Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-26T09:15:23.663Z Has data issue: false hasContentIssue false
  • English
  • Français

Metazoan-protozoan parasite co-infections and host body weight in St Kilda Soay sheep

Published online by Cambridge University Press:  24 January 2008

B. H. CRAIG ,
L. J. TEMPEST ,
J. G. PILKINGTON  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
L. J. TEMPEST
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
J. M. PEMBERTON
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, Scotland
*
*Corresponding author: Wildlife, Ecology and Management Group H, Veterinary Surveillance, Central Science Laboratory, Sand Hutton, York YO41 1LZ, UK. Tel: +44 (0) 1904 462583. Fax: +44 (0) 1904 462111. E-mail: b.craig@csl.gov.uk
Get access Rights & Permissions [Opens in a new window]

Summary

For hundreds of years, the unmanaged Soay sheep population on St Kilda has survived despite enduring presumably deleterious co-infections of helminth, protozoan and arthropod parasites and intermittent periods of starvation. Important parasite taxa in young Soay sheep are strongyles (Trichostrongylus axei, Trichostrongylus vitrinus and Teladorsagia circumcincta), coccidia (11 Eimeria species) and keds (Melophagus ovinus) and in older animals, Teladorsagia circumcincta. In this research, associations between the intensity of different parasite taxa were investigated. Secondly, the intensities of different parasite taxa were tested for associations with variation in host weight, which is itself a determinant of over-winter survival in the host population. In lambs, the intensity of strongyle eggs was positively correlated with that of Nematodirus spp. eggs, while in yearlings and adults strongyle eggs and coccidia oocysts were positively correlated. In lambs and yearlings, of the parasite taxa tested, only strongyle eggs were significantly and negatively associated with host weight. However, in adult hosts, strongyles and coccidia were independently and negatively associated with host weight. These results are consistent with the idea that strongyles and coccidia are exerting independent selection on Soay sheep.

Keywords

Soay sheepSt Kildaco-infectionbody weightTrichostrongylus spp.Teladorsagia spp.Eimeria spp.Melophagus ovinus
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 4 , April 2008 , pp. 433 - 441
Copyright
Copyright © Cambridge University Press 2008

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

Behnke, J. M., Gilbert, F. S., Abu-Madi, M. A. and Lewis, J. W. (2005). Do the helminth parasites of wood mice interact? Journal of Animal Ecology 74, 982–993.Google Scholar
Beraldi, D., McRae, A. F., Gratten, J., Pilkington, J. G., Slate, J., Visscher, P. M. and Pemberton, J. M. (2007). Quantitative trait loci (QTL) mapping of resistance to strongyles and coccidia in the free-living Soay sheep (Ovis aries). International Journal for Parasitology 37, 121–129.CrossRefGoogle ScholarPubMed
Bishop, S. C., Bairden, K., McKeller, Q. A., Park, M. and Stear, M. J. (1996). Genetic parameters for faecal egg count following mixed, natural, predominantly Ostertagia circumcincta infection and relationships with live weight in young lambs. Animal Science 63, 423–428.Google Scholar
Bishop, S. C. and Stear, M. J. (2000). The use of a gamma-type function to assess the relationship between the number of adult Teladorsagia circumcincta and total egg output. Parasitology 121, 435–440.Google 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.Google Scholar
Chapman, H. D. (1974). The effects of natural and artificially acquired infections of coccidia in lambs. Research in Veterinary Science 16, 1–6.Google 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 ScholarPubMed
Clutton-Brock, T. H. and Pemberton, J. M. (2004). Soay Sheep: Dynamics and Selection in an Island Population (ed. Clutton-Brock, T. H. and Pemberton, J. M.) Cambridge University Press, Cambridge.Google Scholar
Clutton-Brock, T. H., Price, O. F., Albon, S. D. and Jewell, P. A. (1992). Early development and population fluctuations in Soay sheep. Journal of Animal Ecology 61, 381–396.CrossRefGoogle Scholar
Clutton-Brock, T. H., Wilson, K. and Stevenson, I. R. (1997). Density-dependent selection on horn phenotype in Soay sheep. Philosophical Transactions of the Royal Society, B 352, 839–850.Google Scholar
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.Google Scholar
Coltman, D. W., Pilkington, J., Kruuk, L. E. B., Wilson, K. and Pemberton, J. M. (2001 a). Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution 55, 2116–2125.Google Scholar
Coltman, D. W., Wilson, K., Pilkington, J. G., Stear, M. J. and Pemberton, J. M. (2001 b). 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.Google Scholar
Cox, F. E. G. (2001). Concomitant infections, parasites and immune responses. Parasitology 122 (Suppl.) S23–S38.CrossRefGoogle ScholarPubMed
Craig, B. H., Pilkington, J. G. and Pemberton, J. M. (2006). Gastrointestinal nematode species burdens and host mortality in a feral sheep population. Parasitology 133, 485–496.CrossRefGoogle Scholar
Craig, B. H., Pilkington, J. G., Kruuk, L. E. B. and Pemberton, J. M. (2007). Epidemiology of parasitic protozoan infections in Soay sheep (Ovis aries L.) on St Kilda. Parasitology 134, 9–21.Google Scholar
Crawley, M. J. (2003). Model criticism. In Statistical Computing: An Introduction to Data Analysis Using S-Plus. pp. 305–322. John Wiley & Sons Ltd, Chichester, UK.Google Scholar
Forchhammer, M. C., Clutton-Brock, T. H., Lindstrom, J. and Albon, S. D. (2001). Climate and population density induce long-term cohort variation in northern ungulate. Journal of Animal Ecology 70, 721–729.Google Scholar
Gauly, M., Reeg, J., Bauer, C. and Erhardt, G. (2004). Influence of production systems in lambs on the Eimeria oocyst output and weight gain. Small Ruminant Research 55, 159–167.Google Scholar
Gordon, H. M. (1950). Some aspects of parasitic gastro-enteritis of sheep. Australian Veterinary Journal 26, 14–28.Google Scholar
Graham, A. L. (2001). Use of an optimality model to solve the immunological puzzle of concomitant infection. Parasitology 122 (Suppl.) S61–S64.Google 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 ScholarPubMed
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
Haukisalmi, V. and Henttonen, H. (1993). Coexistance in helminths of the bank vole Clethrionomys glareolus. 1. Patterns of co-occurance. Journal of Animal Ecology 62, 221–229.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.Google Scholar
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.Google 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.Google Scholar
Lotz, J. M. and Font, W. F. (1991). The role of positive and negative interspecific associations in the organization of communities of intestinal helminths of bats. Parasitology 103, 127–138.Google Scholar
Lydyard, P. M., Whelan, A. and Fanger, M. W. (2001). Cytokine families. In Immunology (ed. Hames, B. D.), pp. 87–91. Bios Scientific Publishers, Oxford, UK.Google Scholar
M.A.F.F. (1971). Manual of Veterinary Parasitological Laboratory Techniques. HMSO, London.Google Scholar
Montgomery, S. S. J. and Montgomery, W. I. (1990). Structure, stability and species interactions in helminth communities of wood mice Apodemus sylvaticus. International Journal for Parasitology 20, 225–242.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.Google Scholar
Platzer, B., Prosl, H., Cieslicki, M. and Joachim, A. (2005). Epidemiology of Eimeria infections in an Austrian milking sheep flock and control with diclazuril. Veterinary Parasitology 129, 1–9.Google 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. The British Veterinary Journal 130, 388–399.Google Scholar
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43, 223–225.Google Scholar
Smith, J. A., Wilson, K., Pilkington, J. G. and Pemberton, J. M. (1999). Heritable variation in resistance to gastro-intestinal nematodes in an unmanaged mammal population. Proceedings of the Royal Society of London, B 266, 1283–1290.CrossRefGoogle Scholar
Steel, J. W., Jones, W. O. and Symons, L. E. A. (1982). Effects of a concurrent infection of Trichostrongylus colubriformis on the productivity and physiological and metabolic responses of lambs infected with Ostertagia circumcincta. Australian Journal of Agricultural Research 33, 131–140.CrossRefGoogle Scholar
Sykes, A. R., Poppi, D. P. and Elliot, D. C. (1988). Effect of concurrent infection with Ostertagia circumcincta and Trichostrongylus colubriformis on the performance of growing lambs consuming fresh herbage. Journal of Agricultural Science 110, 531–541.Google Scholar
Van Noordwijk, A. J. and de Jong, G. (1986). Acquisition and allocation of resources: their influence on variation in life history tactics. The American Naturalist 128, 137–142.Google Scholar
Wakelin, D. and Blackwell, J. (1988). Genetics of Resistance to Bacterial and Parasitic Infection. Taylor and Francis, London.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 ScholarPubMed
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.Google Scholar
Wimmer, B., Craig, B. H., Pilkington, J. G. and Pemberton, J. M. (2004). Non-invasive assessment of parasitic nematode species diversity in wild Soay sheep using molecular markers. International Journal for Parasitology 34, 625–631.CrossRefGoogle ScholarPubMed