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Conservation Biology, Pages 1686–1690Volume 15, No. 6, December 2001

Effect of the Introduced Common Slipper Shell on the Suprabenthic Biodiversity of the Subtidal Communities in the Bay of Saint-Brieuc

CAROLE VALLET,*†† JEAN-CLAUDE DAUVIN,† DOMINIQUE HAMON,‡ AND CHRISTINE DUPUY§

*Laboratoire de Biologie des Invertébrés Marins et Malacologie, UPRESA 8044, 57 rue Cuvier, Muséum National d’Histoire Naturelle, F-75005 Paris, France†Station Marine de Wimereux, 28 avenue Foch, BP 80, UPRES A 8013 ELICO, 62930 Wimereux, France‡IFREMER, Centre de Brest, B.P. 70, F-29280 Plouzané, France§CNRS/IFREMER CREMA, B.P. 5, F-17137 L’Houmeau, France

Abstract:

Our study compared the suprabenthic fauna collected in the Bay of Saint-Brieuc (western EnglishChannel) in September 1995 and May 1996 at two sites colonized by

Crepidula fornicata

with that of one sitewhere it was absent (site 23–0). Where

Crepidula

was present, no species dominated and abundance re-mained low. At the site without

Crepidula

, abundance was higher and the mysid

Haplostylus lobatus

domi-nated the suprabenthic community. Swimming activity of most suprabenthic species was increased by thepresence of

C. fornicata

. The differential abundance and swimming activity of certain species are linked to theconversion of the formerly soft substrate to now hard, shelled substrate.

Efecto de la Introducción de

Crepidula

fornicata sobre

la Biodiversidad Suprabéntica de las ComunidadesSubmareas en la Bahía de Saint-Brieuc (Canal Inglés del Oeste)

Resumen:

Examinamos la fauna suprabéntica colectada en la Bahía de Saint-Brieuc (Canal Inglés delOeste) en septiembre de 1995 y mayo de 1996 en dos sitios colonizados por

Crepidula fornicata

y en un sitiodonde se encontraba ausente (sitio 23-0). En los sitios donde

Crepidula

se encontraba presente, no había espe-cies que dominaran y la abundancia de especies era baja. En el sitio sin

Crepidula

, la abundancia fue mayory el mísido

Haplostylus lobatus

dominó la comunidad suprabéntica. La actividad de nado de la mayoría delas especies suprabénticas se incrementó con la presencia de

C. fornicata

. Nuestros resultados sugieren unaabundancia y actividad de nado diferencial de ciertas especies vinculada a la conversión de un sustrato ini-

cialmente suave a uno duro, cubierto de conchas.

Introduction

Biological invasions can have a variety of cascading ef-fects in the marine environment (Bertness 1984; Ceccher-elli & Cinelli 1997; Byers 2000; Grosholz et al. 2000), in-cluding interspecific competition, predation, disturbance,

and alterations in energy flow and in the overall equilib-rium of species previously present in the invaded com-munity.

The common slipper shell (

Crepidula fornicata

) wasintroduced on the French coast by accidental transportat the end of World War II, and in later years by de-liberate introduction with the oyster

Crassostrea gigas

( Blanchard 1995; Minchin et al. 1995). From 1974 to1978, the density of

C. fornicata

increased from rare,isolated individuals found in the southwestern part ofthe Bay of Saint-Brieuc in oysterbed areas to 0.07 individ-

††

Current address: Laboratory of Biological Oceanography, Depart-ment of Bioengineering, Faculty of Engineering, Soka University,1–236 Tangi-cho, Hachioji-shi, Tokyo 192–8577, JapanPaper submitted June 14, 1999; revised manuscript accepted Febru-ary 28, 2001.

Conservation BiologyVolume 15, No. 6, December 2001

Vallet et al. Effects of Common Slipper Shell on Suprabenthic Biodiversity

1687

uals m

�

2

throughout the bay ( Dupouy & Latrouite 1979).In 1994, its stock was estimated about 250,000 tonnes(wet weight with shells) in the whole bay (800/ km

2

).Biomass and abundance reached about 1.96 kg m

�

2

and306 individuals m

�

2

in areas where

Crepidula

covered

�

70% of the seabottom benthos ( Blanchard 1995). Bio-mass and abundance were

�

0.02 kg m

�

2

and 3 individ-uals m

�

2

in areas where

Crepidula

covered

�

5% of thesea bottom ( Blanchard 1995).

By removing a huge volume of suspended organic ma-terial from the water column,

C. fornicata

deposits thatfiltered material on the bottom as pseudofeces and thusalters sediment characteristics. De Montaudouin et al.(1999) and de Montaudouin and Sauriau (1999) haveshown, however, that the presence of

C. fornicata

doesnot affect the benthic community and a spatial competi-tion with other macrozoobenthic species didn’t occur,but the habitat becomes more heterogeneous. We cantherefore hypothesize that

C. fornicata

creates novelthree-dimensional episurface structures that can provideincreased habitat heterogeneity on an otherwise softbottom, including hard-surface areas and/or crevices,holes, or cracks for the colonization of sessile and vagilespecies. We sought to estimate the differences of (1) fau-nal composition and (2) quantitative composition anddiversity in the suprabenthic fauna, as defined by Brunelet al. (1978), in the Bay of Saint Brieuc (western EnglishChannel), between areas colonized and areas not colo-nized by

C. fornicata.

Methods

Suprabenthic Sampling

In the Bay of Saint-Brieuc, three sites ( Table 1) werechosen in which to sample suprabenthic fauna. Two ofthem had abundant populations of

C. fornicata

(desig-nated as sites 12–Cf and 23–Cf ), whereas it was absentfrom the other location (site 23–0) because of extensivedredging related to fishery activities ( Blanchard 1995).

Station numbers refer to the depth in meters and Cf or0 refer to presence or rare/absence of

Crepidula forni-

cata

, respectively. Both sites 12–Cf (48

�

35.9

�

N-2

�

37.5

�

W)and 23–Cf (48

�

41.8

�

N-2

�

50.5

�

W) were located on muddy,fine sand substrate. The sediment of site 23–0 (48

�

39.5

�

N-2

�

40.2

�

W ) was medium sand.We collected two series of samples to compare the

species number, abundance, and diversity in two peri-ods: spring (four hauls at sites 12–Cf and 23–0, and fiveat site 23–Cf ) and summer (five hauls at each site) ( Ta-ble 3). Suprabenthic fauna were sampled with a Macer-GIROQ sledge ( Dauvin & Lorgeré 1989). Four 0.6-m-wide boxes were superposed at 0.10–0.40 (net 1), 0.45–0.75 (net 2), 0.80–1.10 (net 3), and 1.15–1.45 m (net 4)above the sea bed, each fitted with a plankton net ofthe 500-

�

m mesh size ( Dauvin et al. 2000). A Tsurimi-Seiki-Kosakusho flowmeter in each box measured thevolume of water filtered. The mean speed, during early15-mn-long hauls against the tide, was 1.5 knots. Theabundance of individuals of each species in each haulwas standardized to 100 m

3

( Vallet & Dauvin 1999).

General Fauna and Biocoenotic Characteristics

A Mann-Whitney

U

test (Scherrer 1984) was used to deter-mine if there were significant differences between averageabundance in the three sites over each season. Diversitywas calculated as Shannon’s index

H

�

and Pielou’s even-ness,

J

, for each date and for each site (Scherrer 1984).We classified collected species biocoenotically using

constancy and fidelity indices (Retière 1979) in order togroup species according to habitat preference. The con-stancy (CI ) and fidelity (FI ) indices were calculated asfollows:

CI

a

/t

i

�

(

N

a

/ti/

N

t

/ti

)

100,FI

a

/t

X

�

(CI

a

/t

X

/CI

a

/ti

)

100,

where

N

a

/ti

is the number of hauls where species

a

waspresent at site

i

, and

N

t

/ti

is the total number of haulssampled at site

i

.

Correspondence Analysis

We conducted a correspondence analysis (Benzecri 1973)and hierarchical classification ( Jambu & Lebeaux 1978)

Table 1. Main characteristics of the three sampling sites during spring and summer in the Bay of Saint-Brieuc (D.H., personal observation).*

Site (code)

Characteristic Dahouet (12–Cf ) Le Palus (23–Cf ) Centre Baie (23–0)

Depth (m) 12 23 23Location lat. 48

�

35.9 N, long. 2

�

37.5 W lat. 48

�

41.8 N, long. 2

�

50.5 W lat. 48

�

39.5 N, long. 2

�

40.2 WType of sediment muddy, fine sand muddy, fine sand medium sandSea bottom covered

by

Crepidula

( %)

�

70

�

70

�

5

Average biomass of

Crepidula

( kg m

�

2

)1.956 1.956 0.02

*

The Cf and 0 refer to presence or rare/absence of

Crepidula fornicata

, respectively.

1688

Effects of Common Slipper Shell on Suprabenthic Biodiversity Vallet et al.

Conservation BiologyVolume 15, No. 6, December 2001

of the 24 main species showing abundance of

�

5 indi-viduals 100 m

�

3

in at least one site during one season.Analysis of all species collected gave similar results, so,for simplicity, only analysis of the 24 main suprabenthicspecies is presented.

Swimming Activity

Swimming activity was measured for each species withthree coefficients: K

1

�

NF2/N

t

; K

2

�

NF3/N

t

; K

3

�

NF4/N

t

, where NF2, NF3 and NF4 are the abundance innets 2, 3, and 4 respectively (100 m�3), and Nt is totaldensity (400 m�3). Each species was classified accordingto its swimming coefficient into five groups from the su-prabenthic species with the strongest swimming activity(group 1, K1 � K2 � K3, � 0.25) to the suprabenthicspecies with the weakest swimming activity (group 5,K1 � K2 � K3, K3 � 0.10) ( Table 2) (see Dauvin et al.2000).

Results

General Fauna and Biocoenotic Characteristics

The total fauna included 162 suprabenthic species with129 species in spring and 128 in summer. The total num-ber of species ranged from a minimum at site 12–Cf inspring to a maximum at site 23–Cf in spring ( Table 3).At each season, mean total abundance was significantlyhigher at site 23–0 than at sites 12–Cf and 23–Cf (U test;p � 0.05).

Diversity was high during spring at all sites, whereasin summer it was high only at sites 12–Cf and 23–Cf ( Ta-ble 3). In summer, the low diversity at site 23–0 was es-sentially due to a high abundance of three species, themysids Haplostylus lobatus and Anchialina agilis andthe cumacean Pseudocuma longicornis) Site 12–Cfshowed similar values of evenness ( J ) during both sea-sons, whereas at sites 23–Cf and 23–0 values of evennessdecreased from spring to summer ( Table 3).

Among the 24 main suprabenthic species, 22 werepresent in all sites, the amphipod Tmetonyx similis wasfound only at deeper sites (23–Cf and 23–0), and thegnathiid isopod only at site 23–Cf. The mysid Haplosty-lus lobatus dominated the suprabenthic fauna at site23–0, whereas at sites 12–Cf and 23–Cf no species domi-nated and average abundance remained at �100 individ-uals 100 m�3.

Biocoenotic analyses showed that most suprabenthicspecies, which were constant in sites with Crepidula,were occasional, rare, or absent at sites without Crepid-ula, especially the decapods Hippolyte varians, Eualusoccultus, Pandalina brevirostris, Pisidia longicornis,and Liocarcinus sp.

Correspondence Analysis

The correspondence analysis on the 24 main suprabenthicspecies showed a good separation of sites: groups I and IIcharacterized site 23–0 in summer and spring, respec-tively, whereas group III combined both sites 23–Cf and12–Cf. Each site was represented by a group of partic-ular species (Fig. 1): group A for site 23–0 in summer,group B for sites 23–Cf (summer and spring) and 12–Cf(summer), and group C for sites 23–0 and 12–Cf in spring.

Among the 24 main species, 20 species were found inspring and 21 in summer ( Table 2). For both seasons,swimming activity was higher at sites 12–Cf and 23–Cfthan at site 23–0. At site 23–0, 80% (in spring) and 87%(in summer) of species showed low or very low swim-ming activity (swimming groups 4 and 5).

Discussion

In the Bay of Saint-Brieuc, the presence of C. fornicatacould have a major effect on the suprabenthic commu-nity by increasing species number and diversity. We haveshown that when C. fornicata occurred in high abun-dance, any suprabenthic species dominated the fauna

Table 2. Percentage of species, with abundance �5 individuals 100 m�3 in each site (12-Cf, 23-Cf, 23-0) at each season, present in each swimming group (K1, K2, K3: swimming activity coefficient).

Spring (20)* Summer (21)*

12–Cf 23–Cf 23–0 12–Cf 23–Cf 23–0

No. of species per site 9 14 15 10 14 15Swimming groups

1: K1 � K2 � K3 � 0.25 22.2 21.4 0 20 28.6 6.72: K1 � K2 K3� K3 � 0.31 22.2 21.4 20 10 0 6.73: K1 � K2 � 0.25 � K3 22.2 7.2 0 20 7.1 04: K1 � K2 � K3, K3 � 0.10 0 21.4 26.7 20 28.6 33.35: K1 � K2 � K3, K3 � 0.10 33.4 28.6 53.3 30 35.7 53.3

*Total number of species in parentheses.

Conservation BiologyVolume 15, No. 6, December 2001

Vallet et al. Effects of Common Slipper Shell on Suprabenthic Biodiversity 1689

and their abundance remained low. Zouhiri et al. (1998),Vallet and Dauvin (1999), and Dauvin et al. (2000) havepointed out that in the Normano-Breton Gulf on coarsesand and pebble substrates, no species dominated andabundance was low, as we also observed on sites 23–Cfand 12–Cf. At medium-sand site 23–0, however, the mysidHaplostylus lobatus dominated during both seasons, withabundance increasing from spring to summer. A similarpattern was seen at two other medium-sand sites in the En-glish Channel, where mysids Schistomysis ornata off ofPlymouth and Gastrosaccus spinifer in the Dover Straitdominated, with abundance increasing from spring to sum-mer (Zouhiri et al. 1998; Dauvin et al. 2000). Brown and

Talbot (1972) and Mauchline (1980) showed that mysidsof the genus Gastrosaccus burrowed more frequentlyinto medium sand than into fine sand, gravels, and peb-bles. The mysid H. lobatus was abundant at site 23–0without Crepidula. It could not burrow easily at siteswhere Crepidula was present, because of the density ofshells on the bottom at those sites. Suprabenthic speciesshow higher swimming activity at Crepidula sites for thesame reason. This behavior has also been observed at apebble site in the Dover Strait in the English Channel(Dauvin et al. 2000), where most species showed highswimming activity because they could not burrow intothe substrate.

Table 3. Number of species, mean abundance (individuals 100 m�3), Shannon diversity (H�) and, evenness ( J ) from three sites (12-Cf, 23-Cf, 23-0) of the Bay of Saint-Brieuc.

Spring Summer

12–Cf 23–Cf 23–0 12–Cf 23–Cf 23–0

No. of species 71 102 74 69 98 81Mean abundance 99 69 429 217 295 1435Diversity (H� ) 3.44 4.87 3.33 3.58 3.59 2.04Evenness ( J ) 0.56 0.73 0.54 0.58 0.54 0.32

Figure 1. Results of the correspondence analysis according to the first two axes with an identification of the inertia groups defined by automatic hierarchical classification, I, II, III; groups of sites, A, B, C; groups of species, 12–Cf is Dahouët, 23–Cf is Le Palus, and 23–0 is Centre Baie; (SU, summer; SP, spring; amsp: Ampelisca spinipes; amso: Am-pelisca spooneri; amte: Ampelisca tenuicornis; amty: Ampelisca typica; atve: Atylus vedlomensis; trgi: Tritaeta gibbosa; orhu: Orchomene humilis; orna: Orchomenella nana; tmsi: Tmetonyx similis; meag: Megaluropus agilis; mosu: Monoc-ulodes subnudus; pelo: Perioculodes longimanus; syma: Synchelidium maculatum; anag: Anchialina agilis; halo: Haplo-stylus lobatus; mygi: Mysidopsis gibbosa; sicl: Siriella clausii; bosc: Bodotria scorpioides; euem: Eudorella emarginata; pslo: Pseudocuma longicornis; eupu: Eurydice pulchra; gnox: Gnathia oxyuraea; gnat: Gnathiidae; neba: Nebalia bipes).

1690 Effects of Common Slipper Shell on Suprabenthic Biodiversity Vallet et al.

Conservation BiologyVolume 15, No. 6, December 2001

Moreover, most species with very strong swimmingactivity at sites 23–Cf and 12–Cf were detritivores or om-nivores, and few species with very low swimming activ-ity were carnivores or scavengers ( personal observation).The latter were often decapods, which were occasionalor rare species at site 23–0. This suggests that, for slowswimmers such as decapods, dead and live individualshells of C. fornicata provide new habitats where theycan hide.

When C. fornicata is not present, certain suprabenthicspecies (such as mysids) are more abundant and swim-ming activity is greatly decreased, which we believe arecorrelated with the conversion of a previous soft-bottomhabitat to a hard, shelly bottom, preventing use of thesoft substrate by suprabenthic species. Although the con-trast in abundance at sites with and without C. fornicatais significantly different between spring and summer, in-terpretation is limited by the number of sites we studied.We suggest additional sites with and without Crepidulabe examined and that experimental studies be under-taken.

Acknowledgments

This study was part of the French Programme National“Biodiversité.” We thank the crew of the OceanographicVessel Le Thalia of the Centre Informatique du Muséumfor help with factorial analysis, K. Ghertsos for help withproof reading, and J. T. Carlton for very useful com-ments on this note.

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