Perception of edges and visual texture in the camouflage of the common cuttlefish, Sepia officinalis

Abstract

The cuttlefish, Sepia officinalis, provides a fascinating opportunity to investigate the mechanisms of camouflage as it rapidly changes its body patterns in response to the visual environment. We investigated how edge information determines camouflage responses through the use of spatially high-pass filtered 'objects' and of isolated edges. We then investigated how the body pattern responds to objects defined by texture (second-order information) compared with those defined by luminance. We found that (i) edge information alone is sufficient to elicit the body pattern known as Disruptive, which is the camouflage response given when a whole object is present, and furthermore, isolated edges cause the same response; and (ii) cuttlefish can distinguish and respond to objects of the same mean luminance as the background. These observations emphasize the importance of discrete objects (bounded by edges) in the cuttlefish's choice of camouflage, and more generally imply that figure-ground segregation by cuttlefish is similar to that in vertebrates, as might be predicted by their need to produce effective camouflage against vertebrate predators.

Cuttlefish see shape from shading, fine-tuning coloration in response to pictorial depth cues and directional illumination

“…Three illumination conditions were used: from left or right (thus congruent or incongruent with shading in the case of asymmetrical stimuli), (a) White square presence A uniform grey background (stimulus 5; negative control) invariably elicited a uniform body pattern with no WS [16], whereas low-contrast circles did so in 73% of tests. These responses are expected from previous studies [11,15], and as the WS was absent, the responses were removed from subsequent analysis of WS asymmetry. Responses to black and white semicircles were more interesting.…”

“…Compared with plain white circles Sepia accentuates the shading in response to white hemispheres and also to shaded two-dimensional circles (figures 1-3). It is noteworthy that uniform circles of the same average contrast as the shaded stimuli failed to elicit a WS in 73% of tests, and instead the cuttlefish produced a uniform body pattern [16], which suggests that the animals see the shaded circles as discrete three-dimensional objects [11,15]. Evidence that the animals are not simply matching the intensity distribution on the surface is given by the observation that the asymmetry displayed in response to the black/white semicircle stimulus was no greater than to an unshaded white circle (figure 3d), and for the black/white semicircles, they were more likely to express the WS, rather than a uniform coloration pattern, when illumination was congruent with the white side of the pattern than when it was incongruent or bi-directional.…”

“…Cuttlefish, along with other cephalopods, offer a unique approach to biological vision through their ability to rapidly change their appearance for camouflage and communication [9][10][11][12]: they can display a wide range of body patterns, and their choice of pattern reports what the animal sees. Cuttlefish have excellent vision, with large eyes giving a near 3608 view of the substrate [13], and visually driven camouflage as a response to the background has been used to investigate visual edge detection, texture perception and object recognition [11,12,14,15].…”

“…Cuttlefish have excellent vision, with large eyes giving a near 3608 view of the substrate [13], and visually driven camouflage as a response to the background has been used to investigate visual edge detection, texture perception and object recognition [11,12,14,15].…”

“…Cuttlefish not only sense depth; they also asymmetrically colour the WS [22,23], which, at least for the human eye, produces pictorial shading, giving a sense of three-dimensional relief and making the WS appear convex when physically it is almost flat (figure 1c) [11,22,23]. Although we cannot be sure how a natural adversary (such as a predatory fish) would see it, the shading could enhance camouflage, either by allowing the WS to resemble a pebble in the background, or by disrupting the planar surface of the mantle and hence obscuring the animal's three-dimensional shape.…”