Lepus corsicanus gastro-intestinal helminths: first report

Usai, F.; Rinnovati, R.; Trocchi, V.; Stancampiano, L.

doi:10.2478/s11687-012-0015-0

Abstract

Italian hare Lepus corsicanus De Winton, 1898, is a true species living in simpatry with Lepus europaeus in mainland Italy and with Oryctolagus cuniculus in Sicily, where L. europaeus is absent. Up to date, nobody has studied the helminths of this endemic Italian Mammal. Therefore, in order to describe Italian hare gastro-intestinal helminths, gastro-intestinal tract of 29 Italian hares, coming from mainland Italy (#14) and from Sicily (#15) were collected between 1997 and 2009. Twentyfive hares were positive for at least one parasite (86 %). Six parasite species were isolated, 2 cestodes (Cittotaenia pectinata, prevalence 3 %) and Paranoplocephala sp., 3 %) and 4 nematodes (Trichostrongylus retortaeformis, 86 %, Graphidium strigosum, 14 %, Trichuris sp., 10 % and Teladorsagia circumcincta, 7 %). Both Teladorsagia circumcincta circumcincta and Teladorsagia circumcincta trifurcata morphotypes were identified. Comparison with available data regarding L. europaeus and O. cuniculus in Italy is provided. Being not T. circumcincta and Paranoplocephala sp. typical parasites of leporids, a description of the observed specimens is given.

References

[1] Alzaga, V., Tizzani, P., Acevedo, P., Ruiz-Fons, F., Vicente, J., Gortàzar C. (2009): Deviance partitioning of host factors affecting parasitization in the European brown hare (Lepus europaeus). Naturwissenschafte 96: 1157–1168 http://dx.doi.org/10.1007/s00114-009-0577-y10.1007/s00114-009-0577-y19565211
Search in Google Scholar
[2] Angelici, F. M., Luiselli, L. (2001): Distribution and status of the Apennine hare Lepus corsicanus in continental Italy and Sicily. Oryx, 35: 245–249. DOI: 10.1046/j.1365-3008.2001.00182.x 10.1046/j.1365-3008.2001.00182.x
Search in Google Scholar
[3] Angelici, F. M., Randi, E., Riga, F., Trocchi, V. (2008): Lepus corsicanus. In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.1. 〈www.iucnredlist.org〉
Search in Google Scholar
[4] Becklund, W. W., Walker, M. L. (1971): Nomenclature and morphology of Ostertagia trifurcata Ransom, 1907, with data on spicule lengths of five stomach worms of ruminants. J. Parasitol., 57: 508–516 http://dx.doi.org/10.2307/327790410.2307/3277904
Search in Google Scholar
[5] Bordes, F., Langand, J., Feliu, C., Morand S. (2007): Helminth Communities of an Introduced Hare (Lepus granatensis) and a Native Hare (Lepus europaeus) in Southern France. J. Wildl. Dis., 43: 747–751
Search in Google Scholar
[6] Bush, A. O., Lafferty, K. D., Lotz, J. M., Shostak, A. W. (1997): Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol., 83, 575–583 http://dx.doi.org/10.2307/328422710.2307/3284227
Search in Google Scholar
[7] Cabon-Raczynska, K. (1964): Studies on the European hare. III. Morphological variation of the skull. Acta Theriol. 9: 249–285 10.4098/AT.arch.64-33
Search in Google Scholar
[8] Canestri Trotti, G., Corradini, L., Bassi, S. (1988): Osservazioni sulle elmintiasi gastrointestinali di lepri delle province di Ferrara e Modena e lepri di importazione. Suppl. Ric Biol Selvaggina 14: 317–321
Search in Google Scholar
[9] Capelli, G., Stancampiano, L., dal Colle, S., Bozzolan, G., Parenti, E., Pietrobelli M. (1998): Gastrointestinal parasite community in roe deer (Capreolus capreolus) and interactions between wild and domenstic ruminants. Parassitologia 40(Suppl. 1): 30
Search in Google Scholar
[10] Citterio, C. V., Caslini, C., Milani, F., Sala, M., Ferrari, N., Lanfranchi, P. (2006): Abomasal nematode community in an Alpine chamois (Rupicapra r. rupicapra) population before and after a die-off. J. Parasitol., 92: 918–927. DOI: 10.1645/GE-3551.1 http://dx.doi.org/10.1645/GE-3551.110.1645/GE-3551.117152929
Search in Google Scholar
[11] Craig, B. H., Pilkington, J. G., Pemberton, J. M. (2010): Sex ratio and morphological polymorphism in an isolated, endemic Teladorsagia circumcincta population. J. Helminthol., 84: 208–215. DOI: 10.1017/S0022149X09990551 http://dx.doi.org/10.1017/S0022149X0999055110.1017/S0022149X0999055119761627
Search in Google Scholar
[12] Dantas-Torres, F., Testini, G., Digeronimo, P.M., Lorusso, V., Mallia, E., Otranto, D. (2011): Ticks infesting the endangered Italian hare (Lepus corsicanus) and their habitat in an ecological park in southern Italy. Exp. Appl. Acarol., 53: 95–102. DOI: 10.1007/s10493-010-9387-3 http://dx.doi.org/10.1007/s10493-010-9387-310.1007/s10493-010-9387-320711803
Search in Google Scholar
[13] Dubinský, P., Vasilková, Z., Hurníková, Z., Miterpáková, M., Slamečka, J., Jurčík, R. (2010): Parasitic infections of the European brown hare (Lepus europaeus Pallas, 1778) in south-western Slovakia. Helminthologia., 47: 219–225. DOI: 10.2478/s11687-010-0034-7 http://dx.doi.org/10.2478/s11687-010-0034-710.2478/s11687-010-0034-7
Search in Google Scholar
[14] Eira, C., Torres, J., Miquel, J., Vingada, J. (2007): The helminth parasites of the wild rabbit Oryctolagus cuniculus and their effect on host condition in Dunas de Mira, Portugal. J. Helminthol., 81: 239–246. DOI: 10.1017/S0022149X07727426 http://dx.doi.org/10.1017/S0022149X0772742610.1017/S0022149X0772742617594739
Search in Google Scholar
[15] Erickson A. B. (1944): Helminth infections in relation to population fluctuations in snowshoe hares. J. Wildl. Manage., 8: 134–153 http://dx.doi.org/10.2307/379644610.2307/3796446
Search in Google Scholar
[16] Giannetto, S., Virga, A., Baccarani, E. M., Canestri Trotti G. (1998): Elminti intestinali in conigli selvatici (Oryctolagus cuniculus). Atti SISVet., 52: 165–166.
Search in Google Scholar
[17] Gibbons, L. M., Khalil, L. F. (1982): A key for the identification of genera of the nematode family Trichostrongylidae Leiper, 1912. J. Helminthol. 56: 185–233. http://dx.doi.org/10.1017/S0022149X0003458110.1017/S0022149X00034581
Search in Google Scholar
[18] Graybill, H. W. (1923): A new genus of nematodes from the domestic rabbit. Parasitology. 12: 340–342. http://dx.doi.org/10.1017/S003118200001482710.1017/S0031182000014827
Search in Google Scholar
[19] Guberti, V., De Marco, M. A., Riga, F., Cavazza, A., Trocchi, V., Capucci, L. (2000): Virology and species conservation: the case of EBHSV and the Italian hare (Lepus corsicanus De Winton, 1898). Proceeding of V International Congress of European Society for Veterinary Virology. 198–199
Search in Google Scholar
[20] Haukisalmi, V., Henttonen, H. (2003): What is Paranoplocephala macrocephala (Douthitt, 1915) (Cestoda: Anoplocephalidae)? Syst. Parasitol. 54: 53–69. DOI: 10.1023/A:1022141809571 http://dx.doi.org/10.1023/A:102214180957110.1023/A:1022141809571
Search in Google Scholar
[21] Haukisalmi, V., Wickström, L. M. (2005): Morphological characterisation of Andrya Railliet, 1893, Neandrya n. g. and Paranoplocephala Lühe, 1910 (Cestoda: Anoplocephalidae) in rodents and lagomorphs. Syst. Parasitol. 62: 209–219. DOI: 10.1007/s11230-005-5499-2 http://dx.doi.org/10.1007/s11230-005-5499-210.1007/s11230-005-5499-2
Search in Google Scholar
[22] Haukisalmi, V. (2009): A taxonomic revision of the genus Anoplocephaloides Baer, 1923 sensu Rausch (1976), with the description of four new genera (Cestoda: Anoplocephalidae). Zootaxa. 2057: 1–31. 10.11646/zootaxa.2057.1.1
Search in Google Scholar
[23] Lai, M., Arru, E. (1969): Trichostrongylidae del coniglio selvatico (Oryctolagus cuniculus). Parassitologia 11: 97–99
Search in Google Scholar
[24] Leignel, V., Cabaret, J., Humbert, J. F. (2002): New molecular evidence that Teladorsagia circumcincta (Nematoda: Trichostrongylidea) is a species complex. J. Parasitol. 88: 135–140. DOI: 10.1645/0022-3395(2002)088[0135:NMETTC]2.0.CO;2
Search in Google Scholar
[25] Lichtenfels, J. R., Hoberg, E. P. (1993): The systematics of nematodes that cause ostertagiasis in domestic and wild ruminants in North America: an update and a key to species. Vet. Parasitol. 46: 33–53. DOI: 10.1016/0304-4017(88)90056-8 http://dx.doi.org/10.1016/0304-4017(93)90046-P10.1016/0304-4017(88)90056-8
Search in Google Scholar
[26] Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M., Schad, G. A. (1982): The use of ecological terms in parasitology. J. Parasitol., 68: 131–133 http://dx.doi.org/10.2307/328133510.2307/3281335
Search in Google Scholar
[27] Meneguz, P. G., Tizzani, P. (2004): First report of Obeliscoides cuniculi in European brown hare (Lepus europaeus). Parassitologia. 46(Suppl. 1): 51.
Search in Google Scholar
[28] Palacios, F. (1996): Systematics of the indigenous hares of Italy traditionally identified as Lepus europeus Pallas, 1778 (Mammalia: Leporidae). Bonner Zoologische Beiträge. 46: 59–91
Search in Google Scholar
[29] Palacios, F., Orueta, J. F., Tapia, G. G. (1989): Taxonomic review of the Lepus europaeus group in Italy and Corsica. Abstract of Papers and Poster, V International Theriological Congress. 1: 189–190
Search in Google Scholar
[30] Pierpaoli, M., Riga, F., Trocchi, V., Randi, E. (1999): Species distinction and evolutionary relationships of the Italian hare (Lepus corsicanus) as described by mitochondrial DNA sequencing. Mol. Ecol. 8: 1805–1817. DOI: 10.1046/j.1365-294x.1999.00766.x http://dx.doi.org/10.1046/j.1365-294x.1999.00766.x10.1046/j.1365-294x.1999.00766.x
Search in Google Scholar
[31] Poglayen, G., Gaglio, G., Brianti, E., Agretti, D., Capelli, G. (2002): Monitoraggio sanitario della lepre (Lepus europaeus): la fauna parassitaria. Atti SISVet. 56: 199–200
Search in Google Scholar
[32] Reiczigel J., Rózsa L. (2005): Quantitative Parasitology 3.0. Budapest.
Search in Google Scholar
[33] Riga, F., Trocchi, V., Toso, S. (2001): Morphometric differentiation between the Italian hare (Lepus corsicanus De Winton, 1898) and European brown hare (Lepus europaeus Pallas, 1778). J. Zool. 253: 241–252. DOI: 10.1017/S0952836901000218 http://dx.doi.org/10.1017/S095283690100021810.1017/S0952836901000218
Search in Google Scholar
[34] Saulai, M., Cabaret, J. (1998): Limited role of lagomorphs (Oryctolagus cuniculus and Lepus capensis) in the dispersion of parasite nematodes of ruminants. Vet. Parasitol. 77: 301–304. DOI: 10.1016/S0304-4017(98)00113-7 http://dx.doi.org/10.1016/S0304-4017(98)00113-710.1016/S0304-4017(98)00113-7
Search in Google Scholar
[35] Sorgi, C., Tribulato, D., Miccichè, A., Billeri, F., Gaglio, G., Poglayen, G., Giannetto, S. (2004): A parasitological survey on wild rabbits (Oryctolagus cuniculus) living in Stagnone Archipelago natural preserve of Trapani, Italy. Parassitologia. 46(Suppl. 1): 66.
Search in Google Scholar
[36] Soulsby, E. J. L. (1968): Helminths, arthropods and Protozoa of Domesticated Animals. 7th Edition, London, Baillière Tindall, 809 pp
Search in Google Scholar
[37] Stancampiano, L., Battelli, G. (2002): Gastrointestinal nematodes of Chamois (Rupicapra rupicapra): relationship between host density and parasite community. Parassitologia. 44(Suppl. 1): 176.
Search in Google Scholar
[38] Stott, P., O’Callaghan, M., Phillips, P., Verbyla, A. (2009): The experimental establishment of ruminant nematodes in European hares (Lepus europaeus). Vet. Parasitol., 159: 82–85. DOI: 10.1016/j.vetpar.2008.10.016 http://dx.doi.org/10.1016/j.vetpar.2008.10.01610.1016/j.vetpar.2008.10.016
Search in Google Scholar
[39] Stringfellow, F. (1972): Comparative morphology of genital cones of Ostertagia from sheep in the United States. J. Parasitol. 58: 265–270. http://dx.doi.org/10.2307/327808610.2307/3278086
Search in Google Scholar
[40] Stunkard, H.W. (1941): Studies on the Life History of the Anoplocephaline Cestodes of Hares and Rabbits. J. Parasitol., 27: 299–325. http://dx.doi.org/10.2307/327281410.2307/3272814
Search in Google Scholar
[41] Tenora, F., Murai, É., Vaucher, C. (1986): On Andrya Railliet, 1893 and Paranoplocephala Lühe, 1910 (Cestoda, Monieziinae). Parasitol. Hung., 19: 43–75
Search in Google Scholar
[42] Tizzani, P., Lavazza, A., Capucci L., Meneguz, P.G. (2002): Presence of infectious agents and parasites in wild population of cottontail (Sylvilagus floridanus) and consideration on its role in the diffusion of pathogens infecting hares. Proceeding of the IV Scientific Meeting of the European Association of Zoo- and Wildlife Veterinarians (EAZWV) joint with the Annual Meeting of the European Wildlife Disease Association (EWDA).
Search in Google Scholar
[43] Trocchi, V., Riga, F. (Eds) (2001): Piano d’azione nazionale per la Lepre italica (Lepus corsicanus). Quaderni di Conservazione della Natura 9: 1–108. Ministero dell’Ambiente, Istituto Nazionale per la Fauna Selvatica.
Search in Google Scholar
[44] Zaffaroni, E., Manfredi, M. T., Citterio, C., Sala, M., Piccolo, G., Lanfranchi, P. (2000): Host specificity of abomasal nematodes in free ranging alpine ruminants. Vet. Parasitol., 90: 221–230. DOI: 10.1016/S0304-4017(00)00240-5 http://dx.doi.org/10.1016/S0304-4017(00)00240-510.1016/S0304-4017(00)00240-5
Search in Google Scholar

Lepus corsicanus gastro-intestinal helminths: first report

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