Article

Nadezhda Yu. Kirillova, PhD, Senior Researcher of the Institute of Ecology of Volga Basin of RAS (445003, Russia, Togliatti, Komzina Street, 10); iD ORCID: https://orcid.org/0000-0002-4585-8970; e-mail: parasitolog@yandex.ru
Alexander A. Kirillov, PhD, Senior Researcher of the Institute of Ecology of Volga Basin of RAS (445003, Russia, Togliatti, Komzina Street, 10); iD ORCID: https://orcid.org/0000-0002-4374-8858; e-mail: parasitolog@yandex.ru
Vladimir P. Vekhnik, Researcher of the Zhiguli State Nature Biosphere Reserve (445362, Russia, Samara Region, Bakhilova Polyana village, Zhigulevskaya Street, 1); iD ORCID: https://orcid.org/0000-0002-5091-0358; e-mail: vekhnik@mail.ru

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. https://dx.doi.org/10.24189/ncr.2022.026

The article presents the comparative analysis of the helminth fauna of the sympatric bat species, Myotis mystacinus and M. brandtii (Chiroptera, Vespertilionidae), in the Samarskaya Luka National Park (Russia). Twelve species of parasites were recorded in both bat species in 2005–2007, including nine species of Trematoda, one species of Cestoda, and two species of Nematoda. All of these 12 species were noted in M. brandtii. The helminth fauna of M. mystacinus included a slightly depleted parasite fauna of M. brandtii being represented by seven species of parasites found in M. mystacinus, including six species of Trematoda and one species of Cestoda. The helminth fauna of both bat species has a moderate level of the fauna similarity. Differences in the infection level of the two bat species are found in both number of helminth species and quantitative rates of the helminth fauna. Helminth infection of M. brandtii is significantly higher than of M. mystacinus. The helminth fauna of M. mystacinus and M. brandtii is driven by the bat lifestyle and diet. Both bat species are being infected by helminths through food items. The broader diet composition of M. brandtii and its feeding on a wider number of insect groups increases the infection probability of this bat species by rare and accidental parasites, and it also increases the infection rates by obligate species of trematodes. Therefore, M. brandtii has a more diverse helminth fauna and a higher number of abundant parasite species as well. The diet of M. mystacinus contains a limited number of food items. This reduces the probability of its infection by several helminth species and, on the other hand, it causes a relatively high infection rates for some trematode species. The similarity of helminth faunas of M. brandtii and M. mystacinus is caused by the use of the same feeding habitats and the similarity of their diet. The obtained data confirm the partial overlap of spatial and trophic niches of the two studied bat species.

Brandt's bat, Middle Volga Region, parasitic worms, sympatry, Whiskered bat

Received: 17.04.2022. Revised: 23.05.2022. Accepted: 24.06.2022.

Anikanova V.S., Bugmyrin S.V., Ieshko E.P. 2007. Methods of the collection and studies of helminths of small mammals. Petrozavodsk: Karelian Scientific Center of RAS. 145 p. [In Russian]
Bakanov A.I. 1987. Quantitated estimation of dominance in ecological communities. Borok. 64 p. Deposited in VINITI on 08.12.1987, No. 8593‒В87. [In Russian]
Bychkova E.I., Akimova L.N., Degtyarik S.M., Yakovich M.M. 2017. Helminths of vertebrares and people in Belarus. Minsk: Belarusskaya Nauka. 316 p. [In Russian]
de Jong Y., Verbeek M., Michelsen V., Bjørn P., Los W., Steeman F., Bailly N., Basire C., Chylarecki P., Stloukal E., Hagedorn G., Wetzel F., Glöckler F., Kroupa A., Korb G., Hoffmann A., Häuser C., Kohlbecker A., Müller A., Güntsch A., Stoev P., Penev L. 2014. Fauna Europaea – all European animal species on the web. Biodiversity Data Journal 2: e4034. DOI: 10.3897/BDJ.2.e4034
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: 101–114. DOI: 10.1186/s13071-015-0707-7
Gause G.F. 1934. The struggle for existence. Baltimore: Williams and Wilkins. 163 p.
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: 9.
Il'in V.Yu., Vekhnik V.P., Smirnov D.G., Kurmaeva N.M., Zolina N.F., Matrosova O.M. 1999. Dynamics of abundance of bats (Chiroptera, Vespertilionidae) during hibernation in caves of the Samarian Luka over a 20-year period. Russian Journal of Ecology 30(6): 428–431.
Ivashkin V.M., Kontrimavichus V.L., Nasarova N.S. 1971. Methods of the collection and studies of helminths of terrestrial mammals. Moscow: Nauka. 123 p. [In Russian]
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.
Kharchenko M.A. 2008. Correlation analysis. Voronezh: Voronezh State University. 30 p. [In Russian]
Khotenovsky I.A. 1970. Family Pleurogenidae Looss, 1899. In: K.I. Skryabin (Ed.): Trematodes of animals and man. Essentials of trematodology. Vol. 23. Moscow: Nauka. P. 135–306. [In Russian]
Kirillov A.A., Kirillova N.Yu., Vekhnik V.P. 2006. Nematodes of genus Myotis bats (Chiroptera, Vespertilionidae) from Samarskaya Luka. Vestnik of Samara State University 49(9): 169–174. [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., Kirillova N.Yu., Krasnobayev Yu.P., Vekhnik V.P. 2017. Parasitic worms of small mammals in Zhiguli State Nature Reserve. Moscow: Committee of RAS for the Conservation of Biological Diversity; A.N. Severtsov Institute of Ecology and Evolution of RAS. 81 p. [In Russian]
Kirillov A.A., Kirillova N.Yu., Chikhlyaev I.V. 2018. Parasites of vertebrate animals from Samara Region. Togliatti: Polyar. 304 p. [In Russian]
Kirillova N.Yu., Kirillov A.A. 2008. Population ecology of trematodes of bat Myotis brandtii (Chiroptera: Vespertilionidae). In: S.O. Movsesyan, S.A. Beer, S.V. Zinovyeva, A.N. Pelgunov, S.E. Spiridonov (Eds.): Biodiversity and ecology of parasites of terrestrial and water cenoses. Moscow: Center of the Parasitology of A.N. Severtsov Institute of Ecology and Evolution of RAS. P. 167–170. [In Russian]
Kirillova N.Yu., Kirillov A.A. 2011. Nematodes (Nematoda) of small mammals from the Samarskaya Luka. Proceedings of Samara Scientific Center of RAS 13(1): 114–122. [In Russian]
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. 2019. Wild vertebrates of the Middle Volga Region as reservoir hosts of Physocephalus sexalatus (Nematoda, Spirocercidae) In: S.A. Senator, O.V. Mukhortova, S.V. Saxonov (Eds.): Ecological digest – 7. Togliatti: Anna. P. 218–219. DOI: 10.24411/9999-010A-2019-10053 [In Russian]
Kirillova N.Yu., Kirillov A.A., Vekhnik V.P. 2008a. Nematodes (Nematoda) from bats (Chiroptera) of the Samarskaya Luka peninsula (Russia). Parazitologiya 42(6): 526–532. [In Russian]
Kirillova N.Yu., Kirillov A.A., Vekhnik V.P. 2008b. Helminth fauna of two sibling species Myotis brandtii (Eversmann, 1845) и M. mystacinus (Kuhl, 1819) (Chiroptera: Vespertilionidae). In: K.V. Galaktionov, A.A. Dobrovolskij (Eds.): Parasitology in XXI century – problems, methods, solution. Vol. 2. St. Petersburg: Lema. P. 38–40. [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 Karelian Research Centre of Russian Academy of Science 8: 120–125. DOI: 10.17076/bg1142
Lissovsky А.А., Sheftel B.I., Saveljev А.P., Ermakov О.А., Kozlov Yu.А., Smirnov D.G., Stakheev V.V., Glazov D.M. 2019. Mammals of Russia: species list and applied issues. Archives of Zoological Museum of Moscow State University 56: 1–191. [In Russian]
Lühe M. 1909. Parasitische Plattwurmer. I. Trematodes. Die Susswasserfauna Deutschlands. Jena 17: 1–218.
Magurran A.E. 1992. Ecological diversity and its measurement. Moscow: Mir. 182 p. [In Russian]
Matsaberidze G.V., Khotenovsky I.A. 1967. To the trematode fauna of bats in Georgia. In: Helminth fauna of animals and plants in Georgia. Tbilisi: Metsniereba. P. 83–94. [In Russian]
Melnichenko E.D., Panasenko N.A. 1979. To the helminth fauna of bats in the Middle Dnieper Region. Vestnik Zoologii 3: 76–78. [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]
Poulin R. 1998. Comparison of three estimators of species richness in parasite component communities. Journal of Parasitology 84(3): 485–490.
Ruchin A.B., Kirillov A.A., Chikhlyaev I.V., Kirillova N.Y. 2016. Parasitic worms of land vertebrates of the Mordovia State Nature Reserve. Moscow: Committee of RAS for the Conservation of Biological Diversity; A.N. Severtsov Institute of Ecology and Evolution of RAS. 72 p. [In Russian]
Ryzhikov K.M. 1952. On the issue of reservoir parasitism of the nematode of pigs, Physocephalus sexalatus (Molin, 1860). Proceedings of Helminthological Laboratory of the USSR 6: 139‒141.
Shakhtakhtinskaya Z.M., Mustafaev Yu.Sh., Sailov D.I. 1971. About helminths of some bats of Azerbaijan. Scholarly Notes of the Azerbaijan State University. Biological Series 2: 25–30. [In Russian]
Sharpilo V.P., Iskova N.I. 1989. Trematodes. Plagiorchiata. Fauna of Ukraine. Vol. 34(30). Kiev: Naukova Dumka. 280 p. [In Russian]
Skrjabin K.I. 1948. Trematodes of animals and man. Essentials of trematodology. Vol. 2. Moscow; Leningrad: Publisher of AS USSR. 600 p. [In Russian]
Skrjabin K.I., Sobolev A.A., Ivashkin V.M. 1967. Spirurates of animals and humans and the diseases they cause. Essentials of nematodology. Vol. 16(4). Moscow: Nauka. 624 p. [In Russian]
Skvortsov V.G. 1969. Trematodes of the genus Prosthodendrium (family Lecithodendriidae) from bats in Moldavia. In: А.А. Spassky (Ed.): Parasites of vertebrate animals. Kishinev: Stiintsa. P. 87–97. [In Russian]
Skvortsov V.G. 1970. Trematodes of the family Lecithodendriidae from bats in Moldavia. In: Parasites of animals and plants in Moldavia. Vol. 5. Kishinev. P. 17–36. [In Russian]
Skvortsov V.G. 1971. Nematodes of bats from Moldavia (Report 2). In: Parasites of animals and plants in Moldavia. Vol. 7. Kishinev. P. 75–93. [In Russian]
Skvortsov V.G. 1973. Ecological and faunistic analysis of helminth fauna of bats in Moldavia. In: Parasites of animals and plants. Vol. 9. Kishinev. P. 92–155. [In Russian]
Smirnov D.G., Vekhnik V.P. 2011. Abundance and community structure of bats (Chiroptera: Vespertilionidae) hibernating in artificial caves of Samarskaya Luka. Russian Journal of Ecology 42(1): 71–79. DOI: 10.1134/S1067413611010103
Smirnov D.G., Vekhnik V.P. 2011. Relationship between the morphology of an aircraft and the choice of the type of hunting space in the community of bats in the Volga region. Izvestia Penzenskogo Gosudarstvennogo Pedagogicheskogo Universiteta imeni V.G. Belinskogo 25: 247–257. [In Russian]
Smirnov D.G., Vekhnik V.P. 2012. Analysis of the trophic niches of Myotis mystacinus and Myotis brandtii (Chiroptera) in the ecotone communities of the Samarskaya Luka. In: Problems of studying the marginal structures of biocenoses. Saratov: Saratov State University. P. 197–201. [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
Smirnov D.G., Vekhnik V.P., Kurmaeva N.M., Shepelev A.A., Il'in V.Yu. 2007. Species structure and dynamics of bat communities (Chiroptera: Vespertilionidae) hibernating in artificial caves of Samara Luka. Biology Bulletin 34(5): 507–516. DOI: 10.1134/S1062359007050147
Smith E.P., van Belle G. 1984. Nonparametric estimation of species richness. Biometrics 40(1): 119–129. DOI: 10.2307/2530750
Sten'ko R.P., Dulitskiy A.I., Karpenko O.V., Dushevskiy V.P. 1986. Helminthofauna of Crimean chiropterans. Zoologicheskii Zhurnal 65(8): 1133–1139. [In Russian]
Strelkov P.P., Ilyin V.Yu. 1990. Bats of the South of the Middle and Lower Volga regions. Proceedings of Zoological Institute of AS USSR 225: 42–167. [In Russian]
Tkach V.V. 1991. First finding of males of Pterygodermatites bovieri (Nematoda, Rictulariidae) parasitizing bats. Zoologicheskii Zhurnal 70(9): 125–127. [In Russian]
Tkach V.V. 1995. Helminths of bats from the fauna of Ukraine. In: Bats: materials of 6^th meeting on bats of the CIS countries. Khujand: Khujand State University. P. 90–95. [In Russian]
Zdzietowiecki K. 1969a. Helminths of bats in Poland. II. Trematodes of the subfamily Lecithodendriinae. Acta Parasitologica Polonica 16(24): 208–226.
Zdzietowiecki K. 1969b. Helminths of bats in Poland. III. Trematodes of the subfamily Lecithodendriidae, except for Lecithodendriinae. Acta Parasitologica Polonica 16(24): 227–237.
Zdzietowiecki K. 1970. Helminths of bats in Poland. I. Cestodes and trematodes of the family Plagiorchiidae. Acta Parasitologica Polonica 17(20): 175–188.