Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-26T06:02:15.378Z Has data issue: false hasContentIssue false
  • English
  • Français

Observations raise the question if the Pacific oyster, Crassostrea gigas, can act as either a carrier or a reservoir for Bonamia ostreae or Bonamia exitiosa

Published online by Cambridge University Press:  14 April 2010

S. A. LYNCH ,
E. ABOLLO ,
A. RAMILO ,
A. CAO ,
S. C. CULLOTY  and
A. VILLALBA
S. A. LYNCH*
Affiliation:
Department of Zoology, Ecology and Plant Science, University College Cork, The Cooperage, Distillery Fields, North Mall, Cork, Ireland Aquaculture & Fisheries Development Centre, University College Cork, The Cooperage, Distillery Fields, North Mall, Cork, Ireland
E. ABOLLO
Affiliation:
Centro de Investigacións Mariñas, Consellería do Mar, Xunta de Galicia, Aptdo.13, Vilanova de Arousa, 36620, Spain
A. RAMILO
Affiliation:
Centro de Investigacións Mariñas, Consellería do Mar, Xunta de Galicia, Aptdo.13, Vilanova de Arousa, 36620, Spain
A. CAO
Affiliation:
Centro de Investigacións Mariñas, Consellería do Mar, Xunta de Galicia, Aptdo.13, Vilanova de Arousa, 36620, Spain
S. C. CULLOTY
Affiliation:
Department of Zoology, Ecology and Plant Science, University College Cork, The Cooperage, Distillery Fields, North Mall, Cork, Ireland Aquaculture & Fisheries Development Centre, University College Cork, The Cooperage, Distillery Fields, North Mall, Cork, Ireland
A. VILLALBA
Affiliation:
Centro de Investigacións Mariñas, Consellería do Mar, Xunta de Galicia, Aptdo.13, Vilanova de Arousa, 36620, Spain
*
*Department of Zoology, Ecology and Plant Science and Aquaculture & Fisheries Development Centre, University College Cork, The Cooperage, Distillery Fields, North Mall, Cork, Ireland. Tel: +353 (0) 21 4904618. Fax: +353 (0) 21 4904664. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

This study investigated the ability of the Pacific oyster, Crassostrea gigas, to act as a carrier or reservoir of the protistan Bonamia ostreae. Studies were carried out independently in Ireland and in Spain. Naïve C. gigas were exposed to B. ostreae both in the field and in the laboratory via natural exposure or experimental injection. Naïve flat oysters, Ostrea edulis, were placed in tanks with previously exposed C. gigas. Oysters were screened for B. ostreae by examination of ventricular heart smears and by polymerase chain reaction (PCR) screening of tissue samples (gill and/or heart) and shell cavity fluid. PCR-positive oysters were further screened using histology and in situ hybridization (ISH). B. ostreae DNA was detected in the tissues and/or shell cavity fluid of a small number of C. gigas in the field and in the laboratory. B. ostreae-like cells were visualized in the haemocytes of 1 C. gigas and B. ostreae-like cells were observed extracellularly in the connective tissues of 1 other C. gigas. When C. gigas naturally exposed to B. ostreae were held with naïve O. edulis, B. ostreae DNA was detected in O. edulis; however, B. ostreae cells were not visualized. In Spain, B. exitiosa DNA was also detected in Pacific oyster tissues. The results of this study have important implications for C. gigas transfers from B. ostreae-endemic areas to uninfected areas and highlight B. ostreae and B. exitiosa's ability to survive extracellularly and in other non-typical hosts.

Keywords

Bonamia ostreaeBonamia exitiosaCrassostrea gigascarrier/reservoirPCRISH
Type
Research Article
Information
Parasitology , Volume 137 , Issue 10 , September 2010 , pp. 1515 - 1526
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abollo, E., Ramilo, A., Casas, S. M., Comesaña, P., Cao, A., Carballal, M. J. and Villalba, A. (2008). First detection of the protozoan parasite Bonamia exitiosa (Haplosporidia) infecting flat oyster Ostrea edulis grown in European water. Aquaculture 274, 201–207.CrossRefGoogle Scholar
Arzul, I., Gagnaire, B., Bond, C., Chollet, B., Morga, B., Ferrnad, S., Robert, M. and Renault, T. (2009). Effects of temperature and salinity on the survival of Bonamia ostreae parasite infecting flat oyster O. edulis. Diseases of Aquatic Organisms 85, 67–75.CrossRefGoogle Scholar
Bachére, E., Durand, J. and Tigé, G. (1982). Bonamia ostreae (Pichot et al., 1979) parasite de l'huître plate: comparison de deux methods de diagnostic. International Council for the Exploration of the Sea CM, F 28, 1–11.Google Scholar
Balouet, G., Poder, M. and Cahour, A. (1983). Haemocytic parasitosis: Morphology and pathology of lesions in the French flat oyster, Ostrea edulis L. Aquaculture 34, 1–14.CrossRefGoogle Scholar
Boudry, P., Chatain, B., Naciri-Graven, Y., Lemaire, C. and Gerard, A. (1996). Genetic improvement of marine fish and shellfish: a French perspective. Proceedings of the 5th International Conference for Productivity Enhancement of the Coastal Waters 5, 141–150, Pusan, Korea.Google Scholar
Bower, S. M., McGladdery, S. E. and Price, I. M. (1994). Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annual Review of Fish Diseases 4, 1–199.CrossRefGoogle Scholar
Bucke, D. and Feist, S. W. (1985). Bonamiasis in the flat oyster, Ostrea edulis with comments on histological techniques. In Fish and Shellfish Pathology (ed. Ellis, A. E.), pp. 387–392. Academic Press, London, UK.Google Scholar
Burreson, E. M. (2008). Misuse of PCR assay for diagnosis of mollusc protistan infections. Diseases of Aquatic Organisms 80, 81–83.CrossRefGoogle ScholarPubMed
Burreson, E. M. and Ford, S. (2004). A review of recent information on the Haplosporidia, with a special reference to Haplosporidium nelsoni (MSX disease). Aquatic Living Resources 17, 499–517.CrossRefGoogle Scholar
Burreson, E. M., Stokes, N. A. and Friedman, C. S. (2000). Increased virulence in an introduced pathogen: Haplosporidium nelsoni (MSX) in the eastern oyster Crassostrea virginica. Journal of Aquatic Animal Health 12, 1–8.2.0.CO;2>CrossRefGoogle Scholar
Carnegie, R. B., Barber, B. J., Culloty, S. C., Figueras, A. J. and 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. Diseases of Aquatic Organisms 42, 199–206.CrossRefGoogle ScholarPubMed
Carnegie, R. B., Burreson, E. M., Hine, P. M., Stokes, N. A., Audemard, C., Bishop, M. J. and Peterson, C. H. (2006). Bonamia perspora n. sp. (Haplosporidia), a parasite of the oyster Ostreola equestris, is the first Bonamia species known to produce spores. Journal of Eukaryotic Microbiology 53, 232–245.CrossRefGoogle Scholar
Chagot, D., Boulo, V., Hervio, D., Mialhe, E., Bachère, E., Mourton, C. and Grizel, H. (1992). Interactions between Bonamia ostreae (Protozoa: Ascetospora) and hemocytes of Ostrea edulis and Crassostrea gigas (Mollusca: Bivalvia): entry mechanisms. Journal of Invertebrate Pathology 59, 241–249.CrossRefGoogle Scholar
Cochennec, N., LeRoux, F., Berthe, F. and Gerard, A. (2000). Detection of Bonamia ostreae based on small subunit ribosomal probe. Journal of Invertebrate Pathology 76, 26–32.CrossRefGoogle ScholarPubMed
Comps, M., Tigé, G. and Grizel, H. (1980). Etudes ultrastructurales sur un protiste parasite de l'huître plate Ostrea edulis. Les Comptes Rendus de l'Académie des Sciences, Paris 209, 383–384.Google Scholar
Corbeil, S., Arzul, I., Robert, M., Berthe, F. C. J., Besnard-Cochenned, N. and Crane, M. S. J. (2006). Molecular characterization of an Australian isolate of Bonamia exitiosa. Diseases of Aquatic Organisms 71, 81–85.CrossRefGoogle ScholarPubMed
Cranfield, H. J., Dunn, A., Doonan, I. J. and Michael, K. P. (2005). Bonamia exitiosa epizootic in Ostrea chilensis from Foveaux Strait, southern New Zealand between 1986 and 1992. ICES Journal of Marine Science 62, 3–13.CrossRefGoogle Scholar
Culloty, S. C., Cronin, M. A. and 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.CrossRefGoogle Scholar
Culloty, S. C. and Mulcahy, M. F. (1992). An evaluation of anaesthetics for Ostrea edulis (L.). Aquaculture 107, 249–252.CrossRefGoogle Scholar
Culloty, S. C. and 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.CrossRefGoogle Scholar
Culloty, S. C., Novoa, B., Pernas, M., Longshaw, M., Mulcahy, M. F., Feist, S. W. and Figueras, A. (1999). Susceptibility of a number of bivalve species to the protozoan parasite Bonamia ostreae and their ability to act as a vector for this parasite. Diseases of Aquatic Organisms 37, 73–80.CrossRefGoogle Scholar
Da Silva, P. M., Fuentes, J. and Villalba, A. (2005). Growth, mortality and disease susceptibility of oyster Ostrea edulis families obtained from brood stocks of different geographical origins, through on growing in the Ría de Arousa (Galicia, NW Spain). Marine Biology 147, 965–977.CrossRefGoogle Scholar
Da Silva, P. M. and Villalba, A. (2004). Comparison of light microscopic techniques for the diagnosis of the infection of the European flat oyster Ostrea edulis by the protozoan Bonamia ostreae. Journal of Invertebrate Pathology 85, 97–104.CrossRefGoogle ScholarPubMed
Deagle, B. E., Eveson, P. J. and Jarman, S. N. (2006). Quantification of damage in DNA recovered from highly degraded samples- a case study on DNA in faeces. Frontiers in Zoology 3, 11. www.frontiersinzoology.com/content/3/1/11CrossRefGoogle ScholarPubMed
Dinamani, P., Hine, P. M. and Jones, J. B. (1987). Occurrence and characteristics of the haemocyte parasite Bonamia sp. in the New Zealand dredge oyster Tiostrea lutaria. Diseases of Aquatic Organisms 3, 37–44.CrossRefGoogle Scholar
Elston, R. A., Farley, C. A. and Kent, M. L. (1986). Occurrence and significance of bonamiasis in European flat oysters Ostrea edulis in North America. Diseases of Aquatic Organisms, 2, 49–54.CrossRefGoogle Scholar
Elston, R. A., Kent, M. L. and Wilkinson, M. T. (1987). Resistance of Ostrea edulis to Bonamia ostreae infection. Aquaculture 64, 237–242.CrossRefGoogle Scholar
F.A.O. Fisheries Department (2006). The State of World Fisheries and Aquaculure. www.fao.orgGoogle Scholar
Figueras, A. and Robledo, J. A. F. (1994). Bonamia ostreae present in flat oysters (Ostrea edulis) does not infect mussels (Mytilus galloprovincialis). Bulletin of the European Association of Fish Pathologists 14, 98–100.Google Scholar
Ford, S. E., Allam, B. and Xue, Z. (2009). Using bivalves as particle collectors with PCR detection to investigate the environmental distribution of Haplosporidium nelsoni. Diseases of Aquatic Organisms 83, 159–168.CrossRefGoogle ScholarPubMed
Friedman, C. S. (1996). Haplosporidian infection of the Pacific oyster, Crassostrea gigas (Thunberg), in California and Japan. Journal of Shellfish Research 15, 597–600.Google Scholar
Friedman, C. S., Cloney, D. F., Manzer, D. and Hedrick, R. P. (1991). Haplosporidiosis of the Pacific oyster, Crassostrea gigas. Journal of Invertebrate Pathology 58, 367–372.CrossRefGoogle ScholarPubMed
Goff, L. and Moon, D. (1993). PCR amplification of nuclear and plastid genes from algal herbarium specimens and algal spores. Journal of Phycology 29, 381–384.CrossRefGoogle Scholar
Haydon, D. T., Cleaveland, S., Taylor, L. H. and Laurenson, M. K. (2002). Identifying reservoirs of infection: A conceptual and practical challenge. Emerging Infectious Diseases 8, 1468–1473.Google ScholarPubMed
Hervio, D., Bachère, E., Boulo, V., Cochennec, N., Vuillemin, V., Le Coguic, Y., Cailletaux, G., Mazuri, J. and 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.CrossRefGoogle Scholar
Hine, P. M. (1996). The ecology of Bonamia and decline of bivalve mollusks. New Zealand Journal of Ecology 20, 109–116.Google Scholar
Hine, P. M. and Jones, J. B. (1994). Bonamia and other aquatic parasites of importance to New Zealand. New Zealand Journal of Zoology 21, 49–56.CrossRefGoogle Scholar
Howard, D. W. and Smith, C. S. (1983). Histological techniques for bivalve molluscs. NOAA Technical Memorandum NMFS-F/NEC-25. Woods Hole, MA, USA.Google Scholar
Itoh, N., Tun, K. L., Komiyama, H., Ueki, N. and Ogawa, K. (2004). An ovarian infection in the Iwagaki oyster, Crassostrea nippona, with the protozoan parasite Marteilioides chungmuensis. Journal of Fish Diseases 27, 311–314.CrossRefGoogle ScholarPubMed
Lynch, S. A., Armitage, D. V., Mulcahy, M. F. and Culloty, S. C. (2007). Investigating the possible role of benthic macroinvertebrates and zooplankton in the life cycle of the haplosporidian Bonamia ostreae. Experimental Parasitology 115, 359–368.CrossRefGoogle ScholarPubMed
Lynch, S. A., Armitage, D. V., Wylde, S., Mulcahy, M. F. and Culloty, S. C. (2005). The susceptibility of young prespawning oysters, Ostrea edulis, to Bonamia ostreae. Journal of Shellfish Research 24, 1019–1025.Google Scholar
Martin, A. G., Gérard, A., Cochennec, N. and Langlade, A. (1993). Selecting flat oysters, Ostrea edulis, for survival against the parasite Bonamia ostreae: assessment of the resistance of a first selected generation. Special Publication of the European Aquaculture Society 18, 545–554.Google Scholar
McArdle, J., McKiernan, F., Foley, H. and Hugh-Jones, D. (1991). The current status of Bonamia disease in Ireland. Aquaculture 93, 273–278.CrossRefGoogle Scholar
McManus, J. P. C. (1988). A study of the Ostrea edulis L. population in the North Channel, Cork Harbour. M.Sc. thesis. Department of Zoology, University College Cork, Eire.Google Scholar
Mialhe, E., Bachère, E., Chagot, D. and 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.CrossRefGoogle Scholar
Minchin, D. (1996). Management of the introduction and transfer of marine molluscs. Aquatic Conservation of Marine and Freshwater Ecosystems 4, 229–244.3.0.CO;2-7>CrossRefGoogle Scholar
Minchin, D. and Rosenthal, H. (2002). Exotics for stocking and aquaculture, making correct decisions. In Invasive Aquatic Species of Europe: Distribution, Impacts and Management (ed. Leppäkoski, E., Gollasch, S. and Olenin, S.), pp. 206–215. Kluwer Academic Publishers, Dordrecht, The Netherlands.CrossRefGoogle Scholar
Minchin, D., Duggan, C. B., Holmes, J. M. C. and Neiland, S. (1993). Introduction of exotic species associated with Pacific oyster transfers from France to Ireland. International Council for the Exploration of the Sea C. M. 1993/F: 27, 11.Google Scholar
Montes, J. and Figueras, A. (1987). Bonamia ostreae en una población de ostra plana (Ostrea edulis L.) cultivada en tres diferentes areas de la costa gallega. Cuadernos Marisqueros Publicacion Técnica 12, 683–688.Google Scholar
Narcisi, V., Arzul, I., Cargini, D., Mosca, F., Calzetta, A., Traversa, D., Robert, M., Joly, J. P., Chollet, B., Renault, T. and Tiscar, P. G. (2010). Detection of Bonamia ostreae and Bonamia exitiosa (Haplosporidia) in Ostrea edulis from the Adriatic Sea (Italy). Diseases of Aquatic Organisms (in the Press) 10.3354/dao02167.CrossRefGoogle ScholarPubMed
O'Mahony, J. (1993). Phytoplankton species associated with imports of the Pacific oyster Crassostrea gigas, from France to Ireland. International Council for the Exploration of the Sea. C.M. 1993/F: 26, 8.Google Scholar
Polanco, E., Montes, J., Outón, M. J. and Meléndez, M. I. (1984). Situation pathologique du stock d'huîtres plates en Galice (Espagne) en relation avec Bonamia ostreae. Haliotis 14, 91–95.Google Scholar
Renault, T., Cochennec, N. and Grizel, H. (1995). Bonamia ostreae, parasite of the European flat oyster, Ostrea edulis, does not experimentally infect the Japanese oyster, Crassostrea gigas. Bulletin of the European Association of Fish Pathologists 15, 78–80.Google Scholar
Renault, T., Stokes, N., Chollet, B., Cochennec, N., Berthe, F., Gérard, A. and Burreson, E. (2000). Haplosporidiosis in the Pacific oyster Crassostrea gigas from the French Atlantic coast. Diseases of Aquatic Organisms 42, 207–214.CrossRefGoogle ScholarPubMed
Ruesink, J., Lenihan, H., Trimble, A., Heiman, K., Micheli, F., Byers, J. and Kay, M. (2005). Introduction of Non-native Oysters: Ecosystem Effects and Restoration Implications. Annual Review Ecological Evolutionary Systems 36, 643–689.CrossRefGoogle Scholar
Sambrook, J. and Russell, D. (2001). Molecular Cloning: A Laboratory Manual, 3rd Edn.Cold Spring Harbor Laboratory Press, New York, USA.Google Scholar
Shaw, B. L. and Battle, H. I. (1957). The gross and microscopic anatomy of the digestive tract of the oyster Crassostrea virginica (Gmelin). Canadian Journal of Zoology 35, 325–347.CrossRefGoogle Scholar
Van Banning, P. (1987). Further results of the Bonamia ostreae challenge tests in Dutch oyster culture. Aquaculture 67, 191–194.CrossRefGoogle Scholar
Van Banning, P. (1988). Management strategies to control diseases in the Dutch culture of edible oysters. American Fisheries Society Special Publication 18, 243–245.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Walsh, P. S., Metzger, D. A. and Higuchi, R. (1991). ChelexR 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material, Biotechniques 10, 506–513.Google Scholar
Wasson, K., Zabin, C. J., Bedinger, L., Diaz, M. and Pearse, J. (2001). Biological invasions of estuaries without international shipping: the importance of interregional transportation. Biological Conservation 102, 143–153.CrossRefGoogle Scholar