Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-19T08:30:27.776Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasite co-infection of two sympatric bivalves, the Manila clam (Ruditapes philippinarum) and the cockle (Cerastoderma edule) along a latitudinal gradient

Published online by Cambridge University Press:  17 May 2007

Géraldine Lassalle ,
Xavier deMontaudouin ,
Philippe Soudant  and
Christine Paillard
Géraldine Lassalle
Affiliation:
Université Bordeaux 1 – CNRS – UMR EPOC 5805 – Station marine d'Arcachon, 2 rue du Professeur Jolyet, 33120 Arcachon, France
Xavier deMontaudouin
Affiliation:
Université Bordeaux 1 – CNRS – UMR EPOC 5805 – Station marine d'Arcachon, 2 rue du Professeur Jolyet, 33120 Arcachon, France
Philippe Soudant
Affiliation:
Institut Universitaire Européen de la Mer, Laboratoire des sciences de l'environnement marin – LEMAR, UMR 6539 Université de Bretagne Occidentale-CNRS, Technopôle Brest-Iroise, Place Nicolas Copernic, 29280 Plouzané, France
Christine Paillard
Affiliation:
Institut Universitaire Européen de la Mer, Laboratoire des sciences de l'environnement marin – LEMAR, UMR 6539 Université de Bretagne Occidentale-CNRS, Technopôle Brest-Iroise, Place Nicolas Copernic, 29280 Plouzané, France
Get access

Abstract

Among the potential biotic factors affecting population dynamics, parasitism has received relatively little attention. The purpose of this study was to inventory marine bivalve parasites and to investigate relations between different parasite communities. Five intertidal stations along the French Atlantic shore were studied between Brittany and Arcachon Bay. Two bivalves (the edible cockle, Cerastoderma edule, and the Manila clam, Ruditapes philippinarum) were sampled and examined. The parasites included a bacterium (Vibrio tapetis), a protozoan (Perkinsus sp.), and digenetic trematode metacercariae (10 species). Perkinsus sp. prevalence and density in clams were higher than those measured in cockles (30 250 vs. 36 cells g−1 of gill wet weight, respectively) while digeneans were more common in cockles (46 metacercariae per cockle host vs. 1 per clam host). Distributions of digeneans and Perkinsus sp. were similar along the Atlantic shore. However, at each sampling station and at the individual scale, no correlation between Perkinsus sp. and digenean abundance was detected. These results suggest different ecological niches used by these two parasites within a community of bivalves but a similar response to environmental factors such as temperature and salinity. Vibrio tapetis was found at relatively high prevalence in all stations for both bivalve species (from 17% to 43% in cockles and from 23% to 50% in clams), but was associated with a low prevalence of Brown Ring Disease (BRD), a shell disease caused by this pathogen. No statistically significant relationship of these parasitic bacteria with trematodes and Perkinsus sp. was evidenced in the present study.

Keywords

Bivalve molluscDigeneaParasitesHost specificityInfectivityNE Atlantic Ocean
Type
Research Article
Information
Aquatic Living Resources , Volume 20 , Issue 1: New developments in coastal environment research: results from the national coastal environment program , January 2007 , pp. 33 - 42
Copyright
© EDP Sciences, IFREMER, IRD, 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andrew, J.D., Hewatt, W.G., 1957, Oyster mortality studies in Virginia: II. The fungus disease caused by Dermocystidium marinum in oysters of Chesapeake Bay. Ecol. Monogr. 27, 1-25. CrossRef
Auzoux-Bordenave, S., Vigario, A.M., Ruano, F., Domart-Coulon, I., Doumenc, D., 1995, In vitro sporulation of the clam pathogen Perkinsus atlanticus (Apicomplexa, Perkinsea) under various environmental conditions. J. Shellfish Res. 14, 469-475.
Bachelet, G., Simon-Bouhet, B., Desclaux, C., Garcia-Meunier, P., Mairesse, G., de Montaudouin, X., Raigne, H., Randriambao, K., Sauriau, P.G., Viard, F., 2004, Invasion of the eastern Bay of Biscay by the nassariid gastropod Cyclope neritea: origin and effects on resident fauna. Mar. Ecol. Prog. Ser. 276, 147-159. CrossRef
Bartoli, P., 1981, Démographie et phénomène de compétition intraspécifique des Gymnophallidae Morozov chez les deuxièmes hôtes intermédiaires (Trematoda, Digenea). Ann. Parasitol. 56, 33-44.
Bowers, E.A., Bartoli, P., Russel-Pinto, F., James, B.L., 1996, The metacercariae of sibling species of Meiogymnophallus, including M. rebecqui comb. nov. (Digenea: Gymnophallidae), and their effects on closely related Cerastoderma host species (Mollusca: Bivalvia). Parasitol. Res. 82, 505-510. CrossRef
Calvo-Ugarteburu, G., McQuaid, C.D., 1998a, Parasitism and introduced species: epidemiology of trematodes in the intertidal mussels Perna perna and Mytilus galloprovincialis. J. Exp. Mar. Biol. Ecol. 220, 47-65. CrossRef
Calvo-Ugarteburu, G., McQuaid, C.D., 1998b, Parasitism and invasive species: effects of digenetic trematodes on mussels. Mar. Ecol. Prog. Ser. 169, 149-163. CrossRef
Casas S.M., 2002. Estudio de la perkinsosis en la almeja fina Tapes decussatus (Linnaeus, 1758), de Galicia. PhD Thesis, University of Santiago de Compostela, Spain.
Choi, K.S., Wilson, E.A., Lewis, D.H., Powell, E.N., Ray, S.M., 1989, The energetic cost of Perkinsus marinus parasitism in oysters: quantification of the thioglycollate method. J. Shellfish Res. 8, 125-131.
de Montaudouin, X., Kisielewski, I., Bachelet, G., Desclaux, C., 2000, A census of macroparasites in an intertidal bivalve community, Arcachon Bay, France. Oceanol. Acta 23, 453-468. CrossRef
Desclaux C., 2003. Interactions hôtes-parasites: diversité, mécanismes d'infestation et impact des trématodes digènes sur les coques Cerastoderma edule (mollusque bivalve) en milieu lagunaire macrotidal. Thèse de Doctorat, Université Bordeaux I.
Desclaux, C., de Montaudouin, X., Bachelet, G., 2002, Cockle emergence at the sediment surface “favourization” mechanism by digenean parasites? Dis. Aquat. Org. 52, 137-149. CrossRef
Desclaux, C., Russell-Pinto, F., de Montaudouin, X., Bachelet, G., 2006, First record and description of metacercariae of Curtuteria arguinae n. sp. (Digenea: Echinostomatidae), parasite of cockles Cerastorderma edule (Mollusca: Bivalvia) in Arcachon Bay, France. J. Parasitol. 92, 578-587. CrossRef
Drummond L.C., Balboa S., Beaz R., Mulcahy M.F., Barja J.L., Culloty S.C., Romalde J.L., 2007, The susceptibility of Irish-grown and Galician-grown Manila clams, Ruditapes philippinarum, to Vibrio tapetis and Brown Ring Disease. J. Invertebr. Pathol.
Drummond, L.C., O'Reilly, P., Mulcahy, M.F., Culloty, S.C., 2006, Comparison of techniques for diagnosis of Brown Ring Disease and detection of Vibrio tapetis in the Manila clam, Venerupis (Ruditapes) philippinarum. J. Shellfish Res. 25, 1043-1049.
Dungan, C.F., Hamilton, R.M., 1995, Use of a tetrazolium-based cell proliferation assay to measure effects of in vitro conditions on Perkinsus marinus (Apicomplexa) proliferation. J. Eukaryot. Microbiol. 42, 379-388. CrossRef
Flasch, J.P., Leborgne, Y., 1992, Introduction in Europe, from 1972 to 1980, of the manila clam (Tapes philippinarum) and effects on aquaculture production and natural settlement. ICES J. Mar. Sci. 194, 92-96.
Fredensborg, B.L., Mouritsen, K.N., Poulin, R., 2004, Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. J. Exp. Mar. Biol. Ecol. 311, 253-265. CrossRef
Fredensborg, B.L., Poulin, R., 2005, Larval helminths in intermediate hosts: Does competition early in life determine the fitness of adult parasites? Int. J. Parasitol. 35, 1061-1070.
Jensen, K.T., Castro, N.F., Bachelet, G., 1999, Infectivity of Himasthla spp. (Trematoda) in cockle (Cerastoderma edule) spat. J. Mar. Biol. Assoc. UK 79, 265-271. CrossRef
Kuris, A.M., Lafferty, K.D., 1994, Community structure: Larval trematodes in snail hosts. Annu. Rev. Ecol. Syst. 25, 189-217. CrossRef
Lauckner, G., 1971, Zur trematodenfauna der herzmuscheln Cardium edule und Cardium lamarcki. Helgol. Meeresunters 22, 377-400. CrossRef
Lauckner G., 1983, Disease of Mollusca: Bivalvia. In: Kinne O. (Ed) Disease of Marine Animals, Biologische Anstalt Helgoland, pp. 477-961.
Lauckner, G., 1984, Impact of trematode parasitism on the fauna of the North Sea tidal flat. Helgol. Meeresunters 37, 185-199. CrossRef
Maes P., Paillard C., 1992, Effect du Vibrio P1, pathogène de Ruditapes philippinarum, sur d'autres espèces de bivalves. Les Mollusques marins, Biologie et Aquacultures. Ifremer, Actes de Colloques 14, 141-148.
Margolis, L., Esch, G.W., Holmes, J.C., Kuris, A.M., Schad, G.A., 1982, The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). J. Parasitol. 68, 131-133. CrossRef
Mouritsen, K.N., 2002, The Hydrobia ulvae-Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. J. Helminthol. 76, 341-347. CrossRef
Mouritsen, K.N., Jensen, K.T., 1997, Parasite transmission between soft-bottom invertebrates: Temperature mediated infection rates and mortality in Corophium volutator. Mar. Ecol. Prog. Ser. 151, 123-134. CrossRef
Ngo, T.T.T., Choi, K.S., 2004, Seasonal changes of Perkinsus and Cercaria infections in the Manila clam Ruditapes philippinarum from Jeju, Korea. Aquaculture 239, 57-68. CrossRef
Paillard C., 1992. Etiologie et caractérisation de la maladie de l'anneau brun chez la palourde d'élevage, Ruditapes philippinarum. Thèse de Doctorat, Université de Brest.
Paillard, C., 2004, A short-review of brown ring disease, a vibriosis affecting clams, Ruditapes philippinarum and Ruditapes decussatus. Aquat. Living Resour. 17, 467-475. CrossRef
Paillard, C., Ashton-Alcox, K.A., Ford, S.E., 1996, Changes in bacterial densities and hemocyte parameters in oysters affected by Juvenile Oyster Disease. Aquat. Living Resour. 9, 145-158. CrossRef
Paillard, C., Gausson, S., Nicolas, J.L., Le Pennec, J.P., Haras, D., 2006, Molecular identification of Vibrio tapetis, the causative agent of the brown ring disease of Ruditapes philippinarum. Aquaculture 253, 25-38. CrossRef
Paillard, C., Maes, P., 1994, Brown Ring Disease in the Manila clam Ruditapes Philippinarum – Establishment of a classification system. Dis. Aquat. Org. 19, 137-146. CrossRef
Paillard, C., Maes, P., 1995a, The Brown Ring Disease in the Manila clam, Ruditapes Philippinarum .1. Ultrastructural alterations of the periostracal lamina. J. Invertebr. Pathol. 65, 91-100.
Paillard, C., Maes, P., 1995b, The brown ring disease in the Manila clam, Ruditapes philippinarum: II. Microscopic study of the brown ring syndrome. J. Invertebr. Pathol. 65, 91-100.
Paillard, C., Maes, P., Oubella, R., 1994, Brown ring disease in clams. Annu. Rev. Fish Dis. 4, 219-240. CrossRef
Ray, S.M., 1952, A culture technique for the diagnosis of infections with Dermocystidium marinus Mackin, Owen and Collier in Oysters. Science 116, 360-361. CrossRef
Ray, S.M., 1954, Biological studies of Dermocystidium Marinus, a fungus parasite of oysters. Rice Institute Pamphlet 14, 114.
Rodríguez, J.M., López-Romalde, S., Beaz, R., Carmen Alonso, M., Castro, D., Romalde, J.L., 2006, Molecular fingerprinting of Vibrio tapetis strains using three PCR-based methods: ERIC-PCR, REP-PCR and RAPD. Dis. Aquat. Org. 69, 175-183. CrossRef
Rodríguez J.M., Toranzo A.E., Romalde J.L., 2003, Development and optimization of a new PCR-based protocol for rapid diagnosis of Vibrio tapetis, the causative agent of brown ring disease in clams. In: Abstracts of XIth International Conference of the European Association of Fish Pathologists (EAFP).
Saulnier, D., Avarre, J.C., Le Moullac, G., Ansquer, D., Levy, P., Vonau, V., 2000, Rapid and sensitive PCR detection of Vibrio penaeicida, the putative etiological agent of Syndrome 93 in New Caledonia. Dis. Aquat. Org. 40, 109-115. CrossRef
Shostak, A.W., Scott, M.E., 1993, Detection of density-dependent growth and fecundity of helminths in natural infections. Parasitology 106, 527-539. CrossRef
Sousa, W.P., 1993, Interspecific antagonism and species coexistence in a diverse guild of larval trematode parasites. Ecol. Monogr. 63, 103-128. CrossRef
Thieltges, D.W., Krakau, M., Andresen, H., Fottner, S., Reise, K., 2006, Macroparasite community in molluscs of a tidal basin in the Wadden Sea. Helgol. Mar. Res. 60, 307-316. CrossRef
Touassem, R., Theron, A., 1989, Schistosoma rodhaini: Dynamics and cercarial production for mono- and pluri-miracidial infection of Biomphalaria glabrata. J. Helminthol. 63, 79-83. CrossRef
Villalba, A., Casas, S.M., Lopez, C., Carballal, M.J., 2005, Study of perkinsosis in the carpet shell clam Tapes decussatus in Galicia (NW Spain). II. Temporal pattern of disease dynamics and association with clam mortality. Dis. Aquat. Org. 65, 257-267.
Villalba, A., Reece, K.S., Ordás, M.C., Casas, S.M., Figueras, A., 2004, Perkinsosis in molluscs: a review. Aquat. Living Resour. 17, 411-432. CrossRef
Wegeberg A.M., 1998. Digene trematoders (Echinostomatidae) infectionsokologi og effekt pa Cerastoderma edule. PhD Thesis, University of Aarhus.
Wegeberg, A.M., de Montaudouin, X., Jensen, K.T., 1999, Effect of intermediate host size (Cerastoderma edule) on infectivity of cercariae of three Himasthla species (Echinostomatidae, Trematoda). J. Exp. Mar. Biol. Ecol. 238, 259-269. CrossRef
Werding, B., 1969, Morphologie, entwicklung und ökologie digener trematoden-larven der standschnecke Littorina littorea. Mar. Biol. 3, 306-333. CrossRef