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Energy metabolism during endurance flight and the post-flight recovery phase

Journal of Comparative Physiology A volume 203, pages 431–438 (2017)Cite this article

Abstract

Migrating birds are known to fly non-stop for thousands of kilometres without food or water intake and at a high metabolic rate thereby relying on energy stores which were built up preceding a flight bout. Hence, from a physiological point of view the metabolism of a migrant has to switch between an active fasting phase during flight and a fuelling phase during stopover. To meet the energetic and water requirements of endurance flight, migratory birds have to store an optimal fuel composition and they have to be able to quickly mobilize and deliver sufficient energy to the working flight muscles. After flight, birds have to recover from a strenuous exercise and sleeplessness, but, at the same time, they have to be alert to escape from predators and to prepare the next flight bout. In this overview, metabolic adaptations of free-ranging migrants to both phases will be presented and compared with results from windtunnel studies. The questions whether migratory strategy (long distance versus short distance) and diet composition influence the metabolic pathways will be discussed.

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References

  • Bairlein F, Fritz J, Scope A, Schwendenwein I, Stanclova G, van Dijk G, Meijer HA, Verhulst S, Dittami J (2015) Energy expenditure and metabolic changes of free-flying migrating northern bald ibis. PloS One doi:10.1371/journal.pone.0134433

    PubMed  PubMed Central  Google Scholar 

  • Bauchinger U, Biebach H (2001) Differential catabolism of muscle protein in Garden Warblers (Sylvia borin): flight and leg muscle act as a protein source during long-distance migration. J Comp Physiol B 171:293–301

    CAS  Article  PubMed  Google Scholar 

  • Beattie MA, Winder WW (1985) Attenuation of postexercise ketosis in fasted endurance-trained rats. Am J Physiol 248:R63–R67

    CAS  PubMed  Google Scholar 

  • Bishop CM, Butler PJ, El Hai AJ, Egginton S, Gabrielsen GW (1995) Development of metabolic enzyme activity in locomotor and cardiac muscles of the migratory Barnacle goose. Am J Physiol 269:R64–R72

    CAS  PubMed  Google Scholar 

  • Bishop CM, Butler PJ, El Hai AJ, Egginton S, Loonen MJJE (1996) The morphological development of the locomotor and cardiac muscles of the migratory Barnacle goose (Branta leucopsis). J Zool London 239:1–15

    Article  Google Scholar 

  • Bräu L, Nikolovski S, Palmer TN, Fournier PA (1999) Glycogen repletion following burst activity: a carbohydrate-sparing mechanism in animals adapted to arid environments. J Exp Zool 284:271–275

    Article  PubMed  Google Scholar 

  • Butler PJ, Woakes AJ, Bishop CM (1998) Behaviour and physiology of Svalbard barnacle geese Branta leucopsis during their autumn migration. J Avian Biol 29:536–545

    Article  Google Scholar 

  • Carlson LA, Ekelund L-G, Fröberg SO (1971) Concentration of triglycerides, phospholipids and glycogen in skeletal muscle and of FFAs and ß–hydroxybutyric acid in blood in man in response to exercise. Eur J Clin Investig 1:248–254

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  • Debussche M, Cortez J, Rimbault I (1987) Variation in fleshy fruit composition in the Mediterranean region: the importance of ripening season, life-form, fruit type and geographical distribution. Oikos 49:244–252

    Article  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Dohm GL, Beeker RT, Israel RG, Tapscott EB (1986) Metabolic responses to exercise after fasting. J Appl Physiol 61:1363–1368

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Féry F, Balasse EO (1983) Ketone body turnover during and after exercise in overnight-fasted and starved humans. Am J Physiol 245:E318–E325

    PubMed  Google Scholar 

  • Féry F, Plat L, Melot C, Balasse EO (1996) Role off at-derived substrates in the regulation of gluconeogenesis during fasting. Am J Physiol 270:E822–E830

    PubMed  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  Article  Google Scholar 

  • Gerson AR, Guglielmo CG (2011a) Endurance flight at low ambient humidity increases protein catabolism in migratory birds. Science 333:1434–1436

    CAS  Article  PubMed  Google Scholar 

  • Gerson AR, Guglielmo CG (2011b) House sparrows (Passer domesticus) increase protein catabolism in response to water restriction. Am J Regul Integr Comp Physiol 300:R925–R930

    CAS  Article  Google Scholar 

  • Gerson AR, Guglielmo CG (2013) Energetics and metabolite profiles during early flight in American robins (Turdus Migratorius). J Comp Physiol B 183:893–991

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gill RE, 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

    Article  PubMed  Google Scholar 

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

    Article  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

    Article  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  Article  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

    CAS  PubMed  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  Article  Google Scholar 

  • Hargreaves M, Kiens B, Richter EA (1991) Effect of increased fatty acid concentrations on muscle metabolism in exercising men. J Appl Physiol 70:194–201

    CAS  PubMed  Google Scholar 

  • Helge JW, Watt PW, Richter EA, Rennie MJ, Kiens B (2001) Fat utilization during exercise: adaptation to a fat-rich diet increases utilization of plasma fatty acids and very low density proteins-triacylglycerol in humans. J Physiol 537:1009–1020

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Herrera CM (1987) Vertebrate-dispersed plants of the Iberian peninsula: a study of fruit characteristics. Ecol Monogr 57:305–331

    Article  Google Scholar 

  • Hurley BF, Nemeth PM, Martin WH III, Hagberg JM, Dalsky GP, Holloszy JO (1986) Muscles triglyceride utilization during exercise: effect of training. J Appl Physiol 60:562–567

    CAS  PubMed  Google Scholar 

  • Izhaki I, Safriel UN (1989) Why are there so few exclusively frugivorous birds? Experiments on fruit digestibility. Oikos 54:23–32

    Article  Google Scholar 

  • Jenni L, Jenni-Eiermann S (1996) Metabolic responses to diurnal feeding patterns during the post-breeding, moulting and migratory periods in passerine birds. Funct Ecol 10:73–80

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Jenni-Eiermann S, Jenni L (1991) Metabolic responses to flight and fasting in night-migrating passerines. J Comp Physiol B 161:465–474

    Article  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  Article  Google Scholar 

  • Jenni-Eiermann S, Jenni L (1996) Metabolic differences between the postbreeding, moulting and migrator periods in feeding and fasting passerines. Funct Ecol 10:62–72

    Article  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Jenni-Eiermann S, Jenni L (2003) Interdependence off light 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, Heidelberg, pp 293–306

    Chapter  Google Scholar 

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

    PubMed  Google Scholar 

  • Johnson RH, Walton JL, Krebs HA, Williamson DH (1969) Metabolic fuels during and after severe exercise in athletes and non-athletes. Lancet 30:452–455

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Koeslag JH (1982) Post-exercise ketosis and the hormone response to exercise: a review. Med Sci Sports Exerc 14:327–334

    CAS  Article  PubMed  Google Scholar 

  • Lindgård K, Stokkan KA, Le Maho Y, Groscolas R (1992) Protein utilization during starvation in fat and lean Svalbard ptarmigan (Lagopus mutus hyperboreus). J Comp Physiol B 162:607–613

    Article  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

    Article  Google Scholar 

  • Maillet D, Weber JM (2006) Performance-enhancing role of dietary fatty acids in a long-distance migrant shorebird: the semipalmated sandpiper. J Exp Biol 209:2686–2695

    CAS  Article  PubMed  Google Scholar 

  • Maillet D, Weber JM (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

    CAS  Article  PubMed  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

    CAS  Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Mitchell GA, Kassovska-Bratinova S, Boukaftane Y, Robert MF, Wang SP, Ashmarina L, Lambert M, Lapierre P, Potier E (1995) Medical aspects of ketone metabolism. Clin Investig Med 18:192–216

    Google Scholar 

  • Parker GH, George JC (1975) Effects of short and long term exercise on intracellular glycogen and fat in pigeon pectoralis. Jpn J Physiol 25:175–184

    CAS  Article  PubMed  Google Scholar 

  • Pelsers MMAL, Butler PJ, Bishop CM et al (1999) Fatty acid binding protein in heart and skeletal muscles of the migratory barnacle goose throughout development. Am J Physiol 276:R637–R643

    CAS  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Peters Futre EM, Noakes TD, Raine RI, Terblanche SE (1987) Muscle glycogen repletion during active postexercise recovery. Am J Physiol 253:E305–E311

    CAS  PubMed  Google Scholar 

  • Pierce B, McWilliams SR, O’Connor TP et al (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

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  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

    Article  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

    CAS  Article  PubMed  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

    Article  Google Scholar 

  • Price ER, Guglielmo CG (2009) The effect of muscle phospholipid fatty acid composition on exercise performance: a direct test in the migratory white-throated sparrow (Zonotrichia albicollis). Am J Physiol Regul Integr Comp Physiol 297:R775–R782

    CAS  Article  PubMed  Google Scholar 

  • Roberts TJ, Weber JM, Hoppeler H et al (1996) Design of the oxygen and substrate pathways II. Defining the upper limits of carbohydrates and fat oxidation. J Exp Biol 199:1651–1658

    CAS  PubMed  Google Scholar 

  • Robin J-P, Cherel Y, Girard H, Géleon A, Le Maho Y (1987) Uric acid and urea in relation to protein catabolism in long-term fasting geese. J Comp Physiol B 157:491–499

    CAS  Article  PubMed  Google Scholar 

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

    Article  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

    CAS  PubMed  Google Scholar 

  • Salewski V, Kéry M, Herremans M, Liechti F, Jenni L (2009) Estimating fat and protein fuel from fat and muscle scores in passerines. Ibis (supporting information) 151:640–653

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Schmidt-Nielsen K (ed) (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

    Article  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

    Article  Google Scholar 

  • Videler JJ (ed) (2005) Avian flight. Oxford University Press, Oxford

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Volek JS, Noakes T, Phinney SD (2015) Rethinking fat as a fuel for endurance exercise. Eur J Sport Sci 15:13–20

    Article  PubMed  Google Scholar 

  • Volek JS, Freidenreich DJ, Saenz S, Kunces LJ, Creighton BC, Bartley JM, Davitt PM, Munoz CX, Anderson JM, Maresh CM, Lee EC, Schuenke MD, Aerni G, Kraemer WJ, Phinney SD (2016) Metabolic charcteristics of ket-adaptd ultra-endurance runners. Metab Clin Exp 65:100–110

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Weber JM (2009) The physiology of long-distance migration: extending the limits of endurance metabolism. J Exp Biol 212:593–597

    CAS  Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Weber JM, Brichon G, Zwingelstein G et al (1996b) Design of the oxygen and substrate pathways. IV. Partitioning energy provision from fatty acids. J Exp Biol 199:1667–1674

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Zhang Y, King MO, Harmon E, Eyster K, Swanson DL (2015) Migration-induced variation of fatty acid transporters and cellular metabolic intensity in passerine birds. J Comp Physiol B 185:797–810

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

The manuscript is based on data collected during more than 20 years of research. My special thanks and appreciation goes to Lukas Jenni with whom I planned and carried out all the studies together. I would also like to thank the former students Karen Falsone, Ivan Maggini, Michael Schaub and Regine Schwilch for their valuable contributions and the numerous helpers during field work. The studies were financed by the Swiss Ornithological Institute.

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    Susanne Jenni-Eiermann

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Correspondence to Susanne Jenni-Eiermann.

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Jenni-Eiermann, S. Energy metabolism during endurance flight and the post-flight recovery phase. J Comp Physiol A 203, 431–438 (2017). https://doi.org/10.1007/s00359-017-1150-3

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Keywords

  • Endurance exercise
  • Postexercise recovery
  • Fat metabolism
  • Diet
  • Postexercise ketosis