Adaptive coloration in young cuttlefish ( Sepia officinalis L.): the morphology and development of body patterns and their relation to behaviour

Abstract

Young Sepia officinalis (0-5 months) were studied in the laboratory and in the sea, and their appearance and behaviour compared with that of adult animals. Cuttlefish lay large eggs and the hatchlings are miniature replicas of the adults. From the moment of hatching they show body patterns as complex as those of adults and far more elaborate than those shown by most juvenile cephalopods. There are 13 body patterns: 6 of these are ‘chronic’ (lasting for minutes or hours) and 7 are ‘acute’ (lasting for seconds or minutes). The patterns are built up from no fewer than 34 chromatic, 6 textural, 8 postural and 6 locomotor components, used in varying combinations and intensities of expression. Nearly all these components occur in young animals: 26 of the chromatic, all the textural and locomotor, and 6 of the postural components. Nevertheless, patterning does change with age and we have recorded this and correlated the changes with behaviour. The components are built up from units, which themselves comprise four elements organized in precise relation to one another: chromatophores, iridophores, leucophores and skin muscles. The chromatophores are always especially important: they are muscular organs innervated directly from the brain and controlled ultimately by the highest centres (optic lobes). The areas in the Sepia brain that control patterning are already well developed at hatching, for the appearance of the skin is as much part of the brain’s motor program as is the attitude of the arms or fins, or the posture of the entire animal. The iridophores and leucophores develop later and are especially important constituents of many adult patterns, notably the Intense Zebra of the mature male. Experiments confirm that patterning is neurally controlled and apparently mediated exclusively by the visual system. Young cuttlefish use patterning primarily for concealment, utilizing such strategies as general colour resemblance, disruptive coloration, obliterative shading, shadow elimination, disguise and adaptive behaviour. Older animals also conceal themselves but increasingly use patterns for signalling, both interspecifically (warning or ‘deimatic’ displays) and intraspecifically (sexual signalling). Laboratory-reared cuttlefish were released in the sea and observed underwater. They quickly and effectively concealed themselves on the substrate; it was easy for the human observer to lose them and many passing fish behaved as if they were not there. One local predator, Serranus cabrilla , was observed to attack them and no fewer than 35 attacks were recorded, only six of which were successful. Laboratory-reared cuttlefish apparently distinguished between these predators and other, non-predatory, fish the first time they encountered them in nature.

Camouflage and Perceptual Organization in the Animal Kingdom

“…European cuttlefish (Sepia officinalis) body patterns are produced by the controlled expression of about 40 visual features known as behavioural components, and they can also control the physical texture of their skin (Hanlon & Messenger 1988). The level of expression of each component can be varied in a continuous manner (Kelman et al 2008).…”

“…In experimental aquaria, most cuttlefish patterns can indeed by classified by a combination of mottle and disruptive elements, which is comparable to the two degrees of freedom seen in the plaice (Figure 1). The 'disruptive' pattern-components, defined by expert human observers, include about ten comparatively large well-defined light and dark features, including a white square on the centre of the animal and a dark head bar (Fig 1B; Hanlon and Messenger 1988;Chiao et al 2005). The mottle pattern comprises less crisply defined features, and is comparable to the blotches used by flatfish (Hanlon and Messenger 1988).…”

“…At present, however, the way in which the expression of these patterns is coordinated, and the full range of camouflage patterns produced in natural conditions, remains poorly studied. Hanlon and Messenger (1988) suggested that five main body patterns are used for camouflage. These were called: Uniform Light, Stipple, Light Mottle, Dark Mottle and Disruptive.…”

Giant Australian cuttlefish use mutual assessment to resolve male-male contests

“…This provided a clear view of the stimulus male 246 by the focal male, while inducing display behaviour by the live-male stimulus towards his 247 reflection. Cuttlefish generally respond aggressively to opponents of similar size and also to 248 mirror images (see Hanlon & Messenger, 1988). The one-way mirror configuration meant that 249…”

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

“…The cuttlefish coordinate the expression of some 40 discrete visual features on the skin, known as behavioural components, to produce a number of distinct (though variable) body patterns [16]. In particular, on backgrounds containing discrete objects such as pebbles or printed circles cuttlefish often display disruptive body patterns (figure 1c) [14], which often include the white square (WS) component (figure 1c).…”