Neuromuscular control of wingbeat kinematics in Anna's hummingbirds (Calypte anna)

Abstract

SUMMARYHummingbirds can maintain the highest wingbeat frequencies of any flying vertebrate -a feat accomplished by the large pectoral muscles that power the wing strokes. An unusual feature of these muscles is that they are activated by one or a few spikes per cycle as revealed by electromyogram recordings (EMGs). The relatively simple nature of this activation pattern provides an opportunity to understand how motor units are recruited to modulate limb kinematics. Hummingbirds made to fly in low-density air responded by moderately increasing wingbeat frequency and substantially increasing the wing stroke amplitude as compared with flight in normal air. There was little change in the number of spikes per EMG burst in the pectoralis major muscle between flight in normal and low-density heliox (mean1.4spikescycle -1 ). However the spike amplitude, which we take to be an indication of the number of active motor units, increased in concert with the wing stroke amplitude, 1.7 times the value in air. We also challenged the hummingbirds using transient load lifting to elicit maximum burst performance. During maximum load lifting, both wing stroke amplitude and wingbeat frequency increased substantially above those values during hovering flight. The number of spikes per EMG burst increased to a mean of 3.3 per cycle, and the maximum spike amplitude increased to approximately 1.6 times those values during flight in heliox. These results suggest that hummingbirds recruit additional motor units (spatial recruitment) to regulate wing stroke amplitude but that temporal recruitment is also required to maintain maximum stroke amplitude at the highest wingbeat frequencies.

Hummingbirds generate bilateral vortex loops during hovering: evidence from flow visualization

“…The hummingbirds in the kinematics experiment exhibited values for these variables that are similar to what has previously been reported for male C. anna during hovering (Altshuler et al 2010b). On average, the hummingbirds in the flow visualization experiment used lower stroke amplitudes and higher wingbeat frequencies, but the individual birds were also more variable.…”

Wingbeat kinematics and motor control of yaw turns in Anna's hummingbirds (Calypte anna)

“…Hummingbirds can hover like many insects and, during this behavior, the pectoralis major has a relatively simple activation pattern composed of only one to three spikes (Hagiwara et al, 1968). Experiments in lowdensity air, during load lifting and in a wind tunnel demonstrate an association between the maximum electromyogram (EMG) spike amplitude from this muscle and the wingstroke amplitude (Altshuler et al, 2010;Tobalske et al, 2010). The hummingbird therefore presents an opportunity to examine neuromuscular and kinematic mechanisms of turning in birds that can be directly compared with the extensive literature on insect flight control.…”

“…Our intention was to target the pectoralis major (PM) and the pronator superficialis (PS) on both the left and right sides. The PM was targeted because it powers the downstroke and its activity varies in response to mechanical demands (Hagiwara et al, 1968;Altshuler et al, 2010;Tobalske et al, 2010). The PS was targeted because it is one of the larger superficial muscles in the The Journal of Experimental Biology 215 (23) hummingbird wing (Welch and Altshuler, 2009).…”

“…The PM is unusual in having a relatively small number of discrete excitation waveforms, and the spike amplitudes are correlated with wingbeat kinematics and flight speeds (Hagiwara et al, 1968;Altshuler et al, 2010;Tobalske et al, 2010). We accordingly used the occurrence of the first spike (t) as the measure of activation timing relative to the wingbeat, and the normalized maximum spike amplitude (E max ) as the measure of activation intensity.…”

Evolution of avian flight: muscles and constraints on performance

“…Pectoralis strain is 11% in the rufous hummingbird (Selasphorus rufus), much less than in larger bird species where it varies up to 35% or more [36,96]. Neural recruitment of the primary flight muscles is extremely brief in relative duration to the wingbeat, the number of electromyographic spikes per contraction is much smaller than in other species, varying from one to four spikes per contraction [96][97][98].…”