Interpopulation variability of endocrine and metabolic response to cold stress in northern red-backed vole (Myodes rutilus)

Abstract

The stresses faced by animals in nature are reflected in the adrenal cortex functional activity. It is possible to expect that the basal concentrations of glucocorticoid hormones will be increased in animals inhabiting unfavorable conditions (and correspondingly the value of the adrenocortical reaction to acute stress will be decreased). Since mobilization of the organism resources for the compensation of environmental challenges is the main function of the stress reaction, its weakening should result in a decrease in the reserve capabilities of metabolism. To check this assumption, the basal and maximal metabolic rates, body temperature, and corticosterone concentration in plasma measured before and after acute cooling in a helium–oxygen mixture were compared in northern red-backed voles (Myodes rutilus) from two populations differing in their relative abundance. It was found that, despite higher basal levels of corticosterone and decreased stress reaction values, individuals from the population of the forest park zone of Novosibirsk Science Center with a low relative abundance demonstrated a higher maximal metabolic rate than individuals from the mountain–taiga population with a high abundance. The results demonstrated that habitation in unfavorable conditions leads to elaboration of physiological adaptations that increase resistance to acute stress but increase the risk of the development of the chronic stress, which negatively influences adaptability.

This is a preview of subscription content, log in to check access.

References

  1. Bashenina, N.V., Puti adaptatsii myshevidnykh gryzunov (Adaptation Aspects of Murid Rodents), Moscow: Nauka, 1977.

    Google Scholar 

  2. Bolshakov, V.N., Evdokimov, N.G., Moshkin, M.P., and Pozmogova, V.P., Coat color polymorphism and its relationship with stress-reactivity of the northern mole vole (Ellobius talpinus Pallas), Dokl. Akad. Nauk SSSR, 1989, vol. 308, no. 2, pp. 500–502.

    Google Scholar 

  3. Boonstra, R., Equipped for life: the adaptive role of the stress axis in male mammals, J. Mamm., 2005, vol. 86, no. 2, pp. 236–247.

    Article  Google Scholar 

  4. Ganem, G. and Croset, H., Comparative study of the corticoadrenal response to emotional stress in different kinds of natural populations of the house mouse, Neuroendocrinology, 1990, vol. 52, pp. 1–62.

    Google Scholar 

  5. Kalabukhov, N.I., Metodika eksperimental’nykh issledovanii po ekologii nazemnykh pozvonochnykh (Practical Manual for Analysis of Ecology of Terrestrial Vertebrates), Moscow: Sovetskaya Nauka, 1951.

    Google Scholar 

  6. Kugler, J., Lange, K.W., and Kalveram, K.T., Influence of bleeding order on plasma corticosterone concentration in the mouse, Exp. Clin. Endocrinol., 1988, vol. 91, no. 2, pp. 241–243.

    CAS  Article  PubMed  Google Scholar 

  7. Litvinov, Yu.N., Abramov, S.A., Kovaleva, V.Yu., Krivopalov, A.V., Novikov, E.A., and Chechulin, A.I., Structural-temporal organization of a rodent community in the Teletskaya taiga, Altai Mountains, Russ. J. Ecol., 2007, vol. 38, no. 6, pp. 413–418.

    Article  Google Scholar 

  8. McEwen, B.S. and Wingfield, J.C., The concept of allostasis in biology and biomedicine, Horm. Behav., 2003, vol. 43, no. 1, pp. 2–15.

    Article  PubMed  Google Scholar 

  9. McEwen, B.S. and Wingfield, J.C., What’s in a name? Integrating homeostasis, allostasis and stress, Horm. Behav., 2011, vol. 57, no. 2, pp. 1–16.

    Google Scholar 

  10. McNamara, J.M. and Buchanan, K.L., Stress, resource allocation, and mortality, Behav. Ecol., 2005, vol. 16, no. 6, pp. 1008–1017.

    Google Scholar 

  11. Meerson, F.Z., Adaptatsiya, stress i profilaktika (Adaptation, Stress, and Prophylactics), Moscow: Nauka, 1981.

    Google Scholar 

  12. Moshkin, M.P., Role of stress in individual and population responses of mammals on change of environment temperature, in Problemy termoregulyatsii i temperaturnoi adaptatsii (Thermoregulation and Temperature Adaptation), Novosibirsk: Nauka, 1992, pp. 141–157.

    Google Scholar 

  13. Moshkin, M., Dobrotvorsky, A., Novikov, E., Panov, V., Ilyashenko, V., Onishchenko, S., and Sergeev, V., Population dynamics of the bank vole (Clethrionomys glareolus Schreb.) in West Siberia, Pol. J. Ecol., 2000, no. 48, pp. 107–112.

    Google Scholar 

  14. Moshkin, M.P., Evdokimov, N.G., Miroshnichenko, V.A., Pozmogova, V.P., and Bolshakov, V.N., Variability of corticosteroid function in population of the northern mole vole (Ellobius talpinus), Usp. Sovrem. Biol., 1991, vol. 111, no. 1, pp. 95–100.

    Google Scholar 

  15. Moshkin, M., Gerlinskaya, L., and Evsikov, V., Variability of stress-reactivity in a natural population of water vole, Arvicola terrestris, Pol. Ecol. Stud., 1994, vol. 20, nos. 3–4.

  16. Moshkin, M.P., Novikov, E.A., Kolosova, I.E., Surov, A.V., Telitsina, A.Y., and Osipova, O.A., Adrenocortical and bioenergetic responses to cold in five species of murine rodent, J. Mammal., 2002, vol. 83, no. 2, pp. 458–466.

    Article  Google Scholar 

  17. Novikov, E.A., Frugal strategy as a base of mole-vole (Ellobius talpinus: Rodentia) adaptations to the fossorial way of life, Zh. Obshch. Biol., 2007, vol. 68, no. 4, pp. 268–277.

    CAS  PubMed  Google Scholar 

  18. Novikov, E.A., Kondratyuk, E.Y., and Petrovskii, D.V., Effect of the life history pattern on bioenergetic parameters of northern red-backed voles (Myodes rutilus Pall.) in a mountain taiga population from the south of Western Siberia, Russ. J. Ecol., 2015, vol. 46, no. 5, pp. 476–480.

    Article  Google Scholar 

  19. Novikov, E., Kondratyuk, E., Petrovski, D., Krivopalov, A., and Moshkin, M., Effects of parasites and antigenic challenge on metabolic rates and thermoregulation in northern red-backed voles (Myodes rutilus), Parasitol. Res., 2015, vol. 114, no. 12, pp. 4479–4486.

    Article  PubMed  Google Scholar 

  20. Novikov, E.A., Kondratyuk, E.Y., Petrovskii, D.V., and Polikarpov, I.A., Reallocation of organism resources within the gradient optimum- pessimum of northern red-backed vole (Myodes rutilus), IX S’ezd Teriologicheskogo obshchestva pri Rossiiskoi Akademii Nauk “Teriofauna Rossii i sopredel’nykh territorii” (IX Congr. of the Theriological Society at the Russian Academy of Sciences “Theriofauna of Russia and Adjacent Countries”), Moscow: KMK, 2011.

    Google Scholar 

  21. Novikov, E.A., Panov, V.V., and Moshkin, M.P. Densitydependent regulation in populations of northern redbacked voles (Myodes rutilus) in optimal and suboptimal habitats of southwest Siberia, Biol. Bull. Rev., 2012, vol. 2, no. 5, pp. 431–438.

    Article  Google Scholar 

  22. Panov, V.V., Winter in the life of small mammals in Ob pine forests of northern forest-steppe of Western Siberia, Sib. Ekol. Zh., 2001, vol. 8, no. 6, pp. 777–784.

    Google Scholar 

  23. Panov, V.V., Annual cycle of small mammal population by example of red-backed vole, in Soobshchestva i populyatsii zhivotnykh: ekologicheskii i morfologicheskii analiz (Communities and Populations of Animals: Ecological and Morphological Analysis), Litvinov, Yu.N., Ed., Moscow: KMK, 2010, pp. 125–132.

    Google Scholar 

  24. Ravkin, Yu.S., Bogomolova, I.N., Erdakov, L.N., Panov, V.V., Buidalina, F.R., Dobrotvorskii, A.K., et al., Specific distribution of small mammals of West Siberian Plain, Sib. Ekol. Zh., 1996, vol. 3, nos. 3–4, pp. 307–317.

    Google Scholar 

  25. Rich, E.L. and Romero, L.M., Exposure to chronic stress downregulates corticosterone responses to acute stressors, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2005, vol. 288, no. 6, pp. 1628–1636.

    Google Scholar 

  26. Rosenmann, M. and Morrison, P., Maximum oxygen consumption and heat loss facilitation in small homeotherms by He–O2, Am. J. Physiol., 1974, vol. 226.

  27. Sapolsky, R.M., Romero, L.M., and Munck, A.U., How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions, Endocr. Rev., 2000, vol. 21, pp. 55–89.

    CAS  PubMed  Google Scholar 

  28. Selegei, V.V. and Selegei, T.S., Teletskoe ozero (Teletskoe Lake), Leningrad: Gidrometeoizdat, 1978.

    Google Scholar 

  29. Shilov, I.A., Praktikum po ekologii nazemnykh pozvonochnykh zhivotnykh (Practical Manual on Ecology of Terrestrial Vertebrates), Moscow: Vysshaya Shkola, 1961.

    Google Scholar 

  30. Silverin, B., Reproductive adaptations to breeding in the north, Am. Zool., 1995, vol. 35, no. 3, pp. 191–202.

    CAS  Article  Google Scholar 

  31. Silverin, B., Arvidsson, B., and Wingfield, J., The adrenocortical responses to stress in breeding willow warblers Phylloscopus trochilus in Sweden: effects of latitude and gender, Funct. Ecol., 1997, vol. 11, no. 3, pp. 376–384.

    Article  Google Scholar 

  32. Thorpe, J.B., Rajabi, N., and Decatanzaro, D., Circadian rhythm and response to an acute stressor of urinary corticosterone, testosterone, and creatinine in adult male mice, Horm. Metab. Res., 2012, vol. 44, no. 6, pp. 429–435.

    CAS  PubMed  Google Scholar 

  33. Wang L.C.H. Modulation of maximum thermogenesis by feeding in the white rat, J. Appl. Physiol., 1980, vol. 49, pp. 975–978.

  34. Wingfield, J.C., Comparative endocrinology, environment and global change, Gen. Comp. Endocrinol., 2008, vol. 157, no. 3, pp. 207–216.

    CAS  Article  PubMed  Google Scholar 

  35. Wingfield, J.C., Kelley, J.P., and Angelier, F., What are extreme environmental conditions and how do organisms cope with them, Curr. Zool., 2011, vol. 57, no. 3, pp. 363–374.

    Article  Google Scholar 

  36. Wingfield, J.C., O’Reilly, K.M., and Astheimer, L.B., Modulation of the adrenocortical responses to acute stress in arctic birds: a possible ecological basis, Am. Zool., 1995, vol. 35, no. 3, pp. 285–294.

    CAS  Article  Google Scholar 

  37. Wingfield, J.C. and Romero, L.M., Adrenocortical responses to stress and their modulation in free-living vertebrates, in Comprehensive Physiology. Handbook of Physiology, Section 7: The Endocrine System, New York: Wiley, 2001, pp. 211–236.

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to E. A. Novikov.

Additional information

Original Russian Text © I.A. Polikarpov, E.Yu. Kondratyuk, D.V. Petrovskii, E.A. Novikov, 2016, published in Zhurnal Obshchei Biologii, 2016, Vol. 77, No. 4, pp. 284–292.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Polikarpov, I.A., Kondratyuk, E.Y., Petrovskii, D.V. et al. Interpopulation variability of endocrine and metabolic response to cold stress in northern red-backed vole (Myodes rutilus). Biol Bull Rev 7, 56–63 (2017). https://doi.org/10.1134/S2079086417010030

Download citation