Just as the Wright brothers implemented controls to achieve stable airplane flight, flying insects have evolved behavioral strategies that ensure recovery from flight disturbances. Pioneering studies performed on tethered and dissected insects demonstrate that the sensory, neurological, and musculoskeletal systems play important roles in flight control. Such studies, however, cannot produce an integrative model of insect flight stability because they do not incorporate the interaction of these systems with free-flight aerodynamics. We directly investigate control and stability through the application of torque impulses to freely flying fruit flies (Drosophila melanogaster) and measurement of their behavioral response. High-speed video and a new motion tracking method capture the aerial "stumble," and we discover that flies respond to gentle disturbances by accurately returning to their original orientation. These insects take advantage of a stabilizing aerodynamic influence and active torque generation to recover their heading to within 2°in <60 ms. To explain this recovery behavior, we form a feedback control model that includes the fly's ability to sense body rotations, process this information, and actuate the wing motions that generate corrective aerodynamic torque. Thus, like early man-made aircraft and modern fighter jets, the fruit fly employs an automatic stabilization scheme that reacts to short time-scale disturbances.flight control | insect flight | stability | perturbation | fruit fly L ocomotion through natural environments demands mechanisms that maintain stability in the face of unpredictable disturbances. Behavioral strategies play a particularly important role in controlling the flight of insects (1-7), because even gentle air currents can cause large disruptions to the intended flight path. Insects must also contend with the intrinsic instability of flapping flight (8, 9) and the large fluctuations in aerodynamic forces caused by slight variations in wing motions (10, 11). Corrective behavior often takes advantage of vision (1, 2). For fruit flies, however, reaction time to visual stimuli is at least 10 wingbeats (12), so these insects must employ faster sensory circuits to recover from short time-scale disturbances and instabilities. To probe this fast control strategy, we devised an experimental method that imposes impulsive mechanical disturbances (6, 13) to flying insects while allowing us to measure relevant aspects of flight behavior. We first glue tiny ferromagnetic pins to fruit flies and image their free flight using three orthogonally oriented highspeed video cameras (Methods and SI Text). When a fly enters the filming volume, an optical trigger detects the insect, initiates recording, and activates a pair of Helmholtz coils that produce a magnetic field. The field and pin are both oriented horizontally, so the resulting torque on the pin reorients the yaw, or heading angle, of the insect (Fig. 1). We then use a new motion tracking technique to extract the three-dimensional body and w...

Flying insects execute aerial maneuvers through subtle manipulations of their wing motions. Here, we measure the free flight kinematics of fruit flies and determine how they modulate their wing pitching to induce sharp turns. By analyzing the torques these insects exert to pitch their wings, we infer that the wing hinge acts as a torsional spring that passively resists the wing's tendency to flip in response to aerodynamic and inertial forces. To turn, the insects asymmetrically change the spring rest angles to generate rowing motions of their wings. Thus, insects can generate these maneuvers using only a slight active actuation that biases their wing motion.To generate the vertical force necessary to sustain flight, small insects must beat their wings hundreds of times per second. Under this constraint, how do they manipulate these fast wing motions to induce flight maneuvers? Although recent studies have made progress addressing how wing motions generate aerodynamic forces [1,2,3,4], understanding how the wing motions themselves arise and what control variables govern them remains a challenge. To address these questions, we analyze the torques freely-flying fruit flies (D. melanogaster) exert to move their wings. Specifically, we elicit sharp free-flight turns from these flies and measure their wing and body kinematics. By using a model of the aerodynamic forces on flapping wings, we extract the torques the insects exert to generate the wing motions. From these torques, we construct a mechanical model of the wing rotation joints that demonstrates how the interplay of aerodynamic, inertial and biomechanical forces generate the wing kinematics. Finally, we connect this model to the turning dynamics of flies and describe the wing actuation mechanism that unifies these maneuvers.To quantify turning kinematics in fruit flies, we first use three orthogonal cameras to capture their free flight maneuvers at 8000 frames per second or about 35 frames for each wing beat. We then reconstruct the threedimensional wing and body motion of the flies from these videos using the motion tracking techniques described in [5]. The body kinematics, described by the centroid coordinates and three Euler angles -yaw, φ b , body pitch, θ b , and roll, ψ b , are shown in Fig. 1A and visualized in Fig. 1B. During the level flight, the fly performs a 120 • turn in 80 ms, or 18 wing beats.To induce such a turn, the insect generates differences between the motion of its left and right wings. We quantify these changes by plotting in Fig. 1C the time course of three Euler angles -stroke, φ, deviation, θ, and wing pitch, ψ -that describe the orientation of the wings relative to the hinges they rotate about [6]. A three dimensional representation of a typical wing stroke is shown in Fig. 1D. Remarkably subtle asymmetries between the pitch angles of the wings drive the turn. For a discussion of why the other observed asymmetries produce a negligible effect on the yaw dynamics see [7]. To quantify the wing pitch asymmetry that induces the maneuver...

Flying insects have evolved sophisticated sensory–motor systems, and here we argue that such systems are used to keep upright against intrinsic flight instabilities. We describe a theory that predicts the instability growth rate in body pitch from flapping-wing aerodynamics and reveals two ways of achieving balanced flight: active control with sufficiently rapid reactions and passive stabilization with high body drag. By glueing magnets to fruit flies and perturbing their flight using magnetic impulses, we show that these insects employ active control that is indeed fast relative to the instability. Moreover, we find that fruit flies with their control sensors disabled can keep upright if high-drag fibres are also attached to their bodies, an observation consistent with our prediction for the passive stability condition. Finally, we extend this framework to unify the control strategies used by hovering animals and also furnish criteria for achieving pitch stability in flapping-wing robots.

Wing pitch reversal, the rapid change of angle of attack near stroke transition, represents a difference between hovering with flapping wings and with a continuously rotating blade (e.g. helicopter flight). Although insects have the musculature to control the wing pitch during flight, we show here that aerodynamic and wing inertia forces are sufficient to pitch the wing without the aid of the muscles. We study the passive nature of wing pitching in several observed wing kinematics, including the wing motion of a tethered dragonfly, Libellula pulchella, hovering fruitfly, hovering hawkmoth and simplified dragonfly hovering kinematics. To determine whether the pitching is passive, we calculate rotational power about the torsion axis owing to aerodynamic and wing inertial forces. This is done using both direct numerical simulations and quasi-steady fluid force models. We find that, in all the cases studied here, the net rotational power is negative, signifying that the fluid force assists rather than resists the wing pitching. To further understand the generality of these results, we use the quasi-steady force model to analyse the effect of the components of the fluid forces at pitch reversal, and predict the conditions under which the wing pitch reversal is passive. These results suggest the pitching motion of the wings can be passive in insect flight.