3D reconstruction of bird flight trajectories using a single video camera.

Video cameras are finding increasing use in the study and analysis of bird flight over short ranges. However, reconstruction of flight trajectories in three dimensions typically requires the use of multiple cameras and elaborate calibration procedures. We present an alternative approach that uses a single video camera and a simple calibration procedure for the reconstruction of such trajectories. The technique combines prior knowledge of the wingspan of the bird with a camera calibration procedure that needs to be used only once in the lifetime of the system. The system delivers the exact 3D coordinates of the position of the bird at the time of every full wing extension and uses interpolated height estimates to compute the 3D positions of the bird in the video frames between successive wing extensions. The system is inexpensive, compact and portable, and can be easily deployed in the laboratory as well as the field.

Neural basis of forward flight control and landing in honeybees.

The impressive repertoire of honeybee visually guided behaviors, and their ability to learn has made them an important tool for elucidating the visual basis of behavior. Like other insects, bees perform optomotor course correction to optic flow, a response that is dependent on the spatial structure of the visual environment. However, bees can also distinguish the speed of image motion during forward flight and landing, as well as estimate flight distances (odometry), irrespective of the visual scene. The neural pathways underlying these abilities are unknown. Here we report on a cluster of descending neurons (DNIIIs) that are shown to have the directional tuning properties necessary for detecting image motion during forward flight and landing on vertical surfaces. They have stable firing rates during prolonged periods of stimulation and respond to a wide range of image speeds, making them suitable to detect image flow during flight behaviors. While their responses are not strictly speed tuned, the shape and amplitudes of their speed tuning functions are resistant to large changes in spatial frequency. These cells are prime candidates not only for the control of flight speed and landing, but also the basis of a neural 'front end' of the honeybee's visual odometer.

Honeybee navigation: critically examining the role of the polarization compass.

Although it is widely accepted that honeybees use the polarized-light pattern of the sky as a compass for navigation, there is little direct evidence that this information is actually sensed during flight. Here, we ask whether flying bees can obtain compass cues derived purely from polarized light, and communicate this information to their nest-mates through the 'waggle dance'. Bees, from an observation hive with vertically oriented honeycombs, were trained to fly to a food source at the end of a tunnel, which provided overhead illumination that was polarized either parallel to the axis of the tunnel, or perpendicular to it. When the illumination was transversely polarized, bees danced in a predominantly vertical direction with waggles occurring equally frequently in the upward or the downward direction. They were thus using the polarized-light information to signal the two possible directions in which they could have flown in natural outdoor flight: either directly towards the sun, or directly away from it. When the illumination was axially polarized, the bees danced in a predominantly horizontal direction with waggles directed either to the left or the right, indicating that they could have flown in an azimuthal direction that was 90° to the right or to the left of the sun, respectively. When the first half of the tunnel provided axial illumination and the second half transverse illumination, bees danced along all of the four principal diagonal directions, which represent four equally likely locations of the food source based on the polarized-light information that they had acquired during their journey. We conclude that flying bees are capable of obtaining and signalling compass information that is derived purely from polarized light. Furthermore, they deal with the directional ambiguity that is inherent in polarized light by signalling all of the possible locations of the food source in their dances, thus maximizing the chances of recruitment to it.

Honeybee navigation: following routes using polarized-light cues.

While it is generally accepted that honeybees (Apis mellifera) are capable of using the pattern of polarized light in the sky to navigate to a food source, there is little or no direct behavioural evidence that they actually do so. We have examined whether bees can be trained to find their way through a maze composed of four interconnected tunnels, by using directional information provided by polarized light illumination from the ceilings of the tunnels. The results show that bees can learn this task, thus demonstrating directly, and for the first time, that bees are indeed capable of using the polarized-light information in the sky as a compass to steer their way to a food source.

Enhanced cholinergic transmission promotes recall in honeybees.

The involvement of the cholinergic system in learning and memory in honeybees has been well established using olfactory conditioning. We examined the effect of Methyl Parathion (MeP), an acetylcholinesterase inhibitor of the organo-phosphate family, on the learning and recall of visual and olfactory discrimination tasks in honeybees. One of our expectations was to observe the effects induced by both the nicotinic and muscarinic systems, as the blocking of acetylcholinesterase should induce an increase in the activity of both systems. We were also interested in knowing whether the type of tasks could influence the results. The visual tasks involved learning to discriminate the orientation of gratings in a Y-maze; the olfactory task involved learning to discriminate odours in a proboscis extension reflex (PER) paradigm. The results indicate that MeP treatment enhances recall of learned tasks in the visual and olfactory domains, but it does not affect the acquisition phase in either domain. Surprisingly, MeP treatment led to muscarinic-like effects but failed to mimic the nicotinic-like effects already described in relation to learning phases in honeybees. Implications for the role of cholinergic pathways in learning and memory and the nature of their involvement are discussed, and a hypothesis relating to the organisation of the cholinergic system and the relationship between the nicotinic and muscarinic systems in honeybees is proposed. The results are also discussed in terms of their ecotoxicological consequences.

The moment before touchdown: landing manoeuvres of the honeybee Apis mellifera.

Although landing is a crucial part of insect flight, it has attracted relatively little study. Here, we investigate, for the first time, the final moments of a honeybee's (Apis mellifera) landing manoeuvre. Using high-speed video recordings, we analyse the behaviour of bees as they approach and land on surfaces of various orientations. The bees enter a stable hover phase, immediately prior to touchdown. We have quantified behaviour during this hover phase and examined whether it changes as the tilt of the landing surface is varied from horizontal (floor), through sloped (uphill) and vertical (wall), to inverted (ceiling). The bees hover at a remarkably constant distance from the surface, irrespective of its tilt. Body inclination increases progressively as the tilt of the surface is increased, and is accompanied by an elevation of the antennae. The tight correlation between the tilt of the surface, and the orientation of the body and the antennae, indicates that the bee's visual system is capable of inferring the tilt of the surface, and pointing the antennae toward it. Touchdown is initiated by extending the appendage closest to the surface, namely, the hind legs when landing on horizontal or sloping surfaces, and the front legs or antennae when landing on vertical surfaces. Touchdown on inverted surfaces is most likely triggered by a mechanosensory signal from the antennae. Evidently, bees use a landing strategy that is flexibly tailored to the varying topography of the terrain.

Rugged, obstruction-free, mirror-lens combination for panoramic imaging.

We present a new combination of lenses and reflective surfaces for obstruction-free wide-angle imaging. The panoramic imaging system consists of a reflective surface machined into solid Perspex, which together with an embedded lens, can be attached to a video camera lens. Unlike vision sensors with a single mirror mounted in front of a camera, the view in the forward direction (i.e., the direction of the optical axis) is not obstructed. Light rays contributing to the central region of the image are refracted at a centrally positioned lens and at the Perspex enclosure. For the outer image region, rays are reflected at a mirror surface of constant angular gain machined into the Perspex and coated with silver. The design produces a field of view of approximately 260 degrees with only a small separation of viewpoints. The shape of the enclosing Perspex is specifically designed in order to minimize internal reflections.

Two odometers in honeybees?

Although several studies have examined how honeybees gauge and report the distance and direction of a food source to their nestmates, relatively little is known about how this information is combined to obtain a representation of the position of the food source. In this study we manipulate the amount of celestial compass information available to the bee during flight, and analyse the encoding of spatial information in the waggle dance as well as in the navigation of the foraging bee. We find that the waggle dance encodes information about the total distance flown to the food source, even when celestial compass cues are available only for a part of the journey. This stands in contrast to how a bee gauges distance flown when it navigates back to a food source that it already knows. When bees were trained to find a feeder placed at a fixed distance in a tunnel in which celestial cues were partially occluded and then tested in a tunnel that was fully open to the sky, they searched for the feeder at a distance that corresponds closely to the distance that was flown under the open sky during the training. Thus, when navigating back to a food source, information about distance travelled is disregarded when there is no concurrent input from the celestial compass. We suggest that bees may possess two different odometers - a 'community' odometer that is used to provide information to nestmates via the dance, and a 'personal' odometer that is used by an experienced individual to return to a previously visited source.

Honeybee navigation: distance estimation in the third dimension.

Honeybees determine distance flown by gauging the extent to which the image of the environment moves in the eye as they fly towards their goal. Here we investigate how this visual odometer operates when a bee flies along paths that include a vertical component. By training bees to fly to a feeder along tunnels of various three-dimensional configurations, we find that the odometric signal depends only upon the total distance travelled along the path and is independent of its three-dimensional configuration. Hence, unlike walking desert ants, which measure the distance travelled in the horizontal plane whilst traversing undulating terrain, flying bees simply integrate the image motion that is experienced on the way to the goal, irrespective of the direction in which the image moves across the eyes. These findings raise important questions about how honeybee recruits navigate reliably to find the food sources that are advertised by scouts.

Bioinspired engineering of exploration systems for NASA and DoD.

A new approach called bioinspired engineering of exploration systems (BEES) and its value for solving pressing NASA and DoD needs are described. Insects (for example honeybees and dragonflies) cope remarkably well with their world, despite possessing a brain containing less than 0.01% as many neurons as the human brain. Although most insects have immobile eyes with fixed focus optics and lack stereo vision, they use a number of ingenious, computationally simple strategies for perceiving their world in three dimensions and navigating successfully within it. We are distilling selected insect-inspired strategies to obtain novel solutions for navigation, hazard avoidance, altitude hold, stable flight, terrain following, and gentle deployment of payload. Such functionality provides potential solutions for future autonomous robotic space and planetary explorers. A BEES approach to developing lightweight low-power autonomous flight systems should be useful for flight control of such biomorphic flyers for both NASA and DoD needs. Recent biological studies of mammalian retinas confirm that representations of multiple features of the visual world are systematically parsed and processed in parallel. Features are mapped to a stack of cellular strata within the retina. Each of these representations can be efficiently modeled in semiconductor cellular nonlinear network (CNN) chips. We describe recent breakthroughs in exploring the feasibility of the unique blending of insect strategies of navigation with mammalian visual search, pattern recognition, and image understanding into hybrid biomorphic flyers for future planetary and terrestrial applications. We describe a few future mission scenarios for Mars exploration, uniquely enabled by these newly developed biomorphic flyers.

Honeybee dances communicate distances measured by optic flow.

In honeybees, employed foragers recruit unemployed hive mates to food sources by dances from which a human observer can read the distance and direction of the food source. When foragers collect food in a short, narrow tunnel, they dance as if the food source were much farther away. Dancers gauge distance by retinal image flow on the way to their destination. Their visually driven odometer misreads distance because the close tunnel walls increase optic flow. We examined how hive mates interpret these dances. Here we show that recruited bees search outside in the direction of the tunnel at exaggerated distances and not inside the tunnel where the foragers come from. Thus, dances must convey information about the direction of the food source and the total amount of image motion en route to the food source, but they do not convey information about absolute distances. We also found that perceived distances on various outdoor routes from the same hive could be considerably different. Navigational errors are avoided as recruits and dancers tend to fly in the same direction. Reported racial differences in honeybee dances could have arisen merely from differences in the environments in which these bees flew.

Landing strategies in honeybees, and possible applications to autonomous airborne vehicles.

Insects, being perhaps more reliant on image motion cues than mammals or higher vertebrates, are proving to be an excellent organism in which to investigate how information on optic flow is exploited to guide locomotion and navigation. This paper describes one example, illustrating how bees perform grazing landings on a flat surface. A smooth landing is achieved by a surprisingly simple and elegant strategy: image velocity is held constant as the surface is approached, thus automatically ensuring that flight speed is close to zero at touchdown. No explicit knowledge of flight speed or height above the ground is necessary. The feasibility of this landing strategy is tested by implementation in a robotic gantry, and its applicability to autonomous airborne vehicles is discussed.

The concepts of 'sameness' and 'difference' in an insect.

Insects process and learn information flexibly to adapt to their environment. The honeybee Apis mellifera constitutes a traditional model for studying learning and memory at behavioural, cellular and molecular levels. Earlier studies focused on elementary associative and non-associative forms of learning determined by either olfactory conditioning of the proboscis extension reflex or the learning of visual stimuli in an operant context. However, research has indicated that bees are capable of cognitive performances that were thought to occur only in some vertebrate species. For example, honeybees can interpolate visual information, exhibit associative recall, categorize visual information and learn contextual information. Here we show that honeybees can form 'sameness' and 'difference' concepts. They learn to solve 'delayed matching-to-sample' tasks, in which they are required to respond to a matching stimulus, and 'delayed non-matching-to-sample' tasks, in which they are required to respond to a different stimulus; they can also transfer the learned rules to new stimuli of the same or a different sensory modality. Thus, not only can bees learn specific objects and their physical parameters, but they can also master abstract inter-relationships, such as sameness and difference.

Maze navigation by honeybees: learning path regularity.

We investigated the ability of honeybees to learn mazes of four types: constant-turn mazes, in which the appropriate turn is always in the same direction in each decision chamber; zig-zag mazes, in which the appropriate turn is alternately left and right in successive decision chambers; irregular mazes, in which there is no readily apparent pattern to the turns; and variable irregular mazes, in which the bees were trained to learn several irregular mazes simultaneously. The bees were able to learn to navigate all four types of maze. Performance was best in the constant-turn mazes, somewhat poorer in the zig-zag mazes, poorer still in the irregular mazes, and poorest in the variable irregular mazes. These results demonstrate that bees do not navigate such mazes simply by memorizing the entire sequence of appropriate turns. Rather, performance in the various configurations depends on the existence of regularity in the structure of the maze and on the ease with which this regularity is recognized and learned.

How honeybees make grazing landings on flat surfaces.

Freely flying bees were filmed as they landed on a flat, horizontal surface, to investigate the underlying visuomotor control strategies. The results reveal that (1) landing bees approach the surface at a relatively shallow descent angle; (2) they tend to hold the angular velocity of the image of the surface constant as they approach it; and (3) the instantaneous speed of descent is proportional to the instantaneous forward speed. These characteristics reflect a surprisingly simple and effective strategy for achieving a smooth landing, by which the forward and descent speeds are automatically reduced as the surface is approached and are both close to zero at touchdown. No explicit knowledge of flight speed or height above the ground is necessary. A model of the control scheme is developed and its predictions are verified. It is also shown that, during landing, the bee decelerates continuously and in such a way as to keep the projected time to touchdown constant as the surface is approached. The feasibility of this landing strategy is demonstrated by implementation in a robotic gantry equipped with vision.

Honeybee navigation: nature and calibration of the "odometer".

There are two theories about how honeybees estimate the distance to food sources. One theory proposes that distance flown is estimated in terms of energy consumption. The other suggests that the cue is visual, and is derived from the extent to which the image of the world has moved on the eye during the trip. Here the two theories are tested by observing dances of bees that have flown through a short, narrow tunnel to collect a food reward. The results show that the honeybee's "odometer" is visually driven. They also provide a calibration of the dance and the odometer in visual terms.