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Temporal variation of Meiogymnophallus minutus infections in the first and second intermediate host

Published online by Cambridge University Press:  01 February 2010

J. Fermer*
Affiliation:
Department of Zoology, Ecology and Plant Science, University College Cork, Distillery Fields, North Mall, Cork, Ireland
S.C. Culloty
Affiliation:
Department of Zoology, Ecology and Plant Science, University College Cork, Distillery Fields, North Mall, Cork, Ireland Aquaculture and Fisheries Development Centre, University College Cork, Distillery Fields, North Mall, Cork, Ireland
T.C. Kelly
Affiliation:
Department of Zoology, Ecology and Plant Science, University College Cork, Distillery Fields, North Mall, Cork, Ireland
R.M. O'Riordan
Affiliation:
Department of Zoology, Ecology and Plant Science, University College Cork, Distillery Fields, North Mall, Cork, Ireland
*

Abstract

In order to study seasonal patterns of Meiogymnophallus minutus infections in its intermediate hosts, bivalve samples were collected monthly between April 2008 and March 2009 from a high intertidal flat at Courtmacsherry Bay, Ireland. Infection rates in the first intermediate host Scrobicularia plana did not fluctuate significantly with season. Completely developed M. minutus cercariae appeared in daughter sporocysts from June and prevailed from July to October, indicating that transmission of M. minutus from its first to its second intermediate host is confined to this period of the year. All analysed individuals of the second intermediate host Cerastoderma edule were found to be infected with metacercariae. Infection levels significantly increased in September, suggesting recent cercarial invasions. Throughout the year, the majority of metacercariae were hyperinfected by the pathogenic microsporidian Unikaryon legeri. Spreading of hyperinfections was confined to spring and summer. Newly settled metacercariae were not affected by hyperparasitism and presumably retained their infectivity for half a year. Our findings suggest that the spreading of hyperinfections is correlated with higher water temperatures and that the entire metacercarial population has to rebuild every year as a consequence of hyperparasite-induced mortality.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2010

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References

Ataev, G.L. (1991) Temperature influence on the development and biology of rediae and cercariae of Philophthalmus rhionica (Trematoda). Parazitologiya 25, 349359.Google Scholar
Azevedo, C. & Canning, E.U. (1987) Ultrastructure of a microsporidian hyperparasite, Unikaryon legeri (Microsporida), of trematode larvae. Journal of Parasitology 73, 214223.CrossRefGoogle ScholarPubMed
Bowers, E.A. & James, B.L. (1967) Studies on the morphology, ecology and life-cycle of Meiogymnophallus minutus (Cobbold, 1859) comb. nov. (Trematoda: Gymnophallidae). Parasitology 57, 281300.CrossRefGoogle ScholarPubMed
Bowers, E.A., Bartoli, P., Russell-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). Parasitology Research 82, 505510.CrossRefGoogle ScholarPubMed
Canning, E.U. & Nicholas, J.P. (1974) Light and electron microscope observations on Unikaryon legeri (Microsporida, Nosematidae) a parasite of the metacercaria of Meiogymnophallus minutus in Cardium edule. Journal of Invertebrate Pathology 23, 92100.CrossRefGoogle Scholar
de Montaudouin, X., Thieltges, D.W., Gam, M., Krakau, M., Pina, S., Bazaïri, H., Dabouineau, L., Russell-Pinto, F. & Jensen, K.T. (2009) 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 89, 543556.CrossRefGoogle Scholar
Esch, G.W. & Fernandez, J.C. (1994) Snail–trematode interactions and parasite community dynamics in aquatic systems: a review. The American Midland Naturalist 131, 209237.CrossRefGoogle Scholar
Fermer, J., Culloty, S.C., Kelly, T.C. & O'Riordan, R.M. (2009) Intrapopulational distribution of Meiogymnophallus minutus (Digenea, Gymnophallidae) infections in its first and second intermediate host. Parasitology Research 105, 12311238.CrossRefGoogle ScholarPubMed
Fermer, J., Culloty, S.C., Kelly, T.C. & O'Riordan, R.M.Growth and migration of meiogymnophallus minutus metacercariae in the marine bivalve cerastoderma edule. Helminthologia, Submitted.Google Scholar
Field, L.C. & Irwin, S.W.B. (1999) Digenean larvae in Hydrobia ulvae from Belfast Lough (Northern Ireland) and the Ythan Estuary (north-east Scotland). Journal of the Marine Biological Association of the United Kingdom 79, 431435.CrossRefGoogle Scholar
Fingerut, J.T., Zimmer, C.A. & Zimmer, R.K. (2003) Patterns and processes of larval emergence in an estuarine parasite system. Biological Bulletin 205, 110120.CrossRefGoogle Scholar
Gam, M., Bazaïri, H., Jensen, K.T. & 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
Gam, M., de Montaudouin, X. & Bazaïri, H. (2009) Do trematode parasites affect cockle (Cerastoderma edule) secondary production and elimination? Journal of the Marine Biological Association of the United Kingdom 89, 13951402.CrossRefGoogle 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
Green, J. (1957) The growth of Scrobicularia plana (da Costa) in the Gwendraeth Estuary. Journal of the Marine Biological Association of the United Kingdom 36, 4147.CrossRefGoogle Scholar
Huxham, M., Raffaelli, D. & Pike, A. (1993) The influence of Cryptocotyle lingua (Digenea: Platyhelminthes) infections on the survival and fecundity of Littorina littorea (Gastropoda: Prosobranchia). Journal of Experimental Marine Biology and Ecology 168, 223238.CrossRefGoogle Scholar
Jonsson, P.R. & 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
Køie, M. (1975) On the morphology and life-history of Opechona bacillaris (Molin, 1859) Looss, 1907 (Trematoda, Lepocreadiidae). Ophelia 13, 6386.CrossRefGoogle Scholar
Kube, S., Kube, J. & Bick, A. (2002) Component community of larval trematodes in the mudsnail Hydrobia ventrosa: temporal variations in prevalence in relation to host life history. Journal of Parasitology 88, 730737.CrossRefGoogle ScholarPubMed
Lang, W.H. & Dennis, E.A. (1976) Morphology and seasonal incidence of infection of Proctoeces maculatus (Looss, 1901) Odhner, 1911 (Trematoda) in Mytilus edulis L. Ophelia 15, 6575.CrossRefGoogle Scholar
Lauckner, G. (1971) Zur Trematodenfauna der Herzmuscheln Cardium edule und Cardium lamarcki. Helgoländer wissenschaftliche Meeresuntersuchungen 22, 377400.CrossRefGoogle Scholar
Lauckner, G. (1983) Diseases of Mollusca: Bivalvia. pp. 477961in Kinne, O. (Ed.) Diseases of marine animals Vol. II Introduction, Bivalvia to Scaphopoda. Hamburg, Biologische Anstalt Helgoland.Google Scholar
Lo, C.T. & 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.CrossRefGoogle ScholarPubMed
Loos-Frank, B. (1971) Zur Kenntnis der gymnophalliden Trematoden des Nordseeraumes IV. Übersicht über die gymnophalliden Larven aus Mollusken der Gezeitenzone. Zeitschrift für Parasitenkunde 36, 206232.CrossRefGoogle Scholar
McCarthy, A.M. (1999) The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 118, 383388.CrossRefGoogle ScholarPubMed
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, 5768.CrossRefGoogle Scholar
Prah, S.K. & James, C. (1977) The influence of physical factors on the survival and infectivity of miracidia of Schistosoma mansoni and S. haematobium I. Effect of temperature and ultra-violet light. Journal of Helminthology 51, 7385.CrossRefGoogle ScholarPubMed
Prinz, K., Kelly, T.C., O'Riordan, R.M. & Culloty, S.C. (2009) Infection of Mytilus edulis by the trematode Echinostephilla patellae (Digenea: Philophthalmidae). Journal of Helminthology DoI 10.1017/S0022149X09990472, in press.Google Scholar
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.CrossRefGoogle Scholar
Sannia, A. & 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.CrossRefGoogle Scholar
Sindermann, C.J. & Farrin, A.E. (1962) Ecological studies of Cryptocotyle lingua (Trematoda: Heterophyidae) whose larvae cause ‘pigment spots’ in marine fish. Ecology 43, 6975.CrossRefGoogle Scholar
Sola, J.C. (1997) Reproduction, population dynamics, growth and production of Scrobicularia plana da Costa (Pelecypoda) in the Bidasoa estuary, Spain. Netherlands Journal of Aquatic Ecology 30, 283296.CrossRefGoogle Scholar
Thieltges, D.W. (2006) Parasite induced summer mortality in the cockle Cerastoderma edule by the trematode Gymnophallus choledochus. Hydrobiologia 559, 455461.CrossRefGoogle Scholar
Thieltges, D.W. & 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.Google ScholarPubMed
Thieltges, D.W., Krakau, M., Andresen, H., Fottner, S. & Reise, K. (2006) Macroparasite community in molluscs of a tidal basin in the Wadden Sea. Helgoland Marine Research 60, 307316.CrossRefGoogle Scholar
Upatham, E.S. (1973) The effect of water temperature on the penetration and development of St. Lucian Schistosoma mansoni miracidia in local Biomphalaria glabrata. Southeast Asian Journal of Tropical Medicine and Public Health 4, 367370.Google ScholarPubMed
Vanoverschelde, R. (1982) Studies on the life-cycle of Himasthla militaris (Trematoda: Echinostomatidae): influence of temperature and salinity on the life-span of the miracidium and the infection of the first intermediate host, Hydrobia ventrosa. Parasitology 84, 131135.CrossRefGoogle Scholar