Contractile activity of the pectoralis in the zebra finch according to mode and velocity of flap-bounding flight

SUMMARY We studied flying zebra finch (Taeniopygia guttata, N=12), to provide a new test of a long-standing `fixed-gear' hypothesis that flap-bounding birds use only intermittent non-flapping phases, instead of variation in muscle activity, to vary mechanical power output in flight. Using sonomicrometry and electromyography, we measured in vivo fascicle length and neuromuscular recruitment in the pectoralis as the birds flew in different flight modes (level, ascending, descending; mean velocity 1.6±0.3 m s–1) and across velocities in a new, variable-speed wind tunnel (0–12 m s–1). Synchronized high-speed digital video (250 Hz) provided a record of wing kinematics. Flight mode had a significant effect upon pectoralis strain, strain rate, fractional shortening and the relative timing of muscle activity (onset, offset and duration). Among flight velocities, we observed significant variation in pectoralis strain, fractional lengthening and shortening, strain rate, relative electromyographic (EMG) amplitude, and EMG duration and offset. In particular, variation in strain rate and relative EMG amplitude indicates that the fixed-gear hypothesis should be rejected. Instead, it appears that zebra finch vary work and power output within wingbeats by modulating muscle contractile behavior and between wingbeats using intermittent bounds. Muscle activity patterns and wing kinematics were similar between free flight and wind tunnel flight at similar speeds. Comparing flights with and without surgically implanted transducers and electrodes, zebra finch exhibited a reduction in maximum velocity (from 14 to 12 m s–1) and a significant increase in wingbeat frequency and percent time flapping. This identifies a potential limitation of in vivo flight measurements, and similar studies of bird flight should, therefore, include measurements of the extent to which flight performance is compromised by experimental protocol.

[1]  Gareth Jones,et al.  Bird Flight Performance. A Practical Calculation Manual, C.J. Pennycuick. Oxford University Press, Oxford (1989), x, +153. Price £25 , 1990 .

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

[3]  T. Roberts,et al.  Force-velocity properties of two avian hindlimb muscles. , 2004, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

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

[5]  A. Biewener,et al.  Mechanical power output of bird flight , 1997, Nature.

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

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

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

[9]  Felix Liechti,et al.  Wingbeat frequency of barn swallows and house martins: a comparison between free flight and wind tunnel experiments. , 2002, The Journal of experimental biology.

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

[11]  E. Bandman,et al.  Heterogeneity of myosin heavy-chain expression in fast-twitch fiber types of mature avian pectoralis muscle. , 1996, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[12]  C. Pennycuick,et al.  A new low-turbulence wind tunnel for bird flight experiments at Lund University, Sweden , 1997, The Journal of experimental biology.

[13]  K P Dial,et al.  Flight style of the black-billed magpie: variation in wing kinematics, neuromuscular control, and muscle composition. , 1997, The Journal of experimental zoology.

[14]  Benjamin W. C. Rosser,et al.  The avian pectoralis : histochemical characterization and distribution of muscle fiber types , 1986 .

[15]  R. Marsh,et al.  Optimal shortening velocity (V/Vmax) of skeletal muscle during cyclical contractions: length-force effects and velocity-dependent activation and deactivation. , 1998, The Journal of experimental biology.

[16]  William H. Rae,et al.  Low-Speed Wind Tunnel Testing , 1966 .

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

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

[19]  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.

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

[21]  A. Biewener,et al.  Pectoralis muscle performance during ascending and slow level flight in mallards (Anas platyrhynchos). , 2001, The Journal of experimental biology.

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

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

[24]  A. Aulie Electrical activity from the pectoral muscle of a flying bird, the budgerigar☆ , 1970 .

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

[26]  J. Murray,et al.  Scale Effects in Animal Locomotion. , 1978 .