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Helminth parasites and zoonotic risk associated with urban coyotes (Canis latrans) in Alberta, Canada

Published online by Cambridge University Press:  27 December 2018

L.T. Luong Open the ORCID record for L.T. Luong [Opens in a new window] ,
J.L. Chambers ,
A. Moizis ,
T.M. Stock  and
C.C. St. Clair Open the ORCID record for C.C. St. Clair [Opens in a new window]
L.T. Luong*
Affiliation:
Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada
J.L. Chambers
Affiliation:
Department of Biological Studies, MacEwan University, Edmonton, Alberta, Canada
A. Moizis
Affiliation:
Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada
T.M. Stock
Affiliation:
Department of Biological Studies, MacEwan University, Edmonton, Alberta, Canada
C.C. St. Clair
Affiliation:
Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada
*
Author for correspondence: L.T. Luong E-mail: [email protected]
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Abstract

Coyotes (Canis latrans) are resilient, adaptable, cosmopolitan omnivores that are increasingly prevalent in urban environments, where they interact with both humans and domestic dogs. Coyotes potentially transmit zoonotic parasites, including the tapeworm Echinococcus multilocularis, which appears to be increasing in prevalence in western North America. In this study, we analysed the carcasses of 23 urban coyotes in Edmonton, Alberta, Canada. Focusing primarily on the helminth community, we recovered three tapeworm species (E. multilocularis, Taenia pisiformis, T. serialis), four nematodes (Toxascaris leonina, Uncinaria stenocephala, Capillaria sp., Physaloptera sp.), and two trematodes (Alaria arisaemoides and A. americana). Compared to previous studies of urban coyotes conducted in North America, we report one of the highest levels of E. multilocularis infection in North America: 65.2% infection prevalence. These results amplify concerns expressed by others about the increasing prevalence of this zoonotic parasite and the role coyotes may play in parasite transmission. More research is needed to better understand how various ecological factors, urbanization and wildlife management practices influence the transmission of potentially zoonotic parasites such as E. multilocularis.

Keywords

alveolar echinococcosisEchinococcusinfectious diseaseparasite infectionurbanization
Type
Short Communication
Information
Journal of Helminthology , Volume 94 , 2020 , e25
Copyright
Copyright © Cambridge University Press 2018 

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References

Alexander, SM and Quinn, MS (2011) Coyote (Canis latrans) interactions with humans and pets reported in the Canadian print media (1995–2010). Human Dimensions of Wildlife 16, 345–359.Google Scholar
Becker, DJ, Streicker, DG and Altizer, S (2015) Linking anthropogenic resources to wildlife–pathogen dynamics: a review and meta-analysis. Ecology Letters 18, 483–495. doi: 10.1111/ele.12428.Google Scholar
Birnie-Gauvin, K et al. (2016) Sublethal consequences of urban life for wild vertebrates. Environmental Reviews 24, 416–425. doi: 10.1139/er-2016-0029.Google Scholar
Bradley, CA and Altizer, S (2007) Urbanization and the ecology of wildlife diseases. Trends in Ecology & Evolution 22, 95–102. doi: 10.1016/j.tree.2006.11.001.Google Scholar
Catalano, S et al. (2012) Echinococcus multilocularis in urban coyotes, Alberta, Canada. Emerging Infectious Diseases 18, 1625–1628. doi: 10.3201/eid1810.120119.Google Scholar
Craig, PS, Rogan, MT and Allan, JC (1996) Detection, screening and community epidemiology of Taeniid cestode zoonoses: cystic echinococcosis, alveolar echinococcosis and neurocysticercosis. Advances in Parasitology 38, 169–250. doi: 10.1016/s0065-308x(08)60035-4.Google Scholar
Davidson, RK et al. (2012) The impact of globalisation on the distribution of Echinococcus multilocularis. Trends in Parasitology 28, 239–247. doi: 10.1016/j.pt.2012.03.004.Google Scholar
Deplazes, P et al. (2004) Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends in Parasitology 20, 77–84. doi: 10.1016/j.pt.2003.11.011.Google Scholar
Dow, C et al. (1961) Studies on immunity to Uncinaria stenocephala infection in dog - double vaccination with irradiated larvae. American Journal of Veterinary Research 22, 352–354.Google Scholar
Eckert, J and Deplazes, P (2004) Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clinical Microbiology Reviews 17, 107–135. doi: 10.1128/cmr.17.1.107-135.2004.Google Scholar
Eckert, J et al. (2001) WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. Paris, France: World Organisation for Animal Health and the World Health Organization.Google Scholar
Ezenwa, VO (2004) Interactions among host diet, nutritional status and gastrointestinal parasite infection in wild bovids. International Journal for Parasitology 34, 535–542. doi: 10.1016/j.ijpara.2003.11.012.Google Scholar
FAO/WHO (2014) Multicriteria-Based Ranking for Risk Management of Food-Borne Parasites. Rome, Italy: Food and Agriculture Organizaation of the United Nations/World Health Organization.Google Scholar
Gamble, WG et al. (1979) Alveolar hydatid disease in Minnesota: 1st human case acquired in the contiguous United States. Journal of the American Medical Association 241, 904–907. doi: 10.1001/jama.241.9.904.Google Scholar
Gehrt, SD, Anchor, C and White, LA (2009) Home range and landscape use of coyotes in a metropolitan landscape: conflict or coexistence? Journal of Mammalogy 90, 1045–1057. doi: 10.1644/08-Mamm-a-277.1.Google Scholar
Gesy, K et al. (2013) Establishment of a European-type strain of Echinococcus multilocularis in Canadian wildlife. Parasitology 140, 1133–1137. doi: 10.1017/s0031182013000607.Google Scholar
Hildreth, MB et al. (2000) Failure to identify alveolar echinococcosis in trappers from South Dakota in spite of high prevalence of Echinococcus multilocularis in wild canids. Journal of Parasitology 86, 75–77.Google Scholar
Holmes, JC, Mahrt, JL and Samuel, WM (1971) Occurrence of Echinococcus multilocularis Leuckart, 1863 in Alberta. Canadian Journal of Zoology 49, 575–576. doi: 10.1139/z71-090.Google Scholar
James, E and Boyd, W (1937) Echinococcus alveolaris (with the report of a case). Canadian Medical Association Journal 36, 354–356.Google Scholar
Jenkins, EJ et al. (2012) Detection of European strain of Echinococcus multilocularis in North America. Emerging Infectious Diseases 18, 1010–1012. doi: 10.3201/eid1806.111420.Google Scholar
Jones, A and Pybus, MJ (2008) Taeniasis and Echinococcosis. In Samuel, WM, Pybus, MJ and Kocan, AA (Eds), Parasitic Diseases of Wild Mammals. Ames, IA: Iowa State University Press, pp. 150–192.Google Scholar
Kalkofen, UP (1987) Hookworm of dogs and cats. Veterinary Clinics of North America: Small Animal Practice 17, 1341–1354. doi: 10.1016/s0195-5616(87)50005-5.Google Scholar
Kellner, KF et al. (2012) Effects of urbanization on prevalence of Baylisascaris procyonis in intermediate host populations. Journal of Wildlife Diseases 48, 1083–1087. doi: 10.7589/2011-09-267.Google Scholar
Leiby, PD, Carney, WP and Woods, CE (1970) Studies on sylvatic echinococcosis. 3. Host occurrence and geographic distribution of Echinococcus multilocularis in the north central United States. Journal of Parasitology 56, 1141–1150. doi: 10.2307/3277560.Google Scholar
Levine, ND (1980) Nematode Parasites of Domestic Animals and Man. Minneapolis, MN: Burgess Publishing Company.Google Scholar
Liccioli, S et al. (2012) Gastrointestinal parasites of coyotes (Canis latrans) in the metropolitan area of Calgary, Alberta, Canada. Canadian Journal of Zoology-Revue Canadienne De Zoologie 90, 1023–1030. doi: 10.1139/z2012-070.Google Scholar
Liccioli, S et al. (2013) A new intermediate host for Echinococcus multilocularis: the southern red-backed vole (Myodes gapperi) in urban landscape in Calgary, Canada. Parasitology International 62, 355–357. doi: 10.1016/j.parint.2013.03.007.Google Scholar
Liccioli, S et al. (2014) Spatial heterogeneity and temporal variations in Echinococcus multilocularis infections in wild hosts in a North American urban setting. International Journal for Parasitology 44, 457–465. doi: 10.1016/j.ijpara.2014.03.007.Google Scholar
Liccioli, S et al. (2015) Feeding ecology informs parasite epidemiology: prey selection modulates encounter rate with Echinococcus multilocularis in urban coyotes. PLoS ONE 10. doi: 10.1371/journal.pone.0121646.Google Scholar
Marzluff, JM (2001) Worldwide urbanization and its effects on birds. In Marzluff, J, Bowman, R and Donnelly, R (Eds), Avian Ecology and Conservation in an Urbanizing World. Dordrecht: Kluwer Academic Publishers, pp. 19–48.Google Scholar
Massolo, A et al. (2014) Echinococcus multilocularis in North America: the great unknown. Parasite 21. doi: 10.1051/parasite/2014069.Google Scholar
McKinney, ML (2006) Urbanization as a major cause of biotic homogenization. Biological Conservation 127, 247–260. doi: 10.1016/j.biocon.2005.09.005.Google Scholar
Murray, M et al. (2015a) Greater consumption of protein-poor anthropogenic food by urban relative to rural coyotes increases diet breadth and potential for human–wildlife conflict. Ecography 38, 1235–1242. doi: 10.1111/ecog.01128.Google Scholar
Murray, M et al. (2015b) Poor health is associated with use of anthropogenic resources in an urban carnivore. Proceedings of the Royal Society B 282. doi: 10.1098/rspb.2015.0009.Google Scholar
Murray, MH et al. (2016) Urban compost attracts coyotes, contains toxins, and may promote disease in urban-adapted wildlife. Ecohealth 13, 285–292. doi: 10.1007/s10393-016-1105-0.Google Scholar
Oro, D et al. (2013) Ecological and evolutionary implications of food subsidies from humans. Ecology Letters 16, 1501–1514. doi: 10.1111/ele.12187.Google Scholar
Padgett, DA and Glaser, R (2003) How stress influences the immune response. Trends in Immunology 24, 444–448. doi: 10.1016/S1471-4906(03)00173-X.Google Scholar
Poessel, SA, Mock, EC and Breck, SW (2017) Coyote (Canis latrans) diet in an urban environment: variation relative to pet conflicts, housing density, and season. Canadian Journal of Zoology 95, 287–297. doi: 10.1139/cjz-2016-0029.Google Scholar
Prange, S, Gehrt, SD and Wiggers, EP (2003) Demographic factors contributing to high raccoon densities in urban landscapes. Journal of Wildlife Management 67, 324–333. doi: 10.2307/3802774.Google Scholar
R Development Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rausch, RL (1968) Taxonomic characters in the genus Echinococcus (Cestoda: Taeniidae). Bulletin of the World Health Organization 39, 1–4.Google Scholar
Rausch, RL and Fay, FH (2011) Toxascaris leonina in rodents, and relationship to eosinophilia in a human population. Comparative Parasitology 78, 236–244. doi: 10.1654/4504.1.Google Scholar
Recio, MR et al. (2015) Changes in Mediterranean mesocarnivore communities along urban and ex-urban gradients. Current Zoology 61, 793–801. doi: 10.1093/czoolo/61.5.793.Google Scholar
Santa, MA et al. (2018) Detecting co-infections of Echinococcus multilocularis and Echinococcus canadensis in coyotes and red foxes in Alberta, Canada using real-time PCR. International Journal for Parasitology: Parasites and Wildlife 7, 111–115. doi: 10.1016/j.ijppaw.2018.03.001.Google Scholar
Schurer, JM et al. (2018) Echinococcus in wild canids in Quebec (Canada) and Maine (USA). PLoS Neglected Tropical Diseases 12, e0006712. doi: 10.1371/journal.pntd.0006712.Google Scholar
Seesee, FM, Sterner, MC and Worley, DE (1983) Helminths of the coyote (Canis latrans Say) in Montana. Journal of Wildlife Diseases 19, 54–55. doi: 10.7589/0090-3558-19.1.54.Google Scholar
Seguel, M and Gottdenker, N (2017) The diversity and impact of hookworm infections in wildlife. International Journal for Parasitology: Parasites and Wildlife 6, 177–194. doi: 10.1016/j.ijppaw.2017.03.007.Google Scholar
Seto, KC, Guneralp, B and Hutyra, LR (2012) Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proceedings of the National Academy of Sciences of the United States of America 109, 16083–16088. doi: 10.1073/pnas.1211658109.Google Scholar
Strickler, AR (2005) Taenia infections. http://www.cfsph.iastate.edu/DiseaseInfo/factsheets.php (accessed 17 August 2018).Google Scholar
Thompson, RCA, Kutz, SJ and Smith, A (2009) Parasite zoonoses and wildlife: emerging issues. International Journal of Environmental Research and Public Health 6, 678–693. doi: 10.3390/ijerph6020678.Google Scholar
Veit, P et al. (1995) Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110, 79–86.Google Scholar
Wirsing, AJ et al. (2007) Patterns of gastrointestinal parasitism among five sympatric prairie carnivores: are males reservoirs? Journal of Parasitology 93, 504–510. doi: 10.1645/Ge-1067r.1.Google Scholar