Article

Fatimat A. Tembotova, Chief Researcher of the Laboratory for Monitoring of Forest Ecosystems, director of the Tembotov Institute of Ecology of Mountain Territories of RAS (360051, Russia, Nalchik, I. Armand street, 37); e-mail: iemt@mail.ru
Albina Kh. Amshokova, Senior Researcher of the Laboratory for Ecology and Evolution of Vertebrates of the Tembotov Institute of Ecology of Mountain Territories of RAS (360051, Russia, Nalchik, I. Armand street, 37); e-mail: h.a.amshokova@mail.ru
Ekaterina P. Kononenko, Head of the Laboratory for Ecology and Evolution of Vertebrates of the Tembotov Institute of Ecology of Mountain Territories of RAS (360051, Russia, Nalchik, I. Armand street, 37); e-mail: iemt_kate@inbox.ru

Tembotova F.A., Amshokova A.Kh., Kononenko E.P. 2020. Differentiation degree and developmental stability of Chionomys gud (Rodentia: Cricetidae) by nonmetric cranial traits. Nature Conservation Research 5(1): 21–30. https://dx.doi.org/10.24189/ncr.2020.002

The work describes the results of assessing developmental stability and the degree of differentiation in Chionomys gud within Protected Areas of the Central and Western Caucasus. We characterised developmental stability in Chionomys gud in different eco-geographical conditions by means of fluctuating asymmetry levels (FA_nm) in a series of cranium phenes in four geographical populations. Thus we estimated the effect of environmental factors on FA_nm levels. We registered the highest FA_nm value for the sample from middle mountains of the Central Caucasus, i.e. the vicinities of the village Elbrus. The environment conditions of the given sample were the most stressful for the species (annual average temperature below 5°C and annual average precipitation below 1000 mm). Two-way ANOVA for factors «annual average temperature» and «annual average precipitation» verified a correlation between FA_nm levels and complex effects of the two climatic factors. We evaluated the levels of interpopulation phenetic distances by the analysis of frequencies of phenes of nonmetric cranial traits in Chionomys gud populations. Maximum phenetic distances were revealed between geographically distant (over 300 km) populations of the Central and Western Caucasus. The degree of morphological differentiation of the samples from the Central Caucasus, which are apart at the absolute distance of 20–60 km, was less pronounced. Our results suggest that the level of phenetic distances is determined not only by the effect of territorial isolation, but also by climatic peculiarities of a particular locality.

endemic, fluctuating asymmetry, morphological differentiation, middle mountains, nonmetric bilateral traits, Protected Area

Received: 15.08.2019. Revised: 23.10.2019. Accepted: 01.11.2019.

Allenbach D.M. 2011. Fluctuating asymmetry and exogenous stress in fishes: a review. Reviews in Fish Biology and Fisheries 21(3): 355–376. DOI: 10.1007/s11160-010-9178-2
Balakirev A.E., Mironova T.A., Khlyap L.A., Vasilenko L.E., Okulova N.M. 2017. On the species composition, distribution and ecology of voles (Mammalia, Cricetidae, Microtina) in the North-Western Caucasus. Povolzhskiy Journal of Ecology 1: 14–23. DOI: 10.18500/1684-7318-2017-1-14–23 [In Russian]
Bannikova A.A., Sizhazheva A.M., Malikov V.G., Golenishchev F.N., Dzuev R.I. 2013. Genetic diversity of Chionomys genus (Mammalia, Arvicolinae) and comparative phylogeography of snow voles. Russian Journal of Genetics 49(5): 561–575. DOI: 10.1134/S1022795413050025 [In Russian]
Benítez H.A., Lemic D., Püschel T.A., Gasparic H.V., Kos T., Baric B., Bazok R., Zivkovic I. 2018. Fluctuating asymmetry indicates levels of disturbance between agricultural productions: An example in Croatian population of Pterostichus melas melas (Coloptera: Carabidae). Zoologischer Anzeiger 276: 42–49. DOI:10.1016/j.jcz.2018.07.003
Bottaeva Z.Kh., Tembotova F.A., Bersekova Z.A., Emkuzheva M.M., Chapaev A.Kh. 2016. Ecological and geographical variation of immunological peripheral blood parameters of Chionomys gud (Cricetidae, Rodentia) from middle mountains of the Western and Central Caucasus. Proceedings of the Samara Scientific Centre of RAS 18(5): 83–88. [In Russian]
Buzan E.V., Kryštufek B. 2008. Phylogenetic position of Chionomys gud assessed from a complete cytochrome b gene. Folia Zoologica 57(3): 274–282.
Coda J.A., Gomez D., Martínez J.J., Steinmann A.R., Priotto J.W. 2016. The use of fluctuating asymmetry as a measure of farming practice effects in rodents: a species-specific response. Ecological Indicators 70: 269–275. DOI: 10.1016/j.ecolind.2016.06.018
Coda J.A., Martínez J.J., Steinmann A.R., Priotto J., Gomez M.D. 2017. Fluctuating asymmetry as an indicator of environmental stress in small mammals. Mastozoología Neotropical 24(2): 313–321.
Dzuev R.I., Khulamkhanova M.M., Sizhazheva A.M. 2011. Molecular systematics and biological characteristics of Chionomys gud Satunin, 1909 in the Caucasus. Makhachkala. 208 p. [In Russian]
Emelyanov P.F., Teknedzhyan V.A., Kvasov E.M. 1983. An ecology of Chionomys gud in the Western Caucasus. In: Prophylaxis of feral herd infections: Proceedings of the All – Union Scientific conference. Stavropol: Antiplague Research Institute of the Caucasus and Transcaucasia. P. 148–149. [In Russian]
Gileva E.A., Kosareva N.L. 1994. Decrease in fluctuating asymmetry among house mice in territories polluted with chemical and radioactive mutagens. Russian Journal of Ecology 25: 94–97. [In Russian]
Gileva E.A., Nokhrin D.Yu. 2001. Fluctuating asymmetry in cranial traits of east european voles (Microtus rossiaemeridionalis Ognev, 1924) from the zone of radioactive contamination. Russian Journal of Ecology 32(1): 113–120. DOI: 10.1023/A:1009570015708 [In Russian]
Gileva E.A., Yalkovskaya L.E., Borodin A.V., Zykov S.V., Kshnyasev I.A. 2007. Fluctuating asymmetry of craniometric characters in rodents (Mammalia: Rodentia): Interspecific and interpopulation comparisons. Zhurnal Obshchei Biologii 68(3): 221–230. [In Russian]
Graham J.H., Fletcher D., Tigue J., McDonald M. 2000. Growth and developmental stability of Drosophila melanagaster in low frequency magnectic fields. Bioelectromagnetics 21(6): 465–472.
Hammer Ø., Harper D.A.T., Ryan P.D. 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Paleontologia Electronica 4(1): 9.
Khulamkhanova M.M. 2006. Landscape preferences. In: Actual problems of modern science: Proceedings of the international conference of young scientists. Samara. P. 64–68. [In Russian]
Khulamkhanova M.M. 2007. Ecological and biological features of Chionomys gud Satunin, 1909 in the Caucasus. PhD Thesis Abstract. Makhachkala. 23 p. [In Russian]
Khulamkhanova M.M., Dzuev R.I., Pshikhacheva V.B. 2004. Peripheral blood comparative analysis of Caucasian snow vole (Chiomonys gud Sat.) in natural and experimental conditions. Herald of the Kabardino-Balkarian State University. Series Biological Sciences 6: 50–52. [In Russian]
Khulamkhanova M.M., Dzuev R.I. 2005. Ecological characteristics of Caucasian snow vole (Chiomonys gud Satunin, 1910) in natural and experimental conditions. Herald of the Kabardino-Balkarian State University. Series Biological Sciences 7: 75–80. [In Russian]
Kryštufek B. 1999. Snow voles, genus Chionomys of Turkey. Mammalia 63(3): 323–339. DOI: 10.1515/mamm.1999.63.3.323
Markowski J. 1993. Fluctuating asymmetry as an indicator for differentiation among roe deer (Capreolus capreolus) populations. Acta Theriologica 38(2): 19–31.
Mezhzherin S.V., Zagorodnyuk I.V., Khasanova L.V. 1990. Comparison of electrophoretic spectra of Chionomys and Microtus voles: scientific publication. In: 5^fh Congress of the All-Union Teriological Society of AS USSR. Moscow. P. 86. [In Russian]
Nadachowski A. 1991. Systematics, geographic variation and evolution of snow voles (Chionomys) based on dental characters. Acta Theriologica 36(1): 1–45. DOI: 10.4098/AT.arch.91-1
Okulova N.M., Yunicheva Yu.V., Baskevich M.I., Ryabova T.E., Agirov A.Kh., Balakirev A.E., Vasilenko L.E., Potapov S.G. 2005. Species diversity, distribution and population density of small mammals in the southern part of the Krasnodar region and the Republic of Adygeia. In: Mammals of mountain territories. Materials of the international conference. Moscow: KMK Scientific Press Ltd. P. 122–130. [In Russian]
Okulova N.M., Ryabova T.E., Vasilenko L.E., Yunicheva Yu.V. 2007. Overlapping of territorial ecological niches for small mammals in mountains and foothills of the Krasnodar region and Republik of Adygei. In: Mammals of mountain territories. Materials of the international conference. Moscow: KMK Scientific Press Ltd. P. 230–233. [In Russian]
Oleksyk T.K., Novak J.M., Purdue J.R., Gashchak S.P., Smith M.H. 2004. High levels of fluctuating asymmetry in populations of Apodemus flavicollis from the most contaminated areas in Chornobyl. Journal of Environmental Radioactivity 73(1): 1–20. DOI: 10.1016/j.jenvrad.2003.07.001
Pankakoski E., Koivisto I., Hyvarinen H. 1992. Reduced developmental stability as an indicator of heavy metal pollution in the common shrew, Sorex araneus. Acta Zoologica Fennica 191: 137–144.
Peskov V.N., Emelyanov I.G. 2000. Phenetics and phenogeography of the European water vole (Arvicola terrestris L.). Vestnik Zoologii 3: 39–44. [In Russian]
Ryadinskaya G.S., Kokhonov E.V. 2016. The variability of the meristic characters of the skull in red voles (Clethrionomys rutilus) from the territory of three administrative districts of the Tomsk region. In: Teriofauna of Russia and adjacent territories. Moscow. P. 368. [In Russian]
Sizhazheva A.M., Dzuev R.I. 2011. Basic tendencies in distribution and numbers of small mammals from the Caucasus which are determined by dynamics of natural and climatic factors (an example of Chionomys genus). South of Russia: Ecology, Development 6(3): 75–83. DOI: 10.18470/1992-1098-2011-3-75-83 [In Russian]
Sokolov V.E., Tembotov A.K. 1989. Vertebrates of the Caucasus. Mammals. Insectivores. Moscow: Nauka. 547 p. [In Russian]
Tembotov A.K., Shebzukhova E.A., Tembotova F.A., Vorokova I.L. 2001. Ecological problems in mountain areas. Maykop. 186 p. [In Russian]
Tembotova F.A., Amshokova A.Kh. 2018. Developmental Stability of the Skull in the Pygmy Wood Mouse (Mammalia, Rodentia) along Altitudinal Gradient in the Western and Central Caucasus. Russian Journal of Ecology 49(5): 395–400. DOI: 10.1134/S1067413618050144 [In Russian]
Vasil'ev A.G. 1995. Application package of PHEN 3 programs. Available from: http://ecoinf.uran.ru. [In Russian]
Vasil'ev A.G., Vasil'eva I.A., Bolshakov V.N. 1996. Phenetic monitoring of populations of the northern red-backed vole (Clethrionomys rutilus Pall.) in the zone of the Eastern Ural Radioactive Trace. Russian Journal of Ecology 27(2): 113–120.
Vasil'ev A.G., Vasil'eva I.A., Bolshakov V.N. 2000. Evolutionary ecological analysis of stability in the population structure of species: a chronogeographic approach. Yekaterinburg. 132 p. [In Russian]
Vasil'ev A.G. 2005. Epigenetic bases of phenetics: On the way to population meronomy. Yekaterinburg: Akademkniga. 640 p. [In Russian]
Vasil'ev A.G., Vasil'eva I.A. 2009. Homological variability of morphological structures and epigenetic divergence among taxa: Principles of population meronomy. Moscow: KMK Scientific Press Ltd. 511 p. [In Russian]
Vasil'eva I.A., Vasil'ev A.G., Lyubashevskii N.M., Chibiryak M.V., Zakharova E.Yu., Tarasov O.V. 2003. Phenogenetic analysis of pygmy wood mouse (Apodemus uralensis Pall.) populations in the Zone of the Eastern Ural Radioactive Trace (EURT). Russian Journal of Ecology 34(6): 405–412. DOI: 10.1023/A:1027364517929 [In Russian]
Veličković M. 2004. Chromosomal aberrancy and the level of fluctuating asymmetry in black-striped mouse (Apodemus agrarius): Effects of disturbed environment. Hereditas 140(2): 112–122. DOI: 10.1111/j.1601-5223.2004.01827.x
Vishalakshi C., Singh B.N. 2008. Effect of environmental stress on fluctuating asymmetry in certain morphological traits in Drosophila ananassae: nutrition and larval crowding. Canadian Journal of Zoology 86(5) 427–437. DOI: 10.1139/Z08-010
Yalkovskaya L.E., Fominykh M.A., Mukhacheva S.V., Davydova Y.A., Borodin A.V. 2016. Fluctuating asymmetry of rodent cranial structures in an industrial pollution gradient. Russian Journal of Ecology 47(3): 281–288. DOI: 10.1134/S1067413616030176
Yannic G., Burri R., Malikov V.G., Vogel P. 2012. Systematics of snow voles (Chionomys, Arvicolinae) revisited. Molecular Phylogenetics and Evolution 62(3): 806–815. DOI: 10.1016/j.ympev.2011.12.004
Zakharov V.M. 1987. Asymmetry in Animals. Moscow: Nauka. 216 p. [In Russian]
Zakharov V.M., Baranov A.S., Borisov V.I., Valetskiy A.V., Kryazheva N.G., Chistyakova E.K., Chubinishvili A.T. 2000. The Health of the Environment: Methods of Assessment). Moscow. 47 p. [In Russian]
Zhivotovskiy L.A. 1982. Indices of population variation in polymorphic characters. In: Population phenetics. Moscow: Nauka. P. 38–44. [In Russian]