Skip to main content

Fasting in Birds: General Patterns and the Special Case of Endurance Flight

  • Chapter
  • First Online:
Comparative Physiology of Fasting, Starvation, and Food Limitation

Abstract

Birds undergo among the most extraordinary fasting events which may last up to several months as in breeding or moulting penguins during the subantarctic winter or more than 100 h during the migratory flight of bar-tailed godwits (Limosa lapponica) from Alaska to New Zealand across the Pacific ocean. In this review we demonstrate that it is the extraordinary ability of birds to extensively store and use lipids as the main energy source which allows them to fast for long periods during breeding, moulting, and migratory flight despite their high metabolic rates. Long-term fasting birds derive the largest part of the required energy (up to about 95%) from fat and only a minimum amount from protein. In contrast to mammalian running, birds maintain such a high proportion of energy derived from fat also during endurance flight. This is achieved by physiological adaptations during preparation, as well as for the catabolism of fatty acids during flight, such as extensive lipid storage and a specific upgrading of the transport system of fatty acids to the flight muscles and their oxidative capacity. Only little is known about the hormonal regulation of the metabolism during endurance flight, most of it related to the possible actions of the glucocorticoid hormone corticosterone. There are a number of trade-offs between competing physiological processes (e.g. between maximum fat catabolism and upgrading of the metabolic system or between oxygen transport and fuel transport) which likely are linked to the migration strategy of a bird.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alerstam T, Lindström Å (1990) Optimal bird migration: the relative importance of time, energy, and safety. In: Gwinner E (ed) Bird migration. Springer, Berlin

    Google Scholar 

  • Atkinson PW, Baker AJ, Bennett KA, Clark NA, Clark JA, Cole KB, Dekinga A, Dey A, Gillings S, Gonzalez PM, Kalasz K, Minton CDT, Newton J, Niles LJ, Piersma T, Robinson RA, Sitters HP (2007) Rates of mass gain and energy deposition in red knot on their final spring staging site is both time- and condition-dependent. J Appl Ecol 44:885–895

    Google Scholar 

  • Bairlein F (2002) How to get fat: nutritional mechanisms of seasonal fat accumulation in migratory songbirds. Naturwissenschaften 89:1–10

    PubMed  Google Scholar 

  • 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 267:191–195

    CAS  Google Scholar 

  • Battley PF, Dekinga A, Dietz MW, Piersma T, Tang S, Hulsman K (2001a) Basal metabolic rate declines during long-distance migratory flight in great knots. Condor 103:838–845

    Google Scholar 

  • Battley PF, Dietz MW, Piersma T, Dekinga A, Tang S, Hulsman K (2001b) Is long-distance flight equivalent to a high-energy fast? Body composition changes in freely migrating and captive fasting great knots. Physiol Biochem Zool 74:435–449

    PubMed  CAS  Google Scholar 

  • Bauchinger U, Williams SR (2010) Extent of phenotypic flexibility during long-distance flight is determined by tissue turnover rates: a new hypothesis. J Avian Biol 41:603–608

    Google Scholar 

  • Bernard SF, Thil M-A, Groscolas R (2003) Lipolytic and metabolic response to glucagon in fasting king penguins: Phase II vs. Phase III. Am J Physiol 284:R444–R454

    CAS  Google Scholar 

  • Berthold P (1996) Control of bird migration. Chapman & Hall, London

    Google Scholar 

  • Butler PJ, Woakes AJ (1990) The physiology of bird flight. In: Gwinner E (ed) Bird migration. Springer, Berlin, pp 300–318

    Google Scholar 

  • Butler PJ, Woakes AJ (2001) Seasonal hypothermia in a large migrant bird: saving energy for fat deposition? J Exp Biol 204:1361–1367

    PubMed  CAS  Google Scholar 

  • Callow M, Morton A, Guppy M (1986) Marathon fatigue: the role of plasma fatty acids, muscle glycogen and blood glucose. Eur J Appl Physiol 55:654–661

    CAS  Google Scholar 

  • Carmi N, Pinshow B, Porter WP, Jaeger J (1992) Water and energy limitations on flight duration in small migrating birds. Auk 109(2):268–276

    Google Scholar 

  • Carpenter FL, Hixon MA, Beuchat CA, Russell RW, Paton DC (1993) Biphasic mass gain in migrant hummingbirds: body composition changes, torpor, and ecological significance. Ecology 74:1173–1182

    Google Scholar 

  • Catard A, Weimerskirch H (1999) Satellite tracking of White-chinned petrels and comparison with other Procellariiformes. In: Adams NJ, Slotow RH (eds) Proceedings of 22nd International Ornithological Congress. Durban Johannesburg, BirdLife South Africa

    Google Scholar 

  • Cherel Y, Groscolas R (1999) Relationships between nutritient storage and nutritient utilisation in long-term fasting birds and mammals. In: Adams NJ, Slotow RH (eds) Proceedings of 22nd International Ornithological Congress. Durban Johannesburg, BirdLife South Africa

    Google Scholar 

  • Cherel Y, LeMaho Y (1985) Five months of fasting in king penguin chicks: body mass loss and fuel metabolism. Am J Physiol 249:R387–R392

    PubMed  CAS  Google Scholar 

  • Cherel Y, Robin J-P, LeMaho Y (1988a) Physiology and biochemistry of long-term fasting in birds. Can J Zool 66:159–166

    CAS  Google Scholar 

  • Cherel Y, Robin J-P, Walch O, Karmann H, Netchitaiko P, LeMaho Y (1988b) Fasting in king penguin. I. Hormonal and metabolic changes during breeding. Am J Physiol 254:R170–R177

    PubMed  CAS  Google Scholar 

  • Cherel Y, Charassin J-B, Handrich Y (1993) Comparison of body reserve buildup in prefasting chicks and adults of king penguins (Aptenodytes patagonicus). Physiol Zool 66:750–770

    Google Scholar 

  • Cherel Y, Charassin J-B, Challet E (1994) Energy and protein requirements for molt in the king penguin Aptenodytes patagonicus. Am J Physiol 266:R1182–R1188

    PubMed  CAS  Google Scholar 

  • Costantini D, Cardinale M, Carere C (2007) Oxidative damage and anti-oxidant capacity in two migratory bird species at a stop-over site. Comp Biochem Physiol C 144:363–371

    Google Scholar 

  • Cresswell W (1998) Diurnal and seasonal mass starvation in blackbirds Turdus merula: consequences for mass-dependent predation risk. J Anim Ecol 67:78–90

    Google Scholar 

  • Decuypere E, Kuhn ER, Chadwick A (1985) Rhythms in circulating prolactin and thyroid hormones in the early postnatal life of the domestic fowl: influence of fasting and feeding on thyroid rhythmicity. In: Follett BK, Ishii S, Chandola A (eds) The endocrine system and the environment. Springer, Berlin

    Google Scholar 

  • Dohm GL (1986) Protein as a fuel for endurance exercise. Exercise Sport Sci Rev 14:143–173

    CAS  Google Scholar 

  • Driedzic WR, Crowe HL, Hicklin PW, Sephton DH (1993) Adaptation in pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can J Zool 71:1602–1608

    Google Scholar 

  • Engel S, Biebach H, Visser GH (2006) Water and heat balance during flight in the rose-coloured starling (Sturnus roseus). Physiol Biochem Zool 79:763–774

    PubMed  Google Scholar 

  • Falsone K, Jenni-Eiermann S, Jenni L (2009) Corticosterone in migrating songbirds during endurance flight. Horm Behav 56:548–556

    PubMed  CAS  Google Scholar 

  • Fox, AD, King R (2011) Body mass loss amongst moulting Pochard Aythya ferina and Tufted duck A. fuligula at Abberton reservoir, south east England. J Ornithol doi:10.1007/s10336-011-0656-7

  • Fransson T, Barboutis C, Mellroth R, Akriotis T (2008) When and where to fuel before crossing the Sahara desert - extended stopover and migratory fuelling in first-year garden warbler Silvia borin. J Avian Biol 39:133–138

    Google Scholar 

  • Gannes LZ, Hatch KA, Pinshow B (2001) How does time since feeding affect the fuels pigeons use during flight? Physiol Biochem Zool 74:1–10

    PubMed  CAS  Google Scholar 

  • Gauthier G, Bêty J, Hobson KA (2003) Are greater snow geese capital breeders? New evidence from a stable isotope model. Ecology 84:3250–3264

    Google Scholar 

  • George JC, Berger JC (1966) Avian myology. Academic Press London

    Google Scholar 

  • George JC, John TM (1993) Flight effects on certain blood parameters in homing pigeons (Columba livia). Comp Biochem Physiol 106A:707–712

    CAS  Google Scholar 

  • Gerson AR, Guglielmo CG (2010) House sparrows (Passer domesticus) increase protein catabolism in response to water restriction. Am J Physiol 300:R925–R930

    Google Scholar 

  • Giladi I, Pinshow B (1999) Evaporative and excretory water loss during free flight in pigeons. J Comp Physiol B 169:311–318

    Google Scholar 

  • Gill RE Jr, Tibbitts TL, Douglas DC, Handel CM, Mulcahy DM, Gottschalck JC, Warnock N, McCaffery BJ, Battley PF, Piersma T (2009) Extreme endurance flights by landbirds crossing the Pacific ocean: ecological corridor rather than barrier? Proc R Soc B 276:447–457

    PubMed  Google Scholar 

  • Groscolas R (1982) Changes in plasma lipids during breeding, molting, and starvation in male and female Emperor penguins (Aptenodytes forsteri). Physiol Zool 55:45–55

    CAS  Google Scholar 

  • Groscolas R (1986) Changes in body mass, body temperature and plasma fuel levels during natural breeding fast in male and female emperor penguin Aptenodytes forsteri. J Comp Biochem B 156:521–527

    Google Scholar 

  • Groscolas R (1990) Metabolic adaptations to fasting in Emperor and King penguins. In: Davis LS, Darby JT (eds) Penguin Biology, Academic Press, Inc

    Google Scholar 

  • Groscolas R, Cherel Y (1992) How to molt while fasting in the cold: the metabolic and hormonal adaptations of Emperor and King penguins. Orn Scand 23:328–334

    Google Scholar 

  • Guglielmo CG (2010) Move that fatty acid: fuel selection and transport in migratory birds and bats. Integr Comp Biol 50:336–345

    PubMed  Google Scholar 

  • Guglielmo CG, Williams TD (2003) Phenotypic flexibility of body composition in relation to migratory stage, age, and sex in the Western sandpiper (Calidris mauri). Physiol Biochem Zool 76:84–98

    PubMed  Google Scholar 

  • Guglielmo CG, Haunerland NH, Williams TD (1998) Fatty acid binding protein, a major protein in the flight muscle of the Western Sandpiper. Comp Biochem Physiol 119B:549–555

    CAS  Google Scholar 

  • Guglielmo CG, Piersma T, Williams TD (2001) A sport-physiological perspective on bird migration: evidence for flight-induced muscle damage. J Exp Biol 204:2683–2690

    PubMed  CAS  Google Scholar 

  • Guglielmo CG, Haunerland NH, Hochachka PW, Williams TD (2002) Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a long-distance migrant shorebird. Am J Physiol Regul Intgr Comp Physiol 282:R1405–R1413

    CAS  Google Scholar 

  • Gwinner E, Zeman M, Schwabl-Benzinger I, Jenni-Eiermann S, Jenni L, Schwabl H (1992) Corticosterone levels of passerine birds during migratory flight. Naturwissenschaften 79:276–278

    CAS  Google Scholar 

  • Haase E, Rees A, Harvey S (1986) Flight stimulates adrenocortical activity in pigeons (Columba livia). Gen Comp Endocrinol 61:424–427

    PubMed  CAS  Google Scholar 

  • Harvey S, Phillips JG (1982) Adrenocortical responses of ducks to treadmill exercise. J Endocrinol 94:141–146

    PubMed  CAS  Google Scholar 

  • Hasselquist D, Lindström Å, Jenni-Eiermann S, Koolhaas A, Piersma T (2007) Long flights do not influence immune responses of a long-distance migrant bird: a wind-tunnel experiment. J Exp Biol 210:1123–1131

    PubMed  Google Scholar 

  • Holberton RL (1999) Changes in patterns of corticosterone secretion concurrent with migratory fattening in a neotropical migratory bird. Gen Comp Endocrinol 116:49–58

    PubMed  CAS  Google Scholar 

  • Holberton RL, Helmuth B, Wingfield JC (1996) The corticosterone stress response in Gentoo and King Penguins during the non-fasting period. Condor 98:850–854

    Google Scholar 

  • Holberton RL, Boswell T, Hunter MJ (2008) Circulating prolactin and corticosterone concentrations during the development of migratory condition in the dark-eyed junco, Junco hyemalis. Gen Comp Endocrinol 155:641–649

    PubMed  CAS  Google Scholar 

  • Jenni L, Jenni-Eiermann S (1987) Body weight and energy reserves of Bramblings in winter. Ardea 75:271–284

    Google Scholar 

  • Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biol 29:521–528

    Google Scholar 

  • Jenni L, Jenni-Eiermann S (1999) Fat and protein utilisation during migratory flight. In: Adams NJ, Slotow RH (eds) Proceedings of 22nd international ornithological congress, Durban Johannesburg, BirdLife South Africa

    Google Scholar 

  • Jenni L, Jenni-Eiermann S, Spina F, Schwabl H (2000) Regulation of protein breakdown and adrenocortical response to stress in birds during migratory flight. Am J Physiol 278:R1182–R1189

    CAS  Google Scholar 

  • 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 65:112–123

    CAS  Google Scholar 

  • Jenni-Eiermann S, Jenni L (2001) Postexercise ketosis in night-migrating passerine birds. Physiol Biochem Zool 74:90–101

    PubMed  CAS  Google Scholar 

  • Jenni-Eiermann S, Jenni L (2003) Interdependence of flight and stopover in migrating birds: possible effects of metabolic constraints during refuelling on flight metabolism. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer Berlin

    Google Scholar 

  • Jenni-Eiermann S, Jenni l, Kvist A, Lindström Å, Piersma T, Visser GH (2002a) Fuel use and metabolic response to endurance exercise: a windtunnel study of a long-distance migrating shorebird. J Exp Biol 205:2453–2460

    Google Scholar 

  • Jenni-Eiermann S, Jenni L, Piersma T (2002b) Temporal uncoupling of thyroid hormones in Red Knots: T3 peaks in cold weather, T4 during moult. J Ornithol 143:331–340

    Google Scholar 

  • Jenni-Eiermann S, Hasselquist D, Lindström Å, Koolhaas A, Piersma T (2009) Are birds stressed during long-term flights? A windtunnel study on circulating corticosterone in the red knot Gen Comp Endocrinol 164:101–106

    CAS  Google Scholar 

  • Jenni-Eiermann S, Almasi B, Maggini I, Salewski V, Bruderer B, Liechti F, Jenni L (2011) Numbers, foraging and fattening of passerine migrants at a stopover site in the western Sahara: diverse strategies to cross a desert. J Ornithol 152:113–128. doi:10.1007/s10336-010-0572-2

    Google Scholar 

  • John TM, George JC (1973) Effect of prolonged exercise on levels of plasma glucose, free fatty acids and corticosterone and muscle free fatty acids in the pigeon. Arch int Physiol Biochem 81:421–425

    CAS  Google Scholar 

  • Kettelhut IC, Wing SS, Goldberg AL (1988) Endocrine regulation of protein breakdown in skeletal muscle. Diabetes Metab Rev 4:751–772

    PubMed  CAS  Google Scholar 

  • Kirkpinar F, Oguz I (1995) Influence of various dietary protein levels on carcass composition in the male Japanese quail (Coturnix coturnix japonica). Brit Poult Sci 36:605–610

    CAS  Google Scholar 

  • Klaassen M (1996) Metabolic constraints on long-distance migration in birds. J Exp Biol 199:57–64

    PubMed  Google Scholar 

  • Klaassen M (2003) Relationships between migration and breeding strategies in Arctic breeding birds. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer Berlin

    Google Scholar 

  • 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 70:125–133

    PubMed  CAS  Google Scholar 

  • Klaassen M, Kvist A, Lindström Å (2000) Flight costs and fuel composition of a bird migrating in a wind tunnel. Condor 102:444–451

    Google Scholar 

  • Kullberg C, Fransson T, Jakobsson S (1996) Impaired predator evasion in fat blackcaps (Sylvia atricapilla). Proc R Soc London B 263:1671–1675

    Google Scholar 

  • Landys MM, Wingfield JC, Ramenofsky M (2004a) Plasma corticosterone increases during migratory restlessness in the captive white-crowned sparrow Zonotrichia leucophrys gambelii. Horm Behav 46:574–5810

    PubMed  CAS  Google Scholar 

  • Landys MM, Piersma T, Ramenofsky M, Wingfield JC (2004b) Role of the low affinity glucocorticoid receptor in the regulation of behaviour and energy metabolism in the migratory red knot Calidris canutus islandica. Physiol Biochem Zool 77:658–666

    PubMed  CAS  Google Scholar 

  • Landys MM, Ramenofsky M, Guglielmo CG, Wingfield JC (2004c) The low-affinity glucocorticoid receptor regulates feeding and lipid breakdown in the migratory Gambel’s white-crowned sparrow Zonotrichia leucophrys gambelii. J Exp Biol 207:143–154

    PubMed  CAS  Google Scholar 

  • Landys-Cianelli MM, Ramenofsky M, Piersma T, Jukema J, Group CastricumRinging, Wingfield JC (2002) Baseline and stress-induced plasma corticosterone during long-distance migration in the bar-tailed godwit, Limosa lapponica. Physiol Biochem Zool 75:101–110

    Google Scholar 

  • 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 17:151–179

    Google Scholar 

  • LeMaho Y, Van Kahn HV, Koubi H, Dewasmes G, Girard J, Ferré P, Cagnard M (1981) Body composition, energy expenditure, and plasma metabolites in long-term fasting geese. Am J Physiol 241:E342–E354

    CAS  Google Scholar 

  • Lindström Å, Piersma T (1993) Mass changes in migrating birds: the evidence for fat and protein storage re-examined. Ibis 135:70–78

    Google Scholar 

  • Long JA, Holberton RL (2004) Corticosterone secretion, energetic condition, and a test of the migration modulation hypothesis in the hermit thrush (Catharus guttatus), a short-distance migrant. Auk 121:1094–1102

    Google Scholar 

  • Lundgren BO, Kiessling KH (1985) Seasonal variation in catabolic enzyme activities in breast muscle of some migratory birds. Oecologia 66:468–471

    Google Scholar 

  • Lundgren BO, Kiessling KH (1988) Comparative aspects of fibre types, areas, and capillary supply in the pectoralis muscle. J Comp Physiol B 158:165–173

    Google Scholar 

  • Macleod R, Barnett P, Clark JA, Cresswell W (2005) Body mass change strategies in blackbirds Turdus merula: the starvation-predation risk trade-off. J Anim Ecol 74:292–302

    Google Scholar 

  • Maillet D, Weber J-M (2007) Relationship between n-3 PUFA content and energy metabolism in the flight muscles of a migrant shorebird: evidence for natural doping. J Exp Biol 210:413–423

    PubMed  CAS  Google Scholar 

  • Marsh RL (1983) Adaptations of the Gray Catbird (Dumetella carolinensis) to long distance migration: energy stores and substrate concentrations in plasma. Auk 100:170–179

    Google Scholar 

  • McFarlan JT, Bonen A, Guglielmo CG (2009) Seasonal up-regulation of protein mediated fatty acid transport in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J Exp Biol 212:2934–2940

    PubMed  CAS  Google Scholar 

  • McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses: a review. Condor 104:705–724

    Google Scholar 

  • McWilliams SE, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393

    Google Scholar 

  • Mrosovsky N, Sherry DF (1980) Animal anorexias. Science 207:837–842

    PubMed  CAS  Google Scholar 

  • Pant K, Chandola-Saklani A (1993) A role for thyroid hormones in the development of premigratory disposition in redheaded bunting, Emberiza bruniceps. J Comp Physiol 163B:389–394

    Google Scholar 

  • Parker H, Holm H (1990) Patterns of nutrition and energy expenditure in female common eiders nesting in the high Arctic. Auk 107:660–668

    Google Scholar 

  • 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–R643

    PubMed  CAS  Google Scholar 

  • Pennycuick CJ (1998) Computer simulation of fat and muscle burn in long-distance bird migration. J Theor Biol 191:47–61

    PubMed  Google Scholar 

  • Pierce B, McWilliams SR, O’Connor TP, Place AR, Guglielmo CG (2005) Effect of dietary fatty acid composition on depot fat and exercise performance in a migrating songbird, the red-eyed vireo. J Exp Biol 208:1277–1285

    PubMed  CAS  Google Scholar 

  • Piersma T (1988) Breast muscle atrophy and constraints on foraging during the flightless period of wing moulting Great Crested Grebes. Ardea 76:96–106

    Google Scholar 

  • Piersma T, Gill RE Jr (1998) Guts don’t fly: small digestive organs in obese Bar-tailed Godwits. Auk 115:196–203

    Google Scholar 

  • Piersma T, Lindström Å (1997) Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol Evol 12:134–138

    PubMed  CAS  Google Scholar 

  • Piersma T, Everaarts JM, Jukema J (1996) Build-up of red blood cells in refuelling Bar-tailed Godwits in relation to individual migratory quality. Condor 98:363–370

    Google Scholar 

  • 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 72:405–415

    PubMed  CAS  Google Scholar 

  • Piersma T, Reneerkens J, Ramenofsky M (2000) Baseline corticosterone peaks in shorebirds with maximal energy stores for migration: a general preparatory mechanism for rapid behavioral and metabolic transitions? Gen Comp Endocrinol 120:118–126

    CAS  Google Scholar 

  • Piersma T, Brugge M, Spaans B, Battley PF (2008) Endogenous circannual rhythmicity in body mass, molt, and plumage of great knots Calidris tenuirostris. Auk 125:140–148

    Google Scholar 

  • Price ER (2010) Dietary lipid composition and avian migratory flight performance: development of a theoretical framework for avian fat storage. Comp Biochem Physiol A 157:297–309

    Google Scholar 

  • Rees A, Harvey S (1987) Adrenocortical responses of pigeons (Columba livia) to treadwheel exercise. Gen Comp Endocrinol 65:117–120

    PubMed  CAS  Google Scholar 

  • Reinertsen RE (1996) Physiological and ecological aspects of hypothermia. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman and Hall, New York

    Google Scholar 

  • Reneerkens J, Morrison RIG, Ramenofsky M, Piersma T, Wingfield JC (2002) Baseline and stress-induced levels of corticosterone during different life cycle substages in a shorebird on the high arctic breeding grounds. Physiol Biochem Zool 75:200–208

    PubMed  CAS  Google Scholar 

  • Roberts TJ, Weber J-M, Hoppeler H, Weibel ER, Taylor CR (1996) Design of the oxygen and substrate pathways II. Defining the upper limits of carbohydrates and fat oxidation. J Exp Biol 199:1651–1658

    PubMed  CAS  Google Scholar 

  • Robin J-P, Boucontet L, Chillet P, Groscolas R (1998) Behavioral changes in fasting emperor penguins: evidence for a “refeeding signal” linked to a metabolic shift. Am J Physiol 274:R746–R753

    PubMed  CAS  Google Scholar 

  • Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24

    PubMed  CAS  Google Scholar 

  • Romero LM, Ramenofsky M, Wingfield JC (1997) Season and migration alters the corticosterone response to capture and handling in an arctic migrant, the white-crowned sparrow (Zonotrichia leucophrys gambelii). Gen Comp Endocrinol 116C:171–177

    CAS  Google Scholar 

  • Rosebrough RW, McMurtry JP (1993) Protein and energy relationships in the broiler chicken. 11. Effects of protein quantity and quality on metabolism. Brit J Nutr 70:667–678

    PubMed  CAS  Google Scholar 

  • Rothe HJ, Biesel W, Nachtigall W (1987) Pigeon flight in a wind tunnel. II. Gas exchange and power requirements. J Comp Physiol B 157:99–109

    Google Scholar 

  • Sahlin K, Katz A, Broberg S (1990) Tricarboxylic acid cycle intermediates in human muscle during prolonged exercise. Am J Physiol 259:C834–C841

    PubMed  CAS  Google Scholar 

  • 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:487–493

    CAS  Google Scholar 

  • Schaub M, Jenni L (2000) Body mass of six long-distance migrant passerine species along the autumn migration route. J Ornithol 141:441–460

    Google Scholar 

  • Schmaljohann H, Liechti F, Bruderer B (2007) Songbird migration across the Sahara: the non-stop hypothesis rejected! Proc R Soc B 274:735–739

    PubMed  Google Scholar 

  • Schmaljohann H, Bruderer B, Liechti F (2008) Sustained bird flights occur at temperatures far beyond expected limits. Anim Behav 76:1133–1138

    Google Scholar 

  • Schmidt-Nielsen K (1984) Scaling: why is animal size so important?. Cambridge University Press, Cambridge

    Google Scholar 

  • Schwilch R, Jenni L, Jenni-Eiermann S (1996) Metabolic responses of homing pigeons to flight and subsequent recovery. J Comp Physiol B 166:77–87

    Google Scholar 

  • Schwilch R, Grattarola A, Spina F, Jenni L (2002a) Protein loss during long-distance flight in passerine birds: adaptation and constraint. J Exp Biol 205:687–695

    PubMed  CAS  Google Scholar 

  • Schwilch R, Piersma T, Holmgren NMA, Jenni L (2002b) Do migrants need a nap after a long non-stop flight? Ardea 90:149–154

    Google Scholar 

  • Scott I, Evans PR (1992) The metabolic output of avian (Sturnus vulgaris, Calidris alpina) adipose tissue liver and skeletal muscle: implications for BMR/body mass relationships. Comp Biochem Physiol 103A:329–332

    Google Scholar 

  • Silverin B, Viebke PA, Westin J, Scanes CG (1989) Seasonal changes in body weight, fat depots, and plasma levels of thyroxine and growth hormone in free-living great tits (Parus major) and willow tits (P. montanus). Gen Comp Endocrinol 73:404–416

    PubMed  CAS  Google Scholar 

  • Starck JM (1999) Structural flexibility of the gastro-intestinal tract of vertebrates—implications for evolutionary morphology. Zool Anz 238:87–101

    Google Scholar 

  • Swain SD (1991) Flight muscle catabolism during overnight fasting in a passerine bird, Eremophila alpestris. J Comp Biochem B 162:383–392

    CAS  Google Scholar 

  • Thouzeau C, Massemin S, Handrich Y (1997) Bone marrow fat mobilization in relation to lipid and protein catabolism during prolonged fasting in barn owls. J Comp Physiol B 167:17–24

    CAS  Google Scholar 

  • Vaillancourt E, Prud’Homme S, Haman F, Guglielmo CG, Weber JM (2005) Energetics of a long-distance migrant shorebird (Philomachus pugnax) during cold exposure and running. J Exp Biol 208:317–325

    PubMed  Google Scholar 

  • van den Hout PJ, Mathot KJ, Maas LRM, Piersma T (2010) Predator escape tactics in birds: linking ecology and aerodynamics. Behav Ecol 21:16–25

    Google Scholar 

  • van der Meer J, Piersma T (1994) Physiologically inspired regression models for estimating and predicting nutrient stores and their composition in birds. Physiol Zool 67:305–329

    Google Scholar 

  • Videler JJ (2005) Avian Flight Oxford University Press

    Google Scholar 

  • Vock R, Weibel ER, Hoppeler H, Ordway G, Weber JM, Taylor CR (1996) Design of the oxygen and substrate pathways. V. Structural basis of vascular substrate supply to muscle cells. J Exp Biol 199:1675–1688

    PubMed  CAS  Google Scholar 

  • Waugh SM, Weimerskirch H (2003) Environmental heterogeneity and the evolution of foraging behaviour in long ranging greater albatrosses. Oikos 103:374–384

    Google Scholar 

  • Weber JM (1992) Pathways for oxidative fuel provision to working muscles: ecological consequences of maximal supply limitations. Experientia 48:557–564

    PubMed  CAS  Google Scholar 

  • Weber JM, Roberts TJ, Vock R, Weibel ER, Taylor CR (1996a) Design of the oxygen and substrate pathways. III Partitioning energy provision from carbohydrates. J Exp Biol 199:1659–1666

    PubMed  CAS  Google Scholar 

  • Weber JM, Brichon G, Zwingelstein G, McClelland G, Saucedo C, Weibel ER, Taylor CR (1996b) Design of the oxygen and substrate pathways. IV. Partitioning energy provision from fatty acids. J Exp Biol 199:1667–1674

    PubMed  CAS  Google Scholar 

  • Williams JB (1996) Energetics of avian incubation. In: Carey C (ed) Avian energetics and nutritional ecology, Chapman & Hall, New York

    Google Scholar 

  • Williams TD, Ghebremeskel K, Williams G, Crawford MA (1992) Breeding and moulting fasts in macaroni penguins: do birds exhaust their fat reserves? Comp Biochem Physiol 103A:783–785

    CAS  Google Scholar 

  • Williamson RA, Misson BH, Davison TF (1985) The effect of exposure to 40° on the heat production and the serum concentrations of triiodthyronine, thyroxine, and corticosterone in immature domestic fowl. Gen Comp Endocrinol 60:178–186

    PubMed  CAS  Google Scholar 

  • Wingfield JC (2003) Avian migration: regulation of facultative-type movements. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer, Heidelberg

    Google Scholar 

  • Wojciechowski MS, Pinshow B (2009) Heterothermy in small, migrating passerine birds during stopover: use of hypothermia at rest accelerates fuel accumulation. J Exp Biol 212:3068–3075

    PubMed  Google Scholar 

  • Wolfe RR, Klein S, Carraro F, Weber JM (1990) Role of triglyceride-fatty acid cycle in controlling fat metabolism in humans during and after exercise. Am J Physiol 258:E382–E389

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Marshall McCue for inviting us to write this review and for helpful comments. We thank Tony Fox for providing literature about fasting of waterfowl during moult and Chris Guglielmo and Theunis Piersma for constructive comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Susanne Jenni-Eiermann .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Jenni-Eiermann, S., Jenni, L. (2012). Fasting in Birds: General Patterns and the Special Case of Endurance Flight. In: McCue, M. (eds) Comparative Physiology of Fasting, Starvation, and Food Limitation. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-29056-5_11

Download citation

Publish with us

Policies and ethics