Geographic distribution of Microtus arvalis and Microtus rossiaemeridionalis in Eastern Europe

Geographic distribution of Microtus arvalis and Microtus rossiaemeridionalis in Eastern Europe

Stakheev V.V., Khlyap L.A., Mironova T.A., Abramson N.I., Malygin, V.M., Lissovsky A.A.

P. 53-61

We studied a sample of occurrence localities of two sibling species: the common Microtus arvalis and the East-European vole M. rossiaemeridionalis, identified genetically or cytogenetically, by species distribution modelling (MaxEnt) methods for the territory of Eastern Europe. Climate data and remote sensing data were used as predictors. Despite of some difference in modern distribution of the species, we did not find any significant difference between ecological preferences of the common and East-European voles. Thus, we have tried to explain modern differences in distribution without ecological arguments. Such difference can be caused by historical reasons, when one of the species holds the territory on the basis of the founder principle or density-dependent spatial structuring. Another possibility is a segregating based on the behavioral or physiological peculiarities of the vole species. The low AUC values of our spatial models can be explained taking into account the dynamic change of landscapes of the Russian Plain, where the zone of sympatry of the sibling species is located, as well as by poor knowledge of species distribution details.DOI: 10.15298/rusjtheriol.22.1.06

Литература
  • Abramson N.I. & Lissovsky A.A. 2012. Subfamily Arvicolinae // Pavlinov I.Y. & Lissovsky A.A. (eds.). The mammals of Russia: a taxonomic and geographic reference. Archives of Zoological Museum of Moscow State University, Vol.52. Moscow: KMK Scientific Press. P.127–141.
  • Baranovsky P.M. & Okhotsky Yu.V. 1988. [Territory use, diurnal activity and mobility of sibling species Microtus arvalis and M. rossiaemeridionalis in joint colonies] // Zoologicheskii Zhurnal. Vol.67. No.7. P.1090–1094 [in Russian].
  • Baranovsky P.M., Bogomolov P.L., Karaseva E.V. & Demidova T.N. 1994. [Distribution of the East-European and common voles] // Sokolov V.E. & Karaseva E.V. (eds.). Sinantropiya gryzunov. Moscow: IEMEZH RAN. P.77–87 [in Russian].
  • Bashenina N.V., Graevskaya B.M., Zolotareva N.N., Lenets L.I., Malygin V.M. & Mosin A.F. 1988. [Biochemical, ecological, and physiological characteristics of the twin species of the voles Microtus arvalis] // Volskis R.S. (ed.). [The Species Place among Biological Systems]. Vilnus: Institute of Zoology and Parasitology of the Academy of Sciences of the Lithuanian SSR. P.18–44 [in Russian].
  • Bashlykova L.A. & Korolev A.N. 2014. [Records of common (Microtus arvalis) and Eastern European (Microtus rossiaemeridionalis) voles in the central part of the Komi Republic] // Zoologicheskii Zhurnal. Vol.93. No.11. P.1375–1380 [in Russian].
  • Bobrov V.V., Warshavsky A.A. & Khlyap L.A. 2008. [Alien Mammals in the Ecosystems of Russia]. Moscow: KMK Scientific Press. 232 p. [in Russian].
  • Bol’shakov V.N. & Shubnikova V.N. 1988. [Common vole Microtus arvalis (Rodentia, Muridae) on the Svalbard archipelago] // Zoologicheskii Zhurnal. Vol.67. No.2. P.308–310 [in Russian].
  • Boyko N.S. 2003. Microtus arvalis. https://rusman.ru/data/view?id=114437 . Mammals of Russia. Uploaded by Andrey Lissovsky 05.03.2021.
  • Brown J.L. & Carnaval A.C. 2019. A tale of two niches: methods, concepts, and evolution // Frontiers of Biogeography. Vol.11. No.4. P.e44158.
  • Bulatova N.Sh. & Emel’yanova L.G. 2018. [New information on the habitats of cryptic taxa of common voles (Arvicolini, Rodentia) by chromosomal markers] // Proceedings of International Conference “Current Biogeography Issues”. Saint Petersburg: Saint Petersburg State University. P.68–69 [in Russian].
  • Bulatova N.Sh., Golenishchev F.N., Koval’skaya Yu.M., Emel’yanova L.G., Bystrakova N.V., Pavlova S.V., Nadzhafova R.S. & Lavrenchenko L.A. 2010. Cytogenetic study of the parapatric contact zone between two 46-chromosomal forms of the common vole in European Russia // Russian Journal of Genetics. Vol.46. P.443–448.
  • Canestrelli D., Bisconti R. & Carere C. 2016. Bolder takes all? The behavioral dimension of biogeography // Trends in Ecology & Evolution. Vol.31. No.1. P.35–43.
  • Dobrohotov B.P., Baranovsky P.M. & Demidova T.N. 1985. [Peculiarities of stationary distribution of sibling species of the common vole Microtus arvalis and M. rossiaemeridionalis (Rodentia, Microtinae) and their role in natural foci of meadow field type tularemia] // Zoologicheskii Zhurnal. Vol.64. No.2. P.269–275 [in Russian].
  • Fredga K., Jaarola M., Anker Ims R., Steen H. & Yoccoz N.G. 1990. The “common vole” in Svalbard identified as Microtus epiroticus by chromosome analysis // Polar Research. Vol.8. No.2. P.283–290.
  • Karaseva E.V., Telitsina A.Y. & Samoilov B.L. 1999. [Mammals of Moscow in the Past and Present]. Moscow: Nauka. 244 p. [in Russian].
  • Karger D.N., Conrad O., Böhner J., Kawohl T., Kreft H., Soria-Auza R.W., Zimmermann N.E., Linder H.P. & Kessler M. 2017. Climatologies at high resolution for the earth’s land surface areas // Scientific Data. Vol.4. No.1. P.170122.
  • Kartavtseva I.V., Tiunov M.P., Lapin A.S., Vysochina N.P. & Ryabkova A.V. 2012. Invasion of Microtus rossiaemeridionalis into the territory of the Russian Far East // Russian Journal of Biological Invasions. Vol.3. P.11–15.
  • Kass J.M., Muscarella R., Galante P.J., Bohl C.L., Pinilla-Buitrago G.E., Boria R.A., Soley-Guardia M. & Anderson R.P. 2021. “ENMeval 2.0: Redesigned for customizable and reproducible modeling of species’ niches and distributions. // Methods in Ecology and Evolution. Vol.12. P.1602–1608.
  • Khlyap L.A. & Warshavsky A.A. 2010. Synanthropic and agrophilic rodents as invasive alien mammals // Russian Journal of Biological Invasions. Vol.1. P.301–312.
  • Kucheruk V.V. & Rubina M.A. 1953. [Reasons for determining the species composition and number of rodents in stacks of straw and haystacks of southern zones of the Moscow oblast] // Zoologicheskii Zhurnal. Vol.32. No.3. P.495–505 [in Russian].
  • Kulik I.L. 1951. [Rodents in haystacks] // [Issues of Regional, General, Experimental Parasitology, and Medical Zoology]. Moscow. No.7. P.284–316 [in Russian].
  • Lissovsky A.A., Sheftel B.I., Saveljev A.P., Ermakov O.A., Kozlov Y.A., 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, Vol.56. Moscow: KMK Scientific Press. 191 p. [in Russian].
  • Lissovsky A.A., Sheftel B.I., Stakheev V.V., Ermakov O.A., Smirnov D.G., Glazov D.M., Strelnikov D.P., Ekonomov A.V., Titov S.V., Obolenskaya E.V., Kozlov Y.A. & Saveljev A.P. 2018. Creating an integrated information system for the analysis of mammalian fauna in the Russian Federation and the preliminary results of this information system // Russian Journal of Theriology. Vol.17. No.2. P.85–90.
  • Malygin V.M. & Deulin V.B. 1979. [Some features of Microtus arvalis species ecology and behavior] // Zoologicheskii Zhurnal. Vol.58. No.5. P.731–741 [in Russian].
  • Malygin V.M. 1974. [Habitat distribution of sibling species of the common vole] // [Ekologiya]. Vol.5. No.1. P.89–91 [in Russian].
  • Malygin V.M. 1983. [Systematics of Common Voles]. Moscow: Nauka. 206 p. [in Russian].
  • Malygin V.M., Baskevich M.I. & Khlyap L.A. 2020. Invasions of the common vole sibling species // Russian Journal of Biological Invasions. Vol.11. P.47–65.
  • Markova E.A., Starikov V.P., Yalkovskaya L.E., Zykov S.V., Morozkina A.V. & Sibiryakov P.A. 2014. Molecular and cytogenetic evidence for the occurrence of the East European vole Microtus rossiaemeridionalis (Arvicolinae, Rodentia) in the North of West Siberia // Doklady Biological Sciences. Vol.455. No.1. P.129–131.
  • Meyer M.N. & Yatsenko V.N. 1980. [Taxonomic position and distribution of common and Kirghiz voles in southeastern Kazakhstan] // Zoologicheskii Zhurnal. Vol.59. No.2. P.283–288 [in Russian].
  • Meyer M.N. 1968. [Complex taxonomic species analysis by example of some common voles forms (genus Microtus)] // Zoologicheskii Zhurnal. Vol.47. No.6. P.850–859 [in Russian].
  • Meyer M.N., Golenishchev F.N., Radzhabli S.I. & Sablina O.V. 1996. [The Grey Voles (Subgenus Microtus) of Russia and Adjacent Territories]. Saint Petersburg: Zoological Institute RAS. 320 p. [in Russian].
  • Meyer M.N., Orlov V.N. & Skholl E.D. 1969. [Application of the data of karyological, physiological, and cytophysiological analyses for the determination of a new rodent species (Rodentia, Mammalia)] // Reports of the Academy of Sciences of the USSR, series of Biology. Vol.188. No.6. P.1411–1414 [in Russian].
  • Meyer M.N., Orlov V.N. & Skholl E.D. 1972. [Sibling species in the group Microtus arvalis (Rodentia, Cricetidae)] // Zoologicheskii Zhurnal. Vol.51. No.5. P.724–738 [in Russian].
  • Mikhailova T.V., Bernshtein A.D., Balakirev A.E., Apekina N.S., Al’bov S.A. & Novokhatka A.D. 2008. [Some features of Microtus arvalis and M. rossiaemeridionalis (Rodentia, Cricetidae) vole biology and their relationship with Tula hantavirus] // Zoologicheskii Zhurnal. Vol.87. No.2. P.239–247 [in Russian].
  • Mokeeva T.M. & Chentsova N.Yu. 1981. [Some ecological and physiological features of the common vole sibling species — Microtus arvalis and M. subarvalis (Microtinae, Rodentia)] // Zoologicheskii Zhurnal. Vol.60. No.5. P.752–763 [in Russian].
  • Muscarella R., Galante P.J., Soley-Guardia M., Boria R.A., Kass J.M., Uriarte M. & Anderson R.P. 2014. ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models // Methods in Ecology and Evolution. Vol.5. No.11. P.1198–1205.
  • Musser G.G. & Carleton M.D. 2005. Superfamily Muroidea // Wilson D.E. & Reeder D.M. (eds.). Mammal Species of the World: a Taxonomic and Geographic Reference. Third edition. Baltimore: John Hopkins University Press. Vol.2. P.894–1531.
  • Neronov V.M., Khlyap L.A., Tupikova N.V. & Warshavsky A.A. 2001. Formation of rodent communities in arable lands of Northern Eurasia // Russian Journal of Ecology. Vol.32. No.5. P.326–333.
  • Okulova N.M., Sapelnikov S.F., Baskevich M.I., Vlasova O.P., Mayorova A.D., Egorov S.V., Mironova T.A. & Sarychev V.P. 2008. [Comparative ecology of three forms of common voles Microtus arvalis sensu lato in the Central Chernozem region] // [Scientific Bulletin of the Belgorod State University. Ser. Natural Sciences]. No.3(43). P.128–139 [in Russian].
  • Orlov V.N. 1969. [On the possible homology of karyotypes of 46- and 54-chromosomal common voles] // [Mammals (evolution, karyology, taxonomy, faunistics)]. Materials on II All-Union Meeting on Mammals. Novosibirsk. P.139–140 [in Russian].
  • Phillips S.J. 2021. Package: maxnet, version 0.1.4. https://github.com/mrmaxent/maxnet
  • Phillips S.J., Anderson R.P., Dudík M., Schapire R.E. & Blair M.E. 2017. Opening the black box: an open-source release of Maxent // Ecography. Vol.40. No.7. P.887–893.
  • Phillips S.J., Dudík M. & Schapire R.E. 2019. Maxent software for modeling species niches and distributions (version 3.4.1). Available from: . Accessed 2 April 2019.
  • R Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
  • Schoener T.W. 1968. The Anolis lizards of Bimini: resource partitioning in a complex fauna // Ecology. Vol.49. P.704–726.
  • Shchipanov N.A. & Pavlova S.V. 2019. Role of population structuring in the formation of karyotypic diversity of the common shrew Sorex araneus (Lipotyphla, Mammalia) // Russian Journal of Ecology. Vol.50. No.2. P.115–125.
  • Shekhanov M.V. 1979. [Natural carriage of pathogens of human diseases by representatives of the lagomorphs (Lagomorpha) and rodents (Rodentia) orders of the fauna of the USSR] // Kucheruk V.V. (ed.). [Medical Theriology]. Moscow: Nauka. P.280–293 [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.
  • Sokolov V.E. & Bashenina N.V. (eds.). 1994. [Common Voles: Sibling Species Microtus arvalis Pallas, 1779 and Microtus rossiaemeridionalis Ognev, 1928]. Moscow: Nauka. 459 p. [in Russian].
  • Tikhonov I.A., Tikhonova G.N. & Osipova O.V. 2009a. Changes in the common vole (Microtus arvalis) and East European vole (Microtus rossiaemeridionalis) social behavior after combining conspecific groups // Doklady Biological Sciences. Vol.427. P.365–369.
  • Tikhonov I.A., Tikhonova G.N. & Osipova O.V. 2009b. Influence of intra- and interspecific competition on daily activity of common (Microtus arvalis) and East European (Microtus rossiaemeridionalis) voles in experiments // Russian Journal of Ecology. Vol.40. No.1. P.55–60.
  • Tikhonova G.N., Tikhonov I.A. & Osipova O.V. 2007. [Daily activity and intraspecific relations of common vole (Microtus arvalis) and Eastern European (M. rossiaemeridionalis) vole (Rodentia, Cricetidae) in experimental groups] // Zoologicheskii Zhurnal. Vol.86. No.3. P.360–368 [in Russian].
  • Tikhonova G.N., Tikhonov I.A., Bogomolov P.L. & Polyakova L.V. 1999. On ecology of sibling species Microtus arvalis Pallas, 1779 and Microtus rossiaemeridionalis Ognev, 1924 (Rodentia, Cricetidae) in Tsimlyansk sands // Biology Bulletin. Vol.26. No.3. P.247–255.
  • Tikhonova G.N., Tikhonov I.A., Fedorovich E.Yu. & Davydova L.V. 2005. [Comparative analysis of exploratory behavior in sibling species Microtus arvalis and M. rossiaemeridionalis in relation to differences in their predisposition to synanthropy] // Zoologicheskii Zhurnal. Vol.84. No.5. P.618–627 [in Russian].
  • Tikhonova G.N., Tikhonov I.A., Surov A.V., Bogomolov P.L. & Kotenkova E.V. 2012. [Ecological Aspects of the Formation of the Small Mammal Fauna of in the Urban Areas of Central Russia]. Moscow: KMK Scientific Press. 371 p. [in Russian].
  • Trankvilevsky D.V. & Kvasov D.A. 2018. [Number of small mammals in fields, stacks and ricks in the south of the central Black-earth Region] // Povolzhskiy Journal of Ecology. No.4. P.465–484 [in Russian].
  • Tupikova N.V., Khlyap L.A. & Warshavsky A.A. 2000. [Field rodents of northeastern Palaearctic] // Zoologicheskii Zhurnal. Vol.79. No.4. P.480–494 [in Russian].
  • Vodă R., Dapporto L., Dincă V. & Vila R. 2015. Why do cryptic species tend not to co-occur? A case study on two cryptic pairs of butterflies // PLoS ONE. Vol.10. No.2. P.e0117802.
  • Warren D.L., Glor R.E. & Turelli M. 2010. ENMTools: a toolbox for comparative studies of environmental niche models // Ecography. Vol.33. No.3. P.607–611.
  • Waters J.M., Fraser C.I., Godfrey M. & Hewitt G.M. 2013. Founder takes all: density-dependent processes structure biodiversity // Trends in Ecology and Evolution. Vol.28. No.2. P.78–85.
  • Zima J. 1999. Microtus arvalis // Mitchell-Jones A.J., Amori G., Bogdanowicz W., Kryštufek B., Reijnders P.J.H., Spitzenberger F., Stubbe M., Thissen J.B.M., Vohralík V. & Zima J. (eds.). The Atlas of European Mammals. London: Academic Press. P.228–229.
  • Zorenko T.A. 1980. [Comparative and ethological analysis of common vole sibling species] // [Proceedings of the 5th All-Union Meeting Rodents, Saratov]. Moscow: Nauka. P.19–20 [in Russian].