Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T03:03:02.914Z Has data issue: false hasContentIssue false

Climate change and the epidemiology of protostrongylid nematodes in northern ecosystems: Parelaphostrongylus odocoilei and Protostrongylus stilesi in Dall's sheep (Ovis d. dalli)

Published online by Cambridge University Press:  07 December 2005

E. J. JENKINS
Affiliation:
Department of Veterinary Microbiology, Western College of Veterinary Medicine, 52 Campus Drive, University of Saskatchewan, Saskatoon, Saskatchewan, Canada, S7N 5B4
A. M. VEITCH
Affiliation:
Wildlife Management, Environment and Natural Resources, Box 130, Government of the Northwest Territories, Norman Wells, Northwest Territories, Canada, X0E 0V0
S. J. KUTZ
Affiliation:
Department of Veterinary Microbiology, Western College of Veterinary Medicine, 52 Campus Drive, University of Saskatchewan, Saskatoon, Saskatchewan, Canada, S7N 5B4
E. P. HOBERG
Affiliation:
United States Department of Agriculture, Agricultural Research Service, US National Parasite Collection, Animal Parasitic Diseases Laboratory, BARC East No. 1180, 10300 Baltimore Avenue, Beltsville, Maryland, 20705, USA
L. POLLEY
Affiliation:
Department of Veterinary Microbiology, Western College of Veterinary Medicine, 52 Campus Drive, University of Saskatchewan, Saskatoon, Saskatchewan, Canada, S7N 5B4

Abstract

We describe the epidemiology of the protostrongylid parasites Parelaphostrongylus odocoilei and Protostrongylus stilesi in Dall's sheep (Ovis dalli dalli) from the Mackenzie Mountains, Northwest Territories, Canada (65 °N; 128 °W). Peak numbers of 1st-stage larvae of both parasites were shed by Dall's sheep on their winter range from March until May. In larval development experiments in the Mackenzie Mountains, peak numbers of infective 3rd-stage larvae of P. odocoilei were available in gastropod intermediate hosts in August–September. For both protostrongylids, the majority of transmission likely occurs on the winter range, with infection of gastropods when they emerge from hibernation in spring, and infection of Dall's sheep upon their return in fall. We validated a degree-day model for temperature-dependent development of larval P. odocoilei in gastropods, and applied degree-day models to describe and predict spatial and temporal patterns in development of P. odocoilei and P. stilesi in northern North America. Temperature-dependent larval development may currently limit northward range expansion of P. odocoilei into naïve populations of Dall's sheep in the Arctic, but climate warming may soon eliminate such constraints. In Subarctic regions where both P. odocoilei and P. stilesi are endemic, the length of the parasite ‘growing season’ (when temperatures were above the threshold for larval development) and amount of warming available for parasite development has increased over the last 50 years. Further climate warming and extension of the seasonal window for transmission may lead to amplification of parasite populations and disease outbreaks in host populations.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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

Aitchison, C. W. ( 1979). Notes on low temperature activity of oligochaetes, gastropods, and centipedes in southern Canada. American Midland Naturalist 102, 399400.CrossRefGoogle Scholar
Ball, M. C., Lankester, M. W. and Mahoney, S. P. ( 2001). Factors affecting the distribution and transmission of Elaphostrongylus rangiferi (Protostrongylidae) in caribou (Rangifer tarandus caribou) of Newfoundland, Canada. Canadian Journal of Zoology 79, 12651277.CrossRefGoogle Scholar
Boag, D. A. and Wishart, W. D. ( 1982). Distribution and abundance of terrestrial gastropods on a winter range of bighorn sheep in southwestern Alberta. Canadian Journal of Zoology 60, 26332640.CrossRefGoogle Scholar
Bowyer, R. T. and Leslie, D. M. ( 1992). Ovis dalli. Mammalian Species 393, 17.CrossRefGoogle Scholar
Dainton, B. H. ( 1989). Field and laboratory observations on slug and snail behaviour. In Monograph No. 41 Slugs and Snails in World Agriculture ( ed. Henderson, I.), pp. 201207. British Crop Protection Council, Thornton Heath, UK.
Danks, H. V. ( 1992). Arctic insects as indicators of environmental change. Arctic 45, 159166.CrossRefGoogle Scholar
Dau, J. ( 1981). Protostrongylus, Muellerius and Dictyocaulus. In Alaskan Wildlife Diseases ( ed. Dieterich, R. A.), pp. 141146. University of Alaska, Fairbanks, Alaska, USA.
Dobson, A., Kutz, S., Pascual, M. and Winfree, R. ( 2003). Pathogens and parasites in a changing climate. In Climate Change and Biodiversity: Synergistic Impacts, Advances in Applied Biodiversity Science ( ed. Hannah, L. and Lovejoy, T. E.), pp. 3338. Centre for Applied Biodiversity Science, Conservation International, Washington, DC, USA.
Forrester, D. J. and Littell, R. C. ( 1976). Influence of rainfall on lungworm infections in bighorn sheep. Journal of Wildlife Diseases 12, 4851.CrossRefGoogle Scholar
Forrester, D. J. and Senger, C. M. ( 1963). Effect of temperature and humidity on survival of first-stage Protostrongylus stilesi larvae. Experimental Parasitology 13, 8389.CrossRefGoogle Scholar
Forrester, S. G. and Lankester, M. W. ( 1997). Extracting protostrongylid nematode larvae from ungulate feces. Journal of Wildlife Diseases 33, 511516.CrossRefGoogle Scholar
Forrester, S. G. and Lankester, M. W. ( 1998). Over-winter survival of first-stage larvae of Parelaphostrongylus tenuis (Nematoda: Protostrongylidae). Canadian Journal of Zoology 76, 704710.CrossRefGoogle Scholar
Getz, L. L. ( 1959). Notes on the ecology of slugs: Arion circumscriptus, Deroceras reticulatum, and D. laeve. American Midland Naturalist 61, 485498.CrossRefGoogle Scholar
Grenfell, B. T., Wilson, K., Isham, V. S., Boyd, H. E. G. and Dietz, K. ( 1995). Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode-ruminant interactions as a case study. Parasitology 111 (Suppl.), S135S151.CrossRefGoogle Scholar
Halvorsen, O., Skorping, A. and Hansen, K. ( 1985). Seasonal cycles in the output of first stage larvae of the nematode Elaphostrongylus rangiferi from reindeer, Rangifer tarandus tarandus. Polar Biology 5, 4954.CrossRefGoogle Scholar
Halvorsen, O., Stien, A., Irvine, J., Langvain, R. and Albon, S. ( 1999). Evidence for continued transmission of parasitic nematodes in reindeer during the Arctic winter. International Journal for Parasitology 29, 567579.CrossRefGoogle Scholar
Handeland, K. and Slettbakk, T. ( 1994). Outbreaks of clinical cerebrospinal elaphostrongylosis in reindeer (Rangifer tarandus tarandus) in Finnmark, Norway, and their relation to climatic conditions. Journal of Veterinary Medicine Series B 41, 407410.CrossRefGoogle Scholar
Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S. and Samuel, M. D. ( 2002). Climate warming and disease risks for terrestrial and marine biota. Science 296, 21582162.CrossRefGoogle Scholar
Hassol, S. J. ( 2004). Impacts of a Warming Arctic, Arctic Climate Impact Assessment, Cambridge University Press, New York, USA.
Hibler, C. P., Metzger, C. J., Spraker, T. R. and Lange, R. E. ( 1974). Further observations on Protostrongylus sp. infection by transplacental transmission in bighorn sheep. Journal of Wildlife Diseases 10, 3941.Google Scholar
Hoberg, E. P., Kocan, A. A. and Rickard, L. G. ( 2001). Gastrointestinal strongyles in wild ruminants. In Parasitic Diseases of Wild Mammals, 2nd Edn ( ed. Samuel, W. M., Pybus, M. J. and Kocan, A. A.), pp. 193227. Iowa State University Press, Ames, Iowa, USA.CrossRef
Hoberg, E. P., Kutz, S. J., Galbreath, K. and Cook, J. ( 2003). Arctic biodiversity: from discovery to faunal baseline – revealing the history of a dynamic ecosystem. Journal of Parasitology 89 (Suppl.), S84S95.Google Scholar
Hoberg, E. P., Kutz, S. J., Nagy, J., Jenkins, E., Elkin, B., Branigan, M. and Cooley, D. ( 2002). Protostrongylus stilesi (Nematoda: Protostrongylidae): ecological isolation and putative host-switching between Dall's sheep and muskoxen in a contact zone. Comparative Parasitology 69, 19.CrossRefGoogle Scholar
Hoberg, E. P., Polley, L., Gunn, A. and Nishi, J. S. ( 1995). Umingmakstrongylus pallikuukensis gen nov et sp nov (Nematoda: Protostrongylidae) from muskoxen, Ovibos moschatus, in the central Canadian Arctic, with comments on biology and biogeography. Canadian Journal of Zoology 73, 22662282.CrossRefGoogle Scholar
Hoefs, M. and Cowan, I. M. ( 1979). Ecological investigation of a population of Dall sheep (Ovis dalli dalli Nelson). Syesis 12 (Suppl.), S1S81.Google Scholar
Hoffmann, A. A. and Blows, M. W. ( 1994). Species borders: ecological and evolutionary perspectives. Trends in Ecology and Evolution 9, 223227.CrossRefGoogle Scholar
Inglis, W. G. ( 1965). Patterns of evolution in parasitic nematodes. In Evolution of Parasites, Third Symposium of the British Society for Parasitology ( ed. Taylor, A. E. R.), pp. 79124. Blackwell Scientific Publications, Oxford, UK.
Jenkins, E. J. ( 2005). Ecological investigation of a new host-parasite relationship: Parelaphostrongylus odocoilei in thinhorn sheep (Ovis dalli), Ph.D. Thesis, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.
Jenkins, E. J., Appleyard, G. D., Hoberg, E. P., Rosenthal, B. M., Kutz, S. J., Veitch, A. M., Schwantje, H. M., Elkin, B. T. and Polley, L. ( 2005 a). Geographic distribution of the muscle-dwelling nematode Parelaphostrongylus odocoilei in North America, using molecular identification of first-stage larvae. Journal of Parasitology 91, 574584.Google Scholar
Jenkins, E. J., Hoberg, E. P. and Polley, L. ( 2005 b). Development and pathogenesis of Parelaphostrongylus odocoilei (Nematoda: Protostrongylidae) in experimentally infected thinhorn sheep (Ovis dalli). Journal of Wildlife Diseases (in the Press).Google Scholar
Jenkins, E. J., Kutz, S. J., Hoberg, E. P. and Polley, L. ( 2005 c). Bionomics of larvae of Parelaphostrongylus odocoilei (Nematoda: Protostrongylidae) in experimentally-infected gastropod intermediate hosts. Journal of Parasitology (in the Press).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, 109118.CrossRefGoogle Scholar
Kutz, S. J., Hoberg, E. P., Nishi, J. and Polley, L. ( 2002). Development of the muskox lungworm, Umingmakstrongylus pallikuukensis (Protostrongylidae), in gastropods in the Arctic. Canadian Journal of Zoology 80, 19771985.CrossRefGoogle Scholar
Kutz, S. J., Hoberg, E. P. and Polley, L. ( 2000). Emergence of third-stage larvae of Umingmakstrongylus pallikuukensis from three gastropod intermediate host species. Journal of Parasitology 86, 743749.CrossRefGoogle Scholar
Kutz, S. J., Hoberg, E. P., Polley, L. and Jenkins, E. J. ( 2005). Global warming is changing the dynamics of Arctic host-parasite systems. Proceedings of the Royal Society of London, B (in the Press). DOI: 10.1098/rspb.2005.3285CrossRefGoogle Scholar
Kutz, S. J., Veitch, A. M., Hoberg, E. P., Elkin, B. T., Jenkins, E. J. and Polley, L. ( 2001). New host and geographic records for two protostrongylids in Dall's sheep. Journal of Wildlife Diseases 37, 761774.CrossRefGoogle Scholar
Lankester, M. W. and Anderson, R. C. ( 1968). Gastropods as intermediate hosts of Pneumostrongylus tenuis Dougherty of white-tailed deer. Canadian Journal of Zoology 46, 373383.CrossRefGoogle Scholar
Lankester, M. W. and Peterson, W. J. ( 1996). The possible importance of wintering yards in the transmission of Parelaphostrongylus tenuis to white-tailed deer and moose. Journal of Wildlife Diseases 32, 3138.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, 840844.CrossRefGoogle Scholar
Levine, N. D. ( 1963). Weather, climate, and the bionomics of ruminant nematode larvae. Advances in Veterinary Science 8, 215261.Google Scholar
Lorentzen, G. and Halvorsen, O. ( 1986). Survival of the first stage larva of the metastrongyloid nematode Elaphostrongylus rangiferi under various conditions of temperature and humidity. Holarctic Ecology 9, 301304.CrossRefGoogle Scholar
Monson, R. A. and Post, G. ( 1972). Experimental transmission of Protostrongylus stilesi to bighorn-mouflon sheep hybrids. Journal of Parasitology 58, 2933.CrossRefGoogle Scholar
Morgan, E. R., Milner-Gulland, E. J., Torgerson, P. R. and Medley, G. F. ( 2004). Ruminating on complexity: macroparasites of wildlife and livestock. Trends in Ecology and Evolution 19, 181188.CrossRefGoogle Scholar
Ollerenshaw, C. B. and Smith, L. P. ( 1969). Meterological factors and forecasts of helminthic disease. Advances in Parasitology 7, 283323.CrossRefGoogle Scholar
Pilsbry, H. A. ( 1948). Land Mollusca of North America (north of Mexico), Volume II, Part 2. Academy of Natural Sciences Monograph No. 3, Philadelphia, Pennsylvania, USA.
Pybus, M. J., Samuel, W. M., Welch, D. A. and Wilke, C. J. ( 1990). Parelaphostrongylus andersoni (Nematoda: Protostrongylidae) in white-tailed deer from Michigan. Journal of Wildlife Diseases 26, 535537.CrossRefGoogle Scholar
Robb, L. A. and Samuel, W. M. ( 1990). Gastropod intermediate hosts of lungworms (Nematoda: Protostrongylidae) on a bighorn sheep winter range: aspects of transmission. Canadian Journal of Zoology 68, 19761982.CrossRefGoogle Scholar
Rollo, C. D. ( 1991). Endogenous and exogenous regulation of activity in Deroceras reticulatum, a weather-sensitive terrestrial slug. Malacologia 33, 199220.Google Scholar
Rollo, C. D. and Shibata, D. M. ( 1991). Resilience, robustness, and plasticity in a terrestrial slug, with particular reference to food quality. Canadian Journal of Zoology 69, 978987.CrossRefGoogle Scholar
Rose, J. H. ( 1957). Observations on the bionomics of the free-living first stage larvae of the sheep lungworm, Muellerius capillaris. Journal of Helminthology 31, 1728.CrossRefGoogle Scholar
Samson, J. and Holmes, J. C. ( 1985). The effect of temperature on rates of development of larval Protostrongylus spp. (Nematoda, Metastrongyloidea) from bighorn sheep, Ovis canadensis canadensis, in the snail Vallonia pulchella. Canadian Journal of Zoology 63, 14451448.Google Scholar
Samuel, W. M., Platt, T. R. and Knispel-Krause, S. M. ( 1985). Gastropod intermediate hosts and transmission of Parelaphostrongylus odocoilei, a muscle-inhabiting nematode of mule deer, Odocoileus h. hemionus, in Jasper National Park, Alberta. Canadian Journal of Zoology 63, 928932.Google Scholar
Saunders, L. M., Tompkins, D. M. and Hudson, P. J. ( 2002). Stochasticity accelerates nematode egg development. Journal of Parasitology 88, 12711272.CrossRefGoogle Scholar
Shostak, A. W. and Samuel, W. M. ( 1984). Moisture and temperature effects on survival and infectivity of first-stage larvae of Parelaphostrongylus odocoilei and P. tenuis (Nematoda: Metastrongyloidea). Journal of Parasitology 70, 261269.Google Scholar
Simmons, N. M. ( 1982). Seasonal ranges of Dall's sheep, Mackenzie Mountains, Northwest Territories. Arctic 35, 512518.CrossRefGoogle Scholar
Slomke, A. M., Lankester, M. W. and Peterson, W. J. ( 1995). Infrapopulation dynamics of Parelaphostrongylus tenuis in white-tailed deer. Journal of Wildlife Diseases 31, 125135.CrossRefGoogle Scholar
South, A. ( 1989). The effect of weather and other factors on numbers of slugs on permanent pasture. In Monograph No. 41 Slugs and Snails in World Agriculture ( ed. Henderson, I.), pp. 355360. British Crop Protection Council, Thornton Heath, UK.
Uhazy, L. S., Holmes, J. C. and Stelfox, J. G. ( 1973). Lungworms in the Rocky Mountain bighorn sheep of western Canada. Canadian Journal of Zoology 51, 817824.CrossRefGoogle Scholar
Veitch, A. M., Simmons, E., Adamczewski, J. and Popko, R. ( 1998). Status, harvest, and co-management of Dall's sheep in the Mackenzie Mountains, Northwest Territories. Biennial Symposium of the Northern Wild Sheep and Goat Council 11, 134153.Google Scholar
Worley, K., Strobeck, C., Arthur, S., Carey, J., Schwantje, H., Veitch, A. and Coltman, D. W. ( 2004). Population genetic structure of North American thinhorn sheep (Ovis dalli). Molecular Ecology 13, 25452556.CrossRefGoogle Scholar
Yde, C. A., Brown, G. W. and Worley, D. ( 1988). Lungworm larvae discharge levels within the Ural-Tweed bighorn sheep population. Biennial Symposium of the Northern Wild Sheep and Goat Council 6, 8490.Google Scholar
Zarnke, R. L., Samuel, W. M., Franzmann, A. W. and Barrett, R. ( 1990). Factors influencing the potential establishment of the winter tick (Dermacentor albipictus) in Alaska. Journal of Wildlife Diseases 26, 412415.CrossRefGoogle Scholar