Cuttlefish use visual cues to determine arm postures for camouflage

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.     

Coral reef flounders,Bothus lunatus,choose substrates on which they can achieve camouflage with their limited body pattern repertoire

Camouflage is a common tactic to avoid detection or recognition by predators and prey. Flounders have adaptive camouflage but a limited body pattern repertoire. We tested whether peacock flounders actively select or avoid certain substrates to more effectively use their limited camouflaging ability. We acquired and analyzed ten 30‐min videos of individual flounders on a coral reef in Bonaire, Dutch Caribbean. Using Manly's beta resource selection indices, we were able to confirm that peacock flounders at this location preferred to settle on neutral‐coloured substrates, such as sand and dead coral. Moreover, they avoided live coral, cyanobacteria, and sponges, which are often brightly coloured (e.g. yellow, orange, and purple). Quantitative analyses of photographs of settled flounders indicate that they use uniform and mottled camouflage patterns, and that the small‐to‐moderate spatial scale of their physiologically controlled light and dark skin components limits their camouflage capabilities to substrates with similar colour and spatial frequencies. These fishes changed their body pattern very fast. We did not observe disruptive body patterns, which are generally characterized by large‐scale skin components and higher contrast. The results suggest that flounders are using visual information to actively choose substrates on which they can achieve general background resemblance. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 629–638.     

Disruptive coloration provides camouflage independent of background matching

Natural selection shapes the evolution of anti-predator defences, such as camouflage. It is currently contentious whether crypsis and disruptive coloration are alternative mechanisms of camouflage or whether they are interrelated anti-predator defences. Disruptively coloured prey is characterized by highly contrasting patterns to conceal the body shape, whereas cryptic prey minimizes the contrasts to background. Determining bird predation of artificial moths, we found that moths which were dissimilar from the background but sported disruptive patterns on the edge of their wings survived better in heterogeneous habitats than did moths with the same patterns inside of the wings and better than cryptic moths. Despite lower contrasts to background, crypsis did not provide fitness benefits over disruptive coloration on the body outline. We conclude that disruptive coloration on the edge camouflages its bearer independent of background matching. We suggest that this result is explainable because disruptive coloration is effective by exploiting predators' cognitive mechanisms of prey recognition and not their sensory mechanisms of signal detection. Relative to disruptive patterns on the body outline, disruptive markings on the body interior are less effective. Camouflage owing to disruptive coloration on the body interior is background-specific and is as effective as crypsis in heterogeneous habitats. Hence, we hypothesize that two proximate mechanisms explain the diversity of visual anti-predator defences. First, disruptive coloration on the body outline provides camouflage independent of the background. Second, background matching and disruptive coloration on the body interior provide camouflage, but their protection is background-specific.     

Camouflage,communication and thermoregulation: lessons from colour changing organisms

Organisms capable of rapid physiological colour change have become model taxa in the study of camouflage because they are able to respond dynamically to the changes in their visual environment. Here, we briefly review the ways in which studies of colour changing organisms have contributed to our understanding of camouflage and highlight some unique opportunities they present. First, from a proximate perspective, comparison of visual cues triggering camouflage responses and the visual perception mechanisms involved can provide insight into general visual processing rules. Second, colour changing animals can potentially tailor their camouflage response not only to different backgrounds but also to multiple predators with different visual capabilities. We present new data showing that such facultative crypsis may be widespread in at least one group, the dwarf chameleons. From an ultimate perspective, we argue that colour changing organisms are ideally suited to experimental and comparative studies of evolutionary interactions between the three primary functions of animal colour patterns: camouflage; communication; and thermoregulation.     

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.     

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     

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.     

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.     

Identifying the structure in cuttlefish visual signals

The common cuttlefish (Sepia officinalis) communicates and camouflages itself by changing its skin colour and texture. Hanlon and Messenger (1988 Phil. Trans. R. Soc. Lond. B 320, 437-487) classified these visual displays, recognizing 13 distinct body patterns. Although this conclusion is based on extensive observations, a quantitative method for analysing complex patterning has obvious advantages. We formally define a body pattern in terms of the probabilities that various skin features are expressed, and use Bayesian statistical methods to estimate the number of distinct body patterns and their visual characteristics. For the dataset of cuttlefish coloration patterns recorded in our laboratory, this statistical method identifies 12-14 different patterns, a number consistent with the 13 found by Hanlon and Messenger. If used for signalling these would give a channel capacity of 3.4 bits per pattern. Bayesian generative models might be useful for objectively describing the structure in other complex biological signalling systems.     

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.     

Cuttlefish skin papilla morphology suggests a muscular hydrostatic function for rapid changeability

Coleoid cephalopods adaptively change their body patterns (color, contrast, locomotion, posture, and texture) for camouflage and signaling. Benthic octopuses and cuttlefish possess the capability, unique in the animal kingdom, to dramatically and quickly change their skin from smooth and flat to rugose and three‐dimensional. The organs responsible for this physical change are the skin papillae, whose biomechanics have not been investigated. In this study, small dorsal papillae from cuttlefish (Sepia officinalis) were preserved in their retracted or extended state, and examined with a variety of histological techniques including brightfield, confocal, and scanning electron microscopy. Analyses revealed that papillae are composed of an extensive network of dermal erector muscles, some of which are arranged in concentric rings while others extend across each papilla's diameter. Like cephalopod arms, tentacles, and suckers, skin papillae appear to function as muscular hydrostats. The collective action of dermal erector muscles provides both movement and structural support in the absence of rigid supporting elements. Specifically, concentric circular dermal erector muscles near the papilla's base contract and push the overlying tissue upward and away from the mantle surface, while horizontally arranged dermal erector muscles pull the papilla's perimeter toward its center and determine its shape. Each papilla has a white tip, which is produced by structural light reflectors (leucophores and iridophores) that lie between the papilla's muscular core and the skin layer that contains the pigmented chromatophores. In extended papillae, the connective tissue layer appeared thinner above the papilla's apex than in surrounding areas. This result suggests that papilla extension might create tension in the overlying connective tissue and chromatophore layers, storing energy for elastic retraction. Numerous, thin subepidermal muscles form a meshwork between the chromatophore layer and the epidermis and putatively provide active papillary retraction. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.     

Hydrodynamic Analysis of C-start in Crucian Carp

The kinematics of turning maneuvers of startled Crucian Carp (Carassius auratus) are presented. All escape response observed are C-type fast-starts. The position of the center of mass and the me,merit of inertia of the fish are calculated. The results show that the position of the center of mass is always at 35% of the length of the fish from the head and the position of the center of mass and rroment of inertia can be considered unchanged during C-start of Crucian Carp. Hydro-dynamic analysis of the C-start is given based on the kinematics data from our experiments. The C-start consists of three stages. In stage 1, the tail fin of fish rapidly flaps in one direction, and a large moment acts on the fish‘s body, which rotates around the center of mass with an angular acceleration. In stage 2, the tail fin flaps more slowly in the opposite direction at slower speed, the fish‘s body rotates around the center of mass with angular deceleration and the center of mass of the fish moves along an are. In stage 3, the moment approximately equals zero, the fish‘s body stops rotating and the center of mass the moves along a straight line.     

Can't tell the caterpillars from the trees: countershading enhances survival in a woodland

Perception of the body's outline and three-dimensional shape arises from visual cues such as shading, contour, perspective and texture. When a uniformly coloured prey animal is illuminated from above by sunlight, a shadow may be cast on the body, generating a brightness contrast between the dorsal and ventral surfaces. For animals such as caterpillars, which live among flat leaves, a difference in reflectance over the body surface may degrade the degree of background matching and provide cues to shape from shading. This may make otherwise cryptic prey more conspicuous to visually hunting predators. Cryptically coloured prey are expected to match their substrate in colour, pattern and texture (though disruptive patterning is an exception), but they may also abolish self-shadowing and therefore either reduce shape cues or maintain their degree of background matching through countershading: a gradation of pigment on the body of an animal so that the surface closest to illumination is darker. In this study, we report the results from a series of field experiments where artificial prey resembling lepidopteran larvae were presented on the upper surfaces of beech tree branches so that they could be viewed by free-living birds. We demonstrate that countershading is superior to uniform coloration in terms of reducing attack by free-living predators. This result persisted even when we fixed prey to the underside of branches, simulating the resting position of many tree-living caterpillars. Our experiments provide the first demonstration, in an ecologically valid visual context, that shadowing on bodies (such as lepidopteran larvae) provides cues that visually hunting predators use to detect potential prey species, and that countershading counterbalances shadowing to enhance cryptic protection.     

Why the leopard got its spots: relating pattern development to ecology in felids

A complete explanation of the diversity of animal colour patterns requires an understanding of both the developmental mechanisms generating them and their adaptive value. However, only two previous studies, which involved computer-generated evolving prey, have attempted to make this link. This study examines variation in the camouflage patterns displayed on the flanks of many felids. After controlling for the effects of shared ancestry using a fully resolved molecular phylogeny, this study shows how phenotypes from plausible felid coat pattern generation mechanisms relate to ecology. We found that likelihood of patterning and pattern attributes, such as complexity and irregularity, were related to felids' habitats, arboreality and nocturnality. Our analysis also indicates that disruptive selection is a likely explanation for the prevalence of melanistic forms in Felidae. Furthermore, we show that there is little phylogenetic signal in the visual appearance of felid patterning, indicating that camouflage adapts to ecology over relatively short time scales. Our method could be applied to any taxon with colour patterns that can reasonably be matched to reaction-diffusion and similar models, where the kinetics of the reaction between two or more initially randomly dispersed morphogens determines the outcome of pattern development.     

Substrate colour-matching cues in the cryptic grasshopper Circotettix rabula rabula (Rehn & Hebard)

Experiments with two sympatric colour morphs of the cryptic grasshopper Circotettix rabula rabula suggest that substrate colour-matching may be achieved by a visual comparison between body colour and those backgrounds which provide crypsis. The significance of this mechanism of background matching to polymorphic species in heterogeneous environments is discussed.     

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.     

Coincident disruptive coloration

Even if an animal matches its surroundings perfectly in colour and texture, any mismatch between the spatial phase of its pattern and that of the background, or shadow created by its three-dimensional relief, is potentially revealing. Nevertheless, for camouflage to be fully broken, the shape must be recognizable. Disruptive coloration acts against object recognition by the use of high-contrast internal colour boundaries to break up shape and form. As well as the general outline, characteristic features such as eyes and limbs must also be concealed; this can be achieved by having the colour patterns on different, but adjacent, body parts aligned to match each other (i.e. in phase). Such 'coincident disruptive coloration' ensures that there is no phase disjunction where body parts meet, and causes different sections of the body to blend perceptually. We tested this theory using field experiments with predation by wild birds on artificial moth-like targets, whose wings and (edible pastry) bodies had colour patterns that were variously coincident or not. We also carried out an experiment with humans searching for analogous targets on a computer screen. Both experiments show that coincident disruptive coloration is an effective mechanism for concealing an otherwise revealing body form.     

Camouflage through an active choice of a resting spot and body orientation in moths

Cryptic colour patterns in prey are classical examples of adaptations to avoid predation, but we still know little about behaviours that reinforce the match between animal body and the background. For example, moths avoid predators by matching their colour patterns with the background. Active choice of a species‐specific body orientation has been suggested as an important function of body positioning behaviour performed by moths after landing on the bark. However, the contribution of this behaviour to moths’ crypticity has not been directly measured. From observations of geometrid moths, Hypomecis roboraria and Jankowskia fuscaria, we determined that the positioning behaviour, which consists of walking and turning the body while repeatedly lifting and lowering the wings, resulted in new resting spots and body orientations in J. fuscaria and in new resting spots in H. roboraria. The body positioning behaviour of the two species significantly decreased the probability of visual detection by humans, who viewed photographs of the moths taken before and after the positioning behaviour. This implies that body positioning significantly increases the camouflage effect provided by moth’s cryptic colour pattern regardless of whether the behaviour involves a new body orientation or not. Our study demonstrates that the evolution of morphological adaptations, such as colour pattern of moths, cannot be fully understood without taking into account a behavioural phenotype that coevolved with the morphology for increasing the adaptive value of the morphological trait.     

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.     

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.