precise time course of force production, they are typically ignored in biomechanical analyses of insect flight.

The salient feature that distinguishes the translational forces of insect wings from those generated by airplanes, helicopters, and most birds is that the wings flap back and forth at relatively high angles of attack (30-45°). At such high angles, the stream of air separates from the leading edge of the wing, forming a characteristic flow structure called a leading edge vortex. The lift resulting from the leading edge vortex is much greater than that produced by the bound circulation generated at lower angles of attack. This transient increase in lift at the start of motion at high angles of attack, termed delayed stall, was first recognized by aeronautics engineers in England in the early 1930s, but is too brief to be of use to most aircraft. After only a few moments, the vortex structure grows too large and is shed into the wake, resulting in a precipitous drop in lift. Insects, however, can make use of the initial stages of stall because their wings strokes are so brief. At the end of each stroke the wing sheds the vortex, rotates, and develops a new leading edge vortex swirling in the opposite direction. In addition, complex three-dimensional aspects of the flow, such as a base-to-tip helical flow of air through the center of the vortex, may in some cases remove energy from the structure, enabling it to remain attached to the wing throughout the stroke.

Rotating objects are themselves sources of circulation and concomitant lift production, which is why a tennis ball hit with backspin rises as it moves through the air. The physics of circular balls and flat wings is somewhat different because the wing has sharp leading and trailing edges, but in both examples the act of rotation serves as a source of circulation, creating a faster flow of air over the top surface resulting in an elevated pressure force. The direction of this rotational force is such that the wing generates positive lift if it flips over before stroke reversal and negative lift if the wing flip is delayed until after stroke reversal, which are kinematic conditions roughly analogous to backspin and topspin on a tennis ball. Thus, unlike the translational component of the total aerodynamic force, the rotational component is strongly dependent on the precise timing of rotation between strokes. For this reason, rotational forces may be particularly important for steering and flight control.

After reversing direction, the wing does not move through undisturbed air, but rather collides with the wake generated during the previous stroke. Because the leading edge vortex moves downward after it is shed, its influence on the flow around the wing is maximal at the start of wing translation, but then rapidly diminishes. Nevertheless, the instantaneous air velocity experienced by the wing at the start of each stroke can be substantially greater than that caused by its own flapping speed. Under certain conditions, this increased flow can result in additional force by a mechanism called wake capture. Because a vortex wake represents the energy lost to the fluid by a moving object, wake capture is an aerodynamic mechanism that enables an insect to recover some of the energy otherwise lost to the air. As with rotational forces, wake capture may play a particularly important role in flight control and maneuverability. By changing the timing and speed of wing rotation, insects can manipulate the magnitude and direction of forces during stroke reversal, thereby manipulating force moments around the body's center of mass.

The wake generated by the wings influences aerodynamic forces in other ways. Vortices shed from the wings drive a column of air downward from the plane of wing motion, which is a change in fluid momentum that is equivalent to the average upward force on the wings. This downwash alters the flow around the wings, but reduces the effective aerodynamic angle of attack and thus attenuates the production of translational forces. In addition, flow interactions may occur among the wings on the same insect. For example, in some insects the close apposition and subsequent rotation of the wings at the beginning of the downstroke, termed the "clap" and "fling," augment force production at the start of the stroke by enhancing the development of the leading edge vortex. In four-winged insects such as dragonflies, the wake of the forewing might under certain conditions increase the forces created by the hind wing.

Although certain general aerodynamic principles apply to all insects, the precise details of flight aerodynamics likely vary in concert with the extreme morphological and behavioral diversity found among the species. The force-generating mechanisms described above, as well as additional mechanisms yet to be discovered, are best viewed as a palette from which the flight behavior of any given species is constructed. The long-term goal for the study of insect flight aerodynamics is not only to uncover the mechanism by which any particular species stays in the air but also to show how it manipulates various mechanisms to maneuver and accomplish the aerial behaviors that are necessary for its survival and reproduction. Recent work in elucidating specific aerodynamic mechanisms must be viewed as only a starting point toward a more comprehensive understanding of flight mechanics and behavior.

NEURAL CONTROL Sensory Systems

The extreme morphological adaptations associated with flight behavior in insects are paralleled by equally impressive special izations within the nervous system. Perhaps most extreme among these alterations relative to the basic neural organization of wingless insects is the hypertrophy of the compound eyes and associated visual ganglia. Large eyes capable of rapid response and broad adaptation to ambient light level are characteristic of diurnal insects such as butterflies, dragonflies, bees, wasps, and true flies. The visual system provides essential sensory feedback for flight control in most diurnal species and is used for a variety of tasks, including velocity and altitude control, obstacle avoidance, landing responses, target recognition, and spatial memory. Features of the anatomy and physiology of the visual system of individual species correlate well with flight behavior and habitat. The elevated translational and rotational speeds characteristic of flight, particularly compared with those of walking and running, place a premium on rapid response time of the visual system. The enhanced visual processing speeds of insects is exemplified by the flicker fusion rate of house flies, which at roughly 300 Hz is the highest found among all animals.

In addition to the eyes, several other sensory modalities on the head provide critical feedback during flight. Although incapable of extracting detailed spatial information, output from the three ocelli helps to stabilize pitch and roll. Because the associated neural computations are relatively simple, the ocellar system can detect and process changes in body orientation more rapidly than can the visual system. Hair cells on the head and mechanoreceptors at the base of the antennae are capable of measuring the magnitude and direction of airflow during flight. In conjunction with visual measurements of ground speed, the input from these windsensitive cells is crucial for calculating ambient wind direction, an important capability for flying upwind or tracking odor sources, which are detected in part by chemosensory sensilla on the antennae.

Although sensory structures on the head provide relatively slow tonic cues used for modulating wing motion or body posture over many wingbeats, sensory input from mechanosen-sory cells on the thorax provides fast phasic input that can alter wing movements on a cycle-by-cycle basis. These mechanosensory structures include the tegula, an organ below the wing that is stimulated during the downstroke, and stretch receptors embedded in the wing hinge that fire during the upstroke. Wing veins contain arrays of tiny campaniform sensilla that encode deformations of the wing surface throughout the stroke. In flies, these arrays are greatly elaborated at the base of tiny drumstick-shaped hind wings called halteres, which function as equilibrium organs. Associated sensory fields detect the Coriolis forces that deflect the beating haltere when the animal's body rotates during flight. Remarkably, a similar specialization is found among stresipterans, but in these insects it is the forewing that has been transformed into an equilibrium organ, whereas the hind wings retain the aerodynamic function. Although the precise role of the thoracic mechanosensory organs varies from species to species, their general function is to tune the output

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