On the mechanism of speed and altitude control in Drosophila melanogaster

ABSTRACT The total power output of tethered flying Drosophila melanogaster in still air depends on translational velocity components of image flow on the eye, whereas the orientation of the average flight force in the midsagittal plane of the fly is widely independent of visual input (Götz, 1968). The fly does not seem to control the vertical and the horizontal force component independently. Freely flying flies nevertheless generate different ratios between lift and thrust, simply by changing the inclination of their body. By the combined adjustment of the body angle and the total power output a fly appears to be able to stabilize height and speed (David, 1985). Here a possible mechanism is proposed by which the appropriate torque about the transverse body axis could be generated. Translational pattern motion influences the posture of the abdomen and the plane of wing oscillation. Thus the position of the centre of gravity relative to the flight force vector is changed. When abdomen and stroke plane deviate from an equilibrium state, a lever is generated by which the force vector will rotate the fly about its transverse axis.     

How does lateral abdomen deflection contribute to flight control ofDrosophila melanogaster?

Summary Tethered flyingDrosophila melanogaster change the posture of their caudal body appendages in response to visual stimuli. In the present paper the relevance of lateral abdomen deflections for flight control is analysed. During abdomen deflections the line of action of the gravitational force is shifted with the fly's centre of mass. The line of action of aerodynamic drag forces is displaced accordingly, because friction is increased on the side of the body to which the abdomen is deflected. These two passive forces, together with the average flight forces generated actively by the wings, induce a yaw moment. In still air, the axis of this torque is tilted about 30° backwards relative to the vertical body axis. It will be called yaw axis of the flight mechanics. Two sets of observations support the notion of a combined yaw motor output. (a) The elementary motion detectors mediating the lateral abdomen deflection and the dynamics of the response resemble that of the optomotor response measured as yaw torque or as variation of wing beat amplitudes. (b) The asymmetric directional selectivity of the motion detecting system mediating the abdomen deflection corresponds to the orientation of the yaw axis of the flight mechanics. To explain the asymmetry, a nonlinear transfer characteristic is assumed in the motion detecting system.Abbreviations EMD elementary motion detector - MDF motion detector field     

Localization of the receptors that initiate and maintain flight in the cockroach, Periplaneta americana

Using local air streams, screening and surgical removal of the cerci and antennae, studies have been made on the receptors which provide for initiation and maintenance of the flight in the cockroach. It was shown that in suspended insect which lacks any contacts of legs with the base, the flight may be initiated by direct air currents either on the cerci, or antennae. Receptors which maintain the flight are located on the antennae and wings, the prolonged flight being provided mainly by antennae receptors.     

Numerical investigation of the aerodynamic characteristics of a hovering Coleopteran insect

The aerodynamic characteristics of the Coleopteran beetle species Epilachna quadricollis, a species with flexible hind wings and stiff elytra (fore wings), are investigated in terms of hovering flight. The flapping wing kinematics of the Coleopteran insect are modeled through experimental observations with a digital high-speed camera and curve fitting from an ideal harmonic kinematics model. This model numerically simulates flight by estimating a cross section of the wing as a two-dimensional elliptical plane. There is currently no detailed study on the role of the elytron or how the elytron-hind wing interaction affects aerodynamic performance. In the case of hovering flight, the relatively small vertical or horizontal forces generated by the elytron suggest that the elytron makes no significant contribution to aerodynamic force.     

Mosquito bioacoustics: Auditory processing in <Emphasis Type="Italic">Culex pipiens pipiens</Emphasis> L. Males (Diptera,Culicidae) during flight simulation

As a part of mating behavior, male mosquitoes detect and locate females by listening to the sound of their wingbeats. Up to date, the auditory physiological properties in mosquitoes were studied in steady preparations. However, the sensory organs of a flying insect are affected by strong vibrations caused by its own flight muscles and wings. This influence can sufficiently modify the perception due to the nonlinear characteristics of the receptor cells. The aim of this study was to demonstrate the effect of flight conditions on the functioning of Johnston’s organs (hearing organs) in the male mosquitoes Culex pipiens pipiens L. To simulate the flight conditions, a small amount of air around the mosquito was oscillated at 500 Hz along the dorso-ventral axis. These air oscillations affected the pinnate antennae of the mosquito, causing vibration of the antennal flagellum which, in turn, was transmitted to and sensed by Johnston’s organ. Along with the flight simulation, the mosquito was stimulated by low-amplitude sinusoidal auditory signals of different frequencies. The responses were recorded from neurons using glass microelectrodes. The auditory responses contained two rhythms of amplitude modulation which were produced due to nonlinear processes in the receptors: the first rhythm had the difference frequency of flight simulation and the stimulus; the second rhythm corresponded to the beating of heterodyne frequencies. As compared to the steady-state conditions, an additional optimum of auditory sensitivity at 540–640 Hz (the so-called image channel) was shown to appear during flight simulation. This optimum corresponds to the second harmonic of the conspecific female sound. An improvement of sensitivity by 7 dB (2.2-fold) was also observed at the main optimum (220–320 Hz). We conclude that the mechanical influence of locomotor movements not only produces noise but can also improve the sensitivity of the sensory system or even add new properties.     

Activity of descending contralateral movement detector neurons and collision avoidance behaviour in response to head-on visual stimuli in locusts

We recorded the activity of the right and left descending contralateral movement detectors responding to 10-cm (small) or 20-cm (large) computer-generated spheres approaching along different trajectories in the locust's frontal field of view. In separate experiments we examined the steering responses of tethered flying locusts to identical stimuli. The descending contralateral movement detectors were more sensitive to variations in target trajectory in the horizontal plane than in the vertical plane. Descending contralateral movement detector activity was related to target trajectory and to target size and was most sensitive to small objects converging on a direct collision course from above and to one side. Small objects failed to induce collision avoidance manoeuvres whereas large objects produced reliable collision avoidance responses. Large targets approaching along a converging trajectory produced steering responses that were either away from or toward the side of approach of the object, whereas targets approaching along trajectories that were offset from the locust's mid-longitudinal body axis primarily evoked responses away from the target. We detected no differences in the discharge properties of the descending contralateral movement detector pair that could account for the different collision avoidance behaviours evoked by varying the target size and trajectories. We suggest that descending contralateral movement detector properties are better suited to predator evasion than collision avoidance.     

On the coordination of motor output during visual flight control of flies

Summary In tethered flying houseflies (Musca domestica), the yaw torque produced by the wings is accompanied by postural changes of the abdomen and hindlegs. In free flight, these body movements would jointly lead to turning manoeuvres of the animal. By recording the yaw torque together with the lateral deflections of either the abdomen or the hindlegs, it is shown that these motor output systems act in a highly synergistic way during two types of visual orientation behavior, compensatory optomotor turning reactions and orientation turns elicited by moving objects. This high degree of coordination is particularly conspicuous for the pathway activated by moving objects. Here, orientation responses either may be induced or may fail to be generated always simultaneously in all three motor output systems. This suggests that the pathway mediating orientation turns towards objects is gated before it segregates into the respective motor control systems of the wings, the abdomen and the hindlegs.     

Control for small-speed lateral flight in a model insect

Controls required for small-speed lateral flight of a model insect were studied using techniques based on the linear theories of stability and control (the stability and control derivatives were computed by the method of computational fluid dynamics). The main results are as follows. (1) Two steady-state lateral motions can exist: one is a horizontal side translation with the body rolling to the same side of the translation by a small angle, and the other is a constant-rate yaw rotation (rotation about the vertical axis). (2) The side translation requires an anti-symmetrical change in the stroke amplitudes of the contralateral wings, and/or an anti-symmetrical change in the angles of attack of the contralateral wings, with the down- and upstroke angles of attack of a wing having equal change. The constant-rate yaw rotation requires an anti-symmetrical change in the angles of attack of the contralateral wings, with the down- and upstroke angles of attack of a wing having differential change. (3) For the control of the horizontal side translation, control input required for the steady-state motion has an opposite sign to that needed for initiating the motion. For example, to have a steady-state left side-translation, the insect needs to increase the stroke amplitude of the left wing and decrease that of the right wing to maintain the steady-state flight, but it needs an opposite change in stroke amplitude (decreasing the stroke amplitude of the left wing and increasing that of the right wing) to enter the flight.     

Gliding behaviour elicited by lateral looming stimuli in flying locusts

We challenged tethered, flying locusts with visual stimuli looming from the side towards one eye in a way that mimics the approach of a predatory bird. Locusts respond to the lateral approach of a looming object with steering movements and a stereotyped, rapid behaviour in which the wingbeat pattern ceases and the wings are swept into a gliding posture. This gliding behaviour may cause the locust to dive. The gliding posture is maintained for 200 ms or more after which flight is resumed with an increased wingbeat frequency or else the wings are folded. A glide begins with a strong burst of activity in the mesothoracic second tergosternal motor neuron (no. 84) on both sides of the locust. Recordings of descending contralateral movement detector (DCMD) activity in a flying locust show that it responds to small (80-mm diameter) looming stimuli during tethered flight, with a prolonged burst of spikes that tracks stimulus approach and reaches peak instantaneous frequencies as, or after, stimulus motion ceases. There is a close match between the visual stimuli that elicit a gliding behaviour and those that are effective at exciting the DCMD neuron. Wing elevation into the gliding posture occurs during a maintained burst of high frequency DCMD spikes.     

A wing-assisted running robot and implications for avian flight evolution

DASH+Wings is a small hexapedal winged robot that uses flapping wings to increase its locomotion capabilities. To examine the effects of flapping wings, multiple experimental controls for the same locomotor platform are provided by wing removal, by the use of inertially similar lateral spars, and by passive rather than actively flapping wings. We used accelerometers and high-speed cameras to measure the performance of this hybrid robot in both horizontal running and while ascending inclines. To examine consequences of wing flapping for aerial performance, we measured lift and drag forces on the robot at constant airspeeds and body orientations in a wind tunnel; we also determined equilibrium glide performance in free flight. The addition of flapping wings increased the maximum horizontal running speed from 0.68 to 1.29 m s?1, and also increased the maximum incline angle of ascent from 5.6° to 16.9°. Free flight measurements show a decrease of 10.3° in equilibrium glide slope between the flapping and gliding robot. In air, flapping improved the mean lift:drag ratio of the robot compared to gliding at all measured body orientations and airspeeds. Low-amplitude wing flapping thus provides advantages in both cursorial and aerial locomotion. We note that current support for the diverse theories of avian flight origins derive from limited fossil evidence, the adult behavior of extant flying birds, and developmental stages of already volant taxa. By contrast, addition of wings to a cursorial robot allows direct evaluation of the consequences of wing flapping for locomotor performance in both running and flying.     

Control of flight by means of lateral visual stimuli in gregarious desert locusts, Schistocerca gregaria

Abstract. Tethered flying locusts were stimulated either by a periodic grating or by a spotted 'swarm-simulating' pattern moving horizontally, parallel to their longitudinal body axis within their lateral visual fields. The direction of movement of the pattern was changed periodically from progressive to regressive and vice versa.
Both kinds of patterns induced a correlated modulation of yaw-torque and thrust. The two measured flight parameters were modulated independently of each other. Each parameter either increased with progressive and decreased with regressive pattern motion or vice versa. The characteristic curves of thrust and yaw-torque responses - i.e. response amplitude versus contrast frequency resp. angular velocity – measured upon stimulation with the periodic grating between 2 and 70 Hz were at a maximum at 10 Hz and decreased at higher and lower contrast frequencies. The shape of the curves was nearly identical. The characteristic curves measured upon stimulation with the 'swarm-simulating' pattern between 60 and 1500^o s^-1 could be simulated using the spatial wavelength content of the pattern and the characteristic curves for periodic gratings.
Therefore, we suggest that the speed and direction of locusts' flight result from the optomotor effectiveness of the pattern image formed by the neighbouring individuals under free flight. The measured responses would thus contribute to the common orientation of groups of locusts within a migrating swarm and thus to swarm cohesion.     

Kinematic compensation for wing loss in flying damselflies

Flying insects can tolerate substantial wing wear before their ability to fly is entirely compromised. In order to keep flying with damaged wings, the entire flight apparatus needs to adjust its action to compensate for the reduced aerodynamic force and to balance the asymmetries in area and shape of the damaged wings. While several studies have shown that damaged wings change their flapping kinematics in response to partial loss of wing area, it is unclear how, in insects with four separate wings, the remaining three wings compensate for the loss of a fourth wing. We used high-speed video of flying blue-tailed damselflies (Ischnura elegans) to identify the wingbeat kinematics of the two wing pairs and compared it to the flapping kinematics after one of the hindwings was artificially removed. The insects remained capable of flying and precise maneuvering using only three wings. To compensate for the reduction in lift, they increased flapping frequency by 18 ± 15.4% on average. To achieve steady straight flight, the remaining intact hindwing reduced its flapping amplitude while the forewings changed their stroke plane angle so that the forewing of the manipulated side flapped at a shallower stroke plane angle. In addition, the angular position of the stroke reversal points became asymmetrical. When the wingbeat amplitude and frequency of the three wings were used as input in a simple aerodynamic model, the estimation of total aerodynamic force was not significantly different (paired t-test, p = 0.73) from the force produced by the four wings during normal flight. Thus, the removal of one wing resulted in adjustments of the motions of the remaining three wings, exemplifying the precision and plasticity of coordination between the operational wings. Such coordination is vital for precise maneuvering during normal flight but it also provides the means to maintain flight when some of the wings are severely damaged.     

Animal flight dynamics II. Longitudinal stability in flapping flight

Stability is essential to flying and is usually assumed to be especially problematic in flapping flight. If so, problems of stability may have presented a particular hurdle to the evolution of flapping flight. In spite of this, the stability of flapping flight has never been properly analysed. Here we use quasi-static and blade element approaches to analyse the stability provided by a flapping wing. By using reduced order approximations to the natural modes of motion, we show that wing beat frequencies are generally high enough compared to the natural frequencies of motion for a quasi-static approach to be valid as a first approximation. Contrary to expectations, we find that there is noting inherently destabilizing about flapping: beating the wings faster simply amplifies any existing stability or instability, and flapping can even enhance stability compared to gliding at the same air speed. This suggests that aerodynamic stability may not have been a particular hurdle in the evolution of flapping flight. Hovering animals, like hovering helicopters, are predicted to possess neutral static stability. Flapping animals, like fixed wing aircraft, are predicted to be stable in forward flight if the mean flight force acts above and/or behind the centre of gravity. In this case, the downstroke will always be stabilizing. The stabilizing contribution may be diminished by an active upstroke with a low advance ratio and more horizontal stroke plane; other forms of the upstroke may make a small positive contribution to stability. An active upstroke could, therefore, be used to lower stability and enhance manoeuvrability. Translatory mechanisms of unsteady lift production are predicted to amplify the stability predicted by a quasi-static analysis. Non-translatory mechanisms will make little or no contribution to stability. This may be one reason why flies, and other animals which rely upon non-translatory aerodynamic mechanisms, often appear inherently unstable.     

Development of flight behaviour in maturing adults of Locusta migratoria: I. Flight performance and wing-stroke parameters

In tethered Locusta migratoria suspended from a flight balance, flight performance, wing-stroke frequency, stroke angle, and stroke plane angle were studied throughout adult life. No correlation between flight performance and age was found in adults older than 2 days. During continuous flight in locusts of all ages the wing-stroke frequency and the wing-stroke angle of both wings decreases, and the wing-stroke plane angle (forewing) increases slightly. Within 2 weeks of adult life the wing-stroke frequency increases by a factor of ca. 2, whereas the wing-stroke angles and the stroke plane angles remain constant.     

A reconsideration of the central pattern generator concept for locust flight

Summary Although it is generally agreed that locusts can generate flight similar rhythmic motor activity in the absence of sensory feedback from the wings, recent studies indicate that functional deafferentation produces significant changes in the flight motor pattern (Hedwig and Pearson 1984). These findings have raised doubts on the adequacy of the central pattern generator concept for the locust flight system (Pearson 1985). In this paper, we re-investigate the effects of deafferentation on the capacity of adult migratory locusts to generate the flight motor pattern. For this purpose, the experimental animals were dissected to various degrees, ranging from head-ventral nerve cord, to isolated pterothoracic nerve cord, and finally single isolated ganglion preparations. Flight motor activity was released by either wind stimulation, the more traditional method, or by applying octopamine (Sombati and Hoyle 1984; Stevenson and Kutsch 1986). In all cases the released motor activity was analysed, giving details of latency, and phase relationships between specific synergistic and antagonistic motor units, and then compared with the flight motor pattern generated by intact tethered locusts.This analysis shows that deafferentation, although reducing the frequency, does not necessarily disrupt the basic flight motor pattern. By using octopamine we could show that even isolated thoracic nerve cord preparations can generate activity, which in all major aspects corresponds to this motor program. This could also be shown for the fully isolated metathoracic ganglion and we provide some evidence that the mesothoracic ganglion may be capable of a similar performance. In addition to releasing flight activity, octopamine was also found to enhance the responsiveness of deafferentated locusts to wind stimulation. This resulted in a considerable elevation of the frequency and prolongation of the flight motor activity to values comparable to the performance of intact tethered locusts.     

Movement learning of free flying honeybees

Summary Free flying honeybees were conditioned to moving black and white stripe patterns. Bees learn rapidly to distinguish the direction of movement in the vertical and horizontal plane.After being trained to a moving pattern bees do not discriminate the moving alternative from a stationary one. There is no significant velocity discrimination for patterns moving in the same direction.For vertical movements there are clear asymmetries in the spontaneous choice preference and in the learning curves for patterns moving upward or downward.After bees are trained to a stationary pattern they can discriminate it from an upward moving alternative. Learning curves involving movement are generally biphasic, suggesting different adaptive systems depending on the number of rewards.The flight pattern of bees which are trained to movement changes during the process of learning. At the beginning of the learning procedure bees reveal an optokinetic response to the moving patterns, this response is strongly reduced after a number of rewards on a moving pattern.     

Adjustment of flight speed of gregarious desert locusts (Orthoptera: Acrididae) flying side by side

In tethered flying locusts, optomotor thrust responses induced by translatory pattern motion within the lateral visual fields were studied under closed-loop conditions. By modulating thrust in a compensatory manner, locusts counteracted a bias motion superposed on the thrust-related motion. This way, pattern speed was kept at 0° s^–1, indicating the set point of the respective optomotor control circuit. Though the quality of bias compensation varied greatly, it was largely independent from pattern characteristics. It might indicate that the gain of behavior not only is controlled by an automatic mechanism but also is affected by spontaneous modulations. Compensation of bias motion was critically dependent on the relation between self- and bias-generated motion: Locusts did not take control over pattern motion if self- and bias-generated motion differed greatly. Instead, locusts adopted a constant, supposingly preferred, thrust value. Therefore, flight speed is assumed to be controlled by two systems: the optomotor and a preferred thrust system. In free flight, an equalization of the flight speed of locusts within a swarm might result from similar behavior. In combination with a presumed coordination of the locusts' course direction, this may explain the continued cohesion of swarms in the field.     

Movements of the hindwings ofLocusta migratoria,measured with miniature coils

Summary Tethered migratory locusts were induced to fly in an airstream for hours at a time, carrying on their extremely delicate hindwings miniature induction coils by which the hindwing movements were recorded in three dimensions.The two coils were mounted at right angles to one another on the central field of the hindwing, which is in close aerodynamic contact with the forewing. Each coil emitted three signals to define the components of a 3-dimensional vector. The movements of the central field can be described completely by the rotations of the two vectors. The main component of the hindwing movement thus becomes accessible to detailed kinematic analysis (Figs. 2, 3).The results obtained with this inductive method are consistent with the few published data based on photogrammetric samples of the movement.The various forms of movement can all be observed during the flight experiment. The movement spectrum is very broad even in an undisturbed flying animal (Figs. 4, 5).Various wingbeat parameters were calculated, including oscillation period, the durations of upstroke and downstroke, and their ratio (Fig. 6).Simultaneous measurement of the movements of the fore- and hindwings has provided the first documentation of the varying interactions of the wings on side of the body during a long flight. Even small changes in the relative positions of the two wings are measurable (Fig. 7).     

Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster.

Flies display a sophisticated suite of aerial behaviours that require rapid sensory-motor processing. Like all insects, flight control in flies is mediated in part by motion-sensitive visual interneurons that project to steering motor circuitry within the thorax. Flies, however, possess a unique flight control equilibrium sense that is encoded by mechanoreceptors at the base of the halteres, small dumb-bell-shaped organs derived through evolutionary transformation of the hind wings. To study the input of the haltere system onto the flight control system, I constructed a mechanically oscillating flight arena consisting of a cylindrical array of light-emitting diodes that generated the moving image of a 30 degrees vertical stripe. The arena provided closed-loop visual feedback to elicit fixation behaviour, an orientation response in which flies maintain the position of the stripe in the front portion of their visual field by actively adjusting their wing kinematics. While flies orientate towards the stripe, the entire arena was swung back and forth while an optoelectronic device recorded the compensatory changes in wing stroke amplitude and frequency. In order to reduce the background changes in stroke kinematics resulting from the animal's closed-loop visual fixation behaviour, the responses to eight identical mechanical rotations were averaged in each trial. The results indicate that flies possess a robust equilibrium reflex in which angular rotations of the body elicit compensatory changes in both the amplitude and stroke frequency of the wings. The results of uni- and bilateral ablation experiments demonstrate that the halteres are required for these stability reflexes. The results also confirm that halteres encode angular velocity of the body by detecting the Coriolis forces that result from the linear motion of the haltere within the rotating frame of reference of the fly's thorax. By rotating the flight arena at different orientations, it was possible to construct a complete directional tuning map of the haltere-mediated reflexes. The directional tuning of the reflex is quite linear such that the kinematic responses vary as simple trigonometric functions of stimulus orientation. The reflexes function primarily to stabilize pitch and yaw within the horizontal plane.     

Height control by free-flying Drosophila

ABSTRACT. In a horizontal wind tunnel, Drosophila flew at almost constant height along tracks up to 2 m long. The flies rose or sank only slowly when it was so dark that they no longer responded to movements of the tunnel floor, suggesting that their height control is mediated, at least partly, by responses to their movement relative to the air. In the light, the flies maintained height better than in the dark and were very responsive to movements around them. They faithfully followed the up and down movements of horizon screens at their sides whether they were flying in still air or against a wind, even in the presence of many other stationary visual cues. The flies did not respond by compensatory height changes to real vertical movements of a patterned horizontal disc beneath them, nor to changes in the size of the floor pattern. They did respond to horizontal acceleration of the floor pattern in the direction opposite to their flight (optically simulating a descent by the fly), by an apparently compensatory increase in height, but they also rose (instead of sinking) in response to floor acceleration in the direction of their flight. When the floor was accelerated in either direction they showed compensatory groundspeed-controlling responses. The increases in height might be alarm responses to sudden movements in the visual field beneath them. Both speed and height changing responses to floor movement were reduced when the number of stationary visual cues was increased. Drosophila thus control their height mainly by responses to the apparent movement of nearby visual cues at round about their own height.