Interactions between color and gloss in iridescent camouflage.

Iridescence is a taxonomically widespread form of structural coloration that produces often intense hues that change with the angle of viewing. Its role as a signal has been investigated in multiple species, but recently, and counter-intuitively, it has been shown that it can function as camouflage. However, the property of iridescence that reduces detectability is, as yet, unclear. As viewing angle changes, iridescent objects change not only in hue but also in intensity, and many iridescent animals are also shiny or glossy; these "specular reflections," both from the target and background, have been implicated in crypsis. Here, we present a field experiment with natural avian predators that separate the relative contributions of color and gloss to the "survival" of iridescent and non-iridescent beetle-like targets. Consistent with previous research, we found that iridescent coloration, and high gloss of the leaves on which targets were placed, enhance survival. However, glossy targets survived less well than matt. We interpret the results in terms of signal-to-noise ratio: specular reflections from the background reduce detectability by increasing visual noise. While a specular reflection from the target attracts attention, a changeable color reduces the signal because, we suggest, normally, the color of an object is a stable feature for detection and identification.

Beetle iridescence induces an avoidance response in naïve avian predators.

It has recently been found that iridescence, a taxonomically widespread form of animal coloration defined by a change in hue with viewing angle, can act as a highly effective form of camouflage. However, little is known about whether iridescence can confer a survival benefit to prey postdetection and, if so, which optical properties of iridescent prey are important for this putative protective function. Here, we tested the effects of both iridescence and surface gloss (i.e. specular reflection) on the attack behaviour of prey-naïve avian predators. Using real and artificial jewel beetle, Sternocera aequisignata, wing cases, we found that iridescence provides initial protection against avian predation by significantly reducing the willingness to attack. Importantly, we found that the main factor explaining this aversion is iridescence, not multiple colours per se, with surface gloss also having an independent effect. Our results are important because they demonstrate that even when prey are presented up close and against a mismatching background, iridescence may confer a survival benefit by inducing hesitation or even, as sometimes observed, an aversion response in attacking birds. Furthermore, this means that even postdetection, prey do not necessarily need to have secondary defences such as sharp spines or toxins for iridescence to have a protective effect. Taken together, our results suggest that reduced avian predation could facilitate the initial evolution of iridescence in many species of insects and that it is the defining feature of iridescence, its colour changeability, that is important for this effect.

Background complexity can mitigate poor camouflage.

Avoiding detection through camouflage is often key to survival. However, an animal's appearance is not the only factor affecting conspicuousness: background complexity also alters detectability. This has been experimentally demonstrated for both artificially patterned backgrounds in the laboratory and natural backgrounds in the wild, but only for targets that already match the background well. Do habitats of high visual complexity provide concealment to even relatively poorly camouflaged animals? Using artificial prey which differed in their degrees of background matching to tree bark, we were able to determine their survival, under bird predation, with respect to the natural complexity of the background. The latter was quantified using low-level vision metrics of feature congestion (or 'visual clutter') adapted for bird vision. Higher background orientation clutter (edges with varying orientation) reduced the detectability of all but the poorest background-matching camouflaged treatments; higher background luminance clutter (varying achromatic lightness) reduced average mortality for all treatments. Our results suggest that poorer camouflage can be mitigated by more complex backgrounds, with implications for both camouflage evolution and habitat preferences.

Birds learn to avoid aposematic prey by using the appearance of host plants.

The conspicuous warning signal of aposematic animals is learned by their predators, and the resulting avoidance benefits both parties.1-4 Given evidence that birds can distinguish the profitability of prey from the environmental context in which they appear,5 aposematic insects' host plants might also provide an important cue to foraging predators.6 The aposematic cinnabar moth (Tyria jacobaeae) larva is a specialist on its ragwort (Senecio spp.) host plant,7 presenting a consistent environment with which it could be reliably associated. Additionally, ragwort's defensive toxins prevent non-specialist, profitable insects from feeding on it.8 Thus, avian predators may recognize cues from ragwort, most likely its conspicuous yellow flowers,9,10 and use this information to avoid cinnabars. To test this hypothesis, we exposed artificial cinnabar and non-signaling "caterpillar" targets to wild avian predation by presenting them on ragwort and non-toxic host plants. We also manipulated the presence or absence of ragwort flowers on hosts. In doing so, we show that both targets are better protected on the cinnabar's natural ragwort host and that birds use ragwort's distinctive yellow flowers as the cue to avoidance. Additionally, we found that naive predators do not make prey host foraging distinctions, indicating that this avoidance behavior is learned through experience. Our findings are among the first to suggest that a host plant's features act as an extended phenotype that signals the toxicity of the prey that live on it. This prey-host relationship may facilitate the initial evolution of toxicity in non-signaling prey, but also inhibit the evolution of aposematic signals themselves. VIDEO ABSTRACT.

The giant panda is cryptic.

The giant panda (Ailuropoda melanoleuca) is an iconic mammal, but the function of its black-and-white coloration is mysterious. Using photographs of giant pandas taken in the wild and state-of-the-art image analysis, we confirm the counterintuitive hypothesis that their coloration provides camouflage in their natural environment. The black fur blends into dark shades and tree trunks, whereas white fur matches foliage and snow when present, and intermediate pelage tones match rocks and ground. At longer viewing distances giant pandas show high edge disruption that breaks up their outline, and up close they rely more on background matching. The results are consistent across acuity-corrected canine, feline, and human vision models. We also show quantitatively that the species animal-to-background colour matching falls within the range of other species that are widely recognised as cryptic. Thus, their coloration is an adaptation to provide background matching in the visual environment in which they live and simultaneously to afford distance-dependent disruptive coloration, the latter of which constitutes the first computational evidence of this form of protective coloration in mammals.

Colour pattern variation forms local background matching camouflage in a leaf-mimicking toad.

Optimal camouflage can, in principle, be relatively easily achieved in simple, homogeneous, environments where backgrounds always have the same colour, brightness and patterning. Natural environments are, however, rarely homogenous, and species often find themselves viewed against varied backgrounds where the task of concealment is more challenging. One result of variable backgrounds is the evolution of intraspecific phenotypic variation which may either be generalized, with multiple similarly cryptic patterns, or specialized, with each discrete colour form maximizing concealment against a single component of the background. We investigated the role of phenotypic variation in a highly variable population of the Neotropical toad Rhinella margaritifera using visual modelling and a computer-based detection task. We found that phenotypic variation was not divided into discrete colour morphs, and all toads were well camouflaged against the forest floor. However, although the whole population may appear to consist of random samples from the background, the toads were a particularly close match to the leaf litter, suggesting that they masquerade as dead leaves, which are themselves variable. Furthermore, rather than each colour form being equally effective against a single background, each toad was specialized towards its own particular local surroundings, as suggested by a specialist strategy. Taken together, these data highlight the importance of background matching to a nominally masquerading species, as well as how habitat heterogeneity at multiple spatial scales may affect the evolution of camouflage and phenotypic variation.

The Camouflage Machine: Optimizing protective coloration using deep learning with genetic algorithms.

Evolutionary biologists frequently wish to measure the fitness of alternative phenotypes using behavioral experiments. However, many phenotypes are complex. One example is coloration: camouflage aims to make detection harder, while conspicuous signals (e.g., for warning or mate attraction) require the opposite. Identifying the hardest and easiest to find patterns is essential for understanding the evolutionary forces that shape protective coloration, but the parameter space of potential patterns (colored visual textures) is vast, limiting previous empirical studies to a narrow range of phenotypes. Here, we demonstrate how deep learning combined with genetic algorithms can be used to augment behavioral experiments, identifying both the best camouflage and the most conspicuous signal(s) from an arbitrarily vast array of patterns. To show the generality of our approach, we do so for both trichromatic (e.g., human) and dichromatic (e.g., typical mammalian) visual systems, in two different habitats. The patterns identified were validated using human participants; those identified as the best for camouflage were significantly harder to find than a tried-and-tested military design, while those identified as most conspicuous were significantly easier to find than other patterns. More generally, our method, dubbed the "Camouflage Machine," will be a useful tool for identifying the optimal phenotype in high dimensional state spaces.

Imperfect transparency and camouflage in glass frogs.

Camouflage patterns prevent detection and/or recognition by matching the background, disrupting edges, or mimicking particular background features. In variable habitats, however, a single pattern cannot match all available sites all of the time, and efficacy may therefore be reduced. Active color change provides an alternative where coloration can be altered to match local conditions, but again efficacy may be limited by the speed of change and range of patterns available. Transparency, on the other hand, creates high-fidelity camouflage that changes instantaneously to match any substrate but is potentially compromised in terrestrial environments where image distortion may be more obvious than in water. Glass frogs are one example of terrestrial transparency and are well known for their transparent ventral skin through which their bones, intestines, and beating hearts can be seen. However, sparse dorsal pigmentation means that these frogs are better described as translucent. To investigate whether this imperfect transparency acts as camouflage, we used in situ behavioral trials, visual modeling, and laboratory psychophysics. We found that the perceived luminance of the frogs changed depending on the immediate background, lowering detectability and increasing survival when compared to opaque frogs. Moreover, this change was greatest for the legs, which surround the body at rest and create a diffuse transition from background to frog luminance rather than a sharp, highly salient edge. This passive change in luminance, without significant modification of hue, suggests a camouflage strategy, "edge diffusion," distinct from both transparency and active color change.

Camouflage accuracy in Sahara-Sahel desert rodents.

Camouflage helps animals to hide from predators and is therefore key to survival. Although widespread convergence of animal phenotypes to their natural environment is well-established, there is a lack of knowledge about how species compromise camouflage accuracy across different background types in their habitat. Here we tested how background matching has responded to top-down selection by avian and mammalian predators using Sahara-Sahel desert rodents in North Africa. We show that the fur colouration of several species has become an accurate match to different types of desert habitats. This is supported by a correlation analysis of colour and pattern metrics, investigation of animal-to-background similarities at different spatial scales and is confirmed by modelling of two predator vision systems. The background match was closest across large (or global) spatial scales, suggesting a generalist camouflage tactic for many background types. Some species, may have a better match to the background over small (or focal) spatial scales, which could be the result of habitat choices or differential predation. Nevertheless, predicted discrimination distances of fur colouration were virtually indistinguishable for mammalian and low for avian vision model, which implies effective camouflage. Our study provides one of the best documented cases of multilevel camouflage accuracy in geographically widespread taxa. We conclude that background matching has become an effective and common adaptation against predatory threat in Sahara-Sahelian desert rodents.

False holes as camouflage.

Long noted by naturalists, leaf mimicry provides some of the most impressive examples of camouflage through masquerade. Many species of leaf-mimicking Lepidoptera also sport wing markings that closely resemble irregularly shaped holes caused by decay or insect damage. Despite proposals that such markings can either enhance resemblance to damaged leaves or act to disrupt surface appearance through false depth cues, to our knowledge, no attempt has been made to establish exactly how these markings function, or even whether they confer a survival benefit to prey. Here, in two field experiments using artificial butterfly-like targets, we show that false hole markings provide significant survival benefits against avian predation. Furthermore, in a computer-based visual search experiment, we demonstrate that detection of such targets by humans is impeded in a similar fashion. Equally contrasting light marks do not have the same effect; indeed, they lead to increased detection. We conclude that the mechanism is the disruption of the otherwise homogeneous wing surface (surface disruptive camouflage) and that, by resembling the holes sometimes found in real leaves, the disruptive benefits are not offset by conspicuousness costs.

Iridescence as Camouflage.

Iridescence is a striking and taxonomically widespread form of animal coloration [1], but that its intense and varying hues could function as concealment [2] rather than signaling seems completely counterintuitive. Here, we show that the color changeability of biological iridescence, produced by multilayer cuticle reflectors in jewel beetle (Sternocera aequisignata) wing cases, provides effective protection against predation by birds. Importantly, we also show that the most likely mechanism to explain this increase in survival is camouflage and not some other protective function, such as aposematism. In two field experiments using wild birds and humans, we measured both the "survival" and direct detectability of iridescent and non-iridescent beetle models and demonstrated that the iridescent treatment fared best in both experiments. We also show that an increased level of specular reflection (gloss) of the leaf background leads to an increase in the survival of all targets and, for detectability by humans, enhances the camouflage effect of iridescence. The latter suggests that some prey, particularly iridescent ones, can increase their chance of survival against visually hunting predators even further by choosing glossier backgrounds. Our study is the first to present direct empirical evidence that biological iridescence can work as a form of camouflage, providing an adaptive explanation for its taxonomically widespread occurrence. VIDEO ABSTRACT.

Overcoming the detectability costs of symmetrical coloration.

For camouflaged prey, enhanced conspicuousness due to bilaterally symmetrical coloration increases predation risk. The ubiquity of symmetrical body patterns in nature is therefore paradoxical, perhaps explicable through tight developmental constraints. Placing patterns that would be salient when symmetrical (e.g. high contrast markings) away from the axis of symmetry is one possible strategy to reduce the predation cost of symmetrical coloration. Artificial camouflaged prey with symmetrical patterns placed at different distances from the axis were used in both visual search tasks with humans and survival experiments with wild avian predators. Targets were less conspicuous when symmetrical patterning was placed outside a 'critical zone' near the midline. To assess whether real animals have evolved as predicted from these experiments, the saliency of features at different distances from the midline was measured in the cryptically coloured forewings of 36 lepidopteran species. Salience, both in absolute terms and relative to wing area, was greatest away from the axis of symmetry. Our work, therefore, demonstrates that prey morphologies may have evolved to exploit a loophole in the ability of mammalian and avian visual systems to spot symmetrical patterns.

In the corner of the eye: camouflaging motion in the peripheral visual field.

Most animals need to move, and motion will generally break camouflage. In many instances, most of the visual field of a predator does not fall within a high-resolution area of the retina and so, when an undetected prey moves, that motion will often be in peripheral vision. We investigate how this can be exploited by prey, through different patterns of movement, to reduce the accuracy with which the predator can locate a cryptic prey item when it subsequently orients towards a target. The same logic applies for a prey species trying to localize a predatory threat. Using human participants as surrogate predators, tasked with localizing a target on peripherally viewed computer screens, we quantify the effects of movement (duration and speed) and target pattern. We show that, while motion is certainly detrimental to camouflage, should movement be necessary, some behaviours and surface patterns reduce that cost. Our data indicate that the phenotype that minimizes localization accuracy is unpatterned, having the mean luminance of the background, does not use a startle display prior to movement, and has short (below saccadic latency), fast movements.

Effect of glass shape on the pouring accuracy of liquid volume.

BACKGROUND: The shape of glassware may exacerbate or counteract biases in perceived volume, which may lead people to misjudge the pouring of alcoholic drinks. The aim of these studies was to investigate the effect of glass shape on the pouring accuracy of liquid volume. METHODS: In Study 1, using an online computerised task, participants (n = 211) were asked to pour liquid in glasses in a within-subjects design with factors of glass shape (straight, curved) and requested percentage fullness (10, 20, 25, 30, 40, 50, 60, 70, 75, 80, 90%). Curve estimations were carried out to determine if errors followed a linear or non-linear relationship. In Study 2, in a real world experimental study, participants (n = 96) were asked to pour water to the midpoint of pint glasses in a within-subjects design with one factor of glass shape (straight, curved, tulip, inverted). Differences between poured amounts were analysed using one-way repeated measures ANOVA. RESULTS: In Study 1, participants under-poured in curved glasses compared to straight glasses at all requested amounts. In Study 2, participants under-poured in curved (p < 0.001, dz = 1.51) and tulip (p < 0.001, dz = 0.59) glasses compared to straight glasses. Findings were inconclusive as to whether or not a difference was present between pourings in inverted and straight glasses. Participants displayed a tendency to under-pour in all glasses relative to requested amounts in both studies. CONCLUSIONS: The shape of glassware appears to influence the pouring accuracy of liquid. Pouring in tulip and curved glasses was more inaccurate compared to straight glasses, possibly due to the height of liquid within the glass and volume changing in a non-linear relationship.

Distance-dependent defensive coloration in the poison frog Dendrobates tinctorius, Dendrobatidae.

Poison dart frogs provide classic examples of warning signals: potent toxins signaled by distinctive, conspicuous coloration. We show that, counterintuitively, the bright yellow and blue-black color of Dendrobates tinctorius (Dendrobatidae) also provides camouflage. Through computational modeling of predator vision, and a screen-based detection experiment presenting frogs at different spatial resolutions, we demonstrate that at close range the frog is highly detectable, but from a distance the colors blend together, forming effective camouflage. This result was corroborated with an in situ experiment, which found survival to be background-dependent, a feature more associated with camouflage than aposematism. Our results suggest that in D. tinctorius the distribution of pattern elements, and the particular colors expressed, act as a highly salient close range aposematic signal, while simultaneously minimizing detectability to distant observers.

Iridescence impairs object recognition in bumblebees.

Iridescence is a taxonomically widespread and striking form of animal coloration, yet despite advances in understanding its mechanism, its function and adaptive value are poorly understood. We test a counterintuitive hypothesis about the function of iridescence: that it can act as camouflage through interference with object recognition. Using an established insect visual model (Bombus terrestris), we demonstrate that both diffraction grating and multilayer iridescence impair shape recognition (although not the more subtle form of diffraction grating seen in some flowers), supporting the idea that both strategies can be effective means of camouflage. We conclude that iridescence produces visual signals that can confuse potential predators, and this might explain the high frequency of iridescence in many animal taxa.

Distance-dependent aposematism and camouflage in the cinnabar moth caterpillar (Tyria jacobaeae, Erebidae).

Defended prey often use distinctive, conspicuous, colours to advertise their unprofitability to potential predators (aposematism). These warning signals are frequently made up of salient, high contrast, stripes which have been hypothesized to increase the speed and accuracy of predator avoidance learning. Limitations in predator visual acuity, however, mean that these patterns cannot be resolved when viewed from a distance, and adjacent patches of colour will blend together (pattern blending). We investigated how saliency changes at different viewing distances in the toxic and brightly coloured cinnabar moth caterpillar (Tyria jacobaeae). We found that although the caterpillars' orange-and-black stripes are highly salient at close range, when viewed from a distance the colours blend together to match closely those of the background. Cinnabar caterpillars therefore produce a distance-dependent signal combining salient aposematism with targeted background matching camouflage, without necessarily compromising the size or saturation of their aposematic signal.

Stacking Chairs: Local Sense and Global Nonsense.

We report a confusing stimulus which demonstrates the power of local interpretation of three-dimensional structure to disrupt a coherent global perception.

Optimal background matching camouflage.

Background matching is the most familiar and widespread camouflage strategy: avoiding detection by having a similar colour and pattern to the background. Optimizing background matching is straightforward in a homogeneous environment, or when the habitat has very distinct sub-types and there is divergent selection leading to polymorphism. However, most backgrounds have continuous variation in colour and texture, so what is the best solution? Not all samples of the background are likely to be equally inconspicuous, and laboratory experiments on birds and humans support this view. Theory suggests that the most probable background sample (in the statistical sense), at the size of the prey, would, on average, be the most cryptic. We present an analysis, based on realistic assumptions about low-level vision, that estimates the distribution of background colours and visual textures, and predicts the best camouflage. We present data from a field experiment that tests and supports our predictions, using artificial moth-like targets under bird predation. Additionally, we present analogous data for humans, under tightly controlled viewing conditions, searching for targets on a computer screen. These data show that, in the absence of predator learning, the best single camouflage pattern for heterogeneous backgrounds is the most probable sample.

Distance-dependent pattern blending can camouflage salient aposematic signals.

The effect of viewing distance on the perception of visual texture is well known: spatial frequencies higher than the resolution limit of an observer's visual system will be summed and perceived as a single combined colour. In animal defensive colour patterns, distance-dependent pattern blending may allow aposematic patterns, salient at close range, to match the background to distant observers. Indeed, recent research has indicated that reducing the distance from which a salient signal can be detected can increase survival over camouflage or conspicuous aposematism alone. We investigated whether the spatial frequency of conspicuous and cryptically coloured stripes affects the rate of avian predation. Our results are consistent with pattern blending acting to camouflage salient aposematic signals effectively at a distance. Experiments into the relative rate of avian predation on edible model caterpillars found that increasing spatial frequency (thinner stripes) increased survival. Similarly, visual modelling of avian predators showed that pattern blending increased the similarity between caterpillar and background. These results show how a colour pattern can be tuned to reveal or conceal different information at different distances, and produce tangible survival benefits.