Journal of Comparative Physiology B

, Volume 178, Issue 3, pp 235–247 | Cite as

Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review



Comparative analyses of avian energetics often involve the implicit assumption that basal metabolic rate (BMR) is a fixed, taxon-specific trait. However, in most species that have been investigated, BMR exhibits phenotypic flexibility and can be reversibly adjusted over short time scales. Many non-migrants adjust BMR seasonally, with the winter BMR usually higher than the summer BMR. The data that are currently available do not, however, support the idea that the magnitude and direction of these adjustments varies consistently with body mass. Long-distance migrants often exhibit large intra-annual changes in BMR, reflecting the physiological adjustments associated with different stages of their migratory cycles. Phenotypic flexibility in BMR also represents an important component of short-term thermal acclimation under laboratory conditions, with captive birds increasing BMR when acclimated to low air temperatures and vice versa. The emerging view of avian BMR is of a highly flexible physiological trait that is continually adjusted in response to environmental factors such as temperature. The within-individual variation observed in avian BMR demands a critical re-examination of approaches used for comparisons across taxa. Several key questions concerning the shapes and other properties of avian BMR reaction norms urgently need to be addressed, and hypotheses concerning metabolic adaptation should explicitly account for phenotypic flexibility.


Acclimation Acclimatization Comparative methods Migration Reaction norm 



Basal metabolic rate


Air temperature


Body mass


Summit metabolism


Field metabolic rate


Maximal metabolic rate


Temperature at cold limit


  1. Adolph SC, Hardin JS (2007) Estimating phenotypic correlations: correcting for bias due to intraindividual variability. Funct Ecol 21:178–184Google Scholar
  2. Afik D, Caviedes-Vidal E, Martinez del Rio C, Karasov WH (1995) Dietary modulation of intestinal hydrolytic enzymes in yellow-rumped warblers. Am J Physiol 269:R413–R420PubMedGoogle Scholar
  3. Arens JR, Cooper SJ (2005) Metabolic and ventilatory acclimatization to cold stress in house sparrows (Passer domesticus). Physiol Biochem Zool 78:579–589PubMedGoogle Scholar
  4. Battley PF, Dekinga A, Dietz MW, Piersma T, Tang S, Hulsman K (2001) Basal metabolic rate declines during long-distance migratory flight in great knots. Condor 103:838–845Google Scholar
  5. Battley PF, Piersma T, Dietz MW, Tang S, Dekinga A, Hulsman K (2000) Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc R Soc Lond B 267:191–195Google Scholar
  6. Bech C, Langseth I, Gabrielsen GW (1999) Repeatability of basal metabolism in breeding female kittiwakes Rissa tridactyla. Proc R Soc Lond B 266:2161–2167Google Scholar
  7. Benedict FG, Fox EL (1927) The gaseous metabolism of large birds under aviary life. Proc Am Philos Soc 66:511–534Google Scholar
  8. Bennett PM, Harvey PH (1987) Active and resting metabolism in birds: allometry, phylogeny and ecology. J Zool Lond 213:327–363CrossRefGoogle Scholar
  9. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745PubMedGoogle Scholar
  10. Brody S, Proctor RC (1932) Growth and development, with special reference to domestic animals. XXIII. Relation between basal metabolism and mature body weight in different species of mammals and birds. Mo Univ Agric Exp Stn Res Bull 166:89–101Google Scholar
  11. Broggi J, Hohtola E, Koivula K, Orell M, Thomson RL, Nilsson J-A (2007) Sources of variation in winter basal metabolic rate in the great tit. Funct Ecol 21:528–533Google Scholar
  12. Carleton SA, Martinez del Rio C (2005) The effect of cold-induced increased metabolic rate on the rate of 13C and 15N incorporation in house sparrows (Passer domesticus). Oecologia 144:226–232PubMedGoogle Scholar
  13. Chappell MA, Bech C, Buttemer WA (1999) The relationship of central and peripheral organ masses to aerobic performance variation in house sparrows. J Exp Biol 202:2269–2279PubMedGoogle Scholar
  14. Chetty K (2006) Phenotypic flexibility in the basal metabolic rate of laughing doves (Streptopelia senegalensis) in response to short-term thermal acclimation. MSc. thesis, University of the Witwatersrand, JohannesburgGoogle Scholar
  15. Chown SL, Terblanche JS (2007) Physiological diversity in insects: ecological and evolutionary contexts. Adv Insect Physiol 33:50–152Google Scholar
  16. Cooper SJ (2000) Seasonal energetics of mountain chickadees and juniper titmice. Condor 102:635–644Google Scholar
  17. Cooper SJ, Swanson DL (1994) Seasonal acclimatization of thermoregulation in the black-capped chickadee. Condor 96:638–646Google Scholar
  18. Cossins AR, Bowler K (1987) Temperature biology of animals. Chapman and Hall, LondonGoogle Scholar
  19. Daan S, Masman D, Groenewold A (1990) Avian basal metabolic rates: their association with body compostition and energy expenditure in nature. Am J Physiol 259:R333–R340PubMedGoogle Scholar
  20. Davydov AF (1972) Seasonal variations in the energy metabolism and thermoregulation at rest in the black-headed gull. Sov J Ecol 2:436–439Google Scholar
  21. Dawson WR (2003) Plasticity in avian responses to thermal challenges— an essay in honor of Jacob Marder. Isr J Zool 49:95–109Google Scholar
  22. Dawson WR, Buttemer WA, Carey C (1985) A reexamination of the metabolic response of house finches to temperature. Condor 87:424–427Google Scholar
  23. Dawson WR, Carey C (1976) Seasonal acclimation to temperature in Cardueline finches. J Comp Physiol 112:317–333Google Scholar
  24. Dawson WR, Whittow GC (2000) Regulation of body temperature. In: Sturkie PD (ed) Avian physiology. Academic, New York, pp 343–390Google Scholar
  25. Dietz MW, Piersma T, Dekinga A (1999) Body-building without power training: endogenously regulated pectoral muscle hypertrophy in confined shorebirds. J Exp Biol 202:2831–2837PubMedGoogle Scholar
  26. Ellis HI (1984) Energetics of free-ranging seabirds. In: Whittow GC, Rahn H (eds) Seabird energetics. Plenum, New YorkGoogle Scholar
  27. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726PubMedGoogle Scholar
  28. Garland T, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer simulation. System Biol 42:265–292Google Scholar
  29. Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. System Biol 41:18–32Google Scholar
  30. Garland T, Ives AR (2000) Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155:346–364Google Scholar
  31. Gelineo S (1964) Organ systems in adaptation: the temperature regulating system. In: Dill DB (ed) Handbook of physiology, Section 4, Adaptation to the environment. American Physiological Society, Washington DCGoogle Scholar
  32. Gelineo S (1969) Heat production in birds in summer and winter. Srpska Akad. Nauka I Umetnosti Belgrad, Bull Classe Sci Math Sci Nat 12:99–105Google Scholar
  33. Giaja J, Males B (1928) Sur la valeur du métabolisme de base de quelques animaux en fonction de leur surface. Annales de Physiologie et de Physicochimie Biologique 4:875–904Google Scholar
  34. Hammond KA, Chappell MA, Cardullo RA, Lin R-I, Johnsen TS (2000) The mechanistic basis of aerobic performance variation in red junglefowl. J Exp Biol 203:2053–2064PubMedGoogle Scholar
  35. Hart JS (1962) Seasonal acclimatization in four species of small wild birds. Physiol Zool 35:224–236Google Scholar
  36. Haugen MJ, Tieleman BI, Williams JB (2003) Phenotypic flexibility in cutaneous water loss and lipids of the stratum corneum. J Exp Biol 206:3581–3588PubMedGoogle Scholar
  37. Hayworth AM, Weathers WW (1984) Temperature regulation and climatic adaptation in black-billed and yellow-billed magpies. Condor 86:19–26Google Scholar
  38. Hissa R, Palonkangas R (1970) Thermoregulation in the titmouse (Parus major L.). Comp Biochem Physiol 33:941–953Google Scholar
  39. Hoffman TCM, Walsberg GE (1999) Inhibiting ventilatory evaporation produces an adaptive increase in cutaneous evaporation in mourning doves Zenaida macroura. J Exp Biol 202:3021–3028PubMedGoogle Scholar
  40. Irving L, Krog H, Monson M (1955) The metabolism of some Alaskan animals in winter and summer. Physiol Zool 28:173–185Google Scholar
  41. Ives AR, Midford PE, Garland T (2007) Within-species variation and measurement error in phylogenetic comparative methods. System Biol 56:252–270Google Scholar
  42. Karasov WH (1996) Digestive plasticity in avian energetics and feeding ecology. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman and Hall, New York, pp 61–84Google Scholar
  43. Karasov WH, Pinshow B (1998) Changes in lean mass and in organs of nutrient assimilation in a long-distance passerine migrant at a spring stopover site. Physiol Biochem Zool 71:435–448CrossRefGoogle Scholar
  44. Kersten M, Bruinzeel LW, Wiersma P, Piersma T (1998) Reduced basal metabolic rate of migratory waders wintering in coastal Africa. Ardea 86:71–80Google Scholar
  45. Klaassen M, Biebach H (1994) Energetics of fattening and starvation in the long-distance migratory garden warbler, Sylvia borin, during the migratory phase. J Comp Physiol B 164:362–371Google Scholar
  46. Klaassen M, Oltrogge M, Trost L (2004) Basal metabolic rate, food intake, and body mass in cold- and warm-acclimated garden warblers. Comp Biochem Physiol A 137:639–647Google Scholar
  47. Kvist A, Lindström Å (2001) Basal metabolic rate in migratory waders: intra-individual, intraspecific, interspecific and seasonal variation. Funct Ecol 15:465–473Google Scholar
  48. Lasiewski RC, Dawson WR (1967) A re-examination of the relation between standard metabolic rate and body weight in birds. Condor 69:13–23Google Scholar
  49. Levey DJ, Place AR, Rey PJ, Martinez del Rio C (1999) An experimental test of dietary enzyme modulation in pine warblers Dendroica pinus . Physiol Biochem Zool 72:576–587PubMedGoogle Scholar
  50. Liknes ET, Scott SM, Swanson DL (2002) Seasonal acclimatization in the American goldfinch revisited: to what extent do metabolic rates vary seasonally? Condor 104:548–557Google Scholar
  51. Liknes ET, Swanson DL (1996) Seasonal variation in cold tolerance, basal metabolic rate, and maximal capacity for thermogenesis in white-breasted nuthatches Sitta carolinensis and downy woodpeckers Picoides pubescens, two unrelated arboreal temperate residents. J Avian Biol 27:279–288Google Scholar
  52. Lindström Å (1997) Basal metabolic rates of migrating waders in the Eurasian Arctic. J Avian Biol 28:87–92Google Scholar
  53. Lindström Å, Klaassen M (2003) High basal metabolic rates of shorebirds while in the Arctic: a circumpolar view. Condor 105:420–427Google Scholar
  54. Lindström Å, Klaassen M, Kvist A (1999) Variation in energy intake and basal metabolic rate of a bird migrating in a wind tunnel. Funct Ecol 13:352–359Google Scholar
  55. Maddocks TA, Geiser F (2000) Seasonal variations in thermal energetics of Australian silvereyes (Zosterops lateralis). J Zool Lond 252:327–333Google Scholar
  56. Marder J, Arieli U (1988) Heat balance of acclimated pigeons Columba livia exposed to temperatures of up to 60°C T a. Comp Biochem Physiol 91A:165–170Google Scholar
  57. Martinez del Rio C, Brugger KW, Rios JL, Vergara ME, Witmer MC (1995) An experimental and comparative study of dietary modulation of intestinal enzymes in the European starling. Physiol Zool 68:490–511Google Scholar
  58. Martins EP, Hansen TF (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149:646–667Google Scholar
  59. McKechnie AE, Chetty K, Lovegrove BG (2007) Phenotypic flexibility in basal metabolic rate in laughing doves: responses to short-term thermal acclimation. J Exp Biol 210:97–106PubMedGoogle Scholar
  60. McKechnie AE, Freckleton RP, Jetz W (2006) Phenotypic plasticity in the scaling of avian basal metabolic rate. Proc R Soc Lond B 273:931–937Google Scholar
  61. McKechnie AE, Lovegrove BG (2001) Thermoregulation and the energetic significance of clustering behavior in the white-backed mousebird (Colius colius). Physiol Biochem Zool 74:238–249PubMedGoogle Scholar
  62. McKechnie AE, Lovegrove BG (2003) Facultative hypothermic responses in an Afrotropical arid-zone passerine, the red-headed finch (Amadina erythrocephala). J Comp Physiol B 173:339–346PubMedGoogle Scholar
  63. McKechnie AE, Wolf BO (2004a) The allometry of avian basal metabolic rate: good predictions need good data. Physiol Biochem Zool 77:502–521PubMedGoogle Scholar
  64. McKechnie AE, Wolf BO (2004b) Partitioning of evaporative water loss in white-winged doves: plasticity in response to short-term thermal acclimation. J Exp Biol 207:203–210PubMedGoogle Scholar
  65. McNab BK (1988) Food habits and the basal rate of metabolism in birds. Oecologia 77:343–349Google Scholar
  66. McNab BK (1997) On the utility of uniformity in the definition of basal rates of metabolism. Physiol Zool 70:718–720PubMedGoogle Scholar
  67. McNab BK (2001) Energetics of toucans, barbets and a hornbill: implications for avian frugivory. Auk 118:916–933Google Scholar
  68. McNab BK (2003) Ecology shapes bird bioenergetics. Nature 426:620–621PubMedGoogle Scholar
  69. McNab BK (2005) Food habits and the evolution of energetics in birds of paradise (Paradisaeidae). J Compar Physiol B 175:117–132Google Scholar
  70. Merola-Zwartjes M, Ligon JD (2000) Ecological energetics of the Puerto Rican tody: heterothermy, torpor and intra-island variation. Ecology 81:990–1002CrossRefGoogle Scholar
  71. Nagy KA (1987) Field metabolic rate and food requirement scaling in mammals and birds. Ecol Monogr 57:111–128Google Scholar
  72. O’Conner TP (1995) Metabolic characteristics and body composition in house finches: effects of seasonal acclimatization. J Compar Physiol B 165:298–305Google Scholar
  73. Pagel M (1994) Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc R Soc Lond B 255:37–45Google Scholar
  74. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884PubMedGoogle Scholar
  75. Piersma T (2002) Energetic bottlenecks and other design constraints in avian annual cycles. Integr Compar Biol 42:51–67Google Scholar
  76. Piersma T, Cadée N, Daan S (1995) Seasonality in basal metabolic rate and thermal conductance in a long distance migrant shorebird, the knot (Calidris canutus). J Compar Physiol 165:37–45Google Scholar
  77. Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233Google Scholar
  78. Piersma T, Gessaman JA, Dekinga A, Visser GH (2004) Gizzard and other lean mass components increase, yet basal metabolic rates decrease, when red knots Calidris canutus are shifted from soft to hard-shelled food. J Avian Biol 35:99–104Google Scholar
  79. Piersma T, Lindström A (1997) Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol Evol 12:134–138Google Scholar
  80. Pohl H (1971) Seasonal variation in metabolic functions of bramblings. Ibis 113:185–193Google Scholar
  81. Pohl H, West GC (1973) Daily and seasonal variation in metabolic response to cold during rest and exercise in the common redpoll. Comp Biochem Physiol 45A:851–867Google Scholar
  82. Precht H (1973) Limiting temperatures of life functions. In: Precht H, Christophersen J, Hensel H, Larcher W (eds) Temperature and life. Spinger, Berlin, pp 400–440Google Scholar
  83. Prosser CL (1973) Comparative animal physiology. Saunders, PhiladelphiaGoogle Scholar
  84. Reynolds PS, Lee RM (1996) Phylogenetic analysis of avian energetics: passerines and non-passerines do not differ. Am Nat 147:735–759Google Scholar
  85. 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 205:101–107PubMedGoogle Scholar
  86. Ricklefs RE, Konarzewski M, Daan S (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147:1047–1071Google Scholar
  87. Riddle O, Smith GC, Benedict FG (1934) Seasonal and temperature factors and their determination in pigeons of percentage metabolism change per degree of temperature change. Am J Physiol 107Google Scholar
  88. Rising JD, Hudson JW (1974) Seasonal variation in the metabolism and thyroid activity of the black-capped chickadee (Parus atricapillus). Condor 76:198–203Google Scholar
  89. Rønning B, Moe B, Bech C (2005) Long-term repeatability makes basal metabolic rate a likely heritable trait in the zebra finch Taeniopygia guttata. J Exp Biol 208:4663–4669PubMedGoogle Scholar
  90. Saarela S, Hohtola E (2003) Seasonal thermal acclimatization in sedentary and active pigeons. Isr J Zool 49:185–193Google Scholar
  91. Saarela S, Klapper B, Heldmaier G (1988) Thermogenic capacity of greenfinches and siskins in winter and summer. In: Bech C, Reinertsen RE (eds) Physiology of cold adaptation in birds. Plenum, New York, pp 115–122Google Scholar
  92. Schleucher E, Withers PC (2001) Re-evaluation of the allometry of wet thermal conductance for birds. Comp Biochem Physiol A 129:821–827Google Scholar
  93. Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer Associates, SunderlandGoogle Scholar
  94. Sharbaugh SM (2001) Seasonal acclimatization to extreme climatic conditions by black-capped chickadees (Poecile atricapilla) in interior Alaska (64°N). Physiol Biochem Zool 74:568–575PubMedGoogle Scholar
  95. Southwick EE (1980) Seasonal thermoregulatory adjustments in white-crowned sparrows. Auk 97:76–85Google Scholar
  96. Swanson DL (1990) Seasonal variation in cold hardiness and peak rates of cold-induced thermogenesis in the dark-eyed junco (Junco hyemalis). Auk 107:561–566Google Scholar
  97. Swanson DL (1991) Seasonal adjustments in metabolism and insulation in the dark-eyed junco. Condor 93:538–545Google Scholar
  98. Swanson DL (2007) Seasonal metabolic variation in birds: functional and mechanistic correlates. In: Curr Ornithol, vol 17 (in press)Google Scholar
  99. Swanson DL, Dean KL (1999) Migration-induced variation in thermogenic capacity in migratory passerines. J Avian Biol 30:245–254Google Scholar
  100. Swanson DL, Olmstead KL (1999) Evidence for a proximate influence of winter temperatures on metabolism in passerine birds. Physiol Biochem Zool 72:566–575PubMedGoogle Scholar
  101. Swanson DL, Weinacht DP (1997) Seasonal effects on metabolism and thermoregulation in northern bobwhite. Condor 99:478–489Google Scholar
  102. Terblanche JS, Janion C, Chown SL (2007) Variation in scorpion metabolic rate and rate–temperature relationships: implications for the fundamental equation of the metabolic theory of ecology. J Evol Biol 20:1602–1612PubMedGoogle Scholar
  103. Terroine EF, Trautmann S (1927) Influence de la température extérieure sur la production calorique des Homéothermes et loi des surfaces. Annales de Physiologie et de Physicochimie Biologique 3:422–457Google Scholar
  104. Tieleman BI, Williams JB (2000) The adjustment of avian metabolic rates and water fluxes to desert environments. Physiol Biochem Zool 73:461–479PubMedGoogle Scholar
  105. Tieleman BI, Williams JB, Buschur ME, Brown CR (2003) Phenotypic variation of larks along an aridity gradient: are desert birds more flexible? Ecology 84:1800–1815Google Scholar
  106. Tieleman BI, Williams JB, Visser GH (2004) Energy and water budgets of larks in a life history perspective: parental effort varies with aridity. Ecology 85:1399–1410Google Scholar
  107. Veghte JH (1964) Thermal and metabolic responses of the gray jay to cold stress. Physiol Zool 37:316–328Google Scholar
  108. Veghte JH (1975) Thermal exchange between the raven (Corvus corax) and its environment. PhD. Thesis, University of Michigan, Ann ArborGoogle Scholar
  109. Vezina F, Jalvingh K, 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 209:3141–3154PubMedGoogle Scholar
  110. Vézina F, Williams TD (2005) Interaction 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 19:119–128Google Scholar
  111. Wallgren H (1954) Energy metabolism of two species of Emberiza. Acta Zoologica Fennica 84:5–110Google Scholar
  112. Weathers WW (1979) Climatic adaptation in avian standard metabolic rate. Oecologia 42:81–89Google Scholar
  113. Weathers WW, Caccamise DF (1978) Seasonal acclimatization to temperature in monk parakeets. Oecologia 35:173–183Google Scholar
  114. Weathers WW, Sullivan KA (1993) Seasonal patterns of time and energy allocation by birds. Physiol Zool 66:511–536Google Scholar
  115. West GC (1972a) The effect of acclimation and acclimatization on the resting metabolic rate of the common redpoll. Comp Biochem Physiol 43A:293–310Google Scholar
  116. West GC (1972b) Seasonal differences in resting metabolic rate of Alaskan ptarmigan. Comp Biochem Physiol A 41:867–876Google Scholar
  117. White CR, Blackburn TM, Martin GR, Butler PJ (2007) The basal metabolic rate of birds is associated with habitat temperature and precipitation, not productivity. Proc R Soc B 274:287–293PubMedGoogle Scholar
  118. 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 77:929–941PubMedGoogle Scholar
  119. Wiersma P, Muñoz-Garcia A, Walker A, Williams JB (2007) Tropical birds have a slow pace of life. Proc Natl Acad Sci USA 104:9340–9345PubMedGoogle Scholar
  120. Wijnandts H (1984) Ecological energetics of the long-eared owl (Asio otus). Ardea 72:1–92Google Scholar
  121. Wikelski M, Spinney L, Schelsky W, Scheuerlein A, Gwinner E (2003) Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes. Proc R Soc Lond B 270:2383–2388Google Scholar
  122. 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

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.DST/NRF Centre of Excellence at the Percy FitzPatrick Institute, School of Animal, Plant and Environmental SciencesUniversity of the WitwatersrandJohannesburgSouth Africa

Personalised recommendations