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SHORT COMMUNICATION
Trophic ecology of Pomatoschistus microps within anintertidal bay (Roscoff, France), investigated through gutcontent and stable isotope analysesJean-Charles Leclerc1,2, Pascal Riera1,2, Laure M.-L. J. No€el1,2, C�edric Leroux1,3 & Ann C. Andersen1,2
1 UPMC Univ Paris 6, Station Biologique de Roscoff, Roscoff, France
2 CNRS, UMR 7144 AD2M, Station Biologique, Roscoff, France
3 CNRS, FR 2424, Station Biologique, Roscoff, France
Keywords
Gut content analyses; Pomatoschistus
microps; trophic ecology; d13C; d15N.
Correspondence
Jean-Charles Leclerc, UPMC Univ Paris 6,
Station Biologique de Roscoff, Place Georges
Teissier, F-29680 Roscoff, France.
E-mail: [email protected]
Accepted: 16 April 2013
doi: 10.1111/maec.12071
Abstract
The diet of Pomatoschistus microps has been studied using both gut content
and stable isotope analyses. In the Roscoff Aber Bay (Brittany, France), this fish
is commonly found on sandy muddy intertidal flats. Gut content analyses were
also interpreted using trophic indices. Owing to the large diversity of prey
consumed, these indices emphasised the opportunistic feeding behaviour of
P. microps. Here, this species fed mainly on endofauna with meiofauna being
of high relative importance. The main biotic components of its trophic habitat,
characterized by d13C and d15N, provided evidence of a major trophic pathway
based on drift Enteromorpha sp. Trophic positions estimated by both diet
analyses and isotopic analyses led to similar results. In this bay, P. microps is a
first-order predator with a low degree of omnivory. Despite a preferential
consumption of the amphipod Corophium arenarium, we assumed that this
goby behaves as a generalist feeding on a uniform variety of endofauna taxa.
Introduction
Owing to their complexity and productivity, intertidal
areas provide a large range of potential food sources for
fish. Many fish use these areas as nursery grounds and
they are permanent habitats for some of them. Intertidal
fish ecology is particularly studied to differentiate niches
within communities (Gibson 1972; Dolbeth et al. 2008;
Velasco et al. 2010). Among these communities, the
Gobiidae belong to the most common family and are
characteristic of both rocky and muddy shores in tropical
and temperate areas (Gibson & Yoshiyama 1999).
The common goby, Pomatoschistus microps (Krøyer),
has a wide distribution in Northern Europe and in the
Mediterranean Sea. This species is abundant in shallow
coastal soft sediments and in estuarine ecosystems
(Magnhagen & Wiederholm 1982). This fish species stays
within intertidal areas during its whole life and shows
ontogenic diet variations. The diet of young individuals
has been reported to be mainly based on meiofauna,
whereas adults’ diet relied on macrofauna (Pihl 1985;
Jackson et al. 2004). Previous studies indicated that
P. microps feeds mostly on endofauna (i.e. infauna),
whereas P. minutus (Pallas), a slightly bigger fish, con-
sume preferentially epi- and suprabenthic larger prey
(Salgado et al. 2004; Leit~ao et al. 2006). Pomatoschistus
minutus is less tolerant to variations in salinity and is
found lower down on the shore (Dolbeth et al. 2007).
Gut content analyses provide information on the
ingested diet of a consumer. In particular, identification
of the prey at the species level gives a definition of the
degree of specialisation and the main trophic pathways of
species (Gibson 1972; Harmelin-Vivien & Bouchon-
Navaro 1983; Leit~ao et al. 2006). However, identification
of the main food items cannot be based solely on the
presence or number of prey (Berg 1979). It may be more
pertinent to consider trophic indices based on quantita-
tive measurements (Godfriaux 1969). These indices allow
Marine Ecology 35 (2014) 261–270 ª 2013 Blackwell Verlag GmbH 261
Marine Ecology. ISSN 0173-9565
the main food items to be distinguished from secondary
or accidental ones. As pointed out by Berg (1979), the
subjectivity of some indices make comparisons among
studies difficult. However, integrating them in meta-indi-
ces approaches the actual nature of the diet (Pinkas et al.
1971; Cort�es 1997). Gut contents analyses cannot give a
complete picture of the whole food web structure but
contributes to the characterisation of trophic levels and
omnivory (Christensen & Pauly 1992; Pauly & Watson
2005).
Stable isotope analyses allow the determination of the
main trophic pathways and the characterisation of the
food web structure of an ecosystem (Thompson et al.
2005; Layman et al. 2007; Martinez del Rio et al. 2009).
d13C and d15N reflect sources of organic matter and tro-
phic levels, respectively (Fry & Sherr 1984; Post 2002).
This method provides a time-integrative measure of the
food sources actually assimilated, completing gut content
analyses (Cr�each et al. 1997; Carassou et al. 2008). Few
studies using gut content and stable isotope analyses have
dealt with the diet of invertebrates (Cr�each et al. 1997;
Fanelli & Cartes 2008), most of them being focused on
fish. Trophic positions estimated by both stable isotope
and gut content analyses are often well correlated and
such coupling help to characterise inter- and intraspecific
feeding behaviour (e.g. Vander Zanden et al. 1997;
Rybczynski et al. 2008).
The present study, using both gut content and stable
isotope analyses, aims to investigate the trophic status of
P. microp inhabiting an intertidal bay. Particular attention
was given to (i) the determination of the most relevant
sources for this representative fish in the bay, (ii) the
estimation of its trophic position.
Material and Methods
Sampling site
The Roscoff Aber Bay (1 km long and 2 km wide) pre-
sents a tidal estuarine regime, and is located above the
mid-tide level (Fig. 1). Particularly sheltered, the Aber
Bay is dominated by sandy-muddy sediments, with local
freshwater inputs from the river located at the landward
end of the bay and with freshwater seepages. The Aber
Bay invertebrate communities have been investigated
previously by Rullier (1959) and more recently by Hubas
(2006). The sampling site (48°42.821′ N; 4°00.050′ W) is
located along the river on sandy-muddy sediments. The
main primary producers are benthic microalgae, macroal-
gae such as Fucus spiralis, and ephemeral Ulva spp.
(including the former genus Enteromorpha) presenting
remarkable summer blooms, which can affect trophic
web structure and functioning (Hubas & Davoult 2006;
Ouisse et al. 2011). In this area, the seasonal trophic
importance of benthic diatoms and cyanobacteria has
already been highlighted (Riera & Hubas 2003; Riera
2010). Macrofauna is dominated by the amphipod
Corophium arenarium, the bivalve Abra tenuis, the gastro-
pod Hydrobia ulvae and the annelids Nereis diversicolor,
Scoloplos armiger, Notomastus latericeus and Scolelepis
squamata (Hubas 2006). Some of these species capable of
osmoregulation, such as Nereis diversicolor, are locally
abundant due to the presence of freshwater seepages. The
common goby Pomatoschistus microps, and the shrimps
Palaemon elegans and Crangon crangon are found in the
river at low tide. Mysids, mostly Paramysis arenosa, are
abundant in the river but are also found in sandy pools
at low tide. In areas without freshwater input, the bivalve
Cerastoderma edule and the annelid Arenicola marina
contribute heavily to the biomass. Meiofauna is domi-
nated by nematodes which can reach more than 500 indi-
viduals cm�3. Similar densities can be found seasonally
for harpacticoid copepods (Riera & Hubas 2003).
Gut contents analyses and trophic indices
Gut content samplings were performed in September
2008 and November 2009. Individuals of Pomatoschistus
microps were fished at low tide using a landing net
(n = 8 in 2008 and n = 10 in 2009). Individuals of a
given standard body length were selected (19.9–34.6 mm). Fish were anaesthetised with 2-phenoxy-etha-
nol (1%), fixed in a formaldehyde solution (3%) for
3 days and then preserved in ethanol solution (70%).
Their guts were then dissected. The prey encountered
were identified to the lowest possible taxonomic level,
Fig. 1. Localisation of the study site (star) within the Roscoff Aber
Bay.
262 Marine Ecology 35 (2014) 261–270 ª 2013 Blackwell Verlag GmbH
Trophic ecology of Pomatoschistus microps Leclerc, Riera, No€el, Leroux & Andersen
using a binocular stereozoom microscope. Most of the
crustaceans were identified to the species or the genus
level. Calcified parts, such as radulas, helped in gastropod
determination. Annelid families were identified by setae
combination. Meiofauna were considered according to
their large taxonomic groups.
Three elementary indices were used to analyse the gut
contents (Godfriaux 1969). First, the occurrence fre-
quency (%O) was calculated from the number of fish
containing a prey item, excluding empty guts. This quali-
tative approach based on presence/absence gave informa-
tion on the fish feeding behaviour. Secondly, the
numerical frequency (%N) recorded the relative quantity
of a prey in the whole diet. However, this index overesti-
mated small prey, which are generally more numerous.
Diatoms and algal fragments were not counted, but their
presence and relative abundance were recorded. Finally,
the volumetric frequency (%V) is considered the most
representative of the diet (Hyslop 1980). Due to the fish
prey of small size, volumes were estimated from the rela-
tive geometry of each prey item, often cylindrical. For
that purpose, length, width and diameter were measured
using an ocular micrometer with a precision of 10 lm.
The dietary coefficient (Q’) using volumetric frequency
was calculated as a substitute for Hureau’s Q, adapted by
Salgado et al. (2004), which usually uses both numerical
and gravimetric frequencies.
Q0 ¼ %V�%N
Prey were then separated into three clusters: preferential
(Q’ > 200), secondary (200 > Q’ > 20) and accidental (Q′< 20).
IRI, the index of relative importance (Pinkas et al.
1971), was calculated as follow:
IRI ¼ ð%Nþ%VÞ �%O
Taking into account the occurrence, this index gives fur-
ther information on the feeding behaviour of the popula-
tion. IRI was presented as a percentage (Cort�es 1997).%,
%V and %O were represented on radar histograms
(Dolbeth et al. 2008).
Stable isotope analyses of carbon and nitrogen
The most representative sources and consumers in the
sampling location were collected at low tide during
November 2009 for stable isotope analyses. At the river
entrance, two replicates of fresh water (2 l) were collected
to estimate the river particulate organic matter (river
POM). Two replicates of seawater (5 l) were collected off-
shore to assess the marine POM which approximates the
signature of the phytoplankton entering the bay. Back
in the laboratory, water samples were filtered through
pre-combusted (6 h, 550 °C) Whatman GF/F 0.7 lm fil-
ters. Each filter was then acidified rapidlly with HCl (1 N)
to remove carbonates, rinsed thoroughly with distilled
water and dried at 60 °C for 48 h. The upper centimeter
of mud was scraped to measure the isotopic ratios of the
sedimented organic matter (SOM). Samples were
freeze-dried, ground using a mortar and a pestle, and
then acidified with HCl (1 N). To prevent any loss of
dissolved organics, the samples were not rinsed. They were
dried overnight at 50 °C under a slight vacuum to
evaporate the acid. Once dried, the sediment was mixed
with distilled water, frozen, ground again to a fine
powder, and kept frozen at �80 °C until analysed (Riera
1998).
Consumers were starved in filtered seawater (through
pre-combusted GF/F) from the sampling site until their
digestive contents were evacuated completely (24 h) and
stored in glass pill boxes at �30 °C until preparation and
analyses. The isotopic analyses of fish and other consum-
ers were performed on the muscle tissues to minimize
isotopic variability (Pinnegar & Polunin 1999). Owing to
their slow metabolic turnover, the isotopic composition
of muscular tissues revealed the integrative assimilation
of sources by the consumer (De Niro & Epstein 1978,
1981; Yokoyama et al. 2005). Pomatoschistus microps indi-
viduals 19.1–32.7 mm long (standard body sized length)
were selected to take into account potential size-related
diet shifts. Each sample was acidified briefly (HCl, 1 N),
rinsed thoroughly with distilled water, and dried at 60 °Cfor 48 h. The same acid-washed treatment was applied
for all organisms to obtain an analogous effect of acidifi-
cation (Jaschinski et al. 2008). Once dried, the samples
were ground to powder with a mortar and a pestle and
stored in tin capsules before analyses. For Corophium
arenarium, Scolelepis squamata and tubificids, pool
samples were performed to obtain material in tin capsules
for stable isotope analyses.
Carbon and nitrogen isotope ratios were determined
using a Flash EA CN analyser coupled with a Finnigan
Delta Plus mass spectrometer, via a Finnigan Con-Flo III
interface. Data were conventionally expressed in the
standard d unit.
dX ¼ ðRsample=RreferencesÞ � 1� �� 103
where R = 13C/12C for carbon and 15N/14N for nitrogen.
These abundances were calculated in relation to the certi-
fied reference materials Vienna Pee Dee Belemnite-
limestone (V-PDB) and dinitrogen (at-air). The V-PDB
and at-air scales were achieved using in-house protein
standards, calibrated against NBS-19 and IAEA N3
reference materials. The standard deviation of repeated
Marine Ecology 35 (2014) 261–270 ª 2013 Blackwell Verlag GmbH 263
Leclerc, Riera, No€el, Leroux & Andersen Trophic ecology of Pomatoschistus microps
measurements of d13C and d15N values of a laboratory
standard was 0.10& versus V-PDB and 0.05& versus
at-air, respectively.
Stable isotopic discrimination among producer and
consumer species was achieved using non-parametric
Kruskal–Wallis tests owing to the absence of homoscedas-
ticity of the data (Fisher tests).
Estimation of trophic positions from gut content and
isotopic analyses
The dietary composition of Pomatoschistus microps was
used to estimate the trophic level gut content analyses
(TLGCA) and the omnivory index (OI) using the follow-
ing formulas:
TLGCAi¼ 1þ
XTLj � DCij
OI ¼X
ðTLj � TLaverageÞ2 � DCij
These indices depend on trophic level of the prey j (TLj),
considering their contribution (DCij) to the diet of the
fish i. DCij was expressed as the volumetric frequency (%
V) calculated previously. As the omnivory index expresses
the uncertainty of the TLGCA, the squared root of OI
becomes a proxy of its standard error (Pauly & Watson
2005). These estimations can be complemented using sta-
ble isotope analyses (Kline & Pauly 1998).
Theoretical isotopic fractionations of 3.4& for d15Nand of 1& for d13C were usually reported between pri-
mary and secondary consumers (Post 2002). The trophic
position of predators can be estimated from the 15N
enrichment between trophic levels, taking the average
d15N of strict primary consumers as a baseline (Cabana &
Rasmussen 1996; Vander Zanden & Rasmussen 2001). In
the present study, the baseline was represented by Param-
ysis arenosa, Praunus fexuosus, Cerastoderma edule, Abra
tenuis and Hydrobia ulvae. In the case of osteichthyan
fish, studies based on the extensive literature and 15N and13C enrichment experiments reported fractionation coeffi-
cients of 3.2& and 1.5& for d15N and d13C, respectively(Sweeting et al. 2007a,b). These coefficients appeared
more relevant for trophic level estimation of fish, and
have been used in the present study. The trophic level
stable isotope analyses (TLSIA) has been calculated as
follow:
TLSIA ¼ 2þ ðd15Npredator � d15NbaselineÞ3:2
The intraspecific variability of d15N can also give clues as
to the degree of omnivory (France 1997; Sweeting et al.
2005).
Results
Gut contents analyses
The radar histograms of the gut content (Fig. 2) indicated
similar dietary trends in both years. There was a high
occurrence and number of meiofaunal organisms in guts
(especially copepods), highlighting the volumetric domi-
nance of amphipods and annelids in both years. The
amphipod Corophium arenarium was the preferenrred prey
of the common goby (Table 1), as it corresponded to
55.9% and 62.6% of the total volume of prey in 2008 and
2009, respectively. In those years, the dietary coefficients
(Q’) of C. arenarium ranged between 520.7 and 751.6, and
their index of relative importance (IRI) ranged from
35.2% and 44.3%. Annelids contributed 30.0–36.3 %V,
with total Q’ of 120.4–174.7 and IRI of 15.1–17.0%. Two
Fig. 2. Radar histograms of Pomatoschistus microps gut contents in
September 2008 (n = 8) and November 2009 (n = 10). Percentages
of taxonomic groups are presented with numerical (%N, dark grey
diamonds), volumetric (%V, light grey squares), occurrence (%O,
black triangles).
264 Marine Ecology 35 (2014) 261–270 ª 2013 Blackwell Verlag GmbH
Trophic ecology of Pomatoschistus microps Leclerc, Riera, No€el, Leroux & Andersen
families of annelids were found in the gut content both
years, capitellids and sabellids. Only capitellids were
indexed as secondary prey by Q’. Meiofaunal specimens
did not reach high Q’ because of their small volumes.
Their relative importance was nevertheless, representative,
especially of the copepods (IRI 27.9% and 40.1% in 2008
and 2009) and ostracods (IRI 8.2% in 2008). Moreover,
copepods were indexed as secondary prey, as their Q’
values were between 27.5 and 37.1. These meiofaunal taxa
contrasted with the nematodes, which contributed only
0.2–3.3% of the IRI. Some prey were only found once dur-
ing the 2 year survey. In September 2008, chironomid lar-
vae (IRI 3.2%) and the gastropod Hydrobia ulvae (IRI
1.4%) seemed to be consumed in significant numbers. In
2009, tubificids were classified as secondary prey, having a
Q’ of 21.2. The mysid Paramysis arenosa was indexed as
accidental prey in 2009 (Q’ = 4.8).
Using volumetric frequencies of prey as a proxy of
the dietary composition, P. microps trophic levels were
3.17 � 0.42 (OI = 0.18) and 3.00 � 0.02 (OI = 4 9 104)
in 2008 and 2009, respectively.
Isotopic characterization of sources and consumers
d15N and d13C (mean � SD) of the main sources and
consumers of the Roscoff Aber Bay are presented in
Fig. 3 and in the Appendix. d13C of sources ranged from
�24.1& (river POM) to �10.9& (Ulva sp.). Most of
these sources of d13C were significantly different from the
others (Kruskal–Wallis test, H = 11.95, df = 5,
P = 0.035). Macroalgae d13C [between �15.0& (Fucus
spiralis) and �10.9& (Ulva sp.)] were more 13C-enriched
than other sources. The sources did not differ signifi-
cantly for d15N values (H = 6,77, df = 5, P = 0.238),
varying from 4.4& (marine POM) to 9.8& (SOM).
Consumers differed significantly in both d13C and d15N(Kruskal–Wallis test, H = 62.17, df = 18, P < 0.0001 and
H = 46.43, df = 18, P < 0.001, respectively). d13C of
consumers ranged from �19.1& (Palaemon varians) to
�10.9& (Paramysis arenosa), while their d15N ranged
from 5.9& (Gammarus salinus) to 17.3& (Nereis
diversicolor).
The TLSIA estimated on the basis of stable isotope
values (14.6 � 0.6 SD) was 2.90 � 0.18 in 2009.
Discussion
Characterization of Pomatoschistus microps diet by gut
content and stable isotope analyses
In the Roscoff Aber Bay, the sampled species belonged
to three trophic levels, as suggested by the d15N range
Table 1. Pomatoschistus microps gut content analyses presented as numerical (%N), volumetric (%V), occurrence (%O) frequencies, modified
Hureau’s dietary coefficient (Q′ = %N 9 %V) and index of relative importance [IRI = (%N + %V) 9 %O] percentage for the two sampling dates,
September 2008 (n = 8) and November 2009 (n = 10).
Preys September 2008 November 2009
Phylla Taxa %N %V %O Q’ %IRI %N %V %O Q’ %IRI
Annelida Total 13.7 36.3 87.5 120.4 14.3 12.0 30.0 80.0 174.7 17.0
Nephtydae 0.6 10.9 12.5 6.8 1.1
Nereidae 1.2 12.4 25.0 15.4 2.6
Capitellidae 8.1 11.4 62.5 92.4 9.5 6.0 25.5 60.0 153.3 14.9
Sabellidae 3.7 1.6 25.0 5.9 1.0 1.0 0.2 10.0 0.2 0.1
Tubificidae 5.0 4.2 50.0 21.2 3.7
Nematoda 1.2 <0.1 25.0 <0.1 0.2 10.0 0.5 40.0 4.5 3.3
Copepoda 40.4 0.7 87.5 27.5 27.9 56.0 0.7 90.0 37.1 40.1
Ostracoda 20.5 0.6 50.0 12.7 8.2 4.0 <0.1 20.0 0.1 0.6
Mysidacea Paramysis arenosa 1.0 4.8 10.0 4.8 0.5
Amphipoda Total 9.3 55.9 87.5 520.7 44.3 13.0 63.3 70.0 752.3 32.3
Corophium arenarium 9.3 55.9 87.5 520.7 44.3 12.0 62.6 60.0 751.6 32.1
Gammaridae 0.0 1.0 0.7 10.0 0.7 0.1
Arachnida Halacaridae 0.6 <0.1 12.5 <0.1 0.1
Hexapoda Chironomidae 6.8 1.3 50.0 8.8 3.2 4.0 0.7 40.0 2.8 1.5
Bivalvia 0.6 <0.1 12.5 <0.1 0.1
Gastropoda Hydrobia ulvae 3.7 5.2 25.0 19.3 1.7
Bacillariophycae + <0.1 25.0 + <0.1 0.0
Algal fragments + 0.1 37.5 + <0.1 30.0
Sediment + 100.0 + 100.0
Macrofauna prey are in bold, meiofauna in plain, (+) prey present.
Marine Ecology 35 (2014) 261–270 ª 2013 Blackwell Verlag GmbH 265
Leclerc, Riera, No€el, Leroux & Andersen Trophic ecology of Pomatoschistus microps
(Vander Zanden et al. 1997). The 13C-depleted value for
river POM suggested a negligible utilisation of this
source. In contrast, the d13C range of primary consumers
suggested that other organic matter sources (SOM, POM,
macroalgae) were exploited in their entire diversity. Po-
matoschistus microps likely relied on a preferential trophic
pathway mostly involving macroalgae that were13C-enriched compared with the other sources (Fig. 2).
Within the study site, the contribution of drift-macroal-
gae (especially Enteromopha sp.) to benthic consumers
has been highlighted already (Riera & Hubas 2003; Hubas
2006).
The revised dietary coefficients Q’ of the present study
were similar to Leit~ao et al. (2006) in Mondego estuary,
Portugal. In that estuary, amphipods Corophium spp.
were a preferential prey (Q = 507), whereas capitellids
(Q = 125) and spionids (Q = 88) were secondary prey.
However, the consistent consumption of the bivalve
Scrobicularia plana as a preferential prey (Q = 217) found
by these authors was not observed in our study. Low
consumption of bivalves in the Aber Bay could be
explained by the rarity of species with prominent siphons.
In contrast, the common goby preyed on S. plana
siphons in Mondego and Tagus estuaries (Salgado et al.
2004; Leit~ao et al. 2006). Molluscs were mostly repre-
sented in gut contents by the gastropod Hydrobia ulvae,
but these were devoid of their shells, evidencing a
capability of P. microps to remove individuals from their
shells before consumption. Although mysids are abundant
in the Aber Bay environment, P. microps foraged Paramysis
arenosa as accidental prey. However, mysids represented a
large contribution to the diet of some populations of
P. microps in other estuaries: Westerschelde (Hampel &
Cattrijsse 2004), Tagus (Salgado et al. 2004) and
Mondego (Leit~ao et al. 2006).
In the present study, meiofauna occurred in large
numbers in P. microps guts, as already reported from
Portugal to Sweden in several studies. For instance, in
western Sweden, Pihl (1985) observed that harpacticoid
copepods and ostracods dominated the digestive content
weight over a whole year. In both Aber Bay and Tagus
estuaries (Salgado et al. 2006), copepods were indexed as
secondary prey. Within the present site, although nema-
todes dominated the meiofauna with a biomass five times
higher than that of copepods (Hubas 2006) and densities
reaching 500 cm�3 (Riera & Hubas 2003), they appar-
ently only contribute only a small part of the diet. How-
ever, nematodes might be underestimated in the diet
owing to the non-selective choice of prey by P. microps.
In addition, nematodes might be quickly digested and
therefore only detectable in the pharynx.
According to the present study, P. microps feeds prefer-
entially on endobenthic fauna and thus differs from
Pomatoschistus minutus, which preferentially forages on
Fig. 3. Scatter plot of mean d13C (&) and
d15N (&) values (�SD) of the main sources of
organic matter (grey) and consumers
(numbered) within the sandy-muddy bottom
of the Roscoff Aber Bay, during November
2009. Shadowed vertical bands correspond to
trophic levels of sources (TL1) and to strict
primary consumers (TL2) and predators (TL3)
based on their feeding mode. The theoretical
food source of P. microps (dotted dark grey)
takes into account a mean trophic
enrichment of 3.2& and 1.5& for 15N and13C, respectively (see details in the text). The
dotted square illustrates the standard
deviation for d13C and d15N of P. microps,
around its theoretical source. 1. Hydrobia
ulvae, 2. Cerastoderma edule, 3. Corophium
arenarium, 4. Scoloplos armiger, 5. Praunus
flexuosus, 6. Paramysis arenosa, 7. Scolelepis
squamata, 8. Carcinus maenas, 9. Tubificids,
10. Liza aurata, 11. Palaemon elegans, 12.
Crangon crangon, 13. Arenicola marina, 14.
Abra tenuis, 15. Cyathura carinata, 16.
Palaemon varians, 17. Nereis diversicolor.
266 Marine Ecology 35 (2014) 261–270 ª 2013 Blackwell Verlag GmbH
Trophic ecology of Pomatoschistus microps Leclerc, Riera, No€el, Leroux & Andersen
epibenthic mysids and carid prawns (Salgado et al. 2004;
Leit~ao et al. 2006). Pomatoschistus minutus is commonly
found on homogeneous fine sands at high salinity, thus
lower in the estuary than P. microps, which is more
tolerant to heterogeneous substrates, variable salinity and
prefers algal mats (Dolbeth et al. 2007). The present
results appear to be in agreement with trophic niche
differences between these two Pomatoschistus species
(Salgado et al. 2004; Leit~ao et al. 2006).
Despite a preferential consumption of the amphipod
Corophium arenarium, it is difficult to consider P. microps
a specialist predator as suggested by Pasquaud et al.
(2010a), because many prey items were encountered in
the gut contents. Pomatoschistus microps has been
reported to feed on the closest mobile prey (Magnhagen
& Wiederholm 1982) and also on the biggest prey
available (Jackson et al. 2004). Corophium arenarium is
voluminous compared with other prey and is particularly
mobile as it swims and scrapes sediment during high tide.
Corophium arenarium consumption probably results not
only from selection but also from a trade-off between
availability and energetic needs, which might reflect an
opportunistic behaviour.
Trophic position and omnivory of Pomatoschistus microps
Standard deviations estimated by the omnivory index
suggested that no difference of TLGCA occurred between
2008 and 2009. The trophic levels estimated by both gut
content and stable isotope analyses placed P. microps as a
first-order predator. This result was in accordance with
Pasquaud et al. (2010b) who calculated trophic levels of
3.14 for pooled Pomatoschistus spp. from d15N(10.7 � 0.5&) in the Gironde estuary, France.
Large variability is expected in the d15N and d13C of
consumers in several scenarios (Bearhop et al. 2004). In
fact, generalist consumer diets may vary in response to
local variation of food availability or rapid ontogenic
changes. Conversely, low variability of isotopic values is
expected with either specialist or generalist consumers
exposed to a uniform food input. For instance, Nereis
diversicolor d15N variability observed in the Aber Bay
(2.2& SD) confirmed its opportunistic feeding behaviour
(Riera 1998). This could be due either to omnivory or to
consumption of the first trophic level of food sources
determined by a wide range of d15N. In the present study,
similar variability was encountered for Arenicola marina
(2.2& SD), Carcinus maenas (1.8&), and Crangon
crangon (2.4&), which are detrivorous, omnivorous and
carnivorous, respectively. Their isotopic signatures were15N-enriched, indicating that omnivory rates increased
with trophic levels (France 1997). Digestive analyses also
indicated that P. microps fed on several trophic levels
despite a preferential consumption of C. arenarium.
However, the calculated omnivory index was low, due to
the dominance of primary consumers in the diet.
Pomatoschistus microps may behave as a type A generalist
(Bearhop et al. 2004), i.e. with a uniform and constant
diet that reduces isotopic variability.
Feasible contribution of sources to the diet of Pomatoschistus
microps
According to gut content analyses, in both 2008 and 2009
the preferential prey of the common goby was Corophium
arenarium. This amphipod also displayed an isotopic
composition close to the theoretical source for the goby
(Fig. 3). Moreover, the isotopic position of the theoretical
source for P. microps was also located among the macro-
fauna signatures. This is consistent with the generalist
behaviour of a first-order predator fish. Therefore,
according to gut contents analyses, we assume that a wide
range of species characterised by different signatures
might contribute to the diet. Four other large groups
were highlighted as significantly consumed: meiofauna,
annelids, gastropods and mysids. Annelids might contrib-
ute to the P. microps signature as they account for IRI
17.0% in 2009. Paramysis arenosa and Hydrobia ulvae,
both found in gut contents and patchily abundant (Hu-
bas 2006), might contribute significantly to the isotopic
signature of the fish. These species were poorly repre-
sented in gut contents but might be consumed earlier in
the year. Indeed, some food sources may be consumed
seasonally and thus be undetected in the gut sampled at a
given time of the year. However, they could be detected
by isotope analyses which reflect food sources actually
assimilated. Hampel & Cattrijsse (2004) observed gravi-
metric frequencies of mysids reaching 60% in August in
the P. microps diet of Westerschelde estuary, and Salgado
et al. (2004) also found a maximum consumption of
mysids in summer (%N = 31.0%). Young prey recruits
were probably more vulnerable to predation during this
period than in autumn. During a monthly survey of 1 1/
2 years, Dunne (1978) observed real seasonal cycles in
the consumption of some prey categories of the rock
goby Gobius paganellus (L.) at Carna, Ireland. In that
area, gastropods were absent from the digestive contents
in November but represented 70% in June. Similar obser-
vations were made on bivalves and decapods (Dunne
1978; Salgado et al. 2004). These changes reflect the life
cycle of preys of greater density and vulnerability to
predation during periods of settlement.
Meiofaunal organisms likely contribute significantly
to the diet of P. microps as they reached IRI 44.6% in
2009. Unfortunately, we did not sample meiofauna for
stable isotope analyses in the present study. However,
Marine Ecology 35 (2014) 261–270 ª 2013 Blackwell Verlag GmbH 267
Leclerc, Riera, No€el, Leroux & Andersen Trophic ecology of Pomatoschistus microps
nematodes, the most abundant component of meiofauna
in this bay (Hubas 2006), are known to rely mostly on
drift Enteromorpha sp. (Riera & Hubas 2003). Hence, in
this bay, Enteromorpha sp. is clearly the basis of a major
trophic pathway involving meio- and macrobenthic inver-
tebrates on which P. microps relies.
In conclusion, our results demonstrate that gut content
and stable isotope analyses can be used simultaneously to
form parallel observations. Some sources can be con-
sumed without total assimilation, whereas those totally
assimilated can stay undetected in the gut content due to
their small size or their state of digestion. For instance,
the diet of the large-scale mullet, Liza macrolepis (Smith),
was identified as detrivorous by gut content analyses but
stable isotopes analyses suggested consumption of micro-
and macroalgae periphyton (Lin et al. 2007). In the pres-
ent study, similar results were observed for trophic level
estimates using both methods. This suggested that pri-
mary producers were not underestimated in our gut con-
tent analyses. In the Roscoff Aber Bay, C. arenarium is
likely to be the main food item of the common goby, as
estimated similarly by IRI, Q’ and isotopic data, but the
results also indicated the generalist feeding behaviour of
Pomatoschistus microps.
Acknowledgements
The authors thank F. Gentil and C. Broudin for helping
in prey identification. We are grateful to G. Schaal and
an anonymous reviewer for their comments, which
improved the manuscript. We would also like to thank
J. Guelinckx, who shared his PhD thesis, providing us
with a broader view on isotopic studies of goby.
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Appendix
d13C and d15N (range of values,&) of the main sources
of organic matter and consumers within the sandy-
muddy bottom of the Roscoff Aber Bay during
November 2009.
Range d15N (&) Range d13C (&) n
River POM 7.5–7.6 �24.1 to �23.6 2
Sea POM 4.4 �19.4 to �19.0 2
SOM 9.8 �18.3 1
Chlorophyceae
Enteromorpha sp. 7.2–8.9 �14.6 to �11.3 3
Ulva sp. 6.5–7.9 �12.0 to �10.9 3
1,2. Continued
Range d15N (&) Range d13C (&) n
Phaephyceae
Fucus spiralis 5.8–6.1 �15.0 to �14.4 3
Annelida
Arenicola marina 11.9–15.7 �17.6 to �15.7 4
Nereis diversicolor 12.7–17.3 �14.7 to �13.8 4
Scolelepis squamata 12.9 �16.4 to �16.3 2
Scoloplos armiger 11.8–11.9 �14.8 to �14.7 2
Tubificidae 13 �15.6 1
Mysida
Paramysis arenosa 12.2–12.9 �11.8 to �10.9 5
Praunus flexuosus 12.1–12.6 �12.3 to �11.3 3
Isopoda
Cyathura carinata 14.7–15.1 �12.1 to �11.9 2
Amphipoda
Corophium arenarium 11.0–12.1 �14.2 to �13.8 5
Gammarus salinus 5.9 �14.6 1
Caridea
Crangon crangon 11.2–16.1 �12.6 to �10.6 5
Palaemon elegans 13.4–13.8 �14.1 to �12.9 5
Palaemon varians 15.7–15.9 �19.1 to �17.3 2
Brachyura
Carcinus maenas 11.2–15.1 �14.7 to �13.3 5
Gastropoda
Hydrobia ulvae 9.2–10.2 �13.9 to �12.8 5
Bivalvia
Abra tenuis 13.8–14.3 �13.6 to �13.1 5
Cerastoderma edule 9.8–10.9 �17.7 to �17.1 3
Actinopterygii
Liza aurata 13.2–12.9 �15.9 to �14.9 3
Pomatoschistus microps 14.0–15.2 �12.4 to �11.0 5
n, number of replicates.
270 Marine Ecology 35 (2014) 261–270 ª 2013 Blackwell Verlag GmbH
Trophic ecology of Pomatoschistus microps Leclerc, Riera, No€el, Leroux & Andersen