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.

Spatial integration in polarization-sensitive interneurones of crickets: a survey of evidence, mechanisms and benefits.

Many insects exploit the polarization pattern of the sky for compass orientation in navigation or cruising-course control. Polarization-sensitive neurones (POL1-neurones) in the polarization vision pathway of the cricket visual system have wide visual fields of approximately 60 degrees diameter, i.e. these neurones integrate information over a large area of the sky. This results from two different mechanisms. (i) Optical integration; polarization vision is mediated by a group of specialized ommatidia at the dorsal rim of the eye. These ommatidia lack screening pigment, contain a wide rhabdom and have poor lens optics. As a result, the angular sensitivity of the polarization-sensitive photoreceptors is very wide (median approximately 20 degrees ). (ii) Neural integration; each POL1-neurone receives input from a large number of dorsal rim photoreceptors with diverging optical axes. Spatial integration in POL1-neurones acts as a spatial low-pass filter. It improves the quality of the celestial polarization signal by filtering out cloud-induced local disturbances in the polarization pattern and increases sensitivity.

Polarization-sensitive interneurons in the optic lobe of the desert ant Cataglyphis bicolor.

Desert ants, Cataglyphis bicolor (Hymenoptera), navigate by using compass information provided by skylight polarization. In this study, electrophysiological recordings were made from polarization-sensitive interneurons (POL-neurons) in the optic lobe of Cataglyphis. The POL-neurons exhibit a characteristic polarization opponency. They receive monochromatic input from the UV receptors of the specialized dorsal rim area of the compound eye. Both polarization opponency and monochromacy are features also found in the POL-neurons of crickets (Orthoptera).

Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye.

We made intracellular recordings from the photoreceptors of the polarisation-sensitive dorsal rim area of the cricket compound eye combined with dye marking. By measuring visual field sizes and optical axes in different parts of the dorsal rim area, we assessed the optical properties of the ommatidia. Due to the large angular sensitivities (median about 20 degrees) and the high sampling frequency (about 1 per degree), the visual fields overlap extensively, such that a given portion of the sky is viewed simultaneously by a large number of ommatidia. By comparing the dye markings in the retina and in the optic lobe, the axon projections of the retinula cells were examined. Receptors R1, R2, R5 and R6 project to the lamina, whereas R7 projects to the medulla. The microvilli orientation of the two projection types differ by 90 degrees indicating the two analyser channels that give antagonistic input to polarisation-sensitive interneurons. Using the retinal marking pattern as an indicator for the quality of the intracellular recordings, the polarisation sensitivity of the photoreceptors was re-examined. The polarisation sensitivity of recordings from dye-coupled cells was much lower (median: 4.5) than that of recordings in which only one cell was marked (median: 9.8), indicating that artefactual electrical coupling between photoreceptors can significantly deteriorate polarisation sensitivity. The physiological value of polarisation sensitivity in the cricket dorsal rim area is thus typically about 10.

Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye.

Apart from the sun, the polarization pattern of the sky offers insects a reference for visual compass orientation. Using behavioral experiments, it has been shown in a few insect species (field crickets, honey bees, desert ants, and house flies) that the detection of the oscillation plane of polarized skylight is mediated exclusively by a group of specialized ommatidia situated at the dorsal rim of the compound eye (dorsal rim area). The dorsal rim ommatidia of these species share a number physiological properties that make them especially suitable for polarization vision: each ommatidium contains two sets of homochromatic, strongly polarization-sensitive photoreceptors with orthogonally-arranged analyzer orientations. The physiological specialization of the dorsal rim area goes along with characteristic changes in ommatidial structure, providing actual anatomical hallmarks of polarized skylight detection, that are readily detectable in histological sections of compound eyes. The presence of anatomically specialized dorsal rim ommatidia in many other insect species belonging to a wide range of different orders indicates that polarized skylight detection is a common visual function in insects. However, fine-structural disparities in the design of dorsal rim ommatidia of different insect groups indicate that polarization vision arose polyphyletically in the insects.

How polarization-sensitive interneurones of crickets see the polarization pattern of the sky: a field study with an opto-electronic model neurone

Many insects gain directional information from the polarization pattern of the sky. Polarization vision is mediated by the specialized ommatidia of the dorsal rim area of the compound eye, which contains highly polarization-sensitive photoreceptors. In crickets Gryllus campestris, polarized light information conveyed by the dorsal rim ommatidia was found to be processed by polarization-opponent interneurones (POL-neurones). In this study, a field-proof opto-electronic model of a POL-neurone was constructed that implements the physiological properties of cricket POL-neurones as measured by previous electrophysiological experiments in the laboratory. Using this model neurone, both the strength of the celestial polarization signal and the directional information available to POL-neurones were assessed under a variety of meteorological conditions. We show that the polarization signal as experienced by cricket POL-neurones is very robust, both because of the special filtering properties of these neurones (polarization-antagonism, spatial low-pass, monochromacy) and because of the relatively stable e-vector pattern of the sky.

How polarization-sensitive interneurones of crickets perform at low degrees of polarization

In crickets, polarized-light information from the blue sky is processed by polarization-opponent interneurones (POL-neurones). These neurones receive input from the polarization-sensitive blue receptors found in the specialized dorsal rim area of the compound eye. Even under optimal conditions, the degree of polarization d does not exceed 0.75 in the blue region of the spectrum and it is normally much lower. The aim of this study is to assess how POL-neurones perform at low, physiologically relevant degrees of polarization. The spiking activity of POL-neurones is a sinusoidal function of e-vector orientation with a 180 ° period. The modulation amplitude of this function decreases strongly as the degree of polarization decreases. However, our data indicate that POL-neurones can signal e-vector information at d-values as low as 0.05, which would allow the polarization-sensitive system of crickets to exploit polarized light from the sky for orientation even under unfavourable meteorological conditions.

Specialized ommatidia for polarization vision in the compound eye of cockchafers, Melolontha melolontha (Coleoptera, Scarabaeidae).

The superposition eye of the cockchafer, Melolontha melolontha, exhibits the typical features of many nocturnal and crepuscular scarabaeid beetles: the dioptric apparatus of each ommatidium consists of a thick corneal lens with a strong inner convexity attached to a crystalline cone, that is surrounded by two primary and 9-11 secondary pigment cells. The clear zone contains the unpigmented extensions of the secondary pigment cells, which surround the cell bodies of seven retinula (receptor) cells per ommatidium and a retinular tract formed by them. The seven-lobed fused rhabdoms are composed by the rhabdomeres of the receptor cells 1-7. The rhabdoms are optically separated from each other by a tracheal sheath around the retinulae. The orientation of the microvilli diverges in a fan-like fashion within each rhabdomere. The proximally situated retinula cell 8 does not form a rhabdomere. This standard form of ommatidium stands in contrast to another type of ommatidium found in the dorsal rim area of the eye. The dorsal rim ommatidia are characterized by the following anatomical specializations: (1) The corneal lenses are not clear but contain light-scattering, bubble-like inclusions. (2) The rhabdom length is increased approximately by a factor of two. (3) The rhabdoms have unlobed shapes. (4) Within each rhabdomere the microvilli are parallel to each other. The microvilli of receptor 1 are oriented 90 degrees to those of receptors 2-7. (5) The tracheal sheaths around the retinulae are missing. These findings indicate that the photoreceptors of the dorsal rim area are strongly polarization sensitive and have large visual fields. In the dorsal rim ommatidia of other insects, functionally similar anatomical specializations have been found. In these species, the dorsal rim area of the eye was demonstrated to be the eye region that is responsible for the detection of polarized light. We suggest that the dorsal rim area of the cockchafer eye subserves the same function and that the beetles use the polarization pattern of the sky for orientation during their migrations.

Spectral sensitivity, absolute threshold, and visual field of two tick species, Hyalomma dromedarii and Amblyomma variegatum.

1. The spectral sensitivity in the wavelength range of 340-750 nm was determined by both a behavioral approach based on spontaneous positive phototaxis and the electroretinogram (ERG). 2. Concerning phototaxis the camel tick, Hyalomma dromedarii, showed two sensitivity maxima, one in the UV range (ca. 380 nm) and another in the blue-green range (ca. 500 nm). At higher intensities the relative sensitivity was more pronounced in the UV and at lower intensities more pronounced in the blue-green (reverse Purkinje shift). In the tropical bont tick, Amblyomma variegatum, there was a single sensitivity maximum in the blue range (ca. 480 nm). 3. In the ERG there was a maximum in the blue range (ca. 470 nm) in both species and a weak secondary maximum in the UV in Hyalomma. 4. The absolute sensitivity was very high. The threshold irradiance of phototaxis was as low as 5.2 x 10(6) photons.s-1.cm-2 in Hyalomma and 5.2 x 10(8) photons.s-1.cm-2 in Amblyomma. 5. When the eyes of Hyalomma were covered, the threshold irradiance was still very low, namely 5.2 x 10(8) photons.s-1.cm-2, indicating high absolute sensitivity of the extraretinal photoreceptors. 6. The visual field of the eyes was determined by ERG measurements. In both species the optical axis of each eye, i.e., the center of the visual field, was directed somewhat to the side and above the horizon. In Hyalomma this direction was 35 degrees to the long axis of the animal and 30 degrees above the horizon for natural body posture during walking. In Amblyomma the corresponding angles were 39 degrees and 33 degrees, respectively. The size of the field (at 50% sensitivity) in Hyalomma was relatively small, namely 14 degrees in the horizontal and 25 degrees in the vertical direction, compared with that of Amblyomma with 43 degrees and 49 degrees, respectively. 7. This is the first demonstration in ticks of spectral and absolute sensitivity by the behavioral approach and of the visual field by ERG. The results suggest that tick eyes possess features of both spider eyes and insect ocelli.

Pore canals in the cornea of a functionally specialized area of the honey bee's compound eye.

The fine structure of the cornea in an anatomically and functionally specialized part of the honey bee's compound eye (dorsal rim area) was examined by light microscopy, transmission electron and scanning electron microscopy. Under incident illumination the cornea appears grey and cloudy, leaving only the centers of the corneal lenses clear. This is due to numerous pore canals that penetrate the cornea from the inside, ending a few micron below the outer surface. They consist of (1) a small cylindrical cellular evagination of a pigment cell (proximal), and (2) a rugged-walled, pinetree-shaped extracellular part (distal). The functional significance of these pore canals is discussed. It is concluded that their light scattering properties cause the wide visual fields of the photoreceptor cells measured electrophysiologically in the dorsal rim area, and that this is related to the way this eye region detects polarization in skylight.