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

Abstract

Summary The biomechanical and neuromuscular mechanisms used by different animals to generate turns in flight are highly variable. Body size and body plan exert some influence, e.g., birds typically roll their body to orient forces generated by the wings whereas insects are capable of turning via left-right wingbeat asymmetries. Turns are also relatively brief and have low repeatability with almost every wingbeat serving a different function throughout the change in heading. Here we present an analysis of Anna’s hummingbirds (Calypte anna) as they fed continuously from an artificial feeder revolving around the outside of the animal. This setup allowed for examination of sustained changes in yaw without requiring any corresponding changes in pitch, roll, or body position. Hummingbirds sustained yaw turns by expanding the wing stroke amplitude of the outer wing during the downstroke and by altering the deviation of the wingtip path during both downstroke and upstroke. The latter led to a shift in the inner-outer stroke plane angle during the upstroke and shifts in the elevation of the stroke plane and in the deviation of the wingtip path during both strokes. These features are generally more similar to how insects, as opposed to birds, turn. However, time series analysis also revealed considerable stroke-to-stroke variation. Changes in the stroke amplitude and the wingtip velocity were highly cross-correlated as were changes in the stroke deviation and the elevation of the stroke plane. As was the case for wingbeat kinematics, electromyogram recordings from pectoral and wing muscles were highly variable, but no correlations were found between these two features of motor control. The high variability of both kinematic and muscle activation features indicates a high level of wingbeat-to-wingbeat adjustments during sustained yaw. The activation timing of the muscles was more repeatable than the activation intensity, which suggests that the former may be constrained by harmonic motion and that the latter may play a large role in kinematic adjustments. Comparing the revolution frequency of the feeder to measurements of free flight yaws reveals that feeder tracking, even at one revolution every two seconds, is well below the maximum yaw capacity of the hummingbirds.

Flight mechanics and control of escape manoeuvres in hummingbirds I. Flight kinematics

“…2B). Similar bilateral-asymmetric changes in the wing deviation and stroke plane angle have been observed in significantly slower yaw turns in Anna's hummingbirds (Calypte anna) as they fed continuously from a revolving artificial feeder (Altshuler et al, 2012;Read et al, 2016). Bilateral differences of wing spanwise rotation corresponded to reduced pronation and enhanced supination for the inner wing so that its stroke-averaged lift was reoriented backwards and was more perpendicular to the body longitudinal axis.…”

“…6) and, correspondingly, the wing velocity led to an imbalance of lift between the inner and outer wings, and therefore also created a liftbased roll moment. Bilateral-asymmetric changes in the wing stroke amplitude were also observed by Altshuler et al (2012). Roll moment was mostly created during the downstrokes, when total force was mostly perpendicular to the body longitudinal axis; during the upstroke, the total force was approximately parallel to the longitudinal body axis, and was thus less effective in creating roll moment, but more effective in creating yaw moment; this interpretation is confirmed through aerodynamic analysis (Cheng et al, 2016).…”

Evolution of avian flight: muscles and constraints on performance

“…All of the distal wing muscles exhibit neuromuscular activation during steady fight, but they exhibit increased recruitment in non-steady modes such as take-off or manoeuvring [77][78][79]84]. It is not clear that bilateral asymmetry in activation of these muscles is necessary for manoeuvring [77,84,85]. New tests of muscular contributions to wing morphing are warranted, and this is a prominent example of where we have extremely limited comparative data.…”

Flight mechanics and control of escape manoeuvres in hummingbirds II. Aerodynamic force production, flight control and performance limitations

“…For flying animals, the primary limiting factors of flight performance or manoeuvrability are arguably twofold: (1) attainable muscle mechanical power output (Altshuler et al, 2010a;Ellington, 1985Ellington, 1991Marden, 1994) associated with generation of aerodynamic manoeuvring forces and moments that create and maintain fast body movements, and (2) effective coordination of these movements using fast and accurate flightsensing and motor-control systems (Altshuler et al, 2012(Altshuler et al, , 2010bGoller and Altshuler, 2014;Iwaniuk and Wylie, 2007;Warrick et al, 2002). Limits of muscle mechanical power of hummingbirds have been extensively tested using load-lifting performance in short-burst flight (Altshuler et al, 2010a;Chai and Dudley, 1995;Marden, 1987Marden, , 1994.…”