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

Abstract

The superior manoeuvrability of hummingbirds emerges from complex interactions of specialized neural and physiological processes with the unique flight dynamics of flapping wings. Escape manoeuvring is an ecologically relevant, natural behaviour of hummingbirds, from which we can gain understanding into the functional limits of vertebrate locomotor capacity. Here, we extend our kinematic analysis of escape manoeuvres from a companion paper to assess two potential limiting factors of the manoeuvring performance of hummingbirds: (1) muscle mechanical power output and (2) delays in the neural sensing and control system. We focused on the magnificent hummingbird (Eugenes fulgens, 7.8 g) and the black-chinned hummingbird (Archilochus alexandri, 3.1 g), which represent large and small species, respectively. We first estimated the aerodynamic forces, moments and the mechanical power of escape manoeuvres using measured wing kinematics. Comparing active-manoeuvring and passive-damping aerodynamic moments, we found that pitch dynamics were lightly damped and dominated by the effect of inertia, while roll dynamics were highly damped. To achieve observed closed-loop performance, pitch manoeuvres required faster sensorimotor transduction, as hummingbirds can only tolerate half the delay allowed in roll manoeuvres. Accordingly, our results suggested that pitch control may require a more sophisticated control strategy, such as those based on prediction. For the magnificent hummingbird, we estimated that escape manoeuvres required muscle mass-specific power 4.5 times that during hovering. Therefore, in addition to the limitation imposed by sensorimotor delays, muscle power could also limit the performance of escape manoeuvres.

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

“…In load lifting, hummingbirds rely primarily on increased stroke amplitude to augment lift Chai and Dudley, 1995). A major difference between the load-lifting experiment and the present experiment was that the former usually lasted longer periods of time, as the birds were required to take off by overcoming gravity and then sustain hovering for approximately 1 s, while the duration of escape manoeuvres in our study was ∼0.15 s. At least within the few wingbeats for generating higher manoeuvring forces and moments, the hummingbirds in our study appeared capable of boosting muscle mass-specific power to a substantially higher level than previously observed (Cheng et al, 2016).…”

“…To quantify wing twist for blade-element analysis (Cheng et al, 2016), we assumed that all wing chord sections shared the same stroke and derivation angles while having a linearly varying rotation angle from wing base to tip (e.g. a linear twist model; Leishman, 2006;Walker et al, 2009), where local rotation angle of a wing chord section is a linear function of dimensionless spanwise locationr (0 r 1, where 0 represents the wing base and 1 represents the wing tip):…”

“…Compared with banked yaw turns (Clark, 2011;Muijres et al, 2015), which may create similar global yaw turning angle and end forward velocity, a pitch-roll turn allows a bird to almost instantly burst into backward flight to evade the startle stimulus (or creating larger backward acceleration at the start of the manoeuvre; also see Clark, 2011) and then smoothly transition to forward flight by rolling its body. It also ensures a nearly continuous acceleration towards the direction of escape, but it should require accurate control or preplanning of the timing of roll rotation (Cheng et al, 2016). This interpretation assumes near-maximal flight performance, which is reasonable because the hummingbirds remained vigilant during the experiments.…”

“…Mass-specific power available for loadlifting appears to be invariant with body mass (Altshuler et al, 2004), and this empirical evidence leads to the prediction that capacity for manoeuvring should scale similarly. In contrast, scaling theory (Kumar and Michael, 2012) suggests that smaller species should manoeuvre more easily than larger species so that larger species may require larger wing kinematic changes to achieve similar levels of performance (this has been discussed in a companion paper, Cheng et al, 2016). We address these questions here using detailed examination of the kinematics of escape manoeuvres of four species of hummingbirds that vary in body mass and wing and tail morphology.…”

“…With the goal of improving the understanding of mechanics and control (see companion paper, Cheng et al, 2016), herein we report on the free-flight body and wing kinematics of hummingbirds, during escape from a perceived threat in which their manoeuvring flight performance should be close to maximal (Jackson and Dial, 2011). We hypothesize that hummingbirds take advantage of their jointed wing-skeleton to produce larger deviations in wing kinematics than those used by insects during startle or looming avoidance manoeuvres, allowing for multi-axis acrobatic manoeuvres.…”