Energetics of arousal episodes in hibernating arctic ground squirrels

Abstract

Arctic ground squirrels overwintering in northern Alaska experience average soil temperature of −10°C. To examine energetic costs of arousing from hibernation under arctic compared to temperate conditions, captive ground squirrels were maintained in ambient temperatures (T a) of 2, −5 and −12°C. Rates of oxygen consumption and carbon dioxide production were used to estimate metabolic rate and fuel use during the three phases of arousal episodes: rewarming, euthermia, and recooling. Respiratory quotient comparisons suggest exclusive use of lipid during rewarming and mixed fuel use during euthermia. Animals rewarming from torpor at T a −12°C took longer, consumed more oxygen, and attained higher peak rates of oxygen consumption when compared to 2°C. T a had no significant effect on cost or duration of the euthermic phase. Animals recooled faster at −12°C than at 2°C, but total oxygen consumption was not different. T a had no significant effect on the total cost of arousal episodes when all three phases are included. Arousal episodes account for 86% of estimated costs of a complete hibernation cycle including torpor when at 2°C and only 23% at −12°C. Thus, due to the higher costs of steady-state metabolism during torpor, proportional metabolic costs of arousal episodes at T a characteristic of the Arctic are diminished compared to relative costs of arousals in more temperate conditions.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

Abbreviations

T a :

Ambient temperature

T b :

Body temperature

MR:

Metabolic rate

BMR:

Basal metabolic rate

RQ:

Respiratory quotient

References

  1. Arnold W, Heldmaier G, Ortmann S, Pohl H, Ruf T, Steinlechner S (1991) Ambient temperatures in hibernacula and their energetic consequences for alpine marmots (Mamota marmota). J Therm Biol 16:223–226

    Article  Google Scholar 

  2. Barnes BM (1989) Freeze avoidance in a mammal: body temperatures below 0°C in an arctic hibernator. Science 244:1521–1616

    Article  Google Scholar 

  3. Barnes BM (1996) Relationships between hibernation and reproduction in male ground squirrels. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold: 10th international hibernation symposium. University of New England Press, Armidale, pp 71–80

    Google Scholar 

  4. Barnes BM, Ritter D (1993) Patterns of body temperature change in hibernating arctic ground squirrels. In: Carey C, Florant GL, Wunder BA, Horwitz B (eds) Life in the cold: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, pp 119–130

    Google Scholar 

  5. Barnes BM, Omtzigt C, Daan S (1993) Hibernators periodically arouse in order to sleep. In: Carey C, Florant GL, Wunder BA, Horwitz B (eds) Life in the cold: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, pp 555–558

    Google Scholar 

  6. Buck CL, Barnes BM (1999) Temperatures of hibernacula and changes in body composition of arctic ground squirrels over winter. J Mammal 80:1264–1276

    Article  Google Scholar 

  7. Buck CL, Barnes BM (2000) Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. Am J Physiol 279:R255–R262

    CAS  Google Scholar 

  8. Buck CL, Breton A, Tøien Ø, Barnes BM (2008) Overwinter body temperature patterns of free-living arctic ground squirrels (Spermophilus parryii). In: Lovegrove BG, McKechnie AE (eds) Hypometabolism in animals: torpor, hibernation and cryobiology. University of KwaZulu-Natal, Pietermaritzburg, pp 317–326

    Google Scholar 

  9. Daan S, Barnes BM, Strijkstra AM (1991) Warming up for sleep?—ground squirrels sleep during arousals from hibernation. Neurosci Lett 128:265–268

    PubMed  Article  CAS  Google Scholar 

  10. Erikson H (1956) Observations on the metabolism of arctic ground squirrels (Citellus parryi) at different environmental temperatures. Acta Physiol Scand 36:66–74

    PubMed  Article  CAS  Google Scholar 

  11. Ferron J (1996) How do woodchucks (Marmota monax) cope with harsh winter conditions? J Mammal 77:412–416

    Article  Google Scholar 

  12. Florant GL, Heller HC (1977) CNS regulation of body temperature in euthermic and hibernating marmots (Marmota flaviventris). Am J Physiol 232:R203–R208

    PubMed  CAS  Google Scholar 

  13. Florant GL, Hill V, Ogilvie MD (2000) Circadian rhythms of body temperature in laboratory and field marmots (Marmota flaviventris). In: Heldmaier G, Klingenspor M (eds) Life in the cold: eleventh international hibernation symposium. Springer, Berlin, pp 223–231

    Google Scholar 

  14. Galster W, Morrison P (1970) Cyclic changes in carbohydrate concentrations during hibernation in the arctic ground squirrel. Am J Physiol 218:1228–1232

    PubMed  CAS  Google Scholar 

  15. Galster W, Morrison P (1975) Gluconeogenesis in arctic ground squirrels between periods of hibernation. Am J Physiol 228:325–330

    PubMed  CAS  Google Scholar 

  16. Geiser F (1988) Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? J Comp Physiol B 158:25–37

    PubMed  Article  CAS  Google Scholar 

  17. Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66:239–274

    PubMed  Article  CAS  Google Scholar 

  18. Geiser F, Kenagy GJ (1988) Torpor duration in relation to temperature and metabolism in hibernating ground squirrels. Physiol Zool 61:442–449

    Google Scholar 

  19. Haldane JS (1912) Methods of air analysis. Charles Griffin & Co Ltd., JB Lippincott Co., Philadelphia

    Google Scholar 

  20. Haman F (2006) Shivering in the cold: from mechanisms of fuel selection to survival. J Appl Physiol 100:1702–1708

    PubMed  Article  CAS  Google Scholar 

  21. Hayes JP, Shonkwiler JS (1996) Analyzing mass-independent data. Physiol Zool 69:974–980

    Google Scholar 

  22. Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Respir Physiol Neurobiol 141:317–329

    PubMed  Article  Google Scholar 

  23. Heller HC, Colliver GW (1974) CNS regulation of body temperature during hibernation. Am J Physiol 227:583–589

    PubMed  CAS  Google Scholar 

  24. Isler D, Hill HP, Meier MK (1987) Glucose metabolism in isolated brown adipocytes under beta-adrenergic stimulation. Quantitative contribution of glucose to total thermogenesis. Biochem J 245:789–793

    PubMed  CAS  Google Scholar 

  25. Kauffmann AS, Paul MJ, Zucker I (2004) Increased heat loss affects hibernation in golden-mantled ground squirrels. Am J Physiol Integr Physiol 287:R167–R173

    Google Scholar 

  26. Kenagy GJ, Sharbaugh SM, Nagy KA (1989) Annual cycle of energy and time expenditure in a golden-mantled ground squirrel population. Oecologia 78:269–282

    Article  Google Scholar 

  27. Long RA, Martin TJ, Barnes BM (2005) Body temperature and activity patterns in free-living arctic ground squirrels. J Mammal 86:312–322

    Google Scholar 

  28. Long RA, Hut RA, Barnes BM (2007) Simultaneous collection of body temperature and activity data in burrowing mammals: a new technique. J Wildl Manage 71(4):1375–1379

    Article  Google Scholar 

  29. Lyman CP (1948) The oxygen consumption and temperature regulation of hibernating hamsters. J Exp Zool 109:55–78

    PubMed  Article  CAS  Google Scholar 

  30. Malan A (1993) Temperature regulation, enzyme kinetics, and metabolic depression in mammalian hibernation. In: Carey C, Florant GL, Wunder BA, Horwitz B (eds) Life in the cold: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, pp 241–252

    Google Scholar 

  31. Michener GR (1992) Sexual differences in over-winter torpor pattern of Richardson’s ground squirrels in natural hibernacula. Oecologia 89:397–406

    Google Scholar 

  32. Nestler JR (1990) Relationship between respiratory quotient and metabolic rate during entry to and arousal from daily torpor in deer mice (Peromyscus maniculatus). Physiol Zool 63:406–413

    Google Scholar 

  33. Ortmann S, Heldmaier G (2000) Regulation of body temperature and energy requirements of hibernating Alpine marmonts (Marmota marmota). Am J Physiol Regul Integr Comp Physiol 278:R698–R704

    PubMed  CAS  Google Scholar 

  34. Prendergast BJ, Freeman DA, Zucker I, Nelson RJ (2002) Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. Am J Physiol Regul Integr Comp Physiol 282:R1054–R1062

    PubMed  CAS  Google Scholar 

  35. Scholander PF, Hock R, Walters V, Irving L (1950) Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation and basal metabolic rate. Biol Bull 99:259–271

    PubMed  Article  CAS  Google Scholar 

  36. Snapp BD, Heller HC (1981) Suppression of metabolism during hibernation in ground squirrels (Citellus lateralis). Physiol Zool 54:297–307

    Google Scholar 

  37. Song X, Körtner G, Geiser F (2000) Temperature selection and energy expenditure in the marsupial hibernator Cercartetus nanus. In: Heldmaier G, Klingenspor M (eds) Life in the cold: eleventh international hibernation symposium. Springer, Berlin, pp 119–126

    Google Scholar 

  38. Staples JF, Hochachka PW (1998) The effect of hibernation status and cold-acclimation on hepatocyte gluconeogenesis in the golden-mantled ground squirrel (Spermophilus lateralis). Can J Zool 76:1734–1740

    Article  Google Scholar 

  39. Strijkstra AM (1999) Energy expenditure during hibernation in European ground squirrels (Spermophilus citellus). In: Periodic euthermy during hibernation in the European ground squirrel: causes and consequences. PhD dissertation, University of Groningen, Haren, The Netherlands

  40. Tøien Ø (1992) Data acquisition in thermal physiology: measurements of shivering. J Therm Biol 17:357–366

    Article  Google Scholar 

  41. Tøien Ø, Drew KL, Chao ML, Rice ME (2001) Ascorbate dynamics and oxygen consumption during arousal from hibernation in arctic ground squirrels. Am J Physiol 281:R572–R583

    Google Scholar 

  42. Trachsel L, Edgar DM, Heller HC (1991) Are ground squirrels sleep deprived during hibernation? Am J Physiol Regul Integr Comp Physiol 260:R1123–R1129

    CAS  Google Scholar 

  43. Twente JW, Twente JA (1965) Effects of core temperature upon duration of hibernation of Citellus lateralis. J Appl Physiol 20:411–416

    PubMed  CAS  Google Scholar 

  44. Van Breukelen F, Martin SL (2001) Translational initiation is uncoupled from elongation at 18° C during mammalian hibernation. Am J Physiol Reg Integr Comp Phys 281:R1374–R1379

    Google Scholar 

  45. Wagner JA, Horwath SM, Dahms TE, Reed S (1973) Validation of open-circuit method for the determination of oxygen consumption. J Appl Physiol 34:859–863

    PubMed  CAS  Google Scholar 

  46. Wang LCH (1978) Energetics and field aspects of mammalian torpor: the Richardson’s ground squirrel. In: Wang LCH, Hudson JW (eds) Strategies in the cold. Academic Press, New York, pp 109–145

    Google Scholar 

  47. Willis JS (1982) The mystery of the periodic arousal. In: Lyman CP, Willis JS, Malan A, Wang LCH (eds) Hibernation and torpor in mammals and birds. Academic Press, New York, pp 92–101

    Google Scholar 

  48. Wilson S, Thurlby PL, Arch JR (1987) Substrate supply for thermogenesis induced by the beta-adrenoceptor agonist BRL 26830A. Can J Physiol Pharmacol 65:113–119

    PubMed  CAS  Google Scholar 

  49. Withers PC, Casey TM, Casey KK (1979) Allometry of respiratory and haematological parameters of arctic mammals. J Comp Physiol 64:343–350

    Google Scholar 

  50. Young PJ (1990) Hibernating patterns of free-ranging Columbian ground squirrels. Oecologia 83:504–511

    Article  Google Scholar 

  51. Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice-Hall Inc., Simon and Schuster

    Google Scholar 

Download references

Acknowledgments

This study was supported by grants from the NSF (9819540 and 0732755), the US Army Medical Research (W81XMH-06) and the Institute of Arctic Biology. Animals were maintained according to the Animal Care and Use Committee regulations of the University of Alaska Fairbanks.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Brian M. Barnes.

Additional information

Communicated by H. V. Carey.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Karpovich, S.A., Tøien, Ø., Buck, C.L. et al. Energetics of arousal episodes in hibernating arctic ground squirrels. J Comp Physiol B 179, 691–700 (2009). https://doi.org/10.1007/s00360-009-0350-8

Download citation

Keywords

  • Oxygen consumption
  • Ground squirrel
  • Spermophilus
  • Metabolic rate
  • Arousal
  • Arctic