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Helminth parasites in the endangered Ethiopian wolf, Canis simensis

Published online by Cambridge University Press:  09 July 2014

F. van Kesteren ,
K.J. Piggott ,
T. Bengui ,
S.B. Kubri ,
A. Mastin ,
C. Sillero-Zubiri ,
M. Paris ,
R.P. Millar ,
D.W. Macdonald  and
F. Shiferaw
...Show all authors
F. van Kesteren*
Affiliation:
Cestode Zoonoses Research Group, School of Environment and Life Sciences, University of Salford, M5 4WT, Salford, UK
K.J. Piggott
Affiliation:
Cestode Zoonoses Research Group, School of Environment and Life Sciences, University of Salford, M5 4WT, Salford, UK
T. Bengui
Affiliation:
Cestode Zoonoses Research Group, School of Environment and Life Sciences, University of Salford, M5 4WT, Salford, UK
S.B. Kubri
Affiliation:
Cestode Zoonoses Research Group, School of Environment and Life Sciences, University of Salford, M5 4WT, Salford, UK
A. Mastin
Affiliation:
Cestode Zoonoses Research Group, School of Environment and Life Sciences, University of Salford, M5 4WT, Salford, UK
C. Sillero-Zubiri
Affiliation:
Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, The Recanati-Kaplan Centre, Tubney House, TubneyOX13 5QL, UK Ethiopian Wolf Conservation Programme, PO Box 215, Robe, Bale, Ethiopia
M. Paris
Affiliation:
Institute for Breeding Rare and Endangered African Mammals (IBREAM), Mammal Research Institute, University of Pretoria, Lynnwood Road, Pretoria0028, South Africa School of Animal Biology, Faculty of Natural and Agricultural Sciences, University of Western Australia, 35 Stirling Highway, CrawleyWA6009, Australia
R.P. Millar
Affiliation:
Institute for Breeding Rare and Endangered African Mammals (IBREAM), Mammal Research Institute, University of Pretoria, Lynnwood Road, Pretoria0028, South Africa Mammal Research Institute, University of Pretoria, Pretoria0028, South Africa UCT/MRC Receptor Biology Unit, University of Cape Town, Observatory7925, South Africa
D.W. Macdonald
Affiliation:
Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, The Recanati-Kaplan Centre, Tubney House, TubneyOX13 5QL, UK
F. Shiferaw
Affiliation:
Ethiopian Wildlife Conservation Authority, PO Box 386, Addis Ababa, Ethiopia Zoological Society of London, Conservation Programmes, King Khalid Wildlife Research Centre, POB 61681, Riyadh11575, Saudi Arabia
P.S. Craig
Affiliation:
Cestode Zoonoses Research Group, School of Environment and Life Sciences, University of Salford, M5 4WT, Salford, UK
*
*E-mail: [email protected]
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Abstract

Ethiopian wolves, Canis simensis, are an endangered carnivore endemic to the Ethiopian highlands. Although previous studies have focused on aspects of Ethiopian wolf biology, including diet, territoriality, reproduction and infectious diseases such as rabies, little is known of their helminth parasites. In the current study, faecal samples were collected from 94 wild Ethiopian wolves in the Bale Mountains of southern Ethiopia, between August 2008 and February 2010, and were screened for the presence of helminth eggs using a semi-quantitative volumetric dilution method with microscopy. We found that 66 of the 94 faecal samples (70.2%) contained eggs from at least one group of helminths, including Capillaria, Toxocara, Trichuris, ancylostomatids, Hymenolepis and taeniids. Eggs of Capillaria sp. were found most commonly, followed by Trichuris sp., ancylostomatid species and Toxocara species. Three samples contained Hymenolepis sp. eggs, which were likely artefacts from ingested prey species. Four samples contained taeniid eggs, one of which was copro-polymerase chain reaction (copro-PCR) and sequence positive for Echinococcus granulosus, suggesting a spillover from a domestic parasite cycle into this wildlife species. Associations between presence/absence of Capillaria, Toxocara and Trichuris eggs were found; and egg burdens of Toxocara and ancylostomatids were found to be associated with geographical location and sampling season.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 4 , July 2015 , pp. 487 - 495
Copyright
Copyright © Cambridge University Press 2014 

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References

Abbasi, I., Branzburg, A., Campos-Ponce, M., Hafez, S.K.A., Raoul, F., Craig, P.S. & Hamburger, J. (2003) Copro-diagnosis of Echinococcus granulosus infection in dogs by amplification of a newly identified repeated DNA sequence. American Journal of Tropical Medicine and Hygiene 69, 324–330.CrossRefGoogle ScholarPubMed
Ash, L. & Orihel, T. (1997) Atlas of human parasitology. 4th edn.Chicago, USA, American Society of Clinical Pathologists.Google Scholar
Ashford, R.W., Hall, A.J. & Babona, D. (1981) Distribution and abundance of intestinal helminths in man in western Papua New Guinea with special reference to Strongyloides. Annals of Tropical Medicine and Parasitology 75, 269–279.CrossRefGoogle ScholarPubMed
Atickem, A., Bekele, A. & Williams, S.D. (2009) Competition between domestic dogs and Ethiopian wolf (Canis simensis) in the Bale Mountains National Park, Ethiopia. African Journal of Ecology 48, 401–407.CrossRefGoogle Scholar
Bekele, K., Mukasa-Mugerwa, E. & Kasali, O.B. (1988) The prevalence of cysticercosis and hydatidosis in Ethiopian sheep. Veterinary Parasitology 28, 267–270.CrossRefGoogle ScholarPubMed
Blower, J. (1968) The wildlife of Ethiopia. Oryx 9, 276–283.CrossRefGoogle Scholar
Boufana, B.S., Campos-Ponce, M., Naidich, A., Buishi, I., Lahmar, S., Zeyhle, E., Jenkins, D.J., Combes, B., Wen, H., Xiao, N., Nakao, M., Ito, A., Qiu, J. & Craig, P.S. (2008) Evaluation of three PCR assays for the identification of the sheep strain (genotype 1) of Echinococcus granulosus in canid feces and parasite tissues. American Journal of Tropical Medicine and Hygiene 78, 777–783.CrossRefGoogle ScholarPubMed
Ceruti, R., Sonzogni, O., Origgi, F., Vezzoli, F., Cammarata, S., Giusti, A.M. & Scanziani, E. (2001) Capillaria hepatica infection in wild brown rats (Rattus norvegicus) from the urban area of Milan, Italy. Journal of Veterinary Medicine B 48, 235–240.CrossRefGoogle ScholarPubMed
Craig, H.L. & 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, 95–103.Google Scholar
Crowell, W.A., Klei, T.R., Hall, D.I., Smith, N.K. & Newsom, J.D. (1978) Capillaria hepatica infection in coyotes of Louisiana. Journal of the American Veterinary Medical Association 173, 1171–1172.Google ScholarPubMed
Curi, N.H., Coelho, C.M., de Campos Cordeiro Malta, M., Magni, E.M.V., Sabato, M.A.L., Araujo, A.S., Lobato, Z.I.P., Santos, J.L.C., Santos, H.A., Ragozo, A.A.M. & de Souza, S.L.P. (2012) Pathogens of wild maned wolves (Chrysocyon brachyurus) in Brazil. Journal of Wildlife Diseases 48, 1052–1056.CrossRefGoogle Scholar
Dalimi, A., Sattari, A. & Motamedi, G. (2006) A study on intestinal helminthes of dogs, foxes and jackals in the western part of Iran. Veterinary Parasitology 142, 129–133.CrossRefGoogle Scholar
Degefu, H., Tefera, A. & Yohannes, M. (2011) Zoonotic helminth parasites in faecal samples of household dogs in Jimma Town, Ethiopia. Journal of Public Health and Epidemiology 3, 138–143.Google Scholar
Di Cesare, A., Castagna, G., Meloni, S., Otranto, D. & Traversa, D. (2012a) Mixed trichuroid infestation in a dog from Italy. Parasites and Vectors 5, 128–134.CrossRefGoogle Scholar
Di Cesare, A., Castagna, G., Otranto, D., Meloni, S., Milillo, P., Latrofa, M.S., Paoletti, B., Bartolini, R. & Traversa, D. (2012b) Molecular detection of Capillaria aerophila, an agent of canine and feline pulmonary capillariosis. Journal of Clinical Microbiology 50, 1958–1963.CrossRefGoogle ScholarPubMed
Eckert, J. & Deplazes, P. (2004) Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clinical Microbiology Reviews 17, 107–135.CrossRefGoogle ScholarPubMed
Elmore, S.A., Lalonde, L.F., Samelius, G., Alisauskas, R.T., Gajadhar, A.A. & Jenkins, E.J. (2013) Endoparasites in the feces of arctic foxes in a terrestrial ecosystem in Canada. International Journal for Parasitology: Parasites and Wildlife 2, 90–96.Google Scholar
Fok, E., Szatmári, V., Busák, K. & Rozgonyi, F. (2001) Epidemiology: prevalence of intestinal parasites in dogs in some urban and rural areas of Hungary. Veterinary Quarterly 23, 96–98.CrossRefGoogle Scholar
Fromsa, A. & Jobre, Y. (2011) Infection prevalence of hydatidosis (Echinococcus granulosus, Batsch, 1786) in domestic animals in Ethiopia: A synthesis report of previous surveys. Ethiopian Veterinary Journal 15, 11–33.CrossRefGoogle Scholar
Gamboa, M.I. (2005) Effects of temperature and humidity on the development of eggs of Toxocara canis under laboratory conditions. Journal of Helminthology 79, 327–331.CrossRefGoogle ScholarPubMed
Gemmell, M.A. (1987) Population dynamics in echinococcosis and cysticercosis: evaluation of the biological parameters of Taenia hydatigena and T. ovis and comparison with those of Echinococcus granulosus. Parasitology 94, 161–180.CrossRefGoogle Scholar
Glickman, L.T. & Schantz, P.M. (1981) Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiologic Reviews 3, 230–250.CrossRefGoogle ScholarPubMed
Gompper, M.E., Goodman, R.M., Kays, R.W., Ray, J.C. & Fiorello, C.V. (2003) A survey of the parasites of coyotes (Canis latrans) in New York based on fecal analysis. Journal of Wildlife Diseases 39, 712–717.CrossRefGoogle ScholarPubMed
Gottelli, D., Sillero-Zubiri, C., Applebaum, G.D., Roy, M.S., Girman, D.J., Garcia-Moreno, J., Ostrander, E.A. & Wayne, R.K. (1994) Molecular genetics of the most endangered canid: the Ethiopian wolf Canis simensis. Molecular Ecology 3, 301–312.CrossRefGoogle ScholarPubMed
Haukisalmi, V. & Henttononen, H. (1993) Population dynamics of Taenia polyacantha metacestodes in the bank vole Clethrionomys glareolus. Annales Zoologici Fennici 30, 81–84.Google Scholar
Haydon, D.T., Laurenson, M.K. & Sillero-Zubiri, C. (2002) Integrating epidemiology into population viability analysis: managing the risk posed by rabies and canine distemper to the Ethiopian wolf. Conservation Biology 16, 1372–1385.CrossRefGoogle Scholar
Hillman, J.C. (1988) The Bale Mountains National Park area, Southeast Ethiopia, and its management. Mountain Research and Development 8, 253–258.CrossRefGoogle Scholar
Hoberg, E.P. (2002) Taenia tapeworms: their biology, evolution and socioeconomic significance. Microbes and Infection 4, 859–866.CrossRefGoogle ScholarPubMed
Hothorn, T., Bretz, F. & Westfall, P. (2008) Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.CrossRefGoogle ScholarPubMed
Jebessa, D. (2009) Some helminths of the Ethiopian wolf (Canis simensis Rüpell 1840, Canidae) and its prey in the Bale Mountains National Park. Ethiopian Journal of Science 32, 81–84.Google Scholar
Jenkins, D.J. & Rickard, M.D. (1985) Specific antibody responses to Taenia hydatigena, Taenia pisiformis and Echinococcus granulosus infection in dogs. Australian Veterinary Journal 62, 72–78.CrossRefGoogle ScholarPubMed
Johnson, N., Mansfield, K.L., Marston, D.A., Wilson, C., Goddard, T., Selden, D., Hemson, G., Edea, L., Van Kesteren, F., Shiferaw, F., Stewart, A.E., Sillero-Zubiri, C. & Fooks, A.R. (2010) A new outbreak of rabies in rare Ethiopian wolves (Canis simensis). Archives of Virology 155, 1175–1177.CrossRefGoogle ScholarPubMed
Kassa, S.A. (2012) Cystic hydatidosis in Ethiopia: a review. Scientific Journal of Crop Science 1, 1–8.Google Scholar
Kirkova, Z. & Dinev, I. (2005) Morphological changes in the intestine of dogs experimentally infected with Trichuris vulpis. Bulgarian Journal of Veterinary Medicine 8, 239–243.Google Scholar
Laurenson, K., Sillero-Zubiri, C., Thompson, H., Shiferaw, F., Thirgood, S. & Malcolm, J. (1998) Disease as a threat to endangered species: Ethiopian wolves, domestic dogs and canine pathogens. Animal Conservation 1, 273–280.CrossRefGoogle Scholar
Lloyd, S., Elwood, C.M. & Smit, K.C. (2002) Capillaria hepatica (Calodium hepaticum) infection in a British dog. Veterinary Record 151, 419–420.CrossRefGoogle Scholar
Malcolm, J. (1997) The diet of Ethiopian wolf (Canis simensis Ruppell) from a grassland area of the Bale Mountains, Ethiopia. African Journal of Ecology 35, 162–164.CrossRefGoogle Scholar
Marino, J. & Sillero-Zubiri, C. (2011) Canis simensis. In IUCN Red List of Threatened Species. Version 2013.2. Available atwww.iucnredlist.org (accessed 1 June 2014).Google Scholar
Marino, J., Sillero-Zubiri, C. & Macdonald, D.W. (2006) Trends, dynamics and resilience of an Ethiopian wolf population. Animal Conservation 9, 49–58.CrossRefGoogle Scholar
Matthews, B.E. (1985) The influence of temperature and osmotic stress on the development and eclosion of hookworm eggs. Journal of Helminthology 59, 217–224.CrossRefGoogle ScholarPubMed
Meijer, T., Mattsson, R., Angerbjörn, A., Osterman-Lind, E., Fernández-Aguilar, X. & Gavier-Widén, D. (2011) Endoparasites in the endangered Fennoscandian population of arctic foxes (Vulpes lagopus). European Journal of Wildlife Research 57, 923–927.CrossRefGoogle Scholar
Naidich, A., McManus, D.P., Canova, S.G., Gutierrez, A.M., Zhang, W., Guarnera, E.A. & Rosenzvit, M.C. (2006) Patent and pre-patent detection of Echinococcus granulosus genotypes in the definitive host. Molecular and Cellular Probes 20, 5–10.CrossRefGoogle ScholarPubMed
Randall, D., Williams, S.D., Kuzmin, I.V., Rupprecht, E., Tallents, L.A., Tefera, Z., Argaw, K., Shiferaw, F., Knobel, D.L., Sillero-Zubiri, C. & Laurenson, M.K. (2004) Rabies in endangered Ethiopian wolves. Emerging Infectious Diseases 10, 2214–2217.CrossRefGoogle ScholarPubMed
R Development Core Team. (2013) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Senior, D., Solomon, G., Goldschmidt, M., Joyce, T. & Bovee, K. (1980) Capillaria plica infection in dogs. Journal of the American Veterinary Medical Association 176, 901–905.Google ScholarPubMed
Shiferaw, F. & Laurenson, K. (2011) Risk of disease transmission between domestic livestock and wild ungulates in the Bale Mountains National Park, Ethiopia. Walia, Special edition on the Bale Mountains 269–281.Google Scholar
Sillero-Zubiri, C. & Gottelli, D. (1994) Canis simensis. Mammalian Species 485, 1–6.CrossRefGoogle Scholar
Sillero-Zubiri, C. & Gottelli, D. (1995a) Diet and feeding behavior of Ethiopian wolves (Canis simensis). Journal of Mammalogy 76, 531–541.CrossRefGoogle Scholar
Sillero-Zubiri, C. & Gottelli, D. (1995b) Spatial organization in the Ethiopian wolf Canis simensis: large packs and stable home ranges. Journal of Zoology 237, 65–81.CrossRefGoogle Scholar
Sillero-Zubiri, C. & Macdonald, D.W. (Eds). (1997) The Ethiopian wolf – status survey and conservation action plan. Gland, Switzerland and Cambridge, UK, IUCN.Google Scholar
Sillero-Zubiri, C. & Macdonald, D.W. (1998) Scent-marking and territorial behaviour of Ethiopian wolves Canis simensis. Journal of Zoology 245, 351–361.CrossRefGoogle Scholar
Sillero-Zubiri, C., Gottelli, D. & Macdonald, D.W. (1996a) Male philopatry, extra-pack copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behavioral Ecology and Sociobiology 38, 331–340.CrossRefGoogle Scholar
Sillero-Zubiri, C., King, A.A. & Macdonald, D.W. (1996b) Rabies and mortality in Ethiopian wolves (Canis simensis). Journal of Wildlife Diseases 32, 80–86.CrossRefGoogle ScholarPubMed
Soulsby, E.J.L. (1974) Helminths, arthropods and protozoa of domesticated animals. 6th edn.London, Balliere, Tindall and Cassell.Google Scholar
Spratt, D.M. & Singleton, G.R. (2001) Hepatic capillariasis. pp. 365–379in Samuel, W.M., Pybus, M.J. & Kocan, A.A. (Eds) Parasitic diseases of wild mammals. Iowa, USA, Iowa State University Press.CrossRefGoogle Scholar
Thompson, R.C.A. (2008) The taxonomy, phylogeny and transmission of Echinococcus. Experimental Parasitology 119, 439–446.CrossRefGoogle ScholarPubMed
Traub, R.J., Robertson, I.D., Irwin, P., Mencke, N. & Thompson, R.C.A. (2004) Application of a species-specific PCR-RFLP to identify Ancylostoma eggs directly from canine faeces. Veterinary Parasitology 123, 245–255.CrossRefGoogle ScholarPubMed
Traversa, D., Di Cesare, A., Lia, R.P., Castagna, G., Meloni, S., Heine, J., Strube, K., Millillo, P., Otranto, D., Meckes, O. & Schaper, R. (2011) New insights into morphological and biological features of Capillaria aerophila (Trichocephalida, Trichuridae). Parasitology Research 109, 97–104.CrossRefGoogle ScholarPubMed
Urquhart, G.M., Armour, J., Duncan, J.L., Dunn, A.M. & Jennings, F.W. (1996) Veterinary parasitology. Glasgow, Scotland, Blackwell Science.Google Scholar
van Kesteren, F., Sillero-Zubiri, C., Millar, R., Argaw, K., Macdonald, D.W. & Paris, M. (2012) Sex, stress and social status: patterns in fecal testosterone and glucocorticoid metabolites in male Ethiopian wolves. General and Comparative Endocrinology 179, 30–37.CrossRefGoogle ScholarPubMed
van Kesteren, F., Paris, M., Macdonald, D.W., Millar, R., Argaw, K., Johnson, P.J., Farstad, W. & Sillero-Zubiri, C. (2013) The physiology of cooperative breeding in a rare social canid; sex, suppression, and pseudopregnancy in female Ethiopian wolves. Physiology and Behavior 122, 34–45.CrossRefGoogle Scholar
Varcasia, A., Lightowlers, M.W., Cattoli, G., Cancedda, G.M., Canu, S., Garippa, G. & Scala, A. (2006) Genetic variation within Taenia multiceps in Sardinia, Western Mediterranean (Italy). Parasitology Research 99, 622–626.CrossRefGoogle ScholarPubMed
Venables, W.N. & Ripley, B.D. (2002) Modern applied statistics with S. 4th edn.New York, Springer.CrossRefGoogle Scholar
Vervaeke, M., Dorny, P., De Bruyn, L., Vercammen, F., Jordaens, K., Van Den Berghe, K. & Verhagen, R. (2005) A survey of intestinal helminths of red foxes (Vulpes vulpes) in northern Belgium. Acta Parasitologica 50, 221–227.Google Scholar
Vial, F., Sillero-Zubiri, C., Marino, J., Haydon, D.T. & Macdonald, D.W. (2010) An analysis of long-term trends in the abundance of domestic livestock and free-roaming dogs in the Bale Mountains National Park, Ethiopia. African Journal of Ecology 49, 91–102.CrossRefGoogle Scholar
von Nickisch-Rosenegk, M., Silva-Gonzalez, R. & Lucius, R. (1999) Modification of universal 12S rDNA primers for specific amplification of contaminated Taenia spp. (Cestoda) gDNA enabling phylogenetic studies. Parasitology Research 85, 819–825.CrossRefGoogle ScholarPubMed
Warren, E.G. (1969) Infections of Toxocara canis in dogs fed infected mouse tissues. Parasitology 59, 837–841.CrossRefGoogle ScholarPubMed
Woodland, W.N.F. (1924) On the life-cycle of Hymenolepis fraterna (H. nana var. fraterna Stiles) of the white mouse. Parasitology 16, 69–83.CrossRefGoogle Scholar
Yacob, H.T., Ayele, T., Fikru, R. & Basu, A.K. (2007) Gastrointestinal nematodes in dogs from Debre Zeit, Ethiopia. Veterinary Parasitology 148, 144–148.CrossRefGoogle ScholarPubMed
Yalden, D.W. & Largen, M.J. (1992) The endemic mammals of Ethiopia. Mammal Review 22, 115–150.CrossRefGoogle Scholar
Zewdu, E., Semahegn, Y. & Mekibib, B. (2010) Prevalence of helminth parasites of dogs and owners' awareness about zoonotic parasites in Ambo town, central Ethiopia. Ethiopian Veterinary Journal 14, 17–30.Google Scholar
Zhang, Y., Bart, J.M., Hao, W., Ma, X., Miao, Y. & Chen, X. (2006) PCR method for diagnosis of dogs infected with Echinococcus: specificity and application in clinical diagnosis. Chinese Journal of Endemiology 25, 56–58(in Chinese).Google Scholar