Article
| Article name | DIVERSITY OF HELMINTHS IN BATS (CHIROPTERA) IN THE MORDOVIA STATE NATURE RESERVE (EUROPEAN RUSSIA) |
| Authors | Nadezhda Yu. Kirillova, PhD, Senior Researcher of the Institute of Ecology of the Volga River Basin of RAS – a branch of the Samara Federal Research Center of RAS (445003, Russia, Togliatti, Komzina Street, 10); iD ORCID: https://orcid.org/0000-0002-4585-8970; e-mail: parasitolog@yandex.ru |
| Reference to article | Kirillova N.Yu., Kirillov A.A. 2026. Diversity of helminths in bats (Chiroptera) in the Mordovia State Nature Reserve (European Russia). Nature Conservation Research 11(2): 24–42. https://dx.doi.org/10.24189/ncr.2026.011 |
| Section | Research articles |
| DOI | https://dx.doi.org/10.24189/ncr.2026.011 |
| Abstract | Chiroptera (hereinafter – bats) are the only order of mammals capable of active flight, which has a strong influence on their diet and the structure of their parasite fauna. Of interest is the study of bat helminths, which are characterised by a high degree of host specificity, indicating a high degree of ecological isolation of bats and longtime of their co-evolution with parasites. The aim of this paper was to study the species diversity of bat helminths in the Mordovia State Nature Reserve (Russia). In 2022–2024, we studied the helminth fauna of eight bat species at 17 localities in the Mordovia State Nature Reserve, using the full helminthological dissection method. In total, 29 species of parasites were registered in the studied bat species, including 20 trematode species, two cestode species and seven nematode species. We revealed the highest species diversity of the parasite composition in Nyctalus noctula (17 species), followed by Vespertilio murinus (12 species), Pipistrellus nathusii, Myotis daubentonii, M. dasycneme, and M. brandtii (ten species each). The lowest number of parasitic worms was recorded in Pipistrellus pygmaeus (nine species). Helminths were not detected in the Plecotus auritus individuals examined. A comparison of the helminth fauna among the bat species showed that the structure of parasites is most similar in those bat species, which trophic niches coincide or partially overlap. Most of the helminth species, recorded in bats in the Mordovia State Nature Reserve, are common and widespread parasites of bats, occurring in the studied host species throughout their entire range. The relatively constant composition of helminths is caused by uniformity of the bat lifestyle and by feeding mainly on flying insects. A comparative analysis of the helminth fauna in bats from various Protected Areas of the Middle Volga Region showed that bat species studied in the Mordovia State Nature Reserve have the highest number of helminth species. A high similarity of the helminth composition of bats in the Mordovia State Nature Reserve with other Protected Areas in the Middle Volga Region was found. |
| Keywords | biodiversity, chiropterans, Middle Volga Region, parasitic worms, Protected Areas, Republic of Mordovia, Vespertilionidae |
| Artice information | Received: 08.09.2025. Revised: 07.11.2025. Accepted: 18.02.2026. |
| The full text of the article | |
| References |
Altman I. 2010. Trematode parasites of the mudsnail Ilyanassa obsoleta: an analysis of parasite communities at different scales. PhD Thesis. Durham: University of New Hampshire. 151 p. Anderson R. 2000. Nematode parasites of vertebrates, their development and transmission, 2nd ed. Wallingford: CAB International, Oxon. 650 p. Anikanova V.S., Bugmyrin S.V., Ieshko E.P. 2007. Methods of the collection and studies of helminths of small mammals. Petrozavodsk: Karelia Scientific Centre of RAS. 145 p. [In Russian] Artaev O.N., Ruchin A.B., Bugaev K.E., Grishutkin G.F., Potapov S.K., Spiridonov S.N. 2012. Vertebrates of the Mordovia State Nature Reserve. Flora and Fauna of Nature Reserves. Vol. 120. Moscow: Committee of RAS for the Conservation of Biological Diversity. 64 p. [In Russian] Artaev O.N., Grishutkin O.G. 2014. Lakes of Mordovia. Mordovskiy Zapovednik 6: 20–23. [In Russian] Artaev O.N., Smirnov D.G. 2016. The bats (Chiroptera; Mammalia) of Mordovia: specific structure and features of distribution. Nature Conservation Research 1(1): 38–51. [In Russian] Bakanov A.I. 1987. Quantitative estimation of dominance in ecological communities. Borok. 64 p. Deposited to VINITI on 08.12.1987, №8593-В87. [In Russian] Beklemishev V.N. 1970. Biocenotic foundations of comparative parasitology. Moscow: Nauka. 502 p. [In Russian] Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83(4): 575–583. DOI: 10.2307/3284227 Chikhlyaev I.V., Kirillova N.Yu., Kirillov A.A. 2018. Ecological analysis of trematodes (Trematoda) of marsh frog Pelophylax ridibundus (Ranidae, Anura) from various habitats of the National Park «Samarskaya Luka» (Russia). Nature Conservation Research 3(Suppl.1): 36–50. DOI: 10.24189/ncr.2018.039 [In Russian] Demidova T.N., Vekhnik V.P. 2004. Trematodes (Trematoda, Monorchiidae) of Myotis brandtii and M. mystacinus (Chiroptera, Vespertilionidae) from the Samarskaya Luka (Russia). Vestnik Zoologii 38(5): 71–74. [In Russian] Directive. 2010. Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Official Journal of the European Union L276: 33–79. Frank R., Kuhn T., Werblow A., Liston A., Kochmann J., Klimpel S. 2015. Parasite diversity of European Myotis species with special emphasis on Myotis myotis (Microchiroptera, Vespertilionidae) from a typical nursery roost. Parasites and Vectors 8: 101. DOI: 10.1186/s13071-015-0707-7 Gafferberg I.G. 1960. Mordovia State Nature Reserve. Proceedings of the Mordovia State Nature Reserve 1: 5–24. [In Russian] Genov T. 1984. Helminths of Insectivores and Rodents in Bulgaria. Sofia: Bulgarian Academy of Sciences. 348 p. Grishutkin O.G. 2013. Patterns of peatland distribution based on absolute relief marks on the territory of the Mordovia State Nature Reserve. Proceedings of the Mordovia State Nature Reserve 11: 259–263. [In Russian] Guerrero R., Martin C., Gardner S.L., Bain O. 2002. New and known species of Litomosoides (Nematoda: Filarioidea): important adult and larval characters and taxonomic changes. Comparative Parasitology 69(2): 177–195. DOI: 10.1654/1525-2647(2002)069[0177:NAKSOL]2.0.CO;2 Gulyaev V.D., Orlovskaya O.M., Dokuchaev N.E. 2002. Helminths of bats from Magadan Region. Plecotus et al. 5: 86–92. [In Russian] Hammer Ø., Harper D.A.T., Ryan P.D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1): 1–9. Jones C., McShea W.J., Conroy M.J., Kunz J.H. 1996. Capturing mammals. In: D.E. Wilson, F.R. Cole, J.D. Nichols, R. Rudran, M.S. Foster (Eds.): Measuring and Monitoring Biological Diversity: Standard Methods for Mammals. Washington DC: Smithsonian Institution Press. P. 115–155. Johnson P.T.J., Wood C.L., Joseph M.B., Preston D.L., Haas S.E., Springer Y.P. 2016. Habitat heterogeneity drives the host‐diversity‐begets‐parasite‐diversity relationship: evidence from experimental and field studies. Ecology Letters 19(7): 752–761. DOI: 10.1111/ele.12609 Khotenovskiy I.A. 1972. To the evolution of trematodes from bats. Parazitologiya 6(1): 79–82. [In Russian] Kirillov A.A., Kirillova N.Yu., Vekhnik V.P. 2012a. Trematodes (Trematoda) of bats (Chiroptera) from the Middle Volga region. Parazitologiya 46(5): 384–413. [In Russian] Kirillov A.A., Kirillova N.Yu., Chikhlyaev I.V. 2012b. Trematodes of terrestrial vertebrates of the Middle Volga region. Togliatti: Cassandra. 329 p. [In Russian] Kirillov A.A., Ruchin A.B., Artaev O.N. 2015. Helminths of bats (Chiroptera) from Mordovia. Bulletin of Tatishchev' Volga University 4(19): 319–328. [In Russian] Kirillov A.A., Kirillova N.Yu., Krasnobaev Yu.P., Vekhnik V.P. 2017. Parasitic worms of small mammals of Zhiguli State Nature Reserve. Flora and Fauna of Nature Reserves. Vol. 128. Moscow: Committee of RAS for the Conservation of Biological Diversity. 77 p. [In Russian] Kirillov A.A., Kirillova N.Yu., Chikhlyaev I.V., Ruchin A.B. 2024. Parasitic worms of terrestrial vertebrates of the National Park «Smolny». Flora and Fauna of National Parks. Vol. 13. Moscow: Committee of RAS for the Conservation of Biological Diversity. 118 p. [In Russian] Kirillov A.A., Kirillova N.Yu., Ruchin A.B. 2025. Ecological Analysis of Helminth Communities of the Grass Snake Natrix natrix (Reptilia, Colubridae) from the Semiaquatic Habitats of the National Park “Smolny" (European Russia). Inland Water Biology 18(4): 914–929. DOI: 10.1134/S1995082925600553 Kirillova N.Yu., Kirillov A.A. 2017. Overview of helminths in small mammals in the Zhiguli State Reserve. Nature Conservation Research 2(2): 24–37. DOI: 10.24189/ncr.2017.007 [In Russian] Kirillova N.Yu., Kirillov A.A. 2023. The first record of Nyctalus leisleri (Kuhl, 1817) (Chiroptera, Vespertilionidae) in the Mordovia Nature Reserve (European Russia). Proceedings of Samara Scientific Center of RAS 25(5): 31–37. DOI: 10.37313/1990-5378-2023-25-5-31-37 [In Russian] Kirillova N.Yu., Kirillov A.A. 2024. Helminth fauna of bats (Chiroptera) of the National Park «Smolny» (European Russia). Russian Journal of Parasitology 18(4): 366–380. [In Russian] Kirillova N.Yu., Kirillov A.A., Vekhnik V.P. 2022. Comparative analysis of the helminth fauna of Myotis brandtii and Myotis mystacinus (Chiroptera, Vespertilionidae) in the Samarskaya Luka National Park (Russia). Nature Conservation Research 7(3): 1–14. DOI: 10.24189/ncr.2022.026 Kirillova N.Yu., Kirillov A.A., Ruchin A.B. 2025. The first record of the greater noctule bat, Nyctalus lasiopterus (Schreber, 1780) (Chiroptera, Vespertilionidae), in the Republic of Mordovia (European Russia). Acta Biologica Sibirica 11: 1223–1233. DOI: 10.5281/zenodo.17595757 Kurochkin Yu.V., Kurochkina Z.A. 1962. To the helminth fauna of bats in the Astrakhan State Nature Reserve. Proceedings of the Astrakhan State Nature Reserve 6: 127–134. [In Russian] Lebedeva D.I., Belkin V.V., Stanyukovich M.K., Bespyatova L.A., Bugmyrin S.V. 2020. First records of bat parasites in Karelia. Transactions of the Karelian Research Centre of the Russian Academy of Sciences 8: 120–125. DOI: 10.17076/bg1142 Lühe M. 1909. Parasitische Plattwurmer. I. Trematodes. Die Süßwasserfauna Deutschlands. Vol. 17. Jena: Gustav Fischer. 218 p. Magurran A.E. 2004. Measuring Biological diversity. Oxford: Blackwell Publishing. 256 p. Markova L.I. 1938. Influence of winter hibernation on the parasite fauna of bats. Zoologicheskii Zhurnal 17(1): 133–145. [In Russian] Naumkin D.V., Sivkova T.N. 2019. New data on bats (Chiroptera: Vespertilionidae) of the Ural region. Proceedings of Samara Scientific Center of RAS 21(2): 210–214. [In Russian] Nigmatullin Ch.M. 2004. Towards theory of parasite life cycles. Terminology and classification of hosts by their role in helminth life cycles. In: Modern problems of parasitology, zoology and ecology. Kaliningrad: Kaliningrad State Technical University. P. 97–119. [In Russian] Podvyaznaya I.M. 1994. The fine structure of the digestive tract of Allassogonoporus amphoraeformis (Trematoda: Allassogonoporidae). Parazitologiya 28(5): 403–412. [In Russian] Podvyaznaya I.M. 1996. The fine structure of the male reproductive system and genital atrium of bat parasite Allassogonoporus amphoraeformis (Trematoda: Allassogonoporidae). Parazitologiya 30(3): 229–235. [In Russian] R Core Team. 2025. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available from https://www.R-project.org Rossolimo O.L., Pavlinov I.Ya., Kruskop S.V., Lissovsky A.A., Spasskaya N.N., Borisenko A.V., Panyutina A.A. 2004. Diversity of Mammals. Part I. Moscow: KMK Scientific Press Ltd. 366 p. [In Russian] Ruchin A.B., Kirillov A.A., Chikhlyaev I.V., Kirillova N.Yu. 2016. Parasitic worms of land vertebrates of the Mordovia State Nature Reserve. Flora and Fauna of Nature Reserves. Vol. 124. Moscow: Committee of RAS for the Conservation of Biological Diversity. 72 p. [In Russian] Ryzhikov K.M. 1952. On the problem of reservoir parasitism of Physocephalus sexalatus (Molin, 1860), a nematode of pigs. Proceedings of the Helminthological Laboratory of AS USSR 6: 139‒141. [In Russian] Ryzhikov K.M., Gvozdev E.V., Tokobaev M.M., Shaldybin L.S., Matsaberidze G.V., Merkusheva I.V., Nadtochiy E.V., Khokhlova I.G., Sharpilo L.D. 1979. Keys to helminths of rodents of the fauna of the USSR. Nematodes and acanthocephalans. Moscow: Nauka. 277 p. [In Russian] Shaldybin L.S. 1964. Helminth fauna of mammals of the Mordovia State Nature Reserve // Proceedings of the Mordovia State Nature Reserve 2: 135–180. [In Russian] Sharpilo V.P., Iskova N.I. 1989. Trematodes. Plagiorchiata. Fauna of Ukraine. Vol. 34. Issue 3. Kiev: Naukova Dumka. 280 p. [In Russian] Sharpilo V.P., Salamatin R.V. 2005. Paratenic parasitism: origins and development of the concept. Kiev: Logos. 237 p. [In Russian] Skrjabin K.I. 1948. Trematodes of animals and man. Foundations of trematodology. Vol. 2. Moscow; Leningrad: AS USSR. 600 p. [In Russian] Smirnov D.G., Vekhnik V.P. 2014. Ecology of nutrition and differentiation of the trophic niches of bats (Chiroptera: Vespertilionidae) in floodplain ecosystems of the Samara Bend. Biology Bulletin 41(1): 60–70. DOI: 10.1134/S1062359014010105 Sokolov S.G., Shchenkov S.V., Kalmykov A.P., Smirnova A.D. 2020. Morphology and Phylogenetic Position of Two Microphalloid Trematode Species, Parasites of the Vesper Bat Pipistrellus kuhlii in the Lower Volga Region of Russia. Zoologicheskii Zhurnal 99(3): 261–274. DOI: 10.31857/s0044513420030125 Stenko R.P., Dulitskiy A.I., Karpenko O.V., Dushevskiy V.P. 1986. Helminthofauna of Crimean chiropterans. Zoologicheskii Zhurnal 65(8): 1133–1139. [In Russian] Thewissen J.G.M., Babcock S.K. 1992. The origin of flight in bats. BioScience 42(5): 340–345. DOI: 10.2307/1311780 Tomba A.M. 2006. Effects of trematode parasites on habitat use and disturbance response of freshwater snails in the genus Elimia. PhD Thesis. Auburn, Alabama. 76 p. Wilkins D. 2021. Treemapify: Draw Treemaps in 'ggplot2'. R Package Version 2.5.5. Available from https://CRAN.R-project.org/package=treemapify Wickham H. 2016. ggplot2: Elegant Graphics for Data Analysis. 3rd ed. New York: Springer. 260 p. DOI: 10.1007/978-3-319-24277-4 |