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Determination of the effects of temperature on viability, metabolic activity and proliferation of two Perkinsus species, and its significance to understanding seasonal cycles of perkinsosis

Published online by Cambridge University Press:  04 February 2008

M. K. LA PEYRE
Affiliation:
US Geological Survey, Louisiana Fish and Wildlife Cooperative Research Unit, School of Renewable Natural Resources, Louisiana State University Agricultural Center, Baton Rouge, Louisiana 70803, USA
S. M. CASAS
Affiliation:
Cooperative Aquatic Animal Health Research Program, Department of Veterinary Science, Louisiana State University Agricultural Center, Baton Rouge, Louisiana 70803, USA
A. VILLALBA
Affiliation:
Centro de Investigacións Mariñas, Consellería de Pesca e Asuntos Marítimos, Xunta de Galicia, Aptdo. 13, E-36620 Vilanova de Arousa, Spain
J. F. LA PEYRE*
Affiliation:
Cooperative Aquatic Animal Health Research Program, Department of Veterinary Science, Louisiana State University Agricultural Center, Baton Rouge, Louisiana 70803, USA
*
*Corresponding author: Department of Veterinary Science, 111 Dalrymple Building, Louisiana State University, Baton Rouge, Louisiana 70803, USA. Tel: +225 578 5419. Fax: +225 578 4890. E-mail: jlapeyre@agctr.lsu.edu

Summary

The range of water temperatures in which Perkinsus species can survive and proliferate remains ill-defined, particularly at lower temperatures. The in vitro viability, metabolic activity, and proliferation of 3 isolates each of P. marinus and P. olseni trophozoites at 28°C, and at 15 and 4°C, after transfer from 28°C, were compared. Both species showed declines in metabolic activity and proliferation from 28°C to 15°C. At 4°C, both species had viability after 30 days incubation time (P. marinus 49%, P. olseni 58%), but limited metabolic activity and no proliferation. Perkinsus marinus viability was further compared when transferred directly from 28°C, 18°C and progressively from 18°C (0·5°C/day) to 2, 4 and 6°C and maintained for up to 4 months. Viability was highest under progressive transfer (77% and 54% after 30 and 60 days exposure to test temperatures). The decrease in P. marinus viability at the lower temperatures in vitro only partially explains decreasing parasite infection intensities in eastern oysters in the colder months of the year. Moreover, the significant decrease in parasite infection intensities in late winter and early spring, as temperatures increase, is likely due to an active process of elimination by oyster host defences.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2008

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References

REFERENCES

Abollo, E., Casas, S. M., Ceschia, G. and Villalba, A. (2006). Differential diagnosis of Perkinsus species by polymerase chain reaction-restriction fragment length polymorphism assay. Molecular and Cellular Probes 20, 323329.CrossRefGoogle ScholarPubMed
Ahn, K. J. and Kim, K. H. (2001). Effect of temperature and salinity on in vitro zoosporulation of Perkinsus sp. in Manila clams Ruditapes philippinarum. Diseases of Aquatic Organisms 48, 4346.CrossRefGoogle ScholarPubMed
Andrews, J. D. (1965). Infection experiments in nature with Dermocystidium marinum in Chesapeake Bay. Chesapeake Science 6, 6067.CrossRefGoogle Scholar
Andrews, J. D. (1988). Epizootiology of the disease caused by the oyster pathogen Perkinsus marinus and its effects on the oyster industry. American Fisheries Society Special Publications 18, 4763.Google Scholar
Andrews, J. D. and Hewatt, W. G. (1957). Oyster mortality in Virginia II. The fungus disease caused by Dermocystidium marinum in oysters of Chesapeake Bay. Ecological Monographs 27, 125.CrossRefGoogle Scholar
Azevedo, C. (1989). Fine structure of Perkinsus atlanticus n. sp. (Apicomplexa, Perkinsea) parasite of the clam Ruditapes decussatus from Portugal. Journal of Parasitology 75, 627635.CrossRefGoogle Scholar
Burreson, E. M. and Ragone Calvo, L. M. (1996). Epizootiology of Perkinsus marinus disease of oysters in Chesapeake Bay, with emphasis on data since 1985. Journal of Shellfish Research 15, 1734.Google Scholar
Burreson, E. M., Ragone Calvo, L. M., La Peyre, J. F., Counts, F. and Paynter, K. T. (1994). Acute osmotic tolerance of cultured cells of the oyster pathogen Perkinsus marinus (Apicomplexa: Perkinsida). Comparative Biochemistry and Physiology A 109, 575582.CrossRefGoogle ScholarPubMed
Bushek, D., Ford, S. E. and Allen, S. K. Jr. (1994). Evaluation of methods using Ray's fluid thioglycollate medium for diagnosis of Perkinsus marinus infection in the eastern oyster, Crassostrea virginica. Annual Review of Fish Diseases 4, 201217.CrossRefGoogle Scholar
Casas, S. M., Villalba, A. and Reece, K. S. (2002 a). Study of perkinsosis in the carpet shell clam Tapes decussatus in Galicia (NW Spain). I. Identification of the aetiological agent and in vitro modulation of zoosporulation by temperature and salinity. Diseases of Aquatic Organisms 50, 5165.CrossRefGoogle Scholar
Casas, S. M., La Peyre, J. F., Reece, K. S., Azevedo, C. and Villalba, A. (2002 b). Continuous in vitro culture of the carpet shell clam Tapes decussatus protozoan parasite Perkinsus atlanticus. Diseases of Aquatic Organisms 52, 217231.CrossRefGoogle ScholarPubMed
Choi, K.-S., Park, K.-I., Lee, K.-W. and Matsuoka, K. (2002). Infection intensity prevalence and histopathology of Perkinsus sp. in the Manila clam, Ruditapes philippinarum, in Isahaya Bay, Japan. Journal of Shellfish Research 21, 119125.Google Scholar
Chu, F.-L. E. and Greene, K. H. (1989). Effect of temperature and salinity on in vitro culture of the oyster pathogen, Perkinsus marinus (Apicomplexa: Perkinsea). Journal of Invertebrate Pathology 53, 260268.CrossRefGoogle Scholar
Cook, T., Folli, M., Klinck, J., Ford, S. and Miller, J. (1998). The relationship between increasing sea-surface temperature and the Northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuarine, Coastal and Shelf Science 46, 587597.CrossRefGoogle Scholar
Cremonte, F., Balseiro, P. and Figueras, A. (2005). Occurrence of Perkinsus olseni (Protozoa: Apicomplexa) and other parasites in the venerid commercial clam Pitar rostrata from Uruguay southwestern Atlantic coast. Diseases of Aquatic Organisms 64, 8590.CrossRefGoogle ScholarPubMed
Dungan, C. F. and Hamilton, R. M. (1995). Use of the tetrazolium-based cell proliferation assay to measure effects of in vitro conditions on Perkinsus marinus (Apicomplexan) proliferation. Journal of Eukaryotic Microbiology 42, 379388.CrossRefGoogle Scholar
Dungan, C. F., Reece, K. S., Moss, J. A., Hamilton, R. M. and Diggles, B. K. (2007). Perkinsus olseni in vitro isolates from the New Zealand Clam Austrovenus stutchburyi. Journal of Eukaryotic Microbiology 54, 263270.CrossRefGoogle ScholarPubMed
Elston, R. A., Dungan, C. F., Meyers, T. R. and Reece, K. S. (2004). Perkinsus sp. infection risk for Manila clams, Venerupis philippinarum (A. Adam and Reeve, 1850), on the Pacific coast of North and Central America. Journal of Shellfish Research 23, 101105.Google Scholar
Fields, R. D. and Lancaster, M. V. (1993). Dual-attribute continuous monitoring of cell proliferation/cytotoxicity. American Biotechnology Laboratory 11, 4850.Google ScholarPubMed
Ford, S. E. (1996). Range extension by the oyster parasite Perkinsus marinus into the North Eastern United States: response to climate change? Journal of Shellfish Research 15, 4556.Google Scholar
Ford, S. E. and Chintala, M. M. (2006). Northward expansion of a marine parasite: testing the role of temperature adaptation. Journal of Experimental Marine Biology and Ecology 339, 226235.CrossRefGoogle Scholar
Ford, S. E. and Smolowitz, R. (2007). Infection dynamics of an oyster parasite in its newly expanded range. Marine Biology 151, 119133.CrossRefGoogle Scholar
Ford, S. E., Schotthoefer, A. and Spruck, C. (1999). In vivo dynamics of the microparasite Perkinsus marinus during progression and regression of infections in eastern oysters. Journal of Parasitology 85, 273282.CrossRefGoogle ScholarPubMed
Gauthier, J. and Vasta, G. (1993). Continuous in vitro culture of the eastern oyster parasite Perkinsus marinus. Journal of Invertebrate Pathology 62, 321323.CrossRefGoogle Scholar
Gauthier, J. and Vasta, G. (1995). In vitro culture of the eastern oyster parasite Perkinsus marinus: optimisation of the methodology. Journal of Invertebrate Pathology 66, 156168.CrossRefGoogle Scholar
Goggin, C. L. and Lester, R. J. G. (1995). Perkinsus, a protistan parasite of abalone in Australia: A review. Marine Freshwater Research 46, 639646.CrossRefGoogle Scholar
Goggin, C. L., Sewell, K. B. and Lester, R. J. G. (1990). Tolerances of Perkinsus spp. (Protozoa, Apicomplexa) to temperature chlorine and salinity. Journal of Shellfish Research 9, 14451448.Google Scholar
Guppy, M. and Withers, P. (1999). Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biological Reviews 74, 140.CrossRefGoogle ScholarPubMed
Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S. and Samuel, M. D. (2002). Climate warming and disease risks for terrestrial and marine biota. Science 296, 21582162.CrossRefGoogle ScholarPubMed
Hewatt, W. G. and Andrews, J. D. (1956). Temperature control experiments on the fungus disease, Dermocystidium marinum, of oysters. Proceedings of the National Shellfisheries Association 46, 129133.Google Scholar
Hine, P. M. (2001). Problems of applying risk analysis to aquatic organisms. In Proceedings of the OIE International Conference on Risk Analysis in Aquatic Animal Health (ed. Rogers, C. J.), pp. 7182 (http:www.oie.int/eng/publicat/ouvrages/a_101.htm).Google Scholar
Hyun, K.-P., Pang, I.-C., Klinck, J. M., Choi, K. S., Lee, J. B., Powell, E. N., Hoffman, E. E. and Bochenek, E. A. (2001). The effect of food composition on Pacific oyster Crassostrea gigas (Thunberg) growth in Korea: a modeling study. Aquaculture 199, 4162.CrossRefGoogle Scholar
Kang, S. G., Choi, K.-S., Bulgakow, A. A., Kim, Y. and Kim, S.-Y. (2003). Enzyme-linked immunosorbent assay (ELISA) used in quantification output in the pacific oyster, Crassostrea gigas, in Korea. Journal of Experimental Marine Biology and Ecology 282, 121.CrossRefGoogle Scholar
La Peyre, J. F. (1996). Propagation and in vitro studies of Perkinsus marinus. Journal of Shellfish Research 15, 89101.Google Scholar
La Peyre, J. F. and Chu, F.-L. E. (1994). Simple procedure for the isolation of Perkinsus marinus merozoites, a pathogen of the eastern oyster, Crassostrea virginica. Bulletin of the European Association of Fish Pathologists 14, 101103.Google Scholar
La Peyre, J. F. and Faisal, M. (1996). Optimal culture conditions for the propagation of the oyster pathogen Perkinsus marinus (Apicomplexa) in protein deficient medium. Parasite 3, 147153.CrossRefGoogle Scholar
La Peyre, J. F., Faisal, M. and Burreson, E. M. (1993). In vitro propagation of the protozoan Perkinsus marinus, a pathogen of the eastern oyster, Crassostrea virginica. Journal of Eukaryotic Microbiology 40, 304310.CrossRefGoogle Scholar
La Peyre, M., Casas, S. and La Peyre, J. (2006). Salinity effects on viability, metabolic activity and proliferation of three Perkinsus species. Diseases of Aquatic Organisms 71, 5974.CrossRefGoogle ScholarPubMed
Le Pape, P., Pagniez, F. and Abdala, H. (2002). A new automatized fluorometric assay for anti-Leishmania drug screening. Acta Parasitologica 47, 7981.Google Scholar
Leethochavalit, L., Upatham, E. S., Choi, K. S., Sawangwong, P., Chalermwat, K. and Kruatrachue, M. (2003). Ribosomal RNA characterization of non-transcribed spacer and two internal transcribed spacers with 5·8S ribosomal RNA of Perkinsus sp. found in undulated surf clams (Paphia undulata) from Thailand. Journal of Shellfish Research 22, 431434.Google Scholar
Leite, R. B., Afonso, R. and Cancela, M. L. (2004). Perkinsus sp. infestation in carpet-shell clams, Ruditapes decussatus (L.), along the Portuguese coast. Results from a 2-year survey. Aquaculture 240, 3953.CrossRefGoogle Scholar
Lester, R. J. G. (1986). Abalone die-back caused by protozoan parasite? Australian Fisheries 45, 2627.Google Scholar
Lester, R. J. G. and Davis, G. H. G. (1981). A new Perkinsus species (Apicomplexa, Perkinsea) from the abalone Haliotis ruber. Journal of Invertebrate Pathology 37, 181187.CrossRefGoogle Scholar
Lester, R. J. G., Goggin, C. L. and Sewell, K. B. (1990). Perkinsus in Australia. In Pathology in Marine Science (ed. Perkins, F. O. and Cheng, T. C.), pp. 189199. Academic Press Inc. San Diego, CA, USA.Google Scholar
Lewis, R. K., Shepherd, S. A., O'Donoghue, P. J. and Phillips, P. H. (1987). Protozoan parasite (Perkinsus) infection in abalone: a progress report. South Australia FISH 11, 78.Google Scholar
Mackin, J. G. (1962). Oyster disease caused by Dermocystidium marinum and other microorganisms in Louisiana. Publications of the Institute of Marine Science, University of Texas 7, 132229.Google Scholar
McLaughlin, S. M. and Faisal, M. (2000). Prevalence of Perkinsus spp. in Chesapeake Bay softshell clams Mya arenaria Linnaeus, 1758 during 1990–1998. Journal of Shellfish Research 19, 349352.Google Scholar
Menendez, M. and Comin, F. A. (2000). Spring and summer proliferation of floating macroalgae in a Mediterranean Coastal Lagoan (Tancada Lagoon, Ebro Delta, NE Spain). Estuarine Coastal and Shelf Science 51, 215223.CrossRefGoogle Scholar
Murrell, A., Kleeman, S. N., Barker, S. C. and Lester, R. J. G. (2002). Synonymy of Perkinsus olseni Lester & Davis, 1981 and Perkinsus atlanticus Azevedo, 1989 and an update on the phylogenetic position of the genus Perkinsus. Bulletin of the European Association of Fish Pathology 22, 258265.Google Scholar
Ngo, T. T. T., Berthe, F. C. J. and Choi, K. S. (2003). Prevalence and infection intensity of the ovarian parasite Marteiliodes chungmuensis during an annual reproductive cycle of the oyster Crassostrea gigas. Diseases of Aquatic Organisms 56, 259267.CrossRefGoogle ScholarPubMed
O'Farrell, C., La Peyre, J. F., Paynter, K. T. and Burreson, E. M. (2000). Osmotic tolerance and volume regulation in in vitro cultures of the oyster pathogen Perkinsus marinus. Journal of Shellfish Research 19, 139145.Google Scholar
Oliver, L. M., Fisher, W. S., Ford, S. E., Ragone Calvo, L. M., Burreson, E. M., Sutton, E. B. and Gandy, J. (1998). Perkinsus marinus tissue distribution and seasonal variation in oysters Crassostrea virginica from Florida, Virginia and New York. Diseases of Aquatic Organisms 34, 5161.CrossRefGoogle ScholarPubMed
Park, K.-I. and Choi, K.-S. (2001). Spatial distribution of the protozoan parasite Perkinsus sp. found in the Manila clams, Ruditapes philippinarum, in Korea. Aquaculture 203, 922.CrossRefGoogle Scholar
Park, K.-I. and Choi, K.-S. (2004). Application of enzyme-linked immunosorbent assay for studying of reproduction in the Manila clam Ruditapes philippinarum (Mollusca: Bivalvia). I. Quantifying eggs. Aquaculture 241, 667687.Google Scholar
Park, K.-I., Park, J.-I., Lee, J. and Choi, K.-S. (2005). Use of molecular markers for species identification of Korean Perkinsus sp. isolated from Manila clams Ruditapes philippinarum. Diseases of Aquatic Organisms 66, 255263.CrossRefGoogle ScholarPubMed
Perkins, F. O. (1966). Life history studies of Dermocystidium marinum, an oyster pathogen. Ph.D. dissertation, Florida State University, Tallahassee, Florida.Google Scholar
Powell, E. N., Gauthier, J. D., Wilson, E. A., Nelson, A., Fay, R. R. and Brooks, J. M. (1992). Oyster disease and climate change. Are yearly changes in Perkinsus marinus parasitism in oysters (Crassostrea virginica) controlled by climactic cycles in the Gulf of Mexico. P.S.Z.N.I: Marine Ecology 13, 243270.CrossRefGoogle Scholar
Ragone Calvo, L. M. and Burreson, E. M. (1994). Characterization of overwintering infections of Perkinsus marinus (Apicomplexa) in Chesapeake Bay oysters. Journal of Shellfish Research 13, 123130.Google Scholar
Ragone Calvo, L. M., Wetzel, R. L. and Burreson, E. M. (2000). Development and verification of a model for the population dynamics of the protistan parasite, Perkinsus marinus, within its host, the eastern oyster, Crassostrea virginica, in Chesapeake Bay. Journal of Shellfish Research 20, 231241.Google Scholar
Ray, S. M. (1954). Biological studies of Dermocystidium marinum. Rice Institute Pamphlet, Special Issue 41, 1114.Google Scholar
Ruano, F. and Cachola, R. (1986). Outbreak of a severe epizootic of Perkinsus marinus (Levin - 78) at Ria de Faro clam's culture beds. Second International Colloquium on Pathology in Marine Aquaculture, 7–11 September 1986, Porto (Portugal), pp. 41–42.Google Scholar
Santmarti, M. M., García Valero, J., Montes, J., Pech, A. and Durfort, M. (1995). Seguimiento del protozoo Perkinsus sp. en las poblaciones de Tapes decussatus y Tapes semidecussatus del delta del Ebro. In Actas del V Congreso Nacional de Acuicultura, 10–13 May 1995 (ed. Castelló, F, Calderer, ), pp. 260265. S. Carlos de la Rápita, Universidad de Barcelona (Spain).Google Scholar
Soniat, T. M. (1985). Changes in levels of infection of oysters by Perkinsus marinus, with special reference to the interaction of temperature and salinity upon parasitism. Northeast Gulf Science 7, 171174.CrossRefGoogle Scholar
Soniat, T. M. (1996). Epizootiology of Perkinsus marinus disease of eastern oysters in the Gulf of Mexico. Journal of Shellfish Research 15, 3543.Google Scholar
Soudant, P., Chu, F.-L. E. and Lund, E. D. (2005). Assessment of the cell viability of cultured Perkinsus marinus (Perkinsea) a parasitic protozoan of the eastern oyster, Crassostrea virginica, using SYBRgreen-propidium iodide double staining and flow cytometry. Journal of Eukaryotic Microbiology 52, 492499.CrossRefGoogle ScholarPubMed
Stickler, S. (2004). Natural Dermo resistance and related defense mechanisms in eastern oysters, Crassostrea virginica, with implications for restoration. Ph.D. dissertation, The College of William and Mary, Williamsburg, Virginia.Google Scholar
Stickler, S., Wagner, E., Encomio, V., Allen, S. and La Peyre, J. (2001). Natural Dermo resistance and its role in the development of hatcheries for the Gulf of Mexico. Journal of Shellfish Research 20, 557.Google Scholar
Vidal, M., Morgui, J. A., Latasa, M., Romero, J. and Camp, J. (1997). Factors controlling seasonal variability of benthic ammonium release and oxygen uptake in Alfacs Bay (Ebro Delta, NW Mediterranean). Hydrobiologia 350, 169178.CrossRefGoogle Scholar
Villalba, A., Casas, S. M., López, C. and Carballal, M. J. (2005). Study of perkinsosis in the carpet shell clam Tapes decussatus in Galicia (NW Spain). II Temporal pattern of disease dynamics and association with clam mortality. Diseases of Aquatic Organisms 65, 257267.CrossRefGoogle ScholarPubMed
Villalba, A., Reece, K. S., Ordas, M. C., Casas, S. M. and Figueras, A. (2004). Perkinsosis in molluscks: a review. Aquatic Living Resources 17, 411432.CrossRefGoogle Scholar