Ecosystem Transformation (), 87-101

Helminth infestation of the northern red-backed vole Clethrionomys rutilus in the North-Western Siberia

Zhigileva O.N. , Levykh A.Yu., Perevalova A.S., Chernyavsky L.Yu.

Protected areas (PAs) in northern Western Siberia, being important biodiversity hotspots, still remain relatively understudied for the diversity of many taxa. We present the first data on helminth infestation of the northern red-backed vole Clethrionomys rutilus, which is the dominant rodent species in the protected areas located in the taiga zone (Malaya Sosva State Nature Reserve, Kunovatsky Biological Sanctuary, and Angalsky Mys Natural Monument), the outskirts of Nadym town (Nadym Hills), and the Taz River floodplain. In 2019 and 2021, 231 northern red-backed voles were captured; 12 helminth species were registered as their parasites. The highest parasite species richness and
abundance were observed for the northern red-backed vole inhabiting the protected areas located in the taiga zone. The parasite prevalence (P) and the abundance (A) were the highest in the Kunovatsky Biological Sanctuary (P = 53%, A = 0.79) and the Malaya Sosva State Nature Reserve (P = 45%, A = 2.39), decreasing northwards. The decline in helminth diversity from middle taiga to tundra was consistent with a corresponding change in rodent abundance. In the northern areas of Western Siberia, the helminth diversity in the northern red-backed vole was significantly lower comparing to the southern areas of the region. The obtained data on helminth species composition and infestation rates in C. rutilus
allowed to fill a gap in the study of the helminth fauna of vast territories of North-Western Siberia, including those with conservation status.

O. N. Zhigileva
Tyumen State University
Volodarskogo St. 6, Tyumen, 625003 Russia

zhigileva@mail.ru

A. Yu. Levykh
Scientific Center for Arctic Studies
Respubliki St. 20, Salekhard, Tyumen Oblast, Yamalo-Nenets Autonomous Okrug, 629008 Russia


A. S. Perevalova
Tyumen State University
Volodarskogo St. 6, Tyumen, 625003 Russia


L. Yu. Chernyavsky
Tyumen State University
Volodarskogo St. 6, Tyumen, 625003 Russia

Anikanova, V.S., Bugmyrin, S.V., Ieshko, E.P., 2007. Metody sbora i izucheniia gel'mintov melkikh mlekopitaiushchikh [Methods of collecting and studying helminths of small mammals]. Karelian Scientific Center of the Russian Academy of Sciences, Petrozavodsk, Russia, 115 р. (In Russian).
Avenant, N.L., Cavallini, P., 2007. Correlating rodent community structure with ecological integrity, Tussen-die-Riviere Nature Reserve, Free State province, South Africa. Integrative Zoology 2 (4), 212–219. https://doi.org/10.1111/j.1749-4877.2007.00064.x
Bogdanova, O.V., 2022. Problemy prirodopol'zovaniia v gosudarstvennom prirodnom zakaznike regional'nogo znacheniia «Nadymskii», YaNAO [Problems of nature management in the Nadymsky State Nature Reserve of regional significance, YNAO]. Moskovskii ekonomicheskii zhurnal [Moscow Economic Journal] 7 (3), 34. (In Russian). https://doi.org/10.55186/2413046X_2022_7_3_159
Bugmyrin, S.V., Korosov, A.V., Bespiatova, L.A., Ieshko, E.P., 2015. Gel'mintofauna ryzhei polevki Myodes glareolus (Schreber, 1780) Kizhskogo arkhipelaga [Helminth fauna of the bank vole Myodes glareolus (Schreber, 1780) in the Kizhi Archipelago]. Parazitologiia [Parasitology] 49 (1), 61–71. (In Russian).
Chechulin, A.I., Guliaev, V.D., 1998. Paranoplocephala longivaginata sp.n. (Cyclophyllidea: Anoplocephalidae) – novaia tsestoda ot gryzunov (Rodentia) Vostochnoi Sibiri [Paranoplocephala longivaginata sp.n. (Cyclophyllidea: Anoplocephalidae) – new cestode from rodents (Rodentia) of Eastern Siberia]. Parazitologiia [Parasitology] 32 (4), 352–356. (In Russian).
Galbreath, K.E., Ragaliauskaite, K., Kontrimavichus, L., Makarikov, A.A., Hoberg, E.P., 2013. A widespread distribution for Arostrilepis tenuicirrosa (Eucestoda: Hymenolepididae) in Myodes voles (Cricetidae: Arvicolinae) from the Palearctic based on molecular and morphological evidence: historical and biogeographic implications. Acta Parasitologica 58 (4), 441–452. https://doi.org/10.2478/s11686-013-0170-6
Gashev, S.N., Zhigileva, O.N., Sazonova, N.A., Seliukov, A.G., Shapovalov, S.I. et al., 2006. Zooindikatory v sisteme regional'nogo ekologicheskogo monitoringa Tiumenskoi oblasti: metodika ispol'zovaniia [Zooindicators in the system of regional environmental monitoring of the Tyumen region: methods of use]. Tyumen State University, Tyumen, Russia, 132 p. (In Russian).
Groisman, P.Y., Blyakharchuk, T.A., Chernokulsky, A.V., Arzhanov, M.M., Marchesini, L.B. et al., 2013. Climate changes in Siberia. In: Groisman, P., Gutman, G. (eds.), Regional environmental changes in Siberia and their global consequences. Springer Environmental Science and Engineering. Springer, Dordrecht, 57–109. https://doi.org/10.1007/978-94-007-4569-8_3
Guliaev, V.D., Chechulin, A.I., 1996–1997. Differentsial'naia diagnostika Paranoplocephala omphalodes (Hermann, 1783) i P. blanchardi (Moniez, 1891) (Cestoda: Anoplocephalidae) [Differential diagnostics of Paranoplocephala omphalodes (Hermann, 1783) and P. blanchardi (Moniez, 1891) (Cestoda: Anoplocephalidae)]. Selevinia, 1–4. (In Russian).
Haukisalmi, V., Wickström, 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 33 (3), 277–290. https://doi.org/10.1111/j.0300-3256.2004.00148.x
Haukisalmi, V., Hardman, L.M., Hardman, M., Laakkonen, J., Niemimaa, J., Henttonen, H., 2007.
Morphological and molecular characterisation of Paranoplocephala buryatiensis n. sp. and P. longivaginata Chechulin and Gulyaev, 1998 (Cestoda: Anoplocephalidae) in voles of the genus Clethrionomys. Systematic Parasitology 66, 55–71. https://doi.org/10.1007/s11230-006-9059-1
Haukisalmi, V., Hardman, L.M., Hoberg, E.P., Henttonen, H., 2014. Phylogenetic relationships and taxonomic revision of Paranoplocephala Lühe, 1910 sensu lato (Cestoda, Cyclophyllidea, Anoplocephalidae). Zootaxa 3873, 371–415. https://doi.org/10.11646/ZOOTAXA.3873.4.3
Kislyi, A.A., Ravkin, Y.S., Bogomolova, I.N., Tsybulin, S.M., Panov, V.V. et al., 2019. Distribution of norhern red-backed vole Myodes rutilus (Pallas, 1779) in Western Siberia. Contemporary Problems of Ecology 12 (1), 10–22. https://doi.org/10.1134/S1995425519010086
Kononova, M., Prisniy, Yu., 2020. Helminthes of mouse-like rodents in the Belogorye State Nature Reserve (Russia). Nature Conservation Research 5 (Suppl. 2), 11–18. https://doi.org/10.24189/ncr.2020.036
Krivopalov, A., Vlasenko, P., Abramov, S., Akimova, L., Barkhatova, A. et al., 2022. Distribution and molecular diversity of Paranoplocephala kalelai (Tenora, Haukisalmi & Henttonen, 1985) Tenora, Murai & Vaucher, 1986 in voles (Rodentia: Myodes) in Eurasia. Diversity 14 (6), 472–478. https://doi.org/10.3390/d14060472
Levykh, A.Yu., 2018. Melkie mlekopitaiushchie v biomonitoringe okhraniaemykh territorii (na primere Ishimskogo raiona Tiumenskoi oblasti) [Small mammals in the biomonitoring system of protected areas (on the example of the Ishim district of the Tyumen Region)]. Samarskii nauchnyi vestnik [Samara Journal of Science] 7 (3), 65–72. (In Russian).
Makarikov, A.A., Dokuchaev, N.E., 2021. Tapeworms in rodents from the Lower Anabar River Basin, with a review of species diversity of Ccestodes in Yakutia, Russia. Acta Parasitologica 66, 1012–1020. https://doi.org/10.1007/s11686-021-00376-6
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 (Praha) 58 (2), 108–120. https://doi.org/10.14411/fp.2011.011
Makarikov, A.A., Galbreath, K.E., Hoberg, E.P., 2013. Parasite diversity at the Holarctic nexus: species of Arostrilepis (Eucestoda: Hymenolepididae) in voles and lemmings (Cricetidae: Arvicolinae) from greater Beringia. Zootaxa 3608 (6), 401–439. https://doi.org/10.11646/zootaxa.3608.6.1
Makarikov, A.A., Dokuchaev, N.E., Koniaev, S.V., 2016. Tsestody gryzunov Severnogo Priokhot'ia [Cestodes of rodents of Northern Priokhotye]. Vestnik Severo-Vostochnogo nauchnogo tsentra DVO RAN [Bulletin of the North-Eastern Scientific Center of the Far Eastern Branch of the Russian Academy of Sciences] 4, 52–61. (In Russian).
Morand, S., Krasnov, B.R., Poulin, R. (eds.), 2006. Micromammals and macroparasites from evolutionary ecology to management. Springer-Verlag, Tokyo, Japan, 647 p.
Morgun, E.N., Istrati, O.S., 2019. Osobo okhraniaemye prirodnye territorii v Iamalo-Nenetskom avtonomnom okruge: garmoniia, konflikty, prirodookhranno-proizvodstvennyi kompromiss [Specially protected natural areas in the Yamal-Nenets Autonomous District: harmony, conflicts, environmental and industrial compromise]. Nauchnyi vestnik Iamalo-Nenetskogo avtonomnogo okruga [Scientific Bulletin of the Yamalo-Nenets Autonomous Okrug] 1 (102), 5–11. (In Russian). https://doi.org/10.26110/ARCTIC.2019.102.1.001
Morgun, E.N., Levykh, A.Iu., Il'iasov, R.M., Kremenetskaia, M.V., Suppes, N.E., 2022. K sozdaniiu lokal'noi sistemy OOPT IaNAO: sviashchennoe mesto “Angal'skii mys” kak pamiatnik prirody [Reating a local protected area system in Yamalo-Nenets Autonomous District: the sacred site “Angalsky Mys” as a natural monument]. Samarskii nauchnyi vestnik [Samara Journal of Science] 11 (1), 86–98. (in Russian). https://doi.org/10.55355/snv2022111111
Pastukhov, A.M., 2013. Rol' zapovednika “Verkhne-Tazovskii” v podderzhanii bioraznoobraziia v basseine reki Taz [The role of the Verkhne-Tazovsky Nature Reserve in maintaining biodiversity in the Taz River basin]. Samarskaia Luka: problemy regional'noi i global'noi ekologii [Samara Luka: Problems of Regional and Global Ecology] 22 (4), 152–153. (In Russian).
Pospekhova, N.A., Pereverzeva, V.V., Dokuchaev, N.E., Primak, A.A., 2023. Filogeneticheskie sviazi predstavitelei roda Mesocestoides Vaillant, 1863 ot mikromammalii Vostoka Rossii i Aliaski [Phylogenetic relationships of representatives of the genus Mesocestoides Vaillant, 1863 from small mammals in the East of Russia and Alaska]. Vestnik Severo-Vostochnogo nauchnogo tsentra DVO RAN [The Bulletin of the North-East Scientific Center] 3, 67–79. (In Russian). https://doi.org/10.34078/1814-0998-2023-3-67-79
Reiczigel, J., Rózsa, L., 2005. Quantitative Parasitology 3.0. Budapest. Version: 20 April 2025. Web page. URL: http://www.zoologia.hu/qp/qp.html (accessed: 25.07.2025).
Reshet'ko, M.V., Moiseeva, Yu.A., 2016. Klimaticheskie osobennosti i statisticheskie otsenki izmeneniia elementov klimata v raionakh vechnoi merzloty na territorii severa Zapadnoi Sibiri [Climatic features and statistical assessments of changes in climate elements in permafrost areas in the north of Western Siberia]. Izvestiia Tomskogo politekhnicheskogo universiteta. Inzhiniring georesursov [Bulletin of the Tomsk Polytechnic University. Geo Assets Engineering] 327 (4), 108–118. (In Russian).
Ryzhikov, K.N., Gvozdev, E.V., Tokobaev, M.N., Shaldybin, L.S., Matsaberidze, G.V. et al., 1978.
Opredelitel' gel'mintov gryzunov fauny SSSR: tsestody i trematody [Identifier of helminths of rodents of the fauna of the USSR: Cestodes and Trematodes]. Nauka, Moscow, Russia, 232 p. (In Russian).
Ryzhikov, K.N., Gvozdev, E.V., Tokobaev, M.N., Shaldybin, L.S., Matsaberidze, G.V. et al., 1979.
Opredelitel' gel'mintov gryzunov fauny SSSR: nematody i akantotsefaly [Identifier of helminths of rodents of the fauna of the USSR: Nematodes and Acanthocephalans]. Nauka, Moscow, Russia, 279 p. (In Russian).
Sheftel, B.I., Yakushov, V.D., 2022. Impacts of climate warming on terrestrial species in the Middle Yenisei taiga. Contemporary Problems of Ecology 15 (1), 1–10. https://doi.org/10.1134/S1995425522010073
Sheikina, Z.V., Zhigileva, O.N., 2018. Gel'minty zemleroek (Soricidae) zapovednika “Malaia Sos'va” (Rossiia) [Helminths of shrews (Soricidae) of the Malaya Sosva Nature Reserve (Russia)]. Nature conservation research 3 (3), 28–36. (In Russian). https://doi.org/10.24189/ncr.2018.019
Starikov, V.P., Vartapetov, L.G., 2021. Geographic ecological analysis of small mammals of the northern taiga of Western Siberia. Contemporary Problems of Ecology 14 (1), 49–61. https://doi.org/10.1134/S1995425521010078
Talanova, G.I., 2018. Klimat zapovednika “Malaia Sos'va”: mnogoletnie dannye [Climate of the Malaya Sosva Nature Reserve: long-term data]. Dinamika okruzhaiushchei sredy i global'nye izmeneniia klimata [Environmental Dynamics and Global Climate Change] 9 (1), 22–45. (In Russian). https://doi.org/10.17816/edgcc8946
Tchebakova, N.M., Parfenova, E., Soja, A.J., 2009. The effects of climate, permafrost and fire on vegetation change in Siberia in a changing climate. Environmental Research Letters 4 (4), e045013. https://doi.org/10.1088/1748-9326/4/4/045013
Vlasenko, P., Abramov, S., Bugmyrin, S., Dupal, T., Fomenko, N. et al., 2019. Geographical distribution and hosts of the cestode Paranoplocephala omphalodes (Hermann, 1783) Lühe, 1910 in Russia and adjacent territories. Parasitology Research 118 (12), 3543–3548. https://doi.org/10.1007/s00436-019-06462-z
Wickström, L.M., Haukisalmi, V., Varis, S., Hantula, J., Henttonen, H., 2005. Molecular phylogeny and systematics of anoplocephaline cestodes in rodents and lagomorphs. Systematic Parasitology 62, 83–99. https://doi.org/10.1007/s11230-005-5488-5
Yushkov, V.F., Ivashevskii, G.A., 1999. Parazity pozvonochnykh zhivotnykh Evropeiskogo SeveroVostoka Rossii. Katalog [Parasites of vertebrates animals of European North-East of Russia. The catalogue]. Publishing house of the Komi scientific center of the Ural Branch of the Russian Academy of Sciences, Syktyvkar, Russia, 232 p. (In Russian).
Zhigileva, O.N., 2011. Correlation between biodiversity indices of small mammals and their helminthes in West Siberian ecosystems. Contemporary Problems of Ecology 4 (4), 416–422. https://doi.org/10.1134/S1995425511040114
Zhigileva, O.N., 2018. Zarazhennost' gel'mintami krasnoi i ryzhei polevok pri sovmestnom obitanii [Helminth infestation of red and bank voles in cohabitation]. Sbornik trudov Vserossiiskoi nauchnoi konferentsii s mezhdunarodnym uchastiem “Sovremennye problemy parazitologii i ekologii. Chteniia, posviashchennye pamiati S.S. Shul'mana” [Proceedings of the All-Russian scientific conference with international participation “Modern problems of parasitology and ecology. Readings dedicated to the memory of S.S. Shulman”]. Tolyatti, Russia, 99–109. (In Russian).
Zhigileva, O.N., Gorbacheva, E.V., Ahmetshina, R.Z., 2016. Ekologo-parazitologicheskii monitoring populiatsii melkikh mlekopitaiushchikh gorodskikh i prigorodnykh territorii [Ecological and parasitological monitoring of small mammals populations in urban and suburban areas]. Ekologicheskii monitoring i bioraznoobrazie [Environmental Monitoring and Biodiversity] 1 (11), 41–45. (In Russian).