Skip to main content
Log in

Power and metabolic scope of bird flight: a phylogenetic analysis of biomechanical predictions

  • Short Communication
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

For flying animals aerodynamic theory predicts that mechanical power required to fly scales as P ∝ m 7/6 in a series of isometric birds, and that the flight metabolic scope (P/BMR; BMR is basal metabolic rate) scales as P scope ∝ m 5/12. I tested these predictions by using phylogenetic independent contrasts from a set of 20 bird species, where flight metabolic rate was measured during laboratory conditions (mainly in wind tunnels). The body mass scaling exponent for P was 0.90, significantly lower than the predicted 7/6. This is partially due to the fact that real birds show an allometric scaling of wing span, which reduces flight cost. P scope was estimated using direct measurements of BMR in combination with allometric equations. The body mass scaling of P scope ranged between 0.31 and 0.51 for three data sets, respectively, and none differed significantly from the prediction of 5/12. Body mass scaling exponents of P scope differed significantly from 0 in all cases, and so P scope showed a positive body mass scaling in birds in accordance with the prediction.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig 3

Abbreviations

A :

equivalent flat plate area

A 1 :

field resting metabolic rate

A 2 :

metabolic rate of arbitrary non-foraging behaviour

b :

wing span

BMR:

basal metabolic rate

C :

rate of energy consumption during foraging

E :

gross energy intake

g :

acceleration due to gravity

k :

induced drag factor

K :

metabolic ceiling

m, m 0 :

body mass

P :

mechanical power required to fly

P dep :

rate of energy accumulation

P flight :

flight metabolic rate

P mp :

mechanical power required to fly at minimum power speed

P scope :

flight metabolic scope

RMR:

resting metabolic rate

S d :

wing disc area (πb 2/4)

t 1, t 2 :

time periods

U :

flight speed through the air

U migr :

overall migration speed

λ :

phylogenetic dependence

ρ :

air density

ΔT 50H:

temperature at 50% DNA dissociation in DNA–DNA hybridization

References

  • Aschoff J, Pohl H (1970) Der Ruheumsatz von Vögeln als Funktion der Tagezeit und der Körpergrösse. J Ornithol 111:38–47

    Article  Google Scholar 

  • Askew EN, Ellerby DJ (2007) The mechanical power requirements of avian flight. Biol Lett 3:445–448

    Article  PubMed  CAS  Google Scholar 

  • Bennett PM, Owens, IPF (2002) Evolutionary ecology of birds. Oxford University Press

  • Berger M (1985) Sauerstoffverbrauch von Kolibris (Colibri coruscans und C. thallassinus) beim Horizontalflug. In: Nachtigall W (ed) Bird flight, Biona report 3. Gustav Fischer, Stuttgart, pp 307–314

    Google Scholar 

  • Berger M, Hart JS, Roy OZ (1970) Respiration, oxygen consumption and heart rate in some birds during rest and flight. Z Vergl Physiol 66:201–214

    Article  Google Scholar 

  • Bernstein MH, Thomas SP, Schmidt-Nielsen K (1973) Power input during flight of the fish crow, Corvus ossifragus. J Exp Biol 58:401–410

    Google Scholar 

  • Bishop CM (1999) The maximum oxygen consumption and aerobic scope of birds and mammals: getting to the heart of the matter. Proc R Soc Lond B 266:2275–2281

    Article  CAS  Google Scholar 

  • Butler PJ, Bishop CM (2000) Flight. In: Whittow GC (ed) Sturkies’s avian physiology, 5th edn. Academic Press, New York, pp 391–435

    Google Scholar 

  • Ellington CP (1991) Limitations on animal flight performance. J Exp Biol 160:71–91

    Google Scholar 

  • Engel S, Biebach H, Visser GH (2006) Metabolic costs of avian flight in relation to flight velocity: a study in rose coloured starlings (Sturnus roseus, Linnaeus). J Comp Physiol B 176:415–427

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    Article  Google Scholar 

  • Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Article  Google Scholar 

  • Garland T Jr, Ives AR (2000) Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am Nat 155:346–364

    Article  Google Scholar 

  • Garland T Jr, Midford PE, Jones JA, Dickerman AW, Diaz-Uriarte R (2002) PDAP: phenotypic diversity analysis programs. Ver. 6.0.

  • Gessaman JA (1980) An evaluation of heart rate as an indirect measure of daily energy metabolism of the American kestrel. Comp Biochem Physiol 65A:273–289

    Article  Google Scholar 

  • Hainsworth FR, Wolf LL (1970) Regulation of oxygen consumption and body temperature during torpor in a hummingbird, Eulampis jugularis. Science 168:368–369

    Article  PubMed  CAS  Google Scholar 

  • Hammond KA, Diamond J (1997) Maximal sustained energy budgets in humans and animals. Nature 386:457–462

    Article  PubMed  CAS  Google Scholar 

  • Haus C (2001) Flugkosten von Rauchschwalben (Hirundo rustica) in Abhängigkeit von ihrer Körpermasse. Master thesis, Munich University

    Google Scholar 

  • Hedenström A (2002) Aerodynamics, evolution and ecology of bird flight. Trends Ecol Evol 17:415–422

    Article  Google Scholar 

  • Hedenström A (2003) Scaling migration speed in animals that run, swim and fly. J Zool 259:155–160

    Article  Google Scholar 

  • Hedenström A, Alerstam T (1995) Optimal flight speed of birds. Phil Trans R Soc Lond B 348:471–487

    Article  Google Scholar 

  • Hedenström A, Alerstam T (1997) Optimum fuel loads in migratory birds: distinguishing between time and energy minimization. J Theor Biol 189:227–234

    Article  PubMed  Google Scholar 

  • Hedenström A, Alerstam T (1998) How fast can birds migrate? J Avian Biol 29:424–432

    Article  Google Scholar 

  • Hudson DM, Bernstein MH (1983) Gas exchange and energy cost of flight in the white-necked raven, Corvus cryptoleucus. J Exp Biol 103:121–130

    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

    Article  Google Scholar 

  • Kleiber M (1961) The fire of life. Wiley, New York

    Google Scholar 

  • Kvist A, Klaassen M, Lindström Å (1998) Energy expenditure in relation to flight speed: what is the power of mass loss rate estimates? J Avian Biol 29:485–498

    Article  Google Scholar 

  • Kvist A, Lindström Å, Green M, Piersma T, Visser GH (2001) Carrying large fuel loads during sustained bird flight is cheaper than expected. Nature 413:730–732

    Article  PubMed  CAS  Google Scholar 

  • Lasiewski RC (1963) Oxygen consumption of torpid, resting, active, and flying hummingbirds. Physiol Zool 36:122–140

    CAS  Google Scholar 

  • Lighthill J (1977) Introduction to the scaling of animal locomotion. In: Pedley TJ (ed) Scale effects in animal locomotion. Academic Press, London, pp 365–404

    Google Scholar 

  • Lindström Å (1991) Maximum fat deposition rates in migrating birds. Ornis Scand 22:12–19

    Article  Google Scholar 

  • 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 13:352–359

    Article  Google Scholar 

  • 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 35:377–393

    Article  Google Scholar 

  • Masman D, Klaassen M (1987) Energy expenditure during free flight in trained and free-living Eurasian kestrels (Falco tinnunculus). Auk 104:603–616

    Google Scholar 

  • Norberg UM (1996) Energetics of flight. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman & Hall, New York, pp 199–249

    Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    Article  PubMed  CAS  Google Scholar 

  • Pennyuick CJ (1975) Mechanics of flight. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol. 5. Academic Press, New York, pp 1–75

    Google Scholar 

  • Pennyuick CJ (1978) Fifteen testable predictions about bird flight. Oikos 30:165–176

    Article  Google Scholar 

  • Pennyuick CJ (1992) Newton rules biology: a physical approach to biological problems. Oxford University Press, Oxford

    Google Scholar 

  • Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge

    Google Scholar 

  • Rayner JMV (1988) Form and function in avian flight. Curr Ornithol 5:1–66

    Google Scholar 

  • Reynolds PS, Lee RMIII (1996) Phylogenetic analysis of avian energetics: passerines and nonpasserines do not differ. Am Nat 147:735–759

    Article  Google Scholar 

  • 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 205:101–107

    PubMed  Google Scholar 

  • Ricklefs RE, Konarzewski M, Daan S (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147:1047–1071

    Article  Google Scholar 

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

    Google Scholar 

  • Schmidt-Nielsen K (1984) Scaling. Cambridge University Press, Cambridge

    Google Scholar 

  • Schuchmann KL (1979) Metabolism of flying hummingbirds. Ibis 121:85–86

    Article  Google Scholar 

  • Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven

    Google Scholar 

  • Swofford DL (1993) Paup—a computer-program for phylogenetic inference using maximum parsimony. J Gen Physiol 102:A9

    Google Scholar 

  • Tobalske BW, Hedrick TL, Dial KP, Biewener AA (2003) Comparative power curves in bird flight. Nature 421:363–366

    Article  PubMed  CAS  Google Scholar 

  • Tucker VA (1968) Respiratory exchange and evaporative water loss in the flying budgerigar. J Exp Biol 48:67–87

    Google Scholar 

  • Tucker VA (1972) Metabolism during flight in the laughing gull, Larus atricilla. Am J Physiol. 222:237–245

    PubMed  CAS  Google Scholar 

  • Ward S, Möller U, Rayner JMV, Jackson DM, Bilo D, Nachtigall W, Speakman JR (2001) Metabolic power, mechanical power and efficiency during wind tunnel flight by the European starling, Sturnus vulgaris. J Exp Biol 204:3311–3322

    PubMed  CAS  Google Scholar 

  • Ward S, Bishop CM, Woakes AJ, Butler PJ (2002) Heart rate and the rate of oxygen consumption of flying and walking barnacle geese (Branta leucopsis) and bar-headed geese (Anser indicus). J Exp Biol 205:3347–3356

    PubMed  CAS  Google Scholar 

  • 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 27:215–224

    Article  Google Scholar 

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

    Google Scholar 

Download references

Acknowledgments

I am grateful to Olof Hellgren for patience, advice and help with phylogenetic procedures, Christoffer Johansson, Erik Svensson and two anonymous referees for constructive comments on the manuscript. This research was supported by the Swedish Research Council and my position as Royal Swedish Academy of Sciences Research Fellow is supported by a grant from the Knut and Alice Wallenberg Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anders Hedenström.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hedenström, A. Power and metabolic scope of bird flight: a phylogenetic analysis of biomechanical predictions. J Comp Physiol A 194, 685–691 (2008). https://doi.org/10.1007/s00359-008-0345-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-008-0345-z

Keywords

Navigation