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Gastrointestinal nematode species burdens and host mortality in a feral sheep population

Published online by Cambridge University Press:  04 July 2006

B. H. CRAIG ,
J. G. PILKINGTON  and
J. M. PEMBERTON
B. H. CRAIG
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Scotland
J. G. PILKINGTON
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Scotland
J. M. PEMBERTON
Affiliation:
Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Scotland
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Abstract

Every few years a large proportion of the feral sheep on Hirta, St Kilda die due to food shortage. The effects of malnutrition are exacerbated by gastrointestinal nematodes. As found in sheep flocks in mainland Britain, Teladorsagia circumcincta has long been considered the predominant and most pathogenic nematode species in all age classes of Soay sheep. Previous research indicated that intensity of this species showed a negative association with host age and comprised 75% of the entire gastrointestinal burden. Here we present new data that show Trichostrongylus axei and Trichostrongylus vitrinus to be the predominant worm pathogens in young Soay sheep. In the present study, Trichostrongylus spp. burdens declined with host age whereas T. circumcincta actually increased in burden over the first few age classes. Also, male hosts had significantly higher burdens of Trichostrongylus spp. than females, with this genus making up a higher proportion of the strongyle egg producing community in male hosts than female hosts. These new findings raise questions concerning our previous interpretation of the main nematode species contributing to strongyle egg count in the population, and the contrasting infection patterns of these nematode species in unmanaged St Kilda Soay sheep compared with domestic sheep in mainland Britain.

Keywords

Soay sheepSt KildaTeladorsagia circumcinctaTrichostrongylus axeiTrichostrongylus vitrinus
Type
Research Article
Information
Parasitology , Volume 133 , Issue 4 , October 2006 , pp. 485 - 496
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Balic, A., Bowles, V. M. and Meeusen, E. N. T. ( 2000). The immunobiology of gastrointestinal nematode infections in ruminants. Advances in Parasitology 45, 181–241.CrossRefGoogle Scholar
Bartley, D. J., Jackson, E., Johnston, K., Coop, R. L., Mitchell, G. B. B., Sales, J. and Jackson, F. ( 2003). A survey of anthelmintic resistant nematode parasites in Scottish sheep flocks. Veterinary Parasitology 117, 61–71.CrossRefGoogle Scholar
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.CrossRefGoogle 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.CrossRefGoogle Scholar
Boag, B. and Thomas, R. J. ( 1971). Epidemiological studies on gastrointestinal nematode parasites of sheep. Research in Veterinary Science 12, 132–139.Google Scholar
Boag, B. and Thomas, R. J. ( 1977). Epidemiological studies on gastrointestinal nematode parasites of sheep: the seasonal number of generations and succession of species. Research in Veterinary Science 22, 62–67.Google Scholar
Bowman, D. D. ( 1995). Parasitology for Veterinarians, W.B. Saunders, Philadelphia, USA.
Braisher, T. L. ( 1999). Genetic variation in trichostrongylid parasites of the Soay sheep of Hirta, St Kilda. Ph.D. thesis, University of Cambridge.
Buchanan, M. ( 1995). Introduction. In St Kilda: The Continuing Story of the Islands ( ed. Buchanan, M.), pp. 11–24. HMSO, Edinburgh.CrossRef
Cabaret, J., Mage, C. and Bouilhol, M. ( 2002). Helminth intensity and diversity in organic meat sheep farms in centre of France. Veterinary Parasitology 105, 33–47.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., Grenfell, B. T., Coulson, T., MacColl, A. D. C., Illius, A. W., Forchhammer, M. C., Wilson, K., Lindstrom, J., Crawley, M. J. and Albon, S. D. ( 2004). Population dynamics in Soay sheep. In Soay Sheep: Dynamics and Selection in an Island Population ( ed. Clutton-Brock, T. H. and Pemberton, J. M.), pp. 52–112. 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.
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 of London, B 352, 839–850.CrossRefGoogle 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.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
Dunsmore, J. D. ( 1963). Effect of the removal of an adult population of Ostertagia from sheep on concurrently existing arrested larvae. Australian Veterinary Journal 39, 459–463.CrossRefGoogle Scholar
Dybdahl, M. F. and Lively, C. M. ( 1998). Host-parasite co-evolution: evidence for rare advantage and time lagged selection in a natural population. Evolution 52, 1057–1066.CrossRefGoogle Scholar
Fowler, J. and Cohen, L. ( 1990). Practical Statistics for Field Biology. John Wiley and Sons Ltd., Chichester, UK.
Gibson, T. E. ( 1952). The development of acquired resistance by sheep to infestation with the nematode Trichostrongylus axei. Journal of Helminthology 26, 43–53.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
Gulland, F. M. D. ( 1991). The role of parasites in the population dynamics of Soay sheep on St. Kilda, Ph.D. thesis, University of Cambridge.
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
Gulland, F. M. D., Albon, S. D., Pemberton, J. M., Moorcroft, P. and Clutton-Brock, T. H. ( 1993). Parasite-associated polymorphism in a cyclic ungulate population. Proceedings of the Royal Society of London, B 254, 7–13.CrossRefGoogle 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.
Kennedy, M. S. and Todd, A. C. ( 1975). Age group interactions of Haemonchus contortus in premunized lambs. American Journal of Veterinary Research 36, 1195–1198.Google Scholar
Kloosterman, A., Permentier, H. K. and Ploeger, H. W. ( 1992). Breeding cattle and sheep for resistance to gastrointestinal nematodes. Parasitology Today 8, 330–335.CrossRefGoogle Scholar
Leignel, V., Cabaret, J. and Humbert, J. F. ( 2002). New molecular evidence that Teladorsagia circumcincta (nematoda: Trichostrongylidea) is a species complex. Journal of Parasitology 88, 135–140.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
M.A.F.F. ( 1986). Manual of Veterinary Parasitological Laboratory Techniques. HMSO, London.
Michel, J. F. ( 1969). The regulation of egg output by Ostertagia ostertagi in calves infected once only. Parasitology 59, 767–774.Google Scholar
Parnell, I. W., Rayski, C., Dunn, A. M. and Mackintosh, G. M. ( 1954). A survey of the helminths of Scottish hill sheep. Journal of Helminthology 28, 53–110.CrossRefGoogle Scholar
Polak, M. ( 2003). Heritability of resistance against ectoparasitism in the Drosophila-Macrocheles system. Journal of Evolutionary Biology 16, 74–82.CrossRefGoogle Scholar
Poulin, R. ( 2001). Interactions between species and the structure of helminth communities. Parasitology 122 (Suppl.) S3–S11.CrossRefGoogle Scholar
Read, A. F. and Taylor, L. H. ( 2001). The ecology of genetically diverse infections. Science 292, 1099–1102.CrossRefGoogle Scholar
Reid, J. F. S. and Armour, J. ( 1975 a). Studies in Scottish hill sheep: I. Changes in the susceptibility of the breeding ewe to Ostertagia spp. Journal of Comparative Pathology 85, 163–170.Google Scholar
Reid, J. F. S. and Armour, J. ( 1975 b). Studies in Scottish hill sheep: II. Changes in the susceptibility of the lamb to Ostertagia spp. Journal of Comparative Pathology 85, 269–275.Google Scholar
Roberts, M. G., Dobson, A. P., Arneberg, P., de Leo, G. A., Krecek, R. C., Manfredi, M. T., Lanfranchi, P. and Zaffaroni, E. ( 2002). Parasite community ecology and biodiversity. In The Ecology of Wildlife Diseases ( ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 63–82. Oxford University Press, Oxford, UK.
Ross, J. G. ( 1970). Acquired immunity to Trichostrongylus axei in lambs: investigations of the development of immune competence. Journal of Helminthology 44, 199–210.CrossRefGoogle Scholar
Samuel, W. M., Pybus, M. J. and Kocan, A. A. ( 2001). Parasitic Diseases of Wild Mammals. Iowa State University Press, Iowa, USA.CrossRef
Smith, W. D., Jackson, F., Jackson, E. and Williams, J. ( 1985). Age immunity to Ostertagia circumcincta: comparison of the local immune responses of 4 1/2 and 10 month-old lambs. Journal of Comparative Pathology 95, 235–245.CrossRefGoogle Scholar
Soulsby, E. J. L. ( 1986). Helminths, Arthropods and Protozoa of Domesticated Animals. Balliere Tindall, London, UK.
Stear, M. J., Abuagob, O., Benothman, M., Bishop, S. C., Innocent, G., Kerr, A. and Mitchell, S. ( 2006). Variation among faecal egg counts following natural nematode infection in Scottish blackface lambs. Parasitology 132, 1–6.CrossRefGoogle Scholar
Stear, M. J., Bairden, K., Bishop, S. C., Gettinby, G., McKellar, Q. A., Park, M., Strain, S. and Wallace, D. S. ( 1998). The processes influencing the distribution of parasite nematodes among naturally infected lambs. Parasitology 117, 165–171.CrossRefGoogle Scholar
Stear, M. J., Bairden, K., Bishop, S. C., Suitkamp, J., Duncan, J. L., Gettinby, G., McKellar, Q. A., Park, M., Parkins, J. J., Reid, S. W. J., Strain, S. and Murray, M. ( 1997). The genetic basis of resistance to Ostertagia circumcincta in lambs. The Veterinary Journal 154, 111–119.CrossRefGoogle Scholar
Stear, M. J., Bishop, S. C., Doligalska, M., Duncan, J. L., Holmes, P. H., Irvine, J., McCririe, L., McKellar, Q. A., Sinski, E. and Murray, M. ( 1995). Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunology 17, 643–652.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
Stevenson, L. A., Gasser, R. B. and Chilton, N. B. ( 1996). The ITS-2 rDNA of Teladorsagia circumcincta, T. trifurcata and T. davtiani (nematoda:Trichostrongylidae) indicates that these taxa are one species. International Journal for Parasitology 26, 1123–1126.Google 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.CrossRefGoogle Scholar
Tetzlaff, R. D. and Todd, A. C. ( 1973). Protective effects of premunition and age group interaction of Haemonchus contortus in sheep. American Journal of Veterinary Research 34, 1549–1554.Google Scholar
Urquhart, G. M., Armour, J., Duncan, J. L., Dunn, A. M. and Jennings, F. W. ( 1999). Veterinary Parasitology, Blackwell Science Ltd., Oxford, UK.
Wakelin, D. and Blackwell, J. ( 1988). Genetics of Resistance to Bacterial and Parasitic Infection. Taylor and Francis, London, UK.
Waller, P. J. and Thomas, R. J. ( 1978). Nematode parasitism in sheep in north-east England: the epidemiology of Ostertagia spp. International Journal for Parasitology 8, 275–283.CrossRefGoogle Scholar
Waller, P. J. and Thomas, R. J. ( 1981). The natural regulation of Trichostrongylus spp. populations in young grazing sheep. Veterinary Parasitology 9, 47–55.Google Scholar
Wilson, K. and Grenfell, B. T. ( 1997). Generalized linear modelling for parasitologists. Parasitology Today 13, 33–38.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, UK.
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 Scholar