Hostname: page-component-7c8c6479df-ph5wq Total loading time: 0 Render date: 2024-03-28T11:37:20.793Z Has data issue: false hasContentIssue false

Helminth parasites of wolves (Canis lupus): a species list and an analysis of published prevalence studies in Nearctic and Palaearctic populations

Published online by Cambridge University Press:  22 February 2007

H.L. Craig
Affiliation:
School of Biological Sciences, University of Liverpool, Liverpool, L69 3BX, UK
P.S. Craig*
Affiliation:
Cestode Zoonoses Research Group, School of Environment and Life Sciences, University of Salford, Salford, M5 4WT, UK
*
*Author for correspondence Fax: 0161 295 5210 E-mail: p.s.craig@salford.ac.uk

Abstract

A literature survey was undertaken in order to draw up a definitive list of helminth parasites of the wolf, Canis lupus. From 27 papers a total of 72 helminth species from 40 genera were recorded that infect wolves, of which 93% were identified from the gastrointestinal tract at necropsy. They comprised 28 species of nematode, 27 species of cestode, 16 species of trematode and one acanthocephalan. Of these, 46 species were able to be included in further meta-analysis of prevalence data derived from 25 publications for which the total number of wolves examined was 1282 (1066 from Nearctic populations, and 216 from the Palaearctic region). These two populations were further subdivided into three relevent ecosystems or biomes, i.e. temperate/montane (n=216), boreal (n=805) or tundra (n=261). The meta-analysis of relative prevalence indicated the most common helminth species to be the tapeworm Taenia hydatigena, which occurred at relative rates of >30% for either zoogeographic region as well as in each of the three biomes. The related tapeworm, Echinococcus granulosus also exhibited high meta-prevalence (>19%) in all host biomes. The hookworm Uncinaria stenocephala was the most prevalent nematode species by meta-analysis (meta-prevalence 44.9%) in the temperate/montane biome, while the ascarid Toxascaris leonina was the dominant helminth species (meta-prevalence 73.9%) in the tundra wolf populations. Trematodes in the genus Alaria were the dominant fluke (meta-prevalence 3–5%) in all biomes. Analysis of published studies for helminth biodiversity using the Shannon-Wiener index based on species number and meta-prevalence by region or biome, indicated that highest helminth diversity occurred in wolf populations of the temperate/ montane biome (Palaearctic), and was lowest in tundra wolf populations of the Nearctic (P<0.05). Helminth species assemblage in European wolf populations was therefore at least as great or more varied than was recorded for the larger less disturbed wolf populations of North America.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2005

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

Abbasi, I., Branzburg, A., Campos-Ponce, M., Abdel-Hafez, S.K., Raoul, F., Craig, P.S. & Hamburger, J. (2003) Coprodiagnosis of Echinococcus granulosus infection in dogs by amplification of a newly identified repeated DNA sequence. American Journal of Tropical Medicine and Hygiene 69, 324330.Google Scholar
Archer, J., Taft, S.J. & Thiel, R.P. (1986) Parasites of wolves, Canis lupus , in Wisconsin, as determined from faecal examinations. Proceedings of the Helminthological Society of Washington 53, 290291.Google Scholar
Byman, D., Van Ballenberghe, V., Schlottauer, J.C. & Erickson, A.W. (1977) Parasites of wolves, Canis lupus L., in northeastern Minnesota, as indicated by analysis of fecal samples. Canadian Journal of Zoology 55, 376380.Google Scholar
Choquette, L.P.E., Gibson, G.G., Kuyt, E. & Pearson, A.M. (1973) Helminths of wolves, Canis lupus, L., in the Yukon and Northwest Territories. Canadian Journal of Zoology 51, 10871091.CrossRefGoogle ScholarPubMed
Combes, C. (2001) Parasitism. The ecology and evolution of intimate interactions. 728 pp. Chicago, Chicago University Press.Google Scholar
Craig, P.S., Gasser, R.B., Parada, L., Cabrera, P., Parietti, S., Borgues, C., Acuttis, A., Agulla, J., Snowden, K. & Paolillo, E. (1995) Diagnosis of canine echinococcosis: comparison of coproantigen and serum antibody tests with arecoline purgation in Uruguay. Veterinary Parasitology 56, 293301.CrossRefGoogle ScholarPubMed
Craig, P.S., Rogan, M.T. & Campos-Ponce, M. (2003) Echinococcosis: disease, detection and transmission. Parasitology 127, S5S20.Google Scholar
Cuesta, L., Barcena, F., Palacios, F. & Reig, S. (1991) The trophic ecology of the Iberian wolf (Canis lupus sigriafus Cabrera, 1907). A new analysis of stomach data. Mammalia 55, 239254.CrossRefGoogle Scholar
Custer, J.E. & Pence, D.B. (1981) Ecological analyses of helminth populations of wild canids from the gulf coastal prairies of Texas and Louisiana. Journal of Parasitology 67, 289307.Google Scholar
Dunn, A. (1969) Veterinary helminthology. 302 pp. London: Heinmann Press.Google Scholar
Erickson, A.B. (1944) Helminths of Minnesota Canidae in relation to food habits, and a host list and key to the species reported from North America. American Midland Naturalist 32, 358372.CrossRefGoogle Scholar
Fowler, J. & Cohen, L. (1992) Practical statistics for field biology. pp. 174175. New York, John Wiley and Sons.Google Scholar
Freeman, R.S., Adorjan, A. & Pimlott, D.H. (1961) Cestodes of wolves, coyotes and coyote–dog hybrids in Ontario. Canadian Journal of Zoology 39, 527532.Google Scholar
Guberti, V.L., Stancampino, L. & Francisci, F. (1993) Intestinal helminth parasite community in wolves (Canis lupus) in Italy. Parassitologia 55, 5965.Google Scholar
Hampton, B. (1997) The great American wolf. 308 pp. New York, Henry Holt & Company.Google Scholar
Hirvela-Koski, V., Haukisalami, V., Kilpela, S-S., Nylund, M. & Koski, P. (2003) Echinococcosis in Finland. Veterinary Parasitology 111, 175192.Google Scholar
Holmes, J.C. & Podesta, R. (1968) The helminths of wolves and coyotes from forested regions of Alberta. Canadian Journal of Zoology 46, 11931204.Google Scholar
Jenkins, D., Fraser, A., Bradshaw, H. & Craig, P.S. (2000) Detection of Echinococcus granulosus coproantigens in Australian canids with natural or experimental infection. Journal of Parasitology 86, 140145.Google Scholar
Jones, A. & Pybus, M.J. (2001) Taeniasis and echinococcosis Parasitic diseases of wild mammals pp. 150192 in Samuel, W.M., Pybus, M.J. & Kocan, A.A. (Eds) London, Manson Publishing.Google Scholar
Kozlov, D.P. (1977) Key to helminths of carnivorous mammals of the USSR. pp. 124Ryzhikov, K.M.Moscow, Nauka (in Russian).Google Scholar
Magurran, A.E. (1988) Ecological diversity and its measurement. pp. 145149. London, Croom Helm.Google Scholar
Marquard-Peterson, U.L.F. (1997) Endoparasites of Arctic wolves in Greenland. Arctic 50, 349354.Google Scholar
Martinek, K., Kolarova, L., Hapl, E. & Literak, I. (2001) Echinococcus multilocularis in European wolves (Canis lupus). Parasitology Research 87, 838839.Google ScholarPubMed
McNeil, M.A., Raus, M.E. & Messier, F. (1984) Helminths of wolves (Canis lupus) from southwestern Quebec. Canadian Journal of Zoology 62, 16591660.CrossRefGoogle Scholar
Mech, L.D. (1970) The wolf. The ecology and behaviour of an endangered species. 384 pp. New York, Natural History Press.Google Scholar
Messier, F., Rau, M.E. & McNeill, M.A. (1989) Echinococcus granulosus (Cestoda: Taeniidae) infections and moose-wolf population dynamics in southwestern Quebec. Canadian Journal of Zoology 67, 216219.Google Scholar
Mituch, J., Hovorka, J., Hovorka, I. & Vilagiova, I. (1994) Helminths of carnivores in the model territory of the High Tatra National Park. Folia Venatoria 22, 191200.Google Scholar
Nowak, R.M. (1999) Walker's mammals of the World. 836 pp. Vol. 1, 6th edn. Baltimore, Johns Hopkins University Press.Google Scholar
Oivanen, L., Kapel, C.M., Pozio, E., La Rosa, G., Mikkonen, T. & Sukura, A. (2002) Relations between Trichinella species and host species in Finland. Journal of Parasitology 88, 8488.Google Scholar
Papadopoulos, H., Himonas, C., Papazahariadou, M. & Antoniadou-Sotiriadou, K. (1997) Helminths of foxes and other wild carnivores from rural areas in Greece. Journal of Helminthology 71, 227231.Google Scholar
Pozio, E., La Rosa, G., Serrano, F.J., Barrat, J. & Rossi, L. (1996) Environmental and human influence on the ecology of Trichinella spiralis and Trichinella britovi in Western Europe. Parasitology 113, 527533.CrossRefGoogle ScholarPubMed
Pozio, E., Casulli, A., Bologov, V.V., Marucci, G. & La Rosa, G. (2001) Hunting practices increase the prevalence of Trichinella infection in wolves from European Russia. Journal of Parasitology 87, 14981501.Google Scholar
Priemer, J., Krone, O. & Schuster, R. (2002) Taenia krabbei (Cestoda: Cyclophyllidea) in Germany and its delimitation from T. ovis. Zoologischer Anzeiger 241, 333337.CrossRefGoogle Scholar
Rausch, R.L. (2003) Cystic echinococcosis in the Arctic and sub-Arctic. Parasitology 127, S73S85.CrossRefGoogle ScholarPubMed
Rausch, R. & Williamson, S.L. (1959) Studies on the helminth fauna of Alaska. XXXIV. The parasites of wolves, Canis lupus. Journal of Parasitology 45, 395403.Google Scholar
Rausch, R., Babero, B.B. & Schiller, E.L. (1956) Studies on the helminth fauna of Alaska. XXVII. The occurrence of larvae of Trichinella spiralis in Alaskan mammals. Journal of Parasitology 42, 259271.Google Scholar
Riley, W.A. (1939) Maintenance of Echinococcus in the United States. Journal of the American Veterinary Medical Association 95, 170172.Google Scholar
Samuel, W.M., Ramalingam, S. & Carbyn, L.N. (1978) Helminths in coyotes (Canis latrans Say), wolves (Canis lupus L.), and red foxes (Vulpes vulpes L.) of southwest Manitoba. Canadian Journal of Zoology 56, 26142617.CrossRefGoogle Scholar
Segovia, J.M., Torres, J., Miquel, J., Llaneza, J. & Feliu, C. (2001) Helminths in the wolf, Canis lupus , from north-western Spain. Journal of Helminthology 75, 183192.Google Scholar
Shimalov, V.V. & Shimalov, V.T. (2000) Helminth fauna of the wolf (Canis lupus Linnaeus, 1758) in Belorussian Polesie. Parasitology Research 86, 163164.CrossRefGoogle ScholarPubMed
Stancampino, L., Guberti, V., Francisci, F., Magi, M. & Bandi, C. (1994) Trichinellosis in wolf (Canis lupus) in Italy pp. 585589 in Campbell, C.(Ed.) Eighth International Conference on Trichinellosis. Rome, ISS Press.Google Scholar
Sweatman, G.K. (1952) Distribution and incidence of Echinococcus granulosus in man and other animals with special reference to Canada. Canadian Journal of Public Health 43, 480486.Google Scholar
Tang, C.T., Quian, Y.C., Kang, Y.M., Cui, G.W., Lu, H.C., Shu, L.M., Wang, Y.H. & Tang, L. (2004) Study on the ecological distribution of alveolar Echinococcus in Hulunbeier Pasture of Inner Mongolia, China. Parasitology 128, 187194.Google Scholar
Torres, J., Segovia, J.M., Miquel, J., Feliu, C., Llaneza, L. & Petrucci-Fonseca, F. (1996) The use of parasitological data for the theriological studies. The case of the Iberian wolf (Canis lupus signatus Cabrera, 1907). Carnivoros: evolucion, ecologia y conservacion. Organised by Cosejo Superiorde Investigaciones Cientificas, Madrid: 11–15 November 1996, 319 pp.Google Scholar
Treves, A., Naughton-Treves, L., Harper, E.K., Mladenoff, D.J., Rose, R.A., Sickley, T.A. & Wydeven, A.P. (2004) Predicting human–carnivore conflict: a spatial model derived from 25 years of data on wolf predation on livestock. Conservation Biology 18, 114125.CrossRefGoogle Scholar
Trouve, S., Morand, S. & Gabrion, C. (2003) Asexual multiplication of larval parasitic worms: a predictor of adult life-history traits in Taeniidae. Parasitology Research 89, 8188.Google Scholar
Zarnke, R.L., Worley, D.E., Ver Hoef, J.M. & McNay, M.E. (1999) Trichinella sp. in wolves from interior Alaska. Journal of Wildlife Diseases 35, 9497.Google Scholar