Skip to main content
Log in

Seasonal changes in body mass, energy intake and thermogenesis in Maximowiczi’s voles (Microtus maximowiczii) from the Inner Mongolian grassland

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Small mammals inhabiting temperate and arctic regions exhibit annual adaptive adjustments in physiology, anatomy, and behavior. No data on the physiology of Maximowicz’s voles (Microtus maximowiczii) are available at present. Here we examined the seasonal changes in body mass, food intake, thermogenic capacity, serum leptin and thyroid hormone levels in wild-captured individuals from Inner Mongolian grassland, China. We further examined the effects of photoperiod on these parameters. Energy intake, resting metabolic rate, nonshivering thermogenesis (NST), and serum tri-iodothyronine (T3) levels increased while serum leptin and body mass decreased in the cold seasons. Serum T3 levels were positively correlated with NST and uncoupling protein 1 (UCP1) contents in brown adipose tissue, and leptin levels were negatively correlated with energy intake and resting metabolic rate. Furthermore, laboratory data showed these changes could be induced by short photoperiod alone. Taken together, our results indicate that Maximowicz’s voles can increase thermogenic capacity and energy intake to cope with cold stress. Serum leptin seems to be involved in the regulation of energy intake and changes in T3 level may be important for the variations in NST and/or UCP1. Short photoperiod can serve as a seasonal cue for the winter acclimatization of energy balance in free-living Maximowicz’s voles.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abelenda M, Ledesma A, Rial E, Puerta M (2003) Leptin administration to cold-acclimated rats reduces both food intake and brown adipose tissue thermogenesis. J Therm Biol 28:525–530

    Article  CAS  Google Scholar 

  • Ahima RS, Flier JS (2000) Leptin. Annu Rev Physiol 62:413–437

    Article  PubMed  CAS  Google Scholar 

  • Banin D, Haim A, Arad Z (1994) Metabolism and thermoregulation in the Levant vole Microtus guentheri: the role of photoperiodicity. J Therm Biol 19:55–62

    Article  Google Scholar 

  • Bartness TJ, Goldman BD (1989) Mammalian pineal melatonin: a clock for all seasons. Experientia 45:939–945

    Article  PubMed  CAS  Google Scholar 

  • Bartness TJ, Wade GN (1985) Photoperiodic control of seasonal body weight cycles in hamsters. Neurosci Biobehav Rev 9(4):599–612

    Article  PubMed  CAS  Google Scholar 

  • Bartness TJ, Elliott JA, Goldman BD (1989) Control of torpor and body weight patterns by a seasonal timer in Siberian hamsters. Am J Physiol 257:R142–R149

    PubMed  CAS  Google Scholar 

  • Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359

    Article  PubMed  CAS  Google Scholar 

  • Chen JF, Zhong WQ, Wang DH (2006) Metabolism and thermoregulation in Maximowicz’s voles (Microtus maximowiczii) and Djungarian hamsters (Phodopus campbelli). J Therm Biol 31:583–587

    Article  Google Scholar 

  • Commins SP, Watson PM, Frampton IC, Gettys TW (2001) Leptin selectively reduces white adipose tissue in mice via a UCP-1 dependent mechanism in brown adipose tissue. Am J Physiol Endocrinol Metab 280:E372–E377

    PubMed  CAS  Google Scholar 

  • Concannon P, Levac K, Rawson R, Tennant B, Bensadoun A (2001) Seasonal changes in serum leptin, food intake, and body weight in photoentrained woodchucks. Am J Physiol 281:R951–R959

    CAS  Google Scholar 

  • Dark J, Zucker I (1986) Photoperiodic regulation of body mass and fat reserves in the meadow vole. Physiol Behav 38:851–854

    Article  PubMed  CAS  Google Scholar 

  • Dark J, Zucker I, Wade GN (1983) Photoperiodic regulation of body mass, food intake, and reproduction in the meadow vole (Microtus pennsylvanicus). Am J Physiol 245:R334–R338

    PubMed  CAS  Google Scholar 

  • Dehnel A (1949) Studies on the genus Sorex L. Ann Univ Marine Curie-Sklodowska Sect C Biol 4:17–102

    Google Scholar 

  • Drazen DL, Kriegsfeld LG, Schneider JE, Nelson RJ (2000) Leptin, but not immune function, is linked to reproductive responsiveness to photoperiod. Am J Physiol 278:R1401–R1407

    CAS  Google Scholar 

  • Foster DO, Frydman ML (1979) Tissue distribution of cold-induced thermogenesis in conscious warm- or cold-acclimated rats re-evaluated from changes in tissue blood flow. Can J Physiol Pharm 57:257–270

    Article  CAS  Google Scholar 

  • Friedman JM, Halaas JL (1998) Leptin and the regulation of body weight in mammals. Nature 395:763–770

    Article  PubMed  CAS  Google Scholar 

  • Grodzinski W, Wunder BA (1975) Ecological energetics of small mammals. In: Golley FB, Petrusewicz K, Ryszkowski L (eds) Small mammals: their productivity and population dynamics. Cambridge University Press, Cambridge, pp 173–204

    Google Scholar 

  • Haim A (1996) Food and energy intake, non-shivering thermogenesis and daily rhythm of body temperature in the bushy-tailed gerbil (Sekeetamys calurus): The role of photoperiod manipulations. J Therm Biol 21:37–42

    Article  Google Scholar 

  • Haim A, Yedidia I, Haim D, Zisaple N (1994) Photoperiodicity in daily rhythms of body temperature, food and energy intake of the golden spiny mouse (Acomy russatus). Isr J Zool 40:145–150

    Google Scholar 

  • Haim A, Shablay A, Arad Z (1999) The thermoregulatory and metabolic responses to photoperiod manipulations of the Macedonian mouse (Mus macedonicus), a post-fire invader. J Therm Biol 24:279–286

    Article  Google Scholar 

  • Heldmaier G (1971) Zitterfreie warmebidung und korpergrobe saugetieren. Z Vergl Physiol 73:222–248

    Article  Google Scholar 

  • Heldmaier G (1989) Seasonal acclimatization of energy requirements in mammals: functional significance of body weight control hypothermia, torpor and hibernation. In: Wieser W, Gnaiger E (eds) Energy transformations in cells and organisms. Thieme, Stuttgart, pp 130–139

    Google Scholar 

  • Heldmaier G, Lynch GR (1986) Pineal involvement in thermoregulation and acclimatization. Pineal Res Rev 4:97–139

    CAS  Google Scholar 

  • Heldmaier G, Steinlechner S, Rafael J, Vsiansky P (1981) Photoperiod control and effects of melatonin on nonshivering thermogenesis and brown adipose tissue. Science 212:917–919

    Article  PubMed  CAS  Google Scholar 

  • Heldmaier G, Steinlechner S, Rafael J (1982) Nonshivering thermogenesis and cold resistance during seasonal acclimatization in the Djungarian hamster. J Comp Physiol B 149:1–9

    Article  Google Scholar 

  • Jackson DM, Trayhurn P, Speakman JR (2001) Associations between energetics and over-winter survival in the short-tailed field vole Microtus agrestis. J Anim Ecol 70:633–640

    Article  Google Scholar 

  • Jansky L (1973) Non-shivering thermogenesis and its thermoregulatory significance. Biol Rev 48:85–132

    PubMed  CAS  Google Scholar 

  • Jansky L, Haddad G, Pospisilova D, Dvorak P (1986) Effect of external factors on gonadal activity and body mass of male golden hamsters (Mesocricetus auratus). J Comp Physiol B 156:717–725

    Article  PubMed  CAS  Google Scholar 

  • Johnson MS, Onorato DP, Gower BA, Nagy TR (2004) Weight change affects serum leptin and corticosterone in the collared lemming. Gen Comp Endocrinol 136:30–36

    Article  PubMed  CAS  Google Scholar 

  • Kennedy GC (1953) The role of depot fat in the hypothalamic control of food intake in the rat. Proc R Soc Lond B 140:578–592

    Article  PubMed  CAS  Google Scholar 

  • Klingenspor M, Niggemann H, Heldmaier G (2000) Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian hamster Phodopus sungorus. J Comp Physiol B 170:37–43

    Article  PubMed  CAS  Google Scholar 

  • Krauss S, Zhang CY, Lowell BB (2005) The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Biol 6:248–261

    Article  PubMed  CAS  Google Scholar 

  • Kriegsfeld LJ, Nelson RJ (1996) Gonadal and photoperiodic influences on body mass regulation in adult male and female prairie voles. Am J Physiol 270:R1013–R1018

    PubMed  CAS  Google Scholar 

  • Krόl E, Speakman JR (2007) Regulation of body mass and adiposity in the field vole, Microtus agrestis: a model of leptin resistance. J Endocrinol 192(2):271–278

    Article  Google Scholar 

  • Król E, Duncan JS, Redman P, Morgan PJ, Mercer JG, Speakman JR (2006a) Photoperiod regulates leptin sensitivity in field voles, Microtus agrestis. J Comp Physiol B 176:153–163

    Article  PubMed  Google Scholar 

  • Krόl E, Redman P, Thomson PJ, Williams R, Mayer C, Mercer JG, Speakman JR (2006b) Effect of photoperiod on body mass, food intake and body composition in the field vole, Microtus agrestis. J Exp Biol 208:571–584

    Article  Google Scholar 

  • Kronfeld-Schor N, Haim A, Dayan T, Zisapel N, Klingenspr M, Heldmaier G (2000) Seasonal thermogenic acclimation of diurnally and nocturnally active desert spiny mice. Physiol Biochem Zool 73:37–44

    Article  PubMed  CAS  Google Scholar 

  • Kunz TH, Bicer E, Hood WR, Axtell MJ, Harrington WR, Silvia BA, Widmaier EP (1999) Plasma leptin decreases during lactation in insectivorous bats. J Comp Physiol B 169:61–66

    Article  PubMed  CAS  Google Scholar 

  • Li XS, Wang DH (2005a) Regulation of body weight and thermogenesis in seasonally acclimatized Brandt’s voles (Microtus bandti). Horm Behav 48(3):321–328

    Article  PubMed  Google Scholar 

  • Li XS, Wang DH (2005b) Seasonal adjustments in body mass and thermogenesis in Mongolian gerbils (Meriones unguiculatus): the roles of short photoperiod and cold. J Comp Physiol B 175:593–600

    Article  PubMed  CAS  Google Scholar 

  • Li QF, Sun RY, Huang CX, Wang ZK, Liu XT, Hou JJ (2001) Cold adaptive thermogenesis in small mammals from different geographical zones of China. Comp Biochem Physiol A Mol Integr Physiol 129:949–961

    Article  PubMed  CAS  Google Scholar 

  • Liu QS, Wang DH (2007) Effects of diet quality on phenotypic flexibility of organ size and digestive function in Mongolian gerbils (Meriones unguiculatus). J Comp Physiol 177:509–518

    Article  CAS  Google Scholar 

  • Liu H, Wang DH, Wang ZW (2002) Maximum metabolizable energy intake in the Mongolian gerbil (Meriones unguiculatus). J Arid Environ 52:405–411

    Article  Google Scholar 

  • Lovegrove BG (2005) Seasonal thermoregulatory responses in mammals. J Comp Physiol B 175:231–247

    Article  PubMed  Google Scholar 

  • Lowell BB, Spiegelman BM (2000) Towards a molecular understanding of adaptive thermogenesis. Nature 404:652–660

    PubMed  CAS  Google Scholar 

  • Lowry OH, Rosbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin–Phenol reagents. J Biol Chem 193:265

    PubMed  CAS  Google Scholar 

  • Mercer JG, Tups A (2003) Neuropeptides and anticipatory changes in behavior and physiology: seasonal body weight regulation in the Siberian hamster. Eur J Pharmacol 480(1–3):43–50

    Article  PubMed  CAS  Google Scholar 

  • Merritt JF (1986) Winter survival adaptations of the short-tailed shrew (Blarina brevicauda) in an Appalachian montane forest. J Mammal 67:450–464

    Article  Google Scholar 

  • Merritt JF (1995) Seasonal thermogenesis and body changes in body mass of masked shrews, Sorex cinereus. J Mammal 76:1020–1035

    Article  Google Scholar 

  • Merritt JF, Zegerts DA (1991) Seasonal thermogenesis and body mass dynamics of Clethrionomys gapperi. Can J Zool 69:2771–2777

    Article  Google Scholar 

  • Mezhzherin VA (1964) Dehnel’s phenomenon and its possible explanation. Acta Theriol 8:95–114

    Google Scholar 

  • Nagy TR (1993) Effects of photoperiod history and temperature on male collared lemmings, Dicrostonyx groenlandicus. J Mammal 74:990–998

    Article  Google Scholar 

  • Nicholls DG, Locke RM (1984) Thermogenic mechanisms in brown fat. Physiol Rev 64:1–64

    PubMed  CAS  Google Scholar 

  • Powell CS, Blaylock ML, Wang R, Hunter HL, Johanning GL, Nagy TR (2002) Effects of energy expenditure and UCP1 on photoperiod-induced weight gain in collared lemmings. Obes Res 10:541–550

    Article  PubMed  CAS  Google Scholar 

  • Rousseau K, Atcha Z, Loudon ASI (2003) Leptin and seasonal mammals. J Neuroendocrinol 15:409–414

    Article  PubMed  CAS  Google Scholar 

  • Scarpace PJ, Matheny M, Pollock BH, Tümer N (1997) Leptin increases uncoupling protein expression and energy expenditure. Am J Physiol Endocrinol Metab 273(1):226–230

    Google Scholar 

  • Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG (2000) Central nervous system control of food intake. Nature 404:661–671

    PubMed  CAS  Google Scholar 

  • Silva JE (2006) Thermogenic mechanisms and their hormonal regulation. Physiol Rev 86:435–464

    Article  PubMed  CAS  Google Scholar 

  • Speakman JR (1996) Energetics and the evolution of body size in small terrestrial mammals. Symp Zool Soc Lond 69:63–81

    Google Scholar 

  • Tang GB, Cui JG, Wang DH (2009) Role of hypoleptinemia during cold adaptation in Brandt’s voles (Lasiopodomys brandtii). Am J Physiol Regul Integr Comp Physiol 297(5):R1293–R1301

    Article  PubMed  CAS  Google Scholar 

  • Voltura MB, Wunder BA (1998) Effects of ambient temperature, diet quality, and food restriction on body composition dynamics of the prairie vole, Microtus ochrogaster. Physiol Zool 71:321–328

    PubMed  CAS  Google Scholar 

  • Wang DH, Wang ZW (1996) Seasonal variations in thermogenesis and energy requirements of plateau pikas (Ochotona curzoniae) and root voles (Microtus oeconomus). Acta Theriol 41(3):225–236

    Google Scholar 

  • Wang DH, Wang YS, Wang ZW (2000) Metabolism and thermoregulation in the Mongolian gerbil (Meriones unguiculatus). Acta Theriol 45:183–192

    CAS  Google Scholar 

  • Wang JM, Zhang YM, Wang DH (2006a) Seasonal regulation in serum leptin and uncoupling protein 1 content in brown adipose tissue in root voles from the Qinghai-Tibetan plateau. J Comp Physiol B 176:663–671

    Article  PubMed  CAS  Google Scholar 

  • Wang JM, Zhang YM, Wang DH (2006b) Seasonal thermogenesis and body mass regulation in plateau pikas (Ochotona curzoniae). Oecologia 149:373–382

    Article  PubMed  Google Scholar 

  • Wang JM, Zhang YM, Wang DH (2006c) Photoperiodic regulation in energy intake, thermogenesis and body mass in root voles (Microtus oeconomus). Comp Biochem Physiol A 145:546–553

    Article  Google Scholar 

  • Wiesinger H, Heldmaier G, Buchberger A (1989) Effect of photoperiod and acclimation temperature on nonshivering thermogenesis and GDP-binding of brown fat mitochondria in the Djungarian hamster Phodopus s. sungorus. Pflugers Arch 413:667–672

    Article  PubMed  CAS  Google Scholar 

  • Zhang XY, Wang DH (2007) Thermogenesis food intake and serum leptin in cold-exposed lactating Brandt’s voles Lasiopodomys brandtii. J Exp Biol 210:512–521

    Article  PubMed  Google Scholar 

  • Zhang Y, Proenca R, Maffei M, Barone M, Leopoid L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425–432

    Article  PubMed  CAS  Google Scholar 

  • Zhao ZJ, Wang DH (2005) Short photoperiod enhances thermogenic capacity in Brandt’s voles. Physiol Behav 85:143–149

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Many thanks go to Dr. Gregory E. Steinbaugh for help to improve the language of the paper. Thanks to all the members of Animal Physiological Ecology Group of the Institute of Zoology, Chinese Academy of Sciences, for their help with the experiments and helpful discussions. This study was supported by grants from National Science Foundation of China (30625009) and the Chinese Academy of Sciences (KSCX2-EW-N-005) to DHW.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to De-Hua Wang.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, JF., Zhong, WQ. & Wang, DH. Seasonal changes in body mass, energy intake and thermogenesis in Maximowiczi’s voles (Microtus maximowiczii) from the Inner Mongolian grassland. J Comp Physiol B 182, 275–285 (2012). https://doi.org/10.1007/s00360-011-0608-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-011-0608-9

Keywords

Navigation