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Is there a cost of parasites to caribou?

Published online by Cambridge University Press:  22 December 2008

J. HUGHES ,
S. D. ALBON ,
R. J. IRVINE  and
S. WOODIN
J. HUGHES*
Affiliation:
Centre for Ecology and Hydrology, Hill of Brathens, Banchory, AberdeenshireAB31 4BW, UK
S. D. ALBON
Affiliation:
Centre for Ecology and Hydrology, Hill of Brathens, Banchory, AberdeenshireAB31 4BW, UK
R. J. IRVINE
Affiliation:
Centre for Ecology and Hydrology, Hill of Brathens, Banchory, AberdeenshireAB31 4BW, UK
S. WOODIN
Affiliation:
Centre for Ecology and Hydrology, Hill of Brathens, Banchory, AberdeenshireAB31 4BW, UK
*
*Corresponding author: Wildlife Conservation Research Unit, Zoology Department, University of Oxford, UK. E-mail: joelene.hughes@zoo.ox.ac.uk
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Summary

Macroparasites potentially play a significant but often ignored role in the ecology and dynamics of wild ruminant populations. In the Arctic, parasites may impact on host populations by exacerbating the effects of seasonal and limited forage availability on the condition, fecundity and survival of individuals. We studied the effects of abomasal nematode parasites and warble flies, Hypoderma tarandi, on condition and pregnancy of caribou Rangifer tarandus in the Dolphin-Union herd, Nunavut, Canada. By the end of winter, female caribou over 2 years old showed a significant decrease in body weight with increasing nematode burden, and a decrease in back fat depth with increasing warble abundance. These effects were exaggerated in the non-pregnant fraction of the population. High warble larvae burdens were also associated with significantly reduced probability of being pregnant. Our research demonstrates a negative relationship between parasites and caribou condition that may have consequences for their fitness. Additionally, we discuss the possibility that muskox Ovibos moschatus share some parasite species with the caribou and could lead to elevated burdens in the sympatric host. Parasites may have been a contributory factor in a previous winter range-shift of the caribou herd and this may reflect a form of apparent competition between the two ungulate species.

Keywords

competitionreproductionRangifer tarandusmuskoxOvibos moschatusparasiteOstertagiaTeladorsagiawarble fly
Type
Research Article
Information
Parasitology , Volume 136 , Issue 2 , February 2009 , pp. 253 - 265
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Albon, S. D., Stien, A., Irvine, R. J., Langvatn, R., Ropstad, E. and Halvorsen, O. (2002). The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London, B 269, 1625–1632.CrossRefGoogle ScholarPubMed
Alerstam, T., Hedenstrom, A. and Akesson, S. (2003). Long-distance migration: evolution and determinants. Oikos 103, 247–260.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–247.CrossRefGoogle Scholar
Arneberg, P., Folstad, I. and Karter, A. J. (1996). Gastrointestinal nematodes depress food intake in naturally infected reindeer. Parasitology 112, 213–219.CrossRefGoogle ScholarPubMed
Bergerud, A. T. (1996). Evolving perspectives on caribou population dynamics, have we got it right yet? Rangifer 95–116.CrossRefGoogle Scholar
Bye, K. (1987). Abomasal nematodes from 3 Norwegian wild reindeer populations. Canadian Journal of Zoology-Revue Canadienne De Zoologie 65, 677–680.Google Scholar
Dallas, J. F., Irvine, R. J. and Halvorsen, O. (2000). DNA evidence that Ostertagia gruehneri and Ostertagia arctica (Nematoda: Ostertagiinae) in reindeer from Norway and Svalbard are conspecific. International Journal for Parasitology 30, 655–658.CrossRefGoogle ScholarPubMed
Ezenwa, V. O. (2004). Selective defecation and selective foraging: antiparasite behavior in wild ungulates? Ethology 110, 851–862.Google Scholar
Fauchald, P., Rodven, R., Bardsen, B. J., Langeland, K., Tveraa, T., Yoccoz, N. G. and Ims, R. A. (2007). Escaping parasitism in the selfish herd: age, size and density-dependent warble fly infestation in reindeer. Oikos 116, 491–499.CrossRefGoogle Scholar
Folstad, I., Nilssen, A. C., Halvorsen, O. and Andersen, J. (1991). Parasite avoidance – the cause of post-calving migrations in Rangifer. Canadian Journal of Zoology-Revue Canadienne De Zoologie 69, 2423–2429.CrossRefGoogle Scholar
Fox, M. T. (1997). Pathophysiology of infection with gastrointestinal nematodes in domestic ruminants: recent developments. Veterinary Parasitology 72, 285–297.CrossRefGoogle ScholarPubMed
Gerhart, K. L., White, R. G., Cameron, R. D. and Russell, D. E. (1996). Body composition and nutrient reserves of arctic caribou. Canadian Journal of Zoology-Revue Canadienne De Zoologie 74, 136–146.Google Scholar
Gould, W. A., Edlund, S., Zoltai, S., Raynolds, M., Walker, D. A. and Maier, H. (2002). Canadian Arctic vegetation mapping. International Journal of Remote Sensing 23, 4597–4609.CrossRefGoogle Scholar
Gulland, F. M. D. (1995). The impact of infectious diseases on wild animal populations – a review. In Ecology of Infectious Diseases in Natural Populations, (ed. Grenfell, B. T. and Dobson, A. P.), pp. 20–51. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Gunn, A. (1990). The decline and recovery of caribou and muskoxen on Victoria Island. In Canada's Missing Dimension: Science and History in the Canadian Arctic Islands, (ed. Harrington, C. R.), pp. 590–607. Canadian Museum of Nature, Ottawa, Canada.Google Scholar
Gunn, A., Buchan, A., Fournier, B. and Nishi, J. (1997). Victoria Island Caribou Migrations Across Dolphin and Union Strait and Coronation Gulf from the Mainland Coast, 1976–94. Manuscript Report, Canada No. 94 Government of the N.W.T.Google Scholar
Gunn, A. and Irvine, R. J. (2003). Subclinical parasitism and ruminant foraging strategies – a review. Wildlife Society Bulletin 31, 117–126.Google Scholar
Hagemoen, R. I. M. and Reimers, E. (2002). Reindeer summer activity pattern in relation to weather and insect harassment. Journal of Animal Ecology 71, 883–892.CrossRefGoogle Scholar
Halvorsen, O. and Bye, K. (1999). Parasites, biodiversity, and population dynamics in an ecosystem in the High Arctic. Veterinary Parasitology 84, 205–227.Google Scholar
Halvorsen, O., Stien, A., Irvine, J., Langvatn, R. and Albon, S. (1999). Evidence for continued transmission of parasitic nematodes in reindeer during the Arctic winter. International Journal for Parasitology 29, 567–579.Google Scholar
Hoberg, E. P., Kocan, A. and Rickard, L. G. (2001). Gastrointestinal strongyles in wild ruminants. In Parasitic Diseases of Wild Mammals, (ed. Samuel, W., Pybus, M. and Kocan, A.), pp. 193–227. Iowa State University Press, Ames, Iowa, USA.CrossRefGoogle Scholar
Hoberg, E. P., Monsen, K. J., Kutz, S. and Blouin, M. S. (1999). Structure, biodiversity, and historical biogeography of nematode faunas in Holarctic ruminants: morphological and molecular diagnoses for Teladorsagia boreoarcticus N-sp (Nematoda: Ostertagiinae), a dimorphic cryptic species in muskoxen (Ovibos moschatus). Journal of Parasitology 85, 910–934.CrossRefGoogle ScholarPubMed
Holmes, P. H. (1987). Pathophysiology of nematode infections. International Journal for Parasitology 17, 443–451.CrossRefGoogle ScholarPubMed
Hutchings, M. R., Gordon, I. J., Kyriazakis, I. and Jackson, F. (2001 a). Sheep avoidance of faeces-contaminated patches leads to a trade-off between intake rate of forage and parasitism in subsequent foraging decisions. Animal Behaviour 62, 955–964.CrossRefGoogle Scholar
Hutchings, M. R., Kyriazakis, I. and Gordon, I. J. (2001 b). Herbivore physiological state affects foraging trade-off decisions between nutrient intake and parasite avoidance. Ecology 82, 1138–1150.Google Scholar
Hutchings, M. R., Kyriazakis, I., Gordon, I. J. and Jackson, F. (1999). Trade-offs between nutrient intake and faecal avoidance in herbivore foraging decisions: the effect of animal parasitic status, level of feeding motivation and sward nitrogen content. Journal of Animal Ecology 68, 310–323.CrossRefGoogle Scholar
Irvine, R. J. (2006). Parasites and the dynamics of wild mammal populations. Animal Science 82, 775–781.Google Scholar
Irvine, R. J., Corbishley, H., Pilkington, J. G. and Albon, S. D. (2006). Low-level parasitic worm burdens may reduce body condition in free-ranging red deer (Cervus elaphus). Parasitology 133, 465–475.Google Scholar
Irvine, R. J., Stien, A., Dallas, J. F., Halvorsen, O., Langvatn, R. and Albon, S. D. (2001). Contrasting regulation of fecundity in two abomasal nematodes of Svalbard reindeer (Rangifer tarandus platyrhynchus). Parasitology 122, 673–681.Google Scholar
Irvine, R. J., Stien, A., Halvorsen, O., Langvatn, R. and Albon, S. D. (2000). Life-history strategies and population dynamics of abomasal nematodes in Svalbard reindeer (Rangifer tarandus platyrhynchus). Parasitology 120, 297–311.Google Scholar
Jingfors, K. (1984). Abundance, composition and distribution of Muskoxen on Southeastern Victoria Island. In File Report No. 36, Vol. Northwest Territories RWED.Google Scholar
Kutz, S. J., Hoberg, E. P., Nagy, J., Polley, L. and Elkin, B. (2004). “Emerging” parasitic infections in arctic ungulates. Integrative and Comparative Biology 44, 109–118.CrossRefGoogle ScholarPubMed
Lichtenfels, J. R. and Hoberg, E. P. (1993). The systematics of nematodes that cause ostertagiasis in domestic and wild ruminants in North America – an update and a key to species. Veterinary Parasitology 46, 33–53.Google Scholar
Manning, T. H. (1960). The relationship of the Peary and Barren Ground Caribou. Arctic Institute of North America Technical Paper No. 4.Google Scholar
MAFF/ADAS (1986). Manual of Veterinary Parasitological Laboratory Techniques. Reference Book 418, London: Her Majesty's Stationary Office.Google Scholar
May, R. M. and Anderson, R. M. (1978). Regulation and stability of host-parasite population interactions. II. Destabilising processes. Journal of Animal Ecology 47, 249–267.Google Scholar
Miller, F. L. (2003). Caribou Rangifer tarandus. In Wild Mammals of North America, (ed. Feldhammer, G. A., Thompson, B. C. and Chapman, J. A.), pp. 965–997. The John Hopkins University Press, Baltimore and London.Google Scholar
SAS (2002). The SAS System for Windows. SAS Institute Inc., Cary, USA.Google Scholar
Shaw, D. J., Grenfell, B. T. and Dobson, A. P. (1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.Google Scholar
Stien, A., Irvine, R. J., Ropstad, E., Halvorsen, O., Langvatn, R. and Albon, S. D. (2002). The impact of gastrointestinal nematodes on wild reindeer: experimental and cross-sectional studies. Journal of Animal Ecology 71, 937–945.Google Scholar
Suarez, V. H. and Cabaret, J. (1991). Similarities between species of the Ostertagiinae (Nematoda, Trichostrongyloidea) in relation to host-specificity and climatic environment. Systematic Parasitology 20, 179–185.Google Scholar
Thomas, D. C. (1982). The relationship between fertility and fat reserves of Peary Caribou. Canadian Journal of Zoology-Revue Canadienne De Zoologie 60, 597–602.Google Scholar
Van Der Wal, R., Irvine, J., Stien, A., Shepherd, N. and Albon, S. D. (2000). Faecal avoidance and the risk of infection by nematodes in a natural population of reindeer. Oecologia 124, 19–25.CrossRefGoogle Scholar
Walker, M. D., Wahren, C. H., Hollister, R. D., Henry, G. H. R., Ahlquist, L. E., Alatalo, J. M., Bret-Harte, M. S., Calef, M. P., Callaghan, T. V., Carroll, A. B., Epstein, H. E., Jonsdottir, I. S., Klein, J. A., Magnusson, B., Molau, U., Oberbauer, S. F., Rewa, S. P., Robinson, C. H., Shaver, G. R., Suding, K. N., Thompson, C. C., Tolvanen, A., Totland, O., Turner, P. L., Tweedie, C. E., Webber, P. J. and Wookey, P. A. (2006). Plant community responses to experimental warming across the tundra biome. Proceedings of the National Academy of Sciences, USA 103, 1342–1346.CrossRefGoogle ScholarPubMed
Weladji, R. B., Holand, O. and Almoy, T. (2003). Use of climatic data to assess the effect of insect harassment on the autumn weight of reindeer (Rangifer tarandus) calves. Journal of Zoology 260, 79–85.CrossRefGoogle Scholar
Wilson, K., Bjornstad, O. N., Dobson, A. P., Merler, S., Poglayen, G., Randolph, S. E., Read, A. F. and Skorping, A. (2002). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases, (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 6–44. Oxford University Press, New York.Google Scholar