Hostname: page-component-cd4964975-pf4mj Total loading time: 0 Render date: 2023-03-29T14:29:00.463Z Has data issue: true Feature Flags: { "useRatesEcommerce": false } hasContentIssue true

Do trematode parasites affect cockle (Cerastoderma edule) secondary production and elimination?

Published online by Cambridge University Press:  15 May 2009

Meriame Gam
Université Hassan II Aïn Chock, Faculté des Sciences, Km7 Route El Jadida, Casablanca, Morocco
Xavier de Montaudouin*
Station Marine d'Arcachon, UMR EPOC 5805 Université Bordeaux 1–CNRS, 2 rue du Pr Jolyet, F-33120 Arcachon, France
Hocein Bazairi
Université Hassan II Aïn Chock, Faculté des Sciences, Km7 Route El Jadida, Casablanca, Morocco
Correspondence should be addressed to: X. de Montaudouin, Station Marine d'Arcachon, UMR EPOC 5805Université Bordeaux 1–CNRS2 rue du Pr Jolyet, F-33120 ArcachonFrance email:


Digenean trematodes are omnipresent in the cockle Cerastoderma edule, a common coastal bivalve of (semi-)sheltered north-eastern Atlantic coasts. They can use their host as a second intermediate host where they remain in a relatively latent stage as metacercariae. Cockle population dynamics and trematode parasite load were monitored for two years in two sites, Arcachon (France) and Merja Zerga (Morocco) for the cockle cohort of 2005. Individual growth was slightly higher at Arcachon than at Merja Zerga (Von Bertalanffy parameters: K = 1.5 yr−1 in both sites but L = 31.2 mm at Merja Zerga against 38.3 mm at Arcachon). Production during cockle life was twice as high at Merja Zerga (48.5 compared to 22.2 gDW.m−2 at Arcachon). Elimination compensated production at Merja Zerga while elimination was low at Arcachon (8.1 gDW.m−2) due to sediment dynamics which concentrated cockles within the sampling area. P/B was similar in both sites (2.4–2.6 yr−1) while E/B was higher at Merja Zerga (2.2 yr−1 versus 1.0 yr−1). Trematode communities were similar in both sites in terms of species and abundance. During the cockle cohort lifespan, there were 3 to 5 events in the parasite abundance survey that suggested parasite-dependent mortality. At Merja Zerga, trematodes metacercariae did not affect P/B (2.4 yr−1) but increased E/B (+14%). At Arcachon, they also had no effect on P/B (2.6 yr−1) but on the contrary increased E/B (+20%). The threshold of metacercariae abundance beyond which cockles are affected was lower for Echinostomatid trematodes at Merja Zerga, suggesting an interaction with other factors such as temperature which is higher at the southern limit of cockle distribution.

Research Article
Copyright © Marine Biological Association of the United Kingdom 2009

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.)



Anderson, R.M. and Gordon, D.M. (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373398.CrossRefGoogle ScholarPubMed
Babirat, C., Mouritsen, K.N. and Poulin, R. (2004) Equal partnership: two trematode species, not one, manipulate the burrowing behaviour of the New Zealand cockle, Austrovenus stutchburyi. Journal of Helminthology 78, 195199.Google Scholar
Bartoli, P. (1976) Modification de la croissance et du comportement de Venerupis aurea parasité par Gymnophallus fossarum P. Bartoli, 1965 (Trematoda, Digenea). Haliotis 7, 2328.Google Scholar
Beukema, J.J. and Dekker, R. (2006) Annual cockle Cerastoderma edule production in the Wadden Sea usually fails to sustain both wintering birds and a commercial fishery. Marine Ecology Progress Series 309, 189204.CrossRefGoogle Scholar
Bhattacharya, C.G. (1967) A simple method of resolution of a distribution into gaussian components. Biometrics 23, 115135.CrossRefGoogle ScholarPubMed
Brock, V. (1980) Notes on relations between density, settling, and growth of two sympatric cockles, Cardium edule (L.) and C. glaucum (Bruguière). Ophelia Supplement 1, 241248.Google Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. and Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Crisp, D.J. (1984) Energy flow measurements. In Holme Holme, N.A. and McIntyre, A.D. (eds) Methods for the study of marine benthos. IBP Handbook No. 16. Oxford: Blackwell, pp. 284372.Google Scholar
Curtis, L.A. (1995) Growth, trematode parasitism, and longevity of a long-lived marine gastropod (Ilyanassa obsoleta). Journal of the Marine Biological Association of the United Kingdom 75, 913925.CrossRefGoogle Scholar
Curtis, L.A., Kinley, J.L. and Tanner, N.L. (2000) Longevity of oversized individuals: growth, parasitism, and history in an estuarine snail population. Journal of the Marine Biological Association of the United Kingdom 80, 811820.CrossRefGoogle Scholar
de Montaudouin, X. and Bachelet, G. (1996) Experimental evidence of complex interactions between biotic and abiotic factors in the dynamics of an intertidal population of the bivalve Cerastoderma edule. Oceanologica Acta 19, 449463.Google Scholar
de Montaudouin, X., Kisielewski, I., Bachelet, G. and Desclaux, C. (2000) A census of macroparasites in an intertidal bivalve community, Arcachon Bay, France. Oceanologica Acta 23, 453468.CrossRefGoogle Scholar
de Montaudouin, X., Blanchet, H., Kisielewski, I., Desclaux, C. and Bachelet, G. (2003) Digenean trematodes moderately alter Hydrobia ulvae population size structure. Journal of the Marine Biological Association of the United Kingdom 83, 297305.CrossRefGoogle Scholar
de Montaudouin, X., Thieltges, D.W., Gam, M., Krakau, M., Pina, S., Bazaïri, H., Dabouineau, L., Russell-Pinto, F. and Jensen, K.T. (in press) Digenean trematode species in the cockle Cerastoderma edule: identification key and distribution along the north-east Atlantic shoreline. Journal of the Marine Biological Association of the United Kingdom.Google Scholar
Desclaux, C., de Montaudouin, X. and Bachelet, G. (2004) Cockle (Cerastoderma edule) population mortality: the role of the digenean parasite Himasthla quissetensis. Marine Ecology Progress Series 279, 141150.CrossRefGoogle Scholar
Desclaux, C., Russell-Pinto, F., de Montaudouin, X. and Bachelet, G. (2006) First record and description of metacercariae of Curcuteria arguinae n. sp. (Digenea: Echinostomatidae), parasite of cockles Cerastoderma edule (Mollusca: Bivalvia) in Arcachon Bay, France. Journal of Parasitology 92, 578587.CrossRefGoogle ScholarPubMed
Fredensborg, B.L. and Poulin, R. (2006) Parasitism shaping host life-history evolution: adaptative responses in a marine gastropod to infection by trematodes. Journal of Animal Ecology 75, 4453.CrossRefGoogle Scholar
Gam, M., Bazaïri, H., Jensen, K.T. and de Montaudouin, X. (2008) Metazoan parasites in an intermediate host population near its southern border: the common cockle (Cerastoderma edule) and its trematodes in a Moroccan coastal lagoon (Merja Zerga). Journal of the Marine Biological Association of the United Kingdom 88, 357364.CrossRefGoogle Scholar
Gayanilo, F.C., Sparre, P. and Pauly, D. (2005) FAO–ICLARM stock assessment tools II— revised version. Rome: FAO.Google Scholar
Goater, C.P. (1993) Population biology of Meiogymnophallus minutus (Trematoda: Gymnophallidae) in cockles from the Exe Estuary. Journal of the Marine Biological Association of the United Kingdom 73, 163177.CrossRefGoogle Scholar
Gorbushin, A.M. (1997) Field evidence of trematode-induced gigantism in Hydrobia spp. (Gastropoda: Prosobranchia). Journal of the Marine Biological Association of the United Kingdom 77, 785800.CrossRefGoogle Scholar
Hibbert, C.J. (1976) Biomass and production of bivalve community on an intertidal mud-flat. Journal of Experimental Marine Biology and Ecology 25, 249261.CrossRefGoogle Scholar
Iglesias, J.I.P. and Navarro, E. (1990) Shell growth of the cockle Cerastoderma edule in the Mundaca estuary (North Spain). Journal of Molluscan Studies 56, 229238.Google Scholar
James, B.L., Sannia, A. and Bowers, E.A. (1977) Parasites of birds and shellfish. In Nelson-Smith, A. and Bridges, E.M. (eds) Problems of a small estuary. Swansea: Publication of the Institute of Marine Studies and Quadrant Press, pp. 116.Google Scholar
Jensen, K.T. (1992) Dynamics and growth of the cockle, Cerastoderma edule, on an intertidal mud-flat in the Danish Wadden Sea: effects of submersion time and density. Netherlands Journal of Sea Research 28, 335345.CrossRefGoogle Scholar
Jensen, K.T. (1993) Density-dependent growth in cockles (Cerastoderma edule): evidence from interannual comparisons. Journal of the Marine Biological Association of the United Kingdom 73, 333342.CrossRefGoogle Scholar
Jensen, K.T., Latama, G. and Mouritsen, K.N. (1996) The effect of larval trematodes on the survival rates of two species of mud snails (Hydrobiidae) experimentally exposed to desiccation, freezing and anoxia. Helgoländer Meeresuntersuchungen 50, 327335.CrossRefGoogle Scholar
Jonsson, P.R. and André, C. (1992) Mass mortality of the bivalve Cerastoderma edule on the Swedish west coast caused by infestation with the digenean trematode Cercaria cerastodermae I. Ophelia 36, 151157.CrossRefGoogle Scholar
Kennedy, C.R. (1984) The use of frequency distribution in an attempt to detect host mortality induced by infections of diplostomatid metacercariae. Parasitology 89, 209220.CrossRefGoogle Scholar
Krist, A.C. (2001) Variation in fecundity among populations of snails is predicted by prevalence of castrating parasites. Evolutionary Ecology Research 3, 191197.Google Scholar
Kube, S., Kube, J. and Bick, A. (2006) A loss of fecundity in a population of mudsnails Hydrobia ventrosa caused by larval trematodes does not measurably affect host population equilibrium level. Parasitology 132, 725732.CrossRefGoogle Scholar
Labbardi, H., Ettahiri, O., Lazar, S., Massik, Z. and El Antri, S. (2005) Etude de la variation spatio-temporelle des paramètres physico-chimiques caractérisant la qualité des eaux d'une lagune côtière et ses zonations écologiques: cas de Moulay Bousselham, Maroc. Comptes Rendus de Géoscience 337, 504514.CrossRefGoogle Scholar
Lajtner, J., Luciæ, A., Marušiæ, M. and Erben, R. (2008) The effects of trematode Bucephalus polymorphus on the reproductive cycle of the zebra mussel Dreissena polymorpha in the Drava River. Acta Parasitologica 53, 8592.CrossRefGoogle Scholar
Lauckner, G. (1980) Diseases of Mollusca: Gastropoda. In Kinne, O. (ed.) Diseases of marine animals. Chichester: Wiley, pp. 311424.Google Scholar
Lauckner, G. (1983) Diseases of Mollusca: Bivalvia. In Kinne, O. (ed.) Diseases of marine animals. Hamburg: Biologische Anstalt Helgoland, pp. 477961.Google Scholar
Lauckner, G. (1987a) Effects of parasites on juvenile Wadden Sea invertebrates. In Tougaard, S. and Asbirk, S. (eds) 5th International Wadden Sea Symposium. The National Forest and Nature Agency and the Museum of Fisheries and Shipping, Esbjerg, pp. 103121.Google Scholar
Lauckner, G. (1987b) Ecological effects of larval trematode infestation on littoral marine invertebrate populations. International Journal for Parasitology 17, 391398.CrossRefGoogle Scholar
Lester, R.J.G. (1984) A review of methods for estimating mortality due to parasites in wild fish populations. Helgoländer Meeresuntersuchungen 37, 5364.CrossRefGoogle Scholar
Leung, T.L.F. and Poulin, R. (2007) Interactions between parasites of the cockle Austrovenus stutchburyi: hitch-hikers, resident-cleaners, and habitat-facilitators. Parasitology 134, 247255.CrossRefGoogle ScholarPubMed
Madani, I. (1989) Dynamique des populations et processus de recrutement chez quatre espèces de bivalves appartenant aux genres Abra et Cerastoderma, dans le Bassin d'Arcachon. PhD thesis. University Bordeaux I.Google Scholar
Möller, P. and Rosenberg, R. (1983) Recruitment, abundance and production of Mya arenaria and Cardium edule in marine shallow waters, Western Sweden. Ophelia 22, 3355.CrossRefGoogle Scholar
Mouritsen, K.N., Gorbushin, A.M. and Jensen, K.T. (1999) Influence of trematode infections on in situ growth rates of Littorina littorea. Journal of the Marine Biological Association of the United Kingdom 79, 425430.CrossRefGoogle Scholar
Oliva, M.E., Olivares, A.N., Diaz, C.D. and Pasten, M.V. (1999) Parasitic castration in Concholepas concholepas (Gastropoda: Muricidae) due to a larval digenean in northern Chile. Diseases of Aquatic Organisms 36, 6165.CrossRefGoogle Scholar
Pauly, D. and Munro, J.L. (1984) Once more on the comparison of growth in fish and invertebrates. Fishbyte 2, 21.Google Scholar
Probst, S. and Kube, J. (1999) Histopathological effects of larval trematode infections in mudsnails and their impact on host growth: what causes gigantism in Hydrobia ulvae (Gastropoda: Prosobranchia)? Journal of Experimental Marine Biology and Ecology 238, 4968.CrossRefGoogle Scholar
Ramón, M. (2003) Population dynamics and secondary production of the cockle Cerastoderma edule (L.) in a backbarrier tidal flat of the Wadden Sea. Scientia Marina 67, 429443.CrossRefGoogle Scholar
Rice, T., McGraw, E., O'Brien, E.K., Reverter, A., Jackson, D.J. and Degnan, B.M. (2006) Parasitic castration by the digenean trematode Allopodocotyle sp. alters gene expression in the brain of the host mollusc Haliotis asinina. FEBS Letters 580, 37693774.CrossRefGoogle ScholarPubMed
Robert, R., Guillocheau, N. and Collos, Y. (1987) Hydrobiological parameters during an annual cycle in the Arcachon Basin. Marine Biology 95, 631640.CrossRefGoogle Scholar
Rothschild, M. (1941) The effect of trematode parasites on the growth of Littorina neritoides (L.). Journal of the Marine Biological Association of the United Kingdom 25, 6980.CrossRefGoogle Scholar
Sanchez-Salazar, M.E., Griffith, C.L. and Seed, R. (1987) The interactive roles of predation and tidal elevation in structuring populations of the edible cockle, Cerastoderma edule. Estuarine, Coastal and Shelf Science 25, 245260.CrossRefGoogle Scholar
Schulte-Oehlmann, U., Oehlmann, J., Fioroni, P. and Bauer, B. (1997) Imposex and reproductive failure in Hydrobia ulvae (Gastropoda: Prosobranchia). Marine Biology 128, 257266.CrossRefGoogle Scholar
Sokal, R. and Rohlf, F. (1981) Biometry. 2nd edition. New York: W.H. Freeman.Google Scholar
Tebble, N. (1966) British bivalve seashells. London: Alden Press Osney Mead.Google Scholar
Thieltges, D.W. (2006a) Parasite induced summer mortality in the cockle Cerastoderma edule by the trematode Gymnophallus choledochus. Hydrobiologia 559, 455461.CrossRefGoogle Scholar
Thieltges, D.W. (2006b) Effect of infection by metacercarial trematode Renicola roscovita on growth in intertidal blue mussel Mytilus edulis. Marine Ecology Progress Series 319, 129134.CrossRefGoogle Scholar
Thieltges, D.W. and Reise, K. (2006) Metazoan parasites in intertidal cockles Cerastoderma edule from the northern Wadden Sea. Journal of Sea Research 56, 284293.CrossRefGoogle Scholar
Thieltges, D.W., Krakau, M., Andresen, H., Fottner, S. and Reise, K. (2006) Macroparasite community in molluscs of a tidal basin in the Wadden Sea. Helgoland Marine Research 60, 307316.CrossRefGoogle Scholar
Thieltges, D.W., de Montaudouin, X., Fredensborg, B.L., Jensen, K.T., Koprivnika, J. and Poulin, R. (2008) Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Marine Ecology Progress Series 372, 147155.CrossRefGoogle Scholar
Wegeberg, A.M. and Jensen, K.T. (1999) Reduced survivorship of Himasthla (Trematoda, Digenea)-infected cockles (Cerastoderma edule) exposed to oxygen depletion. Journal of Sea Research 42, 325331.CrossRefGoogle Scholar
Wegeberg, A.M. and Jensen, K.T. (2003) In situ growth of juvenile cockles, Cerastoderma edule, experimentally infected with larval trematodes (Himasthla interrupta). Journal of Sea Research 50, 3743.CrossRefGoogle Scholar
Wegeberg, A.M., de Montaudouin, X. and Jensen, K.T. (1999) Effect of intermediate host size (Cerastoderma edule) on infectivity of cercariae of three Himasthla species (Echinostomatidae, Trematoda). Journal of Experimental Marine Biology and Ecology 238, 259269.CrossRefGoogle Scholar
Wilson, K., Bjørnstad, O.N., Dobson, A.P., Merler, S., Poglayen, G., Randolph, S.E., Read, A.F. and Skorping, A. (2002) Heterogeneities in macroparasite infections: patterns and processes. In Hudson, P.J., Rizzoli, A., Grenfell, B., Heesterbeek, H. and Dobson, A.P. (eds) The ecology of wildlife diseases. Oxford: Oxford University Press, pp. 644.Google Scholar
Zwarts, L. and Wanink, J. (1989) Siphon size and burying depth in deposit- and suspension-feeding benthic bivalves. Marine Biology 100, 227240.CrossRefGoogle Scholar