Skip to main content
×
×
Home

The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash

  • F. M. D. Gulland (a1)
Summary

In early 1989, two-thirds of the Soay sheep population on St Kilda died over 12 weeks. Post-mortem examinations revealed emaciated carcasses and considerable nematode burdens, with protein-energy malnutrition as the probable cause of death. Haematological and blood biochemical changes in the sheep, as well as fecundity of gastrointestinal nematodes, suggested the hosts were immunosuppressed. In parallel, laboratory experiments in which Soay sheep on a high plane of nutrition were artificially infected with Ostertagia circumcincta, showed no clinical signs or mortality when supporting worm burdens similar to those recorded in dead sheep on St Kilda. Anthelmintic treatment of a group of animals increased daily survival rates in ewes and male lambs, although treated animals became re-infected as the ‘crash’ progressed. It is suggested that parasites contribute to mortality in malnourished hosts, exacerbating the effects of food shortage.

Copyright
References
Hide All
Anderson, R. M. (1980). Depression of host population abundance by direct life cycle macroparasites. Journal of Theoretical Biology 82, 283311.
Anderson, R. M. & Crombie, J. A. (1984). Experimental studies of age-prevalence curves for Schistosoma mansoni infections in populations of Biomphalaria glabrata. Parasitology 89, 79105.
Anderson, R. M. & May, R. M. (1978). Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–48.
Anderson, R. M. & May, R. M. (1985). Helminth infections of humans: Mathematical models, population dynamics and control. Advances in Parasitology 24, 1101.
Anderson, R. M. & Schad, G. A. (1985). Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 812–15.
Barger, I. A. (1985). The statistical distribution of trichostrongylid nematodes in grazing lambs. International Journal for Parasitology 15, 645–9.
Behnke, J. M. & Barnard, C. J. (1990). Coevolution of parasites and hosts: host–parasite arms races and their consequences. In Parasites: Immunity and Pathology, (ed. Behnke, J. M.), pp. 123, London: Taylor & Francis.
Benjamin, M. M. (1978). Outline of Veterinary Clinical Pathology. 3rd Edn.Ames: USA, Iowa State University Press.
Bhat, T. K., Sharma, R. L. & Dhar, D. N. (1986). Serum lactate dehydrogenase: clinical significance of alterations in its activity in lambs infected with Dictyocaulus filaria. Research in Veterinary Science 42, 127–9.
Blood, D. C., Henderson, J. A. & Radostits, O. M. (1981). Veterinary Medicine. London: Baillere Tindall.
Blunt, M. H. (1975). The Blood of Sheep. Composition and Function. Berlin: Springer-Verlag.
Boonstra, R. (1977). Effect of the parasite Wohlfahrtia vigil on Microtus townsendii populations. Canadian Journal of Zoology 55, 1057–60.
Boonstra, R., Krebs, C. J. & Beacham, T. D. (1980). Impact of botfly parasitism on Microtus townsendii populations. Canadian Journal of Zoology 58, 1683–92.
Brown, M. D., Poppi, D. P. & Sykes, A. R. (1989). The effects of a concurrent infection of Trichostrongylus colubriformis and Ostertagia circumcincta on calcium, phosphorus and magnesium transactions along the digestive tract of lambs. Journal of Comparative Pathology and Therapeutics 101, 1120.
Bundy, D. A. P., Cooper, E. S., Thompson, D. E., Anderson, R. M. & Didier, J. M. (1987). Age-related prevalence and intensity of Trichuris trichiura infection in a St Lucian community. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 8594.
Callinan, A. P. L. & Arundel, J. H. (1982). Population dynamics of the parasitic stages of Ostertagia spp. in sheep. International Journal for Parasitology 12, 531–5.
Chandra, R. K. & Newberne, P. M. (1977). Nutrition, Immunity, and Infection. Mechanisms of Interactions. New York: Plenum Press.
Clutton-Brock, T. H., Price, O. F., Albon, S. D. & Jewell, P. A. (1991). Persistent instability and population regulation in Soay sheep. Journal of Animal Ecology 60, 593608.
Fowler, C. W. (1987). A review of density dependence in populations of large mammals. In Current Mammalogy, Vol. 1. (ed. Genoways, H. H.) pp. 401441. New York: Plenum Publishing Corporation.
Grenfell, B. T., Price, O. F., Albon, S. D. & Clutton-Brock, T. H. (1992). Overcompensation and population cycles in an ungulate. Nature, London 335, 823–6.
Grobler, J. H. (1981). Parasites and mortality of Sable Hippotragus Niger Niger (Harris, 1838) in the Matopos, Zimbabwe. Koedoe 24, 119–23.
Grubb, P. J. (1974). Population dynamics of Soay sheep. In Island Survivors, (ed. Jewell, P. A., Milner, C. & Boyd, J. M.) pp. 195223. London: Athlone Press.
Gulland, F. M. D. & Fox, M. (1992). Epidemiology of nematode infections of Soay sheep (Ovis aries L.) on St Kilda. Parasitology 105, 481–92.
Guyatt, H. L., Bundy, D. A. P., Medley, G. F. & Grenfell, B. T. (1990). The relationship between the frequency distribution of Ascaris lumbricoides and the prevalence and intensity of infection in human communities. Parasitology 101, 139–43.
Hall, J. G. (1971). The lymph-borne cells of the immune response: A review. In The Scientific Basis of Medicine Annual Reviews (ed. Gilliband, I. & Francis, J.) pp. 3957. London: Athlone Press.
Healy, M. J. R. (1988). Glim: An Introduction. Oxford: Clarendon Press.
Holmes, P. H. (1985). Pathogenesis of trichostrongylosis. Veterinary Parasitology 18, 89101.
Holmes, P. H. (1987). Pathophysiology of parasitic infections. Parasitology 94, S29–S51.
Hudson, P. J. (1986). The effect of a parasitic nematode on the breeding production of red grouse. Journal of Animal Ecology 55, 8592.
Ito, A., Kano, S., Hioki, A., Kasuyu, S. & Ohtomo, H. (1986). Reduced fecundity of Hymenolepis nana due to thymus dependent immunological responses in mice. International Journal for Parasitology 16, 81–5.
Jones, J. T., Breeze, P. & Kusel, J. R. (1989). Schistosome fecundity: influence of host genotype and intensity of infection. International Journal for Parasitology 19, 769–77.
Kaneko, J. J. & Carroll, E. J. (1967). The clinical significance of serum protein fractionation by electrophoresis. Californian Veterinarian 21, 22–8.
Keith, L. B., Cary, J. R., Yuill, T. M. & Keith, I. M. (1985). Prevalence of helminths in a cyclic snowshoe hare population. Journal of Wildlife Diseases 21, 233–53.
Kerr, M. G. (1987). Veterinary laboratory medicine: clinical biochemistry and haematology. Oxford: Blackwells Scientific Publications.
Keusch, G. T., Wilson, C. S. & Waksal, S. D. (1983). Nutrition, host defences and the lymphoid system. In Advances in Host Defence Mechanisms, Vol. 2. (ed. Gallin, J. I. & Fauci, A. S.) pp. 275359, New York: Plenum Press.
Keymer, A. E. (1981). Population dynamics of Hymenolepis diminuta in the intermediate host. Journal of Animal Ecology 50, 941–50.
Keymer, A. E. & Hiorns, R. W. (1987). Faecal egg counts and nematode fecundity: Heligmosomoides polygyrus and laboratory mice. Parasitology 93, 189203.
Keymer, A. E., Crompton, D. W. T. & Walters, D. E. (1983). Nippostrongylus (Nematoda) in protein-malnourished rats: host mortality, morbidity and rehabilitation. Parasitology 86, 461–75.
Lloyd, S. & Soulsby, E. J. L. (1988). Immunological response of the host. Gastrointestinal nematodes. In Parasitology in Focus. Facts and Trends, (ed. Melhorn, H.) pp. 627647, Berlin: Springer-Verlag.
May, R. M. & Anderson, R. M. (1978). Regulation and stability of host–parasite population interactions. II. Destabilizing processes. Journal of Animal Ecology 47, 249–67.
May, R. M. & Anderson, R. M. (1979). Population biology of infectious diseases: II. Nature, London 280, 455–61.
Mcfarlane, H. (1976). Malnutrition and impaired immune response to infection. Proceedings of the Nutritional Society 35, 263–83.
Michel, J. F. (1969). The regulation of egg output by Ostertagia ostertagi in calves infected once only. Parasitology 59, 767–75.
Moqbel, R. & Macdonald, A. J. (1990). Immunological and inflammatory responses in the small intestine associated with helminthic infections. In Parasites:Immunity and Pathology, (ed. Behnke, J. M.), pp. 249282. London: Taylor & Francis.
Morgan, D. O., Parnell, I. W. & Rayski, C. (1951). The seasonal variations in the worm burden of Scottish Hill Sheep. Journal of Helminthology 25, 177212.
Nelson, W. A. & Hironaka, R. (1966). Effect of protein and vitamin A intake of sheep on numbers of the sheep ked, Melophagus ovinus (L.). Parasitology 18, 274–80.
Nelson, W. A. & Qually, M. C. (1958). Annual cycles in numbers of the sheep ked, Melophagus ovinus (L.). Canadian Journal of Animal Science 38, 194–9.
Panaretto, B. A. (1964). Body composition in vivo 6. The composition of ewes during prolonged undernutrition. Australian Journal of Agricultural Research 15, 771–87.
Scott, M. E. (1987). Regulation of mouse colony abundance by Heligmosomoides polygyrus Parasitology 95, 111–24.
Scott, M. E. & Anderson, R. M. (1984). The population dynamics of Gyrodactylus bullatarudis (Monogea) on guppies (Poecilia reticulata). Parasitology 89, 159–94.
Scott, M. E. & Dobson, A. (1989). The role of parasites in regulating host abundance. Parasitology Today 5, 176–83.
Sinclair, A. R. E. (1974). The natural regulation of buffalo populations in East Africa. III. Population trends and mortality. East African Wildlife Journal 12, 185200.
Slater, A. F. G. (1988). The influence of dietary protein on the experimental epidemiology of Heligmosomoides polygyrus (Nematoda) in the laboratory mouse. Proceedings of the Royal Society, B 234, 239–54.
Slater, A. F. G. & Keymer, A. E. (1986). Heligmosomoides polygyrus (Nematoda): the influence of dietary protein on the dynamics of repeated infection. Proceedings of the Royal Society, B 229, 6983.
Soulsby, E. J. L. (1981). Helminths, Arthropods and Protozoa of Domesticated Animals. London: Baillere Tindall.
Southwood, T. R. E. (1966). Ecological Methods, with Particular Reference to Insect Populations. London: Methuen.
Soveri, T., Henttonen, H., Rudback, E., Sukura, A., Tanskanen, R., Schildt, R., & Husu, J. (1990). Diseases in a field vole population during a cyclic decline. VIth International Congress on Wildlife Diseases, p. 75.
Sykes, A. R., Poppi, D. P. & 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, 531–41.
Symons, L. E. A. (1985). Anorexia: occurrence, pathophysiology, and possible causes in parasitic infections. Advances in Parasitology 24, 103–33.
Symons, L. E. A. (1989). Pathophysiology of Endoparasitic Infection Compared With Ectoparasitic Infestation and Microbial Infection. London: Academic Press.
Thomas, R. J., Nunns, V. J.Boag, B. (1970). The incidence of lungworm infection in sheep in North-East England. Veterinary Record 87, 70–5.
Whitlock, J. H., Crofton, H. D. & Georgi, J. R. (1972). Characteristics of parasite populations in endemic trichostrongylidosis. Parasitology 64, 413–27.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed