Polarotaxis and scototaxis in the supratidal amphipod Platorchestia platensis

Talitrid amphipods use many cues for orientation during forays between temporary burrows and feeding areas, and for locating beaches when submerged, with visual cues being particularly important. Little evidence exists for polarized light among these visual cues despite extensive orientation by celestial and underwater polarized light in other crustaceans and in insects. We used electroretinography to assess spectral sensitivity in the eye of the beach flea Platorchestia platensis, and behavioral studies to test whether linearly polarized light serves as an orientation cue. Two spectral classes were present in the P. platensis eye with maxima at 431 and 520 nm. Non-uniform orientation of amphipods in the laboratory arena required either light/dark or polarized cues. Scototactic movements depended on arena conditions (day/night, wet/dry), while orientation under linearly polarized light was wavelength-dependent and parallel to the e-vector. Subsequent tests presented conflicting and additive scototactic and polarotactic cues to differentiate among these responses. In dry conditions, orientation parallel to the polarization e-vector overcame a dominant negative scototaxis, confirming that polarotaxis and scototaxis are separate orientation responses in this species. These behavioral results demonstrate talitrid amphipods can perceive and orient to linearly polarized light, and may use it to orient toward preferred zones on beaches.     

Polarization-based brightness discrimination in the foraging butterfly, Papilio xuthus

The human eye is insensitive to the angular direction of the light e-vector, but several animal species have the ability to discriminate differently polarized lights. How the polarization is detected is often unclear, however. Egg-laying Papilio butterflies have been shown to see false colours when presented with differently polarized lights. Here we asked whether this also holds in foraging butterflies. After training individuals to feed on nectar in front of an unpolarized spectral light, we carried out three dual-choice tests, where the discrimination of (i) the spectral content, (ii) the light intensity, and (iii) the e-vector orientation were investigated. In the first test, the butterflies selected the trained spectrum irrespective of its intensity, and in the second test they chose the light with the higher intensity. The result of the e-vector discrimination test was very similar to that of the second test, suggesting that foraging butterflies discriminate differently polarized lights as differing in brightness rather than as differing in colour. Papilio butterflies are clearly able to use at least two modes of polarization vision depending on the behavioural context.     

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.     

Cone photoreceptor mechanisms and the detection of polarized light in fish

Summary Although numerous studies have demonstrated the detection of polarized light in vertebrates, little is known of the photoreceptor mechanisms involved. Recent evidence, however, indicates that cyprinid fishes possess both ultraviolet (UV) and polarization sensitivity suggesting that some vertebrates, like many invertebrates, may employ UV-sensitive cone receptors in polarization sensitivity. In this report, we describe experiments that determine which spectral types of receptors participate in the detection of polarized light. We used a heart-rate conditioning technique to measure increment thresholds of immobilized goldfish for plane-polarized, narrow-band (10 nm half max.) spectral stimuli (380 nm, 460 nm, 540 nm, 660 nm). A typical experiment involved isolating the activity of a cone photoreceptor mechanism by chromatic adaptation and measuring increment thresholds for spectral stimuli at e-vector orientations of the polarizer between 0° to 180° in 30° steps. The UV-, green- and red-sensitive cone receptor mechanisms showed clear evidence of polarization sensitivity while the blue-sensitive cone receptor mechanism was polarizationally insensitive. The average amplitude (base to peak height on Fig. 4) of the polarization sensitivity curves (UV-, green- and red-curves) was 0.67 log unit (standard deviation of 0.12 log unit), with the UV-sensitive cone receptor mechanism most sensitive to the vertical e-vector axis and the green- and red-sensitive cone receptor mechanisms most sensitive to the horizontal e-vector axis. The observation that different cone photoreceptor mechanisms have orthogonal polarization sensitivity in fish suggests that the perception of polarized light may enhance the capacity for visual discrimination in lower vertebrates.     

Polarized skylight orientation in the desert antCataglyphis

Summary The desert antCataglyphis bicolor is able to use the pattern of polarized light in the sky as compass. By confronting the ant to single spots of artificially and naturally polarized light it is shown howCataglyphis uses the polarization pattern.When exposed to a horizontal e-vector,Cataglyphis was always oriented correctly. Orientation errors occurred, however, when other e-vector directions were presented. This indicates that the e-vector positions assumed by the ant do not coincide with the e-vector positions actually realized in the sky. From this it is concluded thatCataglyphis has no detailed knowledge of the actual azimuthal positions of the e-vectors. Instead, it is relying on a simplified celestial map of the polarization patterns in the sky (Fig. 7).Usually, the ant did not confuse celestial spots with identical e-vector directions. Even at sunset when the polarization pattern is completely ambiguous, correct orientation occurred. This suggests that the ant uses additional celestial cues such as the degree of polarization, the color or the intensity to find its way home when the sun is obscured.     

Polarized-light sensitivity in rainbow trout (Oncorhynchus mykiss): characterization from multi-unit responses in the optic nerve

Integrated spike activity of axons from the optic nerve was measured in an investigation of the e-vector sensitive mechanism underlying the ability of rainbow trout (Oncorhynchus mykiss) for orientation in downwelling, linearly-polarized light. In anaesthetized, immobilized fish, one eye was exposed to incremental light flashes which were superimposed over closely controlled background conditions. Under scotopic and various photopic conditions, intensity/response curves were generated from the on-response of the optic nerve. Relative sensitivity curves were then obtained as a function of e-vector direction for the 5 kinds of receptor cells in this trout's retina: rods, ultraviolet cones (UV), short wavelength cones (S), medium wavelength cones (M), and long wavelength cones (L).Under scotopic conditions, no sensitivity to e-vector was apparent: thus, rods do not mediate polarization sensitivity. Under photopic conditions, parr weighing 8–10 g exhibited e-vector sensitivity in two orthogonal channels. A UV stimulus (380 nm) on a white background evoked a three-peaked response (0°, 90°, and 180°) to the e-vector orientations presented in 30° increments between 0° and 180°. In contrast, when the background was illuminated with appropriate short and long wavelength cut-off filters, M-and L-cones showed maximum responses only to the horizontal (90°) plane whether they were stimulated at their -absorption band or their -absorption band in the near UV. Isolated UV-cones gave maximum responses to the vertical (0° and 180°) e-vector, thus corresponding to a second channel. The blue sensitive, S-cones, did not show evidence of polarization sensitivity. As well, no evidence of the polarization sensitivity was observed under UV isolating background conditions in larger individuals, 50–78 g smolts, although the other cone mechanisms responded as in smaller individuals.     

Polarization vision in crayfish motion detectors

Motion detector interneurons were examined to determine their responsiveness to the motion of polarized light images (i.e. images segmented by spatial variations in e-vector angle). Computer generated images were displayed as intensity contrasts or polarization contrasts on a modified LCD projection panel. The stimuli included the motion of a single stripe (45 degrees -55 degrees /s) and the global motion of a square wave grating (3.3 degrees /s). Neurons were impaled in the medulla interna. Of the neurons which exhibited a directional response to the motion of intensity contrast stimuli, about 2/3 were also directional in the response to polarized light images. Transient (nondirectional) stimuli included looming and jittery motions. The responses to the transient motions of the polarized light images were roughly comparable to those elicited by intensity contrast. The results imply that behavioral responses to polarized light images (i.e. optokinetic and defense reflexes) may have a basis in the polarization sensitivity and synaptic organization of the medulla interna.     

Polarization contrast and motion detection

Form and motion perception rely upon the visual system’s capacity to segment the visual scene based upon local differences in luminance or wavelength. It is not clear if polarization contrast is a sufficient basis for motion detection. Here we show that crayfish optomotor responses elicited by the motion of images derived from spatiotemporal variations in e-vector angles are comparable to contrast-elicited responses. Response magnitude increases with the difference in e-vector angles in adjacent segments of the scene and with the degree of polarization but the response is relatively insensitive to the absolute values of e-vector angles that compose the stimulus. The results indicate that polarization contrast can support visual motion detection.     

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.     

Why do dusk-active cockchafers detect polarization in the green? The polarization vision in Melolontha melolontha is tuned to the high polarized intensity of downwelling light under canopies during sunset

In the retina of dusk-active European cockchafers, Melolontha melolontha, the linear polarization of downwelling light (skylight or light from the tree canopy) is detected by photoreceptors in upward-pointing ommatidia with maximal sensitivity at 520 nm in the green portion of the spectrum. To date no attempt has been made to answer the question of why these beetles detect polarization in the green. Here we present an atmospheric optical and receptor-physiological explanation of why longer wavelengths are advantageous for the perception of polarization of downwelling light under canopies illuminated by the setting sun. Our explanation focuses on illumination situations during sunset in canopied optical environments, because cockchafers are active at sunset and fly predominantly under canopies during their swarming, feeding, and mating periods. Using three simple atmospheric optical models, we computed the degree of linear polarization, the linearly polarized intensity of downwelling light, the quantum catch, and quantum catch difference between polarization detectors with orthogonal microvilli under canopies illuminated by the setting sun as functions of wavelength and solar zenith angle. Based upon these computations, we show that the green sensitivity of polarization detectors in M. melolontha is tuned to the high polarized intensity of downwelling light in the green under canopies during sunset, an optimal compromise between simultaneous maximization of the quantum catch and the quantum catch difference. We also briefly discuss how green-sensitive polarization detectors can function efficiently enough during the pre-feeding and egg-laying flights of cockchafers, which always occur prior to sunset and under the sky.     

Motor Responses to Polarized Light and Gravity Sensing in Euglena gracilis*†

SYNOPSIS. Euglena gracilis strain Z has a motor response which results in orientation with respect to the polarization of a light stimulus. Cells swim preferentially in a direction perpendicular to the plane of polarization of the stimulus. If 2 polarized stimuli are given from opposite directions, the preferred direction is, under certain circumstances, at right angles to the directions of both stimuli. Euglena also preferentially assumes an orientation that is at right angles to the force of gravity. The relationships between these responses and phototactic movements oriented with respect to the direction of the stimulus are discussed.     

Behavioral analysis of polarization vision in tethered flying locusts

For spatial navigation many insects rely on compass information derived from the polarization pattern of the sky. We demonstrate that tethered flying desert locusts (Schistocerca gregaria) show e-vector-dependent yaw-torque responses to polarized light presented from above. A slowly rotating polarizer (5.3° s^–1) induced periodic changes in yaw torque corresponding to the 180° periodicity of the stimulus. Control experiments with a rotating diffuser, a weak intensity pattern, and a stationary polarizer showed that the response is not induced by intensity gradients in the stimulus. Polarotaxis was abolished after painting the dorsal rim areas of the compound eyes black, but remained unchanged after painting the eyes except the dorsal rim areas. During rotation of the polarizer, two e-vectors (preferred and avoided e-vector) induced no turning responses: they were broadly distributed from 0 to 180° but, for a given animal, were perpendicular to each other. The data demonstrate polarization vision in the desert locust, as shown previously for bees, flies, crickets, and ants. Polarized light is perceived through the dorsal rim area of the compound eye, suggesting that polarization vision plays a role in compass navigation of the locust.     

Homothorax switches function of Drosophila photoreceptors from color to polarized light sensors

Different classes of photoreceptors (PRs) allow animals to perceive various types of visual information. In the Drosophila eye, the outer PRs of each ommatidium are involved in motion detection while the inner PRs mediate color vision. In addition, flies use a specialized class of inner PRs in the "dorsal rim area" of the eye (DRA) to detect the e-vector of polarized light, allowing them to exploit skylight polarization for orientation. We show that homothorax is both necessary and sufficient for inner PRs to adopt the polarization-sensitive DRA fate instead of the color-sensitive default state. Homothorax increases rhabdomere size and uncouples R7-R8 communication to allow both cells to express the same opsin rather than different ones as required for color vision. Homothorax expression is induced by the iroquois complex and the wingless (wg) pathway. However, crucial wg pathway components are not required, suggesting that additional signals are involved.     

Behavioural evidence for polarization vision in crickets

ABSTRACT. Tethered field crickets, Gryllus campestris L., walking on an air-suspended bail exhibit a spontaneous response to the e-vector of polarized light presented from above: E-vector orientation controls strength and direction of turning tendency. Experiments in which different eye regions are covered with paint suggest that this response is mediated by the anatomically and physiologically specialized dorsal rim area of the compound eye. We conclude that crickets have polarization vision and that the dorsal rim area of the eye plays a key role in this sensory capacity.     

Retinal ultrastructure may mediate polarization sensitivity in larvae of the Sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae)

A number of invertebrates are known to be sensitive to the polarization of light and use this trait in orientation, communication, or prey detection. In these animals polarization sensitivity tends to originate in rhabdomeric photoreceptors that are more or less uniformly straight and parallel. Typically, polarization sensitivity is based on paired sets of photoreceptors with orthogonal orientation of their rhabdomeres. Sunburst diving beetle larvae are active swimmers and highly visual hunters which could potentially profit from polarization sensitivity. These larvae, like those of most Dytiscids, have a cluster of six lens eyes or stemmata (designated E1 through E6) on each side of the head capsule. We examined the ultrastructure of the photoreceptor cells of the principal eyes (E1 and E2) of first instar larvae to determine whether their rhabdomeric organization could support polarization sensitivity. A detailed electron microscopical study shows that the proximal retinas of E1 and E2 are in fact composed of photoreceptors with predominantly parallel microvilli and that neighboring rhabdomeres are oriented approximately perpendicularly to one another. A similar organization is observed in the medial retina of E1, but not in the distal retinas of E1&2. Our findings suggest that T. marmoratus larvae might be able to analyze polarized light. If so, this could be used by freshly hatched larvae to find water or within the water to break the camouflage of common prey items such as mosquito larvae. Physiological and behavioral tests are planned to determine whether larvae of T. marmoratus can actually detect and exploit polarization signals.     

Evidence for true polarization vision based on a two-channel analyzer system in the eye of the water bug,Notonecta glauca

Summary Water bugs (Notonecta glauca) were set into flight in a room with a homogeneously illuminated ceiling and a light-emitting platform on the floor. In these conditions polarized UV light from the platform was more effective in causing the animals to fly down to the surface of the platform than was unpolarized UV light several times as intense. Experiments with an array of baffles that restricted the directions from which the polarization film on the platform could be seen showed that the polarized UV light is effective in eliciting descent only when the e-vector is perpendicular to the median sagittal plane of the animal (horizontal). It can be concluded that polarized UV light with horizontal e-vector is distinguished, as a special sensory quality, from unpolarized UV light.Notonecta thus provides an example of true polarization vision.The special orthogonal arrangement of the microvilli in the rhabdomeres of the UV visual cells in the ventral part of the eye (cf. Schwind 1983 b and Schwind et al., in press) is suggestive with regard to polarization vision. The microvilli of the two UV visual cells in the ommatidia looking forward and down are horizontal and vertical, respectively, and hence could serve as a two-channel analyzer system capable of distinguishing the polarized UV light reflected by a water surface from unpolarized UV light.     

Neurobiology of polarization vision in the locust Schistocerca gregaria

The polarization pattern of the blue sky serves as an important reference for spatial orientation in insects. To understand the neural mechanisms involved in sky compass orientation we have analyzed the polarization vision system in the locust Schistocerca gregaria. As in other insects, photoreceptors adapted for the detection of sky polarization are concentrated in a dorsal rim area (DRA) of the compound eye. Stationary flying locusts show polarotactic yaw-torque responses when illuminated through a rotating polarizer from above. This response is abolished after painting the DRAs. Central stages of the polarization vision system, revealed through tracing studies, include dorsal areas in the lamina and medulla, the anterior lobe of the lobula, the anterior optic tubercle, the lateral accessory lobe and the central complex. Physiological analysis of polarization-sensitive (POL) neurons has focussed on the optic tubercle and on the central complex. Each POL neuron was maximally excited at a certain e-vector (phimax) and was maximally inhibited at an e-vector perpendicular to phimax. The neurons had large visual fields, and many neurons received input from both eyes. The neuronal organization of the central complex suggests a role as a spatial compass within the locust brain.     

Navigation by light polarization in clear and turbid waters

Certain terrestrial animals use sky polarization for navigation. Certain aquatic species have also been shown to orient according to a polarization stimulus, but the correlation between underwater polarization and Sun position and hence the ability to use underwater polarization as a compass for navigation is still under debate. To examine this issue, we use theoretical equations for per cent polarization and electric vector (e-vector) orientation that account for the position of the Sun, refraction at the air-water interface and Rayleigh single scattering. The polarization patterns predicted by these theoretical equations are compared with measurements conducted in clear and semi-turbid coastal sea waters at 2 m and 5 m depth over sea floors of 6 m and 28 m depth. We find that the per cent polarization is correlated with the Sun's elevation only in clear waters. We furthermore find that the maximum value of the e-vector orientation angle equals the angle of refraction only in clear waters, in the horizontal viewing direction, over the deeper sea floor. We conclude that navigation by use of underwater polarization is possible under restricted conditions, i.e. in clear waters, primarily near the horizontal viewing direction, and in locations where the sea floor has limited effects on the light's polarization.