Helminths of grizzly bears (Ursus arctos) and American black bears (Ursus americanus) in Alberta and British Columbia, Canada
Abstract
Between May 2011 and June 2013, we collected the carcasses and gastrointestinal tracts of 40 American black bears (Ursus americanus Pallas, 1780) and 13 grizzly bears (Ursus arctos L., 1758) from populations of Alberta and British Columbia, Canada. Specimens were examined for helminths, which were identified to the species level by applying an integrated morphological and molecular approach. Our goal was to investigate parasite biodiversity and infection parameters in the sampled grizzly and black bears. We found seven parasite taxa: Dirofilaria ursi Yamaguti, 1941, Baylisascaris transfuga (Rudolphi, 1819), Uncinaria rauschi Olsen, 1968, Uncinaria yukonensis (Wolfgang, 1956), Taenia arctos Haukisalmi, Lavikainen, Laaksonen and Meri, 2011, Diphyllobothrium dendriticum (Nitzsch, 1824), and Diphyllobothrium nihonkaiense Yamane, Kamo, Bylund and Wikgren, 1986. The statistical significance of infection prevalence, intensity, and abundance for each helminth species was assessed relative to host species, gender, age class, sampling season, and location. This is the first unequivocal report of the potentially zoonotic tapeworms D. dendriticum and D. nihonkaiense in North American bears. Furthermore, we provide insight into the biology and ecology of the nematodes B. transfuga, D. ursi, and species of Uncinaria Frölich, 1789, and enrich the information available on the recently described tapeworm T. arctos.
Résumé
De mai 2011 à juin 2013, nous avons recueilli les carcasses et tubes digestifs de 40 ours noirs (Ursus americanus Pallas, 1780) et de 13 grizzlis (Ursus arctos L., 1758) de populations de l’Alberta et de la Colombie-Britannique (Canada). Les spécimens ont été examinés pour vérifier la présence d’helminthes, qui ont été identifiés au niveau de l’espèce en utilisant une approche morphologique et moléculaire intégrée. L’objectif de ces travaux consistait en l’étude de la biodiversité des parasites et des paramètres d’infection dans les grizzlis et ours noirs échantillonnés. Nous avons trouvé les sept taxons de parasites suivants : Dirofilaria ursi Yamaguti, 1941, Baylisascaris transfuga (Rudolphi, 1819), Uncinaria rauschi Olsen, 1968, Uncinaria yukonensis (Wolfgang, 1956), Taenia arctos Haukisalmi, Lavikainen, Laaksonen et Meri, 2011, Diphyllobothrium dendriticum (Nitzsch, 1824) et Diphyllobothrium nihonkaiense Yamane, Kamo, Bylund et Wikgren, 1986. La signification statistique de la prévalence, de l’intensité et de l’abondance des infections pour chaque espèce d’helminthe a été évaluée en fonction de l’espèce hôte, du sexe, de la classe d’âge, de la saison d’échantillonnage et de l’emplacement. Il s’agit du premier signalement non équivoque des ténias potentiellement zoonotiques D. dendriticum et D. nihonkaiense chez des ours nord-américains. Nous jetons de plus un nouvel éclairage sur la biologie et l’écologie des nématodes B. transfuga, D. ursi et d’espèces d’Uncinaria Frölich, 1789, et ajoutons à l’information disponible sur le ténia T. arctos décrit récemment. [Traduit par la Rédaction]
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References
Addison E.M. 1980. Transmission of Dirofilaria ursi Yamaguti, 1941 (Nematoda: Onchocercidae) of black bears (Ursus americanus) by blackflies (Simuliidae). Can. J. Zool. 58(10): 1913–1922.
Addison E.M., Pybus M.J., and Rietveld H.J. 1978. Helminth and arthropod parasites of black bear, Ursus americanus, in central Ontario. Can. J. Zool. 56(10): 2122–2126.
Andersen K., Ching H.L., and Vik R. 1987. A review of freshwater species of Diphyllobothrium with redescriptions and the distribution of D. dendriticum (Nitzsch, 1824) and D. ditremum (Creplin, 1825) from North America. Can. J. Zool. 65(9): 2216–2228.
Anderson, R.C. 2000. Nematode parasites of vertebrates: their development and transmission. 2nd ed. CABI, Wallingford, UK.
Arizono N., Shedko M., Yamada M., Uchikawa R., Tegoshi T., Takeda K., and Hashimoto K. 2009a. Mitochondrial DNA divergence in populations of the tapeworm Diphyllobothrium nihonkaiense and its phylogenetic relationship with Diphyllobothrium klebanovskii. Parasitol. Int. 58(1): 22–28.
Arizono N., Yamada M., Nakamura-Uchiyama F., and Ohnishi K. 2009b. Diphyllobothriasis associated with eating raw Pacific salmon. Emerg. Infect. Dis. 15(6): 866–870.
Beaver P.C., Wolfson J.S., Waldron M.A., Swartz M.N., Evans G.W., and Adler J. 1987. Dirofilaria ursi-like parasites acquired by humans in the northern United States and Canada: report of two cases and brief review. Am. J. Trop. Med. Hyg. 37(2): 357–362.
Bowles J., Blair D., and McManus D.P. 1992. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol. Biochem. Parasitol. 54(2): 165–173.
Bryan H.M., Darimont C.T., Hill J.E., Paquet P.C., Thompson R.C., Wagner B., and Smits J.E. 2012. Seasonal and biogeographical patterns of gastrointestinal parasites in large carnivores: wolves in a coastal archipelago. Parasitology, 139(6): 781–790.
Catalano, S. 2014. Morphological and molecular insights into the biodiversity of gastrointestinal parasites from Canadian grizzly (Ursus arctos horribilis) and black bears (Ursus americanus). M.Sc. thesis, Faculty of Veterinary Medicine, University of Calgary, Calgary, Alta. Available from http://hdl.handle.net/11023/1403 [accessed 15 September 2015].
Catalano S., Lejeune M., Verocai G.G., and Duignan P.J. 2014. First report of Taenia arctos (Cestoda: Taeniidae) from grizzly (Ursus arctos horribilis) and black bears (Ursus americanus) in North America. Parasitol. Int. 63(2): 389–391.
Catalano S., Lejeune M., van Paridon B., Pagan C.A., Wasmuth J.D., Tizzani P., Duignan P.J., and Nadler S.A. 2015. Morphological variability and molecular identification of Uncinaria spp. (Nematoda: Ancylostomatidae) from grizzly and black bears: new species or phenotypic plasticity? J. Parasitol. 101(2): 182–192.
Choquette L.P.E., Gibson G.G., and Pearson A.M. 1969. Helminths of the grizzly bear, Ursus arctos L., in northern Canada. Can. J. Zool. 47(2): 167–170.
Cleaveland, S., Hess, G.R., Dobson, A.P., Laurenson, M.K., McCallum, H.I., Roberts, M., and Woodroffe, R. 2002. The role of pathogens in biological conservation. In The ecology of wildlife diseases. Edited by P.J. Hudson, A. Rizzoli, B.T. Grenfell, H. Heesterbeek, and A.P. Dobson. Oxford University Press, Oxford. pp. 139–150.
COSEWIC. 2012. COSEWIC assessment and status report on the grizzly bear Ursus arctos in Canada. Committee on the Status of Endangered Wildlife in Canada, Ottawa, Ont. Available from http://www.sararegistry.gc.ca/virtual_sara/files/cosewic/sr_ours_grizz_bear_1012_e.pdf [accessed 15 September 2015].
de Vos T., Szalai A.J., and Dick T.A. 1990. Genetic and morphological variability in a population of Diphyllobothrium dendriticum (Nitzsch, 1824). Syst. Parasitol. 16(2): 99–105.
Dick T.A., Nelson P.A., and Choudhury A. 2001. Diphyllobothriasis: update on human cases, foci, patterns and sources of human infections and future considerations. Southeast Asian J. Trop. Med. Public Health, 32(2): 59–76.
Dies K.H. 1979. Helminths recovered from black bears in the Peace River Region of northwestern Alberta. J. Wildl. Dis. 15(1): 49–50.
Duffy M.S., Greaves T.A., and Burt M.D.B. 1994. Helminths of the black bear, Ursus americanus, in New Brunswick. J. Parasitol. 80(3): 478–480.
Festa-Bianchet, M. 2010. Status of the grizzly bear (Ursus arctos) in Alberta: update 2010. Alberta Environment and Sustainable Resource Development, Government of Alberta, Edmonton, Report No. 37. Available from http://esrd.alberta.ca/fish-wildlife/species-at-risk/species-at-risk-publications-web-resources/mammals/documents/SAR-StatusGrizzlyBearAlbertaUpdate2010-Feb2010.pdf [accessed 15 September 2015].
Foster G.W., Cunningham M.W., Kinsella J.M., and Forrester D.J. 2004. Parasitic helminths of black bear cubs (Ursus americanus) from Florida. J. Parasitol. 90(1): 173–175.
Frechette J.-L. and Rau M.E. 1977. Helminths of the black bear in Quebec. J. Wildl. Dis. 13(4): 432–434.
Frechette J.-L. and Rau M.E. 1978. Seasonal changes in the prevalence of ova of Diphyllobothrium ursi and Baylisascaris transfuga in the feces of the black bear (Ursus americanus). J. Wildl. Dis. 14(3): 342–344.
Gau R.J., Kutz S., and Elkin B.T. 1999. Parasites in grizzly bears from the Central Canadian Arctic. J. Wildl. Dis. 35(3): 618–621.
Gulland F.M.D. 1992. The role of nematode parasites in Soay sheep (Ovis aries L.) mortality during a population crash. Parasitology, 105(3): 493–503.
Hair J.D. and Mahrt J.L. 1970. Eimeria albertensis n. sp. and E. borealis n. sp. (Sporozoa: Eimeridae) in black bears Ursus americanus from Alberta. J. Protozool. 17(4): 663–664.
Haldane D.J., Johnston B.L., and Walsh N.M. 1996. Subcutaneous dirofilariasis in Nova Scotia. Can. J. Infect. Dis. 7(1): 67–69.
Haukisalmi V., Lavikainen A., Laaksonen S., and Meri S. 2011. Taenia arctos n. sp. (Cestoda: Cyclophyllidea: Taeniidae) from its definitive (brown bear Ursus arctos Linnaeus) and intermediate (moose/elk Alces spp.) hosts. Syst. Parasitol. 80(3): 217–230.
Hilderbrand G.V., Schwartz C.C., Robbins C.T., Jacoby M.E., Hanley T.A., Arthur S.M., and Servheen C. 1999. The importance of meat, particularly salmon, to body size, population productivity, and conservation of North American brown bears. Can. J. Zool. 77(1): 132–138.
Hoberg E.P. and Brooks D.R. 2015. Evolution in action: climate change, biodiversity dynamics and emerging infectious diseases. Philos. Trans. R. Soc. B Biol. Sci. 370(1665): 20130553.
Hristienko H. and McDonald J.E. 2007. Going into the 21st century: a perspective on trends and controversies in the management of the American black bear. Ursus, 18(1): 72–88.
Johnson, D., Larter, N.C., Elkin, B., and Allaire, D.G. 2013. An opportunistic parasitological and serological examination of nuisance black bears in the Dehcho region of the Northwest Territories. Department of Environment and Natural Resources, Government of the Northwest Territories, Yellowknife, N.W.T., Report No. 227. Available from http://www.enr.gov.nt.ca/sites/default/files/227_manuscript.pdf [accessed 15 September 2015].
Jonkel C.J. and Cowan I.M. 1971. The black bear in the spruce–fir forest. Wildl. Monogr. 27: 3–57. Available from http://www.jstor.org/stable/3830521 [accessed 15 September 2015].
Kazacos, K.R. 2001. Baylisascaris procyonis and related species. In Parasitic diseases of wild mammals. 2nd ed. Edited by W.M. Samuel, M.J. Pybus, and A.A. Kocan. Iowa State University Press, Ames. pp. 301–341.
Khalil, L.F., Jones, A., and Bray, R.A. 1994. Keys to the cestode parasites of vertebrates. CABI, Wallingford, UK.
Kuchta R., Brabec J., Kubáčková P., and Scholz T. 2013. Tapeworm Diphyllobothrium dendriticum (Cestoda)—neglected or emerging human parasite? PLoS Negl. Trop. Dis. 7(12): e2535.
Kutz S.J., Ducrocq J., Verocai G.G., Hoar B.M., Colwell D.D., Beckmen K.B., Polley L., Elkin B.T., and Hoberg E.P. 2012. Parasites in ungulates of Arctic North America and Greenland: a view of contemporary diversity, ecology, and impact in a world under change. Adv. Parasitol. 79: 99–252.
Lavikainen A., Laaksonen S., Beckmen K., Oksanen A., Isomursu M., and Meri S. 2011. Molecular identification of Taenia spp. in wolves (Canis lupus), brown bears (Ursus arctos) and cervids from North Europe and Alaska. Parasitol. Int. 60(3): 289–295.
Michalski M.L., Bain O., Fischer K., Fischer P.U., Kumar S., and Foster J.M. 2010. Identification and phylogenetic analysis of Dirofilaria ursi (Nematoda: Filarioidea) from Wisconsin black bears (Ursus americanus) and its Wolbachia endosymbiont. J. Parasitol. 96(2): 412–419.
Mowat G., Heard D.C., Seip D.R., Poole K.G., Stenhouse G., and Paetkau D.W. 2005. Grizzly Ursus arctos and black bear U. americanus densities in the interior mountains of North America. Wildl. Biol. 11(1): 31–48.
Munro R.H.M., Nielsen S.E., Price M.H., Stenhouse G.B., and Boyce M.S. 2006. Seasonal and diel patterns of grizzly bear diet and activity in west-central Alberta. J. Mammal. 87(6): 1112–1121.
Nadler S.A., Adams B.J., Lyons E.T., DeLong R.L., and Melin S.R. 2000a. Molecular and morphometric evidence for separate species of Uncinaria (Nematoda: Ancylostomatidae) in California sea lions and northern fur seals: hypothesis testing supplants verification. J. Parasitol. 86(5): 1099–1106.
Nadler S.A., Hoberg E.P., Hudspeth D.S.S., and Rickard L.G. 2000b. Relationships of Nematodirus species and Nematodirus battus isolates (Nematoda: Trichostrongyloidea) based on nuclear ribosomal DNA sequences. J. Parasitol. 86(3): 588–601.
Olsen O.W. 1968. Uncinaria rauschi (Strongyloidea: Nematoda), a new species of hookworms from Alaskan bears. Can. J. Zool. 46(6): 1113–1117.
Pelton, M.R. 2003. Black bear (Ursus americanus). In Wild mammals of North America: biology, management, and conservation. 2nd ed. Edited by G.A. Feldhamer, B.C. Thompson, and J.A. Chapman. Johns Hopkins University Press, Baltimore, Md. pp. 547–555.
Pence D.B., Crum J.M., and Conti J.A. 1983. Ecological analyses of helminth populations in the black bear, Ursus americanus, from North America. J. Parasitol. 69(5): 933–950.
Proctor M.F., McLellan B.N., Strobeck C., and Barclay R.M. 2005. Genetic analysis reveals demographic fragmentation of grizzly bears yielding vulnerably small populations. Proc. R. Soc. B Biol. Sci. 272(1579): 2409–2416.
Proctor M.F., Paetkau D., McLellan B.N., Stenhouse G.B., Kendall K.C., Mace R.D., Kasworm W.F., Servheen C., Lausen C.L., Gibeau M.L., Wakkinen W.L., Haroldson M.A., Mowat G., Apps C.D., Ciarniello L.M., Barclay R.M.R., Boyce M.S., Schwartz C.C., and Strobeck C. 2012. Population fragmentation and inter-ecosystem movements of grizzly bears in western Canada and the northern United States. Wildl. Monogr. 180(1): 1–46.
Rausch R.L. 1961. Notes on the black bear, Ursus americanus Pallas, in Alaska, with particular reference to dentition and growth. Z. Saugetierkd. 26: 65–128.
R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.r-project.org/ [accessed 15 September 2015].
Rogers L.L. 1975. Parasites of black bears of the Lake Superior region. J. Wildl. Dis. 11(2): 189–192.
Rogers, L.L. 1993. The role of habitat quality in the natural regulation of black bear populations. In Proceedings of the Fourth Western Black Bear Workshop, Yosemite National Park, Calif., 2–5 April 1991. Edited by J.A. Keay. Tech. Rep. NPS/NRWR/NRTR-93/12. U.S. Department of the Interior, National Park Service, Natural Resources Publication Office, Denver, Colo. pp. 95-102. Available from http://www.bearstudy.org/website/images/stories/Publications/Role_of_Habitat_Quality_in_the_Natural_Regulation_of_Black_Bear_Populations.pdf [accessed 15 September 2015].
Rogers, L.L., and Rogers, S.M. 1976. Parasites of bears: a review. In Third International Conference on Bear Research and Management, Binghamton, N.Y., USA, and Moscow, USSR, June 1974. Edited by M.R. Pelton, J.W. Lentfer, and G.E. Folk. International Union for Conservation of Nature and Natural Resources, Morges, Switzerland. pp. 411–430. Available from http://www.bearbiology.com/fileadmin/tpl/Downloads/URSUS/Vol_3/Rogers___Rogers_Vol_3.pdf [accessed 15 September 2015].
Rózsa L., Reiczigel J., and Majoros G. 2000. Quantifying parasites in samples of hosts. J. Parasitol. 86(2): 228–232.
Sawaya M.A., Stetz J.B., Clevenger A.P., Gibeau M.L., and Kalinowski S.T. 2012. Estimating grizzly and black bear population abundance and trend in Banff National Park using noninvasive genetic sampling. PloS ONE, 7(5): e34777.
Scholz T., Garcia H.H., Kuchta R., and Wicht B. 2009. Update on the human broad tapeworm (genus Diphyllobothrium), including clinical relevance. Clin. Microbiol. Rev. 22(1): 146–160.
Schwartz, C.C., Miller, S.D., and Haroldson, M.A. 2003. Grizzly bear (Ursus arctos). In Wild mammals of North America: biology, management, and conservation. 2nd ed. Edited by G.A. Feldhamer, B.C. Thompson, and J.A. Chapman. Johns Hopkins University Press, Baltimore, Md. pp. 556–586.
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. J. Anim. Ecol. 71(6): 937–945.
Wicht B., de Marval F., and Peduzzi R. 2007. Diphyllobothrium nihonkaiense (Yamane et al., 1986) in Switzerland: first molecular evidence and case reports. Parasitol. Int. 56(3): 195–199.
Wicht B., Scholz T., Peduzzi R., and Kuchta R. 2008. First record of human infection with the tapeworm Diphyllobothrium nihonkaiense in North America. Am. J. Trop. Med. Hyg. 78(2): 235–238.
Wolfgang R.W. 1956. Dochmoides yukonensis sp. nov. from the brown bear (Ursus americanus) in the Yukon. Can. J. Zool. 34(1): 21–27.
Zhang J.S., Daszak P., Huang H.L., Yang G.Y., Kilpatrick A.M., and Zhang S. 2008. Parasite threat to panda conservation. EcoHealth, 5(1): 6–9.
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Published In
Canadian Journal of Zoology
Volume 93 • Number 10 • October 2015
Pages: 765 - 772
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Received: 18 March 2015
Accepted: 24 June 2015
Accepted manuscript online: 23 July 2015
Version of record online: 23 July 2015
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S. Catalano, M. Lejeune, P. Tizzani, G.G. Verocai, H. Schwantje, C. Nelson, and P.J. Duignan. 2015. Helminths of grizzly bears (Ursus arctos) and American black bears (Ursus americanus) in Alberta and British Columbia, Canada. Canadian Journal of Zoology. 93(10): 765-772. https://doi.org/10.1139/cjz-2015-0063