trophic ecology of pomatoschistus microps within an intertidal bay...

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


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).



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.



(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.



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,



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.



trophic ecology of pomatoschistus microps within an intertidal bay...

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