Spacing and parental behavior in the Mongolian vole (Microtus mongolicus)

Spacing and parental behavior in the Mongolian vole (Microtus mongolicus)

Dontsova P.S., Smorkatcheva A.V., Bazhenov Y.A.

P. 121-132

The relationship between parental care patterns and mating system in voles has not been fully elucidated. Whereas mating and parental strategies have been reported for many New World arvicolines, such information is lacking for most Palearctic voles. Nothing is known about the social organization of Microtus mongolicus inhabiting mesic habitats of Central Asia. We investigated spacing of free-ranging M. mongolicus in Zabaykalsky Kray using mark-recapture method, and we assessed the parental care exhibited by Mongolian voles in laboratory. Home ranges (HR) and movement distances of overwintered males exceeded those of other categories of voles. HR overlapped within sexes and between sexes in linear habitat at high population density as well as in non-linear habitat at low density. The revealed pattern of spacing is consistent with promiscuous mating system. In laboratory, both the parent-litter separation tests and undisturbed observations of animals in large enclosures showed that most males displayed paternal behavior at the level comparable to that of socially monogamous species. Our results demonstrate that monogamous mating system cannot be inferred from biparental care detected in captivity. DOI: 10.15298/rusjtheriol.15.2.05

Literature
  • Abramsky Z. & Tracy C.R. 1980. Relation between home range size and regulation of population size in Microtus ochrogaster // Oikos. Vol.34. P.347–355.
  • Abramson N.I., Lebedev V.S., Tesakov A.S. & Bannikova A.A. 2009. [Supraspecies relationships in the subfamily Arvicolinae (Rodentia, Cricetidae): an unexpected result of nuclear gene analysis] // Molekulyarnaya Biologiya. Vol.43. P.834–846 [in Russian, with English abstract].
  • Agrell J. 1994. A shift in female social organization independent of relatedness: an experimental study on the field vole (Microtus agrestis) // Behavioral Ecology. Vol.6. P.182–191.
  • Altmann J. 1974. Observational study of behaviour: sampling methods // Behavioral. Vol.49. P.227–267
  • Bannikova A.A., Lebedev V.S., Lissovsky A.A., Matrosova V., Abramson N.I., Obolenskaya E.V. & Tesakov A.S. 2010. Molecular phylogeny and evolution of the Asian lineage of vole genus Microtus (Rodentia: Arvicolinae) inferred from mitochondrial cytochrome b sequence // Biological Journal of the Linnean Society. Vol.99. P.595–613.
  • Bazhenov Y.A. 2011. [New data on the ecology of the Mongolian vole (Microtus mongolicus) in Transbaikalia region] // Proceedings of the International Meeting “Theriofauna of Russia and Adjacent Territories” (9 Congress of the Theriological Society of RAS), Moscow. P.36 [in Russian].
  • Borkowska A. & Ratkiewicz M. 2010. Promiscuity, male reproductive success and mate relatedness in a natural population of the common vole // Journal of Zoology. Vol.280. P.195–201.
  • Boyce C.C.K. & Boyce J.L. 1988a. Population biology of Microtus arvalis. II Natal and breeding dispersal of females // Journal of Animal Ecology. Vol.57. P.723–736.
  • Boyce C.C.K. & Boyce J.L. 1988b. Population biology of Microtus arvalis. III. Regulation of numbers and breeding dispersion of females // Journal of Animal Ecology. Vol.57. P.737–754.
  • Buchan J.C., Alberts S.C., Silk J.B. & Altmann J. 2003. True paternal care in a multi-male primate society // Nature. Vol.425. P.179–181.
  • Conroy C.J. & Cook J.A. 2000. Molecular systematics of a Holarctic rodent (Microtus: Muridae) // Journal of Mammalogy. Vol.81. P.344–359.
  • Dewsbury. 1985. Paternal behavior in rodents // American Zoologist. Vol.25. P.841–52.
  • Elwood R.V. 1985. Inhibition of infanticide and onset of paternal care in male mice (Mus musculus) // Journal of Comparative Psychology. Vol.99. P.457–467.
  • Evsikov V.I., Kokenova G.T., Zadubrovskii P.A., Potapova O.F. & Potapov M.A. 2006. Monogamy as one of the ways of realization of the adaptive potential in mammals as exemplified by the steppe lemming Lagurus lagurus Pallas // Doklady Biological Sciences. T.411. P.501–503.
  • Fauske J., Andreassen H.P. & Ims R.A. 1997. Spatial organization in a small population of the root vole Microtus oeconomus in a linear habitat // Acta Theriologica. Vol.42. P.79–90.
  • Fietz J. & Dausmann K.H. 2003. Cost and potential benefits of parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius) // Folia Primatologica. Vol.74. No.5–6. P.246–268.
  • FitzGerald R.W. & Madison D.M. 1983. Social organization of a free-ranging population of pine voles, Microtus pinetorum // Behavioral Ecology and Sociobiology. Vol.13. P.183–187.
  • Gaines M.S. & Johnson M.L. 1982. Home range size and population dynamics in the prairie vole, Microtus ochrogaster // Oikos. Vol.39. P.63–70.
  • Gajda A.M. & Brooks R.J. 1993. Paternal care in collared lemmings (Dicrostonyx richardsoni): artifact or adaptation? // Arctic. Vol.46. P.312–315.
  • Galewski T., Tilak M., Sanchez S., Chevret P., Paradis E. & Douzery E. 2006. The evolutionary radiation of Arvicolinae rodents (voles and lemmings): relative contribution of nuclear and mitochondrial DNA phylogenies // BMC Evolutionary Biology. 6: 80.
  • Gaulin S.J.C & FitzGerald R.W. 1988. Home range size as a predictor of mating systems in Microtus // Journal of Mammalogy. Vol.69. P.311–319.
  • Gliwicz J. 1997. Space use in the root vole: basic patterns and variability // Ecography. Vol.20. P.383–389.
  • Gromov V.S. 2009. Parental care in captive red-backed vole (Clethrionomys rutilus) // Contemporary Problems of Ecology. Vol.16. No.3. P.467–473.
  • Gromov V.S. 2010. Interactions in family pairs and parental care in captive steppe lemming (Lagurus lagurus) // Contemporary Problems of Ecology. Vol. 3. P.133–139.
  • Gromov V.S. 2011. Pair-bonding and parental care in cricetid rodents: a comparative study // Acta Theriologica. Vol.56. P.23–33.
  • Gromov V.S. 2013. [Parental care, in rodents: physiological, behavioral and evolutionary aspects]. Moscow: KMK Scientific Press. 584 p. [in Russian].
  • Gromov V.S. & Osadchuk L.V. 2013. Parental care and testosterone in males of the bank vole (Myodes glareolus): sensitization and androgenic stimulation of paternal behavior // Biological Bulletin. T.40. No.1. P.114–118.
  • Hartung T.G. & Dewsbury D.A. 1979. Paternal care in six species of muroid rodents // Behavioral and Neural Biology. Vol.26. P.466–478.
  • Hasler J.F. 1975. A review of reproduction and sexual maturation in the microtine rodents // The Biologist. Vol.57. P.52–86.
  • Heske E.J. 1987. Spatial structuring and dispersal in a high density population of the California vole Microtus californicus // Holarctic Ecology. Vol.10. No.2. P.137–148.
  • Ims R.A. 1987. Responses in spatial-organization and behavior to manipulations of the food resource in the vole Clethrionomys rufocanus // Journal of Animal Ecology. Vol.56. P.585–96.
  • Jaarola M., Martнnkovб N., Gьndьz I., Brunhoff C., Zima J., Nadachowski A., Amori G., Bulatova N.S., Chondropoulos B., Fraguedakis-Tsolis S., Gonzбlez-Esteban J., Lуpez-Fuster M.J., Kandaurov A.S., Kefelioglu H., Mathias M.D., Villate I. & Searle J.B. 2004. Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences // Molecular Phylogenetics and Evolution. Vol.33. P.647–663.
  • Jannett F.J., Jr. 1978. The density-dependent formation of extended maternal families of the montane vole, Microtus montanus nanus // Behavioral Ecology and Sociobiology. Vol.3. P.245–263.
  • de Jong T.R., Chauke M., Harris B.N. & Saltzman W. 2009. From here to paternity: neural correlates of the onset of paternal behavior in California mice (Peromyscus californicus) // Hormones and Behavioral. Vol.56. P.220–231.
  • Komers P.E. & Brotherton P.N.M. 1997. Female space use is the best predictor of monogamy in mammals // Proceedings: Biological Sciences. Vol.264. P.1261–1270.
  • Lambin X., Krebs C. & Scott B. 1992. Spacing system of tundra vole (Microtus oeconomus) during the breeding season in Canada’s western Arctic // Canadian Journal of Zoology. Vol.70. P.2068–2072.
  • Libhaber N. & Eilam D. 2004. Parental investment in social voles varies and is relatively independent of litter size // Journal of Mammalogy. Vol.85. P.748–755.
  • Lonstein J.S. & De Vries G.J. 1999. Sex differences in the parental behaviour of adult virgin prairie voles: Independence from gonadal hormones and vasopressin // Journal of Neuroendocrinology. Vol.11. P.441–449.
  • Madison D.M. 1980. Space use and social structure in meadow vole, Microtus pennsylvanicus // Behavioral Ecology and Sociobiology. Vol.7. P.65–71.
  • Malkova M.G., Palchekh N.A., Yakimenko V.V. & Kuzmin I.V. 2004. [The spatiotemporal structure of rodent populations in the steppe zone of Western Siberia] // Ekologiya. Vol.1. P.34–42 [in Russian, with English abstract].
  • McGuire B. 1997. Influence of father and pregnancy on maternal care in red-backed voles // Journal of Mammalogy. Vol.78. No.3. P.839–849.
  • McGuire B. & Bemis W. 2007. Litter size influences maternal but not paternal care in three species of voles, as measured by nest attendance // Journal of Mammalogy. Vol.88. No.6. P.1420–1426.
  • McGuire B. & Getz L.L. 1998. The nature and frequency of social interactions among free-living prairie voles (Microtus ochrogaster) // Behavioral Ecology and Sociobiology. Vol.43. P.271-279.
  • McGuire B. & Novak M. 1984. A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum) // Animal Behaviour. Vol.32. P.1132–1141.
  • McGuire B. & Novak M. 1986. Parental care and its relationship to social organization in the montane vole (Microtus montanus) // Journal of Mammalogy. Vol.67. P.305–11.
  • Meyer M.N., Golenishchev F.N., Radjabli S.I. & Sablina O. V. 1996. [Voles (subgenus Microtus Schrank) of Russia and adjacent territories] // Proceedings of the Zoological Institute RAS. Vol.232. P.1–320 [in Russian].
  • Miller D.H. & Getz L.L. 1969. Life-history notes on Microtus pinetorum in Central Connecticut // Journal of Mammalogy. Vol.50. P.777–784.
  • Myllymaki A. 1977. Intraspecific competition and home range dynamics in the field vole Microtus agrestis // Oikos. Vol.29. P.553–569.
  • Nekipelov N.V. 1935. [Data on the ecology of the rodents from vicinity of Barun-Torey Lake] // Izvestiya Irkutskogo Nauchnogo Issledovatel’skogo Protivochumnogo Instituta Sibiri i Dal’nego Vostoka. T.2. P.64–103 [in Russian].
  • Oliveras D. & Novak M. 1986. A comparison of paternal behaviour in the meadow vole Microtus pennsylvanicus, the pine vole M. pinetorum and the prairie vole M. ochrogaster // Animal Behavior. Vol.34. P.519–526.
  • Ostfeld R.S. 1985. Limiting resources and territoriality in microtine rodents // The American Naturalist. Vol. 126. P.1–15.
  • Ostfeld R.S. 1986. Territoriality and mating system of California voles // Journal of Animal Ecology. Vol.55. P.691–706.
  • Ostfeld R.S. 1990. The ecology of territoriality in small mammals // Trends in Ecology and Evolution Vol.5. P.411–415.
  • Ostfeld R.S., Pugh S.R., Seamon J.O. & Tamarin R.H. 1988. Space use and reproductive success in a population of meadow voles // Journal of Animal Ecology. Vol.57. P.385–394.
  • Parker K.J. & Lee T.M. 2001. Social and environmental factors influence the suppression of pub-directed aggression and development of paternal behavior in captive meadow voles (Microtus pennsylvanicus) // Journal of Comparative Psychology. Vol.115. P.331–336.
  • Pusenius J. & Viitala J. 1995. Familiarity of breeding field vole (Microtus agrestis) females does not affect their space use and demography of the population // Annales Zoologici Fennici. Vol.32. P.217–223.
  • Schradin C. & Pillay N. 2003. Paternal care in the social and diurnal striped mouse (Rhabdomys pumilio): laboratory and field evidence // Journal of Comparative Psychology. Vol.117. P.317–324.
  • Schradin C. & Pillay N. 2005. Intraspecific variation in the spatial and social organization of the African striped mouse // Journal of Mammalogy. Vol.86. P.99107.
  • Shilton C.M. & Brooks R.J. 1989. Paternal care in captive collared lemmings (Dicrostonyx richardsoni) and its effect on development of the offspring // Canadian Journal of Zoology. Vol.67. P.2740–2745.
  • Smorkatcheva A.V. 2003. Parental care in the captive mandarin vole, Lasiopodomys mandarinus // Canadian Journal of Zoology. Vol.81. P.1339–1345.
  • Smorkatcheva A.V. & Bulatova E.V. 2009. [Social structure and spacing in the yellow steppe lemming, Eolagurus luteus, under semi-natural conditions] // Proceedings of the Scientific Conference on Mammalian Behavior and Behavioral Ecology, Moscow. P.42 [in Russian].
  • Smorkatcheva A.V., Bychenkova T.N. & Zavjalov E.L. 2010. Parental responsiveness negatively correlates with fecal testosterone concentration in male mandarin voles (Microtus mandarinus) // Journal of Ethology. Vol.28. P.53–60.
  • Smorkatcheva A.V., Bychenkova T.N. & Kowalskaya Y.M. 2011. [Parental responsiveness in voles: the effect of mating system and phylogeny] // Proceedings of the International Meeting “Theriofauna of Russia and Adjacent Territories” (9 Congress of the Theriological Society of RAS), Moscow. P.449 [in Russian].
  • Solomon N.G. 1993. Comparison of parental behaviour in male and female prairie voles (Microtus ochrogaster) // Canadian Journal of Zoology. Vol.71. P.434–37.
  • Storey A.E. & Joyce T.L. 1995. Pup contact promotes paternal responsiveness in male meadow voles // Animal Behavior. Vol.49. P.1–10.
  • Storey A.E. & Snow D.T. 1987. Male identity and enclosure size affect paternal attendance of meadow voles, Microtus pennsylvanicus // Animal Behavior. Vol.35. P.411–419.
  • Tast J. 1966. The root vole, Microtus oeconomus (Pallas), as an inhabitant of seasonally flooded land // Annales Zoologici Fennici. Vol.3. P.127–171.
  • Terleph T.A., Jean-Baptiste N. & Bamshad M. 2004. Mechanisms and time course for induction of paternal behavior in prairie voles (Microtus ochrogaster) // Journal of Mammalogy. Vol.85. P.1124–1129.
  • Topping M.G. & Millar J.S. 1996. Spatial distribution in the bushy-tailed woodrat (Neotoma cinerea) and its implications for the mating system // Canadian Journal of Zoology. Vol.74. P.565–569.
  • Wolff J.O., Edge W.D. & Bentley R. 1994. Reproductive and behavioral biology of the gray-tailed vole // Journal of Mammalogy. Vol.75. P.873–879.
  • Xia X. & Millar J.S. 1988. Paternal behavior by Peromyscus leucopus in enclosures // Canadian Journal of Zoology. Vol.66. P.1184–87.