Thermoregulatory Adaptations to Starvation in Birds

  • Esa Hohtola


Birds have body temperatures that are typically higher than those of mammals, and thus spend a large proportion of their total energy budget maintaining these temperatures—particularly in cold environments. Birds also have high surface to volume ratios and comparatively small energy reserves causing additional energetic challenges during periods of food limitation or complete starvation. During starvation, energy can be saved if the need for active thermogenesis can be reduced. Such a hypometabolic state can be achieved by reducing body temperature in a regulated manner or by increasing thermal insulation, or by employing both of these mechanisms. Adaptive changes in heat loss (thermal conductance) is well known among birds, but a growing number of studies are documenting how birds are able to conserve limited energy by reducing body temperature in a regulated manner. Rest-phase hypothermia and shallow torpor involve decreases in body temperature ranging from 1 to 10°C, with the birds retaining responsiveness to the environment, whereas deep torpor is characterized by a larger decrease, with body temperatures often approaching ambient temperature and resulting in true torpidity. Starvation is well known to induce deep torpor in some avian groups, notably hummingbirds and swifts; however, recent studies show that basically all avian groups can save energy during starvation by entering shallow torpor during the rest-phase of their daily cycle. So far, such responses have been found in at least 29 avian families. This chapter reviews our current understanding of how birds alter their thermoregulatory patterns in the face of starvation and underscores the need to: (1) investigate the neurohumoral responses underlying hypothermia and (2) better quantify the energy savings ensuing from small decreases in body temperature.


Torpor Bout King Penguin Body Mass Loss Starvation Resistance Avian Group 
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 the Academy of Finland and Thule Institute, University of Oulu, for financial support.


  1. Aschoff J (1981) The 24-hour-rhythm of body temperature in birds as a function of body weight. J Orn 122:129–152CrossRefGoogle Scholar
  2. Astheimer LB, Buttemer WA, Wingfield JC (1992) Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scand 23:355–365CrossRefGoogle Scholar
  3. Bech C, Abe AS, Steffensen JF, Berger M, Bicudo JEPW (1997) Torpor in three species of Brazilian hummingbirds under semi-natural conditions. Condor 99:780–788CrossRefGoogle Scholar
  4. Bech C, Praesteng KE (2004) Thermoregulatory use of heat increment of feeding in the tawny owl (Strix aluco). J Therm Biol 29:649–654CrossRefGoogle Scholar
  5. Ben-Hamo M, Pinshow B, McCue MD, McWilliams SR, Bauchinger U (2010) Fasting triggers hypothermia, and ambient temperature modulates its depth in Japanese quail Coturnix japonica. Comp Biochem Physiol A 156:84–91CrossRefGoogle Scholar
  6. Blem CR (1976) Patterns of lipid storage and utilization in birds. Am Zool 16:671–684Google Scholar
  7. Boismenu C, Gauthier G, Larochelle J (1992) Physiology of prolonged fasting in greater snow geese (Chen caerulescens atlantica). Auk 109:511–521Google Scholar
  8. Brigham M (1992) Daily torpor in a free-ranging goatsucker, the common poorwill (Phalaenoptilus nuttallii). Physiol Zool 65:457–472Google Scholar
  9. Brigham RM, Körtner G, Maddocks TA, Geiser F (2000) Seasonal use of torpor by free-ranging Australian owlet-nightjars (Aegotheles cristatus). Physiol Biochem Zool 73:613–620PubMedCrossRefGoogle Scholar
  10. Broggi J, Orell M, Hohtola E, Nilson JA (2004) Metabolic response to temperature variation in the great tit: an interpopulation comparison. J Anim Ecol 73:967–972CrossRefGoogle Scholar
  11. Butler PJ, Woakes AJ (2001) Seasonal hypothermia in a large migrating bird: saving energy for fat deposition? J Exp Biol 204:1361–1367PubMedGoogle Scholar
  12. Carpenter FL, Hixon MA (1988) A new function of torpor: fat conservation in a wild migrating hummingbird. Condor 90:373–378CrossRefGoogle Scholar
  13. Chaplin SB, Diesel DA, Kasparie JA (1984) Body temperature regulation in red-tailed hawks and great horned owls: responses to air temperature and food deprivation. Condor 86:175–181CrossRefGoogle Scholar
  14. Cherel Y, Le Maho Y (1985) Five months of fasting in king penguin chicks: body mass loss and fuel metabolism. Am J Physiol 249:R387–R392PubMedGoogle Scholar
  15. Cherel Y, Robin JP, Le Maho Y (1988) Physiology and biochemistry of long-term fasting in birds. Can J Zool 66:159–166CrossRefGoogle Scholar
  16. Chossat C (1843) Recherches expérimentales sur l’inanition. Impremerie Royale, ParisGoogle Scholar
  17. Dewasmes G, Buchet C, Loen A G, Le Maho Y (1989) Sleep changes in emperor penguins during fasting. Am J Physiol 256:R476–R480PubMedGoogle Scholar
  18. Doucette LI, Brigham RM, Pavey CR, Geiser F (2012) Prey availability affects daily torpor by free-ranging Australian owlet-nightjars (Aegotheles cristatus). Oecologia. doi: 10.1007/s00442-011-2214-7
  19. Downs CT, Brown M (2002) Nocturnal heterothermy and torpor in the malachite sunbird (Nectarinia famosa). Auk 119:251–260Google Scholar
  20. Eichhorn G, Groscolas R, Le Glaunec G, Parisel C, Arnold L, Medina P, Handrich Y (2011) Heterothermy in growing king penguins. Nat Commun 2:435PubMedCrossRefGoogle Scholar
  21. Ekimova IV (2005) Thermoregulation in the pigeon Columbia livia during the stress produced by food deprivation. J Evol Biochem Physiol 41:78–86CrossRefGoogle Scholar
  22. Fahlman A, Schmidt A, Handrich Y, Woakes AJ, Butler PJ (2005) Metabolism and thermoregulation during fasting in king penguins, Aptenodytes patagonicus, in air and water. Am J Physiol Reg Int Comp Physiol 289:R670–R679CrossRefGoogle Scholar
  23. Geiser F (2008) Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comp Biochem Physiol A 150:176–180CrossRefGoogle Scholar
  24. Geiser F, Körtner G, Schmidt I (1998) Leptin increases energy expenditure of a marsupial by inhibition of daily torpor. Am J Physiol Reg Int Comp Physiol 44:R1627–R1632Google Scholar
  25. Graf R, Krishna S, Heller HC (1989) Regulated nocturnal hypothermia induced in pigeons by food deprivation. Am J Physiol Reg Int Comp Physiol 256:R733–R738Google Scholar
  26. Grubb TC Jr, Pravosudov VV (1994) Toward a general theory of energy management in wintering birds. J Avian Biol 25:255–260CrossRefGoogle Scholar
  27. Hainsworth FR, Collins BG, Wolf LL (1977) The function of torpor in hummingbirds. Physiol Zool 50:215–222Google Scholar
  28. Heller HC, Ruby NF (2004) Sleep and circadian rhythms in mammalian torpor. Annu Rev Physiol 66:275–289PubMedCrossRefGoogle Scholar
  29. Hiebert SM (1990) Energy costs and temporal organization of torpor in the rufous hummingbird (Selasphorus rufus). Physiol Zool 63:1082–1097Google Scholar
  30. Hiebert SM (1991) Seasonal differences in the response of rufous hummingbirds to food restriction: body mass and the use of torpor. Condor 93:526–537CrossRefGoogle Scholar
  31. 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
  32. Hohtola E, Hissa R, Pyörnilä A, Rintamäki H, Saarela S (1991) Nocturnal hypothermia in fasting Japanese quail: the effect of ambient temperature. Physiol Behav 49:563–567PubMedCrossRefGoogle Scholar
  33. Hohtola E, Pyörnilä A, Rintamäki H (1994) Fasting endurance and cold resistance without hypothermia in a small predatory bird—the metabolic strategy of Tengmalm’s Owl, Aegolius funereus. J Comp Physiol B 164:430–437CrossRefGoogle Scholar
  34. Hohtola E, Rintamäki H, Hissa R (1980) Shivering and ptiloerection as complementary cold defense responses in the pigeon during sleep and wakefulness. J Comp Physiol B 136:77–81CrossRefGoogle Scholar
  35. Hutchinson JMC, McNamara JM, Cuthill IC (1993) Song, sexual selection, starvation and strategic handicaps. Anim Behav 45:1153–1177CrossRefGoogle Scholar
  36. Irving L, Krog J (1954) Body temperatures of arctic and subarctic birds and mammals. J Appl Physiol 6:667–680PubMedGoogle Scholar
  37. Jaeger E (1948) Does the poorwill “hibernate”? Condor 50:45–46Google Scholar
  38. Jaeger EC (1949) Further observations on the hibernation of the poor-will. Condor 51:105–109CrossRefGoogle Scholar
  39. Jensen C, Bech C (1992) Ventilation and gas exchange during shallow hypothermia in pigeons. J Exp Biol 165:111–120Google Scholar
  40. 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
  41. Koskimies J (1950) The life of the swift, Micropus apus (L.), in relation to the weather. Ann Acad Sci Fenn Ser A 15:1–151Google Scholar
  42. Koubi HE, Robin JP, Dewasmes G, Le Maho Y, Frutoso J, Minaire Y (1991) Fasting-induced rise in locomotor activity in rats coincides with increased protein utilization. Physiol Behav 50:337–343PubMedCrossRefGoogle Scholar
  43. Körtner G, Brigham RM, Geiser F (2000) Winter torpor in a large bird. Nature 407:318PubMedGoogle Scholar
  44. Körtner G, Geiser F (2000) The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol Int 17:103–128PubMedCrossRefGoogle Scholar
  45. Lane JE, Brigham RM, Swanson DL (2004) Daily torpor in free-ranging whip-poor-wills (Caprimulgus vociferus). Physiol Biochem Zool 77:297–304PubMedCrossRefGoogle Scholar
  46. Laurila M, Hohtola E (2005) The effect of ambient temperature and simulated predation risk on fasting-induced nocturnal hypothermia of pigeons in outdoor conditions. J Therm Biol 30:392–399CrossRefGoogle Scholar
  47. Laurila M, Pilto T, Hohtola E (2005) Testing the flexibility of fasting-induced hypometabolism in birds: effect of photoperiod and repeated food deprivations. J Therm Biol 30:131–138CrossRefGoogle Scholar
  48. Le Maho Y (1983) Metabolic adaptations to long term fasting in Antarctic penguins and domestic geese. J Therm Biol 8:91–96CrossRefGoogle Scholar
  49. Marjoniemi K (2000) The effect of short-term fasting on shivering thermogenesis in Japanese quail chicks (Coturnix coturnix japonica): indications for a significant role of diet-induced/growth related thermogenesis. J Therm Biol 25:459–465PubMedCrossRefGoogle Scholar
  50. McCue MD (2006) Specific dynamic action: a century of investigation. Comp Biochem Physiol A 144:381–394CrossRefGoogle Scholar
  51. McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A 156:1–18Google Scholar
  52. McKechnie AE, Ashdown RAM, Christian MB, Brigham RM (2007) Torpor in an African caprimulgid, the freckled nightjar Caprimulgus tristigma. J Avian Biol 38:261–266Google Scholar
  53. McKechnie AE, Lovegrove BG (1999) Circadian metabolic responses to food deprivation in the Black-shouldered kite. Condor 101:426–432CrossRefGoogle Scholar
  54. McKechnie AE, Lovegrove BG (2001a) Heterothermic responses in the speckled mousebird (Colius striatus). J Comp Physiol B 171:507–518PubMedCrossRefGoogle Scholar
  55. McKechnie AE, Lovegrove BG (2001b) Thermoregulation and the energetic significance of clustering behavior in the white-backed mousebird (Colius colius). Physiol Biochem Zool 74:238–249PubMedCrossRefGoogle Scholar
  56. McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses: a review. Condor 104:705–724CrossRefGoogle Scholar
  57. Nagy KA (2005) Field metabolic rate and body size. J Exp Biol 208:1621–1625PubMedCrossRefGoogle Scholar
  58. Ostheim J (1992) Coping with food-limited conditions: feeding behavior, temperature preference, and nocturnal hypothermia in pigeons. Physiol Behav 51:353–361PubMedCrossRefGoogle Scholar
  59. Peiponen V (1966) The diurnal heterothermy of the Nightjar (Caprimulgus europaeus L.). Ann Acad Sci Fenn Ser A 101:1–35Google Scholar
  60. Peters RH (1983) The ecological implications of body size. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  61. Petherick JC, Waddington D (1991) Can domestic fowl (Gallus gallus domesticus) anticipate a period of food deprivation? Appl Anim Behav Sci 32:219–226CrossRefGoogle Scholar
  62. Phillips DL, Rashotte ME, Henderson RP (1991) Energetic responses of pigeons during food deprivation and restricted feeding. Physiol Behav 50:195–203PubMedCrossRefGoogle Scholar
  63. Phillips NH, Berger RJ (1991) Regulation of body temperature, metabolic rate, and sleep in fasting pigeons diurnally infused with glucose or saline. J Comp Physiol B 161:311–318PubMedCrossRefGoogle Scholar
  64. Prinzinger R, Pressmar A, Schleucher E (1991) Body temperature in birds. Comp Biochem Physiol A 99:499–506CrossRefGoogle Scholar
  65. Prinzinger R, Schleucher E, Pressmar A (1992) Long-term telemetry of body temperature with synchronous measurement of metabolic rate in torpid and non-torpid blue-naped mousebirds (Urocolius macrourus). J Orn 133:446–450CrossRefGoogle Scholar
  66. Prinzinger R, Siedle K (1988) Ontogeny of metabolism, thermoregulation and torpor in the house martin Delichon urbica urbica (L.) and its ecological significance. Oecologia 76:307–312CrossRefGoogle Scholar
  67. Rashotte ME, Basco PS, Henderson RP (1995) Daily cycles in body temperature, metabolic rate, and substrate utilization in pigeons: influence of amount and timing of food consumption. Physiol Behav 57:731–746PubMedCrossRefGoogle Scholar
  68. Rashotte ME, Geran LC (1997) Participation of gastrointestinal-load volume in “setting” the pigeon’s nocturnal body temperature. Naturwissenschaften 84:350–353CrossRefGoogle Scholar
  69. Rashotte ME, Pastukhov IF, Poliakov EL, Henderson RP (1998) Vigilance states and body temperature during the circadian cycle in fed and fasted pigeons (Columba livia). Am J Physiol Reg Int Comp Physiol 275:R1690–R1702Google Scholar
  70. Rashotte ME, Saarela S, Henderson RP, Hohtola E (1999) Shivering and digestion-related thermogenesis in pigeons during dark phase. Am J Physiol Reg Int Comp Physiol 277:R1579–R1587Google Scholar
  71. Reinertsen RE (1996) Physiological and ecological aspects of hypothermia. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman and Hall, New York, pp 125–157CrossRefGoogle Scholar
  72. Reinertsen RE, Bech C (1994) Hypothermia in pigeons: relating body temperature regulation to the gastrointestinal system. Naturwissenschaften 81:133–136PubMedCrossRefGoogle Scholar
  73. Reinertsen RE, Haftorn S (1984) Effect of short-term fasting on metabolism and nocturnal hypothermia in the willow tit, Parus montanus. J Comp Physiol B 154:23–28CrossRefGoogle Scholar
  74. Reinertsen RE, Haftorn S (1986) Different metabolic strategies of northern birds for nocturnal survival. J Comp Physiol B 156:655–664CrossRefGoogle Scholar
  75. Sartori DRS, Migliorini RH, Veiga JAS, Moura JL, Kettelhut IC, Linder C (1995) Metabolic adaptations induced by long-term fasting in quails. Comp Biochem Physiol 111A:487–493CrossRefGoogle Scholar
  76. Schaub R, Prinzinger R, Schleucher E (1999) Energy metabolism and body temperature in the Blue-naped Mousebird (Urocolius macrourus) during torpor. Ornis Fenn 76:211–219Google Scholar
  77. Schleucher E (2004) Torpor in birds: taxonomy, energetics, and ecology. Physiol Biochem Zool 77:942–949PubMedCrossRefGoogle Scholar
  78. Secor S (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56PubMedCrossRefGoogle Scholar
  79. Sherry DF, Mrosovsky N, Hogan JA (1980) Weight loss and anorexia during incubation in birds. J Comp Physiol Psychol 94:89–98CrossRefGoogle Scholar
  80. Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New HavenGoogle Scholar
  81. Simon E (1974) Temperature regulation: the spinal cord as a site of extrahypothalamic thermoregulatory functions. Rev Physiol Biochem Pharmacol 71:2–76Google Scholar
  82. Spée M, Marchal L, Thierry A-M, Chastel O, Enstipp M, Maho YL, Beaulieu M, Raclot T (2011) Exogenous corticosterone mimics a late fasting stage in captive Adélie penguins (Pygoscelis adeliae). Am J Physiol Reg Int Comp Physiol 300:R1241–R1249CrossRefGoogle Scholar
  83. Steen J (1958) Climatic adaptation in some small Northern birds. Ecol 39:625–629CrossRefGoogle Scholar
  84. Stokkan KA (1992) Energetics and adaptations to cold in ptarmigan in winter. Ornis Scand 23:366–370CrossRefGoogle Scholar
  85. Sulkava S (1969) On small birds spending the night in snow. Aquilo Ser Zool 7:33–37Google Scholar
  86. Swoap SJ, Rathvon M, Gutilla M (2007) AMP does not induce torpor. Am J Physiol Reg Int Comp Physiol 293:R468–R473CrossRefGoogle Scholar
  87. Thouzeau C, Duchamp C, Handrich Y (1999) Energy metabolism and body temperature of barn owls fasting in the cold. Physiol Biochem Zool 72:170–178PubMedCrossRefGoogle Scholar
  88. Underwood H, Steele CT, Zivkovic B (1999) Effects of fasting on the circadian body temperature rhythm of Japanese quail. Physiol Behav 66:137–143PubMedCrossRefGoogle Scholar
  89. Walker LE, Walker JM, Palca JW, Berger RJ (1983) A continuum of sleep and shallow torpor in fasting doves. Science 221:194–195Google Scholar
  90. Wall JP, Cockrem JF (2009) Effects of corticosterone treatment on responses to fasting in Japanese quail. Comp Biochem Physiol A 154:211–215Google Scholar
  91. Wang T, Hung CCY, Randall DJ (2006) The comparative physiology of food deprivation: From feast to famine. Annu Rev Physiol 68:223–251PubMedCrossRefGoogle Scholar
  92. Watanabe M, Houten SM, Mataki C, Christoffolete MA, Kim BW, Sato H, Messaddeq N, Harney JW, Ezaki O, Kodama T, Schoonjans K, Bianco AC, Auwerx J (2006) Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439:484–489PubMedCrossRefGoogle Scholar
  93. Welton NJ, Houston AI, Ekman J, McNamara JM (2002) A dynamic model of hypothermia as an adaptive response by small birds to winter conditions. Acta Biotheor 50:39–56PubMedCrossRefGoogle Scholar
  94. Westman W, Geiser F (2004) The effect of metabolic fuel availability on thermoregulation and torpor in a marsupial hibernator. J Comp Physiol B 174:49–57PubMedCrossRefGoogle Scholar
  95. Wojciechowski MS, Pinshow B (2009) Heterothermy in small, migrating passerine birds during stopover: use of hypothermia at rest accelerates fuel accumulation. J Exp Biol 212:3068–3075PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of BiologyUniversity of OuluOuluFinland

Personalised recommendations