Visual guidance of honeybees approaching a vertical landing surface.

Landing is a critical phase for flying animals, whereby many rely on visual cues to perform controlled touchdown. Foraging honeybees rely on regular landings on flowers to collect food crucial for colony survival and reproduction. Here, we explored how honeybees utilize optical expansion cues to regulate approach flight speed when landing on vertical surfaces. Three sensory-motor control models have been proposed for landings of natural flyers. Landing honeybees maintain a constant optical expansion rate set-point, resulting in a gradual decrease in approach velocity and gentile touchdown. Bumblebees exhibit a similar strategy, but they regularly switch to a new constant optical expansion rate set-point. In contrast, landing birds fly at a constant time to contact to achieve faster landings. Here, we re-examined the landing strategy of honeybees by fitting the three models to individual approach flights of honeybees landing on platforms with varying optical expansion cues. Surprisingly, the landing model identified in bumblebees proved to be the most suitable for these honeybees. This reveals that honeybees adjust their optical expansion rate in a stepwise manner. Bees flying at low optical expansion rates tend to increase their set-point stepwise, while those flying at high optical expansion rates tend to decrease it stepwise. This modular landing control system enables honeybees to land rapidly and reliably under a wide range of initial flight conditions and visual landing platform patterns. The remarkable similarity between the landing strategies of honeybees and bumblebees suggests that this may also be prevalent among other flying insects. Furthermore, these findings hold promising potential for bioinspired guidance systems in flying robots.

The effect of optic flow cues on honeybee flight control in wind.

To minimize the risk of colliding with the ground or other obstacles, flying animals need to control both their ground speed and ground height. This task is particularly challenging in wind, where head winds require an animal to increase its airspeed to maintain a constant ground speed and tail winds may generate negative airspeeds, rendering flight more difficult to control. In this study, we investigate how head and tail winds affect flight control in the honeybee Apis mellifera, which is known to rely on the pattern of visual motion generated across the eye-known as optic flow-to maintain constant ground speeds and heights. We find that, when provided with both longitudinal and transverse optic flow cues (in or perpendicular to the direction of flight, respectively), honeybees maintain a constant ground speed but fly lower in head winds and higher in tail winds, a response that is also observed when longitudinal optic flow cues are minimized. When the transverse component of optic flow is minimized, or when all optic flow cues are minimized, the effect of wind on ground height is abolished. We propose that the regular sidewards oscillations that the bees make as they fly may be used to extract information about the distance to the ground, independently of the longitudinal optic flow that they use for ground speed control. This computationally simple strategy could have potential uses in the development of lightweight and robust systems for guiding autonomous flying vehicles in natural environments.

Vision, perception, navigation and 'cognition' in honeybees and applications to aerial robotics.

This review summarizes research carried out in the author's laboratory investigating the ways in which honeybees use vision to guide their flight and navigate in their environment, and describes how these principles have been used to design, build and test biologically-inspired systems for the guidance and navigation of unmanned aerial vehicles. It also outlines studies investigating the capacities of honeybees in the areas of visual perception, pattern recognition, and 'cognition'.

Budgerigars adopt robust, but idiosyncratic flight paths.

We have investigated the paths taken by Budgerigars while flying in a tunnel. The flight trajectories of nine Budgerigars (Melopsittacus undulatus) were reconstructed in 3D from high speed stereo videography of their flights in an obstacle-free tunnel. Individual birds displayed highly idiosyncratic flight trajectories that were consistent from flight to flight over the course of several months. We then investigated the robustness of each bird's trajectory by interposing a disk-shaped obstacle in its preferred flight path. We found that each bird continued to fly along its preferred trajectory up to a point very close to the obstacle before veering over the obstacle rapidly, making a minimal deviation to avoid a collision, and subsequently returning to its original path. Thus, Budgerigars show a high propensity to stick to their individual, preferred flight paths even when confronted with a clearly visible obstacle, and do not adopt a substantially different, unobstructed route. The robust preference for idiosyncratic flight paths, and the tendency to pass obstacles by flying above them, provide new insights into the strategies that underpin obstacle avoidance in birds. We believe that this is the first carefully controlled study of the behaviour of birds in response to a newly introduced obstacle in their flight path. The insights from the study could also have implications for conservation efforts to mitigate collisions of birds with man-made obstacles.

Contrast sensitivity and visual acuity of Queensland fruit flies (Bactrocera tryoni).

This study examines the visual acuity of Queensland fruit flies (Bactrocera tryoni) by analysing their turning responses to an immersive visual stimulus consisting of a pattern of vertical stripes presented at various angular periods and rotational rates. The results infer that these flies possess an interommatidial angle of approximately [Formula: see text], and an ommatidial acceptance angle of approximately [Formula: see text]. This suggests that the visual acuity of Queensland fruit flies is substantially better than that of the classical vinegar fly (Drosophila melanogaster), and is comparable to those of the housefly (Musca domestica) and the honeybee (Apis mellifera). The contrast sensitivity of Queensland fruit flies is comparable to that of the housefly.

Author Correction: Coordinated Turning Behaviour of Loitering Honeybees.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has not been fixed in the paper.

Coordinated Turning Behaviour of Loitering Honeybees.

Turning during flight is a complex behaviour that requires coordination to ensure that the resulting centrifugal force is never large enough to disrupt the intended turning trajectory. The centrifugal force during a turn increases with the curvature (sharpness) of the turn, as well as the speed of flight. Consequently, sharp turns would require lower flight speeds, in order to limit the centrifugal force to a manageable level and prevent unwanted sideslips. We have video-filmed honeybees flying near a hive entrance when the entrance is temporarily blocked. A 3D reconstruction and analysis of the flight trajectories executed during this loitering behaviour reveals that sharper turns are indeed executed at lower speeds. During a turn, the flight speed is matched to the curvature, moment to moment, in such a way as to maintain the centrifugal force at an approximately constant, low level of about 30% of the body weight, irrespective of the instantaneous speed or curvature of the turn. This ensures that turns are well coordinated, with few or no sideslips - as it is evident from analysis of other properties of the flight trajectories.

Comparison of Visually Guided Flight in Insects and Birds.

Over the last half century, work with flies, bees, and moths have revealed a number of visual guidance strategies for controlling different aspects of flight. Some algorithms, such as the use of pattern velocity in forward flight, are employed by all insects studied so far, and are used to control multiple flight tasks such as regulation of speed, measurement of distance, and positioning through narrow passages. Although much attention has been devoted to long-range navigation and homing in birds, until recently, very little was known about how birds control flight in a moment-to-moment fashion. A bird that flies rapidly through dense foliage to land on a branch-as birds often do-engages in a veritable three-dimensional slalom, in which it has to continually dodge branches and leaves, and find, and possibly even plan a collision-free path to the goal in real time. Each mode of flight from take-off to goal could potentially involve a different visual guidance algorithm. Here, we briefly review strategies for visual guidance of flight in insects, synthesize recent work from short-range visual guidance in birds, and offer a general comparison between the two groups of organisms.

How lost "passenger" ants find their way home.

Animal navigation has fascinated biologists and engineers for centuries, and some of the most illuminating discoveries have come from the study of creatures with a brain no larger than a sesame seed. In an elegant recent study, Pfeiffer and Wittlinger (Science, 353, 1155-1157, 2016) have shown the means by which desert ants, carried from one nest to another by a relative, find their own way back home if they are accidentally dropped en route.

Obstacle traversal and route choice in flying honeybees: Evidence for individual handedness.

Flying insects constantly face the challenge of choosing efficient, safe and collision-free routes while navigating through dense foliage. We examined the route-choice behavior of foraging honeybees when they encountered a barrier which could be traversed by flying through one of two apertures, positioned side by side. When the bees' choice behavior was averaged over the entire tested population, the two apertures were chosen with equal frequency when they were equally wide. When the apertures were of different width, the bees, on average, showed a preference for the wider aperture, which increased sharply with the difference between the aperture widths. Thus, bees are able to discriminate the widths of oncoming gaps and choose the passage which is presumably safer and quicker to transit. Examination of the behavior of individual bees revealed that, when the two apertures were equally wide, ca. 55% of the bees displayed no side bias in their choices. However, the remaining 45% showed varying degrees of bias, with one half of them preferring the left-hand aperture, and the other half the right-hand aperture. The existence of distinct individual biases was confirmed by measuring the times required by biased bees to transit various aperture configurations: The transit time was longer if a bee's intrinsic bias forced it to engage with the narrower aperture. Our results show that, at the population level, bees do not exhibit 'handedness' in choosing routes; however, individual bees display an idiosyncratic bias that can range from a strong left bias, through zero bias, to a strong right bias. In honeybees, previous studies of olfactory and visual learning have demonstrated clear biases at the population level. To our knowledge, our study is the first to uncover the existence of individually distinct biases in honeybees. We also show how a distribution of biases among individual honeybees can be advantageous in facilitating rapid transit of a group of bees through a cluttered environment, without any centralized decision-making or control.

UAS stealth: target pursuit at constant distance using a bio-inspired motion camouflage guidance law.

The aim of this study is to derive a guidance law by which an unmanned aerial system(s) (UAS) can pursue a moving target at a constant distance, while concealing its own motion. We derive a closed-form solution for the trajectory of the UAS by imposing two key constraints: (1) the shadower moves in such a way as to be perceived as a stationary object by the shadowee, and (2) the distance between the shadower and shadowee is kept constant. Additionally, the theory presented in this paper considers constraints on the maximum achievable speed and acceleration of the shadower. Our theory is tested through Matlab simulations, which validate the camouflage strategy for both 2D and 3D conditions. Furthermore, experiments using a realistic vision-based implementation are conducted in a virtual environment, where the results demonstrate that even with noisy state information it is possible to remain well camouflaged using the constant distance motion camouflage technique.

In search of evidence for the experience of pain in honeybees: A self-administration study.

Despite their common use as model organisms in scientific experiments, pain and suffering in insects remains controversial and poorly understood. Here we explore potential pain experience in honeybees (Apis mellifera) by testing the self-administration of an analgesic drug. Foragers were subjected to two different types of injuries: (i) a clip that applied continuous pressure to one leg and (ii) amputation of one tarsus. The bees were given a choice between two feeders, one offering pure sucrose solution, the other sucrose solution plus morphine. We found that sustained pinching had no effect on the amount of morphine consumed, and hence is unlikely to be experienced as painful. The amputated bees did not shift their relative preference towards the analgesic either, but consumed more morphine and more solution in total compared to intact controls. While our data do not provide evidence for the self-administration of morphine in response to pain, they suggest that injured bees increase their overall food intake, presumably to meet the increased energy requirements for an immune response caused by wounding. We conclude that further experiments are required to gain insights into potential pain-like states in honeybees and other insects.

Flight control of fruit flies: dynamic response to optic flow and headwind.

Insects are magnificent fliers that are capable of performing many complex tasks such as speed regulation, smooth landings and collision avoidance, even though their computational abilities are limited by their small brain. To investigate how flying insects respond to changes in wind speed and surrounding optic flow, the open-loop sensorimotor response of female Queensland fruit flies (Bactrocera tryoni) was examined. A total of 136 flies were exposed to stimuli comprising sinusoidally varying optic flow and air flow (simulating forward movement) under tethered conditions in a virtual reality arena. Two responses were measured: the thrust and the abdomen pitch. The dynamics of the responses to optic flow and air flow were measured at various frequencies, and modelled as a multicompartment linear system, which accurately captured the behavioural responses of the fruit flies. The results indicate that these two behavioural responses are concurrently sensitive to changes of optic flow as well as wind. The abdomen pitch showed a streamlining response, where the abdomen was raised higher as the magnitude of either stimulus was increased. The thrust, in contrast, exhibited a counter-phase response where maximum thrust occurred when the optic flow or wind flow was at a minimum, indicating that the flies were attempting to maintain an ideal flight speed. When the changes in the wind and optic flow were in phase (i.e. did not contradict each other), the net responses (thrust and abdomen pitch) were well approximated by an equally weighted sum of the responses to the individual stimuli. However, when the optic flow and wind stimuli were presented in counterphase, the flies seemed to respond to only one stimulus or the other, demonstrating a form of 'selective attention'.

Strategies for Pre-Emptive Mid-Air Collision Avoidance in Budgerigars.

We have investigated how birds avoid mid-air collisions during head-on encounters. Trajectories of birds flying towards each other in a tunnel were recorded using high speed video cameras. Analysis and modelling of the data suggest two simple strategies for collision avoidance: (a) each bird veers to its right and (b) each bird changes its altitude relative to the other bird according to a preset preference. Both strategies suggest simple rules by which collisions can be avoided in head-on encounters by two agents, be they animals or machines. The findings are potentially applicable to the design of guidance algorithms for automated collision avoidance on aircraft.

Anticipatory Manoeuvres in Bird Flight.

It is essential for birds to be agile and aware of their immediate environment, especially when flying through dense foliage. To investigate the type of visual signals and strategies used by birds while negotiating cluttered environments, we presented budgerigars with vertically oriented apertures of different widths. We find that, when flying through narrow apertures, birds execute their maneuvers in an anticipatory fashion, with wing closures, if necessary, occurring well in advance of the aperture. When passing through an aperture that is narrower than the wingspan, the birds close their wings at a specific, constant distance before the aperture, which is independent of aperture width. In these cases, the birds also fly significantly higher, possibly pre-compensating for the drop in altitude. The speed of approach is largely constant, and independent of the width of the aperture. The constancy of the approach speed suggests a simple means by which optic flow can be used to gauge the distance and width of the aperture, and guide wing closure.

Budgerigar flight in a varying environment: flight at distinct speeds?

How do flying birds respond to changing environments? The behaviour of budgerigars, Melopsittacus undulatus, was filmed as they flew through a tapered tunnel. Unlike flying insects-which vary their speed progressively and continuously by holding constant the optic flow induced by the walls-the birds showed a tendency to fly at only two distinct, fixed speeds. They switched between a high speed in the wider section of the tunnel, and a low speed in the narrower section. The transition between the two speeds was abrupt, and anticipatory. The high speed was close to the energy-efficient, outdoor cruising speed for these birds, while the low speed was approximately half this value. This is the first observation of the existence of two distinct, preferred flight speeds in birds. A dual-speed flight strategy may be beneficial for birds that fly in varying environments, with the high speed set at an energy-efficient value for flight through open spaces, and the low speed suited to safe manoeuvring in a cluttered environment. The constancy of flight speed within each regime enables the distances of obstacles and landmarks to be directly calibrated in terms of optic flow, thus facilitating simple and efficient guidance of flight through changing environments.

Using an abstract geometry in virtual reality to explore choice behaviour: visual flicker preferences in honeybees.

Closed-loop paradigms provide an effective approach for studying visual choice behaviour and attention in small animals. Different flying and walking paradigms have been developed to investigate behavioural and neuronal responses to competing stimuli in insects such as bees and flies. However, the variety of stimulus choices that can be presented over one experiment is often limited. Current choice paradigms are mostly constrained as single binary choice scenarios that are influenced by the linear structure of classical conditioning paradigms. Here, we present a novel behavioural choice paradigm that allows animals to explore a closed geometry of interconnected binary choices by repeatedly selecting among competing objects, thereby revealing stimulus preferences in an historical context. We used our novel paradigm to investigate visual flicker preferences in honeybees (Apis mellifera) and found significant preferences for 20-25 Hz flicker and avoidance of higher (50-100 Hz) and lower (2-4 Hz) flicker frequencies. Similar results were found when bees were presented with three simultaneous choices instead of two, and when they were given the chance to select previously rejected choices. Our results show that honeybees can discriminate among different flicker frequencies and that their visual preferences are persistent even under different experimental conditions. Interestingly, avoided stimuli were more attractive if they were novel, suggesting that novelty salience can override innate preferences. Our recursive virtual reality environment provides a new approach to studying visual discrimination and choice behaviour in animals.

Insects modify their behaviour depending on the feedback sensor used when walking on a trackball in virtual reality.

When using virtual-reality paradigms to study animal behaviour, careful attention must be paid to how the animal's actions are detected. This is particularly relevant in closed-loop experiments where the animal interacts with a stimulus. Many different sensor types have been used to measure aspects of behaviour, and although some sensors may be more accurate than others, few studies have examined whether, and how, such differences affect an animal's behaviour in a closed-loop experiment. To investigate this issue, we conducted experiments with tethered honeybees walking on an air-supported trackball and fixating a visual object in closed-loop. Bees walked faster and along straighter paths when the motion of the trackball was measured in the classical fashion - using optical motion sensors repurposed from computer mice - than when measured more accurately using a computer vision algorithm called 'FicTrac'. When computer mouse sensors were used to measure bees' behaviour, the bees modified their behaviour and achieved improved control of the stimulus. This behavioural change appears to be a response to a systematic error in the computer mouse sensor that reduces the sensitivity of this sensor system under certain conditions. Although the large perceived inertia and mass of the trackball relative to the honeybee is a limitation of tethered walking paradigms, observing differences depending on the sensor system used to measure bee behaviour was not expected. This study suggests that bees are capable of fine-tuning their motor control to improve the outcome of the task they are performing. Further, our findings show that caution is required when designing virtual-reality experiments, as animals can potentially respond to the artificial scenario in unexpected and unintended ways.

Direct Evidence for Vision-based Control of Flight Speed in Budgerigars.

We have investigated whether, and, if so, how birds use vision to regulate the speed of their flight. Budgerigars, Melopsittacus undulatus, were filmed in 3-D using high-speed video cameras as they flew along a 25 m tunnel in which stationary or moving vertically oriented black and white stripes were projected on the side walls. We found that the birds increased their flight speed when the stripes were moved in the birds' flight direction, but decreased it only marginally when the stripes were moved in the opposite direction. The results provide the first direct evidence that Budgerigars use cues based on optic flow, to regulate their flight speed. However, unlike the situation in flying insects, it appears that the control of flight speed in Budgerigars is direction-specific. It does not rely solely on cues derived from optic flow, but may also be determined by energy constraints.