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Seasonal and biogeographical patterns of gastrointestinal parasites in large carnivores: wolves in a coastal archipelago

  • HEATHER M. BRYAN (a1) (a2) (a3), CHRIS T. DARIMONT (a2) (a4), JANET E. HILL (a5), PAUL C. PAQUET (a2) (a6), R. C. ANDREW THOMPSON (a7), BRENT WAGNER (a5) and JUDIT E. G. SMITS (a1) (a3)...

Parasites are increasingly recognized for their profound influences on individual, population and ecosystem health. We provide the first report of gastrointestinal parasites in gray wolves from the central and north coasts of British Columbia, Canada. Across 60 000 km2, wolf feces were collected from 34 packs in 2005–2008. At a smaller spatial scale (3300 km2), 8 packs were sampled in spring and autumn. Parasite eggs, larvae, and cysts were identified using standard flotation techniques and morphology. A subset of samples was analysed by PCR and sequencing to identify tapeworm eggs (n=9) and Giardia cysts (n=14). We detected ⩾14 parasite taxa in 1558 fecal samples. Sarcocystis sporocysts occurred most frequently in feces (43·7%), followed by taeniid eggs (23·9%), Diphyllobothrium eggs (9·1%), Giardia cysts (6·8%), Toxocara canis eggs (2·1%), and Cryptosporidium oocysts (1·7%). Other parasites occurred in ⩽1% of feces. Genetic analyses revealed Echinococcus canadensis strains G8 and G10, Taenia ovis krabbei, Diphyllobothrium nehonkaiense, and Giardia duodenalis assemblages A and B. Parasite prevalence differed between seasons and island/mainland sites. Patterns in parasite prevalence reflect seasonal and spatial resource use by wolves and wolf-salmon associations. These data provide a unique, extensive and solid baseline for monitoring parasite community structure in relation to environmental change.

Corresponding author
*Corresponding author: Department of Ecosystem and Public Health, University of Calgary, 3280 Hospital Drive NW, Alberta T2N 4N1, Canada. Tel: +403 210 7869. Fax: +403 210 9740. E-mail:
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Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467484. doi: 10.1111/j.1461-0248.2005.00879.x.
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403410. doi: 10.1016/S0022-2836(05)80360-2.
Arizono, N., Shedko, M., Yamada, M., Uchikawa, R., Tegoshi, T., Takeda, K. and Hashimoto, K. (2009). Mitochondrial DNA divergence in populations of the tapeworm Diphyllobothrium nihonkaiense and its phylogenetic relationship with Diphyllobothrium klebanovskii. Parasitology International 58, 2228.
Bagrade, G., Kirjusina, M., Vismanis, K. and Ozolins, J. (2009). Helminth parasites of the wolf Canis lupus from Latvia. Journal of Helminthology 83, 6368. doi: 10.1017/s0022149x08123860.
Biek, R. and Real, L. A. (2010). The landscape genetics of infectious disease emergence and spread. Molecular Ecology 19, 35153531. doi: 10.1111/j.1365-294X.2010.04679.x.
Booth, A. J., Stogdale, L. and Grigor, J. A. (1984). Salmon poisoning disease in dogs on southern Vancouver Island. Canadian Veterinary Journal 25, 26.
Bowles, J. and McManus, D. P. (1993). NADH dehydrogenase 1 gene sequences compared for species and strains of the genus Echinococcus. International Journal for Parasitology 23, 969972. doi: 10.1016/0020-7519(93)90065-7.
Bryan, H. M., Sim, K. A., Darimont, C. T., Paquet, P. C., Wagner, B. W., Muñoz-Fuentes, V., Smits, J. E. and Chilton, N. B. (2010). Identification of Parelaphostrongylus odocoilei (Nematoda: Protostrongylidae) first-stage larvae in the feces of gray wolves (Canis lupis) by molecular methods. Journal of Wildlife Diseases 46, 297302.
Bush, A. O. and Lotz, J. M. (2000). The ecology of “crowding”. Journal of Parasitology 86, 212213. doi: 10.1645/0022-3395(2000)086[0212:TEOC]2.0.CO;2.
Conlan, J. V., Vongxay, K., Fenwick, S., Blacksell, S. D. and Thompson, R. C. A. (2009). Does interspecific competition have a moderating effect on Taenia solium transmission dynamics in Southeast Asia? Trends in Parasitology 25, 398403. doi: 10.1016/
Covacin, C., Aucoin, D., Elliot, A. and Thompson, R. (2011). Genotypic characterisation of Giardia from domestic dogs in the USA. Veterinary Parasitology 177, 2832.
Craig, H. L. and Craig, P. S. (2005). Helminth parasites of wolves (Canis lupus): a species list and an analysis of published prevalence studies in Nearctic and Palaearctic populations. Journal of Helminthology 79, 95103. doi: 10.1079/joh2005282.
Darimont, C., Paquet, P. and Reimchen, T. (2008 a). Spawning salmon disrupt trophic coupling between wolves and ungulate prey in coastal British Columbia. BMC Ecology 8, 14. doi: 10.1186/1472-6785-8-14.
Darimont, C. T., Paquet, P. C. and Reimchen, T. E. (2009). Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate. Journal of Animal Ecology 78, 126133. doi: 10.1111/j.1365-2656.2008.01473.x.
Darimont, C. T., Paquet, P. C., Reimchen, T. E. and Crichton, V. (2005). Range expansion by moose into coastal temperate rainforests of British Columbia, Canada. Diversity and Distributions 11, 235239. doi: 10.1111/j.1366-9516.2005.00135.x.
Darimont, C. T., Price, M. H. H., Winchester, N. N., Gordon-Walker, J. and Paquet, P. C. (2004). Predators in natural fragments: foraging ecology of wolves in British Columbia's central and north coast archipelago. Journal of Biogeography 31, 18671877. doi: 10.1111/j.1365-2699.2004.01141.x.
Darimont, C. T., Reimchen, T. E., Bryan, H. M. and Paquet, P. C. (2008 b). Faecal-centric approaches to wildlife ecology and conservation; methods, data and ethics. Wildlife Biology in Practice 4, 7387.
Darimont, C. T., Reimchen, T. E. and Paquet, P. C. (2003). Foraging behaviour by gray wolves on salmon streams in coastal British Columbia. Canadian Journal of Zoology 81, 349353. doi: 10.1139/z02-246.
Daszak, P. (2000). Emerging infectious diseases of wildlife – Threats to biodiversity and human health. Science 287, 443449. doi: 10.1126/science.287.5452.443.
Despommier, D., Ellis, B. and Wilcox, B. (2006). The role of ecotones in emerging infectious diseases. EcoHealth 3, 281289. doi: 10.1007/s10393-006-0063-3.
Dubey, J. P. and Odening, K. (2001). Toxoplasmosis and related infections. In Parasitic Diseases of Wild Mammals, 2nd Edn (ed. Samuel, W. D., Pybus, M. J. and Kocan, A. A.), pp. 478519. Iowa State University Press, Ames, Iowa.
Foreyt, W. J. (1989). Diagnostic parasitology. Veterinary Clinics of North America Small Animal Practice 19, 9791000.
Foreyt, W. J. (2001 a). Salmon poisoning disease. In Infectious Diseases of Wild Mammals, 3rd Edn (ed. Williams, E. S. and Barker, I. K.), pp. 480486. Blackwell Publishing, Ames, Iowa, USA.
Foreyt, W. J. (2001 b). Veterinary Parasitology Reference Manual, 5th Edn. Blackwell Publishing Professional, Ames, Iowa, USA.
Foreyt, W. J., Drew, M. L., Atkinson, M. and McCauley, D. (2009). Echinococcus granulosus in gray wolves and ungulates in Idaho and Montana, USA. Journal of Wildlife Diseases 45, 12081212.
Frechette, J. L. (1978). Seasonal changes in the prevalence of ova of Diphyllobothrium ursi and Baylisascaris transfuga in the feces of the black bear (Ursus americanus). Journal of Wildlife Diseases 14, 342344.
Gau, R. J., Kutz, S. and Elkin, B. T. (1999). Parasites in grizzly bears from the central Canadian arctic. Journal of Wildlife Diseases 35, 618621.
Gentes, M.-L., Whitworth, T. L., Waldner, C., Fenton, H. and Smits, J. E. (2007). Tree swallows (Tachycineta bicolor) nesting on wetlands impacted by oil sands mining are highly parasitized by the bird blow fly Protocalliphora spp. Journal of Wildlife Diseases 43, 167178.
Giraudoux, P., Craig, P. S., Delattre, P., Bao, G., Bartholomot, B., Harraga, S., Quere, J. P., Raoul, F., Wang, Y., Shi, D. and Vuitton, D. A. (2003). Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitology 127, S121S131. doi: 10.1017/s0031182003003512.
Goüy de Bellocq, J., Sarà, M., Casanova, J. C., Feliu, C. and Morand, S. (2003). A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitology Research 90, 6470. doi: 10.1007/s00436-002-0806-1.
Greer, A., Ng, V. and Fisman, D. (2008). Climate change and infectious diseases in North America: the road ahead. Canadian Medical Association Journal 178, 715722. doi: 10.1503/cmaj.081325.
Hildreth, M. B., Blunt, D. S. and Oaks, J. A. (2004). Lethal effects of freezing Echinococcus multilocularis eggs at ultralow temperatares. Journal of Parasitology 90, 841844. doi: 10.1645/GE-221R.
Himsworth, C. G., Jenkins, E., Hill, J. E., Nsungu, M., Ndao, M., Andrew Thompson, R. C., Covacin, C., Ash, A., Wagner, B. A., McConnell, A., Leighton, F. A. and Skinner, S. (2010). Emergence of sylvatic Echinococcus granulosus as a parasitic zoonosis of public health concern in an indigenous community in Canada. American Journal of Tropical Medicine and Hygiene 82, 643645. doi: 10.4269/ajtmh.2010.09-0686.
Hudson, P. J., Dobson, A. P. and Lafferty, K. D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends in Ecology & Evolution 21, 381385. doi: 10.1016/j.tree.2006.04.007.
Jenkins, D. J., Romig, T. and Thompson, R. C. A. (2005). Emergence/re-emergence of Echinococcus spp. – a global update. International Journal for Parasitology 35, 12051219. doi: 10.1016/j.ijpara.2005.07.014.
Jolles, A. E., Etienne, R. S. and Olff, H. (2006). Independent and competing disease risks: implications for host populations in variable environments. American Naturalist 167, 745757. doi: 10.1086/503055.
Jones, A. and Pybus, M. J. (2001). Taeniasis and Echinococcosis. In Parasitic diseases of Wild Mammals, 2nd Edn (ed. Samuel, W. M., Pybus, M. J. and Kocan, A. A.), pp. 150192. Iowa State University Press, Ames, Iowa, USA.
Kreeger, T. J. (2003). The internal wolf: physiology, pathology, and pharmacology. In Wolves: Behaviour, Ecology, and Conservation. (ed. Mech, L. D. and Boitani, L.), pp. 192217. The University of Chicago Press, Chicago, IL, USA.
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 272, 25712576. doi: 10.1098/rspb.2005.3285.
Lasek-Nesselquist, E., Bogomolni, A., Gast, R., Welch, D., Ellis, J., Sogin, M. and Moore, M. (2008). Molecular characterization of Giardia intestinalis haplotypes in marine animals: variation and zoonotic potential. Diseases of Aquatic Organisms 81, 3951. doi: 10.3354/dao01931.
McManus, D. P., Zhang, L. H., Castrodale, L. J., Le, T. H., Pearson, M. and Blair, D. (2002). Short report: Molecular genetic characterization of an unusually severe case of hydatid disease in Alaska caused by the cervid strain of Echinococcus granulosus. American Journal of Tropical Medicine and Hygiene 67, 296298.
Mech, D. L. (1970). The Wolf: The Ecology and Behavior of an Endangered Species, University of Minnesota Press, Minneapolis, USA.
Messier, F., Rau, M. E. and McNeill, M. A. (1989). Echinococcus granulosus (Cestoda, Taeniidae) infections and moose-wolf population dynamics in southwestern Quebec. Canadian Journal of Zoology 67, 216219.
Muñoz-Fuentes, V., Darimont, C. T., Wayne, R. K., Paquet, P. C. and Leonard, J. A. (2009). Ecological factors drive differentiation in wolves from British Columbia. Journal of Biogeography 36, 15161531. doi: 10.1111/j.1365-2699.2008.02067.x.
Nieberding, C., Morand, S., Libois, R. and Michaux, J. R. (2006). Parasites and the island syndrome: the colonization of the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845). Journal of Biogeography 33, 12121222. doi: 10.1111/j.1365-2699.2006.01503.x.
Paquet, P. C., Alexander, S. M., Swan, P. L. and Darimont, C. T. (2006). Influence of natural landscape fragmentation and resource availability on distribution and connectivity of gray wolves (Canis lupus) in the archipelago of coastal British Columbia, Canada. In Connectivity Conservation. Conservation Biology Book Series (ed. Crooks, K. R. and Sanjayan, M. A.), pp. 130156. Cambridge University Press, Cambridge, UK.
Pinch, L. W. and Wilson, J. F. (1973). Non-surgical management of cystic hydatid disease in Alaska – review of 30 cases of Echinococcus granulosus infection treated without operation. Annals of Surgery 178, 4548.
Price, K., Roburn, A. and MacKinnon, A. (2009). Ecosystem-based management in the Great Bear Rainforest. Forest Ecology and Management 258, 495503. doi: 10.1016/j.foreco.2008.10.010.
Read, C. P. (1951). The crowding effect in tapeworm infections. Journal of Parasitology 37, 174178.
Roberts, L. S. (2000). The crowding effect revisited. The Journal of Parasitology 86, 209211. doi: 10.1645/0022-3395(2000)086[0209:TCER]2.0.CO;2.
Scholz, T., Garcia, H. H., Kuchta, R. and Wicht, B. (2009). Update on the Human Broad Tapeworm (Genus Diphyllobothrium), including clinical relevance. Clinical Microbiology Reviews 22, 146160. doi: 10.1128/cmr.00033-08.
Stien, A., Voutilainen, L., Haukisalmi, V., Fugelei, E., Mørk, T., Yoccoz, N. G., Ims, R. A. and Henttonen, H. (2010). Intestinal parasites of the Arctic fox in relation to the abundance and distribution of intermediate hosts. Parasitology 137, 149157. doi: doi:10.1017/S0031182009990953.
Stronen, A. V., Sallows, T., Forbes, G. J., Wagner, B. and Paquet, P. C. (2011). Diseases and parasites in wolves of the Riding Mountain National Park Region, Manitoba, Canada. Journal of Wildlife Diseases 47, 222227.
Telfer, S., Lambin, X., Birtles, R., Beldomenico, P., Burthe, S., Paterson, S. and Begon, M. (2010). Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243246. doi: 10.1126/science.1190333.
Thompson, R. C. A. (2004). The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Veterinary Parasitology 126, 1535. doi: 10.1016/j.vetpar.2004.09.008.
Thompson, R. C. A. (2008). The taxonomy, phylogeny and transmission of Echinococcus. Experimental Parasitology 119, 439446. doi: 10.1016/j.exppara.2008.04.016.
Thompson, R. C. A., Boxell, A. C., Ralston, B. J., Constantine, C. C., Hobbs, R. P., Shury, T. and Olson, M. E. (2006). Molecular and morphological characterization of Echinococcus in cervids from North America. Parasitology 132, 439447. doi: 10.1017/S0031182005009170.
Turner, W. C. and Getz, W. M. (2010). Seasonal and demographic factors influencing gastrointestinal parasitism in ungulates of Etosha National Park. Journal of Wildlife Diseases 46, 11081119.
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