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.     

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.     

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 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.     

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     

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.     

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.     

Quantification of cuttlefish (Sepia officinalis) camouflage: a study of color and luminance using in situ spectrometry

Cephalopods are renowned for their ability to adaptively camouflage on diverse backgrounds. Sepia officinalis camouflage body patterns have been characterized spectrally in the laboratory but not in the field due to the challenges of dynamic natural light fields and the difficulty of using spectrophotometric instruments underwater. To assess cuttlefish color match in their natural habitats, we studied the spectral properties of S. officinalis and their backgrounds on the Aegean coast of Turkey using point-by-point in situ spectrometry. Fifteen spectrometry datasets were collected from seven cuttlefish; radiance spectra from animal body components and surrounding substrates were measured at depths shallower than 5 m. We quantified luminance and color contrast of cuttlefish components and background substrates in the eyes of hypothetical di- and trichromatic fish predators. Additionally, we converted radiance spectra to sRGB color space to simulate their in situ appearance to a human observer. Within the range of natural colors at our study site, cuttlefish closely matched the substrate spectra in a variety of body patterns. Theoretical calculations showed that this effect might be more pronounced at greater depths. We also showed that a non-biological method (“Spectral Angle Mapper”), commonly used for spectral shape similarity assessment in the field of remote sensing, shows moderate correlation to biological measures of color contrast. This performance is comparable to that of a traditional measure of spectral shape similarity, hue and chroma. This study is among the first to quantify color matching of camouflaged cuttlefish in the wild.     

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.     

The preferences of the honeybee (Apis mellifera) for different visual cues during the learning process

By working with very simple images, a number of different visual cues used by the honeybee have been described over the past decades. In most of the work, the bees had no control over the choice of the images, and it was not clear whether they learned the rewarded pattern or the difference between two images. Preferences were known to exist when untrained bees selected one pattern from a variety of them, but because the preferences of the bees were ignored, it was not possible to understand how natural images displaying several cues were detected. The preferences were also essential to make a computer model of the visual system. Therefore experiments were devised to show the order of preference for the known cues in the training situation. Freely flying bees were trained to discriminate between a rewarded target with one pattern on the left side and a different one on the right, versus a white or neutral target. This arrangement gave the bees a choice of what to learn. Tests showed that in some cases they learned two or three cues simultaneously; in other cases the bees learned one, or they preferred to avoid the unrewarded target. By testing with different combinations of patterns, it was possible to put the cues into an order of preference. Of the known cues, loosely or tightly attached to eye coordinates, a black or blue spot was the most preferred, followed by strong modulation caused by edges, the orientation of parallel bars, six equally spaced spokes, a clean white target, and then a square cross and a ring. A patch of blue colour was preferred to yellow.     

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.     

Influence of visual cues on host‐searching and learning behaviour of the egg parasitoids Telenomus podisi and Trissolcus basalis

Insect parasitoids use a variety of chemical and physical cues when foraging for hosts and food. Parasitoids can learn cues that lead them to the hosts, thus contributing to better foraging. One of the cues that influence host‐searching behaviour could be colour. In this study, we investigated the ability of females of the parasitoid wasps Telenomus podisi Ashmead and Trissolcus basalis Wollaston (both Hymenoptera: Scelionidae) to respond to colours and to associate the presence of hosts – eggs of Euschistus heros (Fabricius) (Hemiptera: Pentatomidae) – with coloured substrates after training (associative learning). Two sets of experiments were conducted: in one the innate preference for substrate colours was examined, in the other associative learning of substrate colour and host presence was tested in multiple‐choice and dual‐choice experiments. In the associative learning experiments, Te. podisi and Tr. basalis were trained to respond to differently coloured substrates containing hosts in two sessions of 2 h each, with 1‐h intervals. In multiple‐choice experiments, the wasps displayed innate preference for yellow substrates over green, brown, black, or white ones. Even after being trained on substrates of different colours, both parasitoids continued to show preference for yellow substrates. The response to the colours of substrates of both parasitoids was related with the orientation to the plant foliage during the search for hosts.     

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.     

Hearing is not necessarily believing in nocturnal anurans

The recent discovery of the use of visual cues for mate choice by nocturnal acoustic species raises the important, and to date unaddressed, question of how these signals affect the outcome of mate choice predicted by female preference for male calls. In order to address this question, we presented female Hyla arborea tree frogs with a series of choices between combinations of acoustic and visual cues of varying quality in nocturnal conditions. While females exhibited the expected preference for a combination of attractive values for visual and acoustic signals over combinations of unattractive values for both signals, when presented with conflicting acoustic and visual cues, they equally adopted one of two strategies, preferring either attractive calls or intense vocal sac coloration. This constitutes novel evidence that the outcome of mate choice, as predicted on the basis of male calling quality, can be drastically different when additional communication modalities—in this case vision—are taken into account. These results also highlight the possible existence of individual variation in female rules for cue prioritization. The implications of these results for the study of mate choice in nocturnal acoustic species are discussed.     

Cryptically Patterned Moths Perceive Bark Structure When Choosing Body Orientations That Match Wing Color Pattern to the Bark Pattern

Many moths have wing patterns that resemble bark of trees on which they rest. The wing patterns help moths to become camouflaged and to avoid predation because the moths are able to assume specific body orientations that produce a very good match between the pattern on the bark and the pattern on the wings. Furthermore, after landing on a bark moths are able to perceive stimuli that correlate with their crypticity and are able to re-position their bodies to new more cryptic locations and body orientations. However, the proximate mechanisms, i.e. how a moth finds an appropriate resting position and orientation, are poorly studied. Here, we used a geometrid moth Jankowskia fuscaria to examine i) whether a choice of resting orientation by moths depends on the properties of natural background, and ii) what sensory cues moths use. We studied moths’ behavior on natural (a tree log) and artificial backgrounds, each of which was designed to mimic one of the hypothetical cues that moths may perceive on a tree trunk (visual pattern, directional furrow structure, and curvature). We found that moths mainly used structural cues from the background when choosing their resting position and orientation. Our findings highlight the possibility that moths use information from one type of sensory modality (structure of furrows is probably detected through tactile channel) to achieve crypticity in another sensory modality (visual). This study extends our knowledge of how behavior, sensory systems and morphology of animals interact to produce crypsis.     

In situ tests on inducible defenses in Dictyota kunthii and Macrocystis integrifolia (Phaeophyceae) from the Chilean coast

Numerous experimental studies have reported inducible defenses in macroalgae, but most of them have been conducted in laboratory environments where algae were maintained detached from the substratum and in artificial flow regimes. The results of those experiments might not reflect the natural situation, which can only be studied in situ. We examined whether the brown macroalgae Dictyota kunthii (C. Agardh) Greville and Macrocystis integrifolia (Bory) show inducible defenses following exposure to different grazing levels (direct, water-borne cues from nearby grazed conspecifics, presence of a non-grazing herbivore and natural grazing) in field experiments, striving to maintain natural conditions as much as possible. We measured palatability of algae after exposure to different grazing levels by using live algae and agar-based food containing non-polar extracts. M. integrifolia showed no induction of defenses (at least not of non-polar compounds), suggesting constitutive defenses, absence of defenses (tolerance) or use of another strategy to avoid herbivory. These results are similar to those from previous laboratory experiments. In D. kunthii, defense was induced after two weeks of direct grazing by amphipods under field conditions. Water-borne cues from nearby grazed conspecifics, presence of a non-grazing herbivore and natural grazing did not induce defenses. Induction of defense in response to direct grazing agrees with results from a previous laboratory study, but while indirect cues induced defenses in the laboratory, there was no measurable induced defense in the field. Probably chemical cues from grazers are diluted quickly in the field, not reaching concentrations that cause induction of defenses. This might be the reason why in some algae induction by direct grazing is a more important defensive strategy than induction by water-borne cues. The results from our study also suggest that laboratory experiments showing induced defenses in response to grazed neighbours or mere grazer presence need to be interpreted with caution.     

The Use of Artificial Benthic Collectors for Assessment of Spatial Patterns of Settlement of Megalopae of Carcinus maenas (L.) (Brachyura: Portunidae) in the Lower Mira Estuary, Portugal

Artificial benthic collectors have been widely used for the assessment of settlement rates of decapod crustaceans. However, to date no consistent works have addressed spatial patterns of settlement in different estuarine habitats, and no specific studies targeted the interaction of artificial surfaces with the surrounding natural substrate. It may be expected that the artificial surface may produce a different thigmotactic response when compared to the natural substrate, which may limit the use of this technique for assessment of natural settlement rates. In this study the settlement rates of megalopae of the estuarine crab Carcinus maenas were addressed, specifically deploying artificial benthic collectors in different habitats both intertidal and subtidal in the lower Mira estuary. A number of experiments were performed concerning stratification and temporal fluctuations of settlement. Further, the interaction of collector surface with the surrounding substrate was investigated, by comparing settlement rates in natural and artificial substrates in different habitats. Results have shown significant differences in settlement between different estuarine habitats, both in spatially replicated experiments and in a high-resolution temporal experiment. However, comparison between settlement rates in artificial and natural substrates has shown that there is a strong interference between collectors and surrounding substrate, limiting interpretation of results concerning settlement rates in artificial substrate alone.