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Parasite assemblages in the Western whip snake Hierophis viridiflavus carbonarius (Colubridae) from southern Italy

Published online by Cambridge University Press:  13 June 2012

M. Santoro ,
F.J. Aznar ,
S. Mattiucci ,
J.M. Kinsella ,
F. Pellegrino ,
P. Cipriani  and
G. Nascetti
M. Santoro*
Affiliation:
Department of Public Health and Infectious Diseases, Section of Parasitology, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185Rome, Italy Department of Ecology and Biology, Tuscia University, Viale dell'Università sn 01100, Viterbo, Italy
F.J. Aznar
Affiliation:
Instituto Cavanilles de Biodiversidad y Biología Evolutiva, y Departamento de Zoología, Universitat de València, P.O. Box 22085, Valencia46071, Spain
S. Mattiucci
Affiliation:
Department of Public Health and Infectious Diseases, Section of Parasitology, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185Rome, Italy
J.M. Kinsella
Affiliation:
Helm West Laboratory, 2108 Hilda Avenue, Missoula, Montana59801, USA
F. Pellegrino
Affiliation:
Faculty of Natural Sciences, Università della Calabria, Arcavacata di Rende, Cosenza, Italy
P. Cipriani
Affiliation:
Department of Public Health and Infectious Diseases, Section of Parasitology, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185Rome, Italy Department of Ecology and Biology, Tuscia University, Viale dell'Università sn 01100, Viterbo, Italy
G. Nascetti
Affiliation:
Department of Ecology and Biology, Tuscia University, Viale dell'Università sn 01100, Viterbo, Italy
*
* E-mail: marisant@libero.it
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Abstract

Parasite assemblages of the Western whip snake Hierophis viridiflavus carbonarius were investigated from the Calabria region in southern Italy. A total of 14 parasite taxa including 6 nematodes, 3 acanthocephalans, 2 cestodes, 2 digeneans and a single pentastomid was identified. Within the study area, H. v. carbonarius serves as the final host for seven species of helminths, of which only four (Hexametra quadricornis, Kalicephalus viperae, Paracapillaria sonsinoi and Renifer aniarum) can be considered as snake specialists, while one (Oswaldocruzia filiformis) is shared with other reptiles and amphibians, and two (Paradistomum mutabile and Rhabdias fuscovenosa) with lizards. A large proportion of larval forms of six helminth taxa (about 95% of all helminths collected) was found, for which H. v. carbonarius serves as an intermediate and/or paratenic host; however, adult stages of helminths were prevalent in snakes with snout-to-vent length greater than 70 cm. Our results suggest that ontogenetic and ecological factors should exert a strong influence upon the helminth assemblage of Western whip snakes. We concluded that H. v. carbonarius plays an important role in southern Italy as an intermediate/paratenic host for species of helminths infecting vertebrate groups which may include this snake species within their feeding chain. Eleven taxa, including three potential agents of zoonosis, were added to the poorly known parasite fauna of this host.

Type
Research Papers
Information
Journal of Helminthology , Volume 87 , Issue 3 , September 2013 , pp. 277 - 285
Copyright
Copyright © Cambridge University Press 2012 

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References

Aho, J.M. (1990) Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. pp. 157–195in Esch, G.W., Bush, A.O. & Aho, J.M. (Eds) Parasite communities: Patterns and processes. New York, Chapman and Hall.CrossRefGoogle Scholar
Ali, J.H., Riley, J. & Self, J.T. (1985) A review of the taxonomy and systematics of the pentastomid genus Raillietiella Sambon, 1910 with a description of a new species. Systematic Parasitology 7, 111–123.CrossRefGoogle Scholar
Anderson, M.J., Gorley, R.N. & Clarke, K.R. (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. 214 pp. Plymouth, PRIMER-E Ltd.Google Scholar
Anderson, R.C. (2000) Nematode parasites of vertebrates. Their development and transmission. 650 pp. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Biserkov, V. & Kostadinova, A. (1998) Intestinal helminth communities in the green lizard, Lacerta viridis, from Bulgaria. Journal of Helminthology 72, 267–271.CrossRefGoogle ScholarPubMed
Borkovcová, M. & Kopřiva, J.K. (2005) Parasitic helminths of reptiles (Reptilia) in south Moravia (Czech Republic). Parasitology Research 5, 77–78.CrossRefGoogle Scholar
Buchvarov, G., Kirin, D. & Kostadinova, A. (2000) Platyhelminth parasite assemblages in two species of snakes Natrix natrix and Natrix tessellata (Reptilia, Colubridae) from Bulgaria: seasonal variation. Journal of Environmental Protection Ecology 1, 124–131.Google Scholar
Bush, A.O., Heard, R.W. Jr & Overstreet, R.M. (1993) Intermediate hosts as source communities. Canadian Journal of Zoology 71, 1358–1363.CrossRefGoogle Scholar
Capizzi, D., Capula, M., Rugiero, L. & Luiselli, L. (2008) Dietary patterns of two sympatric Mediterranean snakes (Hierophis viridiflavus and Zamenis longissimus) along a gradient of habitat alteration. Herpetological Journal 18, 141–146.Google Scholar
Capuse, I. (1971) Contributions à l'étude des trematodes parasites chez les reptiles du Roumanie. Travaux du Museum d'Histoire Naturelle ‘Grigore Antipa’ 11, 33–40.Google Scholar
Cipriani, P., Mattiucci, S., Paoletti, M., Santoro, M. & Nascetti, G. (2012) Rhabdias esculentarum n. sp. (Nematoda: Rhabdiasidae) from the green frogs of the Rana esculenta species complex in Italy: molecular evidence, morphological description and genetic differentiation from its congeners in frogs and toads. Systematic Parasitology 82, 131–146.CrossRefGoogle Scholar
Clarke, K.R. & Warwick, R.M. (2001) Change in marine communities: an approach to statistical analysis and interpretation. 2nd edn.172 pp. Plymouth, PRIMER-E.Google Scholar
Dollfus, R. (1922) Observations sur la morphologie de Paradistoma mutabile (Molin) (Dicrocoelide nouveau pour la faune française). Bulletin de la Société Zoologique de France 47, 387–404.Google Scholar
Engqvist, L. (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioral and evolutionary ecology studies. Animal Behavior 70, 967–971.CrossRefGoogle Scholar
Galdón, M.A., Roca, V., Barbosa, D. & Carretero, M.A. (2006) Intestinal helminth communities of Podarcis bocagei and Podarcis carbonelli (Sauria: Lacertidae) in NW Portugal. Helminthologia 43, 37–41.CrossRefGoogle Scholar
Jiménez-Ruiz, F.A., García-Prieto, L. & Pérez-Ponce de León, G. (2002) Helminth infracommunity structure of the sympatric garter snakes Thamnophis eques and Thamnophis melanogaster from the Mesa Central of Mexico. Journal of Parasitology 88, 454–460.CrossRefGoogle ScholarPubMed
Jones, H.J. (1995) Pathology associated with physalopterid larvae (Nematoda: Spirurida) in the gastric tissues of Australian reptiles. Journal of Wildlife Diseases 31, 299–306.CrossRefGoogle ScholarPubMed
Kagei, N., Kihata, M., Shimizu, S., Urabe, M. & Ishii, A. (1974) The 10th cases of human infection with Mesocestoides lineatus (Cestoda: Cyclophyllidea) in Japan. Japanese Journal of Parasitology 23, 376–382.Google Scholar
Khalil, L.F., Jones, A. & Bray, R.A. (1994) Keys to the cestode parasites of vertebrates. 751 pp. Wallingford, CAB International.CrossRefGoogle Scholar
Langford, G.J. & Janovy, J. (2009) Comparative life cycles of north American Rhabdias spp. (Nematoda: Rhabdiasidae) from snakes and anurans. Journal of Parasitology 95, 1145–1155.CrossRefGoogle ScholarPubMed
Luiselli, L. & Angelici, F.M. (1996) The prey spectrum of terrestrial snakes in the Tolfa Mountains (Latium, Central Italy). A synthesis from earlier analyses. Herpetozoa 9, 111–119.Google Scholar
Martin, J.E. & Roca, V. (2005) Helminths of the Atlantic lizard, Gallotia atlantica (Reptilia: Lacertidae), in the Canary Islands (Eastern Atlantic): composition and structure of component communities. Acta Parasitologica 50, 85–89.Google Scholar
McAllister, C.T. & Bursey, C.R. (2008) First report of Ochetosoma aniarum from the Brazos water snake, Nerodia harteri, in Texas, with a summary of definitive hosts of this parasite. Texas Journal of Science 60, 63–68.Google Scholar
McAllister, C.T., Conn, D.B., Freed, P.S. & Brudick, D.A. (1991) A new host and locality record for Mesocestoides sp. tetrathyridia (Cestoidea; Cyclophyllidea), with a summary of the genus from snakes of the world. Journal of Parasitology 77, 329–331.CrossRefGoogle ScholarPubMed
McAllister, C.T., Aaron, M. & Russell, A.P. (1995) Nonproliferous tetrathyridia of Mesocestoides sp. (Eucestoda: Mesocestoididea) in Ptenopus garrulus maculatus (Sauria: Gekkonidae) from Namibia, South West Africa, with a summary of the genus from Old World lizards. Journal of Helminthological Society of Washington 62, 94–99.Google Scholar
Mihalca, A.D., Gherman, C., Ghira, I. & Cozma, V. (2007) Helminth parasites of reptiles (Reptilia) in Romania. Parasitology Research 101, 491–492.CrossRefGoogle ScholarPubMed
Moravec, F. (1986) Review of capillariid nematodes (Capillariinae) parasitic in amphibians and reptiles. Part 3. Genus Paracapillaria. Věstník Československé Společnosti Zoologické 50, 273–289.Google Scholar
Naulleau, G. (1997) Coluber viridiflavus Lacépède, 1789. pp. 342–343in Gasc, J.P., Cabela, A., Crnobrnja-Isailovic, J., Dolmen, D., Grossenbacher, K., Haffner, P., Lescure, J., Martens, H., Martinez Rica, J.P., Maurin, H., Oliveira, M.E., Sofianidou, T.S., Veith, M. & Zuiderwijk, A. (Eds) Atlas of amphibians and reptiles in Europe. Paris, Societas Europaea Herpetologica and Museum National d'Histoire Naturelle.Google Scholar
Parona, C. (1897) I tricosomi degli ofidi. Bollettino dei Musei di Zoologia e Anatomia Comparata della R. Università di Genova 58, 1–7.Google Scholar
Petrochenko, V.I. (1971) Acanthocephala of domestic and wild animals. 478 pp. Jerusalem, Israel Program for Scientific Translations Ltd.Google Scholar
Poulin, R. (1997) Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28, 341–358.CrossRefGoogle Scholar
Poulin, R. (2007) Evolutionary ecology of parasites. 332 pp. Princeton, Princeton University Press.CrossRefGoogle Scholar
Reiczigel, J. (2003) Confidence intervals for the binomial parameter: some new considerations. Statistics in Medicine 22, 611–621.CrossRefGoogle ScholarPubMed
Reiczigel, J. & Rózsa, L. (2005) Quantitative parasitology 3.0. Budapest. Available online athttp://www.zoologia.hu/qp/qp.html (accessed accessed June 2011).Google Scholar
Ribas, A., Lopez, S. & Roca, V. (2010) Helminths from snakes from Northeast Spain. Boletín de la Asociación Herpetológica Española 21, 44–46.Google Scholar
Rizzo, A. (1902) La fauna elmintologica dei rettili nella provincia di Catania. Archives de Parasitologie 6, 26–41.Google Scholar
Roca, V. (1995) An approach to the knowledge of the helminth infracommunities of Mediterranean insular lizards (Podarcis spp.). pp. 285–292in Llorente, G., Montori, A., Santos, X. & Carretero, M.A. (Eds) Scientia Herpetologica. Barcelona, AHE.Google Scholar
Roca, V. (1999) Relación entre las faunas endoparásitas de reptiles y su tipo de alimentación. Revista Española de Herpetología 13, 101–121.Google Scholar
Roca, V., Foufopoulos, J., Valakos, E. & Pafilis, P. (2009) Parasitic infracommunities of the Aegean wall lizard Podarcis erhardii (Lacertidae, Sauria): isolation and impoverishment in small island populations. Amphibia–Reptilia 30, 493–503.Google Scholar
Röhlig, D., Dunlop, J.A., Horacio-Grau, J. & Friederichs, A. (2010) An annotated catalogue of the tongue worms (Pentastomida) held in the Museum für Naturkunde Berlin. Zoosystematics and Evolution 86, 129–154.CrossRefGoogle Scholar
Rózsa, L., Reiczigel, J. & Majoros, G. (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232.CrossRefGoogle ScholarPubMed
Rudolphi, C.A. (1819) Entozoorum Synopsis cui Accedunt Mantissa Duplex et Indices Locupletissimi. 811 pp. Berlin, Augusti Rücker.CrossRefGoogle Scholar
Santoro, M., Tripepi, M., Kinsella, J.M., Panebianco, A. & Mattiucci, S. (2010) Helminth infestation in birds of prey (Accipitriformes and Falconiformes) in southern Italy. The Veterinary Journal 186, 119–122.CrossRefGoogle ScholarPubMed
Santoro, M., Tkach, V.V., Mattiucci, S., Kinsella, J.M. & Nascetti, G. (2011) Renifer aniarum (Digenea: Reniferidae), an introduced North American parasite in the grass snake (Natrix natrix) in Calabria, southern Italy. Diseases of Aquatic Organisms 95, 233–240.CrossRefGoogle Scholar
Santoro, M., Kinsella, J.M., Galiero, G., degli Uberti, B. & Aznar, F.J. (2012) Helminth community structures in birds of prey (Accipitriformes and Falconiformes) in southern Italy. Journal of Parasitology 98, 22–29.CrossRefGoogle ScholarPubMed
Santos, X., Martínez-Freiría, F., Pleguezuelos, J.M. & Roca, V. (2006) First helminthological data on Iberian vipers: helminth communities and host–parasite relationships. Acta Parasitologica 51, 130–135.CrossRefGoogle Scholar
Schmidt, G.D. (1986) Handbook of tapeworm identification. 675 pp. Boca Raton, CRC Press Inc.Google Scholar
Sharpilo, V.P. (1976) Parasitic worms of the reptiles of the fauna of the USSR. 287 pp. Kiev, Naukova Dumka.Google Scholar
Sharpilo, V.P., Biserkov, V., Kostadinova, A., Behnke, J.M. & Kuzmin, Y.I. (2001) Helminths of the sand lizard, Lacerta agilis (Reptilia, Lacertidae), in the Palaearctic: faunal diversity and spatial patterns of variation in the composition and structure of component communities. Parasitology 123, 389–400.CrossRefGoogle ScholarPubMed
Shimalov, V.V. (2010) Helminthofauna of reptiles in the Republic of Belarus. Parazitologiya 44, 22–29.Google ScholarPubMed
Shimalov, V.V. & Shimalov, V.T. (2000) Helminth fauna of snakes (Reptilia, Serpentes) in Bielorussian Polesie. Parasitology Research 86, 340–341.CrossRefGoogle Scholar
Shmida, A. & Wilson, M.V. (1985) Biological determinants of species diversity. Journal of Biogeography 12, 1–20.CrossRefGoogle Scholar
Sonsino, P. (1889) Studi e notizie elmintologiche. Atti della Società Toscana di Scienze Naturali, Processi Verbali 6, 224–237.Google Scholar
Sonsino, P. (1893) Trematodi di rettili e anfibi della collezione del Museo di Pisa. Atti della Società Toscana di Scienze Naturali, Processi Verbali 8, 183–190.Google Scholar
Sprent, J.F.A. (1978) Ascaridoid nematodes of amphibians and reptiles: Polydelphis, Travassosascaris n.g. and Hexametra. Journal of Helminthology 52, 355–384.CrossRefGoogle Scholar
Timon-David, J. & Timon-David, P. (1967) Contribution to the knowledge of the biology of the Dicrocoeliidae (Trematoda, Digenea). Experimental studies on the life cycle of Paradistomum mutabile (Molin), parasite of the biliary tract of Lacerta muralis (Laurenti). Annales de Parasitologie Humaine et Comparée 42, 187–206.CrossRefGoogle Scholar
Vogrin, M., Corti, C., Pérez-Mellado, V., Sá-Sousa, P., Cheylan, M., Pleguezuelos, J.M., Meyer, A., Schmidt, B., Sindaco, R., Romano, A. & Martínez-Solano, I. (2011) Hierophis viridiflavus IUCN Red List of Threatened Species, Version 2010.4. Available at websitehttp://www.iucnredlist.org (accessed May 2011).Google Scholar
Yao, M.H., Wu, F. & Tang, L.F. (2008) Human pentastomiasis in China: case report and literature review. Journal of Parasitology 96, 1295–1298.CrossRefGoogle Scholar
Yildirimhan, H.S., Bursey, C.R. & Altunel, F.N. (2011) Helminth parasites of the Balkan green lizard, Lacerta trilineata Bedriaga 1886, from Bursa, Turkey. Turkish Journal of Zoology 35, 519–535.Google Scholar