00% (.36 cm). species which were also consumed by demersal predators in the
The volumetric importance of juvenile anchovy in the diet of these size range 7.5 –8.9 cm were small individuals of the prey species,
species ranged annually between 0 and 15% in hake and between 0 as their maximum length was generally much larger (FishBase,
and 31% in megrim. 2011; SeaLifeBase, 2011; F. Velasco, pers. comm.).
Regardless of the predator, the bulk of anchovy consumption The PCA analysis identified the main prey species responsible
(.75%) was found to occur between sunrise (approximately for the variability in the predator diets during the study period
06:00 UTC) and 08:00 UTC independently of the digestion state, (Figure 4). The first PCA of the Lepidorhombus whiffiagonis diet,
pointing to a time-constrained consumption of anchovy, preferen- which explained 88.0% of the diet variability, was almost uniquely
tially during night and early morning. driven by the euphausiid Meganyctiphanes norvegica, and the
The size of anchovy preyed upon in this study corresponded to second PCA (11.2% of the variability) by blue whiting. Although
age 0, as identified with the age –length keys. Its size distribution these two prey items controlled the variability in the L. whiffiagonis
ranged between 2.0 and 15.0 cm, with the first and third quartiles diet, anchovy was the third prey item in order of importance
of the distribution being 7.5 and 8.9 cm, respectively. Comparing (Figure 4). In the diet of Merluccius merluccius, the number of con-
the size of the anchovy juveniles with the size of other items in the tributors to the diet variability was much higher, and anchovy was
predator diets, clear differences between hake and megrim arose. well represented in both the first and the second PCA (explaining
In the case of megrim, the size of anchovy juveniles was larger 55.4 and 14.6%, respectively, of the diet variability), occupying the
1398 L. López-López et al.

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Figure 4. Prey species with the highest contribution (loadings .0.05) to the diet variability of Lepidorhombus whiffiagonis as resulting from
the first component (a) and second component (b) of the principal component analysis of the species diet. Similarly, prey species which
contribute to the diet variability of Merluccius merluccius as resulting from the first (c) and second (d) components of the principal
component analysis of the species diet.

Figure 6. (a) Estimated abundance of anchovy recruits in the Bay of

Figure 5. Average annual fullness index of the ontogenetic groups of Biscay, and (b) abundance of anchovy juveniles in the Bay of Biscay
Lepidorhombus whiffiagonis and Merluccius merluccius which prey on estimated in biomass by demersal trawls (points) and number of
juvenile anchovy. The standard error of the mean is represented by a anchovy juveniles found as part of the diet of demersal predators
grey bar behind each individual value. (solid line).

second position in both components after Micromesistius poutaus- third group of megrim, a similar pattern occurred (r ¼ 0.69,
sou and Gadiculus argenteus, respectively. p , 0.01). The time-series of fullness index of the smaller size
The fullness index of M. merluccius and L. whiffiagonis showed classes were, however, not significantly correlated. In the smaller
high variability during the study period (Figure 5), ranging from 3 size classes, positive peaks occurred in 1991, 2000, and 2010
to 16%. Although trends during the two decades could not be (Figure 5), suggesting opposite trends between the fullness of
recognized, there was a remarkable resemblance in the variability large and small predators in years of high anchovy consumption.
of the fullness index between the largest ontogenetic group of The occurrence of anchovy in predator diets conforms to its
megrim and of hake (Figure 5). High correlations were found abundance in bottom trawl hauls (Pearson correlation ¼ 0.66;
between the annual fullness index of the last ontogenetic group p ¼ 0.002), except in 2000 and 2006 when abundance of
in hake and megrim (r ¼ 0.96; p , 0.01). In these two groups, anchovy in the hauls was remarkably high in comparison to its
anchovy consumption seems to have coincided with periods presence in the diet of the demersal fish community (Figure 6).
when the fullness index decreased, such as in 1991, 2000, and For each sampling station, there was, however, no significant rela-
2010 (Figure 5). Between the second group of hake and the tionship between anchovies consumed and anchovies trawled
Is juvenile anchovy a feeding resource for demersal predators? 1399

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Figure 8. Spatial differences in size of anchovy juveniles in the
Cantabrian Sea estimated from pelagic hauls (black line), bottom
trawls (light grey line), and anchovy prey found during the stomach
content determination of demersal predators (dark grey line). The
thin lines correspond to average values for a particular location,
while the thick lines correspond to a lower pass filter applied to the
previous in order to identify the general tendency.

anchovy is recognized as an important food resource for hake

throughout European basins (Bozzano et al., 1997; Carpentieri
et al., 2005; Mahe et al., 2007). Our study shows the importance
of juvenile anchovy as a food resource for hake in the southern
Bay of Biscay. In the Celtic Sea and the northern Bay of Biscay,
Figure 7. Frequency of occurrence of anchovy juveniles in the diet hake preferentially consumed conspecifics and small clupeid fish,
of demersal predators integrated over the 21 years of study on the such as Engraulis encrasicolus, Sardina pilchardus, and Argentina
Cantabrian shelf (between 9 and 18W) (upper panel). Interannual sphyraena, while selecting negatively Trachurus trachurus and
variation of the frequency in anchovy predation on the Cantabrian Micromesistius poutassou, despite their high occurrence in the en-
shelf (lower panel). The greyscale of the points reflects the number of vironment (Mahe et al., 2007). A preference for anchovy over
anchovy found as prey in a particular location and year. other suitable prey species could stem from the higher energy
content that clupeids have relative to gadoids, as suggested by
(r 2 ¼ 0.001). Although the peaks in recruitment were related to Pinnegar et al. (2003). However, some other factors should not
increased consumption of anchovy juveniles in the previous be overlooked; for instance, the abundance of clupeid fishes
year, as happened in 1991–1992, 2000–2001, and 2010–2011 might be underestimated when sampling with a bottom trawl
(Figure 6), the general resemblance between anchovy consump- net due to their primarily pelagic life style (Preciado et al.,
tion and Bay of Biscay recruits from the analytical assessment 2008). In addition, size is an important variable characterizing
(one-year-old anchovy the following year) was low (Figure 6). predator diets (Preciado et al., 2008), as our study also shows.
This suggests that factors other than anchovy abundance might Seasonal cycles can also exist for consumption. Different size
be controlling anchovy consumption by demersal predators. groups of hake change their preferences toward anchovy seasonal-
Anchovy consumption varied longitudinally in the Cantabrian ly. Large hake feed on anchovy during spring, while during
Sea, with two relative maxima at ca. 5 and 28W (Figure 7). The autumn, both small and large hake have a significant proportion
major contribution to these maxima corresponded mainly to of anchovy in their diets (Olaso, 1990; Bozzano et al., 1997).
anchovy consumed during the last three years of the series Anchovy, therefore, might not have the same significance for the
(2008– 2010) (Figure 7). During the study period, anchovy con- demersal community diet during the entire year. In early
sumption was noted preferentially between 2 and 78W, although autumn, the particular size of anchovy juveniles allows other de-
important interannual variability occurred (Figure 6). mersal predators, such as megrim and blue whiting, to consume
Comparison of the size of anchovy juveniles in the Cantabrian Sea it. However, in spring, anchovy might have already achieved a
highlighted the significant differences between sampling methods size too large to be eaten by megrim, blue whiting, or small
and focus of the surveys used (i.e. bottom trawl vs. acoustic hake. In the central Mediterranean Sea, anchovy was found in
surveys). Although there was relatively high variability among the diets of hake ranging in length from 11 to 90 cm, attaining
fishing locations for a given sampling method, the general trend greater relevance in the diet of 11 –15.9 cm hake (Carpentieri
was that the largest anchovies were caught with bottom trawl, and et al., 2005). This suggests that some of the anchovies consumed
that anchovies found in the demersal predator diets were generally consisted of young-of-the-year individuals.
smaller. However, juvenile anchovies sampled in the pelagic surveys Some other studies on the diet of European hake have not iden-
were still smaller than those sampled by the other two methods tified anchovy as an important food item (Velasco and Olaso,
(Figure 8). 1998; Cartes et al., 2004). Nevertheless, these studies were based
on a different approach, with intensive sampling effort during
Discussion shorter time-periods. Due to the high variability both in
Anchovy species account for a substantial portion of the diet of de- anchovy abundance and anchovy consumption, it is perfectly feas-
mersal predators (Byron and Link, 2010). Specifically, European ible that anchovy did not occur during a particular year in
1400 L. López-López et al.

predator diets, notwithstanding their importance as a food re- can affect the relationship. In our study, several predators with
source when considering longer time-periods. Cartes et al. benthic and benthic –demersal diets (such as the four-spotted
(2004) did not find anchovy in the diet of hake during late megrim, Lepidorhombus boscii) consumed anchovy with a relative-
spring, when sardine was an important prey item instead. As ly high frequency during the study period. This suggests that ju-
sardine and anchovy have temporally segregated spawning venile anchovy can get sufficiently close to the bottom to
periods in the Gulf of Lion (Olivar et al., 2001), the consumption become suitable prey for these predators. Uriarte et al. (2001)
of sardine in late spring could respond to a size constraint, and be studied juvenile anchovy aggregations during 1998 and 1999 and
replaced by anchovy consumption later in the year. found the majority of the shoals to be in the upper 25 m of the
Regarding megrim, the second-most important predator of water column, mainly associated with less saline water off the

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anchovy in our study area, studies on its feeding ecology are shelf. Although daily vertical migration of juvenile anchovy
scarce. Santic et al. (2009) studied megrim diet in the eastern- shoals occurred to some degree, with a shallower and more dis-
central Adriatic, but did not observe any anchovy. In the persed distribution at night, they were not found under 40 m
Adriatic Sea, however, anchovy spawning sites are located in the depth in any case. Once over the continental shelf, anchovy start
northern and western continental shelves (Regner, 1996), and, displaying circadian migrations, aggregating in tight shoals close
therefore, the study site of Santic et al. (2009) was out of the mi- to the sea bottom during the day then dispersing and ascending
gration area of anchovy juveniles. In our study site, megrim fed ex- towards the surface at night. Massé et al. (1996) showed significant
clusively on suprabenthic and demersal prey, except anchovy. This percentages of anchovy in shoals that were ,10 m from the
suggests that megrim are not highly mobile in the water column. bottom during 1989–1994. The dispersion at night could increase
Similarities concerning the fullness index of hake and megrim anchovy vulnerability to predation (Hoare et al., 2000 and refer-
did not stem directly from their predation on anchovy, but pos- ences therein), concurring with the higher anchovy consumption
sibly were influenced by other common prey, such as blue we found in early morning. However, interannual variability in
whiting and other small demersal and pelagic fish. The role of the vertical position of the shoals could also be a factor limiting
anchovy in the diet differed for large and small predators. Years anchovy availability to demersal predators. Variability in the
with strong anchovy consumption seemed to decrease the depth of the shoals could depend on the size of the aggregations
stomach fullness of large hake (whose prey are generally larger and also on climate conditions, as they define the seasonal thermo-
than juvenile anchovy), while increasing the fullness in small cline (Muiño et al., 2003). In the southern Bay of Biscay, there is
megrim and hake (which generally prey on smaller items). high interannual variability in the upwelling index (Alvarez
However, we cannot rule out the importance of other major et al., 2011), which causes differential distribution of temperature
prey (such as blue whiting) in driving the variability in the preda- in the water column. The upwelling intensity in the southern Bay
tor fullness indices. of Biscay has been suggested as affecting anchovy recruitment
Several factors support the importance of anchovy juveniles as a success (Borja et al., 2008), and could also be one of the factors
food resource for demersal predators, among which we can high- affecting the depth positioning of E. encrasicolus juvenile shoals.
light their suitable size, high energy content in comparison with We found significant differences between the size of juvenile
other small fish (Spitz et al., 2010), and short reaction distance anchovy obtained from the acoustic surveys, bottom trawling,
in the presence of a predator (Scharf et al., 2003). The latter char- and stomach content determination. The acoustic surveys re-
acterizes clupeid fish, which allow predators to get close before ini- turned a lower size for juvenile anchovy than the other two
tiating an escape response (Scharf et al., 2003). As predators tend methods; however, while bottom trawling and thus diet determi-
to target the largest fish they can handle (Pinnegar et al., 2003), the nations took place strictly on the shelf, the acoustic transects
low reaction distance of anchovy could favour its consumption by extended to the continental slope. We cannot rule out the possibil-
predators that generally prey on smaller items. Nevertheless, selec- ity that the size differences stem from this spatial mismatch, since
tion by predators might rely on physiological traits other than size. acoustic estimates corresponded mainly to the outer edge of the
Takasuka et al. (2007) showed that some predators specifically continental shelf (data not shown), and thus to anchovies that
target slow-growing larvae independently of their actual size. had just started their cross-shelf migration from the oceanic area
Slow-growing individuals might have lower potential for antipre- and outer shelf to the inner shelf. Differences in size were,
dator behaviour and might be isolated from the shoals due to their however, exceptional between anchovies preyed upon and those
poorer condition, thus increasing the risk of predation. Larger caught with the bottom trawl. While anchovies in the hauls were
individuals would also have better swimming condition and a close to the 10-cm size reported by Uriarte et al. (2001) as the
faster response in the presence of a predator. size at which juvenile anchovies would start their cross-shelf mi-
Our study demonstrated that not only did piscivorous fish gration, the size of the prey was smaller. Size-selective mortality
benefit from juvenile anchovy, but also fish that generally fed on can be due to different constraints, such as mouth gape-size limi-
crustaceans. The fact that anchovy consumption simultaneously tation, behavioural selection, or reduced escape capability of
increased during certain years by predators with different diets smaller prey (Sogard, 1997). In addition, smaller individuals
speaks against considering anchovy as a substitute in times of within a shoal might experience stronger foraging competition
shortage of other prey, and points to a higher availability of due to their higher metabolic requirements and lower competing
anchovy to the demersal community during these years. ability, compromising at times their antipredator behaviour in
However, anchovy consumption by demersal predators did not favour of an increasing foraging prospect (reviewed in Hoare
totally comply with anchovy abundance in the southern Bay of et al., 2000).
Biscay. Prey consumption is known to be both a function of Interannual variation in juvenile anchovy size (Villamor et al.,
prey abundance and prey –predator overlap both in space and 2011) could thus condition anchovy consumption by demersal
time. In the case of pelagic species, not only the geographical predators. These size fluctuations could respond to variability in
overlap, but also the vertical positioning of predator and prey peak spawning due to water temperature (Bellier et al., 2007),
Is juvenile anchovy a feeding resource for demersal predators? 1401

upwelling intensity, or interspecific competition when there is a Bellier, E., Planque, B., and Petitgas, P. 2007. Historical fluctuations in
high abundance of juvenile anchovies. In addition to annual fluc- spawning location of anchovy (Engraulis encrasicolus) and sardine
tuations in size, the spatial distribution of anchovy juveniles in the (Sardina pilchardus) in the Bay of Biscay during 1967– 73 and
2000– 2004. Fisheries Oceanography, 16: 1 – 15.
Cantabrian Sea also exhibits high interannual variability (Uriarte
et al., 2001). Our results demonstrate agreement between exten- Bertrand, A., Segura, M., Gutierrez, M., and Vasquez, L. 2004. From
small scale habitat loop-holes to decadal cycles: a habitat based hy-
sion of the area in which predation on anchovy was found and
pothesis explaining fluctuation in pelagic fish populations off Peru.
total abundance of anchovy recruits the following year Fish and Fisheries, 5: 296– 316.
(recruitment). This association could reflect the spatial shrinkage Borja, A., Fontán, A., Sáenz, J., and Valencia, V. 2008. Climate, ocean-
that occurs at small population levels in pelagic fish (Bertrand ography and recruitment: the case of the Bay of Biscay anchovy

Downloaded from http://icesjms.oxfordjournals.org/ at Frankfurt University Library, Section Stadt- und Universitaetsbibliothek on May 28, 2015
et al., 2004). Thus, in years of high recruitment, the population (Engraulis encrasicolus). Fisheries Oceanography, 17: 477 – 493.
would be likely to be distributed over the entire continental shelf Boyra, G., Cotano, U., Álvarez, P., and Uriarte, A. 2005. JUVENA
in the Cantabrian Sea. SERIES. Acoustic surveys for anchovy juveniles 2003 – 2005.
Advection of larvae and cross-shelf migration of juveniles seem Working Document to Working Group on Acoustic and Egg
to be widespread in Engraulis encrasicolus in European waters. In Surveys for Sardine and Anchovy in ICES Areas VIII and IX
the Gulf of Lion, larvae are advected offshore following the low sal- (WGACEGG), Vigo, October 2005. ICES Document CM 2005/
inity plume of the River Rhone outflow and a southward track of LRC: 05.
eddies originating in the Gulf of Lion (Sabates et al., 2007). Boyra, G., Martı́nez, U., Cotano, U., Peña, M., and Uriarte, A. 2007.
Acoustic surveying of anchovy juveniles in the Bay of Biscay:
Similarly, in the northern Adriatic Sea, there is a transport of
JUVENA 2007 Survey Report (Includes an Appendix with the revi-
post-larvae offshore influenced by the outflow of the River Po sion of the series). Working Document to Working Group on
(Santojanni et al., 2006). The migration of juveniles to coastal Acoustic and Egg Surveys for Sardine and Anchovy in ICES
areas seems thus to be a common feature across anchovy spawning Areas VIII and IX (WGACEGG), Palma de Mallorca, November
sites (Agostini and Bakun, 2002), and the consumption of these 2007. ICES Document CM 2007/LRC: 16.
potential prey by demersal predators might be similarly wide- Boyra, G., Martı́nez, U., Cotano, U., and Uriarte, A. 2006. Acoustic
spread in European waters. surveying of anchovy juveniles in the Bay of Biscay: JUVENA
Interannual variability in anchovy abundance and availability 2006 Survey Report. Working Document to Working Group on
might not strongly affect predator diets, as most demersal preda- Acoustic and Egg Surveys for Sardine and Anchovy in ICES
Areas VIII and IX (WGACEGG), Lisbon, November 2006. ICES
tors have a wide trophic niche and demonstrate high adaptability
Document CM 2006/LRC: 18.
to environmental prey abundance (Scharf et al., 2000).
Boyra, G., Martinez, U., and Uriarte, A. 2008. Acoustic surveying of
Nevertheless, predation on anchovy juveniles by demersal fish anchovy juveniles in the Bay of Biscay: JUVENA 2008 Survey
contributes to the natural mortality of the species, together with Report. Working Document to Working Group on Acoustic and
predation on all anchovy life stages that is well studied in the Egg Surveys for Sardine and Anchovy in ICES Areas VIII and IX
pelagic realm (Okes et al., 2009; Lezama-Ochoa et al., 2010; (WGACEGG), Nantes, November 2008. ICES Document CM
Sabates et al., 2010; Luczak et al., 2011). 2008/LRC: 17.
Bozzano, A., Recasens, L., and Sartor, P. 1997. Diet of European hake
Merluccius merluccius (Pisces: Merluciidae) in the Western
Acknowledgements Mediterranean (Gulf of Lions). Scientia Marina, 61: 1– 8.
The authors are grateful to all the scientific staff and crew partici- Byron, C. J., and Link, J. S. 2010. Stability in the feeding ecology of
pating in the “Demersales” and “Pelacus 10” surveys, especially all four demersal fish predators in the US Northeast Shelf Large
the researchers who participated in the trophic ecology team Marine Ecosystem. Marine Ecology Progress Series, 406: 239 – 250.
during the study period. We thankfully acknowledge the work of Carpentieri, P., Colloca, F., Cardinale, M., Belluscio, A., and
Pilar Pereda, who was responsible for the Fisheries area of the Ardizzone, J. D. 2005. Feeding habits of European hake
IEO (2003 –2011) and who made possible the participation of (Merluccius merluccius) in the central Mediterranean Sea.
LL-L in the “Demersales” surveys. We thank the researchers Fisheries Bulletin US, 103: 411– 416.
involved in the development and maintenance of the online data- Cartes, J. E., Rey, J., Lloris, D., and Gil de Sola, L. 2004. Influence of
environmental variables in the feeding and diet of European hake
bases SeaLifeBase and FishBase. We are grateful to Jorge Landa
(Merluccius merluccius) on the Mediterranean Iberian coasts.
for providing guidance and information regarding megrim (L. whif- Journal of the Marine Biological Association of the UK, 84:
fiagonis) ecology, and to Sylvain Lenoir for useful comments on an 831– 835.
early version of the manuscript. Casini, M., Hjelm, J., Molinero, J. C., Lovgren, J., Cardinale, M.,
Bartolino, V., Belgrano, A., et al. 2009. Trophic cascades promote
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