Polarization vision in terrestrial hermit crabs.

Polarization vision is used by a wide range of animals for navigating, orienting, and detecting objects or areas of interest. Shallow marine and semi-terrestrial crustaceans are particularly well known for their abilities to detect predator-like or conspecific-like objects based on their polarization properties. On land, some terrestrial invertebrates use polarization vision for detecting suitable habitats, oviposition sites or conspecifics, but examples of threat detection in the polarization domain are less well known. To test whether this also applies to crustaceans that have evolved to occupy terrestrial habitats, we determined the sensitivity of two species of land and one species of marine hermit crab to predator-like visual stimuli varying in the degree of polarization. All three species showed an ability to detect these cues based on polarization contrasts alone. One terrestrial species, Coenobita rugosus, showed an increased sensitivity to objects with a higher degree of polarization than the background. This is the inverse of most animals studied to date, suggesting that the ecological drivers for polarization vision may be different in the terrestrial environment.

Why don't horseflies land on zebras?

Stripes deter horseflies (tabanids) from landing on zebras and, while several mechanisms have been proposed, these hypotheses have yet to be tested satisfactorily. Here, we investigated three possible visual mechanisms that could impede successful tabanid landings (aliasing, contrast and polarization) but additionally explored pattern element size employing video footage of horseflies around differently patterned coats placed on domestic horses. We found that horseflies are averse to landing on highly but not on lightly contrasting stripes printed on horse coats. We could find no evidence for horseflies being attracted to coats that better reflected polarized light. Horseflies were somewhat less attracted to regular than to irregular check patterns, but this effect was not large enough to support the hypothesis of disrupting optic flow through aliasing. More likely it is due to attraction towards larger dark patches present in the irregular check patterns, an idea bolstered by comparing landings to the size of dark patterns present on the different coats. Our working hypothesis for the principal anti-parasite features of zebra pelage are that their stripes are sharply outlined and thin because these features specifically eliminate the occurrence of large monochrome dark patches that are highly attractive to horseflies at close distances.

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.

Fiddler crab electroretinograms reveal vast circadian shifts in visual sensitivity and temporal summation in dim light.

Many animals with compound eyes undergo major optical changes to adjust visual sensitivity from day to night, often under control of a circadian clock. In fiddler crabs, this presents most conspicuously in the huge volume increase of photopigment-packed rhabdoms and the widening of crystalline cone apertures at night. These changes are hypothesised to adjust the light flux to the photoreceptors and to alter optical sensitivity as the eye moves between light- and dark-adapted states. Here, we compared optical sensitivity in fiddler crab (Gelasimus dampieri) eyes during daytime and night via three electroretinogram (ERG) experiments performed on light- and dark-adapted crabs. (1) Light intensity required to elicit a threshold ERG response varied over six orders of magnitude, allowing more sensitive vision for discriminating small contrasts in dim light after dusk. During daytime, the eyes remained relatively insensitive, which would allow effective vision on bright mudflats, even after prolonged dark adaptation. (2) Flicker fusion frequency (FFF) experiments indicated that temporal summation is employed in dim light to increase light-gathering integration times and enhance visual sensitivity during both night and day. (3) ERG responses to flickering lights during 60 min of dark adaptation increased at a faster rate and to a greater extent after sunset compared with daytime. However, even brief, dim and intermittent light exposure strongly disrupted dark-adaptation processes. Together, these findings demonstrate effective light adaptation to optimise vision over the large range of light intensities that these animals experience.

Polarization contrasts and their effect on the gaze stabilization of crustaceans.

Many animals go to great lengths to stabilize their eyes relative to the visual scene and do so to enhance the localization of moving objects and to functionally partition the visual system relative to the outside world. An important cue that is used to control these stabilization movements is contrast within the visual surround. Previous studies on insects, spiders and fish have shown that gaze stabilization is achromatic ('colour blind'), meaning that chromatic contrast alone (in the absence of apparent intensity contrasts) does not contribute to gaze stabilization. Following the assumption that polarization vision is analogous in many ways to colour vision, the present study shows that five different crustacean species do not use the polarization of light alone for gaze stabilization, despite being able to use this modality for detecting predator-like objects. This work therefore suggests that the gaze stabilization in many crustaceans cannot be elicited by the polarization of light alone.

Polarization contrasts and their effect on the gaze stabilization of crustaceans.

Many animals go to great lengths to stabilize their eyes relative to the visual scene and do so to enhance the localization of moving objects and to functionally partition the visual system relative to the outside world. An important cue that is used to control these stabilization movements is contrast within the visual surround. Previous studies on insects, spiders and fish have shown that gaze stabilization is achromatic ('colour blind'), meaning that chromatic contrast alone (in the absence of apparent intensity contrasts) does not contribute to gaze stabilization. Following the assumption that polarization vision is analogous in many ways to colour vision, the present study shows that five different crustacean species do not use the polarization of light alone for gaze stabilization, despite being able to use this modality for detecting predator-like objects. This work therefore suggests that the gaze stabilization in many crustaceans cannot be elicited by the polarization of light alone.

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.

Zebra stripes, tabanid biting flies and the aperture effect.

Of all hypotheses advanced for why zebras have stripes, avoidance of biting fly attack receives by far the most support, yet the mechanisms by which stripes thwart landings are not yet understood. A logical and popular hypothesis is that stripes interfere with optic flow patterns needed by flying insects to execute controlled landings. This could occur through disrupting the radial symmetry of optic flow via the aperture effect (i.e. generation of false motion cues by straight edges), or through spatio-temporal aliasing (i.e. misregistration of repeated features) of evenly spaced stripes. By recording and reconstructing tabanid fly behaviour around horses wearing differently patterned rugs, we could tease out these hypotheses using realistic target stimuli. We found that flies avoided landing on, flew faster near, and did not approach as close to striped and checked rugs compared to grey. Our observations that flies avoided checked patterns in a similar way to stripes refutes the hypothesis that stripes disrupt optic flow via the aperture effect, which critically demands parallel striped patterns. Our data narrow the menu of fly-equid visual interactions that form the basis for the extraordinary colouration of zebras.

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.

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.

Toxicity and taste: unequal chemical defences in a mimicry ring.

Mimicry of warning signals is common, and can be mutualistic when mimetic species harbour equal levels of defence (Müllerian), or parasitic when mimics are undefended but still gain protection from their resemblance to the model (Batesian). However, whether chemically defended mimics should be similar in terms of toxicity (i.e. causing damage to the consumer) and/or unpalatability (i.e. distasteful to consumer) is unclear and in many studies remains undifferentiated. In this study, we investigated the evolution of visual signals and chemical defences in a putative mimicry ring of nudibranch molluscs. First, we demonstrated that the appearance of a group of red spotted nudibranchs molluscs was similar from the perspective of potential fish predators using visual modelling and pattern analysis. Second, using phylogenetic reconstruction, we demonstrated that this colour pattern has evolved multiple times in distantly related individuals. Third, we showed that these nudibranchs contained different chemical profiles used for defensive purposes. Finally, we demonstrated that although levels of distastefulness towards Palaemon shrimp remained relatively constant between species, toxicity levels towards brine shrimp varied significantly. We highlight the need to disentangle toxicity and taste when considering chemical defences in aposematic and mimetic species, and discuss the implications for aposematic and mimicry signal evolution.

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).

Stabilizing selection on individual pattern elements of aposematic signals.

Warning signal variation is ubiquitous but paradoxical: low variability should aid recognition and learning by predators. However, spatial variability in the direction and strength of selection for individual elements of the warning signal may allow phenotypic variation for some components, but not others. Variation in selection may occur if predators only learn particular colour pattern components rather than the entire signal. Here, we used a nudibranch mollusc, Goniobranchus splendidus, which exhibits a conspicuous red spot/white body/yellow rim colour pattern, to test this hypothesis. We first demonstrated that secondary metabolites stored within the nudibranch were unpalatable to a marine organism. Using pattern analysis, we demonstrated that the yellow rim remained invariable within and between populations; however, red spots varied significantly in both colour and pattern. In behavioural experiments, a potential fish predator, Rhinecanthus aculeatus, used the presence of the yellow rims to recognize and avoid warning signals. Yellow rims remained stable in the presence of high genetic divergence among populations. We therefore suggest that how predators learn warning signals may cause stabilizing selection on individual colour pattern elements, and will thus have important implications on the evolution of warning signals.

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.

Disruptive colouration in reef fish: does matching the background reduce predation risk?

Animals use disruptive colouration to prevent detection or recognition by potential predators or prey. Highly contrasting elements within colour patterns, including vertical or horizontal bars, are thought to be effective at distracting attention away from body form and reducing detection likelihood. However, it is unclear whether such patterns need to be a good match to the spatial characteristics of the background to gain cryptic benefits. We tested this hypothesis using the iconic vertically barred humbug damselfish, Dascyllus aruanus (Linneaus 1758), a small reef fish that lives among the finger-like projections of branching coral colonies. Using behavioural experiments, we demonstrated that the spatial frequency of the humbug pattern does not need to exactly match the spatial frequency of the coral background to reduce the likelihood of being attacked by two typical reef fish predators: slingjaw wrasse, Epibulus insidiator (Pallas 1770), and coral trout, Plectropomus leopardus (Lacépède 1802). Indeed, backgrounds with a slightly higher spatial frequency than the humbug body pattern provided more protection from predation than well-matched backgrounds. These results were consistent for both predator species, despite differences in their mode of foraging and visual acuity, which was measured using anatomical techniques. We also showed that a slight mismatch in the orientation of the vertical bars did not increase the chances of detection. However, the likelihood of attack did increase significantly when the bars were perpendicular to the background. Our results provide evidence that fish camouflage is more complex than it initially appears, with likely many factors influencing the detection likelihood of prey by relevant predators.

Polarization distance: a framework for modelling object detection by polarization vision systems.

The discrimination of polarized light is widespread in the natural world. Its use for specific, large-field tasks, such as navigation and the detection of water bodies, has been well documented. Some species of cephalopod and crustacean have polarization receptors distributed across the whole visual field and are thought to use polarized light cues for object detection. Both object-based polarization vision systems and large field detectors rely, at least initially, on an orthogonal, two-channel receptor organization. This may increase to three-directional analysis at subsequent interneuronal levels. In object-based and some of the large-field tasks, the dominant e-vector detection axes are often aligned (through eye, head and body stabilization mechanisms) horizontally and vertically relative to the outside world. We develop Bernard and Wehner's 1977 model of polarization receptor dynamics to apply it to the detection and discrimination of polarized objects against differently polarized backgrounds. We propose a measure of 'polarization distance' (roughly analogous to 'colour distance') for estimating the discriminability of objects in polarized light, and conclude that horizontal/vertical arrays are optimally designed for detecting differences in the degree, and not the e-vector axis, of polarized light under natural conditions.

Null point of discrimination in crustacean polarisation vision.

The polarisation of light is used by many species of cephalopods and crustaceans to discriminate objects or to communicate. Most visual systems with this ability, such as that of the fiddler crab, include receptors with photopigments that are oriented horizontally and vertically relative to the outside world. Photoreceptors in such an orthogonal array are maximally sensitive to polarised light with the same fixed e-vector orientation. Using opponent neural connections, this two-channel system may produce a single value of polarisation contrast and, consequently, it may suffer from null points of discrimination. Stomatopod crustaceans use a different system for polarisation vision, comprising at least four types of polarisation-sensitive photoreceptor arranged at 0, 45, 90 and 135 deg relative to each other, in conjunction with extensive rotational eye movements. This anatomical arrangement should not suffer from equivalent null points of discrimination. To test whether these two systems were vulnerable to null points, we presented the fiddler crab Uca heteropleura and the stomatopod Haptosquilla trispinosa with polarised looming stimuli on a modified LCD monitor. The fiddler crab was less sensitive to differences in the degree of polarised light when the e-vector was at -45 deg than when the e-vector was horizontal. In comparison, stomatopods showed no difference in sensitivity between the two stimulus types. The results suggest that fiddler crabs suffer from a null point of sensitivity, while stomatopods do not.