On the encoding of movement vectors by honeybees. Are distance and direction represented independently?

Honeybees flying repeatedly over the same trajectory link it to an associated visual stimulus such that on viewing the stimulus they perform a trajectory in the habitual direction. To test if trajectory length can also be linked to a visual stimulus, bees were trained to fly through a multi-comparmented maze. Bees flew through a multi-compartmented maze. In one compartment a short trajectory could be linked to a stripe pattern oriented at 45° to the horizontal. In another compartment a longer trajectory could be linked to 135° stripes. Bees made both associations: their trajectories were short when viewing 45° stripes and longer when viewing 135° stripes. 90° stripes evoked trajectories of intermediate length.To test if distance and direction are linked independently to stripe orientation, a bee's trajectory was linked to 135° stripes in one compartment and to 45° stripes in another. These trajectories were the same length but differed in their horizontal direction by 60° or by 120°. 90° stripes evoked trajectories of intermediate direction which were shorter than those elicited by either training pattern. Bees were also trained to generate one long and one short trajectory with directions 120° apart. The trajectories elicited by 90° stripes were then biased towards the direction of the long training vector. Length and direction are not treated separately. The rules for combining trajectories resemble those of vector averaging.     

The generalization of directional visual stimuli in the honey bee, Apis mellifera

In transfer tests the ability of bees to generalize visual stimuli was tested by using differently inclined stripes and stripe patterns offered on a vertical screen. After having been trained to single stripes or equidistant stripe patterns, which were orientated by α₊ = 45° to the horizontal, the bees had to discriminate between the training direction α₊ and the competition direction α_c = 135° by means of special stripe configurations. These transfer patterns were obtained by varying different stimulus parameters of the original training stripes, for example by (1) reversing contrast between a stripe and the surrounding visual field, (2) changing the ratio of length/width and by this the dimensions of the stripe, and (3) inserting white intervals into the black stripes. In all three test series the bees succeeded in detecting the α₊-direction along a broad range of stimulus variations. As the bees in the transfer tests positively responded to patterns, which on the other side were significantly discriminated from the training pattern (control tests), the information about the direction of the visual cue had been transferred to a new pattern configuration never seen by the bees during the training situation.     

Places and patterns — a study of context learning in honeybees

To investigate the priming of memories by contextual cues, bees were trained to negotiate two mazes in different places 25?m apart. In the first maze, bees flew leftwards when the inner wall of the maze was covered with 45° stripes or rightwards when the inner wall was coloured yellow. In the second maze, bees flew rightwards on viewing 135° diagonal stripes or leftwards on viewing blue. The trajectories evoked by 45° or 135° stripes were similar in both mazes. However, vertical stripes were treated like 45° stripes in maze 1 and like 135° stripes in maze 2. Contextual cues prime the response to stripes that are oriented in the training condition for that site so influencing responses to stripes in closely neighbouring orientations. What objects in a bee's surroundings determine its sense of place? Bees were trained to different visual patterns at two sites 40?m apart (A+ versus A– at site A, and E+ versus E– at site E). A+ was preferred over A– and E+ was preferred over E– at both training sites. A preference for A+ over E+ exhibited at site A dropped gradually with distance to suggest that spatial context includes both close and distant objects.     

Sequence learning by honeybees

Bees of several genera make foraging trips on which they visit a series of plants in a fixed order. To help understand how honeybees might acquire such routes, we examined whether (1) bees learn motor sequences, (2) they link motor instructions to visual stimuli, (3) their visual memories are triggered by contextual cues associated with the bees' position in a sequence.

Visual scanning behaviour in honeybees

Freely flying bees were rewarded with sugar solution on a variety of black-and-white shapes as well as on coloured gratings in various training situations. In subsequent dual-choice tests, the bees' discrimination between the various shapes was measured. In addition, the bees were video-filmed while flying in front of the shapes. The scanning patterns thus obtained were then quantified in order to characterize scanning behaviour and its relationship to the geometrical parameters of the scanned shapes, investigate whether scanning plays a role in pattern discrimination and examine the influence of training on the characteristics of scanning. The scanning patterns clearly mirror the contours of the scanned shape in all cases, i.e. the bees fly along the contours contained in the shape. This behaviour does not depend on whether the scanned shape is one that was previously rewarded, or one that is completely novel to the bees. Comparison of the results of quantifying the scanning patterns with the results of dual-choice tests reveals that scanning behaviour is independent of discrimination performance. On the average, horizontal scanning directions occur more often than vertical directions. Variations of the training situation produce measurable differences in scanning behavior. However, except in the case of vertical scanning on a vertical grating, these differences are quite small, indicating that following contours is a largely stereotyped behaviour. Horizontal gratings are very well discriminated from vertical ones even if they offer contrast to only one receptor type, i.e. blue or green, demonstrating that the direction of contours is visible to the pattern recognition system even under these conditions. However, vertical and horizontal coloured gratings offering only blue-contrast do not elicit contour-following, whereas gratings offering only green-contrast do. Thus, the bees' scanning behaviour is colour-blind and most probably governed by the green receptors. We suggest that contour-following is the by-product of a behavioural mode which serves to prevent retinal image movement during flight in front of a contoured visual pattern.     

Visually induced height orientation of the fly Musca domestica

The visually controlled height orientation of fixed flying flies (Musca domestica) was investigated. The flight lift force measured by a transducer drives the vertical motion of a panorama. The dynamical conditions of the free flight are electronically simulated for the fly with respect to this degree of freedom of motion. In most of the experimentally investigated cases the panorama consists of a horizontally oriented narrow dark stripe on a bright background. The fly orientates with respect to the stripe, transporting it into a stable fixation position just below the equatorial plane of its compound eyes. It is experimentally demonstrated that the formalism of the linearized theory of the pattern induced flight orientation — Poggio and Reichardt (1973a) — can be applied to describe the height orientation of the fly. The experimental evidence concerning the simultaneous perception of stripes moving in a well defined manner in front of each of the two compound eyes is consistent with the hypothesis that the two halves of the visual system are perceptually additive.     

Visuomotor Response to Object Expansion in Free-Flying Bumble Bees

The flight control systems of flying insects enable many kinds of sophisticated maneuvers, including avoidance of midair collisions. Visuomotor response to an approaching object, received as image expansion on insects’ retina, is a complex event in a dynamic environment where both animals and objects are moving. There are intensive free flight studies on the landing response in which insects receive image expansion by their own movement. However, few studies have been conducted regarding how freely flying insects respond to approaching objects. Here, using common laboratory insects for behavioral research, the bumblebee Bombus ignitus, we examined their visual response to an approaching object in the free-flying condition. While the insect was slowly flying in a free-flight arena, an expanding stripe was projected laterally from one side of the arena with a high-speed digital mirror device projector. Rather than turning away reported before, the bumble bees performed complex flight maneuvers. We synchronized flight trajectories, orientations and wing stroke frequencies with projection parameters of temporal resolution in 0.5 ms, and analyzed the instantaneous relationship between visual input and behavioral output. In their complex behavioral responses, we identified the following two visuomotor behaviors: increasing stroke frequency when the bumble bees confront the stripe expansion, and turning towards (not away) the stripe expansion when it is located laterally to the bee. Our results suggested that the response to object expansion is not a simple and reflexive escape but includes object fixation, presumably for subsequent behavioral choice.     

Das Landschaftsgedächtnis der Bienen. Kleine Gehirne – überraschendes Orientierungsvermögen

We have used a new device, the harmonic radar, to monitor continously the flight paths of bees. Bees are well oriented within the area they have explored during their orientation flights. Bees transported and released at an unexpected site within this area are not lost but fly back to the hive on direct routes after a short search phase. Bees that have been trained to a feeding place may fly first to the feeding place and then back to the hive indicating that they are able to decide between two destinations for their fast return flights. Since bees could not use a beacon at the indicated goals or the structure of the horizon we conclude that their navigation memory is organized according to a geometric map.     

Competition between fixed and moving stripes in the control of orientation by flying Drosophila

ABSTRACT. The direction in which Drosophila hydei Sturtevant flew in response to the movement of a striped pattern beneath them was biased along a direction parallel to the long axis of a stationary stripe between them and the pattern. This was not due to the flies reacting to the movement of the ends of the stripes along the long edges of the stationary one, since a stationary stripe above the flies, not between them and the pattern, similarly biased their flight direction. It was due instead to an optomotor turning reaction induced by the edges of the stationary stripe as the flies were led towards or away from it by their turning and speed control reactions to the moving stripes.     

Target-directed Orientation in Displaced Honeybees

Under sunny weather conditions, displaced honeybees (Apis mellifera) usually fly into the celestial compass direction and thus may be misled from their goal, or they are disorientated. Under cloudy conditions, they may determine the celestial compass direction from prominent landmarks. They may also fly directly toward their goal from a release site. In two experiments, we investigated the orientation of displaced bees when a landmark (target) was close to the goal under different weather conditions. It is shown that in sunny conditions, the celestial compass will override target orientation under most conditions. Under 100% cloud cover, the celestial compass direction retrieved from landmarks modulates target-orientated behaviour but is not by itself a primary orientation factor. The bees will fly toward a previously encountered landmark that signals the target, and in case of several similar landmarks which are visible to the bees, they will choose the one in the direction nearest the celestial compass direction. The results indicate that honeybee orientation is the result of a set of context-specific interdependent orientation mechanisms.     

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

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

Large scale homing in honeybees

Honeybee foragers frequently fly several kilometres to and from vital resources, and communicate those locations to their nest mates by a symbolic dance language. Research has shown that they achieve this feat by memorizing landmarks and the skyline panorama, using the sun and polarized skylight as compasses and by integrating their outbound flight paths. In order to investigate the capacity of the honeybees' homing abilities, we artificially displaced foragers to novel release spots at various distances up to 13 km in the four cardinal directions. Returning bees were individually registered by a radio frequency identification (RFID) system at the hive entrance. We found that homing rate, homing speed and the maximum homing distance depend on the release direction. Bees released in the east were more likely to find their way back home, and returned faster than bees released in any other direction, due to the familiarity of global landmarks seen from the hive. Our findings suggest that such large scale homing is facilitated by global landmarks acting as beacons, and possibly the entire skyline panorama.     

Evidence for instantaneous e-vector detection in the honeybee using an associative learning paradigm

Many insects use the polarization pattern of the sky for obtaining compass information during orientation or navigation. E-vector information is collected by a specialized area in the dorsal-most part of the compound eye, the dorsal rim area (DRA). We tested honeybees' capability of learning certain e-vector orientations by using a classical conditioning paradigm with the proboscis extension reflex. When one e-vector orientation (CS+) was associated with sugar water, while another orientation (CS-) was not rewarded, the honeybees could discriminate CS+ from CS-. Bees whose DRA was inactivated by painting did not learn CS+. When ultraviolet (UV) polarized light (350 nm) was used for CS, the bees discriminated CS+ from CS-, but no discrimination was observed in blue (442 nm) or green light (546 nm). Our data indicate that honeybees can learn and discriminate between different e-vector orientations, sensed by the UV receptors of the DRA, suggesting that bees can determine their flight direction from polarized UV skylight during foraging. Fixing the bees' heads during the experiments did not prevent learning, indicating that they use an 'instantaneous' algorithm of e-vector detection; that is, the bees do not need to actively scan the sky with their DRAs ('sequential' method) to determine e-vector orientation.     

The interaction of edge-fixation and negative phototaxis in the orientation of walking gypsy moths,Lymantria dispar

Summary The visual orientation towards single black stripes and more complex patterns, comprising smooth gradients of brightness was studied in walking gypsy moths. Depending on the width of a black stripe, up to three walking directions are preferred within one stimulus situation: towards the centre of the stripe and towards a region within the stripe closer to each edge. The observed responses are explained by a compromise between edge-fixation and negative phototaxis. This hypothesis turned out to be also applicable to more complex patterns.     

Vector systems and rhythms in movements and orientation of elk (Alces alces L.) and other wild animals (Mammalia)

The orientation of elk and other mammals studied in fields with visual and instrumental tracing has obviously hierarchical organization. Animals usually choose general direction headed for distant markers and then select short-distance landmarks. Movements of animals to distant and close landmarks is characterized by almost constant or regularly changing angles between main direction and movement vector. Fragments of trajectories represent left-side or right-side spirals with decreasing or increasing curvature according to the main direction. Three types of spirals differed by average values of initial angles are considered. Orientation to distant landmarks or along direction of movement possesses discrete reaction on the given landmarks and has some characters of iteration process. Special rhythms of activity (rhythms of orientation changing) participate in regulation of changing of movement directions and orientation reactions. They take part in formation of sinusoid, spiral and other trajectories. Rhythmic regulation involves great statistical variability of parameters (lengths, angles, time periods between consecutive orientations) that can be adaptive meaning. Lengths of orientation vectors and trajectory fragments are similar to some linear elements of landscape. Angular parameters of orientation are more variable. The main ones are similar to the angular parameters of Earth rotation. It looks, that orientation parameters evolved under the influence of Sun-Earth compass in inertial field of Earth rotation.     

Fast and slow flight torque responses in flies and their possible role in visual orientation behaviour

The flight torque responses of tethered flying houseflies to motion and presentation or removal of a vertical dark stripe on a bright background were recorded in real time. Motion with constant speed of 100° s^-1 from front to back elicits a strong fast response following the diraction of the stimulus motion. Motion from back to front elicits a weaker response. Instantaneous presentation and removal of a stationary stripe elicit weak, slow response. Apparent motion from front to back and from back to front elicit weak responses with a fast, directionally selective, transient peak followed by a slow response component oriented towards the stripes position. The fast transient peak response is not elicited if the animals were stimulated before with real movement of the stripe. The results are discussed and an earlier proposed model for free flight tracking and fixation is extended.     

The ocelli control the flight course in honeybees

Abstract Fully-sighted honeybees and bees with all ocelli occluded were trained to fly through an arena to arrive at a feeding place. After training, the bees were exposed to side-light flashes during their feeding flights. The flight paths were recorded on video and analysed frame by frame at 40 ms intervals with reference to the main parameters, the coordinates of the thorax and the yaw angle of the bee. Course angles, translational course velocities and accelerations were calculated, and the responses to side light flashes evaluated with respect to 'on' and 'off.
Immediately after light on, fully-sighted bees respond slightly positively by yawing and flying toward the side light. Bees in which all ocelli are occluded are greatly disturbed and respond with negative yawing and flight path directions.
The ocelli apparently help to control phototactic alertness in the bee. They determine whether phototactic orienting or pattern-induced orienting behaviour is more important in a particular state of motivation. They help to minimize the level of disturbance in flight course control, obviously by activating a neuronal circuit with comparator attributes. It is assumed that this kind of compensation or suppression of phototactically guided reflexes occurs only for a few 100 ms. Consequently, the biological significance of light flashes shorter than 400 ms is very slight.
Fully-sighted bees decelerate strongly when a side light is switched on. Bees in which the ocelli are occluded behave less cautiously: they generally fly faster and need more reaction time. Thus, the ocelli help the bee to react photokinetically to photic stimuli in a much shorter time than do the compound eyes alone.     

A Mathematical Model for Flight Guidance in Honeybee Swarms

When a colony of honeybees relocates to a new nest site, less than 5?% of the bees (the scout bees) know the location of the new nest. Nevertheless, the small minority of informed bees manages to provide guidance to the rest and the entire swarm is able to fly to the new nest intact. The streaker bee hypothesis, one of the several theories proposed to explain the guidance mechanism in bee swarms, seems to be supported by recent experimental observations. The theory suggests that the informed bees make high-speed flights through the swarm in the direction of the new nest, hence conspicuously pointing to the desired direction of travel. This work presents a mathematical model of flight guidance in bee swarms based on the streaker bee hypothesis. Numerical experiments, parameter studies, and comparison with experimental data are presented.     

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.     

Orientation by polarized light in the crayfish dorsal light reflex: behavioral and neurophysiological studies

In decapod crustaceans, the dorsal light reflex rotates the eyestalk so that the dorsal retina faces the brightest segment of dorsal visual space. Stepwise displacements of white stripes elicit eyestalk rotations in the same direction as that of the stripe. Conversely, stepwise displacements of black stripes on a white background elicit eyestalk rotations in the opposite direction as that of the stripe. The reversal of the response with contrast inversion distinguishes the dorsal light reflex from an optokinetic reflex. When the visual scene is composed of polarized light, segmented by variations in e-vector orientation, displacement of segments containing near vertical e-vectors elicit responses similar to those elicited by a white stripe. Displacement of polarized stripes containing near horizontal e-vectors elicit eyestalk rotations similar to those elicited by a black stripe. The results are consistent with the use of polarized light in orientation. The stimulus conditions described above were also applied to visual interneurons (sustaining fibers) and oculomotor neurons and the results were generally in accord with the behavior. In the neural studies, it was possible to show that responses to polarized stripe displacements are predictable from the receptive field location and the neuron’s polarization tuning function. John P. Schroeter deceased on September 14, 2006.