A simple vision-based algorithm for decision making in flying Drosophila

Animals must quickly recognize objects in their environment and act accordingly. Previous studies indicate that looming visual objects trigger avoidance reflexes in many species [1-5]; however, such reflexes operate over a close range and might not detect a threatening stimulus at a safe distance. We analyzed how fruit flies (Drosophila melanogaster) respond to simple visual stimuli both in free flight and in a tethered-flight simulator. Whereas Drosophila, like many other insects, are attracted toward long vertical objects [6-10], we found that smaller visual stimuli elicit not weak attraction but rather strong repulsion. Because aversion to small spots depends on the vertical size of a moving object, and not on looming, it can function at a much greater distance than expansion-dependent reflexes. The opposing responses to long stripes and small spots reflect a simple but effective object classification system. Attraction toward long stripes would lead flies toward vegetative perches or feeding sites, whereas repulsion from small spots would help them avoid aerial predators or collisions with other insects. The motion of flying Drosophila depends on a balance of these two systems, providing a foundation for studying the neural basis of behavioral choice in a genetic model organism.     

A New Chamber for Studying the Behavior of Drosophila

Methods available for quickly and objectively quantifying the behavioral phenotypes of the fruit fly, Drosophila melanogaster, lag behind in sophistication the tools developed for manipulating their genotypes. We have developed a simple, easy-to-replicate, general-purpose experimental chamber for studying the ground-based behaviors of fruit flies. The major innovative feature of our design is that it restricts flies to a shallow volume of space, forcing all behavioral interactions to take place within a monolayer of individuals. The design lessens the frequency that flies occlude or obscure each other, limits the variability in their appearance, and promotes a greater number of flies to move throughout the center of the chamber, thereby increasing the frequency of their interactions. The new chamber design improves the quality of data collected by digital video and was conceived and designed to complement automated machine vision methodologies for studying behavior. Novel and improved methodologies for better quantifying the complex behavioral phenotypes of Drosophila will facilitate studies related to human disease and fundamental questions of behavioral neuroscience.     

Experimental analysis of the pattern of tethered flight in the Queensland fruit fly, Dacus tryoni

ABSTRACT. The tethered flight of the Queensland fruit fly, Dacus tryoni Frogg. (Diptera, Tephritidae), was investigated, and the duration of each flight during a 2-h experimental period was recorded. The pattern of flight was analysed, and related to the age, sex and origin of the specimens, and to the availability of host fruit during the rearing of the adults. The effect of adult crowding on the pattern of flight was also briefly examined. The results indicated that the origin of the flies had little effect on the pattern of flight; male and female flies showed different trends with respect to the proportion of short flights undertaken as the flies matured; and the availability of fruit had a marked effect on the pattern of flight in recently mature flies. These data are discussed with respect to the dispersive/non-dispersive movements of the flies postulated from previously documented field data. It is suggested that there is a characteristic pattern of tethered flight, which can be related to the absence of hosts in the immediate environment, and would be likely to lead to greater dispersal under natural conditions.     

Dynamic properties of large-field and small-field optomotor flight responses in <Emphasis Type="Italic">Drosophila</Emphasis>

Optomotor flight control in houseflies shows bandwidth fractionation such that steering responses to an oscillating large-field rotating panorama peak at low frequency, whereas responses to small-field objects peak at high frequency. In fruit flies, steady-state large-field translation generates steering responses that are three times larger than large-field rotation. Here, we examine the optomotor steering reactions to dynamically oscillating visual stimuli consisting of large-field rotation, large-field expansion, and small-field motion. The results show that, like in larger flies, large-field optomotor steering responses peak at low frequency, whereas small-field responses persist under high frequency conditions. However, in fruit flies large-field expansion elicits higher magnitude and tighter phase-locked optomotor responses than rotation throughout the frequency spectrum, which may suggest a further segregation within the large-field pathway. An analysis of wing beat frequency and amplitude reveals that mechanical power output during flight varies according to the spatial organization and motion dynamics of the visual scene. These results suggest that, like in larger flies, the optomotor control system is organized into parallel large-field and small-field pathways, and extends previous analyses to quantify expansion-sensitivity for steering reflexes and flight power output across the frequency spectrum.     

Virtual-reality techniques resolve the visual cues used by fruit flies to evaluate object distances

Insects can estimate distance or time-to-contact of surrounding objects from locomotion-induced changes in their retinal position and/or size. Freely walking fruit flies (Drosophila melanogaster) use the received mixture of different distance cues to select the nearest objects for subsequent visits. Conventional methods of behavioral analysis fail to elucidate the underlying data extraction. Here we demonstrate first comprehensive solutions of this problem by substituting virtual for real objects; a tracker-controlled 360 degrees panorama converts a fruit fly's changing coordinates into object illusions that require the perception of specific cues to appear at preselected distances up to infinity. An application reveals the following: (1) en-route sampling of retinal-image changes accounts for distance discrimination within a surprising range of at least 8-80 body lengths (20-200 mm). Stereopsis and peering are not involved. (2) Distance from image translation in the expected direction (motion parallax) outweighs distance from image expansion, which accounts for impact-avoiding flight reactions to looming objects. (3) The ability to discriminate distances is robust to artificially delayed updating of image translation. Fruit flies appear to interrelate self-motion and its visual feedback within a surprisingly long time window of about 2 s. The comparative distance inspection practiced in the small fruit fly deserves utilization in self-moving robots.     

Tracking and chasing in houseflies (Musca)

The flight trajectories of free flying female and male houseflies have been analyzed in 3 dimensions. Both female and male flies track other flies. The turning velocity α (around the vertical axis) is linearly dependent upon the horizontal angle ψ_F (that is the angle between the trajectory of the tracking fly and the target) for small values of ψ_F in females and for the whole range of ψ_F in males. The 3-dimensional velocity υ _xyz of the chasing fly is linearly dependent upon the distance between leading and chasing fly in males but not in females. Male chasing thus appears to be more efficient than female tracking. It is shown that earlier assumptions on visual control of flight in female flies derived from experiments on fixed flying flies are justified.     

Search strategies of fruit flies in steady and shifting winds in the absence of food odours

Abstract. Flight behaviour by females of two species of fruit flies, Drosophila funebris and Drosophila immigrans , was videorecorded in a wind tunnel in still air and in wind with a constant or shifting direction. Flies which were deprived of food overnight took flight in the absence of food odours. Both species responded to the presented winds in agreement with two models that predict the shortest distance to an odour plume. According to these models, the shortest distance to an odour plume is travelled when insects fly at right angles to the wind with a steady direction. In winds shifting over more than 60, the shortest distance to an odour plume is achieved when insects fly parallel to the time-averaged wind direction. We propose a behavioural mechanism which accomplishes the observed flight directions taken by the two species of fruit flies in response to the tested wind regimes.     

Object detection in the fly during simulated translatory flight

Translatory movement of an animal in its environment induces optic flow that contains information about the three-dimensional layout of the surroundings: as a rule, images of objects that are closer to the animal move faster across the retina than those of more distant objects. Such relative motion cues are used by flies to detect objects in front of a structured background. We confronted flying flies, tethered to a torque meter, with front-to-back motion of patterns displayed on two CRT screens, thereby simulating translatory motion of the background as experienced by an animal during straight flight. The torque meter measured the instantaneous turning responses of the fly around its vertical body axis. During short time intervals, object motion was superimposed on background pattern motion. The average turning response towards such an object depends on both object and background velocity in a characteristic way: (1) in order to elicit significant responses object motion has to be faster than background motion; (2) background motion within a certain range of velocities improves object detection. These properties can be interpreted as adaptations to situations as they occur in natural free flight. We confirmed that the measured responses were mediated mainly by a control system specialized for the detection of objects rather than by the compensatory optomotor system responsible for course stabilization. Accepted: 20 March 1997     

Crossmodal visual input for odor tracking during fly flight

Flies generate robust and high-performance olfactory and visual behaviors. Adult fruit flies can distinguish small differences in odor concentration across antennae separated by less than 1 mm [1], and a single olfactory sensory neuron is sufficient for near-normal gradient tracking in larvae [2]. During flight a male housefly chasing a female executes a corrective turn within 40 ms after a course deviation by its target [3]. The challenges imposed by flying apparently benefit from the tight integration of unimodal sensory cues. Crossmodal interactions reduce the discrimination threshold for unimodal memory retrieval by enhancing stimulus salience [4], and dynamic crossmodal processing is required for odor search during free flight because animals fail to locate an odor source in the absence of rich visual feedback [5]. The visual requirements for odor localization are unknown. We tethered a hungry fly in a magnetic field, allowing it to yaw freely, presented odor plumes, and examined how visual cues influence odor tracking. We show that flies are unable to use a small-field object or landmark to assist plume tracking, whereas odor activates wide-field optomotor course control to enable accurate orientation toward an attractive food odor.     

Flying bats use serial sampling to locate odour sources

Olfactory tracking generally sacrifices speed for sensitivity, but some fast-moving animals appear surprisingly efficient at foraging by smell. Here, we analysed the olfactory tracking strategies of flying bats foraging for fruit. Fruit- and nectar-feeding bats use odour cues to find food despite the sensory challenges derived from fast flight speeds and echolocation. We trained Jamaican fruit-eating bats (Artibeus jamaicensis) to locate an odour reward and reconstructed their flight paths in three-dimensional space. Results confirmed that bats relied upon olfactory cues to locate a reward. Flight paths revealed a combination of odour- and memory-guided search strategies. During ‘inspection flights’, bats significantly reduced flight speeds and flew within approximately 6 cm of possible targets to evaluate the presence or absence of the odour cue. This behaviour combined with echolocation explains how bats maximize foraging efficiency while compensating for trade-offs associated with olfactory detection and locomotion.     

Sexual dimorphism inAnastrepha suspensa (Loew) and other tephritid fruit flies (Diptera: Tephritidae): Possible roles of developmental rate,fecundity, and dispersal

Larger male Caribbean fruit flies are more likely to be chosen as mates and defeat rivals in territorial contests. Yet males are smaller than females. Adaptive explanations for relatively small male size include (1) acceleration of male development to maximize female encounter rates, (2) selection for greater female size to increase fecundity, and (3) selection for body sizes most suitable for sexually dimorphic degrees of mobility, speed, and distance flight. None of these unambiguously accounts for the degree of sexual dimorphism. Male development is not accelerated relative to that of females. On average, males remain inside fruit longer than females and those males with extended development periods are smaller than more rapidly developing individuals. There is no evidence that female enlargement alone, presumably for greater fecundity, has generated the degree of dimorphism in the Caribbean fruit fly or other fruit flies. The relationship between dimorphism and mean female body size in 27 species of Tephritidae is the opposite of what would be predicted if differences in dimorphism were due to differences in unilateral female enlargement. Larger size in a species or in one sex of a species may be an adaptation for extensive flight. In general, among 32 species of fruit flies, as body size increases, wing shape becomes progressively more suited for distance flight. However, there are important exceptions to this correlation. Both sexual selection and nonadaptive allometries may contribute to the range of dimorphisms within the family.     

Interactions between the Social Digger Wasp, <Emphasis Type="Italic">Cerceris rubida</Emphasis>, and Its Brood Parasitic Flies at a Mediterranean Nest Aggregation

The fitness consequence of many behaviours of the small digger wasp, Cerceris rubida (Hymenoptera: Crabronidae), the only European species of its genus in which females share nests, are still unknown. Here, I present novel data on the nesting patterns and nest parasites of an Italian population of this wasp, with emphasis on which behavioural strategies may have evolved to reduce brood parasitism. Nests were established mainly in horizontal surfaces with scarce vegetation and hard soil, resulting in spatially clumped nests; the extent of nest aggregation increased over a 6-year period. Wasp brood cells are attacked by the miltogrammine fly Pterella grisea (Diptera: Sarcophagidae), which waits for nest-returning wasps on perching sites and then follows them in flight (satellite flight), eventually landing on the nest entrance and larvipositing without entering further in the tunnel. This technique seems to be adaptive for the parasitic flies, which would be rejected from nests by the guarding wasps if attempting to enter. The daily activity of the flies closely matched the host wasp’s provisioning activity, but C. rubida females were able to partially confound the tracking flies by performing evasive manoeuvres while returning to the nest. Patches with higher nest density and nests with more resident females did suffer more fly landings on nest entrances (a prerequisite for larviposition). These trends, however, disappeared on a per nest basis and on a per wasp provisioning flight basis, respectively. Across two years, only 6% of brood cells were parasitized, a picture similar to what observed for miltogrammine flies at nest aggregations of other Cerceris spp., and new data are necessary to test if there is a benefit of either nest density or nest sharing against P. grisea parasitism.     

High-Resolution Video Tracking of Locomotion in Adult Drosophila Melanogaster

Flies provide an important model for studying complex behavior due to the plethora of genetic tools available to researchers in this field. Studying locomotor behavior in Drosophila melanogaster relies on the ability to be able to quantify changes in motion during or in response to a given task. For this reason, a high-resolution video tracking system, such as the one we describe in this paper, is a valuable tool for measuring locomotion in real-time. Our protocol involves the use of an initial air pulse to break the flies momentum, followed by a thirty second filming period in a square chamber. A tracking program is then used to calculate the instantaneous speed of each fly within the chamber in 10 msec increments. Analysis software then compiles this data, and outputs a variety of parameters such as average speed, max speed, time spent in motion, acceleration, etc. This protocol will discuss proper feeding and management of flies for behavioral tasks, handling flies without anesthetization or immobilization, setting up a controlled environment, and running the assay from start to finish.Open in a separate windowClick here to view.^{(55M, flv)}     

Shoals and schools: back to the heuristic definitions and quantitative references

The terms ??shoal??, ??swarm?? and ??school?? are very frequently used in research on collective behaviours in animals. Pitcher??s definitions are accepted as the authority in the field but are based on a conceptual criterion of sociability. Without call into question the basis of these definitions, they do not provide tools to determine these behaviours quantitatively. To compare studies between populations, species, taxa or different experimental treatments, and between different authors, quantitative references are necessary. Quantitative measurements of collective behaviours can also test and validate the predictive capacity of computer models by comparing real data from nature so that different models can be compared. The first part of this paper succinctly reviews the definitions and meanings of these behaviours, with particular attention paid to quantitative aspects. This review underlines a series of conceptual confusions concerning these behavioural terms observed in the scientific literature and oral scientific communications. The second part reviews the quantitative parameters developed by biologists studying collective fish behaviours, mainly fish shoals, and by theoretical biologists and physicists studying computer modelling of collective behaviours. The parameters reviewed herein make no attempt to explain the mechanisms and causes that create a shoal, a swarm or a school, but rather try to describe these collective behaviours, and to connect local and global properties with individual and collective behaviours. Recent development over the last decade in technology, data processing capacity, cameras, and video tracking tools have provided the opportunity to obtain quantitative measures of collective dynamic behaviours in animals both rapidly and precisely.     

An Improved Method for Accurate and Rapid Measurement of Flight Performance in Drosophila

Drosophila has proven to be a useful model system for analysis of behavior, including flight. The initial flight tester involved dropping flies into an oil-coated graduated cylinder; landing height provided a measure of flight performance by assessing how far flies will fall before producing enough thrust to make contact with the wall of the cylinder. Here we describe an updated version of the flight tester with four major improvements. First, we added a "drop tube" to ensure that all flies enter the flight cylinder at a similar velocity between trials, eliminating variability between users. Second, we replaced the oil coating with removable plastic sheets coated in Tangle-Trap, an adhesive designed to capture live insects. Third, we use a longer cylinder to enable more accurate discrimination of flight ability. Fourth we use a digital camera and imaging software to automate the scoring of flight performance. These improvements allow for the rapid, quantitative assessment of flight behavior, useful for large datasets and large-scale genetic screens.     

Effect of sex,age and morphological traits on tethered flight of Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) at different temperatures

The oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), is a pest of fruit and vegetable production that has become established in 42 countries in Africa after its first detection in 2003 in Kenya. It is likely that this rapid expansion is partly due to the reported strong capacity for flight by the pest. This study investigated the tethered flight performance of B. dorsalis over a range of constant temperatures in relation to sex and age. Tethered flight of unmated B. dorsalis aged 3, 10 and 21 days was recorded for 1 h using a computerized flight mill at temperatures of 12, 16, 20, 24, 28, 32 and 36 °C. Variations in fly morphology were observed as they aged. Body mass and wing loading increased with age, whereas wing length and wing area reduced as flies aged. Females had slightly larger wings than males but were not significantly heavier. The longest total distance flown by B. dorsalis in 1 h was 1559.58 m. Frequent short, fast flights were recorded at 12 and 36 °C, but long-distance flight was optimal between 20 and 24 °C. Young flies tended to have shorter flight bouts than older flies, which was associated with them flying shorter distances. Heavier flies with greater wing loading flew further than lighter flies. Flight distances recorded on flight mills approximated those recorded in the field, and tethered flight patterns suggest a need to factor temperature into the interpretation of trap captures.     

The neuro-ecology of resource localization in Drosophila: Behavioral components of perception and search

From the moment an adult fruit fly ecloses, its primary objective in life is to disperse and locate the source of an attractive food odor upon which to feed and reproduce. The evolution of flight has greatly enhanced the success of fruit flies specifically and insects more generally.1 Control of flight by Drosophila melanogaster is unequivocally visual. Strong optomotor reflexes towards translatory and rotational visual flow stabilize forward flight trajectory, altitude, and speed. 2, 3 The steering responses to translatory and rotational flow in particular are mediated by computationally separate neural circuits in the fly’s visual system,4 and gaze-stabilizing body saccades are elicited by threshold integration of expanding visual flow .5 However, visual information is not alone sufficient to enable a fruit fly to recognize and locate an appropriately smelly object due in part to the relatively poor resolution of its compound eyes. Rather, the animal uses an acute sense of smell to actively track odors during flight. Without a finely adapted olfactory system, the fly’s remarkable visual capabilities are for naught. The relative importance of vision is apparent in the cross-modal fusion of the two modalities for stable active odor tracking.6, 7 Olfactory processing in Drosophila is shaped by ecological and functional forces which are inextricably linked. Thus physiologists seeking the functional determinants of olfactory coding as well as ecologists seeking to understand the mechanisms of speciation do well to consider each others’ point of view. Here we synthesize a broad perspective that integrates across ultimate and proximate mechanisms of odor tracking in Drosophila.     

Individual Pause-and-Go Motion Is Instrumental to the Formation and Maintenance of Swarms of Marching Locust Nymphs

The principal interactions leading to the emergence of order in swarms of marching locust nymphs was studied both experimentally, using small groups of marching locusts in the lab, and using computer simulations. We utilized a custom tracking algorithm to reveal fundamental animal-animal interactions leading to collective motion. Uncovering this behavior introduced a new agent-based modeling approach in which pause-and-go motion is pivotal. The behavioral and modeling findings are largely based on motion-related visual sensory inputs obtained by the individual locust. Results suggest a generic principle, in which intermittent animal motion can be considered as a sequence of individual decisions as animals repeatedly reassess their situation and decide whether or not to swarm. This interpretation implies, among other things, some generic characteristics regarding the build-up and emergence of collective order in swarms: in particular, that order and disorder are generic meta-stable states of the system, suggesting that the emergence of order is kinetic and does not necessarily require external environmental changes. This work calls for further experimental as well as theoretical investigation of the neural mechanisms underlying locust coordinative behavior.     

Independently Controlled Wing Stroke Patterns in the Fruit Fly Drosophila melanogaster

Flies achieve supreme flight maneuverability through a small set of miniscule steering muscles attached to the wing base. The fast flight maneuvers arise from precisely timed activation of the steering muscles and the resulting subtle modulation of the wing stroke. In addition, slower modulation of wing kinematics arises from changes in the activity of indirect flight muscles in the thorax. We investigated if these modulations can be described as a superposition of a limited number of elementary deformations of the wing stroke that are under independent physiological control. Using a high-speed computer vision system, we recorded the wing motion of tethered flying fruit flies for up to 12 000 consecutive wing strokes at a sampling rate of 6250 Hz. We then decomposed the joint motion pattern of both wings into components that had the minimal mutual information (a measure of statistical dependence). In 100 flight segments measured from 10 individual flies, we identified 7 distinct types of frequently occurring least-dependent components, each defining a kinematic pattern (a specific deformation of the wing stroke and the sequence of its activation from cycle to cycle). Two of these stroke deformations can be associated with the control of yaw torque and total flight force, respectively. A third deformation involves a change in the downstroke-to-upstroke duration ratio, which is expected to alter the pitch torque. A fourth kinematic pattern consists in the alteration of stroke amplitude with a period of 2 wingbeat cycles, extending for dozens of cycles. Our analysis indicates that these four elementary kinematic patterns can be activated mutually independently, and occur both in isolation and in linear superposition. The results strengthen the available evidence for independent control of yaw torque, pitch torque, and total flight force. Our computational method facilitates systematic identification of novel patterns in large kinematic datasets.     

Sex-specific differences in the chasing behaviour of houseflies (Musca)

Flies were filmed simultaneously from above and from the side. Their flight tracks were analyzed frame by frame. Male and female flies were found to chase other flies. But female chases are brief and poorly controlled as compared to male chases. Female flies use the lower frontal part of their visual field for tracking other flies. Male flies use the upper frontal part of their visual field for that purpose. Male flies are capable of controlling their forward velocity roughly proportional to the distance to their target. Implications for the function of recently found sexdimorph visual interneurones are discussed.