Disruptive Coloration Research Articles

Camouflage

AbstractAnimal camouflage has long been used to illustrate the power of natural selection, and provides an excellent testbed for investigating the trade‐offs affecting the adaptive value of colour. However, the contemporary study of camouflage extends beyond evolutionary biology, co‐opting knowledge, theory and methods from sensory biology, perceptual and cognitive psychology, computational neuroscience and engineering. This is because camouflage is an adaptation to the perception and cognition of the species (one or more) from which concealment is sought. I review the different ways in which camouflage manipulates and deceives perceptual and cognitive mechanisms, identifying how, and where in the sequence of signal processing, strategies such as transparency, background matching, disruptive coloration, distraction marks, countershading and masquerade have their effects. As such, understanding how camouflage evolves and functions not only requires an understanding of animal sensation and cognition, it sheds light on perception in other species.

Imperfect camouflage: how to hide in a variable world?

Camouflage is an important anti-predator strategy for many animals and is traditionally thought of as being tightly linked to a specific visual background. While much work focuses on optimizing camouflage against one background, this may not be relevant for many species and contexts, as animals may encounter many different habitats throughout their lives due to temporal and spatial variation in their environment. How should camouflage be optimized when an animal or object is seen against multiple visual backgrounds? Various solutions may exist, including colour change to match new environments or use of behaviour to maintain crypsis by choosing appropriate substrates. Here, we focus on a selection of approaches under a third alternative strategy: animals may adopt (over evolution) camouflage appearances that represent an optimal solution against multiple visual scenes. One approach may include a generalist or compromise strategy, where coloration matches several backgrounds to some extent, but none closely. A range of other camouflage types, including disruptive camouflage, may also provide protection in multiple environments. Despite detailed theoretical work determining the plausibility of compromise camouflage and elucidating the conditions under which it might evolve, there is currently mixed experimental evidence supporting its value and little evidence of it in natural systems. In addition, there remain many questions including how camouflage strategies should be defined and optimized, and how they might interact with other types of crypsis and defensive markings. Overall, we provide a critical overview of our current knowledge about how camouflage can enable matching to multiple backgrounds, discuss important challenges of working on this question and make recommendations for future research.

Disruptive coloration and binocular disparity: breaking camouflage.

Many species employ camouflage to disguise their true shape and avoid detection or recognition. Disruptive coloration is a form of camouflage in which high-contrast patterns obscure internal features or break up an animal's outline. In particular, edge enhancement creates illusory, or ‘fake’ depth edges within the animal's body. Disruptive coloration often co-occurs with background matching, and together, these strategies make it difficult for an observer to visually segment an animal from its background. However, stereoscopic vision could provide a critical advantage in the arms race between perception and camouflage: the depth information provided by binocular disparities reveals the true three-dimensional layout of a scene, and might, therefore, help an observer to overcome the effects of disruptive coloration. Human observers located snake targets embedded in leafy backgrounds. We analysed performance (response time) as a function of edge enhancement, illumination conditions and the availability of binocular depth cues. We confirm that edge enhancement contributes to effective camouflage: observers were slower to find snakes whose patterning contains ‘fake’ depth edges. Importantly, however, this effect disappeared when binocular depth cues were available. Illumination also affected detection: under directional illumination, where both the leaves and snake produced strong cast shadows, snake targets were localized more quickly than in scenes rendered under ambient illumination. In summary, we show that illusory depth edges, created via disruptive coloration, help to conceal targets from human observers. However, cast shadows and binocular depth information improve detection by providing information about the true three-dimensional structure of a scene. Importantly, the strong interaction between disparity and edge enhancement suggests that stereoscopic vision has a critical role in breaking camouflage, enabling the observer to overcome the disruptive effects of edge enhancement.

A remarkable new sinoalid froghopper with probable disruptive colouration in mid-Cretaceous Burmese amber (Hemiptera, Cicadomorpha)

The Mesozoic froghopper family Sinoalidae was reported from the uppermost Middle–lowermost Upper Jurassic Daohugou Biota and coeval strata of northeastern China, and mid-Cretaceous Kachin amber of northern Myanmar. Herein, a remarkably new sinoalid froghopper, Ornatiala amoena Chen, Wang and Zhang, gen. et sp. nov., is reported from Kachin amber. The new taxon is distinctly different from all known sinoalids in possessing the following characters: the head strongly produced anteriorly, slightly longer than wide; the pronotum relatively long, with length/width ratio about 0.6; the tegmen with post-claval margin beyond termination of CuP strongly convex, making tegmen widest near termination of CuA2, and a long stalk ScP+R+MP present. Additionally, this new remarkable sinoalid bears a novel prominent colouration pattern (probable disruptive colouration) on tegmina, further confirming that this froghopper group was likely to be undergoing high morphological and ecological diversification in the mid-Cretaceous.

Disruptive coloration and habitat use by seahorses

ABSTRACT Predation avoidance is a primary factor influencing survival. Therefore, any trait that affects the risk of predation, such as camouflage, is expected to be under selection pressure. Background matching (homochromy) limits habitat use, especially if the habitat is heterogeneous. Another camouflage mechanism is disruptive coloration, which reduces the probability of detection by masking the prey’s body contours. Here we evaluated if disruptive coloration in the longsnout seahorse, Hippocampus reidi, allows habitat use diversification. We analyzed 82 photographs of animals, comparing animal and background color, and registering anchorage substrate (holdfast). We tested whether the presence (disruptive coloration) or absence of bands (plain coloration) predicted occupation of backgrounds of different colors. We also calculated the connectance between seahorse morph and background color or holdfast, as well as whether color morph differed in their preferences for holdfast. Animals with disruptive coloration were more likely to be found in environments with colors different from their own. Furthermore, animals with disruptive coloration occupied more diversified habitats, but as many holdfasts as plain colored animals. Therefore, animals with disruptive coloration were less selective in habitat use than those lacking disruptive color patterns, which agrees with the disruptive coloration hypothesis.

Cryptic speciation yields remarkable mimics: A new genus of sea slugs that masquerade as toxic algae (Caulerpa spp.)

Abstract“Cryptic” can refer to species that match their background through camouflage or disruptive colouration, or in taxonomy to externally similar but unrecognized congeners. In adaptive resemblance, organisms resemble parts of a larger host animal or plant on which the mimic is highly cryptic. Mimetic lineages that radiate onto superficially similar hosts may contain cryptic species in both senses: taxa that are difficult to detect, and challenging for taxonomists to distinguish. Here, we describe a new genus and four species of herbivorous sea slugs (Gastropoda, Heterobranchia, Sacoglossa), including remarkable mimics of toxic green algae (Caulerpa spp.) on which the slugs feed. The long‐recognized Stiliger smaragdinus Baba 1949 is highly mimetic of “sea grapes” (Caulerpa racemosa‐lentillifera), but phylogenetic analyses of four genes indicated Stiliger was polyphyletic: the name‐bearing species grouped within Placida, whereas Caulerpa‐mimetic lineages were phylogenetically distinct. We erect the genus Sacoproteus gen. n. for S. smaragdinus (Baba 1949), and describe four new species: S. nishae sp. n. from the Indo‐Pacific, which mimics Caulerpa chemnitzia; Sacoproteus yhiae sp. n. and Sacoproteus browni sp. n. from southern Australia, which mimic Caulerpa cactoides and Caulerpa gemminata; and Sacoproteus thomasleei sp. n., a non‐mimetic west Pacific species that shared key features. Stiliger s.s. and Placida species show crypsis and aposematism but not host mimicry, although Stiliger spp. feeding on undefended algae may be Batesian mimics. Investigating the ecology and biogeography of Sacoproteus gen. n. will yield insight into how selection generates such extraordinary examples of adaptive resemblance in the marine realm.

Camouflage strategies interfere differently with observer search images.

Numerous animals rely on camouflage for defence. Substantial past work has identified the presence of multiple strategies for concealment, and tested the mechanisms underpinning how they work. These include background matching, D-RUP coloration to destroy target edges, and distractive markings that may divert attention from key target features. Despite considerable progress, work has focused on how camouflage types prevent initial detection by naive observers. However, predators will often encounter multiple targets over time, providing the opportunity to learn or focus attention through search images. At present, we know almost nothing about how camouflage types facilitate or hinder predator performance over repeated encounters. Here, we use experiments with human subjects searching for targets on touch screens with different camouflage strategies, and control the experience that subjects have with target types. We show that different camouflage strategies affect how subjects improve in detecting targets with repeated encounters, and how performance in detection of one camouflage type depends on experience of other strategies. In particular, disruptive coloration is effective at preventing improvements in camouflage breaking during search image formation, and experience with one camouflage type (distraction) can decrease the ability of subjects to switch to and from search images for new camouflage types (disruption). Our study is, to our knowledge, the first to show how the success of camouflage strategies depends on how they prevent initial and successive detection, and on predator experience of other strategies. This has implications for the evolution of prey phenotypes, how we assess the efficacy of defences, and predator–prey dynamics.

Dissociating the effect of disruptive colouration on localisation and identification of camouflaged targets

Disruptive camouflage features contrasting areas of pigmentation across the animals’ surface that form false edges which disguise the shape of the body and impede detection. In many taxa these false edges feature local contrast enhancement or edge enhancement, light areas have lighter edges and dark areas have darker edges. This additional quality is often overlooked in existing research. Here we ask whether disruptive camouflage can have benefits above and beyond concealing location. Using a novel paradigm, we dissociate the time courses of localisation and identification of a target in a single experiment. We measured the display times required for a stimulus to be located or identified (the critical duration). Targets featured either uniform, disruptive or edge enhanced disruptive colouration. Critical durations were longer for identifying targets with edge enhanced disruptive colouration camouflage even when presented against a contrasting background, such that all target types were located equally quickly. For the first time, we establish empirically that disruptive camouflage not only conceals location, but also disguises identity. This shows that this form of camouflage can be useful even when animals are not hidden. Our findings offer insights into how edge enhanced disruptive colouration undermines visual perception by disrupting object recognition.

Tadpoles respond to background colour under threat

The ability to respond to background colour is an important feature of species that might benefit from background matching camouflage. Tadpole colour patterns vary and could be associated with several functions, including defense. Because tadpoles are exposed to a wide array of visually oriented predators, they represent good models to study defensive colouration and associated behaviours. We tested whether a potentially disruptively camouflaged tadpole with a dark body crossed by yellow bars (Ololygon machadoi) is able to respond differently to matching light and dark natural background colours and an artificial blue contrasting background. We used a syntopic contrasting black tadpole (Bokermannohyla martinsi) as a control, expecting it not to respond to background colour in search for camouflage. Ololygon machadoi tadpoles chose light over blue backgrounds under threat, as expected, however they did not show preferential use of dark vs. blue backgrounds. Bokermannohyla martinsi did not respond to any combination of background colours. Our results suggest that O. machadoi tadpoles are able to respond to background colour, and may favor matching backgrounds under some circumstances. The potentially disruptive colouration of O. machadoi tadpoles may increase their repertoire of escape strategies, background matching being one of the options to escape predation.

Is tadpole coloration adaptive against bird predation?

Birds are visually oriented predators, and some are known or supposed to prey upon tadpoles. Neotropical tadpoles exhibit several colorations that could potentially improve survivorship through camouflage, aposematism, or mimetism. In this study, we tested tadpoles of two hylid species for protective effects of their colorations, one potentially aposematic (Bokermannohyla martinsi) and another (Ololygon machadoi) previously hypothesized as disruptive and/or mimetic to a naucorid insect (Limnocoris porphyros). We conducted in situ and ex situ experiments and observed that the uniformly black B. martinsi tadpoles were more intensely preyed upon by birds than those of O. machadoi, regardless of background color, which may have happened because the disruptive coloration of O. machadoi hampered its detection. Alternatively, the duration of the experiments may have been too short for birds to learn about a possible toxicity of B. martinsi tadpoles, which are more active and thus more visible. Birds that had a previous experience with L. porphyros tended to attack tadpoles of O. machadoi less than naive birds. On the other hand, we did not observe any change in predation levels upon B. martinsi tadpoles whether presented to birds before or after L. porphyros. Our results indicate that the predation by birds, although apparently occasional, is likely to be influenced by tadpole coloration.

Mesozoic diversity of relict subfamily Kempyninae (Neuroptera: Osmylidae)

A new genus and two new species of Kempyninae (Osmylidae), Ponomarenkius excellens gen. et sp. nov. and Arbusella magna sp. nov., are described from the Middle-Upper Jurassic of Daohugou (China). The finding demonstrates that extant kempynins, a typical Gondwanan group, are overshadowed by their Mesozoic relatives in taxonomic diversity and variety of wing venation. Striped patterns of both newly described species are an example of cryptic and disruptive coloration, possibly pinnate leaf mimesis. Eyespot patterns of Arbusella magna sp. nov. can be explained as a result of sexual selection. The abundance and distribution of the Mesozoic kempynins are discussed.http://zoobank.org/urn:lsid:zoobank.org:pub:CF33DEB4-0A69-407D-B1B2-1EC6537E4095

Two ways to hide: predator and prey perspectives of disruptive coloration and background matching in jumping spiders

Two ways to hide: predator and prey perspectives of disruptive coloration and background matching in jumping spiders

Disruptive colouration in reef fish: does matching the background reduce predation risk?

Animals use disruptive colouration to prevent detection or recognition by potential predators or prey. Highly contrasting elements within colour patterns, including vertical or horizontal bars, are thought to be effective at distracting attention away from body form and reducing detection likelihood. However, it is unclear whether such patterns need to be a good match to the spatial characteristics of the background to gain cryptic benefits. We tested this hypothesis using the iconic vertically barred humbug damselfish, Dascyllus aruanus (Linneaus 1758), a small reef fish that lives among the finger-like projections of branching coral colonies. Using behavioural experiments, we demonstrated that the spatial frequency of the humbug pattern does not need to exactly match the spatial frequency of the coral background to reduce the likelihood of being attacked by two typical reef fish predators: slingjaw wrasse, Epibulus insidiator (Pallas 1770), and coral trout, Plectropomus leopardus (Lacépède 1802). Indeed, backgrounds with a slightly higher spatial frequency than the humbug body pattern provided more protection from predation than well-matched backgrounds. These results were consistent for both predator species, despite differences in their mode of foraging and visual acuity, which was measured using anatomical techniques. We also showed that a slight mismatch in the orientation of the vertical bars did not increase the chances of detection. However, the likelihood of attack did increase significantly when the bars were perpendicular to the background. Our results provide evidence that fish camouflage is more complex than it initially appears, with likely many factors influencing the detection likelihood of prey by relevant predators.

Rapid body color brightening is associated with exposure to a stressor in anAnolislizard

Many species use color change to optimize body coloration to changing environmental conditions, and drivers of rapid color change in natural populations are numerous and poorly understood. We examined factors influencing body coloration in the Water Anole (Anolis aquaticus Taylor, 1956), a lizard possessing color-changing stripes along the length of its body. We quantified the color of three body regions (the eye stripe, lateral stripe, and dorsum) before and after exposure to a mild stressor (handling and restraint). Based on current understanding of the genus Anolis Daudin, 1802, we hypothesized that exposure to a stressor would generate genus-typical skin darkening (i.e., increased melanism). Contrary to expectations, stress consistently brightened body coloration: eye and lateral stripes transitioned from brown to pale blue and green and the dorsum became lighter brown. Sex, size, and body temperature did not correlate with any aspect of body coloration, and a laboratory experiment confirmed that light exposure did not drive brightening. We propose that color change may serve to reduce conspicuousness through disruptive camouflage; lizards tended to display brighter stripes on mottled green–brown substrates. Together, these results improve our understanding of Anolis color change diversity and emphasize the need for a broader interpretation of the mechanism and functions of color change across taxa.

Quantifying camouflage: how to predict detectability from appearance

BackgroundQuantifying 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.ResultsOur 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.ConclusionsThe 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.

Edge enhancement improves disruptive camouflage by emphasising false edges and creating pictorial relief.

Disruptive colouration is a visual camouflage composed of false edges and boundaries. Many disruptively camouflaged animals feature enhanced edges; light patches are surrounded by a lighter outline and/or a dark patches are surrounded by a darker outline. This camouflage is particularly common in amphibians, reptiles and lepidopterans. We explored the role that this pattern has in creating effective camouflage. In a visual search task utilising an ultra-large display area mimicking search tasks that might be found in nature, edge enhanced disruptive camouflage increases crypsis, even on substrates that do not provide an obvious visual match. Specifically, edge enhanced camouflage is effective on backgrounds both with and without shadows; i.e. this is not solely due to background matching of the dark edge enhancement element with the shadows. Furthermore, when the dark component of the edge enhancement is omitted the camouflage still provided better crypsis than control patterns without edge enhancement. This kind of edge enhancement improved camouflage on all background types. Lastly, we show that edge enhancement can create a perception of multiple surfaces. We conclude that edge enhancement increases the effectiveness of disruptive camouflage through mechanisms that may include the improved disruption of the object outline by implying pictorial relief.

Camouflage élargi. Sur l’individuation esthétique

Animal camouflage is said to be a mode of being negative, implying a setback visibility. On the contrary, we try here to restore all its aesthetic positivity considering the singularity of extremely varied forms it produces. It soon becomes apparent that the camouflage forces us to question the privilege of individuality and traditional drawdown on singularity. The disruptive camouflage, especially, that crushes the individual formal unity provides the argument in favor of an individuation with the environment, and more with the world: the animal camoufleur disappears under only an individual visibility; it appears on the contrary in all its pre-individual splendor when it involves with environment components to make them the most expressive.

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.

Camouflage and Clutch Survival in Plovers and Terns

Animals achieve camouflage through a variety of mechanisms, of which background matching and disruptive coloration are likely the most common. Although many studies have investigated camouflage mechanisms using artificial stimuli and in lab experiments, less work has addressed camouflage in the wild. Here we examine egg camouflage in clutches laid by ground-nesting Snowy Plovers Charadrius nivosus and Least Terns Sternula antillarum breeding in mixed aggregations at Bahía de Ceuta, Sinaloa, Mexico. We obtained digital images of clutches laid by both species. We then calibrated the images and used custom computer software and edge detection algorithms to quantify measures related to three potential camouflage mechanisms: pattern complexity matching, disruptive effects and background color matching. Based on our image analyses, Snowy Plover clutches, in general, appeared to be more camouflaged than Least Tern clutches. Snowy Plover clutches also survived better than Least Tern clutches. Unexpectedly, variation in clutch survival was not explained by any measure of egg camouflage in either species. We conclude that measures of egg camouflage are poor predictors of clutch survival in this population. The behavior of the incubating parents may also affect clutch predation. Determining the significance of egg camouflage requires further testing using visual models and behavioral experiments.

3D Camouflage in an Ornithischian Dinosaur

SummaryCountershading was one of the first proposed mechanisms of camouflage [1, 2]. A dark dorsum and light ventrum counteract the gradient created by illumination from above, obliterating cues to 3D shape [3, 4, 5, 6]. Because the optimal countershading varies strongly with light environment [7, 8, 9], pigmentation patterns give clues to an animal’s habitat. Indeed, comparative evidence from ungulates [9] shows that interspecific variation in countershading matches predictions: in open habitats, where direct overhead sunshine dominates, a sharp dark-light color transition high up the body is evident; in closed habitats (e.g., under forest canopy), diffuse illumination dominates and a smoother dorsoventral gradation is found. We can apply this approach to extinct animals in which the preservation of fossil melanin allows reconstruction of coloration [10, 11, 12, 13, 14, 15]. Here we present a study of an exceptionally well-preserved specimen of Psittacosaurus sp. from the Chinese Jehol biota [16, 17]. This Psittacosaurus was countershaded [16] with a light underbelly and tail, whereas the chest was more pigmented. Other patterns resemble disruptive camouflage, whereas the chin and jugal bosses on the face appear dark. We projected the color patterns onto an anatomically accurate life-size model in order to assess their function experimentally. The patterns are compared to the predicted optimal countershading from the measured radiance patterns generated on an identical uniform gray model in direct versus diffuse illumination. These studies suggest that Psittacosaurus sp. inhabited a closed habitat such as a forest with a relatively dense canopy.Video