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.

Long-Wavelength Reflecting Filters Found in the Larval Retinas of One Mantis Shrimp Family (Nannosquillidae).

Both vertebrates and invertebrates commonly exploit photonic structures adjacent to their photoreceptors for visual benefits. For example, use of a reflecting structure (tapetum) behind the retina increases photon capture, enhancing vision in dim light [1-5]. Colored filters positioned lateral or distal to a photoreceptive unit may also be used to tune spectral sensitivity by selective transmission of wavelengths not absorbed or scattered by the filters [6-8]. Here we describe a new category of biological optical filter that acts simultaneously as both a transmissive spectral filter and narrowband reflector. Discovered in the larval eyes of only one family of mantis shrimp (stomatopod) crustaceans (Nannosquillidae), each crystalline structure bisects the photoreceptive rhabdom into two tiers and contains an ordered array of membrane-bound vesicles with sub-wavelength diameters of 153 ± 5 nm. Axial illumination of the intrarhabdomal structural reflector (ISR) in vivo produces a narrow band of yellow reflectance (mean peak reflectivity, 572 ± 18 nm). The ISR is similar to several synthetic devices, such as bandgap filters, laser mirrors, and (in particular) fiber Bragg gratings used in optical sensors for a wide range of industries. To our knowledge, the stomatopod larval ISR is the first example of a naturally occurring analog to these human-made devices. Considering what is known about these animals' visual ecology, we propose that these reflecting filters may help improve the detection of pelagic bioluminescence in shallow water at night. VIDEO ABSTRACT.

Using micro-CT techniques to explore the role of sex and hair in the functional morphology of bumblebee (Bombus terrestris) ocelli.

Many insects have triplets of camera type eyes, called ocelli, whose function remains unclear for most species. Here, we investigate the ocelli of the bumblebee, Bombus terrestris, using reconstructed 3D data from X-ray microtomography scans combined with computational ray-tracing simulations. This method enables us, not only to predict the visual fields of the ocelli, but to explore for the first time the effect that hair has on them as well as the difference between worker female and male ocelli. We find that bumblebee ocellar fields of view are directed forward and dorsally, incorporating the horizon as well as the sky. There is substantial binocular overlap between the median and lateral ocelli, but no overlap between the two lateral ocelli. Hairs in both workers and males occlude the ocellar field of view, mostly laterally in the worker median ocellus and dorsally in the lateral ocelli. There is little to no sexual dimorphism in the ocellar visual field, suggesting that in B. terrestris they confer no advantage to mating strategies. We compare our results with published observations for the visual fields of compound eyes in the same species as well as with the ocellar vision of other bee and insect species.

Hermit crabs (Pagurus bernhardus) use visual contrast in self-assessment of camouflage.

Animals can make use of camouflage to reduce the likelihood of visual detection or recognition and thus improve their chances of survival. Background matching, where body colouration is closely matched to the surrounding substrate, is one form of camouflage. Hermit crabs have the opportunity to choose their camouflage independently of body colouration as they inhabit empty gastropod shells, making them ideal to study their choice of camouflage. We used 3D-printed artificial shells of varying contrasts against a grey substrate to test whether hermit crabs prefer shells that they perceive as less conspicuous. Contrast-minimising shells were chosen for Weber contrasts stronger than -0.5. However, in looming experiments, animals responded to contrasts as weak as -0.2, indicating that while they can detect differences between shells and the background, they are only motivated to move into those shells when the alternatives contrast strongly. This suggests a trade-off between camouflage and vulnerability introduced by switching shells.

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).

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.

Selection of the intrinsic polarization properties of animal optical materials creates enhanced structural reflectivity and camouflage.

Many animals use structural coloration to create bright and conspicuous visual signals. Selection of the size and shape of the optical structures animals use defines both the colour and intensity of the light reflected. The material used to create these reflectors is also important; however, animals are restricted to a limited number of materials: commonly chitin, guanine and the protein, reflectin. In this work we highlight that a particular set of material properties can also be under selection in order to increase the optical functionality of structural reflectors. Specifically, polarization properties, such as birefringence (the difference between the refractive indices of a material) and chirality (which relates to molecular asymmetry) are both under selection to create enhanced structural reflectivity. We demonstrate that the structural coloration of the gold beetle Chrysina resplendens and silvery reflective sides of the Atlantic herring, Clupea harengus are two examples of this phenomenon. Importantly, these polarization properties are not selected to control the polarization of the reflected light as a source of visual information per se. Instead, by creating higher levels of reflectivity than are otherwise possible, such internal polarization properties improve intensity-matching camouflage.This article is part of the themed issue 'Animal coloration: production, perception, function and application'.

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.

Spatial summation improves bird color vision in low light intensities.

Color guides many important behaviors in birds. Previously we have shown that the intensity threshold for color discrimination in the chicken depends on the color contrast between stimuli and their brightness. The birds could discriminate larger color contrasts and brighter colors in lower light intensities. We suggested that chickens use spatial summation of cone signals to maintain color vision in low light levels. Here we tested this hypothesis by determining the intensity thresholds of color discrimination using similar stimuli, patterns of grey tiles of varying intensity interspersed with color tiles, adjusted for this specific aim. Chickens could discriminate stimuli with a larger single color tile, or with a larger proportion of small color tiles, in lower light intensities. This is in agreement with the hypothesis that spatial summation improves color discrimination in low light levels. There was no difference in the intensity threshold for discrimination of stimuli with a single 6×6mm color tile, stimuli with 30% colored tiles and stimuli in which color filled the whole pattern. This gives a first indication to the degree of spatial summation that can be performed. We compare this level of spatial summation to predictions from mathematical model calculations.

Losing focus: how lens position and viewing angle affect the function of multifocal lenses in fishes.

Light rays of different wavelengths are focused at different distances when they pass through a lens (longitudinal chromatic aberration [LCA]). For animals with color vision this can pose a serious problem, because in order to perceive a sharp image the rays must be focused at the shallow plane of the photoreceptor's outer segments in the retina. A variety of fish and tetrapods have been found to possess multifocal lenses, which correct for LCA by assigning concentric zones to correctly focus specific wavelengths. Each zone receives light from a specific beam entrance position (BEP) (the lateral distance between incoming light and the center of the lens). Any occlusion of incoming light at specific BEPs changes the composition of the wavelengths that are correctly focused on the retina. Here, we calculated the effect of lens position relative to the plane of the iris and light entering the eye at oblique angles on how much of the lens was involved in focusing the image on the retina (measured as the availability of BEPs). We used rotational photography of fish eyes and mathematical modeling to quantify the degree of lens occlusion. We found that, at most lens positions and viewing angles, there was a decrease of BEP availability and in some cases complete absence of some BEPs. Given the implications of these effects on image quality, we postulate that three morphological features (aphakic spaces, curvature of the iris, and intraretinal variability in spectral sensitivity) may, in part, be adaptations to mitigate the loss of spectral image quality in the periphery of the eyes of fishes.

Complementary shifts in photoreceptor spectral tuning unlock the full adaptive potential of ultraviolet vision in birds.

Color vision in birds is mediated by four types of cone photoreceptors whose maximal sensitivities (λmax) are evenly spaced across the light spectrum. In the course of avian evolution, the λmax of the most shortwave-sensitive cone, SWS1, has switched between violet (λmax > 400 nm) and ultraviolet (λmax < 380 nm) multiple times. This shift of the SWS1 opsin is accompanied by a corresponding short-wavelength shift in the spectrally adjacent SWS2 cone. Here, we show that SWS2 cone spectral tuning is mediated by modulating the ratio of two apocarotenoids, galloxanthin and 11',12'-dihydrogalloxanthin, which act as intracellular spectral filters in this cell type. We propose an enzymatic pathway that mediates the differential production of these apocarotenoids in the avian retina, and we use color vision modeling to demonstrate how correlated evolution of spectral tuning is necessary to achieve even sampling of the light spectrum and thereby maintain near-optimal color discrimination.

Quantitative studies of animal colour constancy: using the chicken as model.

Colour constancy is the capacity of visual systems to keep colour perception constant despite changes in the illumination spectrum. Colour constancy has been tested extensively in humans and has also been described in many animals. In humans, colour constancy is often studied quantitatively, but besides humans, this has only been done for the goldfish and the honeybee. In this study, we quantified colour constancy in the chicken by training the birds in a colour discrimination task and testing them in changed illumination spectra to find the largest illumination change in which they were able to remain colour-constant. We used the receptor noise limited model for animal colour vision to quantify the illumination changes, and found that colour constancy performance depended on the difference between the colours used in the discrimination task, the training procedure and the time the chickens were allowed to adapt to a new illumination before making a choice. We analysed literature data on goldfish and honeybee colour constancy with the same method and found that chickens can compensate for larger illumination changes than both. We suggest that future studies on colour constancy in non-human animals could use a similar approach to allow for comparison between species and populations.

A shape-anisotropic reflective polarizer in a stomatopod crustacean.

Many biophotonic structures have their spectral properties of reflection 'tuned' using the (zeroth-order) Bragg criteria for phase constructive interference. This is associated with a periodicity, or distribution of periodicities, parallel to the direction of illumination. The polarization properties of these reflections are, however, typically constrained by the dimensional symmetry and intrinsic dielectric properties of the biological materials. Here we report a linearly polarizing reflector in a stomatopod crustacean that consists of 6-8 layers of hollow, ovoid vesicles with principal axes of ~550 nm, ~250 nm and ~150 nm. The reflection of unpolarized normally incident light is blue/green in colour with maximum reflectance wavelength of 520 nm and a degree of polarization greater than 0.6 over most of the visible spectrum. We demonstrate that the polarizing reflection can be explained by a resonant coupling with the first-order, in-plane, Bragg harmonics. These harmonics are associated with a distribution of periodicities perpendicular to the direction of illumination, and, due to the shape-anisotropy of the vesicles, are different for each linear polarization mode. This control and tuning of the polarization of the reflection using shape-anisotropic hollow scatterers is unlike any optical structure previously described and could provide a new design pathway for polarization-tunability in man-made photonic devices.

Optics of cone photoreceptors in the chicken (Gallus gallus domesticus).

Vision is the primary sensory modality of birds, and its importance is evident in the sophistication of their visual systems. Coloured oil droplets in the cone photoreceptors represent an adaptation in the avian retina, acting as long-pass colour filters. However, we currently lack understanding of how the optical properties and morphology of component structures (e.g. oil droplet, mitochondrial ellipsoid and outer segment) of the cone photoreceptor influence the transmission of light into the outer segment and the ultimate effect they have on receptor sensitivity. In this study, we use data from microspectrophotometry, digital holographic microscopy and electron microscopy to inform electromagnetic models of avian cone photoreceptors to quantitatively investigate the integrated optical function of the cell. We find that pigmented oil droplets primarily function as spectral filters, not light collection devices, although the mitochondrial ellipsoid improves optical coupling between the inner segment and oil droplet. In contrast, unpigmented droplets found in violet-sensitive cones double sensitivity at its peak relative to other cone types. Oil droplets and ellipsoids both narrow the angular sensitivity of single cone photoreceptors, but not as strongly as those in human cones.