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Landscape influence on spatial patterns of meningeal worm and liver fluke infection in white-tailed deer

Published online by Cambridge University Press:  11 December 2014

KIMBERLY L. VANDERWAAL ,
STEVE K. WINDELS ,
BRYCE T. OLSON ,
J. TREVOR VANNATTA  and
RON MOEN
KIMBERLY L. VANDERWAAL*
Affiliation:
Conservation Department, Minnesota Zoo, 13000 Zoo Blvd., Apple Valley, Minnesota 55124, USA Natural Resources Research Institute, University of Minnesota, Duluth. 5013 Miller Trunk Highway, Duluth, Minnesota 55811, USA
STEVE K. WINDELS
Affiliation:
Voyageurs National Park, 360 Hwy 11. E, International Falls, Minnesota 56649, USA
BRYCE T. OLSON
Affiliation:
Voyageurs National Park, 360 Hwy 11. E, International Falls, Minnesota 56649, USA
J. TREVOR VANNATTA
Affiliation:
Natural Resources Research Institute, University of Minnesota, Duluth. 5013 Miller Trunk Highway, Duluth, Minnesota 55811, USA
RON MOEN
Affiliation:
Natural Resources Research Institute, University of Minnesota, Duluth. 5013 Miller Trunk Highway, Duluth, Minnesota 55811, USA
*
* Corresponding author. Department of Veterinary Population Medicine, University of Minnesota, 1365 Gortner Avenue, St. Paul, Minnesota 55108, USA. E-mail: kvw@umn.edu
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Summary

Parasites that primarily infect white-tailed deer (Odocoileus virginianus), such as liver flukes (Fascioloides magna) and meningeal worm (Parelaphostrongylus tenuis), can cause morbidity and mortality when incidentally infecting moose (Alces alces). Ecological factors are expected to influence spatial variation in infection risk by affecting the survival of free-living life stages outside the host and the abundance of intermediate gastropod hosts. Here, we investigate how ecology influenced the fine-scale distribution of these parasites in deer in Voyageurs National Park, Minnesota. Deer pellet groups (N = 295) were sampled for the presence of P. tenuis larvae and F. magna eggs. We found that deer were significantly more likely to be infected with P. tenuis in habitats with less upland deciduous forest and more upland mixed conifer forest and shrub, a pattern that mirrored microhabitat differences in gastropod abundances. Deer were also more likely to be infected with F. magna in areas with more marshland, specifically rooted-floating aquatic marshes (RFAMs). The environment played a larger role than deer density in determining spatial patterns of infection for both parasites, highlighting the importance of considering ecological factors on all stages of a parasite's life cycle in order to understand its occurrence within the definitive host.

Keywords

disease ecologyhabitatinfection riskparasite transmissionwildlife diseasewetlands

Information

Type
Research Article
Information
Parasitology , Volume 142 , Issue 5 , April 2015 , pp. 706 - 718
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Copyright © Cambridge University Press 2014 

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References

REFERENCES

Aho, R. W. and Hendrickson, J. (1989). Reproduction and mortality of moose translocated from Ontario to Michigan. Alces 25, 75–80.Google Scholar
Altizer, S., Nunn, C., Thrall, P., Gittleman, J., Antonovics, J., Cunningham, A., Dobson, A., Ezenwa, V., Jones, K., Pederson, A., Poss, M. and Pulliam, J. (2003). Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution and Systematics 34, 517–547.CrossRefGoogle Scholar
Belovsky, G. E. (1981). Optimal activity times and habitat choice of moose. Oecologia 48, 22–30.CrossRefGoogle ScholarPubMed
Cobb, M. A., Gogan, P. J. P., Kozie, K. D., Olexa, E. M., Lawrence, R. L. and Route, W. T. (2004). Relative spatial distributions and habitat use patterns of sympatric moose and white-tailed deer in Voyageurs National Park, Minnesota. Alces 40, 169–191.Google Scholar
Cole, G. F. (1987). Changes in interacting species with disturbance. Environmental Management 11, 257–264.Google Scholar
Cyr, T., Windels, S. K., Moen, R. A. and Warmblood, J. W. (2014). Diversity and abundance of terrestrial gastropods in Voyageurs National Park, MN: implications for risk of moose to Parelaphostrongylus tenuis infection. Alces 50, 121–132.Google Scholar
DelGiudice, G. D. (2014). 2014 Aerial Moose Survey. Minnesota Department of Natural Resources, St. Paul, MN. 1–6.Google Scholar
Demarchi, M. W. and Bunnell, F. L. (1993). Estimating forest canopy effects on summer thermal cover for Cervidae (deer family). Canadian Journal of Forest Research 23, 2419–2426.Google Scholar
Diefenbach, D. R. and Shea, S. M. (2011). Managing white-tailed deer: Eastern North America. In Biology and Management of White-tailed Deer (ed. Hewitt, D. G.), pp. 481–500. CRC Press, Boca Raton, FL.Google Scholar
Dunkel, A. M., Rognlie, M. C., Johnson, G. R. and Knapp, S. E. (1996). Distribution of potential intermediate hosts for Fasciola hepatica and Fascioloides magna in Montana, USA. Veterinary Parasitology 62, 63–70.Google Scholar
Faber-Langendoen, D., Aaseng, N., Hop, K., Lew-Smith, M. and Drake, J. (2007). Vegetation classification, mapping, and monitoring in Voyageurs National Park, Minnesota: an amplication of the U.S. National Vegetation Classification. Applied Vegetation Science 10, 361–374.Google Scholar
Foreyt, W. J. and Todd, A. C. (1976). Development of large American liver fluke, Fascioloides magna, in white-tailed deer, cattle, and sheep. Journal of Parasitology 62, 26–32.CrossRefGoogle ScholarPubMed
Forrester, S. G. and Lankester, M. W. (1997). Extracting protostrongylid nematode larvae from ungulate feces. Journal of Wildlife Diseases 33, 511–516.Google Scholar
Fraser, D., Thompson, B. K. and Arthur, D. (1982). Aquatic feeding by moose: seasonal variation in relation to plant chemical composition and use of mineral licks. Canadian Journal of Zoology 60, 3121–3126.Google Scholar
Fraser, D., Chavez, E. R. and Paloheimo, J. E. (1984). Aquatic feeding by moose: selection of plant species and feeding areas in relation to plant chemical composition and characteristics of lakes. Canadian Journal of Zoology 62, 80–87.CrossRefGoogle Scholar
Gillispie, T. R. (2006). Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. International Journal of Parasitology 27, 1129–1143.Google Scholar
Gogan, P. J. P., Kozie, K. D., Olexa, E. M. and Duncan, N. S. (1997). Ecological status of moose and white-tailed deer at Voyageurs National Park, Minnesota. Alces 33, 187–201.Google Scholar
Graveland, J. and van der Wal, R. (1996). Decline in snail abundance due to soil acidification causes eggshell defects in forest passerines. Oecologia 105, 351–360.Google Scholar
Guthery, F. S. and Beason, S. L. (1979). Cerebrospinal nematodiasis caused by Parelaphostrongylus tenuis in angora goats in Texas. Journal of Wildlife Diseases 15, 37–42.CrossRefGoogle ScholarPubMed
Hawkins, J. W., Lankester, M. W., Lautenschlager, R. A. and Bell, F. W. (1997). Effects of alternative conifer release treatments on terrestrial gastropods in northwestern Ontario. Forestry Chronicle 73, 91–98.Google Scholar
Hawkins, J. W., Lankester, M. W. and Nelson, R. A. (1998). Sampling terrestrial gastropods using corrugated cardboard sheets. Malacologia 39, 1–9.Google Scholar
Hennings, K. R. (1977). Aquatic feeding by white-tailed deer and moose in northeastern Minnesota. Vol. M.Sc. University of Minnesota, St. Paul, MN.Google Scholar
Jeglum, J. K. (1971). Plant indicators of pH and water level in peatlands at Candle Lake, Saskatchewan. Canadian Journal of Botany 49, 1661–1676.Google Scholar
Johnston, C. A. and Naiman, R. J. (1990). Aquatic patch creation in relation to beaver population trends. Ecology 71, 1617–1621.Google Scholar
Kallemeyn, L. W., Holmberg, K. L., Perry, J. A. and Odde, B. Y. (2003). Aquatic Synthesis for Voyageurs National Park. No. USGS/BRD/ITR-2003–0001. Environmental and Contaminants Research Center, U.S. Geological Survey, Columbia, MO.Google Scholar
Kearney, S. R. and Gilbert, F. F. (1978). Terrestrial gastropods from the Himsworth Game Preserve, Ontario, and their significance in Parelaphostrongylus tenuis transmission. Canadian Journal of Zoology 56, 688–694.CrossRefGoogle Scholar
Kurmis, V., Webb, S. L. and Merriam, L. C. J. (1986). Plant communities of Voyaguers National Park, Minnesota, USA. Canadian Journal of Botany 64, 531–540.Google Scholar
Lankester, M. W. (2010). Understanding the impact of meningeal worm, Parelaphostrongylus tenuis, on moose populations. Alces 46, 53–70.Google Scholar
Lankester, M. W. and Anderson, R. C. (1968). Gastropods as intermediate hosts of Pneumostrongylus tenuis Daugherty of white-tailed deer. Canadian Journal of Zoology 46, 373–383.Google Scholar
Lankester, M. W. and Foreyt, W. J. (2011). Moose experimentally infected with giant liver fluke (Fascioloides magna). Alces 47, 9–15.Google 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, 31–38.Google Scholar
Lankester, M. W. and Samuel, W. M. (1998). Pests, parasites and diseases. In Ecology and Management of the North American Moose (ed. Franzmann, A. W. and Schwartz, C. C.), pp. 479–517. Smithsonian Institution, Washington, DC.Google Scholar
Lankester, M. W., Peterson, W. and Ogunremi, O. (2007). Diagnosing Parelaphostrongylosis in moose (Alces alces). Alces 43, 49–59.Google Scholar
Laursen, J. R., Averback, G. A. and Conboy, G. A. (1989). Preliminary survey of pulmonate snails in central Minnesota. Minnesota Department of Natural Resources, St. Paul, MN, USA.Google Scholar
Lenarz, M. S. (2009). A review of the ecology of Parelaphostrongylus tenuis in relation to deer and moose in North America. In Summaries of Wildlife Research Findings (ed. DonCarlos, M. W., Kimmel, R. O., Lawrence, J. S. and Lenarz, M. S.), Minnesota Department of Natural Resources, St. Paul, MN.Google Scholar
Lenarz, M. S. (2011). Population trends of white-tailed deer in the forest zone – 2011. In Status of Wildlife Populations, 2011. Minnesota Department of Natural Resources, St. Paul, MN.Google Scholar
Lenarz, M. S., Wright, R. G., Schrage, M. W. and Edwards, A. J. (2011). Compositional analysis of moose habitat in northeastern Minnesota. Alces 47, 135–149.Google Scholar
Maskey, J. J. (2008). Movements, resource selection, and risk analyses for parasitic disease in an expanding moose population in the northern Great Plains. Vol. Ph.D. University of North Dakota, Grand Forks, ND.Google Scholar
Maze, R. J. and Johnstone, C. (1986). Gastropod intermediate hosts of the meningeal worm Parelaphostrongylus tenuis in Pennsylvania: observations of their ecology. Canadian Journal of Zoology 64, 185–188.Google Scholar
McCann, N. P., Moen, R. A. and Windels, S. K. (In review). Identifying thermal refugia for a cold-adapted mammal facing climate change. Oecologia.Google Scholar
McGraw, A. M., Moen, R. and Overland, L. (2012). Effective temperature differences among cover types in northeast Minnesota. Alces 48, 45–52.Google Scholar
MNDNR (2007). Ecological Classification System. http://www.dnr.state.mn.us/ecs/index/html%3E. Minnesota Department of Natural Resources, St. Paul, MN, USA.Google Scholar
MNDNR (2011). Minnesota Moose Research and Management Plan. Minnesota Department of Natural Resources, St. Paul, MN.Google Scholar
Mulvey, M. and Aho, J. M. (1993). Parasitism and mate competition: liver flukes in white-tailed deer. Oikos 66, 187–192.Google Scholar
Mulvey, M., Aho, J. M., Lydeard, C., Leberg, P. L. and Smith, M. H. (1991). Comparative population genetic structure of a parasite (Fascioloides magna) and its definitive host. Evolution 45, 1628–1640.Google Scholar
Mulvey, M., Aho, J. M. and Rhodes, O. E. (1994). Parasitism and white-tailed deer: timing and components of female reproduction. Oikos 70, 177–182.CrossRefGoogle Scholar
Murray, D. L., Cox, E. W., Ballard, W. B., Whitlaw, H. A., Lenarz, M. S., Custer, T. W., Barnett, T. and Fuller, T. K. (2006). Pathogens, nutritional deficiency, and climate influences on a declining moose population. Wildlife Monographs 166, 1–30.Google Scholar
Nankervis, P. J., Samuel, W. M., Schmitt, S. M. and Sikarskie, J. G. (2000). Ecology of meningeal worm, P. tenuis (Nematoda), in white-tailed deer and terrestrial gastropods of Michigan's Upper Peninsula with implications for moose. Alces 36, 163–181.Google Scholar
Olson, B., Windels, S. K., Fulton, M. and Moen, R. (2014). Fine-scale temperature patterns in the southern boreal forest: implications for the cold-adapted moose. Alces 50, 105–120.Google Scholar
Ostfeld, R. S., Glass, G. E. and Keesing, F. (2005). Spatial epidemiology: an emerging (or re-emerging) discipline. Trends in Ecology and Evolution 20, 328–336.Google Scholar
Peterson, W. J. and Lankester, M. W. (1991). Aspects of the epizootiology of Parelaphostrongylus tenuis in a white-tailed deer population. Alces 27, 183–192.Google Scholar
Peterson, W. J., Lankester, M. W. and Riggs, M. R. (1996). Seasonal and annual changes in shedding of Parelaphostrongylus tenuis larvae by white-tailed deer in northeastern Minnesota. Alces 32, 61–74.Google Scholar
Peterson, W. J., Lankester, M. W., Kie, J. G. and Bowyer, R. T. (2013). Geospatial analysis of giant liver flukes among moose: effects of white-tailed deer. Acta Theriologica 58, 359–365.Google Scholar
Pickles, R. A., Thornton, D., Feldman, R., Marques, A. and Murray, D. L. (2013). Predicting shifts in parasite distribution with climate change: a multitrophic level approach. Global Change Biology 19, 2646–2654.Google Scholar
Prior, D. J. (1985). Water-regulatory behaviour in terrestrial gastropods. Biological Reviews 60, 403–424.Google Scholar
Pybus, M. J. (2001). Liver flukes. In Parasitic Diseases of Wild Mammals (ed. Samuel, W. M., Pybus, M. J. and Kocan, A. A.), pp. 121–149. Iowa State University Press, Ames.Google Scholar
Raskevitz, R. F., Kocan, A. A. and Shaw, J. H. (1991). Gastropod availability and habitat utilization by wapiti and white-tailed deer sympatric on range enzootic for meningeal worm. Journal of Wildlife Diseases 27, 92–101.CrossRefGoogle ScholarPubMed
Rowe, R. J. (1978). The incidence of Parelaphostrongylus tenuis and other helminth parasites in cervids of Voyageurs National Park 1977–1978. Contract No. PX 6000–8–0218. In Rainy River Community College.Google Scholar
Schwab, F. E. and Pitt, M. D. (1991). Moose selection of canopy cover types related to operative temperature, forage, and snow depth. Canadian Journal of Zoology 69, 3071–3077.Google Scholar
Shostak, A. W. and Samuel, W. M. (1984). Moisture and temperature effects on survival and infectivity of first-state larvae of Parelaphostrongylus odocoilei and P. tenuis (Nematoda: Metastrongyloidea). Journal of Parasitology 70, 262–269.Google Scholar
Suhardono, , Roberts, J. A. and Copeman, D. B. (2006). The effect of temperature and humidity on longevity of metacercariae of Fasciola gigantica . Tropical Animal Health and Production 38, 371–377.Google Scholar
Swales, W. E. (1935). The life cycle of Fascioloides magna (Bassi, 1875), the large liver fluke of ruminants, in Canada. Canadian Journal of Research, 12, 177–215.CrossRefGoogle Scholar
Thompson, I. D., Flannigan, M. D., Wotton, B. M. and Suffling, R. (1998). The effects of climate change on landscape diversity: an example in Ontario. Environmental Monitoring and Assessment 49, 213–233.Google Scholar
Thomson, M. C., Obsomer, V., Dunne, M., Connor, S. J. and Molyneux, D. H. (2000). Satellite mapping of Loa loa prevalence in relation to ivermectin use in west and central Africa. Lancet 356, 1077–1078.Google Scholar
Wasel, S. M., Samuel, W. M. and Crichton, V. (2003). Distribution and ecology of meningeal worm, Parelaphostrongylus tenuis (Nematoda), in northcentral North America. Journal of Wildlife Diseases 39, 338–346.Google Scholar
Whitlaw, H. A. and Lankester, M. W. (1994). A retrospective evaluation of the effects of Parelaphostrongylosis on moose populations. Canadian Journal of Zoology 72, 1–7.Google Scholar
Windels, S. K. (2014). Voyageurs National Park moose population survey report, Natural Resource Data Series NPS/VOYA/NRDS—2014/645. National Park Service, Fort Collins, CO.Google Scholar
Wünschmann, A., Armien, A. G., Butler, E., Schrage, M., Stromberg, B., Bender, J. B., Firshman, A. M. and Carstensen, M. (In press). Necropsy findings in 62 opportunistically collected free-ranging moose (Alces alces) from Minnesota, USA (2003–2013). Journal of Wildlife Diseases. Online advanced access: http://dx.doi.org/10.7589/2014-02-037 Google Scholar