Fruit Flies Modulate Passive Wing Pitching to Generate In-Flight Turns

Abstract

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...

Discovering the flight autostabilizer of fruit flies by inducing aerial stumbles

“…Determination of the wiring and firing of these neurons would offer insight into the neurological basis of signal integration and summation (27). Third, we find that wing orientation adjustments during autostabilization are remarkably similar to those used for voluntary turns (15) and hypothesize that they result from the same musculoskeletal elements (21). We stress, however, that our experiments strictly address the fruit fly's reflexive turning response to mechanical stimuli rather than visually induced turning behavior.…”

“…This important effect is, of course, entirely removed in studies that rigidly tether insects (12). Even in experimental preparations that loosely confine the motion of insects (23,24), turning kinematics are different from those observed in free-flight studies (10,15,25). These discrepancies indicate that restrictive preparations interfere with flight behavior, and the results of such studies must be interpreted in light of this influence.…”

“…In the third image, the right and left wings have different projected areas due to different attack angles. When the attack angle on one wing is greater than the other, the larger area presented to the flow induces a greater drag force, and this unbalanced drag causes the insect to rotate (15). We quantify the asymmetric "rowing" wing motions by measuring the complete wing kinematics (14), and we verify that fruit flies drive yaw corrective maneuvers by differentially varying wing angle of attack.…”

“…To reorient its body, the fly induces differences between the right and left wing motions, thus generating aerodynamic torque. A recent analysis of free-flight turning maneuvers of fruit flies indicates that these insects generate yaw torque by asymmetrically adjusting the wing angles of attack, α, defined as the inclination angle of each wing relative to its velocity (15). Qualitatively, these differences can be seen in the top-view stills from the flight videos, as shown in Fig.…”

“…4C and D, and torque is generated from unbalanced drag on the wings. For example, to turn rightward, the fly employs a higher average attack angle α on the right wing for the forward stroke and a higher α on the left wing for the backward stroke (15). These rowing motions generate differential drag on the wings and thus produce the yaw torque, N fly , that drives the corrective body rotation.…”