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Bonamia ostreae-induced mortalities in one-year old European flat oysters Ostrea edulis: experimental infection by cohabitation challenge

Published online by Cambridge University Press:  23 October 2008

Delphine Lallias ,
Isabelle Arzul ,
Serge Heurtebise ,
Sylvie Ferrand ,
Bruno Chollet ,
Maeva Robert ,
Andy R. Beaumont ,
Pierre Boudry ,
Benjamin Morga  and
Sylvie Lapègue
Delphine Lallias
Affiliation:
IFREMER, Laboratoire Génétique et Pathologie, Ronce-les-bains, 17390 La Tremblade, France School of Ocean Sciences, College of Natural Sciences, Bangor University, Menai Bridge, Anglesey, LL59 5AB, UK
Isabelle Arzul
Affiliation:
IFREMER, Laboratoire Génétique et Pathologie, Ronce-les-bains, 17390 La Tremblade, France
Serge Heurtebise
Affiliation:
IFREMER, Laboratoire Génétique et Pathologie, Ronce-les-bains, 17390 La Tremblade, France
Sylvie Ferrand
Affiliation:
IFREMER, Laboratoire Génétique et Pathologie, Ronce-les-bains, 17390 La Tremblade, France
Bruno Chollet
Affiliation:
IFREMER, Laboratoire Génétique et Pathologie, Ronce-les-bains, 17390 La Tremblade, France
Maeva Robert
Affiliation:
IFREMER, Laboratoire Génétique et Pathologie, Ronce-les-bains, 17390 La Tremblade, France
Andy R. Beaumont
Affiliation:
School of Ocean Sciences, College of Natural Sciences, Bangor University, Menai Bridge, Anglesey, LL59 5AB, UK
Pierre Boudry
Affiliation:
IFREMER, Laboratoire Génétique et Pathologie, Ronce-les-bains, 17390 La Tremblade, France
Benjamin Morga
Affiliation:
IFREMER, Laboratoire Génétique et Pathologie, Ronce-les-bains, 17390 La Tremblade, France
Sylvie Lapègue
Affiliation:
IFREMER, Laboratoire Génétique et Pathologie, Ronce-les-bains, 17390 La Tremblade, France
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Abstract

Bonamiosis is a parasitic disease (causative agent: Bonamia ostreae) affecting the European flat oyster Ostrea edulis, responsible for a drastic decline in its aquaculture production. Selective breeding programs for resistance to bonamiosis have been undertaken to counter this disease. In the present study, a 6-month cohabitation challenge experiment was performed in order to transmit the disease from wild oysters injected with the parasite to two tested families of oysters (20 and 8-month old at the beginning of the experiment, with different genetic backgrounds) originating from a selective breeding program developed by IFREMER in France. Mortalities were checked daily and ventricular heart smears were performed on dying or moribund oysters to detect the level of infection by B. ostreae. Mortality started after 4 months of cohabitation in the tested oysters. The cumulative mortalities after 6 months were 58% for the wild oysters, 9% for Family 1 (20-month old) and 20% for Family 2 (8-month old). In the dying oysters, the parasite could be detected in 67% of the wild oysters, 68% of Family 1 and 89% of Family 2. It was detected in only 11% of the surviving oysters of Family 2. The mortality and the level of infection by the parasite were significantly higher in Family 2 than in Family 1. Our results demonstrate that prespawning oysters as young as 1 year-old can become infected with the parasite and, most importantly, can die from bonamiosis. This result is inconsistent with the commonly accepted critical age of 2 years-old for the disease development. Additionally, no clear relationship between shell length and level of infection was observed. We also review the different methods for infection of the European flat oyster O. edulis with B. ostreae under experimental conditions and their main results.

Keywords

Ostrea edulisBonamia ostreaeCohabitation experimentTransmissionHeart smear
Type
Research Article
Information
Aquatic Living Resources , Volume 21 , Issue 4 , October 2008 , pp. 423 - 439
Copyright
© EDP Sciences, IFREMER, IRD, 2008

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References

Audemard, C., Carnegie, R.B., Bishop, M.J., Peterson, C.H., Burreson, E.M., 2008, Interacting effects of temperature and salinity on Bonamia sp. parasitism in the Asian oyster Crassostrea ariakensis. J. Invertebr. Pathol. 98, 344–350. CrossRef
Balouet, G., Poder, J., Cahour, A., 1983, Haemocytic parasitosis: morphology and pathology of lesions in the French flat oyster, Ostrea edulis L. Aquaculture 34, 1–14 CrossRef
Balseiro, P., Conchas, R.F., Montes, J., Gómez-León, J., Novoa, B., Figueras, A., 2006, Comparison of diagnosis techniques for the protozoan parasite Bonamia ostreae in flat oyster Ostrea edulis. Aquaculture 261, 1135–1143. CrossRef
Barber, B.J., Davis, C.V., 1994, Prevalence of Bonamia ostreae in Ostrea edulis populations in Maine. J. Shellfish Res. 13, 298.
Bucke, D., Hepper, B., Key, D., Bannister, C.A., 1984, A report on Bonamia ostreae in Ostrea edulis in the UK. ICES C.M. 1984/K 9, 1–7.
Cáceres-Martínez, J., Robledo, J.A.F., Figueras, A., 1995, Presence of Bonamia and its relation to age, growth rates and gonadal development of the flat oyster, Ostrea edulis, in the Ria de Vigo, Galicia (NW Spain). Aquaculture 130, 15–23. CrossRef
Carnegie, R.B., Barber, B.J., Culloty, S.C., Figueras, A.J., Distel, D.L., 2000, Development of a PCR assay for detection of the oyster pathogen Bonamia ostreae and support for its inclusion in the Haplosporidia. Dis. Aquat. Org. 42, 199–206. CrossRef
Cochennec-Laureau, N., Auffret, M., Renault, T., Langlade, A., 2003, Changes in circulating and tissue-infiltrating hemocyte parameters of European flat oysters, Ostrea edulis, naturally infected with Bonamia ostreae. J. Invertebr. Pathol. 83, 23–30. CrossRef
Cochennec, N., Le Roux, F., Berthe, F., Gérard, A., 2000, Detection of Bonamia ostreae based on small subunit ribosomal probe. J. Invertebr. Pathol. 76, 26–32. CrossRef
Comps M., Duthoit J.L., 1976, Infection virale associée à la “maladie des branchies” de l'huître portugaise Crassostrea angulata Lmk. C. R. Acad. Sci. Paris 283, Ser. D, 1595–1596.
Comps M., Tigé G., Grizel H., 1980, Étude ultrastructurale d'un Protiste parasite de l'huître Ostrea edulis L. C. R. Acad. Sci. Paris 290, Ser. D, 383–385.
Corbeil, S., Arzul, I., Diggles, B., Heasman, M., Chollet, B., Berthe, F.C.J., Crane, M.S.J., 2006, Development of a TaqMan PCR assay for the detection of Bonamia species. Dis. Aquat. Org. 71, 75–80. CrossRef
Culloty, S.C., Cronin, M.A., Mulcahy, M.F., 2004, Potential resistance of a number of populations of the oyster Ostrea edulis to the parasite Bonamia ostreae. Aquaculture 237, 41–58. CrossRef
Culloty, S.C., Mulcahy, M.F., 1992, An evaluation of anaesthetics for Ostrea edulis (L.). Aquaculture 107, 249–252. CrossRef
Culloty, S.C., Mulcahy, M.F., 1996, Season-, age-, and sex-related variation in the prevalence of bonamiasis in flat oysters (Ostrea edulis L.) on the south coast of Ireland. Aquaculture 144, 53–63. CrossRef
Culloty, S.C., Novoa, B., Pernas, M., Longshaw, M., Mulcahy, M.F., Feist, S.W., Figueras, A., 1999, Susceptibility of a number of bivalve species to the protozoan parasite Bonamia ostreae and their ability to act as vectors for this parasite. Dis. Aquat. Org. 37, 73–80. CrossRef
Elston, R.A., Farley, C.A., Kent, M.L., 1986, Occurrence and significance of bonamiasis in European flat oysters Ostrea edulis in North America. Dis. Aquat. Org. 2, 49–54. CrossRef
Elston, R.A., Kent, M.L., Wilkinson, M.T., 1987, Resistance of Ostrea edulis to Bonamia ostreae infection. Aquaculture 64, 237–242. CrossRef
Figueras, A.J., 1991, Bonamia status and its effects in cultured flat oysters in the Ria de Vigo, Galicia (N.W. Spain). Aquaculture 93, 225–233. CrossRef
Food and Agriculture Organization of the United Nations (FAO), 2007, FishStat, http://www.fao.org/fi/statist/FISOFT/FISHPLUS.asp
Friedman, C.S., McDowell, T., Groff, J.M., Hollibaugh, J.T., Manzer, D., Hedrick, R.P., 1989, Presence of Bonamia ostreae among populations of the European flat oyster, Ostrea edulis Linnaeus, in California, USA. J. Shellfish Res. 8, 133–137.
Friedman, C.S., Perkins, F.O., 1994, Range extension of Bonamia ostreae to Maine, USA. J. Invertebr. Pathol. 64, 179–181. CrossRef
Grizel H., 1985, Etudes des récentes épizooties de l'huître plate Ostrea edulis L. et de leur impact sur l'ostréiculture bretonne. Thèse de doctorat, USTL Montpellier.
Hervio, D., Bachère, E., Boulo, V., Cochennec, N., Vuillemin, V., Le Coguic, Y., Cailletaux, G., Mazurie, J., Mialhe, E., 1995, Establishment of an experimental infection protocol for the flat oyster, Ostrea edulis, with the intrahaemocytic protozoan parasite, Bonamia ostreae: application in the selection of parasite-resistant oysters. Aquaculture 132, 183–194. CrossRef
Hine, P.M., Diggles, B.K., Parsons, M.J.D., Pringle, A., Bull, B., 2002, The effects of stressors on the dynamics of Bonamia exitiosus Hine, Cochennec-Laureau & Berthe, infections in flat oysters Ostrea chilensis (Philippi). J. Fish Dis. 25, 545–554. CrossRef
Jaziri H., 1985, Biogéographie et polymorphisme enzymatique chez l'huître plate Ostrea edulis L. 1758. Mémoire de DEA, USTL Montpellier.
Lapègue, S., Bédier, E., Goyard, E., Dégremont, L., Baud, J.-P., Gérard, A., Goulletquer, P., Boudry, P., 2004, Apport d'un programme de génétique à une filière de production aquacole: l'exemple de l'ostréiculture. In: Trente ans de crevetticulture en Nouvelle-Calédonie. Actes Colloq. IFREMER 38, 113–121.
Lallias D., 2007, Genetic linkage mapping in the blue mussel Mytilus edulis and the European flat oyster Ostrea edulis, and the search for Quantitative Trait Loci of resistance to a disease in O. edulis. PhD thesis, University of Wales, Bangor, College of Natural Sciences, School of Ocean Sciences.
Launey S., 1998, Marqueurs microsatellites chez l'huître plate Ostrea edulis L. : caractérisation et applications à un programme de sélection pour une résistance au parasite Bonamia ostreae et à l'étude de populations naturelles. Thèse de doctorat. Institut national agronomique Paris-Grignon.
Launey, S., Barre, M., Gérard, A., Naciri-Graven, Y., 2001, Population bottleneck and effective size in Bonamia ostreae-resistant populations of Ostrea edulis as inferred by microsatellite markers. Genet. Res. 78, 259–270. CrossRef
Le Dantec, J., Marteil, L., 1976, La reproduction des huîtres. Rev. Trav. Inst. Pêches Marit. 40, 233–256.
Lynch, S.A., Armitage, D.V., Coughlan, J., Mulcahy, M.F., Culloty, S.C., 2007, Investigating the possible role of benthic macroinvertebrates and zooplankton in the life cycle of the haplosporidian Bonamia ostreae. Exp. Parasitol. 115, 359–368. CrossRef
Lynch, S.A., Armitage, D.V., Wylde, S., Mulcahy, M.F., Culloty, S.C., 2005, The susceptibility of young, prespawning oysters, Ostrea edulis, to Bonamia ostreae. J. Shellfish Res. 24, 1019–1025.
Martin A.-G., Gérard A., Cochennec N., Langlade A., 1993, Selecting flat oysters, Ostrea edulis, for survival against the parasite Bonamia ostreae: assessment of the resistance of a first selected generation. In: Barnabé G., Kestemont P. (Eds.), Production, Environment and Quality. Bordeaux Aquaculture 1992. Eur. Aquac. Soc. Spec. Publ. No. 18, pp. 547–554.
Marty, G.D., Bower, S.M., Clarke, K.R., Meyer, G., Lowe, G., Osborn, A.L., Chow, E.P., Hannah, H., Byrne, S., Sojonky, K., Robinson, J.H., 2006, Histopathology and a real-time PCR assay for detection of Bonamia ostreae in Ostrea edulis cultured in western Canada. Aquaculture 261, 33–42. CrossRef
McArdle, J.F., McKiernan, F., Foley, H., Jones, D.H., 1991, The current status of Bonamia disease in Ireland. Aquaculture 93, 273–278. CrossRef
Mialhe, E., Bachère, E., Chagot, D., Grizel, H., 1988, Isolation and purification of the protozoan Bonamia ostreae (Pichot et al. 1980), a parasite affecting the flat oyster Ostrea edulis L. Aquaculture 71, 293–299. CrossRef
Montes J., 1990, Development of Bonamia ostreae parasitosis of flat oyster, Ostrea edulis, from Galicia, northwest Spain. In: Perkins F.O., Cheng T.C. (Eds.) Pathology in Marine Science, Academic Press, San Diego, CA.
Montes, J., 1991, Lag time for the infestation of flat oyster (Ostrea edulis L.) by Bonamia ostreae in estuaries of Galicia (N.W. Spain). Aquaculture 93, 235–239. CrossRef
Montes, J., Ferro-Soto, B., Conchas, R.F., Guerra, A., 2003, Determining culture strategies in populations of the European flat oyster, Ostrea edulis, affected by bonamiosis. Aquaculture 220, 175–182. CrossRef
Montes, J., Melendez, M.I., 1987, Données sur la parasitose de Bonamia ostreae chez l'huître plate de Galice, côte nord-ouest de l'Espagne. Aquaculture 67, 195–198. CrossRef
Naciri-Graven, Y., Martin, A.-G., Baud, J.-P., Renault, T., Gérard, A., 1998, Selecting the flat oyster Ostrea edulis (L.) for survival when infected with the parasite Bonamia ostreae. J. Exp. Mar. Biol. Ecol. 224, 91–107. CrossRef
Pichot, Y., Comps, M., Tigé, G., Grizel, H., Rabouin, M.A., 1979, Recherches sur Bonamia ostreae gen. n., sp. n., parasite nouveau de l'huître plate Ostrea edulis L. Rev. Trav. Inst. Pêches Marit. 43, 131–140.
Poder M., Cahour A., Balouet G., 1982, Hemocytic parasitosis in European oyster Ostrea edulis L.: pathology and contamination. Proc. 15th annual meeting of the society for invertebrate pathology, Brighton, pp. 254–257.
Tigé, G., Grizel, H., 1984, Essai de contamination d'Ostrea edulis Linné par Bonamia ostreae (Pichot et al., 1979) en rivière de Crach (Morbihan). Rev. Trav. Inst. Pêches Marit. 328, 3–13.
Van Banning P., 1985, Control of Bonamia in Dutch oyster culture. In: Ellis A.E. (Ed.), Fish and Shellfish Pathology. Academic Press, London, pp. 393–396.
Van Banning, P., 1991, Observations on bonamiasis in the stock of the European flat oyster, Ostrea edulis, in the Netherlands, with special reference to the recent developments in Lake Grevelingen. Aquaculture 93, 205–211. CrossRef
Walne P.R., 1974, Culture of bivalve molluscs: fifty years experience at Conwy. Whitefriars Press Ltd, London.
Yonge C.M., 1960, Oysters. The New Naturalist, Collins, London.