Seasonal Metabolic Variation in Birds: Functional and Mechanistic Correlates

Part of the Current Ornithology book series (CUOR, volume 17)


The influence of seasonal changes in temperature and climate on metabolic rates in birds has been a topic of interest to ornithologists and ecophysiologists for decades (e.g., Hart 1962; Dawson 1958; Miller 1939). Because metabolic rates increase linearly with temperature in endotherms outside the thermal neutral zone, comparisons of metabolic rates among seasons or species require standardized measurements of metabolic rates. The most common of these standardized metabolic rates used for comparisons of energetics among seasons or species is basal, or resting, metabolic rate. It often serves as a baseline for comparisons of metabolic costs of activities within species, and for comparisons of the “rate of living” among species or species groups (e.g., Wiersma et al. 2007a; White et al. 2007; McKechnie et al. 2006; McKechnie and Wolf 2004; Trevelyan et al. 1990; McNab 1988; Bennett and Harvey 1987; Kersten and Piersma 1987). Theoretically, basal metabolic rate (BMR) is the minimum metabolic rate required for maintenance in endotherms. BMR is measured within the thermal neutral zone under postabsorptive digestive conditions during the resting phase of the daily cycle on resting, nongrowing, nonreproductive animals (McNab 1997). It is doubtful whether truly BMRs can ever be achieved in the laboratory, so the term resting metabolic rate (RMR) is often used to refer to such measurements, even when the standard conditions for BMR have been met. Here, I will revert to the standard terminology and consider BMR as the metabolic rate measured under the standard conditions listed above, recognizing that this may not, in fact, represent truly basal rates.


Cold Tolerance Basal Metabolic Rate Rest Metabolic Rate House Sparrow Metabolic Intensity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



I thank Eric Liknes, Theunis Piersma, and an anonymous reviewer for comments that improved an earlier version of this manuscript. I also thank Eric Liknes for help with constructing some of the figures.


  1. Abumrad N, Coburn C, Ibrahimi A (1999) Membrane proteins implicated in long-chain fatty acid uptake by mammalian cells: CD36, FATP and FABPm. Biochim Biophys Acta 1441:4–13PubMedGoogle Scholar
  2. Ambrose SJ, Bradshaw SD (1988) Seasonal changes in standard metabolic rates in the White-browed Scrubwren Sericornis frontalis (Acanthizidae) from arid, semi-arid, and mesic ­environments. Comp Biochem Physiol 89A:79–83Google Scholar
  3. Anava A, Kam M, Shkolnik A, Degen AA (2000) Seasonal field metabolic rate and dietary intake in Arabian Babblers (Turdoides squamiceps) inhabiting extreme deserts. Functional Ecol 14:607–613Google Scholar
  4. Anava A, Kam M, Shkolnik A, Degen AA (2002) Seasonal daily, daytime and night-time field metabolic rates in Arabian Babblers. J Exp Biol 205:3571–3575PubMedGoogle Scholar
  5. Anderson CL, Kabalka GW, Layne DG, Dyke JP, Burghardt GM (2000) Noninvasive high field MRI brain imaging of the Garter Snake (Thamnophis sirtalis). Copeia 2000:265–269Google Scholar
  6. Arens JR, Cooper SJ (2005a) Metabolic and ventilatory acclimatization to cold stress in House Sparrows (Passer domesticus). Physiol Biochem Zool 78:579–589PubMedGoogle Scholar
  7. Arens JR, Cooper SJ (2005b) Seasonal and diurnal variation in metabolism and ventilation in House Sparrows. Condor 107:433–444Google Scholar
  8. Aulie A, Tøien O (1988) Threshold for shivering in aerobic and anaerobic muscles in bantam cocks and incubating hens. J Comp Physiol B 158:431–435PubMedGoogle Scholar
  9. Baggott GK (1975) Moult, flight muscle “hypertrophy” and premigratory lipid deposition of the juvenile Willow Warbler, Phylloscopus trochilus. J Zool Lond 175:299–314Google Scholar
  10. Barré H, Bailly L, Rouanet JL (1987) Increased oxidative capacity in skeletal muscles from cold acclimated ducklings: a comparison with rats. Comp Biochem Physiol 88B:519–522Google Scholar
  11. 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
  12. Battley PF, Dietz MW, Piersma T, Dekinga A, Tang S, Julsman K (2001) Is long-distance bird flight equivalent to a high-energy fast? Body composition changes in freely migrating and captive fasting Great Knots. Physiol Biochem Zool 74:435–449PubMedGoogle Scholar
  13. Bauchinger U, Wohlmann A, Biebach H (2005) Flexible remodeling of organ size during spring migration of the Garden Warbler (Sylvia borin). Zoology 108:97–106PubMedGoogle Scholar
  14. Bech C, Ostnes JE (1999) Influence of body composition on the metabolic rate of nestling European Shags (Phalacrocorax aristotelis). J Comp Physiol B 169:263–270Google Scholar
  15. Bech C, Præstang KE (2004) Thermoregulatory use of heat increment of feeding in the Tawny Owl (Strix aluco). J Therm Biol 29:649–654Google Scholar
  16. Bennett AF (1991) The evolution of activity capacity. J Exp Biol 160:1–23PubMedGoogle Scholar
  17. Bennett PM, Harvey PH (1987) Active and resting metabolism in birds: allometry, phylogeny and ecology. J Zool Lond 213:327–363Google Scholar
  18. Biebach H (1998) Phenotypic organ flexibility in Garden Warblers Sylvia borin during long-­distance migration. J Avian Biol 29:529–535Google Scholar
  19. Bishop CM, Butler PJ (1995) Physiological modelling of oxygen consumption in birds during flight. J Exp Biol 198:2153–2163PubMedGoogle Scholar
  20. Blem CR, Blem LB (2006) Variation in mass of female Prothonotary Warblers during nesting. Wilson J Ornithol 118:3–12Google Scholar
  21. Bonen A, Campbell SE, Benton CR, Chabowski A, Coort SLM, Han X-X, Koonen DPY, Glatz JFC, Luiken JJFP (2004) Regulation of fatty acid transport by fatty acid translocase/CD36, Proc. Nutr Soc 63:245–249Google Scholar
  22. Bordel R, Haase E (1993) Effects of flight on blood parameters in homing pigeons. J Comp Physiol B 163:219–224Google Scholar
  23. Brackenbury J (1984) Physiological responses of birds to flight and running. Biol Rev 59:559–575PubMedGoogle Scholar
  24. Breuer K, Lill A, Baldwin J (1995) Haematological and body-mass changes of small passerines overwintering in south-eastern Australia. Aust J Zool 43:31–38Google Scholar
  25. Brigham RM (1992) Daily torpor in a free-ranging goatsucker, the Common Poorwill (Phalaenoptilus nuttallii). Physiol Zool 65:457–472Google Scholar
  26. Brigham RM, Trayhurn P (1994) Brown fat in birds? A test for the mammalian BAT-specific mitochondrial uncoupling protein in Common Poorwills. Condor 96:208–211Google Scholar
  27. Brigham RM, Woods CP, Lane JE, Fletcher QE, Geiser F (2006) Ecological correlates of torpor use among five caprimulgiform birds. Acta Zoologica Sinica 52 (suppl):401–404Google Scholar
  28. 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
  29. Bruinzeel LW, Piersma T (1998) Cost reduction in the cold: heat generated by terrestrial locomotion partly substitutes for thermoregulation costs in Knot Calidris canutus. Ibis 140:323–328Google Scholar
  30. Bryant DM (1988) Energy expenditure and body mass changes as measures of reproductive costs in birds. Funct Ecol 2:23–34Google Scholar
  31. Bundle MW, Hoppeler H, Vock R, Tester JM, Weyand PG (1999) High metabolic rates in running birds. Nature 397:31–32Google Scholar
  32. Burness GP, Ydenberg RC, Hochachka PW (1998) Interindividual variability in body composition and resting oxygen consumption rate in breeding Tree Swallows, Tachycineta bicolor. Physiol Zool 71:247–256PubMedGoogle Scholar
  33. Butler PJ, Turner DL (1988) Effect of training on maximal oxygen uptake and aerobic capacity of locomotory muscles in Tufted Ducks, Aythya fuligula. J Physiol 401:347–359PubMedGoogle Scholar
  34. Campbell SE, Tandon NN, Woldegiorgis G, Luiken JJFP, Glatz JFC, Bonen A (2004) A novel function for fatty acid translocase (FAT)/CD36. J Biol Chem 35:36235–36241Google Scholar
  35. Carey C, Dawson WR, Maxwell LC, Faulkner JA (1978) Seasonal acclimatization to temperature in cardueline finches. II. Changes in body composition and mass in relation to season and acute cold stress. J Comp Physiol 125:101–113Google Scholar
  36. Carey C, Marsh RL, Bekoff A, Johnston RM, Olin AM (1989) Enzyme activities in muscles of seasonally acclimatized House Finches. In: Bech C, Reinertsen RE (eds) Physiology of cold adaptation in birds. Plenum Life Sciences, New York, pp 95–104Google Scholar
  37. Cavieres G, Sabat P (2008) Geographic variation in the response to thermal acclimation in Rufous-collared Sparrows: are physiological flexibility and environmental heterogeneity ­correlated? Funct Ecol 22:509–515Google Scholar
  38. Chai P, Dudley R (1995) Limits to vertebrate locomotor energetics suggested by hummingbirds hovering in heliox. Nature 377:722–725Google Scholar
  39. Chai P, Dudley R (1996) Limits to flight energetics of hummingbirds hovering in hypodense and hypoxic gas mixtures. J Exp Biol 199:2285–2295PubMedGoogle Scholar
  40. Chai P, Chang AC, Dudley R (1998) Flight thermogenesis and energy conservation in hovering hummingbirds. J Exp Biol 201:963–968PubMedGoogle Scholar
  41. Chappell MA, Bachman GC, Hammond KA (1997) The heat increment of feeding in House Wren chicks: magnitude, duration, and substitution for thermostatic costs. J Comp Physiol B 167:313–318Google Scholar
  42. 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
  43. Chastel O, Kersten M (2002) Brood size and body condition in the House Sparrow Passer domesticus: the influence of brooding behavior. Ibis 144:284–292Google Scholar
  44. Cichon M (2001) Body-mass changes in female Collared Flycatchers: state-dependent strategy. Auk 118:550–552Google Scholar
  45. Collin A, Buyse J, Van As P, Darras VM, Malheiros RD, Moraes VMB, Reyns GE, Taouis M, Decuypere E (2003a) Cold-induced enhancement of avian uncoupling protein expression, heat production, and triiodothyronine concentrations in broiler chicks. Gen Comp Endocrinol 130:70–77PubMedGoogle Scholar
  46. Collin A, Taouis M, Buyse J, Ifuta NB, Darras VM, Van As P, Malheiros RD, Moraes VMB, Decuypere E (2003b) Thyroid status, but not insulin status, affects expression of avian uncoupling protein mRNA in chicken. Am J Physiol Endocrinol Metab 284:E771–E777PubMedGoogle Scholar
  47. Conley KE, Weibel ER, Taylor CR, Hoppeler H (1985) Aerobic capacity estimated by exercise vs cold exposure: endurance training effects in rats. Respir Physiol 62:273–280PubMedGoogle Scholar
  48. Cooper SJ (2000) Seasonal energetics of Mountain Chickadees and Juniper Titmice. Condor 102:635–644Google Scholar
  49. Cooper SJ (2002) Seasonal metabolic acclimatization in Mountain Chickadees and Juniper Titmice. Physiol Biochem Zool 74:386–395Google Scholar
  50. Cooper SJ, Same DR (2000) Ventilatory accommodation under cold stress in seasonally acclimatized Black-capped Chickadees. Am Zool 40:980AGoogle Scholar
  51. Cooper SJ, Sonsthagen S (2007) Heat production from foraging activity contributes to thermoregulation in Black-capped Chickadees. Condor 109:446–451Google Scholar
  52. Cooper SJ, Swanson DL (1994) Seasonal acclimatization of thermoregulation in the Black-capped Chickadee. Condor 96:638–646Google Scholar
  53. Cottam M, Houston D, Lobley G, Hamilton I (2002) The use of muscle protein for egg production in the Zebra Finch Taeniopygia guttata. Ibis 144:210–217Google Scholar
  54. Croll DA, Gaston AJ, Noble DG (1991) Adaptive loss of mass in Thick-billed Murres. Condor 93:496–502Google Scholar
  55. Daan S, Masman D, Groenewold A (1990) Avian basal metabolic rates: their association with body composition and energy expenditure in nature. Am J Physiol 259:R333–R340PubMedGoogle Scholar
  56. Dawson WR (1958) Relation of oxygen consumption and evaporative water loss to temperature in the cardinal. Physiol Zool 31:37–48Google Scholar
  57. Dawson WR, Carey C (1976) Seasonal acclimatization to temperature in cardueline finches. I. insulative and metabolic adjustments. J Comp Physiol 112:317–333Google Scholar
  58. 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 83–94Google Scholar
  59. 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 85–124Google Scholar
  60. Dawson WR, Smith BK (1986) Metabolic acclimatization in the American Goldfinch (Carduelis tristis). In: Heller HC, Musacchia XJ, Wang LCH (eds) Living in the cold: physiological and biochemical adaptations. Elsevier, New York, pp 427–437Google Scholar
  61. Dawson WR, Marsh RL, Yacoe ME (1983a) Metabolic adjustments of small passerine birds for migration and cold. Am J Physiol 245:R755–R767PubMedGoogle Scholar
  62. Dawson WR, Marsh RL, Buttemer WA, Carey C (1983b) Seasonal and geographic variation of cold resistance in house finches. Physiol Zool 56:353–369Google Scholar
  63. deGraw WA, Kern MD, King JR (1979) Seasonal changes in the blood composition of captive and free-living White-crowned Sparrows. J Comp Physiol B 129:151–162Google Scholar
  64. Dietz MW, Piersma T, Dekinga A (1999a) Body-building without power training: endogenously regulated pectoral muscle hypertrophy in confined shorebirds. J Exp Biol 202:2831–2837PubMedGoogle Scholar
  65. Dietz MW, Dekinga A, Piersma T, Verhulst S (1999b) Estimating organ size in small migrating shorebirds with ultrasonography: an intercalibration exercise. Physiol Biochem Zool 72:28–37PubMedGoogle Scholar
  66. Doherty PF Jr, Williams JB, Grubb TC Jr (2001) Field metabolism and water flux of Carolina Chickadees during breeding and nonbreeding seasons: a test of the “peak-demand” and ­“reallocation” hypotheses. Condor 103:370–375Google Scholar
  67. Driedzic WR, Crowe HL, Hicklin PW, Sephton DH (1993) Adaptations of pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in Semipalmated Sandpipers (Calidris pusilla). Can J Zool 71:1602–1608Google Scholar
  68. Duchamp C, Barre H (1993) Skeletal muscle as the major site of nonshivering thermogenesis in cold-acclimated ducklings. Am J Physiol 265:R1076–R1083PubMedGoogle Scholar
  69. Duchamp C, Cohen-Adad F, Rouanet J-L, Dumonteil E, Barre H (1993) Existence of nonshivering thermogenesis in birds. In: Carey C, Florant GL, Wunder BA, Horwitz B (eds) Life in the cold: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, Colorado, pp 529–533Google Scholar
  70. Dutenhoffer MS, Swanson DL (1996) Relationship of basal to summit metabolic rate in passerine birds and the aerobic capacity model for the evolution of endothermy. Physiol Zool 69:1232–1254Google Scholar
  71. Dykstra CR, Karasov WH (1992) Changes in gut structure and function of House Wrens (Troglodytes aedon) in response to increased energy demands. Physiol Zool 65:422–442Google Scholar
  72. Ellegren H (1993) Speed of migration and migratory flight lengths of passerine birds ringed during autumn migration in Sweden. Ornis Scand 24:220–228Google Scholar
  73. Ellis HI (1984) Energetics of free-ranging seabirds. In: Whittow GC, Rahn H (eds) Seabird energetics. Plenum, New York, pp 203–234Google Scholar
  74. Emre Y, Hurtaud C, Ricquier D, Bouillaud F, Hughes J, Criscuolo F (2007) Avian UCP: the killjoy in the evolution of the mitochondrial uncoupling proteins. J Mol Evol 65:392–402PubMedGoogle Scholar
  75. Evans PR, Davidson NC, Uttley JD, Evans RD (1992) Premigratory hypertrophy of flight muscles: an ultrastructural study. Ornis Scand 23:238–243Google Scholar
  76. Fair J, Whitaker S, Pearson B (2007) Sources of variation in haematocrit in birds. Ibis 149:535–552Google Scholar
  77. Fenna L, Boag DA (1974) Adaptive significance of the caeca in Japanese Quail and Spruce Grouse (Galliformes). Can J Zool 52:1577–1584PubMedGoogle Scholar
  78. Fransson T (1995) Timing and speed of migration in North and West European populations of Sylvia warblers. J Avian Biol 26:39–48Google Scholar
  79. Freed LM (1981) Loss of mass in breeding wrens: stress or adaptation? Ecology 62:1179–1186Google Scholar
  80. French AR (1993) Hibernation in birds: comparisons with mammals. In: Carey C, Florant GL, Wunder BA, Horwitz B (eds) Life in the cold: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, Colorado, pp 43–53Google Scholar
  81. Fry CH, Ferguson-Lees IJ, Dowsett RJ (1972) Flight muscle hypertrophy and ecophysiological variation of Yellow Wagtail Motacilla flava races at Lake Chad. J Zool 167:293–306Google Scholar
  82. Fyhn M, Gabrielsen GW, Nordøy ES, Moe B, Langseth I, Bech C (2001) Individual variation in field metabolic rate of kittiwakes (Rissa tridactyla) during the chick-rearing period. Physiol Biochem Zool 74:343–355PubMedGoogle Scholar
  83. Gannes LZ, Hatch KA, Pinshow B (2001) How does time since feeding affect the fuels pigeons use during flight? Physiol Biochem Zool 74:1–10PubMedGoogle Scholar
  84. Gaunt AS, Hikida RS, Jehl JR Jr, Fenbert L (1990) Rapid atrophy and hypertrophy of an avian flight muscle. Auk 107:649–659Google Scholar
  85. 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, D.C., pp 259–282Google Scholar
  86. George JC, Vallyathan NV (1964) Lipase and succinic dehydrogenase activity of the particulate fractions of the breast muscle homogenate of the migratory starling Sturnus roseus in the pre-migratory and post-migratory periods. Can J Physiol Pharmacol 42:447–452PubMedGoogle Scholar
  87. Gessaman JA, Nagy KA (1988) Transmitter loads affect the flight speed and metabolism of homing pigeons. Condor 90:662–668Google Scholar
  88. Gessaman JA, Workman GW, Fuller MR (1991) Flight performance, energetics and water turnover of Tippler Pigeons with a harness and dorsal load. Condor 93:546–554Google Scholar
  89. Goldstein DL (1990) Energetics of activity and free living in birds. Stud Avian Biol 13:423–426Google Scholar
  90. Golet GH, Irons DB (1999) Raising young reduces body condition and fat stores in Black-legged Kittiwakes. Oecologia 120:530–538Google Scholar
  91. Guglielmo CG, Williams TD (2002) Phenotypic flexibility of body composition in relation to migratory state, age and sex in the Western Sandpiper (Calidris mauri). Physiol Biochem Zool 76:84–98Google Scholar
  92. Guglielmo CG, Haunerland NH, Williams TD (1998) Fatty acid binding protein, a major protein in the flight muscle of migrating Western Sandpipers. Comp Biochem Physiol B 119:549–555PubMedGoogle Scholar
  93. Guglielmo CG, Haunerland NH, Hochachka PW, Williams TD (2002) Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird. Am J Physiol 282:R1405–R1413Google Scholar
  94. Gwinner E (ed) (1990) Bird migration: physiology and ecophysiology. Springer, BerlinGoogle Scholar
  95. Hagan JM, Lloyd-Evans TL, Atwood JL (1991) The relationship between latitude and the timing of spring migration of North American landbirds. Ornis Scand 22:129–136Google Scholar
  96. Hails CJ (1983) The metabolic rate of tropical birds. Condor 85:61–65Google Scholar
  97. 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
  98. Harms SJ, Hickson RC (1983) Skeletal muscle mitochondria and myoglobin, endurance, and intensity of training. J Appl Physiol 54:798–802PubMedGoogle Scholar
  99. Harri M, Dannenberg T, Oksanen-Rossi R, Hohtola E, Sundin U (1984) Related and unrelated changes in response to exercise and cold in rats: a reevaluation. J Appl Physiol 57:1489–1497PubMedGoogle Scholar
  100. Hart JS (1962) Seasonal acclimatization in four species of small wild birds. Physiol Zool 35:224–236Google Scholar
  101. Hartman FA (1961) Locomotor mechanisms of birds. Smithsonian Misc Coll 143:1–91Google Scholar
  102. Hawkins PAJ, Butler PJ, Woakes AJ, Gabrielsen GW (1997) Heat increment of feeding in Brunnich’s Guillemot, Uria lomvia. J Exp Biol 200:1757–1763PubMedGoogle Scholar
  103. Hayes JP, Chappell MA (1986) Effects of cold acclimation on maximum oxygen consumption during cold exposure and treadmill exercise in deer mice, Peromyscus maniculatus. Physiol Zool 59:473–481Google Scholar
  104. Hayes JP, Chappell MA (1990) Individual consistency of maximal oxygen consumption in deer mice. Funct Ecol 4:495–503Google Scholar
  105. Hickson RC (1981) Skeletal muscle cytochrome c and myoglobin, endurance, and frequency of training. J Appl Physiol 51:746–749PubMedGoogle Scholar
  106. Hohtola E (1982) Thermal and electromyographic correlates of shivering thermogenesis in the pigeon. Comp Biochem Physiol 73A:159–166Google Scholar
  107. Hohtola E (2002) Facultative and obligatory thermogenesis in young birds: a cautionary note. Comp Biochem Physiol A 131:733–739Google Scholar
  108. Hohtola E, Henderson RP, Rashotte ME (1998) Shivering thermogenesis in the pigeon: the effects of activity, diurnal factors, and feeding state. Am J Physiol 275:R1553–R1562PubMedGoogle Scholar
  109. Holloway GP, Bezaire V, Heigenhauser GJF, Tandon NN, Glatz JFC, Luiken JJFP, Bonen A, Spriet LL (2006) Mitochondrial long chain fatty acid oxidation, fatty acid translocase/CD36 content and carnitine palmitoyltransferase 1 activity in human skeletal muscle during aerobic exercise. J Physiol 571(1):201–210PubMedGoogle Scholar
  110. Holt S, Whitfield DP, Duncan K, Rae S, Smith RD (2002) Mass loss in incubating Eurasian Dotterel: adaptation or constraint? J Avian Biol 33:219–224Google Scholar
  111. Hoppeler H, Weibel ER (1998) Limits for oxygen and substrate transport in mammals. J Exp Biol 201:1051–1064PubMedGoogle Scholar
  112. Houston DC, Donnan D, Jones P, Hamilton I, Osborne D (1995) Changes in the muscle condition of female Zebra Finches Poephila guttata during egg laying and the role of protein storage in bird skeletal muscle. Ibis 137:322–328Google Scholar
  113. Huet C, Li Z-F, Liu H-Z, Black RA, Galliano M-F, Engvall E (2001) Skeletal muscle cell hypertrophy induced by inhibitors of metalloproteinases; myostatin as a potential mediator. Am J Physiol 281:C1624–C1634Google Scholar
  114. Jaeger EC (1949) Further observations on the hibernation of the Poor-will. Condor 51:105–109Google Scholar
  115. Jehl JR Jr (1994) Field estimates of energetics in migrating and downed Black-necked Grebes. J Avian Biol 25:63–68Google Scholar
  116. Jehl JR Jr (1997) Cyclical changes in body composition in the annual cycle and migration of the Eared Grebe Podiceps nigricollis. J Avian Biol 28:132–142Google Scholar
  117. Jenni-Eiermann S, Jenni L (1992) High plasma triglyceride levels in small birds during migratory flight: a new pathway for fuel supply during endurance locomotion at very high mass-specific metabolic rates. Physiol Zool 65:112–123Google Scholar
  118. Jenni-Eiermann S, Jenni L (2001) Postexercise ketosis in night-migrating passerine birds. Physiol Biochem Zool 74:90–101PubMedGoogle Scholar
  119. Jenni-Eiermann S, Jenni L, Kvist A, Lindström Å, Piersma T, Visser GH (2002) Fuel use and metabolic response to endurance exercise: a wind tunnel study of a long-distance migrant shorebird. J Exp Biol 205:2453–2460PubMedGoogle Scholar
  120. Jones MM (1991) Muscle protein loss in laying House Sparrows Passer domesticus. Ibis 133:193–198Google Scholar
  121. Jones IL (1994) Mass changes of Least Auklets Aethia pusilla during the breeding season: evidence for programmed loss of mass. J Anim Ecol 63:71–78Google Scholar
  122. Karasov WH (1990) Digestion in birds: chemical and physiological determinants and ecological implications. Stud Avian Biol 13:391–415Google Scholar
  123. Karasov WH (1996) Digestive plasticity in avian energetics and feeding ecology. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman & Hall, New York, pp 61–84Google Scholar
  124. Kaseloo PA, Lovvorn JR (2003) Heat increment of feeding and thermal substitution in mallard ducks feeding voluntarily on grain. J Comp Physiol B 173:207–213PubMedGoogle Scholar
  125. Kersten M, Piersma T (1987) High levels of energy expenditure in shorebirds; metabolic adaptations to an energetically expensive way of life. Ardea 75:175–187Google Scholar
  126. 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
  127. Kim YS, Bobbili NK, Paek KS, Jin HJ (2006) Production of a monoclonal anti-myostatin antibody and the effects of in ovo administration of the antibody on posthatch broiler growth and muscle mass. Poult Sci 85:1062–1071PubMedGoogle Scholar
  128. Kim YS, Bobbili NK, Lee YK, Jin HJ, Dunn MA (2007) Production of a polyclonal anti-myostatin antibody and the effects of in ovo administration of the antibody on posthatch broiler growth and muscle mass. Poult Sci 86:1196–1205PubMedGoogle Scholar
  129. Klaassen M (1995) Moult and basal metabolic costs in males of two species of stonechats: the European Saxicola torquata rubicula and the East African S. t. axillaris. Oecologia 104:424–432Google Scholar
  130. Klaassen M (1996) Metabolic constraints on long-distance migration. J Exp Biol 199:57–64PubMedGoogle Scholar
  131. 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
  132. Klaassen M, Lindström Å, Zijlstra R (1997) Composition of fuel stores and digestive limitations to fuel deposition rate in the long-distance migratory thrush nightingale, Luscinia luscinia. Physiol Zool 70:125–133PubMedGoogle Scholar
  133. Klaassen M, Kvist A, Lindström Å (2000) Flight costs and fuel composition of a bird migrating in a wind tunnel. Condor 102:444–451Google Scholar
  134. Kullberg C, Metcalfe NB, Houston DC (2002) Impaired flight ability during incubation in the Pied Flycatcher. J Avian Biol 33:179–183Google Scholar
  135. Landys MM, Piersma T, Guglielmo CG, Jukema J, Ramenofsky M, Wingfield JC (2005) Metabolic profile of long-distance migratory flight and stopover in a shorebird. Proc Roy Soc B 272:295–302Google Scholar
  136. Landys-Ciannelli MM, Jukema J, Piersma T (2002) Blood parameter changes during stopover in a long-distance migratory shorebird, the Bar-tailed Godwit Limosa lapponica taymyrensis. J Avian Biol 33:451–455Google Scholar
  137. Landys-Ciannelli MM, Piersma T, Jukema J (2003) Strategic size changes of internal organs and muscle tissue in the Bar-tailed Godwit during fat storage on a spring stopover site. Funct Ecol 17:151–159Google Scholar
  138. Lee S-J (2004) Regulation of muscle mass by myostatin. Annu Rev Cell Dev Biol 20:61–86PubMedGoogle Scholar
  139. Lee S-J, McPherron AC (2001) Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci USA 98:9306–9311PubMedGoogle Scholar
  140. Liknes ET (2005) Seasonal acclimatization patterns and mechanisms in small, temperate-resident passerines: phenotypic flexibility of complex traits. Ph.D. dissertation, University of South Dakota, VermillionGoogle Scholar
  141. 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
  142. Liknes ET, Scott SM, Swanson DL (2002) Seasonal acclimatization in the American goldfinch revisited: to what extent to metabolic rates vary seasonally? Condor 104:548–557Google Scholar
  143. Lindström Å (1997) Basal metabolic rates of migrating waders in the Eurasian Arctic. J Avian Biol 28:87–92Google Scholar
  144. Lindström Å, Piersma T (1993) Mass changes in migrating birds: the evidence for fat and protein storage re-examined. Ibis 135:70–78Google Scholar
  145. 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
  146. Lindström Å, Kvist A, Piersma T, Dekinga A, Dietz M (2000) Avian pectoral muscle size rapidly tracks body mass changes during flight, fasting and fuelling. J Exp Biol 203:913–919PubMedGoogle Scholar
  147. Liu J-S, Li M (2006) Phenotypic flexibility of metabolic rate and organ masses among tree ­sparrows Passer montanus in seasonal acclimatization, Acta Zool. Sinica 52:469–477Google Scholar
  148. López-Calleja MV, Bozinovic F (1995) Maximum metabolic rate, thermal insulation and aerobic scope in a small-sized Chilean hummingbird (Sephanoides sephanoides). Auk 112:1034–1036Google Scholar
  149. Luiken JJFP, Schaap FG, van Nieuwenhoven FA, van der Vusse GJ, Bonen A, Glatz JFC (1999) Cellular fatty acid transport in heart and skeletal muscle as facilitated by proteins. Lipids 34:S169–S175PubMedGoogle Scholar
  150. Lundgren BO (1988) Catabolic enzyme activities in the pectoralis muscle of migratory and non-migratory Goldcrests, Great Tits, and Yellowhammers. Ornis Scand 19:190–194Google Scholar
  151. Lundgren BO, Kiessling K-H (1985) Seasonal variation in catabolic enzyme activities in breast muscle of some migratory birds. Oecologia 66:468–471Google Scholar
  152. Lundgren BO, Kiessling K-H (1986) Catabolic enzyme activities in the pectoralis muscle of ­premigratory and migratory juvenile Reed Warblers Acrocephalus scirpaceus (Herm.). Oecologia 68:529–532Google Scholar
  153. Lundgren BO, Kiessling K-H (1988) Comparative aspects of fibre types, areas, and capillary ­supply in the pectoralis muscle of some passerine birds with differing migratory behavior. J Comp Physiol B 158:165–173Google Scholar
  154. Marjoniemi K, Hohtola E (1999) Shivering thermogenesis in leg and breast muscles of Galliform chicks and nestlings of the domestic pigeon. Physiol Biochem Zool 72:484–492PubMedGoogle Scholar
  155. Marsh RL (1981) Catabolic enzyme activities in relation to premigratory fattening and muscle hypertrophy in the Gray Catbird (Dumetella carolinensis). J Comp Physiol 141:417–423Google Scholar
  156. Marsh RL (1984) Adaptations of the Gray Catbird Dumetella carolinensis to long-distance migration: flight muscle hypertrophy associated with elevated body mass. Physiol Zool 57:105–117Google Scholar
  157. Marsh RL (1993) Does regulatory nonshivering thermogenesis exist in birds? In: Carey C, Florant GL, Wunder BA, Horwitz B (eds) Life in the cold: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, Colorado, pp 535–538Google Scholar
  158. Marsh RL, Dawson WR (1982) Substrate metabolism in seasonally acclimatized American Goldfinches. Am J Physiol 242:R563–R569PubMedGoogle Scholar
  159. Marsh RL, Dawson WR (1989) Avian adjustments to cold. In: Wang LCH (ed) Advances in comparative and environmental physiology 4: animal adaptation to cold. Springer, Berlin, pp 206–253Google Scholar
  160. Marsh RL, Carey C, Dawson WR (1984) Substrate concentrations and turnover of plasma glucose during cold exposure in seasonally acclimatized house finches, Carpodacus mexicanus. J Comp Physiol B 154:469–476Google Scholar
  161. Masman D, Gordijn M, Daan S, Dijkstra C (1986) Ecological energetics of the kestrel: field ­estimates of energy intake throughout the year. Ardea 74:24–39Google Scholar
  162. Masman D, Daan S, Dietz M (1989) Heat increment of feeding in the kestrel, Falco tinnunculus, and its natural seasonal variation. In: Bech C, Reinertsen RE (eds) Physiology of cold adaptation in birds. Plenum Life Sciences, New York, pp 123–135Google Scholar
  163. Mathieu-Costello O, Suarez RK, Hochachka PW (1992) Capillary-to-fiber geometry and ­mitochondrial density in hummingbird flight muscle. Respir Physiol 89:113–132PubMedGoogle Scholar
  164. Mathieu-Costello O, Agey PJ, Logemann RB, Florez-Duquet M, Bernstein MH (1994) Effect of flying activity on capillary-fiber geometry in pigeon flight muscle. Tissue Cell 26:57–73PubMedGoogle Scholar
  165. Mathieu-Costello O, Agey PJ, Quintana ES, Rousey K, Wu L, Bernstein MH (1998) Fiber ­capillarization and ultrastructure of pigeon pectoralis muscle after cold acclimation. J Exp Biol 201:3211–3220PubMedGoogle Scholar
  166. Mawhinney K, Diamond AW, Kehoe FP (1999) The use of energy, fat, and protein reserves by breeding Great Black-backed Gulls. Can J Zool 77:1459–1464Google Scholar
  167. McDonald RB, Horwitz BA, Stern JS (1988) Cold-induced thermogenesis in younger and older Fischer 344 rats following exercise training. Am J Physiol 254:R908–R916PubMedGoogle Scholar
  168. McFarlan JT (2007) Seasonal upregulation of fatty acid uptake proteins in flight muscles of Zonotrichia sparrows during migration. M.S. Thesis, University of Western Ontario, London, ONGoogle Scholar
  169. McKechnie AE (2008) Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J Comp Physiol B 178:235–247PubMedGoogle Scholar
  170. McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses: a review. Condor 104:705–724Google Scholar
  171. McKechnie AE, Lovegrove BG (2006) Evolutionary and ecological determinants of avian torpor: a conceptual model. Acta Zoologica Sinica 52 (suppl):409–413Google Scholar
  172. McKechnie AE, Wolf BO (2004) The allometry of avian basal metabolic rate: good predictions need good data. Physiol Biochem Zool 77:502–521PubMedGoogle Scholar
  173. McKechnie AE, Freckleton RP, Jetz W (2006) Phenotypic plasticity in the scaling of avian metabolic rate. Proc R Soc B 1589:931–937Google Scholar
  174. McNab BK (1988) Food habits and the basal rate of metabolism in birds. Oecologia 77:343–349Google Scholar
  175. McNab BK (1997) On the utility of uniformity in the definition of basal rate of metabolism. Physiol Zool 70:718–720PubMedGoogle Scholar
  176. McPherron AC, Lee S-J (1997) Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA 94:12457–12461PubMedGoogle Scholar
  177. McWilliams SR, Karasov WH (2001) Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. Comp Biochem Physiol A 128:579–593Google Scholar
  178. McWilliams SR, Caviedes-Vidal E, Karasov WH (1999) Digestive adjustments in Cedar Waxwings to high feeding rate. J Exp Zool 283:394–407Google Scholar
  179. McWilliams SR, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393Google Scholar
  180. Merola-Zwartjes M (1998) Metabolic rate, temperature regulation, and the energetic implications of roost nests in the Bananaquit (Coereba flaveola). Auk 115:780–786Google Scholar
  181. Mezentseva NV, Kumaratilake JS, Newman SA (2008) The brown adipocyte differentiation pathway in birds: an evolutionary road not taken. BMC Biol 6:17. doi: 10.1186/1741-7007-6-17 PubMedGoogle Scholar
  182. Miller DS (1939) A study of the physiology of the sparrow thyroid. J Exp Zool 80:259–281Google Scholar
  183. Moe B, Langseth I, Fyhn M, Gabrielsen GW, Bech C (2002) Changes in body condition in ­breeding kittiwakes Rissa tridactyla. J Avian Biol 33:225–234Google Scholar
  184. Moreno J (1989) Strategies of mass change in breeding birds. Biol J Linn Soc 37:297–310Google Scholar
  185. Morris SR, Richmond ME, Holmes DW (1994) Patterns of stopover by warblers during spring and fall migration on Appledore Island, Maine. Wilson Bull 106:703–718Google Scholar
  186. Mozo J, Emre Y, Bouillaud F, Ricquier D, Criscuolo F (2005) Thermoregulation: what role for UCPs in mammals and birds? Biosci Rep 25:227–249PubMedGoogle Scholar
  187. Murphy MT, Armbrecth B, Vlamis E, Pierce A (2000) Is reproduction by tree swallows cost free? Auk 117:902–912Google Scholar
  188. Nagy LR, Stanculescu D, Holmes RT (2007) Mass loss by breeding female songbirds: food ­supplementation supports energetic stress hypothesis in Black-throated Blue Warblers. Condor 109:304–311Google Scholar
  189. Newton I, Dale LC (1996) Bird migration at different latitudes in eastern North America. Auk 113:626–635Google Scholar
  190. Nilsson J-A, Råberg L (2001) The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia 128:187–192Google Scholar
  191. Norberg Å (1981) Temporary weight decrease in breeding birds may result in more fledged young. Am Nat 118:838–850Google Scholar
  192. Novoa FF, Veloso C, López-Calleja MV, Bozinovic F (1996) Seasonal changes in diet, digestive morphology and digestive efficiency in the Rufous-collared Sparrow (Zonotrichia capensis) in central Chile. Condor 98:873–876Google Scholar
  193. Nudds RL, Bryant DM (2000) The energetic cost of short flights in birds. J Exp Biol 203:1561–1572PubMedGoogle Scholar
  194. Nur N (1984) The consequences of brood size for breeding Blue Tits I. Adult survival, weight change and the cost of reproduction. J Anim Ecol 53:479–496Google Scholar
  195. O’Connor TP (1995a) Metabolic characteristics and body composition in house finches: effects of seasonal acclimatization. J Comp Physiol B 165:298–305Google Scholar
  196. O’Connor TP (1995b) Seasonal acclimatization of lipid mobilization and catabolism in House Finches (Carpodacus mexicanus). Physiol Zool 68:985–1005Google Scholar
  197. O’Reilly KM, Wingfield JM (1995) Spring and autumn migration in Arctic shorebirds: same distance, different strategies. Am Zool 35:222–233Google Scholar
  198. Olson JM, Dawson WR, Camilliere JJ (1988) Fat from Black-capped Chickadees: avian brown adipose tissue? Condor 90:529–537Google Scholar
  199. Palacios L, Palomeque J, Riera M, Pages T, Viscor G, Planas J (1984) Oxygen transport properties in the starling, Sturnus vulgaris L. Comp Biochem Physiol 77A:255–260Google Scholar
  200. Paladino FV, King JR (1984) Thermoregulation and oxygen consumption during terrestrial locomotion by White-crowned Sparrows, Zonotricia leucophrys gambelii. Physiol Zool 57:226–236Google Scholar
  201. Pearson DJ, Lack PC (1992) Migration patterns and habitat use by passerine and near- passerine migrant birds in eastern Africa. Ibis 134 (suppl):89–98Google Scholar
  202. Pelsers MMAL, Butler PJ, Bishop CM, Glatz JFC (1999) Fatty acid binding protein in heart and skeletal muscles of the migratory Barnacle Goose throughout development. Am J Physiol 276:R637–R643PubMedGoogle Scholar
  203. Phillips RA, Furness RW (1997) Sex-specific loss of mass by breeding Arctic Skuas. J Avian Biol 28:163–170Google Scholar
  204. 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 208:1277–1285PubMedGoogle Scholar
  205. Piersma T (1998) Phenotypic flexibility during migration: optimization of organ size contingent on the risks and rewards of fueling and flight? J Avian Biol 29:511–520Google Scholar
  206. Piersma T (2002) Energetic bottlenecks and other design constraints in avian annual cycles. Integ Comp Biol 42:51–67Google Scholar
  207. Piersma T, Dietz MW (2007) Twofold seasonal variation in the supposedly constant, species-specific, ratio of upstroke to downstroke flight muscles in Red Knots Calidris canutus. J Avian Biol 35:536–540Google Scholar
  208. Piersma T, Gill RE Jr (1998) Guts don’t fly: small digestive organs in obese Bar-tailed Godwits. Auk 115:196–203Google Scholar
  209. Piersma T, Jukema J (2002) Contrast in adaptive mass gains: Eurasian Golden Plovers store fat before midwinter and protein before prebreeding flight. Proc R Soc Lond B 269:1101–1105Google Scholar
  210. 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 Comp Physiol B 165:37–45Google Scholar
  211. Piersma T, Bruinzeel L, Drent R, Kersten M, Van der Meer J, Wiersma P (1996a) Variability in basal metabolic rate of a long-distance migrant shorebird (Knot Calidris canutus) reflects shifts in organ size. Physiol Zool 69:191–217Google Scholar
  212. Piersma T, Everaarts JM, Jukema J (1996b) Build-up of red blood cells in refueling Bar-tailed Godwits in relation to individual migratory quality. Condor 98:363–370Google Scholar
  213. Piersma T, Gudmundsson GA, Lilliendahl K (1999) Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. Physiol Biochem Zool 72:405–415PubMedGoogle Scholar
  214. Piersma T, Koolhaas A, Dekinga A, Gwinner E (2000) Red blood cell and white blood cell counts in sandpipers (Philomachus pugnax, Calidris canutus): effects of captivity, season, nutritional status, and frequent bleedings. Can J Zool 78:1349–1355Google Scholar
  215. 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
  216. Raimbault S, Dridi S, Denjean F, Lachuer J, Couplan E, Bouillaud F, Bordas A, Duchamp C, Taouis M, Ricquier D (2001) An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds. Biochem J 353:441–444PubMedGoogle Scholar
  217. Ramenofsky M (1990) Fat storage and fat metabolism in relation to migration. In: Gwinner E (ed) Bird migration: physiology and ecophysiology. Springer, Berlin, pp 214–231Google Scholar
  218. Ramenofsky M, Savard R, Greenwood MRC (1999) Seasonal and diel transitions in physiology and behavior in the migratory dark-eyed junco. Comp Biochem Physiol A 122:385–397Google Scholar
  219. Rashotte ME, Saarela S, Henderson RP, Hohtola E (1999) Shivering and digestion-related ­thermogenesis in pigeons during dark phase. Am J Physiol 277:R1579–R1587PubMedGoogle Scholar
  220. Reinertsen RE (1996) Physiological and ecological aspects of hibernation. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman & Hall, New York, pp 125–157Google Scholar
  221. 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
  222. Ricklefs RE, Hussell DJT (1984) Changes in adult mass associated with the nesting cycle in the European Starling. Ornis Scand 15:155–161Google Scholar
  223. Roberts TJ, Weber J-M, Hoppeler H, Weibel EW, Taylor CR (1996) Design of the oxygen and substrate pathways, II. Defining the upper limits of carbohydrate and fat oxidation. J Exp Biol 199:1651–1658PubMedGoogle Scholar
  224. Rønning B, Moe B, Chastel O, Broggi J, Langset M, Bech C (2008) Metabolic adjustments in breeding female kittiwakes (Rissa tridactyla) include changes in kidney metabolic intensity. J Comp Physiol B 178:779–784PubMedGoogle Scholar
  225. Rosenmann M, Morrison P (1974) Maximum oxygen consumption and heat loss facilitation in small homeotherms by He-O2. Am J Physiol 226:490–495PubMedGoogle Scholar
  226. Saarela S, Hissa R, Pyörnilä A, Harjula R, Ojanen M, Orell M (1989a) Do birds possess brown adipose tissue? Comp Biochem Physiol 92A:219–228Google Scholar
  227. Saarela S, Klapper B, Heldmaier G (1989b) 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
  228. Saarela S, Keith JS, Hohtola E, Trayhurn P (1991) Is the “mammalian” brown fat-specific mitochondrial uncoupling protein present in adipose tissues of birds? Comp Biochem Physiol 100B:45–49Google Scholar
  229. Saarela S, Klapper B, Heldmaier G (1995) Daily rhythm of oxygen consumption and thermoregulatory responses in some European winter- or summer-acclimatized finches at different ambient temperatures. J Comp Physiol B 165:366–376Google Scholar
  230. Sanz JJ, Moreno J (1995) Mass loss in brooding female Pied Flycatchers Ficedula hypoleuca: no evidence for reproductive stress. J Avian Biol 26:313–320Google Scholar
  231. Saunders DK, Fedde MR (1991) Physical conditioning: effect on the myoglobin concentration in skeletal and cardiac muscle of Bar-headed Geese. Comp Biochem Physiol 100A:349–352Google Scholar
  232. Savard R, Ramenofsky M, Greenwood MRC (1991) A north-temperate migratory bird: a model for the fate of lipids during exercise of long duration. Can J Physiol Pharmacol 69:1443–1447PubMedGoogle Scholar
  233. Schwilch R, Jenni L, Jenni-Eiermann S (1996) Metabolic responses of homing pigeons to flight and subsequent recovery. J Comp Physiol B 166:77–87Google Scholar
  234. Scott I, Mitchell PI, Evans PR (1996) How does variation in body composition affect the basal metabolic rate of birds? Funct Ecol 10:307–313Google Scholar
  235. Seymour RS, Runciman S, Baudinette RV (2008) Development of maximum metabolic rate and pulmonary diffusing capacity in the superprecocial Australian Brush Turkey Alectura lathami: an allometric and morphometric study. Comp Biochem Physiol A 150:169–175Google Scholar
  236. Speakman JR (1997) Doubly labelled water theory and practice. Chapman & Hall, LondonGoogle Scholar
  237. Stevens L (1996) Avian biochemistry and molecular biology. Cambridge University Press, CambridgeGoogle Scholar
  238. Strømme SB, Hammel HT (1967) Effects of physical training on tolerance to cold in rats. J Appl Physiol 23:815–824PubMedGoogle Scholar
  239. Suarez RK (1998) Oxygen and the upper limits to animal design and performance. J Exp Biol 201:1065–1072PubMedGoogle Scholar
  240. Swanson DL (1990a) Seasonal variation in cold hardiness and peak rates of cold-induced thermogenesis in the Dark-eyed Junco (Junco hyemalis). Auk 107:561–566Google Scholar
  241. Swanson DL (1990b) Seasonal variation of vascular oxygen transport in the Dark-eyed Junco. Condor 92:62–66Google Scholar
  242. Swanson DL (1991a) Seasonal adjustments in metabolism and insulation in the Dark-eyed Junco. Condor 93:538–545Google Scholar
  243. Swanson DL (1991b) Substrate metabolism under cold stress in seasonally acclimatized Dark-eyed Juncos. Physiol Zool 64:1578–1592Google Scholar
  244. Swanson DL (1993) Cold tolerance and thermogenic capacity in Dark-eyed Juncos in winter: geographic variation and comparison with American Tree Sparrows. J Therm Biol 18:275–281Google Scholar
  245. Swanson DL (1995) Seasonal variation in thermogenic capacity of migratory Warbling Vireos. Auk 112:870–877Google Scholar
  246. Swanson DL (2001) Are summit metabolism and thermogenic endurance correlated in winter acclimatized passerine birds? J Comp Physiol B 171:475–481PubMedGoogle Scholar
  247. Swanson DL, Dean KL (1999) Migration-induced variation in thermogenic capacity in migratory passerines. J Avian Biol 30:245–254Google Scholar
  248. Swanson DL, Liknes ET (2006) A comparative analysis of thermogenic capacity and cold tolerance in small birds. J Exp Biol 209:466–474PubMedGoogle Scholar
  249. Swanson DL, Olmstead KL (1999) Evidence for a proximate influence of winter temperature on metabolism in passerine birds. Physiol Biochem Zool 72:566–575PubMedGoogle Scholar
  250. Swanson DL, Weinacht DP (1997) Seasonal effects on metabolism and thermoregulation in Northern Bobwhite. Condor 99:478–489Google Scholar
  251. Swanson DL, Sabirzhanov B, VandeZande A, Clark TG (2009) Down-regulation of myostatin gene expression in pectoralis muscle is associated with elevated thermogenic capacity in winter acclimatized house sparrows (Passer domesticus). Physiol Biochem Zool 82:121–128PubMedGoogle Scholar
  252. Sweazea KL, Braun EJ (2006) Oleic acid uptake by in vitro English Sparrow muscle. J Exp Zool 305A:268–276Google Scholar
  253. Taigen TL (1983) Activity metabolism of anuran amphibians: implication for the origin of endothermy. Am Nat 121:94–109Google Scholar
  254. Tatner P, Bryant DM (1986) Flight cost of a small passerine measured using doubly labeled water: implications for energetics studies. Auk 103:169–180Google Scholar
  255. Taylor CR, Weibel ER (1981) Design of the mammalian respiratory system. I. Problem and strategy. Respir Physiol 44:1–10PubMedGoogle Scholar
  256. Tøien O (1992) Data acquisition in thermal physiology: measurements of shivering. J Therm Biol 17:357–366Google Scholar
  257. Trevelyan R, Harvey PH, Pagel MD (1990) Metabolic rates and life histories in birds. Funct Ecol 4:135–141Google Scholar
  258. Turner DL, Hoppeler H, Hokanson J, Weibel ER (1995) Cold acclimation and endurance training in guinea pigs: changes in daily and maximal metabolism. Respir Physiol 101:183–188PubMedGoogle Scholar
  259. Vaillancourt E, Prud’Homme S, Haman F, Guglielmo CG, Weber J-M (2005) Energetics of a long-distance migrant shorebird (Philomachus pugnax) during cold exposure and running. J Exp Biol 208:317–325PubMedGoogle Scholar
  260. Vezina F, Williams TD (2002) Metabolic cost of egg production in the European Starling (Sturnus vulgaris). Physiol Biochem Zool 75:377–385PubMedGoogle Scholar
  261. Vezina F, Williams TD (2003) Plasticity in body composition in breeding birds: what drives the metabolic costs of egg production? Physiol Biochem Zool 76:716–730PubMedGoogle Scholar
  262. Vezina 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
  263. Vezina 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 209:3141–3154PubMedGoogle Scholar
  264. Vezina F, Jalvingh KM, Dekinga A, Piersma T (2007) Thermogenic side effects to migratory disposition in shorebirds. Am J Physiol Regul Integr Comp Physiol 292:1287–1297Google Scholar
  265. Vianna CR, Hagen T, Zhang C-Y, Bachman E, Boss O, Gereben B, Moriscot AS, Lowell BB, Bicudo JEPW, Bianco AC (2001) Cloning and functional characterization of an uncoupling protein homolog in hummingbirds. Physiol. Genomics 5:137–145Google Scholar
  266. Vittoria JC, Marsh RL (1996) Cold-acclimated ducklings shiver when exposed to cold. Am Zool 36:66AGoogle Scholar
  267. Vleck CM, Vleck D (1979) Metabolic rate in five tropical bird species. Condor 81:89–91Google Scholar
  268. Weathers WW (1979) Climatic adaptation in avian standard metabolic rate. Oecologia 42:81–89Google Scholar
  269. Weathers WW (1997) Energetics and thermoregulation by small passerines of the humid lowland tropics. Auk 114:341–353Google Scholar
  270. Weathers WW, Caccamise DR (1978) Seasonal acclimatization to temperature in Monk Parakeets. Oecologia 35:173–183Google Scholar
  271. Weathers WW, Sullivan KA (1993) Seasonal patterns of time and energy allocation by birds. Physiol Zool 66:511–536Google Scholar
  272. Weathers WW, Olson CR, Siegel RB, Davidson CL, Famula TR (1999) Winter and breeding-season energetics of nonmigratory White-crowned Sparrows. Auk 116:842–847Google Scholar
  273. 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 27:215–224Google Scholar
  274. Weber J-M, Brichon G, Zwingelstein G, McClelland G, Saucedo C, Weibel ER, Taylor CR (1996) Design of the oxygen and substrate pathways, IV. Partitioning energy provision from fatty acids. J Exp Biol 199:1667–1674PubMedGoogle Scholar
  275. Webster MD, Weathers WW (1990) Heat produced as a by-product of foraging activity contributes to thermoregulation by verdins, Auriparus flaviceps. Physiol Zool 63:777–794Google Scholar
  276. Webster MD, Weathers WW (2000) Seasonal changes in energy and water use by Verdins, Auriparus flaviceps. J Exp Biol 203:3333–3344PubMedGoogle Scholar
  277. 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 R Soc B 274:287–293PubMedGoogle Scholar
  278. Wiersma P, Piersma T (1994) Effects of microhabitat, flocking, climate and migratory goal on energy expenditure in the annual cycle of Red Knots. Condor 96:257–279Google Scholar
  279. Wiersma P, Muñoz-Garcia A, Walker A, Williams JB (2007a) Tropical birds have a slow pace of life. Proc Natl Acad Sci USA 104:9340–9345PubMedGoogle Scholar
  280. Wiersma P, Chappell MA, Williams JB (2007b) Cold-and exercise-induced peak metabolic rates in tropical birds. Proc Natl Acad Sci USA 104:20866–20871PubMedGoogle Scholar
  281. Williams JB (2001) Energy expenditure and water flux of free-living Dune Larks in the Namib: a test of the reallocation hypothesis on a desert bird. Funct Ecol 15:175–185Google Scholar
  282. 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
  283. Williams CT, Kildaw SD, Buck CL (2007) Sex-specific differences in body condition indices and seasonal mass loss in Tufted Puffins. J Field Ornithol 78:369–378Google Scholar
  284. Winker K, Warner DW, Weisbrod AR (1992) Timing of songbird migration in the St. Croix River Valley, Minnesota, 1984-1986. Loon 64:131–137Google Scholar
  285. Wolfman NM, McPherron AC, Pappano WN, Davies MV, Song K, Tomlinson KN, Wright JF, Zhao L, Sebald SM, Greenspan DS, Lee S-J (2003) Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci USA 100:15842–15846PubMedGoogle Scholar
  286. Yacoe ME, Dawson WR (1983) Seasonal acclimatization in American goldfinches: the role of the pectoralis muscle. Am J Physiol 245:R265–R271PubMedGoogle Scholar
  287. Zerba E, Walsberg GE (1992) Exercise-generated heat contributes to thermoregulation by Gambel’s Quail in the cold. J Exp Biol 171:409–422Google Scholar
  288. Zerba E, Dana AN, Lucia MA (1999) The influence of wind and locomotor activity on surface temperature and energy expenditure of the eastern House Finch (Carpodacus mexicanus) during cold stress. Physiol Biochem Zool 72:265–276PubMedGoogle Scholar
  289. Zheng W-H, Li M, Liu J-S, Shao S-L (2008) Seasonal acclimatization of metabolism in Eurasian Tree Sparrows (Passer montanus). Comp Biochem Physiol A 151:519–525Google Scholar

Copyright information

© Springer New York 2010

Authors and Affiliations

  1. 1.Department of BiologyUniversity of South DakotaVermillionUSA

Personalised recommendations