Diet selection by the social vole Microtus socialis (Pallas, 1773) in the Northwest Caspian Lowland

Scopin A.E., Dzhapova V.V., Bembeeva O.G., Ayusheva E.Ch., Dzhapova R.R., Abaturov B.D.

P. 136-148

The article presents the research results the food selection and preferences of the social vole Microtus socialis in the dry steppes (northern subzone of the deserts) in the Chernye Zemli State Biosphere Reserve (north-western part of the Caspian Lowland). It is the first time when the data on seasonal variability of food composition of social voles in their permanent settlements has been obtained by means of cuticular microhistological feces analysis. The diet of the voles consists of 31 plant species. The basis of the diet is grasses (55–95%), mainly Poa bulbosa. Forbs are consumed in smaller amounts, but they play an important role in the summer life of the rodent. In spring, the tulip bulbs (Tulipa biebersteiniana) and the terrestrial parts of Chorispora tenella are of greatest importance in the nutrition of the vole. These herbivores do not eat Bassia hyssopifolia, Phlomis pungens, Carduus acanthoides at all. Voles maximize the use of forage diversity in the area of their settlements. The trophic interactions of rodents to certain plant species were evaluated through the preferences of baits containing plant extracts. The social voles consume baits with extracts from different plant species in varying degrees. In general, the consumption of baits containing grass extracts is higher than that of baits containing extracts from most species of forbs. In the group of forbs, the social vole unequivocally prefer baits containing tulip extracts. The baits with other forbs are consumed by two or more times less than those with grass extracts. The social vole gives the least preference to baits with extracts from Senecio vernalis and Tanacetum achilleifolium. Most likely, a high concentration of toxic secondary metabolites is the main reason for voles avoiding certain baits with plant extracts.DOI: 10.15298/rusjtheriol.19.2.04

• Abaturov B.D. 1984. [Mammals as a Component of Ecosystems]. Moscow: Nauka. 286 p. [in Russian].
• Abaturov B.D., Dzhapova R.R., Kazmin V.D., Ajusheva E.Ch. & Dzhapova V.V. 2019. Comparative features of the nutrition of the Przewalski horse Equus przewalskii, the camel Camelus bactrianus, and the saiga Saiga tatarica on an isolated steppe pasture // Biology Bulletin. Vol.46. P.594–607.
• Abaturov B.D., Kazmin V.D., Dzhapova R.R., Kolesnikov M.P., Ayusheva E.Ch., Dzhapova V.V., Nokhaeva D.V., Kolesnikov M.P., Minoranskiy V.A. & Kuznetsov Yu.E. 2018. [Forage resources, nutrition and food supply of free-grazing camels (Camelus bactrianus) in a pasture in the natural steppe zone] // Zoologicheskii Zhurnal. Vol.97. No.3. P.348–361 [in Russian with English summary].
• Abaturov B.D. & Khashaeva M.G. 1995. [Digestion of green vegetable food by rodents with different nutritional types and in relation to the phenophases of plants] // Zoologicheskii Zhurnal. Vol.74. No.4. P.132–142 [in Russian with English summary].
• Abaturov B.D. & Scopin A.E. 2019. [Grasses and forbs in steppe pastures, their toxic properties and comparative role in nutrition of herbivorous mammals] // Zhurnal Obshchei Biologii. Vol.80. No.3. P.226–237 [in Russian with English summary].
• Andrushko A.M. 1939. [The Role of Rodents in the Dry Pastures of the Central Asia]. Leningrad: Leningrad State University Press. 153 p. [in Russian with English summary].
• Archibald S., Bond W.J., Hoffmann W., Lehmann C., Staver C.& Stevens N. 2020. Distribution and determinants of savannas // Scogings P.F. & Sankaran M. (eds.). Savanna Woody Plants and Large Herbivores. Hoboken: John Wiley & Sons Ltd. P.3–24.
• Argiropulo A.I. 1935. [Notes about the summer biology of the social vole in the Transcaucasus (in the conditions of a virgin mixed grass steppe)] // Trudy Azerbaijanskogo Microbiologicheskogo Instituta. Vol.5. No.1. P.217–227 [in Russian with German summary].
• Bashenina N.V. 1962. [Ecology of the Common Vole (Microtus arvalis) and Some Features of its Geographical Variability]. Moscow: Moscow State University Press. 308 p. [in Russian].
• Bashenina N.V. 1977. [Adaptive Strategies of Microtine Rodents]. Moscow: Nauka. 356 p. [in Russian].
• Batzli G.O. 1985. Nutrition // Tamarin R.H. (ed.). Biology of New World Microtus. Special Publication of the American Society of Mammalogists. No.8. P.779–811.
• Bergeron J.-M., Jodoin L. & Jean Y. 1987. Pathology of voles (Microtus pennsylvanicus) fed with plant extracts // Journal of Mammalogy. Vol.68. No.1. P.73–79.
• Berishvili I.M. 1968. [Voles of Georgia (Microtus socialis Pall. and Microtus arvalis Pall.) and effective measures to combat them]. Abstract of Dr.Sci. Thesis. Tbilisi: Georgian Agriculture Institute. 53 p. [in Russian].
• Bucyanayandi J.-D. & Bergeron J.-M. 1990. Effects of food quality on feeding patterns of meadow voles (Microtus pennsylanicus) along a community gradient // Journal of Mammalogy. Vol.71. No.3. P.390–396.
• Bukreeva O.M. & Lidzhi-Garyaeva G.V. 2018. [Mass migration and death of the social voles (Microtus socialis (Pallas, 1773) in the Northwest Caspian Lowland] // Aridnye Ekosystemy. Vol.24. No.2 (75). P.82–88 [in Russian].
• Bukhareva O.A. & Bykov A.V. 2014. [Spatial and temperature characteristics of social vole (Microtus socialis) burrows in the clay semi-desert of the Trans-Volga Region] // Zoologicheskii Zhurnal. Vol.93. No.12. P.1461–1469 [in Russian].
• Butovsky P.M. 1955. [Seasonal changes in the nutrition of the little ground squirrel (Spermophilus pygmaeus) and the nature of its distribution in the Western Kazakhstan]. Abstract of PhD Thesis. Alma-Ata: Institut Zoologii Akademii Nauk Kazakhskoi SSR. 15 p. [in Russian].
• Bykov A.V., Kolesnikov A.V., Kulakova N.Yu. & Shabanova N.P. 2008. Accumulation of moisture and soil erosion in the territory of social vole (Microtus socialis) settlements in the Northern Caspian Lowland // Eurasian Soil Science. Vol.41. No.8. P.902–906.
• Bykov A.V., Shabanova N.P. & Bukhareva O.A. 2011. Distribution and survival of the social vole in a clayey semidesert of the Trans-Volga Region // Biology Bulletin. Vol.38. No.10. P.957–961.
• Bykov B.A. 1978. [Geobotany]. Alma-Ata: Nauka. 288 p. [in Russian].
• Byrom A.E., Ruscoe W.A., Nkwabi A.K., Metzger K.L., Forrester G.J., Craft M.E., Durant S.M., Makacha S., Bukombe J., Mchetto J., Mduma S.A.R., Reed D.N., Hampson K. & Sinclair A.R.E. 2015. Small mammal diversity and population dynamics in the Greater Serengeti Ecosystem // Sinclair A.R.E., Metzger K.L., Mduma S.A.R. & Fryxell J.M. (eds.). Serengeti IV. Sustaining Biodiversity in a Coupled Human-Natural System. Chicago: University of Chicago Press. P.323–357.
• Chizhikov O.N. 1954. [Vegetation of Chernye Zemli pastures (Astrakhan Oblast) in connection with the features of their use]. Abstract of PhD Thesis. Moscow: Williams Fodder Research Institute. 20 p. [in Russian].
• Doskach A.G. 1979. [Natural Division of the Caspian Semi-Desert]. Moscow: Nauka. 142 p. [in Russian].
• Dzhapova R.R., Ayusheva E.Ch., Bembeeva O.G., Dzhapova V.V., Daltaeva Yu.N., Nokhaeva D.V., Nonieva Z.A. & Babusheva D.B. 2019. [Atlas of the Standard Samples of the Cuticular Surface of Various Plants in the Steppes and Semi-Deserts]. Elista: Kalmyk State University Press. 94 p. [in Russian].
• Formozov A.N. & Kiris I.B. 1937. [Rodent activity on pastures and hayfields. The influence of the social vole (Microtus socialis Pall.) and some other rodents on the vegetation of the Kizlyar district of the Dagestan ASSR] // Uchenye Zapiski Moskovskogo Gosudarstvennogo Universiteta. Zoologiya. Vol.13. P.59–70 [in Russian with English summary].
• Gordon I.J. 2006. Restoring the functions of grazed ecosystems // Danell K., Duncan P., Bergstrom R. & Pastor J. (eds.). Large Herbivore Ecology, Ecosystem Dynamics and Conservation. Cambridge: Cambridge University Press. P.449–467.
• Gromov I.M. & Polyakov I.Ya. 1977. [Fauna of the USSR. Mammals. Vol.3. No.7. Voles (Microtinae)]. Leningrad: Nauka. 504 p. [in Russian].
• Gusynin I.A. 1955. [Toxicology of Poisonous Plants]. Moscow: Selkhozizdat. 330 p. [in Russian].
• Haken A.E. & Batzli G.O. 1996. Effects of availability of food and interspecific competition on diets of prairie voles (Microtus ochrogaster) // Journal of Mammalogy. Vol.77. No.2. P.315–324.
• Ivanenko I.D. 1940. [Microtus socialis Pall. as the principal component of the ecosystem of the Prisivash steppe] // Naukovi Zapiski Khersonskogo Derzhavnogo Pedagogichnogo Instituta N.K. Krupskoi. No.1. P.149–173 [in Ukrainian with English summary].
• Ivlev V.S. 1946. The dependence of the food electivity of fishes on the character of its distribution at the bottom of the sea // Zoologicheskii Zhurnal. Vol.25. No.3. P.269–276 [in Russian with English summary].
• Jung H.-J.C. & Batzli G.O. 1981. Nutritional ecology of microtine rodents: effects of plant extracts on the growth of Arctic microtines // Journal of Mammalogy. Vol.62. No.2. P.286–292.
• Kasatkin M.V. 2002. [Features of biology and population structure of the social vole (Microtus socialis Pall.)] // Sbornik Nauchnykh Rabot Gosudarstvennogo Biologicheskogo Muzeya K.A. Timiryazeva. Moscow: Erudite-K. P.103–142 [in Russian].
• Kasatkin M.V., Isaev S.I. & Savinetskaya L.E. 1998. [Some features of the ecology of the social vole (Microtus socialis) in the Chernye Zemli (Kalmykia) during increasing numbers] // Zoologicheskii Zhurnal. Vol.77. No.5. P.582–592 [in Russian with English summary].
• Kaufman G.A. & Kaufman D.W. 1997. Ecology of small mammals in prairie landscapes // Knopf F.L. & Samson F.B. (eds.). Ecology and Conservation of Great Plains Vertebrates. New York: Springer. P.207–243.
• Kazmin V.D., Demina O.N., Pozdnyakova M.K., Rozenfeld S.B. & Abaturov B.D. 2013. [The current state of plant forage resources and feeding selectivity of free horses (Equus caballus) on Steppe Island in Lake Manych-Gudilo] // Zoologicheskii Zhurnal. Vol.92. No.2. P.231–237 [in Russian with English summary].
• Khalilaria A. & Çolak E. 2013. Some ecological aspects of the genus Microtus Schrank, 1798 (Mammalia: Rodentia) in Northwest of Iran // Iranian Journal of Animal Biosystematics. Vol.9. No.2. P.135–146.
• Khashaeva M.G. 1993. [Comparative analysis of food consumption and digestion by rodents (for example, Meriones tamariscinus, Mesocricetus raddei, Microtus socialis)]. Abstract of PhD Thesis. Moscow: Institute of Evolutionary Morphology and Animal Ecology. 23 p. [in Russian].
• Khodashova K.S. 1960. [The Natural Environment and Fauna of the Clay Semi-deserts of the Volga Region]. Moscow–Leningrad: Izdatelstvo Akademii Nauk SSSR. 140 p. [in Russian]. Kokhiya S.S. 1968. [Social Vole (Microtus socialis Pall.) in Georgia]. Tbilisi: Metzniereba. 135 p. [in Russian].
• Krebs Ch. 2013. Population Fluctuations in Rodents. Chicago: University of Chicago Press. 306 p.
• Kryltsov A.I. 1964. [Steppe lemmings (Lagurus lagurus) and narrow-headed voles (Lasiopodomys gregalis) in the north of the Kazakhstan] // Trudy Instituta Zashchity Rastenii. Vol.8. P.1–183 [in Russian].
• Kryštufek B., Bužan E., Vohralik V., Zareie R. & Özkan B. 2009. Mitochondrial cytochrome b sequence yields new insight into the speciation of social voles in south-west Asia // Biological Journal of the Linnean Society. Vol.98. P.121–128.
• Kryštufek B., Zorenko T. & Bužan E. 2012. New insights into the taxonomy and phylogeny of social voles inferred from mitochondrial cytochrome b sequences // Mammalian Biology. Vol.77. P.178–182.
• Larionov K.O., Bykov A.V., Vyshivkin A.A. & Shadrina M.B. 2011. The diet composition of the social vole at the beginning stage of colonization of a zonal plain in a clayey semidesert of the Trans-Volga Region // Biology Bulletin. Vol.38. No.10. P.997–1000.
• Luthi M., Nentwig W. & Airoldi J.-P. 2010. Nutritional ecology of Microtus arvalis (Pallas, 1779) in sown wild flower fields and quasi-natural habitats // Revue Suisse de Zoologie. Vol.117. No.4. P.811–828.
• Magomedov M.Sh. 2017. [An analysis of rodent feeding in the foothill zone of the Republic of Dagestan: a microhistological cuticular-coprological method] // Zoologicheskii Zhurnal. Vol.96. No.5. P.581–588 [in Russian with English summary]. Moshkin M.P. & Shilova S.A. 2008. [Morpho-behavioral heterogeneity as the basis of population stability] // Uspekhi Sovremennoi Biologii. Vol.128. No.3. P.307–320 [in Russian with English summary].
• Mironov N.P. 1945. [The species composition and ecological distribution of rodents in the Northwestern Caspian Lowland] // Trudy Rostov-na-Donu Protivochumnogo Instituta. Vol.4. P.77–93 [in Russian with English summary].
• Naumov N.P. 1948. [Essays on the Comparative Ecology of Microtine Rodents]. Moscow–Leningrad: Izdatelstvo Akademii Nauk USSR. 204 p. [in Russian].
• Neronov V.V. 1999. [Natural conditions of the Chernye Zemli Biosphere Reserve] // Zapovednoe Delo. Vol.4. P.87–103 [in Russian].
• Nurgeldyev O.N. 1956. [On the geographical distribution and ecology of the social vole (Microtus socialis paradoxus Ogn. et Heptn.) in the Turkmenistan] // Trudy Instituta Biologii Akademii Nauk Turkmenskoi SSR. Vol.4. P.36–44 [in Russian].
• Okulova N.M., Mironova T.A., Sapel’nikov S.F., Nikonova O.A., Abaturov B.D. & Baskevich M.I. 2015. Autumn diets of sibling species Microtus arvalis sensu lato and M. agrestis (Rodentia, Arvicolinae) in the forest-steppe of the Central Chernozem Zone // Russian Journal of Ecology. Vol.46. No.2. P.181–188.
• Owen-Smith N. 2005. Adaptive Herbivore Ecology: From Resources to Populations in Variable Environments. Johannesburg: Wits University Press. 392 p.
• Pardinas U.F.S., Myers P., Leon-Paniagua L., Ordonez Garza N., Cook J.A., Krystufek B., Haslauer R., Bradley R.D., Shenbrot G.I. & Patton J.L. 2017. Family Cricetidae // Handbook of the Mammals of the World. Vol.7. Rodents II. Barcelona: Lynx Edicions. P.204–535.
• Pavlov A.N. 1959. [On the nutrition of Meriones meridianus and M. tamariscinus in the Northwest Caspian Lowland] // Trudy Rostov-na-Donu Gosudarstvennogo Protivochumnogo Instituta i Stalingradskoi Protivochumnoi Stantsii. Vol.14. P.245–257 [in Russian].
• Phillipson J., Sarrasin-Comans M. & Stomatopoulos C. 1983. Food consumption by Microtus agrestis and the unsuitability of faecal analysis for the determination of preference // Acta Theriologica. Vol.28. P.397–416.
• Polishchuk I.K. 1985. [Nutrition of the social vole on the virgin steppe “Askania Nova” and surrounding agroecosystems] // Vestnik Zoologii. No.3. P.70–72 [in Russian].
• Ponyatovskaya V.M. 1964. [Accounting for the abundance and features of the distribution of species in the natural plant community] // Polevaya Geobotanika. Vol.3. P.209–299 [in Russian].
• Rodionov Z.S. 1924. [Biology of the Social Vole and Experiments in Combating it in the Caucasus]. Leningrad: Tipografiya Gutenberga. 191 p. [in Russian].
• Rosenthal G.A. & Berenbaum M.R. (eds.). 1991. Herbivores. Their Interactions with Secondary Plant Metabolites. Vol.1. San Diego: Academic Press. 468 p.
• Scholes R.J. & Walker B.H. 1993. An African Savanna. Cambridge: Cambridge University Press. 306 p.
• Scopin A.E. 2000. [The selective preference of plant baits by the common vole (Microtus arvalis)] // Aktualnye Problemy Biologii i Ekologii. Vol.2. Syktyvkar: Institut Biologii Komi Nauchogo Tsentra. P.202–203 [in Russian].
• Scopin A.E. 2003. [The Significance of the Components of the Qualitative Composition of Forage Plants for Wild Animals]. Kirov: VNIIOZ. 203 p. [in Russian].
• Shilova S.A. & Kasatkin M.V. 2000. Comparative analysis of the population structure of social vole (Microtus socialis Pall., 1773, Cricetidae, Rodentia) in different areas of its range // Russian Journal of Ecology. Vol.31. No.4. P.262–268.
• Shorygin A.A. 1939. Food and food preference of some Gobiidae of the Caspian Sea // Zoologicheskii Zhurnal. Vol.18. No.1. P.27–53 [in Russian with English summary].
• Stapp P., Van Horne B. & Lindquist M.D. 2008. Ecology of mammals of the short-grass steppe // Lauenroth W.K. & Burke I.C. (eds.). Ecology of the Shortgrass Steppe. A Long-Term Perspective. Oxford: Oxford University Press. P.132–180.
• Stewart D.R.M. 1967. Analysis of plant epidermis in faeces: a technique of studying the food preference of grazing herbivores // Journal of Applied Ecology. Vol. 4. P.83–111.
• Trofimov I.A. 1995. [Natural pasture lands of the Chernye zemli] // Zonn I.S. & Neronov V.M. (eds.). Biota i Prirodnaya Sreda Kalmykii. Moscow–Elista: Korkis. P.53–83 [in Russian].
• Tsatsenkin I.A., Maksimova V.F. & Shcherbinovskaya T.N. 1957. [Geobotanical division] // Voronov A.G. (ed.). Trudy Prikaspiskoi Ekspeditsii. Rastitelnost’ i Kormovye Resursy Zapadnoi Chasti Prikaspiskoi Nizmennosti i Ergenei. Moscow: Moscow State University Press. P.158–165 [in Russian].
• Vereshchagin N.K. 1946. [The main ecological features of the social vole in the semi-desert zone of the Azerbaijan Republic] // Trudy Instituta Zoologii Akademii Nauk Azerbaijanskoi SSR. Vol.11. P.144–182 [in Russian].
• Voronov A.G. 1935a. [Some observations of the activity of the social vole (Microtus socialis Pall.) on the foothill pastures of the Dagestan] // Byulleten Moskovskogo Obshchestva Ispytatelei Prirody. Otdel Biologicheskii. Vol.44. No.6. P.314–322 [in Russian with French summary].
• Voronov A.G. 1935b. [Some observations of the activity of the social vole (Microtus socialis Pall.) on the foothill pastures of the Dagestan] // Byuleten Moskovskogo Obshchestva Ispytatelei Prirody. Otdel Biologicheskii. Vol.44. No.7/8. P.391–413 [in Russian with French summary].