Its cold, alien eyes watched me with an unreadable expression. Every time I 'chuffed' into my snorkel, it momentarily blushed iridescent purple before returning to a translucent bronze. Its dorsal surface was a shimmering dance of colour, as waves of yellow, brown, red, and black washed over it--punctuated at each of my 'chuffs' with splash of brilliant violet. What did this Caribbean reef squid (Sepioteuthis sepioidea) make of me, I wondered. Did its colour changes carry any meaning? Was it trying to communicate with me and, if so, what? And how can a squid control its colour so readily, anyway?
Cephalopods-squids, octopuses, and their relatives--have long been acknowledged as experts of near-instantaneous colour change. A lot of marine critters can change colour, but most of them require several seconds to a few minutes to do so. The main reason for this disparity is differences in the structure and function of their chromatophores (specialized colour cells). In fish, for example, each chromatophore is a rigid, star-shaped cell; it takes a while for hormones to percolate into the cell, causing the pigments to disperse and become visible. In cephalopods, each chromatophore is wagon wheel-shaped: a flexible bag of pigment at the 'hub' surrounded by 'spokes' of muscle; it only takes an instant for a nerve impulse to cause the muscular 'spokes' to contract, expanding the bag and drawing the pigments apart, making them visible. Cephalopods are thus able to change colour at the speed of thought.
Of course, no one can know what goes on in the mind of another creature, but the context of cephalopods' colour changes can provide some clues about their motivational state. Consider squid courtship. Mating requires mutual understanding and co-operation in order to occur. Many squids are known to accomplish this through colour signals. When courting, males of the Pacific market squid (Loligo opalescens) display Technicolor shimmers to a mature female. If she blanches white, that's his signal to grab her by the head and inseminate her; as he transfers his spermatophore (sperm packet), he blushes bright red with success. When wooing a prospective mate, the Caribbean reef squid becomes pitch black all over--except for his single testis, which fairly glows white.
Of course, to live long enough and have the strength to mate requires avoiding predators and efficient hunting strategies. Colour changes help squid accomplish these things, too. A whole school of squid can become invisible in a moment. Once, while I was watching a school of American squid (Loligo pealeii) trapped in a pool near shore, a kid lobbed a large rock into the water. Every squid sank like a stone and when the ripples cleared the pool appeared to be empty. Only close inspection revealed that all the squids were lying motionless on the sandy bottom, their colour perfectly mimicking the background. The squids remained like this for five minutes. Other squids show employ similar tactics while hunting. The short-finned squid ( Illex illecebrosus ) has been observed preying on mackerel. These squids are normally thickly spotted with red and brown, but when darting among the mackerel they became pale and almost translucent--not unlike the fish themselves. A proverbial wolf in sheep's clothing?
Octopuses apparently use colour to communicate their emotional state. Although it has taken a while for orthodox ethology to recognize the fact, it is now widely held that animals do have 'emotions' of sorts. Some octopuses seem to advertise their mood through colour . The giant Pacific octopus (Octopus dofleini) is normally a rich reddish-brown. When resting in its grotto after finishing a crab meal, this species takes on a contented hue of pale bluish-grey. When persistently pulled or poked at by a pushy diver, the octopus takes on an angry dark brick red colour ; if the threat persists, it may blanch with fear, turning ghostly white and jetting away, sometimes expelling a brownish-black squirt of ink as it goes. It is likely that octopuses show other colours to signal different, perhaps more subtle, moods.
Perhaps the best studied cephalopod with respect to colour changes is the common cuttlefish (Sepia officinalis), which adapts well to laboratory tanks. This cuttlefish displays some dramatic colour changes when pursued, cornered, or courting. When actively pursued, the cuttlefish pales and takes on a symmetrical pattern of four dark, thin longitudinal stripes - one on either side of the midline of the body and another at the base of each of the continuous mantle fins. When cornered, these stripes disappear and are replaced by two dark 'false eye spots' near the front of its mantle, dark margins appear along the periphery of its fins, and the eyes are underscored with dark semi-circles - looking a bit like thick mascara, but serving to make the cuttle 's real eyes resemble its false eye spots. Whether this confuses a potential predator as to which end is the front or makes one cuttle look like two is unknown.
But there is nothing ambiguous about the courtship display in the common cuttlefish. On the approach of another cuttlefish, a male in breeding condition takes on a startling 'zebra' pattern of black stripes on a white background and prominently displays the striped fourth arm (the one specialized to transfer spermatophores) on the side approached. If the approaching cuttle is another male, it will return this display and the animals maneuver to lie side-by-side. Then a sort of 'visual duel' takes place; eventually, the less brilliant (and usually smaller) of the two fades and then retreats. Females and unripe males do not return this zebra display and copulation may follow. Or maybe not. Perhaps female cuttlefish have a display which means, "not tonight, I have a headache"!
We are only just beginning to understand what some cephalopods colour displays mean. If you are lucky enough to observe a squid, octopus, or cuttlefish in the wild, I encourage you to pay particular attention to any colour changes it may make and to look for correlations between these changes and what's happening in the immediate environment. Note how the cephalopod responds to your movements and how it responds to other animals and objects nearby. Notice, too, such fundamental things as the depth, time of day, and specific location. Record these data and report them to some one who has a professional interest in cephalopod behavioral ecology. Who knows? Perhaps you will see cephalopod behaviours no one had even suspected. More exciting yet, your observations might provide clues about what goes on in the mind behind those cold, alien eyes.