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.

The role of the sun in the celestial compass of dung beetles.

Recent research has focused on the different types of compass cues available to ball-rolling beetles for orientation, but little is known about the relative precision of each of these cues and how they interact. In this study, we find that the absolute orientation error of the celestial compass of the day-active dung beetle Scarabaeus lamarcki doubles from 16° at solar elevations below 60° to an error of 29° at solar elevations above 75°. As ball-rolling dung beetles rely solely on celestial compass cues for their orientation, these insects experience a large decrease in orientation precision towards the middle of the day. We also find that in the compass system of dung beetles, the solar cues and the skylight cues are used together and share the control of orientation behaviour. Finally, we demonstrate that the relative influence of the azimuthal position of the sun for straight-line orientation decreases as the sun draws closer to the horizon. In conclusion, ball-rolling dung beetles possess a dynamic celestial compass system in which the orientation precision and the relative influence of the solar compass cues change over the course of the day.

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.

How dim is dim? Precision of the celestial compass in moonlight and sunlight.

Prominent in the sky, but not visible to humans, is a pattern of polarized skylight formed around both the Sun and the Moon. Dung beetles are, at present, the only animal group known to use the much dimmer polarization pattern formed around the Moon as a compass cue for maintaining travel direction. However, the Moon is not visible every night and the intensity of the celestial polarization pattern gradually declines as the Moon wanes. Therefore, for nocturnal orientation on all moonlit nights, the absolute sensitivity of the dung beetle's polarization detector may limit the precision of this behaviour. To test this, we studied the straight-line foraging behaviour of the nocturnal ball-rolling dung beetle Scarabaeus satyrus to establish when the Moon is too dim--and the polarization pattern too weak--to provide a reliable cue for orientation. Our results show that celestial orientation is as accurate during crescent Moon as it is during full Moon. Moreover, this orientation accuracy is equal to that measured for diurnal species that orient under the 100 million times brighter polarization pattern formed around the Sun. This indicates that, in nocturnal species, the sensitivity of the optical polarization compass can be greatly increased without any loss of precision.

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.

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.

Polarized light detection in spiders.

We describe here the detection of polarized light by the simple eyes of spiders. Using behavioural, morphological, electrophysiological and optical studies, we show that spiders have evolved two different mechanisms to resolve the e-vector of light. Wolf spiders (Lycosidae), are able to turn in response to rotation of a polarized pattern at the zenith of their visual fields, and we also describe a strip in the ventral retina of the principal (anterio-median) eyes that views this location and has receptors tiered into two layers. This provides each pair of receptors with a similar optical solution to that provided by the 'dorsal rim area' of the insect compound eye. In contrast, gnaphosid spiders have evolved a pair of lensless secondary eyes for the detection of polarized light. These two eyes, each sensitive to orthogonal directions of polarization, are perfectly designed to integrate signals from the larger part of the sky and cooperate to analyse the polarization of light. Built-in polarizers help to improve signal purity. Similar organisation in the eyes of several other spider families suggests that these two mechanisms are not restricted to only a few families.

A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle Pachysoma striatum.

Many animals have been shown to use the pattern of polarized light in the sky as an optical compass. Specialised photoreceptors are used to analyse this pattern. We here present evidence for an eye design suitable for polarized skylight navigation in the flightless desert scarab Pachysoma striatum. Morphological and electrophysiological studies show that an extensive part of the dorsal eye is equivalent to the dorsal rim area used for polarized light navigation in other insects. A polarization-sensitivity of 12.8 (average) can be recorded from cells sensitive to the ultraviolet spectrum of light. Features commonly known to increase the visual fields of polarization-sensitive photoreceptors, or to decrease their spatial resolution, are not found in the eye of this beetle. We argue that in this insect an optically unspecialised area for polarized light detection allows it not be used exclusively for polarized light navigation.