Non-celestial polarization vision in arthropods.

Most insects can detect the pattern of polarized light in the sky with the dorsal rim area in their compound eyes and use this visual information to navigate in their environment by means of 'celestial' polarization vision. 'Non-celestial polarization vision', in contrast, refers to the ability of arthropods to analyze polarized light by means of the 'main' retina, excluding the dorsal rim area. The ability of using the main retina for polarization vision has been attracting sporadic, but steady attention during the last decade. This special issue of the Journal of Comparative Physiology A presents recent developments with a collection of seven original research articles, addressing different aspects of non-celestial polarization vision in crustaceans and insects. The contributions cover different sources of linearly polarized light in nature, the underlying retinal and neural mechanisms of object detection using polarization vision and the behavioral responses of arthropods to polarized reflections from water.

Behavioral responses of free-flying Drosophila melanogaster to shiny, reflecting surfaces.

Active locomotion plays an important role in the life of many animals, permitting them to explore the environment, find vital resources, and escape predators. Most insect species rely on a combination of visual cues such as celestial bodies, landmarks, or linearly polarized light to navigate or orient themselves in their surroundings. In nature, linearly polarized light can arise either from atmospheric scattering or from reflections off shiny non-metallic surfaces like water. Multiple reports have described different behavioral responses of various insects to such shiny surfaces. Our goal was to test whether free-flying Drosophila melanogaster, a molecular genetic model organism and behavioral generalist, also manifests specific behavioral responses when confronted with such polarized reflections. Fruit flies were placed in a custom-built arena with controlled environmental parameters (temperature, humidity, and light intensity). Flight detections and landings were quantified for three different stimuli: a diffusely reflecting matt plate, a small patch of shiny acetate film, and real water. We compared hydrated and dehydrated fly populations, since the state of hydration may change the motivation of flies to seek or avoid water. Our analysis reveals for the first time that flying fruit flies indeed use vision to avoid flying over shiny surfaces.

Stable flies sense and behaviorally respond to the polarization of light.

Insects use their polarization-sensitive photoreceptors in a variety of ecological contexts including host-foraging. Here, we investigated the effect of polarized light on host foraging by the blood-feeding stable fly, Stomoxys calcitrans, a pest of livestock. Electroretinogram recordings with chromatic adaptation demonstrated that the spectral sensitivity of stable flies resembles that of other calyptrate flies. Histological studies of the flies' compound eye revealed differences in microvillar arrangement of ommatidial types, assumed to be pale and yellow, with the yellow R7 and pale R8 photoreceptors having the greatest polarization sensitivity. In behavioural experiments, stable flies preferred to alight on horizontally polarized stimuli with a high degree of linear polarization. This preferential response disappeared when either ultraviolet (UV) or human-visible wavelengths were omitted from light stimuli. Removing specific wavelength bands further revealed that the combination of UV (330-400 nm) and blue (400-525 nm) wavelength bands was sufficient to enable polarized light discrimination by flies. These findings enhance our understanding of polarization vision and foraging behavior among hematophagous insects and should inform future trap designs.

A hypothesis for robust polarization vision: an example from the Australian imperial blue butterfly, Jalmenus evagoras.

The Australian lycaenid butterfly Jalmenus evagoras has iridescent wings that are sexually dimorphic, spectrally and in their degree of polarization, suggesting that these properties are likely to be important in mate recognition. We first describe the results of a field experiment showing that free-flying individuals of J. evagoras discriminate between visual stimuli that vary in polarization content in blue wavelengths but not in others. We then present detailed reflectance spectrophotometry measurements of the polarization content of male and female wings, showing that female wings exhibit blue-shifted reflectance, with a lower degree of polarization relative to male wings. Finally, we describe a novel method for measuring alignment of ommatidial arrays: by measuring variation of depolarized eyeshine intensity from patches of ommatidia as a function of eye rotation, we show that (a) individual rhabdoms contain mutually perpendicular microvilli; (b) many rhabdoms in the array have their microvilli misaligned with respect to neighboring rhabdoms by as much as 45 deg; and (c) the misaligned ommatidia are useful for robust polarization detection. By mapping the distribution of the ommatidial misalignments in eye patches of J. evagoras, we show that males and females exhibit differences in the extent to which ommatidia are aligned. Both the number of misaligned ommatidia suitable for robust polarization detection and the number of aligned ommatidia suitable for edge detection vary with respect to both sex and eye patch elevation. Thus, J. evagoras exhibits finely tuned ommatidial arrays suitable for perception of polarized signals, likely to match sex-specific life history differences in the utility of polarized signals.

Neurons sensitive to non-celestial polarized light in the brain of the desert locust.

Owing to alignment of rhodopsin in microvillar photoreceptors, insects are sensitive to the oscillation plane of polarized light. This property is used by many species to navigate with respect to the polarization pattern of light from the blue sky. In addition, the polarization angle of light reflected from shiny surfaces such as bodies of water, animal skin, leaves, or other objects can enhance contrast and visibility. Whereas photoreceptors and central mechanisms involved in celestial polarization vision have been investigated in great detail, little is known about peripheral and central mechanisms of sensing the polarization angle of light reflected from objects and surfaces. Desert locusts, like other insects, use a polarization-dependent sky compass for navigation but are also sensitive to polarization angles from horizontal directions. In order to further analyze the processing of polarized light reflected from objects or water surfaces, we tested the sensitivity of brain interneurons to the angle of polarized blue light presented from ventral direction in locusts that had their dorsal eye regions painted black. Neurons encountered interconnect the optic lobes, invade the central body, or send descending axons to the ventral nerve cord but are not part of the polarization vision pathway involved in sky-compass coding.

Polarization sensitivity and decentralized visual processing in an animal with a distributed visual system.

The marine mollusc Acanthopleura granulata (Mollusca; Polyplacophora) has a distributed visual array composed of hundreds of small image-forming eyes embedded within its eight dorsal shell plates. As in other animals with distributed visual systems, we still have a poor understanding of the visual capabilities of A. granulata and we have yet to learn where and how it processes visual information. Using behavioral trials involving isoluminant looming visual stimuli, we found that A. granulata demonstrates spatial vision with an angular resolution of 6 deg. We also found that A. granulata responds to looming stimuli defined by contrasting angles of linear polarization. To learn where and how A. granulata processes visual information, we traced optic nerves using fluorescent lipophilic dyes. We found that the optic nerves innervate the underlying lateral neuropil, a neural tissue layer that circumnavigates the body. Adjacent optic nerves innervate the lateral neuropil with highly overlapping arborizations, suggesting it is the site of an integrated visuotopic map. Using immunohistochemistry, we found that the lateral neuropil of A. granulata is subdivided into two separate layers. In comparison, we found that a chiton with eyespots (Chiton tuberculatus) and two eyeless chitons (Ischnochiton papillosus and Chaetopleura apiculata) have lateral neuropil that is a singular circular layer without subdivision, findings consistent with previous work on chiton neuroanatomy. Overall, our results suggest that A. granulata effectuates its visually mediated behaviors using a unique processing scheme: it extracts spatial and polarization information using a distributed visual system, and then integrates and processes that information using decentralized neural circuits.

The sky compass network in the brain of the desert locust.

Many arthropods and vertebrates use celestial signals such as the position of the sun during the day or stars at night as compass cues for spatial orientation. The neural network underlying sky compass coding in the brain has been studied in great detail in the desert locust Schistocerca gregaria. These insects perform long-range migrations in Northern Africa and the Middle East following seasonal changes in rainfall. Highly specialized photoreceptors in a dorsal rim area of their compound eyes are sensitive to the polarization of the sky, generated by scattered sunlight. These signals are combined with direct information on the sun position in the optic lobe and anterior optic tubercle and converge from both eyes in a midline crossing brain structure, the central complex. Here, head direction coding is achieved by a compass-like arrangement of columns signaling solar azimuth through a 360° range of space by combining direct brightness cues from the sun with polarization cues matching the polarization pattern of the sky. Other directional cues derived from wind direction and internal self-rotation input are likely integrated. Signals are transmitted as coherent steering commands to descending neurons for directional control of locomotion and flight.

Performance of polarization-sensitive neurons of the locust central complex at different degrees of polarization.

The polarization pattern of the sky is exploited by many insects for spatial orientation and navigation. It derives from Rayleigh scattering in the atmosphere and depends directly on the position of the sun. In the insect brain, the central complex (CX) houses neurons tuned to the angle of polarization (AoP), that together constitute an internal compass for celestial navigation. Polarized light is not only characterized by the AoP, but also by the degree of polarization (DoP), which can be highly variable, depending on sky conditions. Under a clear sky, the DoP of polarized sky light may reach up to 0.75 but is usually much lower especially when light is scattered by clouds or haze. To investigate how the polarization-processing network of the CX copes with low DoPs, we recorded intracellularly from neurons of the locust CX at different stages of processing, while stimulating with light of different DoPs. Significant responses to polarized light occurred down to DoPs of 0.05 indicating reliable coding of the AoP even at unfavorable sky conditions. Moreover, we found that the activity of neurons at the CX input stage may be strongly influenced by nearly unpolarized light, while the activity of downstream neurons appears less affected.

Receptive field structures for two celestial compass cues at the input stage of the central complex in the locust brain.

Successful navigation depends on an animal's ability to perceive its spatial orientation relative to visual surroundings. Heading direction in insects is represented in the central complex (CX), a navigation center in the brain, to generate steering commands. In insects that navigate relative to sky compass signals, CX neurons are tuned to celestial cues indicating the location of the sun. The desert locust CX contains a compass-like representation of two related celestial cues: the direction of unpolarized direct sunlight and the pattern of polarized light, which depends on the sun position. Whether congruent tuning to these two compass cues emerges within the CX network or is inherited from CX input neurons is unclear. To address this question, we intracellularly recorded from GABA-immunoreactive TL neurons, which are input elements to the locust CX (corresponding to R neurons in Drosophila), while applying visual stimuli simulating unpolarized sunlight and polarized light across the hemisphere above the animal. We show that TL neurons have large receptive fields for both types of stimuli. However, faithful integration of polarization angles across the dorsal hemisphere, or matched-filter ability to encode particular sun positions, was found in only two out of 22 recordings. Those two neurons also showed a good match in sun position coding through polarized and unpolarized light signaling, whereas 20 neurons showed substantial mismatch in signaling of the two compass cues. The data, therefore, suggest that considerable refinement of azimuth coding based on sky compass signals occurs at the synapses from TL neurons to postsynaptic CX compass neurons.

Possible Role of Polarized Light Information in Spatial Recognition in the Cricket Gryllus bimaculatus.

Many insects are able to use skylight e-vector patterns to deduce their heading direction. Crickets have been well known to orient themselves to certain e-vector orientations to keep their walking direction. However, it is still unknown if crickets are able to utilize polarized light information for spatial recognition. Using an experimental paradigm similar to the Morris water maze for rodents, here we examine the possibility that the cricket Gryllus bimaculatus can utilize polarized light information to find the target place. Crickets were placed in a round arena with a heated floor, a portion of which was cooled, and a cross-shaped e-vector pattern was presented from the top of the arena so that the cricket could find the cool spot by walking along the e-vector direction. When the arrangement of the e-vector pattern and the cool spot were fixed throughout the experiments, the time and the walking distance to find the cool spot were significantly decreased with increasing trials, but not when the e-vector pattern was rotated between each trial. Moreover, a model selection indicated that the visual stimulus contributed to the decrease in time and distance. To investigate the cricket's exploration patterns in the arena, a test trial in which the whole floor was uniformly heated was performed before and after the training trials. In the test trial, the crickets trained with the positionally fixed e-vector pattern showed wall-following behavior for a significantly longer time than those untrained and those trained with random e-vector patterns.

The wing scales of the mother-of-pearl butterfly, Protogoniomorpha parhassus, are thin film reflectors causing strong iridescence and polarization.

The dorsal wings of the mother-of-pearl butterfly, Protogoniomorpha parhassus, display an angle-dependent pink, structural color. This effect is created by light interference in the lower lamina of the wing scales, which acts as an optical thin film. The scales feature extremely large windows that enhance the scale reflectance, because the upper lamina of ridges and cross-ribs is very sparse. Characteristic for thin film reflectors, the spectral shape of the reflected light strongly depends on the angle of light incidence, shifting from pink to yellow when changing the angles of illumination and observation from normal to skew, and also the degree of polarization strongly varies. The simultaneous spectral and polarization changes serve a possibly widespread, highly effective system among butterflies for intraspecific communication during flight.

Approach trajectory and solar position affect host plant attractiveness to the small white butterfly.

While it is well documented that insects exploit polarized sky light for navigation, their use of reflected polarized light for object detection has been less well studied. Recently, we have shown that the small white butterfly, Pieris rapae, distinguishes between host and non-host plants based on the degree of linear polarization (DoLP) of light reflected from their leaves. To determine how polarized light cues affect host plant foraging by female P. rapae across their entire visual range including the ultraviolet (300-650 nm), we applied photo polarimetry demonstrating large differences in the DoLP of leaf-reflected light among plant species generally and between host and non-host plants specifically. As polarized light cues are directionally dependent, we also tested, and modelled, the effect of approach trajectory on the polarization of plant-reflected light and the resulting attractiveness to P. rapae. Using photo polarimetry measurements of plants under a range of light source and observer positions, we reveal several distinct effects when polarized reflections are examined on a whole-plant basis rather than at the scale of pixels or plant canopies. Most notably from our modeling, certain approach trajectories are optimal for foraging butterflies, or insects generally, to discriminate between plant species on the basis of the DoLP of leaf-reflected light.

The development and function of neuronal subtypes processing color and skylight polarization in the optic lobes of Drosophila melanogaster.

The retinal mosaics of many insects contain different ommatidial subtypes harboring photoreceptors that are both molecularly and morphologically specialized for comparing between different wavelengths versus detecting the orientation of skylight polarization. The neural circuits underlying these different inputs and the characterization of their specific cellular elements are the subject of intense research. Here we review recent progress on the description of both assembly and function of color and skylight polarization circuitry, by focusing on two cell types located in the distal portion of the medulla neuropil of the fruit fly Drosophila melanogaster's optic lobes, called Dm8 and Dm9. In the main part of the retina, Dm8 cells fall into two molecularly distinct subtypes whose center becomes specifically connected to either one of randomly distributed 'pale' or 'yellow' R7 photoreceptor fates during development. Only in the 'dorsal rim area' (DRA), both polarization-sensitive R7 and R8 photoreceptors are connected to different Dm8-like cell types, called Dm-DRA1 and Dm-DRA2, respectively. An additional layer of interommatidial integration is introduced by Dm9 cells, which receive input from multiple neighboring R7 and R8 cells, as well as providing feedback synapses back into these photoreceptors. As a result, the response properties of color-sensitive photoreceptor terminals are sculpted towards being both maximally decorrelated, as well as harboring several levels of opponency (both columnar as well as intercolumnar). In the DRA, individual Dm9 cells appear to mix both polarization and color signals, thereby potentially serving as the first level of integration of different celestial stimuli. The molecular mechanisms underlying the establishment of these synaptic connections are beginning to be revealed, by using a combination of live imaging, developmental genetic studies, and cell type-specific transcriptomics.

Spatial orientation of social caterpillars is influenced by polarized light.

Processionary caterpillars of Thaumetopoea pityocampa (in Europe) and Ochrogaster lunifer (in Australia) (Lepidoptera: Notodontidae) form single files of larvae crawling head-to-tail when moving to feeding and pupation sites. We investigated if the processions are guided by polarization vision. The heading orientation of processions could be manipulated with linear polarizing filters held above the leading caterpillar. Exposure to changes in the angle of polarization around the caterpillars resulted in corresponding changes in heading angles. Anatomical analysis indicated specializations for polarization vision of stemma I in both species. Stemma I has a rhabdom with orthogonal and aligned microvilli, and an opaque and rugged surface, which are optimizations for skylight polarization vision, similar to the dorsal rim of adult insects. Stemmata II-VI have a smooth and shiny surface and lobed rhabdoms with non-orthogonal and non-aligned microvilli; they are thus optimized for general vision with minimal polarization sensitivity. Behavioural and anatomical evidence reveal that polarized light cues are important for larval orientation and can be robustly detected with a simple visual system.

Orientation to polarized light in tethered flying honeybees.

Many insects exploit the partial plane polarization of skylight for visual compass orientation and/or navigation. In the present study, using a tethering system, we investigated how flying bees respond to polarized light stimuli. The behavioral responses of honeybees (Apis mellifera) to a zenithal polarized light stimulus were observed using a tethered animal in a flight simulator. Flight direction of the bee was recorded by monitoring the horizontal movement of its abdomen, which was strongly anti-correlated with its torque. When the e-vector orientation of the polarized light was rotated clockwise or counterclockwise, the bee responded with periodic right-and-left abdominal movements; however, the bee did not show any clear periodic movement under the static e-vector or depolarized stimulus. The steering frequency of the bee was well coordinated with the e-vector rotation frequency of the stimulus, indicating that the flying bee oriented itself to a certain e-vector orientation, i.e. exhibited polarotaxis. The percentage of bees exhibiting clear polarotaxis was much smaller under the fast stimulus (3.6 deg s-1) compared with that under a slow stimulus (0.9 or 1.8 deg s-1). Bees did not demonstrate any polarotactic behavior after the dorsal rim area of the eyes, which mediates insect polarization vision in general, was bilaterally covered with black paint. Preferred e-vector orientations under the clockwise stimulus varied among individuals and distributed throughout -90 to 90 deg. Some bees showed similar preferred e-vector orientations for clockwise and counterclockwise stimuli whereas others did not. Our results strongly suggest that flying honeybees utilize the e-vector information from the skylight to deduce their heading orientation for navigation.

Neural processing of linearly and circularly polarized light signal in a mantis shrimp Haptosquilla pulchella.

Stomatopods, or mantis shrimp, are the only animal group known to possess circular polarization vision along with linear polarization vision. By using the rhabdomere of a distally located photoreceptor as a wave retarder, the eyes of mantis shrimp are able to convert circularly polarized light into linearly polarized light. As a result, their circular polarization vision is based on the linearly polarized light-sensitive photoreceptors commonly found in many arthropods. To investigate how linearly and circularly polarized light signals might be processed, we presented a dynamic polarized light stimulus while recording from photoreceptors or lamina neurons in intact mantis shrimp Haptosquilla pulchella The results indicate that all the circularly polarized light-sensitive photoreceptors also showed differential responses to the changing e-vector angle of linearly polarized light. When stimulated with linearly polarized light of varying e-vector angle, most photoreceptors produced a concordant sinusoidal response. In contrast, some lamina neurons doubled the response frequency in reacting to linearly polarized light. These responses resembled a rectified sum of two-channel linear polarization-sensitive photoreceptors, indicating that polarization visual signals are processed at or before the first optic lobe. Noticeably, within the lamina, there was one type of neuron that showed a steady depolarization response to all stimuli except right-handed circularly polarized light. Together, our findings suggest that, between the photoreceptors and lamina neurons, linearly and circularly polarized light may be processed in parallel and differently from one another.

Visual metamorphoses in insects and malacostracans: Transitions between an aquatic and terrestrial life.

Arthropods operate in an outrageous diversity of environments. From the deep sea to dense tropical forests, to wide open arctic tundra, they have colonized almost every possible habitat. Within these environments, the presence of light is nearly ubiquitous, varying in intensity, wavelength, and polarization. Light provides critical information about the environment, such as time of day or where food sources may be located. Animals take advantage of this prevalent and informative cue to make behavioral choices. However, the types of choices animals face depend greatly on their environments and needs at any given time. In particular, animals that undergo metamorphosis, with arthropods being the prime example, experience dramatic changes in both behavior and ecology, which in turn may require altering the structure and function of sensory systems such as vision. Amphibiotic organisms maintain aquatic lifestyles as juveniles before transitioning to terrestrial lifestyles as adults. However, light behaves differently in water than in air, resulting in distinct aquatic and terrestrial optical environments. Visual changes in response to these optical differences can occur on multiple levels, from corneal structure down to neural organization. In this review, we summarize examples of alterations in the visual systems of amphibiotic larval and adult insects and malacostracan crustaceans, specifically those attributed to environmental differences between metamorphic phases.

Spatial Contrast Sensitivity to Polarization and Luminance in Octopus.

While color vision is achieved by comparison of signals of photoreceptors tuned to different parts of light spectra, polarization vision is achieved by comparison of signals of photoreceptors tuned to different orientations of the electric field component of visible light. Therefore, it has been suggested that polarization vision is similar to color vision. In most animals that have color vision, the shape of luminance contrast sensitivity curve differs from the shape of chromatic contrast sensitivity curve. While luminance contrast sensitivity typically decreases at low spatial frequency due to lateral inhibition, chromatic contrast sensitivity generally remains high at low spatial frequency. To find out if the processing of polarization signals is similar to the processing of chromatic signals, we measured the polarization and luminance contrast sensitivity dependence in a color-blind animal with well-developed polarization vision, Octopus tetricus. We demonstrate that, in Octopus tetricus, both luminance and polarization contrast sensitivity decrease at low spatial frequency and peak at the same spatial frequency (0.3 cpd). These results suggest that, in octopus, polarization and luminance signals are processed via similar pathways.

Horsefly reactions to black surfaces: attractiveness to male and female tabanids versus surface tilt angle and temperature.

Tabanid flies (Diptera: Tabanidae) are attracted to shiny black targets, prefer warmer hosts against colder ones and generally attack them in sunshine. Horizontally polarised light reflected from surfaces means water for water-seeking male and female tabanids. A shiny black target above the ground, reflecting light with high degrees and various directions of linear polarisation is recognised as a host animal by female tabanids seeking for blood. Since the body of host animals has differently oriented surface parts, the following question arises: How does the attractiveness of a tilted shiny black surface to male and female tabanids depend on the tilt angle δ? Another question relates to the reaction of horseflies to horizontal black test surfaces with respect to their surface temperature. Solar panels, for example, can induce horizontally polarised light and can reach temperatures above 55 °C. How long times would horseflies stay on such hot solar panels? The answer of these questions is important not only in tabanid control, but also in the reduction of polarised light pollution caused by solar panels. To study these questions, we performed field experiments in Hungary in the summer of 2019 with horseflies and black sticky and dry test surfaces. We found that the total number of trapped (male and female) tabanids is highest if the surface is horizontal (δ = 0°), and it is minimal at δ = 75°. The number of trapped males decreases monotonously to zero with increasing δ, while the female catch has a primary maximum and minimum at δ = 0° and δ = 75°, respectively, and a further secondary peak at δ = 90°. Both sexes are strongly attracted to nearly horizontal (0° ≤ δ ≤ 15°) surfaces, and the vertical surface is also very attractive but only for females. The numbers of touchdowns and landings of tabanids are practically independent of the surface temperature T. The time period of tabanids spent on the shiny black horizontal surface decreases with increasing T so that above 58 °C tabanids spent no longer than 1 s on the surface. The horizontally polarised light reflected from solar panels attracts aquatic insects. This attraction is adverse, if the lured insects lay their eggs onto the black surface and/or cannot escape from the polarised signal and perish due to dehydration. Using polarotactic horseflies as indicator insects in our field experiment, we determined the magnitude of polarised light pollution (being proportional to the visual attractiveness to tabanids) of smooth black oblique surfaces as functions of δ and T.

Polarized light sensitivity in Pieris rapae is dependent on both color and intensity.

There is an ever increasing number of arthropod taxa shown to have polarization sensitivity throughout their compound eyes. However, the downstream processing of polarized reflections from objects is not well understood. The small white butterfly, Pieris rapae, has been demonstrated to exploit foliar polarized reflections, specifically the degree of linear polarization (DoLP), to recognize host plants. The well-described visual system of P. rapae includes several photoreceptor types (red, green, blue) that are sensitive to polarized light. Yet, the roles and interaction among photoreceptors underlying the behavioral responses of P. rapae to stimuli with different DoLP remain unknown. To investigate potential neurological mechanisms, we designed several two-choice behavioral bioassays, displaying plant images on paired LCD monitors, which allowed for independent control of polarization, color and intensity. When we presented choices between stimuli that differed in either color or DoLP, both decreasing and increasing the intensity of the more attractive stimulus reduced the strength of preference. This result suggests that differences in color and DoLP are perceived in a similar manner. When we offered a DoLP choice between plant images manipulated to minimize the response of blue, red, or blue and red photoreceptors, P. rapae shifted its preference for DoLP, suggesting a role for all of these photoreceptors. Modeling of P. rapae photoreceptor responses to test stimuli suggests that differential DoLP is not perceived solely as a color difference. Our combined results suggest that Prapae females process and interpret polarization reflections in a way different from that described for other polarization-sensitive taxa.