Skip to main content
Log in

Metabolic costs of avian flight in relation to flight velocity: a study in Rose Coloured Starlings (Sturnus roseus, Linnaeus)

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

The metabolic costs of flight at a natural range of speeds were investigated in Rose Coloured Starlings (Sturnus roseus, Linnaeus) using doubly labelled water. Eight birds flew repeatedly and unrestrained for bouts of 6 h at speeds from 9 to 14 m s−1 in a low-turbulence wind tunnel, corresponding to travel distances between 200 and 300 km, respectively. This represents the widest speed range where we could obtain voluntarily sustained flights. From a subset of these flights, data on the wing beat frequency (WBF) and intermittent flight behaviour were obtained. Over the range of speeds that were tested, flight costs did not change with velocity and were on an average 8.17±0.64 W or 114 W kg−1. Body mass was the only parameter with a significant (positive) effect on flight costs, which can be described as EEf=0.741 M 0.554. WBF changed slightly with speed, but correlated better with body mass. Birds showed both types of intermittent flight, undulating and bounding, but their frequencies did not systematically change with flight speed.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

EEf :

Flight energy expenditure (W)

DLW:

Doubly labelled water

M :

Body mass (g)

V mr :

Maximum range speed (m s−1)

V mp :

Minimum power speed (m s−1)

η:

Flight muscle efficiency

IRMS:

Isotope ratio mass spectrometer

WP:

Size of total body water pool (mol)

k d :

Fractional turnover rate for 2H (day−1)

k o :

Fractional turnover rate for 18O (day−1)

C iH :

Average 2H concentration of blood sample 1 (atom percent)

C iO :

Average 18O concentration of blood sample 1 (atom percent)

C bH :

Average background concentration of sample 0 for 2H (atom percent)

C bO :

Average background concentration of sample 0 for 18O (atom percent)

C fH :

Average 2H concentration of sample 2 (atom percent)

C fO :

Average 18O concentration of sample 2 (atom percent)

t :

Time (s)

rCO2 :

Rate of CO2 production (l day−1)

rG:

Assumed fraction of water flux lost through evaporative pathways

WBF:

Wing beat frequency (Hz)

B U :

Number of gliding bouts in undulating flight (bouts min−1)

D U :

Mean duration per gliding bout in undulating flight (s)

G U :

Total duration of gliding in undulating flight per sample (s)

B B :

Number of gliding bouts in bounding flight (bouts min−1)

D B :

Mean duration per gliding bout in bounding flight (s)

G B :

Total duration of gliding in bounding flight per sample (s)

References

  • Alexander RM (1997) The U, J and L of bird flight. Nature 390:13

    Article  CAS  Google Scholar 

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

    Article  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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Bernstein MH, Thomas SP, Schmidt-Nielsen K (1972) Power input during flight of the fish crow, Corvus ossifragus. J Exp Biol 58:401–410

    Google Scholar 

  • Biebach H (1992) Flight-range estimates for small trans-Sahara migrants. Ibis:47–54

  • Bishop CM (2005) Circulatory variables and the flight performance of birds. J Exp Biol 208:1695–1708

    Article  PubMed  Google Scholar 

  • Bishop CM, Ward S, Woakes AJ, Butler PJ (2002) The energetics of barnacle geese (Branta leucopsis) flying in captive and wild conditions. Comp Biochem Physiol A 133:225–237

    Article  CAS  Google Scholar 

  • Bruderer B, Boldt A (2001) Flight characteristics of birds: 1. Radar measurements of speeds. Ibis 143:178–204

    Article  Google Scholar 

  • Bryant DM (1997) Energy expenditure in wild birds. Proc Nutr Soc 56:1025–1039

    Article  PubMed  CAS  Google Scholar 

  • Bundle MW, Dial KP (2000) The metabolic cost of flight in budgies: revisiting an outlier. Am Zool 40:959–960

    Google Scholar 

  • Butler JP, Woakes AJ (1990) The physiology of bird flight. In: Gwinner E (ed) Bird migration. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Butler PJ (1981) Respiration during flight. In: Hutas I, Debreczeni LA (eds) Respiration. Pergamon, New York pp 155–164

  • Butler PJ (1991) Exercise in birds. J Exp Biol 160:233–262

    Google Scholar 

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

    Chapter  Google Scholar 

  • Butler PJ, Woakes AJ, Bishop CM (1989) Behaviour and physiology of Svalbard Barnacle Geese Branta leucopsis during their autumn migration. J Avian Biol 29:536–545

    Article  Google Scholar 

  • Chai P, Dudley R (1995) Limits to vertebrate locomotor energetics suggested by hummingbirds hovering in heliox. Nature 377:722–725

    Article  CAS  Google Scholar 

  • Dial KP, Biewener AA, Tobalske BW, Warrick DR (1997) Mechanical output of bird flight. Nature 390:67–70

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Greenewalt CH (1975) The flight of birds. Trans Am Philos Soc 65:1–67

    Article  Google Scholar 

  • Gudmundsson GA, Lindström A, Alerstam T (1991) Optimal fat loads and long-distance flights by migrating knots—Calidris canutus, sanderlings—Calidris alba and turnstones—Arenaria interpres. Ibis 133:140–152

    Article  Google Scholar 

  • Hambly C, Harper EJ, Speakman JR (2004a) The energy cost of loaded flight is substantially lower than expected due to alterations in flight kinematics. J Exp Biol 207:3969–3976

    Article  CAS  Google Scholar 

  • Hambly C, Pinshow B, Wiersma P, Verhulst S, Piertney SB, Harper EJ, Speakman JR (2004b) Comparison of the cost of short flights in a nectarivorous and a non-nectarivorous bird. J Exp Biol 207:3959–3968

    Article  CAS  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 

  • Hill AV (1938) The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond B 126:136–195

    Google Scholar 

  • Hudde H (1993) Sturnus roseus. In: von Glutz Blotzheim UN (ed) Handbuch der Vögel Mitteleuropas. Aula-Verlag, Wiesbaden, pp 2115–2144

    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 

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

    PubMed  Google Scholar 

  • Kendeigh SC, Dolnik VR, Gavrilov VM (1977) Avian energetics. In: Pinkowski J, Kendeigh SC (eds) Granivorous birds in ecosystems. Cambridge University Press, Cambridge, pp 127–203

    Google Scholar 

  • Klaassen M (1995) Water and energy limitations on flight range. Auk 112:260–262

    Google Scholar 

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

    Article  Google Scholar 

  • Kokshaysky NV (1979) Tracing the wake of a flying bird. Nature 279:146–148

    Article  Google Scholar 

  • Kvist A, Klaassen M, Lindström A (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 A, 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 

  • Lifson N, McClintock R (1966) Theory of use of the turnover rates of body water for measuring energy and material balance. J Theor Biol 12:46–74

    Article  PubMed  CAS  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 (1990) Vertebrate flight. Springer, Berlin Heidelberg New York

    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 

  • Norberg UM, Kunz TH, Steffensen JF, Winter YF, van Helversen O (1993) The cost of hovering and forward flight in a nectar-feeding bat, Glossophaga soricina, estimated from aerodynamic theory. J Exp Biol 182:207–227

    PubMed  CAS  Google Scholar 

  • Nudds RL, Bryant DM (2000) The energetic cost of short flights in birds. J Exp Biol 203:1561–1572

    PubMed  CAS  Google Scholar 

  • Pennycuick CJ (1975) Mechanics of flight. In: Farner DS, King JR (eds) Avian biology. Academic, London, pp 1–75

    Google Scholar 

  • Pennycuick CJ (1989) Bird flight performance: a practical calculation manual. Oxford University Press, Oxford

    Google Scholar 

  • Pennycuick CJ (2001) Flight for windows. Version 1.10

  • Pennycuick CJ, Alerstam T, Hedenström A (1997) A new low-turbulence wind tunnel for bird flight experiments at Lund University, Sweden. J Exp Biol 200:1441–1449

    PubMed  Google Scholar 

  • Pennycuick CJ, Hedenstöm A, Rosén M (2000) Horizontal flight of a swallow (Hirundo rustica) observed in a wind tunnel, with a new method for directly measuring mechanical power. J Exp Biol 203:1755–1765

    PubMed  CAS  Google Scholar 

  • Rayner JMV (1979a) A vortex theory of animal flight. Part 2. The forward flight of birds. J Fluid Mech 91:731–763

    Article  Google Scholar 

  • Rayner JMV (1979b) A new approach to animal flight mechanics. J Exp Biol 80:17–54

    Google Scholar 

  • Rayner JMV (1985) Bounding and undulating flight in birds. J Theor Biol 117:47–77

    Article  Google Scholar 

  • Rayner JMV (1990) The mechanics of flight and bird migration performance. In: Gwinner E (ed) Bird migration: physiology and ecophysiology. Springer, Berlin Heidelberg New York, pp 283–299

    Google Scholar 

  • Rayner JMV (1994) Aerodynamic corrections for the flight of birds and bats in wind tunnels. J Zool 234:537–563

    Article  Google Scholar 

  • Rayner JMV (1999) Estimating power curves of flying vertebrates. J Exp Biol 202:3449–3461

    PubMed  CAS  Google Scholar 

  • Rayner JMV, Ward S (1999) On the power curves of flying birds. 22 Int Ornithol Congr. Johannesburg: BirdLife South Africa, Durban, pp 1786–1809

    Google Scholar 

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

    Article  Google Scholar 

  • Schmidt-Nielsen K (1972) Locomotion: energy cost of swimming, running and flying. Science 177:222–228

    Article  PubMed  CAS  Google Scholar 

  • Schmidt-Nielsen K (1997) Animal physiology. Adaptation and environment. 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 

  • Speakman JR (1997) Doubly labelled water. Theory and practice. Chapman and Hall, London

    Google Scholar 

  • Spedding GR (1986) The wake of a jackdaw Corvus monedula in slow flight. J Exp Biol 125:287–308

    Google Scholar 

  • Spedding GR (1987) The wake of a kestrel Falco tinnunculus in flapping flight. J Exp Biol 127:59–78

    Google Scholar 

  • Spedding GR, Rayner Jeremy MV, Pennycuick CJ (1984) Momentum and energy in the wake of a pigeon Columba livia in slow flight. J Exp Biol 111:81–102

    Google Scholar 

  • Spedding GR, Rosen M, Hedenström A (2003) A family of vortex wakes generated by a thrush nightingale in free flight in a wind tunnel over its entire natural range of flight speeds. J Exp Biol 206:2313–2344

    Article  PubMed  CAS  Google Scholar 

  • Tatner P, Bryant DM (1986) Flight costs of a small passerine measured using doubly labelled water: implications for energetic studies. Auk 103:169–180

    Google Scholar 

  • Tobalske BW (1995) Neuromuscular control and kinematics of intermittent flight in the European starling (Sturnus vulgaris). J Exp Biol 198:1259–1273

    PubMed  Google Scholar 

  • Tobalske BW, Dial KP (1994) Neuromuscular control and kinematics of intermittent flight in budgerigars (Melopsittacus undulatus). J Exp Biol 187:1–18

    PubMed  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 

  • Torre-Bueno JR, Larochelle J (1978) The metabolic cost of flight in unrestrained birds. J Exp Biol 75:223–329

    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 

  • Tucker VA (1973) Bird metabolism during flight: evaluation of a theory. J Exp Biol 58:689–709

    Google Scholar 

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

    Google Scholar 

  • Videler JJ, Stamhuis EJ, Povel GDE (2004) Leading-edge vortex lifts swifts. Science 306:1960–1962

    Article  PubMed  CAS  Google Scholar 

  • Visser GH, Dekinga A, Achterkamp B, Piersma T (2000) Ingested water equilibrates isotopically with the body water pool of a shorebird with unrivaled water fluxes. Am J Physiol 279:1795–1804

    Google Scholar 

  • Visser GH, Schekkerman H (1999) Validation of the doubly labeled water method in growing precocial birds: the importance of assumptions concerning evaporative water loss. Physiol Biochem Zool 72:740–749

    Article  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 

  • 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, Möller U, Rayner JMV, Jackson DM, Nachtigall W, Speakman JR (2004) Metabolic power of European starlings Sturnus vulgaris during flight in a wind tunnel, estimated from heat transfer modelling, doubly labelled water and mask respirometry. J Exp Biol 207:4291–4298

    Article  PubMed  CAS  Google Scholar 

  • Ward S, Rayner JM, Möller U, Jackson DM, Nachtigall W, Speakman JR (1999) Heat transfer from starlings Sturnus vulgaris during flight. J Exp Biol 202:1589–1602

    PubMed  Google Scholar 

  • Ward-Smith AJ (1984) Aerodynamic and energetic considerations relating to undulating and bounding flight in birds. J Theor Biol 111:407–417

    Article  Google Scholar 

  • Weber TP, Ens BJ, Houston AI (1998) Optimal avian migration: a dynamic model of fuel stores and site use. Evol Ecol 12:377–401

    Article  Google Scholar 

  • Weimerskirch H, Martin J, Clerquin Y, Alexandre P, Jiraskova S (2001) Energy saving in flight formation. Nature 413:697–698

    Article  PubMed  CAS  Google Scholar 

  • Westerterp KR, Drent RH (1985) Energetic costs and energy-saving mechanisms in parental care of free-living passerine birds as determined by the D 182 O method. 18 Intern Ornithol Congr. Nauka Press, Moskow, pp 392–398

    Google Scholar 

  • Wikelski M, Tarlow EM, Raim A, Diehl RH, Larkin RP, Visser GH (2003) Costs of migration in free-flying songbirds. Nature 423:704

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Andrea Wittenzellner, Brigitte Biebach, and Ninon Ballerstädt for their technical assistance during bird training and the experiments. We are especially indebted to Ninon Ballerstädt for her help in analysing the video recordings. Berthe Verstappen determined the isotope enrichments. David Rummel from the Department of Statistics of the Ludwig-Maximilian-University Munich kindly helped with the mixed models statistics. We are grateful to Martha Merrow for proofreading this manuscript and improving our writing. Serge Daan and John Videler helped to improve earlier versions of this manuscript. We are greatly indebted to the late Prof. Dr. E. Gwinner whose enthusiasm led to the realization of the wind tunnel and has inspired us throughout the project. All experiments were in accordance with the German legislation on the protection of animals.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sophia Engel.

Additional information

Communicated by G. Heldmaier

Rights and permissions

Reprints and permissions

About this article

Cite this article

Engel, S., Biebach, H. & Visser, G.H. 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 (2006). https://doi.org/10.1007/s00360-006-0063-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-006-0063-1

Keywords

Navigation