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Horizontal transmission of Thelohania contejeani in the endangered white-clawed (Austropotamobius pallipes) and the invasive signal crayfish (Pacifastacus leniusculus)

Published online by Cambridge University Press:  20 July 2012

EMILY M. IMHOFF
Affiliation:
Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK
ROBERT J. G. MORTIMER
Affiliation:
School of Earth and the Environment, University of Leeds, Leeds LS2 9JT, UK
MARTIN CHRISTMAS
Affiliation:
Environment Agency, Phoenix House, Global Avenue, Millshaw LS11 8PG, UK
ALISON M. DUNN*
Affiliation:
Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, UK
*
*Corresponding author: Institute of Integrative and Comparative Biology, University of Leeds, Leeds LS2 9JT, UK. Tel: +44 (0)113 3432856. Fax: +44 (0)113 3432835. E-mail:[email protected]

Summary

The microsporidian parasite Thelohania contejeani causes porcelain disease and has been implicated in mass mortalities in populations of the endangered European crayfish Austropotamobius pallipes. However, the route of parasite transmission is not known. This paper investigates the horizontal transmission of T. contejeani between A. pallipes hosts as well as its transmissibility to the invasive signal crayfish (Pacifastacus leniusculus). Field collected juvenile A. pallipes and P. leniusculus were assigned to 1 of 3 experimental treatments; fed heavily infected A. pallipes tissue, exposed to water from tanks housing heavily parasitized A. pallipes, and a control group to provide an estimate of the baseline infection levels in the field. After 26 weeks, abdominal muscle samples were screened by PCR for T. contejeani. Infection was significantly higher in the treatment groups (83% in the cannibalism treatment, 42% in the water exposure treatment) than in the control group (4%), providing evidence for horizontal transmission of the parasite between A. pallipes hosts. Cannibalism and scavenging are common amongst crayfish, providing transmission opportunities in the field. The study also provides the first direct evidence for transmission of the parasite from an indigenous European crayfish species to the invasive signal crayfish, with 50% of P. leniusculus in each treatment, and 8% of control animals infected. We discuss the possibility that high density populations of the invasive signal crayfish may serve either as reservoirs or sinks for the parasite.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Abrahamsson, S. A. A. (1966). Dynamics of an isolated population of the crayfish Astacus astacus Linné. Oikos 17, 96107.CrossRefGoogle Scholar
Alderman, D. J. (1996). Geographical spread of bacterial and fungal diseases of crustaceans. Revue Scientifique et Technique de l'Office International des Epizooties. 15, 603632.CrossRefGoogle ScholarPubMed
Arrignon, J. C. V. and Roché, B. (1983). Population of the crayfish Austropotamobius pallipes pallipes Lereboullet in a brook of Corsica, France. Freshwater Crayfish 5, 229238.Google Scholar
Cossins, A. R. and Bowler, K. (1974). An histological and ultrastructural study of Thelohania contejeani Henneguy, 1892 (Nosematidae), Microsporidian parasite of the crayfish Austropotamobius pallipes Lereboullet. Parasitology 68, 8191.CrossRefGoogle Scholar
Diéguez-Uribeondo, J., Pinedo-Ruíz, J. and Muzquiz, J. L. (1997). Thelohania contejeani in the province of Alava, Spain. Bulletin Francais de la Pêche et de la Pisciculture 347, 749752.CrossRefGoogle Scholar
Duffield, J. E. (1933). Fluctuations in numbers among freshwater crayfish, Potamobius pallipes Lereboullet. Journal of Animal Ecology 2, 184196.CrossRefGoogle Scholar
Dunn, A. M. (2009). Parasites and biological invasions. Advances in Parasitology 68, 161184.CrossRefGoogle ScholarPubMed
Dunn, A. M., Torchin, M. E., Hatcher, M. J., Kotanen, P. M., Blumenthal, D. M., Byers, J. E., Coon, C. A. C, Frankel, V. M., Holt, R. D., Hufbauer, R. A., Kanarek, A. R., Shierenbeck, K. A., Wolfe, L. M. and Perkins, S. E. (2012). Indirect effects of parasites on invasions. Functional Ecology (in the Press).CrossRefGoogle Scholar
Dunn, J. C., McClymont, H. E., Christmas, M. and Dunn, A. M. (2009). Competition and parasitism in the native white-clawed crayfish Austropotamobius pallipes and the invasive signal crayfish Pacifastacus leniusculus in the UK. Biological Invasions 11, 315324.CrossRefGoogle Scholar
El-Matbouli, M. and Soliman, H. (2006). Molecular diagnostic methods for detection of Thelohania contejeani (Microsporidia), the causative agent of porcelain disease in crayfish. Diseases of Aquatic Organisms 69, 205211.CrossRefGoogle ScholarPubMed
Fischer, H. (1992). The porcelain disease of the freshwater crayfish Astacus astacus L., caused by Thelohania contejeani. DVM Thesis, Tierärztliche Fakultät, Universität München, München, Germany.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates Molecular Marine Biology and Biotechnology 3, 294299.Google ScholarPubMed
Graham, L. and France, R. (1986). Attempts to transmit experimentally the microsporidian Thelohania contejeani in freshwater crayfish (Orconectes virilis). Crustaceana 51, 208211.CrossRefGoogle Scholar
Guan, R. and Wiles, P. R. (1996). Growth, density and biomass of crayfish, Pacifastacus leniusculus, in a British lowland river. Aquatic Living Resources 9, 265272.CrossRefGoogle Scholar
Hatcher, M. J. and Dunn, A. M. (2011). Parasites in Ecological Communities. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Hatcher, M. J., Dick, J. and Dunn, A. M. (2012). Disease emergence and invasions. Functional Ecology (in the Press)CrossRefGoogle ScholarPubMed
Henneguy, G. and Thélohan, P. (1892). Myxosporidies parasites des muscles chez quelques crustacés décapodes. Annuales Micrographie 4, 617641.Google Scholar
Hoffman, R. W., El-Matbouli, M., Oidtmann, B. and Fischer, H. (1999). Light and electron microscopic studies on porcelain disease (Thelohania contejeani) in noble crayfish (Astacus astacus). Freshwater Crayfish 12, 933934.Google Scholar
Holdich, D. M. and Domaniewski, J. C. J. (1995). Studies on a mixed population of the crayfish Austropotamobius pallipes and Pacifastacus leniusculus in England. Freshwater Crayfish 10, 3745.Google Scholar
Holdich, D. M. and Reeve, I. D. (1991). The distribution of freshwater crayfish in the British Isles with particular reference to crayfish plague, alien introductions and water quality. Aquatic Conservation 1, 139158.CrossRefGoogle Scholar
Holdich, D., Sibley, P. and Peay, S. (2004). The white-clawed crayfish – a decade on. British Wildlife 15, 153164.Google Scholar
Horton, M. P. (2009). Establishing the island of Ireland's first ark site for the white-clawed crayfish Austropotamobius pallipes in the Ballinderry river system, Co. Tyrone. In Crayfish Conservation in the British Isles (ed. Brickland, J., Holdich, D. M. and Imhoff, E. M.), Proceedings of a conference held on 25 March 2009, Leeds, UK, pp. 8794.Google Scholar
Hutchings, A. (2009). Monitoring Austopotamobius pallipes (Lereboullet) in a chalk stream in southern England. In Crayfish Conservation in the British Isles (ed. Brickland, J., Holdich, D. M. and Imhoff, E. M.), Proceedings of a conference held on 25 March 2009, Leeds, UK, pp. 99119.Google Scholar
Imhoff, E., Mortimer, R. J. G., Christmas, M. and Dunn, A. M. (2011). Invasion progress of the signal (Pacifastacus leniusculus (Dana)) crayfish and displacement of the native white-clawed crayfish (Austropotamobius pallipes (Lereboullet)) in the River Wharfe, UK. Freshwater Crayfish 18, 4553.CrossRefGoogle Scholar
Imhoff, E., Mortimer, R. J. G., Christmas, M. and Dunn, A. M. (2010). Non-lethal tissue sampling allows molecular screening for microsporidian parasites in signal (Pacifastacus leniusculus Dana) and vulnerable white-clawed crayfish (Austropotamobius pallipes Lereboullet). Freshwater Crayfish 17, 145150.Google Scholar
Imhoff, E., Mortimer, R. J. G., Christmas, M. and Dunn, A. M. (2009). Porcelain disease in white-clawed and signal crayfish in the UK. In Crayfish Conservation in the British Isles (ed. Brickland, J., Holdich, D. M. and Imhoff, E. M.), Proceedings of a conference held on 25 March 2009, Leeds, UK, pp. 4956.Google Scholar
IUCN, 2010. IUCN Red List of Threatened Species. Version 2010.4. www.iucnredlist.org. Accessed 14 February 2011.Google Scholar
Kemp, E., Birkinshaw, N., Peay, S. and Hiley, P. D. (2003). Reintroducing the white-clawed crayfish Austropotamobius pallipes. Conserving Natura 2000 Rivers Conservation Techniques Series No. 1. English Nature, Peterborough, UK.Google Scholar
Kocher, T. D., Thomas, W. K., Meyer, A., Edwards, S. V., Paabo, S., Villablanca, F. X. and Wilson, A. C. (1989). Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences, USA 86, 61966200.CrossRefGoogle ScholarPubMed
Lom, J., Nilson, F. and Dykova, I. (2001). Thelohania contejeani Henneguy, 1892: dimorphic life cycle and taxonomic affinities, as indicated by ultrastructural and molecular study. Parasitology Research 87, 860872.CrossRefGoogle ScholarPubMed
Mason, J. C. (1977). Reproductive efficiency of Pacifastacus leniusculus in culture. Freshwater Crayfish 3, 101117.Google Scholar
Mazylis, A. (1978). Astacus astacus L. infected with Thelohania contejeani Henneguy. Freshwater Crayfish 4, 472473.Google Scholar
Moodie, E. G., Le Jambre, L. F. and Katz, M. E. (2003 a). Thelohania montirivulorum sp. nov. (Microspora: Thelohaniidae), a parasite of the Australian freshwater crayfish, Cherax destructor (Decapoda: Parastacidae): fine ultrastructure, molecular characteristics and phylogenetic relationships. Parasitology Research 91, 215228.CrossRefGoogle ScholarPubMed
Moodie, E. G., Le Jambre, L. F. and Katz, M. E. (2003 b). Thelohania parastaci sp. nov. (Microspora: Thelohaniidae), a parasite of the Australian freshwater crayfish, Cherax destructor (Decapoda: Parastacidae). Parasitology Research 91, 151165.CrossRefGoogle ScholarPubMed
Mori, M. and Salvidio, S. (2000). The occurrence of Thelohania contejeani Henneguy, a microsporidian parasite of the crayfish Austropotamobius pallipes (Lereboullet), in Liguria Region (NW Italy). Journal of Limnology 59, 167169.CrossRefGoogle Scholar
Nightingale, J. (2009). Conservation of the white-clawed crayfish in South-west England. In Crayfish Conservation in the British Isles (ed. Brickland, J., Holdich, D. M. and Imhoff, E. M.), Proceedings of a conference held on 25 March 2009, Leeds, UK, pp. 8586.Google Scholar
Oidtmann, B., El-Matbouli, M., Fischer, H., Hoffmann, R., Klärding, K., Schmid, I. and Schmidt, R. (1996). Light microscopy of Astacus astacus L. under normal and selected pathological conditions, with special emphasis to porcelain disease and crayfish plague. Freshwater Crayfish 11, 465480.Google Scholar
O'Keefe, C. and Reynolds, J. D. (1983). The occurrence of crayfish diseases and their significance in Ireland. Freshwater Crayfish 5, 299306.Google Scholar
Peay, S. (2002). Monitoring the White-clawed Crayfish. English Nature, Peterborough, UK.Google Scholar
Peay, S. (2009). Selection criteria for “ark sites” for white-clawed crayfish. In Crayfish Conservation in the British Isles (ed. Brickland, J., Holdich, D. M. and Imhoff, E. M.), Proceedings of a conference held on 25 March 2009, Leeds, UK, pp. 4956.Google Scholar
Pixell Goodrich, H. (1956). Crayfish epidemics. Parasitology 46, 480483.CrossRefGoogle Scholar
Poulin, R., Paterson, R. A., Townsend, C. R., Tompkins, D. M. and Kelly, D. W. (2011). Biological invasions and the dynamics of endemic diseases in freshwater ecosystems. Freshwater Biology 56, 676688.CrossRefGoogle Scholar
Prenter, J., MacNeil, C., Dick, J. T. A. and Dunn, A. M. (2004). Roles of parasites in animal invasions. Trends in Ecology and Evolution 19, 385390.CrossRefGoogle ScholarPubMed
Schäperclaus, W. (1954). Fischkrankheiten. Akademie-Verlag, Berlin, Germany.Google Scholar
Solter, L. F. and Maddox, J. V. 1998. Physiological host specificity of microsporidia as an indicator of ecological host specificity. Journal of Invertebrate Pathology 71, 207216.CrossRefGoogle ScholarPubMed
Tompkins, D. M., Dunn, A. M., Smith, M. J. and Telfer, S. (2011). Wildlife diseases, from individuals to ecosystems. Journal of Animal Ecology 80, 1938.CrossRefGoogle ScholarPubMed
Vey, A. and Vago, C. (1973). Protozoan and fungal diseases of Austropotamobius pallipes Lereboullet in France. Freshwater Crayfish 1, 165180.Google Scholar
Voronin, V. N. (1971). New data on microsporidiosis of the crayfish, Astacus astacus (L. 1758). Parazitologya 5, 186191.Google Scholar
Weiss, L. M., Zhu, X., Cali, A., Tanowitz, H. B. and Wittner, M. (1994). Utility of microsporidian ribosomal-RNA in diagnosis and phylogeny – a review. Folia Parasitologia 41, 8190.Google ScholarPubMed