Cuttlefish camouflage: visual perception of size, contrast and number of white squares on artificial checkerboard substrata initiates disruptive coloration
Marine Resources Center, Marine Biological Laboratory, Woods Hole, MA 02543, USA
* Present address: Howard Hughes Medical Institute, 50 Blossom Street, Wellman 429, Massachusetts General Hospital, Boston, MA 02114, USA
e-mail: rhanlon{at}mbl.edu
Accepted March 29, 2001
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Summary |
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Key words: camouflage, visual perception, sensory, colour patterns, disruptive coloration, cuttlefish, Sepia pharaonis.
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Introduction |
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Cuttlefish use tens of skin patterns for camouflage on benthic substrata, yet the repertoire can be grouped into three general categories of pattern: uniformly stippled, mottled and disruptive (Hanlon and Messenger, 1988). We measured only the extremes of this continuum, looking particularly for visual features of the substratum that would produce a change from uniformly stippled to the disruptive body patterns that can be so effective for camouflage (Fig.1). Cephalopod body patterns can be analyzed into their components, which may be postural, locomotor, textural or chromatic (Packard and Hochberg, 1977). The chromatic components, which result mostly from direct neural control of skin patterns, are discrete entities that can number 1545 in different species. There are several chromatic components that are particularly well defined and are major contributors to the disruptive patterns; these are the components White square and White mantle bar on the mantle, and the transverse White head bar (outlined in Fig.2). These chromatic components can be thought of not only as morphological units in the skin but also as physiological units in the brain (Packard, 1982). That is, expression of these morphological units is determined by the physiological units in the brain of cuttlefish that control the skin through the pathway: visual input eyes
optical lobes
lateral basal lobes
chromatophore lobes
skin. Thus, the appearance of certain chromatic components against well-defined backgrounds may give us clues about the visual perception and neural processing of body patterning. Since the major chromatic components of the disruptive body patterns of Sepia spp. are white rectangles, splotches and bars, we decided to test various features of dark and light substrata whose features we could control with some precision. A similar approach has been applied in flatfish (Ramachandran et al., 1996) to examine basic components of the skin patterns. In the present study, black/white checkerboard patterns with various sizes (experiment 1) and contrasts (experiment 2) were used to determine which visual features cuttlefish use to select disruptive patterns in the skin. Then, in experiment 3, various numbers of regularly spaced white squares in the black background were used to examine more closely the effects of background features on the expression of disruptive body patterns.
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Materials and methods |
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A simple grading scheme of patterning (Fig.2) was used to determine the responses of the animals to different substrata. The assigned grades were: 1, uniformly stippled pattern; 2, indistinct pattern; 3, disruptive pattern. We graded 1 if the animal was uniformly stippled, 3 if it clearly and distinctively showed the White square or White mantle bar on its mantle, and 2 if it showed anything in between. For example, in grade 2, there were elements of both a uniform stipple and a partial disruptive pattern (see Fig.3, Fig.4, Fig.5). Fig.2B illustrates some details of grading the White square. Often only a part of the White square on the animals mantle was expressed unilaterally (e.g. Fig.3B) or the White square itself was not uniformly white (e.g. Fig.2B, Fig.3D). We did not grade the White head bar, nor did we assess features such as the dark contrast of skin on other parts of the mantle. Grading was conducted by playing the video tape back and assigning a grade (whole integer, 13) every 10s. Thus, since all tapes lasted 60s, six grades were determined for each animal on each substratum. The mean values (and overall standard deviation) of all animals combined were plotted in the figures.
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Results |
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In experiment 1, we tested substratum checker sizes of 2.6, 6.5, 13.0, 19.5 and 26.0mm. The White square component on the dorsal mantle of the cuttlefish was approximately 1822mm (long dimension). Cuttlefish generally showed uniformly stippled body patterns when the checker size was 2.6 or 26.0mm (Fig.3A,E). Checker sizes of 6.5 and 19.5mm produced mixtures of patterning in which the White square was partially expressed (e.g. Fig.3B,D; see also Fig.2B, grade 2). With a checker size of 13.0mm, the cuttlefish almost always showed a consistent and clear expression of White square (Fig.3C,F; see also Fig.2B, grade 3). The white checkers were approximately half the size of the White square component (Fig.3C). The same trend of expression was seen in the White head bar, which is not present in Fig.3A,E, but is slightly expressed in Fig.3B,D and most strongly expressed in Fig.3C with 13.0mm squares.
In experiment 2, we altered the contrast between black and white squares by presenting checkerboards at different contrast values: 10, 20, 30, 50 and 100% (note that no unit value can be assigned since this is a relative measurement). The White square was expressed occasionally at 10% contrast (Fig.4A), but its incidence and clarity of expression increased at 20 and 30% contrast (Fig.4B,C). The clearest responses occurred at 50 and 100% contrast (Fig.4D,E). There was no clear threshold at which visual contrast suddenly induced all of the cuttlefish to produce the White square (Fig.4F). It is evident from Fig.4BD that White square could be shown in different gradations, particularly within the square. For example, Fig.4B,C were scored as 2 because there are dark stipples within the square, whereas in Fig.4D,E, a score of 3 was assigned because fewer or no stipples were present within the square, resulting in a whiter and thus stronger disruptive effect. Furthermore, note that the White head bar was not expressed at 10% contrast, slightly expressed at 20 and 30% contrast and expressed most strongly at 50 and 100% contrast.
In experiment 3, we tested various numbers of regularly spaced white squares on a black background, all with 100% contrast (note that our standard checkerboard pattern had 160 white squares and 160 black squares, each with 13.0mm sides). First, on a completely black background (i.e. no white squares; Fig.5A), no cuttlefish showed the White square component on its mantle. Second, when only four white squares were present (out of a total of 320 black and white squares, or 1.25%), some cuttlefish showed partial White squares (Fig.5B). Third, when 20 white squares (or 6.25% of the 320) were present, the White square on the mantle was shown often, albeit in various forms with other chromatic components (Fig.5C). Fourth, with increased numbers (i.e. proportions) of white squares, the frequency and clarity of expression of the White square chromatic component did not increase substantially (Fig.5D,E), as indicated by the fairly large amount of variation (note the standard deviations in Fig.5F). Note also that the White head bar was absent when no white squares were present, that it was expressed vaguely with four white squares, yet it was expressed strongly with 20 or more white squares on the substratum.
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Discussion |
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Two complementary definitions of camouflage are appropriate for cephalopods and for interpreting this laboratory study. Edmunds (Edmunds, 1974) stated that animals which are camouflaged to resemble part of the environment are said to be cryptic, while Endler (Endler, 1991) stated that colour or pattern is cryptic if it resembles a random sample of the visual background as perceived by the predator at the time and place at which the prey is most vulnerable to predation. The uniformly stippled patterns shown by cuttlefish in this study neatly fit the definition of Edmunds (Edmunds, 1974), while the disruptive patterns function in the manner described by Endler (1991). In particular, the brightness and conspicuousness of the White square are used by cuttlefish to represent a random sample of other white objects that are common in marine habitats (see Fig.1 plus numerous illustrations in) (Hanlon and Messenger, 1988).
We developed a laboratory technique, not unlike that of Marshall and Messenger (Marshall and Messenger, 1996), whereby we manipulated the visual environment to elicit certain skin patterns in young cuttlefish. This direct relationship provides the opportunity to study aspects of visual perception in a non-invasive manner. This technique is similar to the method used by Ramachandran et al. (Ramachandran et al., 1996), in which the rapid adaptive camouflage of tropical flatfish was examined. We concentrated on the ability of cuttlefishes to use other visual features to produce disruptive coloration. Our results indicate that the size, contrast and number of white squares in the black background are cues that the cuttlefish use to regulate the change from uniformly stippled skin patterns (general resemblance) to disruptive skin patterns (see Table1 for a summary of the results).
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Substratum contrast influenced disruptive patterning, although there was a good deal of variability in the results (Fig.4F). When contrast was increased from 10 to 20 to 30%, the disruptive effect increased, but the effects were more consistent above 50% contrast (Fig.4). This indicates that edge detection may play a role in assessing the pattern of the substratum. The transition from uniformly stippled to disruptive patterns also depended upon the number of regularly spaced white squares in the black background (Fig.5), indicating that the number of light objects viewed on the dark substratum is a cue to producing disruptive patterns for camouflage. As with contrast, there were large variations (Fig.5F) that may be due partly to each eye receiving different visual input depending upon its exact positioning at the time the pattern was graded. By using regularly spaced white checkerboards (rather than randomly generated and distributed ones, which we tried first), we minimized the variation that each eye was likely to receive.
Some marine flatfish are good at camouflaging themselves on substrata (e.g. Mast, 1916; Burton, 1981; Saidel, 1988) and one species, the tropical flatfish Bothus lunatus, has shown an impressive ability to match black and white substrata somewhat similar to those we used in our cuttlefish study (Ramachandran et al., 1996). The flatfish B. lunatus and our cuttlefish Sepia pharaonis responded differently to small versus larger checkerboards. Both showed uniformly stippled patterns on small checkers, but flatfish showed a mottled pattern on large squares whereas cuttlefish showed either disruptive patterns or stippled patterns depending on the checker size. Although cuttlefish possess a large repertoire of patterns, including mottled patterns, they did not use mottling because this does not camouflage as well on checkerboards as do disruptive patterns. In this respect, the more refined skin of cuttlefish (with its neural correlates) imparts a more flexible and adaptive system for camouflage than that of flatfishes. Nevertheless, both organisms provide behavioral assays (manifest through adaptive skin) that provide insights into visual perception.
From knowledge of the natural habitat of Sepia spp. (e.g. Boletzky, 1983; Hanlon and Messenger, 1988; Hanlon and Messenger, 1996), one would predict that checkerboard substrata would be extremely unnatural and challenging for cuttlefish to adapt to. Nevertheless, the cuttlefish did attempt to match these artificial substrata and respond to changes in their features. Our use of checkerboards as the substratum was appropriate only insofar as we were testing for the presence/absence of the White square component in cuttlefish.
Our results revealed two ideas worthy of future investigation. First, it is probably not the shape per se (i.e. square) that is most important to the cuttlefish for producing disruptive patterns, but the contrast and size of an object in the substratum background. Second, Fig.5BE (which shows some mottled skin patterns) provides clues about how to test for mottled patterns using various combinations of different sizes, contrasts and numbers of light objects against dark backgrounds. Further analyses of the spatial frequency components of the experimental substrata may also shed light on the mechanism of skin patterning (e.g. principal component analysis in flatfish) (Ramachandran et al., 1996) (independent component analysis in both flatfish and cuttlefish, J. C. Anderson, R. J. Baddeley, D. Osorio, N. Shashar, C. W. Tyler, V. S. Ramachadran, A. C. Crook and R. T. Hanlon, in preparation). Sepia spp. may provide a particularly good model of visual perception because the rigid mantle (due to the presence of the cuttlebone) presents an immovable and non-flexible body part that relies on fine-tuned skin patterning to achieve a wide range of optical illusions. As pointed out previously (Hanlon and Messenger, 1988), the wide range of disruptive patterns shown by Sepia spp. are carried out with five light chromatic and six dark chromatic components of patterning; we concentrated on only two of these: the White square and White head bar. Perhaps most useful for future studies is the fact that several optical principles of disruption (first mentioned by Cott, 1940) are found in Sepia spp. and are illustrated in Fig.1. These include first the principle of differential blending, achieved when some chromatic components blend with the substratum while others contrast sharply with it, thus allowing some body parts to stand out and others to fade away. In addition, the principle of maximum disruptive contrast operates when adjacent components of the pattern have great tonal contrast and, thus, provide a strong disruptive function. In another principle, that of adjacent contrast, a broken visual pattern made up of sudden transitions of color, sharply contrasted passages of tone and of irregular shapes of all kinds results in an image of multiple objects rather than parts of one form. Finally, gradations of tone within individual components such as the White square can also produce the visual illusion of relief to a human observer, giving the impression that the square is elevated or depressed, making it seem even more separate from the body. Thus, it is clear that aspects of grading the resultant skin patterning can be refined and correlated with increasingly sophisticated substrata, both of which could be quantified in a manner not attempted in this initial experiment.
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Acknowledgments |
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References |
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Boletzky, S. v. (1983). Sepia officinalis. In Cephalopod Life Cycles, vol. I, Species Accounts (ed. P. R. Boyle), pp. 3152. London: Academic Press.
Boycott, B. B. (1961). The functional organization of the brain of the cuttlefish Sepia officinalis. Proc. R. Soc. Lond. B 153, 503534.
Burton, D. (1981). Physiological responses of melanophores and xanthophores of hypophysectomized and spinal winter flounder, Pseudopleuronectes americanus Walbaum. Proc. R. Soc. Lond. B 213, 217231.
Cott, H. B. (1940). Adaptive Coloration in Animals. London: Methuen & Co., Ltd.
Edmunds, M. (1974). Defence in Animals. A Survey of Anti-Predator Defences. New York: Longman Group, Ltd.
Endler, J. A. (1991). Interactions between predator and prey. In Behavioural Ecology. An Evolutionary Approach (ed. J. R. Krebs and N. B. Davies), pp. 169196. Oxford: Blackwell Scientific Publications.
Hanlon, R. T., Forsythe, J. W. and Joneschild, D. E. (1999). 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. Biol. J. Linn. Soc. 66, 122.
Hanlon, R. T. and Messenger, J. B. (1988). Adaptive coloration in young cuttlefish (Sepia officinalis L.): The morphology and development of body patterns and their relation to behaviour. Phil. Trans. R. Soc. Lond. B 320, 437487.
Hanlon, R. T. and Messenger, J. B. (1996). Cephalopod Behaviour. Cambridge: Cambridge University Press.
Holmes, W. (1940). The colour changes and colour patterns of Sepia officinalis L. Proc. Zool. Soc., Lond. 110, 235.
Marshall, N. J. and Messenger, J. B. (1996). Colour-blind camouflage. Nature 382, 408409.[Medline]
Mast, S. O. (1916). Changes in shape, color and pattern in fishes and their bearing on the problems of adaptation and behavior, with special reference to the flounders, Paralichthys and Ancylopsetta. Bull. U.S. Bur. Fish. 34, 173238.
Messenger, J. B. (1991). Photoreception and vision in molluscs. In Evolution of the Eye and Visual System (ed. J. R. Cronly-Dillon and R. L. Gregory), pp. 364367. London: Macmillan Press.
Packard, A. (1982). Morphogenesis of chromatophore patterns in cephalopods: Are morphological and physiological units the same? Malacologia 23, 193201.
Packard, A. (1995). Organization of cephalopod chromatophore systems: A neuromuscular image-generator. In Cephalopod Neurobiology (ed. N. J. Abbott, R. Williamson and L. Maddock), pp. 331367. New York: Oxford University Press.
Packard, A. and Hochberg, F. G. (1977). Skin patterning in Octopus and other genera. Symp. Zool. Soc. Lond. 38, 191231.
Ramachandran, V. S., Tyler, C. W., Gregory, R. L., Rogers-Ramachandran, D., Duensing, S., Pillsbury, C. and Ramachandran, C. (1996). Rapid adaptive camouflage in tropical flounders. Nature 379, 815818.[Medline]
Saidel, W. M. (1988). How to be unseen: An essay in obscurity. In Sensory Biology of Aquatic Animals (ed. J. Atema, R. R. Fay, A. N. Popper and W. N. Tavolga), pp. 487513. New York: Springer-Verlag.