Cuttlefish adopt disruptive camouflage under dynamic lighting.

Many animals avoid detection or recognition using camouflage tailored to the visual features of their environment.1,2,3 The appearance of those features, however, can be affected by fluctuations in local lighting conditions, making them appear different over time.4,5 Despite dynamic lighting being common in many terrestrial and aquatic environments, it is unknown whether dynamic lighting influences the camouflage patterns that animals adopt. Here, we test whether a common form of underwater dynamic lighting, consisting of moving light bands that can create local fluctuations in the intensity of light ("water caustics"), affects the camouflage of cuttlefish (Sepia officinalis). Owing to specialized pigment cells (chromatophores) in the skin,6 these cephalopod mollusks can dynamically adjust their body patterns in response to features of their visual scene.7,8,9 Although cuttlefish resting on plain or patterned backgrounds usually expressed uniform or disruptive body patterns, respectively,10,11,12 exposure to these backgrounds in dynamic lighting induced stronger disruptive patterns regardless of the background type. Dynamic lighting increased the maximum contrast levels within scenes, and these maximum contrast levels were associated with the degree of cuttlefish disruptive camouflage. This adoption of disruptive camouflage in dynamically lit scenes may be adaptive, reducing the likelihood of detection, or alternatively, it could represent a constraint on visual processing.

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.

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.

Increased water temperature and turbidity act independently to alter social behavior in guppies (Poecilia reticulata).

Changes in environmental conditions can shift the costs and benefits of aggregation or interfere with the sensory perception of near neighbors. This affects group cohesion with potential impacts on the benefits of collective behavior such as reduced predation risk. Organisms are rarely exposed to one stressor in isolation, yet there are only a few studies exploring the interactions between multiple stressors and their effects on social behavior. Here, we tested the effects of increased water temperature and turbidity on refuge use and three measures of aggregation in guppies (Poecilia reticulata), increasing temperature and turbidity in isolation or in combination. When stressors were elevated in isolation, the distribution of fish within the arena as measured by the index of dispersion became more aggregated at higher temperatures but less aggregated when turbidity was increased. Another measure of cohesion at the global scale, the mean inter-individual distance, also indicated that fish were less aggregated in turbid water. This is likely due to turbidity acting as a visual constraint, as there was no evidence of a change in risk perception as refuge use was not affected by turbidity. Fish decreased refuge use and were closer to their nearest neighbor at higher temperatures. However, the nearest neighbor distance was not affected by turbidity, suggesting that local-scale interactions can be robust to the moderate increase in turbidity used here (5 NTU) compared with other studies that show a decline in shoal cohesion at higher turbidity (>100 NTU). We did not observe any significant interaction terms between the two stressors, indicating no synergistic or antagonistic effects. Our study suggests that the effects of environmental stressors on social behavior may be unpredictable and dependent on the metric used to measure cohesion, highlighting the need for mechanistic studies to link behavior to the physiology and sensory effects of environmental stressors.

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.

Polarization vision mitigates visual noise from flickering light underwater.

In shallow water, downwelling light is refracted from surface waves onto the substrate creating bands of light that fluctuate in both time and space, known as caustics. This dynamic illumination can be a visual hindrance for animals in shallow underwater environments. Animals in such habitats may have evolved to use polarization vision for discriminating objects while ignoring the variations in illumination caused by caustics. To explore this possibility, crabs (Carcinus maenas) and cuttlefish (Sepia officinalis), both of which have polarization vision, were presented with moving stimuli overlaid with caustics. Dynamic caustics inhibited the detection of an intensity-based stimulus but not when these stimuli were polarized. This study is the first to demonstrate that polarization vision reduces the negative impacts that dynamic illumination can have on visual perception.

Cuttlefish camouflage: Blending in by matching background features.

Cuttlefish are masters of camouflage and show a remarkable ability to hide in plain sight. A new study reveals how these animals translate visual information about their surroundings into effective camouflage patterns.

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.

Adding colour-realistic video images to audio playbacks increases stimulus engagement but does not enhance vocal learning in zebra finches.

Bird song and human speech are learned early in life and for both cases engagement with live social tutors generally leads to better learning outcomes than passive audio-only exposure. Real-world tutor-tutee relations are normally not uni- but multimodal and observations suggest that visual cues related to sound production might enhance vocal learning. We tested this hypothesis by pairing appropriate, colour-realistic, high frame-rate videos of a singing adult male zebra finch tutor with song playbacks and presenting these stimuli to juvenile zebra finches (Taeniopygia guttata). Juveniles exposed to song playbacks combined with video presentation of a singing bird approached the stimulus more often and spent more time close to it than juveniles exposed to audio playback only or audio playback combined with pixelated and time-reversed videos. However, higher engagement with the realistic audio-visual stimuli was not predictive of better song learning. Thus, although multimodality increased stimulus engagement and biologically relevant video content was more salient than colour and movement equivalent videos, the higher engagement with the realistic audio-visual stimuli did not lead to enhanced vocal learning. Whether the lack of three-dimensionality of a video tutor and/or the lack of meaningful social interaction make them less suitable for facilitating song learning than audio-visual exposure to a live tutor remains to be tested.

A shark's eye view: testing the 'mistaken identity theory' behind shark bites on humans.

Shark bites on humans are rare but are sufficiently frequent to generate substantial public concern, which typically leads to measures to reduce their frequency. Unfortunately, we understand little about why sharks bite humans. One theory for bites occurring at the surface, e.g. on surfers, is that of mistaken identity, whereby sharks mistake humans for their typical prey (pinnipeds in the case of white sharks). This study tests the mistaken identity theory by comparing video footage of pinnipeds, humans swimming and humans paddling surfboards, from the perspective of a white shark viewing these objects from below. Videos were processed to reflect how a shark's retina would detect the visual motion and shape cues. Motion cues of humans swimming, humans paddling surfboards and pinnipeds swimming did not differ significantly. The shape of paddled surfboards and human swimmers was also similar to that of pinnipeds with their flippers abducted. The difference in shape between pinnipeds with abducted versus adducted flippers was bigger than between pinnipeds with flippers abducted and surfboards or human swimmers. From the perspective of a white shark, therefore, neither visual motion nor shape cues allow an unequivocal visual distinction between pinnipeds and humans, supporting the mistaken identity theory behind some bites.

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.

Light adaptation mechanisms in the eye of the fiddler crab Afruca tangeri.

A great diversity of adaptations is found among animals with compound eyes and even closely related taxa can show variation in their light-adaptation strategies. A prime example of a visual system evolved to function in specific light environments is the fiddler crab, used widely as a model to research aspects of crustacean vision and neural pathways. However, questions remain regarding how their eyes respond to the changes in brightness spanning many orders of magnitude, associated with their habitat and ecology. The fiddler crab Afruca tangeri forages at low tide on tropical and semi-tropical mudflats, under bright sunlight and on moonless nights, suggesting that their eyes undergo effective light adaptation. Using synchrotron X-ray tomography, light and transmission electron microscopy and in vivo ophthalmoscopy, we describe the ultrastructural changes in the eye between day and night. Dark adaptation at dusk triggered extensive widening of the rhabdoms and crystalline cone tips. This doubled the ommatidial acceptance angles and increased microvillar surface area for light capture in the rhabdom, theoretically boosting optical sensitivity 7.4 times. During daytime, only partial dark-adaptation was achieved and rhabdoms remained narrow, indicating strong circadian control on the process. Bright light did not evoke changes in screening pigment distributions, suggesting a structural inability to adapt rapidly to the light level fluctuations frequently experienced when entering their burrow to escape predators. This should enable fiddler crabs to shelter for several minutes without undergoing significant dark-adaptation, their vision remaining effectively adapted for predator detection when surfacing again in bright light.

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.

Parallel processing of polarization and intensity information in fiddler crab vision.

Many crustaceans are sensitive to the polarization of light and use this information for object-based visually guided behaviors. For these tasks, it is unknown whether polarization and intensity information are integrated into a single-contrast channel, whereby polarization directly contributes to perceived intensity, or whether they are processed separately and in parallel. Using a novel type of visual display that allowed polarization and intensity properties of visual stimuli to be adjusted independently and simultaneously, we conducted behavioral experiments with fiddler crabs to test which of these two models of visual processing occurs. We found that, for a loom detection task, fiddler crabs process polarization and intensity information independently and in parallel. The crab's response depended on whichever contrast was the most salient. By contributing independent measures of visual contrast, polarization and intensity provide a greater range of detectable contrast information for the receiver, increasing the chance of detecting a potential threat.

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.

Benefits of zebra stripes: Behaviour of tabanid flies around zebras and horses.

Averting attack by biting flies is increasingly regarded as the evolutionary driver of zebra stripes, although the precise mechanism by which stripes ameliorate attack by ectoparasites is unknown. We examined the behaviour of tabanids (horse flies) in the vicinity of captive plains zebras and uniformly coloured domestic horses living on a horse farm in Britain. Observations showed that fewer tabanids landed on zebras than on horses per unit time, although rates of tabanid circling around or briefly touching zebra and horse pelage did not differ. In an experiment in which horses sequentially wore cloth coats of different colours, those wearing a striped pattern suffered far lower rates of tabanid touching and landing on coats than the same horses wearing black or white, yet there were no differences in attack rates to their naked heads. In separate, detailed video analyses, tabanids approached zebras faster and failed to decelerate before contacting zebras, and proportionately more tabanids simply touched rather than landed on zebra pelage in comparison to horses. Taken together, these findings indicate that, up close, striped surfaces prevented flies from making a controlled landing but did not influence tabanid behaviour at a distance. To counteract flies, zebras swished their tails and ran away from fly nuisance whereas horses showed higher rates of skin twitching. As a consequence of zebras' striping, very few tabanids successfully landed on zebras and, as a result of zebras' changeable behaviour, few stayed a long time, or probed for blood.

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.