Contemporary Problems of Ecology

, Volume 11, Issue 2, pp 215–220 | Cite as

Sexual Dimorphism of the Protein Level in Urine of Muridae Rodents: Relation to Population Numbers

  • G. G. Nazarova
  • L. P. Proskurnyak
  • O. F. Potapova


The results of a comparative study conducted on the water vole, steppe lemming, and Campbell hamster, fulfilled by data published on seven other Muridae rodent species, have revealed a positive relation between the extent of sexual dimorphism estimated by the protein level in urine and population numbers typical for each species and the amplitude of its variation. In species with usually low population numbers, the ratio of protein in urine of males to females comprises 0.9; in species with relative stable population numbers, it is 3.4; and, in species with a high amplitude of periodically fluctuating population numbers, it is 8.3.


rodents population numbers chemocommunication urine protein sexual dimorphism 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Avenant, N.L., Small mammal community characteristics as indicators of ecological disturbance in the Willem Pretorius Nature Reserve, Free State, South Africa, S. Afr. J. Wildl. Res., 2000, vol. 30, pp. 26–33.Google Scholar
  2. Berdyugin, K.I., Bol’shakov, V.N., Balakhanov, V.S., Paskhal’nyi, S.P., and Shtro, V.G., Mlekopitayushchie Gornogo Urala (Mammals of Mountain Urals), Yekaterinburg: Ural. Gos. Univ., 2007.Google Scholar
  3. Beynon, R.J., Hurst, J.L., Turton, M.J., Robertson, D.H.L., Armstrong, S.D., Cheetham, S.A., Simpson, D., MacNicoll, A., and Humphries, R.E., Urinary lipocalins in Rodenta: is there a generic model? in Chemical Signals in Vertebrates 11, Hurst, J.L., Beynon, R.J., Roberts, S.C., and Wyatt, T.D., Eds., New York: Springer-Verlag, 2008, pp. 37–49.CrossRefGoogle Scholar
  4. Cain, K.A., Burns, T.A., and Stalling, D.T., Urinary proteins in four rodent species, Comp. Biochem. Physiol. B, 1992, vol. 101, pp. 199–204.CrossRefPubMedGoogle Scholar
  5. Chamero, P., Marton, T.F., Logan, D.W., Flanagan, K., Cruz1 J.R., Saghatelian, A., Cravatt, B.F., and Stowers, L., Identification of protein pheromones that promote aggressive behavior, Nature, 2007, vol. 450, pp. 899–903.CrossRefPubMedGoogle Scholar
  6. Cheetham, S.A., Smith, A.L, Armstrong, S.D., Beynon, R.J., and Hurst, J.L., Limited variation in the major urinary proteins of laboratory mice, Physiol. Behav., 2009, vol. 96, pp. 253–261.CrossRefPubMedGoogle Scholar
  7. Daniszova, K, Janotova, K., Jedelsky, P.L, and Stopka, P., Urinary lipocalins in Mastomys coucha, Folia Zool., 2009, vol. 58, suppl. 1, pp. 56–64.Google Scholar
  8. Drickamer, L.C., Urine marking and social dominance in male house mice, Behav. Process., 2001, vol. 53, pp. 113–120.CrossRefGoogle Scholar
  9. Dundjerski, Z., Outbreak of Arvicola terrestris in rice fields in Yugoslavia, EPPO Bull., 1988, vol. 18, pp. 445–451.CrossRefGoogle Scholar
  10. Dupal, T.A., Distribution, population, and structure of populations of the steppe vole (Lagurus lagurus, Rodentia, Arvicolina) at the area margin, Zool. Zh., 2014, vol. 93, no. 12, pp. 1454–1460.Google Scholar
  11. Evsikov, V.I., Potapov, M.A., and Muzyka, V.Yu., Population ecology of water vole (Arvicola terrestris L.) in Western Siberia. II. Special ethological structure of populations, Sib. Ekol. Zh., 1999, vol. 6, no. 1, pp. 69–77.Google Scholar
  12. Feoktistova, N.Yu., Khomyachki roda Phodopus. Sistematika, filogeniya, povedenie, khimicheskaya kommunikatsiya (Hamsters of Genus Phodopus: Systematics, Phylogeny, Behavior, and Chemical Communication), Moscow: KMK, 2008.Google Scholar
  13. Feoktistova, N.Yu., Gureev, S.V., Gureeva, A.V., and Naidenko, S.V., Pre-copulation chemo-communicative mechanisms of isolation in hamsters of genus Phodopus, Sens. Sist., 2011, vol. 25, no. 1, pp. 86–92.Google Scholar
  14. Flower, D.R., The lipocalin protein family: structure and function, Biochem. J., 1996, vol. 318, pp. 1–14.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gerlinskaya, L.A., Frolova, Yu.A., Kondratyuk, E.Yu., and Moshkin, M.P., Scent-marking costs and reproductive success in male mice, Zh. Obshch. Biol., 2007, vol. 68, no. 4, pp. 294–304.Google Scholar
  16. Granjon, L., Duplantier, J.M., Catalan, J., and Britton-Davidian, J., Systematics of the genus Mastomys (Thomas, 1915) (Rodentia, Muridae): a review, Belg. J. Zool., 1997, vol. 127, pp. 7–18.Google Scholar
  17. Gromov, V.S., Prostranstvenno-etologicheskaya struktura populyatsii gryzunov (Spatio-Ethological Structure of Rodent Populations), Moscow: KMK, 2008.Google Scholar
  18. Hansson, L. and Henttonen, H., Gradients in density variations of small rodents: importance of latitude and snow cover, Oecologia, 1985, vol. 67, pp. 394–402.CrossRefPubMedGoogle Scholar
  19. Harvey, S., Jemiolo, B., and Novotny, M., Pattern of volatile compounds in dominant and subordinate male mouse urine, J. Chem. Ecol., 1989, vol. 15, pp. 2061–2072.CrossRefPubMedGoogle Scholar
  20. Hörnfeldt, B., Long-term decline in numbers of cyclic voles in boreal Sweden: analysis and presentation of hypotheses, Oikos, 2004, vol. 107, pp. 376–392.CrossRefGoogle Scholar
  21. Hurst, J.L., Fang, J., and Barnard, C., The role of substrate odours in maintaining social tolerance between male house mice, Mus musculus domesticus, Anim. Behav., 1993, vol. 45, pp. 997–1006.CrossRefGoogle Scholar
  22. Janotova, K. and Stopka, P., Mechanisms of chemical communication: the role of major urinary proteins, Folia Zool., 2009, vol. 58, suppl. 1, pp. 41–55.Google Scholar
  23. Janotova, K. and Stopka, P., The level of major urinary proteins is socially regulated in wild Mus musculus musculus, J. Chem. Ecol., 2011, vol. 37, pp. 647–656.CrossRefPubMedGoogle Scholar
  24. Jones, R.B. and Nowell, N.W., Aversive and aggressionpromoting properties of urine from dominant and subordinate male mice, Anim. Learn. Behav., 1973, vol. 1, pp. 207–210.CrossRefGoogle Scholar
  25. Knopf, J.L., Gallagher, J.F., and Held, W.A., Differential, multihormonal regulation of the mouse major urinary protein gene family in the liver, Mol. Cell. Biol., 1983, vol. 3, pp. 2232–2240.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kruczek, M. and Marchlewska-Koj, A., Androgen-dependent proteins in the urine of bank voles (Clethrionomys glareolus), J. Reprod. Fert., 1985, vol. 75, pp. 179–185.CrossRefGoogle Scholar
  27. Krystufek, B., Haberl, W., and Baxter, R.M., Rodent assemblage in a habitat mosaic within the valley thicket vegetation of the Eastern Cape Province, South Africa, Afr. J. Ecol., 2008, vol. 46, pp. 80–87.CrossRefGoogle Scholar
  28. Lambin, X., Petty, S.J., and Mackinnon, J.L., Cyclical dynamics in field vole populations and generalist predation, J. Anim. Ecol., 2000, vol. 69, pp. 106–118.CrossRefGoogle Scholar
  29. Litvinov, Y.N., Kovaleva, V.Y., Efimov, V.M., and Galaktionov, Y.K., Cyclicity of the European water vole population as a factor of biodiversity in ecosystems of Western Siberia, Russ. J. Ecol., 2013, vol. 44, no. 5, pp. 422–427.CrossRefGoogle Scholar
  30. Malone, N., Armstrong, S.D., Humphries, R.E., Beynon, R.J., and Hurst, J.L., The signaling of competitive ability by male house mice, Chem. Signals Vertebr., 2005, vol. 10, nos. 1–2, pp. 77–88.Google Scholar
  31. Moorhouse, T.P. and Macdonald, D.W., What limits male range sizes at different population densities? Evidence from three populations of water voles, J. Zool., 2008, vol. 274, pp. 395–402.CrossRefGoogle Scholar
  32. Nazarova, G.G., Anogenital distance as a prognostic indicator of puberty in males of European water vole (Arvicola terrestris), Zool. Zh., 2011, vol. 90, no. 1, pp. 121–122.Google Scholar
  33. Nazarova, G.G. and Proskurnyak, L.P., Protein content in urine of male and female water vole (Arvicola amphibius) at the period of spring growth and sexual maturation, J. Evol. Biochem. Physiol., 2013, vol. 49, no. 3, pp. 360–364.CrossRefGoogle Scholar
  34. Nazarova, G.G., Proskurniak, L.P. and Yuzhik, E.I., The presence of strange males’ odor induces behavioral responses and elevated levels of low molecular weight proteins excreted in the urine of mature water vole males (Arvicola amphibius L.), J. Chem. Ecol., 2016, vol. 42, no. 3, pp. 270–276.CrossRefPubMedGoogle Scholar
  35. Novikov, S.N., Churakov, G.A., Philimonenko, A.A., Ermakova, I.I., Fedorova, E.M., and Burkot, I.A., The pattern of major urinary proteins (MUPS) expression during postnatal ontogenesis of the laboratory mouse depends on genotype and sex, Russ. J. Dev. Biol., 2009, vol. 40, no. 4, pp. 204–211.CrossRefGoogle Scholar
  36. Novotny, M.V., Pheromones, binding proteins and receptor responses in rodents, Biochem. Soc. Trans., 2003, vol. 31, no. 1, pp. 117–122.CrossRefPubMedGoogle Scholar
  37. Novotny, M., Harvey, S., Jemiolo, B., and Alberto, J., Synthetic pheromones that promote inter-male aggression in mice, Proc. Natl. Acad. Sci. U.S.A., 1985, vol. 82, pp. 2059–2061.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Novotny, M., Harvey, S., and Jemiolo, B., Chemistry of male dominance in the house mouse, Mus domesticus, Experientia, 1990, vol. 46, pp. 109–113.CrossRefPubMedGoogle Scholar
  39. Oparin, M.L., Oparina, O.S., Matrosov, A.N., and Kuznetsov, A.A., Dynamics of mammal fauna in the steppes of Volga-Ural interfluve over last century, Povolzhsk. Ekol. Zh., 2010, no. 1, pp. 71–85.Google Scholar
  40. Panteleev, P.A., Terekhina, A.N., and Eliseev, L.N., The water vole, in Itogi mecheniya mlekopitayushchikh (The Results of Labeling of Mammals), Moscow: Nauka, 1980, pp. 248–258.Google Scholar
  41. Plyusnin, Yu.M., Ethological structure of populations of water vole at different dynamics of population size, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Novosibirsk, 1988.Google Scholar
  42. Rogov, V.G., Population dynamics and demographic parameters of population of European water vole (Arvicola terrestris L.) in subtaiga zone of Western Siberia, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Novosibirsk, 1999.Google Scholar
  43. Rozenfeld, F.M. and Denoël, A., Chemical signals involved in spacing behavior of breeding female bank voles (Clethrionomys glareolus Schreber 1780, Microtidae, Rodentia), J. Chem. Ecol., 1994, vol. 20, no. 3, pp. 803–813.CrossRefPubMedGoogle Scholar
  44. Sampsell, B. and Held, W., Variation in the major urinary protein multigene family in wild-derived mice, Genetics, 1985, vol. 109, pp. 549–568.PubMedPubMedCentralGoogle Scholar
  45. Shilov, I.A., Formation and supporting mechanisms of spatial-ethological structure within population, in Struktura populyatsii u mlekopitayushchikh (Population Structure in Mammals), Moscow: Nauka, 1991, pp. 65–86.Google Scholar
  46. Singleton, G. Krebs, C.J., Davis, S., Chambers, L., and Brown, P., Populations in southeastern Australia reproductive changes in fluctuating house mouse, Proc. R. Soc. Lond. B, 2001, vol. 268, pp. 1741–1748.CrossRefGoogle Scholar
  47. Skinner, J. and Smithers, R., The Mammals of the South African Subregion, Pretoria: Univ. of Pretoria, 1990.Google Scholar
  48. Sokolov, V.E., Kozhnyi pokrov mlekopitayushchikh (Skin Cover of Mammals), Moscow: Nauka, 1973.Google Scholar
  49. Thompson, R.N., McMillon, R., Napier, A., and Wekesa, K.S., Pregnancy block by MHC class I peptides is mediated via the production of inositol 1,4,5-trisphosphate in the mouse vomeronasal organ, J. Exp. Biol., 2007, vol. 210, pp. 1406–1412.CrossRefPubMedGoogle Scholar
  50. Vasil’eva, N.Yu., Function of specific skin glands. Functional and evolutionary aspects of marking behavior of rodents by example of the members of subfamily Cricetinae, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow, 1990.Google Scholar
  51. Wolff, J.O., Comparative population ecology of Peromyscus leucopus and Peromyscus maniculatus, Can. J. Zool., 1985, vol. 63, pp. 1548–1555.CrossRefGoogle Scholar
  52. Wolff, P.R. and Powell, A.J., Urine patterns in mice: an analysis of male/female counter-marking, Anim. Behav., 1984, vol. 32, pp. 1185–1191.CrossRefGoogle Scholar
  53. Zagorodnyuk, I.V., Geographical distribution and population size of Terricola subterraneus in the Soviet Union, Zool. Zh., 1992, vol. 71, pp. 86–97.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • G. G. Nazarova
    • 1
  • L. P. Proskurnyak
    • 1
  • O. F. Potapova
    • 1
  1. 1.Institute of Systematics and Ecology of Animals, Siberian BranchRussian Academy of SciencesNovosibirskRussia

Personalised recommendations