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Digenean trematode species in the cockle Cerastoderma edule: identification key and distribution along the north-eastern Atlantic shoreline

  • Xavier de Montaudouin (a1), David W. Thieltges (a2), Mériame Gam (a3), Manuela Krakau (a4), Suzana Pina (a5), Hocein Bazairi (a3), Laurent Dabouineau (a6), Fernanda Russell-Pinto (a5) and K. Thomas Jensen (a7)...


We describe the digenean fauna of one of the dominant intertidal hosts, the common cockle Cerastoderma edule, in terms of biomass, off north-eastern Atlantic shores. Using published and unpublished literature we have prepared an identification key and provide an up-date of the large-scale distributional patterns of digenean species of the common cockle. At least sixteen digenean species, belonging to seven families, use cockles as intermediate host. Among these species two utilize cockles as first intermediate host only, whereas two species utilize cockles as both first and second intermediate host. The remaining eleven species have cockles as their second intermediate host. Water birds and fish are the definitive hosts to twelve and four species, respectively.

Cockles are infected with digeneans along the latitudinal gradient from southern Morocco to the western region of the Barents Sea often with high infection levels. Whereas some of these digenean species occur along most of the latitudinal gradient others show a more restricted northern or southern distribution mostly caused by an underlying latitudinal gradient of host species.

Knowledge of digenean species and their large-scale distribution pattern may serve as a baseline for future studies dealing with the effects of climate change on parasite–host systems. For such studies the cockle and its digenean community could be an ideal model system.


Corresponding author

Correspondence should be addressed to: X. de Montaudouin, Université de Bordeaux, UMR EPOC 5805, Station Marine d'Arcachon 2 rue du Pr Jolyet, F-33120 Arcachon, France email:


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Bartoli, P., Jousson, O. and Russell-Pinto, F. (2000) The life cycle of Monorchis parvus (Digenea: Monorchiidae) demonstrated by developmental and molecular data. Journal of Parasitology 86, 479489.
Baudrimont, M., de Montaudouin, X. and Palvadeau, A. (2006) Impact of digenean parasites infection on metallothionein synthesis by the cockle (Cerastoderma edule): a multivariate field monitoring. Marine Pollution Bulletin 52, 494502.
Bowers, E.A. (1969) Cercaria bucephalopsis haimeana (Lacaze-Duthiers, 1854) (Digenea: Bucephalidae) in the cockle, Cardium edule L. in South Wales. Journal of Natural History 3, 409422.
Bowers, E.A. and James, B.L. (1967) Studies on the morphology, ecology and life-cycle of Meiogymnophallus minutus (Cobbold, 1859) comb. nov. (Trematoda: Gymnophallidae). Parasitology 57, 281300.
Bowers, E.A., Bartoli, P. and James, B.L. (1990) A demonstration of allopatric sibling species within the Gymnophallidae (Digenea). Systematic Parasitology 17, 143152.
Bowers, E.A., Bartoli, P., Russell-Pinto, F. and 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). Parasitology Research 82, 505510.
Boyden, C.R. (1971) A comparative study of the reproductive cycles of the cockles Cerastoderma edule and C. glaucum. Journal of the Marine Biological Association of the United Kingdom 51, 605622.
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.
de Montaudouin, X., Wegeberg, A.M., Jensen, K.T. and Sauriau, P.G. (1998) Infection characteristics of Himasthla elongata cercaria in cockles as a function of water current. Diseases of Aquatic Organisms 34, 6370.
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.
de Montaudouin, X., Jensen, K.T., Desclaux, C., Wegeberg, A.M. and Sajus, M.C. (2005) Effect of intermediate host size (Cerastoderma edule) on infectivity of cercariae of Himasthla quissetensis (Echinostomatidae: Trematoda). Journal of the Marine Biological Association of the United Kingdom 85, 809812.
Deltreil, J.P. and His, E. (1972) Evolution d'un gisement de Cardium edule LMK dans le Bassin d'Arcachon. Revue des Travaux de l'Institut des Pêches Maritimes 36, 301308.
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. PhD thesis. University Bordeaux 1.
Desclaux, C., de Montaudouin, X. and Bachelet, G. (2002) Cockle emergence at the sediment surface: ‘favourization’ mechanism by digenean parasites? Diseases of Aquatic Organisms 52, 137149.
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.
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.
Evans, N.A. (1985) The influence of environmental temperature upon transmission of the cercariae of Echinostoma liei (Digenea: Echinostomatidae). Parasitology 90, 269275.
Ferrell, D.L., Negovetich, N.J. and Wetzel, E.J. (2001) Effect of temperature on the infectivity of metacercariae of Zygocotyle lunata (Digenea: Paramphistomidae). Journal of Parasitology 87, 1013.
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.
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.
Goater, C.P. (1995) Population dynamics of two species of intestinal helminth in oystercatchers (Haematopus ostralegus). Canadian Journal of Zoology 73, 296300.
Hakalahti, T., Karvonen, A. and Valtonen, E.T. (2006) Climate warming and disease risks in temperate regions—Argulus coegoni and Diplostomum spathaceum as case studies. Journal of Helminthology 80, 9398.
Hancock, D.A. and Urquhart, A.E. (1965) The determination of natural mortality and its causes in an exploited population of cockles (Cardium edule L.). Fishery Investigations 24, 140.
Hayes, M.L., Bonaventura, J., Mitchell, T.P., Prospero, J.M., Shinn, E.A., Van Dolah, F. and Barber, R.T. (2001) How are climate and marine biological outbreaks functionally linked? Hydrobiologia 460, 213220.
Hechinger, R.F. and Lafferty, K.D. (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society B 272, 10591066.
Hechinger, R.F., Lafferty, K.D., Huspeni, T.C., Brooks, A.J. and Kuris, A.M. (2007) Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia 151, 8292.
Hudson, P.J., Dobson, A.P. and Lafferty, K.D. (2006) Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21, 381385.
James, B.L. and Bowers, E.A. (1967) Reproduction in the daughter sporocyst of Cercaria bucephalopsis haimeana (Lacaze-Duthiers, 1854) (Bucephalidae) and Cercaria dichotoma Lebour, 1911 (non Müller) (Gymnophallidae). Parasitology 57, 607625.
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.
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.
Jensen, K.T., Fernández Castro, N. and Bachelet, G. (1999) Infectivity of Himasthla spp. (Trematoda) in cockle (Cerastoderma edule) spat. Journal of the Marine Biological Association of the United Kingdom 79, 265271.
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.
Kesting, V., Gollasch, S. and Zander, C.D. (1996) Parasite communities of the Schlei Fjord (Baltic coast of northern Germany). Helgoländer Meeresuntersuchungen 40, 477496.
Krakau, M., Thieltges, D.W. and Reise, K. (2006) Native parasites adopt introduced bivalves of the North Sea. Biological Invasions 8, 919925.
Kutz, S.J., Hoberg, E.P., Polley, L. and Jenkins, E.J. (2005) Global warming is changing the dynamics of Arctic host–parasite systems. Proceedings of the Royal Society B 272, 25712576.
Lassalle, G., de Montaudouin, X., Soudant, P. and Paillard, C. (2007) Parasite co-infection of two sympatric bivalves, the Manila clam (Ruditapes philippinarum) and the cockle (Cerastoderma edule) along a latitudinal gradient. Aquatic Living Resource 20, 3342.
Lauckner, G. (1971) Zur Trematodenfauna der Herzmuscheln Cardium edule und Cardium lamarcki. Helgoländer Wissenchaft Meeresuntersuchungen 22, 377400.
Lauckner, G. (1983) Diseases of Mollusca: Bivalvia. In Kinne, O. (ed.) Diseases of marine animals. Hamburg: Biologische Anstalt Helgoland, pp. 477961.
Lauckner, G. (1984) Impact of trematode parasitism on the fauna of a North Sea tidal flat. Helgoländer Meeresuntersuchungen 37, 185199.
Lebour, M.V. (1911) A review of the British marine cercariae. Parasitology 4, 416456.
Littlewood, D.T.J. (2005) Marine parasites and the tree of life. In Rohde, K. (eds) Marine parasitology. Oxford: CABI Publishing, pp. 610.
Lo, C.T. and Lee, K.M. (1996) Pattern of emergence and the effects of temperature and light on the emergence and survival of heterophyid cercariae (Centrocestus formosanus and Haplorchis pumilio). Journal of Parasitology 82, 347350.
Loos-Frank, B. (1968) Der Entwicklungszyklus von Psilostomum brevicolle (Creplin, 1829) [Syn.: P. platyurum (Mühling, 1896)] (Trematoda, Psilostomatidae). Zeitschrift für Parasitenkunde 31, 122131.
Loos-Frank, B. (1969) Zur Kenntis der gymnophalliden Trematoden des Nordseeraumes. I. Die Alternativ-Zyklen von Gymnophallus choledochus Odhner 1900. Zeitschrift für Parasitenkunde 32, 135156.
Loos-Frank, B. (1971) Zur Kenntis der gymnophalliden Trematoden des Nordseeraumes. III. Gymnophallus gibberosus n. sp. und seine Metacercarie. Zeitschrift für Parasitenkunde 35, 270281.
Maillard, C. (1976) Distomatoses de poissons en milieu lagunaire. PhD thesis. University Sciences et Techniques du Languedoc.
Malek, M. (2001) Effects of the digenean parasites Labratrema minimus and Cryptocotyle concavum on the growth parameters of Pomatoschistus microps and P. minutus from Southwest Wales. Parasitology Research 87, 349355.
Markowski, S. (1936) Über die Trematodenfauna der baltischen Mollusken aus der Umgebung der Halbinsel Hel. Bulletin International de l'Académie Polonaise des Sciences et Lettres 1936, 285317.
Mouritsen, K.N. (2002) The parasite-induced surfacing behaviour in the cockle Austrovenus stutchburyi: a test of an alternative hypothesis and identification of potential mechanisms. Parasitology 124, 521528.
Mouritsen, K.N. and Jensen, K.T. (1997) Parasite transmission between soft-bottom invertebrates: temperature mediated infection rates and mortality in Corophium volutator. Marine Ecology Progress Series 151, 123134.
Mouritsen, K.N. and Poulin, R. (2002) Parasitism, community structure and biodiversity in intertidal ecosystem. Parasitology 124, 101117.
Mouritsen, K.N., Tompkins, D.M. and Poulin, R. (2005) Climate warming may cause a parasite-induced collapse in coastal amphipod populations. Oecologia 146, 476483.
Pelseneer, P. (1906) Parasites de mollusques marins. Bulletin Scientifique de la France et de la Belgique 40, 161186.
Pina, S., Barandela, T., Santos, M.J., Russell-Pinto, F. and Rodrigues, P. (in press) Identification and description of Bucephalus minimus (Digenea: Bucephalidae) life cycle in Portugal: morphological, histopathological and molecular data. Journal of Parasitology.
Poulin, R. (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143151.
Poulin, R. and Morand, S. (2000) The diversity of parasites. Quarterly Review of Biology 75, 277293.
Poulin, R. and Mouritsen, K.N. (2006) Climate change, parasitism and the structure of intertidal ecosystems. Journal of Helminthology 80, 183191.
Prévot, G. (1966) Sur deux trématodes larvaires d'Antedon mediterranea Lmk. (Echinoderme): Metacercaria sp. (Monorchiidae Odhner, 1911), et métacercaire de Diphterostomum brusinae Stoss., 1904 (Zoogonidae Odhner, 1911). Annales de Parasitologie 41, 233242.
Reimer, L.W. (1970) Digene Trematoden und Cestoden der Ostseefische als natürliche Fischmarken. Parasitologische Schriftenreihe 20, 1144.
Reimer, L.W. (1973) Das Auftreten eines Fischtrematoden der Gattung Asymphylodora Looss, 1899, bei Nereis diversicolor O.F. Müller als Beispiel für einen Alternativzyklus. Zoologischer Anzeiger 191, 187196.
Russell-Pinto, F. (1990) Differences in infestation intensity and prevalence of hinge and mantle margin Meiogymnophallus minutus metacercariae (Gymnophallidae) in Cerastoderma edule (Bivalvia): possible species coexistence in Ria de Aveiro. Journal of Parasitology 76, 653659.
Russell-Pinto, F. (1993) Espécies de digenea que infectam Cerastoderma edule (n.v. berbigão) em Portugal. Caracterização da resposta do hospedeiro à infestação. PhD thesis. University of Porto, Portugal.
Russell-Pinto, F. and Bartoli, P. (1992) Sympatric distribution of Meiogymnophallus minutus and M. fossarum (Digenea: Gymnophallidae) in Cerastoderma edule in the Ria de Aveiro estuary in Portugal. Parasitology Research 78, 617618.
Russell-Pinto, F. and Bowers, E.A. (1998) Ultrastructural studies on the tegument of the metacercariae of Meiogymnophallus minutus and Meiogymnophallus fossarum (Digenea: Gymnophallidae) in Cerastoderma edule from Portugal. Journal of Parasitology 84, 715722.
Russell-Pinto, F., Gonçalves, J.F. and Bowers, E. (2006) Digenean larvae parasitizing Cerastoderma edule (Bivalvia) and Nassarius reticulatus (Gastropoda) from Ria de Aveiro, Portugal. Journal of Parasitology 92, 319332.
Sannia, A. and James, B.L. (1978) The occurrence of Cercaria cerastodermae I Sannia, James, and Bowers, 1978 (Digenea: Monorchiidae) in populations of Cerastoderma edule (L.) from the commercial beds of the Lower Thames Estuary. Zeitschrift für Parasitenkunde 56, 111.
Sannia, A., James, B.L. and Bowers, E.A. (1978) The morphology of Cercaria cerastodermae I nom. nov. (Monorchiidae) (=Cercaria lepidapedon rachion (Cobbold, 1858) sensu Lebour, 1908) a rare digenean parasite of the cockle in Britain. Journal of Natural History 12, 487500.
Sauriau, P.-G. (1992) Les mollusques benthiques du bassin de Marennes-Oléron: estimation et cartographie des stocks non cultivés, compétition spatiale et trophique, dynamique de population de Cerastoderma edule (L.). PhD thesis. University of Bretagne Occidentale.
Smyth, J.D. (1994) Introduction to animal parasitology, 3rd edition.Cambridge, UK: Cambridge University Press.
Sousa, W.P. and Gleason, M. (1989) Does parasitic infection compromise host survival under extreme environmental conditions? The case for Cerithidea californica (Gastropoda: Prosobranchia). Oecologia 80, 456464.
Stunkard, H.W. (1938) The morphology and life cycle of the trematode Himasthla quissetensis (Miller and Northup, 1926). Biological Bulletin. Marine Biological Laboratory, Woods Hole 75, 145164.
Thieltges, D.W. (2006) Parasite induced summer mortality in the cockle Cerastoderma edule by the trematode Gymnophallus choledochus. Hydrobiologia 559, 455461.
Thieltges, D.W. (2007) Habitat and transmission—effect of tidal level and upstream host density on metacercarial load in an intertidal bivalve. Parasitology 134, 599605.
Thieltges, D.W. (2008) Effect of host size and temporal exposure on metacercarial infection levels in the intertidal cockle Cerastoderma edule. Journal of the Marine Biological Association of the United Kingdom 88, 613616.
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.
Thieltges, D.W. and Rick, J. (2006) Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Diseases of Aquatic Organisms 73, 6368.
Thieltges, D.W. and Reise, K. (2007) Spatial heterogeneity in parasite infections at different spatial scales in an intertidal bivalve. Oecologia 150, 569581.
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.
Thieltges, D.W., Hussel, B., Hermann, J., Jensen, K.T., Krakau, M., Taraschewski, H. and Reise, K. (2008) Parasites in the northern Wadden Sea: a conservative ecosystem component over 4 decades. Helgoland Marine Research 62, 3747.
Thieltges, D.W., Donas-Botto Bordalo, M., Cabalero Hernández, A., Prinz, K. and Jensen, K.T. (in press) Ambient fauna impairs parasite transmission in a marine parasite–host system. Parasitology.
Vaullegeard, A. (1894) Note sur la présence du Bucephalus haimeanus (Lacaze Duthiers) dans le Tapes ducussatus (Linné) et dans le Tapes pullastra (Montagu). Bulletin de la Société Linnéenne de Normandie 8, 814.
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.
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.
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.
Werding, B. (1969) Morphologie, Entwicklung und Ökologie digener Trematoden-Larven der Strandschnecke Littorina littorea. Marine Biology 3, 306333.
Windsor, D.A. (1998) Most of the species on Earth are parasites. International Journal for Parasitology 28, 19391941.
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