Pattern Recognition Letters 28 (2007) 1854–1864 www.elsevier.


Body patterns in cephalopods ‘‘Polyphenism’’ as a way of information exchange
Maria Barbato a, Marco Bernard b, Luciana Borrelli a, Graziano Fiorito


Laboratorio di Neurobiologia, Stazione Zoologica A. Dohrn, Villa Comunale, 80121 Napoli, Italy b Archivio Storico, Stazione Zoologica A. Dohrn, Villa Comunale, 80121 Napoli, Italy Available online 12 March 2007

Abstract Here we overview the knowledge available on polyphenism in cephalopods: a peculiar characteristic of the behaviour of octopus, cuttlefish and squid. This is achieved through body patterning that is the mutable appearance of the skin of these species. After a short account on the organization of patterning and on the functions of this feature of cephalopods’ behavioural repertoire, we discuss some preliminary evidence on the causation of this complex form of communication (either dishonest or in terms of signalling). Ó 2007 Elsevier B.V. All rights reserved.
Keywords: Communication; Behavior; Signals; Body patterns; Cephalopods; Mollusca; Invertebrates

1. Prologue Humans exchange a great deal of information by different modalities: the main vehicle being language.1 As reviewed by Cancho and Sole (2001), the human language derives from a virtually infinite range of combinations of a limited set of units (i.e. words). These ‘‘interact in many ways. Some words co-occur with certain words at a higher probability than with others and co-occurrence is not trivial . . .. If a text is scrambled, the frequency distribution is maintained but its content will not make sense. . . . The co-occurrence of words in sentences reflects language organization in a subtle manner that can be described in terms of a graph of word interactions’’ (Cancho and Sole, 2001, p. 2261). The combination of common and rare words is governed by ‘‘network’’ properties such as (i)

Corresponding author. Tel.: +39 081 5833232; fax: +39 081 7641355. E-mail address: (G. Fiorito). 1 About 7300 human languages and dialects are known (Payack, 2004). Among them, more than 210,000 words (about 170,000 current and 47,000 obsolete) are included in the Second Edition of the Oxford English Dictionary; these include adjectives, interjections, conjunctions, prepositions (Anonymous, 2004). 0167-8655/$ - see front matter Ó 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.patrec.2006.12.023


the ‘‘small-world effect’’, and (ii) the ‘‘scale-free distribution of degrees’’ (Cancho and Sole, 2001, p. 2261). The organization of our language reflects the evolution and social history of human beings. Humans developed a ritualization code originated by the cooperation between individuals and based upon a simplified rule system that evolved by natural selection in order to reduce mistakes in reciprocal understanding and failure in communication (Cancho and Sole, 2001; Nowak and Krakauer, 1999). Humans are capable of understanding the meaning of a ‘‘message’’ not only on the basis of its language-content, but also from the ‘‘expressions’’ (sensu Darwin, 1872) that we ‘‘add’’ to it. Darwin wrote: ‘‘The character of the human voice, under the influence of various emotions, has been discussed by Mr. Herbert Spencer in his interesting essay on Music. He clearly shows that the voice alters much under different conditions, in loudness and in quality, that is, in resonance and timbre, in pitch and intervals. No one can listen to an eloquent orator or preacher, or to a man calling angrily to another, or to one expressing astonishment, without being struck with the truth of Mr. Spencer’s remarks. It is curious how early in life the modulation of the voice becomes expressive. With one of my children, under the age of two years, I clearly perceived that his humph of assent was rendered by a slight modulation

1992). 1972).e. endeavour to strike terror into their enemies by its power and harshness. 1992). the vocal organs are efficient in the highest degree as a means of expression. and thus they make themselves appear as large and terrible as possible’’ (Darwin. Packard. Fiorito et al. see for example: Darwin. / Pattern Recognition Letters 28 (2007) 1854–1864 1855 strongly emphatic. 2 For a contemporary view on the communication of emotions and its relationships with vocal expression and music performance. 1995. Evidence of a form of social facilitation has been demonstrated in the feeding behaviour of the common cuttlefish. parr. Cephalopods as learning invertebrates Cephalopods are marine invertebrates (molluscs). Dozens of experiments mainly carried out and published at the Stazione Zoologica of Napoli have led cephalopods. Hanlon and Messenger.e. as the lion does by roaring.. it is interesting to raise questions on the evolutionary processes that gave rise to them. for the reputation of being monsters of the sea (see the tales of Victor Hugo and Jules Verne) or for their ‘‘intelligence’’. naı ¨ve octopuses performed a visual discrimination task following a short demonstration given by conspecifics. . see for example: Juslin and Laukka (2003). a great number of scientific papers has been devoted to provide evidence to what extent social learning (i. In brief. 1999. About 780 living cephalopod species are described today.M. . Spencer further shows that emotional speech.. on the one hand. up to human culture. 3 . cuttlefish raised in a social context showed an increase in predatory efficiency (Warnke. 1992). Reznikova. However. 1986.. 1972). 2. 2004. . and that by a peculiar whine his negative expressed obstinate determination. Marchant et al.. Mr. 2003. and especially when associated with terror. In fact. cuttlefish and squid are known for the taste of their flesh. 1. (2004). Koelsch et al. and consequently to instrumental music’’. because the lion at the same time erects the hair of its mane. 2004. It plays an important role in regulating short-term memory recall. during the first seventy years of the last century an increasing research effort was promoted to the study of the learning and memory capabilities in Octopus. 2001). the vertical lobe (Fiorito and Chichery. Our aim is to contribute to the discussion on ‘‘communication. even though facial emotions may be considered species-specific (i. 1984. . but. 2004. together with the optic and the median superior frontal lobes. and the dog the hair along its back. Moreover. innate. 1994).. they utter fearful sounds.e. 2003). inhabiting almost all available niches in the sea (for a review see: Norman. a fundamental component of the visual learning system (Young. Whiten. 2003). Their performance resulted to be similar to that of their demonstrators (errors were limited to about 10%. vulgaris is a solitary animal and that the reported capabilities to change its behaviour on the basis of information obtained from conspecifics may have an extraordinary adaptive value. and the dog by growling.e.4 It is noteworthy to remember that O. 1987). Our cultural heritage affects our language and the way our emotions and expressions are interpreted by others (for a review see Ekman. As summarized in Fig. Cattle and horses suffer great pain in silence. sharing behavioural ‘‘patterns’’ of non-genetic origin) and induce any form of cultural sharing in non-human animals (Byrne et al. Rendell and Whitehead.1. 2001. 1996) although it does not seem able of crossmodality (Michels et al. 1872. and the common octopus (Octopus vulgaris) in particular. social learning) has also been reported in this species. Barbato et al. 84–88). 4 The vertical lobe is an area of the octopus ‘‘brain’’ that is. 1872. very ‘‘simple’’ animals when compared with higher vertebrates. Whiten et al. in all the above respects is intimately related to vocal music.2 And continuing: ‘‘with some kinds of animals. 2004. i. but see also Russell et al.. Octopus. 2000. 1991).e. Von Frisch.. cephalopods present astonishing levels of functional convergence with vertebrates (Packard. Eibl-Eibesfeldt. Here we do not want to provide a review of the knowledge available on the exchange of information in animals and how this ‘‘evolves’’ in traditions and culture. probably because of co-existence during the History of Life on Earth. 1970). man included. 2001. 1996. to be considered the main character of our endeavour in understanding the learning capabilities of animals. birds and mammals have shown that complex communication may evolve without the need of a grammar-based structure or of large vocabularies of symbols (Hauser. Danchin et al. 1998). Resnicow et al.. the capability to learn from conspecifics) may produce traditions (i. also considering the limited life span of a cephalopod. 1967). These studies demonstrated that O. Studies on bees. 1975). Sepia officinalis. In recent years. some animals. on the other. as a read-in and read-out device (Sanders. but when this excessive. Fiorito and Scotto. . vicarious learning in Octopus seems to require a neural circuitry similar to the one utilized by animals to learn individually. when enraged. . Mesoudi et al. (2004). 2004. When studying human language and their expressions.. Observational learning was faster than individual learning3 and allowed a good and stable memory recall for at least five days after the observational phase (Fiorito and Scotto. and it is a centre of activity-dependent synaptic plasticity (Hochner et al. vulgaris is capable of learning to discriminate different objects using visual and tactile cues (for review see: Boyle. no evidence of The number of trials required to train a ‘‘demonstrator’’ octopus to learn the simultaneous discrimination was significantly higher than the four trials of observation (vicarious experience) necessary to ‘‘observers’’ to reach a level of accuracy higher than 80% in solving the task (for details see Fiorito and Scotto. although results are apparently contradictory. Observational learning (i. The ‘‘complexity’’ of cephalopods 2. Moore. interaction and integration’’ by providing a series of examples taken from ‘‘simple’’ animals: the cephalopods. I infer that their object is to strike terror.

Data on cephalopods were obtained from: Hanlon and Messenger (1996). 1911. Sanders (1975) and Dialog Classic (Dialog Corporation. October 2004). it changes constantly in both colour and texture as the animal moves. that elicited the attack response. 5–6). Their conclusion was that ‘‘the colour changes which occurred during attacks on the crab also occurred during attacks on the conditioned stimulus. 5 the movements of the chromatophores. covering and finally catching it. one of the most impressive features of a living cephalopod is its skin. Wells. 31). it is – in our view – a useful way of drawing their parallel processing capabilities. October 2004). Warren and co-workers were intrigued by asking whether these changes. by unequal dilation in different regions [of the body] a great variety of patterns may be produced’’ (Cowdry. and that the relation between background and cryptic displays may be complex’’ The great variety of patterns that the cephalopods’ skin is capable to produce are due to chromatophore organs that are under the direct neuromuscular control of the ‘‘brain’’ (for a review see Messenger. 1969). vulgaris. Fig. Colours and skin textures are regulated by elaborate neuromuscular mechanisms that make the cephalopod skin a very complex and sophisticated organ.6 Animals exhibit this peculiar feature in ‘‘parallel’’ with the actions required to accomplish a given response. but we think that this occurs not because both the colour reactions and the attack behaviour are learned responses to the conditioned stimulus but because the colour changes are inevitable given the changes in locomotor activity which occur during attacks .e. depended from the nature of the stimulus (i. was oriented to disclose the learning capabilities of mammalian models (rats or mice: about 1150 papers appeared during 1951–1960.5 2. cephalopods are also known for the complexity of their behavioural repertoire. O. 1996). although colour displays of the octopus may on occasion serve a cryptic function (Packard and Sanders. that surround the oesophagus in molluscs of more primitive design. The study on learning capabilities in the octopus was. and 3700 from 1961– 1970). it should be noted that the animals utilized in these two studies differed for their relative size (=age?) and that a sort of behavioural hierarchy could be invoked to explain this contrasting evidence. the changes in the appearance of the skin of an octopus is a ‘‘result from O. Its central nervous system is made up by the coalescence of neural ganglia.1856 M. and by the growth of tracts and fibres that connect these ganglia. over the same period of time. does not possess a real ‘‘brain’’. Apart from the analytical potentials of representing the behaviour of a cephalopod in this way. data on rodents were deduced from Dialog databases (Dialog Corporation. learning in Octopus corresponds to at least two memory systems (review in Young. our data suggest the possibility that even those displays which so obviously hide the animal may not be independent of the animal’s locomotor adjustments. These structures are large pigment-containing cells distributed in the superficial layers of the skin over the whole surface of the body. . / Pattern Recognition Letters 28 (2007) 1854–1864 80 70 Number of publications 60 50 40 30 20 10 0 1900-1910 1911-1920 1921-1930 1931-1940 1941-1950 1951-1960 1961-1970 1971-1980 1981-1990 1991-2000 2001-2004 Fig. social learning was found while attacking a crab (Boal. In the words of Hanlon and Messenger: ‘‘Cephalopod chromatophores are thus unique in the animal kingdom. Cephalopods’ body patterns Apart from their learning capabilities. Number of articles published from 1900 to the present day on Octopus’ learning capabilities and their neural correlates. last update. vulgaris changes the colour and texture of the skin probably in order to match the background or disorient the ‘‘victim’’. These numbers are only a small part of the quota that. and in many shallow-water forms nearly all behaviours are inextricably bound up with chromatophore activity’’ (1996. The behavioural elements exhibited during the predation are not exclusively motor patterns: the octopus changes its colour from what we call ‘‘Basic’’ to ‘‘Dark Brown’’ (during alerting and attention) to ‘‘Mottle’’ or ‘‘Leopard’’ (during the final part of the capture).J. As described by Cowdry (1911). pp. let’s say a crab.. Many authors provided a more or less detailed description of the chromatic changes occurring in several behavioural contexts by the octopus and other cephalopods. mainly devoted to the analysis of how neural systems modulate behavioural responses. after a short time delay (alerting and attention) it launches itself towards it. back to ‘‘Basic’’ exhibiting more or less papillation of the skin. as for other cephalopod species.2. On the basis of the knowledge available. By equal dilation of these cells the pigmented surface is increased and the animal consequently becomes darker in colour. During the attack on a prey. Barbato et al. on the other hand. as mentioned above. This originates a neural mass (commonly called ‘‘brain’’) that surrounds the oesophagus of the animal and in which we can distinguish more that 60 lobes. 2001). last update. 2 is a simple representation of how different animals exhibit simultaneously different components of their behaviour during the attack on a crab. When an octopus recognizes a prey. or from a species-specific module of responses that necessarily depended on the behavioural context. p. Among them. 1991) made of a series of matrices involving several lobes of the brain. However. a natural prey or an artificial discriminandum). 6 . To paraphrase M. 1. Thus. .

The term ‘‘Body patterning’’. iridocytes. unpublished. locomotor) that are on their own a by-product of ‘‘units’’.. ‘‘There are as many patterns as can be recognized by the classifier’’ (Packard and Sanders. 1974. A proper classification of the patterns would probably distinguish between essential and inessential components. postural and locomotor components. answer is. according to Warren and co-workers. etc. . 1996). 1971). A ‘‘taxonomy’’ for body patterning in cephalopods It is widely recognized in the cephalopod literature and elsewhere that the contribution of Packard and co-workers in providing a hierarchical system (a kind of taxonomy) to describe and analyze body patterns has been fundamental (Packard and Hochberg. as mentioned. . Each line represents a time course of one or more behavioural elements belonging to the same category (e. Data from Fiorito et al. and that a particular octopus can take on different appearances over a period of time. can be described in terms of the relative positions (arrangement) and intensity (value) of the components regularly present. . cephalopods ‘‘acquire’’ a novel ‘‘dimension’’ of the phenotype that is also a novel dimension of their behavioural repertoire. are perceived as part of the whole and the observer needs to perform a second operation to dissect them out’’ (Packard and Sanders. motor patterns.e. 32). pp. 780–781). 1971. examples taken from two focal observations. The essentials of this hierarchy are given in Hanlon and Messenger (see Box 3.g. a muscular constraint has to be invoked as a major reason for chromatic changes during predatory behaviour. when applied to cephalopods. Components are built from themselves. 1969. Body patterns are.. According to this hierarchical system (review in Messenger. The mutable appearance of the animal at a given time is called ‘‘body pattern’’. . though hardly satisfactory. 218–219). i. by the white surfaces of the suckers . textural. Barbato et al.) as indicated in the left column. Thus. .. 1996. acquires a novel and more dynamic meaning than the simple ‘‘morphological expression of genetic control of body shape’’ as is traditionally defined. . . dermal and ‘‘skeletal’’ muscle fibres and/or are supplied by movement. These are ‘‘the parts that go to make up the whole.M. Nowadays it is widely recognized that the changes in colour and texture of the skin of cephalopods are unique in the animal kingdom and to some extent ‘‘magical’’ (Hanlon and Messenger. These effectors are the output elements of visual expression. pp. / Pattern Recognition Letters 28 (2007) 1854–1864 1857 Fig. in contributing to the whole. Different patterns are perceived and recognized on a ‘‘Gestalt’’ basis much as we recognize faces or facial expression independently of such things as size. . Components are analysable in terms of the effects of chromatophores. As stated by Packard and co-workers: ‘‘Anyone who has watched a group of small octopuses soon notices that they look individually different. 1971. 2001). Packard and Sanders. 2. a body pattern is made up by a combination of some (from one to many) ‘‘components’’ (chromatic. 2. 780). postural.3. p. . of Hanlon and Messenger. 1977. . Parallel processing in the behavioural repertoire of Octopus vulgaris while preying upon a crab (Carcinus mediterraneus). . Cephalopods’ body patterning is produced by a combination of chromatic. . Whereas most components. A single component does not itself comprise a given body pattern though it may be the dominant feature in a pattern. orientation or the angle from which the animal is viewed. (Warren et al. Thus. and . but we are not yet in a position to do this. at least when the attack is launched. The appearance at any one moment we call the body pattern. Such are the white spots on the front of the head .. p. textural. a morphological . by the pupil. made up by components.1. And if we ask ‘‘How many patterns are there in the octopus?’’ the best.

‘‘lines’’ may refer to components that lie in either orientation . This has been named ‘‘Dark’’ (Idiosepius pygmaeus). Within the limitations of the ‘‘naming system’’ available. Polyphenism in cephalopods One of the most striking features of the biology of coleoid cephalopods is their capability to display several environmentally-cued phenotypes as an expression of their phenotypic plasticity (West-Eberhard. we capitalize the first letter of a component name and the first letter of each word of a body pattern or display’’ (Hanlon and Messenger. p. On the basis of their duration. aggression. For example. The second is for communication with hetero. eight postural and seven locomotor components. Although this system has been utilized from the ’80s for almost all published accounts of cephalopod body patterns. when an animal expands the chromatophores almost entirely over the body. known since Aristotle. Regarding their adaptive meaning. This was due to the fact that the authors stuck to the original descriptions or because the same item was described with different denominations (Borrelli et al. different species exhibit a different number of body patterns. . a pattern-based language has been suggested for example in Sepioteuthis sepioidea (Moynihan and Rodaniche. As mentioned above.htm. the result is the darkening of the skin. L. from published papers. These have been indexed by the way of a relational database so that a query on the name of a given pattern or of a species may result in a set of images (see the World Web page at: http://www.). 35) and proposed to use ‘‘for chromatic components: ‘‘bands’’ or ‘‘bars’’ to name transverse components. 2006). cephalopods appear to know how the visual system of higher teleosts works. to cite some.e. but also to conspecifics especially during courtship and agonistic contexts. 1988). 1989) or polyphenism (Mayr. In addition. 3. Hanlon and Messenger (1996) have suggested ‘‘that some convention be established in the future’’ (p. although the total repertoire is genetically endowed. For example.. Some species seem to be able to organize complex social interactions by these visual signals. In O. regarding 21 species of cephalopods. Alloteuthis subulata) or ‘‘Uniform Dark-phase’’ (Octopus bimaculoides). With an extraordinary speed they appear and disappear. each cephalopod can produce tens of body patterns and. vulgaris reynaudi.1858 M. For convention. For this aim. 1982). 87). cells with reflective properties. ‘‘the knowledge being stored in the brain ready to be printed out on the surface of the animal at the approach of its fish predators’’ (1972. illustrated and indexed. . A separate work is also available through the Internet. vulgaris 19 chromatic components.7 and compiled a list of more than 3000 items with obvious duplicates (synonyms). In order to contribute to this end.g. Their work represents a reference of the various behavioural items (i. . 1971). p. last visited March. 34 chromatic components have been described for S.g. which includes a collection of photographs and video-clips of several species of cephalopods. leading Mather (2001) to ask: ‘‘Do squid make a visual language on their skin?’’ (p. the ‘‘name’’ of components and/or body patterns is not universal. body patterns are also categorized into ‘‘chronic’’ and ‘‘acute’’. including both the external surroundings of the organism (e. thanks to the properties of the chromatophores and to the direct control of the ‘‘brain’’. officinalis that. 1996. 2005). 2006). the paramount variety of body patterning exhibited by cephalopods (Borrelli et al. acute are very short. and provides a tool for a comparative behavioural analysis in the taxon. patterning in cephalopods is dynamic and subject to immediate change and countless gradations. In Packard’s words. As we mentioned above. evidence is accumulating that they are used in communicative systems by transferring information not only to potential predators.. Borrelli and co-workers collected. components and body patterns) described in different species of cephalopods. is for concealment from predators that is the first function. homogeneous description of a given component/body pattern among the many definitions and names found in the literature. 293). being exhibited only for few seconds or minutes. L. The first. 1988). six textural. are known to produce about 13 body patterns (Hanlon and Poster2001A/poster01A1. In addition. / Pattern Recognition Letters 28 (2007) 1854–1864 entity constituted by ‘‘elements’’ that are the morphological basics in the skin (chromatophore organs. 1972). Body patterns function for crypsis and/or mimesis and evolved as defence systems against vertebrate predators (Packard.. or reproduction). from barely perceptible to fully expressed. in a simplified way. L. 35). Moreover.utmb. internal organs. pealeii.and conspecifics. the authors analyzed more than 180 published works. plei. the background or the social partner) and its motivations (e. body patterns thus seem to be produced for two different reasons. The above works are particularly useful in helping cephalopod and animal behaviour students to have a reference for their work and also in assisting them to distinguish among several cephalopod species otherwise not easily recognizable (Hanlon. ‘‘stripes’’ or ‘‘streaks’’ to name components aligned along the longitudinal axis. defence.cephdev. etc. ‘‘A Catalogue of Body Patterning in Cephalopoda’’ is an aid for obtaining a single. Barbato et al. Components vary in the extent of their expression. Chronic are those that are exhibited for a long time (even hours) in a steady-state. together with six textural. a function that 7 Descriptions on cephalopod body patterns has been provided only for a very few species. 14 postural and four locomotor components are known to assemble more that 10 body patterns (Packard and Sanders. 1963). any one of these patterns – with many gradations – can be displayed according to its environment. ‘‘All dark’’ (Loligo vulgaris vulgaris.

and therefore can be adopted as a hidden or ‘‘secret’’ channel of intraspecific communication (Shashar et al. 2001. and (iv) Deceptive Resemblance (by resembling an inanimate object in the environment). octopuses protect themselves with materials (broken shells. However. S. 1996). it has been recently discovered that a number of species produce distinctive polarization patterns in the skin (Cronin et al. 1975) such as ‘‘I am not an octopus but a random sample of the background’’. The acceptance of this view contradicts the label of antidisplays that Moynihan and Rodaniche (1982) assigned to cryptic patterns. (i) General Background Resemblance (by conforming to the appearance of the background in brightness. 3. 1971. contrary to the authors’ expectations. in which octopuses took on the body pattern and shape of rocks and – in a stealthy manner – used the tips of their arms to slowly move across open substrates. a foraging octopus made itself only moderately cryptic or. they can be seen as signalling false or dishonest information (Zahavi. vulgaris: Packard and Sanders. belonging to the latter category. a common species inhabiting the shallow waters of coral reefs throughout the Indo-Pacific.. (ii) the grading in intensity of signals. 2003. This would suggest that the polarization patterning is used for visual communication in a medium that cannot be detected by polarization-insensitive animals such as many predatory fish and marine mammals. (iii) Disruptive coloration (by visually uncoupling a part of the body from the rest. 1969. Ma ¨ thger and Denton. Like soldiers behind the enemy line. officinalis: Hanlon and Messenger. The rarity of any phenotype might in fact counteract the habit of many predators to prey differentially upon more common phenotypes. 3.6 times/min to 4. In addition. Although the adoption of non-visual channels to transmit information requires further and more detailed investigations.1. Using the skin to conceal (Curio. Hanlon and Messenger (1996) listed a number of advantages arising from the use of the neurally-controlled chromatophores as the main elements of body patterning in the cephalopod system of communication. i. and not only of shallow-water species..6 times/min in the two study sites. sepioidea: Moynihan and Rodaniche. 1995) and that. fluctuating like algae on the sea floor (O. In particular. A plausible answer to the question as to why a foraging octopus. (iii) the potential for bilateral signalling (individuals can on one side repel rivals and on the other . Barbato et al. cyanea’s unique ability for rapid polyphenism is used to interfere with any fish predator’s ability to form a search image Difficulties arise when these patterns used for concealment and deception are to be explained within the more general theory of animal communication. by assuming the characteristic forms and shades of the background. and texture). For these reasons. 1996) or drifting with the current as pieces of seaweed (S. This process helps animals to make choices and to select among alternatives. varying from 2. they make themselves perfectly indistinguishable. the communication of cephalopods. so seemingly vulnerable to predation. was the ‘‘Moving Rock’’. recent studies have shown unexpected properties in their visual sensory modalities. A peculiar pattern.M. Shashar et al. One example is the field study of Hanlon and colleagues (1999) on the foraging behaviour of Octopus cyanea. during foraging excursions in daylight hours. pattern. breaking up the wholeness of the animal). A further result was that the rate at which this species can change its body pattern is considerably high. But cephalopods can also pretend to be plants. at least in cuttlefish. octopuses showed to be capable of mimicking parrotfish. They are able to disappear from your sight fading away in the landscape. The list includes: (i) the rapidity of signalling and change of signals due to the direct neural control from the brain. the appearance of polarization patterns is associated with specific behaviours. which are not designed to transmit information but instead to impede it. Using the skin to communicate The mimetic talent of cephalopods is extraordinary and outstanding. Alternatively. colour. By acquiring information an entity becomes more able to anticipate and to respond appropriately to events and to use feedbacks to select changes in its state. In practice. even conspicuous (for 22–50% of the time) when it was in the open.. ‘‘information’’ refers to the view that the acquisition and use of information reduces uncertainty. stones and pebbles) found on the spot that adhere to the suckers and help in assuming the features of the particular background on which they are. prey remains. four mechanisms of concealment listed by Messenger (2001) were observed during the study. 1976). a quantitative estimate of the time spent in the different body postures and patterns showed that. However. Hanlon and Messenger (1996) claimed that cryptic body patterns cannot be seen as forms of communication. (ii) Countershading. The authors’ starting hypothesis was that octopuses should be highly cryptic the vast majority of the time they are out of their dens. surprisingly. changes in the polarization appearance of an animal can bring to a change in the behaviour of a conspecific observing it (Ma ¨ thger. They have at their own disposal a variety of ways to pretend to be what they are not.2.e. is largely visual and obviously relies upon the complexity and efficiency of their eyes. Recent studies on crypsis and mimesis in cephalopods have obtained unexpected results. in fact. 1982). chose most of its time not to be cryptic even though it was capable to was that O. One operative definition was provided by Smith (1997): ‘‘communication’’ is any sharing of information between entities – between individual animals in the case of social communication. 2002). particularly abundant in their local habitats. / Pattern Recognition Letters 28 (2007) 1854–1864 1859 has been highly debated for the consequences it can lead to ethology. Ethological literature abounds of attempts to define animal communication unambiguously.

(ii) modifiers (that encode less information such as adverbs and adjectives). signalling agonistic intentions during a fight is an evolutionary stable strategy (Maynard Smith. S. Such individuals are apparently simultaneously sending two messages to the adjacent male: ‘‘I am a male (so don’t copulate with me)’’. stereotyped. spend a considerable proportion of their time signalling about the most important things of life (their signals are concerned with attack. the authors found that the various signals did not differ only for their physical size. In fact. they also differed for strength. there is the general impression that at least in some species (S. However. and that in male–male encounters paler-faced males are less likely to escalate any contest to physical contact and fighting. escape. 1939).1860 M. however complex the communicative system can be. intra. In particular. probably indicating stress (Boal et al. 1982) under the condition that the cost of cheating. One well-described intraspecific display is the Intense Zebra of the common cuttlefish. A conclusion was that the sepioidea system shows a number of design features proper of the most elaborate repertoires of birds and primates. squid seem to associate between signals and some features of the world (Hockett. 1988. That most cephalopods adopt an elaborate and refined system of intraspecific communication has two main implications for those scientists interested in their behaviour. Flamboyant.. interchangeability. sepioidea. officinalis: (Hanlon and Messenger. A more cautious interpretation was recently provided by Hanlon and Messenger (1996). have sentinels that may transmit subtle alarm signals. officinalis. 1972). arbitrariness. On the other. Adamo and Hanlon (1996) demonstrated that one signal contributing to the Intense Zebra display – ‘‘Dark face’’ – can be modified to be significantly paler than the other signals. sepioidea is endowed with the feature of semanticity. This display is highly conspicuous and intensity modulated (high contrast black-and-white).g. Moynihan and Rodaniche (1982) suggested that the communicative system of S. 1988). specialization. sepioidea (Moynihan and Rodaniche. is very high (Maynard Smith and Harper. It may also appear in crowded tanks. vulgaris and O. Second. Three categories of signals were identified in S. scope. Moynihan and Rodaniche (1982) provided evidence that shoals of the Caribbean reef squid. In addition. We have no data on whether they can recognize individuals of their species such as kin. 1977. as it may be in this case. Extending this reasoning to other cephalopods. chromatic patterns provide a number of simultaneous or sequential signals that contribute in moulding the total appearance of a communicating cephalopod. The adoption of more complex body patterns to communicate with conspecifics has been described in several shallow-water species such as Loligo plei (DiMarco and Hanlon. Because species-specificity prevents interbreeding between sympatric sibling species. 1996). which could result in physical injury. As we reported above. since animal signals are foremost tools of social behaviour. sepioidea with the purpose of evaluating the characteristics of the signals adopted by this species that are shared by human languages. the messages that most animals transmit are few in number and relatively simple. S. First. the arm posture is exaggerated and the whole body of the transmitter is oriented towards the receiver. S. the degree of sociality in cephalopods remains unclear. the discovery that some species possess a communicative system with a surprising degree of flexibility and complexity has encouraged several authors to suggest that visual signals do constitute a language (Moynihan and Rodaniche. These two honest signals seem to be advantageous for the sender: on the one hand. and (iii) positionals (that provide convenient supports or springboards for other reactions). thus signalling their motivational state. / Pattern Recognition Letters 28 (2007) 1854–1864 attract sexual partners). and (iv) the lack of interference of signals with other motor acts since the chromatophores are independent of the other body muscles. 1982). They argued that signalling is certainly a widespread phenomenon amongst animals and many animals. it includes a series of stripes and circles. sepioidea) individuals school in more than a simple random association as is found in most fish schools. exaggerated or otherwise specialized to facilitate the transmission of information (Hanlon and Messenger. 1999). In addition to broadcast transmission and directional reception. 1982). 1982). cephalopods do not signal about their environment and there are no conspicuous alarm signals. Tinbergen. displays (e. a comparative analysis has been conducted in S. 1987) and appear conspicuous. including cephalopods. 1997. for defence or agonistic and courtship behaviours. Barbato et al. which demonstrated the lack of social recognition in cuttlefish dominance hierarchies. Lateral Display) may occur in different contexts. Nor do we know if they can communicate the position of food sources or other information that might strengthen group adhesion. and ‘‘I am going to back down’’. body patterns that are related to courtship and reproduction can be particularly useful as valid taxonomic traits in behavioural taxonomy (Hanlon. Passing Cloud. and specificity of the messages encoded. Hanlon. Moynihan and Rodaniche (1982) concluded that the communicative system adopted by this taxon fulfils many of the requirements of what is usually defined as language. former rivals. rapid fading. an exception being Boal’s (1996) study. by signalling their gender males prevent conspecific males from attempting to copulate with them. and sex. Yet. As defined in the ethological literature. and discreteness. 1960). or its displays. Dymantic. 1988). Males (and females according to Boal.or inter-specific. However. S. sepioidea and termed: (i) signifiers (that encode much information such as nouns and verbs). or former sexual partners. and perhaps feeding and gregariousness in some cases). cyanea (Wells and Wells. 1997) use the Intense Zebra display for agonistic signalling. first described in detail by Tinbergen (1939). In cephalopods. displays are often the result of ritualization (McFarland. As far as we know. These communicative systems are ‘‘closed’’ or ‘‘finite’’ since an animal has to say only a few things to bring about a suc- . precision. O.

displacement (i. etc. a true language is an ‘‘open’’ or ‘‘productive’’ system of communication that can transmit a virtually infinite number of messages (Hockett. vulgaris and S. their richness may depend from the relative complexity of the part of the ‘‘brain’’ that takes the ‘‘higher’’ neural control (Boycott. Barbato et al. to protect its offspring or to draw attention to potential predators. In the second cluster (Loligo forbesi and Lolliguncula brevis). they are merged together by Hanlon and Messenger (1996) in the ‘‘coral reef’’ group. although they seem to be similar in habitat complexity and patterning richness. morphological respectively) the combination of data was found only for a few species (seven). Data were deduced by combining different data-sets. Nevertheless. On the other hand. In particular.73). temperate rock reefs or kelp habitats all have rich patterning repertoires (all of these species live on or near the substrate). officinalis are outliers. the account of Hanlon and Messenger (1996) was utilized to count the chromatic components while the paper of Maddock and Young (1987) was considered as a source to obtain the proportion of the chromatophore lobes relative to the whole ‘‘brain’’ size. Hockett. where habitat complexity means either its physical diversity. 1960) and duality of pattering (i. According to Hanlon and Messenger (1996). vulgaris has the largest lobe (2. we cannot exclude that a potential bias was intrinsic of the data itself due to the different accuracy of describing the repertoire of the two species. chromatophore lobe: 0.e. forbesi: 17.74) and the number of chromatic components (L. together with openness or productivity. brevis: 13). 3 illustrates the results obtained from the application of a hierarchical cluster analysis following the method of Ward (1963).M. 1960).99. chromatophore lobe: 0. O. It was shown that species inhabiting tropical coral reefs. similar to species living in murky waters or ‘‘bland’’ environments. 1960). Hockett. officinalis is the species with the highest number of components (35) described among all cephalopods.75) with an ‘‘average’’ number of components (19) described. the potential of morphemes to change their meaning in relation to the relative position of their components. etc. L.e. In fact. Therefore. nocturnal species of octopuses living in the same complex habitats have more limited repertoires. In the cluster. sepioidea. This might be due to the fact that S. chromatic components: 20). a more reliable measure could be one that takes into account the neural organization: i. L. a minimum of 10 components has been identified for Octopus ornatus or 11 for Sepiola affinis up to a maximum of 35 described for S. officinalis. sepioidea and Octopus bimaculoides: these two species show strong similarity in both lobe size and chromatic richness (S. Even if there may be non-randomness in the combinations and sequences of the signals shown by squid. O. it should be taken into account that body patterns are a ‘‘neural’’ product. Because of the intrinsic differences in the datasets (behavioural vs. the ability to communicate about things that are remote in time and space. our present knowledge does not allow us to confirm that the manifold signals and displays of Sepioteuthis and other cephalopods are endowed with the most advanced design features of language.e. vulgaris and S. By contrast.43. This is possible because the structural units of language (‘‘morphemes’’) are assembled into groups following specific sets of rules (Chomsky’s ‘‘deep structure’’ or ‘‘grammar’’). brevis: 0. this corresponds to an average-sized chromatophore lobe (0.42. In order to complement this view we correlated the size of the chromatophore lobes (centres in the ‘‘brain’’ of the octopus that seem to be the ‘‘special’’ units of the neural control of body patterning) with the number of described components for that species. chromatic components: 23. such as. these two species belong to the ‘‘social squids’’ and ‘‘murky habitat’’ categories.. officinalis) are ‘‘outliers’’ in respect with the two main nodes. again the two species are grouped for similarity in both the size of the chromatophore lobes (L. it is not obvious that there is a wealth of meanings concealed in these combinations and sequences. we should also take into account that the relative volume of the chromatophore lobe (or in general of any lobe of the brain of cephalopods) is not necessarily an index of complexity.. both O. or full stops. Finally. the authors plotted the number of chromatic components exhibited by the species versus increasing ‘‘habitat complexity’’. The first cluster is the one combining S. Hanlon and Messenger (1996) compiled a table to estimate the richness of body patterns in different species. as already mentioned. Exploring the causations of body patterns in cephalopods In reviewing cephalopods’ behaviour. Furthermore. neuropile versus ‘‘cortex’’ size or the density of fibres. we will justify their position later on. pauses. chromatic components: 15) results to be associated to both clusters and is reported in the ‘‘murky habitat’’ group. 1953).54. and sentences do not seem to be marked by internal starts or restarts. In addition. 4. this variability in magnitude may be correlated with the characteristics of the habitat that different species occupy. To demonstrate this point. in their communicative system there is an apparent absence of phrases or locutions. bimaculoides. They clusterize with relatively high ‘‘distance’’ from the other species and are not significantly clustered together. respectively. Because our dataset was based on the ‘‘naming’’ and counting of body patterns. Humans can easily coin new utterances by putting together pieces familiar from old utterances. As underlined by Hanlon and Messenger (1996). On the other hand. . two species (O. Eledone cirrhosa (chromatophore lobe: 1. transparency of the seawater. / Pattern Recognition Letters 28 (2007) 1854–1864 1861 cessful act of reproduction. The table shows that the range of body patterns and chromatic components is variable (in magnitude) among species. forbesi: 0. Fig.

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