Diversity of Helminths of Insectivorous Mammals (Mammalia: Eulipothyphla) from Large Forest Protected Areas of the Middle Volga Region (European Russia)
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Area Description
2.2. Parasite Collection and Examination
2.3. Data Analysis
3. Results
3.1. Parasitic Worms of Insectivorous Mammals in the Protected Areas of Mordovia (European Russia)
3.2. List of Helminths of Insectivorous Mammals in the Middle Volga Region
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Sinclair, A.R.E. The role of mammals as ecosystem landscapers. Alces 2003, 39, 161–176. [Google Scholar]
- Lacher, T.E., Jr.; Davidson, A.D.; Fleming, T.H.; Gomez-Ruiz, E.P.; McCracken, G.F.; Owen-Smith, N.; Peres, C.A.; Vander Wall, S.B. The functional roles of mammals in ecosystems. J. Mamm. 2019, 100, 942–964. [Google Scholar] [CrossRef]
- Kirilyuk, A.V.; Kirilyuk, V.E.; Minaev, A.N. Daily activity patterns of wolves in open habitats in the Dauria ecoregion, Russia. Nat. Conserv. Res. 2021, 6, 95–109. [Google Scholar] [CrossRef]
- Sokolova, N.A.; Litvinova, E.M.; Sorokin, P.A.; Hernandez-Blanco, J.A. How Eurasian otters (Lutra lutra) use suboptimal habitats? Space use dynamics in forest streams of Central Russian Upland. Nat. Conserv. Res. 2022, 7, 54–65. [Google Scholar] [CrossRef]
- Coutinho, P.D.F.; Matte, A.L.L.; Bezerra, B. Manatee watching is widespread and seasonally affected in Northeast Brazil: A case of the Endangered Trichechus manatus manatus (Sirenia: Trichechidae). Nat. Conserv. Res. 2023, 8, 61–75. [Google Scholar] [CrossRef]
- Hayward, G.F.; Phillipson, J. Community structure and functional role of small mammals in ecosystems. In Ecology of Small Mammals; Stoddart, D.M., Ed.; Chapman and Hall: London, UK; Wiley: New York, NY, USA, 1979; pp. 135–211. [Google Scholar] [CrossRef]
- Bazhenov, Y.A. Ecology of bat species in the arid region of the Daurian steppe at the peak of drought. Nat. Conserv. Res. 2021, 6, 42–49. [Google Scholar] [CrossRef]
- Martínez-Sotelo, J.; Sanchez-Jasso, J.M.; Ibarra-Zimbron, S.; Sanchez-Nava, P. Zoonotic intestinal parasites in free-ranging dogs (Canis lupus familiaris): A risk to public health in a Mexican Protected Area. Nat. Conserv. Res. 2022, 7, 21–31. [Google Scholar] [CrossRef]
- Kaicheen, S.S.; Mohd-Azlan, J. Community structures of mid-sized to large-bodied mammals in tropical lowland and lower montane forests in Gunung Pueh National Park, Western Sarawak, Borneo. Nat. Conserv. Res. 2022, 7, 70–79. [Google Scholar] [CrossRef]
- Strann, K.; Yoccoz, N.; Ims, R. Is the heart of Fennoscandian rodent cycle still beating? A 14-year study of small mammals and Tengmalm’s owls in northern Norway. Ecography 2002, 25, 81–87. [Google Scholar] [CrossRef]
- Elkinton, J.S.; Liebhold, A.M.; Muzika, R.-M. Effects of alternative prey on predation by small mammals on gypsy moth pupae. Pop. Ecol. 2004, 46, 171–178. [Google Scholar] [CrossRef]
- Davidson, A.D.; Detling, J.; Brown, J.H. Ecological roles and conservation challenges of social, burrowing, herbivorous mammals in the world’s grasslands. Front. Ecol. Environ. 2012, 10, 477–486. [Google Scholar] [CrossRef] [PubMed]
- Kollberg, I.; Bylund, H.; Huitu, O.; Björkman, C. Regulation of forest defoliating insects through small mammal predation: Reconsidering the mechanisms. Oecologia 2014, 176, 975–983. [Google Scholar] [CrossRef] [PubMed]
- Krebs, C.J.; Boonstra, R.; Boutin, S.; Sinclair, A.R.E.; Smith, J.N.M.; Gilbert, B.S.; Martin, K.; O’Donoghue, M.; Turkington, R. Trophic dynamics of the boreal forests of the Kluane region. Arctic 2014, 67, 71–81. [Google Scholar] [CrossRef]
- Bobretsov, A.V. Population Ecology of Small Mammals in Plain and Mountain Landscapes of the North-East of the European Part of Russia; KMK: Moscow, Russia, 2016; pp. 3–381. [Google Scholar]
- Yakimova, A.E.; Gaidysh, I.S. The species composition and abundance of terrestrial small mammals in the Finnish-Russian Friendship Nature Reserve. Nat. Conserv. Res. 2021, 6, 127–136. [Google Scholar] [CrossRef]
- Churchfield, S. The Natural History of Shrews; Comstock Pub. Associates: New York, NY, USA, 1990; pp. 3–178. [Google Scholar]
- Khodasheva, K.S.; Eliseeva, V.I. Shrews in the Ecosystems of the Central Forest-Steppe of the Russian Plain; Science: Moscow, Russia, 1992; pp. 3–212. [Google Scholar]
- Liebhold, A.M.; Elkinton, J.; Williams, D.; Muzika, R. What causes outbreaks of the gypsy moth in North America? Pop. Ecol. 2000, 42, 257–266. [Google Scholar] [CrossRef]
- Rutovskaya, M.V.; Aleksandrov, A.N.; Podshivalina, V.N.; Soboleva, A.S.; Glushenkov, O.V. Habitat conditions of Desmana moschata (Talpidae, Eulipotyphla, Mammalia) in the buffer zone of the Prisurskiy State Nature Reserve (Russia). Nat. Conserv. Res. 2020, 5, 36–46. [Google Scholar] [CrossRef]
- Shchipanov, N.A.; Alexandrov, D.Y.; Alexandrova, A.V. Distribution of spores of microscopic fungi of small mammals. Zool. Zhurn. 2006, 85, 101–113. [Google Scholar]
- Alexandrov, D.Y. Distribution of Microscopic Fungal Spores on the Fur of Small Mammals. Ph.D. Thesis, Institute of Problems of Ecology and Evolution of RAS, Moscow, Russia, 2008; 172p. [Google Scholar]
- Shimalov, V.V. Helminth fauna in insectivores of canal bamks in meliorared territories. Parazitologiia 2007, 41, 201–205. [Google Scholar] [PubMed]
- Romashov, B.V.; Odoevskaya, I.M.; Romashova, N.B.; Golubova, N.A. Ecology of trichinellosis transmission in the Voronezh State Nature Reserve and adjacent areas, Russia. Nat. Conserv. Res. 2021, 6, 1–15. [Google Scholar] [CrossRef]
- Kirillov, A.A.; Kirillova, N.Y.; Ruchin, A.B. Helminths of Erinaceus roumanicus (Eulipotyphla, Erinaceidae) in Mordovia (Russia) with an overview of helminth fauna of Erinaceus spp. inhabiting the Palaearctic region. Diversity 2022, 14, 165. [Google Scholar] [CrossRef]
- Price, P.W. Evolutionary Biology of Parasites; Princeton University Press: Princeton, NJ, USA, 1980; pp. 3–237. [Google Scholar]
- Poulin, R.; Morand, S. Parasite Biodiversity; Smithsonian Institution Press: Washington, DC, USA, 2004; pp. 3–216. [Google Scholar]
- Horwitz, P.; Wilcox, B. Parasites, ecosystems and sustainability: An ecological and complex systems perspective. Int. J. Parasitol. 2005, 35, 725–732. [Google Scholar] [CrossRef] [PubMed]
- Poulin, R. Phylogeny, ecology and the richness of parasite communities in vertebrates. Ecol. Monogr. 1995, 65, 283–302. [Google Scholar] [CrossRef]
- Lafferty, K.D.; Allesina, S.; Arim, M.; Briggs, C.J.; De Leo, G.; Dobson, A.P.; Dunne, J.A.; Johnson, P.T.; Kuris, A.M.; Marcogliese, D.J.; et al. Parasites in food webs: The ultimate missing links. Ecol. Lett. 2008, 11, 533–546. [Google Scholar] [CrossRef] [PubMed]
- Marcogliese, D.J. Parasites: Small players with crucial roles in the ecological theater. EcoHealth 2004, 1, 151–164. [Google Scholar] [CrossRef]
- Stammer, H.J. Die Parasiten deutscher kleinsauger verhandlungen der Deutschen zoologischen gesselschaft in Erlangen. Zool. Anz. 1956, 19, 362–390. [Google Scholar]
- Brendow, V. Ein beitrag zur trematodenfauna der Soricidae im raume gieben sowie im Naturpark Hoher Vogelsberg. Z. Parasitenk. 1970, 33, 282–313. [Google Scholar] [CrossRef] [PubMed]
- Vaucher, C. Les cestodes, parasites de Soricidae d’Europe. Etude anatomique, revision taxonomique et biologie. Rev. Suisse Zool. 1971, 78, 1–113. [Google Scholar] [CrossRef]
- Pecher, W.T.; Mokhtari-Derakhshan, F.; Böckeir, W. Epidemiologische Bemerkungen zur Helminthen fauna von zwei Spitzmausarten (Sorex araneus L. 1758, S. minutus L., 1766) mit unterschiedlichen ökologischen Ansprüchen. Mitt. Osterr. Ges. Trop. Med. Parasitol. 1996, 18, 183–190. [Google Scholar]
- Pfaffle, M.P.; Bolfíkova, B.C.; Hulva, P.; Petney, T. Different parasite faunas in sympatric populations of sister hedgehog species in a secondary contact zone. PLoS ONE 2014, 9, e114030. [Google Scholar] [CrossRef]
- Lambert, D. Parasitosen und Mykosen des Igels, 2nd ed.; Pro Igel e.V., Arbeitskreis Igelschutz Berlin e.V.: Berlin, Germany, 2019; pp. 3–149. [Google Scholar]
- Soltys, A. The helminthes of common shrew (Sorex araneus L.) of the National Park of Bialowieza (Poland). Ann. Univ. Marie Curie Sklodowska 1952, 5, 165–202. [Google Scholar]
- Soltys, A. Helmintofauna of Soricidae in the Bialowieza National Park. Acta Parasitol. Polon. 1954, 16, 353–402. [Google Scholar]
- Zarnowski, E. Parasitic worms of forest micromammalians (Rodentia and Insectivora) of the enviroment of Pulawy (district Lublin). I. Cestoda. Acta Parasitol. Polon. 1955, 8, 127–168. [Google Scholar]
- Zarnowski, E. Parasitic worms of forest micromammalians (Rodentia and Insectivora) of the enviroment of Pulawy (district Lublin). II. Trematoda. Acta Parasitol. Polon. 1960, 3, 279–368. [Google Scholar]
- Furmaga, F. Materials to the helminth fauna of hedgehogs Erinaceus roumanicus Barrett-Hamilton. Acta Parasitol. 1961, 9, 441–445. [Google Scholar]
- Kisielewska, K. Circulation of tapeworms in Sorex araneus L. in biocenosis of Bialowieza National Park. Acta Parasitol. Polon. 1961, 9, 331–369. [Google Scholar]
- Pojmanska, T. Investigations on the occurrence and biology of trematodes of Sorex araneus araneus L. in Bialowieza National Park. Acta Parasitol. Polon. 1961, 9, 305–330. [Google Scholar]
- Mizgajska-Wiktor, H.; Jarosz, W.; Pilacinska, B.; Dziemian, S. Helminths of hedgehogs, Erinaceus europaeus and E. roumanicus from Poznan region, Poland–coprological study. Wiad. Parazytol. 2010, 56, 329–332. [Google Scholar] [PubMed]
- Merkusheva, I.V.; Bobkova, A.F. Helminths of Domesticated and Wild Animals in Belarus; Nauka i Tehnika: Minsk, Belarus, 1981; pp. 3–120. [Google Scholar]
- Shimalov, V.V.; Shimalov, V.V. Helminth fauna of the European mole (Talpa europea Linnaeus, 1758) in Bielorussian Polesie. Parasitol. Res. 2001, 87, 790–791. [Google Scholar] [CrossRef] [PubMed]
- Shimalov, V.V. Monitoring of the helminth of insectivorous of meliorative canal banks in Belorussian Polesie. Parazitologiia 2012, 46, 472–478. [Google Scholar]
- Shimalov, V.V. Helminth parasites of the Eurasian water shrew (Neomys fodiens Pennant, 1771) in South-West Belarus. J. Parasit. Dis. 2017, 41, 602–604. [Google Scholar] [CrossRef]
- Bychkova, E.I.; Akimova, L.N.; Degtyarik, S.M.; Yakovich, M.M. Helminths of Vertebrates and Man in Belarus; Belarusskaya Nauka Publishing House: Minsk, Belarus, 2017; pp. 3–316.
- Shimalov, V.V.; Zhukovsky, A.T. The Bicolored Shrew (Crocidura leucodon Hermann, 1780) and its helminth fauna on the reclamation systems of the Brest Polesie. Proc. Brest Univ. 2019, 2, 55–59. [Google Scholar]
- Genov, T. Helminths of Insectivores and Rodents in Bulgaria; Bulgarian Academy of Sciences: Sofia, Bulgaria, 1984; pp. 3–348. [Google Scholar]
- Vasileva, G.P.; Tkach, V.V.; Genov, T. Two new hymenolepidid species (Cestoda, Hymenolepididae) from water shrews Neomys fodiens Pennant (Insectivora, Soricidae) in Bulgaria. Acta Parasitol. 2005, 50, 56–64. [Google Scholar]
- Prokopic, J. Faunistic study of helminths of shrews from the genus Neomys. Acta Soc. Zool. Boh.-Slov. 1957, 21, 44–64. [Google Scholar]
- Prokopic, J. Vysledky helmintologickeho vyzkumu nasich jezku. Vest. Ceskosl. Zool. Spol. 1957, 21, 97–111. [Google Scholar]
- Prokopic, J. The parasitic helminths of insectivora in CSR. Cesk. Parasitol. 1959, 6, 87–134. [Google Scholar]
- Meszaros, F.; Stollmann, A. Results of complex parasitological investigations on small mammals in the Cergov Mountains (Western Carpathians, Czechoslovakia). Misc. Zool. Hung. 1984, 2, 7–11. [Google Scholar]
- Murai, E.; Meszaros, F. Helminths from small mammals in the Cergov Mountains (Western Carpatians, Czecoslovakia). Misc. Zool. Hung. 1984, 2, 17–28. [Google Scholar]
- Slapeta, J.R. Endoparasites of hedgehogs in the Czech Republic. Veterinarstvi 1999, 49, 248–252. [Google Scholar]
- Mas-Coma, S. Metastrongylides parasites des Soricides d’Europe. Ann. Parasitol. 1977, 52, 447–456. [Google Scholar] [CrossRef]
- Cordero del Campillo, M.; Castanon Ordonez, L.; Reguera Feo, A. Index-Catalogue of Iberian Parasites of Animals, 2nd ed.; Universidad de Leon, Secretariado de Publicaciones: Leon, Spain, 1994; pp. 3–650. [Google Scholar]
- Fuentes, M.V.; Cerezuela, A.M.; Galan-Puchades, M.T. A helmithological survey of small mammals (insectivores and rodents) in the Serra Calderona mountains (Valencian Community, Spain). Res. Rev. Parasitol. 2000, 60, 25–35. [Google Scholar]
- Mas-Coma, S.; Esteban, J.G.; Fuentes, M.V.; Bargues, M.D.; Valero, M.A.; Galan-Puchades, M.T. Helminth parasites of small mammals (insectivores and rodents) on the Pityusic Island of Eivissa (Balearic Archipelago). Res. Rev. Parasitol. 2000, 60, 41–49. [Google Scholar]
- Feliu, C.; Blasco, S.; Torres, J.; Miquel, J.; Casanova, J.C. On the helminthfauna of Erinaceus europaeus Linnaeus, 1758 (Insectivora, Erinaceidae) in the Iberian Peninsula. Res. Rev. Parasitol. 2001, 61, 31–37. [Google Scholar]
- Portoles, E.; Granel, P.; Esteban, J.G.; Cabaret, J. Helminth associations in white-toothed shrews Crocidura russula (Insectivora: Soricidae) from the Albufera Natural Park, Spain. J. Parasitol. 2004, 90, 572–578. [Google Scholar] [CrossRef] [PubMed]
- Ribas, A.; Casanova, J.C. Helminth parasites of Talpa europaea (Insectivora, Talpidae) in southwestern Europe. Acta Parasitol. 2005, 50, 161–167. [Google Scholar]
- Galan-Puchades, M.T.; Mas-Coma, S.; Valero, M.A.; Fuentes, M.V. First data on the helminth community of the smallest living mammal on Earth, the Etruscan pygmy shrew, Suncus etruscus (Savi, 1822) (Eulipotyphla: Soricidae). Animals 2021, 11, 2074. [Google Scholar] [CrossRef] [PubMed]
- Bernard, L. Quelques especes d’helminthes de micromammiferes recoltes en France et en Espagne. Vie Milieu 1961, 2, 125–149. [Google Scholar]
- Euset, L.; Jourdane, J. Helminthes parasites des micromammiferes des Pyrenees-Orientales. I, cestodes de Neomys fodiens (Schreber). Bull. Soc. Neuchatel. Sci. Nat. 1968, 91, 31–42. [Google Scholar]
- Jourdane, J. Deux nouvelles especes de Trematodes parasites des Soricinae dans les Pyrenees. Ann. Parasitol. 1973, 58, 667–676. [Google Scholar] [CrossRef]
- Quentin, J.C. Nematodes parasites de musareignes en Sologne. Symbioses 1986, 18, 265–279. [Google Scholar]
- Joyeux, C.; Baer, J.G. Quelques helminthes nouveaux et peu connus de la musaraigne, Crocidura russula Herm. (Premiere partie, Trematodes et Cestodes). Rev. Suiss. Zool. 1936, 43, 25–50. [Google Scholar]
- Joyeux, C.; Baer, J.G. Quelques helminthes nouveaux et peu connus de la musaraigne, Crocidura russula Herm. (Deuxieme partie, Nematodes et Acanthocephales). Rev. Suiss. Zool. 1937, 44, 27–40. [Google Scholar]
- Vaucher, C.; Hunkeler, P. Contribution to the study of cestodes and trematodes parasites of micromammals in Switzerland I. Bull. Neuchatel Soc. Nat. Sci. 1967, 90, 161–184. [Google Scholar]
- Liesegang, A.; Lehmann, M.C. Haufigkeit von krankheit und abgangsursachen bei igeln. Schweiz. Arch. Tierheil. 2003, 145, 589–591. [Google Scholar] [CrossRef] [PubMed]
- Edelenyi, B. Saugwürmer in einheimischen Kleinsäugern II. Ann. Hist.-Nat. Mus. Nat. Hung. 1965, 57, 217–222. [Google Scholar]
- Murai, E.; Meszaros, F.; Sey, O. On parasitic helminths of mammals living in the environs of Lake Balaton. Parasitol. Hung. 1992, 25, 23–36. [Google Scholar]
- Žąsityte, R.; Grikieniene, J. Some data on endoparasites of common mole in Lithuania. Acta Zool. Lituan. 2002, 12, 403–409. [Google Scholar] [CrossRef]
- Žąsityte, R. Cestodes of shrews (Insectivora, Soricidae) from Lithuania. Ekologija 2001, 3, 19–22. [Google Scholar]
- Binkiene, R. Helminth fauna of shrews (Sorex spp.) in Lithuania. Acta Zool. Lituan. 2006, 16, 241–245. [Google Scholar] [CrossRef]
- Haukisalmi, V. Intestinal helminth communities of Sorex shrews in Finland. Ann. Zool. Fenn. 1989, 26, 401–409. [Google Scholar]
- Haukisalmi, V.; Henttonen, H. Distribution patterns and microhabitat segregation in gastrointestinal helminths of Sorex shrews. Oecologia 1994, 97, 236–242. [Google Scholar] [CrossRef]
- Haukisalmi, V. Checklist of tapeworms (Platyhelminthes, Cestoda) of vertebrates in Finland. ZooKeys 2015, 533, 1–61. [Google Scholar] [CrossRef] [PubMed]
- Rautio, A.; Isomursu, M.; Valtonen, A.; Hirvela-Koski, V.; Kunnasranta, M. Mortality, diseases and diet of European hedgehogs (Erinaceus europaeus) in an urban environment in Finland. Mammal Res. 2016, 61, 161–169. [Google Scholar] [CrossRef]
- Bychovskaya-Pavlovskaya, I.E.; Vysotzkaya, S.O.; Kulakova, A.P. Trematodes of small mammals from Transkarpathian region. Parazitologiia 1970, 4, 25–33. [Google Scholar]
- Melnichenko, E.D.; Panasenko, N.A. To the helminth fauna of some insectivorous mammals of the Middle Dnieper region. Vestn. Zool. 1979, 5, 79–81. [Google Scholar]
- Iskova, N.I.; Sharpilo, V.P.; Sharpilo, L.D.; Tkach, V.V. Catalogue of Helminths of Vertebrates in the Ukraine. Trematodes of Terrestrial Vertebrates; Naukova Dumka: Kiev, Ukraine, 1995; pp. 3–93. [Google Scholar]
- Vysotskaya, S.O. Helminths of small mammals from Transcarpathian region (The East Carpathians, Ukraine). Parazitologiia 1997, 31, 346–353. [Google Scholar]
- Andreyko, O.F.; Spassky, A.A. Nematodes of insectivorous mammals from Prut-Dniester interfluve. Par. Anim. Plant. 1969, 4, 44–59. [Google Scholar]
- Andreyko, O.F. Trematodes of insectivores (Insectivora) in Moldavia. Par. Anim. Plant. 1970, 5, 3–17. [Google Scholar]
- Andreyko, O.F.; Spassky, A.A. Cestodes of insectivorous mammals in Moldavia. Par. Anim. Plant. 1970, 5, 44–59. [Google Scholar]
- Andreyko, O.F. Overview of helminth fauna of insectivores (Insectivora) of the USSR and adjacent countries. Par. Anim. Plant. 1973, 9, 3–34. [Google Scholar]
- Andreyko, O.F. Parasites of Mammals in Moldavia; Știința: Chisinau, Moldova, 1973; pp. 3–185. [Google Scholar]
- Lewis, J.W. Studies on the helminth parasites of voles and shrews from Wales. J. Zool. 1968, 154, 313–331. [Google Scholar] [CrossRef]
- Lewis, J.W. Helminth parasites of British rodents and insectivores. Mammal Rev. 1987, 17, 81–93. [Google Scholar] [CrossRef]
- Boag, B.; Fowler, P. The prevalence of helminth parasites from the hedgehog Erinaceus europaeus in Great Britain. J. Zool. 1988, 215, 379–382. [Google Scholar] [CrossRef]
- Bunnell, T. The incidence of disease and injury in displaced wild hedgehogs (Erinaceus europaeus). Lutra 2001, 44, 3–14. [Google Scholar]
- Gaglio, G.; Allen, S.; Bowden, L.; Bryant, M.; Morgan, E.R. Parasites of European hedgehogs (Erinaceus europaeus) in Britain: Epidemiological study and coprological test evaluation. Eur. J. Wildl. Res. 2010, 56, 839–844. [Google Scholar] [CrossRef]
- Haigh, A.; O’Keeffe, J.; O’Riordan, R.M.; Butler, F. A preliminary investigation into the endoparasite load of the European hedgehog (Erinaceus europaeus) in Ireland. Mammalia 2013, 78, 103–107. [Google Scholar] [CrossRef]
- Bernard, J. Liste des nematodes parasites des micromarnmiferes de la faune Beige. Ann. Parasitol. Hum. Comp. 1961, 6, 775–784. [Google Scholar] [CrossRef]
- Rasmussen, S.L.; Hallig, J.; van Wijk, R.E.; Petersen, H.H. An investigation of endoparasites and the determinants of parasite infection in European hedgehogs (Erinaceus europaeus) from Denmark. Int. J. Parasitol. Par. Wildl. 2021, 16, 217–227. [Google Scholar] [CrossRef] [PubMed]
- Casanova, J.C.; Miquel, J.; Fons, R.; Molina, X.; Feliu, C.; Mathias, M.L.; Torres, J.; Libois, R.; Santos-Reis, M.; Collares-Pereira, M.; et al. On the helminthfauna of wild mammals (Rodentia, Insectivora and Lagomorpha) in Azores archipelago (Portugal). Vie Milieu/Life Environ. 1996, 46, 253–259. [Google Scholar]
- Fuentes, M.V.; Saez, S.; Trellis, M.; Cruz, J.; Sarmento, P.; Casanova, J.C.; Torres, J.; Feliu, C.; Esteban, J.G. Helmintofauna of small mammals (Insectivora, Rodentia) collected in the Serra da Malcata (Portugal). Rev. Iber. Parasitol. 2003, 63, 89–92. [Google Scholar]
- Milazzo, C.; Casanova, J.C.; Aloise, G.; Ribas, A.; Cagnin, M. The helminth community of Talpa romana (Thomas, 1902) (Insectivora, Talpidae) in southern Italy. Parasitol. Res. 2002, 88, 979–983. [Google Scholar]
- Poglayen, G.; Giannetto, S.; Scala, A.; Garippa, G.; Capelli, G.; Scaravelli, D.; Brianti, E.; Reeve, N.J. Helminths found in hedgehogs (Erinaceus europaeus) in three areas of Italy. Vet. Rec. 2003, 152, 22–24. [Google Scholar] [CrossRef] [PubMed]
- Mariacher, A.; Santini, A.; Del Lesto, I.; Tonon, S.; Cardini, E.; Barone, A.; Eleni, C.; Fichi, G.; Perrucci, S. Endoparasite infections of the European hedgehog (Erinaceus europaeus) in Central Italy. Animals 2021, 11, 3171. [Google Scholar] [CrossRef] [PubMed]
- Prokopic, J.; Mahnert, V. Über Helminthen der Kleinseuger (Insectivora, Rodentia) Tirols (Osterreichs). Ber. Naturwiss.-Med. Ver. Innsbr. 1970, 58, 143–154. [Google Scholar]
- Hoerweg, C. The helminth fauna of the common shrew, Sorex araneus L., from two sites near Vienna, Austria. Bull. Scandinav. Soc. Parasitol. 2000, 10, 112. [Google Scholar]
- Liatis, T.K.; Monastiridis, A.A.; Birlis, P.; Prousali, S.; Diakou, A. Endoparasites of wild mammals sheltered in wildlife hospitals and rehabilitation centres in Greece. Front. Vet. Sci. 2017, 4, 220. [Google Scholar] [CrossRef]
- Pavlovic, I.; Savic, B. Helminth fauna of the northern white-breasted hedgehog (Erinaceus roumanicus) in Serbia. J. Parasit. Dis. 2017, 41, 605–606. [Google Scholar] [CrossRef]
- Chiriak, E.; Hamar, M. Contributions a la connaissance des helminthes des petits mammiferes (Rongeurs, Insectivores) de la Roumanie. Acta Parasitol. Polon. 1966, 14, 61–72. [Google Scholar]
- Ribas, A.; Casanova, J.C. Helminth fauna of Talpa spp. in the Palaearctic Realm. J. Helminthol. 2006, 80, 1–6. [Google Scholar] [CrossRef]
- Nikonorova, I.A.; Binkiene, R.; Bugmyrin, S.V.; Ieshko, E.P. Helminth fauna of the common shrew Sorex araneus L. in the European part of the species range. Parazitologiia 2018, 52, 41–69. [Google Scholar]
- Haukisalmi, V.; Hardman, L.M.; Foronda, P.; Feliu, C.; Laakkonen, J.; Niemimaa, J.; Lehtonen, J.T.; Henttonen, H. Systematic relationships of hymenolepidid cestodes of rodents and shrews inferred from sequences of 28S ribosomal RNA. Zool. Scr. 2010, 39, 631–641. [Google Scholar] [CrossRef]
- Binkiene, R.; Kontrimavichus, V.; Hoberg, E.P. Overview of the cestode fauna of European shrews of the genus Sorex with comments on the fauna in Neomys and Crocidura and an exploration of historical processes in post-glacial Europe. Helminthologia 2011, 48, 207–228. [Google Scholar] [CrossRef]
- Binkiene, R.; Kornienko, S.A.; Tkach, V.V. Soricinia genovi n. sp. from Neomys fodiens in Bulgaria, with redescription of Soricinia globosa (Baer, 1931) (Cyclophyllidea: Hymenolepididae). Parasitol. Res. 2015, 114, 209–218. [Google Scholar] [CrossRef] [PubMed]
- Kornienko, S.A.; Binkiene, R. Redescription and systematic position of Soricinia tripartita Żarnowski, 1955 (Cestoda: Cyclophyllidea), a cestode species parasitic in shrews of the genus Sorex, including erection of Gulyaevilepis gen. n. Fol. Parasitol. 2014, 61, 141–147. [Google Scholar] [CrossRef]
- Neov, B.; Vasileva, G.P.; Radoslavov, G.; Hristov, P.; Littlewood, D.T.J.; Georgiev, B.B. Phylogeny of hymenolepidid cestodes (Cestoda: Cyclophyllidea) from mammalian hosts based on partial 28S rDNA, with focus on parasites from shrews. Parasitol. Res. 2019, 118, 73–88. [Google Scholar] [CrossRef] [PubMed]
- Binkiene, R. Specific and non-specific cestodes of shrews (Eulipotyphla: Soricidae) in Europe with a description of Coronacanthus longicirrosus n. sp (Cestoda: Hymenolepididae). Syst. Parasitol. 2021, 98, 321–332. [Google Scholar] [CrossRef]
- Yushkov, V.F. Helminth fauna of mammals (insectivores, predators, lagomorphs and rodents) of the Komi ASSR. Tr. Gel’mintologicheskoi Lab. 1971, 22, 232–248. [Google Scholar]
- Yushkov, V.Y. Helminths of Mammals. Fauna of the European North-East of Russia; Nauka: St. Petersburg, Russia, 1995; Volume 3, pp. 3–202. [Google Scholar]
- Novikov, M.V. The trematodes and cestodes of Sorex araneus L. in Valaam island (Ladoga Lake, USSR). Mem. Inst. Oswaldo Cruz 1992, 87, 155–160. [Google Scholar] [CrossRef]
- Anikanova, V.S.; Ieshko, E.P.; Bugmyrin, S.V.; Borodina, K.A. Peculiarities of biotopic distribution of cestodes from the common shrew Sorex araneus in southern Karelia. Parazitologiia 2003, 37, 479–487. [Google Scholar] [PubMed]
- Anikanova, V.S.; Ieshko, E.P.; Boyko, N.S. Helminths of shrews of genus Sorex (Soricidae, Insectivora) from the Kandalaksha Reserve. Parazitologiia 2005, 39, 559–568. [Google Scholar]
- Anikanova, V.S.; Bugmyrin, S.V.; Ieshko, E.P. Methods of the Collection and Studies of Helminths of Small Mammals; Karelian Scientific Center of RAS: Petrozavodsk, Russia, 2007; pp. 3–145. [Google Scholar]
- Anikanova, V.S.; Ieshko, E.P.; Bugmyrin, S.V. Dynamics of the helminth fauna in the common shrew (Sorex araneus L.) from cut-over lands of different age in Karelia. Parazitologiia 2009, 43, 79–89. [Google Scholar]
- Nikanorova, I.A.; Kutenkov, A.P.; Bugmyrin, S.V.; Ieshko, E.P. Helminths of the common shrew Sorex araneus in the Kivach Nature Reserve. Proc. Karel. Sci. Cent. RAS 2019, 1, 106–111. [Google Scholar] [CrossRef]
- Kirillova, N.Y. Helminth fauna of insectivorous mammals (Insectivora) of Samarskaya Luka. Proc. Sam. Sci. Cent. RAS 2004, 6, 334–340. [Google Scholar]
- Kirillova, N.Y.; Kirillov, A.A. Helminth fauna of the common shrew Sorex araneus L. (Soricidae) from Samarskaya Luka. Parazitologiia 2007, 41, 392–398. [Google Scholar] [PubMed]
- Kirillova, N.Y. Helminths in Small Mammals from the Samarskaya Luka (Fauna and Ecology); Lambert Academic Publishing: Saarbrucken, Germany, 2011; pp. 3–251. [Google Scholar]
- Kirillova, N.Y.; Kirillov, A.A. Overview of helminths in small mammals in the Zhiguli State Reserve. Nat. Conserv. Res. 2017, 2, 24–37. [Google Scholar] [CrossRef]
- Kirillov, A.A.; Kirillova, N.Y.; Krasnobaev, Y.P.; Vekhnik, V.P. Parasitic Worms of Small Mammals of Zhiguli State Reserve. Flora and Fauna of Reserves; Committee of RAS for the Conservation of Biological Diversity: Moscow, Russia, 2017; Volume 128, 77p. [Google Scholar]
- Troitskaya, A.A. Helminth fauna of wild fur animals in the Tatarskaya ASSR. Proc. Soc. Natur. 1960, 63, 335–358. [Google Scholar]
- Lubarskaya, O.D. On the nematode fauna of Neomys fodiens. Zool. Zhurn. 1962, 41, 833–838. [Google Scholar]
- Dubinin, E.B. Parasite fauna of myomorph rodents and its changes in the Volga delta. Parasitol. Misc. 1953, 15, 252–301. [Google Scholar]
- Ivanov, V.M. Monitoring, Structural Changes and Ecological Features of the Trematode Fauna of Vertebrates in the Volga Delta and North of the Caspian Sea. Ph.D. Thesis, Institute for Parasitology of RAS, Moscow, Russia, 2003; 323p. [Google Scholar]
- Petrov, A.M.; Savinov, V.A. Helminth fauna of moles in the Vologda region. Misc. Vologda Res. Vet. Stat. 1956, 3, 107–115. [Google Scholar]
- Romashov, B.V. Capillariids (Nematoda, Capillariidae) from the bladder of shrews: Capillaria incrassata and C. konstantini sp. n. Zool. Zhurn. 1999, 78, 929–938. [Google Scholar]
- Romashova, N.B. Retrospective analysis of the helminth fauna of mammals in the Khopersky Nature Reserve. In The State of Specially Protected Areas in the European Part of Russia; Voronezh State University: Voronezh, Russia, 2005; pp. 418–423. [Google Scholar]
- Vlasov, E.A. First data on the helminth fauna of the shrews (Eulipotyphila, Soricidae) from Central Chernozem State Nature Reserve. In Contemporary Problems of Zoology and Parasitology: Proceedings of the VII International Scientific Conference Voronezh, Russia, 10 April 2015; VSU Publishing House: Voronezh, Russia, 2015; pp. 32–38. [Google Scholar]
- Vlasov, E.A. Helminths of Wild Mammals of the Central Chernozem Reserve (Fauna, Ecology, Pathogenic Significance). Ph.D. Thesis, All-Russian Scientific Research Institute for Fundamental and Applied Parasitology of Animals and Plants, Moscow, Russia, 2017; 166p. [Google Scholar]
- Vasilyev, V.V. Parasites fauna of rodents and insectivorous from vicinity of Leningrad. Proc. Leningrad Univ. Biol. Ser. 1949, 101, 73–80. [Google Scholar]
- Fedoseev, S.D. To the nematode fauna in mammals from the Gorky region. Proc. Gorky St. Ped. Inst. 1937, 1, 121–133. [Google Scholar]
- Morosov, F.N. Helminth fauna of moles in Gorky region. Proc. Gorky St. Ped. Inst. 1957, 19, 27–29. [Google Scholar]
- Kostyunin, V.M. Materials for the study of the trematode fauna of the common shrew in the Nizhny Novgorod region. In Zoological Studies of Regions of Russia and Adjacent Territories; Zryanin, V.A., Ed.; Novosibirsk State Pedagogical University: Novosibirsk, Russia, 2002; pp. 124–125. [Google Scholar]
- Petrov, A.M.; Savinov, V.A. To the helminth fauna in moles in the Kalinin region. Proc. All-Union Inst. Helminthol. 1959, 6, 160–166. [Google Scholar]
- Shaldybin, L.S. Helminth fauna of mammals in Mordovia State Nature Reserve. Proc. Mord. St. Nat. Res. 1964, 2, 135–180. [Google Scholar]
- Ruchin, A.B.; Kirillov, A.A.; Chikhlyaev, I.V.; Kirillova, N.Y. Parasitic Worms of Land Vertebrates of the Mordovia Nature Reserve. Flora and Fauna of Reserves; Committee of RAS for the Conservation of Biological Diversity: Moscow, Russia, 2016; Volume 124, pp. 3–72. [Google Scholar]
- Kirillova, N.Y.; Ruchin, A.B.; Kirillov, A.A.; Chikhlyaev, I.V.; Alpeev, M.A. Overview of helminths in land vertebrates from the Mordovia Nature Reserve, European Russia. Nat. Environ. Pollut. Technol. 2023, 22, 1667–1690. [Google Scholar] [CrossRef]
- Artaev, O.N.; Ruchin, A.B.; Bugaev, K.E.; Grishutkin, G.F.; Potapov, S.K.; Spiridonov, S.N. Vertebrates of the Mordovia State Nature Reserve. Flora and Fauna of Reserves; Committee of RAS for the Conservation of Biological Diversity: Moscow, Russia, 2012; Volume 120, pp. 3–64. [Google Scholar]
- Grishutkin, O.G. Patterns of the distribution of swamps depending on the absolute marks of the relief on the territory of the Mordovia State Nature Reserve. Proc. Mord. St. Nat. Res. 2013, 11, 259–263. [Google Scholar]
- Artaev, O.N.; Grishutkin, O.G. Lakes of Mordovia. Mord. Res. 2014, 6, 20–23. [Google Scholar]
- Artaev, O.N.; Smirnov, D.G. Bats (Chiroptera; Mammalia) of Mordovia: Specific structure and features of distribution. Nat. Conserv. Reserve 2016, 1, 38–51. [Google Scholar] [CrossRef]
- Grishutkin, G.F.; Lapshin, A.S.; Spiridonov, S.N.; Artaev, O.N.; Ruchin, A.B.; Kuznetsov, V.A.; Andreychev, A.V. Vertebrate Animals of National Park “Smolny”. Flora and Fauna of Reserves; Committee of RAS for the Conservation of Biological Diversity: Moscow, Russia, 2013; pp. 3–56. [Google Scholar]
- Kirillova, N.Y.; Kryštufek, B.; Kirillov, A.A.; Ruchin, A.B.; Grishutkin, G.F. The first record of Microtus subterraneus (de Sélys-Longchamps, 1836) (Rodentia, Cricetidae) for Mordovia, Russia. Acta Biol. Sib. 2019, 5, 145–149. [Google Scholar] [CrossRef]
- Smirnov, D.G.; Kirillova, N.Y.; Kirillov, A.A.; Ruchin, A.B.; Vekhnik, V.A. New records of Nyctalus leisleri (Kuhl, 1817) and Myotis nattereri (Kuhl, 1817) (Mammalia: Chiroptera: Vespertilionidae) from National Park “Smolny” and its surroundings, Republic of Mordovia. J. Threat. Taxa 2022, 14, 21553–21560. [Google Scholar] [CrossRef]
- Kirillova, N.Y.; Kirillov, A.A.; Ruchin, A.B.; Alpeev, M.A.; Smirnov, D.G.; Vekhnik, V.P. Occurrence of Small Mammals in Mordovia State Nature Reserve and National Park “Smolny” (European Russia), Version 1.1. Occurrence Dataset. Joint Directorate of the Mordovia State Nature Reserve and National Park “Smolny”: Copenhagen, Denmark, 2024. [CrossRef]
- Ivashkin, V.M.; Kontrimavichus, V.L.; Nasarova, N.S. Methods of the Collection and Studies of Helminths of Land Mammals; Nauka: Moscow, Russia, 1971; pp. 3–123. [Google Scholar]
- Zander, R.H. Four water-soluble mounting media for microslides. Phytoneuron 2014, 32, 1–4. [Google Scholar]
- Bakanov, A.I. Quantitated Estimation of Dominance in Ecological Communities; All-Union Institute of Scientific and Technical Information (VINITI): Borok, Russia, 1987; 64p, No. 8593–B87. [Google Scholar]
- Hammer, O.; Harper, D.A.T.; Ryan, P.D. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 2001, 4, 9. Available online: http://palaeo-electronica.org/2001_1/past/issue1_01.htm (accessed on 24 December 2023).
- Artyukh, E.S. Helminth fauna of beneficial and harmful wild mammals (rodents, insectivores and bats) if the Middle Trans-Volga region. Proc. Kuyb. Agricult. Inst. 1950, 10, 31–39. [Google Scholar]
- Kirillova, N.Y.; Kirillov, A.A.; Vekhnik, V.A.; Ruchin, A.B. Trematodes of Small Mammals (Soricomorpha, Erinaceomorpha, Chiroptera, Rodentia) in the Middle-Volga Region (European Russia). Occurrence Dataset. Version 1.6. 2023. Available online: https://www.gbif.org/dataset/25dee5e7-4e48-49a3-987f-a6799c9ed568 (accessed on 4 March 2024).
- Sobolev, A.A.; Mashkov, V.V.; Mashkov, N.V. New trematode Skrjabinomerus desmanae. Proc. Gorky St. Ped. Inst. 1939, 4, 83–84. [Google Scholar]
- Troitskaya, A.A. To the study of the helminth fauna of wild animals of the Middle Volga region and the Bashkirskaya ASSR. Proc. All-Union Res. Inst. Anim. Raw Mat. Fur. 1967, 21, 266–277. [Google Scholar]
- Sobolev, A.A.; Mashkov, V.V.; Mashkov, N.V. New trematode species from Russian desman. Proc. Gorky St. Ped. Inst. 1940, 5, 57–60. [Google Scholar]
- Romashov, B.V. Life cycle of nematoda Capillaria erinacei (Capillariidae). Helminthologia 1981, 17, 181–189. [Google Scholar]
- Majeed, S.; Morris, P.; Cooper, J. Occurrence of the lungworms Capillaria and Crenosoma spp. in British hedgehogs (Erinaceus europaeus). J. Comp. Pathol. 1989, 100, 27–36. [Google Scholar] [CrossRef] [PubMed]
- Mozgovoy, A.A. To the study of nematodes of the genus Porrocaecum Railliet et Henry, 1912. Proc. Helminthol. Lab. USSR 1949, 2, 42–49. [Google Scholar]
- Spassky, A.A. On the question of the development cycle of anisakids (Ascaridata, Anisakidae). Proc. Helminthol. Lab. USSR 1952, 6, 72–73. [Google Scholar]
- Karmanova, E.M. Dioctophymidea in Animals and Humans and the Diseases they Cause. Essentials of Nematodology; Nauka: Moscow, Russia, 1968; Volume 20, pp. 3–262. [Google Scholar]
- Ryzhikov, K.M.; Gvozdev, E.V.; Tokobaev, M.M.; Shaldybin, L.C.; Matsaberidze, G.V.; Merkusheva, I.V.; Nadtochiy, E.V.; Khokhlova, I.G.; Sharpilo, L.D. Keys to the Helminths of Rodents in the USSR Fauna, Nematodes and Acanthocephalans; Nauka: Moscow, Russia, 1979; pp. 3–272. [Google Scholar]
- Ryzhikov, K.M. On the question of paratenic parasitism of the pig nematode Physocephalus sexalatus (Molin, 1860). Proc. Helminthol. Lab. USSR 1952, 6, 139–141. [Google Scholar]
- Chabaud, A.G. Sur le cycle evolutif des spirurides et de nematodes ayant une biologie comparable. Ann. Parasitol. Hum. Comp. 1954, 29, 206–249. [Google Scholar] [CrossRef] [PubMed]
- Grewal, P.S.; Grewal, S.K.; Tan, L.; Adams, B.J. Parasitism of molluscs by nematodes: Types of associations and evolutionary trends. J. Nematol. 2003, 35, 146–156. [Google Scholar] [PubMed]
- Barus, V.K.; Blazek, K. The life cycle and the pathogenicity of the nematode Crenosoma striatum (Zeder, 1800). Fol. Parasitol. 1971, 18, 215–226. [Google Scholar]
- Jourdane, J. Recherches sur le cycle biologique de Pseudoleucochloridium soricis (Soltys, 1952) dans les Pyrenees. Ann. Parasitol. 1976, 50, 421–432. [Google Scholar] [CrossRef]
- Macy, R.W.; Moore, D.J. The life cycle of Opisthioglyphe locellus Kossack, 1910 with a redescription of the species. Transact. Amer. Microscop. Soc. 1958, 77, 396–403. [Google Scholar] [CrossRef]
- Bock, D. The life cycle of Opisthioglyphe locellus Kossack, 1910 (Trematoda: Plagiorchiidae) a parasite of shrews (Soricidae). Zeit. Parasitenk. 1982, 67, 155–163. [Google Scholar] [CrossRef]
- Sharpilo, V.P.; Iskova, N.I. Trematodes. Plagiorchiata. Fauna of Ukraine; Naukova Dumka: Kiev, Ukraine, 1989; pp. 3–280. [Google Scholar]
- Busta, J.; Nasincova, V. Developmental cycle of Rubenstrema exasperatum (Rudolphi, 1819) (Trematoda: Omphalometridae). Fol. Parasitol. 1991, 38, 209–215. [Google Scholar]
- Nasincova, V.; Busta, J.; Krasnolobova, T.A. Contribution to the developmental cycle and taxonomy of Neoglyphe sobolevi Schaldybin 1953 (Trematoda: Omphalometridae). Fol. Parasitol. 1989, 36, 313–319. [Google Scholar]
- Faltynkova, A.; Nasinkova, V.; Kablaskova, L. Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gastropoda, Pulmonata) in Central Europe: A survey of species and key to their identification. Parasite 2007, 14, 39–51. [Google Scholar] [CrossRef]
- Kirillova, N.Y.; Kirillov, A.A. Trematodes (Trematoda) of small mammals in the Middle Volga region. Parazitologiia 2009, 43, 225–239. [Google Scholar] [PubMed]
- Radev, V.; Kanev, I.; Khrusanov, D.; Fried, B. Reexamination of the life cycle of Isthmiophora melis (Trematoda: Echinostomatidae) on material from southeast Europe. Parazitologiia 2009, 43, 445–453. [Google Scholar] [PubMed]
- Sudarikov, V.E.; Shigin, A.A.; Kurochkin, Y.V.; Lomakin, V.V.; Sten’ko, R.P.; Yurlova, N.I. Metacercariae of Trematodes—Parasites of Freshwater Aquatic Organisms in Central Russia; Nauka: Moscow, Russia, 2002; pp. 3–298. [Google Scholar]
- Procopic, J. The life cycle of the cestode Rodentolepis erinacei (Gmelin, 1789). Fol. Parasitol. 1971, 18, 27–32. [Google Scholar]
- Joyeux, C. Recherches sur le cycle evolutif d’Hymenolepis erinacei (Gmelin, 1789). Annales Par. Hum Comp. 1927, 5, 20–26. [Google Scholar] [CrossRef]
- Ishigenova, L.A.; Kornienko, S.A. Development of cysticercoids in Monocercus arionis (Cestoda, Dilepididae). Zool. Zhur. 2013, 92, 1–6. [Google Scholar]
- Kabilov, T.K. Some data on the larval forms of helminths of vertebrate animals among beetles of pasture biotopes of the Fergana region. In Ecology and Biology of Animals of Uzbekistan; Gan, E.I., Ed.; Fan: Tashkent, Uzbekistan, 1969; pp. 65–68. [Google Scholar]
- Khokhlova, I.G. Acanthocephals of Terrestrial Vertebrates of the USSR Fauna; Nauka: Moscow, Russia, 1986; pp. 3–277. [Google Scholar]
- Sharpilo, V.P. Parasitic Worms of Reptiles of Fauna of the USSR; Naukova Dumka: Kiev, Ukraine, 1976; pp. 3–287. [Google Scholar]
- Lewin, J. Parasitic worms in a slowworm (Anguis fragilis L.) population from the Bieszczady Mountains (Poland). Acta Parasitol. Polon. 1990, 35, 207–215. [Google Scholar]
- Kornienko, S.A.; Dokuchaev, N.E.; Odnokurtsev, V.A. Cestodes of shrews in Yakutia. In Proceedings of the Center for Parasitology; Center for Parasitology of the Institute of Ecology and Evolution: Moscow, Russia, 2018; Volume 50, pp. 104–106. [Google Scholar]
- Sheykina, Z.V.; Zhigileva, O.N. Helminthes of shrews (Soricidae) in the Malaya Sosva Nature Reserve (Russia). Nat. Conserv. Res. 2018, 3, 28–36. [Google Scholar] [CrossRef]
Species | Mordovia Nature Reserve | National Park “Smolny” |
---|---|---|
Sorex araneus | 118 | 247 |
Sorex minutus | 64 | 12 |
Sorex isodon | 12 | – |
Neomys fodiens | 3 | 3 |
Neomys milleri | 1 | – |
Crocidura suaveolens | 3 | – |
Talpa europaea | 1 | 6 |
Erinaceus roumanicus | 3 | 5 |
Total | 205 | 273 |
Species | Host | Site | MNR | NP “Smolny” | ||
---|---|---|---|---|---|---|
P, % | MA | P, % | MA | |||
Family Dilepididae Dilepis undula (Schrank, l788), larvae | Sorex araneus | small intestine | 1.7 | 0.1 | 4.5 | 0.4 |
Family Hymenolepididae Hymenolepis erinacei (Gmelin, 1789) (=Rodentolepis erinacei (Gmelin, 1789), Rodentolepis steudeneri (Janicki, 1904)) | Erinaceus roumanicus | small intestine | 66.7 (in 2 of 3 examined) | 36.3 | 80.0 (in 4 of 5 examined) | 8.0 |
Ditestolepis diaphana (Cholodkowsky, 1906) | Sorex araneus | small intestine | 28.8 | 2.1 | 21.1 | 1.1 |
Sorex isodon | 41.7 | 1.7 | – | |||
Sorex minutus | 50.8 | 1.3 | 41.7 | 1.6 | ||
Monocercus arionis Siebold, 1850 (=Molluscotaenia crassiscolex (von Linstow, 1890)) | Sorex araneus | small intestine | 78.0 | 3.4 | 74.5 | 5.8 |
Sorex isodon | 58.3 | 2.5 | – | |||
Sorex minutus | 34.9 | 0.8 | 75.0 | 3.5 | ||
Neoskrjabinolepis schaldybini Spasskii, 1947 | Sorex araneus | small intestine | 28.8 | 1.0 | 25.1 | 1.8 |
Sorex isodon | 8.3 | 0.3 | – | |||
Staphylocystis brusatae (Vaucher, 1971) | Crocidura suaveolens | small intestine | 66.7 (in 2 of 3 examined) | 4.0 | – | |
Vigisolepis spinulosa (Cholodkowsky, 1906) | Sorex araneus | small intestine | – | 5.7 | 0.2 | |
Family Brachylaimidae Brachylaima fulvum Dujardin, 1843 (=Brachylaemus oesophagei Shaldybin, 1953) | Sorex araneus | small intestine | 4.2 | 0.9 | 3.2 | 0.1 |
Sorex isodon | 16.7 | 0.3 | – | |||
Family Panopistidae Pseudoleucochloridium soricis (Soltys, 1952) (=Leucochloridium skrjabini (Shaldybin, 1953)) | Sorex araneus | stomach, small intestine | 6.8 | 0.2 | 5.0 | 0.2 |
Sorex isodon | 8.3 | 0.1 | – | |||
Sorex minutus | 1.6 | 0.02 | – | |||
Neomys fodiens | 100 (in 3 examined) | 3.7 | 66.7 (in 2 of 3 examined) | 1.7 | ||
Family Strigeidae Strigea strigis (Schrank, 1788), mtc. | Erinaceus roumanicus | fat tissue between esophagus and trachea | – | 40.0 (in 2 of 5 examined) | 1.2 | |
Talpa europaea | – | 1.6 | 0.03 | |||
Family Echinostomatidae Isthmiophora melis (Schrank, 1788) (=Euparyphium melis (Schrank, 1788)) | Erinaceus roumanicus | small intestine | – | 40.0 (in 2 of 5 examined) | 1.4 | |
Family Omphalometridae Neoglyphe locellus (Kossack, 1910) (=Opistioglyphe oschmarini Shaldybin, 1953) | Neomys fodiens | small intestine | 33.3 (in 1 of 3 examined) | 1.0 | 66.7 (in 2 of 3 examined) | 0.7 |
Neoglyphe sobolevi Schaldybin, 1953 | Sorex araneus | small intestine | 5.9 | 0.8 | 1.6 | 0.5 |
Rubenstrema exasperatum (Rudolphi, 1819) | Sorex araneus | stomach | 21.2 | 0.9 | 7.0 | 0.2 |
Sorex isodon | 16.7 | 0.9 | – | |||
Sorex minutus | 34.9 | 1.4 | 58.3 | 1.2 | ||
Neomys fodiens | 66.7 (in 2 of 3 examined) | 1.0 | – | |||
Neomys milleri | in one examined | 1.0 | – | |||
Rubenstrema opisthovitellinus (Soltys, 1954). | Sorex araneus | small intestine | – | 1.2 | 0.03 | |
Neomys fodiens | 33.3 (in 1 of 3 examined) | 1.0 | – | |||
Family Centrorhynchidae Centrorhynchus aluconis (Müller, 1780), larvae | Sorex araneus | liver | 0.8 | 0.02 | 1.2% | 0.02 |
Sorex isodon | 8.3 | 0.2 | – | |||
Family Capillariidae Aonchotheca erinacei (Rudolphi, 1819) (=Capillaria erinacei (Rudolphi, 1819)) | Erinaceus roumanicus | small intestine | 100 (in 3 examined) | 7.7 | 100 (in 5 examined) | 24.8 |
Aonchotheca exigua (Dujardin, 1845) | Sorex minutus | stomach | 6.4 | 0.2 | – | |
Neomys fodiens | – | 100 (in 3 examined) | 1.7 | |||
Aonchotheca kutorii (Ruchljadeva, 1964) | Sorex araneus | stomach | 2.5 | 0.1 | 9.3 | 0.4 |
Neomys fodiens | – | 100 (in 3 examined) | 2.3 | |||
Calodium soricicola (Yokogava et Nishigori, 1924) (=Hepaticola soricicola (Yokogava et Nishigori, 1924)) | Sorex araneus | Liver parenchyma | 5.1 | 2.3 | 2.8 | 0.1 |
Sorex isodon | 8.3 | 0.8 | – | |||
Eucoleus oesophagicola (Soltys, 1952) (=Thominx blarinae (Ogran, 1953)) | Sorex araneus | mucous membrane of esophagus | 3.4 | 0.2 | 17.4 | 0.5 |
Sorex isodon | 8.3 | 1.2 | – | |||
Liniscus incrassatus Diesing, 1851 (=Capillaria incrassata (Diesing, 1851)) | Sorex araneus | bladder | 12.7 | 0.8 | 15.0 | 0.9 |
Sorex isodon | 50.0 | 3.9 | – | |||
Neomys fodiens | 33.3 (in 1 of 3 examined) | 0.7 | – | |||
Neomys milleri | in one examined | 1.0 | – | |||
Family Soboliphymidae Soboliphyme soricis Baylis et King, 1932 | Sorex araneus | stomach | 0.8 | 0.01 | 5.3 | 0.1 |
Family Metastrongylidae Crenosoma striatum Zeder, 1800 | Erinaceus roumanicus | bronchi | – | 40.0 (in 2 of 5 examined) | 6.0 | |
Paracrenosoma skrjabini (Pologentsev, 1935) | Sorex minutus | bronchi | 1.6 | 0.03 | – | |
Family Heligmosomidae Longistriata paradoxi Schaldybin, 1964 | Sorex araneus | small intestine | 70.3 | 4.0 | 71.7 | 10.8 |
Sorex isodon | 75.0 | 7.7 | – | |||
Sorex minutus | 55.6 | 1.9 | 75.0 | 3.2 | ||
Longistriata neomi Lubarskaja, 1962 | Neomys fodiens | small intestine | 100 (in 3 examined) | 10.3 | – | |
Neomys milleri | in one examined | 3.0 | – | |||
Tricholinstowia linstowi Travassos, 1918 (=Longistriata vigisi Petrov et Savinov, 1959) | Talpa europaea | small intestine | in one examined | 20.0 | 50.0 (in 3 of 6 examined) | 15.8 |
Family Anisakidae Porrocaecum depressum (Zeder, 1800), juveniles | Sorex araneus | mesentery, serous integument of gastrointestinal tract | 11.0 | 0.3 | 11.7 | 0.5 |
Sorex isodon | 8.3 | 0,2 | – | |||
Talpa europaea | in one examined | 11.0 | 83.3 (in 5 of 6 examined) | 15.7 | ||
Family Habronematidae Hadjelia truncata (Creplin, 1825), juveniles | Sorex araneus | small intestine | 1.7 | 0.02 | 1.2 | 0.1 |
Family Physalopteridae Physaloptera clausa Rudolphi, 1819 | Erinaceus roumanicus | stomach (adults) | 66.7 (in 2 of 3 examined) | 7.0 | 100 (in 5 examined) | 9.4 |
Sorex araneus | gastric mucosa (juveniles) | 5.1 | 0.1 | 1.2 | 0.01 | |
Pseudophysaloptera soricina Baylis, 1934 (=Physaloptera soricina (Baylis, 1934)) | Sorex araneus | stomach | – | 2.0 | 0.1 | |
Sorex minutus | 3.2 | 0.1 | – | |||
Neomys fodiens | – | 33.3 (in 1 of 3 examined) | 0.3 | |||
Family Spirocercidae Physocephalus sexalatus (Molin, 1860), juveniles | Erinaceus roumanicus | walls of stomach and small intestine | – | 80.0 (in 4 of 5 examined) | 61.8 | |
Species insertae sedis Agamospirura minuta (Sharpilo, 1963), juveniles | Erinaceus roumanicus | walls of stomach and small intestine | – | 40.0 (in 2 of 5 examined) | 1.0 |
Helminth Species | D | Hosts | Locality | References |
---|---|---|---|---|
Family Hymenolepididae Hymenolepis erinacei (Gmelin, 1789) | Palaearctic | Erinaceus roumanicus | Mordovia (MNR, NP “Smolny”) | this study |
Samara region (Zhiguli Reserve) | [128,130,131,132] | |||
Monocercus arionis Siebold, 1850 | Palaearctic | Sorex araneus, Sorex isodon, Sorex minutus, Neomys fodiens | Mordovia (MNR, NP “Smolny”) | [147], this study |
Sorex araneus, Sorex minutus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Neoskrjabinolepis schaldybini Spasskii, 1947 | Palaearctic | Sorex araneus, Sorex isodon, Sorex minutus, Neomys fodiens | Mordovia (MNR, NP “Smolny”) | [147], this study |
Sorex araneus | Nizhny Novgorod region | [145] | ||
Sorex araneus, Sorex minutus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Ditestolepis diaphana (Cholodkowsky, 1906) | Palaearctic | Sorex araneus, Sorex isodon, Sorex minutus, Neomys fodiens | Mordovia (MNR, NP “Smolny”) | [147], this study |
Sorex araneus, Sorex minutus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Insectivorolepis infirma Zarnowski, 1955 | Palaearctic | Sorex araneus, Sorex minutus | Mordovia (MNR) | [147] |
Neomylepis magnirostellata (Baer, 1931) | Palaearctic | Neomys fodiens | Mordovia (MNR) | [147] |
Pseudobothrialepis mathevossianae Schaldybin, 1957 | Palaearctic | Sorex araneus, Sorex minutus | Mordovia (MNR) | [147] |
Sorex araneus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Soricinia soricis (Baer, 1928) | Palaearctic | Sorex araneus, Sorex minutus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] |
Spasskylepis ovaluteri Schaldybin, 1964 | Palaearctic | Sorex araneus, Sorex minutus, Neomys fodiens | Mordovia (MNR) | [147] |
Staphylocystis brusatae (Vaucher, 1971) | Europe | Crocidura suaveolens | Mordovia (MNR), Samara region (NP “Samarskaya Luka”) | [128,130], this study |
Staphylocystis furcata (Stieda, 1862) | Palaearctic | Sorex araneus, Sorex minutus | Mordovia (MNR), Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132,147] |
Staphylocystoides stefanskii (Zarnowski, 1954) | Palaearctic | Sorex araneus | Mordovia (MNR) | [147] |
Vigisolepis spinulosa (Cholodkowsky, 1906) | Palaearctic | Sorex araneus, Sorex minutus | Mordovia (MNR, NP “Smolny”) | [147], this study |
Sorex araneus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Family Dilepididae Dilepis undula (Schrank, l788), larvae | Palaearctic | Sorex araneus | Mordovia (MNR, NP “Smolny”) | this study |
Family Brachylaimidae Brachylaima fulvum Dujardin, 1843 | Palaearctic | Sorex araneus, Sorex isodon, Sorex minutus, Neomys fodiens | Mordovia (MNR, NP “Smolny”) | [147,162], this study |
Sorex araneus | Nizhny Novgorod region | [145] | ||
Ityogonimus talpae (Goeze, 1782) | Palaearctic | Talpa europaea | Nizhny Novgorod region | [144] |
Family Panopistidae Pseudoleucochloridium soricis (Soltys, 1952) | Palaearctic | Sorex araneus, Sorex isodon, Sorex minutus, Neomys fodiens | Mordovia (MNR, NP “Smolny”) | [147,162], this study |
Family Opisthorchiidae Metorchis bilis (Braun, 1890) | Holarctic | Neomys fodiens | Mordovia (MNR) | [147] |
Family Echinostomatidae Isthmiophora melis (Schrank, 1788) | Holarctic | Erinaceus roumanicus | Mordovia (NP “Smolny”) | this study |
Family Omphalometridae Neoglyphe locellus (Kossack, 1910) | Holarctic | Neomys fodiens | Mordovia (MNR, NP “Smolny”) | [147,162], this study |
Neoglyphe sobolevi Schaldybin, 1953 | Holarctic | Sorex araneus, Sorex minutus | Mordovia (MNR, NP “Smolny”) | [147,162], this study |
Sorex araneus | Nizhny Novgorod region | [145] | ||
Sorex araneus, Sorex minutus | Samara region (NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Rubenstrema exasperatum (Rudolphi, 1819) | Holarctic | Sorex araneus, Sorex isodon, Sorex minutus, Neomys fodiens, Neomys milleri | Mordovia (MNR, NP “Smolny”) | [147,162], this study |
Sorex araneus | Nizhny Novgorod region | [145] | ||
Sorex araneus, Sorex minutus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Rubenstrema opisthovitellinus (Soltys, 1954) | Palaearctic | Sorex araneus, Neomys fodiens | Mordovia (MNR, NP “Smolny”) | [162], this study |
Omphalometra desmanae (Sobolev, Maschkov et Maschkov, 1939) | Europe | Desmana moschata | Nizhny Novgorod region | [163] |
Mordovia (MNR) | [147] | |||
Tatarstan | [164] | |||
Samara region | [165] | |||
Family Diplostomidae Alaria alata (Goeze, 1782), mesocercaria | Cosmopolitan | Sorex araneus | Samara region (NP “Samarskaya Luka”) | [128,129,130] |
Family Strigeidae Strigea strigis (Schrank, 1788), metacercaria | Palaearctic | Erinaceus roumanicus, Sorex araneus | Mordovia (NP “Smolny”) | this study |
Holostephanus desmanae | Europe | Desmana moschata | Nizhny Novgorod region | [166] |
Family Capillariidae Aonchotheca kutorii (Ruchljadeva, 1964) | Palaearctic | Sorex araneus Neomys fodiens | Mordovia (MNR, NP “Smolny”) | [147], this study |
Sorex araneus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Aonchotheca erinacei (Rudolphi, 1819) | Palaearctic | Erinaceus roumanicus | Mordovia (MNR, NP “Smolny”) Samara region (Zhiguli Reserve) | [128,130,131,132], this study |
Aonchotheca exigua (Dujardin, 1845) | Europe | Sorex minutus, Neomys fodiens | Mordovia (MNR, NP “Smolny”) | this study |
Sorex minutus, Crocidura suaveolens | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,130,131,132] | ||
Calodium soricicola (Yokogava et Nishigori, 1924) | Palaearctic | Sorex araneus, Sorex isodon | Mordovia (MNR, NP “Smolny”) | this study |
Sorex araneus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Eucoleus oesophagicola (Soltys, 1952) | Palaearctic | Sorex araneus, Sorex isodon, Neomys fodiens | Mordovia (MNR, NP “Smolny”) | [147], this study |
Sorex araneus, Erinaceus roumanicus, Talpa europaea | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Liniscus incrassatus Diesing, 1851 | Palaearctic | Sorex araneus, Sorex isodon, Neomys fodiens, Neomys milleri | Mordovia (MNR, NP “Smolny”) | [147], this study |
Neomys fodiens | Tatarstan | [134] | ||
Sorex araneus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Nematoideum talpae Siebold, 1850 | Palaearctic | Talpa europaea | Samara region (Zhiguli Reserve) | [128,130,131,132] |
Family Soboliphymidae Soboliphyme soricis Baylis et King, 1932 | Palaearctic | Sorex araneus, Neomys fodiens | Mordovia (MNR, NP “Smolny”) | [147], this study |
Sorex araneus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Family Metastrongylidae Crenosoma striatum Zeder, 1800 | Palaearctic | Erinaceus roumanicus | Mordovia (NP “Smolny”), Samara region (Zhiguli Reserve), Nizhny Novgorod region | [128,130,131,132,143], this study |
Paracrenosoma skrjabini (Pologentsev, 1935) | Palaearctic | Sorex minutus | Mordovia (MNR), Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,130,131,132], this study |
Family Heligmosomidae Longistriata paradoxi Schaldybin, 1964 | Palaearctic | Sorex araneus, Sorex isodon, Sorex minutus | Mordovia (MNR, NP “Smolny”) | [147], this study |
Sorex araneus, Sorex minutus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Longistriata codrus Thomas, 1953 | Palaearctic | Sorex araneus, Sorex minutus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] |
Longistriata neomi Lubarskaja, 1962 | Palaearctic | Neomys fodiens | Tatarstan | [134] |
Neomys fodiens, Neomys milleri | Mordovia (MNR) | [147], this study | ||
Tricholinstowia linstowi Travassos, 1918 | Palaearctic | Talpa europaea | Mordovia (MNR, NP “Smolny”), Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,130,131,132], this study |
Tricholinstowia talpae (Morgan, 1928) | Palaearctic | Talpa europaea | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,130,131,132] |
Family Anisakidae Porrocaecum depressum (Zeder, 1800), juveniles | Cosmopolitan | Talpa europaea | Chuvashia, Mari El | [133] |
Sorex araneus, Sorex isodon, Talpa europaea | Mordovia (MNR, NP “Smolny”) | this study | ||
Neomys fodiens Talpa europaea | Tatarstan | [133,134] | ||
Talpa europaea | Nizhny Novgorod region | [144] | ||
Sorex araneus, Talpa europaea, Erinaceus roumanicus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Family Habronematidae Hadjelia truncata (Creplin, 1825), juveniles | Palaearctic | Sorex araneus | Mordovia (MNR, NP “Smolny”) | this study |
Family Physalopteridae Physaloptera clausa Rudolphi, 1819 | Holarctic | Erinaceus roumanicus (adults), Sorex araneus (larvae) | Mordovia (MNR, NP “Smolny”), Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,130,131,132], this study |
Erinaceus roumanicus | Nizhny Novgorod region | [143] | ||
Pseudophysaloptera soricina Baylis, 1934 | Holarctic | Sorex araneus, Sorex minutus, Neomys fodiens | Mordovia (MNR, NP “Smolny”) | this study |
Sorex araneus, Sorex minutus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Family Spiruridae Spirura talpae (Gmelin, 1790) | Europe | Talpa europaea | Tatarstan | [133] |
Family Spirocercidae Physocephalus sexalatus (Molin, 1860), juveniles | Cosmopolitan | Erinaceus roumanicus | Mordovia (NP “Smolny”) | this study |
Species insertae sedis Agamospirura minuta (Sharpilo, 1963), juveniles | Palaearctic | Erinaceus roumanicus | Mordovia (NP “Smolny”) | this study |
Family Centrorhynchidae Centrorhynchus aluconis (Müller, 1780), larvae | Palaearctic | Sorex araneus, Sorex isodon | Mordovia (MNR) | this study |
Sorex araneus, Sorex minutus | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] | ||
Family Oligacanthorhynchidae Oligacanthorhynchus citilli (Rudolphi, 1806) | Palaearctic | Crocidura suaveolens | Samara region (NP “Samarskaya Luka”) | [128,130] |
Family Moniliformidae Moniliformis moniliformis (Bremser, 1811), larvae | Cosmopolitan | Sorex araneus, Sorex minutus, Crocidura suaveolens | Samara region (Zhiguli Reserve, NP “Samarskaya Luka”) | [128,129,130,131,132] |
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Kirillova, N.Y.; Kirillov, A.A.; Ruchin, A.B.; Fayzulin, A.I. Diversity of Helminths of Insectivorous Mammals (Mammalia: Eulipothyphla) from Large Forest Protected Areas of the Middle Volga Region (European Russia). Diversity 2024, 16, 307. https://doi.org/10.3390/d16050307
Kirillova NY, Kirillov AA, Ruchin AB, Fayzulin AI. Diversity of Helminths of Insectivorous Mammals (Mammalia: Eulipothyphla) from Large Forest Protected Areas of the Middle Volga Region (European Russia). Diversity. 2024; 16(5):307. https://doi.org/10.3390/d16050307
Chicago/Turabian StyleKirillova, Nadezhda Yu., Alexander A. Kirillov, Alexander B. Ruchin, and Alexander I. Fayzulin. 2024. "Diversity of Helminths of Insectivorous Mammals (Mammalia: Eulipothyphla) from Large Forest Protected Areas of the Middle Volga Region (European Russia)" Diversity 16, no. 5: 307. https://doi.org/10.3390/d16050307
APA StyleKirillova, N. Y., Kirillov, A. A., Ruchin, A. B., & Fayzulin, A. I. (2024). Diversity of Helminths of Insectivorous Mammals (Mammalia: Eulipothyphla) from Large Forest Protected Areas of the Middle Volga Region (European Russia). Diversity, 16(5), 307. https://doi.org/10.3390/d16050307