Through an animal's eye: the implications of diverse sensory systems in scientific experimentation.

'Accounting for the sensory abilities of animals is critical in experimental design.' No researcher would disagree with this statement, yet it is often the case that we inadvertently fall for anthropocentric biases and use ourselves as the reference point. This paper discusses the risks of adopting an anthropocentric view when working with non-human animals, and the unintended consequences this has on our experimental designs and results. To this aim, we provide general examples of anthropocentric bias from different fields of animal research, with a particular focus on animal cognition and behaviour, and lay out the potential consequences of adopting a human-based perspective. Knowledge of the sensory abilities, both in terms of similarities to humans and peculiarities of the investigated species, is crucial to ensure solid conclusions. A more careful consideration of the diverse sensory systems of animals would improve many scientific fields and enhance animal welfare in the laboratory.

Through Hawks' Eyes: Synthetically Reconstructing the Visual Field of a Bird in Flight.

Birds of prey rely on vision to execute flight manoeuvres that are key to their survival, such as intercepting fast-moving targets or navigating through clutter. A better understanding of the role played by vision during these manoeuvres is not only relevant within the field of animal behaviour, but could also have applications for autonomous drones. In this paper, we present a novel method that uses computer vision tools to analyse the role of active vision in bird flight, and demonstrate its use to answer behavioural questions. Combining motion capture data from Harris' hawks with a hybrid 3D model of the environment, we render RGB images, semantic maps, depth information and optic flow outputs that characterise the visual experience of the bird in flight. In contrast with previous approaches, our method allows us to consider different camera models and alternative gaze strategies for the purposes of hypothesis testing, allows us to consider visual input over the complete visual field of the bird, and is not limited by the technical specifications and performance of a head-mounted camera light enough to attach to a bird's head in flight. We present pilot data from three sample flights: a pursuit flight, in which a hawk intercepts a moving target, and two obstacle avoidance flights. With this approach, we provide a reproducible method that facilitates the collection of large volumes of data across many individuals, opening up new avenues for data-driven models of animal behaviour. Supplementary Information: The online version contains supplementary material available at 10.1007/s11263-022-01733-2.

Semper's cells in the insect compound eye: Insights into ocular form and function.

The arthropod compound eye represents one of two major eye types in the animal kingdom and has served as an essential experimental paradigm for defining fundamental mechanisms underlying sensory organ formation, function, and maintenance. One of the most distinguishing features of the compound eye is the highly regular array of lens facets that define individual eye (ommatidial) units. These lens facets are produced by a deeply conserved quartet of cuticle-secreting cells, called Semper cells (SCs). Also widely known as cone cells, SCs were originally identified for their secretion of the dioptric system, i.e. the corneal lens and underlying crystalline cones. Additionally, SCs are now known to execute a diversity of patterning and glial functions in compound eye development and maintenance. Here, we present an integrated account of our current knowledge of SC multifunctionality in the Drosophila compound eye, highlighting emerging gene regulatory modules that may drive the diverse roles for these cells. Drawing comparisons with other deeply conserved retinal glia in the vertebrate single lens eye, this discussion speaks to glial cell origins and opens new avenues for understanding sensory system support programs.

Rapid Body Color Change Provides Lizards with Facultative Crypsis in the Eyes of Their Avian Predators.

AbstractColor change serves many antipredator functions and may allow animals to better match environments or disrupt outlines to prevent detection. Rapid color change could potentially provide camouflage to animals that frequently move among microhabitats. Determining the adaptiveness of whole-animal rapid color changes in natural habitats with respect to predator visual systems would greatly broaden our fundamental understanding of the evolution of rapid color change. We tested whether whole-body color change provides water anoles (Anolis aquaticus) with camouflage against avian predators and whether these rapid changes allow them to shift between environment matching and edge disruption. We manipulated A. aquaticus placement in natural microhabitats and used digital image analysis to quantify color matching, pattern matching, and edge disruption produced by microhabitat-induced color change. Color change reduced lizard detectability to predators in microhabitat-specific ways. Environment matching was favored when lizards were in solid-colored microhabitats, regardless of exposure to predators. Edge disruption was instead induced by high exposure and varied by body region. We provide the first evidence that rapid color change permits a tetrapod to flexibly employ the most optimal camouflaging strategy by form (e.g., color matching vs. edge disruption) to minimize detection in the eyes of its predators.

Cuttlefish see shape from shading, fine-tuning coloration in response to pictorial depth cues and directional illumination.

Humans use shading as a cue to three-dimensional form by combining low-level information about light intensity with high-level knowledge about objects and the environment. Here, we examine how cuttlefish Sepia officinalis respond to light and shadow to shade the white square (WS) feature in their body pattern. Cuttlefish display the WS in the presence of pebble-like objects, and they can shade it to render the appearance of surface curvature to a human observer, which might benefit camouflage. Here we test how they colour the WS on visual backgrounds containing two-dimensional circular stimuli, some of which were shaded to suggest surface curvature, whereas others were uniformly coloured or divided into dark and light semicircles. WS shading, measured by lateral asymmetry, was greatest when the animal rested on a background of shaded circles and three-dimensional hemispheres, and less on plain white circles or black/white semicircles. In addition, shading was enhanced when light fell from the lighter side of the shaded stimulus, as expected for real convex surfaces. Thus, the cuttlefish acts as if it perceives surface curvature from shading, and takes account of the direction of illumination. However, the direction of WS shading is insensitive to the directions of background shading and illumination; instead the cuttlefish tend to turn to face the light source.

Angular dependence of polarisation contrast sensitivity in octopus.

Cephalopod photoreceptors are polarisation-sensitive, giving them an ability to discriminate between lights of different angle and degree of polarisation. While colour vision is achieved by comparison of signals of photoreceptors tuned to different parts of light spectra, polarisation vision is achieved by comparison of signals of photoreceptors tuned to different orientations of e-vector. Therefore, from a theoretical point of view, polarisation vision is similar to colour vision. In particular, detection of polarised light against an unpolarised background is analogous to detection of chromatic light against grey. The dependence of polarisation contrast sensitivity on the angle of polarisation can be theoretically predicted using a receptor noise limited model in much the same way as it has been done for predicting the shape of the increment threshold spectral sensitivity in animals with colour vision. Here we report angular dependence of polarisation contrast sensitivity in octopus (O. tetricus, Gould 1852) and compare the theoretical predictions of polarisation contrast with the experimental results. Polarisation gratings were generated using LCD screens with removed polarisers and the orientation of polarisation was changed by rotating the screen. Reaction to the stimulus was recorded using a fixation reflex. We show that, in agreement with the theoretical predictions, the maximum contrast sensitivity is achieved at horizontal and vertical orientations of polarisation. Our results demonstrate that the dependence of polarisation contrast sensitivity on the angle of polarisation can be analysed in the same way as the dependence of colour thresholds on wavelength of monochromatic light added to a grey background.

Eye movements in man and other animals.

Good vision requires a near stationary image if motion blur is to be avoided. All animals with good eyesight (principally the vertebrates, arthropods and cephalopod molluscs) have adopted a very similar strategy for achieving this: fixations in which gaze is kept still, with saccades to change gaze direction as fast as possible. In all these groups the stability of fixations is maintained by reflexes that oppose the effects of head or body movement (the vestibulo-ocular reflex in vertebrates), and that oppose drift of the image on the retina (optokinetic and optomotor reflexes). A small number of species of molluscs and arthropods have adopted a different strategy: allowing the retinas to scan across the surroundings to acquire information. The retinas in these animals are all linear structures a few receptors wide, and scan at right angles to their long dimension. The speed of scanning varies with retinal resolution, ensuring that scan speed does not produce deleterious blur.

I see your false colours: how artificial stimuli appear to different animal viewers.

The use of artificially coloured stimuli, especially to test hypotheses about sexual selection and anti-predator defence, has been common in behavioural ecology since the pioneering work of Tinbergen. To investigate the effects of colour on animal behaviour, many researchers use paints, markers and dyes to modify existing colours or to add colour to synthetic models. Because colour perception varies widely across species, it is critical to account for the signal receiver's vision when performing colour manipulations. To explore this, we applied 26 typical coloration products to different types of avian feathers. Next, we measured the artificially coloured feathers using two complementary techniques-spectrophotometry and digital ultraviolet--visible photography-and modelled their appearance to mammalian dichromats (ferret, dog), trichromats (honeybee, human) and avian tetrachromats (hummingbird, blue tit). Overall, artificial colours can have dramatic and sometimes unexpected effects on the reflectance properties of feathers, often differing based on feather type. The degree to which an artificial colour differs from the original colour greatly depends on an animal's visual system. 'White' paint to a human is not 'white' to a honeybee or blue tit. Based on our analysis, we offer practical guidelines for reducing the risk of introducing unintended effects when using artificial colours in behavioural experiments.

A generalized equation for the calculation of receptor noise limited colour distances in n-chromatic visual systems.

Researchers must assess similarities and differences in colour from an animal's eye view when investigating hypotheses in ecology, evolution and behaviour. Nervous systems generate colour perceptions by comparing the responses of different spectral classes of photoreceptor through colour opponent mechanisms, and the performance of these mechanisms is limited by photoreceptor noise. Accordingly, the receptor noise limited (RNL) colour distance model of Vorobyev and Osorio (Vorobyev & Osorio 1998 Proc. R. Soc. Lond. B265, 351-358 (doi:10.1098/rspb.1998.0302)) generates predictions about the discriminability of colours that agree with behavioural data, and consequently it has found wide application in studies of animal colour vision. Vorobyev and Osorio (1998) provide equations to calculate RNL colour distances for animals with di-, tri- and tetrachromatic vision, which is adequate for many species. However, researchers may sometimes wish to compute RNL colour distances for potentially more complex colour visual systems. Thus, we derive a simple, single formula for the computation of RNL distance between two measurements of colour, equivalent to the published di-, tri- and tetrachromatic equations of Vorobyev and Osorio (1998), and valid for colour visual systems with any number of types of noisy photoreceptors. This formula will allow the easy application of this important colour visual model across the fields of ecology, evolution and behaviour.

Nest covering in plovers: How modifying the visual environment influences egg camouflage.

Camouflage is one of the most widespread antipredator defences, and its mechanistic basis has attracted considerable interest in recent years. The effectiveness of camouflage depends on the interaction between an animal's appearance and its background. Concealment can therefore be improved by changes to an animal's own appearance, by behaviorally selecting an optimal background, or by modifying the background to better match the animal's own appearance. Research to date has largely focussed on the first of these mechanisms, whereas there has been little work on the second and almost none on the third. Even though a number of animal species may potentially modify their environment to improve individual-specific camouflage, this has rarely if ever been quantitatively investigated, or its adaptive value tested. Kittlitz's plovers (Charadrius pecuarius) use material (stones and vegetation) to cover their nests when predators approach, providing concealment that is independent of the inflexible appearance of the adult or eggs, and that can be adjusted to suit the local surrounding background. We used digital imaging and predator vision modeling to investigate the camouflage properties of covered nests, and whether their camouflage affected their survival. The plovers' nest-covering materials were consistent with a trade-off between selecting materials that matched the color of the eggs, while resulting in poorer nest pattern and contrast matching to the nest surroundings. Alternatively, the systematic use of materials with high-contrast and small-pattern grain sizes could reflect a deliberate disruptive coloration strategy, whereby high-contrast material breaks up the telltale outline of the clutch. No camouflage variables predicted nest survival. Our study highlights the potential for camouflage to be enhanced by background modification. This provides a flexible system for modifying an animal's conspicuousness, to which the main limitation may be the available materials rather than the animal's appearance.