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Camouflage is frequently used in the animal kingdom in order to conceal oneself from visual detection or surveillance. In the late 1800’s, an American artist named Abbott Thayer was the first one to make an important research on animals’ protective coloration in nature, and that became a useful tool in developing modern camouflage.
There has been a long time for biologists to study camouflage, and the numerous examples found in the animal kingdom provided them with illustrations of ideas of natural selection and adaptation. The mechanisms of camouflage include background matching, disruptive coloration and self-shadow concealment via countershading (Thayer 1909; Cott 1940). The presence of diversity of camouflage strategies is important to avoid predation which is one of the most important selection pressures. With most examples, visual camouflage involving body coloration is usually used by animals to make detection or recognition more difficult.
As experts in the art of camouflage, cephalopods – octopus, squid, and cuttlefish – are more attractive to scientists to decipher the secrets. Cephalopods show an impressive skill of changing body patterns for camouflage and signaling almost instantaneously.
It is found that the camouflage ability is mediated by pigmented chromatophore organs (sacs of red, yellow or brown pigment), structurally reflecting iridophores and light scattering leucophores in the skin. Cephalopods’ final ability to change color and pattern are by photophores. The expression of body patterns for camouflage is visually driven. The background variables involved include contrast, brightness, edge, size of objects, etc (Mathger, 2008).
Scientists have been provided with many inspirations from the study of mechanism of camouflage. It is found that the various optical coatings, paints, cosmetics and anti-counterfeiting devices are being developed by biomimeticists inspired by naturally occurring iridescent colors from iridophores in cephalopods, for example (Meadows et al, 2009).
Considering those intriguing factors, the mechanism for cephalopods camouflage is analyzed.
The outermost layer of a cephalopod’s skin allows the animal to change color. It’s full of chromatophore, consisting of pigment-containing sacs that have dozens of radial muscles attached to its periphery. These muscles are neural controlled, and nerves connect the chromatophores directly to the animal’s brain, so the creature doesn’t have to rely upon hormones or some other signaling mechanism in order to change color. The pigment sac increases or decreases in area in less than a second by contracting and relaxing the chromatophore muscles. By selectively expanding and retracting distinct groups of chromatophores, cephalopods can produce an array of patterns, such as bands, stripes and spots. It is interesting to note that many deep water forms of cephalopods possess fewer chromatophores as they are less useful in an environment in little or no light.
The next layer under the chromatophores is a reflective layer of skin made up of iridophores. Iridophores are colourless cells. These cells reflect color and are responsible for producing the metallic looking greens, blues, and silver shades in the animal’s skin. In contrast to the chromatophores that can change within a fraction of a second, iridophore reflectance changes take longer, e.g. several seconds to minutes.
The mechanism of reflectance is the same as that of colored soap bubbles. If the soap film (or multilayer plate) is very thin, shorter wavelengths are reflected, e.g. blue light; if it is thicker, longer wavelengths, such as yellow and red, are reflected. Multilayer reflectors have distinct optical features, the most obvious of which is the effect of changing the angle of observation on the spectrum of the reflected light. The reflected light is highly polarized. Many iridophores are oriented in precise ways to facilitate reflectance in specific directions. Iridophores provide a range of wavelengths that complement the yellow, red and brown pigments in the chromatophores, so that camouflage can encompass the entire visible spectrum. Additionally, some squid are able to regulate the intensity of light reflected from iridophores, and matching the intensities of the ambient light field is a key step towards achieving effective camouflage. Furthermore, the silvery iridescence that is found around the
eyes, the ink sac and the sides of the mantle suggests a role in camouflage by acting as vertically oriented mirrors. The reflective plates are tilted towards the vertical and they maximally reflect the incident light, much in the same way as silvery fish.
Most marine organisms get their reflective properties from purine crystals in their skin, but in cephalopods, reflectance arises from proteins known as reflectins. These protein form platelets within the skin, and it is to create thin-film interference for creature to manipulate incident light. Their amino acid sequence is different from that of any known protein. Four relatively rare amino acids-tyrosine, methionine, arginine, and tryptophan make up about 57% of the protein. In addition, the amino acids-alanine, leucine, isoleucine, and lysine are completely absent from that protein. In vivo, the reflectins’ structure is not fully understood. Hopefully, the study of the properties of reflectins in vitro inspires new insights for materials design and optical nanotechnology in researchers.
The innermost layer uses light-scattering leucophore cells to reflect ambient light. The leucophores look red in red light, blue in blue light, white in white, etc. It provides a sort of base coat that helps cephalopods to match their surroundings. They provide light areas that may facilitate both background matching (by resembling specific light objects in the background) and disruptive coloration (by visually breaking the body into distinct objects of high contrasting patches) (Cott 1940; Hanlon et al. 2009).
Leucophores are not physiologically active (as some iridophores are), they do not polarize light and look equally bright from all angles of view. It may aid both wavelength and intensity matching at least at a localized level in the skin and this may be particularly useful in the habitats in which shorter (blue and green) wavelengths predominate, primarily those of greater depths (Jerlov 1976).
The photophores are cephalopods’ final ability to change color and pattern. Photophores produce light by bioluminescence. For cephalopods in habitats at night and at greater depths to which daylight does not penetrate, they use luminescence for camouflage. Bioluminescence is produced by a chemical reaction similar to that of a chemical light stick. Photophores may produce light constantly or flash light intermittently. The mechanism for this is not yet known, but one theory is that the photophores can be covered up by pigments in the chromatophores when the animal does not wish for them to be present.
Colorful and Color-blind (1112)
Despite the cephalopods’ sophisticated color and pattern change, most of them (e.g. cuttlefish) are color-blind due to only one visual pigment (Marshall and Messenger, 1996; Mathger et al., 2006; Messenger, 1977). The question of how a colorblind animal can achieve camouflage in their chromatically rich environments is investigated. Lydia Mathger set up an experiment to measure the spectral reflectance of the camouflaged patterns in cuttlefish and some backgrounds by using a fiber optic spectrometer. The spectral properties of animal and background are analyzed and compared. For the theoretical treatment of color match at various depths, the assumption is that cuttlefish chose the same body pattern on a given substrate, independent of depth, so they should perceive illumination at increasing depth as becoming increasing dim. It is found that the reflectance spectra of cuttlefish correlate closely with the spectra of a small variety of natural substrates. The variations in substrate and animal skin coloration are very similar and that this may facilitate color match on natural substrates in the absence of color vision.
Camouflage-3D Texture (1111)
In addition to cephalopods’ ability of changing skin’s coloration, cuttlefish and octopus could change the physical texture of their skin through the expression of papillae. The skin could range from being smooth to very spiky. (Hanlon and Messenger 1988; Hanlon 2007). Although papillae morphology is unknown, it is likely that they rely on a muscular hydrostatic mechanism. The elasticity in the dermis could antagonize the muscle fibers that erect the papillae (W. Kier 2007, personal communication). Each papilla has a fixed maximum size but cuttlefish can control their shape and degree of expression from not expressed (i.e., invisible, skin appears flat and smooth) to fully expressed (papillae are extended maximally). Papillae are an important aspect of camouflage as they allow cuttlefish and octopus to instantly change their textural appearance; in octopus, the skin can switch from being highly papillate to completely smooth in just over 2 s (Hanlon 2007). It appears that squid do not have changeable papillae.
The question that whether the papillae expression is driven by visual stimuli is investigated. The research was done by Justine Allen to test whether visual cues alone are enough to stimulate the expression of papillae and whether there is a difference in papillae expression between Uniform/Stipple, Mottle and Disruptive body patterns. It was found that cuttlefish responded to the three-dimensional and two-dimensional version of each substrate with similar papillae expression, and fewer small dorsal papillae are expressed in disruptive camouflage patterns than in Uniform/Stipple or Mottle camouflage patterns. Cephalopods may be the only taxon with changeable papillae. Regardless, there are obviously advantages to having three-dimensional physical textures to aid camouflage, yet the visual mechanisms of how they deceive predator vision remain to be elucidated.
Reflectins, a recently identified protein family that is enriched in aromatic and sulphur-containing amino acids, are used by certain cephalopods to manage and manipulate incident light in their environment. These proteins are the predominant constituent of nanoscaled photonic structures that function in static and adaptive coloration. It is found that reflectins cast into a thin film from an ionic liquid solution will organize themselves into diffraction gratings that are defect-free over a length of several millimeters. Those suggest that reflectins could be useful for photonic applications.
Thus, various forms of camouflage have become classical examples of evolution. In a broader sense, camouflage has been adopted by humans, most notably by the military and hunters, but it has also influenced other parts of society, for example, arts, popular culture and design. The recent study showed that color-shifting cuttlefish inspires scientists to develop new TV screens.
Currently, there are a growing number of researchers interested in camouflage, producing more interdisciplinary links between biology, visual psychology, computer science and art.
Scientists are trying to decipher the secrets of cephalopod skin, hoping to find the mechanisms that make the creatures masters of disguise. Studying their artful concealment could also provide new camouflage strategies for military applications.
In summary, studying animal structural coloration is mesmerizing not only because of the sheer beauty that is created by the microscopic assemblies of reflective materials with highly precise arrangements and orientations, but also because of what we can learn from
these biophotonic structures in our efforts to produce electronic visual displays as well as various kinds of paints and coatings (e.g. Vaia & Baur 2008). Despite the recent attention to cephalopod structural coloration, many questions remain unanswered. For example, what are the behavioural functions of iridescent signals? What other structural light reflectors
are present in the diverse class Cephalopoda? Cephalopods have made their way into all the world’s oceans, including the tropics and polar waters, and even to the depths exceeding 3000 m (Hanlon & Messenger 1996), so we are likely to find more fascinating structural reflectors in the future.
Iridophores are the cells that are made up of stacks of thin protein plates that function as multilayer reflectors, whereas leucophores contain spherical protein assemblages that scatter light equally well throughout the visible, IR and UV parts of the spectrum. Changeable iridescence is not common in the animal kingdom, presumably because of the physical challenge of creating such devices. Squid are one of a few known animals that have changeable iridescence. In recent years, cephalopod iridophores and chromatophores have received interest from materials scientists who aim to model the optical properties of these structures and create synthetic materials with similar characteristics for various applications in optical nanotechnology (e.g. Crookes et al. 2004; Kramer et al. 2007; Sutherland et al. 2008a,b; Vaia & Baur 2008).
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