Biomechanics of bird flight

Journal of Experimental Biology

Volumn 210, Issue 18, 2007, Pages 3135-3146

  Tobalske, Bret W ^a  

^a UNIVERSITY OF PORTLAND   (United States)

Author keywords

Intermittent; Kinematic; Maneuver; Muscle; Power; Stability; Take off; Wake; Wing; Work

Indexed keywords

ANIMAL; BIOMECHANICS; BIRD; FLYING; FORELIMB; HISTOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; BIOMECHANICS; BIRDS; FLIGHT, ANIMAL; WING;

AVES;

EID: 35648935918     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.000273     Document Type: Review

References (116)

1. Alexander, R. McN. (1989). Optimization and gaits in the locomotion of vertebrates. Physiol. Rev. 69, 1199-1227.
2. Altshuler, D. L., Dudley, R. and McGuire, J. A. (2004). Resolution of a paradox: hummingbird flight at high elevation does not come without a cost. Proc. Natl. Acad. Sci. USA 101, 17731-17736.
3. Askew, G. N. and Ellerby, D. J. (2007). The mechanical power requirements of avian flight. Biol. Lett. 3, 445-448.
4. Askew, G. N. and Marsh, R. L. (1997). The effects of length trajectory on the mechanical power output of mouse skeletal muscles. J. Exp. Biol. 200, 3119-3131.
5. Askew, G. N. and Marsh, R. L. (2001). The mechanical power output of the pectoralis muscle of blue-breasted quail (Coturnix chinensis): in vivo length cycle and its implications for muscle performance. J. Exp. Biol. 204, 3587-3600.
6. Askew, G. N., Marsh, R. L. and Ellington, C. P. (2001). The mechanical power output of the flight muscles of blue-breasted quail (Coturnix chinensis) during take-off. J. Exp. Biol. 204, 3601-3619.
7. Barclay, C. J. (1996). Mechanical efficiency and fatigue of fast and slow muscles of the mouse. J. Physiol. Lond. 497, 781-794.
8. Biewener, A. A. and Roberts, T. J. (2000). Muscle and tendon contributions to force, work, and elastic energy savings: a comparative perspective. Exerc. Sport Sci. Rev. 28, 99-107.
9. Biewener, A. A., Corning, W. R. and Tobalske, B. W. (1998). In vivo pectoralis muscle force-length behavior during level flight in pigeons (Columba livid). J. Exp. Biol. 201, 3293-3307.
10. Bilo, D. (1971). Flugbiophysik von Kleinvögeln. I. Kinematik und Aerodynamik des Flügelabschlages beim Haussperling (Passer domesticus L.). Z. Vergl. Physiol. 71, 382-454.
11. Bilo, D. (1972). Flugbiophysik von Kleinvögeln. II. Kinematik und Aerodynamik des Flügelaufschlages beim Haussperling (Passer domesticus L.). Z. Vergl. Physiol. 76, 426-437.
12. Brown, R. H. J. (1963). The flight of birds. Biol. Rev. 38, 460-489.
13. Bruderer, L., Liechti, F. and Bilo, D. (2001). Flexibility in flight behaviour of barn swallows (Hirundo rustica) and house martins (Delichon urbica) tested in a wind tunnel. J. Exp. Biol. 204, 1473-1484.
14. Bundle, M. W., Hansen, K. S. and Dial, K. P. (2007). Does the metabolic rate-flight speed relationship vary among geometrically similar birds of different mass? J. Exp. Biol. 210, 1075-1083.
15. Chai, P. and Dudley, R. (1995). Limits to vertebrate locomotor energetics suggested by hummingbirds hovering in heliox. Nature 377, 722-725.
16. Chai, P. and Millard, D. (1997). Flight and size constraints: hovering performance of large hummingbirds under maximal loading. J. Exp. Biol. 200, 2757-2763.
17. Csicsáky, M. J. (1977). Body-gliding in the zebra finch. Fortschr. Zool. 24, 275-286.
18. Dabiri, J. O. (2005). On the estimation of swimming and flying forces from wake measurements. J. Exp. Biol. 208, 3519-3532.
19. Dejong, M. J. (1983). Bounding flight in birds. PhD thesis, University of Wisconsin, Madison, USA.
20. Dial, K. P. (1992a). Activity patterns of the wing muscles of the pigeon (Columba livia) during different modes of flight. J. Exp. Zool. 262, 357-373.
21. Dial, K. P. (1992b). Avian forelimb muscles and nonsteady flight: can birds fly without using the muscles of their wings? Auk 109, 874-885.
22. Dial, K. P. and Biewener, A. A. (1993). Pectoralis muscle force and power output during different modes of flight in pigeons (Columba livia). J. Exp. Biol. 176, 31-54.
23. Dickinson, M. H. (1996). Unsteady mechanisms of force generation in aquatic and aerial locomotion. Am. Zool. 36, 537-554.
24. Dickinson, M. H., Lehman, F. O. and Sane, S. P. (1999). Wing rotation and the aerodynamic basis of insect flight. Science 284, 1954-1960.
25. Drovetski, S. V. (1996). Influence of the trailing-edge notch on flight performance in galliforms. Auk 113, 802-810.
26. Earls, K. D. (2000). Kinematics and mechanics of ground take-off in the starling Sturnus vulgaris and the quail Coturnix coturnix. J. Exp. Biol. 203, 725-739.
27. Ellington, C. P. (1984). The aerodynamics of hovering insect flight I-V. Philos. Trans. R. Soc. Lond. B Biol. Sci. 305, 1-181.
28. Ellington, C. P. (1991). Limitations on animal flight performance. J. Exp. Biol. 160, 71-91.
29. Engel, S., Biebach, H. and Visser, G. H. (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.
30. Evans, M. R. (2004). Limits on the evolution of tail ornamentation in birds. Am. Nat. 163, 341-357.
31. Evans, M. R., Rosén, M., Park, K. and Hedenström, A. (2002). How do birds' tails work? Delta-wing theory fails to predict tail shape during flight. Proc. Biol. Sci. 269, 1053-1057.
32. Funk, G. D., Steeves, J. D. and Milsom, W. K. (1992). Coordination of wingbeat and respiration in birds. II. 'Fictive' flight. J. Appl. Physiol. 73, 1025-1033.
33. Garland, T., Jr and Adolph, S. C. (1994). Why not to do two species comparative studies: limitations on inferring adaptation. Physiol. Zool. 67, 797-828.
34. Gould, S. J. and Lewontin, R. C. (1979). The spandrels of San Marco and the panglossian paradigm: a critique of the adaptationist programme Proc. R. Soc. Lond. B Biol. Sci. 205, 581-598.
35. 13C labelled bicarbonate. J. Comp. Physiol. B 172, 529-539.
36. Hedenström, A. and Alerstam, T. (1995). Optimal flight speed of birds. Philos. Trans. R. Soc. Lond. B Biol. Sci. 348, 471-487.
37. Hedenström, A. and Liechti, L. (2001). Field estimates of body drag coefficient on the basis of dives in passerine birds. J. Exp. Biol. 204, 1167-1175.
38. Hedenström, A. and Rosén, M. (2001). Predator versus prey: on aerial hunting and escape strategies in birds. Behav. Ecol. 12, 150-156.
39. Hedenström, A. and Rosén, M. (2003). Body frontal area in passerine birds. J. Avian Biol. 34, 159-162.
40. Hedenström, A., Griethuijsen, L. V., Rosén, M. and Spedding, G. R. (2006). Vortex wakes of birds: recent developments using digital particle image velocimetry in a wind tunnel. Anim. Biol. 56, 535-549.
41. Hedrick, T. L. and Biewener, A. A. (2007a). Experimental study of low speed turning flight in cockatoos and cockatiels. 45th AIAA Aerospace Sciences Meeting and Exhibit 8-11 January 2007, Reno, Nevada. AIAA Paper, 2007-0044.
42. Hedrick, T. L. and Biewener, A. A. (2007b). Low speed maneuvering flight of the rose-breasted cockatoo (Eolophus roseicapillus). I. Kinematic and neuromuscular control of turning. J. Exp. Biol. 210, 1897-1911.
43. Hedrick, T. L., Tobalske, B. W. and Biewener, A. A. (2002). Estimates of circulation and gait change based on a three-dimensional kinematic analysis of flight in cockatiels (Nymphicus hollandicus) and ringed turtle doves (Streptopelia risoria). J. Exp. Biol. 205, 1389-1409.
44. Hedrick, T. L., Tobalske, B. W. and Biewener, A. A. (2003). How cockatiels (Nymphicus hollandicus) modulate pectoralis power output across flight speeds. J. Exp. Biol. 206, 1363-1378.
45. Hedrick, T. L., Usherwood, J. R. and Biewener, A. A. (2004). Wing inertia and whole-body acceleration: an analysis of instantaneous aerodynamic force production in cockatiels (Nymphicus hollandicus) flying across a range of speeds. J. Exp. Biol. 207, 1689-1702.
46. Hedrick, T. L., Usherwood, J. R. and Biewener, A. A. (2007). Low speed maneuvering flight of the rose-breasted cockatoo (Eolophus roseicapillus). II. Inertial and aerodynamic reorientation. J. Exp. Biol. 210, 1912-1924.
47. Henry, H. T., Ellerby, D. J. and Marsh, R. L. (2005). Performance of guinea fowl Numida meleagris during jumping requires storage and release of elastic energy. J. Exp. Biol. 208, 3293-3302.
48. Hill, A. V. (1950). The dimensions of animals and their muscular dynamics. Sci. Prog. 38, 209-230.
49. Houston, A. I. (2006). The flight speed of parent birds feeding young. J. Avian Biol. 37, 545-554.
50. Hummel, D. (1992). Aerodynamic investigations on tail effects in birds. Z. Flugwiss. Weltraumforsch. 16, 159-168.
51. Kullberg, C., Jakobsson, S. and Fransson, T. (1998). Predator-induced take-off strategy in Great Tits (Parus major). Proc. R. Soc. Lond. B Biol. Sci. 265, 1659-1664.
52. Lentink, D., Müller, U. K., Stamhuis, E. J., de Kat, R., van Gestel, W., Veldhuis, L. L. M., Henningsson, P., Hedenström, A., Videler, J. J. and van Leeuwen, J. L. (2007). How swifts control their glide performance with morphing wings. Nature 446, 1082-1085.
53. Marden, J. H. (1994). From damselflies to pterosaurs: how burst and sustainable flight performance scale with size. Am. J. Physiol. 266, R1077-R1084.
54. Maybury, W. J. (2000). The aerodynamics of bird bodies. PhD thesis, University of Bristol, UK.
55. Maybury, W. J. and Rayner, J. M. V. (2001). The avian tail reduces body parasite drag by controlling flow separation and vortex shedding. Proc. R. Soc. Lond. B Biol. Sci. 268, 1405-1410.
56. Maybury, W. J., Rayner, J. M. V. and Couldrick, L. B. (2001). Lift generation by the avian tail. Proc. R. Soc. Lond. B Biol. Sci. 268, 1443-1448.
57. Møller, A.P., de Lope, F. and Saino, N. (1995). Sexual selection in the barn swallow Hirundo rustica VI. aerodynamic adaptations. J. Evol. Biol. 8, 671-687.
58. Norberg, U. M. (1990). Vertebrate Flight: Mechanics, Physiology, Morphology, Ecology and Evolution. New York: Springer-Verlag.
59. Nudds, R. L. and Bryant, D. M. (2000). The energetic cost of short flights in birds. J. Exp. Biol. 203, 1561-1572.
60. Nudds, R. L. and Rayner, J. M. V. (2006). Scaling of body frontal area and body width in birds. J. Morphol. 327, 341-346.
61. Park, K. J., Evans, R. M. and Buchanan, K. L. (2000). Assessing the aerodynamic effects of tail elongations in the house martin (Delichon urbica): implications for the initial selection pressures in hirundines. Behav. Ecol. Sociobiol. 48, 364-372.
62. Park, K. J., Rosén, M. and Hedenström, A. (2001). Flight kinematics of the barn swallow Hirundo rustica over a wide range of speeds in a wind tunnel. J. Exp. Biol. 204, 2741-2750.
63. Pennycuick, C. J. (1975). Mechanics of flight. In Avian Biology. Vol. 5 (ed. D. S. Farner and J. R. King), pp. 1-75. New York: Academic Press.
64. Pennycuick, C. J. (1989). Bird Flight Performance: A Practical Calculation Manual. Oxford: Oxford University Press.
65. Pennycuick, C. J., Obrecht, H. H., III and Fuller, M. R. (1988). Empirical estimates of body drag of large waterfowl and raptors. J. Exp. Biol. 135, 253-264.
66. Pennycuick, C. J., Heine, C. E., Kirkpatrick, S. J. and Fuller, M. R. (1992). The profile drag of a hawk's wing, measured by wake sampling in a wind tunnel. J. Exp. Biol. 165, 1-19.
67. Pennycuick, C. J., Hedenström, A. and 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.
68. Poore, S. O., Ashcroft, A., Sanchez-Haiman, A. and Goslow, G. E., Jr (1997). The contractile properties of the M. supracoracoideus in the pigeon and starling: a case for long-axis rotation of the humerus. J. Exp. Biol. 200, 2987-3002.
69. Rayner, J. M. V. (1979a). A vortex theory of animal flight. Part I. The vortex wake of a hovering animal. J. Fluid Mech. 91, 697-730.
70. Rayner, J. M. V. (1979b). A vortex theory of animal flight. Part II. The forward flight of birds. J. Fluid Mech. 91, 731-763.
71. Rayner, J. M. V. (1985). Bounding and undulating flight in birds. J. Theor. Biol. 117, 47-77.
72. Rayner, J. M. V. (1988). Form and function in avian flight. Curr. Ornithol. 5, 1-66.
73. Rayner, J. M. V. (1999). Estimating power curve of flying vertebrates. J. Exp. Biol. 202, 3449-3461.
74. Rayner, J. M. V., Viscardi, P. W., Ward, S. and Speakman, J. R. (2001). Aerodynamics and energetics of intermittent flight in birds. Am. Zool. 41, 188-204.
75. Rosén, M. W., Spedding, G. R. and Hedenström, A. (2004). The relationship between wingbeat kinematics and vortex wake of a thrush nightingale. J. Exp. Biol. 207, 4255-4268.
76. Sane, S. and Dickinson, M. H. (2001). The control of flight force by a flapping wing: lift and drag production. J. Exp. Biol. 204, 2607-2626.
77. Schmidt-Nielsen, K. (1972). Locomotion: energy cost of swimming, running and flying. Science 177, 222-228.
78. Scholey, K. D. (1983). Developments in vertebrate flight: climbing and gliding of mammals and reptiles, and the flapping flight of birds. PhD thesis, University of Bristol, UK.
79. Sokoloff, A. J., Gray-Chickering, J., Harry, J. D., Poore, S. O. and Goslow, G. E., Jr (2001). The function of the supracoracoideus muscle during takeoff in the European starling (Sternus vulgaris): Maxheinz Sy revisited. In New Perspectives on the Origin and Early Evolution of Birds: Proceedings of the International Symposium in Honor of John H. Ostrom (ed. J. Gauthier and L. F. Gall), pp. 319-332. New Haven: Peabody Museum of Natural History, Yale University.
80. Soman, A., Hedrick, T. L. and Biewener, A. A. (2005). Regional patterns of pectoralis fascicle strain in the pigeon Columba livia during level flight. J. Exp. Biol. 208, 771-786.
81. Spedding, G. R. (1987). The wake of a kestrel (Falco tinnunculus) in flapping flight. J. Exp. Biol. 127, 59-78.
82. Spedding, G. R. (1993). On the significance of unsteady effects in the aerodynamic performance of flying animals. Contemp. Math. 141, 401-419.
83. Spedding, G. R., Rayner, J. M. V. and Pennycuick, C. J. (1984). Momentum and energy in the wake of a pigeon (Columba livia) in slow flight. J. Exp. Biol. 111, 81-102.
84. Spedding, G. R., Rosén, M. and 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.
85. Taylor, G. K. and Thomas, A. L. R. (2002). Animal flight dynamics. II. Longitudinal stability in flapping flight. J. Theor. Biol. 214, 351-370.
86. Taylor, G. K. and Thomas, A. L. R. (2003). Dynamic flight stability in the desert locust Schistocerca gregaria. J. Exp. Biol. 206, 2803-2829.
87. Taylor, G. K., Nudds, R. L. and Thomas, A. L. (2003). Flying and swimming animals cruise at a Strouhal number tuned for high power efficiency. Nature 425, 707-711.
88. Thomas, A. L. R. (1993). On the aerodynamics of birds' tails. Philos. Trans. R. Soc. Lond. B Biol. Sci. 340, 361-380.
89. Thomas, A. L. R. and Hedenström, A. (1998). The optimum flight speeds of animals. J. Avian Biol. 29, 469-477.
90. Thomas, A. L. R. and Taylor, G. K. (2001). Animal flight dynamics. I. Stability in gliding fight. J. Theor. Biol. 212, 399-424.
91. Tobalske, B. W. (1996). Scaling of muscle composition, wing morphology, and intermittent flight behavior in woodpeckers. Auk 113, 151-177.
92. Tobalske, B. W. (2000). Biomechanics and physiology of gait selection in flying birds. Physiol. Biochem. Zool. 73, 736-750.
93. Tobalske, B. W. (2001). Morphology, velocity, and intermittent flight in birds. Am. Zool. 41, 177-187.
94. Tobalske, B. W. and Biewener, A. A. (2008). Contractile properties of the pigeon supracoracoideus during different modes of flight. J. Exp. Biol. In press.
95. Tobalske, B.W. and Dial, K.P. (1994). Neuromuscular control and kinematics of intermittent flight in budgerigars (Melopsittacus undulatus). J. Exp. Biol. 187, 1-18.
96. Tobalske, B. W. and Dial, K. P. (1996). Flight kinematics of black-billed magpies and pigeons over a wide range of speeds. J. Exp. Biol. 199, 263-280.
97. Tobalske, B. W. and Dial, K. P. (2000). Effects of body size on take-off flight performance in the Phasianidae (Aves). J. Exp. Biol. 203, 3319-3332.
98. Tobalske, B. W., Peacock, W. L. and Dial, K. P. (1999). Kinematics of flap-bounding flight in the zebra finch over a wide range of speeds. J. Exp. Biol. 202, 1725-1739.
99. Tobalske, B. W., Hedrick, T. L., Dial, K. P. and Biewener, A. A. (2003). Comparative power curves in bird flight. Nature 421, 363-366.
100. Tobalske, B. W., Altshuler, D. L. and Powers, D. A. (2004). Take-off mechanics in hummingbirds (Trochilidae). J. Exp. Biol. 207, 1345-1352.
101. Tobalske, B. W., Puccinelli, L. A. and Sheridan, D. C. (2005). Contractile activity of the pectoralis in the zebra finch according to mode and velocity of flap-bounding flight. J. Exp. Biol. 208, 2895-2901.
102. Tobalske, B. W., Warrick, D. R., Clark, C. J., Powers, D. R., Hedrick, T. L., Hyder, G. A. and Biewener, A. A. (2007). Three-dimensional kinematics of hummingbird flight. J. Exp. Biol. 210, 2368-2382.
103. Usherwood, J. R. and Ellington, C. P. (2002). The aerodynamics of revolving wings. II. Propeller force coefficients from mayfly to quail. J. Exp. Biol. 205, 1565-1576.
104. Usherwood, J. R., Hedrick, T. L. and Biewener, A. A. (2003). The aerodynamics of avian take-off from direct pressure measurements in Canada geese (Branta canadensis). J. Exp. Biol. 206, 4051-4056.
105. Usherwood, J. R., Hedrick, T. L., McGowan, C. P. and Biewener, A. A. (2005). Dynamic pressure maps for wings and tails of pigeons in slow, flapping flight, and their energetic implications. J. Exp. Biol. 208, 355-369.
106. Videler, J. J., Stamhuis, E. J. and Povel, G. D. E. (2004). Leading-edge vortex lifts swifts. Science 306, 1960-1962.
107. Wang, Z. J., Birch, J. and Dickinson, M. H. (2004). Unsteady forces and flows in low Reynolds number hovering flight: two-dimensional computations vs robotic wing experiments. J. Exp. Biol. 207, 449-460.
108. Ward, S., Möller, U., Rayner, J. M. V., Jackson, D. M., Bilo, D., Nachtigall, W. and Speakman, J. R. (2001). Metabolic power, mechanical power and efficiency during wind tunnel flight by European starlings Sturnus vulgaris. J. Exp. Biol. 204, 3311-3322.
109. Ward, S., Möller, U., Rayner, J. M. V., Jackson, D. M., Nachtigall, W. and Speakman, J. R. (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.
110. Warrick, D. R. (1998). The turning and linear manervering performance of birds: the cost of efficiency for coursing insectivores. Can. J. Zool. 7, 1063-1079.
111. Warrick, D. R. and Dial, K. P. (1998). Kinematic, aerodynamic and anatomical mechanisms in the slow, maneuvering flight of pigeons. J. Exp. Biol. 201, 655-672.
112. Warrick, D. R., Dial, K. P. and Biewener, A. A. (1998). Asymmetrical force production in the slow maneuvering flight of birds. Auk 115, 916-928.
113. Warrick, D. R., Bundle, M. W. and Dial, K. P. (2002). Bird maneuvering flight: blurred bodies, clear heads. Integr. Comp. Biol. 42, 141-148.
114. Warrick, D. R., Tobalske, B. W. and Powers, D. P. (2005). Aerodynamics of the hovering hummingbird. Nature 435, 1094-1097.
115. Willmott, A. P., Ellington, C. P. and Thomas, A. L. R. (1997). Flow visualization and unsteady aerodynamics in the flight of the hawkmoth, Manduca sexta. Philos. Trans. R. Soc. Lond. B Biol. Sci. 352, 303-316.
116. Withers, P. C. (1981). An aerodynamic analysis of bird wings as fixed aerofoils. J. Exp. Biol. 90, 143-162.