[Show abstract][Hide abstract] ABSTRACT: To achieve effective visual camouflage, prey organisms must combine cryptic coloration with the appropriate posture and behaviour to render them difficult to be detected or recognized. Body patterning has been studied in various taxa, yet body postures and their implementation on different backgrounds have seldom been studied experimentally. Here, we provide the first experimental evidence that cuttlefish (Sepia officinalis), masters of rapid adaptive camouflage, use visual cues from adjacent visual stimuli to control arm postures. Cuttlefish were presented with a square wave stimulus (period = 0.47 cm; black and white stripes) that was angled 0°, 45° or 90° relative to the animals' horizontal body axis. Cuttlefish positioned their arms parallel, obliquely or transversely to their body axis according to the orientation of the stripes. These experimental results corroborate our field observations of cuttlefish camouflage behaviour in which flexible, precise arm posture is often tailored to match nearby objects. By relating the cuttlefishes' visual perception of backgrounds to their versatile postural behaviour, our results highlight yet another of the many flexible and adaptive anti-predator tactics adopted by cephalopods.
Proceedings of the Royal Society B: Biological Sciences 05/2011; 279(1726):84-90. DOI:10.1098/rspb.2011.0196 · 5.05 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Camouflage versatility is probably no better developed in the animal kingdom than in the coleoid cephalopods (octopus, squid, cuttlefish). These marine molluscs possess soft bodies, diverse behaviour, elaborate skin patterning capabilities and a sophisticated visual system that controls body patterning for communication and camouflage (Packard 1995; Hanlon & Messenger 1996; Messenger 2001). Cephalopods form a key component of the food chain and are preyed upon by nearly all of the major carnivores in the ocean – an enormous variety of marine mammals, diving birds and teleost and elasmobranch fishes. Their primary defence is visual camouflage (Hanlon & Messenger 1996). The diversity of visual systems represented by these predators is quite extraordinary and the camouflaged body patterns of cephalopods have evolved in response to these selective pressures. Benthic shallow-water cephalopods have rapid adaptive camouflage so that they can move about freely (foraging, finding mates, etc.) in multiple ecohabitats and avoid visual predation by tuning their camouflage to nearly any visual background in their natural ranges.
[Show abstract][Hide abstract] ABSTRACT: The sand-dwelling octopus Macrotritopus defilippi was filmed or photographed in five Caribbean locations mimicking the swimming behavior (posture, style, speed, duration) and coloration of the common, sand-dwelling flounder Bothus lunatus. Each species was exceptionally well camouflaged when stationary, and details of camouflaging techniques are described for M. defilippi. Octopuses implemented flounder mimicry only during swimming, when their movement would give away camouflage in this open sandy habitat. Thus, both camouflage and fish mimicry were used by the octopuses as a primary defense against visual predators. This is the first documentation of flounder mimicry by an Atlantic octopus, and only the fourth convincing case of mimicry for cephalopods, a taxon renowned for its polyphenism that is implemented mainly by neurally controlled skin patterning, but also-as shown here-by their soft flexible bodies.
[Show abstract][Hide abstract] ABSTRACT: 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.
[Show abstract][Hide abstract] ABSTRACT: 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.
Proceedings of the Royal Society B: Biological Sciences 12/2009; 277(1684):1031-9. DOI:10.1098/rspb.2009.1694 · 5.05 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Cephalopods (octopus, squid and cuttlefish) are known for their camouflage. Cuttlefish Sepia officinalis use chromatophores and light reflectors for color change, and papillae to change three-dimensional physical skin texture. Papillae vary in size, shape and coloration; nine distinct sets of papillae are described here. The objective was to determine whether cuttlefish use visual or tactile cues to control papillae expression. Cuttlefish were placed on natural substrates to evoke the three major camouflage body patterns: Uniform/Stipple, Mottle and Disruptive. Three versions of each substrate were presented: the actual substrate, the actual substrate covered with glass (removes tactile information) and a laminated photograph of the substrate (removes tactile and three-dimensional information because depth-of-field information is unavailable). No differences in Small dorsal papillae or Major lateral mantle papillae expression were observed among the three versions of each substrate. Thus, visual (not tactile) cues drive the expression of papillae in S. officinalis. Two sets of papillae (Major lateral mantle papillae and Major lateral eye papillae) showed irregular responses; their control requires future investigation. Finally, more Small dorsal papillae were shown in Uniform/Stipple and Mottle patterns than in Disruptive patterns, which may provide clues regarding the visual mechanisms of background matching versus disruptive coloration.
[Show abstract][Hide abstract] ABSTRACT: Individual cuttlefish, octopus and squid have the versatile capability to use body patterns for background matching and disruptive coloration. We define--qualitatively and quantitatively--the chief characteristics of the three major body pattern types used for camouflage by cephalopods: uniform and mottle patterns for background matching, and disruptive patterns that primarily enhance disruptiveness but aid background matching as well. There is great variation within each of the three body pattern types, but by defining their chief characteristics we lay the groundwork to test camouflage concepts by correlating background statistics with those of the body pattern. We describe at least three ways in which background matching can be achieved in cephalopods. Disruptive patterns in cuttlefish possess all four of the basic components of 'disruptiveness', supporting Cott's hypotheses, and we provide field examples of disruptive coloration in which the body pattern contrast exceeds that of the immediate surrounds. Based upon laboratory testing as well as thousands of images of camouflaged cephalopods in the field (a sample is provided on a web archive), we note that size, contrast and edges of background objects are key visual cues that guide cephalopod camouflage patterning. Mottle and disruptive patterns are frequently mixed, suggesting that background matching and disruptive mechanisms are often used in the same pattern.
Philosophical Transactions of The Royal Society B Biological Sciences 12/2008; 364(1516):429-37. DOI:10.1098/rstb.2008.0270 · 7.06 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The camouflaging abilities of cuttlefish (Sepia officinalis) are remarkable and well known. It is commonly believed that cuttlefish-although color blind-actively match various colors of their immediate surroundings, yet no quantitative data support this notion. We assembled several natural substrates chosen to evoke the three basic types of camouflaged body patterns that cuttlefish express (uniform/stipple, mottle, and disruptive) and measured the spectral reflectance of the camouflaged pattern and the respective background using a fiber optic spectrometer. We demonstrate that the reflectance spectra of cuttlefish skin patterns correlate closely with the spectra of these natural substrates. Since pigmented chromatophores play a key role in cephalopod color change, we also measured the spectral reflectance of individual cuttlefish chromatophores under the microscope, and confirm the results from a previous publication reporting three distinct colors of chromatophores (yellow, orange, and dark brown) on the animals' dorsal side. Taken together, our results show that the color variations in substrate and animal skin can be very similar and that this may facilitate color match on natural substrates in the absence of color vision.
[Show abstract][Hide abstract] ABSTRACT: Cuttlefish are cephalopod molluscs that achieve dynamic camouflage by rapidly extracting visual information from the background and neurally implementing an appropriate skin (or body) pattern. We investigated how cuttlefish body patterning responses are influenced by contrast and spatial scale by varying the contrast and the size of checkerboard backgrounds. We found that: (1) at high contrast levels, cuttlefish body patterning depended on check size; (2) for low contrast levels, body patterning was independent of "check" size; and (3) on the same check size, cuttlefish fine-tuned the contrast and fine structure of their body patterns, in response to small contrast changes in the background. Furthermore, we developed an objective, automated method of assessing cuttlefish camouflage patterns that quantitatively differentiated the three body patterns of uniform/stipple, mottle and disruptive. This study draws attention to the key roles played by background contrast and particle size in determining an effective camouflage pattern.
Vision Research 06/2008; 48(10):1242-53. DOI:10.1016/j.visres.2008.02.011 · 1.82 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: 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.
[Show abstract][Hide abstract] ABSTRACT: Cephalopods are known for their ability to change camouflage body patterns in response to changes in the visual background. Recent research has used artificial substrates such as checkerboards to investigate some specific visual cues that elicit the various camouflaged patterns in cuttlefish. In this study, we took information from experiments on artificial substrates and assembled a natural rock substrate (fixed with glue) with those features that are thought to elicit disruptive coloration in cuttlefish. The central hypothesis is that light rocks of appropriate size, substrate contrast and edge characteristics will elicit disruptive camouflage patterns in cuttlefish. By adding graded light sand in successively greater quantities to this glued rock substrate, we predicted that disruptive camouflage patterns would be replaced by progressively more uniform patterns as the visual features of rock size, contrast and edges were altered by the addition of sand. By grading the degree of disruptiveness in the animals' body patterns, we found that the results support this prediction, and that there is a strong correlation between fine details of the visual background properties and the resultant body pattern shown by the cuttlefish. Specifically, disruptive coloration was elicited (1) when one or a few light rocks of approximately the size of the animal's White square skin component were in the surrounding substrate (dark rocks alone did not elicit disruptive coloration), (2) there was moderate-to-high contrast between the light rocks and their immediate surrounds, and (3) the rock edges were well defined. Taken together, the present study provides direct evidence of several key visual features that evoke disruptive skin coloration on natural backgrounds.
[Show abstract][Hide abstract] ABSTRACT: 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.
[Show abstract][Hide abstract] ABSTRACT: We tested color perception based upon a robust behavioral response in which cuttlefish (Sepia officinalis) respond to visual stimuli (a black and white checkerboard) with a quantifiable, neurally controlled motor response (a body pattern). In the first experiment, we created 16 checkerboard substrates in which 16 grey shades (from white to black) were paired with one green shade (matched to the maximum absorption wavelength of S. officinalis' sole visual pigment, 492 nm), assuming that one of the grey shades would give a similar achromatic signal to the tested green. In the second experiment, we created a checkerboard using one blue and one yellow shade whose intensities were matched to the cuttlefish's visual system. In both assays it was tested whether cuttlefish would show disruptive coloration on these checkerboards, indicating their ability to distinguish checkers based solely on wavelength (i.e., color). Here, we show clearly that cuttlefish must be color blind, as they showed non-disruptive coloration on the checkerboards whose color intensities were matched to the Sepia visual system, suggesting that the substrates appeared to their eyes as uniform backgrounds. Furthermore, we show that cuttlefish are able to perceive objects in their background that differ in contrast by approximately 15%. This study adds support to previous reports that S. officinalis is color blind, yet the question of how cuttlefish achieve "color-blind camouflage" in chromatically rich environments still remains.
Vision Research 06/2006; 46(11):1746-53. DOI:10.1016/j.visres.2005.09.035 · 1.82 Impact Factor