Infection dynamics of Bonamia exitiosa on intertidal Ostrea angasi farms.


Journal

Journal of fish diseases
ISSN: 1365-2761
Titre abrégé: J Fish Dis
Pays: England
ID NLM: 9881188

Informations de publication

Date de publication:
Mar 2020
Historique:
received: 31 10 2019
revised: 20 12 2019
accepted: 20 12 2019
pubmed: 10 1 2020
medline: 13 8 2020
entrez: 10 1 2020
Statut: ppublish

Résumé

Bonamia spp. cause epizootics in oysters worldwide. In southern Australia, Bonamia exitiosa Hine, Cochennac and Berthe, 2001 threatens aquaculture of Ostrea angasi Sowerby, 1871. Bonamia spp. infections can display strong seasonality, but seasonal dynamics of B. exitiosa-O. angasi are unknown. Ostrea angasi naïve to B. exitiosa infection were stocked onto farms in three growing regions, and B. exitiosa was monitored seasonally for one year. Environmental parameters we measured did not correlate with B. exitiosa prevalence or infection intensities. Extreme temperatures suggest O. angasi culture systems need development. Bonamia exitiosa prevalence increased over time. After three months, O. angasi had B. exitiosa prevalence of 0.08-0.4, and after one year, the prevalence was 0.57-0.88. At some sites, O. angasi had >0.5 B. exitiosa prevalence in >6 months, but at other sites, >9 months passed before prevalence was >0.5. Bonamia exitiosa infection intensities were low with no seasonal pattern but were affected by the interaction of site, season and oyster meat:shell ratio. Understanding infection and initiating a breeding programme for resistance would provide benefits for O. angasi industry expansion.

Identifiants

pubmed: 31918456
doi: 10.1111/jfd.13134
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

359-369

Subventions

Organisme : South Australian Research and Development Institute
Organisme : Fisheries Research and Development Corporation
ID : 2015-001
Organisme : Flinders University
Organisme : Australian Government Department of Agriculture

Informations de copyright

© 2020 John Wiley & Sons Ltd.

Références

Arzul, I., & Carnegie, R. B. (2015). New perspective on the haplosporidian parasites of molluscs. Journal of Invertebrate Pathology, 131, 32-42. https://doi.org/10.1016/j.jip.2015.07.014
Arzul, I., Gagnaire, B., Bond, C., Chollet, B., Morga, B., Ferrand, S., … Renault, T. (2009). Effects of temperature and salinity on the survival of Bonamia ostreae, a parasite infecting flat oysters Ostrea edulis. Diseases of Aquatic Organisms, 85, 67-75. https://doi.org/10.3354/dao02047
Arzul, I., Miossec, L., Blanchet, E., Garcia, C., François, C., & Joly, J.-P. (2006). Bonamia ostreae and Ostrea edulis: A stable host-parasite system in France? In Proceedings of the XI international symposium for veterinary epidemiology and economics conference, Cairns, Australia, 6-11 August 2006 (p. 5).
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. Journal of Invertebrate Pathology, 98, 344-350. https://doi.org/10.1016/j.jip.2008.03.010
Audemard, C., Carnegie, R. B., Hill, K. M., Peterson, C. H., & Burreson, E. M. (2014). Bonamia exitiosa transmission among and incidence in, Asian oyster Crassostrea ariakensis under warm euhaline conditions. Diseases of Aquatic Organisms, 110, 143-150. https://doi.org/10.3354/dao02648
Audemard, C., Carnegie, R. B., Stokes, N. A., Bishop, M. J., Peterson, C. H., & Burreson, E. M. (2008). Effects of salinity on Bonamia sp. survival in the Asian oyster Crassostrea ariakensis. Journal of Shellfish Research, 27, 535-540. https://doi.org/10.2983/0730-8000(2008)27[535:EOSOBS]2.0.CO;2
Ben-Horin, T., Burge, C. A., Bushek, D., Groner, M. L., Proestou, D. A., Huey, L. I., … Carnegie, R. B. (2018). Intensive oyster aquaculture can reduce disease impacts on sympatric wild oysters. Aquaculture Environment Interactions, 10, 557-567. https://doi.org/10.3354/aei00290
Bidegain, G., Powell, E. N., Klinck, J. M., Hofmann, E. E., Ben-Horin, T., Bushek, D., … Guo, X. (2017). Modeling the transmission of Perkinsus marinus in the Eastern oyster Crassostrea virginica. Fisheries Research, 186, 82-93. https://doi.org/10.1016/j.fishres.2016.08.006
Bishop, M. J., Carnegie, R. B., Stokes, N. A., Peterson, C. H., & Burreson, E. M. (2006). Complications of a non-native oyster introduction: Facilitation of a local parasite. Marine Ecology Progress Series, 325, 145-152. https://doi.org/10.3354/meps325145
T. Bradley (Ed.) (2019). Agriculture Victoria. Aquatic animal health subprogram: Bonamiasis in farmed native oysters (Ostrea angasi). Final report. FRDC project 2015-001, Attwood, Victoria May 2019.
Bush, A. O., Lafferty, K. D., Lotz, J. M., Shostak, A. (1997). Parasitology meets ecology on its own terms: Margolis et al revisited. The Journal of Parasitology, 83(4), 575-583. https://doi.org/10.2307/3284227
Buss, J. J., Harris, J. O., Tanner, J. E., Wiltshire, K. H., & Deveney, M. (2019a). Rapid transmission of Bonamia exitiosa by cohabitation causes mortality in Ostrea angasi. Journal of Fish Diseases. https://doi.org/10.1111/jfd.13116, in press.
Buss, J. J., Wiltshire, K. H., Prowse, T. A. A., Harris, J. O., & Deveney, M. (2019b). Bonamia in Ostrea angasi: Diagnostic performance, field prevalence and intensity. Journal of Fish Diseases, 42, 63-74. https://doi.org/10.1111/jfd.12906
Carnegie, R. B., Stokes, N. A., Audemard, C., Bishop, M. J., Wilbur, A. E., Alphin, T. D., … Burreson, E. M. (2008). Strong seasonality of Bonamia sp. infection and induced Crassostrea ariakensis mortality in Bogue and Masonboro Sounds, North Carolina, USA. Journal of Invertebrate Pathology, 98, 335-343. https://doi.org/10.1016/j.jip.2008.03.009
Cochennec-Laureau, N., & Auffret, M. (2002). Experimental effects of temperature on the Bonamiasis model. European project FAIR-CT98-4120. Environmental Factors and Shellfish Diseases, Final Report, 15/05/2002.
Corbeil, S., Arzul, I., Diggles, B. K., 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. Diseases of Aquatic Organisms, 71, 75-80. https://doi.org/10.3354/dao071075
Corbeil, S., Handlinger, J., & Crane, M. S. J. (2009). Bonamiasis in Australian Ostrea angasi. Australian and New Zealand standard diagnostic procedure (pp. 1-22). Sub-committee of Animal Health Laboratory Standards.
Crawford, C. (2016). National review of Ostrea angasi aquaculture: Historical culture, current methods and future priorities. Hobart, Australia: Institute of Marine and Antarctic Studies.
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. https://doi.org/10.1016/j.aquaculture.2004.04.007
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. https://doi.org/10.1016/S0044-8486(96)01290-2
Dent, J., Mayfield, S., & Carroll, J. (2016). Harvestable biomass of Katelysia spp. in the South Australian commercial mud cockle fishery. Adelaide, Australia: South Australian Research and Development Institute (Aquatic Sciences). SARDI publication No. F2014/000191-2.
Devleesschauwer, B., Torgerson, P., Charlier, J., Levecke, B., Praet, N., Roelandt, S., … Speybroeck, N. (2015). prevalence: Tools for prevalence assessment studies. R package version 0.4.0. Retrieved from http://cran.r-project.org/package=prevalence
Diggles, B. K. (2003). Shellfish disease surveillance programme - Final report June 2003 (pp. 1-24). NIWA Client Report AUS2002-018, June 2003, NIWA Project NAU03911, Prepared for Primary Industries and Resources South Australia (PIRSA).
Diggles, B. K., Cochennec-Laureau, N., & Hine, P. M. (2003). Comparison of diagnostic techniques for Bonamia exitiosus for flat oysters Ostrea chilensis in New Zealand. Aquaculture, 220, 145-156. https://doi.org/10.1016/S0044-8486(02)00635-X
Dix, T. G. (1980). Growth of the Native oysters Ostrea angasi using raft culture in Tasmania, Australia. Aquaculture, 19, 109-115. https://doi.org/10.1016/0044-8486(80)90012-5
Edgar, G. J. (2008). Australian marine life: The plants and animals of temperate waters (2nd ed.). Chatswood, Australia: New Holland Publishers.
Engelsma, M. Y., Kerkhoff, S., Roozenburg, I., Haenen, O. L. M., van Gool, A., Sistermans, W., … Hummel, H. (2010). Epidemiology of Bonamia ostreae infecting European flat oysters Ostrea edulis from Lake Grevelingen, The Netherlands. Marine Ecology Progress Series, 409, 131-142. https://doi.org/10.3354/meps08594
Environment Protection Authority (EPA) (2005). Code of practice for the environmental management of the South Australian oyster farming industry. Adelaide, Australia: EPA.
Feng, C., Lin, X., Wang, F., Zhang, Y., Lv, J., Wang, C., … Li, H. (2013). Detection and characterisation of Bonamia ostreae in Ostrea edulis imported to China. Diseases of Aquatic Organisms, 106, 85-91. https://doi.org/10.3354/dao02631
Figueras, A., & 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, 3, 98-100.
Food and Agriculture Organization of the United Nations (FAO) (2018). The state of world fisheries and aquaculture 2018 - Meeting the sustainable development goals. Rome, Italy: FAO.
Gillies, C. L., Crawford, C., & Hancock, B. (2017). Restoring Angasi oyster reefs: What is the endpoint ecosystem we are aiming for and how do we get there? Ecological Management and Restoration, 18, 214-222. https://doi.org/10.1111/emr.12278
Grangeré, K., Ménesguen, A., Lefebvre, S., Bacher, C., & Pouvreau, S. (2009). Modelling the influence of environmental factors on the physiological status of the Pacific oyster Crassostrea gigas in an estuarine embayment; The Baie des Veys (France). Journal of Sea Research, 62, 147-158. https://doi.org/10.1016/j.seares.2009.02.002
Handlinger, J. H., Rawlin, G., Wilson, J., Johnston, H., Condron, R., O'Donoghue, P., & Phillips, P. (1999). Bonamiasis in Australia. In Annual international conference and exposition of the world aquaculture society, Sydney, New South Wales, 26 April-2 May, 1999.
Héral, M., & Deslous-Paoli, J. M. (1991). Oyster culture in European countries. In W. Menzel (Ed.), Estuarine and marine bivalve mollusk culture (Chapter 13, pp. 154-190). Boca Raton, FL: CRC Press.
Hill, K. M., Stokes, N. A., Webb, S. C., Hine, P. M., Kroeck, M. A., Moore, J. D., … Carnegie, R. B. (2014). Phylogenetics of Bonamia parasites based on small subunit and internal transcribed spacer region ribosomal DNA sequence data. Diseases of Aquatic Organisms, 110, 33-54. https://doi.org/10.3354/dao02738
Hine, P. M. (1991). The annual pattern of infection by Bonamia sp. in New Zealand flat oysters, Tiostrea chilensis. Aquaculture, 93, 241-251. https://doi.org/10.1016/0044-8486(91)90236-Z
Hine, P. M., Diggles, B. K., Parsons, M. J. D., Pringle, A., & Bull, B. (2002). The effects of stressors on the dynamics of Bonamia exitosus Hine, Cochennec-Laureau and Berthe, infections in flat oysters Ostrea chilensis (Philippi). Journal of Fish Diseases, 25, 545-554. https://doi.org/10.1046/j.1365-2761.2002.00410.x
Hine, P. M., & Jones, J. B. (1994). Bonamia and other aquatic parasites of importance to New Zealand. New Zealand Journal of Zoology, 21, 49-56. https://doi.org/10.1080/03014223.1994.9517975
Holliday, J. E. (1995). Nursery culture of Sydney rock oysters, Saccostrea commercialis (Iredale & Roughley, 1933) and Pacific oysters, Crassostrea gigas (Thunberg, 1793). PhD Thesis. University of Tasmania, Australia.
Hone, P. (1993). Introduction of Crassostrea gigas (Pacific oyster) in South Australia. Shellfish Environmental Monitoring Program. Adelaide, Australia: Department of Primary Industries.
Howard, A. E. (1994). The possibility of long distance transmission of Bonamia by fouling on boat hulls. Bulletin of the European Association of Fish Pathologists, 14, 211-212.
Hudson, E. B., & Hill, B. J. (1991). Impact and spread of bonamiasis in the UK. Aquaculture, 93, 279-285. https://doi.org/10.1016/0044-8486(91)90240-8
Lallias, D., Arzul, I., Heurtebise, S., Ferrand, S., Chollet, B., Robert, M., … Lapègue, S. (2008). Bonamia ostreae-induced mortalities in one-year old European flat oysters Ostrea edulis: Experimental infection by cohabitation challenge. Aquatic Living Resources, 21, 423-439. https://doi.org/10.1051/alr:2008053
Leith, P. B., & Haward, M. (2010). Climate change adaptation in the Australian edible oyster industry: An analysis of policy and practice. Hobart, Tasmania, Australia: University of Tasmania.
Li, X., Miller-Ezzy, P. A., Crawford, C., Gardner, D., & Deveney, M. (2019). Future oysters CRC-P: Species diversification to provide alternatives for commercial production. Adelaide, South Australia, Australia: South Australian Research and Development Institute - Aquatic Science Centre.
Lynch, S. A., Abollo, E., Ramilo, A., Cao, A., Culloty, S. C., & Villalba, A. (2010). 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. Parasitology, 137, 1515-1526. https://doi.org/10.1017/S0031182010000326
Lynch, S. A., Flannery, G., Hugh-Jones, T., Hugh-Jones, D., & Culloty, S. C. (2014). Thirty-year history of Irish (Rossmore) Ostrea edulis selectively bred for disease resistance to Bonamia ostreae. Diseases of Aquatic Organisms, 110, 113-121. https://doi.org/10.3354/dao02734
Maiti, S. K., & Chowdhury, A. (2013). Effects of anthropogenic pollution on mangrove biodiversity: A review. Journal of Environmental Protection, 4, 1428-1434. https://doi.org/10.4236/jep.2013.412163
McDonald, J. L., & Hodgson, D. J. (2018). Prior precision, prior accuracy, and the estimation of disease prevalence using imperfect diagnostic tests. Frontiers in Veterinary Science, 5, 83. https://doi.org/10.3389/fvets.2018.00083
Mitchell, I. M., Crawford, C. M., & Rushton, M. J. (2000). Flat oyster (Ostrea angasi) growth and survival rates at Georges Bay, Tasmania (Australia). Aquaculture, 191, 309-321. https://doi.org/10.1016/S0044-8486(00)00441-5
Morley, N. J. (2010). Interactive effects of infectious diseases and pollution in aquatic molluscs. Aquatic Toxicology, 96, 27-36. https://doi.org/10.1016/j.aquatox.2009.09.017
Nell, J. A. (2001). The history of oyster farming in Australia. Marine Fisheries Review, 63, 14-25.
O'Connor, S. J. (2015). Factors effecting reproduction and larval development of Ostrea angasi (Sowerby 1871): Advancing hatchery production. PhD Thesis. University of Tasmania, Australia.
O'Sullivan, B. W. (1980). The fertility of the Port Lincoln oyster (Ostrea angasi, Sowerby) from West Lakes, South Australia. Aquaculture, 19, 1-11. https://doi.org/10.1016/0044-8486(80)90002-2
Peeler, E. J., Oidtmann, B. C., Midtlyng, P. J., Miossec, L., & Gozlan, R. E. (2011). Non-native aquatic animals introductions have driven disease emergence in Europe. Biological Invasions, 13, 1291-1303. https://doi.org/10.1007/s10530-010-9890-9
Plummer, M. (2017). JAGS Version 4.3.0 user manual. Retrieved from https://web.sgh.waw.pl/~atoroj/ekonometria_bayesowska/jags_user_manual.pdf
Primary Industries and Regions SA (2017). Aquaculture public register. Retrieved from https://pir.sa.gov.au/aquaculture/aquaculture_public_register
R Core Team (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Rahman, M. A., Henderson, S., Miller-Ezzy, P., Li, X. X., & Qin, J. G. (2020). Analysis of the seasonal impact of three marine bivalves on seston particles in the water column. Journal of Experimental Marine Biology and Ecology, 522,1-10. ttps://doi.org/10.1016/j.jembe.2019.151251
Rahman, M. A., Henderson, S., Miller-Ezzy, P., Li, X. X., & Qin, J. G. (2019). Immune response to temperature stress in three bivalve species: Pacific oyster Crassostrea gigas, Mediterranean mussel Mytilus galloprovincialis and mud cockle Katelysia rhytiphora. Fish and Shellfish Immunology, 86, 868-874. https://doi.org/10.1016/j.fsi.2018.12.017
Rajagopal, S., van der Velde, G., Jansen, J., van der Gaag, M., Atsma, G., Janssen-Mommen, J. P. M., … Jenner, H. A. (2005). Thermal tolerance of the invasive oyster Crassostrea gigas: Feasibility of heat treatment as antifouling option. Water Research, 39, 4335-4342. https://doi.org/10.1016/j.watres.2005.08.021
Reiczigel, J., Marozzi, M., Fábián, I., & Rózsa, L. (2019). Biostatistics for parasitologists - A primer to Quantitative Parasitology. Trends in Parasitology, 35, 277-281. https://doi.org/10.1016/j.pt.2019.01.003
Rogan, E., Culloty, S. C., Cross, T. F., Mulcahy, M. (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(4), 311-315. https://doi.org/10.1016/0044-8486(91)90323-Y
Scholthof, K.-B.-G. (2007). The disease triangle: Pathogens, the environment and society. Nature Publishing Group, 5, 152-156. https://doi.org/10.1038/nrmicro1596
Standards Australia (2015). Australian fish names standard AS 5300-2015. ACT, Australia: Fisheries Research and Development Corporation (FRDC) Fish Names Committee (FNC). ISBN 978-0-646-93768-7.
Su, Y.-S., & Yajima, M. (2015). R2jags: Using R to Run ‘JAGS’. R package version 0.5-7. Retrieved from https://CRAN.R-project.org/package=R2jags
Tam, N. F. Y., & Wong, Y. S. (1995). Mangrove soils as sinks for wastewater-borne pollutants. Hydrobiologia, 295, 231-241. https://doi.org/10.1007/BF00029130
Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (4th ed.). New York, NY: Springer. https://doi.org/10.1007/978-0-387-21706-2
Wear, R., Theil, M., Bryars, S., Tanner, J., & de Jong, S. (2004). Environmental risk assessment of intertidal shellfish aquaculture in South Australia. Adelaide, Australia: South Australian Research and Development Institute (Aquatic Sciences). SARDI publication No. RD04/0155.
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. R package version 3.2.1. Retrieved from https://cran.r-project.org/web/packages/ggplot2/index.html
Youngflesh, C. (2018). MCMCvis: Tools to visualize, manipulate and summarize MCMC output. Journal of Open Source Software, 3, 640. https://doi.org/10.21105/joss.00640

Auteurs

Jessica Jamuna Buss (JJ)

College of Science and Engineering, Flinders University, Adelaide, SA, Australia.
South Australian Research and Development Institute (SARDI), Aquatic Sciences Centre and Marine Innovation Southern Australia, West Beach, SA, Australia.

Kathryn Helen Wiltshire (KH)

South Australian Research and Development Institute (SARDI), Aquatic Sciences Centre and Marine Innovation Southern Australia, West Beach, SA, Australia.

James Owen Harris (JO)

College of Science and Engineering, Flinders University, Adelaide, SA, Australia.
South Australian Research and Development Institute (SARDI), Aquatic Sciences Centre and Marine Innovation Southern Australia, West Beach, SA, Australia.

Jason Elliot Tanner (JE)

South Australian Research and Development Institute (SARDI), Aquatic Sciences Centre and Marine Innovation Southern Australia, West Beach, SA, Australia.

Marty Robert Deveney (MR)

College of Science and Engineering, Flinders University, Adelaide, SA, Australia.
South Australian Research and Development Institute (SARDI), Aquatic Sciences Centre and Marine Innovation Southern Australia, West Beach, SA, Australia.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH