First record of helminths of the European pine vole, Microtus subterraneus (Rodentia, Cricetidae) in Russia with overview on the rodent’s range

First record of helminths of the European pine vole, Microtus subterraneus (Rodentia, Cricetidae) in Russia with overview on the rodent’s range

Kirillova N.Yu., Kirillov A.A., Ruchin A.B.

P. 19-24

The helminth’s fauna of small mammals of the Smolny National Park (Republic of Mordovia, Russia) was studied during 2018–2019. In total, 973 individuals of 14 species of small mammals were trapped, including 9 individuals of Microtus subterraneus (Rodentia, Cricetidae). Four European pine voles were found to be infected by helminths. The helminth fauna of pine voles was analyzed in Russia for the first time. Average abundance of helminths was found as 1.0. Three species of helminths were reported, namely: Anoplocephaloides dentata s. l., Hydatigera taeniaeformis s. l. (larva) and Heligmosomoides laevis. These are known as common parasites of the Microtus voles. The helminth fauna found in Microtus subterraneus is formed by the rodent’s lifestyle, it defined by herbivory of pine voles. The low species richness of helminths in the pine voles may also associated with a small number of animals studied and the low infection level of the rodents is defined by low abundance of this vole species in a wild. The review on the helminth’s fauna in Microtus subterraneus in the European range is presented. To date, 23 helminth species are recorded for the pine voles, namely: Trematoda — 1, Cestoda — 16 and Nematoda — 6.DOI: 10.15298/rusjtheriol.20.1.03

Литература
  • Abuladze K.I. 1964. [Taeniata of Animals and Man and Diseases Caused by Them. Essentials of Cestodology]. Vol.4. Moscow: Nauka. 530 p. [in Russian].
  • Anikanova V.S., Bugmyrin S.V. & Ieshko E.P. 2007. [Methods of the Collection and Studies of Helminths of Small Mammals]. Petrozavodsk: Izdatel’stvo Karelskogo Nauchnogo Tsentra Rossiiskoi Akademii Nauk. 145 p. [in Russian].
  • Andreyko O.F. 1973. [Parasites of mammals of Moldavia]. Kishinev: Stiintsa. 185 p. [in Russian].
  • Bashenina N.B. 1981. [Ontogenesis] // Bashenina N.B (ed.). Evropeiskaya Ryzhaya Polevka. Moscow: Nauka. P.211–227 [in Russian].
  • Cutillas C., Oliveros R., Rojas M. & Guevarra D.C. 2002. Determination of Trichuris muris from murid hosts and T. arvicolae (Nematoda) from arvicolid rodents by amplification and sequentiation of the ITS1-5.8S-ITS2 segment of the ribosomal DNA // Parasitology Research. No.88. P.574–582.
  • Delattre P., Giraudoux P. & Quere J.-P. 1990. Consequences epidemiologiques de la receptivite d’un nouvel hote intermediaire du Taenia multiloculaire (Echinococcus multilocularis) et de la localisation spatiotemporelle des rongeurs infestes // Comptes Rendus de l’Academie des Sciences. Vol.310. P.339–344.
  • Dogel V.A. 1962. [Common Parasitology]. Leningrad: Izdatel
  • Durette-Desset M.C. 1968. Identification des Strongles des Mulots et Campagnols decrits par Dujardin // Annales de Parasitologie (Paris). Vol.43. No.3. P.387–404.
  • Feliu C., Spakulova, M. Casanova J.C., Renaud F., Morand S., Hugot J.P., Santalla F. & Durand P. 2000. Genetic and morphological heterogeneity in small rodent whipworms in southwestern Europe: characterization of Trichuris muris and description of Trichuris arvicolae n.sp. (Nematoda: Trichuridae) // Journal of Parasitology. Vol.86. No.3. P.442–449.
  • Genov T. 1984. [Helminths of insectivores and rodents in Bulgaria]. Sofia: Izdatel
  • Genov T. & Georgiev B.B. 1988. Review of the species of the genus Anoplocephaloides Baer, 1923 emend Rausch, 1976 (Cestoda: Anoplocephalidae) parasitizing rodents in Bulgaria, with an analysis of the taxonomic structure of the genus // Parasitologica Hungarica. Vol.21. P.31–52.
  • Gromov I.M. & Erbaeva M.A. 1995. [Mammals of Russia and Adjacent Territories. Hares and Rodents]. Saint Petersburg: Izdatel
  • Gubanyi A., Murai E., Hajdu E., Dudich A., Matskasi I. & Meszaros F. 2002. On the parasite fauna of mammals from the Ferto-Hansag National Park and its surroundings (Cestoda, Trematoda, Nematoda, Acanthocephala, Siphonaptera) // The Fauna of the Ferto-Hansag National Park. Budapest: Hungarian Natural History Museum. P.99–110.
  • Haukisalmi V. & Henttonen H. 2003. What is Paranoplocephala macrocephala (Douthitt, 1915) (Cestoda: Anoplocephalidae)? // Systematic Parasitology. Vol.54. P.53–69.
  • Haukisalmi V., Wickstrom L.M., Henttonen H., Hantula J. & Gubanyi A. 2004. Molecular and morphological evidence for multiple species within Paranoplocephala omphalodes (Cestoda, Anoplocephalidae) in Microtus voles (Arvicolinae) // Zoologica Scripta. Vol.33. No.3. P.277–290.
  • Haukisalmi V., Hardman L.M., Henttonen H., Laakkonen J., Niemimaa J., Hardman M. & Gubányi A. 2009. Molecular systematics and morphometrics of Anoplocephaloides dentata (Cestoda, Anoplocephalidae) and related species in voles and lemmings // Zoologica Scripta. Vol.38. No.2. P.199–220.
  • Kirillov A.A., Kirillova N.Yu., Krasnobaev Yu.P. & Vekhnik V.P. 2017. [Parasitic worms of small mammals of Zhiguli State Reserve. ] // [Flora and Fauna of Nature Reserves]. Vol.130. Moscow: Izdatel
  • Kirillova N.Yu. & Kirillov A.A. 2017. [Overview of helminths in small mammals in the Zhiguli State Reserve] // Nature Conservation Research. Vol.2. No.2. P.24–37 [in Russian].
  • Kirillova N.Yu., Kryštufek B., Kirillov A.A., Ruchin A.B. & Grishutkin G.F. 2019. [The first record of Microtus subterraneus (de Sélys-Longchamps, 1836) (Rodentia, Cricetidae) for Mordovia, Russia] // Acta Biologica Sibirica. Vol.5. No.4. P.145–149 [in Russian].
  • Kruskop S.V. 2015. [Animals of Central Russia: Atlas-Identifier of Mammals]. Moscow: Fiton XXI. 264 p. [in Russian].
  • Kryštufek B. 1999. Microtus subterraneus // Mitchell-Jones A.J., Amori G., Bogdanowicz W., Krystufek B., Reijnders P.J.H., Spitzenberger F. & Zima J. (eds.). The Atlas of European Mammals. London: Academic Press. P.250–251.
  • Lavikainen, A., Iwaki T., Nakao M. & Konyaev S.V. 2015. [Genetic diversity of the cryptic Hydatigera taeniaformis complex] // Yurlova N.I & Konyaev S.V. (eds.). Novye znaniya o parazitakh. Parazitologicheskie issledovaniya v Sibiri i na Dal’nem Vostoke: materialy V mezhregional’noi konferentsii. Novosibirsk: Garamond. P.65–66 [in Russian].
  • Lavikainen A., Iwaki T., Haukisalmi V., Konyaev S.V., Casiraghi M., Dokuchaev N.E., Galimberti A., Haljian A., Henttonen H., Ichikawa-Seki M., Itagaki T., Krivopalov A.V., Merri S., Morand S., Nareaho A., Olsson G.E., Ribas A., Terefe Y. & Nakao M. 2016. Reappraisal of Hydatigera taeniaeformis (Batsch, 1786) (Cestoda: Taeniidae) sensu lato with description of Hydatigera kamiyai n. sp. // International Journal of Parasitology. Vol.46. No.5–6. P.361–374.
  • Machinsky A.P. & Semov V.N. 1971. [To the study of helminth larval stages of insectivores and rodents in Mordovia] // Materialy nauchnykh konferentsii Vsesoyuznogo obcshestva gel’mintologov. Vol.23. Moscow: Nauka. P.163–167 [in Russian].
  • Makarikov A.A., Gulyaev V.D. & Kontrimavichus V.L. 2011. A redescription of Arostrilepis horrida (Linstow, 1901) and descriptions of two new species from Palaearctic microtine rodents, Arostrilepis macrocirrosa sp. n. and A. tenuicirrosa sp. n. (Cestoda: Hymenolepididae) // Folia Parasitologica. Vol.58. No.2. P.108–120.
  • Meszaros F. 1972. The occurrence of Angiostrongylus (P.) dujardini Drozdz et Doby, 1970 (Nematoda) in rodents in Hungary // Parasitologia Hungarica. Vol.5. P.163–176.
  • Meszaros F. & Stollmann A. 1984. Results of complex parasitological investigations of small mammals in the Cervov Mountains (Western Carpathians, Czechoslovakia) // Miscellanea Zoologica Hungarica. Vol.2. P.7–11.
  • Murai E., Meszaros F. & Sey O. 1992. On parasitic helminths of mammals living in the environs of Lake Balaton // Parasitologia Hungarica. Vol.25. P.23–36.
  • Ruchin A.B., Kirillov A.A., Chikhlyaev I.V. & Kirillova N.Yu. 2016. [Parasitic Worms of Terrestrial Vertebrates of the Mordovia Nature Reserve. Flora and Fauna of Nature Reserves]. Vol.124. Moscow: Izdatel
  • Shaldybin L.S. 1964. [Helminth fauna of mammals of Mordovia Nature Reserve] // [Proceedings of the Mordovia State Nature Reserve]. Vol.2. P.135–180 [in Russian].
  • Sharpilo L.D. 1975. [General characteristics of helminth fauna of rodents of Ukraine and its ecological analysis] // Masurmovich B.N. (ed.). Parasity i parasitozy zhivotnykh i cheloveka. Kiev: Naukova Dumka. P.62–70 [in Russian].
  • Shenbrot G.I. & Krasnov B.R. 2005. An atlas of the geographic distribution of the arvicoline rodents of the world (Rodentia, Muridae: Arvicolinae). Sofia: Pensoft Publishers. 336 p.
  • Skrjabin K.I., Shikhobalova N.P. & Shults R.S. 1954. [Essentials of Nematodology. Dictiocaulids, Heligmosomatids and Ollulanids of Animals]. Vol.4. Moscow: Izdatel
  • Smirnova M.I. 1978. [Helminth fauna of mouse-like rodents of water reservoir coast and its changes over the last decade] // Popov V.A. (ed). Etapy i tempy stanovleniya pribrezhnykh biotsenozov. Moscow: Nauka. Vol.4. P.46–52 [in Russian].
  • Soltys A. 1957. Badania nad robakami pasozytniczymi drobnych gryzoni Parku Narodowego w Biafowiezy // Acta Parasitologica Polonica. Vol.5. No.20. P.487–504.
  • Spassky A.A. 1951. [Anoplocephalids — tapeworms of domestic and wild animals. Essentials of Cestodology]. Vol.1. Moscow: Izdatel
  • Stammer H.J. 1956. Die Parasiten deutscher Kleinsauger. Verhandlungen der Deutschen Zoologischen Gesselschaft in Erlangen // Zoologischer Anzeiger. Vol.19. P.362–390.
  • Tenora F. & Murai E. 1976. Cestodes parasiting Pitymys subterraneus (Rodentia) from the Pieniny mountains (Poland) // Parasitologia Hungarica. Vol.9. P.63–65.
  • Tenora F., Murai E. & Vaucher C. 1985. On some Paranoplocephala species (Cestoda: Anoplocephalidae) parasitizing rodents (Rodentia) in Europe // Parasitologia Hungarica. Vol.18. P.29–48.
  • Vysotskaya S.O. 1997. Helminths of small mammals from Transcarpathian region (the East Carpathians, Ukraine) // Parasitologiya. Vol.31. No4. P.346–355 [in Russian].
  • Zander R.H. 2014. Four water-soluble mounting media for microslides // Phytoneuron. Vol.32. P.1–4.