Flight of the dragonflies and damselflies

This work is a synthesis of our current understanding of the mechanics, aerodynamics and visually mediated control of dragonfly and damselfly flight, with the addition of new experimental and computational data in several key areas. These are: the diversity of dragonfly wing morphologies, the aerodynamics of gliding flight, force generation in flapping flight, aerodynamic efficiency, comparative flight performance and pursuit strategies during predatory and territorial flights. New data are set in context by brief reviews covering anatomy at several scales, insect aerodynamics, neuromechanics and behaviour. We achieve a new perspective by means of a diverse range of techniques, including laser-line mapping of wing topographies, computational fluid dynamics simulations of finely detailed wing geometries, quantitative imaging using particle image velocimetry of on-wing and wake flow patterns, classical aerodynamic theory, photography in the field, infrared motion capture and multi-camera optical tracking of free flight trajectories in laboratory environments. Our comprehensive approach enables a novel synthesis of datasets and subfields that integrates many aspects of flight from the neurobiology of the compound eye, through the aeromechanical interface with the surrounding fluid, to flight performance under cruising and higher-energy behavioural modes.This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’.     

Spatial facilitation by a high-performance dragonfly target-detecting neuron

Many animals visualize and track small moving targets at long distances-be they prey, approaching predators or conspecifics. Insects are an excellent model system for investigating the neural mechanisms that have evolved for this challenging task. Specialized small target motion detector (STMD) neurons in the optic lobes of the insect brain respond strongly even when the target size is below the resolution limit of the eye. Many STMDs also respond robustly to small targets against complex stationary or moving backgrounds. We hypothesized that this requires a complex mechanism to avoid breakthrough responses by background features, and yet to adequately amplify the weak signal of tiny targets. We compared responses of dragonfly STMD neurons to small targets that begin moving within the receptive field with responses to targets that approach the same location along longer trajectories. We find that responses along longer trajectories are strongly facilitated by a mechanism that builds up slowly over several hundred milliseconds. This allows the neurons to give sustained responses to continuous target motion, thus providing a possible explanation for their extraordinary sensitivity.     

The Role of Soft Vein Joints in Dragonfly Flight

Dragonflies are excellent flyers among insects and their flight ability is closely related to the architecture and material properties of their wings.The veins are main structure components of a dragonfly wing,which are found to be connected by resilin with high elasticity at some joints.A three-dimensional (3D) finite element model of dragonfly wing considering the soft vein joints is developed,with some simplifications.Passive deformation under aerodynamic loads and active flapping motion of the wing are both studied.The functions of soft vein joints in dragonfly flight are concluded.In passive deformation,the chordwise flexibility is improved by soft vein joints and the wing is cambered under loads,increasing the action area with air.In active flapping,the wing rigidity in spanwise direction is maintained to achieve the required amplitude.As a result,both the passive deformation and the active control of flapping work well in dragonfly flight.The present study may also inspire the design of biomimetic Flapping Micro Air Vehicles (FMAVs).     

Mass reproductive wanderings of dragonflies of the genus Sympetrum (Odonata,Libellulidae)

The results of observing mass flights of some dragonflies of the genus Sympetrum forming tandems are presented. These tandems always fly against the wind, some of them landing for oviposition and then joining the flight again. This variant of migration behavior has been unexplained until now. A hypothesis is proposed according to which synchronous mass flights of dragonfly tandems facilitate the most uniform oviposition in all the suitable biotopes. The general direction of the flight depends on the wind. As the wind direction changes, the flight course of the tandems changes accordingly, so that the dragonflies cross the same territory several times, which leads to a denser and more uniform distribution of eggs. It is proposed to refer to this variant of flight as reproductive wanderings. Such a dispersal strategy can maintain the most uniform population density and a more stable abundance of some dragonfly species in the territories with unstable humidity.     

Echolocating bats use a nearly time-optimal strategy to intercept prey

Acquisition of food in many animal species depends on the pursuit and capture of moving prey. Among modern humans, the pursuit and interception of moving targets plays a central role in a variety of sports, such as tennis, football, Frisbee, and baseball. Studies of target pursuit in animals, ranging from dragonflies to fish and dogs to humans, have suggested that they all use a constant bearing (CB) strategy to pursue prey or other moving targets. CB is best known as the interception strategy employed by baseball outfielders to catch ballistic fly balls. CB is a time-optimal solution to catch targets moving along a straight line, or in a predictable fashion--such as a ballistic baseball, or a piece of food sinking in water. Many animals, however, have to capture prey that may make evasive and unpredictable maneuvers. Is CB an optimum solution to pursuing erratically moving targets? Do animals faced with such erratic prey also use CB? In this paper, we address these questions by studying prey capture in an insectivorous echolocating bat. Echolocating bats rely on sonar to pursue and capture flying insects. The bat's prey may emerge from foliage for a brief time, fly in erratic three-dimensional paths before returning to cover. Bats typically take less than one second to detect, localize and capture such insects. We used high speed stereo infra-red videography to study the three dimensional flight paths of the big brown bat, Eptesicus fuscus, as it chased erratically moving insects in a dark laboratory flight room. We quantified the bat's complex pursuit trajectories using a simple delay differential equation. Our analysis of the pursuit trajectories suggests that bats use a constant absolute target direction strategy during pursuit. We show mathematically that, unlike CB, this approach minimizes the time it takes for a pursuer to intercept an unpredictably moving target. Interestingly, the bat's behavior is similar to the interception strategy implemented in some guided missiles. We suggest that the time-optimal strategy adopted by the bat is in response to the evolutionary pressures of having to capture erratic and fast moving insects.     

Eye movements and target fixation during dragonfly prey-interception flights

The capture of flying insects by foraging dragonflies is a highly accurate, visually guided behavior. Rather than simply aiming at the prey’s position, the dragonfly aims at a point in front of the prey, so that the prey is intercepted with a relatively straight flight trajectory. To better understand the neural mechanisms underlying this behavior, we used high-speed video to quantify the head and body orientation of dragonflies (female Erythemis simplicicollis flying in an outdoor flight cage) relative to an artificial prey object before and during pursuit. The results of our frame-by-frame analysis showed that during prey pursuit, the dragonfly adjusts its head orientation to maintain the image of the prey centered on the “crosshairs” formed by the visual midline and the dorsal fovea, a high acuity streak that crosses midline at right angles about 60° above the horizon. The visual response latencies to drifting of the prey image are remarkably short, ca. 25 ms for the head and 30 ms for the wing responses. Our results imply that the control of the prey-interception flight must include a neural pathway that takes head position into account.     

Discontinuity of sarcoplasmic reticulum in the mid-sarcomere region in flight muscle of dragonflies

The sarcoplasmic reticulum organization of dragonfly flight muscles is analyzed, with particular reference to the doubling existing at H-band level. This doubling could be explained as a consequence of a regular discontinuity in the sarcoplasmic reticulum covering myofibrils. In each sarcomere, two sleeves of the sarcoplasmic reticulum seem to overlap forming a telescopic system which can slide outside each other during the lengthening and shortening movements of the fiber.     

Schema generation in recurrent neural nets for intercepting a moving target

The grasping of a moving object requires the development of a motor strategy to anticipate the trajectory of the target and to compute an optimal course of interception. During the performance of perception-action cycles, a preprogrammed prototypical movement trajectory, a motor schema, may highly reduce the control load. Subjects were asked to hit a target that was moving along a circular path by means of a cursor. Randomized initial target positions and velocities were detected in the periphery of the eyes, resulting in a saccade toward the target. Even when the target disappeared, the eyes followed the target’s anticipated course. The Gestalt of the trajectories was dependent on target velocity. The prediction capability of the motor schema was investigated by varying the visibility range of cursor and target. Motor schemata were determined to be of limited precision, and therefore visual feedback was continuously required to intercept the moving target. To intercept a target, the motor schema caused the hand to aim ahead and to adapt to the target trajectory. The control of cursor velocity determined the point of interception. From a modeling point of view, a neural network was developed that allowed the implementation of a motor schema interacting with feedback control in an iterative manner. The neural net of the Wilson type consists of an excitation-diffusion layer allowing the generation of a moving bubble. This activation bubble runs down an eye-centered motor schema and causes a planar arm model to move toward the target. A bubble provides local integration and straightening of the trajectory during repetitive moves. The schema adapts to task demands by learning and serves as forward controller. On the basis of these model considerations the principal problem of embedding motor schemata in generalized control strategies is discussed.     

Visual receptive field properties of feature detecting neurons in the dragonfly

The dragonfly, (Aeshna, Anax) which feeds on small flying insects, requires a visual system capable of signaling the movements of airborne prey. A group of 8 descending feature detectors in the dragonfly are tuned exclusively to moving contrasting objects. These target-selective descending neurons project from the brain to the thoracic ganglia. Their activity drives steering movement of the wings.In this study, we recorded target-selective descending neuron activity intracellularly.To define their receptive fields, we recorded responses to the movement of black square targets projected onto a screen in front of the animal. Each neuron was identified by dye injection.Target-selective descending neurons exhibit several receptive field properties. Our results show that they are strongly directionally selective. Two TSDNs, exclusively tuned to small targets, have receptive fields restricted to visual midline. Others, which are not selective for target size, have asymmetric receptive fields centered laterally.We suggest that the behavioral function of these specialized feature detectors is to steer the dragonfly during prey-tracking so as to fix the position of the prey image on the retina. If the dragonfly maintains a constant visual bearing to its prey over time it will intercept its prey.Abbreviations TSDN target-selective descending neuron - DCMD descending contralateral movement detector - MDT median dorsal tract - DIT dorsal intermediate tract - VNC ventral nerve cord     

On the existence of 'fast' and 'slow' directionally sensitive motion detector neurons in insects.

In a fly, butterfly, locust and dragonfly we examined the responses of a variety of directional motion-sensitive neurons which run from the brain down the ventral cord. The stimulus was a sinusoidally modulated moving pattern of regular stripes presented at a range of velocities in random order for either 0.1 s or 2.0 s. The response was measured as the total number of spikes to each stimulus. The neurons fall into two groups, 'fast' and 'slow'. The responses of the fast type rise progressively to a peak contrast frequency at 15-20 Hz for all four insects, and decline at higher contrast frequencies. The responses of slow neurons rise rapidly to a peak at 1-10 Hz and then decline more slowly across the range where the fast neurons are at their peak. The existence of two groups of neurons with overlapping response ranges to different velocities of the same pattern, presented in exactly the same way, provides the insect with a means of measuring angular velocity irrespective of contrast, spatial frequency or intensity. As an input mechanism it is proposed that there are two types of unit motion detector, fast and slow, the latter being the main input to the optomotor system. It is also argued that even these inputs are not sufficient to provide a mechanism for the whole repertoire of normal insect vision.     

Honeybees change their height to restore their optic flow

To further elucidate the mechanisms underlying insects’ height and speed control, we trained outdoor honeybees to fly along a high-roofed tunnel, part of which was equipped with a moving floor. Honeybees followed the stationary part of the floor at a given height. On encountering the moving part of the floor, which moved in the same direction as their flight, honeybees descended and flew at a lower height, thus gradually restoring their ventral optic flow (OF) to a similar value to that they had percieved when flying over the stationary part of the floor. This was therefore achieved not by increasing their airspeed, but by lowering their height of flight. These results can be accounted for by a control system called an optic flow regulator, as proposed in previous studies. This visuo-motor control scheme explains how honeybees can navigate safely along tunnels on the sole basis of OF measurements, without any need to measure either their speed or the clearance from the surrounding walls.     

The high number of neurons contributes to the robustness of the locust flight-CPG against parameter variation

 Real pattern-generating networks often consist of more neurons than necessary for the production of a certain rhythm. We investigated the question of whether these neurons contribute to the robustness of a pattern-generating system of using the central pattern generator (CPG) for flight of the locust, generating the deafferented activity pattern of wing elevator and wing depressor motoneurons, as an example of a rhythm-generating system. The neuronal network was reconstructed, based on the known connectivity of the interneurons in the flight CPG, using a biologically orientated network simulator (BioSim 3.0). This simulator allows a physiologically realistic simulation of particular neurons as well as the synaptic connections between them. The flight CPG consists of at least five cyclic loops. The simulation shows that each of them is in principle able to produce a rhythm comparable to the rhythm produced by the whole network, i.e. the ‘deafferented’ flight pattern of elevator and depressor motoneurons. Varying the parameter ‘synaptic strength’ in each of these loops and in the complete system shows that this parameter can be changed within certain ranges without loosing the ability to produce oscillations. These ranges are much smaller in each of the subloops than in the whole network. This result demonstrates that the robustness of the system is increased by supranumerary neurons and connections. Changing the active properties of the simulated neurons so that they are able to produce plateau potentials has no effect on the robustness of the simulated network. Received: 13 April 1994/Accepted in revised form: 15 September 1994     

Structural organization of male-specific visual neurons in calliphorid optic lobes

Summary The superiority of male flies over female flies in locating and intercepting small rapidly moving targets has been ascribed to differences in their visual systems. In males, this sexual dimorphism is externally expressed by an area of high visual acuity called the acute zone. Selective cobalt uptake reveals 12 types of male-specific visual interneurons in the male lobula, the axons of which terminate in neuropil supplying premotor descending neurons to neck and flight motor circuits. The dendritic fields of the individual male-specific neurons can be extrapolated out into visual space to demonstrate that each is assigned a discrete area of the visual panorama. The dendritic fields of 10 of the 12 male-specific neurons subtend areas of the retina associated with the male acute zone. The functional significance of male-specific neurons is discussed with respect to their putative receptive field and a model circuit for target location by male flies.     

An image-free opto-mechanical system for creating virtual environments and imaging neuronal activity in freely moving Caenorhabditis elegans

Non-invasive recording in untethered animals is arguably the ultimate step in the analysis of neuronal function, but such recordings remain elusive. To address this problem, we devised a system that tracks neuron-sized fluorescent targets in real time. The system can be used to create virtual environments by optogenetic activation of sensory neurons, or to image activity in identified neurons at high magnification. By recording activity in neurons of freely moving C. elegans, we tested the long-standing hypothesis that forward and reverse locomotion are generated by distinct neuronal circuits. Surprisingly, we found motor neurons that are active during both types of locomotion, suggesting a new model of locomotion control in C. elegans. These results emphasize the importance of recording neuronal activity in freely moving animals and significantly expand the potential of imaging techniques by providing a mean to stabilize fluorescent targets.     

Analysis of Maneuvering Flight of an Insect

Wing motion of a dragonfly in the maneuvering flight, which was measured by Wang et al. was investigated. Equations of motion for a maneuvering flight of an insect were derived. These equations were applied for analyzing the maneuvering flight. Inertial forces and moments acting on a body and wings were estimated by using these equations and the measured motions of the body and the wings. The results indicated the following characteristics of this flight: ( 1 ) The phase difference in flapping motion between the two fore wings and two hind wings, and the phase difference between the flapping motion and the feathering motion of the four wings are equal to those in a steady forward flight with the maximum efficiency. (2)The camber change and the feathering motion were mainly controlled by muscles at the wing bases.     

Topographic anatomy of ascending and descending neurons of the supraesophageal,meso- and metathoracic ganglia in paleo- and neopterous insects

Topographic anatomy of ascending (AN) and descending (DN) neurons of the supraesophageal and thoracic ganglia in the nervous system of winged insects (Pterygota), representatives of the infraclasses Palaeoptera (Odonata, Aeschna grandis, dragonfly) and Neoptera (Blattoptera, Periplaneta americana, cockroach), was studied. These insects differ in ecological niches, lifestyles, sets of behavioral complexes, levels of locomotor system development, evolutionary age and systematic position. Cell bodies and processes of ANs and DNs were stained with nickel chloride (NiCl₂), and their topography was studied on total preparations of the supraesophageal and thoracic ganglia. Unlike cockroaches, the dragonfly protocerebrum was found to contain DNs sending their processes to ocelli. Dragonfly DN processes exhibit a specific branching pattern in thoracic ganglia, with collaterals coming off both ipsi- and contralaterally. In cockroaches, collaterals of DN processes come off ipsilaterally. The AN cell bodies in dragonfly meso- and metathoracic ganglia lie both ipsi- and contralaterally relative to the ascending process, whereas in cockroaches most of the AN cell bodies in the same ganglia are located contralaterally. Substantial differences in the distrubution of DNs and ANs in insects with different manners of locomotion appear to reflect different degrees of control the supraesophageal ganglion exerts over the activity of segmental centers. This does not seem to be related to the evolutionary age of insects or their systematic position. Probably, different degrees of control over locomotion depend on the way of food acquisition: catching prey in the air in “paleopterous” dragonflies versus maneuverable walking or running over a solid substrate in “neopterous” cockroaches.     

Serotonergic neurons of the Drosophila air-puff-stimulated flight circuit

Monoaminergic modulation of insect flight is well documented. Recently, we demonstrated that synaptic activity is required in serotonergic neurons for Drosophila flight. This requirement is during early pupal development, when the flight circuit is formed, as well as in adults. Using a Ca²⁺-activity-based GFP reporter, here we show that serotonergic neurons in both prothoracic and mesothoracic segments are activated upon air-puff-stimulated flight. Moreover ectopic activation of the entire serotonergic system by TrpA1, a heat activated cation channel, induces flight, even in the absence of an air-puff stimulus.     

Specializations in the lumbosacral vertebral canal and spinal cord of birds: evidence of a function as a sense organ which is involved in the control of walking

Birds are bipedal animals with a center of gravity rostral to the insertion of the hindlimbs. This imposes special demands on keeping balance when moving on the ground. Recently, specializations in the lumbosacral region have been suggested to function as a sense organ of equilibrium which is involved in the control of walking. Morphological, electrophysiological, behavioral and embryological evidence for such a function is reviewed. Birds have two nearly independent kinds of locomotion and it is suggested that two different sense organs play an important role in their respective control: the vestibular organ during flight and the lumbosacral system during walking.     

Spatiotemporal analysis of simultaneous single-unit activity in the dragonfly

The present work describes a new technique for the identification of functional connectivity between neural firing patterns. The simultaneous singleunit recordings obtained from over 50 individual cells in the dragonfly mesothoracic ganglion during three consecutive behavioral states: pre-flight, flight and postflight were evaluated. Each individual spike train was converted into a synthesized analog gradient designed to capture crucial physiological characteristics of the cell from which the spike train emanated. Estimates of network functional connectivity were calculated using correlations between analog gradient spike trains for all possible cell pairings. Both functional excitation and inhibition could be detected in the correlations. The detection of functional connectivity was relatively independent of cell firing rate. More detailed analyses indicated the existence of cellular firing histories and connectivity patterns during flight that strongly resembled the characteristics of a bi-stable oscillator. Such an oscillator, hypothetically, could drive the elevator and depressor motor neuron firing paterns that support wing kinematics. There was no evidence for the functional existence of such an oscillator within either preor post-flight spike records. The detected spatiotemporal patterns of neural activity are hypothesized to be consistent with neural command sequences that the dragonfly might use to control flight. The demonstrated capability to define short-time scale functional relationships between spike trains obtained from dragonfly ganglia should have valuable applications to the comparative study of neural information processing strategies in a variety of other neural systems.