The predation costs of symmetrical cryptic coloration

In psychological studies of visual perception, symmetry is accepted as a potent cue in visual search for cryptic objects, yet its importance for non-human animals has been assumed rather than tested. Furthermore, while the salience of bilateral symmetry has been established in laboratory-based search tasks using human subjects, its role in more natural settings, closer to those for which such perceptual mechanisms evolved, has not, to our knowledge, been investigated previously. That said, the salience of symmetry in visual search has a plausible adaptive rationale, because biologically important objects, such as prey, predators or conspecifics, usually have a plane of symmetry that is not present in their surroundings. We tested the conspicuousness to avian predators of cryptic artificial, moth-like targets, with or without bilateral symmetry in background-matching coloration, against oak trees in the field. In two independent experiments, symmetrical targets were predated at a higher rate than otherwise identical asymmetrical targets. There was a small, but significant, fitness cost to symmetry in camouflage patterns. Given that birds are the most commonly invoked predators shaping the evolution of defensive coloration in insects, this raises the question of why bilateral asymmetry is not more common in cryptic insects.     

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.     

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.     

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.     

Change in protective coloration in the striated shieldbug <Emphasis Type="Italic">Graphosoma lineatum</Emphasis> (Heteroptera: Pentatomidae): predator avoidance and generalization among different life stages

There are two major forms of protective coloration, camouflage and warning coloration, which often entail different colour pattern characteristics. Some species change strategy between or within life stages and one such example is the striated shieldbug, Graphosoma lineatum. The larvae and the pale brownish-and-black striated pre-diapause adults are more cryptic in the late summer environment than is the red-and black striation that the adults change to after diapause in spring. Here we investigate if the more cryptic pre-diapause adult and larval coloration may affect the aposematic function of the coloration as compared to the red adult form. In a series of trials we presented fifth instar larvae, pale or red adults to shieldbug-naïve domestic chicks, Gallus gallus domesticus, to investigate the birds’ initial wariness, avoidance learning, and generalization between the three prey types. The naïve chicks found the red adults most aversive followed by pale adults, and they found the larvae the least aversive. The birds did not find the larvae unpalatable and did not learn to avoid them, while they learned to avoid the two adult forms and then to a similar degree. Birds generalized asymmetrically between life stages, positively from larvae to adults and negatively from adults to larvae. We conclude that the lower conspicuousness in the pale forms of G. lineatum may entail a reduced aposematic function, namely a reduced initial wariness in inexperienced birds. The maintenance of the colour polymorphism is discussed.     

Visual background complexity facilitates the evolution of camouflage

Abstract.— Cryptic animal coloration or camouflage is an adaptation that decreases the risk of detection. The study of the evolution of camouflage has strongly emphasized the minimization of visual information that predators receive from prey, by means of background matching. However, the evolutionary effects of information processing after its reception have been virtually ignored. I constructed a model that employs an artificial neural network and simulates the evolution of prey coloration in a visually complex and simple habitat. The model suggests: (1) the difficulty of a detection task is related to the visual complexity of the habitat; (2) it is easier to decrease the risk of detection by the means of camouflage in a visually complex habitat; (3) selection on camouflage can exploit limitations in predators information processing; and (4) there are shortcomings in using the degree of background matching as the measure of camouflage.     

Plant coloration undermines herbivorous insect camouflage

The main point of our hypothesis "coloration undermines camouflage" is that many color patterns in plants undermine the camouflage of invertebrate herbivores, especially insects, thus exposing them to predation and causing them to avoid plant organs with unsuitable coloration, to the benefit of the plants. This is a common case of "the enemy of my enemy is my friend" and a visual parallel of the chemical signals that plants emit to call wasps when attacked by caterpillars. Moreover, this is also a common natural version of the well-known case of industrial melanism, which illustrates the great importance of plant-based camouflage for herbivorous insects and can serve as an independent test for our hypothesis. We claim that the enormous variations in coloration of leaves, petioles and stems as well as of flowers and fruits undermine the camouflage of invertebrate herbivores, especially insects. We assume that the same principle might operate in certain animal-parasite interactions. Our hypothesis, however, does not contrast or exclude other previous or future explanations of specific types of plant coloration. Traits such as coloration that have more than one type of benefit may be selected for by several agents and evolve more rapidly than ones with a single type of advantage.     

Adaptive body patterning,three‐dimensional skin morphology and camouflage measures of the slender filefish Monacanthus tuckeri on a Caribbean coral reef

The slender filefish is a master of adaptive camouflage and can change its appearance within 1–3 s. Videos and photographs of this animal's cryptic body patterning and behavior were collected in situ under natural light on a Caribbean coral reef. We present an ethogram of body patterning components that includes large‐ and small‐scale spots, stripes and bars that confer a variety of cryptic patterns amidst a range of complex backgrounds. Field images were analyzed to investigate two aspects of camouflage effectiveness: (1) the degree of colour resemblance between animals and their nearby visual stimuli; and (2) the visibility of each fish's actual body outline vs. its illusory outline. Most animals more closely matched the colour of nearby visual stimuli than that of the surrounding background. Three‐dimensional dermal flaps complement the melanophore skin patterns by enhancing the complexity of the fish's physical skin texture to disguise its actual body shape, and the morphology of these structures was studied. The results suggest that the body patterns, skin texture, postures and swimming orientations putatively hinder both the detection and recognition of the fish by potential visual predators. Overall, the rapid speed of change of multiple patterns, colour blending with nearby backgrounds, and the physically complicated edge produced by dermal flaps effectively camouflage this animal among soft corals and macroalgae in the Caribbean Sea.     

Camouflage by edge enhancement in animal coloration patterns and its implications for visual mechanisms.

Animal camouflage patterns may exploit, and thus give an insight into, visual processing mechanisms. In one common type of camouflage the borders of the coloured patterns are enhanced by high contrast lines. This type of camouflage is seen on many frogs and we use it as the basis for speculating about vision in a small, frog-eating snake. It is argued that a simple categorization of intensity profiles, such as that invoked by a mechanism that detects phase-congruence, occurs at an early stage of snake vision. We show that edge-detectors using a phase-congruence strategy will be unable to distinguish between 'natural' step-edges and the enhanced border profiles commonly seen on cryptic animals, and that the camouflage will be effective over a wide range of spatial scales.     

Constrained camouflage facilitates the evolution of conspicuous warning coloration

The initial evolution of aposematic and mimetic antipredator signals is thought to be paradoxical because such coloration is expected to increase the risk of predation before reaching a stage when predators associate it effectively with a defense. We propose, however, that constraints associated with the alternative strategy, cryptic coloration, may facilitate the evolution of antipredator signals and thus provide a solution for the apparent paradox. We tested this hypothesis first using an evolutionary simulation to study the effect of a constraint due to habitat heterogeneity, and second using a phylogenetic comparison of the Lepidoptera to investigate the effect of a constraint due to prey motility. In the evolutionary simulation, antipredator warning coloration had an increased probability to invade the prey population when the evolution of camouflage was constrained by visual difference between microhabitats. The comparative study was done between day-active lepidopteran taxa, in which camouflage is constrained by motility, and night-active taxa, which rest during the day and are thus able to rely on camouflage. We compared each of seven phylogenetically independent day-active groups with a closely related nocturnal group and found that antipredator signals have evolved at least once in all the diurnal groups but in none of their nocturnal matches. Both studies lend support to our idea that constraints on crypsis may favor the evolution of antipredator warning signals.     

Seasonal changes in the dorsal coloration in the lizard Aspidoscelis costata costata (Squamata: Teiidae)

Color and color patterns in animals are important characteristics that bring protection, by dampening the ability of predators that depend on their sight to detect their preys. In lizards, the dorsal coloration plays a key role in communication of intraspecific signals such as social cues. In this study, we evaluated the seasonal changes in the dorsal coloration of the wide foraging lizard A. costata costata, in Tonatico, State of Mexico, Mexico. The seasonal evaluation included: the rainy season from mid June to mid September (can also include the end of May to early October); and the dry season for the rest of the year. The dorsal coloration of A. costata costata and their microhabitats were evaluated by contrasting the color pattern with an identification guide and the control colors of Pantone, during 11 samplings carried out from February-October 2007. Individual lizard analysis recorded snout-vent length, sex and stage (juveniles and adults). Besides, all animals were marked by toe-clipping, allowing to distinguish dorsal coloration between seasons, sex and stage. A total of 95 lizards were analyzed (53 and 42 for the dry and rainy seasons respectively). We found that the dorsal coloration in A. costata costata varies seasonally and with microhabitats: during the dry season individuals show a brown coloration whereas during the rainy season becomes greener, as the background dominant vegetation color. The results of the present study suggest that: 1) the variation in dorsal coloration in A. costata costata plays an important role in the survival (by cryptic camouflage) of this widely foraging species; 2) the changes in the dorsal coloration of A. costata costata are individually expressed traits, since the coloration of the same lizard is either brown or green depending on the season; and 3) the cryptic functions of the dorsal coloration in widely foraging species have been largely underestimated. We discuss the possible influence of the changes in coloration in an habitat that changes drastically between both dry and rainy seasons.     

Cuttlefish use visual cues to determine arm postures for camouflage

To achieve effective visual camouflage, prey organisms must combine cryptic coloration with the appropriate posture and behaviour to render them difficult to be detected or recognized. Body patterning has been studied in various taxa, yet body postures and their implementation on different backgrounds have seldom been studied experimentally. Here, we provide the first experimental evidence that cuttlefish (Sepia officinalis), masters of rapid adaptive camouflage, use visual cues from adjacent visual stimuli to control arm postures. Cuttlefish were presented with a square wave stimulus (period = 0.47 cm; black and white stripes) that was angled 0°, 45° or 90° relative to the animals' horizontal body axis. Cuttlefish positioned their arms parallel, obliquely or transversely to their body axis according to the orientation of the stripes. These experimental results corroborate our field observations of cuttlefish camouflage behaviour in which flexible, precise arm posture is often tailored to match nearby objects. By relating the cuttlefishes' visual perception of backgrounds to their versatile postural behaviour, our results highlight yet another of the many flexible and adaptive anti-predator tactics adopted by cephalopods.     

Background-matching and disruptive coloration, and the evolution of cryptic coloration

Cryptic prey coloration typically bears a resemblance to the habitat the prey uses. It has been suggested that coloration which visually matches a random sample of the background maximizes background matching. We studied this previously untested hypothesis, as well as another, little studied principle of concealment, disruptive coloration, and whether it could, acting in addition to background matching, provide another plausible means of achieving camouflage. We presented great tits (Parus major) with artificial background-matching and disruptive prey (DP), and measured detection times. First, we studied whether any random sample of a background produces equally good crypsis. This turned out to not be the case. Next, we compared the DP and the best background-matching prey and found that they were equally cryptic. We repeated the tests using prey with all the coloration elements being whole, instead of some of them being broken by the prey outline, but this did not change the result. We conclude that resemblance of the background is an important aspect of concealment, but that coloration matching a random visual sample of the background is neither sufficient nor necessary to minimize the probability of detection. Further, our study lends empirical support to the principle of disruptive coloration.     

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.     

Cuttlefish dynamic camouflage: responses to substrate choice and integration of multiple visual cues

Prey camouflage is an evolutionary response to predation pressure. Cephalopods have extensive camouflage capabilities and studying them can offer insight into effective camouflage design. Here, we examine whether cuttlefish, Sepia officinalis, show substrate or camouflage pattern preferences. In the first two experiments, cuttlefish were presented with a choice between different artificial substrates or between different natural substrates. First, the ability of cuttlefish to show substrate preference on artificial and natural substrates was established. Next, cuttlefish were offered substrates known to evoke three main camouflage body pattern types these animals show: Uniform or Mottle (function by background matching); or Disruptive. In a third experiment, cuttlefish were presented with conflicting visual cues on their left and right sides to assess their camouflage response. Given a choice between substrates they might encounter in nature, we found no strong substrate preference except when cuttlefish could bury themselves. Additionally, cuttlefish responded to conflicting visual cues with mixed body patterns in both the substrate preference and split substrate experiments. These results suggest that differences in energy costs for different camouflage body patterns may be minor and that pattern mixing and symmetry may play important roles in camouflage.     

Symmetry perception by poultry chicks and its implications for three-dimensional object recognition

Bilateral symmetry is visually salient to diverse animals including birds, but whereas experimental studies typically use bilaterally symmetrical two-dimensional patterns that are viewed approximately fronto-parallel; in nature, animals observe three-dimensional objects from all angles. Many animals and plant structures have a plane of bilateral symmetry. Here, we first (experiment I) give evidence that young poultry chicks readily generalize bilateral symmetry as a feature of two-dimensional patterns in fronto-parallel view. We then test the ability of chicks to recognize symmetry in images that would be produced by the transformed view produced by a 40° horizontal combined with a 20° vertical rotation of a pattern on a spherical surface. Experiment II gives evidence that chicks trained to distinguish symmetrical from asymmetrical patterns treat rotated views of symmetrical 'objects' as symmetrical. Experiment III gives evidence that chicks trained to discriminate rotated views of symmetrical 'objects' from asymmetrical patterns generalize to novel symmetrical objects either in fronto-parallel or rotated view. These findings emphasize the importance of bilateral symmetry for three-dimensional object recognition and raise questions about the underlying mechanisms of symmetry perception.     

Changeable cuttlefish camouflage is influenced by horizontal and vertical aspects of the visual background

Cuttlefish change their appearance rapidly for camouflage on different backgrounds. Effective camouflage for a benthic organism such as cuttlefish must deceive predators viewing from above as well as from the side, thus the choice of camouflage skin pattern is expected to account for horizontal and vertical background information. Previous experiments dealt only with the former, and here we explore some influences of background patterns oriented vertically in the visual background. Two experiments were conducted: (1) to determine whether cuttlefish cue visually on vertical background information; and (2) if a visual cue presented singly (either horizontally or vertically) is less, equally or more influential than a visual cue presented both horizontally and vertically. Combinations of uniform and checkerboard backgrounds (either on the bottom or wall) evoked disruptive coloration in all cases, implying that high-contrast, non-uniform backgrounds are responded to with priority over uniform backgrounds. However, there were differences in the expression of disruptive components if the checkerboard was presented simultaneously on the bottom and wall, or solely on the wall or the bottom. These results demonstrate that cuttlefish respond to visual background stimuli both in the horizontal and vertical plane, a finding that supports field observations of cuttlefish and octopus camouflage. Both A. Barbosa and L. Litman are first authors. An erratum to this article can be found at     

THE STRIPED COLOUR PATTERN AND STRIPED/NON-STRIPED POLYMORPHISM IN SNAKES (REPTILIA: OPHIDIA)*

The occurrence of striped colour patterns and of striped/non-striped polymorphism systems among snakes is reviewed from literature data augmented by some personal observations. Among 1367 species, 190 were striped or had striped morphs. Of 11 families, the striped pattern was common mainly among Colubridae, presumably in relation to the active escape behaviour strategy, prevalent in this family. The striped species tended to cluster in a small number of genera. The 40 striped/non-striped polymorphism systems found, fall into five categories, according to the coloration patterns of the alternative morphs: (I) blotched (cryptic); (2) barred (or ringed); (3) plain; (4) melanistic; (5) albinistic. Most polymorphisms are presumably maintained by eco-behavioural trade-offs, depending on the category and on the habitat: The striped morph is presumed more effective in active escape and sometimes also in camouflage; the alternative morph may be more effective in camouflage, in active escape or in thermoregulation. Hence morph frequency depends on the habitat. Striped-albinistic polymorphism in Elaphe climacophora presumably depends on human protection of the albino morph.     

Cuttlefish use visual cues to control three-dimensional skin papillae for camouflage

Cephalopods (octopus, squid and cuttlefish) are known for their camouflage. Cuttlefish Sepia officinalis use chromatophores and light reflectors for color change, and papillae to change three-dimensional physical skin texture. Papillae vary in size, shape and coloration; nine distinct sets of papillae are described here. The objective was to determine whether cuttlefish use visual or tactile cues to control papillae expression. Cuttlefish were placed on natural substrates to evoke the three major camouflage body patterns: Uniform/Stipple, Mottle and Disruptive. Three versions of each substrate were presented: the actual substrate, the actual substrate covered with glass (removes tactile information) and a laminated photograph of the substrate (removes tactile and three-dimensional information because depth-of-field information is unavailable). No differences in Small dorsal papillae or Major lateral mantle papillae expression were observed among the three versions of each substrate. Thus, visual (not tactile) cues drive the expression of papillae in S. officinalis. Two sets of papillae (Major lateral mantle papillae and Major lateral eye papillae) showed irregular responses; their control requires future investigation. Finally, more Small dorsal papillae were shown in Uniform/Stipple and Mottle patterns than in Disruptive patterns, which may provide clues regarding the visual mechanisms of background matching versus disruptive coloration.     

The multiple disguises of spiders: web colour and decorations, body colour and movement

Diverse functions have been assigned to the visual appearance of webs, spiders and web decorations, including prey attraction, predator deterrence and camouflage. Here, we review the pertinent literature, focusing on potential camouflage and mimicry. Webs are often difficult to detect in a heterogeneous visual environment. Static and dynamic web distortions are used to escape visual detection by prey, although particular silk may also attract prey. Recent work using physiological models of vision taking into account visual environments rarely supports the hypothesis of spider camouflage by decorations, but most often the prey attraction and predator confusion hypotheses. Similarly, visual modelling shows that spider coloration is effective in attracting prey but not in conveying camouflage. Camouflage through colour change might be used by particular crab spiders to hide from predator or prey on flowers of different coloration. However, results obtained on a non-cryptic crab spider suggest that an alternative function of pigmentation may be to avoid UV photodamage through the transparent cuticle. Numerous species are clearly efficient locomotory mimics of ants, particularly in the eyes of their predators. We close our paper by highlighting gaps in our knowledge.