Octopus (9 page)

Learning may account for the fact that the octopuses we studied in Bonaire were what we labeled specializing generalists. We were studying squid, but we couldn't ignore the octopuses moving under us as we squid-watched. So we sampled the remains of what they ate, and over three years there were seventy-five different crab, clam, and snail species. But some of the octopuses specialized, often narrowly. One ate immature queen conch snails (Strombus gigas), and another dug the fragile pen shells (Pinna carnea)
out of the sandy mud. Habitat couldn't account for these differences, since they were all living in a mixed rock-rubble-sand-mud habitat. Maybe each octopus learned a special foraging technique that fit particular species. It's ironic, though, that the species is generalist but some individuals are specialists.

Besides learning where to find prey, octopus choices of areas to hunt may be restricted by mammals in the area, like sea otters, both as predators and as competitors for the same food species. We wondered whether a predator would learn where to find common octopuses. The octopuses we watched in Bermuda had very small home ranges but shifted them on average every ten days, maybe because they had used up all the easily accessible food, or perhaps because they were working out a balance of energy spent in hunting and energy gained by eating. We wondered whether they shifted home ranges because ten days is about right for a predator fish to catch on to where an octopus lived. And in fact, this speculation has foundation. As we got to know the area as the local fish might, we learned to gather clues to an octopus's possible den site. A fish might find an octopus in this way, then grab it when it's out hunting. The octopuses didn't spend much of their time carefully balancing energy tradeoff and deciding whether this hermit crab or that snail was worth a try. Besides, they were gaining weight. But while hunting, their appearance was disguised and they were always looking for predators. One false move and they would be prey themselves.

Part of the wide choice of prey species may be because of octopus energetics. Unlike homeotherms, such as mammals that keep their bodies heated and spend a lot of energy doing so, octopuses are poikilotherms: their metabolism slows down in cooler water, and they become less active and waste less energy. A major amount of an octopus's energy can be spent on digestion, so energy expenditure for foraging may loom less large in their energy equation. They don't have to eat regularly just to keep going. In the lab, our healthy young pygmy octopuses didn't eat anything at all some days. Octopuses are so efficient at converting food calories to body weight that energy output may be a smaller part of their daily budget than it is for us.

Every researcher has found prey species that their octopuses wouldn't eat. Two-spot octopuses from California and the day octopus of Hawaii wouldn't touch one species of top snail; giant Pacific octopuses didn't eat hairy crabs; and Bermuda common octopuses seldom touched chitons. Perhaps the answer to this issue is preference; we don't know.

Prey species have evolved many ways to avoid being caught by octopuses. Many mollusks count on their protective shell to save them from predators. While providing some resistance, the shell doesn't stop predation by a variety of animals. Scallops can swim away by clapping the valves together, a successful method for avoiding capture by slow sea star predators but not for avoiding the jet-propelled grab of an octopus. The fragile-shelled, scalloplike file clam hides in crevices; scavenging wrasse can't get them but they are vulnerable to the common octopuses with its flexible arms. Octopuses normally hunt by feeling around in the landscape, with touch and chemical receptors in their suckers probably helping them recognize sources of prey. The approach is an effective one. We timed common octopuses in Bermuda, and it took five minutes for them to snake an arm into a crevice, capture the prey, throw away the shell, and start to digest the meat.

Crabs, being mobile, are a tougher challenge for octopuses to catch than the slower snails and often immobile clams. If you lift a rock, crabs
will scrabble out from under it and hide under one nearby, and when you pick up the second rock, they will scurry back under the first rock. Foraging common octopuses and Hawaiian day octopuses are often trailed by wrasse and other fishes as they move across the bottom, and perhaps the fish are planning to eat the small animals escaping from the octopus's menace. We watched a blenny fish in Bermuda go around to the far side of a rock intent on doing just that, waiting for escaping crabs as a foraging octopus slid under the rock. And crabs also pinch. Octopuses—and people—trying to collect them eventually learn to grab the crab from behind. Swimming crabs, like the blue crab, besides hiding under rocks or running away, can also swim away. In response to an escape attempt, an octopus can go from crawling to jet propulsion and can launch a mid-water grab.

The champion octopus evasion technique belongs to some hermit crabs that have a symbiotic relationship with sea anemones. Hermit crabs pull these flowerlike but stinging animals off their perch on the rocks and place them on top of the borrowed snail shells they use as homes. Predators such as octopuses and crabs, when reaching for the hermit crab, are stopped short by the sting of the sea anemone. The anemone benefits from this arrangement: it gets a free ride on this new home as well as castoff scraps from the crab's scavenging. This cooperative relationship has been noted in the lab. A group of anemone-carrying hermit crabs had been kept in a tank at Banyuls, southern France, for months and had gradually dumped their anemones off their shells onto the rocks. In their 1979 study, Donald Ross and Sigurd von Boletzky got some water from the octopus's tank and added it to the crabs' aquarium's saltwater intake pipe. Chemicals in the water from the octopuses must have been carried to the hermit crabs and served as a warning that trouble was around. The hermit crabs rushed over to the discarded anemones, manipulated them off the rocks, plopped them onto their shells, and again were protected.

What we call prey “handling time” varies widely with prey species and ought to but doesn't always influence prey choice. Handling time is the time and effort involved in actually getting at the food within the prey. We come back to the example of crabs: octopuses often choose to eat crabs. Most shallow-water species take crabs in the wild, and the Hawaiian day octopus eats crabs almost exclusively. Octopuses are well equipped to handle most prey. But for many prey species, before it can eat, the octopus sometimes is faced with the “packaging problem.” The octopus's strong arms are very good at pulling apart shells as well as pulling animals from
hiding or even off the rocks. And in addition to their parrotlike beak that can grasp and bite with efficiency, octopuses also have a ribbon of teeth, or radula, for small jobs. They also produce venom from the posterior salivary gland that can paralyze prey and start digestion.

When the octopus catches a crab or lobster, this arsenal of prey handling tools is supremely effective. A bite or drill through the joint or skeleton and the injection of venom from the salivary gland result in a quick death for prey. The pygmy octopus can subdue a crab its own size very quickly. Marion Nixon and Peter Dilly (1977) studied the remains of crabs that they had fed their common octopuses in the lab. The remains were disarticulated—all the units of the shell were separated, probably by digestion of the tendons, and the meat was totally cleaned out of the individual units. Once in a while, we'll see juvenile common octopuses save a particular part of a large crab until the next day, probably because they already had a full meal. Sometimes they will drill a neat hole into a crab claw, maybe to get better access to the muscle inside the exoskeleton. This approach might loosen the hold of the muscle from the shell plate that controls the thumb of the claw, for easier access.

For octopuses preying on clams, which have solid defenses, the situation is quite different. Because for millennia many different kinds of animals have used penetration techniques to get into mollusk shells, mollusks have evolved bigger, thicker shells for protection. Sea stars pull clams apart and slide their stomach in to start digestion. Crows pick up clams in their beaks, fly up, and drop them onto the rocks to crack the shells. Oystercatchers stab into them with their bill, crabs break them with strong crusher claws, and some oyster drill snails drill holes into the clam's shells. Octopuses are different only in that they have several different penetration techniques: an octopus can pull a bivalve shell apart. But if the clam is too strong, it can drill a hole and inject venom or chip the edge off a valve and do the same, weakening the clam's adductor muscles so it can't stay tightly shut. Octopuses try the easiest way first, pulling the clam apart.

Just as energetics is a good explanation for trying to pin down prey choice, we can turn to energetics to explain why the octopus uses different penetration techniques to obtain food. We found that the common octopus trying to pull apart the valves of a clam used 1.3 times as much energy as it would have spent in drilling. But drilling took much longer: Michael Steer and Jayson Semmens found in 2003 that it took sixty to eighty minutes for a red-spot night octopus (Octopus dierythraeus) to drill a clam shell, compared
to ten to twenty minutes for pulling valves apart. So we would expect the octopus to try pulling first, and go to drilling if the clam's muscles are too strong. We may also expect the octopus to select clams based on size. Using the pulling technique gives a good energy return, yet the food from a small clam might not be worth the work of finding, holding, and pulling. Generally, small octopuses open and eat small clams. Larger octopuses, on average, eat clams of a size that can be opened by pulling, but the variation in size selection is wide. And one octopus given two clams of the same size will sometimes pull and sometimes drill. So energetics is only part of the reason that octopuses use different techniques in getting at their food.

An octopus drilling through a mollusk shell is a neat trick. Early researchers took it for granted that the octopus drilled by using its radula, because other mollusks, like oyster drill snails, use rasping with the radula to drill into bivalves. But Nixon and Dilly found that hole boring alternated rasping with extension of the salivary papilla, which secreted acid into the shell hole from a different gland than the venom-producing one and dissolved the calcium carbonate of the shell. The octopus also has the challenge of where to drill the hole. Shells are different thickness in different areas, and they contain water as well as a mollusk body. The challenge seems to be guided partly by preprogramming and partly by learning. Common octopuses drill at the shell's edge in clams, for snails they drill high in the upper spiral near the retractor muscle attachment (see plate 11), and for mussels they drill in the center over the heart. Red octopuses and Octopus mimus drill over the adductor muscles that hold the valves of the clam together, and giant Pacific octopuses drill into the umbo, the thinnest part of the shell, and over the clam's body. The red-spot night octopus drills at the edges of the shells where they are thinnest.

To study how octopuses choose where to drill, in 1969 Jerome Wodinsky watched common octopuses drilling conch snails right at the location in the spire where the retractor muscle meets the shell and helps the snail pull back into hiding. He covered this area to see whether the octopus would change drilling locations. When he put on a rubber covering, the octopus just pulled it off, and when he applied a dental plastic covering, the octopus drilled through both layers. When he put a metal coating over the spire, the octopus drilled just at the edge of the metal: it knew where it wanted to drill and got as close as it could. He found that female octopuses that were tending their eggs and had no digestive gland activity occasion-ally
ate conch snails. But without salivary gland venom to inject, they didn't drill and so just pulled the snail out.