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.

Multiple axes of visual system diversity in Ithomiini, an ecologically diverse tribe of mimetic butterflies.

The striking structural variation seen in arthropod visual systems can be explained by the overall quantity and spatio-temporal structure of light within habitats coupled with developmental and physiological constraints. However, little is currently known about how fine-scale variation in visual structures arises across shorter evolutionary and ecological scales. In this study, we characterise patterns of interspecific (between species), intraspecific (between sexes) and intraindividual (between eye regions) variation in the visual system of four ithomiine butterfly species. These species are part of a diverse 26-million-year-old Neotropical radiation where changes in mimetic colouration are associated with fine-scale shifts in ecology, such as microhabitat preference. Using a combination of selection analyses on visual opsin sequences, in vivo ophthalmoscopy, micro-computed tomography (micro-CT), immunohistochemistry, confocal microscopy and neural tracing, we quantify and describe physiological, anatomical and molecular traits involved in visual processing. Using these data, we provide evidence of substantial variation within the visual systems of Ithomiini, including: (i) relaxed selection on visual opsins, perhaps mediated by habitat preference, (ii) interspecific shifts in visual system physiology and anatomy, and (iii) extensive sexual dimorphism, including the complete absence of a butterfly-specific optic neuropil in the males of some species. We conclude that considerable visual system variation can exist within diverse insect radiations, hinting at the evolutionary lability of these systems to rapidly develop specialisations to distinct visual ecologies, with selection acting at the perceptual, processing and molecular level.

The marine gastropod Conomurex luhuanus (Strombidae) has high-resolution spatial vision and eyes with complex retinas.

All species within the conch snail family Strombidae possess large camera-type eyes that are surprisingly well-developed compared with those found in most other gastropods. Although these eyes are known to be structurally complex, very little research on their visual function has been conducted. Here, we use isoluminant expanding visual stimuli to measure the spatial resolution and contrast sensitivity of a strombid, Conomurex luhuanus. Using these stimuli, we show that this species responds to objects as small as 1.06 deg in its visual field. We also show that C. luhuanus responds to Michelson contrasts of 0.07, a low contrast sensitivity between object and background. The defensive withdrawal response elicited by visual stimuli of such small angular size and low contrast suggests that conch snails may use spatial vision for the early detection of potential predators. We support these findings with morphological estimations of spatial resolution of 1.04 deg. These anatomical data therefore agree with the behavioural measures and highlight the benefits of integrating behavioural and morphological approaches in animal vision studies. Using contemporary imaging techniques [serial block-face scanning electron microscopy (SBF-SEM), in conjunction with transmission electron microscopy (TEM)], we found that C. luhuanus have more complex retinas, in terms of cell type diversity, than expected based on previous studies of the group using TEM alone. We find the C. luhuanus retina comprises six cell types, including a newly identified ganglion cell and accessory photoreceptor, rather than the previously described four cell types.

Hoverflies use a time-compensated sun compass to orientate during autumn migration.

The sun is the most reliable celestial cue for orientation available to daytime migrants. It is widely assumed that diurnal migratory insects use a 'time-compensated sun compass' to adjust for the changing position of the sun throughout the day, as demonstrated in some butterfly species. The mechanisms used by other groups of diurnal insect migrants remain to be elucidated. Migratory species of hoverflies (Diptera: Syrphidae) are one of the most abundant and beneficial groups of diurnal migrants, providing multiple ecosystem services and undergoing directed seasonal movements throughout much of the temperate zone. To identify the hoverfly navigational strategy, a flight simulator was used to measure orientation responses of the hoverflies Scaeva pyrastri and Scaeva selenitica to celestial cues during their autumn migration. Hoverflies oriented southwards when they could see the sun and shifted this orientation westward following a 6 h advance of their circadian clocks. Our results demonstrate the use of a time-compensated sun compass as the primary navigational mechanism, consistent with field observations that hoverfly migration occurs predominately under clear and sunny conditions.

Thresholds of polarization vision in octopuses.

Polarization vision is widespread in nature, mainly among invertebrates, and is used for a range of tasks including navigation, habitat localization and communication. In marine environments, some species such as those from the Crustacea and Cephalopoda that are principally monochromatic, have evolved to use this adaptation to discriminate objects across the whole visual field, an ability similar to our own use of colour vision. The performance of these polarization vision systems varies, and the few cephalopod species tested so far have notably acute thresholds of discrimination. However, most studies to date have used artificial sources of polarized light that produce levels of polarization much higher than found in nature. In this study, the ability of octopuses to detect polarization contrasts varying in angle of polarization (AoP) was investigated over a range of different degrees of linear polarization (DoLP) to better judge their visual ability in more ecologically relevant conditions. The 'just-noticeable-differences' (JND) of AoP contrasts varied consistently with DoLP. These JND thresholds could be largely explained by their 'polarization distance', a neurophysical model that effectively calculates the level of activity in opposing horizontally and vertically oriented polarization channels in the cephalopod visual system. Imaging polarimetry from the animals' natural environment was then used to illustrate the functional advantage that these polarization thresholds may confer in behaviourally relevant contexts.

Gaze stabilization in mantis shrimp in response to angled stimuli.

Gaze stabilization is a fundamental aspect of vision and almost all animals shift their eyes to compensate for any self-movement relative to the external environment. When it comes to mantis shrimp, however, the situation becomes complicated due to the complexity of their visual system and their range of eye movements. The stalked eyes of mantis shrimp can independently move left and right, and up and down, whilst simultaneously rotating about the axis of the eye stalks. Despite the large range of rotational freedom, mantis shrimp nevertheless show a stereotypical gaze stabilization response to horizontal motion of a wide-field, high-contrast stimulus. This response is often accompanied by pitch (up-down) and torsion (about the eye stalk) rotations which, surprisingly, have no effect on the performance of yaw (side-to-side) gaze stabilization. This unusual feature of mantis shrimp vision suggests that their neural circuitry for detecting motion is radially symmetric and immune to the confounding effects of torsional self-motion. In this work, we reinforce this finding, demonstrating that the yaw gaze stabilization response of the mantis shrimp is robust to the ambiguous motion cues arising from the motion of striped visual gratings in which the angle of a grating is offset from its direction of travel.

Polarisation signals: a new currency for communication.

Most polarisation vision studies reveal elegant examples of how animals, mainly the invertebrates, use polarised light cues for navigation, course-control or habitat selection. Within the past two decades it has been recognised that polarised light, reflected, blocked or transmitted by some animal and plant tissues, may also provide signals that are received or sent between or within species. Much as animals use colour and colour signalling in behaviour and survival, other species additionally make use of polarisation signalling, or indeed may rely on polarisation-based signals instead. It is possible that the degree (or percentage) of polarisation provides a more reliable currency of information than the angle or orientation of the polarised light electric vector (e-vector). Alternatively, signals with specific e-vector angles may be important for some behaviours. Mixed messages, making use of polarisation and colour signals, also exist. While our knowledge of the physics of polarised reflections and sensory systems has increased, the observational and behavioural biology side of the story needs more (and more careful) attention. This Review aims to critically examine recent ideas and findings, and suggests ways forward to reveal the use of light that we cannot see.

Haidinger's brushes elicited at varying degrees of polarization rapidly and easily assesses total macular pigmentation.

Macular pigments (MPs), by absorbing potentially toxic short-wavelength (400-500 nm) visible light, provide protection against photo-chemical damage thought to be relevant in the pathogenesis of age-related macular degeneration (AMD). A method of screening for low levels of MPs could be part of a prevention strategy for helping people to delay the onset of AMD. We introduce a new method for assessing MP density that takes advantage of the polarization-dependent absorption of blue light by MPs, which results in the entoptic phenomenon called Haidinger's brushes (HB). Subjects were asked to identify the direction of rotation of HB when presented with a circular stimulus illuminated with an even intensity of polarized white light in which the electric field vector was rotating either clockwise or anti-clockwise. By reducing the degree of polarization of the stimulus light, a threshold for perceiving HB (degree of polarization threshold) was determined and correlated (r2=0.66) to macular pigment optical density assessed using dual-wavelength fundus autofluoresence. The speed and ease of measurement of degree of polarization threshold makes it well suited for large-scale screening of macular pigmentation.

Behavioural evidence for polychromatic ultraviolet sensitivity in mantis shrimp.

Stomatopod crustaceans are renowned for their elaborate visual systems. Their eyes contain a plethora of photoreceptors specialized for chromatic and polarization detection, including several that are sensitive to varying wavelength ranges and angles of polarization within the ultraviolet (UV) range (less than 400 nm). Behavioural experiments have previously suggested that UV photoreception plays a role in stomatopod communication, but these experiments have only manipulated the entire UV range. Here, using a behavioural approach, we examine UV vision in the stomatopod Haptosquilla trispinosa Using binary trained choice assays as well as innate burrow-choice experiments, we assessed the ability of H. trispinosa to detect and respond to narrow-band LED stimuli peaking near 314 nm (UVB) versus 379 nm (UVA) in wavelength. We find that H. trispinosa can discriminate these stimuli and appears to display an aversive reaction to UVB light, suggesting segregated behavioural responses to stimuli within the UV range. Furthermore, we find that H. trispinosa can discriminate stimuli peaking near 379 nm versus 351 nm in wavelength, suggesting that their wavelength discrimination in the UV is comparable to their performance in the human-visible range.

Complex gaze stabilization in mantis shrimp.

Almost all animals, regardless of the anatomy of the eyes, require some level of gaze stabilization in order to see the world clearly and without blur. For the mantis shrimp, achieving gaze stabilization is unusually challenging as their eyes have an unprecedented scope for movement in all three rotational degrees of freedom: yaw, pitch and torsion. We demonstrate that the species Odontodactylus scyllarus performs stereotypical gaze stabilization in the yaw degree of rotational freedom, which is accompanied by simultaneous changes in the pitch and torsion rotation of the eye. Surprisingly, yaw gaze stabilization performance is unaffected by both the torsional pose and the rate of torsional rotation of the eye. Further to this, we show, for the first time, a lack of a torsional gaze stabilization response in the stomatopod visual system. In the light of these findings, we suggest that the neural wide-field motion detection network in the stomatopod visual system may follow a radially symmetric organization to compensate for the potentially disorientating effects of torsional eye movements, a system likely to be unique to stomatopods.

Molecular palaeontology illuminates the evolution of ecdysozoan vision.

Colour vision is known to have arisen only twice-once in Vertebrata and once within the Ecdysozoa, in Arthropoda. However, the evolutionary history of ecdysozoan vision is unclear. At the molecular level, visual pigments, composed of a chromophore and a protein belonging to the opsin family, have different spectral sensitivities and these mediate colour vision. At the morphological level, ecdysozoan vision is conveyed by eyes of variable levels of complexity; from the simple ocelli observed in the velvet worms (phylum Onychophora) to the marvellously complex eyes of insects, spiders, and crustaceans. Here, we explore the evolution of ecdysozoan vision at both the molecular and morphological level; combining analysis of a large-scale opsin dataset that includes previously unknown ecdysozoan opsins with morphological analyses of key Cambrian fossils with preserved eye structures. We found that while several non-arthropod ecdysozoan lineages have multiple opsins, arthropod multi-opsin vision evolved through a series of gene duplications that were fixed in a period of 35-71 million years (Ma) along the stem arthropod lineage. Our integrative study of the fossil and molecular record of vision indicates that fossils with more complex eyes were likely to have possessed a larger complement of opsin genes.

Polarisation vision: overcoming challenges of working with a property of light we barely see.

In recent years, the study of polarisation vision in animals has seen numerous breakthroughs, not just in terms of what is known about the function of this sensory ability, but also in the experimental methods by which polarisation can be controlled, presented and measured. Once thought to be limited to only a few animal species, polarisation sensitivity is now known to be widespread across many taxonomic groups, and advances in experimental techniques are, in part, responsible for these discoveries. Nevertheless, its study remains challenging, perhaps because of our own poor sensitivity to the polarisation of light, but equally as a result of the slow spread of new practices and methodological innovations within the field. In this review, we introduce the most important steps in designing and calibrating polarised stimuli, within the broader context of areas of current research and the applications of new techniques to key questions. Our aim is to provide a constructive guide to help researchers, particularly those with no background in the physics of polarisation, to design robust experiments that are free from confounding factors.

Correction to: Polarisation vision: overcoming challenges of working with a property of light we barely see.

In "Polarisation vision: overcoming challenges of working with a property of light we barely see" (Foster et al. 2018) we provide a basic description of how Stokes parameters can be estimated and used to calculate the angle of polarisation (AoP).

Denoising imaging polarimetry by adapted BM3D method.

In addition to the visual information contained in intensity and color, imaging polarimetry allows visual information to be extracted from the polarization of light. However, a major challenge of imaging polarimetry is image degradation due to noise. This paper investigates the mitigation of noise through denoising algorithms and compares existing denoising algorithms with a new method, based on BM3D (Block Matching 3D). This algorithm, Polarization-BM3D (PBM3D), gives visual quality superior to the state of the art across all images and noise standard deviations tested. We show that denoising polarization images using PBM3D allows the degree of polarization to be more accurately calculated by comparing it with spectral polarimetry measurements.

Optical influence of oil droplets on cone photoreceptor sensitivity.

Oil droplets are spherical organelles found in the cone photoreceptors of vertebrates. They are generally assumed to focus incident light into the outer segment, and thereby improve light catch because of the droplets' spherical lens-like shape. However, using full-wave optical simulations of physiologically realistic cone photoreceptors from birds, frogs and turtles, we find that pigmented oil droplets actually drastically reduce the transmission of light into the outer segment integrated across the full visible wavelength range of each species. Only transparent oil droplets improve light catch into the outer segments, and any enhancement is critically dependent on the refractive index, diameter of the oil droplet, and diameter and length of the outer segment. Furthermore, oil droplets are not the only optical elements found in cone inner segments. The ellipsoid, a dense aggregation of mitochondria situated immediately prior to the oil droplet, mitigates the loss of light at the oil droplet surface. We describe a framework for integrating these optical phenomena into simple models of receptor sensitivity, and the relevance of these observations to evolutionary appearance and loss of oil droplets is discussed.

Circularly polarized light detection in stomatopod crustaceans: a comparison of photoreceptors and possible function in six species.

A combination of behavioural and electrophysiological experiments have previously shown that two species of stomatopod, Odontodactylus scyllarus and Gonodactylaceus falcatus, can differentiate between left- and right-handed circularly polarized light (CPL), and between CPL and linearly polarized light (LPL). It remains unknown if these visual abilities are common across all stomatopod species, and if so, how circular polarization sensitivity may vary between and within species. A subsection of the midband, a specialized region of stomatopod eyes, contains distally placed photoreceptor cells, termed R8 (retinular cell number 8). These cells are specifically built with unidirectional microvilli and appear to be angled precisely to convert CPL into LPL. They are mostly quarter-wave retarders for human visible light (400-700 nm), as well as being ultraviolet-sensitive linear polarization detectors. The effectiveness of the R8 cells in this role is determined by their geometric and optical properties. In particular, the length and birefringence of the R8 cells are crucial for retardation efficiency. Here, our comparative studies show that most species investigated have the theoretical ability to convert CPL into LPL, such that the handedness of an incoming circular reflection or signal could be discriminated. One species, Haptosquilla trispinosa, shows less than quarter-wave retardance. Whilst some species are known to produce circularly polarized reflections (some Odontodactylus species and G. falcatus, for example), others do not, so a variety of functions for this ability are worth considering.

The independence of eye movements in a stomatopod crustacean is task dependent.

Stomatopods have an extraordinary visual system, incorporating independent movement of their eyes in all three degrees of rotational freedom. In this work, we demonstrate that in the peacock mantis shrimp, Odontodactylus scyllarus, the level of ocular independence is task dependent. During gaze stabilization in the context of optokinesis, there is weak but significant correlation between the left and right eyes in the yaw degree of rotational freedom, but not in pitch and torsion. When one eye is completely occluded, the uncovered eye does not drive the covered eye during gaze stabilization. However, occluding one eye does significantly affect the uncovered eye, lowering its gaze stabilization performance. There is a lateral asymmetry, with the magnitude of the effect depending on the eye (left or right) combined with the direction of motion of the visual field. In contrast, during a startle saccade, the uncovered eye does drive a covered eye. Such disparate levels of independence between the two eyes suggest that responses to individual visual tasks are likely to follow different neural pathways.

Evolution under pressure and the adaptation of visual pigment compressibility in deep-sea environments.

Understanding the link between how proteins function in animals that live in extreme environments and selection on specific properties of amino acids has proved extremely challenging. Here we present the discovery of how the compressibility of opsin proteins in two evolutionarily distinct animal groups, teleosts and cephalopods, appears to be adapted to the high-pressure environment of the deep-sea. We report how in both groups, opsins in deeper living species are calculated to be less compressible. This is largely due to a common set of amino acid sites (bovRH# 159, 196, 213, 275) undergoing positive destabilizing selection in six of the twelve amino acid physiochemical properties that determine protein compressibility. This suggests a common evolutionary mechanism to reduce the adiabatic compressibility of opsin proteins. Intriguingly, the sites under selection are on the proteins' outer faces at locations known to be involved in opsin-opsin dimer interactions.

Magnetic Control of the Light Reflection Anisotropy in a Biogenic Guanine Microcrystal Platelet.

Bioinspired but static optical devices such as lenses, retarders, and reflectors have had a significant impact on the designs of many man-made optical technologies. However, while numerous adaptive and flexible optical mechanisms are found throughout the animal kingdom, highly desirable biomimetic copies of these remarkable smart systems remain, in many cases, a distant dream. Many aquatic animals have evolved highly efficient reflectors based on multilayer stacks of the crystallized nucleic acid base guanine. With exceptional levels of spectral and intensity control, these reflectors represent an interesting design pathway towards controllable micromirror structures. Here we show that individual guanine crystals, with dimensions of 5 µm × 20 µm × 70 nm, can be magnetically controlled to act as individual micromirrors. By applying magnetic fields of 500 mT, the reflectivity of these crystals can be switched off and on for the change in reflectivity. Overall, the use of guanine represents a novel design scheme for a highly efficient and controllable synthetic organic micromirror array.

Perceiving polarization with the naked eye: characterization of human polarization sensitivity.

Like many animals, humans are sensitive to the polarization of light. We can detect the angle of polarization using an entoptic phenomenon called Haidinger's brushes, which is mediated by dichroic carotenoids in the macula lutea. While previous studies have characterized the spectral sensitivity of Haidinger's brushes, other aspects remain unexplored. We developed a novel methodology for presenting gratings in polarization-only contrast at varying degrees of polarization in order to measure the lower limits of human polarized light detection. Participants were, on average, able to perform the task down to a threshold of 56%, with some able to go as low as 23%. This makes humans the most sensitive vertebrate tested to date. Additionally, we quantified a nonlinear relationship between presented and perceived polarization angle when an observer is presented with a rotatable polarized light field. This result confirms a previous theoretical prediction of how uniaxial corneal birefringence impacts the perception of Haidinger's brushes. The rotational dynamics of Haidinger's brushes were then used to calculate corneal retardance.We suggest that psychophysical experiments, based upon the perception of polarized light, are amenable to the production of affordable technologies for self-assessment and longitudinal monitoring of visual dysfunctions such as age-related macular degeneration.