Biomechanics of bird flight

SUMMARY Power output is a unifying theme for bird flight and considerable progress has been accomplished recently in measuring muscular, metabolic and aerodynamic power in birds. The primary flight muscles of birds, the pectoralis and supracoracoideus, are designed for work and power output, with large stress (force per unit cross-sectional area) and strain (relative length change) per contraction. U-shaped curves describe how mechanical power output varies with flight speed, but the specific shapes and characteristic speeds of these curves differ according to morphology and flight style. New measures of induced, profile and parasite power should help to update existing mathematical models of flight. In turn, these improved models may serve to test behavioral and ecological processes. Unlike terrestrial locomotion that is generally characterized by discrete gaits, changes in wing kinematics and aerodynamics across flight speeds are gradual. Take-off flight performance scales with body size, but fully revealing the mechanisms responsible for this pattern awaits new study. Intermittent flight appears to reduce the power cost for flight, as some species flap–glide at slow speeds and flap–bound at fast speeds. It is vital to test the metabolic costs of intermittent flight to understand why some birds use intermittent bounds during slow flight. Maneuvering and stability are critical for flying birds, and design for maneuvering may impinge upon other aspects of flight performance. The tail contributes to lift and drag; it is also integral to maneuvering and stability. Recent studies have revealed that maneuvers are typically initiated during downstroke and involve bilateral asymmetry of force production in the pectoralis. Future study of maneuvering and stability should measure inertial and aerodynamic forces. It is critical for continued progress into the biomechanics of bird flight that experimental designs are developed in an ecological and evolutionary context.

[1]  A. Biewener,et al.  Contractile properties of the pigeon supracoracoideus during different modes of flight , 2008, Journal of Experimental Biology.

[2]  D. Ellerby,et al.  The mechanical power requirements of avian flight , 2007, Biology Letters.

[3]  C. J. Clark,et al.  Three-dimensional kinematics of hummingbird flight , 2007, Journal of Experimental Biology.

[4]  A. Biewener,et al.  Low speed maneuvering flight of the rose-breasted cockatoo (Eolophus roseicapillus). II. Inertial and aerodynamic reorientation , 2007, Journal of Experimental Biology.

[5]  A. Biewener,et al.  Low speed maneuvering flight of the rose-breasted cockatoo (Eolophus roseicapillus). I. Kinematic and neuromuscular control of turning , 2007, Journal of Experimental Biology.

[6]  Matthew W Bundle,et al.  Does the metabolic rate–flight speed relationship vary among geometrically similar birds of different mass? , 2007, Journal of Experimental Biology.

[7]  Tyson L. Hedrick,et al.  Experimental Study of Low Speed Turning Flight in Cockatoos and Cockatiels , 2007 .

[8]  J. L. Leeuwen,et al.  How swifts control their glide performance with morphing wings , 2006, Nature.

[9]  A. Houston The flight speed of parent birds feeding young , 2006 .

[10]  R. Nudds,et al.  Scaling of body frontal area and body width in birds , 2006, Journal of morphology.

[11]  Herbert Biebach,et al.  Metabolic costs of avian flight in relation to flight velocity: a study in Rose Coloured Starlings (Sturnus roseus, Linnaeus) , 2006, Journal of Comparative Physiology B.

[12]  Anders Hedenström,et al.  Vortex wakes of birds: recent developments using digital particle image velocimetry in a wind tunnel , 2006 .

[13]  John O. Dabiri,et al.  On the estimation of swimming and flying forces from wake measurements , 2005, Journal of Experimental Biology.

[14]  R. Marsh,et al.  Performance of guinea fowl Numida meleagris during jumping requires storage and release of elastic energy , 2005, Journal of Experimental Biology.

[15]  Bret W Tobalske,et al.  Contractile activity of the pectoralis in the zebra finch according to mode and velocity of flap-bounding flight , 2005, Journal of Experimental Biology.

[16]  B. Tobalske,et al.  Aerodynamics of the hovering hummingbird , 2005, Nature.

[17]  Andrew A Biewener,et al.  Regional patterns of pectoralis fascicle strain in the pigeon Columba livia during level flight , 2005, Journal of Experimental Biology.

[18]  Andrew A Biewener,et al.  Dynamic pressure maps for wings and tails of pigeons in slow, flapping flight, and their energetic implications , 2005, Journal of Experimental Biology.

[19]  R. Dudley,et al.  Resolution of a paradox: hummingbird flight at high elevation does not come without a cost. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[20]  G D E Povel,et al.  Leading-Edge Vortex Lifts Swifts , 2004, Science.

[21]  W. Nachtigall,et al.  Metabolic power of European starlings Sturnus vulgaris during flight in a wind tunnel, estimated from heat transfer modelling, doubly labelled water and mask respirometry , 2004, Journal of Experimental Biology.

[22]  A Hedenström,et al.  The relationship between wingbeat kinematics and vortex wake of a thrush nightingale , 2004, Journal of Experimental Biology.

[23]  Tyson L. Hedrick,et al.  Wing inertia and whole-body acceleration: an analysis of instantaneous aerodynamic force production in cockatiels (Nymphicus hollandicus) flying across a range of speeds , 2004, Journal of Experimental Biology.

[24]  Bret W Tobalske,et al.  Take-off mechanics in hummingbirds (Trochilidae) , 2004, Journal of Experimental Biology.

[25]  M. R. Evans,et al.  Limits on the Evolution of Tail Ornamentation in Birds , 2004, The American Naturalist.

[26]  Z. J. Wang,et al.  Unsteady forces and flows in low Reynolds number hovering flight: two-dimensional computations vs robotic wing experiments , 2004, Journal of Experimental Biology.

[27]  Dietrich Bilo,et al.  Flugbiophysik von Kleinvögeln , 1971, Zeitschrift für vergleichende Physiologie.

[28]  Andrew A Biewener,et al.  The aerodynamics of avian take-off from direct pressure measurements in Canada geese (Branta canadensis) , 2003, Journal of Experimental Biology.

[29]  Adrian L. R. Thomas,et al.  Flying and swimming animals cruise at a Strouhal number tuned for high power efficiency , 2003, Nature.

[30]  Adrian L. R. Thomas,et al.  Dynamic flight stability in the desert locust Schistocerca gregaria , 2003, Journal of Experimental Biology.

[31]  A Hedenström,et al.  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 , 2003, Journal of Experimental Biology.

[32]  A. Hedenström,et al.  Body frontal area in passerine birds , 2003 .

[33]  Bret W. Tobalske,et al.  How cockatiels (Nymphicus hollandicus) modulate pectoralis power output across flight speeds , 2003, Journal of Experimental Biology.

[34]  A. Biewener,et al.  Comparative power curves in bird flight , 2003, Nature.

[35]  J. Speakman,et al.  Cost of flight in the zebra finch (Taenopygia guttata): a novel approach based on elimination of 13C labelled bicarbonate , 2002, Journal of Comparative Physiology B.

[36]  J. Usherwood,et al.  The aerodynamics of revolving wings II. Propeller force coefficients from mayfly to quail. , 2002, The Journal of experimental biology.

[37]  Matthew R Evans,et al.  How do birds' tails work? Delta–wing theory fails to predict tail shape during flight , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  A. Biewener,et al.  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). , 2002, The Journal of experimental biology.

[39]  Adrian L. R. Thomas,et al.  Animal flight dynamics II. Longitudinal stability in flapping flight. , 2002, Journal of theoretical biology.

[40]  D R Warrick,et al.  Bird Maneuvering Flight: Blurred Bodies, Clear Heads1 , 2002, Integrative and comparative biology.

[41]  R. Marsh,et al.  The mechanical power output of the flight muscles of blue-breasted quail (Coturnix chinensis) during take-off. , 2001, The Journal of experimental biology.

[42]  R. Marsh,et al.  The mechanical power output of the pectoralis muscle of blue-breasted quail (Coturnix chinensis): the in vivo length cycle and its implications for muscle performance. , 2001, The Journal of experimental biology.

[43]  G. Taylor,et al.  Animal flight dynamics I. Stability in gliding flight. , 2001, Journal of theoretical biology.

[44]  W. Nachtigall,et al.  Metabolic power, mechanical power and efficiency during wind tunnel flight by the European starling Sturnus vulgaris. , 2001, The Journal of experimental biology.

[45]  M. Dickinson,et al.  The control of flight force by a flapping wing: lift and drag production. , 2001, The Journal of experimental biology.

[46]  A. Hedenström,et al.  Flight kinematics of the barn swallow (Hirundo rustica) over a wide range of speeds in a wind tunnel. , 2001, The Journal of experimental biology.

[47]  J. Rayner,et al.  Lift generation by the avian tail , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[48]  J. M. V. Rayner,et al.  The avian tail reduces body parasite drag by controlling flow separation and vortex shedding , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[49]  F. Liechti,et al.  Flexibility in flight behaviour of barn swallows (Hirundo rustica) and house martins (Delichon urbica) tested in a wind tunnel. , 2001, Journal of Experimental Biology.

[50]  Bret W. Tobalske,et al.  Morphology, Velocity, and Intermittent Flight in Birds1 , 2001 .

[51]  A Hedenström,et al.  Field estimates of body drag coefficient on the basis of dives in passerine birds. , 2001, The Journal of experimental biology.

[52]  Anders Hedenström,et al.  Predator versus prey: on aerial hunting and escape strategies in birds , 2001 .

[53]  W.,et al.  Aerodynamics and Energetics of Intermittent Flight in Birds , 2001 .

[54]  Bret W. Tobalske,et al.  Biomechanics and Physiology of Gait Selection in Flying Birds* , 2000, Physiological and Biochemical Zoology.

[55]  K P Dial,et al.  Effects of body size on take-off flight performance in the Phasianidae (Aves). , 2000, The Journal of experimental biology.

[56]  M. R. Evans,et al.  Assessing the aerodynamic effects of tail elongations in the house martin (Delichon urbica): implications for the initial selection pressures in hirundines , 2000, Behavioral Ecology and Sociobiology.

[57]  A A Biewener,et al.  Muscle and Tendon Contributions to Force, Work, and Elastic Energy Savings: A Comparative Perspective , 2000, Exercise and sport sciences reviews.

[58]  A Hedenström,et al.  Horizontal flight of a swallow (Hirundo rustica) observed in a wind tunnel, with a new method for directly measuring mechanical power. , 2000, The Journal of experimental biology.

[59]  R. Nudds,et al.  The energetic cost of short flights in birds. , 2000, The Journal of experimental biology.

[60]  K D Earls,et al.  Kinematics and mechanics of ground take-off in the starling Sturnis vulgaris and the quail Coturnix coturnix. , 2000, The Journal of experimental biology.

[61]  J. Rayner Estimating power curves of flying vertebrates. , 1999, The Journal of experimental biology.

[62]  Tobalske,et al.  Kinematics of flap-bounding flight in the zebra finch over a wide range of speeds , 1999, The Journal of experimental biology.

[63]  M. Dickinson,et al.  Wing rotation and the aerodynamic basis of insect flight. , 1999, Science.

[64]  A. Biewener,et al.  In vivo pectoralis muscle force-length behavior during level flight in pigeons (Columba livia) , 1998, The Journal of experimental biology.

[65]  Anders Hedenström,et al.  THE OPTIMUM FLIGHT SPEEDS OF FLYING ANIMALS , 1998 .

[66]  Andrew A. Biewener,et al.  Asymmetrical Force Production in the Maneuvering Flight of Pigeons , 1998 .

[67]  T. Fransson,et al.  Predator–induced take–off strategy in great tits (Parus major) , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[68]  D. Warrick,et al.  The turning- and linear-maneuvering performance of birds : the cost of efficiency for coursing insectivores , 1998 .

[69]  K. Dial,et al.  Kinematic, aerodynamic and anatomical mechanisms in the slow, maneuvering flight of pigeons , 1998, The Journal of experimental biology.

[70]  G. E. Goslow,et al.  The contractile properties of the M. supracoracoideus In the pigeon and starling: a case for long-axis rotation of the humerus , 1997, The Journal of experimental biology.

[71]  R. Marsh,et al.  The effects of length trajectory on the mechanical power output of mouse skeletal muscles. , 1997, The Journal of experimental biology.

[72]  P. Chai,et al.  Flight and size constraints: hovering performance of large hummingbirds under maximal loading. , 1997, The Journal of experimental biology.

[73]  Adrian L. R. Thomas,et al.  FLOW VISUALIZATION AND UNSTEADY AERODYNAMICS IN THE FLIGHT OF THE HAWKMOTH, MANDUCA SEXTA , 1997 .

[74]  C. Barclay Mechanical efficiency and fatigue of fast and slow muscles of the mouse. , 1996, The Journal of physiology.

[75]  M. Dickinson UNSTEADY MECHANISMS OF FORCE GENERATION IN AQUATIC AND AERIAL LOCOMOTION , 1996 .

[76]  S. Drovetski,et al.  Influence of the trailing-edge notch on flight performance of galliforms , 1996 .

[77]  Tobalske,et al.  Flight kinematics of black-billed magpies and pigeons over a wide range of speeds , 1996, The Journal of experimental biology.

[78]  Bret W. Tobalske,et al.  SCALING OF MUSCLE COMPOSITION, WING MORPHOLOGY, AND INTERMITTENT FLIGHT BEHAVIOR IN WOODPECKERS , 1996 .

[79]  A. Møller,et al.  Sexual selection in the barn swallow Hirundo rustica. VI. Aerodynamic adaptations , 1995 .

[80]  R. Dudley,et al.  Limits to vertebrate locomotor energetics suggested by hummingbirds hovering in heliox , 1995, Nature.

[81]  A. Hedenström,et al.  OPTIMAL FLIGHT SPEED OF BIRDS , 1995 .

[82]  T. Garland,et al.  Why Not to Do Two-Species Comparative Studies: Limitations on Inferring Adaptation , 1994, Physiological Zoology.

[83]  J. Marden From damselflies to pterosaurs: how burst and sustainable flight performance scale with size. , 1994, The American journal of physiology.

[84]  Tobalske,et al.  NEUROMUSCULAR CONTROL AND KINEMATICS OF INTERMITTENT FLIGHT IN BUDGERIGARS (MELOPSITTACUS UNDULATUS) , 1994, The Journal of experimental biology.

[85]  Adrian L. R. Thomas On the aerodynamics of birds’ tails , 1993 .

[86]  A. Biewener,et al.  PECTORALIS MUSCLE FORCE AND POWER OUTPUT DURING DIFFERENT MODES OF FLIGHT IN PIGEONS (COLUMBA LIVIA) , 1993 .

[87]  G. Jenkins,et al.  Spatial variation in feeding, prey distribution and food limitation of juvenile flounder Rhombosolea tapirina Günther , 1992 .

[88]  K. Dial,et al.  AVIAN FORELIMB MUSCLES AND NONSTEADY FLIGHT: CAN BIRDS FLY WITHOUT USING THE MUSCLES IN THEIR WINGS? , 1992 .

[89]  J. Steeves,et al.  Coordination of wingbeat and respiration in birds. II. "Fictive" flight. , 1992, Journal of applied physiology.

[90]  K. Dial Activity patterns of the wing muscles of the pigeon (Columba livia) during different modes of flight , 1992 .

[91]  C. Pennycuick,et al.  The profile drag of a hawk's wing, measured by wake sampling in a wind tunnel , 1992 .

[92]  Colin J Pennycuick,et al.  Bird flight performance: a practical calculation manual , 1992 .

[93]  D. Hummel,et al.  Aerodynamic investigations on tail effects in birds , 1992 .

[94]  C. Ellington Limitations on Animal Flight Performance , 1991 .

[95]  R. M. Alexander,et al.  Optimization and gaits in the locomotion of vertebrates. , 1989, Physiological reviews.

[96]  C. J. Pennycuick,et al.  Empirical estimates of body drag of large waterfowl and raptors , 1988 .

[97]  Jeremy M. V. Rayner,et al.  Form and Function in Avian Flight , 1988 .

[98]  G. Spedding The Wake of a Kestrel (Falco Tinnunculus) in Flapping Flight , 1987 .

[99]  Jeremy M. V. Rayner,et al.  Bounding and undulating flight in birds , 1985 .

[100]  Jmv Rayner,et al.  Momentum and energy in the wake of a pigeon (Columba livia) in slow flight , 1984 .

[101]  C. Ellington The Aerodynamics of Hovering Insect Flight. I. The Quasi-Steady Analysis , 1984 .

[102]  K. D. Scholey,et al.  Developments in vertebrate flight : climbing and gliding of mammals and reptiles, and the flapping flight of birds , 1982 .

[103]  P. Withers An Aerodynamic Analysis of Bird Wings as Fixed Aerofoils , 1981 .

[104]  S. Gould,et al.  The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[105]  J. Rayner A vortex theory of animal flight. Part 1. The vortex wake of a hovering animal , 1979, Journal of Fluid Mechanics.

[106]  J. Rayner A vortex theory of animal flight. Part 2. The forward flight of birds , 1979, Journal of Fluid Mechanics.

[107]  C. J. Pennycuick,et al.  Chapter 1 – MECHANICS OF FLIGHT , 1975 .

[108]  K Schmidt-Nielsen,et al.  Locomotion: energy cost of swimming, flying, and running. , 1972, Science.

[109]  A. Hill Dimensions of Animals and their Muscular Dynamics , 1949, Nature.

[110]  H A Hazen,et al.  THE MECHANICS OF FLIGHT. , 1893, Science.

[111]  HORACE B. Porter Flight of Birds , 1874, Nature.