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Evidence of an altered protective effect of metallothioneins after cadmium exposure in the digenean parasite-infected cockle (Cerastoderma edule)

Published online by Cambridge University Press:  11 October 2006

M. BAUDRIMONT  and
X. de MONTAUDOUIN
M. BAUDRIMONT
Affiliation:
UMR EPOC 5805 Université Bordeaux 1-CNRS, Arcachon Marine Station, 2 rue du Pr Jolyet, 33120 Arcachon, France
X. de MONTAUDOUIN
Affiliation:
UMR EPOC 5805 Université Bordeaux 1-CNRS, Arcachon Marine Station, 2 rue du Pr Jolyet, 33120 Arcachon, France
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Abstract

The aim of the present study was to analyse the relation between parasitism and subsequent metallothioneins (MT) in the case of metal contamination. Experimental exposure of parasitized and unparasitized cockles (Cerastoderma edule) to cadmium (Cd) was performed, with the cockle as first or second intermediate host of 2 digenean species. After 7 days of Cd exposure in microcosms, cockles infected as first intermediate host by Labratrema minimus exhibited metal concentrations in tissues double that in uninfected cockles. Jointly, MT concentrations of parasitized cockles were not modified in comparison with uninfected individuals in which concentrations were increased 4·3-fold compared with controls. In cockles experimentally infected as the second intermediate host by Himasthla elongata, cadmium concentrations significantly increased again in parasitized cockles compared with uninfected individuals in contaminated conditions. Simultaneously, MT concentrations in healthy cockles increased, whereas they significantly decreased in parasitized individuals. Therefore, the presence of digenean parasites in Cd-exposed cockles leads to a maintenance or a decrease in MT concentrations compared with healthy individuals, whereas Cd accumulation in tissues is significantly increased. These experiments indicate a significant alteration of the protective effect of metallothioneins towards metals which could consequently enhance cockle vulnerability. Moreover, these results highlight the limit of the use of MT as a biomarker of metal pollution in field monitoring if parasitism is not taken into account.

Keywords

metallothioneinscadmiumLabratrema minimusHimasthla elongatadigeneansCerastoderma edulebioaccumulation
Type
Research Article
Information
Parasitology , Volume 134 , Issue 2 , February 2007 , pp. 237 - 245
Copyright
2006 Cambridge University Press

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References

REFERENCES

Amiard, J. C., Amiard-Triquet, C., Barka, S., Pellerin, J. and Rainbow, P. S. ( 2006). Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquatic Toxicology 76, 160–202.CrossRefGoogle Scholar
Andrès, S., Baudrimont, M., Lapaquellerie, Y., Ribeyre, F., Maillet, N., Latouche, C. and Boudou, A. ( 1999). Field transplantation of the freshwater bivalve Corbicula fluminea along a polymetallic contamination gradient (river Lot, France): I. Geochemical characteristics of the sampling sites and cadmium and zinc bioaccumulation kinetics. Environmental Toxicology and Chemistry 18, 2462–2471.Google Scholar
Barlow, M. J. and Kingston, P. F. ( 2001). Observations on the effects of barite on the gill tissues of the suspension feeder Cerastoderma edule (Linné) and the deposit feeder Macoma balthica. Marine Pollution Bulletin 42, 71–76.CrossRefGoogle Scholar
Baudrimont, M., Andrès, S., Metivaud, J., Lapaquellerie, Y., Ribeyre, F., Maillet, N., Latouche, C. and Boudou, A. ( 1999). Field transplantation of the freshwater bivalve Corbicula fluminea along a polymetallic contamination gradient (river Lot, France): II. Metallothionein response to metal exposure. Environmental Toxicology and Chemistry 18, 2472–2477.Google Scholar
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, 494–502.CrossRefGoogle Scholar
Baudrimont, M., Lemaire-Gony, S., Ribeyre, F., Métivaud, J. and Boudou, A. ( 1997 a). Seasonal variations of metallothionein concentrations in the asiatic clam (Corbicula fluminea). Comparative Biochemistry and Physiology 118C, 361–367.Google Scholar
Baudrimont, M., Metivaud, J., Maury-Brachet, R., Ribeyre, F. and Boudou, A. ( 1997 b). Bioaccumulation and metallothionein response in the asiatic clam (Corbicula fluminea) after experimental exposure to cadmium and inorganic mercury. Environmental Toxicology and Chemistry 16, 2096–2105.Google Scholar
Bordin, G., McCourt, J., Cordeiro Raposo, F. and Rodriguez, A. R. ( 1997). Metallothionein-like metallothioneins in the Baltic clam Macoma balthica: Seasonal variations and induction upon metal exposure. Marine Biology 129, 453–463.CrossRefGoogle Scholar
Chan, M. K., Othman, R., Zubir, D. and Salmijah, S. ( 2002). Induction of a putative metallothionein gene in the blood cockle, Anadara granosa, exposed to cadmium. Comparative Biochemistry and Physiology 131, 123–132.CrossRefGoogle Scholar
Cheggour, M., Chafik, A., Langston, W. J., Burt, G. R., Benbrahim, S. and Texier, H. ( 2001). Metals in sediments and the edible cockle Cerastoderma edule from two Moroccan Atlantic lagoons: Moulay Bou Selham and Sidi Moussa. Environmental Pollution 115, 149–160.CrossRefGoogle Scholar
Ciocan, C. M. and Rotchell, J. M. ( 2004). Cadmium induction of metallothionein isoforms in juvenile and adult mussel (Mytilus edulis). Environmental Science and Technology 38, 1073–1078.CrossRefGoogle Scholar
Coleman, F. F. and Travis, J. ( 1998). Phenology of recruitment and infection patterns of Ascocotyle pachycystis, a digenean parasite in the sheepshead minnow, Cyprinodon variegatus. Environmental Biology of Fishes 51, 87–96.CrossRefGoogle Scholar
Cotou, E., Vagias, C., Rapti, T. and Roussis, V. ( 2001). Metallothionein levels in the bivalves Callista chione and Venus verrucosa from two Mediterranean sites. Zeitschrift für Naturforschung 56c, 848–852.CrossRefGoogle 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, 453–468.CrossRefGoogle Scholar
Deltreil, J.-P. and His, E. ( 1970). Sur la présence d'une cercaire de trématode chez Cardium edule L. dans le Bassin d'Arcachon. Revue des Travaux de l'Institut des Pêches Maritimes 34, 1225–1232.Google Scholar
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, 137–149.Google 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, 578–587.Google Scholar
Dobson, A. P. ( 1988). The population biology of parasite-induced changes in host behavior. The Quarterly Review of Biology 63, 139–165.CrossRefGoogle Scholar
Durrieu, G., Maury-Brachet, R., Girardin, M., Rochard, E. and Boudou, A. ( 2005). Contamination by heavy metals (Cd, Zn, Cu, and Hg) of eight fish species in the Gironde estuary (France). Estuaries 28, 581–591.CrossRefGoogle Scholar
Fried, B., Idris, N. and Ohsawa, T. ( 1995). Experimental infection of juvenile Biomphalaria glabrata with cercariae of Echinostoma trivolvis. Journal of Parasitology 81, 308–310.CrossRefGoogle Scholar
Funes, V., Alhama, J., Navas, J. I., López-Barea, J. and Peinado, J. ( 2006). Ecotoxicological effects of metal pollution in two mollusc species from Spanish South Atlantic littoral. Environmental Pollution 139, 214–223.CrossRefGoogle Scholar
Géret, F., Jouan, A., Turpin, V., Bebianno, M. J. and Cosson, R. P. ( 2002). Influence of metal exposure on metallothionein synthesis and lipid peroxidation in two bivalve mollusks: the oyster (Crassostrea gigas) and the mussel (Mytilus edulis). Aquatic Living Resource 15, 61–66.CrossRefGoogle Scholar
Gimazane, J. P. and Lubet, P. ( 1972). Etude expérimentale de l'action de la nutrition, de la température et de la lumière sur le cycle sexuel de Cardium edule L. (Mollusque Bivalve). Bulletin de la Société Linnéenne de Normandie 103, 137–146.Google Scholar
Griscom, S. B., Fisher, N. S. and Luoma, S. N. ( 2002). Kinetic modeling of Ag, Cd and Co bioaccumulation in the clam Macoma balthica: quantifying dietary and dissolved sources. Marine Ecology Progress Series 240, 127–141.CrossRefGoogle Scholar
Holmes, J. C. and Bethel, W. H. ( 1972). Modification of intermediate host behaviour by parasites. Zoological Journal of the Linnean Society 51, 123–149.Google 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, 151–157.CrossRefGoogle Scholar
Kägi, J. H. R. ( 1991). Overview of metallothionein. In Methods in Enzymology ( ed. Abelson, J. N. and Simon, M. I.), pp. 613–626. Academic Press, San Diego.
Kesting, V., Gollasch, S. and Zander, C. D. ( 1996). Parasite communities of the Schlei Fjord (Baltic coast of northern Germany). Helgoländer Meeresuntersuchungen 40, 477–496.CrossRefGoogle Scholar
Lafferty, K. D., Porter, J. and Ford, S. E. ( 2004). Are diseases increasing in the ocean? Annual Review of Ecology, Evolution, and Systematics 35, 31–54.Google Scholar
Lauckner, G. ( 1983). Diseases of Mollusca: Bivalvia. In Diseases of Marine Animals ( ed. Kinne, O.), pp. 477–961. Biologische Anstalt Helgoland, Hamburg.
Lauckner, G. ( 1984). Impact of trematode parasitism on the fauna of a North Sea tidal flat. Helgoländer Meeresuntersuchungen 37, 185–199.CrossRefGoogle Scholar
Lauckner, G. ( 1987). Effects of parasites on juvenile Wadden Sea invertebrates. In 5th International Wadden Sea Symposium ( ed. Tougaard, S. and Asbirk, S.), pp. 103–121. The National Forest and Nature Agency and the Museum of Fisheries and Shipping, Esbjerg.
Lebour, M. V. ( 1911). A review of the British marine cercariae. Parasitology 4, 416–456.CrossRefGoogle Scholar
Leiniö, S. and Lehtonen, K. K. ( 2005). Seasonal variability in biomarkers in the bivalves Mytilus edulis and Macoma balthica from the northern Baltic Sea. Comparative Biochemistry and Physiology Part C 140, 408–421.CrossRefGoogle Scholar
Leung, K. M. Y. and Furness, R. W. ( 1999). Induction of metallothionein in dogwhelk Nucella lapillus during and after exposure to cadmium. Ecotoxicology and Environmental Safety 43, 156–464.CrossRefGoogle Scholar
Leung, K. M. Y. and Furness, R. W. ( 2001). Survival, growth, metallothionein and glycogen levels of Nucella lapillus (L.) exposed to subchronic cadmium stress: the influence of nutritional state and prey type. Marine Environmental Research 52, 173–194.Google Scholar
Liang, L. N., He, B., Jiang, G. B., Chen, D. Y. and Yao, Z. W. ( 2004). Evaluation of mollusks as biomonitors to investigate heavy metal contaminations along the Chinese Bohai Sea. Science of the Total Environment 324, 105–113.CrossRefGoogle Scholar
Maillard, C. ( 1976). Distomatoses de poissons en milieu lagunaire. Ph.D. thesis University Sciences et Techniques du Languedoc.
Mourgaud, Y., Martinez, E., Geffard, A., Andral, B., Stanisière, J. Y. and Amiard, J. C. ( 2002). Metallothionein concentration in the mussel Mytilus galloprovincialis as biomarker of response to metal contamination: validation in the field. Biomarkers 7, 479–490.CrossRefGoogle Scholar
Mouritsen, K. N. and Poulin, R. ( 2002). Parasitism, community structure and biodiversity in intertidal ecosystem. Parasitology 124, 101–117.CrossRefGoogle Scholar
Neuberger-Cywiak, L., Achituv, Y. and Garcia, E. M. ( 2003). Effects of zinc and cadmium on the burrowing behavior, LC50, and LT50 on Donax trunculus Linnaeus (Bivalvia-Donacidae). Bulletin of Environmental Contamination and Toxicology 70, 713–722.CrossRefGoogle Scholar
Poulin, R. ( 1994). Meta-analysis of parasite-induced behavioural changes. Animal Behaviour 48, 137–146.CrossRefGoogle Scholar
Sokolowski, A., Wolowicz, M., Hummel, H. and Bogaards, R. ( 1999). Physiological responses of Macoma balthica to copper pollution in the Baltic. Oceanologica Acta 22, 431–439.CrossRefGoogle Scholar
Sures, B. ( 2004). Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 20, 170–177.CrossRefGoogle Scholar
Sures, B., Jürges, G. and Taraschewski, H. ( 1998). Relative concentrations of heavy metals in the parasites Ascaris suum (Nematoda) and Fasciola hepatica (Digenea) and their respective porcine and bovine definitive hosts. International Journal for Parasitology 28, 1173–1178.CrossRefGoogle Scholar
Tanguy, A., Boutet, I., Riso, R., Boudry, P., Auffret, M. and Moraga, D. ( 2003). Metallothionein genes in the European flat oyster Ostrea edulis: a potential ecological tool for environmental monitoring? Marine Ecology Progress Series 257, 87–97.Google Scholar
Tebble, N. ( 1966). British Bivalve Seashells. Alden Press Osney Mead, London.
Thieltges, D. W. ( 2006). Parasite induced summer mortality in the cockle Cerastoderma edule by the trematode Gymnophallus choledochus. Hydrobiologia 559, 455–461.CrossRefGoogle Scholar
Thomas, F., Cezilly, F., Meeüs, T.de, Crivelli, A. and Renaud, F. ( 1997). Parasitism and ecology of wetlands: a review. Estuaries 20, 646–654.CrossRefGoogle Scholar
Tran, D., Boudou, A. and Massabuau, J.-C. ( 2001). How water oxygenation level influences cadmium accumulation pattern in the asiatic clam Corbicula fluminea: a laboratory and field study. Environmental Toxicology and Chemistry 20, 2073–2080.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, 259–269.CrossRefGoogle Scholar