Disruptive Body Patterning of Cuttlefish (Sepia officinalis) Requires Visual Information Regarding Edges and Contrast of Objects in Natural Substrate Backgrounds

Abstract

Cuttlefish (Sepia officinalisLinnaeusCephalopods have a remarkable ability to change the color and pattern of their skin, and research has demonstrated that visual input regulates these changes. Cuttlefish skin can show 20 -50 chromatophore patterns that are used for both camouflage and communication (1). Cuttlefish can change their body patterns within a fraction of a second because chromatophore organs are innervated directly from the brain (2, 3). Because of its speed and diversity, body patterning in cuttlefish is the most sophisticated form of adaptive coloration in the animal kingdom (4). Although many aspects of cephalopod vision are known (5), the visual features of a given substrate that evoke adaptive coloration are relatively unstudied.Recently we developed a quantifiable behavioral assay based upon single, static, computer-generated images that allow us to control detailed aspects of visual input. With this method, we first showed that certain visual background features were used by cuttlefish to produce disruptive coloration (6). Specifically, when the size of white squares on a checkerboard was similar to that of the "White square" component in the animal's skin, the cuttlefish produced a disruptive color pattern; this response occurred over a large contrast range and required only that a few white checks be present in the visual background. A subsequent study (7) showed that, to produce disruptive body patterns for camouflage, cuttlefish cue visually on the area-not the shape or aspect ratio-of light objects in a dark substrate. Most recently, we found that if the background was composed of a high density of small light and dark objects, the cuttlefish would produce mottled skin patterns; but if the background was uniform, uniformly stippled skin patterns would be produced (8). We also applied this behavioral assay to the study of the polarization vision of cuttlefish; although the results were mixed, they indicated that cuttlefish perceive differently polarized checks as light or dark objects and

Camouflage and Perceptual Organization in the Animal Kingdom

“…In experimental aquaria, most cuttlefish patterns can indeed by classified by a combination of mottle and disruptive elements, which is comparable to the two degrees of freedom seen in the plaice (Figure 1). The 'disruptive' pattern-components, defined by expert human observers, include about ten comparatively large well-defined light and dark features, including a white square on the centre of the animal and a dark head bar (Fig 1B; Hanlon and Messenger 1988;Chiao et al 2005). The mottle pattern comprises less crisply defined features, and is comparable to the blotches used by flatfish (Hanlon and Messenger 1988).…”

Cephalopod dynamic camouflage: bridging the continuum between background matching and disruptive coloration

“…Disruptive coloration (see definition by Stevens & Merilaita 2009a,b) has not been proved experimentally in cephalopods but we posit that it occurs and we provide some evidence herein. The common European cuttlefish, Sepia officinalis, has a repertoire of 'disruptive patterns' expressed with combinations of 11 skin components (five light and six dark; details in Hanlon & Messenger 1988; see also Holmes 1940;Chiao et al 2005Chiao et al , 2007Kelman et al 2007;Mäthger et al 2007). Cott (1940) provided some basic features and capabilities of presumed disruptive patterns, yet the specific components of disruptive patterns remain to be described and defined for different taxa.…”

“…Forsythe & Hanlon 1988;Hanlon & Messenger 1988, 1996Mather & Mather 1994;Hanlon et al 1999Hanlon et al , 2007 and very recently a significant literature on laboratory experimentation with cuttlefish has begun to sort out the visual stimuli that evoke different camouflage patterns (Marshall & Messenger 1996;Chiao & Hanlon 2001a,b;Barbosa et al 2004Barbosa et al , 2007Barbosa et al , 2008aChiao et al 2005Chiao et al , 2007Mäthger et al 2006Mäthger et al , 2007Shohet et al 2006Shohet et al , 2007Kelman et al 2007Kelman et al , 2008.…”

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

“…Cuttlefish camouflage is robust; these animals will camouflage on any substrate, natural or artificial (e.g. Chiao et al 2005;Allen et al 2009;Zylinski et al 2009), regardless of the presence of a predator in the tank (J. J. Allen, L. M. Mäthger, K. C. Buresch, R. T. Hanlon et al 2009, unpublished data).…”