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.     

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.     

Great tits (Parus major) searching for artificial prey: implications for cryptic coloration and symmetry

It has been suggested that bilateral symmetry may impose a costfor animals relying on camouflage because symmetric color patternsmight increase the risk of detection. We tested the effect ofsymmetry on crypsis, carrying out a predation experiment withgreat tits (Parus major) and black-and-white–patterned,artificial prey items and background. First, we found that detectiontime was significantly longer for a highly cryptic, asymmetricpattern based on a random sample of the background than forits symmetric variants. Second, we were able to arrange theelements of a prey pattern in a way that the resulting asymmetricpattern was highly cryptic and, furthermore, its symmetric variantwas highly cryptic as well. We conclude that symmetry may imposea substantial cost on cryptic patterns, but this cost variesamong patterns. This suggests that for prey, which predatorstypically view from an angle exposing their symmetry, selectionfor pattern asymmetry may be less important and selection fordecreased detectability cost of symmetry may be more importantthan previously thought. This may help to understand the existenceof so many prey with cryptic, symmetric color patterns.     

Concealed by conspicuousness: distractive prey markings and backgrounds

High-contrast markings, called distractive or dazzle markings, have been suggested to draw and hold the attention of a viewer, thus hindering detection or recognition of revealing prey characteristics, such as the body outline. We tested this hypothesis in a predation experiment with blue tits (Cyanistes caeruleus) and artificial prey. We also tested whether this idea can be extrapolated to the background appearance and whether high-contrast markings in the background would improve prey concealment. We compared search times for a high-contrast range prey (HC-P) and a low-contrast range prey (LC-P) in a high-contrast range background (HC-B) and a low-contrast range background (LC-B). The HC-P was more difficult to detect in both backgrounds, although it did not match the LC-B. Also, both prey types were more difficult to find in the HC-B than in the LC-B, in spite of the mismatch of the LC-P. In addition, the HC-P was more difficult to detect, in both backgrounds, when compared with a generalist prey, not mismatching either background. Thus, we conclude that distractive prey pattern markings and selection of microhabitats with distractive features may provide an effective way to improve camouflage. Importantly, high-contrast markings, both as part of the prey coloration and in the background, can indeed increase prey concealment.     

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.     

Behaviourally mediated crypsis in two nocturnal moths with contrasting appearance

The natural resting orientations of several species of nocturnal moth on tree trunks were recorded over a three-month period in eastern Ontario, Canada. Moths from certain genera exhibited resting orientation distributions that differed significantly from random, whereas others did not. In particular, Catocala spp. collectively tended to orient vertically, whereas subfamily Larentiinae representatives showed a variety of orientations that did not differ significantly from random. To understand why different moth species adopted different orientations, we presented human subjects with a computer-based detection task of finding and ‘attacking’ Catocala cerogama and Euphyia intermediata target images at different orientations when superimposed on images of sugar maple (Acer saccharum) trees. For both C. cerogama and E. intermediata, orientation had a significant effect on survivorship, although the effect was more pronounced in C. cerogama. When the tree background images were flipped horizontally the optimal orientation changed accordingly, indicating that the detection rates were dependent on the interaction between certain directional appearance features of the moth and its background. Collectively, our results suggest that the contrasting wing patterns of the moths are involved in background matching, and that the moths are able to improve their crypsis through appropriate behavioural orientation.     

Coincident disruptive coloration

Even if an animal matches its surroundings perfectly in colour and texture, any mismatch between the spatial phase of its pattern and that of the background, or shadow created by its three-dimensional relief, is potentially revealing. Nevertheless, for camouflage to be fully broken, the shape must be recognizable. Disruptive coloration acts against object recognition by the use of high-contrast internal colour boundaries to break up shape and form. As well as the general outline, characteristic features such as eyes and limbs must also be concealed; this can be achieved by having the colour patterns on different, but adjacent, body parts aligned to match each other (i.e. in phase). Such 'coincident disruptive coloration' ensures that there is no phase disjunction where body parts meet, and causes different sections of the body to blend perceptually. We tested this theory using field experiments with predation by wild birds on artificial moth-like targets, whose wings and (edible pastry) bodies had colour patterns that were variously coincident or not. We also carried out an experiment with humans searching for analogous targets on a computer screen. Both experiments show that coincident disruptive coloration is an effective mechanism for concealing an otherwise revealing body form.     

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.     

Revisiting Abbott Thayer: non-scientific reflections about camouflage in art,war and zoology

This paper reviews the achievements of Abbott Handerson Thayer (1849–1921), an American painter and naturalist whose pioneering writings on animal camouflage addressed shared concerns among artists, zoologists and military tacticians. It discusses his beliefs about camouflage (both natural and military) in the context of his training as an artist, with particular emphasis on three of his major ideas: countershading, ruptive (or disruptive) coloration and background picturing.     

Animal camouflage: compromise or specialize in a 2 patch-type environment?

Many animals possess camouflage markings that reduce the riskof detection by visually hunting predators. A key aspect ofcamouflage involves mimicking the background against which theanimal is viewed. However, most animals experience a wide varietyof backgrounds and cannot change their external appearance tomatch each selectively. We investigate whether such animalsshould adopt camouflage specialized with respect to one backgroundor adopt a compromise between the attributes of multiple backgrounds.We do this using a model consisting of predators that hunt preyin patches of 2 different types, where prey adopt the camouflagethat minimizes individual risk of predation. We show that theoptimal strategy of the prey is affected by a number of factors,including the relative frequencies of the patch types, the traveltime of predators between patches, the mean prey number in eachpatch type, and the trade-off function between the levels ofcrypsis in the patch types. We find evidence that both specialistand compromise strategies of prey camouflage are favored underdifferent model parameters, indicating that optimal concealmentmay not be as straightforward as previously thought.     

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.     

Background choice as an anti-predator strategy: the roles of background matching and visual complexity in the habitat choice of the least killifish

Because background matching improves concealment, prey animals have traditionally been expected to prefer parts of the habitat that match their visual appearance. However, empirical support for this is scarce. Moreover, this idea has recently been challenged by an alternative hypothesis: visual complexity of the background impedes prey detection, and hence prey could instead prefer complex parts of the habitat. We used the least killifish to test, with and without predation threat, for the importance of the visual similarity between the fish and the background, and the level of visual complexity of the background. We observed their choice between backgrounds patterned with elements based on the longitudinal black stripe of the fish. Predation risk was important under some circumstances, and induced a preference for a background of matching horizontal stripes compared with mismatching vertical stripes. Interestingly, females under predation threat showed a preference for a complex background of randomly oriented and overlapping stripes compared with matching stripes, whereas males did not discriminate between these two. Additionally, males showed a preference for matching stripes compared with complex shapes, whereas females did not discriminate between these backgrounds. We conclude that matching is important in the choice for safe habitat, but some aspects of visual complexity may override or act together with background matching.     

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.     

The key role of behaviour in animal camouflage

Animal camouflage represents one of the most important ways of preventing (or facilitating) predation. It attracted the attention of the earliest evolutionary biologists, and today remains a focus of investigation in areas ranging from evolutionary ecology, animal decision‐making, optimal strategies, visual psychology, computer science, to materials science. Most work focuses on the role of animal morphology per se, and its interactions with the background in affecting detection and recognition. However, the behaviour of organisms is likely to be crucial in affecting camouflage too, through background choice, body orientation and positioning; and strategies of camouflage that require movement. A wealth of potential mechanisms may affect such behaviours, from imprinting and self‐assessment to genetics, and operate at several levels (species, morph, and individual). Over many years there have been numerous studies investigating the role of behaviour in camouflage, but to date, no effort to synthesise these studies and ideas into a coherent framework. Here, we review key work on behaviour and camouflage, highlight the mechanisms involved and implications of behaviour, discuss the importance of this in a changing world, and offer suggestions for addressing the many important gaps in our understanding of this subject.     

Coral reef flounders,Bothus lunatus,choose substrates on which they can achieve camouflage with their limited body pattern repertoire

Camouflage is a common tactic to avoid detection or recognition by predators and prey. Flounders have adaptive camouflage but a limited body pattern repertoire. We tested whether peacock flounders actively select or avoid certain substrates to more effectively use their limited camouflaging ability. We acquired and analyzed ten 30‐min videos of individual flounders on a coral reef in Bonaire, Dutch Caribbean. Using Manly's beta resource selection indices, we were able to confirm that peacock flounders at this location preferred to settle on neutral‐coloured substrates, such as sand and dead coral. Moreover, they avoided live coral, cyanobacteria, and sponges, which are often brightly coloured (e.g. yellow, orange, and purple). Quantitative analyses of photographs of settled flounders indicate that they use uniform and mottled camouflage patterns, and that the small‐to‐moderate spatial scale of their physiologically controlled light and dark skin components limits their camouflage capabilities to substrates with similar colour and spatial frequencies. These fishes changed their body pattern very fast. We did not observe disruptive body patterns, which are generally characterized by large‐scale skin components and higher contrast. The results suggest that flounders are using visual information to actively choose substrates on which they can achieve general background resemblance. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 629–638.     

Adaptive change in protective coloration in adult striated shieldbugs Graphosoma lineatum (Heteroptera: Pentatomidae): test of detectability of two colour forms by avian predators

1. Protective coloration in insects may be aposematic or cryptic, and some species change defensive strategy between instars. In Sweden, the adult striated shieldbugs Graphosoma lineatum (Heteroptera: Pentatomidae) undergo a seasonal colour change from pale brown and black striation in the pre‐hibernating adults, to red and black striation in the same post‐hibernating individuals. To the human eye the pre‐hibernating adults appear cryptic against the withered late summer vegetation, whereas the red and black post‐hibernating adults appear aposematic. This suggests a possibility of a functional colour change. However, what is cryptic to the human eye is not necessarily cryptic to a potential predator. 2. Therefore we tested the effect of coloration in adult G. lineatum on their detectability for avian predators. Great tits (Parus major) were trained to eat sunflower seeds hidden inside the emptied exoskeletons of pale or red G. lineatum. Then the detection time for both colour forms was measured in a dry vegetation environment. 3. The birds required a longer time to find the pale form of G. lineatum than the red one. The pale form appears more cryptic on withered late summer vegetation than the red form, not only to the human eye but also to avian predators. The result supports the idea that the adult individuals of G. lineatum undergo a functional change from a cryptic protective coloration to an aposematic one.     

Computer vision, camouflage breaking and countershading

Camouflage is frequently used in the animal kingdom in order to conceal oneself from visual detection or surveillance. Many camouflage techniques are based on masking the familiar contours and texture of the subject by superposition of multiple edges on top of it. This work presents an operator, D arg, for the detection of three-dimensional smooth convex (or, equivalently, concave) objects. It can be used to detect curved objects on a relatively flat background, regardless of image edges, contours and texture. We show that a typical camouflage found in some animal species seems to be a 'countermeasure' taken against detection that might be based on our method. Detection by D arg is shown to be very robust, from both theoretical considerations and practical examples of real-life images.     

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, ?? , ??–??.