Octopus (12 page)

Another demand for locomotion is maneuverability or change in direction. This feature is very useful in the short run, for a predator can be dodged if it can't be outrun. Thompson's gazelles and squid do this very well, since both can pivot 180 degrees while moving just their own body length. For the near-shore squid, this ability is crucial, because predators like barracuda specialize in sudden acceleration and short dashes. For the less maneuverable octopuses, hiding and camouflage replace speed.

While maximum speed, sustained speed, and maneuverability clearly matter to getting around, a wider view of the cephalopod locomotion system is important. But over the long term, energy spent on locomotion is also important, especially when it's calculated as a tradeoff for how far it gets the animal. Octopuses and squid move through the water by propelling water jets one after another through their funnel. Since squid can outjet octopuses, their jet propulsion has been studied more and squid often are used as examples when writing about cephalopod issues. Jet propulsion in squid is not an energy-effective way to get through the water, however, especially compared to the sinusoidal, or sideways-flowing, body bending of fish—an important point because cephalopods have evolved competing with fish.

A second issue for all moving animals is resisting the pull of gravity—staying upright in the case of land animals and staying up within the water in the case of many marine animals and a few cephalopods. Some unusual cephalopods have made drastic changes in their body structure to stay buoyant: for example, the air-filled chambered shell of the nautilus, the gas-filled swim bladder of the football octopus, and the ammonia-filled organ in the mantle cavity of the glass octopus (Vitreledonella richardi). These cephalopods have sacrificed speed so they can stay up in the water column, as do octopus paralarvae, which need to stay near the surface where the light is and therefore where phytoplankton and zooplankton grow and where most marine animals are. Other animals, like squid and tuna, don't sink in the water because they keep swimming to stay afloat, and that process is effective while energetically costly. Some animals, like mature octopuses,
are heavier than water, but since they mostly crawl on the bottom and only lift off some of the time, buoyancy doesn't matter much.

Alexander points out that evolutionary background is significant in locomotion. Octopuses have to work with energetics and a demand for speed and maneuverability, but they are limited by the basic molluscan model. An animal can only improve the efficiency of the model it has to work with, and the basic molluscan model isn't a good one for speed. Minimizing or getting rid of the heavy shell through evolution has increased the possibility of speed and maneuverability, true for both cephalopods and the shell-less nudibranchs. Gastropods that can stay up in the water include the sea angel (Clione limacina), which swims with fleshy “wings,” the lion nudibranch (Melibe leonina), which undulates a laterally flattened body (see plate 14), and the janthina sea snail (Janthina janthina), which drifts on the sea surface attached to a bubble raft. The cephalopods have developed a specialized way to keep moving in the water, through contraction of the mantle, which has been freed from its shell to allow for water ejection and therefore jet propulsion.

Many mollusks, like the scallop and the Lima clam, have turned their shell into a movement advantage. By clapping their two valves together and forcing the water out between them at the back, scallops and Lima clams (see plate 15), jet propel themselves through the water. The elastic hinge opens the shell again, so the scallop can flap through the water for a couple of minutes. While not well-directed movement, the water expulsion lifts the animal off the bottom and sends it a couple of yards, and when it stops, the flat shell acts as hydrofoil and the animal drifts gradually to the bottom. Mollusks such as scallops swim to escape sea star predators; just the touch of the sea star's tube feet or the saponin chemical in them sets mollusks off in escape responses. Scallops only need to get off the bottom and away, because sea stars aren't fast moving either. But this type of movement isn't successful when scallops are pursued by octopuses, which can lift off the bottom and chase them by jet propulsion. Octopus middens commonly have a few scallop shells, bearing witness to this fact.

The jet propulsion of cephalopods is fairly fast in the short term and is well directed. On the same principle as octopuses but more effectively, the well-muscled mantle of squid, which we humans eat as calamari or squid rings, exerts pressure inward with circular muscle contraction, and the flexible funnel aims the water flow to direct the movement. The connective
fibers in the mantle store tension during this contraction, and their elastic recoil pulls the mantle back out, drawing in water for another jet.

The energetic efficiency of jet propulsion is low. The jetting system is designed for another purpose, maximum acceleration from rest. Not only does the fast contraction mean a powerful jet, but also the nervous system of the squid is set up to make it faster yet. A few very large nerve cells, or axons, come from the base of the brain to the squid's mantle, branching extensively. Each giant fiber is different in diameter and placed so that all the areas of the mantle get a nerve signal very quickly and at the same time. This system was discovered by zoologist and neurophysiologist J. Z. Young (1971) in the late 1930s, and because of these giant axons, squid became a valuable species for study at the marine research center in Woods Hole, Massachusetts, near Boston. Much of what we know about how nerve cells work is based on how these squid giant axons perform. The principle of a few big neurons setting up fast escape responses isn't used just by the cephalopods, either. Crayfish have a similar set of giant axons leading to the tail to set up sudden escape tail flips. And the octopus uses sudden jet-propelled acceleration when a predator discovers it despite its camouflage: a couple of jets can take it far enough away so that it can send out an ink cloud screen or hide again decked out in new camouflage. One of our colleagues, Ron O'Dor (1998), described true squid as the Ferraris of the cephalopods and the bumbling little sepiolid squid as the Volkswagens. We'd extend the analogy and describe the octopuses as the Mack trucks.

Cephalopods don't only use jet propulsion for getting across the ocean floor. Squid use fins, ranging in size from little posterior flaps that probably help only in steering, to the wide “wings” of Humboldt squid (Dosidicus gigas), or the ribbon of cuttlefish fins that runs along the edge of the mantle. These fins have the same combination of muscle types and elastic connective tissue and use the same kind of motion that fish have. Watching a Caribbean reef squid holding stationary or moving slowly, you can see the ripple of fin undulation and the slow puff of minimal water jets from the down-turned funnel. It's a neat slow-fast system: the fins tuck in along the mantle when the squid jets away (see plate 16). Fishes have a dual muscle system for accomplishing slow-fast movement, a combination of well-oxygenated red muscles that can keep contracting for long periods of time and white anaerobic muscles that need recovery periods. Squid, too, have some muscles used for slow cruising and others used only for escape.

A dual slow-fast movement system is particularly important for octopuses.
Normally they move slowly along the bottom by both pulling with the arms and jetting through the funnel. Their speed of progress is one-tenth that of jetting, 10 seconds per ft. (30 seconds per m). Octopuses move slowly, which is logical since they are feeling around for food. Octopuses also use jet locomotion just to get someplace directly. Individuals of some octopus species, such as the giant Pacific octopus, make fairly long migrations, possibly for reproduction (see plate 17). Whenever the octopuses we watched in Bermuda wanted to go somewhere directly, they would lift off the bottom and go several yards with a few jets. In this type of movement, the octopus's flexible body shape is very useful. The giant Pacific octopus, in particular, can spread its arms and flatten them dorsoventrally, presenting a hydrofoil-type surface, which makes motion through the water easier and slows sinking. This motion may look inefficient if you value speed, but octopuses get around effectively.

Regarding the octopus's movement of separate parts such as limbs, we must first think about support systems. No motor system can move an animal without some sort of support to move against or it would simply collapse in a heap. Vertebrates and arthropods have solved the support problem so important in air by evolving skeletons—internal for fish and birds and external for ants and crabs. The limbs are organized as a set of levers with skeletons as the shafts. The benefit of a lever system is that it can get excellent mechanical advantage that gives strength, depending on where the muscles are attached to the bone. The disadvantage is that such a limb can only move at the joints and only in the direction the joint allows. We can't bend the human knee joint sideways, nor move an arm with the flexible grace of an octopus arm. Crab movement is even more limited: most crabs are like medieval knights in armor, clumping across the ocean bottom. The exoskeleton, however, gives crabs protection as well as support.

Without a permanent rigid skeleton, cephalopods have solved the support problem in their own way. William Kier and Andrew Smith (1990) point out that the principle that allows many mollusks to move is that of the muscular hydrostat. A limb or body using such a system stays at a constant volume, but a change in one dimension results in a reactive change in another. It's easier to get the idea of constant volume with variable shape if you envision a water-filled but half-expanded balloon. Press it on one side and it bulges out on the other; squeeze it so it's narrower and it gets longer. This flexibility is used in a lot of molluscan movement, and is the secret behind clams being able to dig into sand. When a clam starts to push its
foot down into the beach, the shell is kept spread apart as an anchor while the narrow foot is pushed down into the sand. Then a valve opens and blood rushes into the foot, which swells like a balloon and anchors the animal. The shell valves then close and the now-anchored foot pulls the shell down toward it—a neat trick indeed. Several of these moves, and razor clams disappear into the sand in seconds.

There are no cavities for the blood flow of cephalopods to use to change shape, since they have enclosed arteries and veins like humans. Their muscular hydrostat arrangement follows the same principle of holding volume constant, but depends on the contraction of some muscles acting as a skeleton to oppose others that change the limb's shape or position. Octopus arms have circular muscles around the outside, radial ones from the center to the periphery, and transverse ones spiraling around the length in left-hand or right-hand coils. That's a lot of muscle in the arms, more than half the body's volume. It also means a lot of strength. An octopus can resist a pull of 100 times its body weight. Octopus arms are tubes of a constant volume: radial muscles contract and longitudinal ones extend, letting the animal reach out to grab a hermit crab. And the opposite actions will contract the arm and bring the crab closer to the octopus. Bending resulting from contraction of ventral longitudinal muscles in the arm gets the crab up to the octopus's mouth.

Muscular hydrostats can elongate, bend, or twist by stiffening, relaxing, or contracting different sets of these muscles. We have calculated that each octopus arm is made up of three units—arm tube, sucker stalk, and sucker—all of which can do much the same actions and can do so together or separately. An octopus can extend an arm straight out into the water, reaching toward but not touching potential food and thus not using suckers or stalk (see plate 18). From video analysis of these actions, scientists have deciphered the dynamics of simple octopus arm extension. An octopus starts straightening the arm at the base and unrolls it outward until it gets it where it wants it. Suckers can also be a separate moving unit. Once when we watched a Hawaiian day octopus resting in its den, a tiny foraging hermit crab fell on it. Without moving its coiled arm, the octopus picked the crab up with a single sucker, extended the sucker stalk, and dropped the offender a bit farther away. In a 1994 study, Satoko Seino and colleagues poked an endoscope viewer on the end of a long stick inside the pouch of arms made when a female giant Pacific octopus was laying eggs. They filmed the octopus weaving the long stalks of the eggs around each other
before attaching them to the roof of her den, using only movement of the sucker stalks.

The suckers are a particularly intriguing arm unit. William Kier and Kathleen Smith worked out the biomechanics in 1985. There's a cavity, the acetabulum, at the end of the sucker. The animal attaches to some object, such as a clamshell it wants to open, with the sucker rim. Then it decreases the pressure inside the acetabulum, making a vacuum in the sucker that keeps it attached to the object. Because there's local control by a cluster of nerve cells in each sucker ganglion for muscles of the sucker rim, the sucker edge can bend to fit the contours of whatever it's grasping without losing its grip. A fixed sucker, with a rigid edge, can't hold the knobby surface of a crab leg, but the flexible one has no problem holding on to a relatively flat surface. The sucker surface also has touch and chemical receptors, making that surface perfect for exploring and gaining information about whether something is edible. Flies “taste” with receptors on their feet, and octopuses “taste” with receptors in their suction cups.

The octopus sucker can also be folded in half to form a grasping surface. We humans are proud of our thumb-and-finger pincer grasp that lets us hold spoons, pens, hammers, paper—the objects that build our civilization. Octopuses have hundreds of suckers that can make pincer grasps all down the ventral side of the arms. These variable-sized grips are very effective, and octopuses can perform very fine actions with them, like untying knots in surgical silk. Wodinsky (1977) discovered this ability after he'd done surgical operations on several common octopuses, watched them come out from the anesthetic, and then he went home for the night. When he returned in the morning, the octopuses were holding on to the side of their tank with the wound gaping, and the lengths of surgical silk were lying on the bottom, untied.