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Epidemiology of parasitic protozoan infections in Soay sheep (Ovis aries L.) on St Kilda

Published online by Cambridge University Press:  18 September 2006

B. H. CRAIG ,
J. G. PILKINGTON ,
L. E. B. KRUUK  and
J. M. PEMBERTON
B. H. CRAIG
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, Scotland
J. G. PILKINGTON
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, Scotland
L. E. B. KRUUK
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, Scotland
J. M. PEMBERTON
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, Scotland
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Abstract

The feral Soay sheep (Ovis aries L.) population on Hirta, St Kilda, is host to a diverse component parasite community, but previous parasitological studies of the population have only focussed on the metazoan species. This paper reports the first epidemiological study of the protozoan species comprising Cryptosporidium parvum, Giardia duodenalis and 11 species of Eimeria in Soay sheep across 3 years of varying host population density. Prevalence and intensity of almost all species of protozoa significantly decreased with host age, with the exception of E. granulosa, which increased in prevalence with host age. The prevalence of C. parvum appeared to vary positively with host population density but that of G. duodenalis did not vary significantly with density. Most species of Eimeria showed a distinct lag in infection level following the host population crash of 2002, taking up to 2 years to decrease. Mixed Eimeria species intensity and diversity were highest in 2002, a year of low host density. Parasite diversity decreased with host age and was higher in males. There were 5 positive pair-wise associations between protozoa species in terms of prevalence. The results of this study highlight the potential for protozoal infection to shape the evolution of parasite resistance in wild host populations harbouring diverse parasite species.

Keywords

Soay sheepSt KildaCryptosporidium parvumGiardia duodenalisEimeria spp
Type
Research Article
Information
Parasitology , Volume 134 , Issue 1 , January 2007 , pp. 9 - 21
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Abo-Shehada, M. N. and Muwalla, M. M. ( 1989). The effect of three planes of nutrition on natural coccidial infections in Awassi sheep yearlings. Veterinary Parasitology 32, 279–283.CrossRefGoogle Scholar
Allam, A. F., Abou-Shousha, S. A. and Abou-Shamaa, L. A. ( 2002). Antibody profile, interferon-gamma and nutritional status in Cryptosporidial infection among school children. Journal of the Egyptian Society of Parasitology 32, 755–766.Google Scholar
Anderson, R. M. ( 1998). Epidemiology. In Modern Parasitology ( ed. Cox, F. E. G.), pp. 75–116. Blackwell Science Ltd, UK.
Anwar, M. A., Newman, C., MacDonald, D. W., Woolhouse, M. E. J. and Kelly, D. W. ( 2000). Coccidiosis in the European badger (Meles meles) from England, an epidemiological study. Parasitology 120, 255–260.CrossRefGoogle Scholar
Arslan, M. O., Umur, S. and Kara, M. ( 1999). The prevalence of coccidian species in sheep in Kars province of Turkey. Tropical Animal Health and Production 31, 161–165.CrossRefGoogle Scholar
Atwill, E. R., Sweitzer, R. A., Pereira, M. D. C., Gardner, I. A., Van Vuren, D. and Boyce, W. M. ( 1997). Prevalence of and associated risk factors for shedding Cryptosporidium parvum oocysts and Giardia cysts within feral pig populations in California. Applied and Environmental Microbiology 63, 3946–3949.Google Scholar
Bajer, A., Bednarska, M., Pawelczyk, A., Behnke, J. M., Gilbert, F. S. and Sinski, E. ( 2002). Prevalence and abundance of Cryptosporidium parvum and Giardia spp. in wild rural rodents from the Mazury lake district region of Poland. Parasitology 125, 21–34.Google Scholar
Behnke, J. M., Gilbert, F. S., Abu-Madi, M. A. and Lewis, J. W. ( 2005). Do helminth parasites of wood mice interact? Journal of Animal Ecology 74, 982–993.Google Scholar
Berriatua, E., Green, L. E. and Morgan, K. L. ( 1994). A descriptive epidemiological study of coccidiosis in early lambing housed flocks. Veterinary Parasitology 54, 337–351.CrossRefGoogle Scholar
Brackett, S. and Bliznick, A. ( 1952). The reproductive potential of five species of coccidia of the chicken as demonstrated by oocyst production. Journal of Parasitology 38, 133–139.CrossRefGoogle Scholar
Buchanan, M. ( 1995). Introduction. In St. Kilda: The Continuing Story of the Islands ( ed. Buchanan, M.), pp. xi–xxiv. HMSO, Edinburgh.
Catchpole, J., Norton, C. C. and Joyner, L. P. ( 1976). Experiments with defined multispecific coccidial infections in lambs. Parasitology 72, 137–147.CrossRefGoogle Scholar
Chapman, H. D. ( 1974 a). The effects of natural and artificially acquired infections of coccidia in lambs. Research in Veterinary Science 16, 1–6.Google Scholar
Chapman, H. D. ( 1974 b). The immunity of lambs to coccidia acquired in the field and by artificial infection. Research in Veterinary Science 16, 7–11.Google Scholar
Chappell, C. L., Okhuysen, P. C., Sterling, C. R., Wang, C., Jakubowski, W. and Dupont, H. L. ( 1999). Infectivity of Cryptosporidium parvum in healthy adults with pre-existing anti-C. parvum serum immunoglobulin G. American Journal of Tropical Medicine and Hygiene 60, 157–164.CrossRefGoogle Scholar
Christensen, N. O., Nansen, P. and Fagbemi, B. O. ( 1987). Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitology Research 73, 387–410.CrossRefGoogle Scholar
Clutton-Brock, T. H. ( 2004). The causes and consequences of instability. In Soay Sheep: Dynamics and Selection in an Island Population ( ed. Clutton-Brock, T. H. and Pemberton, J. M.), pp. 276–310. Cambridge University Press, Cambridge.
Clutton-Brock, T. H. and Pemberton, J. M. ( 2004). Soay Sheep: Dynamics and Selection in an Island Population. Cambridge University Press, Cambridge.
Coltman, D. W., Pilkington, J. G., Smith, J. A. and Pemberton, J. M. ( 1999). Parasite-mediated selection against inbred Soay sheep in a free-living Island population. Evolution 53, 1259–1267.CrossRefGoogle Scholar
Coltman, D. W., Wilson, K., Pilkington, J. G., Stear, M. J. and Pemberton, J. M. ( 2001). A microsatellite polymorphism in the gamma interferon gene is associated with resistance to gastrointestinal nematodes in a naturally-parasitized population of Soay sheep. Parasitology 122, 571–582.CrossRefGoogle Scholar
Cox, F. E. G. ( 2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl.), S23–S38.CrossRefGoogle Scholar
Craig, B. H., Pilkington, J. G. and Pemberton, J. M. ( 2006). Gastrointestinal nematode species burdens and host mortality in a feral sheep population. Parasitology (in the Press).CrossRef
De Graaf, D. C., Vanopdenbosch, E., Ortega-Mora, L. M., Abbassi, H. and Peeters, J. E. ( 1999). A review of the importance of Cryptosporidiosis in farm animals. International Journal for Parasitology 29, 1269–1287.CrossRefGoogle Scholar
Duszynski, D. W. and Upton, S. J. ( 2001). Cyclospora, Eimeria, Isospora and Cryptosporidium spp. In Parasitic Diseases of Wild Mammals ( ed. Samuel, W. M., Pybus, M. J. and Kocan, A. A.), pp. 416–459. Iowa State University Press, USA.CrossRef
Duszynski, D. W. and Wilber, P. G. ( 1997). A guideline for the preparation of species descriptions in the Eimeriidae. Journal of Parasitology 83, 333–336.CrossRefGoogle Scholar
Faubert, G. ( 2000). Immune response to Giardia duodenalis. Clinical Microbiology Reviews 13, 35–54.CrossRefGoogle Scholar
Gendrel, D., Treluyer, J. M. and Richard-Lenoble, D. ( 2003). Parasitic diarrhoea in normal and malnourished children. Fundamental and Clinical Pharmacology 17, 189–197.CrossRefGoogle Scholar
Graham, A. L. ( 2002). When T-helper cells don't help: immunopathology during concomitant infection. The Quarterly Review of Biology 77, 409–434.CrossRefGoogle Scholar
Gregory, M. W. and Catchpole, J. ( 1989). Ovine coccidiosis: heavy infection in young lambs increases resistance without causing disease. Veterinary Record 124, 458–461.CrossRefGoogle Scholar
Gulland, F. M. D. ( 1992). The role of nematode parasites in Soay sheep (Ovies aries L.) mortality during a population crash. Parasitology 105, 493–503.Google Scholar
Haberkorn, A. ( 1996). Chemotherapy of human and animal coccidioses: state and perspectives. Parasitology Research 82, 193–199.CrossRefGoogle Scholar
Huetink, R. E. C., Van der Giessen, J. W. B., Noordhuizen, J. P. T. M. and Ploeger, H. W. ( 2001). Epidemiology of Cryptosporidium spp. and Giardia duodenalis on a dairy farm. Veterinary Parasitology 102, 53–67.Google Scholar
Illius, A. W., Albon, S. D., Pemberton, J. M., Gordon, I. J. and Clutton-Brock, T. H. ( 1995). Selection for foraging efficiency during a population crash in Soay sheep. Journal of Animal Ecology 64, 481–492.CrossRefGoogle Scholar
Jewell, P. ( 1995). Soay sheep. In St. Kilda: The Continuing Story of the Islands ( ed. Buchanan, M.), pp. 73–93. HMSO, Edinburgh.
Jorg Reeg, K., Gauly, M., Bauer, C., Mertens, C., Erhardt, G. and Zahner, H. ( 2005). Coccidial infections in housed lambs: oocyst excretion, antibody levels and genetic influences on the infection. Veterinary Parasitology 127, 209–219.CrossRefGoogle Scholar
Kirkpatrick, B. D., Daniels, M. M., Jean, S. S., Pape, J. W., Karp, C., Littenberg, B., Fitzgerald, D. W., Lederman, H. M., Nataro, J. P. and Sears, C. L. ( 2002). Cryptosporidiosis stimulates an inflammatory intestinal response in malnourished Haitian children. The Journal of Infectious Diseases 186, 94–101.CrossRefGoogle Scholar
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. ( 2004). Competition and mutualism among the gut helminths of a mammalian host. Nature, London 428, 840–844.CrossRefGoogle Scholar
Levine, N. D. ( 1973). Protozoan Parasites of Domestic Animals and of Man. Burgess Publishing Company, USA.
Lorenzo, M. J., Casal, J. A., Freire, F., Castro, J. A., Vergara, C. A. and Ares-Mazas, M. E. ( 1998). Determination of immuno-cross-reactivity between Cryptosporidium parvum and Eimeria spp. Veterinary Parasitology 76, 1–8.CrossRefGoogle Scholar
M.A.F.F. ( 1971). Manual of Veterinary Parasitological Laboratory Techniques. HMSO, London.
M.A.F.F. ( 1986). Manual of Veterinary Parasitological Laboratory Techniques. HMSO, London.
Macfarlane, D. E. and Horner-Bryce, J. ( 1987). Cryptosporidiosis in well-nourished and malnourished children. Acta Paediatrica Scandinavica 76, 474–477.CrossRefGoogle Scholar
Magurran, A. E. ( 2004). Introduction: measurement of (biological) diversity. In Measuring Biological Diversity ( ed. Magurran, A. E.), pp. 1–17. Blackwell Publishing, UK.
Maingi, N. and Munyua, W. K. ( 1994). The prevalence and intensity of infection with Eimeria species in sheep in Nyandarua district of Kenya. Veterinary Research Communications 18, 19–25.CrossRefGoogle Scholar
Majewska, A. C., Werner, A., Sulima, P. and Luty, T. ( 2000). Prevalence of Cryptosporidium in sheep and goats bred on five farms in west-central region of Poland. Veterinary Parasitology 89, 269–275.CrossRefGoogle Scholar
Newman, C., MacDonald, D. W. and Anwar, M. A. ( 2001). Coccidiosis in the European badger, Meles meles in Wytham woods: infection and consequences for growth and survival. Parasitology 123, 133–142.CrossRefGoogle Scholar
O'Callaghan, M. G., O'Donoghue, P. J. and Moore, E. ( 1987). Coccidia in sheep in south Australia. Veterinary Parasitology 24, 175–183.CrossRefGoogle Scholar
Okhuysen, P. C., Chappell, C. L., Sterling, C. R., Jakubowski, W. and Dupont, H. L. ( 1998). Susceptibility and serologic response of healthy adults to reinfection with Cryptosporidium parvum. Infection and Immunity 66, 441–443.Google Scholar
Olson, M. E. and Buret, A. G. ( 2001). Giardia and Giardiasis. In Parasitic Diseases of Wild Mammals ( ed. Samuel, W. M., Pybus, M. J. and Kocan, A. A.), pp. 399–416. Iowa State University Press, USA.CrossRef
Olson, M. E., Thorlakson, C. L., Deselliers, L., Mork, D. W. and McAllister, T. A. ( 1997). Giardia and Cryptosporidium in Canadian farm animals. Veterinary Parasitology 68, 375–381.CrossRefGoogle Scholar
Ortega-Mora, L. M. and Wright, S. E. ( 1994). Age-related resistance in ovine cryptosporidiosis: patterns of infection and humoral immune response. Infection and Immunity 62, 5003–5009.Google Scholar
Paterson, S., Wilson, K. and Pemberton, J. M. ( 1998). Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proceedings of the National Academy of Sciences, USA 95, 3714–3719.CrossRefGoogle Scholar
Poulin, R. ( 2001). Interactions between species and the structure of helminth communities. Parasitology 122 (Suppl.), S3–S11.CrossRefGoogle Scholar
Pout, D. D. and Catchpole, J. ( 1974). Coccidiosis of lambs. V. The clinical response to long term infection with a mixture of different species of coccidia. British Veterinary Journal 130, 388–399.Google Scholar
Rice, W. R. ( 1989). Analyzing tables of statistical tests. Evolution 43, 223–225.CrossRefGoogle Scholar
Smith, J. A. ( 1999). Heritable variation in resistance to gastrointestinal nematodes in an unmanaged mammal population. Proceedings of the Royal Society of London, B 266, 1283–1290.CrossRefGoogle Scholar
Soulsby, E. J. L. ( 1986). Helminths, Arthropods and Protozoa of Domesticated Animals. Balliere Tindall, London, UK.
Taylor, M. ( 2000). Protozoal disease in cattle and sheep. In Practice 22, 604–617.CrossRefGoogle Scholar
Torres, J., Gracenea, M., Gomez, M. S., Arrizabalaga, A. and Gonzalez-Moreno, O. ( 2000). The occurance of Cryptosporidium parvum and C. muris in wild rodents and insectivores in Spain. Veterinary Parasitology 92, 253–260.Google Scholar
Wade, S. E., Mohammed, H. O. and Schaaf, S. L. ( 2000). Epidemiologic study of Giardia sp. infection in dairy cattle in southeastern New York state. Veterinary Parasitology 89, 11–21.Google Scholar
Williams, R. B. ( 1973). Effects of different infection rates on the oocyst production of Eimeria acervulina or Eimeria tenella in the chicken. Parasitology 67, 279–288.CrossRefGoogle Scholar
Wilson, K., Grenfell, B. T., Pilkington, J. G., Boyd, H. E. G. and Gulland, F. M. D. ( 2004). Parasites and their impact. In Soay Sheep: Dynamics and Selection in an Island Population ( ed. Clutton-Brock, T. H. and Pemberton, J. M.), pp. 113–165. Cambridge University Press, Cambridge.
Xiao, L. ( 1994). Giardia infection in farm animals. Parasitology Today 10, 436–438.CrossRefGoogle Scholar
Yun, C. H., Lillehoj, H. S. and Lillehoj, E. P. ( 2000). Intestinal immune response to coccidiosis. Developmental and Comparative Immunology 24, 303–324.CrossRefGoogle Scholar