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Influence of host reproductive state on Sphaerothecum destruens prevalence and infection level

  • D. ANDREOU (a1), M. HUSSEY (a2), S. W. GRIFFITHS (a1) and R. E. GOZLAN (a3)
Summary
SUMMARY

Sphaerothecum destruens is an obligate intracellular parasite with the potential to cause high mortalities and spawning inhibition in the endangered cyprinid Leucaspius delineatus. We investigated the influence of L. delineatus’s reproductive state on the prevalence and infection level of S. destruens. A novel real time quantitative polymerarse chain reaction (qPCR) was developed to determine S. destruens’ prevalence and infection level. These parameters were quantified and compared in reproductive and non-reproductive L. delineatus. The detection limit of the S. destruens specific qPCR was determined to be 1 pg of purified S. destruens genomic DNA. Following cohabitation in the lab, reproductive L. delineatus had a significantly higher S. destruens prevalence (P<0·05) and infection levels (P<0·01) compared to non-reproductive L. delineatus. S. destruens prevalence was 19% (n=40) in non-reproductive L. delineatus and 41% (n=32) in reproductive L. delineatus. However, there was no difference in S. destruens prevalence in reproductive and non-reproductive fish under field conditions. Mean infection levels were 18 and 99 pg S. destruens DNA per 250 ng L. delineatus DNA for non-reproductive and reproductive L. delineatus respectively. The present work indicates that S. destruens infection in L. delineatus can be influenced by the latter's reproductive state and provides further support for the potential adverse impact of S. destruens on the conservation of L. delineatus populations.

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Corresponding author
*Corresponding author: School of Conservation Sciences, Bournemouth University, Poole BH12 5BB, UK. Tel: +44 1202 965 268. Fax: +44 1202 965 046. E-mail: dandreou@bournemouth.ac.uk
References
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Andreou D., Gozlan R. E. and Paley R. (2009). Temperature influence on production and longevity of Sphaerothecum destruens’ zoospores. Journal of Parasitology 95, 15391541.
Arkush K. D., Frasca S. and Hedrick R. P. (1998). Pathology associated with the rosette agent, a systemic protist infecting salmonid fishes. Journal of Aquatic Animal Health 10, 111.
Arkush K. D., Mendoza L., Adkison M. A. and Hedrick R. P. (2003). Observations on the life stages of Sphaerothecum destruens N. G., N. Sp., a mesomycetozoean fish pathogen formally referred to as the rosette agent. Journal of Eukaryotic Microbiology 50, 430438.
Arnold K. E., Adam A., Orr K. J., Griffiths R. and Barber I. (2003). Sex-specific survival and parasitism in three-spined sticklebacks: seasonal patterns revealed by molecular analysis. Journal of Fish Biology 63, 10461050.
Bettge K., Wahli T., Segner H. and Schmidt-Posthaus H. (2009). Proliferative kidney disease in rainbow trout: time- and temperature-related renal pathology and parasite distribution. Diseases of Aquatic Organisms 83, 6776.
Bowden T. J. (2008). Modulation of the immune system of fish by their environment. Fish & Shellfish Immunology 25, 373383.
Browne R. K., Li H. and Vaughan M. (2006). Sexually mediated shedding of Myxobolus fallax spores during spermiation of Litoria fallax (Anura). Diseases of Aquatic Organisms 72, 7175.
Buchmann K. (1997). Population increase of Gyrodactylus derjavini on rainbow trout induced by testosterone treatment of the host. Diseases of Aquatic Organisms 30, 145150.
Connors V. A. and Nickol B. B. (1991). Effects of Plagiorhynchus cylindraceus (Acanthocephala) on the energy-metabolism of adult starlings, Sturnus vulgaris. Parasitology 103, 395402.
Fange R. and Nilsson S. (1985). The fish spleen – structure and function. Experientia 41, 152158.
Fels D. and Kaltz O. (2006). Temperature-dependent transmission and latency of Holospora undulata, a micronucleus-specific parasite of the ciliate Paramecium caudatum. Proceedings of the Royal Society of London, B 273, 10311038.
Funk V. A., Raap M., Sojonky K., Jones S., Robinson J., Falkenberg C. and Miller K. M. (2007). Development and validation of an RNA- and DNA-based quantitative PCR assay for determination of Kudoa thyrsites infection levels in Atlantic salmon Salmo salar. Diseases of Aquatic Organisms 75, 239249.
Gozlan R. E., St-Hilaire S., Feist S. W., Martin P. and Kent M. L. (2005). Biodiversity – Disease threat to European fish. Nature, London 435, 1046.
Gozlan R. E., St-Hilaire S., Feist S. W., Longshaw M. and Peeler E. J. (2006). The effect of microbial pathogens on the diversity of aquatic populations, notably in Europe. Microbes & infections 8, 13581364.
Gozlan R. E., Whipps C., Andreou D. and Arkush K. (2009). Characterisation and geographical isolation of Sphaerothecum destruens in Europe. International Journal for Parasitology 39, 10551058.
Hallett S. L. and Bartholomew J. L. (2006). Application of a real-time PCR assay to detect and quantify the Myxozoan parasite Ceratomyxa shasta in river water samples. Diseases of Aquatic Organisms 71, 109118.
Hamilton W. D. and Zuk M. (1982). Heritable true fitness and bright birds – a role for parasites. Science 218, 384387.
Jones S. R. M., Prosperi-Porta G., Dawe S. C. and Barnes D. P. (2003). Distribution, prevalence and severity of Parvicapsula minibicornis infections among anadromous salmonids in the Fraser River, British Columbia, Canada. Diseases of Aquatic Organisms 54, 4954.
Kerans B. L., Stevens R. I. and Lemmon J. C. (2005). Water temperature affects a host-parasite interaction: Tubifex tubifex and Myxobolus cerebralis. Journal of Aquatic Animal Health 17, 216221.
Kortet R., Taskinen J., Sinisalo T. and Jokinen I. (2003). Breeding-related seasonal changes in immunocompetence, health state and condition of the cyprinid fish, Rutilus rutilus, L. Biological Journal of the Linnean Society 78, 117127.
Kozubikova E., Petrusek A., Duris Z., Martin M. P., Dieguez-Uribeondo J. and Oidtmann B. (2008). The old menace is back: recent crayfish plague outbreaks in the Czech Republic. Aquaculture 274, 208217.
Kurtz J., Kalbe M., Langefors Ả., Mayer I., Milinski M. and Hasselquist D. (2007). An experimental test of the immunocompetence handicap hypothesis in a teleost fish: 11-ketotestosterone suppresses innate immunity in three-spined sticklebacks. The American Naturalist 170, 509519.
Lamkova K., Simkova A., Palikova M., Jurajda P. and Lojek A. (2007). Seasonal changes of immunocompetence and parasitism in Chub (Leuciscus cephalus), a freshwater cyprinid fish. Parasitology Research 101, 775789.
Lochmiller R. L., Vestey M. R. and Boren J. C. (1993). Relationship between protein nutritional-status and immunocompetence in northern bobwhite chicks. Auk 110, 503510.
Mendonca H. L. and Arkush K. D. (2004). Development of PCR-based methods for detection of Sphaerothecum destruens in fish tissues. Diseases of Aquatic Organisms 61, 187197.
Nelson R. J. and Demas G. E. (1996). Seasonal changes in immune function. Quarterly Review of Biology 71, 511548.
Nordling D., Andersson M., Zohari S. and Gustafsson L. (1998). Reproductive effort reduces specific immune response and parasite resistance. Proceedings of the Royal Society of London, B 265, 12911298.
Ostlund-Nilsson S., Curtis L., Nilsson G. E. and Grutter A. S. (2005). Parasitic isopod Anilocra apogonae, a drag for the cardinal fish Cheilodipterus quinquelineatus. Marine Ecology-Progress Series 287, 209216.
Phelps N. B. D. and Goodwin A. E. (2007). Validation of a quantitative PCR diagnostic method for detection of the Microsporidian Ovipleistophora ovariae in the cyprinid fish Notemigonus crysoleucas. Diseases of Aquatic Organisms 76, 215221.
Pinder A. C. and Gozlan R. E. (2004). Early ontogeny of sunbleak. Journal of Fish Biology 64, 762775.
Quinn T. P. (2004). The Behavior and Ecology of Pacific Salmon and Trout. University of Washington Press, Washington, WA, USA.
Reimchen T. E. and Nosil P. (2001). Ecological causes of sex-biased parasitism in threespine stickleback. Biological Journal of the Linnean Society 73, 5163.
Sanz J. J., Arriero E., Moreno J. and Merino S. (2001). Interactions between hemoparasite status and female age in the primary reproductive output of pied flycatchers. Oecologia 126, 339344.
Sheldon B. C. and Verhulst S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution 11, 317321.
Simkova A., Jarkovsky J., Koubkova B., Barus V. and Prokes M. (2005). Associations between fish reproductive cycle and the dynamics of Metazoan parasite infection. Parasitology Research 95, 6572.
Simkova A., Lafond T., Ondrackova M., Jurajda P., Ottova E. and Morand S. (2008). Parasitism, life history traits and immune defence in cyprinid fish from central Europe. BMC Evolutionary Biology 8.
Skarstein F. and Folstad I. (1996). Sexual dichromatism and the immunocompetence handicap: an observational approach using Arctic charr. Oikos 76, 359367.
Skarstein F., Folstad I. and Liljedal S. (2001). Whether to reproduce or not: immune suppression and costs of parasites during reproduction in the Arctic charr. Canadian Journal of Zoology-Revue Canadienne De Zoologie 79, 271278.
Slater C. H. and Schreck C. B. (1993). Testosterone alters the immune response of Chinook salmon Oncorhynchus tshawytscha. General and Comparative Endocrinology 89, 291298.
Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F. and Higgins D. G. (1997). The Clustal_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.
True K., Purcell M. K. and Foott J. S. (2009). Development and validation of a quantitative PCR to detect Parvicapsula minibicornis and comparison to histologically ranked infection of juvenile Chinook salmon, Oncorhynchus tshawytscha (Walbaum), from the Klamath River, USA. Journal of Fish Diseases 32, 183192.
Vainikka A., Jokinen E. I., Kortet R. and Taskinen J. (2004). Gender- and season-dependent relationships between testosterone, oestradiol and immune functions in wild roach. Journal of Fish Biology 64, 227240.
Wang N., Xu X. L. and Kestemont P. (2009). Effect of temperature and feeding frequency on growth performances, feed efficiency and body composition of pikeperch juveniles (Sander lucioperca). Aquaculture 289, 7073.
WCMC (1996). Leucaspius delineatus. In IUCN 2007. 2007 IUCN Red List of Threatened Species. www.iucnredlist.org.
Wolinska J. and King K. C. (2009). Environment can alter selection in host-parasite interactions. Trends in Parasitology 25, 236244.
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