Journal of Comparative Physiology B

, Volume 187, Issue 8, pp 1039–1056 | Cite as

How low can you go? An adaptive energetic framework for interpreting basal metabolic rate variation in endotherms

  • David L. SwansonEmail author
  • Andrew E. McKechnie
  • François Vézina


Adaptive explanations for both high and low body mass-independent basal metabolic rate (BMR) in endotherms are pervasive in evolutionary physiology, but arguments implying a direct adaptive benefit of high BMR are troublesome from an energetic standpoint. Here, we argue that conclusions about the adaptive benefit of BMR need to be interpreted, first and foremost, in terms of energetics, with particular attention to physiological traits on which natural selection is directly acting. We further argue from an energetic perspective that selection should always act to reduce BMR (i.e., maintenance costs) to the lowest level possible under prevailing environmental or ecological demands, so that high BMR per se is not directly adaptive. We emphasize the argument that high BMR arises as a correlated response to direct selection on other physiological traits associated with high ecological or environmental costs, such as daily energy expenditure (DEE) or capacities for activity or thermogenesis. High BMR thus represents elevated maintenance costs required to support energetically demanding lifestyles, including living in harsh environments. BMR is generally low under conditions of relaxed selection on energy demands for high metabolic capacities (e.g., thermoregulation, activity) or conditions promoting energy conservation. Under these conditions, we argue that selection can act directly to reduce BMR. We contend that, as a general rule, BMR should always be as low as environmental or ecological conditions permit, allowing energy to be allocated for other functions. Studies addressing relative reaction norms and response times to fluctuating environmental or ecological demands for BMR, DEE, and metabolic capacities and the fitness consequences of variation in BMR and other metabolic traits are needed to better delineate organismal metabolic responses to environmental or ecological selective forces.


Basal metabolic rate Endotherms Selection Evolutionary physiology Daily energy expenditure Energetics 



We thank three anonymous reviewers for their valuable and constructive comments on a previous version of this manuscript. DLS was supported by IOS-1021218 from the US National Science Foundation.


  1. Aschoff J, Pohl H (1970) Rhythmic variations in energy metabolism. Fed Proc 291:1541–1552Google Scholar
  2. Ashton KG (2002) Patterns of within-species body size variation of birds: strong evidence for Bergmann’s rule. Global Ecol Biogeogr 11:505–523CrossRefGoogle Scholar
  3. Ashton KG, Tracy MC, de Queiroz A (2000) Is Bergmann’s rule valid for mammals? Am Nat 156:391–415Google Scholar
  4. Bacigalupe LD, Nespolo RF, Bustamante DM, Bozinovic F (2004) The quantitative genetics of sustained energy budget in a wild mouse. Evolut Int J Org Evolut 58:421–429CrossRefGoogle Scholar
  5. Bacigalupe LD, Bustamante DM, Bozinovic F, Nespolo RF (2010) Phenotypic integration of morphology and energetic performance under routine capacities: a study in the leaf-eared mouse Phyllotis darwini. J Comp Physiol B 180:293–299PubMedCrossRefGoogle Scholar
  6. Bai M, Wu X, Cai K, Zheng W, Liu J-S (2016) Relationships between interspecific differences in the mass of internal organs, biochemical markers of metabolic activity and the thermogenic properties of three small passerines. Avian Res 7:11.CrossRefGoogle Scholar
  7. Barceló G, Love OP, Vézina F (2017) Uncoupling basal and summit metabolic rates in white-throated sparrows: digestive demand drives maintenance costs but changes in muscle mass are not needed to improve thermogenic capacity. Physiol Biochem Zool 90:153–165PubMedCrossRefGoogle Scholar
  8. Bartholomew GA, Trost CH (1970) Temperature regulation in the speckled mousebird, Colius striatus. Condor 72:141–146CrossRefGoogle Scholar
  9. Benedict FG (1938) Vital energetics: a study in comparative basal metabolism. Carnegie Inst, Washington (Publication 503)Google Scholar
  10. Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206:649–654PubMedCrossRefGoogle Scholar
  11. Bergmann C (1847) Ueber die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Gottinger Studien 3:595–708Google Scholar
  12. Bishop CM, Butler PJ, Atkinson NM (1995) The effect of elevated levels of thyroxine on the aerobic capacity of locomotor muscles of the tufted duck. Aythya fuligula J Comp Physiol B 164:618–621CrossRefGoogle Scholar
  13. Blackburn TM, Hawkins BA (2004) Bergmann’s rule and the mammal fauna of northern North America. Ecography 27:715–724CrossRefGoogle Scholar
  14. Bligh J, Johnson KG (1973) Glossary of terms for thermal physiology. J Appl Physiol 35:941–961PubMedGoogle Scholar
  15. Boily P (2002) Individual variation in metabolic traits of wild nine-banded armadillos (Dasypus novemcinctus), and the aerobic capacity model for the evolution of endothermy. J Exp Biol 205:3207–3214PubMedGoogle Scholar
  16. Boratyński Z, Koteja P (2009) The association between body mass, metabolic rates and survival of bank voles. Funct Ecol 23:330–339CrossRefGoogle Scholar
  17. Boratyński Z, Koskela E, Mappes T, Schroderus E (2013) Quantitative genetics and fitness effects of basal metabolism. Evol Ecol 27:301–314CrossRefGoogle Scholar
  18. Boratyński JS, Jefimow M, Wojciechowski MS (2016) Phenotypic flexibility of energetics in acclimated Siberian hamsters has a narrower scope in winter than in summer. J Comp Physiol B 186:387–402PubMedPubMedCentralCrossRefGoogle Scholar
  19. Bozinovic F, Sabat P (2010) On the intraspecific variability in basal metabolism and the food habits hypothesis in birds. Curr Zool 56:759–766Google Scholar
  20. Bozinovic F, Novoa FF, Veloso C (1990) Seasonal changes in energy expenditure and digestive tract of Abrothrix andinus in the Andes Range. Physiol Zool 63:1216–1231CrossRefGoogle Scholar
  21. Bozinovic F, Rojas JM, Broitman BR, Vásquez RA (2009) Basal metabolism is correlated with habitat productivity among populations of degus (Octodon degus). Comp Biochem Physiol A 152:560–564CrossRefGoogle Scholar
  22. Brinkmann L, Gerken M, Hambly C, Speakman JR, Ried A (2016) Thyroid hormones correlate with field metabolic rate in ponies, Equus ferus caballus. J Exp Biol 219:2559–2566PubMedCrossRefGoogle Scholar
  23. Brzęk P, Bielawska K, Książek A, Konarzewski M (2007) Anatomic and molecular correlates of divergent selection for basal metabolic rate in laboratory mice. Physiol Biochem Zool 80:491–499PubMedCrossRefGoogle Scholar
  24. Buffenstein R, Yahav S (1991) Is the naked mole-rat Heterocephalus glaber an endothermic yet poikilothermic mammal? J Therm Biol 16:227–232CrossRefGoogle Scholar
  25. Burger MF, Denver RJ (2002) Plasma thyroid hormone concentrations in a wintering passerine bird: their relationship to geographic variation, environmental factors, metabolic rate and body fat. Physiol Biochem Zool 75:187–199PubMedCrossRefGoogle Scholar
  26. Burton T, Killen SS, Armstrong JD, Metcalfe NB (2011) What causes intraspecific variation in resting metabolic rate and what are its ecological consequences. Proc Roy Soc B Biol Sci 278:3465–3473CrossRefGoogle Scholar
  27. Careau V (2013) Basal metabolic rate, maximum thermogenic capacity and aerobic scope in rodents: interaction between environmental temperature and torpor use. Biol Lett 9:20121104PubMedPubMedCentralCrossRefGoogle Scholar
  28. Careau V, Garland T Jr (2012) Performance, personality and energetics: correlation, causation, and mechanism. Physiol Biochem Zool 85:543–571PubMedCrossRefGoogle Scholar
  29. Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117:641–653CrossRefGoogle Scholar
  30. Careau V, Thomas D, Pelletier F, Turki L, Landry F, Garant D, Réale D (2011) Genetic correlation between resting metabolic rate and exploratory behaviour in deer mice (Peromyscus maniculatus). J Evol Biol 24:2153–2163PubMedCrossRefGoogle Scholar
  31. Careau V, Bergeron P, Garant D, Réale D, Speakman JR, Humphries MM (2013a) The energetic and survival costs of growth in free-ranging eastern chipmunks. Oecologia 171:11–23PubMedCrossRefGoogle Scholar
  32. Careau V, Réale D, Garant D, Pelletier F, Speakman JR, Humphries MM (2013b) Context-dependent correlation between resting metabolic rate and daily energy expenditure in wild chipmunks. J Exp Biol 216:418–426PubMedCrossRefGoogle Scholar
  33. Careau V, Killen SS, Metcalfe NB (2014) Adding fuel to the “fire of life”: energy budgets across levels of variation in ectotherms and endotherms. In: Martin LB, Ghalambor CK, Woods HA (eds) Integrative organismal biology. Wiley, Hoboken, pp 219–233Google Scholar
  34. Chappell M, Bech C, Buttemer W (1999) The relationship of central and peripheral organ masses to aerobic performance variation in house sparrows. J Exp Biol 202:2269–2279PubMedGoogle Scholar
  35. Clarke A, Rothery P (2008) Scaling of body temperature in mammals and birds. Funct Ecol 22:58–67Google Scholar
  36. Clarke A, Rothery P, Isaac NJB (2010) Scaling of basal metabolic rate with body mass and temperature in mammals. J Anim Ecol 79:610–619PubMedCrossRefGoogle Scholar
  37. Clavijo-Baquet S, Bozinovic F (2012) Testing the fitness consequences of the thermoregulatory and parental care models for the origin of endothermy. PLoS One 7:e37069CrossRefGoogle Scholar
  38. Crompton AW, Taylor CR, Jagger JA (1978) Evolution of homeothermy in mammals. Nature 272:333–336PubMedCrossRefGoogle Scholar
  39. Cruz-Neto AP, Bozinovic F (2004) The relationship between diet quality and basal metabolic rate in endotherms: insights from intraspecific analyses. Physiol Biochem Zool 77:877–889PubMedCrossRefGoogle Scholar
  40. Dawson WR, Marsh RL (1989) Metabolic acclimatization to cold and season in birds. In: Bech C, Reinertsen RE (eds) Physiology of cold adaptation in birds. Plenum Life Sciences, New York, pp. 83–94CrossRefGoogle Scholar
  41. Dawson WR, O’Connor TP (1996) Energetic features of avian thermoregulatory responses. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman & Hall, New York, pp 85–124CrossRefGoogle Scholar
  42. Dittmann MR, Hummel J, Runge U, Galeffi C, Kreuzer M, Clauss M (2014) Characterising an artiodactyl family inhabiting arid habitats by its metabolism: low metabolism and maintenance requirements in camelids. J Arid Env 107:41–48CrossRefGoogle Scholar
  43. Dohm MR, Hayes JP, Garland T Jr (2001) The quantitative genetics of maximal and basal rates of oxygen consumption in mice. Genetics 159:267–277PubMedPubMedCentralGoogle Scholar
  44. Dutenhoffer MS, Swanson DL (1996) Relationship of basal to summit metabolic rate in passerine birds and the aerobic capacity model for the origin of endothermy. Physiol Zool 69:1232–1254CrossRefGoogle Scholar
  45. Elia M (1992) Organ and tissue contribution to metabolic rate. In: Kinney JM, Tucker HN (eds) Energy metabolism: tissue determinants and cellular corollaries. Raven Press, New York, pp 61–77Google Scholar
  46. Enstipp MR, Grémillet D, Jones DR (2008) Heat increment of feeding in double-crested cormorants (Phalacrocorax auritis) and its potential for thermal substitution. J Exp Biol 211:49–57PubMedCrossRefGoogle Scholar
  47. Finke C, Misovic A, Prinzinger R (1995) Growth, the development of endothermy, and torpidity in blue-naped mousebirds Urocolius macrourus. Ostrich 66:1–9CrossRefGoogle Scholar
  48. Fristoe TS, Burger JR, Balk MA, Khaliq I, Hof C, Brown JH (2015) Metabolic heat production and thermal conductance are mass-independent adaptations to thermal environment in birds and mammals. Proc Natl Acad Sci USA 52:15934–15939CrossRefGoogle Scholar
  49. Gardner JL, Peters A, Kearney MR, Joseph L, Heinsohn R (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 26:285–291PubMedCrossRefGoogle Scholar
  50. Gębczyński AK, Konarzewski M (2009) Locomotor activity of mice divergently selected for basal metabolic rate: a test of hypotheses on the evolution of endothermy. J Evol Biol 22:1212–1220PubMedCrossRefGoogle Scholar
  51. Geiser F, Baudinette RV (1987) Seasonality of torpor and thermoregulation in three dasyurid marsupials. J Comp Physiol B 157:335–344CrossRefGoogle Scholar
  52. Geist V (1987) Bergmann’s rule is invalid. Can J Zool 65:1035–1038CrossRefGoogle Scholar
  53. Glazier DS (2015) Is metabolic rate a universal ‘pacemaker’ for biological processes? Biol Rev 90:377–407PubMedCrossRefGoogle Scholar
  54. Goodman RE, Lebuhn G, Seavy NE, Gardali T, Bluso-Demers JD (2012) Avian body size changes and climate change: warming or increasing variability? Global Change Biol 18:63–73CrossRefGoogle Scholar
  55. Green JA, Aitken-Simpson EJ, White CR, Bunce A, Butler PJ, Frappell PB (2013) An increase in minimum metabolic rate and not activity explains field metabolic rate changes in a breeding seabird. J Exp Biol 216:1726–1735PubMedCrossRefGoogle Scholar
  56. Guglielmo CG, Williams TD, Zwingelstein G, Brichon G, Weber J-M (2002) Plasma and muscle phospholipids are involved in the metabolic response to long-distance migration in a shorebird. J Comp Physiol B 172:409–417PubMedCrossRefGoogle Scholar
  57. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768PubMedCrossRefGoogle Scholar
  58. Haggerty C, Hoggard N, Brown DS, Clapham JC, Speakman JR (2008) Intra-specific variation in resting metabolic rate in MF1 mice is not associated with membrane desaturation in the liver. Mech Ageing Dev 129:129–137PubMedCrossRefGoogle Scholar
  59. Hammond KA, Kristan DM (2000) Responses to lactation and cold exposure by deer mice (Peromyscus maniculatus). Physiol Biochem Zool 73:547–556PubMedCrossRefGoogle Scholar
  60. Hammond KA, Roth J, Janes DN, Dohm MR (1999) Morphological and physiological responses to altitude in deer mice Peromyscus maniculatus. Physiol Biochem Zool 72:613–622PubMedCrossRefGoogle Scholar
  61. Hayes JP, Garland T Jr (1995) The evolution of endothermy: testing the aerobic capacity model. Evolut Int J org Evolut 49:836–847CrossRefGoogle Scholar
  62. Hayes JP, O’Connor CS (1999) Natural selection on thermogenic capacity of high-altitude deer mice. Evolut Int J org Evolut 53:1280–1287CrossRefGoogle Scholar
  63. Heldmaier G, Steinlechner S (1981) Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopus sungorus), living in natural photoperiod. J Comp Physiol 142:429–437CrossRefGoogle Scholar
  64. Hindle AG, McIntyre IW, Campbell KL, MacArthur RA (2003) The heat increment of feeding and its thermoregulatory implications in the short-tailed shrew (Blarina brevicauda). Can J Zool 81:1445–1453CrossRefGoogle Scholar
  65. Hislop MS, Buffenstein R (1994) Noradrenaline induces nonshivering thermogenesis in both the naked mole-rat (Heterocephalus glaber) and the Damara mole-rat (Cryptomys damarensis) despite very different modes of thermoregulation. J Therm Biol 19:25–32CrossRefGoogle Scholar
  66. Hoppeler H, Altpeter E, Wagner M, Turner DL, Hokanson J, König M, Stalder-Navarro VP, Weibel ER (1995) Cold acclimation and endurance training in guinea pigs: changes in lung, muscle and brown fat tissue. Resp Physiol 101:189–198CrossRefGoogle Scholar
  67. Houle-Leroy P, Garland T Jr, Swallow JG, Guderley H (2000) Effects of voluntary actiity and genetic selection on muscle metabolic capacities in house mice Mus domesticus. J Appl Physiol 89:1608–1616PubMedGoogle Scholar
  68. Hu S-N, Zhu Y-Y, Lin L, Zheng W-H, Liu J-S (2017) Temperature and photoperiod as environmental cues affect body mass and thermoregulation in Chinese bulbuls Pycnonotus sinensis. J Exp Biol 220:844–855PubMedGoogle Scholar
  69. Hulbert AJ, Else PL (1999) Membranes as possible pacemakers of metabolism. J Theor Biol 199:257–274PubMedCrossRefGoogle Scholar
  70. Hulbert AJ, Else PL (2000) Mechanisms underlying the cost of living in animals. Annu Rev Physiol 62:207–235PubMedCrossRefGoogle Scholar
  71. Hulbert AJ, Else PL (2004) Basal metabolic rate: history, composition, regulation and usefulness. Physiol Biochem Zool 77:869–876PubMedCrossRefGoogle Scholar
  72. Humphries MM, Careau V. (2011) Heat for nothing or activity for free? Evidence and implications of activity-thermoregulatory heat substitution. Integr Comp Biol 51:419–431PubMedCrossRefGoogle Scholar
  73. Jefimow M, Wojciechowski M, Masuda A, Oishi T (2004) Correlation between torpor frequency and capacity for non-shivering thermogenesis in the Siberian hamster (Phodopus songorus). J Therm Biol 29:641–647CrossRefGoogle Scholar
  74. Jetz W, Freckleton RP, McKechnie AE (2008) Environment, migratory tendency, phylogeny and basal metabolic rate in birds. PLoS One 3:e3261PubMedPubMedCentralCrossRefGoogle Scholar
  75. Jimenez AG, Van Brocklyn J, Wortman M, Williams JB (2014) Cellular metabolic rate is influenced by life-history traits in tropical and temperate birds. PLoS One 9:e87349PubMedPubMedCentralCrossRefGoogle Scholar
  76. Kane SL, Garland T Jr, Carter PA (2008) Basal metabolic rate of aged mice is affected by random genetic drift but not be selective breeding for high early-age locomotor activity or chronic wheel access. Physiol Biochem Zool 81:288–300PubMedCrossRefGoogle Scholar
  77. Kelly SA, Gomes FR, Kolb EM, Malisch JL, Garland T Jr (2017) Effects of activity, genetic selection, and their interaction on muscle metabolic capacities and organ masses in mice. J Exp Biol 220:1038–1047PubMedCrossRefGoogle Scholar
  78. Killen SS, Glazier DS, Rezende EL, Clark TD, Atkinson D, Willener AST, Halsey LG (2016) Ecological influences and morphological correlates of resting and maximal metabolic rates across teleost fish species. Am Nat 187:592–606PubMedCrossRefGoogle Scholar
  79. Kim B (2008) Thyroid hormone as a determinant of energy expenditure and the basal metabolic rate. Thyroid 18:141–144PubMedCrossRefGoogle Scholar
  80. King MO, Swanson DL (2013) Activation of the immune system incurs energetic costs but has no effect on the thermogenic performance of house sparrows during acute cold challenge. J Exp Biol 216:2097–2102PubMedCrossRefGoogle Scholar
  81. Kleiber M (1961) The fire of life. Wiley, New YorkGoogle Scholar
  82. Koch LG, Britton SL (2005) Divergent selection for aerobic capacity in rats as a model for complex disease. Integr Comp Biol 45:405–415PubMedCrossRefGoogle Scholar
  83. Konarzewski M, Diamond J (1995) Evolution of basal metabolic rate and organ masses in laboratory mice. Evolut Int J org Evolut 49:1239–1248CrossRefGoogle Scholar
  84. Konarzewski M, Książek A, Lapo IB (2005) Artificial selection of metabolic rates and related traits in rodents. Integr Comp Biol 45:416–425PubMedCrossRefGoogle Scholar
  85. Książek A, Konarzewski M, Lapo IB (2004) Anatomic and energetic correlates of divergent selection for basal metabolic rate in laboratory mice. Physiol Biochem Zool 77:890–899PubMedCrossRefGoogle Scholar
  86. Książek A, Czerniecki J, Konarzewski M (2009) Phenotypic flexibility of traits related to energy acquisition in mice divergently selected for basal metabolic rate (BMR). J Exp Biol 212:808–814PubMedCrossRefGoogle Scholar
  87. Larsen FJ, Schiffer TA, Sahlin K, Ekblom B, Weitzberg E, Lundberg JO (2011) Mitochondrial oxygen affinity predicts basal metabolic rate in humans. FASEB J 25:2843–2852PubMedCrossRefGoogle Scholar
  88. Lewden A, Petit M, Vézina F (2012) Dominant black-capped chickadees pay no maintenance energy costs for their wintering status and are not better at enduring cold than subordinate individuals. J Comp Physiol B 182:381–392PubMedCrossRefGoogle Scholar
  89. Li X-S, Wang D-H (2005) Seasonal adjustments in body mass and thermogenesis in Mongolian gerbils (Meriones unguiculatus): the roles of short photoperiod and cold. J Comp Physiol B 175:593–600PubMedCrossRefGoogle Scholar
  90. Li Q, Sun R-Y, Huang C, Wang Z, Liu X, Hou J, Liu J-S, Cai L, Li N, Zhang S, Wang Y (2001) Cold adaptive thermogenesis in small mammals from different geographical zones of China. Comp Biochem Physiol A 129:949–961CrossRefGoogle Scholar
  91. Liang Q-J, Zhao L, Wang J-Q, Chen Q, Zheng W-H, Liu J-S (2015) Effect of food restriction on the energy metabolism of the Chinese bulbul (Pycnonotus sinensis). Zool Res 36:79–87PubMedPubMedCentralGoogle Scholar
  92. Liknes ET, Swanson DL (2011) Phenotypic flexibility in passerine birds: seasonal variation of aerobic enzyme activities in skeletal muscle. J Therm Biol 36:430–436CrossRefGoogle Scholar
  93. Liu J-S, Chen Y-Q, Li M (2006) Thyroid hormones increase liver and muscle thermogenic capacity in little buntings (Emberiza pusilla). J Therm Biol 31:386–393CrossRefGoogle Scholar
  94. Liu J-S, Li M, Shao S-L (2008) Seasonal changes in thermogenic properties of liver and muscle in tree sparrows Passer montanus. Acta Zool Sinica 54:777–784Google Scholar
  95. Liu J-S, Yang M, Sun R-Y, Wang D-H (2009) Adaptive thermogenesis in Brandt’s vole (Lasiopodomys brandti) during cold and warm acclimation. J Therm Biol 34:60–69CrossRefGoogle Scholar
  96. Liwanag HEM, Williams TM, Costa DP, Kanatous SB, Davis RW, Boyd IL (2009) The effects of water temperature on the energetic costs of juvenile and adult California sea lions (Zalophus californianus): the importance of skeletal muscle thermogenesis for thermal balance. J Exp Biol 212:3977–3984PubMedCrossRefGoogle Scholar
  97. Londoño GA, Chappell MA, Castañeda MR, Jankowski JE, Robinson SK (2015) Basal metabolism in tropical birds: latitute, altitude, and the “pace of life”. Funct Ecol 29:338–346CrossRefGoogle Scholar
  98. Lovegrove BG (2003) The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. J Comp Physiol B 173:87–112PubMedGoogle Scholar
  99. Lovegrove BG (2005) Seasonal thermoregulatory responses in mammals. J Comp Physiol B 175:231–247PubMedCrossRefGoogle Scholar
  100. Lovegrove BG (2012) The evolution of endothermy in Cenozoic mammals: a plesiomorphic-apomorphic continuum. Biol Rev 87:128–162PubMedCrossRefGoogle Scholar
  101. Luna F, Naya H, Naya DE (2017) Understanding evolutionary variation in basal metabolic rate: an analysis in subterranean rodents. Comp Biochem Physiol A 206:87–94CrossRefGoogle Scholar
  102. Maldonado K, Cavieres G, Veloso C, Canals M, Sabat P (2009) Physiological responses in rufous-collared sparrows to thermal acclimation and seasonal acclimatization. J Comp Physiol B 179:335–343PubMedCrossRefGoogle Scholar
  103. Maldonado K, van Dongen WFD, Vásquez RA, Sabat P (2012) Geographic variation in the association between exploratory behavior and physiology in rufous-collared sparrow. Physiol Biochem Zool 85:618–624PubMedCrossRefGoogle Scholar
  104. Mathot KJ, Nicolaus M, Araya-Ajoy YG, Dingemanse NJ, Kempenaers B (2015) Does metabolic rate predict risk-taking behaviour? A field experiment in a wild passerine bird. Funct Ecol 29:239–249CrossRefGoogle Scholar
  105. McKechnie AE (2008) Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J Comp Physiol B 178:235–247PubMedCrossRefGoogle Scholar
  106. McKechnie AE, Lovegrove BG (2001) Thermoregulation and the energetic significance of clustering behavior in the white-backed mousebird (Colius colius). Physiol Biochem Zool 74:238–249PubMedCrossRefGoogle Scholar
  107. McKechnie AE, Swanson DL (2010) Sources and significance of variation in basal, summit and maximal metabolic rates in birds. Curr Zool 56:741–758Google Scholar
  108. McKechnie AE, Körtner G, Lovegrove BG (2004) Rest-phase thermoregulation in free-ranging white-backed mousebirds. Condor 106:144–150CrossRefGoogle Scholar
  109. McKechnie AE, Körtner G, Lovegrove BG (2006) Thermoregulation under semi-natural conditions in specked mousebirds: the role of communal roosting. Afr Zool 41:155–163CrossRefGoogle Scholar
  110. McKechnie AE, Noakes MJ, Smit B (2015) Global patterns of seasonal acclimatization in avian resting metabolic rates. J Ornithol 156(Suppl 1):S367–S376CrossRefGoogle Scholar
  111. McNab BK (1978) The evolution of endothermy in the phylogeny of mammals. Am Nat 112:1–21CrossRefGoogle Scholar
  112. McNab BK (1988) Food habits and the basal rate of metabolism in birds. Oecologia 77:343–349PubMedCrossRefGoogle Scholar
  113. McNab BK (1997) On the utility of uniformity in the definition of the basal rate of metabolism. Physiol Zool 70:718–720PubMedCrossRefGoogle Scholar
  114. McNab BK (2008) An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Physiol A 151:5–28CrossRefGoogle Scholar
  115. McNab BK (2012) Extreme measures: the ecological energetics of birds and mammals. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  116. Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. Global Ecol Biogeogr 30:331–351Google Scholar
  117. Mineo PM, Cassell EA, Roberts ME, Schaeffer PJ (2012) Chronic cold acclimation increases thermogenic capacity, non-shivering thermogenesis and muscle citrate synthase activity in both wild-type and brown adipose tissue deficient mice. Comp Biochem Physiol A 161:395–400CrossRefGoogle Scholar
  118. Møller AP (2009) Basal metabolic rate and risk taking behaviour in birds. J Evol Biol 22:2420–2429PubMedCrossRefGoogle Scholar
  119. Mueller P, Diamond J (2001) Metabolic rate and environmental productivity: well-provisioned animals evolved to run and idle fast. Proc Natl Acad Sci USA 98:12550–12554PubMedPubMedCentralCrossRefGoogle Scholar
  120. Naya DE, Spangenberg L, Naya H, Bozinovic F (2013) How does evolutionary variation in basal metabolic rates arise? A statistical assessment and a mechanistic model. Evolut Int J org Evolut 67:1463–1476Google Scholar
  121. Nespolo RF, Bacigalupe LD, Sabat P, Bozinovic F (2002) Interplay among energy metabolism, organ mass and digestive enzyme activity in the mouse-opossum Thylamys elegans: the role of thermal acclimation. J Exp Biol 205:2697–2703PubMedGoogle Scholar
  122. Nespolo RF, Bustamante DM, Bacigalupe LD, Bozinovic F (2005) Quantitative genetics of bioenergetics and growth-related traits in the wild mammal, Phyllotis darwini. Evolut Int J org Evolut 59:1829–1837Google Scholar
  123. Nespolo RF, Baciagalupe LD, Figueroa CC, Koteja P, Opazo JC (2011) Using new tools to solve an old problem: the evolution of endothermy in vertebrates. Trends Ecol Evol 26:414–423PubMedCrossRefGoogle Scholar
  124. Nespolo RF, Solano-Iguaran JJ, Bozinovic F (2017) Phylogenetic analysis supports the aerobic-capacity model for the evolution of endothermy. Am Nat 189:13–27PubMedCrossRefGoogle Scholar
  125. Nilsson JF, Nilsson J-A (2016) Fluctuating selection on basal metabolic rate. Ecol Evolut 6:1197–1202CrossRefGoogle Scholar
  126. Noakes MJ, Wolf BO, McKechnie AE (2017) Seasonal metabolic acclimatization varies in direction and magnitude among populations of an Afrotropical passerine bird. Physiol Biochem Zool 90:178–189PubMedCrossRefGoogle Scholar
  127. Oelkrug R, Heldmaier G, Meyer CW (2011) Torpor patterns, arousal rates, and temporal organization of torpor entry in wildtype and UCP1-ablated mice. J Comp Physiol B 181:137–145PubMedCrossRefGoogle Scholar
  128. Olson VA, Davies RG, Orme CDL, Thomas GH, Meiri S, Blackburn TM, Gaston KJ, Owens IPF, Bennett PM (2009) Global biogeography and the ecology of body size in birds. Ecol Lett 12:249–259PubMedCrossRefGoogle Scholar
  129. Pauli JN, Peery MZ, Fountain ED, Karasov WH (2016) Arboreal folivores limit their energetic output, all the way to slothfulness. Am Nat 188:196–204PubMedCrossRefGoogle Scholar
  130. Peña-Villalobos I, Nuñez-Villegas M, Bozinovic F, Sabat P (2014) Metabolic enzymes in seasonally acclimatized and cold acclimated rufous-collared sparrows inhabiting a Chilean Mediterranean environment. Curr Zool 60:338–350CrossRefGoogle Scholar
  131. Petit M, Lewden A, Vézina F (2013) Intra-seasonal flexibility in avian metabolic performance highlights the uncoupling of basal metabolic rate and thermogenic capacity. PLoS One 8:e68292PubMedPubMedCentralCrossRefGoogle Scholar
  132. Petit M, Lewden A, Vézina F (2014) How does flexibility in body composition relate to seasonal changes in metabolic performance in a small passerine wintering at northern latitude? Physiol Biochem Zool 87:539–549PubMedCrossRefGoogle Scholar
  133. Petit M, Clavijo-Baquet S, Vézina F (2017) Increasing winter maximal metabolic rate improves intra-winter survival in small birds. Physiol Biochem Zool 90:166–177PubMedCrossRefGoogle Scholar
  134. Pierce BJ, McWilliams SR, O’Connor TP, Place AR, Guglielmo CG (2005) Effect of dietary fatty acid composition on depot fat and exercise performance in a migrating songbird, the red-eyed vireo. J Exp Biol 208:1277–1285PubMedCrossRefGoogle Scholar
  135. Piersma T, van Gils J (2011) The flexible phenotype: A body-centred integration of ecology, physiology, and behavior. Oxford University Press, OxfordGoogle Scholar
  136. Porter WP, Kearney M (2009) Size, shape and the thermal niche of endotherms. Proc Natl Acad Sci USA 106(suppl 2):19666–19672PubMedPubMedCentralCrossRefGoogle Scholar
  137. Portugal SJ, Green JA, Halsey LG, Arnold W, Careau V, Dann P, Frappell PB, Grémillet D, Handrich Y, Martin GR, Ruf T, Guillemette MM, Butler PJ (2016) Associations between resting, activity, and daily metabolic rate in free-living endotherms: no universal rule in birds and mammals. Physiol Biochem Zool 89:251–261PubMedCrossRefGoogle Scholar
  138. Price ER, Staples JF, Milligan CL, Guglielmo CG (2011) Carnitine palmitoyl transferase activity and whole muscle oxidation rates vary with fatty acid substrate in avian flight muscle. J Comp Physiol B 181:565–573PubMedGoogle Scholar
  139. Prinzinger R (1988) Energy metabolism, body-temperature and breathing parameters in non-torpid blue-naped mousebirds Urocolius macrourus. J Comp Physiol B 157:801–806CrossRefGoogle Scholar
  140. Prinzinger R, Göppel R, Lorenz A, Kulzer E (1981) Body temperature and metabolism in the red-backed mousebird (Colius castanotus) during fasting and torpor. Comp Biochem Physiol A 69:689–692CrossRefGoogle Scholar
  141. Prum RO, Berv JS, Dornburg A, Field DJ, Townsend JP, Lemmon EM Lemmon AR (2015) A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526:569–573PubMedCrossRefGoogle Scholar
  142. Raichlen DA, Gordon AD, Muchlinski MN, Snodgrass JJ (2010) Causes and significance of variation in mammalian basal metabolism. J Comp Physiol B 180:301–311PubMedCrossRefGoogle Scholar
  143. Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio P-O (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Phil Trans Roy Soc B 36:4051–4063CrossRefGoogle Scholar
  144. Rezende EL, Bacigalupe LD (2015) Thermoregulation in endotherms: physiological principles and ecological consequences. J Comp Physiol B 185:709–727PubMedCrossRefGoogle Scholar
  145. Rezende EL, Swanson DL, Novoa FF, Bozinovic F (2002) Passerines versus nonpasserines: so far, no statistical differences in the scaling of avian energetics. J Exp Biol 20:101–107Google Scholar
  146. Rezende EL, Bozinovic F, Garland, T Jr (2004) Climatic adaptation and the evolution of basal and maximal rates of metabolism in rodents. Evolut Int J org Evolut 58:1361–1374CrossRefGoogle Scholar
  147. Ricklefs RE, Konarzewski M, Daan S (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147:1047–1071CrossRefGoogle Scholar
  148. Riddle O, Smith GC, Benedict FG (1932) The basal metabolism of the mourning dove and some of its hybrids. Am J Physiol 101:206–267Google Scholar
  149. Rimbach R, Pillay N, Schradin C (2017) Both thyroid hormone levels and resting metabolic rate decrease in African striped mice when food availability decreases. J Exp Biol 220:837–843PubMedGoogle Scholar
  150. Rodríguez MA, López-Sañudo IL, Hawkins BA (2006) The geographic distribution of mammal body size in Europe. Global Ecol Biogeogr 15:173–181CrossRefGoogle Scholar
  151. Rodríguez MA, Olalla-Tárraga, Hawkins BA (2008) Bergmann’s rule and the geography of mammal body size in the Western Hemisphere. Global Ecol Biogeogr 17:274–283CrossRefGoogle Scholar
  152. Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758PubMedGoogle Scholar
  153. Rønning B, Jensen H, Moe B, Bech C (2007) Basal metabolic rate: heritability and genetic correlations with morphological traits in the zebra finch. J Evol Biol 20:1815–1822PubMedCrossRefGoogle Scholar
  154. Rønning B, Broggi J, Bech C, Moe B, Ringsby TH, Pärn H, Hagen IJ, Saether B-E, Jensen H (2016) Is basal metabolic rate associated with recruit production and survival in free-living house sparrows? Funct Ecol 30:1140–1148CrossRefGoogle Scholar
  155. Rubner M (1883) Ueber den Eifluss der Körpergrösse auf Sttoffund Kraftwechsel. Z Biol 19:535–562Google Scholar
  156. Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev 90:891–926PubMedCrossRefGoogle Scholar
  157. Sabat P, Ramirez-Otarola N, Barceló G, Salinas J, Bozinovic F (2010) Comparative basal metabolic rate among passerines and the food habit hypothesis. Comp Biochem Physiol A 157:35–40CrossRefGoogle Scholar
  158. Sadowska ET, Labocha MK, Baliga K, Stanisz A, Wróblewska AK, Jagusiak W, Koteja P (2005) Genetic correlations between basal and maximum metabolic rates in a wild rodent: consequences for evolution of endothermy. Evolut Int J org Evolut 59:672–681CrossRefGoogle Scholar
  159. Sadowska ET, Baliga-Klimczyk K, Labocha MK, Koteja P (2009) Genetic correlations in a wild rodent: grass-eaters and fast-growers evolve high basal metabolic rates. Evolut Int J org Evolut 63:1530–1539CrossRefGoogle Scholar
  160. Schmidt-Nielsen K (1984) Scaling. Why is animal size so important? Cambridge Univ Press, CambridgeCrossRefGoogle Scholar
  161. Scholander PF, Hock R, Walters V, Johnson F, Irving L (1950a) Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. Biol Bull 99:259–271PubMedCrossRefGoogle Scholar
  162. Scholander PF, Hock R, Walters V, Johnson F, Irving L (1950b) Heat regulation in some arctic and tropical mammals and birds. Biol Bull 99:237–258PubMedCrossRefGoogle Scholar
  163. Sears MW, Hayes JP, O’Connor CS, Geluso K, Sedinger JS (2006) Individual variation in thermogenic capacity affects above-ground activity of high-altitude deer mice. Funct Ecol 20:97–104CrossRefGoogle Scholar
  164. Seidel A, Heldmaier G, Schulz F (1988) Effect of triiodothyronine, thyrotropin-releasing hormone and propylthiouracil on the thermogenic capacities of Djangarian hamsters living in natural photoperiod. J Therm Biol 13:49–51CrossRefGoogle Scholar
  165. Selman C, Lumsden S, Bünger L, Hill WG, Speakman JR (2001) Resting metabolic rate and morphology in mice (Mus musculus) selected for high and low food intake. J Exp Biol 204:777–784PubMedGoogle Scholar
  166. Sheridan JA, Bickford D (2011) Shrinking body size as an ecological response to climate change. Nat Climate Change 1:401–406CrossRefGoogle Scholar
  167. Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds. Yale University Press, New HavenGoogle Scholar
  168. Speakman JR (2005) Body size, energy metabolism and lifespan. J Exp Biol 208:1717–1730PubMedCrossRefGoogle Scholar
  169. Speakman JR, Król E (2010) Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J Anim Ecol 79:726–746PubMedGoogle Scholar
  170. Speakman JR, Król E (2011) Limits to sustained energy intake. XIII. Recent progress and future perspectives. J Exp Biol 214:230–241PubMedCrossRefGoogle Scholar
  171. Speakman JR, Król E, Johnson MS (2004) The functional significance of individual variation in basal metabolic rate. Physiol Biochem Zool 77:900–915PubMedCrossRefGoogle Scholar
  172. Swallow JG, Rhodes JS, Garland T Jr (2005) Phenotypic and evolutionary plasticity of organ masses in response to voluntary exercise in house mice. Integr Comp Biol 45:426–437PubMedCrossRefGoogle Scholar
  173. Swanson DL (2010) Seasonal metabolic variation in birds: functional and mechanistic correlates. Curr Ornithol 17:75–129Google Scholar
  174. Swanson DL, Bozinovic F (2011) Metabolic capacity and the evolution of biogeographic patterns in oscine and suboscine passerine birds. Physiol Biochem Zool 84:185–194PubMedCrossRefGoogle Scholar
  175. Swanson DL, Garland T Jr (2009) The evolution of high summit metabolism and cold tolerance in birds and its impact on present-day distributions. Evolut Int J org Evolut 63:184–194CrossRefGoogle Scholar
  176. Swanson DL, Thomas NE (2007) The relationship of plasma indicators of lipid metabolism and muscle damage to overnight temperature in winter-acclimatized small birds. Comp Biochem Physiol A 146:87–94CrossRefGoogle Scholar
  177. Swanson DL, Thomas NE, Liknes ET, Cooper SJ (2012) Intraspecific correlations of basal and maximal metabolic rates in birds and the aerobic capacity model for the evolution of endothermy. PLoS One 7:e34271PubMedPubMedCentralCrossRefGoogle Scholar
  178. Tieleman BI, Williams JB, Buschur ME, Brown CR (2003) Phenotypic variation of larks along an aridity gradient: are desert birds more flexible. Ecology 84:1800–1815CrossRefGoogle Scholar
  179. Tieleman BI, Versteegh MA, Helm B, Dingemanse NJ (2009) Quantitative genetics parameters show partial independent evolutionary potential for body mass and metabolism in stonechats from different populations. J Zool Lond 279:129–136CrossRefGoogle Scholar
  180. van de Ven TMFN, Mzilikazi N, McKechnie AE (2013) Seasonal metabolic variation in two populations of an Afrotropical Euplectid bird. Physiol Biochem Zool 86:19–26PubMedCrossRefGoogle Scholar
  181. Versteegh MA, Schwabl I, Jaquier S, Tieleman BI (2012) Do immunological, endocrine and metabolic traits fall on a single Pace-of-Life axis? Covariation and constraints among physiological systems. J Evol Biol 25:1864–1876PubMedCrossRefGoogle Scholar
  182. Vézina F, Salvante KG (2010) Behavioral and physiological flexibility are used by birds to manage energy and support investment in the early stages of reproduction. Curr Zool 56:767–792Google Scholar
  183. Vézina F, Williams TD (2003) Plasticity in body composition in breeding birds: what drives the metabolic costs of egg production? Physiol Biochem Zool 76:716–730PubMedCrossRefGoogle Scholar
  184. Vézina F, Williams TD (2005) Interactions between organ mass and citrate synthase activity as an indicator of tissue maximal oxidative capacity in breeding European starlings: implications for metabolic rate and organ mass relationships. Funct Ecol 19:119–128CrossRefGoogle Scholar
  185. Vézina F, Jalvingh KM, Dekinga A, Piersma T (2006) Acclimation to different thermal conditions in a northerly wintering shorebird is driven by body mass-related changes in organ size. J Exp Biol 209:3141–3154PubMedCrossRefGoogle Scholar
  186. Vézina F, Love OP, Lessard M, Williams TD (2009) Shifts in metabolic demands in growing altricial nestlings illustrate context-specific relationships between basal metabolic rate and body composition. Physiol Biochem Zool 82:248–257PubMedCrossRefGoogle Scholar
  187. Villarin JJ, Schaeffer PJ, Markle RA, Lindstedt SL (2003) Chronic cold exposure increases liver oxidative capacity in the marsupial Monodelphis domestica. Comp Biochem Physiol A 136:621–630CrossRefGoogle Scholar
  188. Walsberg GE (1990) Communal roosting in a very small bird: consequences for the thermal and respiratory environments. Condor 92:795–798CrossRefGoogle Scholar
  189. Weathers WW (1979) Climatic adaptation in avian standard metabolic rate. Oecologia 42:81–89PubMedCrossRefGoogle Scholar
  190. Weber TP, Piersma T (1996) Basal metabolic rate and the mass of tissues differing in metabolic scope: migration-related covariation between individual knots, Calidris canutus. J Avian Biol 27:215–224CrossRefGoogle Scholar
  191. Welcker J, Chastel O, Gabrielsen GW, Guillaumin J, Kitaysky AS, Speakman JR, Tremblay Y, Bech C (2013) Thyroid hormones correlate with basal metabolic rate but not field metabolic rate in a wild bird species. PLoS One 8:e56229PubMedPubMedCentralCrossRefGoogle Scholar
  192. Welcker J, Speakman JR, Elliott KH, Hatch SA, Kitaysky AS (2015) Resting and daily energy expenditure during reproduction are adjusted in opposite directions in free-living birds. Funct Ecol 29:250–258CrossRefGoogle Scholar
  193. Wells ME, Schaeffer PJ (2012) Seasonality of peak metabolic rate in non-migrant tropical birds. J Avian Biol 43:481–485CrossRefGoogle Scholar
  194. White CR, Seymour RS (2004) Does basal metabolic rate contain a useful signal? Mammalian BMR allometry and correlations with a selection of physiological, ecological and life-history variables. Physiol Biochem Zool 77:929–941PubMedCrossRefGoogle Scholar
  195. White CR, Blackburn TM, Martin GR, Butler PJ (2007) Basal metabolic rate of birds is associated with habitat temperature and precipitation, not primary productivity. Proc Roy Soc B Biol Sci 274:287–293CrossRefGoogle Scholar
  196. Wickler SJ (1981) Seasonal changes in enzymes of aerobic heat production in the white-footed mouse. Am J Physiol Reg Integr Comp Physiol 240:R289–R294Google Scholar
  197. Wiersma P, Muñoz-Garcia A, Walker A, Williams JB (2007) Tropical birds have a slow pace of life. Proc Nal Acad Sci USA 104:9340–9345CrossRefGoogle Scholar
  198. Wiersma P, Nowak B, Williams JB (2012) Small organ size contributes to the slow pace of life in tropical birds. J Exp Biol 215:1662–1669PubMedCrossRefGoogle Scholar
  199. Williams JB, Tieleman BI (2000) Flexibility in basal metabolic rate and evaporative water loss among hoopoe larks exposed to different environmental temperatures. J Exp Biol 203:3153–3159PubMedGoogle Scholar
  200. Williams TM, Haun J, Davis RW, Fuiman LA, Kohn S (2001) A killer apetite: metabolic consequences of carnivory in marine mammals. Comp Biochem Physiol A 129:785–796CrossRefGoogle Scholar
  201. Williams JB, Miller RA, Harper JM, Wiersma P (2010) Functional linkages for the pace of life, life history and environment in birds. Integr Comp Biol 50:855–868PubMedPubMedCentralCrossRefGoogle Scholar
  202. Wone B, Sears MW, Lobacha MK, Donovan ER, Hayes JP (2009) Genetic variances and covariances of aerobic metabolic rates in laboratory mice. Proc R Soc B 276:3695–3704PubMedPubMedCentralCrossRefGoogle Scholar
  203. Wone B, Donovan ER, Cushman JC, Hayes JP (2013) Metabolic rates associated with membrane fatty acids in mice selected for increased maximal metabolic rate. Comp Biochem Physiol A 165:70–78CrossRefGoogle Scholar
  204. Wone B, Madsen P, Donovan ER, Lobacha MK, Sears MW, Downs CJ, Sorenson DA, Hayes JP (2015) A strong response to selection on mass-independent maximal metabolic rate without a correlated response in basal metabolic rate. Heredity 114:419–427PubMedPubMedCentralCrossRefGoogle Scholar
  205. Woodley R, Buffenstein R (2002) Thermogenic changes with chronic cold exposure in the naked mole-rat (Heterocephalus glaber). Comp Biochem Physiol A 133:827–834CrossRefGoogle Scholar
  206. Yahav S, Buffenstein R (1991) Huddling behavior facilitates homeothermy in the naked mole rat Heterocephalus glaber. Physiol Zool 64:871–884CrossRefGoogle Scholar
  207. Zheng W-H, Li M, Liu J-S, Shao S-L (2008a) Seasonal acclimatization of metabolism in Eurasian tree sparrows (Passer montanus). Comp Biochem Physiol A 151:519–525CrossRefGoogle Scholar
  208. Zheng W-H, Liu J-S, Jang XH, Fang YY, Zhang G-K (2008b) Seasonal variation in metabolism and thermoregulation in the Chinese bulbul. J Therm Biol 33:315–319CrossRefGoogle Scholar
  209. Zheng W-H, Fang YY, Jiang X-H, Zhang G-K, Liu J-S (2010) Comparison of thermogenic character of liver and muscle in Chinese bulbul Pycnonotus sinensis between summer and winter. Zool Res 31:319–327PubMedGoogle Scholar
  210. Zheng W-H, Fang YY, Jiang X-H, Li M (2013) Geographic variation in basal thermogenesis in little buntings: relationship to cellular thermogenesis and thyroid hormone concentrations. Comp Biochem Physiol A 164:483–490CrossRefGoogle Scholar
  211. Zheng W-H, Liu J-S, Swanson DL (2014a) Seasonal phenotypic flexibility of body mass, organ masses, and tissue oxidative capacity and their relationship to resting metabolic rate in Chinese bulbuls. Physiol Biochem Zool 87:432–444PubMedCrossRefGoogle Scholar
  212. Zheng W-H, Li M, Liu J-S, Xu X-J, Shao S-L, Xu X-J (2014b) Seasonal variation of metabolic thermogenesis in Eurasian tree sparrows (Passer montanus) over a latitudinal gradient. Physiol Biochem Zool 87:704–718PubMedCrossRefGoogle Scholar
  213. Zhou L-M, Xia S-S, Chen Q, Wang R-M, Zheng W-H, Liu J-S (2016) Phenotypic flexibility of thermogenesis in hwamei (Garrulax canorus): responses to cold acclimation. Am J Physiol Regul Integr Comp Physiol 310:R330–R336PubMedCrossRefGoogle Scholar
  214. Zhu W-L, Zhang H, Wang Z-K (2012) Seasonal changes in body mass and thermogenesis in tree shrews (Tupaia belangeri): the roles of photoperiod and cold. J Therm Biol 37:479–484CrossRefGoogle Scholar
  215. Zub K, Borowski Z, Szafransk PA, Wieczorek M, Konarzewski M (2014) Lower body mass and higher metabolic rate enhance winter survival in root voles, Microtus oeconomus. Biol J Linnaean Soc 113:297–309CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of BiologyUniversity of South DakotaVermillionUSA
  2. 2.Department of Zoology and Entomology, DST-NRF Centre of Excellence at the Percy FitzPatrick InstituteUniversity of PretoriaHatfieldSouth Africa
  3. 3.Département de Biologie, Chimie et GéographieUniversité du Québec à RimouskiRimouskiCanada
  4. 4.Groupe de recherche sur les environnements nordiques BORÉAS, Centre d’Études NordiquesCentre de la Science de la Biodiversité du QuébecRimouskiCanada

Personalised recommendations