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Cuttlefish use multiple camouflage tactics to evade their predators. Two common tactics are background matching (resembling the background to hinder detection) and masquerade (resembling an uninteresting or inanimate object to impede detection or recognition). We investigated how the distance and orientation of visual stimuli affected the choice of these two camouflage tactics. In the current experiments, cuttlefish were presented with three visual cues: 2D horizontal floor, 2D vertical wall, and 3D object. Each was placed at several distances: directly beneath (in a circle whose diameter was one body length (BL); at zero BL [(0BL); i.e., directly beside, but not beneath the cuttlefish]; at 1BL; and at 2BL. Cuttlefish continued to respond to 3D visual cues from a greater distance than to a horizontal or vertical stimulus. It appears that background matching is chosen when visual cues are relevant only in the immediate benthic surroundings. However, for masquerade, objects located multiple body lengths away remained relevant for choice of camouflage., (© 2015 Marine Biological Laboratory.)

We review recent research on the visual mechanisms of rapid adaptive camouflage in cuttlefish. These neurophysiologically complex marine invertebrates can camouflage themselves against almost any background, yet their ability to quickly (0.5-2 s) alter their body patterns on different visual backgrounds poses a vexing challenge: how to pick the correct body pattern amongst their repertoire. The ability of cuttlefish to change appropriately requires a visual system that can rapidly assess complex visual scenes and produce the motor responses-the neurally controlled body patterns-that achieve camouflage. Using specifically designed visual backgrounds and assessing the corresponding body patterns quantitatively, we and others have uncovered several aspects of scene variation that are important in regulating cuttlefish patterning responses. These include spatial scale of background pattern, background intensity, background contrast, object edge properties, object contrast polarity, object depth, and the presence of 3D objects. Moreover, arm postures and skin papillae are also regulated visually for additional aspects of concealment. By integrating these visual cues, cuttlefish are able to rapidly select appropriate body patterns for concealment throughout diverse natural environments. This sensorimotor approach of studying cuttlefish camouflage thus provides unique insights into the mechanisms of visual perception in an invertebrate image-forming eye.

The eyes of cuttlefish (Sepia officinalis) have a modified horizontal slit-pupil with a distinctive W-shape in bright light, while in darkness the pupil is circular. Two suggestions have previously been made for a function of the W-shape: (1) camouflaging the eye; (2) providing distance information. Since neither of these suggestions can fully explain the function of this pupil across the entire visual field, particularly the frontal and caudal periphery, we re-addressed the question of its functional significance. We took infra-red images of the eyes of live S. officinalis at different light intensities and from different viewing angles. This allowed us to determine the shape and light-admitting area of the pupil for different parts of the visual field. Our data show that the W-shaped pupil projects a blurred "W" directly onto the retina and that it effectively operates as vertical slits for the frontal and caudal parts of the visual field. We also took images of the natural habitat of S. officinalis and calculated the average vertical brightness distribution in the visual habitat. Computing a retinal illumination map shows that the W-shaped pupil is effective in balancing a vertically uneven light field: The constricted pupil reduces light from the dorsal part of the visual field significantly more than it reduces light from the horizontal band. This will cut the amount of direct sunlight that is scattered by the lens and ocular media, and thus improve image contrast particularly for the dimmer parts of the scene. We also conclude that the pupil provides even attenuation along the horizontal band, whereas a circular pupil would attenuate the image relatively more in the important frontal and caudal periphery of the visual field., (Copyright © 2013 Elsevier Ltd. All rights reserved.)

Rapid adaptive camouflage is the primary defense of soft-bodied cuttlefish. Previous studies have shown that cuttlefish body patterns are strongly influenced by visual edges in the substrate. The aim of the present study was to examine how cuttlefish body patterning is differentially controlled by various aspects of edges, including contrast polarity, contrast strength, and the presence or absence of "line terminators" introduced into a pattern when continuous edges are fragmented. Spatially high- and low-pass filtered white or black disks, as well as isolated, continuous and fragmented edges varying in contrast, were used to assess activation of cuttlefish skin components. Although disks of both contrast polarities evoked relatively weak disruptive body patterns, black disks activated different skin components than white disks, and high-frequency information alone sufficed to drive the responses to white disks whereas high- and low-frequency information were both required to drive responses to black disks. Strikingly, high-contrast edge fragments evoked substantially stronger body pattern responses than low-contrast edge fragments, whereas the body pattern responses evoked by high-contrast continuous edges were no stronger than those produced by low-contrast edges. This suggests that line terminators vs. continuous edges influence expression of disruptive body pattern components via different mechanisms that are controlled by contrast in different ways., (Copyright © 2013 Elsevier Ltd. All rights reserved.)

Cuttlefish, Sepia officinalis, commonly use their visually-guided, rapid adaptive camouflage for multiple tactics to avoid detection or recognition by predators. Two common tactics are background matching and resembling an object (masquerade) in the immediate area. This laboratory study investigated whether cuttlefish preferentially camouflage themselves to resemble a three-dimensional (3D) object in the immediate visual field (via the mechanism of masquerade/deceptive resemblance) rather than the 2D benthic substrate surrounding them (via the mechanisms of background matching or disruptive coloration). Cuttlefish were presented with a combination of benthic substrates (natural rocks or artificial checkerboard and grey printouts) and 3D objects (natural rocks or cylinders with artificial checkerboards and grey printouts glued to the outside) with visual features known to elicit each of three camouflage body pattern types (Uniform, Mottle and Disruptive). Animals were tested for a preference to show a body pattern appropriate for the 3D object or the benthic substrate. Cuttlefish responded by masquerading as the 3D object, rather than resembling the benthic substrate, only when presented with a high-contrast object on a substrate of lower contrast. Contrast is, therefore, one important cue in the cuttlefish's preference to resemble 3D objects rather than the benthic substrate., (Copyright © 2011 Elsevier Ltd. All rights reserved.)

Prey camouflage is an evolutionary response to predation pressure. Cephalopods have extensive camouflage capabilities and studying them can offer insight into effective camouflage design. Here, we examine whether cuttlefish, Sepia officinalis, show substrate or camouflage pattern preferences. In the first two experiments, cuttlefish were presented with a choice between different artificial substrates or between different natural substrates. First, the ability of cuttlefish to show substrate preference on artificial and natural substrates was established. Next, cuttlefish were offered substrates known to evoke three main camouflage body pattern types these animals show: Uniform or Mottle (function by background matching); or Disruptive. In a third experiment, cuttlefish were presented with conflicting visual cues on their left and right sides to assess their camouflage response. Given a choice between substrates they might encounter in nature, we found no strong substrate preference except when cuttlefish could bury themselves. Additionally, cuttlefish responded to conflicting visual cues with mixed body patterns in both the substrate preference and split substrate experiments. These results suggest that differences in energy costs for different camouflage body patterns may be minor and that pattern mixing and symmetry may play important roles in camouflage.

Cuttlefish and other cephalopods achieve dynamic background matching with two general classes of body patterns: uniform (or uniformly stippled) patterns and mottle patterns. Both pattern types have been described chiefly by the size scale and contrast of their skin components. Mottle body patterns in cephalopods have been characterized previously as small-to-moderate-scale light and dark skin patches (i.e. mottles) distributed somewhat evenly across the body surface. Here we move beyond this commonly accepted qualitative description by quantitatively measuring the scale and contrast of mottled skin components and relating these statistics to specific visual background stimuli (psychophysics approach) that evoke this type of background-matching pattern. Cuttlefish were tested on artificial and natural substrates to experimentally determine some primary visual background cues that evoke mottle patterns. Randomly distributed small-scale light and dark objects (or with some repetition of small-scale shapes/sizes) on a lighter substrate with moderate contrast are essential visual cues to elicit mottle camouflage patterns in cuttlefish. Lowering the mean luminance of the substrate without changing its spatial properties can modulate the mottle pattern toward disruptive patterns, which are of larger scale, different shape and higher contrast. Backgrounds throughout nature consist of a continuous range of spatial scales; backgrounds with medium-sized light/dark patches of moderate contrast are those in which cuttlefish Mottle patterns appear to be the most frequently observed.

Cuttlefish change their appearance rapidly for camouflage on different backgrounds. Effective camouflage for a benthic organism such as cuttlefish must deceive predators viewing from above as well as from the side, thus the choice of camouflage skin pattern is expected to account for horizontal and vertical background information. Previous experiments dealt only with the former, and here we explore some influences of background patterns oriented vertically in the visual background. Two experiments were conducted: (1) to determine whether cuttlefish cue visually on vertical background information; and (2) if a visual cue presented singly (either horizontally or vertically) is less, equally or more influential than a visual cue presented both horizontally and vertically. Combinations of uniform and checkerboard backgrounds (either on the bottom or wall) evoked disruptive coloration in all cases, implying that high-contrast, non-uniform backgrounds are responded to with priority over uniform backgrounds. However, there were differences in the expression of disruptive components if the checkerboard was presented simultaneously on the bottom and wall, or solely on the wall or the bottom. These results demonstrate that cuttlefish respond to visual background stimuli both in the horizontal and vertical plane, a finding that supports field observations of cuttlefish and octopus camouflage.

Disruptive body coloration is a primary camouflage tactic of cuttlefish. Because rapid changeable coloration of cephalopods is guided visually, we can present different visual backgrounds (e.g., computer-generated, two-dimensional prints) and video record the animal's response by describing and grading its body pattern. We showed previously that strength of cuttlefish disruptive patterning depends on the size, contrast, and density of discrete light elements on a homogeneous dark background. Here we report five experiments on the interactions of these and other features. Results show that Weber contrast of light background elements is--in combination with element size--a powerful determinant of disruptive response strength. Furthermore, the strength of disruptive patterning decreases with increasing mean substrate intensity (with other factors held constant). Interestingly, when element size, Weber contrast and mean substrate intensity are kept constant, strength of disruptive patterning depends on the configuration of clusters of small light elements. This study highlights the interactions of multiple features of natural microhabitats that directly influence which camouflage pattern a cuttlefish will choose.

Among the changeable camouflage patterns of cuttlefish, disruptive patterning is shown in response to certain features of light objects in the visual background. However, whether animals show disruptive patterns is dependent not only on object size but also on their body size. Here, we tested whether cuttlefish (Sepia officinalis) are able to match their disruptive body patterning with increasing size of background objects as they grow from hatchling to adult size (0.7 to 19.6 cm mantle length; factor of 28). Specifically, do cuttlefish have a single ;visual sampling rule' that scales accurately during ontogeny? For each of seven size classes of cuttlefish, we created black and white checkerboards whose check sizes corresponded to 4, 12, 40, 120, 400 and 1200% of the area of the cuttlefish's White square, which is a neurophysiologically controlled component of the skin. Disruptive body patterns were evoked when, regardless of animal size, the check size measured either 40 or 120% of the area of the cuttlefish's White square, thus demonstrating a remarkable ontogenetic conformity to a single visual sampling rule. Cuttlefish have no known visual feedback loop with which to adjust their skin patterns. Since the area of a cuttlefish's White square skin component is a function of body size, our results indicate that cuttlefish are solving a visual scaling problem of camouflage presumably without visual confirmation of the size of their own skin component.

Cephalopods behaviorally respond to polarized light. Electrophysiology experiments with the squid, Loligo pealeii, demonstrated that spike responses from individual photoreceptors are a cosine2 function of the e-vector orientation of a polarized stimulus. The discrimination limit to this polarization sensitivity depended upon the difference between the orientation of a polarized stimulus with a preferred e-vector. The limit ranged from 2 degrees to 9.2 degrees with a direct stimulus in the dark or 4.8 degrees -22.1 degrees with non-directed background illumination and the cells were least discriminative at the preferred orientations. This limit can be explained partly by the variability in anatomical alignment of microvilli in the photoreceptors around a dominant axis. A few light-sensitive retinal fibers showed no polarization sensitivity. The coding of polarization information suggests that light intensity is transformed into an average spike rate. This average results from silent periods interspersed between bursts of spikes, each burst possessing a consistent interspike interval. The variations in the length and frequency of silent periods depend upon the difference between the polarization e-vector and a preferred e-vector orientation. The minimal discriminated orientation of a squid photoreceptor agrees well with the minimum behavioral discrimination of polarized light by another cephalopod, the octopus.

We investigated some visual background features that influence young cuttlefish, Sepia pharaonis, to change their skin patterning from 'general resemblance' of the substratum to disruptive coloration that breaks up their body form. Using computer-generated black/white checkerboard patterns as substrata, we first found that the size of the white squares had to be within a certain narrow range (relative to the size of the cuttlefish 'white square') for the animal to exhibit disruptive skin patterning. Second, given the appropriate size of checker, cuttlefish regulated their disruptive skin patterns according to the contrast between white and black squares. Third, by manipulating the number of white squares on a black background, we found that as few as four white squares among 316 black squares (or 1.25%) produced disruptive patterning, yet increasing the number of white squares to 20, 40 or 80 did not increase the frequency of appearance of the cuttlefish 'white square', but only its clarity of expression. These results demonstrate that the size, contrast and number of white objects in the surrounding substratum influence the production and expression of disruptive skin patterns in young cuttlefish.