Skip to main content
SpringerLink
Log in

Changes to Metabolism and Cell Physiology that Enable Mammalian Hibernation

  • Narrative Student Review
  • Published:
Springer Science Reviews

Abstract

Heterothermy is a widespread, adaptive strategy used by many species of bird and mammal to conserve energy during periods of energetic deficit, the expression of which varies greatly depending on the species and environment. A temporary, reversible reduction in metabolic rate and body temperature (i.e., torpor) is an adaptive response used by many species of birds and mammals to conserve energy during periods of resource scarcity. Long-term employment of torpor (i.e., hibernation) is a seasonally expressed phenotype, the genetic and regulated pathways of which can be found throughout all mammal lineages, including hibernators and nonhibernators alike. In mammals, adaptations that allow for hibernation can be classified as those involved in preparation for hibernation, metabolic reduction, continued cellular function and protection, and arousal. Key physiological changes involve seasonal regulation of metabolic hormones, a shift to largely using endogenous fuel sources (i.e., increased lipolysis), global down regulation of protein transcription by posttranslational modification and microRNA save for the increased production of a small number of protective proteins, shifts in membrane composition, and thermogenesis by brown adipose tissue. There is some evidence of cold acclimations in nonhibernators, such as during fetal development, but responses are limited and cursory, and eventually cellular damage occurs. Therefore, it appears that a complete suite of adaptations to metabolism, vital physiological functions, and thermogenic mechanisms is required for the successful expression of the hibernation phenotype.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ATP:

Adenosine triphosphate

BAT:

Brown adipose tissue

MR:

Metabolic rate

PUFA:

Polyunsaturated fatty acid

T a :

Ambient temperature

T b :

Body temperature

T set :

Hypothalamic body temperature setpoint

WAT:

White adipose tissue

References

  1. Abnous K, Storey KB (2007) Regulation of skeletal muscle creatine kinase from a hibernating mammal. Arch Biochem Biophys 467:10–19

    CAS  PubMed  Google Scholar 

  2. Abnous K, Storey KB (2008) Skeletal muscle hexokinase: regulation in mammalian hibernation. Mol Cell Biol 319:41–50

    CAS  Google Scholar 

  3. Allan SM, Rothwell NJ (2003) Inflammation in central nervous system injury. Philos Trans R Soc Lond B 358:1669–1677

    CAS  Google Scholar 

  4. Aloia RC, Raison JK (1989) Membrane function in mammalian hibernation. Biochemica et Biophysica Acta 988:123–146

    CAS  Google Scholar 

  5. Andrews MT (2004) Genes controlling the metabolic switch in hibernating mammals. Biochem Soc Trans 32:1021–1024

    CAS  PubMed  Google Scholar 

  6. Andrews MT (2007) Advances in the molecular biology of hibernation in mammals. BioEssays 29:431–440

    CAS  PubMed  Google Scholar 

  7. Andrews MT, Squire TL, Bowen CM, Rollins MB (1998) Low-temperature carbon utilization is regulated by novel gene activity in the heart of a hibernating mammal. Proc Natl Acad Sci 95:8392–8397

    PubMed Central  CAS  PubMed  Google Scholar 

  8. Angilletta MJ, Cooper BS, Schuler MS, Boyles JG (2010) The evolution of thermal physiology in endotherms. Front Biosci E2:861–881

    Google Scholar 

  9. Armitage KB, Blumstein DT, Woods BC (2003) Energetics of hibernating yellow-bellied marmots (Marmota flaviventris). Comp Biochem Physiol 134A:101–114

    CAS  Google Scholar 

  10. Baker CJ, Flore AJ, Frazzini VI, Choudhri TF, Zubay GP, Solomon RA (1995) Intraischemic hypothermia decreases the release of glutamate in the cores of permanent focal cerebral infarcts. Neurosurgery 36:994–1001

    CAS  PubMed  Google Scholar 

  11. Barnes BM (1989) Freeze avoidance in a mammal: body temperatures below 0°C in an Arctic hibernator. Science 244:1593–1595

    CAS  PubMed  Google Scholar 

  12. Barnes BM, Kretzmann M, Licht P, Zucker I (1986) The influence of hibernation on testis growth and spermatogenesis in the golden-mantled ground squirrel, Spermophilus lateralis. Biol Reprod 35:1289–1297

    CAS  PubMed  Google Scholar 

  13. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism and function. Cell 116:281–297

    CAS  PubMed  Google Scholar 

  14. Bauman WA (1990) Seasonal changes in pancreatic insulin and glucagon in the little brown bat (Myotis lucifugus). Pancreas 5:342–346

    CAS  PubMed  Google Scholar 

  15. Bintz GL, Mackin WW (1980) The effect of water availability on tissue catabolism during starvation in Richardson’s ground squirrels. Comp Biochem Physiol 65A:181–186

    CAS  Google Scholar 

  16. Bintz GL, Palmer DL, Mackin WW, Blanton FY (1979) Selective tissue catabolism and water balance during starvation in Richardson’s ground squirrels. Comp Biochem Physiol 64A:399–403

    CAS  Google Scholar 

  17. Blake BH (1972) The annual cycle and fat storage in two populations of golden-mantled grounds squirrels. J Mammal 53:157–167

    CAS  PubMed  Google Scholar 

  18. Boersma PD (1986) Body temperature, torpor, and growth in chicks of fork-tailed strom-petrels (Oceanodroma furcata). Physiol Zool 59:10–19

    Google Scholar 

  19. Boonstra R, Mo K, Monks DA (2014) Managing anabolic steroids in pre-hibernating Arctic ground squirrels: obtaining their benefits and avoiding their costs. Biol Lett 10:20140734

    PubMed  Google Scholar 

  20. Born J, Rasch B, Gais S (2006) Sleep to remember. Neuroscientist 12:410–424

    PubMed  Google Scholar 

  21. Boswell T, Woods SC, Kenagy GJ (1994) Seasonal changes in body mass, insulin, and glucocorticoids of free-living golden-mantled ground squirrels. Gen Comp Endocrinol 96:339–346

    CAS  PubMed  Google Scholar 

  22. Bouma HR, Carey HV, Kroese FGM (2010) Hibernation: the immune system at rest? J Leukoc Biol 88:619–624

    CAS  PubMed  Google Scholar 

  23. Bouma HR, Strijkstra AM, Talaei F, Henning RH, Carey HV, Kroese FGM (2012) The hibernating immune system. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world: thermoregulatory and metabolic adaptations. Springer-Verlag, Berlin, pp 259–270

    Google Scholar 

  24. Bramlett HM, Dietrich WD (2004) Pathophysiology of cerebral ischemia and brain trauma: similarities and differences. J Cereb Blood Flow Metab 24:133–150

    PubMed  Google Scholar 

  25. Brauch KM, Dhruv ND, Hanse EA, Andrews MT (2005) Digital transcriptome analysis indicates adaptive mechanisms in the heart of a hibernating mammal. Physiol Genomics 23:227–234

    CAS  PubMed  Google Scholar 

  26. Brigham RM, Ianuzzo CD, Hamilton N, Fenton MB (1990) Histochemical and biochemical plasticity of muscle fibers in the little brown bat (Myotis Iucifugus). J Comp Physiol B 160:183–186

    CAS  PubMed  Google Scholar 

  27. Brigham RM, McKechnie AE, Doucette LI, Geiser F (2012) Heterothermy in caprimulgid birds: a review of inter- and intraspecific variation in free-ranging populations. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world: thermoregulatory and metabolic adaptations. Springer-Verlag, Berlin, pp 175–187

    Google Scholar 

  28. Brooks NE, Myburgh KH, Storey KB (2011) Myostatin levels in skeletal muscle of hibernating ground squirrels. J Exp Biol 214:2522–2527

    PubMed Central  CAS  PubMed  Google Scholar 

  29. Brooks SPJ, Storey KB (1992) Mechanisms of glycolytic control during hibernation in the ground squirrel Spermophilus lateralis. J Comp Physiol B 162:23–28

    CAS  Google Scholar 

  30. Brunet-Rossinni AK (2004) Reduced free-radical production and extreme longevity in the little brown bat (Myotis lucifugus) versus two non-flying mammals. Mech Ageing Dev 125:11–20

    CAS  PubMed  Google Scholar 

  31. Buck CL, Barnes BM (1999) Annual cycle of body composition and hibernation in free-living Arctic ground squirrels. J Mammal 80:430–442

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  33. Burlington RF, Darvish A (1988) Low-temperature performance of isolated working hearts from a hibernator and a nonhibernator. Physiol Zool 61:387–395

    Google Scholar 

  34. Burton RS, Reichman OJ (1999) Does immune challenge affect torpor duration? Funct Ecol 13:232–237

    Google Scholar 

  35. Cammisotto PG, Bendayan M (2007) Leptin secretion by white adipose tissue and gastric mucosa. Histol Histopathol 22:199–210

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  37. Carey HV (1990) Seasonal changes in mucosal structure and function in ground squirrel intestine. Am J Physiol Regul Integr Comp Physiol 259:R385–R392

    CAS  Google Scholar 

  38. Carey HV, Mangino MJ, Southard JH (2001) Changes in gut function during hibernation: implications for bowel transplantation and surgery. Gut 49:459–461

    PubMed Central  CAS  PubMed  Google Scholar 

  39. Carey HV, Martin SL (1996) Preservation of intestinal gene expression during hibernation. Am J Physiol Gastrointest Liver Physiol 271:G804–G813

    CAS  Google Scholar 

  40. Carey HV, Sills NS (1992) Maintenance of intestinal nutrient transport during hibernation. Am J Physiol Regul Integr Comp Physiol 263:R517–R523

    CAS  Google Scholar 

  41. Chan JA, Krichevsky AM, Kosik KS (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65:6029–6033

    CAS  PubMed  Google Scholar 

  42. Chapman D (1975) Phase transitions and fluidity characteristics of lipids and cell membranes. Q Rev Biophys 8:185–235

    CAS  PubMed  Google Scholar 

  43. Chen JF et al (2006) The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38:228–233

    PubMed Central  CAS  PubMed  Google Scholar 

  44. Clemens LE, Heldmaier G (2009) Keep cool: memory is retained during hibernation in Alpine marmots. Physiol Behav 98:78–84

    CAS  PubMed  Google Scholar 

  45. 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 Regul Integr Comp Physiol 281:R951–R959

    CAS  PubMed  Google Scholar 

  46. Cossins AR, Prosser CL (1978) Evolutionary adaptation of membranes to temperature. Proc Natl Acad Sci 75:2040–2043

    PubMed Central  CAS  PubMed  Google Scholar 

  47. Cotton CJ, Harlow HJ (2010) Avoidance of skeletal muscle atrophy in spontaneous and facultative hibernators. Physiol Biochem Zool 83:551–560

    PubMed  Google Scholar 

  48. Cummings DE (2006) Ghrelin and the short- and long-term regulation of appetite and body weight. Physiol Behav 89:71–84

    CAS  PubMed  Google Scholar 

  49. Currie SE, Körtner G, Geiser F (2014) Heart rate as a predictor of metabolic rate in heterothermic bats. J Exp Biol 217:1519–1524

    PubMed  Google Scholar 

  50. Currie SE, Noy K, Geiser F (2015) Passive rewarming from torpor in hibernating bats: minimizing metabolic costs and cardiac demands. Am J Physiol Regul Integr Comp Physiol 308:R34–R41

    CAS  PubMed  Google Scholar 

  51. Czenze ZJ, Park AD, Willis CKR (2013) Staying cold through dinner: cold-climate bats rewarm with conspecifics but not sunset during hibernation. J Comp Physiol B 183:859–866

    PubMed  Google Scholar 

  52. Dausmann KH (2014) Flexible patterns in energy savings: heterothermy in primates. J Zool 292:101–111

    Google Scholar 

  53. Davis WH, Reite OB (1967) Response of bats from temperate regions to changes in ambient temperature. Biol Bull 132:320–328

    CAS  PubMed  Google Scholar 

  54. de Meis L (2002) Ca2+-ATPases (SERCA): energy transduction and heat production in transport. J Membr Biol 188:1–9

    PubMed  Google Scholar 

  55. Deboer T, Tobler I (1994) Sleep EEG after daily torpor in the Djungarian hamster: similarity to the effects of sleep deprivation. Neurosci Lett 166:35–38

    CAS  PubMed  Google Scholar 

  56. Dunbar MB, Tomasi TE (2006) Arousal patterns, metabolic rate, and an energy budget of eastern red bats (Lasiurus borealis) in winter. J Mammal 87:1096–1102

    Google Scholar 

  57. Eddy SF, Morin PJ, Storey KB (2006) Differential expression of selected mitochondrial genes in hibernating little brown bats, Myotis lucifugus. J Exp Zool 305A:620–630

    CAS  Google Scholar 

  58. Eddy SF, Storey KB (2003) Differential expression of Akt, PPARγ, and PGC-1 during hibernation in bats. Biochem Cell Biol 81:269–274

    CAS  PubMed  Google Scholar 

  59. Eddy SF, Storey KB (2007) p38MAPK regulation of transcription factor targets in muscle and heart of the hibernating bat, Myotis lucifugus. Cell Biochem Funct 25:759–765

    CAS  PubMed  Google Scholar 

  60. Ellory JC, Willis JS (1982) Kinetics of the sodium pump in red cells of different temperature sensitivity. J Gen Physiol 79:1115–1130

    CAS  PubMed  Google Scholar 

  61. Else PL, Turner N, Hulbert AJ (2004) The evolution of endothermy: role for membranes and molecular activity. Physiol Biochem Zool 77:950–958

    PubMed  Google Scholar 

  62. Epperson LE, Martin SL (2002) Quantitative assessment of ground squirrel mRNA levels in multiple stages of hibernation. Physiol Genomics 10:93–102

    CAS  PubMed  Google Scholar 

  63. Epperson LE, Rose JC, Carey HV, Martin SL (2010) Seasonal proteomic changes reveal molecular adaptations to preserve and replenish liver proteins during ground squirrel hibernation. Am J Physiol Regul Integr Comp Physiol 298:R329–R340

    PubMed Central  CAS  PubMed  Google Scholar 

  64. Esau C et al (2006) miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 3:87–98

    CAS  PubMed  Google Scholar 

  65. Florant GL, Healy JE (2012) The regulation of food intake in mammalian hibernators: a review. J Comp Physiol B 182:451–467

    CAS  PubMed  Google Scholar 

  66. Florant GL, Lawrence AK, Williams K, Bauman WA (1985) Seasonal changes in pancreatic B-cell function in euthermic yellow-bellied marmots. Am J Physiol Regul Integr Comp Physiol 249:R159–R165

    CAS  Google Scholar 

  67. Florant GL et al (2004) Fat-cell mass, serum leptin and adiponectin changes during weight gain and loss in yellow-bellied marmots (Marmota flaviventris). J Comp Physiol B 174:633–639

    CAS  PubMed  Google Scholar 

  68. Florant GL, Richter MM, Fried SK (2012) The effect of ambient temperature on body mass, torpor, food intake, and leptin levels: implications on the regulation of food intake in mammalian hibernators. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world: thermoregulatory and metabolic adaptations. Springer-Verlag, Berlin, pp 507–517

    Google Scholar 

  69. Frank CJ (1992) The influence of dietary fatty acids on hibernation by golden-mantled ground squirrels (Spermophilus lateralis). Physiol Zool 65:906–920

    CAS  Google Scholar 

  70. Frank CL, Storey KB (1995) The optimal depot fat composition for hibernation by golden-mantled ground squirrels (Spermophilus lateralis). J Comp Physiol B 164:536–542

    CAS  PubMed  Google Scholar 

  71. French AR (1988) The patterns of mammalian hibernation. Am Sci 76:569–575

    Google Scholar 

  72. French AR (2008) Patterns of heterothermy in rodents. In: Lovegrove BG, McKechnie AE (eds) Hypometabolism in animals: torpor, hibernation and cryobiology. 13th International Hibernation Symposium. University of KwaZulu-Natal, Pietermaritzburg, pp 337–352

  73. Frerichs KU et al (1998) Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc Natl Acad Sci 95:14511–14516

    PubMed Central  CAS  PubMed  Google Scholar 

  74. 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

    CAS  PubMed  Google Scholar 

  75. Geiser F (1991) The effect of unsaturated and saturated dietary lipids on the pattern of daily torpor and the fatty acid composition of tissues and membranes of the deer mouse Peromyscus maniculatus. J Comp Physiol B 161:590–597

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  77. Geiser F (2008) Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comp Biochem Physiol 150A:176–180

    CAS  Google Scholar 

  78. Geiser F, Broome LS (1993) The effect of temperature on the pattern of torpor in a marsupial hibernator. J Comp Physiol B 163:133–137

    CAS  PubMed  Google Scholar 

  79. Geiser F, Currie SE, O’Shea KA, Hiebert SM (2014) Torpor and hyporthemia: reversed hysteresis of metabolic rate and body temperature. Am J Physiol Regul Integr Comp Physiol 307:R1324–R1329

    CAS  PubMed  Google Scholar 

  80. Geiser F, Drury RL (2003) Radiant heat affects thermoregulation and energy expenditure during rewarming from torpor. J Comp Physiol B 173:55–60

    CAS  PubMed  Google Scholar 

  81. Geiser F, Kenagy GJ (1987) Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator. Am J Physiol Regul Integr Comp Physiol 252:R897–R901

    CAS  Google Scholar 

  82. Geiser F, Kenagy GJ (1988) Torpor duration in relation to temperature and metabolism in hibernating ground squirrels. Physiol Zool 61:422–449

    Google Scholar 

  83. Geiser F, Kenagy GJ, Wingfield JC (1997) Dietary cholesterol enhances torpor in a rodent hibernator. J Comp Physiol B 167:416–422

    CAS  PubMed  Google Scholar 

  84. Geiser F, Körtner G (2010) Hibernation and daily torpor in Australian mammals. Aust Zool 35:204–215

    Google Scholar 

  85. Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935–966

    Google Scholar 

  86. Girdwood DW, Tatham MH, Hay RT (2004) SUMO and transcriptional regulation. Semin Cell Dev Biol 15:201–210

    CAS  PubMed  Google Scholar 

  87. Giroud S, Frare C, Strijkstra A, Boerema A, Arnold W, Ruf T (2013) Membrane phospholipid fatty acid composition regulates cardiac SERCA activity in a hibernator, the Syrian hamster (Mesocricetus auratus). PLoS ONE 8:e63111

    PubMed Central  CAS  PubMed  Google Scholar 

  88. Hall AC, Wolowyk MW, Wang LCH, Ellory JC (1987) The effects of temperature on Ca2+ transport in red cells from a hibernator (Spermophilus richardsonii). J Therm Biol 12:61–63

    CAS  Google Scholar 

  89. Halsall AL, Boyles JG, Whitaker JO Jr (2012) Body temperature of big brown bats during winter in a building hibernaculum. J Mammal 93:497–503

    Google Scholar 

  90. Hardie DG, Hawley SA, Scott JW (2006) AMP-activated protein kinase—development of the energy sensor concept. J Physiol 574:7–15

    PubMed Central  CAS  PubMed  Google Scholar 

  91. Hardy RN (1979) Temperature and animal life, 2nd edn. Edward Arnold, London

    Google Scholar 

  92. Hayashi K, Kugimiya M, Funatsu M (1968) Heat stability of lysozyme-substrate complex. J Biochem 64:93–97

    CAS  PubMed  Google Scholar 

  93. Hays GC, Webb PI, Speakman JR (1991) Arrhythmic breathing in torpid pipistrelle bats, Pipistrellus pipistrellus. Respir Physiol 85:185–192

    CAS  PubMed  Google Scholar 

  94. Hayward JS, Lisson PA (1992) Evolution of brown fat: its absence in marsupials and monotremes. Can J Zool 70:171–179

    Google Scholar 

  95. Hazel JR (1995) Thermal adaptations in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42

    CAS  PubMed  Google Scholar 

  96. Healy JE, Florant GL (2012) Ghrelin, leptin, and fatty acids in free-living Callospermophilus lateralis (golden-mantled ground squirrels). In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world: thermoregulatory and metabolic adaptations. Springer-Verlag, Berlin, pp 519–529

    Google Scholar 

  97. Healy JE, Bateman JL, Ostrom CE, Florant GL (2011) Peripheral ghrelin stimulates feeding behavior and positive energy balance in a sciurid hibernator. Horm Behav 59:512–519

    PubMed Central  CAS  PubMed  Google Scholar 

  98. Healy JE, Gearhart CN, Bateman JL, Handa RJ, Florant GL (2011) AMPK and ACC change with fasting and physiological condition in euthermic and hibernating golden-mantled ground squirrels (Callospermophilus lateralis). Comp Biochem Physiol A 159:322–331

    Google Scholar 

  99. Healy JE, Ostrom CE, Wilkerson GK, Florant GL (2010) Plasma ghrelin concentrations change with physiological state in a sciurid hibernator (Spermophilus lateralis). Gen Comp Endocrinol 166:372–378

    PubMed Central  CAS  PubMed  Google Scholar 

  100. Heldmaier G, Elvert R (2004) How to enter torpor: thermodynamic and physiological mechanisms of metabolic depression. In: Barnes BM, Carey HV (eds) Life in the cold: evolution, mechanisms, adaptation, and application. Twelfth International Hibernation Symposium. Institute of Arctic Biology, University of Alaska, Fairbanks, pp 185–198

    Google Scholar 

  101. Heller HC (1979) Hibernation: neural aspects. Annu Rev Physiol 41:305–321

    CAS  PubMed  Google Scholar 

  102. Heller HC, Colliver GW, Beard J (1977) Thermoregulation during entrance into hibernation. Pflügers Archiv 369:55–59

    CAS  PubMed  Google Scholar 

  103. Hermanson JW (2009) Cool muscle properties in hibernating and summer Eptesicus fuscus in New York. Bat Res News 50:111

    Google Scholar 

  104. Hillenius WJ, Ruben JA (2004) The evolution of endothermy in terrestrial vertebrates: Who? When? Why? Physiol Biochem Zool 77:1019–1042

    PubMed  Google Scholar 

  105. Hindle AG, Otis JP, Epperson LE, Hornberger TA, Goodman CA, Carey HV, Martin SL (2014) Prioritization of skeletal muscle growth for emergence from hibernation. J Exp Biol. doi:10.1242/jeb.109512

    PubMed  Google Scholar 

  106. Hittle D, Storey KB (2002) The translation state of differentially expressed mRNAs in the hibernating thirteen-lined ground squirrel (Spermophilus tridecemlineatus). Arch Biochem Biophys 401:244–254

    Google Scholar 

  107. Hope PR, Jones G (2013) An entrained circadian cycle of peak activity in a population of hibernating bats. J Mammal 94:497–505

    Google Scholar 

  108. Horman S, Hussain N, Dilworth SM, Storey KB, Rider MH (2005) Evaluation of the role of AMP-activated protein kinase and its downstream targets in mammalian hibernation. Comp Biochem Physiol B 142:374–382

    PubMed  Google Scholar 

  109. Hulbert AJ (2007) Membrane fatty acids as pacemakers of animal metabolism. Lipids 42:811–819

    CAS  PubMed  Google Scholar 

  110. Hulbert AJ, Else PL (2000) Mechanisms underlying the cost of living in animals. Annu Rev Physiol 62:207–235

    CAS  PubMed  Google Scholar 

  111. Hume ID, Beiglböck C, Ruf T, Frey-Roos F, Bruns U, Arnold W (2002) Seasonal changes in morphology and function of the gastrointestinal tract of free-living alpine marmots (Marmota marmota). J Comp Physiol B 172:197–207

    CAS  PubMed  Google Scholar 

  112. Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179

    PubMed  Google Scholar 

  113. Iliff BW, Swoap SJ (2012) Central adenosine receptor signaling is necessary for daily torpor in mice. Am J Physiol Regul Integr Comp Physiol 303:R477–R484

    CAS  PubMed  Google Scholar 

  114. IUPS Thermal Commission (2003) Glossary of terms for thermal physiology. J Therm Biol 28:75–106

    Google Scholar 

  115. Jackman RW, Kandarian SC (2004) The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 287:834–843

    Google Scholar 

  116. Jinka TR, Tøien Ø, Drew KL (2011) Season primes the brain in an Arctic hibernator to facilitate entrance into torpor mediated by adenosine A1 receptors. J Neurosci 31:10752–10758

    PubMed Central  CAS  PubMed  Google Scholar 

  117. Kamezaki F et al (2013) Association of seasonal variation in the prevalence of metabolic syndrome with insulin resistance. Hypertens Res 36:398–402

    PubMed  Google Scholar 

  118. Kelly DA, Storey KB (1995) Glycolysis and energetics in organs of hibernating mice (Zapus hudsonius). Can J Zool 73:202–207

    Google Scholar 

  119. Kenagy GJ (1980) Effects of day length, temperature, and endogenous control on annual rhythms of reproduction and hibernation in chipmunks (Eutamias spp.). J Comp Physiol A 141:369–378

    Google Scholar 

  120. Kitao N, Hashimoto M (2012) Increased thermogenic capacity of brown adipose tissue under low temperature and its contribution to arousal from hibernation in Syrian hamsters. Am J Physiol Regul Integ Comp Physiol 302:R118–R125

    CAS  Google Scholar 

  121. Klaus S, Casteilla L, Bouillaud F, Ricquier D (1991) The uncoupling protein UCP: a membraneous mitochondrial ion carrier exclusively expressed in brown adipose tissue. Int J Biochem 23:791–801

    CAS  PubMed  Google Scholar 

  122. Knight JE, Narus EN, Martin SL, Jacobson A, Barnes BM, Boyer BB (2000) mRNA stability and polysome loss in hibernating Arctic ground squirrels (Spermophilus parryii). Mol Cell Biol 20:6374–6379

    PubMed Central  CAS  PubMed  Google Scholar 

  123. Kola B (2008) Role of AMP-activated Protein Kinase in the control of appetite. J Neuroendocrinol 20:942–951

    PubMed Central  CAS  PubMed  Google Scholar 

  124. Körtner G, Geiser F (2000) The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol Int 17:103–128

    PubMed  Google Scholar 

  125. Krilowicz BL, Glotzbach SF, Heller HC (1988) Neuronal activity during sleep and complete bouts of hibernation. Am J Physiol Regul Integr Comp Physiol 255:R1008–R1019

    CAS  Google Scholar 

  126. Kronfeld-Schor N, Richardson C, Silvia BA, Kunz TH, Widmaier EP (2000) Dissociation of leptin secretion and adiposity during prehibernatory fattening in little brown bats. Am J Physiol Regul Integr Comp Physiol 279:R1277–R1281

    CAS  PubMed  Google Scholar 

  127. Krüger K, Prinzinger R, Schuchmann K-L (1982) Torpor and metabolism in hummingbirds. Comp Biochem Physiol 73A:679–689

    Google Scholar 

  128. Kunz TH, Wrazen JA, Burnett CD (1998) Changes in body mass and fat reserves in pre-hibernating little brown bats (Myotis lucifugus). Ecoscience 5:8–17

    Google Scholar 

  129. Lal A et al (2009) miR-24 inhibits cell proliferation by targeting E2F2, MYC, and other cell-cycle genes via binding to “Seedless” 3’UTR microRNA recognition elements. Mol Cell 35:610–625

    PubMed Central  CAS  PubMed  Google Scholar 

  130. Lee K, Park JY, Yoo W, Gwag T, Lee J-W, Byun M-W, Choi I-H (2008) Overcoming muscle atrophy in a hibernating mammal despite prolonged disuse in dormancy; proteomic and molecular assessment. J Cell Biochem 104:642–656

    CAS  PubMed  Google Scholar 

  131. Lee Y, Miyake S, Wakita H, McMullen DC, Azuma Y, Auh S, Hallenbeck JM (2007) Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells. J Cereb Blood Flow Metab 27:950–962

    PubMed Central  CAS  PubMed  Google Scholar 

  132. Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128

    CAS  PubMed  Google Scholar 

  133. Li Y, Lasar D, Fromme T, Klingenspor M (2014) White, brite, and brown adipocytes: the evolution and function of a heater organ in mammals. Can J Zool 92:615–626

    CAS  Google Scholar 

  134. Liu B, Belke D, Wang LCH (1997) Ca2+ uptake by cardiac sarcoplasmic reticulum at low temperature in rat and ground squirrel. Am J Physiol Regul Integr Comp Physiol 272:R1121–R1127

    CAS  Google Scholar 

  135. Lotter H, Helk E, Bernin H, Jacobs T, Prehn C, Adamski J, González-Roldán N, Holst O, Tannich E (2013) Testosterone increases susceptibility to amebic liver abscess in mice and mediates inhibition of IFNγ secretion in natural killer T cells. PLoS ONE 8:e55694

    PubMed Central  CAS  PubMed  Google Scholar 

  136. Lovegrove BG (2012) A single origin of heterothermy in mammals. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world; thermoregulatory and metabolic adaptations. Springer-Verlag, Berlin, pp 3–11

    Google Scholar 

  137. Lovegrove BG, Lobban KD, Levesque DL (2014) Mammal survival at the Cretaceous-Palaeogene boundary: metabolic homeostasis in prolonged tropical hibernation in tenrecs. Proc R Soc B 281:20141304

    PubMed  Google Scholar 

  138. Lusk G (1924) Animal calorimetry: analysis of the oxidation of mixtures of carbohydrate and fat. J Biol Chem 59:41–42

    CAS  Google Scholar 

  139. Lyman CP (1982) The hibernating state. In: Lyman P, Willis JS, Malan A, Wang LCH (eds) Hibernation and torpor in mammals and birds. Academic Press, New York, pp 54–76

    Google Scholar 

  140. Magariños AM, McEwan BS, Saboureau M, Pevet P (2006) Rapid and reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters. Proc Natl Acad Sci 103:18775–18780

    PubMed Central  PubMed  Google Scholar 

  141. Malan A (2012) The torpor-arousal cycle is controlled by an endogenous clock. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world: thermoregulatory and metabolic adaptations. Springer-Verlag, Berlin, pp 211–218

    Google Scholar 

  142. Malysheva AN, Storey KB, Ziganshin RK, Lopina OD, Rubtsov AM (2001) Characteristics of sarcoplasmic reticulum membrane preparations isolated from skeletal muscles of active and hibernating ground squirrel Spermophilus undulatus. Biochemistry 66:918–925

    CAS  PubMed  Google Scholar 

  143. Marjanovic M, Willis JS (1992) ATP dependence of Na+-K+ pump of cold-sensitive and cold-tolerant mammalian red blood cells. J Physiol 456:575–590

    PubMed Central  CAS  PubMed  Google Scholar 

  144. McNamara MC, Riedesel ML (1973) Memory and hibernation in Citellus lateralis. Science 179:92–94

    CAS  PubMed  Google Scholar 

  145. Mihailovic L, Petrovoc-Minic B, Protic S, Divac J (1968) Effects of hibernation on learning and retention. Nature 218:191–192

    CAS  PubMed  Google Scholar 

  146. Millesi E, Prossinger H, Dittami JP, Fieder M (2001) Hibernation effects on memory in European ground squirrels (Spermophilus citellus). J Biol Rhythms 16:264–271

    CAS  PubMed  Google Scholar 

  147. Minokoshi Y, Shiuchi T, Lee S, Suzuki A, Okamoto S (2008) Role of hypothalamic AMP-kinase in food regulation. Nutrition 24:786–790

    CAS  PubMed  Google Scholar 

  148. Morin PJ, Dubuc A, Storey KB (2008) Differential expression of microRNA species in organs of hibernating ground squirrels: a role in translational suppression during torpor. Biochemica et Biophysica Acta 1779:628–633

    CAS  Google Scholar 

  149. Morrison SF, Nakamura K (2011) Central neural pathways for thermoregulation. Front Biosci 16:74–104

    CAS  Google Scholar 

  150. Morton SR (1978) Torpor and nest-sharing in free-living Sminthopsis crassicaudata (Marsupialia) and Mus musculus (Rodentia). J Mammal 59:569–575

    Google Scholar 

  151. Munro D, Thomas DW (2004) The role of polyunsaturated fatty acids in the expression of torpor by mammals: a review. Zoology 107:29–48

    CAS  PubMed  Google Scholar 

  152. Musacchia XJ, Steffen JM, Fell RD, Dombrowski MJ (1990) Skeletal muscle response to spaceflight, whole body suspension, and recovery in rats. J Appl Physiol 69:2248–2253

    CAS  PubMed  Google Scholar 

  153. Muzzi M, Blasi F, Masi A, Coppi E, Traini C, Felici R, Pittelli M, Cavone L, Pugliese AM, Moroni F, Chiarugi A (2013) Neurological basis of AMP-dependent thermoregulation and its relevance to central and peripheral hyperthermia. J Cereb Blood Flow Metab 33:183–190

    PubMed Central  CAS  PubMed  Google Scholar 

  154. Nedergaard J, Cannon B (1984) Preferential utilization of brown adipose tissue lipids during arousal from hibernation in hamsters. Am J Physiol Regul Integr Comp Physiol 247:R506–R512

    CAS  Google Scholar 

  155. Nelson OL, Jansen HT, Galbreath E, Morgenstern K, Gehring JL, Rigano KS, Lee J, Gong J, Shaywitz AJ, Vella CA, Robbins CT, Corbit KC (2014) Grizzly bears exhibit augmented insulin sensitivity while obese prior to a reversible insulin resistance during hibernation. Cell Metab 20:376–382

    CAS  PubMed  Google Scholar 

  156. Nicol SC, Andersen NA, Mesch U (1992) Metabolic rate and ventilatory pattern in the echidna during hibernation and arousal. In: Augee ML (ed) Platypus and Echidnas. Royal Zoological Society of New South Wales, Sydney, pp 150–159

    Google Scholar 

  157. Norquay KJO, Willis CKR (2014) Hibernation phenology of Myotis lucifugus. J Zool. doi:10.1111/jzo.12155

    Google Scholar 

  158. Oelkrug R, Goetze N, Exner C, Lee Y, Ganjam GK, Kutschke M, Müller S, Stöhr S, Tschöp MH, Crichton PG, Heldmaier G, Jastroch M, Meyer CW (2013) Brown fat in a protoendothermic mammal fuels eutherian evolution. Nat Commun 4:1–8

    Google Scholar 

  159. Offner H, Subramanian S, Parker SM, Afentoulis ME, Vandenbark AA, Hurn PD (2006) Experimental stroke induces massive, rapid activation of the peripheral immune system. J Cereb Blood Flow Metab 26:654–665

    CAS  PubMed  Google Scholar 

  160. Ormseth OA, Nicolson M, Pelleymounter M, Boyer BB (1996) Leptin inhibits prehibernation hyperphagia and reduces body weight in Arctic ground squirrels. Am J Physiol Regul Integr Comp Physiol 40:R1775–R1779

    Google Scholar 

  161. Otis JP, Sahoo D, Drover VA, Yen CE, Carey HV (2011) Cholesterol and lipoprotein dynamics in a hibernating mammal. PLoS ONE 6:e29111

    PubMed Central  CAS  PubMed  Google Scholar 

  162. Pengelley ET, Asmundson SJ, Barnes B, Aloia RC (1976) Relationship of light intensity and photoperiod to circannual rhythmicity in the hibernating ground squirrel, Citellus lateralis. Comp Biochem Physiol A 53:273–277

    CAS  PubMed  Google Scholar 

  163. Popov VI, Bocharova LS, Bragin AG (1992) Repeated changes of dendritic morphology in the hippocampus of ground squirrels in the course of hibernation. Neuroscience 48:45–51

    CAS  PubMed  Google Scholar 

  164. 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

    CAS  PubMed  Google Scholar 

  165. Revel FG et al (2007) The circadian clock stops ticking during deep hibernation in the European hamster. Proc Natl Acad Sci 104:13816–13820

    PubMed Central  CAS  PubMed  Google Scholar 

  166. Reznick RM, Shulman GI (2006) The role of AMP-activated protein kinase in mitochondrial biogenesis. J Physiol 574:33–39

    PubMed Central  CAS  PubMed  Google Scholar 

  167. Riek A, Geiser F (2014) Heterothermy in pouched mammals—a review. J Zool 292:74–85

    Google Scholar 

  168. Riley DA, Ilyina-Kakueva EI, Ellis S, Bain JLW, Slocum GR, Sedlak FR (1990) Skeletal muscle fiber, nerve, and blood vessel breakdown in space-flown rats. FASEB J 4:84–91

    CAS  PubMed  Google Scholar 

  169. Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758

    CAS  PubMed  Google Scholar 

  170. Ross AP, Christian SL, Zhao HW, Drew KL (2006) Persistent tolerance to oxygen and nutrient deprivation and N-methyl-D-aspartate in cultured hippocampal slices from hibernating Arctic ground squirrel. J Cereb Blood Flow Metab 26:1148–1156

    CAS  PubMed  Google Scholar 

  171. Rousseau K et al (2002) Photoperiodic regulation of leptin resistance in the seasonally breeding Siberian hamster (Phodopus sungorus). Endocrinology 143:3083–3095

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  173. Ruby NF (2003) Hibernation: when good clocks go cold. J Biol Rhythms 18:275–286

    PubMed  Google Scholar 

  174. Ruczynski I, Siemers BM (2014) Hibernation does not affect memory retention in bats. Biol Lett 7:153–155

    Google Scholar 

  175. Ruf T, Arnold W (2008) Effects of polyunsaturated fatty acids on hibernation and torpor: a review and hypothesis. Am J Physiol Regul Integr Comp Physiol 294:R1044–R1052

    CAS  PubMed  Google Scholar 

  176. Ruf T, Geiser F (2014) Daily torpor and hibernation in birds and mammals. Biol Rev. doi:10.1111/brv.12137

    PubMed  Google Scholar 

  177. Sheriff MJ, Fridinger RW, Tøien Ø, Barnes BM, Buck CL (2013) Metabolic rate and prehibernation fattening in free-living Arctic ground squirrels. Physiol Biochem Zool 86:515–527

    PubMed  Google Scholar 

  178. Sinensky M (1974) Homeoviscous adaptation—a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci 71:522–525

    PubMed Central  CAS  PubMed  Google Scholar 

  179. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731

    CAS  PubMed  Google Scholar 

  180. Srere HK, Belke D, Wang LCH, Martin SL (1995) α2-macroglobulin gene expression is independent of acute phase response during hibernation in ground squirrels. Am J Physiol Regul Integr Comp Physiol 268:R1507–R1512

    CAS  Google Scholar 

  181. Srere HK, Wang LCH, Martin SL (1992) Central role for differential gene expression in mammalian hibernation. Proc Natl Acad Sci 89:7119–7123

    PubMed Central  CAS  PubMed  Google Scholar 

  182. Stawski C, Willis CKR, Geiser F (2014) The importance of temporal heterothermy in bats. J Zool 292:86–100

    Google Scholar 

  183. Stephens TW, Caro JF (1998) To be lean or not to be lean: is leptin the answer? Exp Clin Endocrinol Diabetes 106:1–15

    CAS  PubMed  Google Scholar 

  184. Storey KB (2010) Out cold: biochemical regulation of mammalian hiberntion—a mini-review. Gerontology 56:220–230

    PubMed  Google Scholar 

  185. Storey KB, Storey JM (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev Camb Philos Soc 79:207–233

    PubMed  Google Scholar 

  186. Strijkstra A, Koopmans T, Bouma HR, de Boer SF, Hut RA, Boerema AS (2012) On the dissimilarity of 5’-AMP induced hypothermia and torpor in mice. In: Ruf T, Bieber C, Arnold W, Millesi E (eds) Living in a seasonal world: thermoregulatory and metabolic adaptations. Springer-Verlag, Berlin, pp 351–362

    Google Scholar 

  187. Swoap SJ, Rathvon M, Gutilla M (2007) AMP does not induce torpor. Am J Physiol Regul Integr Comp Physiol 293:R468–R473

    CAS  PubMed  Google Scholar 

  188. Tähti H (1978) Seasonal differences in O2 consumption and respiratory quotient in a hibernator (Erinaceus europaeus L.). Ann Zool Fenn 15:69–75

    Google Scholar 

  189. Terada T, Nakanuma Y (1995) Expression of pancreatic enzymes (a-amylase, trypsinogen, and lipase) during human liver development and maturation. Gastroenterology 108:1236–1245

    CAS  PubMed  Google Scholar 

  190. Thomas DW (1995) Hibernating bats are sensitive to nontactile human disturbance. J Mammal 76:940–946

    Google Scholar 

  191. Tomanek RJ, Lund DD (1974) Degeneration of different types of skeletal muscle fibres; II. Immobilization. J Anat 118:531–541

    PubMed Central  CAS  PubMed  Google Scholar 

  192. Tschöp M, Smiley DL, Heiman ML (2000) Ghrelin induces adiposity in rodents. Nature 407:908–913

    PubMed  Google Scholar 

  193. Tupone D, Madden CJ, Morrison SF (2013) Central activation of the A1 adenosine receptor (A1AR) induces a hypothermic, torpor-like state in the rat. J Neurosci 33:14512–14525

    PubMed Central  CAS  PubMed  Google Scholar 

  194. Tyml K, Mathieu-Costello O (2001) Structural and functional changes in the microvasculature of disused skeletal muscle. Front Biosci 6:D45–D52

    CAS  PubMed  Google Scholar 

  195. van Breukelen F, Martin SL (2002) Reversible depression of transcription during hibernation. J Comp Physiol B 172:355–361

    PubMed  Google Scholar 

  196. Walker JM, Glotzbach SF, Berger RJ, Heller HC (1977) Sleep and hibernation in ground squirrels (Citellus spp): electrophysiological observations. Am J Physiol Regul Integr Comp Physiol 233:R213–R221

    CAS  Google Scholar 

  197. Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM (1992) Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the “phosphocreatine circuit” for cellular energy homeostasis. Biochem J 281:21–40

    PubMed Central  CAS  PubMed  Google Scholar 

  198. Wang LCH, Wolowyk M (1988) Torpor in mammals and birds. Can J Zool 66:133–137

    CAS  Google Scholar 

  199. Wang LCH, Cao HM, Zhou ZQ (1997) Temperature dependence of the myocardial excitability of ground squirrel and rat. J Therm Biol 22:195–199

    Google Scholar 

  200. Wang LCH, Lakatta EG, Cheng H, Zhou ZQ (2002) Adaptive mechanisms of intracellular calcium homeostasis in mammalian hibernators. J Exp Biol 205:2957–2962

    CAS  PubMed  Google Scholar 

  201. Williams CT, Barnes BM, Kenagy GJ, Buck CL (2014) Phenology of hibernation and reproduction in ground squirrels: integration of environmental cues with endogenous programming. J Zool 292:112–124

    Google Scholar 

  202. Willis CKR, Brigham RM, Geiser F (2006) Deep, prolonged torpor by pregnant, free-ranging bats. Naturwissenschaften 93:80–83

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  204. Wingfield JC, Marler P (1988) Endocrine basis of communication in reproduction and aggression. In: Knobil E, Neill J (eds) The physiology of reproduction. Raven Press, New York, pp 1647–1677

    Google Scholar 

  205. Wolowyk MW (1997) Smooth muscle contractility and calcium channel density in hibernating and nonhibernating animals. Can J Physiol Pharmacol 68:68–70

    Google Scholar 

  206. Woods CP, Brigham RM (2004) The avian enigma: “hibernation” by common poorwills (Phalaenoptilus nuttallii). In: Barnes BM, Carey HV (eds) Life in the cold: evolution, mechanisms, adaptation and application. 12th International Hibernation Symposium. Institute of Arctic Biology, University of Alaska, Fairbanks, pp 129–138

  207. Woods SC, Decke E, Vasselli JR (1974) Metabolic hormones and regulation of body weight. Psychol Rev 81:26–43

    CAS  PubMed  Google Scholar 

  208. Woods SC, Porte D Jr (1978) The central nervous system, pancreatic hormones, feeding and obesity. Adv Metab Disorder 9:283–312

    CAS  Google Scholar 

  209. Wren AM et al (2001) Ghrelin causes hyperphagia and obesity in rats. Diabetes 50:2540–2547

    CAS  PubMed  Google Scholar 

  210. Yacoe ME (1983) Maintenance of the pectoralis muscle during hibernation in the big brown bat, Eptesicus fuscus. J Comp Physiol 152B:97–104

    Google Scholar 

  211. Yenari M, Kitagawa K, Lyden P, Perez-Pinzon M (2008) Metabolic downregulation: a key to successful neuroprotection? Stroke 39:2910–2917

    PubMed Central  CAS  PubMed  Google Scholar 

  212. Zhang J, Kaasik K, Blackburn MR, Lee CC (2006) Constant darkness is a circadian metabolic signal in mammals. Nature 439:340–343

    CAS  PubMed  Google Scholar 

  213. Zhao HW, Ross AP, Christian SL, Buchholz JN, Drew KL (2006) Decreased NR1 phosphorylation and decreased NMDAR function in hibernating Arctic ground squirrels. J Neurosci Res 84:291–298

    PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of Regina, 3737 Wascana Parkway, Regina, SK, S4S 0A2, Canada

    Brandon J. Klug & R. Mark Brigham

Authors
  1. Brandon J. Klug
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Mark Brigham
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brandon J. Klug.

Additional information

Endorsed by R. Mark Brigham.

Glossary

Daily torpor

Short-term employment of torpor characterized by bouts typically lasting less than 24 h with body temperature (T b) often remaining some degrees above ambient temperature (T a).

Endothermy

Regulation of T b using a high rate of metabolism to produce endogenous heat.

Euthermy

Maintenance of T b at a relatively high temperature conducive to normal biological function.

Heterothermy

The diel or seasonal pattern of temperature regulation where T b varies outside the normal euthermic range

Hibernation

Extended employment of torpor characterized by bouts typically lasting days to weeks with T b dropping to near T a. Obligate hibernation lasts for months during predictable periods of energy imbalance (the “hibernation season”) and consists of multiple bouts interspersed with regular arousals. Conversely, facultative hibernation typically occurs during ephemeral energy crises outside of any predictable season

Hypothermia

An uncontrolled state of reduced T b (i.e., heat loss exceeds capacity for heat production)

Torpor

A temporary and controlled reduction in metabolic rate (MR) and body temperature (T b) followed by a return to euthermy using an endogenous source of heat. Torpor is often employed as an adaptive response to conserve energy during periods of resource scarcity

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Klug, B.J., Brigham, R.M. Changes to Metabolism and Cell Physiology that Enable Mammalian Hibernation. Springer Science Reviews 3, 39–56 (2015). https://doi.org/10.1007/s40362-015-0030-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40362-015-0030-x

Keywords

Search

Navigation