Octopus (14 page)

Cephalopod camouflage is actually much more than simple background matching, although it works often enough for an animal to avoid being eaten. Hugh Cott wrote in 1940 about animal visual camouflage in all its variety, and discussed camouflage as simply not looking like an animal, noting that it's not necessary to look exactly like the background as long as you don't look like a recognizable form. This principle of nonform was also used by humans in disruptive camouflage during warfare, in weirdly painted clothes, and tanks or navy ships with wavy stripes of olive and blue and gray. The ships didn't look like the water around them to an observer in a reconnaissance plane, but they didn't look like ships either.

Background-matching camouflage is very common in marine animals. The peacock flounder is a dappled gray that blends with a sandy bottom perfectly, and it can enhance the match by flapping its body to dig into the sand and get loosely covered by it. Another shell-less mollusk, the sea
hare (Aplysia californica), is a splotched pale brown with projecting wavy bits that mimic brown seaweed. Anglerfish are bumpy and gray-brown, blending with the rocks so well that unwary potential prey will swim right up to their open mouth and get eaten. Even the sea lemon nudibranch (Archidoris montereysis), whose clear yellow ought to be easy to see, lives on and eats yellow sponges, with which it blends perfectly. The abilities of octopuses, however, are special because they can use a lot of different background matches and change very fast.

Despite the variety of camouflage techniques available to them, octopuses often use background matching. A foraging common octopus in 3 ft. (l m) of water would be highly visible if it didn't use camouflage. While crawling on a sandy patch and extending arm tips into the sand to explore for clams, it puts small pinpoints of paler and darker gray on its skin. Like the flounder, it flattens slightly and smoothes the skin surface so that it looks just like the sand bottom. Then, moving onto rocks with brown and greenish algae and snaking its arms between the fronds to find small crabs, it changes immediately to larger patches of mid-brown, olive brown, and greenish, more similar to the sea hare (see plate 21). The skin rises from a vague roughness of the surface to small papillae ranging from less than an inch (1 to 2 cm) in height and larger over the now raised head. And moving into the shade of larger rocks where fragile scallops hide, the common octopus becomes a rich plum-purple that matches the dark of the rocks, and its skin texture becomes smooth again.

Disruptive coloration is different from background matching; it can be used over the whole body or in specific surface areas of the cephalopod. The chunky little flamboyant cuttlefish (Metasepia pfefferi) can put wide bands of black, cream, and warm brown irregularly across its skin (see plate 22). The common cuttlefish (Sepia officinalis) can take on a similar kind of deception temporarily. On a rocky habitat, it can assume blotchy patterns of deep brown, tan, and white that match neither the colors nor the texture of the rocks but do make the animal disappear from our perception of an animal. This camouflaging method is a kind of distraction—making some part of itself obvious so that the predator's eye doesn't recognize the animal's form. The common octopus has a couple of white dots on its mantle that can accomplish this distraction.

Disruptive camouflage can be area-specific too. Octopuses especially need to disguise their head. For many animals of different groups, an eye is recognizably an eye and indicates an animal around it. Many animals have
ways to disguise their eyes or to make fake eyes at the wrong end of their bodies. The four-eyed butterfly fish has a vertical black bar through its real eye and a wide round black eyespot at the posterior end of its body. A larger fish will dart at the apparent eye, the butterfly fish jerks forward, and the predator only gets a mouthful of water (see plate 23).

One way that octopuses disguise the slit pupil of the eye is to put an eye bar on the skin of either side measuring about an inch (2.5 cm), changing the eye's appearance so to an observer the eye is not round but just an extended line. The ability of the octopus to raise the skin papillae as horns above the eye's circumference also breaks up the eye outline so it seems to be irregularly wavy instead of circular. And they can extend the skin camouflage of the irregular blobs of color across all the eye skin except the pupil, so the eye seems to be just more skin with a line through it.

The importance of the appearance of the eye region for an octopus is indicated by the amount of neural programming devoted to it. Nine nerves control the expansion of the chromatophores that make the color patterns in all of the skin, but four of these come to just the small eye area. We obtained a clue as to how the octopus can control this appearance when we were studying octopuses' recognition of individual humans. After a few trials, when the person designated as the hassler approached, the octopuses put on eye bars, and when the one who fed them approached, they did not. We are now studying what changes constitute an eye bar and how its appearance can be conditioned.

Roger Hanlon et al. (1999) suggested that octopuses use their quick-change ability to cause even further confusion in predators. Any single altered pattern may not be especially deceptive, but an octopus discovered by a diver or a fish will puzzle the potential predator by using its sequential quick-change abilities. Fish have good visual memory and are likely to seek out prey by remembering what they look like—this is a “search image.” The fish forms a visual search image of the octopus, but can't follow the prey after it changes, and will then lose sight of it. Imagine the challenge to the predator when a common octopus goes from a green and black background match to pale brown as it lifts off the rocky surface, then jets away and assumes stripes or gradually changes to a dark gray that spreads from the arms up over the body, then, settling quickly on the rock again, it becomes green and black by background matching.

The octopus's ability to take on skin patterns is also applied in situations other than camouflage. One dazzling example, which is displayed not to predators but to potential prey, is the Passing Cloud, named for the shadow of a cloud passing over the landscape. Early reports of the appearance of this feature were simply that it was a dark form on the dorsal surface, passing generally forward over the body, but the display was little known since it rarely occurred in the lab.

While studying the effect of food supply on octopus foraging in Hawaii, we kept several day octopuses in an outdoor saltwater pond on Coconut Island. We had a unique chance to watch and videotape behaviors that hadn't yet been described in detail. Back in the lab and replaying the video frame by frame, we found how complex the Passing Cloud display is. The Passing Cloud formed on the posterior mantle, flowed forward past the head and became more of a bar in shape, then condensed into a small blob below the head. The shape then enlarged and moved out onto the outstretched mantle, flowing off the anterior margin and disappearing. The process took less than a second. Since the display is usually used when the octopus is hunting and comes right after an attempt to surround a prey with the spread arms and web, a startle attempt is a likely explanation. Andrew Packard and G. D. Sanders suggested in 1971 that the octopus is conveying, “Move, you animal!” Any sudden movement will startle a crab that has frozen to evade being caught by the octopus. The crab's subsequent motion allows the octopus to notice and catch it.

The details of Passing Cloud displays are easier to understand as communication if you know the neurophysiology behind visual perception. The day octopus also puts an edge of white skin beside or behind the dark blob of the Passing Cloud, which greatly increases the visibility of the cloud shape by tapping into a feature of visual system analysis known as lateral inhibition. Organisms pay attention to change, not stability. No animal cares that the tree is still a tree, but a moving dark edge is likely trouble. By the lateral inhibition process, when receptors in the eye fire, they inhibit their neighbors. When a surface is uniform, that means the receptors cancel each other out and there's no signal to the brain. Edges, on the other hand, don't cause this kind of inhibition and are exaggerated. Darkness next to a bright area is construed as more dark. The day octopus may have evolved the white edges to make the dark cloud most visible to the crabs, which are the common prey of this species.

Another way in which the Passing Cloud production taps into visual physiology is more a matter of perception than physiology, because it produces apparent but not real movement. It's easy to say the cloud shape moves, but in fact no part of the skin or the octopus moves at all. What actually happens is a complicated series of chromatophore expansions and contractions across different skin areas. This phenomenon of seeing movement that isn't really there is called apparent motion, and it's used in light advertisement displays to humans in cities everywhere. If a sequence of dots appears close to each other in space and time, the brain simply constructs them as one moving dot. Making apparent but not real motion is useful to the octopus's own visual processing. Presumably it is looking at where the crab was before it froze and seemed to disappear. If the octopus itself moves to startle the crab, the image of the crab will blur on the retinas of the octopus's eyes, and the now-moving crab will be more difficult to pick out. If the octopus can stay still yet startle the crab by sending a Passing Cloud along its body in apparent motion, it maximizes its own visual ability and has a much better chance of catching the crab if the crab moves. This is a neat perceptual trick.

Octopuses also use this intriguing skin pattern production ability to display to each other. Surprisingly, we hardly know the precise signals and sequence of communication that allow octopuses to find mates and reproduce. We do know that these animals are basically solitary and semelparous—reproducing only once at the end of their lifespan. They aren't concerned with one another until maturity, and large octopuses may even
catch and eat small ones. To reproduce, they must find each other, and ascertain species, sex, and maturity of the other individual. The male must also establish whether the female is ready to mate and bring her into readiness if she is not, and females especially must overcome distrust. Solitary animals have to do this fast; they may not get another chance. Finding, identifying, and mating is a complex sequence, and visual information from the skin must be useful only after animals have located each other, since it can be seen only at a short distance.

For years, Bill van Heukulem (1983) thought that the Hawaiian day octopus (sex unknown) signaled readiness to mate by taking on a pattern of wide chocolate brown and cream stripes that extended over the body and arms. But further observation suggested that the stripe pattern was a warning coloration, more evasive and challenging than sexual. At the pond in Hawaii, we saw mature male octopuses giving another distinct coloration when approaching a female. We named it White Papillae. The skin surface was raised in large papillae all over, the papillae were bright white, and the background skin surface was a deep brown, almost black. Since the octopus is color blind, the mottled black and white display is an easily visible high-contrast signal to the female that an interested male is approaching (see plate 24).

Through the accident of confinement, we learned about what might be referred to as the principle of spatial discouragement. In nonsocial animals widely spread out across space, the opportunities for mating are probably few, and octopuses, particularly males, must quickly take advantage of every reproductive opportunity. In our study in Hawaii, we kept two pairs of day octopuses in the pond for ten days, one pair after the other. Shortly after finding the female, each male spread White Paps gloriously over the skin surface and moved toward her, with his third right arm advanced, ready to find her mantle cavity and pass spermatophores. After some evasion and challenge, each female accepted the male, and mating ensued for about an hour. During the following nine days, as we observed the octopuses hunting and eating, each male tried again and again to mate, and each female rejected him. As in many animals, the female octopus will become uninterested after a successful mating; she can store sperm for months and has no need for more from him. Gradually, as the flashy show failed to win her cooperation, the male reduced the area of skin that displayed the White Paps. First it was only the side toward her; no need to waste a display on areas that she couldn't see anyway. Then it was only a
few arms. Then finally, with rejection after rejection, such as moving off, jetting water at him, and even attacking, only his third right arm displayed the pattern. As his motivation level fell, so did the display, and after a week he quit trying and the pattern was gone.

Complex and varied as octopuses can be, all octopus species are not equally good at these visual skin displays. The shallow-water day octopus and the common octopus are the most studied octopuses, because humans are diurnal and prefer working in shallow tropical waters than in cold dark depths. Night active and deep-sea octopuses have a much smaller repertoire of visual displays. The displays of the small and strictly nocturnal Caribbean pygmy octopus range minimally from pale to blotchy to solid warm brown. The zebra octopus (Octopus chierchiae) has constant zebra stripes, the white-spotted night octopus (O. macropus) is reddish-brown but lines its arms with large white dots, and the deep-sea spoon-arm octopus is nearly a constant red brown. The deep-sea cephalopods have evolved their own ways to contact visual receivers such as other octopuses, predators, or prey. Many, like the vampire squid (Vampyroteuthis infernalis), have bioluminescent spots, and some even replace dark ink with jets of luminous bacteria.