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

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.     

Perception of visual texture and the expression of disruptive camouflage by the cuttlefish, Sepia officinalis

Juvenile cuttlefish (Sepia officinalis) camouflage themselves by changing their body pattern according to the background. This behaviour can be used to investigate visual perception in these molluscs and may also give insight into camouflage design. Edge detection is an important aspect of vision, and here we compare the body patterns that cuttlefish produced in response to checkerboard backgrounds with responses to backgrounds that have the same spatial frequency power spectrum as the checkerboards, but randomized spatial phase. For humans, phase randomization removes visual edges. To describe the cuttlefish body patterns, we scored the level of expression of 20 separate pattern 'components', and then derived principal components (PCs) from these scores. After varimax rotation, the first component (PC1) corresponded closely to the so-called disruptive body pattern, and the second (PC2) to the mottle pattern. PC1 was predominantly expressed on checkerboards, and PC2 on phase-randomized backgrounds. Thus, cuttlefish probably have edge detectors that control the expression of disruptive pattern. Although the experiments used unnatural backgrounds, it seems probable that cuttlefish display disruptive camouflage when there are edges in the visual background caused by discrete objects such as pebbles. We discuss the implications of these findings for our understanding of disruptive camouflage.     

Color matching on natural substrates in cuttlefish, <Emphasis Type="Italic">Sepia officinalis</Emphasis>

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.     

Cuttlefish camouflage: context-dependent body pattern use during motion

It is virtually impossible to camouflage a moving target against a non-uniform background, but strategies have been proposed to reduce detection and targeting of movement. Best known is the idea that high contrast markings produce ‘motion dazzle’, which impairs judgement of speed and trajectory. The ability of the cuttlefish Sepia officinalis to change its visual appearance allows us to compare the animal''s choice of patterns during movement to the predictions of models of motion camouflage. We compare cuttlefish body patterns used during movement with those expressed when static on two background types; one of which promotes low-contrast mottle patterns and the other promotes high-contrast disruptive patterns. We find that the body pattern used during motion is context-specific and that high-contrast body pattern components are significantly reduced during movement. Thus, in our experimental conditions, cuttlefish do not use high contrast motion dazzle. It may be that, in addition to being inherently conspicuous during movement, moving high-contrast patterns will attract attention because moving particles in coastal waters tend to be of small size and of low relative contrast.     

A fish‐eye view of cuttlefish camouflage using in situ spectrometry

Cuttlefish are colour blind yet they appear to produce colour‐coordinated patterns for camouflage. Under natural in situ lighting conditions in southern Australia, we took point‐by‐point spectrometry measurements of camouflaged cuttlefish, Sepia apama, and various natural objects in the immediate visual surrounds to quantify the degree of chromatic resemblance between cuttlefish and backgrounds to potential fish predators. Luminance contrast was also calculated to determine the effectiveness of cuttlefish camouflage to this information channel both for animals with or without colour vision. Uniform body patterns on a homogeneous background of algae showed close resemblance in colour and luminance; a Uniform pattern on a partially heterogeneous background showed mixed levels of resemblance to certain background features. A Mottle pattern with some disruptive components on a heterogeneous background showed general background resemblance to some benthic objects nearest the cuttlefish. A noteworthy observation for a Disruptive body pattern on a heterogeneous background was the wide range in spectral contrasts compared to Uniform and Mottle patterns. This suggests a shift in camouflage tactic from background resemblance (which hinders detection by the predator) to more specific object resemblance and disruptive camouflage (which retards recognition). © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 535–551.     

Cuttlefish use visual cues to control three-dimensional skin papillae for camouflage

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.     

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

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.     

Adaptable night camouflage by cuttlefish

Cephalopods are well known for their diverse, quick-changing camouflage in a wide range of shallow habitats worldwide. However, there is no documentation that cephalopods use their diverse camouflage repertoire at night. We used a remotely operated vehicle equipped with a video camera and a red light to conduct 16 transects on the communal spawning grounds of the giant Australian cuttlefish Sepia apama situated on a temperate rock reef in southern Australia. Cuttlefish ceased sexual signaling and reproductive behavior at dusk and then settled to the bottom and quickly adapted their body patterns to produce camouflage that was tailored to different backgrounds. During the day, only 3% of cuttlefish were camouflaged on the spawning ground, but at night 86% (71 of 83 cuttlefish) were camouflaged in variations of three body pattern types: uniform (n=5), mottled (n=33), or disruptive (n=34) coloration. The implication is that nocturnal visual predators provide the selective pressure for rapid, changeable camouflage patterning tuned to different visual backgrounds at night.     

Changeable cuttlefish camouflage is influenced by horizontal and vertical aspects of the visual background

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. Both A. Barbosa and L. Litman are first authors. An erratum to this article can be found at     

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

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.     

Symmetrical crypsis and asymmetrical signalling in the cuttlefish Sepia officinalis

The salience of bilateral symmetry to humans has led to the suggestion that camouflage may be enhanced in asymmetrical patterns. However, the importance of bilateral symmetry in visual signals (and overall morphology) may constrain the evolution of asymmetrical camouflage, resulting in the bilaterally symmetrical cryptic patterns that we see throughout the animal kingdom. This study investigates the cuttlefish (Sepia officinalis), which can control the degree of symmetry in its coloration. Ten juvenile S. officinalis were filmed in two behavioural contexts (cryptic and threatened) to test the prediction that cryptic patterns will be expressed more asymmetrically than an anti-predator signal known as the 'deimatic display'. Cryptic body patterns, particularly those with a disruptive function, were found to exhibit a high degree of bilateral symmetry. By contrast, the components of the deimatic display were often expressed asymmetrically. These results are contrary to the predicted use of symmetry in defensive coloration, indicating that the role of symmetry in both crypsis and visual signalling is not as straightforward as previously suggested.     

Effects of early visual experience on the background preference in juvenile cuttlefish Sepia pharaonis

Although cuttlefish are capable of showing diverse camouflage body patterns against a variety of background substrates, whether they show background preference when given a choice of substrates is not well known. In this study, we characterized the background choice of post-embryonic cuttlefish (Sepia pharaonis) and examined the effects of rearing visual environments on their background preferences. Different rearing backgrounds (enriched, uniformly grey and checkerboard) were used to raise cuttlefish from eggs or hatchlings, and four sets of two-background-choice experiments (differences in contrast, shape, size and side) were conducted at day 1 and weeks 4, 8 and 12 post-hatch. Cuttlefish reared in the enriched environment preferred high-contrast backgrounds at all post-embryonic stages. In comparison, those reared in the impoverished environments (uniformly grey and checkerboard) had either reversed or delayed high-contrast background preference. In addition, cuttlefish raised on the uniformly grey background, exposed to a checkerboard briefly (0.5 or 3 h) at week 4 and tested at week 8 showed increased high-contrast background preference. Interestingly, cuttlefish in the enriched group preferred an object size similar to their body size at day 1 and week 4, but changed this preference to smaller objects at week 12. These results suggest that high-contrast backgrounds may be more adaptive for juvenile cuttlefish, and visually enriched environments are important for the development of these background preference behaviours.     

Cuttlefish Sepia officinalis Preferentially Respond to Bottom Rather than Side Stimuli When Not Allowed Adjacent to Tank Walls

Cuttlefish are cephalopods capable of rapid camouflage responses to visual stimuli. However, it is not always clear to what these animals are responding. Previous studies have found cuttlefish to be more responsive to lateral stimuli rather than substrate. However, in previous works, the cuttlefish were allowed to settle next to the lateral stimuli. In this study, we examine whether juvenile cuttlefish (Sepia officinalis) respond more strongly to visual stimuli seen on the sides versus the bottom of an experimental aquarium, specifically when the animals are not allowed to be adjacent to the tank walls. We used the Sub Sea Holodeck, a novel aquarium that employs plasma display screens to create a variety of artificial visual environments without disturbing the animals. Once the cuttlefish were acclimated, we compared the variability of camouflage patterns that were elicited from displaying various stimuli on the bottom versus the sides of the Holodeck. To characterize the camouflage patterns, we classified them in terms of uniform, disruptive, and mottled patterning. The elicited camouflage patterns from different bottom stimuli were more variable than those elicited by different side stimuli, suggesting that S. officinalis responds more strongly to the patterns displayed on the bottom than the sides of the tank. We argue that the cuttlefish pay more attention to the bottom of the Holodeck because it is closer and thus more relevant for camouflage.     

Comparison of Bayesian and empirical ranking approaches to visual perception

Much current vision research is predicated on the idea--and a rapidly growing body of evidence--that visual percepts are generated according to the empirical significance of light stimuli rather than their physical characteristics. As a result, an increasing number of investigators have asked how visual perception can be rationalized in these terms. Here, we compare two different theoretical frameworks for predicting what observers actually see in response to visual stimuli: Bayesian decision theory and empirical ranking theory. Deciding which of these approaches has greater merit is likely to determine how the statistical operations that apparently underlie visual perception are eventually understood.     

Cephalopod chromatophores: neurobiology and natural history

The chromatophores of cephalopods differ fundamentally from those of other animals: they are neuromuscular organs rather than cells and are not controlled hormonally. They constitute a unique motor system that operates upon the environment without applying any force to it. Each chromatophore organ comprises an elastic sacculus containing pigment, to which is attached a set of obliquely striated radial muscles, each with its nerves and glia. When excited the muscles contract, expanding the chromatophore; when they relax, energy stored in the elastic sacculus retracts it. The physiology and pharmacology of the chromatophore nerves and muscles of loliginid squids are discussed in detail. Attention is drawn to the multiple innervation of dorsal mantle chromatophores, of crucial importance in pattern generation. The size and density of the chromatophores varies according to habit and lifestyle. Differently coloured chromatophores are distributed precisely with respect to each other, and to reflecting structures beneath them. Some of the rules for establishing this exact arrangement have been elucidated by ontogenetic studies. The chromatophores are not innervated uniformly: specific nerve fibres innervate groups of chromatophores within the fixed, morphological array, producing 'physiological units' expressed as visible 'chromatomotor fields'. The chromatophores are controlled by a set of lobes in the brain organized hierarchically. At the highest level, the optic lobes, acting largely on visual information, select specific motor programmes (i.e. body patterns); at the lowest level, motoneurons in the chromatophore lobes execute the programmes, their activity or inactivity producing the patterning seen in the skin. In Octopus vulgaris there are over half a million neurons in the chromatophore lobes, and receptors for all the classical neurotransmitters are present, different transmitters being used to activate (or inhibit) the different colour classes of chromatophore motoneurons. A detailed understanding of the way in which the brain controls body patterning still eludes us: the entire system apparently operates without feedback, visual or proprioceptive. The gross appearance of a cephalopod is termed its body pattern. This comprises a number of components, made up of several units, which in turn contains many elements: the chromatophores themselves and also reflecting cells and skin muscles. Neural control of the chromatophores enables a cephalopod to change its appearance almost instantaneously, a key feature in some escape behaviours and during agonistic signalling. Equally important, it also enables them to generate the discrete patterns so essential for camouflage or for signalling. The primary function of the chromatophores is camouflage. They are used to match the brightness of the background and to produce components that help the animal achieve general resemblance to the substrate or break up the body's outline. Because the chromatophores are neurally controlled an individual can, at any moment, select and exhibit one particular body pattern out of many. Such rapid neural polymorphism ('polyphenism') may hinder search-image formation by predators. Another function of the chromatophores is communication. Intraspecific signalling is well documented in several inshore species, and interspecific signalling, using ancient, highly conserved patterns, is also widespread. Neurally controlled chromatophores lend themselves supremely well to communication, allowing rapid, finely graded and bilateral signalling.     

Signaling to the enemy? Body pattern expression and its response to external cues during hunting in the cuttlefish Sepia officinalis (Cephalopoda)

Cuttlefish can rapidly alter their appearance by using neurally controlled chromatophore organs. This ability may provide a window into their cognitive capacity. We test whether the changes in body pattern that occur during hunting depend on context. If they do, then it may be possible to use these changes to study cephalopod cognition while the animal is engaged in ecologically relevant tasks. We found consistent individual differences in the tendency of cuttlefish to hunt with the first two arms raised. We also found that cuttlefish usually darken their skin after they seize a prey item. This darkening is observed regardless of the identity of the prey (fish, crab, or shrimp), prey context (buried in sand, in a bare tank, or on top of a rock pile), or the presence of a sudden stimulus. The sudden stimulus was created by presenting an overhead model bird to the cuttlefish. The model induced components of the Deimatic Display, which is a form of antipredator behavior, suggesting that the model was perceived as a potential threat. Passing Cloud displays and the Darkening of the arms were significantly reduced after exposure to the model bird. The effect of a potential predator on body pattern expression during hunting suggests it may be possible to use these changes as a sensitive indicator of ecologically relevant learning.     

The stem cell population of the human colon crypt: analysis via methylation patterns

The analysis of methylation patterns is a promising approach to investigate the genealogy of cell populations in an organism. In a stem cell–niche scenario, sampled methylation patterns are the stochastic outcome of a complex interplay between niche structural features such as the number of stem cells within a niche and the niche succession time, the methylation/demethylation process, and the randomness due to sampling. As a consequence, methylation pattern studies can reveal niche characteristics but also require appropriate statistical methods. The analysis of methylation patterns sampled from colon crypts is a prototype of such a study. Previous analyses were based on forward simulation of the cell content of the whole crypt and subsequent comparisons between simulated and experimental data using a few statistics as a proxy to summarize the data. In this paper we develop a more powerful method to analyze these data based on coalescent modelling and Bayesian inference. Results support a scenario where the colon crypt is maintained by a high number of stem cells; the posterior indicates a number greater than eight and the posterior mode is between 15 and 20. The results also provide further evidence for synergistic effects in the methylation/demethylation process that could for the first time be quantitatively assessed through their long-term consequences such as the coexistence of hypermethylated and hypomethylated patterns in the same colon crypt.     

Comparing entire colour patterns as birds see them

Colour patterns and their visual backgrounds consist of a mosaic of patches that vary in colour, brightness, size, shape and position. Most studies of crypsis, aposematism, sexual selection, or other forms of signalling concentrate on one or two patch classes (colours), either ignoring the rest of the colour pattern, or analysing the patches separately. We summarize methods of comparing colour patterns making use of known properties of bird eyes. The methods are easily modifiable for other animal visual systems. We present a new statistical method to compare entire colour patterns rather than comparing multiple pairs of patches. Unlike previous methods, the new method detects differences in the relationships among the colours, not just differences in colours. We present tests of the method's ability to detect a variety of kinds of differences between natural colour patterns and provide suggestions for analysis.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 405–431.     

It pays to cheat: tactical deception in a cephalopod social signalling system

Signals in intraspecific communication should be inherently honest; otherwise the system is prone to collapse. Theory predicts, however, that honest signalling systems are susceptible to invasion by cheats, the extent of which is largely mediated by fear of reprisal. Cuttlefish facultatively change their shape and colour, an ability that evolved to avoid predators and capture prey. Here, we show that this ability is tactically employed by male mourning cuttlefish (Sepia plangon) to mislead conspecifics during courtship in a specific social context amenable to cheating 39 per cent of the time, while it was never employed in other social contexts. Males deceive rival males by displaying male courtship patterns to receptive females on one side of the body, and simultaneously displaying female patterns to a single rival male on the other, thus preventing the rival from disrupting courtship. The use of tactical deception in such a complex communication network indicates that sociality has played a key role in the cognitive evolution of cephalopods.     

Visual interpolation for contour completion by the European cuttlefish (Sepia officinalis) and its use in dynamic camouflage

Cuttlefish rapidly change their appearance in order to camouflage on a given background in response to visual parameters, giving us access to their visual perception. Recently, it was shown that isolated edge information is sufficient to elicit a body pattern very similar to that used when a whole object is present. Here, we examined contour completion in cuttlefish by assaying body pattern responses to artificial backgrounds of 'objects' formed from fragmented circles, these same fragments rotated on their axis, and with the fragments scattered over the background, as well as positive (full circles) and negative (homogenous background) controls. The animals displayed similar responses to the full and fragmented circles, but used a different body pattern in response to the rotated and scattered fragments. This suggests that they completed the broken circles and recognized them as whole objects, whereas rotated and scattered fragments were instead interpreted as small, individual objects in their own right. We discuss our findings in the context of achieving accurate camouflage in the benthic shallow-water environment.