Background matching can reduce responsiveness of jumping spiders to stimuli in motion.

Motion and camouflage were previously considered to be mutually exclusive, as sudden movements can be easily detected. Background matching, for instance, is a well-known, effective camouflage strategy where the colour and pattern of a stationary animal match its surrounding background. However, background matching may lose its efficacy when the animal moves, as the boundaries of the animal become more defined against its background. Recent evidence shows otherwise, as camouflaged objects can be less detectable than uncamouflaged objects even while in motion. Here, we explored whether the detectability of computer-generated stimuli varies with the speed of motion, background (matching and unmatching) and size of stimuli in six species of jumping spiders (Araneae: Salticidae). Our results showed that, in general, the responsiveness of all six salticid species tested decreased with increasing stimulus speed regardless of whether the stimuli were conspicuous or camouflaged. Importantly, salticid responses to camouflaged stimuli were significantly lower compared with those to conspicuous stimuli. There were significant differences in motion detectability across species when the stimuli were conspicuous, suggesting differences in visual acuity in closely related species of jumping spiders. Furthermore, small stimuli elicited significantly lower responses than large stimuli across species and speeds. Our results thus suggest that background matching is effective even when stimuli are in motion, reducing the detectability of moving stimuli.

Plumage Balances Camouflage and Thermoregulation in Horned Larks (Eremophila alpestris).

AbstractAnimal coloration serves many biological functions and must therefore balance potentially competing selective pressures. For example, many animals have camouflage in which coloration matches the visual background that predators scan for prey. However, different colors reflect different amounts of solar radiation and may therefore have thermoregulatory implications as well. In this study, we examined geographic variation in dorsal patterning, coloration, and solar reflectance among horned larks (Eremophila alpestris) of the western United States. We found that plumage brightness was positively associated with soil granularity, aridity, and temperature. Plumage redness-both in terms of saturation (i.e., chroma) and hue-was positively associated with soil redness and temperature, while plumage patterning was positively associated with soil granularity. Together, these plumage-environment associations support both background matching and Gloger's rule, a widespread ecogeographic pattern in animal coloration. We also constructed thermoregulatory models that estimated cooling benefits provided by solar reflectance profiles of the dorsal plumage of each specimen based on the collection site. We found increased cooling benefits in hotter, more arid environments. Finally, cooling benefits were positively associated with residual brightness, such that individuals that were brighter than expected based on environmental conditions also had higher cooling benefits, suggesting a trade-off between camouflage and thermoregulation. Together, these data suggest that natural selection has balanced camouflage and thermoregulation in horned larks, and they illustrate how multiple competing evolutionary pressures may interact to shape geographic variation in adaptive phenotypes.

Comparative and experimental studies on the relationship between body size and countershading in caterpillars.

Countershading is a gradient of colouration in which the illuminated dorsal surfaces are darker than the unilluminated ventral surface. It is widespread in the animal kingdom and endows the body with a more uniform colour to decrease the chance of detection by predators. Although recent empirical studies support the theory of survival advantage conferred by countershading, this camouflage strategy has evolved only in some of the cryptic animals, and our understanding of the factors that affect the evolution of countershading is limited. This study examined the association between body size and countershading using lepidopteran larvae (caterpillars) as a model system. Specifically, we predicted that countershading may have selectively evolved in large-sized species among cryptic caterpillars if (1) large size constrains camouflage which facilitates the evolution of a trait reinforcing their crypsis and (2) the survival advantage of countershading is size-dependent. Phylogenetic analyses of four different lepidopteran families (Saturniidae, Sphingidae, Erebidae, and Geometridae) suggest equivocal results: countershading was more likely to be found in larger species in Saturniidae but not in the other families. The field predation experiment assuming avian predators did not support size-dependent predation in countershaded prey. Collectively, we found only weak evidence that body size is associated with countershading in caterpillars. Our results suggest that body size is not a universal factor that has shaped the interspecific variation in countershading observed in caterpillars.

Scorpionfish rapidly change colour in response to their background.

BACKGROUND: To facilitate background matching in heterogenous environments, some animals rapidly change body colouration. Marine predatory fishes might use this ability to hide from predators and prey. Here, we focus on scorpionfishes (Scorpaenidae), well-camouflaged, bottom-dwelling sit-and-wait predators. We tested whether Scorpaena maderensis and Scorpaena porcus adjust body luminance and hue in response to three artificial backgrounds and thereby achieve background matching. Both scorpionfish species are also red fluorescent, which could contribute to background matching at depth. Therefore, we tested whether red fluorescence is also regulated in response to different backgrounds. The darkest and the lightest backgrounds were grey, while the third background was orange of intermediate luminance. Scorpionfish were placed on all three backgrounds in a randomised repeated measures design. We documented changes in scorpionfish luminance and hue with image analysis and calculated contrast to the backgrounds. Changes were quantified from the visual perspective of two potential prey fishes, the triplefin Tripterygion delaisi and the goby Pomatoschistus flavescens. Additionally, we measured changes in the area of scorpionfish red fluorescence. Because scorpionfish changed quicker than initially expected, we measured luminance change at a higher temporal resolution in a second experiment. RESULTS: Both scorpionfish species rapidly adjusted luminance and hue in response to a change of background. From prey visual perspective, scorpionfishes' body achromatic and chromatic contrasts against the background were high, indicating imperfect background matching. Chromatic contrasts differed considerably between the two observer species, highlighting the importance of choosing natural observers with care when studying camouflage. Scorpionfish displayed larger areas of red fluorescence with increasing luminance of the background. With the second experiment, we showed that about 50% of the total luminance change observed after one minute is achieved very rapidly, in five to ten seconds. CONCLUSION: Both scorpionfish species change body luminance and hue in response to different backgrounds within seconds. While the achieved background matching was suboptimal for the artificial backgrounds, we propose that the observed changes were intended to reduce detectability, and are an essential strategy to camouflage in the natural environment.

Camouflage using three-dimensional surface disruption.

Disruptive markings are common in animal patterns and can provide camouflage benefits by concealing the body's true edges and/or by breaking the surface of the body into multiple depth planes. Disruptive patterns that are accentuated by high contrast borders are most likely to provide false depth cues to enhance camouflage, but studies to date have used visual detection models or humans as predators. We presented three-dimensional-printed moth-like targets to wild bird predators to determine whether: (1) three-dimensional prey with disrupted body surfaces have higher survival than three-dimensional prey with continuous surfaces, (2) two-dimensional prey with disruptive patterns or enhanced edge markings have higher survival than non-patterned two-dimensional prey. We found a survival benefit for three-dimensional prey with disrupted surfaces, and a significant effect of mean wing luminance. There was no evidence that false depth cues provided the same protective benefits as physical surface disruption in three-dimensional prey, perhaps because our treatments did not mimic the complexity of patterns found in natural animal markings. Our findings indicate that disruption of surface continuity is an important strategy for concealing a three-dimensional body shape.

Predator responses to prey camouflage strategies: a meta-analysis.

Although numerous studies about camouflage have been conducted in the last few decades, there is still a significant gap in our knowledge about the magnitude of protective value of different camouflage strategies in prey detection and survival. Furthermore, the functional significance of several camouflage strategies remains controversial. Here we carried out a comprehensive meta-analysis including comparisons of different camouflage strategies as well as predator and prey types, considering two response variables: mean predator search time (ST) (63 studies) and predator attack rate (AR) of camouflaged prey (28 studies). Overall, camouflage increased the predator ST by 62.56% and decreased the AR of prey by 27.34%. Masquerade was the camouflage strategy that most increased predator ST (295.43%). Background matching and disruptive coloration did not differ from each other. Motion camouflage did not increase ST but decreases AR on prey. We found no evidence that eyespot increases ST and decreases AR by predators. The different types of predators did not differ from each other, but caterpillars were the type of prey that most influenced the magnitude of camouflage's effect. We highlight the potential evolutionary mechanisms that led camouflage to be a highly effective anti-predatory adaptation, as well as potential discrepancies or redundancies among strategies, predator and prey types.

Camouflage in lichen moths: Field predation experiments and avian vision modelling demonstrate the importance of wing pattern elements and background for survival.

Background matching is perhaps the most ubiquitous form of defensive camouflage in the animal kingdom, an adaptive strategy that relies on the visual resemblance between a prey organism and its background to promote concealment from predators. The importance of background matching has been acknowledged for over a century, yet despite its renown and apparent pervasiveness, few studies exist that have objectively quantified its occurrence and tested the functional significance of background matching in a specific animal study system. The North Island lichen moth Declana atronivea presents a fascinating system to investigate such anti-predator coloration. This species possesses high contrast black and white forewings that appear to resemble lichen. Here we assessed the contribution of background matching to the antipredator defence of D. atronivea using field predation experiments with realistic models. We found that D. atronivea coloration confers a significant survival advantage against native avian predators when on lichen backgrounds compared to bark backgrounds, with an intermediate level of predation occurring when models were near, but not on lichen. This suggests that D. atronivea wing patterns are an adaptation for background matching. We subsequently used calibrated digital photography, avian vision modelling and image analysis techniques to objectively quantify the degree of background matching exhibited by D. atronivea and assessed the contribution of different visual elements (colour, luminance and pattern) to camouflage in this species. Only the pattern elements of D. atronivea presented a close match to that of the lichen backgrounds, with both chromatic and achromatic cues found to be poor predictors of background matching in this species. This study is one of the first to integrate vision modelling, quantitative image analysis and field predation experiments using realistic models to objectively quantify the level and functional significance of background matching in a real species, and presents an ideal system for further investigating the interrelation between multiple mechanisms of camouflage.

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.

Partial wing transparency works better when disrupting wing edges: Evidence from a field experiment.

Lepidoptera-a group of insects in which wing transparency has arisen multiple times-exhibits much variation in the size and position of transparent wing zones. However, little is known as to how this variability affects detectability. Here, we test how the size and position of transparent elements affect the predation of artificial moths by wild birds in the field. Morphs with transparent elements touching wing borders showed a reduced predation risk, with the effect being the same regardless of the number of wing borders being touched. By contrast, transparent element size had little to no effect on predation risk. Overall, this experiment shows for the first time that transparency offers higher protection when it disrupts prey contour in terrestrial habitats.

Intertidal gobies acclimate rate of luminance change for background matching with shifts in seasonal temperature.

Rate of colour change and background matching capacity are important functional traits for avoiding predation and hiding from prey. Acute changes in environmental temperature are known to impact the rate at which animals change colour, and therefore may affect their survival. Many ectotherms have the ability to acclimate performance traits such as locomotion, metabolic rate and growth rate with changes in seasonal temperature. However, it remains unclear how other functional traits that are directly linked to behaviour and survival respond to long-term changes in temperature (within an individual's lifetime). We assessed whether the rate of colour change is altered by long-term changes in temperature (seasonal variation) and if rate of colour change can acclimate to seasonal thermal conditions. We used an intertidal rock-pool goby Bathygobius cocosensis, to test this and exposed individuals to representative seasonal mean temperatures (16 or 31°C, herein referred to cold- and warm-exposed fish respectively) for 9 weeks and then tested their rate of luminance change when placed on white and black backgrounds at acute test temperatures 16 and 31°C. We modelled rate of luminance change using the visual sensitives of a coral trout Plectropmus leopardus to determine how well gobies matched their backgrounds in terms of luminance contrast to a potential predator. After exposure to long-term seasonal conditions, the warm-exposed fish had faster rates of luminance change and matched their background more closely when tested at 31 than at 16°C. Similarly, the cold-exposed fish had faster rates of luminance change and matched their backgrounds more closely at 16°C than at 31°C. This demonstrates that rate of luminance change can be adjusted to compensate for long-term changes in seasonal temperature. This is the first study to show that animals can acclimate rate of colour change for background matching to seasonal thermal conditions. We also show that rapid changes in acute temperature reduce background matching capabilities. Stochastic changes in climate are likely to affect the frequency of predator-prey interactions which may have substantial knock-on effects throughout ecosystems.

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.

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.

Quantifying camouflage: how to predict detectability from appearance.

BACKGROUND: Quantifying the conspicuousness of objects against particular backgrounds is key to understanding the evolution and adaptive value of animal coloration, and in designing effective camouflage. Quantifying detectability can reveal how colour patterns affect survival, how animals' appearances influence habitat preferences, and how receiver visual systems work. Advances in calibrated digital imaging are enabling the capture of objective visual information, but it remains unclear which methods are best for measuring detectability. Numerous descriptions and models of appearance have been used to infer the detectability of animals, but these models are rarely empirically validated or directly compared to one another. We compared the performance of human 'predators' to a bank of contemporary methods for quantifying the appearance of camouflaged prey. Background matching was assessed using several established methods, including sophisticated feature-based pattern analysis, granularity approaches and a range of luminance and contrast difference measures. Disruptive coloration is a further camouflage strategy where high contrast patterns disrupt they prey's tell-tale outline, making it more difficult to detect. Disruptive camouflage has been studied intensely over the past decade, yet defining and measuring it have proven far more problematic. We assessed how well existing disruptive coloration measures predicted capture times. Additionally, we developed a new method for measuring edge disruption based on an understanding of sensory processing and the way in which false edges are thought to interfere with animal outlines. RESULTS: Our novel measure of disruptive coloration was the best predictor of capture times overall, highlighting the importance of false edges in concealment over and above pattern or luminance matching. CONCLUSIONS: The efficacy of our new method for measuring disruptive camouflage together with its biological plausibility and computational efficiency represents a substantial advance in our understanding of the measurement, mechanism and definition of disruptive camouflage. Our study also provides the first test of the efficacy of many established methods for quantifying how conspicuous animals are against particular backgrounds. The validation of these methods opens up new lines of investigation surrounding the form and function of different types of camouflage, and may apply more broadly to the evolution of any visual signal.

Differential foraging success across a light level spectrum explains the maintenance and spatial structure of colour morphs in a polymorphic bird.

Detectability of different colour morphs under varying light conditions has been proposed as an important driver in the maintenance of colour polymorphism via disruptive selection. To date, no studies have tested whether different morphs have selective advantages under differing light conditions. We tested this hypothesis in the black sparrowhawk, a polymorphic raptor exhibiting a discrete white and dark morph, and found that prey provisioning rates differ between the morphs depending on light condition. Dark morphs delivered more prey in lower light conditions, while white morphs provided more prey in brighter conditions. We found support for the role of breeding season light level in explaining the clinal pattern of variation in morph ratio across the species range throughout South Africa. Our results provide the first empirical evidence supporting the hypothesis that polymorphism in a species, and the spatial structuring of morphs across its distribution, may be driven by differential selective advantage via improved crypsis, under varying light conditions.

Escape Distance in Ground-Nesting Birds Differs with Individual Level of Camouflage.

Camouflage is one of the most widespread antipredator strategies in the animal kingdom, yet no animal can match its background perfectly in a complex environment. Therefore, selection should favor individuals that use information on how effective their camouflage is in their immediate habitat when responding to an approaching threat. In a field study of African ground-nesting birds (plovers, coursers, and nightjars), we tested the hypothesis that individuals adaptively modulate their escape behavior in relation to their degree of background matching. We used digital imaging and models of predator vision to quantify differences in color, luminance, and pattern between eggs and their background, as well as the plumage of incubating adult nightjars. We found that plovers and coursers showed greater escape distances when their eggs were a poorer pattern match to the background. Nightjars sit on their eggs until a potential threat is nearby, and, correspondingly, they showed greater escape distances when the pattern and color match of the incubating adult's plumage-rather than its eggs-was a poorer match to the background. Finally, escape distances were shorter in the middle of the day, suggesting that escape behavior is mediated by both camouflage and thermoregulation.

The colours of extant mammals.

In this review I survey pelage and skin colouration patterns of the 29 orders of extant mammals and assess their functional significance. The vast majority of mammals are shades of grey or brown. Concealment is probably the principal evolutionary driver of pelage colouration in this Class likely through background matching and self-shadow concealment. A small minority of species are aposematic while many others have distinctive markings used in intraspecific and interspecific communication although the meaning of these markings is unclear. Colouration in mammals also has physiological consequences but these are barely understood as yet.

Background matching ability and the maintenance of a colour polymorphism in the red devil cichlid.

The evolution and maintenance of colour polymorphisms remains a topic of considerable research interest. One key mechanism thought to contribute to the coexistence of different colour morphs is a bias in how conspicuous they are to visual predators. Although individuals of many species camouflage themselves against their background to avoid predation, differently coloured individuals within a species may vary in their capacity to do so. However, to date, very few studies have explicitly investigated the ability of different colour morphs to plastically adjust their colouration to match their background. The red devil (Amphilophus labiatus) is a Neotropical cichlid fish with a stable colour polymorphism, with the gold morph being genetically dominant and having a myriad of documented advantages over the dark morph. However, gold individuals are much rarer, which may be related to their heightened conspicuousness to would-be predators. Here, we tested the ability of differently coloured individuals to phenotypically adjust the shade of their body colour and patterns to match their background. In particular, we filmed dark, gold and mottled (a transitioning phase from dark to gold) individuals under an identical set-up on light vs. dark-coloured substrates. We found that, in contrast to individuals of the dark morph, gold and mottled individuals were less capable of matching their body colouration to their background. As a result, gold individuals appeared to be more conspicuous. These results suggest that a difference in background matching ability could play an important role in the maintenance of colour polymorphisms.

Camouflage during movement in the European cuttlefish (Sepia officinalis).

A moving object is considered conspicuous because of the movement itself. When moving from one background to another, even dynamic camouflage experts such as cephalopods should sacrifice their extraordinary camouflage. Therefore, minimizing detection at this stage is crucial and highly beneficial. In this study, we describe a background-matching mechanism during movement, which aids the cuttlefish to downplay its presence throughout movement. In situ behavioural experiments using video and image analysis, revealed a delayed, sigmoidal, colour-changing mechanism during movement of Sepia officinalis across uniform black and grey backgrounds. This is a first important step in understanding dynamic camouflage during movement, and this new behavioural mechanism may be incorporated and applied to any dynamic camouflaging animal or man-made system on the move.

Background selection for camouflage shifts in accordance with color change in an intertidal prawn.

To maximize camouflage across visually heterogeneous habitats, animals have evolved a variety of strategies, including polyphenism, color change, and behavioral background matching. Despite the expected importance of behavioral processes for mediating camouflage, such as selection for matching substrates, behavior has received less attention than color traits themselves, and interactions between color change and behavior are largely unexplored. Here, we investigated behavioral background matching in green and red chameleon prawns (Hippolyte varians) over the course of a color change experiment. Prawns were housed on mismatching green and red seaweeds for 30 days and periodically given a choice test between the same seaweeds in y-choice trials over the experiment. We found that, as prawns change color and improve camouflage (to the perspective of a fish predator), there is a reinforcing shift in behavior. That is, as prawns shift from red to green color, or vice versa, their seaweed color preference follows this. We provide key empirical evidence that plasticity of appearance (color) is accompanied by a plastic shift in behavior (color preference) that reinforces camouflage in a color changing species on its natural substrate. Overall, our research highlights how short-term plasticity of behavior and longer-term color change act in tandem to maintain crypsis over time.

Scorpionfish adjust skin pattern contrast on different backgrounds.

The two scorpionfish species Scorpaena maderensis and S. porcus are well camouflaged ambush predators that rapidly change body colouration to adjust to background colour in less than 1 min. We tested whether individuals of both species also adjust body pattern to that of the background. We placed fish on backgrounds of different pattern granularity and quantified the change in fish body pattern over 1 min. We used calibrated image analysis to analyse the patterns from the visual perspective of a prey fish species using a granularity (pattern energy) analysis and an image clustering approach. In our experiment, fish did not change their most contrasting pattern components as defined by the dominant marking size, but changed their average marking size. Moreover, fish responded with a change in pattern in contrast to the different experimental backgrounds, especially when compared to the acclimation phase. These results indicate that scorpionfish have one main pattern that can be adjusted by modulating its internal contrast. A reduction in pattern contrast could thereby improve background matching, while an increase could promote camouflage via disruptive colouration.