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Authors: Roland C. Anderson

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One thing we know particularly little about is how the octopus controls all these color and texture changes, mostly because of our lack of research on the brains of these animals. For example, how does a color-insensitive animal know how to do color matches? We just don't know yet, and the problem is far from simple. An octopus receives visual information about its surroundings and situation and then computes their appearances. It must then choose, whether consciously or not, what to do about it. Then it turns on output circuitry that leads to the chromatophores that must be used, and to skin muscles and arm musculature, telling them to carry out the proper action to make texture. Before long, the octopus is also comparing and gauging results to decide what to do next.

Hanlon (2007) was particularly impressed when an octopus did the “moving rock” trick. Crawling across an open sandy area (and thus vulnerable), it went gray-green with a lot of raised papillae, looking much like a rock covered by a clump of seaweed. Instead of walking normally, it drifted irregularly across the sand, swaying slightly as seaweed would if pushed by currents.

We also need to do more study on where and how the brain of the octopus matches and programs the dazzling variety of patterns it assumes. A
chromatophore lobe in the subesophageal part of the octopus brain controls the display system itself, but it's the last step in output, and many of the circuits that control specific changes must be far from there, possibly in the optic lobe with its intimate connection to the eye. Learned visual information is stored in the vertical lobe, and this too must be used if identity of critical stimuli or appropriate responses is learned, which means that all the brain must cooperate, but we don't know exactly how. Roddy Williamson and Abdesslam Chrachri pointed out in 2004 that this interesting neural network has complex descending control but probably no feedback loop. They believe that the octopus doesn't monitor the patterns it's displaying, such as white spots (see plate 25).

Brain control circuits for octopus skin displays, wherever they are, may be of great variety. Any species-typical displays, such as White Paps, must be fairly fixed, because sexual displays need to be clear. If you have only a few chances in your lifetime to seduce a mate, the signals need to be produced without much learning. They also need to be simple and easily recognizable, if every member of the opposite sex is to quickly recognize what each display means.

But the circuitry for camouflage includes commands for posture and skin texture as well as pattern, so camouflage output must be more variable and tied quite directly to perception. The circuitry to control the Passing Cloud display might be fairly simple. Still, the Cloud must “move” toward the location of the prey when an octopus directs a startle display at a particular crab, making the possible programming for controlling chromatophore muscle contraction more complex. Perhaps the biggest challenge in imagining the octopus brain circuitry needed to control appearance is related to changing displays. As Hanlon et al. pointed out (1999), the octopus must be able to choose and produce a display, move, change, measure the results, and make a decision as to which one to make and what to do next. This set of actions is controlled by far more than fixed neural circuits. Perhaps this is what octopus intelligence does best, producing the flexibility and variety in control of a system whose functioning we barely understand yet.

7

Not Getting Eaten

C
ephalopods such as octopuses spend much of their lives working on defense. They have to be constantly vigilant about predators to whom they are a neat unprotected package of protein. Having given up the external shell of their mollusk ancestors, they have to rely on hiding, camouflage, and the intelligence to choose different tactics to avoid getting eaten.

Among the cephalopods, vulnerable octopuses can hide in a den, and juvenile cuttlefish find refuge by burying themselves in the sand, but others such as squid never rest during their waking hours. Sleep has not been reported in squid and only occasionally in buried juvenile cuttlefish, and it has only recently been seen in octopuses. We have spent many hours observing Caribbean reef squid and have never seen any sign of rest. In fact, they appear to be the Nervous Nellies of the cephalopod world: squid schools spook eight times per hour when resting in the open. It's possible that squid sleep with half their brain at a time, like migrating birds and marine mammals, but we have seen no indication of that.

Many ocean animals prey on subadult or adult octopuses. Small octopuses are eaten by small fish and crabs, and most fish would not pass up an octopus away from its den. In the tropics, often-present fish such as grouper and barracuda eat octopuses, and in the North Pacific, lingcod and wolf eels will eat them. John Randall (1967) has pointed out that Caribbean predatory fishes, such as squirrelfish and yellowtail snapper (see plate 26), are generalists: they eat most any fish that will fit into their mouths and many invertebrates including cephalopods. In the 1960s, he discovered this by taking samples of many Caribbean fish by trawling, by hook-and-line fishing, and with the help of narcotizing drugs. He then cut open their stomachs and examined the contents to see what the fish had been eating. He probably wouldn't be able to do such a study nowadays, as many fish stocks are depleted and some species he took are now rare or endangered, so we are grateful for his older, thorough study.

Sharks, especially the many species of dogfish sharks, are octopus predators. Based on the stomach contents of sharks, researchers have established that in shallow tropical waters, octopuses are a big part of the diet of white-tip reef sharks and nurse sharks. And in the deep sea, a number of other deep-water sharks eat octopuses.

Among the best known and most persistent of octopus predators is the moray eel. Because of its body design, it can snake into small areas such as octopus dens for prey, and it also is a major predator of octopus in shallow tropical waters. Moray eels can go through small openings under rocks looking for small fish and crustaceans, and they frequently find an octopus. Morays can sense an octopus chemically. Octopuses and moray eels are about the same size, so when they meet, a battle may ensue, each fighting for its life. An octopus will also readily eat a moray eel. The moray sometimes wins, but many times it only twists off an arm of the octopus. The octopus—now with only seven arms—jets away, still able to hunt its own prey while the arm regrows. In California, scorpionfish and two-spot octopuses have a similar relationship: large scorpionfish eat small octopuses and large octopuses eat small scorpionfish.

We made a discovery about this kind of predator-prey relationship at the Seattle Aquarium. The largest tank there is a multispecies tank of 400,000 gal. (1,560,000 l). Giant Pacific octopuses used to be kept in that tank, several at a time, so that at least one would likely be visible to the public. The tank had a mix of large northeastern Pacific fish, including wolf eels and dogfish sharks about 3 ft. (1 m) long. Since dogfish are known octopus predators, we were a bit leery of putting them together. The public usually doesn't like to see predation in action; we didn't want the dogfish biting arms off the octopus in front of visitors. Things seemed to go well for a while, then something surprising happened: some of the fish, including dogfish, started disappearing. Partially eaten dogfish carcasses were found in the morning on the bottom of the tank. We tracked down the culprit, a 60-lb. (27-kg) male giant Pacific octopus. We eventually were able to videotape this behavior: he would follow the rather slow-moving dogfish, catch it, and eat it. As in the case of the scorpionfish in California, dogfish eat small giant Pacific octopuses and, at least in the confinement of a tank at the Seattle Aquarium, large octopuses eat dogfish.

In Puget Sound, there appears to be competition for den space between octopuses and wolf eels. Wolf eels are wolf fishes, not true eels, that grow to nearly 8 ft. (3 m) in length and weigh about 50 lb. (23 kg). They have
large canine and molar teeth that they use to crush crabs and sea urchins, ignoring the spines piercing their lips. They live in the same caves and crevices that octopuses use and are found around the rim of the North Pacific. Wolf eels are known to eat octopuses, and maybe octopuses eat wolf eels. The giant Pacific octopus gets big, so in this wolf eel–octopus competition, the octopuses usually win the battle over choice dens and also for their lives.

Though we were wary of the octopus–wolf eel interaction, at the Seattle Aquarium we decided to have a multispecies exhibit that contained a giant Pacific octopus and a pair of wolf eels in a 3000-gal. (12,000-l) tank. We designed the tank decor to exhibit both species together by providing a number of clefts, cracks, and overhangs in the rockwork for both the octopus and the wolf eels. When the exhibit opened, we put the wolf eels in the exhibit first and the octopus a day later. The two species immediately took up residence in a different area of the exhibit, showing that they can live in the same area and not kill each other as long as there is enough shelter. Several months later, the 40-lb. (18-kg) octopus was moved out of this exhibit and a smaller one of 15 lb. (7 kg) was moved in. This octopus moved directly into the large male wolf eel's cave and displaced it for two days without any overt sign of aggression; it seemed to have a bold personality. After two days, the wolf eel took back its cave. There may have been wolf eel–octopus wars going on at night for the possession of this prime den, but we don't know.

Other main predators of octopuses are marine mammals, particularly seals. In the North Pacific, sea otters are major predators of the giant Pacific octopus. In Alaska's Prince William Sound, David Scheel et al. (2002, 2007) studied the return of giant Pacific octopuses and sea otters after the Valdez oil spill disaster of 1989. He found that octopuses were using the shallows and intertidal zone and also the area deeper than 100 ft. (30 m), areas above and below the sea otters' usual foraging range. He speculated that the sea otters had simply eaten the octopuses between those two depths. Of course, river otters are casual visitors to the marine world, and in coastal areas they spend considerable time on shore and in the shallows. They, too, have been reported to catch octopuses, so the octopus isn't safe in the intertidal region.

Many sea birds and shore birds will eat octopuses but not as a major part of their diet. Crabs and gulls are thorough foragers in the intertidal zone, so an octopus in a tide pool is at risk. Sea birds such as penguins eat
large quantities of squid, and sometimes cephalopods eat birds, as well. In Puget Sound, giant Pacific octopuses have been seen eating seabirds—gulls and alcids. At low tide, one octopus with a den at the bottom of an intertidal boat launch ramp on Whidbey Island caught and ate both glaucous-winged gulls and pigeon guillemots.

In some cases, supposed octopus predators are probably dining on senescent octopuses, particularly males that have mated already or females whose eggs have hatched. Scavengers along the beach, such as wolves and coyotes, are often blamed for the deaths of octopuses they are feeding on. At the end of their life cycle, octopuses don't act normally—they don't eat and they don't live in dens—so they are extremely susceptible to predation. Even among fish, when stomachs of supposed predators are examined and octopuses are found, it is quite possible that these fish were simply preying on dying, senescent octopuses rather than actively hunting down and eating active, alert octopuses.

It may be surprising to learn that 20-ft. (7-m) killer whales, or orcas, eat giant Pacific octopuses. These orcas live in the North Pacific; they are large, the largest of the dolphins, and can select large prey. Maybe the octopuses they caught were senescent and were crawling or swimming outside of their dens, where they were highly susceptible to being eaten, because it's difficult to believe that an orca could capture an octopus inside a den or a healthy octopus out hunting at night on the bottom.

A recent observation by scuba divers proves the susceptibility of old octopuses to predation when they are exposed. Scuba divers reported seeing three large male giant Pacific octopuses out in the open at a popular dive site in Puget Sound. They estimated that each animal weighed over 60 lb. (27 kg), a normal size for adult male giant Pacific octopuses. Each was missing at least four arms, and one was missing at least half of each of its arms and was crawling around on the stubs. During this same dive, the divers saw a 12-ft. (4-m) six-gill shark make a pass over the octopuses. It is likely that these male octopuses senesced at about the same time, reaching the natural end of their lives, and ended up providing food for predators such as the shark, which was scavenging on the near-dead octopuses.

Although many predators such as sharks prefer to eat live prey, most are not averse to eating carrion like dead octopuses. Carrion—animals that have died from some other means—is a good source of food that doesn't fight back. Many animals we think of as fierce predators eat a lot of carrion. Lions much prefer to eat a dead herbivore on the African veldt than spend
the considerable energy needed to stalk and catch it, running the risk of getting gored by horns or kicked by sharp hooves. The bald eagle, often envisioned as hunting down small mammals, actually gains much of its nourishment from salmon that die after they spawn in rivers.

The main refuge against predators for a shallow-water octopus is its den (see plate 27). Since octopuses live in relatively small dens, often not much larger than themselves, with a small or narrow opening, predators usually can't get to them through the small opening, capture them, and pull them out. We have observed that octopuses need a place of protection while they sleep, and they do this in dens. The octopuses that construct dens in sand or mud are also protected, because predators that would try digging them out would get a mouthful of mud.

If a shallow-water octopus is in its den and a moray eel, wolf eel, or invading octopus comes along, it has several methods to repel them. At rest, it sits in the opening of the den with one dorsal (first) arm across the opening with the suckers facing outward. It usually has one eye peering out over the arm. Incidentally, individual octopuses are either left eyed or right eyed, usually looking consistently with one eye or another, just as we humans are left handed or right handed. In this posture, the octopus can see the action going on outside the den, it can readily lash out one or more arms at the invader, and its mouth is positioned outward, ready to bite with the beak and inject deadly venom, if necessary, when attacked. Octopuses make this defense more effective by blocking up the entrance to their dens with rocks and shells, further preventing predators from seeing them or getting at them. Jennifer calls this construction of a defensive wall “tool use” by the octopus.

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