Muscle function in avian flight: achieving power and control

Abstract

Flapping flight places strenuous requirements on the physiological performance of an animal. Bird flight muscles, particularly at smaller body sizes, generally contract at high frequencies and do substantial work in order to produce the aerodynamic power needed to support the animal's weight in the air and to overcome drag. This is in contrast to terrestrial locomotion, which offers mechanisms for minimizing energy losses associated with body movement combined with elastic energy savings to reduce the skeletal muscles' work requirements. Muscles also produce substantial power during swimming, but this is mainly to overcome body drag rather than to support the animal's weight. Here, I review the function and architecture of key flight muscles related to how these muscles contribute to producing the power required for flapping flight, how the muscles are recruited to control wing motion and how they are used in manoeuvring. An emergent property of the primary flight muscles, consistent with their need to produce considerable work by moving the wings through large excursions during each wing stroke, is that the pectoralis and supracoracoideus muscles shorten over a large fraction of their resting fibre length (33-42%). Both muscles are activated while being lengthened or undergoing nearly isometric force development, enhancing the work they perform during subsequent shortening. Two smaller muscles, the triceps and biceps, operate over a smaller range of contractile strains (12-23%), reflecting their role in controlling wing shape through elbow flexion and extension. Remarkably, pigeons adjust their wing stroke plane mainly via changes in whole-body pitch during take-off and landing, relative to level flight, allowing their wing muscles to operate with little change in activation timing, strain magnitude and pattern.

Muscle architecture of the forelimb of the Golden Pheasant (Chrysolophus pictus) (Aves: Phasianidae) and its implications for functional capacity in flight

“…Electromyographic (EMG) data indicate that intrinsic muscles of the wing contribute little additional mechanical power for flight, but are important in modulating wing orientation and controlling wing shape (Dial 1992a(Dial , 1992bBiewener 2011). Due to the difficulty of in vivo force measurements for smaller muscles located more distally in the wing, the roles of these muscles in adjusting the wing, as well as their functional specializations, remain largely unknown (Biewener 2011). Given this circumstance, analysis of muscle architecture can play an important role in evaluating the role of muscles.…”

Modulation of upper limb joint work and power during sculling while ballasted with varying loads

“…This is unlike flying animals, for example, that store and release wing inertial energy in the tendon of pectoralis (amounting to 18% of the positive work the muscle performs) to aid the upstroke to downstroke transition (Biewener, 2011). The existence of springs in swimming vertebrates is much more controversial.…”

“…Just as humans move their arms for hydrodynamic propulsion, birds generate aerodynamic lift to power flight by moving their wings through large excursions. Rapid wing flap is achieved by large proximal muscles shortening over a significant fraction of their resting fiber length, producing considerable work (Biewener, 2011). Small muscles located at the elbow operate over shorter strains to control wing shape and orientation, yet show both work production and absorption (Robertson and Biewener, 2012).…”

Gamebirds: A sustainable food source in Southern Africa?

“…In poultry, this is sold with the sternum intact (whole breast) or the muscle can be removed and sold as a deboned portion. The large breast muscle (M. pectoralis) is mainly used during flying when it is responsible for the downward movement of the wings and the M. supracoracoideus is the muscle which raises the wing during the upward movement (Poore et al 1997;Dial 1992;Swatland 2000;Biewener 2011). The breast muscle of gamebirds such as Egyptian geese which fly long distances will therefore endure a higher level of activity compared to that of terrestrial gamebird species.…”