| Abstract |
The overall bat (Chiroptera) fauna of Protected Areas in the forest zone of European Russia has not yet been assessed, although papers on some Protected Areas are being published quite regularly. Along its north-to-south gradient, this extensive area spans a great variety of habitats suitable for bat populations with vastly diverse compositions. In our review of bat species, we focused on eight Protected Areas in the northern and middle taiga, as well as on a comparative summary of the faunal data for the forest zone of European Russia in general. Surveys using a bat detector and by mist-netting resulted in identification of the species composition, relative abundance, relative density and spatial distribution of bats in Protected Areas. The following nine bat species were recorded: Myotis nattereri, M. mystacinus, M. brandtii, M. daubentonii, M. dasycneme, Plecotus auritus, Nyctalus noctula, Eptesicus nilssonii, Vespertilio murinus. We regularly recorded ultrasonic signals from Plecotus auritus, Nyctalus noctula and Vespertilio murinus up to 66° N, which is much farther north that the species ranges indicated on IUCN maps. This result came as a surprise, considering there had been no specialised censuses in the Republic of Karelia or the Arkhangelsk region for decades. In Protected Areas, bat communities were dominated by Eptesicus nilssonii, which is specific to the northern taiga and middle taiga subzones. We discuss some ecological preferences of this species, such as a relatively higher tolerance of E. nilssonii towards temperature, but not towards air humidity in winter roosts, which may help it to thrive at high latitudes. At the same time, E. nilssonii is either missing from more southern parts of the forest zone or its relative abundance there is lower, while the dominant faunal elements are Myotis daubentonii (Darwin State Nature Reserve), Nyctalus noctula (Smolenskoye Poozerye National Park, Oksky State Nature Reserve, Bryansky Les State Nature Reserve) and Pipistrellus nathusii (Prioksko-Terrasny State Nature Reserve). Additionally, bat captures by using mist nets in the Vodlozersky National Park revealed the northernmost records of Myotis mystacinus in European Russia (62.224867° N, 37.081629° E and 62.466342° N, 36.673240° E). Finally, we argue that recent bat records demand a revision of the status of bats in regional Red Data Books. |
| References |
Ahlén I., Baagøe H.J., Bach L. 2009. Behavior of Scandinavian bats during migration and foraging at sea. Journal of Mammalogy 90(6): 1318–1323. DOI: 10.1644/09-MAMM-S-223R.1
Ahlén I., Bach L., Baagøe H.J., Pettersson J. 2007. Bats and offshore wind turbines studied in Southern Scandinavia. Report 5571. Stockholm: Swedish EPA. 36 p.
Albov S.A., Kruskop S.V., Rosina V.V. 2009. The bats (Chiroptera) of Prioksko-Terrasny Reserve – thirty years of later. Plecotus et al. 13–12: 24–31. [In Russian]
Ananev V.A., Raevsky B.V., Grabovik S.I. 2001. Organization of forest monitoring in the primeval spruce forests of the national park «Vodlozersky». In: Vodlozersky National Park: natural diversity and cultural heritage. Petrozavodsk: Karelian Scientific Center of RAS. P. 118–122. [In Russian]
Ancillotto L., Santini L., Ranc N., Maiorano L., Russo D. 2016. Extraordinary range expansion in a common bat: the potential roles of climate change and urbanisation. The Science of Nature. 103(3–4): 15. DOI: 10.1007/s00114-016-1334-7
Anufriev A.I. 2008. Wintering and winter sleep of bats in Yakutia. Vestnik of North-Eastern Federal University 5(2): 5–9. [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. DOI: 10.24189/ncr.2016.004
Baagøe H.J. 1973. Taxonomy of two sibling species of bats in Scandinavia Myotis mystacinus and Myotis brandtii (Chiroptera). Videnskabelige Meddelelser Dansk Naturhistorisk Forening 136: 191–216.
Barlow K.E., Jones G. 1999. Roosts, echolocation calls and wing morphology of two phonic types of Pipistrellus pipistrellus. Zeitschrift für Säugetierkunde 64: 257–268.
Belkin V.V., Ilyukha V.A., Khizhkin E.A., Fyodorov F.V., Morozov A.V., Yakimova A.E. 2018. Species composition and distribution of Chiroptera (Vespertilionidae) in Karelia. Principles of the Ecology 7(3): 13‒23. DOI: 10.15393/j1.art.2018.8042 [In Russian]
Belkin V.V., Khizhkin E.A., Yakimova A.E., Antonova E.P., Fyodorov F.V., Kizhina A.G., Uzenbayeva L.B., Ilyina T.N., Baishnikova I.V., Ilyukha V.A. 2019a. Ecological and physiological-biochemical preferences of the northern bat (Eptesicus nilssonii L.) as a factor of species dominance at northern latitudes. In: Ecological problems of the northern regions and ways to solve them. Apatity. P. 204‒206. [In Russian]
Belkin V.V., Ilyukha V.A., Khizhkin E.A., Fyodorov F.V., Yakimova A.E. 2019b. Studies of the bat fauna (Mammalia, Chiroptera) in the Green Belt of Fennoscandia. Transactions of the Karelian Research Centre of the Russian Academy of Sciences 5: 17‒29. DOI: 10.17076/eco1079 [In Russian]
Belkin V.V., Ilyukha V.A., Khizhkin E.A., Fyodorov F.V., Yakimova A.E. 2019c. Underground fortifications in the subzones of the middle and northern taiga as a wintering place for bats. In: Speleology and spelestology. Vol. 10. Naberezhnye Chelny. P. 279–284. [In Russian]
Belkin V.V., Tirronen K.F., Panchenko D.V. 2012. Flying squirrel (Pteromys volans L.) in taiga forests of the European North. Problems of Regional Ecology 1: 101–105. [In Russian]
Bogdarina S.V. 2004. Notes about bats (Chiroptera, Vespertilionidae) on the island of Valaam. Plecotus et al. 7: 18–21. [In Russian]
Bogdarina S.V., Strelkov P.P. 2003. Distribution of bats (Chiroptera) in the north of European Russia. Plecotus et al. 6: 7–28. [In Russian]
Boiko N.S. 2014. The Northern bat. In: Red Data Book of the Murmansk region. Kemerovo: Asia-print. P. 559–560. [In Russian]
Bolshakov V.N., Orlov O.L., Snitko V.P. 2005. Bats of the Urals. Yekaterinburg: Akademkniga. 176 p. [In Russian]
Chistyakov D.V. 2018. Bats – Chiroptera. In: Red Data Book of the Leningrad region: Animals. Saint-Petersburg. P. 475–479. [In Russian]
Dietz C., Helversen von O., Nill D. 2011. Bats of Britain, Europe and Northwest Africa. London: A&C Black. 400 p.
Dietz C., Kiefer A. 2016. Bats of Britain and Europe. UK: Bloomsbury Publishing. 400 p.
Hamphries M.M., Thomas D.W., Speakman J.R. 2002. Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature 418: 313–316. DOI: 10.1038/nature00828
Hanák V. 1970. Notes on the distribution and systematics of Myotis mystacinus Kuhl, 1819. Bijdragen tot de Dierkunde 40(1): 40–44. DOI: 10.1163/26660644-04001012
Ilyin V.Yu., Smirnov D.G., Yanyaeva N.M. 2003. Effects of the Anthropogenic Factor on Bats (Chiroptera: Vespertilionidae) in the Volga Region. Russian Journal of Ecology 34(2): 122–126. DOI: 10.1023/A:1023003215329
Jones K.E., Russ J.A., Bashta A.T., Bilhari Z., Catto C., Csősz I., Gorbachev A., Győrfi P., Hughes A., Ivashkiv I., Koryagina N., Kurali A., Langton S.D., Collen A., Mărginean G., Pandourski I., Parsons S., Prokofev I., Szodoray-Parádi A., Szodoray-Parádi F., Tilova E., Walters C.L., Weatherill A., Zavarzin O. 2013. Indicator bats program: a system for the global acoustic monitoring of bats. In: Collen B., Pettorelli N., Baillie J.E.M., Durant S.M. (Eds.): Biodiversity Monitoring and Conservation: Bridging the Gap between Global Commitment and Local Action. John Wiley-Blackwell. P. 213–247. DOI: 10.1002/9781118490747.ch10
Kataev G.D. 2018. Annotated list of mammal species. In: Vertebrates of the Pasvik State Nature Reserve. Petrozavodsk. P. 193–207. [In Russian]
Konovalov A.F. 2010. Bats – Chiroptera. In: Red Data Book of the Vologda Region. Vol. 3: Animals. Vologda: Poligraf-Kniga. P. 184–185. [In Russian]
Korosov A.V. 2007. Order of bats (Chiroptera). In: Red Data Book of the Republic of Karelia. Petrozavodsk. P. 169–171. [In Russian]
Kravchenko A.V., Lazareva I.P. 1989. Natural conditions. In: Valaam ecosystems and their protection. Petrozavodsk. P. 6–14. [In Russian]
Kruskop S.V. 2007. On distribution of pipistrelles from Pipistrellus pipistrellus/pygmaeus complex (Chiroptera, Vespertilionidae) in Russia. Plecotus et al. 10: 36–46. [In Russian]
Law B., Park K.J., Lacki M.J. 2016. Insectivorous bats and silviculture: balancing timber production and conservation. In: Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer, Cham. P. 105–150. DOI: 10.1007/978-3-319-25220-9_5
Lehmann R. 1983–1984. Myotis mystacinus (Kuhl, 1819) and Myotis brandtii (Eversmann, 1845) in Finland. Myotis 21−22: 96–101.
Lehnert L.S., Kramer-Schadt S., Schönborn S., Lindecke O., Niermann I., Voigt C.C. 2014. Wind farm facilities in Germany kill noctule bats from near and far. PLoS ONE 9(8): e103106. DOI: 10.1371/journal.pone.0103106
Mamontov V.N. 2006. Mammals. In: Nature and historical and cultural heritage of Kozhozerye. Arkhangelsk. P. 233–243. [In Russian]
Michaelsen T.C. 2016. Summer temperature and precipitation govern bat diversity at northern latitudes in Norway. Mammalia 80(1): 1–9. DOI: 10.1515/mammalian-2014-0077
Michaelsen T.C., Jensen K.H., Högstedt G. 2011. Topography is a limiting distributional factor in the soprano pipistrelle at its latitudinal extreme. Mammalian Biology 76(3): 295–301. DOI: 10.1016/j.mambio.2010.12.004
Miller B.W. 2001. A method for determining relative activity of free flying bats using a new activity index for acoustic monitoring. Acta Chiropterology 3(1): 93−106.
Mitchell-Jones A.J., Amori G., Bogdanowicz W., Krystufek B., Reijnders P.J., Spitzenberger F., Stubbe M., Thissen J.B., Vohralik V., Zima J. 1999. The Atlas of European Mammals. London: T&A. D. Poyser. 484 p.
Moshnikov S.A., Ananev V.A., Matyushkin V.A. 2019. Storages of Coarse Woody Debris in Pine Forests of Middle Taiga of Northwestern Russia (Case Study in Karelia). Russian Journal of Forest Science 4: 266–273. DOI: 10.1134/S0024114819040041 [In Russian]
Pereswiet-Soltan A. 2007. Relation between climate and bat fauna in Europe. Travaux du Museum National d'Histoire Naturelle «Grigore Antipa» 50: 505–515.
Poerink B.J., Lagerveld S., Verdaat H. 2013. Pilot study. Bat activity in the Dutch offshore wind farms Owex and Pawp. Groningen: The Fieldwork Company. 19 p.
Rebelo H., Tarroso P., Jones G. 2010. Predicted impact of climate change on European bats in relation to their biogeographic patterns. Global Change Biology 16(2): 561–576. DOI: 10.1111/j.1365-2486.2009.02021.x
Russ J.M., Briffa M., Montgomery W.I. 2003. Seasonal patterns in activity and habitat use by bats (Pipistrellus spp. and Nyctalus leisleri) in Northern Ireland, determined using a driven transect. Journal of Zoology 259(3): 289–299. DOI: 10.1017/S0952836902003254
Russo D., Voigt C.C. 2016. The use of automated identification of bat echolocation calls in acoustic monitoring: A cautionary note for a sound analysis. Ecological Indicators 66: 598–602. DOI: 10.1016/j.ecolind.2016.02.036
Rydell J., Bach L., Bach P., Diaz L.G., Furmankiewicz J., Hagner-Wahlsten N., Kyherцinen E.M., Lilley T., Masing M., Meyer M., Pзtersons G., Рuba J., Vasko V., Vintulis V., Hedenstrцm A. 2014. Phenology of migratory bat activity across the Baltic Sea and the south-eastern North Sea. Acta Chiropterologica 16(1): 139–147. DOI: 10.3161/150811014X683354
Rydell J., Elfstrom M., Eklof J., Sanchez-Navarro S. 2020. Dramatic decline of northern bat Eptesicus nilssonii in Sweden over 30 years. Royal Society Open Science 7(2): 191754. DOI: 10.1098/rsos.191754
Rydell J., Nyman S., Eklцf J., Jones G., Russo D. 2017. Testing the performances of automated identification of bat echolocation calls: a request for prudence. Ecological Indicators 78: 416–420. DOI: 10.1016/j.ecolind.2017.03.023
Rydell J., Strann K.B., Speakman J.R. 1994. First record of breeding bats above the Arctic Circle: northern bats at 68–70°N in Norway. Journal of Zoology 233(2): 335–339. DOI: 10.1111/j.1469-7998.1994.tb08597.x
Rykov A.M. 2008a. Bats. Components of Ecosystems and Biodiversity in Karst Territories of Northern European Russia: The Example of Pinega State Nature Reserve. Arkhangelsk. 293–294. [In Russian]
Rykov A.M. 2008b. Family of vesper bats – Vespertilionidae. In: Red Data Book of the Arkhangelsk Region. Arkhangelsk. P. 298–300. [In Russian]
Semenov-Tjan-Shanskii O.I. 1982. Mammals of the Murmansk region. Murmansk: Murmansk Book Publishing House. 175 p. [In Russian]
Shpak A.V. 2019. Protection and principles of the study of bats in Protected Areas. In: Current Status and Prospects for the Development of Protected Areas (PAs). Minsk. P. 99–103. [In Russian]
Shpilenok I.P., Korshunova E.N., Tarasov A.G. 1997. Rare and threatened mammal species of Nerusso-Desnyansky district. In: Rare and Threatened Plant and Animal Species Nerusso-Desnyansky Physiographic Region. Bryansk: Grany Press. P. 242–249. [In Russian]
Shutova E.V. 2016. The impact of climate warming on the spread of some insect species to the north. In: Proceedings of the All-Russian Scientific and Practical Conference with international participation dedicated to the 25th anniversary of the UNESCO Biosphere Reserve «Vodlozersky National Park». Petrozavodsk. P. 265–266. [In Russian]
Siivonen Y., Wermundsen T. 2008. Characteristics of winter roosts of bat species in southern Finland. Mammalia 72(1): 50–56. DOI: 10.1515/MAMM.2008.003
Sitnikova E.F., Kruskop S.V., Mishta A.V. 2009. Materials on the bat fauna of Bryansk region. Plecotus et al. 11–12: 32–49. [In Russian]
Skorokhodova S.B., Shcherbakov A.N. 2011. Trends in the onset of phenological events in the Kivach State Nature Reserve in 1966–2005. Proceedings of the Kivach State Nature Reserve 5: 207–221. [In Russian]
Snitko V.P. 2000. Proposed activities for the monitoring of bats in protected areas of the Urals. In: Coordination of environmental monitoring in the protected areas of the Urals. Ekaterinburg. P. 239. [In Russian]
Starikov D.A., Popov I.Yu. 2012. Bats in the territory of the Nizhne-Svirsky State Nature Reserve. Proceedings of the Nizhne-Svirsky State Nature Reserve 2: 1–168. [In Russian]
Strelkov P.P. 1997a. Breeding area and its position in range of migratory bats species (Chiroptera, Vespertilionidae) in East Europe and adjacent territories – Communication 1. Zoologicheskii Zhurnal 76(9): 1073–1082. [In Russian]
Strelkov P.P. 1997b. Breeding area and its position in range of migratory bats species (Chiroptera, Vespertilionidae) in east Europe and adjacent territories: Communication 2. Zoologicheskii Zhurnal 76(12): 1381–1390. [In Russian]
Strelkov P.P. 2004. Expansion of habitats by Palearctic bats (Chiroptera, Mammalia) as an example of invasion in anthropogenic biotopes. In: Biological invasions in aquatic and terrestrial ecosystems. Moscow, Saint Petersburg. P. 202–207. [In Russian]
Strelkov P.P., Buntova E.G. 1982. Myotis mystacinus and Myotis brandtii (Chiroptera, Vespertilionidae) and interrelations of these species. Part 1. Zoologicheskii Zhurnal 61(8): 1227–1241. [In Russian]
Strelkov P.P., Ilyin V.Yu. 1990. The bats (Chiroptera, Vespertilionidae) of the south Middle Volga and Lower Volga provinces. Proceedings of the Zoological Institute of the Academy of Sciences of the USSR 225: 42–167. [In Russian]
Tidenberg E.M., Liukko U.M., Stjernber T. 2019. Atlas of Finnish bats. Annales Zoologici Fennici 56(1–6): 207–250. DOI: 10.5735/086.056.0117
Ulrich W., Sachanowicz K., Michalak M. 2007. Environmental correlates of species richness of European bats (Mammalia: Chiroptera). Acta Chiropterologica 9(2): 347–360. DOI: 10.3161/1733-5329(2007)9[347:ECOSRO]2.0.CO;2
Vasenkov D.A., Sidorchuk N.V. 2010. Dynamics of bat species composition by the results of mist-netting in summer period in the Darwin State Nature Reserve. Plecotus et al. 13: 32–33. [In Russian]
Vasenkov D.A., Sidorchuk N.V., Khokhryakov V.R. 2017. «Sedentary» and «migrating» population of bats in the Smolenskoye Poozerye National Park. Plecotus et al. 20: 54–67.
Vekhnik V.P., Sachkov S.A. 2005. Proposals for the programme on eco-faunal monitoring of bats in Protected Areas. Plecotus et al. 8: 77–80. [In Russian]
Verzilin A.V., Kondrashova K.V., Troshchii A.I. 1990. Some biological features of apple trees in the gardens of Valaam. In: Planting of trees and gardens in Karelia. Petrozavodsk: KarRC AS USSR. P. 97–103. [In Russian]
Vlaschenko A., Kravchenko K., Prylutska A., Ivancheva E., Sitnikova E., Mishin A. 2016. Structure of summer bat assemblages in forests in European Russia. Turkish Journal of Zoology 40: 867–893. DOI: 10.3906/zoo-1508-56
Voigt C.C., Lindecke O., Schönborn S., Kramer-Schadt S., Lehmann D. 2016. Habitat use of migratory bats killed during autumn at wind turbines. Ecological Applications 26(3): 771–783. DOI: 10.1890/15-0671
Volkov A.D. 2008. Forest types of Karelia. Petrozavodsk: KarRC of RAS. 180 p. [In Russian]
Zaugolnova L.B., Martynenko V.B. 2014. Colour map of the European part of Russia. In: Key to forest types of European Russia. Available from http://www.cepl.rssi.ru/bio/forest/karta_1.htm [In Russian]
Zimin V.B., Ivanter E.V. 1969. Faunistic survey of terrestrial vertebrates of the Kivach State Nature Reserve. Proceedings of the Kivach State Nature Reserve 1: 22–64. [In Russian] |
