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Review
. 2016 Sep 26;371(1704):20150383.
doi: 10.1098/rstb.2015.0383.

Evolution of avian flight: muscles and constraints on performance

Affiliations
Review

Evolution of avian flight: muscles and constraints on performance

Bret W Tobalske. Philos Trans R Soc Lond B Biol Sci. .

Abstract

Competing hypotheses about evolutionary origins of flight are the 'fundamental wing-stroke' and 'directed aerial descent' hypotheses. Support for the fundamental wing-stroke hypothesis is that extant birds use flapping of their wings to climb even before they are able to fly; there are no reported examples of incrementally increasing use of wing movements in gliding transitioning to flapping. An open question is whether locomotor styles must evolve initially for efficiency or if they might instead arrive due to efficacy. The proximal muscles of the avian wing output work and power for flight, and new research is exploring functions of the distal muscles in relation to dynamic changes in wing shape. It will be useful to test the relative contributions of the muscles of the forearm compared with inertial and aerodynamic loading of the wing upon dynamic morphing. Body size has dramatic effects upon flight performance. New research has revealed that mass-specific muscle power declines with increasing body mass among species. This explains the constraints associated with being large. Hummingbirds are the only species that can sustain hovering. Their ability to generate force, work and power appears to be limited by time for activation and deactivation within their wingbeats of high frequency. Most small birds use flap-bounding flight, and this flight style may offer an energetic advantage over continuous flapping during fast flight or during flight into a headwind. The use of flap-bounding during slow flight remains enigmatic. Flap-bounding birds do not appear to be constrained to use their primary flight muscles in a fixed manner. To improve understanding of the functional significance of flap-bounding, the energetic costs and the relative use of alternative styles by a given species in nature merit study.This article is part of the themed issue 'Moving in a moving medium: new perspectives on flight'.

Keywords: bound; flap; glide; hover; pectoralis; supracoracoideus.

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Figures

Figure 1.
Figure 1.
A cross-section of a shed vortex in the wake of a baby chukar (Alectoris chukar), 6 d.p.h., as measured using particle image velocimetry as the bird engaged in wing-assisted incline running [40].
Figure 2.
Figure 2.
Wing-tip reversal upstroke in a pigeon (Columba livia) engaged in slow forward flight [72]. The wing morphs constantly during the upstroke; where it is flexed, there is long-axis twist due to supination of the distal wing, and the feathers are bent. The relative contribution of the muscles to such morphing is not well understood.
Figure 3.
Figure 3.
Scaling of pectoralis strain during escape take-off in four species in the Phasianidae (from [23]). (a) Species drawn to scale, along with hypothesized phylogenetic relationships: northern bobwhite (Colinus virginianus), chukar (Alectoris chukar), ring-necked pheasant (Phasianus colchicus) and wild turkey (Meleagris gallopavo). Branch lengths are in millions of years. (b) Reduced-major-axis regression of pectoralis strain in relation to body mass; independent contrasts regression has steeper slope: y = 0.23x.
Figure 4.
Figure 4.
Muscle contractile behaviour in hummingbirds. (a) Relative timing of activation in the pectoralis (PECT) and supracoracoideus (SUPRA) of a rufous hummingbird (Selasphorus rufus) and a rock pigeon (Columba livia). Downstroke is defined using wrist motion in the hummingbird and pectoralis length in the pigeon. EMG, electromyography (from [96]). (b) Transmission ration, the ratio of wing flapping amplitude to muscle strain varies proportional to mass-0.20 in a variety of insect and bird species (filled square, ruby-throated hummingbird, Archilocus colubris; circles, Corvidae; diamonds, Phasianidae; open squares, other birds; triangles, insects). From Hedrick et al. [16].
Figure 5.
Figure 5.
Kinematics, aerodynamics and muscle activity during flap-bounding flight in zebra finch (Taeniopygia guttata). (a) Flight in a wind tunnel at 12 m s−1 illustrating body and wing motion, muscle strain as measured using sonomicrometry, and neuromuscular activity measured using EMG. (b) During bounds airflow over the body and tail creates body lift and a pair of counter-rotating vortices are shed into the wake. (c) Contractile velocity in the pectoralis varies significantly among flight speeds (from Tobalske et al. [73,104]).

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