ABSTRACT In the presence of wind or background image motion, flies are able to maintain a constant retinal slip velocity by regulating flight speed to the extent permitted by their locomotor capacity. Here we investigated the retinal slip compensation of tethered blue bottle flies ( Calliphora vomitoria ) flying semi-freely along an annular corridor in a magnetically levitated flight mill enclosed by two motorized cylindrical walls. We perturbed the flies' retinal slip by spinning the cylindrical walls, generating bilaterally averaged retinal slip perturbations from −0.3 to 0.3 m s −1 (or −116.4 to 116.4 deg s −1 ). When the perturbation was less than ∼0.1 m s −1 (38.4 deg s −1 ), the flies successfully compensated the perturbations and maintained a retinal slip velocity by adjusting their airspeed up to 20%. However, with greater retinal slip perturbation, the flies' compensation became saturated as their airspeed plateaued, indicating that they were unable to further maintain a constant retinal slip velocity. The compensation gain, i.e. the ratio of airspeed compensation and retinal slip perturbation, depended on the spatial frequency of the grating patterns, being the largest at 12 m −1 (0.04 deg −1 ).

ABSTRACT Flies fly at a broad range of speeds and produce sophisticated aerial maneuvers with precisely controlled wing movements. Remarkably, only subtle changes in wing motion are used by flies to produce aerial maneuvers, resulting in little directional tilt of the aerodynamic force vector relative to the body. Therefore, it is often considered that flies fly according to a helicopter model and control speed mainly via force vectoring by body pitch change. Here, we examined the speed control of bluebottle flies using a magnetically levitated (MAGLEV) flight mill, as they fly at different body pitch angles and with different augmented aerodynamic damping. We identified wing kinematic contributors to the changes of estimated aerodynamic force through testing and comparing two force-vectoring models – a constant force-vectoring model and a variable force-vectoring model – while using Akaike's information criterion for selection of the best-approximating model. The results show that the best-approximating variable force-vectoring model, which includes the effects of wing kinematic changes, yields a considerably more accurate prediction of flight speed, particularly in higher velocity range, as compared with those of the constant force-vectoring model. Examination of the variable force-vectoring model reveals that, in the flight mill tethered flight, flies use a collection of wing kinematic variables to control primarily the force magnitude, while the force direction is also modulated, albeit to a smaller extent compared with those due to the changes in body pitch. The roles of these wing kinematic variables are analogous to those of throttle, and collective and cyclic pitch of helicopters.

ABSTRACT Hummingbirds are nature's masters of aerobatic manoeuvres. Previous research shows that hummingbirds and insects converged evolutionarily upon similar aerodynamic mechanisms and kinematics in hovering. Herein, we use three-dimensional kinematic data to begin to test for similar convergence of kinematics used for escape flight and to explore the effects of body size upon manoeuvring. We studied four hummingbird species in North America including two large species (magnificent hummingbird, Eugenes fulgens , 7.8 g, and blue-throated hummingbird, Lampornis clemenciae , 8.0 g) and two smaller species (broad-billed hummingbird, Cynanthus latirostris , 3.4 g, and black-chinned hummingbirds Archilochus alexandri , 3.1 g). Starting from a steady hover, hummingbirds consistently manoeuvred away from perceived threats using a drastic escape response that featured body pitch and roll rotations coupled with a large linear acceleration. Hummingbirds changed their flapping frequency and wing trajectory in all three degrees of freedom on a stroke-by-stroke basis, likely causing rapid and significant alteration of the magnitude and direction of aerodynamic forces. Thus it appears that the flight control of hummingbirds does not obey the ‘helicopter model’ that is valid for similar escape manoeuvres in fruit flies. Except for broad-billed hummingbirds, the hummingbirds had faster reaction times than those reported for visual feedback control in insects. The two larger hummingbird species performed pitch rotations and global-yaw turns with considerably larger magnitude than the smaller species, but roll rates and cumulative roll angles were similar among the four species.

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.

SUMMARY Insects produce a variety of exquisitely controlled manoeuvres during natural flight behaviour. Here we show how hawkmoths produce and control one such manoeuvre, an avoidance response consisting of rapid pitching up, rearward flight, pitching down (often past the original pitch angle), and then pitching up slowly to equilibrium. We triggered these manoeuvres via a sudden visual stimulus in front of free-flying hawkmoths ( Manduca sexta ) while recording the animals' body and wing movements via high-speed stereo videography. We then recreated the wing motions in a dynamically scaled model to: (1) associate wing kinematic changes with pitch torque production and (2) extract the open-loop dynamics of an uncontrolled moth. Next, we characterized the closed-loop manoeuvring dynamics from the observed flight behaviour assuming that hawkmoths use feedback control based on translational velocity, pitch angle and angular velocity, and then compared these with the open-loop dynamics to identify the control strategy used by the moth. Our analysis revealed that hawkmoths produce active pitch torque via changes in mean wing spanwise rotation angle. Additionally, body translations produce passive translational damping and pitch torque, both of which are linearly dependent on the translational velocity. Body rotations produce similar passive forces and torques, but of substantially smaller magnitudes. Our comparison of closed-loop and open-loop dynamics showed that hawkmoths rely largely on passive damping to reduce the body translation but use feedback control based on pitch angle and angular velocity to control their orientation. The resulting feedback control system remains stable with sensory delays of more than two wingbeats.