AccessScience from McGraw-Hill Education Page 1 of 7 www.accessscience.com Animal camouflage Contributed by: Chuan-Chin Chiao, Roger T. Hanlon Publication year: 2013 Visual camouflage is recognized as one of the commonest and most powerful forces in natural selection and is found in nearly every ecosystem on Earth, yet curiously it is one of the least-studied phenomena in biology. Camouflage patterns have evolved in animals of every size and shape, including both invertebrates and vertebrates, and occur in aquatic and terrestrial habitats. Camouflage is even employed at night, a seemingly odd notion until it is realized that many nocturnal predators have specialized visual systems for seeing well under lighting conditions that humans cannot perceive. In recent years, camouflage has been studied in considerable experimental detail, and some exciting new discoveries are reshaping our views of the visual mechanisms by which camouflage works. Hide in plain sight Camouflage may be achieved in three ways: background matching, disruptive coloration, and masquerade. Background matching is thought to operate by avoiding detection by the predator, whereas masquerade retards recognition of prey by the predator. Disruptive coloration seems to influence both detection and recognition processes, although few experimental data exist. There is general agreement that background matching, where the appearance generally resembles the color, lightness, and pattern of one or several background types, is one of the most common mechanisms of camouflage. For background matching to be effective, the light and dark patches of the body pattern (regardless of the type of animal) need to generally resemble the size scale and contrast of the light and dark background patches (of course, color and physical texture have to generally match as well). Except for the rare cases of a high-fidelity match, camouflage is not simply looking exactly like the background. Disruptive coloration uses a set of markings that creates the appearance of false edges and boundaries, and it hinders the detection or recognition of an object’s, or part of an object’s, true outline and shape, thus distracting the predator’s attention. The third camouflage tactic is masquerade, in which the prey may be detected as distinct from the visual background but not recognized as edible or interesting (for example, by resembling a leaf or a stick). In this deceptive resemblance, unlike background matching, animals do not generally resemble the background, but rather they actively choose to generally match visual features of objects beyond the immediate surroundings. Camouflage body pattern types The ubiquity of animal camouflage begs a basic question that has not been adequately addressed: How many body patterns for camouflage are there? One way to approach the problem is to study the animals that can best AccessScience from McGraw-Hill Education Page 2 of 7 www.accessscience.com WIDTH:DFig. 1 Three body pattern types (uniform, mottle, and disruptive) are universal for camouflage in the animal kingdom. These patterns have evolved in animals of every size and shape, including both invertebrates and vertebrates, and occur in aquatic and terrestrial habitats. change their appearance for camouflage in a wide variety of visual habitats: that is, the cephalopods (octopus, squid, and cuttlefish in the phylum Mollusca). Extensive studies of cuttlefish in the ocean and laboratory indicate, surprisingly and counterintuitively, only three basic patterning templates: namely, uniform, mottle, and disruptive. A survey of animal body patterns among thousands of camouflage images reveals similar pattern categories ( Fig. 1 ). Of course, there is variation within each broad pattern class. A chief characteristic of uniform body patterns is little or no contrast; that is, there are no light–dark demarcations that produce spots, lines, stripes, or other configurations within the body pattern. Mottle body patterns are defined as small- to moderate-scale light and dark patches (or mottles) distributed somewhat evenly and repeatedly across the body surface. Disruptive body patterns are characterized by large-scale light and dark components of multiple shapes, orientations, scales, and contrasts. Such classification into three categories is relatively new and partly controversial, but recently developed quantitative methods support the morphological and photographic evidence of just a few basic camouflage pattern types, at least in the cuttlefish (see below). Moreover, the pattern types correlate to the visual mechanisms involved with background matching and disruptive coloration, and the basic tenets of deceiving predators by interfering with their perceptual abilities for detection and recognition of prey. The overall hypothesis, based upon the concept of parsimony (the principle that the simplest scientific explanation is best), is that there is a relatively simple “visual sampling rule” for each of the few basic camouflage body pattern types. AccessScience from McGraw-Hill Education Page 3 of 7 www.accessscience.com WIDTH:DFig. 2 Octopus vulgaris reacting to a diver (predator). The initial change from camouflaged to conspicuous takes only milliseconds (ms) as a result of direct neural control of the skin. Full expression of the threat display ( right ) is 2 s. Video frame rate is 30 frames per second. [ Adapted from R. Hanlon, Cephalopod dynamic camouflage, Curr. Biol., 17(11):R400–R404, 2007; http: ∕∕ hermes.mbl.edu ∕ mrc ∕ hanlon ∕ video.html ] Cephalopod dynamic camouflage Cephalopod mollusks possess soft bodies, diverse behavior, elaborate skin patterning capabilities, and a sophisticated visual system that controls body patterning for communication and camouflage. Although most animals have a fixed or slowly changing camouflage pattern, cephalopods have evolved a different defense tactic: they use their keen vision and sophisticated skin, with direct neural control for rapid change and fine-tuned optical diversity, to rapidly adapt their body pattern for appropriate camouflage against a staggering array of visual backgrounds, including colorful coral reefs, temperate rock reefs, kelp forests, sand or mud plains, seagrass beds, and others ( Fig. 2 ). The eye as a sensor of diverse visual backgrounds Testing the visual cues that drive the adjustment of body patterning and posture is possible with cephalopods. European cuttlefish, Sepia officinalis , are particularly suited for this task because they are well adapted to laboratory environments and they are, like many shallow-water benthic (bottom-dwelling) cephalopods, behaviorally driven to camouflage themselves on almost any background; thus, both natural and artificial backgrounds can be presented to cuttlefish in order to observe their camouflaging response ( Fig. 3 ). Which properties of the background determine whether a cuttlefish will produce a uniform, mottle, or disruptive pattern? This issue has received much attention over the past decade. Three of the most important factors are (1) the spatial frequency content of the background, (2) the contrast of the background, and (3) whether or not the background contains any bright elements of roughly the same size as the cuttlefish’s “white square” (a rectangular skin patch on the dorsal mantle; lower right panel in Fig. 3). In addition, increasing substrate luminance tends to attenuate the production of disruptive patterns. The edge of objects and visual depth also provide salient cues in evoking disruptive patterns. AccessScience from McGraw-Hill Education Page 4 of 7 www.accessscience.com WIDTH:DFig. 3 A visual sensorimotor assay for probing cuttlefish ( Sepia officinalis ) perception and subsequent dynamic camouflage. Top row : Visual backgrounds with different size, contrast, edge characteristics, and arrangement are perceived by the cuttlefish, which quickly translates the information into a complex, highly coordinated body pattern type of uniform, mottle, or disruptive. Bottom row : Simple visual stimuli (such as uniformity or small to large high-contrast checkerboards) can elicit uniform, mottle, or disruptive camouflage patterns (left to right) in cuttlefish. The chief differ ence in the latter two backgrounds is the scale of the checker. Both the visual background and the body pattern can be quantified so that correlations can be made between visual input and motor output. [ Adapted from R. Hanlon, Cephalopod dynamic camouflage, Curr. Biol., 17(11):R400–R404, 2007 ] Camouflage may benefit from both optical and physical texture, with the latter being chiefly a result of the changeable skin papillae. Furthermore, arm postures of cuttlefish are often associated with three-dimensional structures (corals, algae, or kelp), and these field observations suggest that this is a visually driven response for camouflage. Camouflage in the eyes of the beholder Many visual predators have keen color perception, and thus camouflage patterns should provide some degree of color matching in addition to other visual factors such as pattern, contrast, and texture. However, most cephalopods, including the cuttlefish, lack color perception; thus, the vexing question of how they achieve color-blind camouflage still remains. Nevertheless, their color resemblance to natural visual backgrounds appears to be excellent. This is not surprising, as many of their predators, including teleost fishes, diving birds, and marine mammals, typically have dichromatic, trichromatic, or even tetrachromatic vision. Although quantifying camouflage effectiveness in the eyes of the predator is challenging,