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.     

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.     

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.     

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 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 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.     

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 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 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 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.     

Resting orientation enhances prey survival on strongly structured background

Prey can use various camouflage types as defense against predators. One of the most common and important types is background matching, which occurs if an animal matches the background in color, brightness, and pattern. Although background matching has been studied intensively, the effects of the resting orientation of prey on the effectiveness of camouflage through background matching are not well known in natural conditions. Several past experimental studies have been conducted on resting orientation in the lab often using the visual system of humans. Their results revealed that the detection rates of predators hinge on the combination of the resting orientation of artificial moths and their background. Here, we studied whether survival rates of artificial moth-like models depend on their resting orientation in the wild where the visual conditions and detection distances vary. We used a 2 × 2 design of two resting positions of a horizontally and a vertically striped morph on tree bark. Our results show that the survival probability of moths depended mainly on the orientation of stripes relative to the vertical structure of tree bark. Thus, resting orientation relative to background affected survival. After reanalyzing Endler’s (Biol J Linn Soc 22:187–231, 1984) data on resting habitats of 317 species of North American moths, we found that horizontally striped moths occurred frequently on small herbs and tree bark. We suggest that it would be beneficial for striped moths to orient non-randomly on strongly structured background, like furrows of tree bark. We further suggest that background matching was more important than coincident disruptive coloration in determining the survival rates of our artificial moths.     

Cuttlefish camouflage: a quantitative study of patterning

To investigate camouflage design, we compared the responses of two species of cuttlefish ( Sepia officinalis and Sepia pharaonis ) with controlled but naturalistic backgrounds, consisting of mixtures of 1-mm and 9-mm diameter coloured pebbles. Quantitative analysis of image data using methods adapted from functional imaging research found differences in how the two species camouflage themselves. Whereas S. officinalis switches from background resemblance to a disruptive pattern as it moves from a fine to a coarsely patterned background particle, S. pharaonis blends the two types of pattern. We suggest that the differences may arise because S. pharaonis needs to produce camouflage that is effective when viewed over a relatively wide range of distances.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 335–345.     

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.     

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.     

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.     

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.     

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.     

Scanning eye movements of the stomatopod crustacean,Neogonodactylus oerstedii,in polarized light fields

ABSTRACT

Stomatopod crustaceans have highly mobile, independently moving compound eyes that are sensitive to both linearly and circularly polarized light. They rotate their eyes to predictable angles when viewing a linearly polarized target, and they scan their eyes frequently to sample the visual field. Angles of scans are roughly perpendicular to the plane of the midband (a set of specialized parallel rows of equatorial ommatidia). We investigated scanning eye movements in one Caribbean stomatopod species (Neogonodactylus oerstedii) in uniform visual fields that were vertically polarized, horizontally polarized, or depolarized. We found that mean eye rotation and scan angles differed significantly among these different treatments. Average scan angles differed by 12°, being more horizontal in a vertically polarized field than in a horizontally polarized one, and also more horizontal in a vertically polarized field than in a depolarized field. Thus, these stomatopods adjusted visual scanning to the polarization of the visual environment.     

Pigeons’ (Columba livia) hierarchical organization of local and global cues in touch screen tasks

Redundant encoding of local and global spatial cues is a common occurrence in many species. However, preferential use of the each type of cue seems to vary across species and tasks. In the current study, pigeons (Columba livia) were trained in three experiments on a touch screen task which included redundant local positional cues and global spatial cues. Specifically, pigeons were required to choose the middle out of three choice squares, such that the position within the array provided local information and the location on the screen provided global information. In Experiment 1, pigeons were trained and tested on vertically aligned arrays. In Experiment 2, pigeons were trained and tested on horizontally aligned arrays, and in Experiment 3, pigeons were trained and tested with vertical, horizontal and diagonally aligned arrays. The results indicate that preference for cue type depends upon the type of spatial information being encoded. Specifically, on vertical and diagonally aligned arrays, pigeons preferred global cues, whereas on horizontally aligned arrays, pigeons preferred local cues.     

Horizontal versus vertical transmission of parasites in a stochastic spatial model

A number of pathogens may be transmitted from parent to child at or before birth (vertically) or from one individual to another by contact (horizontally). A natural deterministic and non-spatial model, introduced by Lipsitch et al. [Proc. Roy. Soc. London Ser. B 260 (1995) 3211 shows that an epidemic is possible if the vertical transmission or the horizontal transmission is high enough. In contrast, we introduce a stochastic spatial model that shows that, on a particular graph, if the vertical transmission is not high enough, then the infected individuals disappear even for very high horizontal transmission. This illustrates the fact that introducing space may greatly change the qualitative behavior of a model.