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.
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
Askew EN, Ellerby DJ (2007) The mechanical power requirements of avian flight. Biol Lett 3:445–448
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
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
Bernstein MH, Thomas SP, Schmidt-Nielsen K (1973) Power input during flight of the fish crow, Corvus ossifragus. J Exp Biol 58:401–410
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
Butler PJ, Bishop CM (2000) Flight. In: Whittow GC (ed) Sturkies’s avian physiology, 5th edn. Academic Press, New York, pp 391–435
Ellington CP (1991) Limitations on animal flight performance. J Exp Biol 160:71–91
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
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15
Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726
Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32
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
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
Hainsworth FR, Wolf LL (1970) Regulation of oxygen consumption and body temperature during torpor in a hummingbird, Eulampis jugularis. Science 168:368–369
Hammond KA, Diamond J (1997) Maximal sustained energy budgets in humans and animals. Nature 386:457–462
Haus C (2001) Flugkosten von Rauchschwalben (Hirundo rustica) in Abhängigkeit von ihrer Körpermasse. Master thesis, Munich University
Hedenström A (2002) Aerodynamics, evolution and ecology of bird flight. Trends Ecol Evol 17:415–422
Hedenström A (2003) Scaling migration speed in animals that run, swim and fly. J Zool 259:155–160
Hedenström A, Alerstam T (1995) Optimal flight speed of birds. Phil Trans R Soc Lond B 348:471–487
Hedenström A, Alerstam T (1997) Optimum fuel loads in migratory birds: distinguishing between time and energy minimization. J Theor Biol 189:227–234
Hedenström A, Alerstam T (1998) How fast can birds migrate? J Avian Biol 29:424–432
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
Klaassen M, Kvist A, Lindström Å (2000) Flight costs and fuel composition of a bird migrating in a wind tunnel. Condor 102:444–451
Kleiber M (1961) The fire of life. Wiley, New York
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
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
Lasiewski RC (1963) Oxygen consumption of torpid, resting, active, and flying hummingbirds. Physiol Zool 36:122–140
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
Lindström Å (1991) Maximum fat deposition rates in migrating birds. Ornis Scand 22:12–19
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
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
Masman D, Klaassen M (1987) Energy expenditure during free flight in trained and free-living Eurasian kestrels (Falco tinnunculus). Auk 104:603–616
Norberg UM (1996) Energetics of flight. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman & Hall, New York, pp 199–249
Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884
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
Pennyuick CJ (1978) Fifteen testable predictions about bird flight. Oikos 30:165–176
Pennyuick CJ (1992) Newton rules biology: a physical approach to biological problems. Oxford University Press, Oxford
Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge
Rayner JMV (1988) Form and function in avian flight. Curr Ornithol 5:1–66
Reynolds PS, Lee RMIII (1996) Phylogenetic analysis of avian energetics: passerines and nonpasserines do not differ. Am Nat 147:735–759
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
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
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
Schmidt-Nielsen K (1984) Scaling. Cambridge University Press, Cambridge
Schuchmann KL (1979) Metabolism of flying hummingbirds. Ibis 121:85–86
Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven
Swofford DL (1993) Paup—a computer-program for phylogenetic inference using maximum parsimony. J Gen Physiol 102:A9
Tobalske BW, Hedrick TL, Dial KP, Biewener AA (2003) Comparative power curves in bird flight. Nature 421:363–366
Tucker VA (1968) Respiratory exchange and evaporative water loss in the flying budgerigar. J Exp Biol 48:67–87
Tucker VA (1972) Metabolism during flight in the laughing gull, Larus atricilla. Am J Physiol. 222:237–245
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
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
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
Videler J (2005) Avian flight. Oxford University Press, Oxford
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
Corresponding author
Rights 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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-008-0345-z