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Benthic community and food web structure on the continental shelf of the Bay
of Biscay (North Eastern Atlantic) revealed by stable isotopes analysis

Article in Journal of Marine Systems · July 2008

DOI: 10.1016/j.jmarsys.2007.05.011

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Journal of Marine Systems 72 (2008) 17 – 34

www.elsevier.com/locate/jmarsys

Benthic community and food web structure on the continental

shelf of the Bay of Biscay (North Eastern Atlantic)
revealed by stable isotopes analysis
François Le Loc'h a,b,⁎, Christian Hily b , Jacques Grall b,c
a
UR 070 RAP, Centre de Recherche Halieutique, Institut de Recherche pour le Développement,
Avenue Jean Monnet, B.P. 171, 34203 Sète Cedex, France
b
Laboratoire des Sciences de l'Environnement Marin, UMR 6539 CNRS, Institut Universitaire Européen de la Mer,
Université de Bretagne Occidentale, Place Nicolas Copernic, 29280 Plouzané, France
c
Observatoire du Domaine Côtier, FR 2195 CNRS, Institut Universitaire Européen de la Mer, Université de Bretagne Occidentale,
Place Nicolas Copernic, 29280 Plouzané, France
Received 15 July 2006; received in revised form 12 March 2007; accepted 5 May 2007
Available online 4 December 2007

Abstract

The North Bay of Biscay continental shelf is a major French demersal fishery, but little was known on the trophic food web of
its benthic communities. In order to determine the benthic trophic web, the objectives of this study are to describe the macro- and
megafaunal benthic community structure (species richness, abundance and biomass) and to establish the trophic pathways (food
sources and trophic levels) by applying carbon and nitrogen stable isotopic analysis to the main benthic and demersal species
(invertebrates and fish). Two distinct benthic communities have been identified: a muddy sand community within the central part of
the bay, and an outer Bay of Biscay Ditrupa sand community of higher species richness, abundance and biomass than the muddy
sand community. Deposit-feeders, suspension feeders and predators, distributed in three main trophic levels, dominate both
communities. Large differences in stable carbon ratio values within the primary consumers provide evidence of two different food
sources: i) a pelagic food source made up of recent sedimenting particulate organic matter on which zooplankton and suprabenthos
feed and ii) a benthic detrital food source supplying deposit feeders and partly benthic suspension feeders. Differences in isotopic
signatures were also observed within the upper trophic levels that allowed estimation of the contribution of each food source
component to the diet of the upper consumers. Finally, the use of stable isotopic composition together with the species' feeding
strategy allow identification of the main differences between the trophic functioning of the two benthic communities and highlight
the importance of the role of detrital pathways in the carbon cycling within the continental shelf benthic trophic web.
© 2007 Elsevier B.V. All rights reserved.

Keywords: Benthic invertebrates; Demersal fish; Detritus; Food sources; Trophic level; Bay of Biscay

1. Introduction
⁎ Corresponding author. UR 070 RAP, Centre de Recherche Halieu-
tique, Institut de Recherche pour le Développement, Avenue Jean Pelagic primary and secondary production, generated
Monnet, B.P. 171, 34203 Sète Cedex, France. Fax: +33 4 99 57 32 95. in the euphotic zone, supply the continental shelf
E-mail address: francois.le.loch@ird.fr (F. Le Loc'h). benthic communities through the sedimentation of
0924-7963/$ - see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.jmarsys.2007.05.011
18 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34
organic material (Graf, 1992). A fundamental require-
ment to understand energy pathways through com-
plex benthic food webs from primary production to the
higher-level consumers is the knowledge of trophic
linkages among organisms (Hobson et al., 2002).
The Bay of Biscay continental shelf supports an
important demersal and benthic fishery, mainly for
European hake (Merluccius merluccius), sole (Solea
solea) and Norway lobster (Nephrops norvegicus).
These benthic and demersal communities have been
recently studied (Poulard et al., 2003; Poulard and
Blanchard, 2005), but no study since that of Glémarec
(1969) has investigated macro- and megafaunal inverte-
brate benthic communities although these potentially
constitute the main prey stock for target fish species.
The reconstruction of marine food webs is largely
constrained by methodological difficulties, especially
those associated with gut content analyses, and these
limitations are particularly evident in the case of small
sized invertebrates. Stable isotope analysis provides a
powerful tool for the study of the trophic relationships
within marine ecosystems (Peterson and Fry, 1987;
Michener and Schell, 1994). Indeed, the stable carbon
and nitrogen isotopic composition of an animal depends
on the stable isotopic composition of its food sources
and on isotopic fractionation during the feeding process.
Stable nitrogen and carbon isotope ratios (expressed
respectively as δ15N and δ13C) are typically enriched
from prey to consumers by 3.4‰ for δ15N and 1‰ for
δ13C (DeNiro and Epstein, 1981; Minagawa and Wada,
1984).
Thus, the large δ15N shift between a consumer and
its prey allows δ15N to be a reliable indicator of the
trophic position of an organism within the food web
relative to the primary producers. However, recent
reviews indicate that δ15N fractionation depends on
multiple factors, such as the N-content of the food,
environmental conditions, taxonomy and even trophic
group (Vander Zanden and Rasmussen, 2001; Vanderk-
lift and Ponsard, 2003; Mc Cutchan et al., 2003). Even if
the application of a unique trophic enrichment factor for
δ15N appears as a simplification of such a complex
system, a mean trophic fractionation of 3.4‰ could be
widely applicable in aquatic food webs according to
Post (2002). The δ13C analysis is useful to elucidate the
origin and pathways of organic matter in food webs, as
the primary sources may be isotopically distinct thus
allowing distinctions to be made between pelagic and
benthic contributions (Hobson et al., 2002) and tracking
fluxes of particulate matter along the food chain up to
the higher trophic levels (Le Loc'h and Hily, 2005). As
primary consumers integrate the temporal isotopic
variation of their food sources (Post, 2002), they can
be used as an isotopic baseline to calculate the reliance
of the upper consumers on benthic food sources
(Sherwood and Rose, 2005). Thus isotopic composition
provides information on the relative importance of each
source within the consumer's diet.
Trophic structure and pelagic–benthic coupling are
now quite well understood in shallow or intertidal
benthic ecosystems (Riera et al., 2002; Vizzini and
Mazzola, 2006). In contrast the functioning of benthic
invertebrate and fish continental shelf communities and
the sources of organic matter for their subsistence have
rarely been studied (Pinnegar and Polunin, 2000).
The main goal of this study is to assess the trophic
origins and pathways within the benthic communities of
the Northern Bay of Biscay continental shelf. Our main
objectives were i) to describe the macro- and mega-
faunal benthic community structure (species richness,
abundance and biomass), ii) to identify the different
trophic levels and the food sources supporting the dom-
inant and commercial species, iii) to link the two ap-
proaches in order to understand how benthic species are
organized to exploit the trophic sources on the continen-
tal shelf soft bottom.
2. Materials and methods
2.1. Study area
The study area is located around 47°N and extends
between 3 and 5°W on the French continental shelf of
the Bay of Biscay (northeast Atlantic Ocean; Fig. 1). A
large sedimentary muddy bank known as the “Grande
Vasière” characterizes the northern continental shelf of
the Bay of Biscay. The Grande Vasière is situated
between a depth range of 80 m to 130 m over a distance
of 275 km from south to north and 55–75 km from east
to west. To the west, hard bottom separates the Grand
Vasière from the outer edge of the continental shelf
constituted by the Ditrupa sands down to 160 m
(Glémarec, 1971).
2.2. Community sampling
During the last week of May and the first week of
June 2001, five areas (four located within the central
part of the Grande Vasière and one on the continental
shelf external margin) were sampled on the Bay of
Biscay continental shelf (Fig. 1). Within each of these
areas, three stations were sampled as zonal-replicates,
except for area B where only two stations were visited.
The faunal sampling strategy was the same as that of Le
 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34 19

Fig. 1. Localization of the sampling stations within the north-western part of the continental shelf of the Bay of Biscay. Stations A, B, C and D are
located on the Grande Vasière inside the dotted marks, stations E are on the external margin.

Loc'h and Hily (2005). A 2-m beam trawl was used to
sample the epibenthos, i.e. invertebrate megafauna
(individual mean size N10 mm) and demersal fish
(Kaiser et al., 1994; Jennings et al., 1999; Ellis et al.,
2000). This proved to be an efficient method for large
and rare species and for the integration of small-scale
seabed patchiness (Frauenheim et al., 1989). The beam
trawl was fitted with a chain mat and a 20-mm mesh
liner. During sampling (20 min), warp length was 3 times
the water depth, and the distance trawled was measured by
onboard differential global positioning system (DGPS).
Five benthic macrofauna (1–10 mm) replicate samples
per station were collected with a Hamon grab (0.25 m2). A
suprabenthic sledge (MACER-GIROQ) was used for
suprabenthos collection (0.5 mm net mesh size) and
zooplankton was sampled throughout the entire water
column using a WP2 zooplankton net (0.2 mm mesh size).
Finally, a Reineck corer was used for granulometric
determinations.
In each of the five zones, particulate organic matter
(POM) was collected with a Niskin bottle twice a day
during four days in May 2002 at two depths. The first
depth was near the fluorescence maximum (identified
using a CTD probe coupled to a fluorimeter) at
approximately 30 m depending on the station and the
time of day, and the second was close to the bottom at a
distance of 1–2 m from the sediment. They were named
POM surface layer and POM bottom respectively.
2.3. Community analyses
Once on board, faunal samples were washed, sorted
on a 1 mm mesh size and preserved in 7% formaldehyde
solution. Benthic macro- and megafaunal organisms
were identified to species level for most taxonomic
groups (except for nematods, nemerteans and phoro-
nids), and counted. Biomass of each taxon was
measured as ash-free dry weight (weight loss after
combustion at 450 °C for 4 h).
2.4. Stable isotopes
Samples were prepared and analysed for stable
isotopes following Le Loc'h and Hily (2005). POM
20 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34

was collected by filtration of seawater (4 l were filtered by continuous flow isotope ratio mass spectrometry
for each sample) on precombusted Whatman GF/F (CF-IRMS) using a Europa Scientific ANCA-NT 20-20
filters and then stored at − 20 °C. Subsequently, the Stable Isotope Analyser together with ANCA-NT Solid/
filters were exposed to HCl vapor for 4 h in order to Liquid Preparation Module. As the samples contained
remove carbonates before being placed in tin cups more than 10% nitrogen, the CF-IRMS was operated
(Lorrain et al., 2003). The samples were analysed for in dual isotope mode, allowing δ15N and δ13C to be
isotope ratios using a Finnigan Delta S isotope ratio measured in the same sample. Analytical precision
mass spectrometer coupled to a Carlo Erba NA 2100 (standard deviation, n = 5) was 0.2‰ for both nitrogen
Elemental Analyser. Because of the low organic matter and carbon, as estimated from standards analysed
content (b2%) and the high carbonate content measured together with the samples. Stable isotope ratios were
in the sediment, total extraction of the sediment organic expressed in conventional δ notation as parts per mil
matter (SOM) without degradation was not possible; (‰) according to the following equation:
therefore isotopic analysis of the sediment organic
matter was not carried out.
Species selected for isotopic analysis were those that dX ¼ ½ð R sample=R standardÞ  1  1000 ð1Þ
were dominant in terms of both abundance and bio-
mass, in order to obtain a synthetic image of the trophic where X is 13C or 15N and R is the corresponding
13 12
structure within each of the communities. Zooplankton C/ C or 15 N/14N ratio, respectively.
and suprabenthos samples were acidified to remove any As δ15N values provide an indication of the trophic
residual carbonates from cuticles and then rinsed with position of a consumer, the following formula was used
distilled water (Riera et al., 2000). Pre-treatment to estimate trophic level:
acidification is necessary to eliminate carbonates;
extended acidification (3 h) may affect δ 15 N values

Trophic Level ¼ d15 Nconsumer  d15 Nmean POM
(Pinnegar and Polunin, 1999; Carabel et al., 2006); our
samples were acidified with HCl 1.2 N for less than =3:4 þ 1 ð2Þ
10 min. It is well known that lipids are depleted in 13 C
compared to carbohydrates and proteins (DeNiro and where 3.4‰ is the assumed 15N trophic enrichment
Epstein, 1977; Griffiths, 1991), implying that fatty factor according to Minagawa and Wada (1984). In a
tissues tend to be isotopically lighter compared to lean benthic ecosystem such as the Grande Vasière (depth N
ones. Therefore, trophic interpretations based on δ13 C 100 m), no primary production can occur on the bottom;
signatures may be cofounded by lipid effects (Wada consequently, the only organic material available for
et al., 1987; Bodin et al., 2007). In order to minimize benthic primary consumers is assumed to be the POM
these effects mega- and macrofaunal (except poly- sedimenting from upper water layers and therefore this is
chaetes) low-lipid muscle tissue was used for stable designated as the first trophic level.
isotope analysis. Muscle samples were taken from the
dorsal musculature of fish, from the pereiopod 1 of the
Brachyura, from the abdomen of the Natantia, Reptan-
Table 1
tia, Macrura, Stomatopoda and large Mysidacea and Sediment characteristics of the sampling stations (mean, standard
from the siphon of bivalves. Polychaete viscera were deviation is given in brackets)
extracted by dissection and the analyses were carried
A B C D E
out on the remaining whole-body, after removal of
Number of stations 3 2 3 3 3
chetae. After dissection, the tissue samples of every
sampled in the area
taxa were washed very carefully with distilled water Water depth (m) 98– 102– 111– 115– 138–
in order to prevent any contamination by sediment 103 110 117 127 143
carbonates (Kharlmamenko et al., 2001; O'Reilly et al., Pelitic fraction 13.7 32.5– 13.4 12.8 8.4
2002). (b63 µm) (%) (2.4) 34.1 (3.1) (1.3) (1.1)
Fine and medium sands 80.7 54.0– 66.9 82.4 79.4
All samples were stored frozen individually at
(63–500 µm) (%) (8.5) 66.0 (20.0) (4.3) (1.8)
− 20 °C before freeze-drying. Each dried sample was Median grain size (µm) 181 109– 210 172 192
then ground to obtain a homogeneous powder, and 1 mg (31) 115 (39) (13) (8)
of this powder was weighed in tin capsules for stable Sediment type FV FV–SHV FV FV SFB
carbon and nitrogen isotopic analyses. The 13C/12C Sediment type as defined in Chassé and Glémarec (1976), FV: fine muddy
and 15N/14N ratios of faunal tissue were determined sands, SHV: heterogeneous muddy sands, SFB: biogenic fine sands.
 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34 21

Table 2
Mean values for abundance, biomass and specific richness (number of species) parameters for the five sampling areas of the North Bay of Biscay
A
A B C D E
Stations sampled in the area 3 2 3 3 3
Abundance (ind m− 2) 263.7 (89.8) 162–213 236.0 (64.2) 437.3 (116.5) 1027.3 (161.3)
Biomass (mg AFDW m− 2) 690 (398) 1117–1163 1097 (182) 975 (303) 2172 (598)
Specific richness per station 52.3 (12.2) 30–38 49.7 (14.2) 67.3 (9.1) 98.3 (4.5)
Total species richness 84 50 87 117 156

B
A B C D E
Stations sampled in the area 1 3 2 3 2
Abundance (ind 1000 m− 2) 44.7 124.3 (33.3) 103.6–199.1 243.0 (57.7) 862.0–1550.6
Biomass (g AFDW 1000 m− 2) 101.8 103.0 (15.0) 91.5–149.7 107.7 (22.9) 185.0–327.5
Specific richness per station 14 26.3 (4.2) 20–27 47.0 (12.8) 84–87
Standard deviations are given between brackets. A) Macrofaunal (1–10 mm) parameters B) megafaunal (N10 mm) parameters.

According to the approach of Vander Zanden and sumer baseline and the bivalve Nucula sulcata and the
Vadeboncoeur (2002) and Sherwood and Rose (2005), gastropod Scaphander lignarius as the benthic primary
we use δ13C values as an indicator of food origin. The consumer baseline (see Table 4). δ13C Consumer II is the
reliance on benthic affinity prey (RBAP) of upper δ13C of the secondary consumer considered. As primary
consumer species was estimated using the formula: consumers are used as baseline, RBAP is calculated for
consumers with TL higher than 2. Moreover, to take into
RBAP ¼ X þ d13 CConsumer II  d13 CConsumer I Pelagic affinity baseline


account the δ13C trophic enrichment along the food wed,

we used a trophic fractionation of 1‰ (DeNiro and
= d13 CConsumer I Benthic affinity baseline  d13 CConsumer I Pelagic affinity baseline
Epstein, 1978) as described by the equation:
 100 ð3Þ


X ¼  TLConsumer II  TLConsumer I Benthic Affinity baseline  1
where δ13C Consumer I Benthic affinity baseline and δ13C Consumer ð4Þ
I Pelagic affinity baseline are the mean δ C of the benthic
13

and pelagic primary consumer used as baseline. Here, where TL Consumer I Benthic affinity baseline and TL Consumer II
zooplankton is considered as the pelagic primary con- are respectively the Trophic Level of the benthic primary

Fig. 2. Multidimensional scaling ordination of square root transformed abundance data.

22 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34

Table 3
Percent dominance in terms of biomass, feeding strategy, spatial localization and taxonomic group for the major biomass species
Species Biomass dominance (%) Feeding Spatial Taxonomic group
strategy localization
Grande Vasière External margin
Brissopsis lyrifera† 15.5 0 SSDF Infauna Echinodermata Echinoidea
Dasybranchus gajolae 11.7 0 SSDF Infauna Annelida Polychaeta
Callianassa subterranea 10.4 0 SF Infauna Crustacea Decapoda
Nephtys caeca 9.5 2.5 P Infauna Annelida Polychaeta
Glycera rouxii 2.3 0.8 P Infauna Annelida Polychaeta
Terebellides stroemi⁎ 2.1 0.3 SDF Infauna Annelida Polychaeta
Aponuphis fauveli 2.0 0 SF Epifauna Annelida Polychaeta
Labidoplax sp. 2.0 0 SDF Infauna Echinodermata
Holothurioidea
Nephrops norvegicus 1.8 0 P Infauna Crustacea Decapoda
Lumbrinereis impatiens⁎ 1.4 1.9 P Infauna Annelida Polychaeta
Natatolana borealis 1.4 0.9 S Supra-benthic Crustacea Isopoda
Munida sarsi 1.3 0 P Epifauna Crustacean Decapoda
Alphaeus glaber 1.3 0 SDF Infauna Crustacea Decapoda
Dosinia lupinus 1.3 0 SF Infauna Mollusca Pelecypoda
Nucula sulcata 1.2 0.1 SDF Infauna Mollusca Pelecypoda
Owenia fusiformis† 1.1 0.1 SDF Epifauna Annelida Polychaeta
Liocarcinus depurator 1.1 0.2 P Epifauna Crustacea Decapoda
Ampharete grubei 1.0 1.3 SDF Infauna Annelida Polychaeta
Arnoglossus laterna 0.9 0 P Epifauna Chordata Osteichtyes
Amphiura filiformis 0.8 0.9 SF Epifauna Echinodermata
Ophiuroidea
Microchirus variegatus 0.8 0.2 P Epifauna Chordata Osteichtyes
Enchelyopsus cimbrius 0.7 0 P Epifauna Chordata Osteichtyes
Merluccius merluccius 0.6 0 P Demersal Chordata Osteichtyes
Goniada sp. 0.5 0.9 P Infauna Annelida Polychaeta
Goneplax rhomboides 0.5 0 P Epifauna Crustacea Decapoda
Ampelisca spinipesnpd 0.5 1.0 SF Epifauna Crustacea Amphipoda
Bryozoa† 0.4 8.6 SF Epifauna
Astropecten irregularis 0.4 0.2 P Epifauna Echinodermata Asterides
Lumbrinereis fragilis 0.3 2.2 P Infauna Annelida polychaeta
Solea vulgaris 0.3 0 P Epifauna Chordata Osteichtyes
Turitella communis 0.2 0.7 SF Epifauna Mollusca Gastropoda
Magelona alleni 0.2 0 SF Epifauna Annelida polychaeta
Venus ovata 0.2 0.1 SF Infauna Mollusca Pelecypoda
Calliostoma granulatum 0.2 0.3 G Epifauna Mollusca Gastropoda
Lesueuriogobius friseii 0.1 0 P Epifauna Chordata Osteichtyes
Aponuphis tubicola 0.1 0.1 P Epifauna Annelida polychaeta
Callionymus lyra⁎ 0.1 0.1 P Epifauna Chordata Osteichtyes
Crangon allmani⁎ 0.1 0 P Supra-benthic Crustacea Eumalacostraca
Sipunculus nudus† 0 13.4 SSDF Infauna Sipuncula Sipunculidea
Ditrupa arietina 0 12.7 SF Epifauna Annelida polychaeta
Spatangus purpureus† 0 8.8 SSDF Infauna Echinodermata Echinoidea
Onchodesma steenstupi† 0.1 4.8 SSDF Infauna Sipuncula Sipunculidea
Aponuphis bilineata 0 4.2 P Epifauna Annelida polychaeta
Scaphander lignarius 0 2.2 SSDF Epifauna Mollusca Gastropoda
Eulalia sanguinea 0 1.0 P Epifauna Annelida polychaeta
Arnoglossus imperialis 0 0.7 P Epifauna Chordata Osteichtyes
Atelecyclus rotundatus 0 0.7 P Epifauna Crustacea Decapoda
Porania pulvillus 0 0.5 P Epifauna Echinodermata Asterides
Pagurus pridauxi 0 0.5 P Epifauna Crustacea Eumalacostraca
Macropipus tuberculatus 0 0.5 P Epifauna Crustacea Decapoda
Lepidorhombus whiffiagonis 0 0.5 P Epifauna Chordata Osteichtyes
Chlamys tigerina 0 0.3 SF Epifauna Mollusca Pelecypoda
Callionymus maculatus 0 0.2 P Epifauna Chordata Osteichtyes
Ebalia tuberosa 0 0.2 P Epifauna Crustacea Decapoda
 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34
Table 3 (continued )
Species Biomass dominance (%)
Grande Vasière External margin
Anapagurus laevis 0 0.1
Lophius piscatorius 0 0.1
Total 76.4 80.4
In bold species analysed for stable isotopes in this study, ⁎species analysed in a previous study (Le Loc'h and Hily, 2005), †species that were
associated with a trophic group based on their feeding strategy. The feeding strategy is based on Pearson (1971), Gros and Hamon (1988), Bonsdorff
and Pearson (1999): P: predator, SF: suspension feeder, SDF: surface deposit feeder, SSDF: sub-surface deposit feeder, G: grazer.
consumer baseline and secondary consumer (calculated
with formula (2)). As they are time integrators of the
primary producer isotopic variability, the primary con-
sumers are often used as isotopic baseline (Vander Zanden
and Vadeboncoeur, 2002; Post, 2002; Jennings and Warr,
2003).
2.5. Statistical analysis
As all POM values follow a normal distribution
according to the Shapiro–Wilk test (p b 0.05), a Student
test was used to compare the differences in mean δ13C
and δ15N between depth and season. In order to identify
group of species, a hierarchical cluster analysis
(Euclidian distance, Ward's minimum-variance method)
was performed on stable nitrogen and carbon values
(Davenport and Bax, 2002; Le Loc'h and Hily, 2005;
Grall et al., 2006). Multidimensional scaling (MDS) was
performed on fourth root transformed abundance data to
identify the benthic communities. Similarities were
calculated using the Bray–Curtis similarity index.
3. Results
3.1. Characteristics of the sampled stations
The depth range was from 98 m (zone A) to 143 m
(zone E) from coast to offshore. According to Chassé
and Glémarec's (1976) biotope classification, the central
Grande Vasière stations belong to fine muddy sands
with a pelitic fraction ranging from 12 to 14% and a
median grain size around 200 µm, with the exception of
area B, with more heterogeneous sediment (pelitic
fraction up to 34% and median grain size around
110 µm) (Table 1). Offshore, on the external margin,
station E sediments are biogenic fine sands with a
similar mean grain size (ca. 192 µm) to that in the
Grande Vasière, but a lower pelitic content (b10%) and
presence of a calcareous coarse fraction (shell fragments
and Ditrupa tubes).
23
Feeding Spatial Taxonomic group
strategy localization
SF Epifauna Crustacea Eumalacostraca
P Epifauna Chordata Osteichtyes
3.2. Communities description
3.2.1. Macrofauna
Within the 14 stations sampled, a total of 7538
individuals were identified belonging to 188 species.
Within the benthic communities, annelids were the most
represented phylum with 81 species, followed by
crustaceans (56 species), molluscs (32 species) and
echinoderms (12 species). Macrofaunal abundances
range from 162 (area B) to 437.3 ind m− 2 (area D)
within the central Grande Vasière while they attain up to
1027.3 ind m− 2 for area E (Table 2A). The same pattern
is observed for species richness per station with a
minimum of 30 species in station B in contrast to a mean
of 98.3 species on the external margin. Biomass is also
higher on area E (2172 mg AFDW m− 2) in comparison
to the Grande Vasière (690 to 1163 mg AFDW m− 2).
3.2.2. Megafauna
Molluscs (48 species), crustaceans (36 species), fish
(22 species) and echinoderms (13 species) were the
dominating phyla among the 128 species collected with
the 2-m beam trawl. Megafaunal densities and biomass
were much lower than those of the macrofauna, with
difference of 1 and 3 orders of magnitude for biomass
and abundance respectively (Table 2B). As for macro-
fauna, megafauna exhibit differences in their distribu-
tion with the highest biomass, abundance and species
richness on the external margin.
3.2.3. Community
Results of the multidimensional scaling (MDS)
based on the abundance of macro- and megafauna
separated the Grande Vasière central stations from
those of the external margin (Fig. 2). Thus, stations A,
B, C and D were pooled and can be considered as part
of a Grande Vasière central community. Within the 322
taxa identified, the 39 species that contributed most
to the biomass accounted for 76.4% and 80.4% of
the mean total biomass of the Grande Vasière and the
24 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34

Ditrupa sand communities respectively (Table 3). nea and Aponuphis fauveli and the predators Nephtys
Among these, the deposit feeders Brissopsis lyrifera, caeca, Glycera rouxii and N. norvegicus represented
Dasybranchus gajolae, Terebellides stroemi, Labido- 57.3% of the Grande Vasière community biomass.
plax sp., the suspension feeders Callianassa subterra- The Ditrupa sand community is characterized by the

Table 4
Stable nitrogen and stable carbon isotope values (mean, standard deviation is given in brackets) of the food web of the Grande Vasière and
corresponding trophic level (TL) and reliance on benthic affinity prey (RBAP), n correspond to the number of individual isotopic values, with the
exception of zooplankton and suprabenthos where n is the number of isotopic values for a pool of individuals
Species Code n C/N ratio δ15N (‰) TL δ13C (‰) RBAP
POM (−30 m) spring 2002 8 3.57 (0.80) − 23.76 (0.70) –
POM (−30 m) end of summer 2002 ⁎ 8 4.14 (1.04) − 23.73 (1.08)
POM bottom spring 2002 8 5.66 (0.40) − 22.95 (0.60) –
POM bottom end of summer 2002 ⁎ 8 4.23 (0.93) − 22.93 (0.63)
Cnidarians
Virgularia mirabilis Vmi 2 5.02 8.79 2.1 − 18.92 –
Crustaceans
Zooplankton ⁎ Zpk 4 5.48 (0.20) 8.17 (0.74) 2.0 − 20.40 (0.82) –
Suprabenthos ⁎ Spb 4 5.59 (0.71) 8.05 (0.59) 1.9 − 19.93 (1.11) –
Callianassa subterranea Csu 5 4.89 (0.24) 8.89 (0.75) 2.2 − 16.98 (0.27) –
Alpheus glaber Agl 10 3.99 (0.05) 9.81 (0.50) 2.4 − 16.03 (0.41) 0.97
Munida sarsi Msa 14 4.04 (0.12) 10.06 (0.70) 2.5 − 16.23 (0.53) 0.91
Nephrops norvegicus Nno 21 4.09 (0.08) 10.70 (0.58) 2.7 − 16.02 (0.39) 0.91
Goneplax rhomboides Grh 10 4.22 (0.14) 11.54 (0.68) 2.9 − 16.15 (0.29) 0.83
Liocarcinus depurator Lde 9 4.15 (0.13) 12.41 (0.62) 3.2 − 15.99 (0.48) 0.80
Meiosquilla desmaresti Mde 1 4.12 12.8 3.3 − 16.3 0.70
Natatolana borealis Nbo 2 6.03 12.81 3.3 − 18.52 0.20
Echinoderms
Holothurian Hol 1 4.30 11.2 2.9 − 15.6 0.98
Polychaetes
Magelona alleni Mal 1 5.24 7.6 1.8 − 17.0 –
Aponuphis fauveli Afa 1 4.91 8.8 2.1 − 17.8 –
Ampharete grubei Agr 3 5.08 (0.65) 9.55 (0.51) 2.4 − 16.58 (0.69) 0.86
Aponuphis tubicola Atu 2 4.40 10.88 2.7 − 16.93 0.69
Nephtys caeca Nca 5 4.37 (0.22) 11.12 (0.95) 2.8 − 16.21 (0.49) 0.84
Dasybranchus gajolae Dga 2 4.42 11.74 3.0 − 16.22 0.71
Glycera rouxii Gro 2 4.53 14.26 3.7 − 15.68 0.75
Bivalves
Chlamys septemradiata Cse 2 4.24 5.15 1.1 − 16.85 –
Pecten maximus Pma 1 4.07 5.3 1.1 − 16.3 –
Venus ovata Vov 2 4.93 6.85 1.6 − 17.36 –
Nucula sulcata Nsu 5 4.57 (0.12) 9.34 (0.44) 2.3 − 16.03 (0.19) –
Gastropods
Calliostoma granulatum Cgr 1 4.09 11.7 3.0 − 17.5 0.50
Pisces
Merluccius merluccius (4–10 cm) Mme j 5 4.12 (0.04) 10.79 (0.57) 2.7 − 18.05 (0.35) 0.44
Callionymus maculatus Cma 3 4.12 (0.06) 11.68 (0.30) 3.0 − 16.41 (0.29) 0.76
Arnoglossus laterna Ala 3 4.13 (0.04) 11.73 (0.32) 3.0 − 17.22 (0.09) 0.57
Merluccius merluccius (19–41 cm) Mme a 3 4.01 (0.02) 12.70 (1.32) 3.3 − 17.04 (0.64) 0.54
Enchelyopsus cimbrius Eci 6 4.02 (0.02) 12.80 (0.71) 3.3 − 16.63 (0.18) 0.63
Lesueuriogobius friseii Lfr 7 4.10 (0.05) 13.11 (0.75) 3.4 − 16.67 (0.20) 0.60
Lepidorhombus whiffiagonis Lwh 6 4.11 (0.08) 13.40 (0.78) 3.5 − 16.38 (0.38) 0.64
Microchirus variegatus Mva 3 4.19 (0.03) 13.60 (0.26) 3.5 − 16.32 (0.15) 0.65
Scyliorhinus canalicula Sca 3 3.59 (0.26) 13.65 (0.88) 3.6 − 16.49 (0.38) 0.61
Lophius piscatorius Lpi 3 4.06 (0.02) 13.98 (0.66) 3.7 − 16.93 (0.70) 0.48
Solea solea Sso 3 4.19 (0.09) 15.39 (1.53) 4.1 − 16.23 (0.35) 0.55
The RBAP were not calculated for TL ≤ 2.2.
⁎ From Le Loc'h and Hily (2005).
 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34 25

deposit feeders Sipunculus nudus, Spatangus pupureus
and Onchodesma steenstrupi, the suspension feeders
Ditrupa arietina and bryozoa, predators Aponuphis
bilineata and N. caeca and the grazer S. lignarius
(57.2% of the biomass).
3.3. Stable isotopes
seasonal δ15N variability, the δ15N mean POM used in
the TL formula (Eq. (2)) is the bottom mean for both
seasons (δ15N mean POM = 4.95‰).
Only two POM samples were collected at both
depths on the Ditrupa sands community at the end of
summer. Therefore, the bottom POM δ15N mean was
used in the TL equation for this community.

3.3.1. POM 3.3.2. TL and RBAP

Significant differences were detected for the Grande
Vasière POM isotopic ratios between depths in spring
(p b 0.001 and p b 0.019 for δ15N and δ13C respectively,
Student test), while no differences were found at the end
of summer (p b 0.431 and p b 0.045 for δ15N and δ13C
respectively, Student test) (Table 4). Moreover seasonal
δ15N bottom POM variations occurred, with higher
values in spring (p b 0.006, Student test), while no
significant differences were detected for δ13C bottom
POM values between the two seasons (p = 0.468,
Student test). Therefore, to take into account the POM
Forty-three species (32 and 18 species, for the
Grande Vasière and the Ditrupa sands communities
respectively) and pools of zooplankton and supra-
benthos were analysed for stable isotopic ratios of the
two benthic communities with 6 species belonging to
both communities (Tables 4 and 5). On the North Bay
of Biscay continental shelf, invertebrates show a wider
range in stable isotope ratios than fish. The stable
nitrogen isotope ratios varied considerably among the
Grande Vasière benthic community from the suspen-
sion feeder Chlamys septemradiata (δ15 N = 5.2‰) to

Table 5
Stable nitrogen and stable carbon isotope values (mean, standard deviation is given in brackets) of the food web of the Ditrupa sand community and
corresponding trophic level (TL) and reliance on benthic affinity prey (RBAP), n correspond to the number of individual isotopic values, with the
exception of zooplankton and suprabenthos where n is the number of isotopic values for a pool of individuals
Species Code n C/N ratio δ15N ‰ TL δ13C ‰ RBAP
POM (−30 m) end of summer 2002 2 3.40 − 22.00
POM bottom end of summer 2002 2 5.00 1 − 23.25
Crustaceans
Zooplankton Zpk 1 5.74 9.8 2.4 − 21.6 –
Suprabenthos Spb 1 6.40 10.0 2.5 − 21.6 –
Anapagurus laevis Ala 1 5.59 8.3 2.0 − 16.5 –
Macropipus tuberculatus Mtu 3 4.28 (0.03) 10.26 (0.23) 2.6 − 16.98 (0.31) 0.74
Galathea dispersa Gdi 3 4.40 (0.08) 10.57 (0.26) 2.6 − 16.43 (0.47) 0.81
Pagurus pridauxi Ppr 6 4.24 (0.08) 10.70 (0.21) 2.7 − 16.06 (0.45) 0.87
Atelecyclus rotundatus Aro 3 4.13 (0.01) 11.21 (0.82) 2.8 − 16.05 (0.14) 0.84
Ebalia tuberosa Atu 1 4.25 12.5 3.2 − 16.9 0.64
Echinoderms
Holothurie Hol 2 4.56 10.29 2.6 − 16.24 0.87
Polychaetes
Ditrupa arietina Dar 1 7.22 6.7 1.5 − 18.0 –
Aponuphis tubicola Atu 2 5.14 8.89 2.1 − 17.83 –
Aponuphis fauveli Afa 1 4.88 9.4 2.3 − 17.9 –
Nephtys caeca Nca 2 4.36 11.71 3.0 − 16.68 0.72
Goniada sp. Gon 1 4.44 12.9 3.3 − 16.2 0.74
Glycera rouxii Gro 1 4.50 13.7 3.6 − 16.8 0.60
Bivalves
Chlamys tigerina Cti 1 4.30 7.9 1.8 − 16.7 –
Arcopella balaustina Aba 1 4.53 9.3 2.3 − 16.6 –
Gastropods
Scaphander lignarius Sli 2 4.38 9.80 2.4 − 15.53 –
Calliostoma granulatum Cgr 2 4.22 11.51 2.9 − 16.73 0.72
Pisces
Arnoglossus imperialis Aim 3 4.13 (0.01) 11.77 (0.22) 3.0 − 17.43 (0.20) 0.59
The RBAP were not calculated for TL ≤ 2.2.
26 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34

the carnivorous flatfish S. solea (δ 15 N = 15.4‰).
While the range is narrower within the Ditrupa sand
community than in the Grande Vasière community,
varying from the suspension feeder D. arietina (δ15 N =
6.7‰) to the predator G. rouxii (δ15 N = 13.7‰). Thus,
a continuum of four trophic levels, from POM (TL1) to
S. solea (TL 4.1) or G. rouxii (TL 3.6) is detected in
both benthic communities. Some TLs derived from
bottom POM values seem surprising: some of the
benthic suspension feeders such as the Pectinidae,
have values inferior to 2, while other primary con-
sumers as zooplankton and suprabenthos have a TL
close to 2.
Among primary consumers, δ13C values vary greatly,
deposit feeders being 13C-enriched in comparison to
zooplankton or suprabenthos. This large δ13C differ-
ence from pelagic (zooplankton δ13C = − 20.40‰ and
− 21.55‰, for Grande Vasière and Ditrupa sands
respectively) to benthic primary consumers (N. sulcata
δ13C = − 16.03‰ and S. lignarius δ13 C = − 16.58‰)
allows their use to estimate the Reliance on Benthic
Affinity Prey (RBAP) of the upper consumers as
illustrated by formula 3 (Tables 4 and 5). Thus, the
RBAP ranges from 0.20 for the scavenger swimming
isopod Natatolana borealis to 0.98 for the deposit
feeder Labidoplax sp. For both communities, almost all
the benthic and demersal taxa have a RBAP greater than
0.50 with the exception of the M. merluccius juveniles
(4–10 cm) (0.46) and the anglerfish L. piscatorius
(0.50).
3.3.3. Identification of trophic groups
According to the results of the cluster analysis
performed on both communities' stable isotopic
nitrogen and carbon ratios, species are grouped in
eight units (Figs. 3 and 4). Comparison between the
clustering results, the TL and the RBAP and the
biological and ecological features, provides a useful
basis for a description of the different feeding patterns
observed. Within the Grande Vasière benthic and
demersal community, suspension and deposit feeders
have the lowest TL. They are divided into four feeding
groups (Fig. 3). Zooplankton and suprabenthos, with
TL 2 and δ 13 C around − 20‰, are clustered in the
primary consumer, water column suspension feeders
group (C1-WCSF). While benthic suspension feeders

Fig. 3. Distribution of carbon and nitrogen stable isotope ratios (mean ± standard deviation) among groups composing the Grande Vasière benthic
food web. The groups of taxa (circled) are chosen from the result of the hierarchical cluster analysis, C1-WCSF: primary consumer-water column
suspension feeders, C1-BSF: primary consumer-benthic suspension feeders, C1-DF: primary consumer-deposit feeders, C1-int: primary consumer
intermediate, C2-BAF: secondary consumer-benthic affinity feeders, C2-PAF: secondary consumer-pelagic affinity feeders, C2-int: secondary
consumer intermediate, C3: tertiary consumers, see Table 4 for label code.
 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34 27

Fig. 4. Distribution of carbon and nitrogen stable isotope ratios (mean ± standard deviation) among groups composing the Ditrupa sand benthic food
web. The groups of taxa (encircled) are chosen from the result of the hierarchical cluster analysis, C1-BSF mix: primary consumer-benthic suspension
feeders, see Fig. 3 for circled group name and Table 5 for label code.

(C1-BSF) had the lowest TL, especially the Pectinidae
(TL 1.1), with δ13 C values around − 17‰. Surface
deposit feeders (C1-DF) such as N. sulcata occupied
an intermediate TL around 2.5 with δ 13 C values close
to those of the benthic suspension feeders. Another
intermediate group (TL between 2.1 and 2.7) clusters
hake juveniles, the Cnidarian Virgularia mirabilis
and the Polychaeta Hyalinoecia fauveli. It is char-
acterized by δ13 C values between − 19 and − 18‰.
The upper consumers are also divided into four
feeding groups. The δ13C allows discrimination between
two groups with a TL close to 3, (1) the predators
(N. norvegicus, N. caeca) and the sub-surface deposit
feeders (D. gajolae) with a RBAP N 0.75 (C2-BAF) and
(2) predator (Arnoglossus laterna), grazer (Calliostoma
granulatum) and scavenger (N. borealis) with RBAP
b 0.70 (C2-PAF). Most of the fish are clustered in the C2
intermediate group, with a TL around 3.5 and a RBAP
between 0.48 and 0.65. Finally, S. solea and G. rouxii are
included in the top-predator group (C3).
Despite the lower number of species analysed for
stable isotopes in the external margin benthic commu-
nity, the same type of classification as for the Grande
Vasière is applied. Eight feeding groups are also detected
with the cluster analysis (Fig. 4). As for the Grande
Vasière, zooplankton and suprabenthos are isolated. Two
groups of benthic suspension feeders are identified, the
first one (C1-BSF) composed of the Pectinidae Chlamys
tigerina and the crustacean Anapagurus laevis and
the second (C1-BSF mix) with the only polychaete
D. arietina. The polychaetes Hyalinoecia tubicola and
H. fauveli are included in a primary consumer inter-
mediate group (C1-int) with a TL around 2.2 and a δ13C
value of − 17.8‰. The bivalve Arcopella balaustina and
the gastropod S. lignarius constitute the primary
consumers deposit feeders group (C1-DF). The upper
consumers are divided into three groups, the first one
clusters carnivorous species with a largely pelagic food
source with TLs close to 3 (Arnoglossus imperialis,
N. caeca), the second one includes the benthic affinity
secondary consumers (C2-BAF) and the third one the
upper consumers with TL N 3.2 (G. rouxii, Goniada sp.
and Ebalia tuberosa).
3.3.4. Food web structure
In order to elucidate the trophic pathways of these
complex benthic systems, we have associated the
biomass of each species with the trophic group in
which they have been included based on stable iso-
topic analyses (Table 6). A more accurate trophic
28 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34

Table 6
Correspondence between biomass structure of the macro and megafaunal benthic communities (percentage) and trophic guilds (trophic level and
reliance on benthic affinity prey) identified by stable isotopes analysis (mean ± standard deviation)
Trophic guild Grande Vasière External margin
Biomass Trophic Reliance on benthic Biomass Trophic Reliance on benthic
contribution (%) level affinity prey contribution (%) level affinity prey
Primary consumers
Benthic suspension feeders 2.2 1.7 (0.1) – 14.2 1.8 (0.3) –
Surface deposit feeders 16.3 2.4 (0.1) 0.91 (0.06) 3.7 2.4 –
Intermediate 2.5 2.4 (0.4) 0.69 8.7 2.5 –
Secondary consumers
Benthic affinity feeders 41.5 2.9 (0.1) 0.84 (0.10) 33.6 2.8 (0.2) 0.91 (0.08)
Pelagic affinity feeders 2.5 3.1 (0.2) 0.42 (0.20) 1.9 3.0 0.66
Intermediate 7.4 3.4 (0.2) 0.62 (0.10) 4.4 3.3 0.69
Tertiary consumers
Top carnivorous 2.6 3.9 0.65 0.8 3.6 0.60
Total 75.0 67.3
Reliance on benthic affinity prey was not calculated for mean trophic level ≤2.5.

structure was also obtained using recent data from a
study on the Grande Vasière (Le Loc'h and Hily,
2005). Moreover, species with well known feeding
strategy were added to the trophic structure (see
Table 3). For example, the urchins B. lyrifera and
Spatangus purpureus which represent an important
biomass were not analysed here because of their high
lipid content which influences the stable isotopic
ratios (Pinnegar and Polunin, 1999; Sotiropoulos
et al., 2004; Bodin et al., 2007). However since they
are sub-surface deposit feeders, their biomass was
added to the C2-BAF group which clusters all the
sub-surface deposit feeders analysed. Thus 75 and
67.3% of the total benthic macrofaunal biomass of
the Grande Vasière and the External Margin commu-
nity respectively, were taken into account to establish
the trophic structure; the species not retained belong
mainly to small size macrofauna.
4. Discussion
4.1. Community structure
Statistical analysis of the grab and beam trawl data
separates two distinct benthic communities: the muddy
sand community, dominated by the carnivorous poly-
chaetes N. caeca, G. rouxii, the deposit feeders T.
stroemi, D. gajolae and the crustacean C. subterranea
on one hand, and the external margin fine sands
community, dominated by the suspension feeder D.
arietina on the other hand. These two main communities
were previously identified by Le Danois (1948) and
described by Glémarec (1969), although the present
study is the first to provide quantitative data from these
bottoms in terms of abundance and biomass. The Di-
trupa sands show the highest values for abundance,
biomass as well as for species richness. The presence of
shell fragments within the biogenic fine sands of the
external margin (i.e. dead Ditrupa tubes) created
complex habitat structure. High habitat heterogeneity
and complexity are directly related to highest diversity
(Le Hir and Hily, 2005) and provide microhabitats for
macrofaunal organisms (Mc Coy and Bell, 1991). Thus,
in contrast to the homogenous muddy sand habitat of the
Grande Vasière, the structurally complex habitat of the
external margin could explain the higher biomass and
biodiversity observed at this site.
4.2. Food web source
Offshore, the continental shelf benthic communities
are coupled to pelagic primary and secondary produc-
tion through the sedimentation of organic material
(Rowe, 1971; Hargrave, 1973; Graf, 1992; Marcus and
Boero, 1998). The isotopic signatures of the North Bay
of Biscay POM are in the same range than those of other
continental shelves (South Bay of Biscay: Fontugne and
Jouanneau, 1987, George Bank: Fry, 1988, Southeastern
Australia: Davenport and Bax, 2002). The North Bay of
Biscay benthic communities are supplied by the
sedimentation of the pelagic primary production asso-
ciated with the Loire and Vilaine river plumes (Lampert
et al., 2002; Loyer et al., 2006). On the Grande Vasière,
at the end of summer, there was no difference between
surface layer and bottom POM stable isotopic composi-
tion, which indicates that the sedimentation occurs
 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34
without qualitative transformation. In contrast, in spring,
bottom POM stable isotopic ratios are significantly
enriched in 13C and 15N in comparison to POM
collected in the surface layer. These differences may
be explained by different biochemical or/and phyto-
plankton species composition.
Indeed, the North Bay of Biscay continental shelf is
characterized by a seasonal succession of phytoplankton
communities, associated with depth segregation (Lun-
ven et al., 2005). Stable isotope fractionation varies both
within groups and between groups of marine phyto-
plankton (Needoba et al., 2003) as well as phytoplank-
ton size classes (Bode et al., 2004). In our study site,
near the sea surface, POM collected in the chlorophyll a
maximum is mainly composed of phytoplankton cells
and sedimenting phytodetritus and other organic
material originating from recent pelagic production
(Lunven et al., 2005). Around 100 m depth, bottom
POM is constituted of a mix of resuspension of sedi-
mented organic matter, benthic organic matter second-
ary production and degradation of organic matter from
both of these sources. Despite this, the lowest pigment
concentrations were measured in bottom water at the
end of summer, the Chlorophyll a/Phaeopigment ratios
were the highest, indicating the presence of less de-
graded phytoplankton at that period (Le Loc'h, 2004).
Moreover, due to different physical forcing (tidal cur-
rents and wind) resuspension was more active during
the spring sampling cruise than at the end of summer
leading to the highest sedimentation in the moored
bottom sediment trap (Le Loc'h, 2004). Therefore,
phytodetritus and other organic material are subject to
bacterial degradation and other physico-chemical pro-
cesses during sinking and resuspension processes,
altering isotopic composition (Macko and Estep, 1984;
Lehmann et al., 2002). These processes lead to temporal
variability of the available organic matter (quality and
quantity) which supply the benthic communities.
4.3. Trophic level and reliance on benthic affinity prey
According to Minagawa and Wada (1984) and Le
Loc'h and Hily (2005), a trophic enrichment factor of
3.4 was used to calculate the TL based on bottom POM.
Although this factor can vary according to the
taxonomic groups and the feeding types in a given
ecosystem (Michener and Schell, 1994; Post, 2002;
Vanderklift and Ponsard, 2003), its range of variation
remains low (3 to 4‰) and can be widely applicable in
aquatic food web studies (Post, 2002).
In the Grande Vasière as well as in the Ditrupa sand
communities, benthic invertebrates extend over a
29
continuum of almost three different trophic levels.
This finding appears to be a general feature of temperate
subtidal benthic ecosystems (Davenport and Bax, 2002;
Grall et al., 2006; Bodin et al., 2008). The large range of
δ13C ratios within primary consumers is also a general
trend off continental shelf communities (Hobson et al.,
2002; Sherwood and Rose, 2005). Zooplankton and
suprabenthos feeding on POM, as attested by their
isotopic signature, are depleted in 13C in comparison to
the benthic deposit feeders that ingest sedimented
organic matter. Because of the degradation and micro-
bial recycling occurring in the bottom nepheloid layer, it
has been suggested that during these processes depos-
ited organic matter could be enriched in 13C (Goering et
al., 1990; Hobson et al., 1995). δ13C clearly discrimi-
nates between different sources of organic matter,
allowing tracking of fluxes of matter along the food
chain up to the higher trophic levels. Thus, the δ13C
range of variation within the primary consumers allows
the distinction between pelagic and benthic affinity
components (Le Loc'h and Hily, 2005). Since their
turnover and lifespan are much longer than those of their
prey, primary consumers integrate the temporal isotopic
variation of their food sources (Post, 2002). Thus, they
can be used as an isotopic baseline to calculate the
reliance of the upper consumers on the benthic affinity
component (Vander Zanden and Vadeboncoeur, 2002;
Sherwood and Rose, 2005).
4.4. Trophic groups
The feeding behaviors of different species are
important elements in the complex relationships that
emerge from stable isotope analyses, especially in
benthic invertebrate communities where a wide range
of isotopic signatures and feeding modes are present
(Davenport and Bax, 2002). The clustering of species in
trophic guilds provides synthetic information to under-
stand the trophic structure of the community. In our
study, both due to sampling and diversity of feeding
modes within the primary consumers, some trophic
groups are comprised of only few species or/and indi-
viduals. This low number of analyses may limit the
significance of some of the clustering. Nevertheless, the
large range of the isotopic signatures allows discrimina-
tion between the food sources of different species as the
variability of isotopic signatures within species is much
lower than the variability among species. Thus, suspen-
sion feeders are divided into three functional groups
according to their δ13C values, revealing a wide diet
spectrum. The first group (C1-WCSF, TL 2) clusters
zooplankton and suprabenthos (mainly Euphausiids) that
30 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34
feed in the water column with δ13C values indicating a diet
based on POM. The second group groups polychaetes,
bivalves and crustaceans (C1-BSF). It shows highly
enriched δ13C signatures close to those measured for the
surface-selective deposit feeders (C1-DF), suggesting that
some benthic suspension feeders and surface deposit
feeders exploit the same food source. Since no primary
production can occur on the sediment surface at a mean
depth of 100 m on the continental shelf, we must consider
that bottom organic matter is a mixture of different
components, originating either from recently sedimented
pelagic production more or less enriched by the bacterial
loop or from benthic detrital secondary production. Thus,
the diet of the C1-DF and C1-BSF groups is composed of
this mixture of detrital material mainly originating from
pelagic sedimented organic matter. The differences
between species of C1-DF and C1-BSF groups are mainly
attributed to differences in feeding mode and anatomy
(i.e. suspension feeders capture particles in suspension in
the interface water whereas selective deposit feeders
ingest the interface superficial film). Finally, the third
suspension feeder group (C1-int) had intermediate δ13C
values suggesting a mixed diet based on both POM and
detrital organic matter.
Surprisingly close δ15N values between POM and
some benthic suspension feeders are measured in the
Grande Vasière as well as in the Ditrupa sand
communities. In particular the Pectinidae bivalves
have very low TL values (TL 1.1 for C. septemradiata
and Pecten maximus), close to those observed for the
polychaete D. arietina (TL 1.5). Similar results were
found on continental shelf communities for benthic
suspension feeders and POM on the Georges Bank (Fry,
1988) and on the Arctic Canadian Basin (Iken et al.,
2005). According to these authors, such low TL cannot
be fully explained by fractionation patterns (Iken et al.,
2005). Some suspension feeders may not assimilate bulk
bottom POM nor bulk detrital organic matter but they
may base their diet on particles selected on the basis of
size and/or biochemical quality, as revealed by their
isotopic composition (Rau et al., 1990; Raikow and
Hamilton, 2001). Furthermore, the diets of some
suspension feeding bivalves such as mussels or cockles
are not only based on suspended organic particles (i.e.
phytoplankton, resuspended deposited material, micro-
heterotrophs and bacteria, Kang et al., 1999; Kreeger
and Newell, 1996, 2001), but also on dissolved organic
carbon (Roditi et al., 2000). These low δ15N values
within some benthic suspension feeders reveal the
complex pathways at the base of the continental shelf
benthic food webs and highlight the capacity of the
primary consumers to consume different food sources,
which favor a high species diversity within the sus-
pension feeders.
Spatial/vertical segregation of the food quality is also
revealed by the three suspension feeder groups: (1) a
group that feed on recently produced material in the
water column (2) an intermediate group composed of
erect epifauna which can feed on both sources and
(3) the detrital benthic layer feeders. Such spatial
segregation within the benthic suspension feeder groups
has already been shown (Le Loc'h and Hily, 2005; Grall
et al., 2006) revealing the diversity of the feeding
strategies and the specific adaptations to the various
food sources available. Therefore, a species trophic
position must be carefully considered in energy budget
analyses and community functional analyses, as beha-
vioral and anatomical organs features are not sufficient
to place a species in a specific trophic group.
The third trophic level of the food web (i.e. the
secondary consumers: predators) are also divided into
three groups based on their RBAP which revealed
different feeding strategies in relation to their spatial
localization on the bottom (i.e. endo- or epifauna).
Indeed, the first group (C2-PAF) is composed of a mix
of species with different feeding strategies: from the
swimming, opportunistic scavenger N. borealis to the
epi-benthic, omnivorous polychaete Aponuphis tubicola
and the benthic carnivorous fish A. laterna. All of them
are able to capture pelagic prey. In contrast, the second
group (C2-BAF) clusters both sub-surface deposit
feeders and endo-benthic or burrowing predators
that capture their prey at the surface or in the sediment.
Sub-surface deposit feeders such as the polychaete
D. gajolae ingest detrital organic matter, micro- and
meio-fauna (Fauchald and Jumars, 1979) while the
predators of this functional group such as the crustacean
N. norvegicus capture benthic macrofauna (Cristo,
1998). The last secondary consumer group includes
the majority of the benthic and demersal fishes and
carnivorous crustaceans and polychaetes. It is consid-
ered as an intermediate group (C2-int) because the
species which are regrouped have RBAP values
intermediate between those of the two others groups
and a slightly higher TL. This trophic position high-
lights the opportunities these predators have to catch
either benthic or pelagic prey.
Finally, the top predators, the benthic fish S. solea
and the polychaete G. rouxii, occupy the fourth TL
on the Grande Vasière. These nitrogen isotopic
signatures are even higher than those of other marine
predators such as dolphins of the Bay of Biscay (Das
et al., 2000), but lower than those of the tope shark
collected in the adjacent Celtic Sea (Domi et al., 2005).
 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34
This highest trophic level occupied by a benthic
invertebrate such as a polychaete appears as a general
feature within benthic continental shelf communities
(Davenport and Bax, 2002; Hobson et al., 2002;
Sherwood and Rose, 2005).
Very similar trophic groups were identified from the
Grande Vasière and the Ditrupa sand benthic commu-
nities, with only slight differences mainly concerning
the suspension feeders. Indeed, the water column
suspension feeders sampled on the Ditrupa sand
community had a higher TL than on the Grande Vasière.
These differences may be partly explained by the
hydrological features of each study site. As for the
benthic communities, the Grande Vasière and the
external margin represent two different hydrological
patterns over the Bay of Biscay which influence the rate
and the nature of the pelagic biological production
(Planque et al., 2004; Puillat et al., 2004). Thus, the
isotopic seasonal variability of the primary producers is
probably associated with the time lag required for a
consumer to reflect the isotopic signature of its diet,
(Vizzini and Mazzola, 2003; Matthews and Mazunder,
2005) and may explain the zooplankton TL 2.4
(calculated from POM isotopic signature). Indeed, our
POM isotopic sampling did not allow integration of the
temporal variability of the POM isotopic composition,
in contrast to that of the consumers.
4.5. Food web structure
Our results show that macrofaunal benthic primary
consumers are the second major trophic group in terms
of biomass, with a domination of the surface deposit
feeders on the Grande Vasière, while the suspension
feeders dominate on the external margin. Taking into
account the higher benthic biomass on the external
margin, we hypothesize that this different trophic
organization between the two benthic communities
reveals the existence of an additional trophic input on
the external margin both in term of quantity and sea-
sonality. Indeed, on the continental shelf break, internal
tidal waves could induce a vertical flux of nutrients
towards the surface layers resulting in phytoplankton
production (Holligan and Groom, 1986). In the Bay
of Biscay, this shelf break, surface primary production
has already been detected (Lampert et al., 2002) and
higher organic matter sedimentation was measured on
the external margin than on the Grande Vasière (Le
Loc'h, 2004). Because suspension feeder biomass is 15
times higher on the external margin, we suggest that
in addition to sedimentation of the continental shelf
primary production, the primary production generated
31
at the shelf break supplies the benthic community of
the external margin. Furthermore, the Grande Vasière
site received its maximum trophic inputs via sedimen-
tation of the pelagic primary production from March to
June, while they are minimum in summer when strati-
fication is established and in winter when primary pro-
duction is weak (Loyer et al., 2006) thus affecting the
benthic food web structure of the Grande Vasière (Le
Loc'h, 2004).
The secondary consumers of benthic affinity, mainly
dominated by the sub-surface deposit feeders, occupied
the major trophic position within the macrobenthic
biomass of both communities. In contrast, the secondary
consumers of pelagic affinity feeders are scarce which
reveals the importance of the detrital pathways for
offshore continental shelf benthic communities. This
contrasts with coastal benthic ecosystems where the
majority of the benthic biomass is trapped in the filter
feeders group supplied by both pelagic and benthic
primary production (Grall et al., 2006).
Predators of the benthic community feed to an
increasing degree in the pelagic zone as they increase in
their trophic position. This could be a general trend of
the continental shelf benthic and demersal ecosystems
and this could be linked to the higher degree of mobility
of the top predators. This is well know in the Bay of
Biscay for top-predator fish such as monkfish or hake
that have a piscivorous diet composed of demersal and
pelagic fishes (Pereda and Olaso, 1990; Guichet, 1995),
but was not previously shown for benthic invertebrates
and for the whole community. Thus it can be concluded
that trophic coupling between benthic and pelagic food
webs exists either through the consumption of pelagic
primary production by benthic suspension feeders and
through the ingestion of pelagic affinity prey by benthic
top predators.
5. Conclusions
This study demonstrated that measurements of stable
isotopes (carbon and nitrogen) constitute an additional
means of understanding the trophic structure of an
ecosystem and tracing its energy flow. In conclusion, our
results provide a novel contribution to the knowledge of
the role of detrital pathways in the carbon cycling within
the benthic trophic web of the continental shelf.
Acknowledgments
This study was funded by the CNRS, University of
Brest and IFREMER. The authors are grateful to the
crews of the RV Côtes de la Manche and Thalassa for
32 F. Le Loc'h et al. / Journal of Marine Systems 72 (2008) 17–34
their assistance in collecting samples, to C. Scrimgeour
and N. Naulet for running samples, Alphonse Tram,
Daniel Guichard, Albert Quentin and Robert Marc. The
manuscript was greatly improved by the comments of
anonymous reviewers.
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