Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-05T06:18:46.962Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  21 July 2010

D. ANDREOU*
Affiliation:
Cardiff School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff CF10 3AX, UK
M. HUSSEY
Affiliation:
Centre for Ecology and Hydrology, Mansfield Road, Oxford OX1 3SR, UK
S. W. GRIFFITHS
Affiliation:
Cardiff School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff CF10 3AX, UK
R. E. GOZLAN
Affiliation:
School of Conservation Sciences, Bournemouth University, Poole BH12 5BB, Dorset, UK
*
*Corresponding author: School of Conservation Sciences, Bournemouth University, Poole BH12 5BB, UK. Tel: +44 1202 965 268. Fax: +44 1202 965 046. E-mail: [email protected]

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.

Type
Research Article
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

Andreou, D., Gozlan, R. E. and Paley, R. (2009). Temperature influence on production and longevity of Sphaerothecum destruens’ zoospores. Journal of Parasitology 95, 15391541.CrossRefGoogle ScholarPubMed
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, 111.2.0.CO;2>CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Bowden, T. J. (2008). Modulation of the immune system of fish by their environment. Fish & Shellfish Immunology 25, 373383.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Buchmann, K. (1997). Population increase of Gyrodactylus derjavini on rainbow trout induced by testosterone treatment of the host. Diseases of Aquatic Organisms 30, 145150.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Fange, R. and Nilsson, S. (1985). The fish spleen – structure and function. Experientia 41, 152158.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds – a role for parasites. Science 218, 384387.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Nelson, R. J. and Demas, G. E. (1996). Seasonal changes in immune function. Quarterly Review of Biology 71, 511548.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Pinder, A. C. and Gozlan, R. E. (2004). Early ontogeny of sunbleak. Journal of Fish Biology 64, 762775.CrossRefGoogle Scholar
Quinn, T. P. (2004). The Behavior and Ecology of Pacific Salmon and Trout. University of Washington Press, Washington, WA, USA.Google Scholar
Reimchen, T. E. and Nosil, P. (2001). Ecological causes of sex-biased parasitism in threespine stickleback. Biological Journal of the Linnean Society 73, 5163.Google Scholar
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.CrossRefGoogle ScholarPubMed
Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution 11, 317321.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Skarstein, F. and Folstad, I. (1996). Sexual dichromatism and the immunocompetence handicap: an observational approach using Arctic charr. Oikos 76, 359367.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Slater, C. H. and Schreck, C. B. (1993). Testosterone alters the immune response of Chinook salmon Oncorhynchus tshawytscha. General and Comparative Endocrinology 89, 291298.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
WCMC (1996). Leucaspius delineatus. In IUCN 2007. 2007 IUCN Red List of Threatened Species. www.iucnredlist.org.Google Scholar
Wolinska, J. and King, K. C. (2009). Environment can alter selection in host-parasite interactions. Trends in Parasitology 25, 236244.CrossRefGoogle ScholarPubMed