Skip to main content
SpringerLink
Log in

Resting metabolic rate, stress, testosterone, and induced immune response in spring- and fall-born males of Campbell’s dwarf hamsters: Maintenance in long-day conditions

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

We have studied morphological and physiological traits of equally aged young males of Campbell’s dwarf hamster (Phodopus campbelli Thomas, 1905) born at the end of summer (fall males) and winter (spring males) in a vivarium with a constant 14-hour day length (LD 14: 10). Animals were removed from parental cages at the age of one month, kept in isolation in the same lighting conditions, and tested at the age of 2 to 3.5 months. Spring males had a higher resting metabolic rate, a higher body mass in the middle of the experiment, bigger testes and seminal vesicles, higher blood testosterone levels, and a stronger T-cell immune response to phytohemagglutinin injected intradermally than fall males. They did not differ significantly from fall males in basal blood cortisol levels or in antibody production in response to the sheep red blood cells (SRBC) antigen challenge, but they showed lower adrenocortical response to a social stressor and to an adrenocorticotropic hormone. A general linear model analysis showed that the blood cortisol level after a 10 min encounter of males in the open arena and the resting metabolic rate were the only factors significantly influencing humoral immune response to SRBC. In the general linear model including the intensity of T-cell immune response or basal testosterone level as dependent variables, birth season was the only factor causing a significant effect.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alexander, J. and Stimson, W.H., Sex hormones and the course of parasitic infection, Parasitol. Today, 1988, vol. 4, pp. 189–193.

    Article  Google Scholar 

  • Amstislavka, T.S., Dynamics of mitotic activity in cover tissues of vole Clethrionomys glareolus from different seasonal groups, Ekologiya, 1970, no. 4, pp. 68–74.

    Google Scholar 

  • Biard, C., Hardy, C., Motreuil, S., and Moreau, J., Dynamics of PHA-induced immune response and plasma carotenoids in birds: should we have a closer look? J. Exp. Biol., 2009, vol. 212, pp. 1336–1343.

    Article  CAS  PubMed  Google Scholar 

  • Bilbo, S.D. and Nelson, R.J., Sex steroid hormones enhance immune function in male and female Siberian hamsters, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2001, vol. 280, pp. 207–213.

    Google Scholar 

  • Biological Rhythmes, Aschoff, J., Ed., New York: Plenum, 1981.

    Google Scholar 

  • Bronson, F.H., Mammalian Reproductive Biology, Chicago, IL: Chicago Univ. Press, 1989.

    Google Scholar 

  • Bronson, F.H. and Perigo, G., Seasonal regulation of reproduction in muroid rodents, Am. Zool., 1987, vol. 27, no. 3, pp. 929–940.

    Google Scholar 

  • Brown, G.M. and Martin, J., Corticosterone, prolactin, and growth hormone responses to handling and new environment in the rat, Psychosom. Med., 1974, vol. 36, pp. 241–247.

    Article  CAS  PubMed  Google Scholar 

  • Buchanan, K.L., Evans, M.R., and Goldsmith, A.R., Testosterone, dominance signaling and immunosupression in the house sparrow, Passer domesticus, Behav. Ecol. Sociobiol., 2003, vol. 55, pp. 50–59.

    Article  Google Scholar 

  • Bujalska, G., Reproduction stabilizing elements in an island population of Clethrionomys glareolus (Schreber, 1889), Acta Theriol., 1970, vol. 15, pp. 381–412.

    Article  Google Scholar 

  • Bujalska, G., Reproduction strategies in population of Microtus arvalis (Pall.) and Apodemus agrarius (Pall.) inhabiting farmland, Pol. Ecol. Stud., 1981, vol. 7, pp. 229–243.

    Google Scholar 

  • Bushuev, A.V., Husby, A., Sternberg, H., and Grinkov, V.G., Quantitative genetics of basal metabolic rate and body mass in free-living pied flycatchers (Ficedula hypoleuca), J. Zool., 2012, vol. 288, pp. 245–251.

    Article  Google Scholar 

  • Bushuev, A.V., Kerimov, A.B., and Ivankina, E.V., Estimation of heritability and repeatability of resting metabolic rate in birds, with free-living pied flycatchers Ficedula hypoleuca (Aves: Passeriformes) as an example, Zh. Obshch. Biol., 2010, vol. 71, no. 5, pp. 402–424.

    CAS  PubMed  Google Scholar 

  • Castro, J.M., Nolan V.Jr., and Ketterson, E.D., Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis), Am. Nat., 2001, vol. 157, pp. 408–420.

    Article  Google Scholar 

  • Chen, J.-F., Zhong, W.-Q., and Wang, D.-H., Metabolism and thermoregulation in Maximowiczi’s voles (Microtus maximowiczii) and Djungarian hamsters (Phodopus campbelli), J. Therm. Biol., 2006, vol. 31, pp. 583–587.

    Article  Google Scholar 

  • Deviche, P. and Cortez, L., Androgen control of immunocompetence in the male house finch, Carpodacus mexicanus Müller, J. Exp. Biol., 2005, vol. 208, pp. 1287–1295.

    Article  CAS  PubMed  Google Scholar 

  • Downs, C.T. and Brown, M., Is respirometry a standardized technique? A review of measurement of avian resting metabolic rates, J. Therm. Biol., 2012, vol. 37, pp. 531–536.

    Article  Google Scholar 

  • Duffy, D.L., Bentley, G.E., Drazen, D.L., and Ball, G.F., Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings, Behav. Ecol., 2000, vol. 11, pp. 654–662.

    Article  Google Scholar 

  • Even, P.C., Mokhtarian, A., and Pel, A., Practical aspects of indirect calorimetry in laboratory animals, Neurosci. Biobehav. Rev., 1994, vol. 18, pp. 435–447.

    Article  CAS  PubMed  Google Scholar 

  • Faivre, B., Préault, M., Salvadori, F., Théry, M., Gaillard, M., and Cézilly, F., Bill color and immunocompetence in the European blackbird, Anim. Behav., 2003, vol. 65, pp. 1125–1131.

    Article  Google Scholar 

  • Feoktistova, N.Yu., Khomyachki roda Phodopus. Sistematika, filogeografiya, ekologiya, fiziologiya, povedenie, khimicheskaya kommunikatsiya (The Hamsters of Genus Phodopus: Systematics, Phylogeny, Ecology, Physiology, Behavior, and Chemical Communication), Moscow: KMK, 2008.

    Google Scholar 

  • Folstadt, I. and Karter, A.J., Parasites, bright males, and the immunocompetence handicap, Am. Nat., 1992, vol. 139, pp. 603–622.

    Article  Google Scholar 

  • Frappell, P.B., Blevin, H.A., and Baudinette, R.V., Understanding respirometry chambers: what goes in must come out, J. Theor. Biol., 1989, vol. 138, pp. 479–494.

    Article  CAS  PubMed  Google Scholar 

  • Goldman, B.D., Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement, J. Biol. Rhythms, 2001, vol. 16, pp. 283–301.

    Article  CAS  PubMed  Google Scholar 

  • Goldman, B.D. and Darrow, J.M., The pineal gland and mammalian photoperiodism, Neiroendocrinology, 1983, vol. 37, pp. 386–396.

    Article  CAS  Google Scholar 

  • Goldman, B.D. and Nelson, R.J., Melatonin and seasonality in mammals, in Melatonin: Biosynthesis, Physiological Effects, and Clinical Applications, Yu, H.S. and Reiter, R.J., Eds., New York: CRC Press, 1993, pp. 225–252.

    Google Scholar 

  • Górecki, A., Kalabukhov-Skvortsov respirometer and resting metabolic rate measurement, in IBP Handbook No. 24: Methods for Ecological Energetics, Grodzinski, W., Klekowski, R.Z., and Duncan, A., Eds., Oxford, UK: Blackwell, 1975, pp. 309–313.

    Google Scholar 

  • Grossman, C.J., Interactions between the gonadal steroids and immune system, Science, 1985, vol. 227, pp. 257–261.

    Article  CAS  PubMed  Google Scholar 

  • Guerrero, J.M. and Reiter, R.J., Melatonin-immune system relationships, Curr. Top. Med. Chem., 2002, vol. 2, pp. 167–179.

    Article  CAS  PubMed  Google Scholar 

  • Hotchkiss, A.K. and Nelson, R.J., Melatonin and immune function: hype or hypothesis, Crit. Rev. Immunol., 2002, vol. 22, pp. 351–371.

    CAS  PubMed  Google Scholar 

  • Kevin, J., McGraw, K.J., and Ardia, D.R., Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test, Am. Nat., 2003, vol. 162, no. 6, pp. 704–712.

    Article  Google Scholar 

  • Lighton, J.R. and Halsey, L.G., Flow-through respirometry applied to chamber systems: pros and cons, hints and tips, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 2011, vol. 158, pp. 265–275.

    Article  CAS  Google Scholar 

  • Lokhmiller, R.P. and Moshkin, M.P., Environmental factors and adaptive significance of immunity lability of small mammals, Sib. Ekol. Zh., 1999, vol. 1, pp. 37–58.

    Google Scholar 

  • Lochmiller, R.L., Vestey, M.R., and McMurry, S.T., Primary immune response of selected small mammal species to heterologous erythrocytes, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 1991, vol. 100, pp. 139–143.

    Article  CAS  Google Scholar 

  • Luft, U.C., Myhre, L.G., and Loeppky, J.A., Validity of Haldane calculation for estimating respiratory gas exchange, J. Appl. Physiol., 1973, vol. 34, pp. 864–865.

    CAS  PubMed  Google Scholar 

  • Majewski, P., Markowska, M., Pawlak, J., Piesiewicz, A., Turkowska, E., and Skwarlo-Sonta, K., Pineal gland and melatonin: impact on the seasonality of immune defense in mammals and birds, Adv. Neuroimmune Biol., 2012, vol. 3, no. 1, pp. 95–108.

    Google Scholar 

  • Male, D., Brostoff, J., Roth, D.B., and Roitt, I.M., Immunology, London: Blackwell, 1998, 5th ed.

    Google Scholar 

  • MartinII, L.B., Han, P., Lewittes, J., Kuhlman, J.R., Klasing, K.C., and Wikelski, M., Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique, Funct. Ecol., 2006, vol. 20, pp. 290–299.

    Article  Google Scholar 

  • Martin, L.B., Weil, Z.M., and Nelson, R.J., Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs, Phil. Trans. R. Soc., 2008, vol. 363, pp. 321–339.

    Article  Google Scholar 

  • Melanson, E.L., Ingebrigtsen, J.P., Bergouignan, A., Ohkawara, K., Kohr, W.M., and Lighton, J.R., A new approach for flow-through respirometry measurements in humans, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2010, vol. 298, pp. 1571–1579.

    Google Scholar 

  • Moore, I.T. and Jessop, T.S., Stress, reproduction, and adrenocortical modulation in amphibians and reptiles, Horm. Behav., 2003, vol. 43, pp. 39–47.

    Article  CAS  PubMed  Google Scholar 

  • Moshkin, M.P., Dobrotvorsky, A.K., Mak, V.V., Panov, V.V., and Dobrotvorskaya, E.A., Variability of immune response to heterologous erythrocytes during population cycles of red (Clethrionomys rutilus) and bank (C. glareolus) voles, Oikos, 1998, vol. 82, pp. 131–138.

    Article  Google Scholar 

  • Moshkin, M.P., Gerlinskaya, L.A., and Evsikov, V.I., The role of immune system in behavioral strategies of reproduction, J. Reprod. Dev., 2000, vol. 46, no. 6, pp. 341–365.

    Article  CAS  Google Scholar 

  • Nelson, R.J. and Demas, G.E., Seasonal changes in immune function, Quart. Rev. Biol., 1996, vol. 71, pp. 511–548.

    Article  CAS  PubMed  Google Scholar 

  • Nelson, R.J., Demas, G.E., and Klein, S.L., Photoperiodic mediation of seasonal breeding and immune function in rodents: a multi-factorial approach, Am. Zool., 1998, vol. 38, no. 1, pp. 226–237.

    Google Scholar 

  • Panin, L.E., Ekologicheskie aspekty adaptatsii (Environmental Aspects of Adaptation), Leningrad: Nauka, 1978.

    Google Scholar 

  • Petrusewicz, K., Bujalska, G., Andrzejewski, R., and Gliwicz, J., Productivity processes in and island population of Clethrionomys glareolus, Ann. Zool. Fenn., 1971, vol. 8, no. 1, pp. 127–132.

    Google Scholar 

  • Pokrovskii, A.V., Growth rate of vole juveniles depending on birth time, Tr. Mosk. O-va. Ispyt. Prir., Otd. Biol., 1967, vol. 25, pp. 85–86.

    Google Scholar 

  • Roberts, M.L., Buchanan, K.L., and Evans, M.R., Testing the immunocompetence hypothesis: a review of the evidence, Anim. Behav., 2004, vol. 68, pp. 227–239.

    Article  Google Scholar 

  • Rogovin, K.A. and Moshkin, M.P., Autoregulation in mammalian populations and stress: an old theme revisited, Zh. Obshch. Biol., 2007, vol. 68, no. 4, pp. 244–267.

    CAS  PubMed  Google Scholar 

  • Saino, N., Canova, L., Fasola, M., and Martinelli, R., Reproduction and population density affect humoral immunity in bank voles under field experimental conditions, Oecologia, 2000, vol. 124, pp. 358–366.

    Article  Google Scholar 

  • Schmidt-Nielsen, K., Animal Physiology: Adaptation and Environment, New York: Cambridge: Cambridge Univ. Press, 1997.

    Google Scholar 

  • Shilov, I.A., Ekologo-fiziologicheskie osnovy populyatsionnykh otnoshenii u zhivotnykh (Ecological and Physiological Principles of the Relations in Animal’s Populations), Moscow: Mosk. Gos. Univ., 1977.

    Google Scholar 

  • Shekarova, O.N., Khrushcheva, A.M., and Rogovin, K.A., Possible noninvasive assessment of the status of Campbell’s dwarf hamster (Phodopus campbelli) according to digital images, Zool. Zh., 2011, vol. 90, no. 1, pp. 67–70.

    Google Scholar 

  • Shvarts, S.S., Ishchenko, V.G., Ovchinnikova, N.A., Olenev, V.G., Pokrovskii, A.V., and Pyastlova, O.A., Heterogenesis and life duration of the rodents, Zh. Obshch. Biol., 1964, vol. 25, no. 6, pp. 417–432.

    CAS  PubMed  Google Scholar 

  • Sinclair, J.A. and Lochmiller, R.L., The winter immunoenhancement hypothesis: associations among immunity, density, and survival in prairie vole (Microtus ochrogaster) populations, Can. J. Zool., 2000, vol. 78, pp. 254–264.

    Article  Google Scholar 

  • Sokolov, V.E. and Orlov, V.N., Opredelitel’ mlekopitayushchikh Mongol’skoi Narodnoi Respubliki (Key to Identification of the Mammals of People’s Republic of Mongolia), Moscow: Nauka, 1980.

    Google Scholar 

  • Tella, J.L., Lemu, J.A., Carrete, M., and Blanco, G., The PHA test reflects acquired T-cell mediated immunocompetence in birds, PLoS One, 2008, vol. 3, p. e3295.

    Article  PubMed Central  PubMed  Google Scholar 

  • Tella, J.L., Scheuerlein, A., and Ricklefs, R.E., Is cell mediated immunity related to the evolution of life history strategies of birds? Proc. R. Soc. Lond. B, 2002, vol. 269, pp. 1059–1066.

    Article  Google Scholar 

  • Tepperman, J. and Tepperman, H., Metabolic and Endocrine Physiology an Introductory Text, Chicago: Year Book Medical Publ., 1987.

    Google Scholar 

  • Vasil’eva, N.Yu. and Parfenova, V.M., Are Campbell’s dwarf hamsters (Phodopus campbelli) hibernating?: experimental approach to this problem, in Teriologicheskie issledovaniya (Theriological Studies), St. Petersburg: Ross. Akad. Nauk, 2003, no. 3, pp. 105–123.

    Google Scholar 

  • Wagner, J.A., Horvath, S.M., Dahms, T.E., and Reed, S., Validation of open-circuit method for the determination of oxygen consumption, J. Appl. Physiol., 1973, vol. 34, pp. 859–863.

    CAS  PubMed  Google Scholar 

  • Wegmann, T.G. and Smithies, O., A simple hemagglutination system requiring small amounts of red cells and antibodies, Transfusion, 1966, vol. 6, no. 1, pp. 67–73.

    Article  Google Scholar 

  • Wiger, R., Demography of a cyclic population of the bank vole Clethrionomys glareolus, Oikos, 1979, vol. 33, pp. 373–385.

    Article  Google Scholar 

  • Zahavi, A., Mate selection: a selection for a handicap, J. Theor. Biol., 1975, vol. 53, pp. 205–214.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, pr. Leninskii 33, Moscow, 119071, Russia

    K. A. Rogovin, A. M. Khruscheva & N. Yu. Vasilieva

  2. Faculty of Biology, Moscow State University, Moscow, 119991, Russia

    A. V. Bushuev

Authors
  1. K. A. Rogovin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. V. Bushuev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. M. Khruscheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. Yu. Vasilieva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. A. Rogovin.

Additional information

Original Russian Text © K.A. Rogovin, A.V. Bushuev, A.M. Khruscheva, N.Yu. Vasilieva, 2013, published in Zhurnal Obshchei Biologii, 2013, Vol. 74, No. 5, pp. 366–378.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rogovin, K.A., Bushuev, A.V., Khruscheva, A.M. et al. Resting metabolic rate, stress, testosterone, and induced immune response in spring- and fall-born males of Campbell’s dwarf hamsters: Maintenance in long-day conditions. Biol Bull Rev 4, 181–191 (2014). https://doi.org/10.1134/S2079086414030062

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086414030062

Keywords

Search

Navigation