Octopus (13 page)

While the design of octopus suckers is fairly similar across many species, there are some fascinating differences among cephalopods. Octopus suckers, with the flexible rim, are better adapted to holding on to hard and smooth surfaces such as clamshells and crab legs. Squid suckers, especially on the tentacles, may have a row of sharp hooks, or teeth, extending inward from the rim that help them hold soft-fleshed prey such as fish. The deep-sea group represented by the vampire squid has cup-shaped suckers. Maybe in the deep, there is more to explore and less to hold tight. There are more sensory receptors in the rim of the octopus suckers on the outer, distal
part of the arms (at the arm ends), with which the octopuses feel, and fewer on the inner (proximal), walking part of the arms.

While an octopus arm has a wide range of freedom of movement, it likely has a smaller number of moves that it can actually make. Still, some of the single-arm moves it makes are fascinating combinations. Repelling a scavenging fish at its den entrance, a common octopus straightens a bent arm suddenly, unrolling it in what we call a “slap.” The common octopus and the Hawaiian day octopus can bend an arm back over their own body surface and even into the mantle cavity (see plate 19) to groom itself, running its suckers over the skin surface, lightly holding to and picking up loose skin, dirt, and parasites even from inside its mantle cavity. Few external parasites of octopuses exist, only internal ones like dicyemid mesozoans in the kidney are common, and it's no wonder—all the external ones are groomed away. Among our favorite single-arm movements is the one we call the conveyor belt: with an arm extended out and held steady, an octopus can pass a small prey item such as a hermit crab in a shell from sucker to sucker along the arm's ventral surface to its mouth. Or it can reject a shell that turns out to be empty, passing it out again the same way.

Foraging octopuses have a great deal of independence in arm movement. Moving across the rocky bottom, an octopus will extend a couple of arms in each direction along a crevice. Going to a patch of algae, it will feel along the algae stalks with several arms, grasping with a few suckers if receptors suggest there's prey present. Often the front arms explore and the back ones walk, depending on what direction an octopus is heading. Octopuses can spread all the arms and extend the web down between them, forming an umbrella shape, or a “webover.” The webover forms an effective and flexibly shaped pouch. Small prey can be held in a kind of enclosure below the mouth, made up of arm bases and the extended web, with a few suckers of each arm holding on. As the octopus lumbers along the landscape feeling for more prey, even eight arms may be too few, and it may lose one or two of the crabs it's captured. A small crab can dart out and be recaptured by one arm, while the disruption allows two more to escape from the pouch. If a swimming crab lifts off the bottom (see plate 20), a quick Hawaiian day octopus can switch from feeling around on the rocks for the crab to enclosing it by a webover in the water and grabbing it with the suckers.

Coordinating the movement of many arms can be problematic. After all, these limbs must stay disentangled from one another. And not surprisingly, the eight arms can run into trouble, especially as they are poked into holes and crevices that might be occupied by an animal with sharp teeth. Octopuses share with lizards and brittle stars the ability to cast off an arm at a structural weak point and regrow that arm. Sometimes as much as half of an octopus population may have arm loss, but since the arms can regenerate before reproduction, this doesn't matter too much over the life span.

Mathilde Lange described this process of regeneration in 1921. At the stump of a cut-off octopus limb, bleeding is minimal at first, probably because the animal has direct nervous control of blood vessels and can close off the artery. After a while, blood is released for clotting at the wound, and the last pair of suckers is pulled toward the arm to minimize tension. There is then degeneration of both muscle connective and nervous tissue at the wound end of the arm before regrowth. A knob forms on the stump, and then over a few weeks, a new narrow arm begins to extend from it, developing new tissue. Chromatophores on the new skin come last. It's a good thing that the coordination of arms is flexible, since the octopus can lose several at different times, and arms grow back slowly.

The process of octopus limb coordination is not well understood. Each arm has a lot of independence, and while arm nerve cords come out from the subesophageal area of the brain, they are all linked by a circular nerve cord above the arms. No study of neural control and coordination of multiarm movement has been done since the work by W. J. ten Cate in 1928.
Still, octopus arm movement looks pretty uncoordinated. This flexibility may be because water offers a lot of support for an octopus, so it doesn't have to worry much about balance, but it also may be because octopuses don't always move forward. With lateral eyes and all those multipurpose arms, octopuses can and do move sideways. Several years ago, we had a student study an octopus walking. He found that the octopus usually walked on arms 3 and 4 of both sides but not always, and that there was no strict sequence of arm use. As in many other aspects of their lives, octopuses' walking is variable, apparently fitting the demands of the moment.

Octopus arms have a lot of jobs to do at once, from walking and feeling on the bottom to capturing and holding prey, grooming, and, for males, passing spermatophores. Unlike the highly specialized crab claws, legs, and mouthparts, physically octopus limbs are generalists, with only the male third right arm structurally different for sending spermatophores down its length to a female. The first pair of arms is generally used for exploration, and sometimes there's a size difference among the arm pairs, as in the Atlantic long-arm octopus, whose anterior arms are much smaller. But arm pairs usually have the same basic capacity.

While each arm can do many tasks, some arms actually perform a task more often. Ruth Byrne et al. (2006) looked further into such specialization in octopus arm use. When reaching out for food or a toy, the common octopus mostly used arms 1 and 2 of either side, but each octopus had a favorite arm of these four, not the same one for each animal. When an octopus needed more than one arm for a task, it recruited the ones next to the arm already in use. If you stimulate an arm nerve cord, the circular nerve cord linking arm to arm passes on the signal and the adjacent arms come into action. We call this the principle of neighborliness: using whichever arm is nearest.

There is a cost to having these multipurpose and multiunit arms. It requires extensive neural programming to set up all those contractions for the muscular hydrostat–based movements. Over half the neurons in the octopus body, therefore, are outside the brain, most of them in the arms controlling all these muscles. A nerve cord—a chain of ganglia—runs down the center of each arm. Below each of these many ganglia, a sucker ganglion controls the suction cup maneuvers. No wonder octopuses can weave and do pincer grasps and pass little crabs from sucker to sucker.

With all those neurons in the arms and only general central coordination of them, control of arm actions must be mostly local. Reflexes or local
circuits control movement of these arm units, correlate a move with touch and chemical information, and even coordinate movement of nearby arm areas. This subject was last studied by C. H. Fraser Rowell in the 1960s. When physically threatened, several species, including the pygmy octopus, will cast off an arm at its base, and the arm then wriggles off on its own. A detached octopus arm can reach out for an object, withdraw from potential harm, and even act like a conveyer belt with a small food item. In the lab, isolated octopus arms (separated from the body) stimulated by electrical currents reached out in a smooth, bending wave from base to tip. Since it was the same motion as for intact octopuses, this organization of reaching seemed to be under local and not central control. That's a lot of decentralization, and the hierarchy of actions and reactions in the octopus needs more study.

Is there a disadvantage to this decentralization? Maybe without central monitoring of position, an animal can't sense its own body position. Wells set up a situation in which octopuses saw a crab through a glass window and then had to detour down a corridor to catch it. He concluded from his study that octopuses didn't know their location in space. We know now that this isn't true for the whole animal, as later studies on spatial memory and returning to home make it clear that the octopus knows where it is in the landscape. But in the smaller sense, what about knowing where all the parts of your body are and how big you are? It would be interesting to know whether a motor system that allows a set of suckers to untie surgical silk might have the down side of not letting the controlling brain know exactly what those suckers, and maybe other parts of the arms, are doing. While this way of controlling a complicated body isn't like the narrow centralizations in a big brain of mammals that we think of as connected to high intelligence, it certainly is a workable system for the octopus.

6

Appearances

O
ctopuses are far better camouflage artists than chameleons. They can change their entire appearance in less than a second. They can take on or get rid of fine gradations of color. They can make local changes like spots, bars, eye rings, and dark mantle edges. In addition to color alterations, they can assume skin texture changes and postures that mimic such things as smooth gravel, wavy curling seaweed, or other animal forms.

When octopuses evolved away from having a protective outer mollusk shell, their newly exposed body surface had a unique and complicated repertoire that allowed them to put patterns on themselves at will. Within the outer layers of octopus skin are many chromatophores—sacs that contain yellow, red, or brown pigment within an elastic container. When a set of muscles pulls a chromatophore sac out to make it bigger, its color is allowed to show. When the muscles relax, the elastic cover shrinks the sac and the color seems to vanish. A nerve connects to each set of chromatophore muscles, so that nervous signals from the brain can cause an overall change in color in less than 100 milliseconds at any point on the body, although local small areas called fields and ridges tend to color alike as units. When chromatophores are contracted, there is another color-producing surface beneath them. A layer of reflecting cells, white leucophores or green iridophores depending on the area of the body, produce color in a different way: Like a hummingbird's feathers, which only reflect color at a specific angle, these cells have no pigment themselves but reflect all or some of the colors in the environment back to the observer (see Messenger 2001).

The octopus's skin itself helps the animal make different appearances. There are small muscles within the skin that can pull it up into little peaks, papillae, to make the surface appear rough or smooth, depending on what texture the octopus wants to assume. These skin peaks are often largest above the eyes, and many photographs of octopuses show skin horns above the eye bulb that mask the appearance of head and eyes. Since octopuses
have no bones and can put their arms into a variety of positions, these skin changes can also help the octopus to match its background. Young octopuses, in particular, can position their arms in fantastic twists and coils, including a set of postures labeled Flamboyant that make an octopus look like seaweed. These skin behaviors truly hide the octopus against its background. For volunteers watching common octopuses in Bermuda, learning how to find and follow the animals who were out hunting was among the more difficult things to learn. We told the observers that if they were looking directly and constantly at a foraging octopus and it apparently disappeared, they shouldn't worry. It was just doing a particularly neat piece of background matching, and if they just kept looking it would reappear when it moved.

While the colors and textures of the octopus skin probably evolved as camouflage, the ability to change them was later available for other uses. The evolution of the bony fishes in the marine environment challenged all the inhabitants of the seas. Only the numerous coleoids and a few nautiloids survived the competition in evolutionary terms. The coleoids did so by gaining jet propulsion, fast-tuned physiology, a skin display system, and intelligence. But researchers wondered: why would an animal that's color-blind evolve a color-displaying skin system? Fish rather than other octopuses were the designers of the cephalopod skin; octopuses that failed in ability to be invisible got eaten and removed from the gene pool. The colors that octopuses produce were aimed at preying fish, which, unlike the cephalopods themselves, can see colors.