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.     

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.     

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.     

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.     

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.     

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.     

Cuttlefish see shape from shading,fine-tuning coloration in response to pictorial depth cues and directional illumination

Humans use shading as a cue to three-dimensional form by combining low-level information about light intensity with high-level knowledge about objects and the environment. Here, we examine how cuttlefish Sepia officinalis respond to light and shadow to shade the white square (WS) feature in their body pattern. Cuttlefish display the WS in the presence of pebble-like objects, and they can shade it to render the appearance of surface curvature to a human observer, which might benefit camouflage. Here we test how they colour the WS on visual backgrounds containing two-dimensional circular stimuli, some of which were shaded to suggest surface curvature, whereas others were uniformly coloured or divided into dark and light semicircles. WS shading, measured by lateral asymmetry, was greatest when the animal rested on a background of shaded circles and three-dimensional hemispheres, and less on plain white circles or black/white semicircles. In addition, shading was enhanced when light fell from the lighter side of the shaded stimulus, as expected for real convex surfaces. Thus, the cuttlefish acts as if it perceives surface curvature from shading, and takes account of the direction of illumination. However, the direction of WS shading is insensitive to the directions of background shading and illumination; instead the cuttlefish tend to turn to face the light source.     

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.     

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 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.     

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     

To be seen or to hide: visual characteristics of body patterns for camouflage and communication in the Australian giant cuttlefish Sepia apama

It might seem obvious that a camouflaged animal must generally match its background whereas to be conspicuous an organism must differ from the background. However, the image parameters (or statistics) that evaluate the conspicuousness of patterns and textures are seldom well defined, and animal coloration patterns are rarely compared quantitatively with their respective backgrounds. Here we examine this issue in the Australian giant cuttlefish Sepia apama. We confine our analysis to the best-known and simplest image statistic, the correlation in intensity between neighboring pixels. Sepia apama can rapidly change their body patterns from assumed conspicuous signaling to assumed camouflage, thus providing an excellent and unique opportunity to investigate how such patterns differ in a single visual habitat. We describe the intensity variance and spatial frequency power spectra of these differing body patterns and compare these patterns with the backgrounds against which they are viewed. The measured image statistics of camouflaged animals closely resemble their backgrounds, while signaling animals differ significantly from their backgrounds. Our findings may provide the basis for a set of general rules for crypsis and signals. Furthermore, our methods may be widely applicable to the quantitative study of animal coloration.     

Freezing behaviour facilitates bioelectric crypsis in cuttlefish faced with predation risk

Cephalopods, and in particular the cuttlefish Sepia officinalis, are common models for studies of camouflage and predator avoidance behaviour. Preventing detection by predators is especially important to this group of animals, most of which are soft-bodied, lack physical defences, and are subject to both visually and non-visually mediated detection. Here, we report a novel cryptic mechanism in S. officinalis in which bioelectric cues are reduced via a behavioural freeze response to a predator stimulus. The reduction of bioelectric fields created by the freeze-simulating stimulus resulted in a possible decrease in shark predation risk by reducing detectability. The freeze response may also facilitate other non-visual cryptic mechanisms to lower predation risk from a wide range of predator types.     

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.     

Comparative morphology of changeable skin papillae in octopus and cuttlefish

A major component of cephalopod adaptive camouflage behavior has rarely been studied: their ability to change the three‐dimensionality of their skin by morphing their malleable dermal papillae. Recent work has established that simple, conical papillae in cuttlefish (Sepia officinalis) function as muscular hydrostats; that is, the muscles that extend a papilla also provide its structural support. We used brightfield and scanning electron microscopy to investigate and compare the functional morphology of nine types of papillae of different shapes, sizes and complexity in six species: S. officinalis small dorsal papillae, Octopus vulgaris small dorsal and ventral eye papillae, Macrotritopus defilippi dorsal eye papillae, Abdopus aculeatus major mantle papillae, O. bimaculoides arm, minor mantle, and dorsal eye papillae, and S. apama face ridge papillae. Most papillae have two sets of muscles responsible for extension: circular dermal erector muscles arranged in a concentric pattern to lift the papilla away from the body surface and horizontal dermal erector muscles to pull the papilla's perimeter toward its core and determine shape. A third set of muscles, retractors, appears to be responsible for pulling a papilla's apex down toward the body surface while stretching out its base. Connective tissue infiltrated with mucopolysaccharides assists with structural support. S. apama face ridge papillae are different: the contraction of erector muscles perpendicular to the ridge causes overlying tissues to buckle. In this case, mucopolysaccharide‐rich connective tissue provides structural support. These six species possess changeable papillae that are diverse in size and shape, yet with one exception they share somewhat similar functional morphologies. Future research on papilla morphology, biomechanics and neural control in the many unexamined species of octopus and cuttlefish may uncover new principles of actuation in soft, flexible tissue. J. Morphol. 275:371–390, 2014. © 2013 Wiley Periodicals, Inc.     

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.     

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.     

Adaptive body patterning,three‐dimensional skin morphology and camouflage measures of the slender filefish Monacanthus tuckeri on a Caribbean coral reef

The slender filefish is a master of adaptive camouflage and can change its appearance within 1–3 s. Videos and photographs of this animal's cryptic body patterning and behavior were collected in situ under natural light on a Caribbean coral reef. We present an ethogram of body patterning components that includes large‐ and small‐scale spots, stripes and bars that confer a variety of cryptic patterns amidst a range of complex backgrounds. Field images were analyzed to investigate two aspects of camouflage effectiveness: (1) the degree of colour resemblance between animals and their nearby visual stimuli; and (2) the visibility of each fish's actual body outline vs. its illusory outline. Most animals more closely matched the colour of nearby visual stimuli than that of the surrounding background. Three‐dimensional dermal flaps complement the melanophore skin patterns by enhancing the complexity of the fish's physical skin texture to disguise its actual body shape, and the morphology of these structures was studied. The results suggest that the body patterns, skin texture, postures and swimming orientations putatively hinder both the detection and recognition of the fish by potential visual predators. Overall, the rapid speed of change of multiple patterns, colour blending with nearby backgrounds, and the physically complicated edge produced by dermal flaps effectively camouflage this animal among soft corals and macroalgae in the Caribbean Sea.     

Use of Hyperspectral Imagery to Assess Cryptic Color Matching in Sargassum Associated Crabs

Mats of the pelagic macroalgae Sargassum represent a complex environment for the study of marine camouflage at the air-sea interface. Endemic organisms have convergently evolved similar colors and patterns, but quantitative assessments of camouflage strategies are lacking. Here, spectral camouflage of two crab species (Portunus sayi and Planes minutus) was assessed using hyperspectral imagery (HSI). Crabs matched Sargassum reflectance across blue and green wavelengths (400–550 nm) and diverged at longer wavelengths. Maximum discrepancy was observed in the far-red (i.e., 675 nm) where Chlorophyll a absorption occurred in Sargassum and not the crabs. In a quantum catch color model, both crabs showed effective color matching against blue/green sensitive dichromat fish, but were still discernible to tetrachromat bird predators that have visual sensitivity to far red wavelengths. The two species showed opposing trends in background matching with relation to body size. Variation in model parameters revealed that discrimination of crab and background was impacted by distance from the predator, and the ratio of cone cell types for bird predators. This is one of the first studies to detail background color matching in this unique, challenging ecosystem at the air-sea interface.