Justine J. Allen

Hyperspectral imaging of cuttlefish camouflage indicates good color match in the eyes of fish predators

Camouflage is a widespread phenomenon throughout nature and an important antipredator tactic in natural selection. Many visual predators have keen color perception, and thus camouflage patterns should provide some degree of color matching in addition to other visual factors such as pattern, contrast, and texture. Quantifying camouflage effectiveness in the eyes of the predator is a challenge from the perspectives of both biology and optical imaging technology. Here we take advantage of hyperspectral imaging (HSI), which records full-spectrum light data, to simultaneously visualize color match and pattern match in the spectral and the spatial domains, respectively. Cuttlefish can dynamically camouflage themselves on any natural substrate and, despite their colorblindness, produce body patterns that appear to have high-fidelity color matches to the substrate when viewed directly by humans or with RGB images. Live camouflaged cuttlefish on natural backgrounds were imaged using HSI, and subsequent spectral analysis revealed that most reflectance spectra of individual cuttlefish and substrates were similar, rendering the color match possible. Modeling color vision of potential di- and trichromatic fish predators of cuttlefish corroborated the spectral match analysis and demonstrated that camouflaged cuttlefish show good color match as well as pattern match in the eyes of fish predators. These findings (i) indicate the strong potential of HSI technology to enhance studies of biological coloration and (ii) provide supporting evidence that cuttlefish can produce color-coordinated camouflage on natural substrates despite lacking color vision.

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.

Use of commercial off-the-shelf digital cameras for scientific data acquisition and scene-specific color calibration

Commercial off-the-shelf digital cameras are inexpensive and easy-to-use instruments that can be used for quantitative scientific data acquisition if images are captured in raw format and processed so that they maintain a linear relationship with scene radiance. Here we describe the image-processing steps required for consistent data acquisition with color cameras. In addition, we present a method for scene-specific color calibration that increases the accuracy of color capture when a scene contains colors that are not well represented in the gamut of a standard color-calibration target. We demonstrate applications of the proposed methodology in the fields of biomedical engineering, artwork photography, perception science, marine biology, and underwater imaging.

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.

Mottle camouflage patterns in cuttlefish: quantitative characterization and visual background stimuli that evoke them

SUMMARY Cuttlefish and other cephalopods achieve dynamic background matching with two general classes of body patterns: uniform (or uniformly stippled) patterns and mottle patterns. Both pattern types have been described chiefly by the size scale and contrast of their skin components. Mottle body patterns in cephalopods have been characterized previously as small-to-moderate-scale light and dark skin patches (i.e. mottles) distributed somewhat evenly across the body surface. Here we move beyond this commonly accepted qualitative description by quantitatively measuring the scale and contrast of mottled skin components and relating these statistics to specific visual background stimuli (psychophysics approach) that evoke this type of background-matching pattern. Cuttlefish were tested on artificial and natural substrates to experimentally determine some primary visual background cues that evoke mottle patterns. Randomly distributed small-scale light and dark objects (or with some repetition of small-scale shapes/sizes) on a lighter substrate with moderate contrast are essential visual cues to elicit mottle camouflage patterns in cuttlefish. Lowering the mean luminance of the substrate without changing its spatial properties can modulate the mottle pattern toward disruptive patterns, which are of larger scale, different shape and higher contrast. Backgrounds throughout nature consist of a continuous range of spatial scales; backgrounds with medium-sized light/dark patches of moderate contrast are those in which cuttlefish Mottle patterns appear to be the most frequently observed.

The use of background matching vs. masquerade for camouflage in cuttlefish Sepia officinalis

Cuttlefish, Sepia officinalis, commonly use their visually-guided, rapid adaptive camouflage for multiple tactics to avoid detection or recognition by predators. Two common tactics are background matching and resembling an object (masquerade) in the immediate area. This laboratory study investigated whether cuttlefish preferentially camouflage themselves to resemble a three-dimensional (3D) object in the immediate visual field (via the mechanism of masquerade/deceptive resemblance) rather than the 2D benthic substrate surrounding them (via the mechanisms of background matching or disruptive coloration). Cuttlefish were presented with a combination of benthic substrates (natural rocks or artificial checkerboard and grey printouts) and 3D objects (natural rocks or cylinders with artificial checkerboards and grey printouts glued to the outside) with visual features known to elicit each of three camouflage body pattern types (Uniform, Mottle and Disruptive). Animals were tested for a preference to show a body pattern appropriate for the 3D object or the benthic substrate. Cuttlefish responded by masquerading as the 3D object, rather than resembling the benthic substrate, only when presented with a high-contrast object on a substrate of lower contrast. Contrast is, therefore, one important cue in the cuttlefishs preference to resemble 3D objects rather than the benthic substrate.

How does the blue-ringed octopus (Hapalochlaena lunulata) flash its blue rings?

SUMMARY The blue-ringed octopus (Hapalochlaena lunulata), one of the worlds most venomous animals, has long captivated and endangered a large audience: children playing at the beach, divers turning over rocks, and biologists researching neurotoxins. These small animals spend much of their time in hiding, showing effective camouflage patterns. When disturbed, the octopus will flash around 60 iridescent blue rings and, when strongly harassed, bite and deliver a neurotoxin that can kill a human. Here, we describe the flashing mechanism and optical properties of these rings. The rings contain physiologically inert multilayer reflectors, arranged to reflect blue–green light in a broad viewing direction. Dark pigmented chromatophores are found beneath and around each ring to enhance contrast. No chromatophores are above the ring; this is unusual for cephalopods, which typically use chromatophores to cover or spectrally modify iridescence. The fast flashes are achieved using muscles under direct neural control. The ring is hidden by contraction of muscles above the iridophores; relaxation of these muscles and contraction of muscles outside the ring expose the iridescence. This mechanism of producing iridescent signals has not previously been reported in cephalopods and we suggest that it is an exceptionally effective way to create a fast and conspicuous warning display.

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 papillas 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 papillas base contract and push the overlying tissue upward and away from the mantle surface, while horizontally arranged dermal erector muscles pull the papillas 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 papillas muscular core and the skin layer that contains the pigmented chromatophores. In extended papillae, the connective tissue layer appeared thinner above the papillas 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.

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 papillas perimeter toward its core and determine shape. A third set of muscles, retractors, appears to be responsible for pulling a papillas 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.

Night vision by cuttlefish enables changeable camouflage.

SUMMARY Because visual predation occurs day and night, many predators must have good night vision. Prey therefore exhibit antipredator behaviours in very dim light. In the field, the giant Australian cuttlefish (Sepia apama) assumes camouflaged body patterns at night, each tailored to its immediate environment. However, the question of whether cuttlefish have the perceptual capability to change their camouflage at night (as they do in day) has not been addressed. In this study, we: (1) monitored the camouflage patterns of Sepia officinalis during the transition from daytime to night-time using a natural daylight cycle and (2) tested whether cuttlefish on a particular artificial substrate change their camouflage body patterns when the substrate is changed under dim light (down to starlight, 0.003 lux) in a controlled light field in a dark room setting. We found that cuttlefish camouflage patterns are indeed adaptable at night: animals responded to a change in their visual environment with the appropriate body pattern change. Whether to deceive their prey or predators, cuttlefish use their excellent night vision to perform adaptive camouflage in dim light.