Поведение самцов обыкновенной полевки хромосомных форм «arvalis» и «obscurus» в тесте форсированного плавания

С.А. Саблина и И.В. Белозерцева

Труды Зоологического института РАН, 2020, 324(2): 252–261 · https://doi.org/10.31610/trudyzin/2020.324.2.252

Резюме

Для определения различий реакции на физический стресс хромосомных форм обыкновенной полевки в тесте форсированного плавания оценивали поведение половозрелых (6–12 месяцев) самцов «arvalis» и «obscurus» из лабораторных популяций. Во время теста полевок аккуратно помещали в стеклянные цилиндры (d=12 см, h=20 см), заполненные водой (h=15 см; 24±1^оС), и в течение 6 мин записывали их действия на видеокамеру для последующей регистрации поведения (Ethograph, ver. 2.7, RITEC, Россия). Сравнивали продолжительность ряда элементов: плавание и гребля (ориентирование); дрейфование (неподвижность) и клаймбинг – залезание на стенку (избавление). Было выполнено 2 серии экспериментов (в мае 2016 и в июне 2017 гг.) с использованием независимых групп: «arvalis» (N=9 для каждого года) и «obscurus» (N=9 и N=22 по годам, соответственно). Представители хромосомных форм обыкновенной полевки существенно различались по реакции на стрессовую ситуацию. Более 35% самцов формы «obscurus» не смогли завершить тест, его прекращали в среднем через 3 мин во избежание гибели животных. Напротив, все полевки формы «arvalis» выполнили тест (значимые различия по точному критерию Фишера). Самцы «arvalis» дольше пытались выбраться из цилиндра (F(1.14)=3.5; P=0.08 – для первой, F(1.20)=15.6; P<0.001 – для второй серии эксперимента), меньше демонстрировали плавание и греблю (значимо в первой серии эксперимента – F(1.14)=14.3; P<0.005), меньше находились в неподвижном состоянии (значимо во второй серии эксперимента – F(1.20)=6.1; P<0.001). Полученные результаты свидетельствуют о существенных отличиях поведенческой реакции полевок двух хромосомных форм на стресс. В тесте форсированного плавания самцы «arvalis» демонстрируют большую выносливость, включая большую длительность активных попыток избегания по сравнению с самцами «obscurus». В дальнейшем следует оценить реакции хромосомных форм Microtus arvalis на другие стрессовые факторы и на водную среду в целом. Последнее может играть важную роль в миграции полевок при встрече водных преград в естественной среде обитания.

Ключевые слова

обыкновенная полевка, поведение, стресс, тест форсированное плавание, хромосомные формы, Microtus arvalis

Поступила в редакцию 27 февраля 2020 г. · Принята в печать 11 апреля 2020 г. · Опубликована 25 июня 2020 г.

Литература

Aubrecht T.G., Weil Z.M. and Nelson R.J. 2014. Melatonin treatment during early life interacts with restraint to alter neuronal morphology and provoke depressive-like responses. Behavioural Brain Research, 263: 90–97. https://doi.org/10.1016/j.bbr.2014.01.025

Baskevich M.I., Potapov S.G., Okulova N.M., Sapelnikov S.F., Vlasov A.A., Oparin M.L., Mironova T.A. and Avilova E.A. 2009. To distribution and variability of sibling species of Microtus arvalis (Rodentia, Arvicolinae) in Central Black Earth Region based on chromosome and molecular-genetic data. Zoologicheskiy zhurnal, 88(4): 473–487. [In Russian].

Baskevich M.I., Mironova T.A., Cherepanova E.V. and Krivonogov D.M. 2016. New data on chromosomal variability, distribution of sibling species, and hybridization of 46-chromosomal forms of Microtus arvalis sensu lato (Rodentia, Arvicolinae) in the Upper Volga basin. Biology Bulletin, 43(9): 1281–1291. https://doi.org/10.1134/s1062359016110042

Baskevich M.I., Khlyap L.A., Mironova T.A., Bogdanov A.S., Malygin V.M., Gadzhiyev A.H., Litvinova E.M. and Sapelnikov S. F. 2018. Role of genetic approaches in studying of areal borders of cryptic species and forms of grey volens in Eastern Europe. Materials of the International Conference: Topical issues of biogeography (9–12 October 2018, Saint Petersburg). Publishing House of Saint Petersburg State University, Saint Petersburg: 36–38. [In Russian].

Bohdal T., Navrátil J. and Sedláček F. 2016. Small terrestrial mammals living along streams acting as natural landscape barriers. Ekológia (Bratislava), 35(2): 191–204. https://doi.org/10.1515/eko-2016-0015

Bulatova N.Sh., Golenishchev F.N., Kovalskaia Yu.M., Emelianova L.G., Bystrakova N.V., Pavlova S.V., Nadzhafova R.S. and Lavrechenko L.A. 2010. Cytogenetic study of the parapatric contact zone between two 46-chromosomal forms of the common vole in European Russia. Genetika, 46(4): 443–448. [In Russian]. https://doi.org/10.1134/s1022795410040095

Bulatova N.Sh., Gromov A.R., Kostin D.C. and Lavrechenko L.A. 2016. Karyomorphs arvalis and obscurus of common vole as genetic species. Theriofauna of Russia and adjacent territories. International Conference X Congress of Russian Theriological Society RAS (1–5 February 2016, Moscow). KMK scientific press, Moscow: 61. [In Russian].

Bulatova, N.Sh., Pavlova, S.V., Potapov S.G. and Gromov A.R. 2017. Nucleolar organizing regions (NORs) of common vole chromosomes as nuclear markers of genome differentiation in data from a hybrid zone of two karyoforms, arvalis and obscurus. Genetika, 53(6): 736–739. [In Russian]. https://doi.org/10.1134/s1022795417060035

Cook W.M., Timm R.M. and Hyman D.E. 2001. Swimming ability in three Costa Rican dry forest rodents. Revista de Biologia Tropical, 49(3–4): 1177–1181.

Duplantier J.M. and Bâ K. 2001. Swimming ability in six West-African rodents under laboratory conditions: evaluation of their potentialities to invade islands. In: C. Denys, L. Granjon and A. Poulet (Eds). African small mammals. IRD, Paris: 331–342.

Giannoni S.M., Borghi C.E. and Martinez-Rica J.P. 1994. Swimming ability of the Mediterranean pine vole Microtus (Terricola) duodecimcostatus. Acta Theriologica, 39(3): 257–265. https://doi.org/10.4098/at.arch.94-29

Giannoni S.M., Borghi C.E. and Laconi M.R. 2001. Swimming ability of the European fossorial vole Microtus (T.) gerbei under different laboratory conditions. Mammalia, 65(2): 143–150. https://doi.org/10.1515/mamm.2001.65.2.143

Golenishchev F.N., Meyer M.N. and Bulatova N.Sh. 2001. The hybrid zone between two karyomorphs of Microtus arvalis (Rodentia, Arvicolinae). Proceedings of the Zoological Institute RAS, 289: 89–94.

Gromov A.R., Bulatova N.Sh., Potapov S.G., Kostin D.C. and Lavrechenko L.A. 2015. Study of the hybrid zone between 46-chromosomal forms of common vole in the Vladimir region. The structure of mammalian species. Scientific Conference (21–23 October 2015, Moscow). KMK Scientific Press, Moscow: 29. [In Russian].

Hickman G.C. and Machiné C. 1986. Swimming behaviour in six species of African Rodents (Cricetidae, Muridae). Acta Theriologica, 31(33): 449–466. https://doi.org/10.4098/at.arch.86-41

Ivanov N.B., Markova E.A., Golenishchev F.N. and Malygin V.M. 2007. Morphological variability and taxonomic status of the kariforms of the common vole Microtus arvalis. Materials of the international meeting: Teriofauna of Russia and adjacent territories. VII Congress of the Theriological society (31 January – 2 February 2007, Moscow). Nauka, Moscow: 173. [In Russian].

Ivlev Yu.F. 1985. To the method of determining the air layer in the hair of mammals in the water. Zoologicheskiy zhurnal, 64(11): 1727–1731. [In Russian].

Ivlev Yu.F. 1995. Functional properties of hair follicles of semi-aquatic mammals (by the example of water voles). Abstract of the Candidate of Biological Sciences. Moscow, 216 p. [In Russian].

Ivlev Yu. F. 2018. Biomechanical analysis of fur as a tool for the study of thermal insulation in semi-aquatic mammals. Zoologicheskiy Zhurnal, 97(8): 1055–1074. [In Russian].

Kloet E.R. and Molendijk M.L. 2016. Coping with the forced swim stressor: Towards understanding an adaptive mechanism. Neural Plasticity, 2016: 1–13. https://doi.org/10.1155/2016/6503162

Kokshaysky N.V. 2008. Selected works. KMK scientific press, Moscow, 410 p. [In Russian].

Kotenkova E.V., Golenishchev F.N., Bulatova N.Sh., Ambaryan A.V., Petkova K. and Lipina N.S. 2006. Role of smell in choosing the sexual partner based on voles of “arvalis” group. Population ecology of animals. Materials of International Conference: Problems in population ecology of animals. Tomsk State University, Tomsk: 140–142. [In Russian].

Kotenkova E.V. and Voznessenskaya V.V. 2005. Mechanisms of isolation in rodents: from behavior to receptors. Behavior and behavioral ecology of mammals: proceedings of the scientific conference (4–8 October 2005, Chernogolovka). KMK scientific press, Moscow: 324–326. [In Russian].

Krivisky K., Ashkenazy T., Kronfeld-Schor N. and Einat H. 2011. Antidepressants reverse short-photoperiod-induced, forced swim test depression-like behavior in the diurnal fat sand rat: further support for the utilization of diurnal rodents for modeling affective disorders. Neuropsychobiology, 63(3): 191–196. https://doi.org/10.1159/000321805

Lavrenchenko L.A., Potapov S.G., Bulatova N.Sh. and Golenishchev F.N. 2009. A genetic study of natural hybridization between two forms of the common vole (Microtus arvalis) with the use of molecular and cyto-genetic methods. Doklady Biological Sciences, 426(1): 222–224. [In Russian]. https://doi.org/10.1134/s0012496609030090

Leach G., Adidharma W. and Yan L. 2013. Depression-like responses induced by daytime light deficiency in the diurnal grass rat (Arvicanthis niloticus). PLoS ONE 8(2): e57115. https://doi.org/10.1371/journal.pone.0057115

Macdonald D. 2002. The new encyclopedia of mammals. University Press, Oxford: 455 p.

Malygin V.M. 1974. A comparative morphometric analysis of karyotypes in two geographical forms of 46-chromosome common vole Microtus arvalis. Zoologicheskiy zhurnal, 53(5): 769–777. [In Russian].

Malygin V.M. 2009. Zoogeographical factor in evolution of voles (“arvalis” group). Modern problems in zoo- and phylogeography of mammals. Materials of Conference (15–29 May 2009). KMK Scientific Press, Penza: 52. [In Russian].

Malygin V.M. 2010. Review on taxonomic status of two karyomorphs of common vole (Microtus arvalis) based on results of experimental hybridization. Materials of Conference: Species integrity of mammals (isolation barriers and hybridization). KMK Scientific Press, Moscow: 55. [In Russian].

Malygin V.M., Baskevich M.I. and Khlyap L.A. 2019. The invasions of the common vole sibling species. Russian Journal of Biological Invasions, 4: 71–93. [In Russian].

Meyer M.N., Orlov V.N. and Skholl E.D. 1972. Sibling species in the group Microtus arvalis (Rodentia, Cricetidae). Zoologicheskiy zhurnal, 51(5): 724–738. [In Russian].

Meyer M.N., Golenishchev F.N., Radjably S.I. and Sablina O.V. 1996. Voles (subgenus Microtus Schrank) of Russia and adjacent territories. Proceedings of the Zoological Institute RAS, 232: 1–320. [In Russian].

Meyer M.N., Golenishchev F.N., Bulatova N.Sh. and Artobolevskiy G.V. 1997. On distribution of two Microtus arvalis chromosomal forms in European Russia. Zoologicheskiy zhurnal, 76(4): 487–493. [In Russian].

Meyer, M.N., Golenishchev, F.N., Bulatova, N.Sh. and Packevich E.S. 2000. The reproductive isolation between two kariomorphs of Microtus arvalis (Rodentia, Arvicolinae). In: A.K. Agadjanian and V.N. Orlov (Eds). Systematic and Phylogeny of the Rodents and Lagomorphs. Russian Academy of Sciences, Moscow: 114–116.

Mironova T.A., Baskevich T.A., Krivonogov D.M. and Lavrechenko L.A. 2016. Intensity of gene flow and structure of hybrid populations of common voles in supra-specific complex Microtus arvalis. Theriofauna of Russia and adjacent territories. International Conference X Congress of Russian Theriological Society RAS (1–5 February 2016, Moscow). KMK Scientific Press, Moscow: 267. [In Russian].

Motulsky H.J. 2014. Common misconceptions about data analysis and statistics. Naunyn-Schmiedeberg’s Archives of Pharmacology, 387: 1017–1023. https://doi.org/10.1007/s00210-014-1037-6

Nicolas V. and Colyn M. 2006. Swimming ability of 5 species of African rainforest murid rodents in relation to their habitat preferences. Zoological Studies, 45(2): 264–268.

Orlov V.N. and Malygin V.M. 1969. Two forms of 46-chromosome common vole, Microtus arvalis. Materials of the 2 all-Union meeting on mammals. Siberian Branch of USSR Academy of Sciences, Novosibirsk: 143–144. [In Russian].

Porsolt R.D., Le Pichon M. and Jalfre M. 1977a. Depression: a new animal model sensitive to antidepressant treatments. Nature, 266: 730–732. https://doi.org/10.1038/266730a0

Porsolt R.D., Bertin A. and Jalfre M. 1977b. Behavioral despair in mice: a primary screening test for antidepressants. Archives Internationales de Pharmacodynamie et de Thérapie, 229(2): 327–336.

Potapov S.G., Okulova N.M. and Baskevich M.I. 2007. Molecular genetic research (RAPD-analysis) of Microtus arvalis s. l. (Rodentia, Arvicolidae) on the Russian plain. Proceedings of the all-Russian meeting: Molecular genetic bases of conservation of Holarctic mammal biodiversity (26–30 November 2007, Chernogolovka). KMK Scientific Press, Moscow: 213–220. [In Russian].

Potapov S.G., Bulatova N. Sh., Lavrechenko L.A. and Golenishchev F.N. 2010. Molecular and genetic characteristics of natural hybridization zone of two common voles (Microtus arvalis) forms in the Vladimir region. Materials of conference: Species integrity of mammals (isolation barriers and hybridization) (12–17 May 2010, Peterhof). KMK Scientific Press, Moscow: 68. [In Russian].

Sablina S.A. and Belozertseva I.V. 2012. Behavior of arvalis and obscurus chromosomal forms of common vole (Microtus arvalis) males in tests of olfactory preference and open field. Zoologicheskiy zhurnal, 91(2): 208–218. [In Russian].

Sablina S.A., Tikhonova E.P. and Belozertseva I.V. 2017. Behavior of arvalis and obscurus chromosomal forms of common vole (Microtus arvalis Pallas, 1779) males in the partition test. Proceedings of the Zoological Institute RAS, 321(2): 218–227. [In Russian].

Sokolov V.E. 1973. Mammal skin. Nauka, Moscow, 487 p. [In Russian].

Sun P., Smith A.S., Lei K., Liu Y. and Wang Z. 2014. Breaking bonds in male prairie vole: long-term effects on emotional and social behavior, physiology, and neurochemistry. Behavioural Brain Research, 265: 22–31. https://doi.org/10.1016/j.bbr.2014.02.016

Tikhonov I.A. and Tikhonova G.N. 2004. The role of olfaction, sight, and vibrissal sense in the exploratory behavior of Microtus arvalis s.l. sibling species. Zoologicheskiy zhurnal, 83(5): 1–8. [In Russian].

Tikhonova G.N., Tikhonov I.A., Davydova L.V. and Osipova O.V. 2003. Intraspecific relationships between sibling species of the common vole under experimental conditions. Zoologicheskiy zhurnal, 82(8): 986–997. [In Russian].

Tikhonova G.N., Tikhonov I.A. and Osipova O.V. 2008. Some behavioral characteristics of common voles Microtus arvalis arvalis and Microtus arvalis obscurus in family groups under experimental conditions. Biology Bulletin, 5: 561–568. [In Russian]. https://doi.org/10.1134/s1062359008050087

Tougardt Ch., Montuire S., Volobouev V., Markova E., Contet J., Aniskin V. and Quere J.P. 2013. Exploring phylogeography and species limits in the Altai vole (Rodentia: Cricetidae). Biological Journal of the Linnean Society, 108: 434–452. https://doi.org/10.1111/j.1095-8312.2012.02034.x

Zagorodnyuk I.V. 1990. Karyotypic variability and systematics of the Arvicolini (Rodentia). Communication 1. Species and chromosomal numbers. Vestnik zoologii, 2: 26–37. [In Russian].

Zagorodnyuk I.V. 1991. Karyotypic variability of 46-chromosome voles of the Microtus arvalis group (Rodentia); taxonomic interpretation. Vestnik zoologii, 1: 36–45. [In Russian].

Zorenko T.A. 1994. Ethology. In: V.E. Sokolov and N.V. Bashenina (Eds). Common Vole: The Sibling-Species. Nauka, Moscow: 299–320. [In Russian].

Zorenko T.A., Zakharov K.V. and Berezina R.Yu. 1989. Exploratory behavior of voles: taxonomical and microevolution aspects of problem. In: T.A. Zorenko (Ed.). Actual problems of Zoology. Latvian State University, Riga: 57–110. [In Russian].