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Microcell parasites of oysters: Recent insights and future trends

Published online by Cambridge University Press:  15 December 2004

Ryan B. Carnegie  and
Nathalie Cochennec-Laureau
Ryan B. Carnegie
Affiliation:
Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA 23062, USA
Nathalie Cochennec-Laureau
Affiliation:
IFREMER, Laboratoire Aquaculture Tropicale, Unité de Pathologie, BP 7004, 98719 Taravao, Tahiti, French Polynesia
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Abstract

Our understanding of the microcell oyster parasites of the genera Bonamia and Mikrocytos has expanded in recent years with the application of ultrastructural and especially molecular biological research approaches. Molecular phylogenetic analyses of SSU rRNA genes have united three species, Bonamiaostreae, Bonamiaexitiosa, and Mikrocytos (now Bonamia) roughleyi, in a microcell clade within the Haplosporidia, supporting both early and recent ultrastructural observations. Ultrastructural and molecular phylogenetic evidence has emerged that Mikrocytos mackini, on the other hand, is a unique protist with unusual adaptations for a parasitic existence. DNA probes and polymerase chain reaction (PCR) assays promise new insights into the life cycles, transmission, and diversity of these organisms. The development of Ostrea edulis lines selected for B. ostreae resistance will increase the viability of aquaculture industries for this species and, combined with rapidly developing biotechnological approaches for studying host defenses and host-parasite interactions, will allow greater insight into the nature of phenomena such as resistance and tolerance to disease in oysters.

Keywords

MicrocellBonamiaMikrocytos
Type
Research Article
Information
Aquatic Living Resources , Volume 17 , Issue 4: Bivalve Diseases , October 2004 , pp. 519 - 528
Copyright
© EDP Sciences, IFREMER, IRD, 2004

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References

Adlard, R.D., Lester, R.J.G., 1995, Development of a diagnostic test for Mikrocytos roughleyi, the aetiological agent of Australian winter mortality of the commercial rock oyster, Saccostrea commercialis (Iredale & Roughley). J. Fish Dis. 18, 609-614. CrossRef
Anderson, T.J., Adlard, R.D., 1994, Nucleotide sequence of a rDNA internal transcribed spacer supports synonomy of Saccostrea commercialis and S. glomerata. J. Mollusc Stud. 60, 196-197. CrossRef
Balouet, G., Poder, M., Cahour, A., 1983, Haemocytic parasitosis: morphology and pathology of lesions in the French flat oyster, Ostrea edulis L. Aquaculture 34, 1-14. CrossRef
Barber, B.J., Davis, C., 1994, Prevalence of Bonamia ostreae in Ostrea edulis populations in Maine. J. Shellfish Res. 13, 298.
Barber, B.J., Davis, C.V., Carnegie, R.B., Boettcher, K.J., 2000, Management of juvenile oyster disease (JOD) in Maine. J. Shellfish Res. 19, 641-645.
Barrow, J.H., 1965, Observations on Minchinia pickfordae (Barrow, 1961) found in snails of the Great Lakes region. Trans. Am. Microscop. Soc. 84, 587-593. CrossRef
Baud, J.P., Gérard, A., Naciri-Graven, Y., 1997, Comparative growth and mortality of Bonamia ostreae-resistant and wild oysters Ostrea edulis in an intensive system. Mar. Biol. 130, 71-79. CrossRef
Bédier E., Cochennec-Laureau N., Langlade A., Kopp J., Goyard E., Gérard A., 2001, Recovery of the European flat oyster Ostrea edulis (L.): new development. Proceedings of the European Aquaculture Society annual meeting 2001.
Bougrier, S., Tigé, G., Bachère, E., Grizel, H., 1986, Ostrea angasi acclimatisation to French coasts. Aquaculture 58, 151-154. CrossRef
Boulo, V., Mialhe, E., Rogier, H., Paolucci, F., Grizel, H., 1989, Immunodiagnosis of Bonamia ostreae (Acetospora) infection of Ostrea edulis L. and subcellular identification of epitopes by monoclonal antibodies. J. Fish Dis. 12, 257-262. CrossRef
Bower, S.M., 1988, Circumvention of mortalities caused by Denman Island oyster disease during mariculture of Pacific oysters. Am. Fish. Soc. Spec. Publ. 18, 246-248.
Bower S.M., 2001, Synopsis of infectious diseases and parasites of commercially exploited shellfish: Mikrocytos roughleyi (Australian Winter Disease) of oysters, http://www-sci.pac.dfo-mpo.gc.ca/shelldis/pages/ mikrouoy_e.htm.
Bower, S.M., Hervio, D., Meyer, G.M., 1997, Infectivity of Mikrocytos mackini, the causative agent of Denman Island disease in Pacific oysters Crassostrea gigas, to various species of oysters. Dis. Aquat. Org. 29, 111-116. CrossRef
Bower, S.M., McGladdery, S.E., Price, I.M., 1994, Synopsis of infectious diseases and parasites of commercially exploited shellfish. Ann. Rev. Fish Dis. 4, 1-199. CrossRef
Brehélin M., Bonami J.R., Cousserans F., Vivarès C., 1982, Existence de formes plasmodiales vraies chez Bonamia ostreae parasite de l'huître plate Ostrea edulis. L.C.R. Acad. Sc., Paris, Sér. III, 295, 45-48.
Bucke, D., 1988, Pathology of bonamiasis. Parasit. Today 4, 174-176. CrossRef
Bucke D., Feist S., 1985, Bonamiasis in the flat oyster, Ostrea edulis, with comments on histological techniques. In: Ellis, A.E. (Ed.), Fish and Shellfish Pathology, Academic Press, London, pp. 387-392.
Bucke, D., Hepper, B., 1987, Bonamia ostreae infecting Ostrea lutaria in the U.K. Bull. Eur. Assoc. Fish Pathol. 7, 79-80.
Burreson, E.M., Stokes, N.A., Carnegie, R.B., Bishop, M.J., 2004, Bonamia sp. (Haplosporidia) Found in Nonnative Oysters Crassostrea ariakensis in Bogue Sound, North Carolina. J. Aquat. Anim. Health 16, 1-9. CrossRef
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
Campalans, M., Rojas, P., Gonzalez, M., 2000, Haemocytic parasitosis in the farmed oyster Tiostrea chilensis. Bull. Eur. Assoc. Fish Pathol. 20, 31-33.
Carnegie, R.B., Barber, B.J., Distel, D.L., 2003, Detection of the oyster parasite Bonamia ostreae by fluorescent in situ hybridization. Dis. Aquat. Org. 55, 247-252. 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
Carnegie, R.B., Meyer, G.R., Blackbourn, J., Cochennec-Laureau, N., Bower, S.M., 2002, Development and application of a PCR for Mikrocytos mackini, the causative agent of Denman Island disease in oysters. J. Shellfish Res. 21, 387.
Carnegie, R.B., Meyer, G.R., Blackbourn, J., Cochennec-Laureau, N., Berthe, F.C.J., Bower, S.M., 2003, Molecular detection of the oyster parasite Mikrocytos mackini, and a preliminary phylogenetic analysis. Dis. Aquat. Org. 54, 219-227. CrossRef
Chagot D., 1989, Caractérisation morphologique et fonctionnelle des hémocytes d'Ostrea edulis et de Crassostrea gigas, mollusques bivalves. Etude in vitro de leurs interactions avec le protozoaire Bonamia ostreae (Ascetospora). Thèse EPHE Sciences de la Vie et de la Terre, Univ. Montpellier, France.
Chagot, D., Boulo, V., Hervio, D., Mialhe, E., Mourton, C., Grizel, H., 1992, Interactions between Bonamia ostreae (Protozoa: Ascetospora) and hemocytes of Ostrea edulis and Crassostrea gigas (Mollusca: Bivalvia): entry mechanisms. J. Invert. Pathol. 51, 207-214.
Cochennec N., 1997, La Bonamiose: caractérisation du parasite Bonamia ostreae et étude de ses interactions avec l'hôte, l'huître plate Ostrea edulis. Memoire Ecole Pratique des Hautes Etudes, Sciences de la Vie et de la Terre. Montpellier, France.
Cochennec N., 2001, Bonamia ostreae, parasite de l'huître plate, Ostrea edulis, sa position taxonomique parmi les parasites du groupe “Microcell,” analyses des interactions hôte/parasite chez plusieurs populations d'huîtres plates. Thèse de Doctorat. Biologie cellulaire, Université de la Rochelle, France.
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
Cochennec-Laureau, N., Reece, K.S., Berthe, F.C.J., Hine, P.M., 2003, Mikrocytos roughleyi taxonomic affiliation leads to the genus Bonamia (Haplosporidia). Dis. Aquat. Org. 54, 209-217. CrossRef
Cochennec, N., Renault, T., Boudry, P., Chollet, B., Gérard, A., 1998, Bonamia-like parasite in the Suminoe oyster, Crassostrea rivularis (Gould) reared in France. Dis. Aquat. Org. 34, 103-107. CrossRef
Cochennec, N., Hervio, D., Panatier, B., Boulo, V., Mialhe, E., Rogier, H., Grizel, H., Paolucci, M., 1992, A direct monoclonal antibody sandwich immunoassay for detection of Bonamia ostreae (Ascetospora) in hemolymph samples of the flat oyster Ostrea edulis (Mollusca: Bivalvia). Dis. Aquat. Org. 12, 129-134. CrossRef
Comps M., Tigé G., Grizel H., 1980, Étude ultrastructurale d'un protiste de l'huître Ostrea edulis L.C.R. Acad. Sc. Paris, Sér. D, 290, 383-384.
Cronin, M.A., Culloty, S.C., Mulcahy, M.F., 2001, Lysozyme activity and protein concentration in the haemolymph of the flat oyster Ostrea edulis (L.). Fish Shellfish Imm. 11, 611-622. CrossRef
Culloty S.C., Mulcahy M.F., 1992, An evaluation of anaesthetics for Ostrea edulis L. 4th Internat. Colloq. Marine Aquaculture, Vigo (Pontevedra), Spain.
Culloty, S.C., Mulcahy, M.F., 1996, Season-, age- and sex-related variation in the prevalence of bonamiasis in flat oyster (Ostrea edulis) L. on the south coast of Ireland. Aquaculture 144, 53-63. CrossRef
Culloty, S.C., Cronin, M.A., Mulcahy, M.F., 2001, An investigation into the relative resistance of Irish flat oysters Ostrea edulis, L. to the parasite Bonamia ostreae (Pichot et al. 1980). Aquaculture 199, 229-244. CrossRef
Culloty, S.C., Duggan, P.F., Quishi, X., Mulcahy, M.F., 2002, Amylase and aspartate aminotransferase in the haemolymph of the European flat oyster Ostrea edulis. Fish Shellfish Immunol. 12, 367-369. 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
Davis, C.V., Crosby, M.A., Barber, B.J., Hawes, R.O., 1997, Genetic selection in oysters for growth and resistance to juvenile oyster disease (JOD). J. Shellfish Res. 16, 328-331.
Diggles, B.K., Cochennec-Laureau, N., Hine, P.M., 2003, Comparison of diagnostic techniques for Bonamia exitiosa from flat oysters Ostrea chilensis in New Zealand. Aquaculture 220, 145-156. CrossRef
Dinamani, P., Hine, P.M., Jones, J.B., 1987, The occurrence and characteristics of the hemocyte parasite Bonamia sp. in New Zealand dredge oyster, Tiostrea lutaria. Dis. Aquat. Org. 3, 37-44. CrossRef
Elston, R., 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
Farley, C.A., Wolf, P.H., Elston, R., 1988, A long-term study of “microcell” disease in oysters with a description of a new genus, Mikrocytos (g. n.), and two new species, Mikrocytos mackini (sp. n.) and Mikrocytos roughleyi (sp. n.). Fish. Bull. 86, 581-593.
Farley, C.A., Lewis, E.J., Relyea, D., Zahtila, J., Rivara, G., 1997, Juvenile oyster disease resistance studies continued: 1994-1996. J. Shellfish Res. 16, 286-291.
Ford S.E., Tripp M.R., 1996, Diseases and defense mechanisms. In: Kennedy V.S., Newell R.I.E., Eble A.F. (Eds.), The Eastern Oyster Crassostrea virginica. Maryland Sea Grant College, College Park, MD.
Friedman, C.S., Perkins, F.O., 1994, Range extension of Bonamia ostreae to Maine, USA J. Invertebr. Pathol. 64, 179-181. CrossRef
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, in California, USA. J. Shellfish Res. 8, 133-137.
Grizel, H., Mialhe, E., Chagot, D., Boulo, V., Bachère, E., 1988, Bonamiasis: A model study of diseases in marine molluscs. Am. Fish. Soc. Spec. Publ. 18, 1-4.
Grizel, H., Comps, M., Raguenes, D., Le Borgne, Y., Tigé, G., Martin, A.G., 1983, Bilan des essais d'acclimatation d'Ostrea chilensis sur les côtes de Bretagne. Rev. Trav. Inst. Pêches Marit. 46, 209-225.
Hand, R.E., Nell, J.A., Smith, I.R., Maguire, G.B., 1998, Studies on triploid oysters in Australia. XI. Survival of diploid and triploid Sydney rock oysters (Saccostrea commercialis (Iredale and Roughley)) through outbreaks of winter mortality caused by Mikrocytos roughleyi infestation. J. Shellfish Res. 17, 334-336.
Haskin, H.H., Ford, S.E., 1978, Mortality patterns and disease resistance in Delaware Bay oysters. Proc. Natl. Shellfish Assoc. 68, 80.
Haskin, H.H., Ford, S.E., 1979, Development of resistance to Minchinia nelsoni (MSX) mortalities in laboratory-reared and native oyster stocks in Delaware Bay. Mar. Fish. Rev. 41, 54-63.
Hervio D., 1992, Contribution à l'étude de Bonamia ostreae (Ascetospora), protozoaire parasite de l'huître plate Ostrea edulis (Bivalvia), et à l'analyse des interactions hôte-parasite. Thèse de 3ème cycle en Biologie fondamentale et appliquée (Spécialité: Protistologie), Université de Clermont Ferrand, France.
Hervio, D., Bower, S.M., Meyer, G.R., 1996, Detection, isolation, and experimental transmission of Mikrocytos mackini, a microcell parasite of Pacific oysters Crassostrea gigas (Thunberg). J. Invertebr. Pathol. 67, 72-79. CrossRef
Hine, P.M., 1991, The annual pattern of infection by Bonamia sp. in New Zealand flat oysters, Tiostrea chilensis. Aquaculture 93, 241-251. CrossRef
Hine, P.M., 1991, Ultrastructural observations on the annual infection pattern of Bonamia sp. in flat oysters Tiostrea chilensis. Dis. Aquat. Org. 11, 163-171. CrossRef
Hine, P.M., 1992, Ultrastructural and ultracytochemical observations on Bonamia sp. in oysters (Tiostrea chilensis), with a consideration of organelle function. Aquaculture 107, 175-183. CrossRef
Hine, P.M., 1996, The ecology of Bonamia and decline of bivalve molluscs. N.Z. J. Ecol. 20, 109-116.
Hine, P.M., Jones, J.B., 1994, Bonamia and other aquatic parasites of importance to New Zealand. N.Z. J. Zool. 21, 49-56. CrossRef
Hine, P.M., Wesney, B., 1992, Interrelationships of cytoplasmic structures in Bonamia sp. (Haplosporidia) infecting oysters Tiostrea chilensis: An interpretation. Dis. Aquat. Org. 14, 59-68. CrossRef
Hine, P.M., Wesney, B., 1994, Interaction of phagocytosed Bonamia sp. (Haplosporidia) with haemocytes of oysters Tiostrea chilensis. Dis. Aquat. Org. 20, 219-229. CrossRef
Hine, P.M., Wesney, B., 1994, The functional cytology of Bonamia sp. (Haplosporidia) infecting oysters Tiostrea chilensis: An ultracytochemical study. Dis. Aquat. Org. 20, 207-217. CrossRef
Hine, P.M., Cochennec-Laureau, N., Berthe, F.C., 2001, Bonamia exitiosa n. sp. (Haplosporidia) infecting flat oysters, Ostrea chilensis, in New Zealand. Dis. Aquat. Org. 47, 63-72. CrossRef
Hine, P.M., Bower, S.M., Meyer, G.R., Cochennec-Laureau, N., Berthe, F.C.J., 2001, Ultrastructure of Mikrocytos mackini, the cause of Denman Island disease in oysters Crassostrea spp. and Ostrea spp. in British Columbia, Canada. Dis. Aquat. Org. 45, 215-227. CrossRef
Hudson E.B., Hill B.J., 1991, Impact and spread of bonamiasis in the UK, Aquaculture 93, 279-285.
Hugh Jones, D., 1999, Breeding ponds as a basis for flat oyster (Ostrea edulis) culture and their use to develop resistance to the disease Bonamia ostreae. J. Shellfish Res. 18, 718.
Katkansky, S.C., Dahlstrom, W.A., Warner, R.W., 1969, Observations on survival and growth of the European flat oyster, Ostrea edulis, in California. Calif. Fish Game 55, 69-74.
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. Gen. Res. 78, 259-270. CrossRef
Le Bec, C., Mazurie, J., Cochennec, N., Le Coguic, Y., 1991, Influence of Crassostrea gigas mixed with Ostrea edulis on the incidence of Bonamia disease. Aquaculture 93, 263-271. CrossRef
Le Borgne, Y., Le Pennec, M., 1983, Elevage expérimental de l'huître asiatique Ostrea denselamellosa (Lischke). Vie Marine 5, 23-28.
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. Eur. Aquac. Soc. Spec. Publ. 18, 545-554.
McArdle, J.F., McKiernan, F., Foley, H., Hugh Jones, D., 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
Mialhe, E., Boulo, V., Elston, R., Hill, B., Hine, M., Montes, J., Van Banning, P., Grizel, H., 1988, Serological analysis of Bonamia in Ostrea edulis and Tiostrea lutaria using polyclonal and monoclonal antibodies. Aquat. Living Resour. 1, 67-69. CrossRef
Montes P., 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, Inc., San Diego, CA.
Montes, J., Melendez, I., 1987, Donnes sur la parasitose de Bonamia ostreae chez l'huitre plate de Galice, Cote Nord-Ouest de l'Espagne. Aquaculture 67, 195-198. CrossRef
Montes, J., Anandon, R., Azevedo, C., 1994, A possible life cycle for Bonamia ostreae on the basis of electron microscopy studies. J. Invertebr. Pathol. 63, 1-6. CrossRef
Morris, D.J., Adams, A., Richards, R.H., 2000, Observations on the electron-dense bodies of the PKX parasite, agent of proliferative kidney disease in salmonids. Dis. Aquat. Org. 39, 201-209. CrossRef
Mourton, C., Boulo, V., Chagot, D., Hervio, D., Mialhe, E., Grizel, H., 1992, Interactions between Bonamia ostreae (Protozoa: Ascetospora) and haemocytes of Ostrea edulis and Crassostrea gigas (Mollusca: Bivalvia): in vitro system establishment. J. Invertebr. Pathol. 59, 235-240. CrossRef
Naciri Y., 1994, Sélection des mollusques: Bilan et nouvelles perspectives concernant la croissance, la qualité et les résistances aux maladies. Bordeaux Aquaculture, pp. 54-61.
Naciri-Graven, Y., Haure, J., Gérard, A., Baud, P., 1999, Comparative growth of Bonamia ostreae resistant and wild flat oyster Ostrea edulis in an intensive system. II. Second year of the experiment. Aquaculture 171, 195-208.
Naciri-Graven, Y., Launey, S., Lebayon, N., Gérard, A., Baud, J.-P., 2000, Influence of parentage upon growth in Ostrea edulis: evidence for inbreeding depression. Gen. Res. 76, 159-168. 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
Nell, J.A., Smith, I.R., McPhee, C.C., 2000, The Sydney rock oyster Saccostrea glomerata (Gould, 1850) breeding programme: progress and goals. Aquac. Res. 31, 45-49. CrossRef
Foighil, Ó Taylor, D. D.J., 2000, Evolution of parental care and ovulation behavior in oysters. Mol. Phylog. Evol. 15, 301-313. CrossRef
Foighil, Ó Marshall, D. Hilbish, B.A. Pino, T.J. M.A., 1999, Trans-Pacific range extension by rafting is inferred for the flat oyster Ostrea chilensis. Biol. Bull. 196, 122-126. CrossRef
Office International des Epizooties (O.I.E.), 2000, International aquatic animal health code, fish, molluscs, and crustaceans. 3rd edition, Paris, France.
Office International des Epizooties (O.I.E.), 2003, International aquatic animal health code 2003, http://www.oie.int/eng/normes/fcode/A_00045.htm.
Pascual M., Martin A.G., Zampatti E., Coatanea D., Defossez J., Robert R., 1991, Testing of the Argentina oyster, Ostrea puelchana, in several French oyster farming sites. International Counc. for the Exploration of the Sea, Shellfish Comm., Copenhagen, Denmark.
Paynter, K.T., Gaffney, P.M., Meritt, D.W., 1997, Evaluation of American oyster stocks: Disease resistance and genetics. J. Shellfish Res. 16, 329-332.
Perkins, F.O., 1979, Cell structure of shellfish pathogens and hyperparasites in the genera Minchinia, Urosporidium, Haplosporidium, and Marteilia: Taxonomic implications. Mar. Fish. Rev. 41, 25-37.
Perkins, F.O., 1987, Protistan parasites of commercially significant marine bivalves, life cycles, ultrastructure, and phylogeny. Aquaculture 67, 240-243. CrossRef
Perkins, F.O., 1988, Structure of protistan parasites found in bivalve molluscs. Am. Fish. Soc. Spec. Publ. 18, 93-111.
Pichot, Y., Comps, M., Grizel, H., Rabouin, M.A., 1980, 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. Proceedings of the 15th annual meeting of the Society for Invertebrate Pathology, Brighton, UK, pp. 254-257.
Reece, K.S., Stokes, N.A., 2003, Molecular analysis of a haplosporidian parasite from cultured New Zealand abalone (Haliotis iris Martyn, 1784). Dis. Aquat. Org. 53, 61-66. CrossRef
Renault T., Cochennec N., Grizel H., 1994, Bonamia ostreae, parasite of the European flat oyster, Ostrea edulis, does not experimentally infect the Japanese oyster, Crassostrea gigas. Bull. Eur. Assoc. Fish Pathol. 15, 78-80.
Rogan, E., Culloty, S.C., Cross, T.F., Mulcahy, M.F., 1991, The detection of Bonamia ostreae (Pichot et al. 1980) in frozen oysters (Ostrea edulis L.) and the effect of the parasite on condition. Aquaculture 97, 311-315. CrossRef
Roughley, T.C., 1926, An investigation of the cause of an oyster mortality on the Georges River, New South Wales, 1924-25. Proc. Linn. Soc. N.S.W. 51, 446-491.
Sprague, V., 1979, Classification of the Haplosporidia. Mar. Fish. Rev. 41, 40-44.
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. 46, 307-317.
Van Banning, P., 1986, Case-history of the Bonamia ostreae control in the Dutch oyster culture. Eur. Aquac. Soc. Spec. Publ. 9, 23-27.
Van Banning, P., 1990, The life cycle of the oyster pathogen Bonamia ostreae with a presumptive phase in the ovarian tissue of the European flat oyster, Ostrea edulis. Aquaculture 84, 189-192. CrossRef
Xue Q., 1998, Caractérisation morphologique et fonctionnelle des hémocytes chez l'huître plate, Ostrea edulis. Thèse de Doctorat de l'Institut Universitaire Européen de la Mer, Brest, France.
Zabaleta, A., Barber, B.J., 1996, Prevalence, intensity and detection of Bonamia ostreae in Ostrea edulis L. in the Damariscotta River area, Maine. J. Shellfish Res. 15, 395-400.