Abstract
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.
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References
Aschoff J, Pohl H (1970) Rhythmic variations in energy metabolism. Fed Proc 291:1541–1552
Ashton KG (2002) Patterns of within-species body size variation of birds: strong evidence for Bergmann’s rule. Global Ecol Biogeogr 11:505–523
Ashton KG, Tracy MC, de Queiroz A (2000) Is Bergmann’s rule valid for mammals? Am Nat 156:391–415
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 58:421–429
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 180:293–299
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.
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 90:153–165
Bartholomew GA, Trost CH (1970) Temperature regulation in the speckled mousebird, Colius striatus. Condor 72:141–146
Benedict FG (1938) Vital energetics: a study in comparative basal metabolism. Carnegie Inst, Washington (Publication 503)
Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206:649–654
Bergmann C (1847) Ueber die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Gottinger Studien 3:595–708
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 164:618–621
Blackburn TM, Hawkins BA (2004) Bergmann’s rule and the mammal fauna of northern North America. Ecography 27:715–724
Bligh J, Johnson KG (1973) Glossary of terms for thermal physiology. J Appl Physiol 35:941–961
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 205:3207–3214
Boratyński Z, Koteja P (2009) The association between body mass, metabolic rates and survival of bank voles. Funct Ecol 23:330–339
Boratyński Z, Koskela E, Mappes T, Schroderus E (2013) Quantitative genetics and fitness effects of basal metabolism. Evol Ecol 27:301–314
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 186:387–402
Bozinovic F, Sabat P (2010) On the intraspecific variability in basal metabolism and the food habits hypothesis in birds. Curr Zool 56:759–766
Bozinovic F, Novoa FF, Veloso C (1990) Seasonal changes in energy expenditure and digestive tract of Abrothrix andinus in the Andes Range. Physiol Zool 63:1216–1231
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 152:560–564
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 219:2559–2566
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 80:491–499
Buffenstein R, Yahav S (1991) Is the naked mole-rat Heterocephalus glaber an endothermic yet poikilothermic mammal? J Therm Biol 16:227–232
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 75:187–199
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 278:3465–3473
Careau V (2013) Basal metabolic rate, maximum thermogenic capacity and aerobic scope in rodents: interaction between environmental temperature and torpor use. Biol Lett 9:20121104
Careau V, Garland T Jr (2012) Performance, personality and energetics: correlation, causation, and mechanism. Physiol Biochem Zool 85:543–571
Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117:641–653
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 24:2153–2163
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 171:11–23
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 216:418–426
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 219–233
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 202:2269–2279
Clarke A, Rothery P (2008) Scaling of body temperature in mammals and birds. Funct Ecol 22:58–67
Clarke A, Rothery P, Isaac NJB (2010) Scaling of basal metabolic rate with body mass and temperature in mammals. J Anim Ecol 79:610–619
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:e37069
Crompton AW, Taylor CR, Jagger JA (1978) Evolution of homeothermy in mammals. Nature 272:333–336
Cruz-Neto AP, Bozinovic F (2004) The relationship between diet quality and basal metabolic rate in endotherms: insights from intraspecific analyses. Physiol Biochem Zool 77:877–889
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. 83–94
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 85–124
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 107:41–48
Dohm MR, Hayes JP, Garland T Jr (2001) The quantitative genetics of maximal and basal rates of oxygen consumption in mice. Genetics 159:267–277
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 69:1232–1254
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 61–77
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 211:49–57
Finke C, Misovic A, Prinzinger R (1995) Growth, the development of endothermy, and torpidity in blue-naped mousebirds Urocolius macrourus. Ostrich 66:1–9
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 52:15934–15939
Gardner JL, Peters A, Kearney MR, Joseph L, Heinsohn R (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 26:285–291
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 22:1212–1220
Geiser F, Baudinette RV (1987) Seasonality of torpor and thermoregulation in three dasyurid marsupials. J Comp Physiol B 157:335–344
Geist V (1987) Bergmann’s rule is invalid. Can J Zool 65:1035–1038
Glazier DS (2015) Is metabolic rate a universal ‘pacemaker’ for biological processes? Biol Rev 90:377–407
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 18:63–73
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 216:1726–1735
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 172:409–417
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 320:1763–1768
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 129:129–137
Hammond KA, Kristan DM (2000) Responses to lactation and cold exposure by deer mice (Peromyscus maniculatus). Physiol Biochem Zool 73:547–556
Hammond KA, Roth J, Janes DN, Dohm MR (1999) Morphological and physiological responses to altitude in deer mice Peromyscus maniculatus. Physiol Biochem Zool 72:613–622
Hayes JP, Garland T Jr (1995) The evolution of endothermy: testing the aerobic capacity model. Evolut Int J org Evolut 49:836–847
Hayes JP, O’Connor CS (1999) Natural selection on thermogenic capacity of high-altitude deer mice. Evolut Int J org Evolut 53:1280–1287
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 142:429–437
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 81:1445–1453
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 19:25–32
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 101:189–198
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 89:1608–1616
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 220:844–855
Hulbert AJ, Else PL (1999) Membranes as possible pacemakers of metabolism. J Theor Biol 199:257–274
Hulbert AJ, Else PL (2000) Mechanisms underlying the cost of living in animals. Annu Rev Physiol 62:207–235
Hulbert AJ, Else PL (2004) Basal metabolic rate: history, composition, regulation and usefulness. Physiol Biochem Zool 77:869–876
Humphries MM, Careau V. (2011) Heat for nothing or activity for free? Evidence and implications of activity-thermoregulatory heat substitution. Integr Comp Biol 51:419–431
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 29:641–647
Jetz W, Freckleton RP, McKechnie AE (2008) Environment, migratory tendency, phylogeny and basal metabolic rate in birds. PLoS One 3:e3261
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:e87349
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 81:288–300
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 220:1038–1047
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 187:592–606
Kim B (2008) Thyroid hormone as a determinant of energy expenditure and the basal metabolic rate. Thyroid 18:141–144
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 216:2097–2102
Kleiber M (1961) The fire of life. Wiley, New York
Koch LG, Britton SL (2005) Divergent selection for aerobic capacity in rats as a model for complex disease. Integr Comp Biol 45:405–415
Konarzewski M, Diamond J (1995) Evolution of basal metabolic rate and organ masses in laboratory mice. Evolut Int J org Evolut 49:1239–1248
Konarzewski M, Książek A, Lapo IB (2005) Artificial selection of metabolic rates and related traits in rodents. Integr Comp Biol 45:416–425
Książek A, Konarzewski M, Lapo IB (2004) Anatomic and energetic correlates of divergent selection for basal metabolic rate in laboratory mice. Physiol Biochem Zool 77:890–899
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 212:808–814
Larsen FJ, Schiffer TA, Sahlin K, Ekblom B, Weitzberg E, Lundberg JO (2011) Mitochondrial oxygen affinity predicts basal metabolic rate in humans. FASEB J 25:2843–2852
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 182:381–392
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 175:593–600
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 129:949–961
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 36:79–87
Liknes ET, Swanson DL (2011) Phenotypic flexibility in passerine birds: seasonal variation of aerobic enzyme activities in skeletal muscle. J Therm Biol 36:430–436
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 31:386–393
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 54:777–784
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 34:60–69
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 212:3977–3984
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 29:338–346
Lovegrove BG (2003) The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. J Comp Physiol B 173:87–112
Lovegrove BG (2005) Seasonal thermoregulatory responses in mammals. J Comp Physiol B 175:231–247
Lovegrove BG (2012) The evolution of endothermy in Cenozoic mammals: a plesiomorphic-apomorphic continuum. Biol Rev 87:128–162
Luna F, Naya H, Naya DE (2017) Understanding evolutionary variation in basal metabolic rate: an analysis in subterranean rodents. Comp Biochem Physiol A 206:87–94
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 179:335–343
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 85:618–624
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 29:239–249
McKechnie AE (2008) Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J Comp Physiol B 178:235–247
McKechnie AE, Lovegrove BG (2001) Thermoregulation and the energetic significance of clustering behavior in the white-backed mousebird (Colius colius). Physiol Biochem Zool 74:238–249
McKechnie AE, Swanson DL (2010) Sources and significance of variation in basal, summit and maximal metabolic rates in birds. Curr Zool 56:741–758
McKechnie AE, Körtner G, Lovegrove BG (2004) Rest-phase thermoregulation in free-ranging white-backed mousebirds. Condor 106:144–150
McKechnie AE, Körtner G, Lovegrove BG (2006) Thermoregulation under semi-natural conditions in specked mousebirds: the role of communal roosting. Afr Zool 41:155–163
McKechnie AE, Noakes MJ, Smit B (2015) Global patterns of seasonal acclimatization in avian resting metabolic rates. J Ornithol 156(Suppl 1):S367–S376
McNab BK (1978) The evolution of endothermy in the phylogeny of mammals. Am Nat 112:1–21
McNab BK (1988) Food habits and the basal rate of metabolism in birds. Oecologia 77:343–349
McNab BK (1997) On the utility of uniformity in the definition of the basal rate of metabolism. Physiol Zool 70:718–720
McNab BK (2008) An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Physiol A 151:5–28
McNab BK (2012) Extreme measures: the ecological energetics of birds and mammals. University of Chicago Press, Chicago
Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. Global Ecol Biogeogr 30:331–351
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 161:395–400
Møller AP (2009) Basal metabolic rate and risk taking behaviour in birds. J Evol Biol 22:2420–2429
Mueller P, Diamond J (2001) Metabolic rate and environmental productivity: well-provisioned animals evolved to run and idle fast. Proc Natl Acad Sci USA 98:12550–12554
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 67:1463–1476
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 205:2697–2703
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 59:1829–1837
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 26:414–423
Nespolo RF, Solano-Iguaran JJ, Bozinovic F (2017) Phylogenetic analysis supports the aerobic-capacity model for the evolution of endothermy. Am Nat 189:13–27
Nilsson JF, Nilsson J-A (2016) Fluctuating selection on basal metabolic rate. Ecol Evolut 6:1197–1202
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 90:178–189
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 181:137–145
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 12:249–259
Pauli JN, Peery MZ, Fountain ED, Karasov WH (2016) Arboreal folivores limit their energetic output, all the way to slothfulness. Am Nat 188:196–204
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 60:338–350
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:e68292
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 87:539–549
Petit M, Clavijo-Baquet S, Vézina F (2017) Increasing winter maximal metabolic rate improves intra-winter survival in small birds. Physiol Biochem Zool 90:166–177
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 208:1277–1285
Piersma T, van Gils J (2011) The flexible phenotype: A body-centred integration of ecology, physiology, and behavior. Oxford University Press, Oxford
Porter WP, Kearney M (2009) Size, shape and the thermal niche of endotherms. Proc Natl Acad Sci USA 106(suppl 2):19666–19672
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 89:251–261
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 181:565–573
Prinzinger R (1988) Energy metabolism, body-temperature and breathing parameters in non-torpid blue-naped mousebirds Urocolius macrourus. J Comp Physiol B 157:801–806
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 69:689–692
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 526:569–573
Raichlen DA, Gordon AD, Muchlinski MN, Snodgrass JJ (2010) Causes and significance of variation in mammalian basal metabolism. J Comp Physiol B 180:301–311
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 36:4051–4063
Rezende EL, Bacigalupe LD (2015) Thermoregulation in endotherms: physiological principles and ecological consequences. J Comp Physiol B 185:709–727
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 20:101–107
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 58:1361–1374
Ricklefs RE, Konarzewski M, Daan S (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147:1047–1071
Riddle O, Smith GC, Benedict FG (1932) The basal metabolism of the mourning dove and some of its hybrids. Am J Physiol 101:206–267
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 220:837–843
Rodríguez MA, López-Sañudo IL, Hawkins BA (2006) The geographic distribution of mammal body size in Europe. Global Ecol Biogeogr 15:173–181
Rodríguez MA, Olalla-Tárraga, Hawkins BA (2008) Bergmann’s rule and the geography of mammal body size in the Western Hemisphere. Global Ecol Biogeogr 17:274–283
Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758
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 20:1815–1822
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 30:1140–1148
Rubner M (1883) Ueber den Eifluss der Körpergrösse auf Sttoffund Kraftwechsel. Z Biol 19:535–562
Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev 90:891–926
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 157:35–40
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 59:672–681
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 63:1530–1539
Schmidt-Nielsen K (1984) Scaling. Why is animal size so important? Cambridge Univ Press, Cambridge
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 99:259–271
Scholander PF, Hock R, Walters V, Johnson F, Irving L (1950b) Heat regulation in some arctic and tropical mammals and birds. Biol Bull 99:237–258
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 20:97–104
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 13:49–51
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 204:777–784
Sheridan JA, Bickford D (2011) Shrinking body size as an ecological response to climate change. Nat Climate Change 1:401–406
Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds. Yale University Press, New Haven
Speakman JR (2005) Body size, energy metabolism and lifespan. J Exp Biol 208:1717–1730
Speakman JR, Król E (2010) Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J Anim Ecol 79:726–746
Speakman JR, Król E (2011) Limits to sustained energy intake. XIII. Recent progress and future perspectives. J Exp Biol 214:230–241
Speakman JR, Król E, Johnson MS (2004) The functional significance of individual variation in basal metabolic rate. Physiol Biochem Zool 77:900–915
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 45:426–437
Swanson DL (2010) Seasonal metabolic variation in birds: functional and mechanistic correlates. Curr Ornithol 17:75–129
Swanson DL, Bozinovic F (2011) Metabolic capacity and the evolution of biogeographic patterns in oscine and suboscine passerine birds. Physiol Biochem Zool 84:185–194
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 63:184–194
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 146:87–94
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:e34271
Tieleman BI, Williams JB, Buschur ME, Brown CR (2003) Phenotypic variation of larks along an aridity gradient: are desert birds more flexible. Ecology 84:1800–1815
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 279:129–136
van de Ven TMFN, Mzilikazi N, McKechnie AE (2013) Seasonal metabolic variation in two populations of an Afrotropical Euplectid bird. Physiol Biochem Zool 86:19–26
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 25:1864–1876
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 56:767–792
Vézina F, Williams TD (2003) Plasticity in body composition in breeding birds: what drives the metabolic costs of egg production? Physiol Biochem Zool 76:716–730
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 19:119–128
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 209:3141–3154
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 82:248–257
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 136:621–630
Walsberg GE (1990) Communal roosting in a very small bird: consequences for the thermal and respiratory environments. Condor 92:795–798
Weathers WW (1979) Climatic adaptation in avian standard metabolic rate. Oecologia 42:81–89
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 27:215–224
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:e56229
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 29:250–258
Wells ME, Schaeffer PJ (2012) Seasonality of peak metabolic rate in non-migrant tropical birds. J Avian Biol 43:481–485
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 77:929–941
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 274:287–293
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–R294
Wiersma P, Muñoz-Garcia A, Walker A, Williams JB (2007) Tropical birds have a slow pace of life. Proc Nal Acad Sci USA 104:9340–9345
Wiersma P, Nowak B, Williams JB (2012) Small organ size contributes to the slow pace of life in tropical birds. J Exp Biol 215:1662–1669
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 203:3153–3159
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 129:785–796
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 50:855–868
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 276:3695–3704
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 165:70–78
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 114:419–427
Woodley R, Buffenstein R (2002) Thermogenic changes with chronic cold exposure in the naked mole-rat (Heterocephalus glaber). Comp Biochem Physiol A 133:827–834
Yahav S, Buffenstein R (1991) Huddling behavior facilitates homeothermy in the naked mole rat Heterocephalus glaber. Physiol Zool 64:871–884
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 151:519–525
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 33:315–319
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 31:319–327
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 164:483–490
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 87:432–444
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 87:704–718
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–R336
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 37:479–484
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 113:297–309
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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.
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Swanson, D.L., McKechnie, A.E. & Vézina, F. How low can you go? An adaptive energetic framework for interpreting basal metabolic rate variation in endotherms. J Comp Physiol B 187, 1039–1056 (2017). https://doi.org/10.1007/s00360-017-1096-3
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DOI: https://doi.org/10.1007/s00360-017-1096-3