Defining disruptive coloration and distinguishing its functions

Disruptive coloration breaks up the shape and destroys the outline of an object, hindering detection. The principle was first suggested approximately a century ago, but, although research has significantly increased, the field remains conceptually unstructured and no unambiguous definition exists. This has resulted in variable use of the term, making it difficult to formulate testable hypotheses that are comparable between studies, slowing down advancement in this field. Related to this, a range of studies do not effectively distinguish between disruption and other forms of camouflage. Here, we give a formal definition of disruptive coloration, reorganize a range of sub-principles involved in camouflage and argue that five in particular are specifically related to disruption: differential blending; maximum disruptive contrast; disruption of surface through false edges; disruptive marginal patterns; and coincident disruptive coloration. We discuss how disruptive coloration can be optimized, how it can relate to other forms of camouflage markings and where future work is particularly needed.     

Disruptive contrast in animal camouflage

Camouflage typically involves colour patterns that match the background. However, it has been argued that concealment may be achieved by strategic use of apparently conspicuous markings. Recent evidence supports the theory that the presence of contrasting patterns placed peripherally on an animal's body (disruptive coloration) provides survival advantages. However, no study has tested a key prediction from the early literature that disruptive coloration is effective even when some colour patches do not match the background and have a high contrast with both the background and adjacent pattern elements (disruptive contrast). We test this counter-intuitive idea that conspicuous patterns might aid concealment, using artificial moth-like targets with pattern elements designed to match or mismatch the average luminance (lightness) of the trees on which they were placed. Disruptive coloration was less effective when some pattern elements did not match the background luminance. However, even non-background-matching disruptive patterns reduced predation relative to equivalent non-disruptive patterns or to unpatterned controls. Therefore, concealment may still be achieved even when an animal possesses markings not found in the background. Disruptive coloration may allow animals to exploit backgrounds on which they are not perfectly matched, and to possess conspicuous markings while still retaining a degree of camouflage.     

Can't tell the caterpillars from the trees: countershading enhances survival in a woodland

Perception of the body's outline and three-dimensional shape arises from visual cues such as shading, contour, perspective and texture. When a uniformly coloured prey animal is illuminated from above by sunlight, a shadow may be cast on the body, generating a brightness contrast between the dorsal and ventral surfaces. For animals such as caterpillars, which live among flat leaves, a difference in reflectance over the body surface may degrade the degree of background matching and provide cues to shape from shading. This may make otherwise cryptic prey more conspicuous to visually hunting predators. Cryptically coloured prey are expected to match their substrate in colour, pattern and texture (though disruptive patterning is an exception), but they may also abolish self-shadowing and therefore either reduce shape cues or maintain their degree of background matching through countershading: a gradation of pigment on the body of an animal so that the surface closest to illumination is darker. In this study, we report the results from a series of field experiments where artificial prey resembling lepidopteran larvae were presented on the upper surfaces of beech tree branches so that they could be viewed by free-living birds. We demonstrate that countershading is superior to uniform coloration in terms of reducing attack by free-living predators. This result persisted even when we fixed prey to the underside of branches, simulating the resting position of many tree-living caterpillars. Our experiments provide the first demonstration, in an ecologically valid visual context, that shadowing on bodies (such as lepidopteran larvae) provides cues that visually hunting predators use to detect potential prey species, and that countershading counterbalances shadowing to enhance cryptic protection.     

Enhancement of chromatic contrast increases predation risk for striped butterflies

Many prey species have evolved defensive colour patterns to avoid attacks. One type of camouflage, disruptive coloration, relies on contrasting patterns that hinder predators' ability to recognize an object. While high contrasts are used to facilitate detection in many visual communication systems, they are thought to provide misleading information about prey appearance in disruptive patterns. A fundamental tenet in disruptive coloration theory is the principle of 'maximum disruptive contrast', i.e. disruptive patterns are more effective when higher contrasts are involved. We tested this principle in highly contrasting stripes that have often been described as disruptive patterns. Varying the strength of chromatic contrast between stripes and adjacent pattern elements in artificial butterflies, we found a strong negative correlation between survival probability and chromatic contrast strength. We conclude that too high a contrast leads to increased conspicuousness rather than to effective camouflage. However, artificial butterflies that sported contrasts similar to those of the model species Limenitis camilla survived equally well as background-matching butterflies without these stripes. Contrasting stripes do thus not necessarily increase predation rates. This result may provide new insights into the design and characteristics of a range of colour patterns such as sexual, mimetic and aposematic signals.     

Disruptive coloration, crypsis and edge detection in early visual processing

Many animals use concealing markings to reduce the risk of predation. These include background pattern matching (crypsis), where the coloration matches a random sample of the background and disruptive patterns, whose effectiveness has been hypothesized to lie in breaking up the body into a series of apparently unrelated objects. We have previously established the effectiveness of disruptive coloration against avian predators, using artificial moth-like stimuli with colours designed to match natural backgrounds as perceived by birds. Here, we investigate the mechanism by which disruptive patterns reduce detectability, using a computational vision model of edge detection applied to photographs of our experimental stimuli, calibrated for bird colour vision. We show that, disruptive coloration is effective by exploiting edge detection algorithms that we use to model early visual processing. Thus, 'false' edges are detected within the body rather than at its periphery, so inhibiting successful detection of the animal's body outline.     

Disruptive camouflage impairs object recognition

Whether hiding from predators, or avoiding battlefield casualties, camouflage is widely employed to prevent detection. Disruptive coloration is a seemingly well-known camouflage mechanism proposed to function by breaking up an object''s salient features (for example their characteristic outline), rendering objects more difficult to recognize. However, while a wide range of animals are thought to evade detection using disruptive patterns, there is no direct experimental evidence that disruptive coloration impairs recognition. Using humans searching for computer-generated moth targets, we demonstrate that the number of edge-intersecting patches on a target reduces the likelihood of it being detected, even at the expense of reduced background matching. Crucially, eye-tracking data show that targets with more edge-intersecting patches were looked at for longer periods prior to attack, and passed-over more frequently during search tasks. We therefore show directly that edge patches enhance survivorship by impairing recognition, confirming that disruptive coloration is a distinct camouflage strategy, not simply an artefact of background matching.     

Teasing apart crypsis and aposematism – evidence that disruptive coloration reduces predation on a noxious toad

Both cryptic and aposematic colour patterns can reduce predation risk to prey. These distinct strategies may not be mutually exclusive, because the impact of prey coloration depends on a predator's sensory system and cognition and on the environmental background. Determining whether prey signals are cryptic or aposematic is a prerequisite for understanding the ecological and evolutionary implications of predator–prey interactions. This study investigates whether coloration and pattern in an exceptionally polymorphic toad, Rhinella alata, from Barro Colorado Island, Panama reduces predation via background matching, disruptive coloration, and/or aposematic signaling. When clay model replicas of R. alata were placed on leaf litter, the model's dorsal pattern – but not its colour – affected attack rates by birds. When models were placed on white paper, patterned and un‐patterned replicas had similar attack rates by birds. These results indicate that dorsal patterns in R. alata are functionally cryptic and emphasize the potential effectiveness of disruptive coloration in a vertebrate taxon.     

The effects of pattern symmetry on detection of disruptive and background-matching coloration

Two, logically distinct but sometimes compatible, mechanismsof camouflage are background-matching and disruptive coloration.In the former, an animal's coloration comprises a random sampleof the background, and so target–background discriminationis impeded. In the latter, object or feature recognition iscompromised by placing bold, high-contrast colors so that theybreak up the prey's body into apparently unconnected objects.Recent experimental evidence for the utility of disruptive colors,above and beyond that conferred by background matching, hasbeen based on artificial prey with patterns lacking a planeof symmetry. However, it is plausible that the bilateral symmetrypresent in natural prey may compromise the efficiency of disruptivecoloration, on account of the potency of symmetry as a cue invisual search. In this study, we tested this prediction in thefield, by tracking the "survival" under bird predation of artificialmothlike targets placed on oak trees. These had background-matchingcolor patches placed either disruptively or nondisruptivelyand with or without bilateral symmetry. We found that symmetryreduced the effectiveness of both nondisruptive and disruptivebackground-matching coloration to a similar degree so that thenegative effects of symmetry on concealment are no greater fordisruptive than nondisruptive patterns.     

Disruptive coloration provides camouflage independent of background matching

Natural selection shapes the evolution of anti-predator defences, such as camouflage. It is currently contentious whether crypsis and disruptive coloration are alternative mechanisms of camouflage or whether they are interrelated anti-predator defences. Disruptively coloured prey is characterized by highly contrasting patterns to conceal the body shape, whereas cryptic prey minimizes the contrasts to background. Determining bird predation of artificial moths, we found that moths which were dissimilar from the background but sported disruptive patterns on the edge of their wings survived better in heterogeneous habitats than did moths with the same patterns inside of the wings and better than cryptic moths. Despite lower contrasts to background, crypsis did not provide fitness benefits over disruptive coloration on the body outline. We conclude that disruptive coloration on the edge camouflages its bearer independent of background matching. We suggest that this result is explainable because disruptive coloration is effective by exploiting predators' cognitive mechanisms of prey recognition and not their sensory mechanisms of signal detection. Relative to disruptive patterns on the body outline, disruptive markings on the body interior are less effective. Camouflage owing to disruptive coloration on the body interior is background-specific and is as effective as crypsis in heterogeneous habitats. Hence, we hypothesize that two proximate mechanisms explain the diversity of visual anti-predator defences. First, disruptive coloration on the body outline provides camouflage independent of the background. Second, background matching and disruptive coloration on the body interior provide camouflage, but their protection is background-specific.     

Background matching,disruptive coloration,and differential use of microhabitats in two neotropical grasshoppers with sexual dichromatism

Cryptic coloration is an adaptative defensive mechanism against predators. Color patterns can become cryptic through background coloration‐matching and disruptive coloration. Disruptive coloration may evolve in visually heterogeneous microhabitats, whereas background matching could be favored in chromatically homogeneous microhabitats. In this work, we used digital photography to explore the potential use of disruptive coloration and background matching in males and females of two grasshopper species of the Sphenarium genus in different habitats. We found chromatic differences in the two grasshopper species that may be explained by local adaptation. We also found that the females and males of both species are dichromatic and seem to follow different color cryptic strategies, males are more disruptive than females, whereas females have a high background matching with less disruptive elements. The selective pressures of the predators in different microhabitats and the differences in mobility between sexes may explain the color pattern divergence between females and males. Nevertheless, more field experiments are needed in order to understand the relative importance of disruptive and background matching coloration in the evolution of sexual dichromatism in these grasshoppers.     

Birds at the Winter Feeder do not Recognize an Artificially Coloured Predator

It is supposed that coloration may affect the recognition of predators by prey species; nevertheless, the significance of the coloration and its particular components in the recognition process remains unknown. We presented dummies of the European sparrowhawk (Accipiter nisus) with changed body coloration, but with all other typical features preserved (body size and shape, beak, eyes, legs), to great tits (Parus major) and blue tits (Cyanistes caeruleus) visiting a winter feeder. A pigeon (Columba livia f. domestica) dummy was used as a harmless control. Neither tit species showed passive avoidance in the presence of a dummy with an artificial, violet‐white chequered coloration. They obviously did not consider such an object to be a predator despite the presence of the raptor beak, eyes and talons. Sparrowhawk dummies with the coloration completely changed (altered with those of a harmless European robin) or with the typical colour feature removed (barred pattern on the underparts) were considered to be as dangerous as the unmodified sparrowhawk. We discuss the possibility that the effect of salient raptor‐like features such as beak shape, eye coloration, and leg and talons shape overwhelmed the effect of body coloration in these cases. Birds visiting the feeder probably were able to generalize the vigilance towards the sparrowhawk to other realistically coloured dummies, but not to the non‐natural dummy.     

What's in a band? The function of the color and banding pattern of the Banded Swallowtail

Butterflies have evolved a diversity of color patterns, but the ecological functions for most of these patterns are still poorly understood. The Banded Swallowtail butterfly, Papilio demolion demolion, is a mostly black butterfly with a greenish‐blue band that traverses the wings. The function of this wing pattern remains unknown. Here, we examined the morphology of black and green‐blue colored scales, and how the color and banding pattern affects predation risk in the wild. The protective benefits of the transversal band and of its green‐blue color were tested via the use of paper model replicas of the Banded Swallowtail with variations in band shape and band color in a full factorial design. A variant model where the continuous transversal green‐blue band was shifted and made discontinuous tested the protective benefit of the transversal band, while grayscale variants of the wildtype and distorted band models assessed the protective benefit of the green‐blue color. Paper models of the variants and the wildtype were placed simultaneously in the field with live baits. Wildtype models were the least preyed upon compared with all other variants, while gray models with distorted bands suffered the greatest predation. The color and the continuous band of the Banded Swallowtail hence confer antipredator qualities. We propose that the shape of the band hinders detection of the butterfly's true shape through coincident disruptive coloration; while the green color of the band prevents detection of the butterfly from its background via differential blending. Differential blending is aided by the green‐blue color being due to pigments rather than via structural coloration. Both green and black scales have identical structures, and the scales follow the Bauplan of pigmented scales documented in other Papilio butterflies.     

Empirical tests of the role of disruptive coloration in reducing detectability

Disruptive patterning is a potentially universal camouflage technique that is thought to enhance concealment by rendering the detection of body shapes more difficult. In a recent series of field experiments, artificial moths with markings that extended to the edges of their 'wings' survived at higher rates than moths with the same edge patterns inwardly displaced. While this result seemingly indicates a benefit to obscuring edges, it is possible that the higher density markings of the inwardly displaced patterns concomitantly reduced their extent of background matching. Likewise, it has been suggested that the mealworm baits placed on the artificial moths could have created differential contrasts with different moth patterns. To address these concerns, we conducted controlled trials in which human subjects searched for computer-generated moth images presented against images of oak trees. Moths with edge-extended disruptive markings survived at higher rates, and took longer to find, than all other moth types, whether presented sequentially or simultaneously. However, moths with no edge markings and reduced interior pattern density survived better than their high-density counterparts, indicating that background matching may have played a so-far unrecognized role in the earlier experiments. Our disruptively patterned non-background-matching moths also had the lowest overall survivorship, indicating that disruptive coloration alone may not provide significant protection from predators. Collectively, our results provide independent support for the survival value of disruptive markings and demonstrate that there are common features in human and avian perception of camouflage.     

Warning coloration can be disruptive: aposematic marginal wing patterning in the wood tiger moth

Warning (aposematic) and cryptic colorations appear to be mutually incompatible because the primary function of the former is to increase detectability, whereas the function of the latter is to decrease it. Disruptive coloration is a type of crypsis in which the color pattern breaks up the outline of the prey, thus hindering its detection. This delusion can work even when the prey's pattern elements are highly contrasting; thus, it is possible for an animal's coloration to combine both warning and disruptive functions. The coloration of the wood tiger moth (Parasemia plantaginis) is such that the moth is conspicuous when it rests on vegetation, but when it feigns death and drops to the grass‐ and litter‐covered ground, it is hard to detect. This death‐feigning behavior therefore immediately switches the function of its coloration from signaling to camouflage. We experimentally tested whether the forewing patterning of wood tiger moths could function as disruptive coloration against certain backgrounds. Using actual forewing patterns of wood tiger moths, we crafted artificial paper moths and placed them on a background image resembling a natural litter and grass background. We manipulated the disruptiveness of the wing pattern so that all (marginal pattern) or none (nonmarginal pattern) of the markings extended to the edge of the wing. Paper moths, each with a hidden palatable food item, were offered to great tits (Parus major) in a large aviary where the birds could search for and attack the “moths” according to their detectability. The results showed that prey items with the disruptive marginal pattern were attacked less often than prey without it. However, the disruptive function was apparent only when the prey was brighter than the background. These results suggest that warning coloration and disruptive coloration can work in concert and that the moth, by feigning death, can switch the function of its coloration from warning to disruptive.     

Beyond morphs: Inter-individual colour variation despite strong genetic determinism of colour morphs in a wild bird

Categorizing individuals into discrete forms in colour polymorphic species can overlook more subtle patterns in coloration that can be of functional significance. Thus, quantifying inter-individual variation in these species at both within- and between-morph levels is critical to understand the evolution of colour polymorphisms. Here we present analyses of inter-individual colour variation in the Reunion grey white-eye (Zosterops borbonicus), a colour polymorphic wild bird endemic to the island of Reunion in which all highland populations contain two sympatric colour morphs, with birds showing predominantly grey or brown plumage, respectively. We first quantified colour variation across multiple body areas by using a continuous plumage colour score to assess variation in brown-grey coloration as well as smaller scale variation in light patches. To examine the possible causes of among-individual variation, we tested if colour variation in plumage component elements could be explained by genotypes at two markers near a major-effect locus previously related to back coloration in this species, and by other factors such as age, sex and body condition. Overall, grey-brown coloration was largely determined by genetic factors and was best described by three distinct clusters that were associated to genotypic classes (homozygotes and heterozygote), with no effect of age or sex, whereas variation in smaller light patches was primarily related to age and sex. Our results highlight the importance of characterizing subtle plumage variation beyond morph categories that are readily observable since multiple patterns of colour variation may be driven by different mechanisms, have different functions and will likely respond in different ways to selection.     

Colour plasticity and background matching in a threespine stickleback species pair

Examining differences in colour plasticity between closely‐related species in relation to the heterogeneity of background colours found in their respective habitats may offer important insight into how cryptic colour change evolves in natural populations. In the present study, we examined whether nonbreeding dorsal body coloration has diverged between sympatric species of stickleback along with changes in habitat‐specific background colours. The small, limnetic species primarily occupies the pelagic zone and the large, benthic species inhabits the littoral zone. We placed benthic and limnetic sticklebacks against extremes of habitat background colours and measured their degree of background matching and colour plasticity. Benthics matched the littoral background colour more closely than did the limnetics, although there was no difference between species in their resemblance to the pelagic background colour. Benthics were able to resemble both background colours by exhibiting greater directional colour plasticity in their dorsal body coloration than limnetics, which may be an adaptive response to the greater spectral heterogeneity of the littoral zone. The present study highlights how habitat‐specific spectral characteristics may shape cryptic coloration differences between stickleback species. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 902–914.     

Spots, stripes, tail tips and dark eyes: Predicting the function of carnivore colour patterns using the comparative method

Animal colour patterns are adaptive for three reasons: camouflage, communication and physico-physiological functions. This study proposes a conceptual framework for predicting the main adaptive function of carnivore colour patterns based on three factors: visibility, shape and location on the body, as well as, their behavioural ecological correlates. Using a comparative phylogenetic approach, the colour patterns present on the body, the tail and the eyes of 200 species of mammalian carnivores were analysed. Their evolutionary history was reconstructed using MacClade and Maddison's concentrated-changes test was used to test the association between species' colour patterns and their behavioural ecology on a composite phylogeny for all the Carnivora. The results for dark spots, vertical stripes, horizontal stripes, ringed tails, black tail tips, white tail tips, dark eye contour and dark eye patches, are presented. The comparative analyses indicate that spotted, vertically striped and horizontally striped coats evolved for camouflage. Tail markings seem to have evolved for intra- and/or inter-specific communication, while dark markings near and around the eyes are associated with variables consistent with a physico-physiological function. These findings suggest that both the physical environment and animal behaviour are important selective factors driving the evolution of animal colour patterns and that both need to be taken into consideration in future studies of animal coloration.     

Progressive background in moths, and a quantitative measure of crypsis

A method is presented for quantitative estimation of the degree of crypsis of species seen by visual predators against known backgrounds. It is based upon a comparison between transects taken across animal and background colour patterns. The method was applied to day-resting moths in deciduous forest in New Jersey. Each species is found for two to four weeks at characteristic dates, and there is a constant turnover of species. In both moths and backgrounds there is a regular change in the colour pattern parameters from winter through spring to early summer. Moths are on average more cryptic at their normal dates than they would be if present earlier or later in the year. Species with known resting sites are on average more cryptic on their resting sites than other background habitats. Species that rest on more than one background habitat are less cryptic on their preferred habitats than are specialists. Species that rest under leaves and are not visible from above are not very cryptic. Specific v. general resemblance, disruptive coloration, and factors affecting 'aspect diversity' are discussed. The new method of estimating crypsis is useful for studies of crypsis as well as in sexual selection. It is necessary to know much about the resting sites and behaviour of moths, as well as other functions of colour patterns, to understand colour pattern evolution.     

Crypsis, conspicuousness, mimicry and polyphenism as antipredator defences of foraging octopuses on Indo-Pacific coral reefs, with a method of quantifying crypsis from video tapes

We tested the hypothesis that soft-bodied octopuses, which spend most of their lives in dens, remain highly cryptic as their primary defence against predation while they forage. We videotaped foraging octopuses on two widely dispersed Pacific coral reefs and developed a rigorous method to analyse the degree of crypsis from videotapes. Five ranks were assigned (two of‘ highly cryptic’, one of ‘moderately cryptic’, and two of ‘conspicuous’) to assess each octopus's body pattern match to its background, using the criteria of brightness, colour, shape and skin patterning. The data do not support the hypothesis. In Tahiti, octopuses were highly cryptic only 54%, moderately cryptic 24% and conspicuous 22% of the time. In Palau, the respective calculations were 31 %, 19% and 50%. A major feature of their behaviour was their remarkable ability to instantly change their body pattern, or phenotype, by direct neural control of the skin. Six chronic and nine acute categories of body patterns were observed. On average, octopuses changed their phenotype 2.95 times/minute, or 177 times per hour, based upon 7.5 hours of videotaped foraging. This rapid neurally controlled polyphenism was used most often to adjust their appearance as they foraged slowly across highly diverse substrates, thus implementing appropriate mechanisms of crypsis over each (e.g. general background resemblance, deceptive resemblance, disruptive coloration). However, when crawling rapidly, or swimming for short distances, octopuses often engaged a second antipredator lactic that was conspicuous: mimicking fishes or showing bold disruptive patterns that rendered them visibly different from an octopus. Nevertheless, sometimes they were simply conspicuous even when moving slowly, particularly in Palau, where the octopuses were larger, there was a high degree of mating“, and fewer signs of predation were evident. The results suggest that, while foraging, the overall strategy is to use polyphenism to produce ‘apparent rarity’ of any single phenotype (or search image) through mechanisms of crypsis, conspicuousness and mimicry, all of which are guided by keen vision in this marine invertebrate.     

Physiological colour change in the Moorish gecko,Tarentola mauritanica (Squamata: Gekkonidae): effects of background,light, and temperature

Colour has many different functions in animals, such as an involvement in thermoregulation, crypsis, and social interactions. Species capable of physiological colour change may alter their coloration in response to ecological conditions. The Moorish gecko, Tarentola mauritanica, is capable of actively changing its body coloration. In the present study, we investigated colour change in this gecko as a function of background, temperature, and light. Our results demonstrate that the Moorish gecko indeed changes its dorsal colour in response to changes in environmental conditions. By contrast to several other reptilian species, this rapid colour change does not appear to be associated with thermoregulation. Background matching, however, did appear to be a prominent function, although illumination appears to be an essential trigger. Future research should concentrate on individual variation and its effectiveness with respect to antipredatory mechanisms. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.