The Soul of an Octopus

by Sy Montgomery

  A 1972 study mistakenly suggested that the platypus, a primitive, egg-laying mammal whose ancient lineage stretches back 80 million years, did not experience REM sleep, the kind of sleep during which humans dream. But those researchers were looking in the wrong place in the brain. In 1998, a new study showed that, in fact, the platypus experiences more REM sleep—some fourteen hours a day—than any other known mammal.

  Much less work has been done on fish than on mammals. But it is known that fish sleep. Even nematodes and fruit flies sleep. A 2012 study showed that if fruit flies’ sleep is interrupted repeatedly, they have trouble flying the next day—just as a person would have trouble concentrating after a sleepless night.

  In a book I love so much that my husband reads it to me every Christmas, Wales’s greatest poet, Dylan Thomas, takes his readers to Milk Wood, a small town by the “slow, black, crowblack, fishing-boat-bobbing sea.” It is night, and the characters in the book are all asleep; the author offers his readers a chance to enter the most alluring and impossible of intimacies: “From where you are,” he promises, “you can hear their dreams.”

  When a fish appears to you in a dream, according to Jungian interpretation, the animal represents insights bubbling up from the intimate, oceanic mystery of the unconscious. But on this morning, on an ordinary day in a public institution, while moms pushed their babies in prams and kids laughed and pointed and squealed around me, I had experienced not just an insight, but a revelation: I had seen the dreams of a fish, hunting and stunning its prey.

  We returned to Octavia, and Scott put the squid on the end of the long grabber so he could hold the food right in front of her face. She seized the squid—and the tongs. I ran up the steps to the tank, stubbing my toe, and plunged both arms into the water. She dropped the squid. She’d wanted the tongs—and now she wanted me, too. While holding fast to the side of the tank with hundreds of suckers, and still holding the tongs in dozens of others, Octavia grabbed my left arm with three of her arms and my right arm with yet another of hers, and began to pull—hard.

  Her thorny red skin showed her excitement. Her suction was strong enough that I felt her drawing the blood to the surface of my skin. I would go home with hickeys that day. I tried to stroke her, but my hands were immobilized. She kept me at arm’s length, but at least I could see her head. It was now the size of a cantaloupe, and each arm was at least three feet long. She had grown dramatically since my previous visit. The giant Pacific octopus is one of the world’s most efficient carnivores in converting food to body mass. Hatching from an egg the size of a grain of rice weighing three-tenths of a gram, a baby giant Pacific octopus doubles its weight every eighty days until it reaches about 44 pounds, then doubles its weight every four months until maturity.

  Scott was pulling with all his considerable strength on the tongs to keep Octavia from pulling me into the tank. I submitted to the tug-of-war. I had no choice. Though fairly fit for a person of my size (five foot five, 125 pounds), age (fifty-three), and sex (female), I didn’t have the upper-body strength to resist Octavia’s hydrostatic muscles. An octopus’s muscles have both radial and longitudinal fibers, thereby resembling our tongues more than our biceps, but they’re strong enough to turn their arms to rigid rods—or shorten them in length by 50 to 70 percent. An octopus’s arm muscles, by one calculation, are capable of resisting a pull one hundred times the octopus’s own weight. In Octavia’s case, that could be nearly 4,000 pounds.

  Though octopuses are usually gentle, there are accounts of people who have drowned, or nearly so, as a result of the animals’ attentions. English missionary William Wyatt Gill spent two decades in the South Seas, among octopuses much smaller than the giant Pacific; but even these species are strong enough to overwhelm a young, strong, fit man. He wrote that “no native of Polynesia doubts the fact” that octopuses are dangerous. Gill reports that one fellow, who was hunting octopus, would have smothered were it not for his son, who rescued him when he surfaced with an octopus blanketing his face.

  Another account comes from waters off New Zealand from a D. H. Norrie, who was wading in sea channels searching for lobsters with Maori friends. Suddenly, one of his companions “began shrieking and trying to free himself from something that was holding him fast. We moved over to help him and found him to be struggling with a young octopus!” The animal was only 30 inches long—and yet without his friends, Norrie told the author Frank Lane, the man would never have escaped, and would have surely drowned.

  Octavia was using only a tiny fraction of her great strength. Compared to what she could do, this was just a playful tug. I didn’t feel I was under attack. I felt I was under investigation.

  I could have been in her grip for only a minute, or it might have been five, but after what felt like a considerable time, suddenly she shrank from us. She let go of me and the tongs at the same moment.

  “Wow!” I said as she retreated to her lair. “That was amazing!”

  “I was pulling with all my strength!” Scott said. “I was afraid I would end up holding you by the ankles!”

  What had happened between Octavia and me? What was she thinking? It was obvious she wasn’t hungry, or she would have eaten the squid. She didn’t seem fearful or angry—I can almost always feel that from a mammal or bird, though I wasn’t sure I could pick it up from a mollusk. Yet Scott and I agreed that this encounter was utterly different from my first, playful encounters with Athena. “This may have been some sort of dominance display,” Scott said. Perhaps she wanted the tongs and concluded, reasonably though incorrectly, that I was keeping them from her. Another thought occurred to me: When I stubbed my toe racing up to the tank, my chemistry changed, as the neurotransmitters associated with pain flooded into my system. Being able to recognize the neurotransmitters of pain would be a useful ability for an octopus; then it could tell whether prey was injured and therefore particularly easy to subdue. Earlier in the day, I had seen a fish’s dreams—and now, perhaps, an octopus had tasted my pain.

  In this watery realm, I was being drawn to possibilities I had never before imagined.

  Those who work with octopuses report seeing things that, according to the way we’ve learned the world normally works, should not be happening.

  Such was the day Alexa Warburton found herself chasing a fist-size octopus as it ran across the floor.

  Yes, ran. “You’d chase them under the tank, back and forth, like you were chasing a cat,” she said. “It’s so weird!”

  Alexa was a pre-veterinary student at Middlebury College’s newly created octopus lab in Vermont. It seemed to her that some of the octopuses were purposely, and sometimes elaborately, uncooperative. When a student would try to scoop an animal from its tank with a net and transfer it to a bucket to run a T-maze, for example, the octopus might hide, squeeze into a corner, or hold fast to some object and refuse to let go. Some would allow themselves to be captured, only to use the net as a trampoline. They’d leap off the mesh like acrobats and dive to the floor—and then run for it.

  Alexa described the experience of working with these small invertebrates as “surreal.” At the little lab, which was located in a former janitorial closet, she and the other students worked with two different species: the tiny Caribbean dwarf octopus, and the larger California two-spot, which can reach a mantle length of seven inches and have arms up to 23 inches long. “They were so strong,” she said. “This animal is so small, it fits in my hand—and yet it’s as strong as I am!”

  The lab’s 400-gallon tank had a weighted lid, and was divided into separate compartments for each animal. But the octopuses would escape. They would push out from under the lid and crawl out, and sometimes die; they would dig beneath the dividers, which the students had hammered in, to get in another octopus’s compartment, and they’d eat each other. Or they’d mate, which was just as lethal for the students’ experiments. After mating, females lay eggs, hole up, and refuse to run mazes, and then when their eggs hatch they die; the males die soon after
mating.

  Even more impressive than the octopuses’ physical strength was the force of their will, the sheer strength of each individual personality. The students were supposed to refer to their animals by numbers in their research papers, but they ended up calling them by name: Jet Stream, Martha, Gertrude, Henry, Bob. Some were so friendly, Alexa said, “they would lift their arms out of the water like a dog jumps up to greet you”—or like a child who wants to be lifted up and hugged. One named Kermit liked Alexa to pet him, and seemed to snuggle into the caress “by raising his shoulders—even though he didn’t have shoulders.”

  Others were irascible. One of the dwarf Caribbeans was such a problem the students called her the Bitch. “Catching her for the maze always took twenty minutes,” Alexa said. This octopus would invariably grip onto something and not let go.

  And then there was Wendy. Alexa used her as part of her thesis presentation. It was a formal event that was videotaped, for which Alexa wore a nice suit. As soon as the cameras started rolling, Wendy drenched the student with salt water. Then the octopus scurried to the bottom of the tank, hid in the sand, and refused to come out. Alexa is convinced the whole debacle occurred because the octopus realized in advance what was going to happen and resolved to prevent it.

  “Wendy,” she said, “just didn’t feel like being caught in the net.”

  Data from Alexa’s experiments showed the California two-spots were quick learners. But Alexa learned far more than a refereed journal could publish. “They’re so curious,” she told me. “They want to know about everything around them. An invertebrate! This supposedly simple, simple animal!

  “We don’t understand them,” she continued. “Try to make a maze that will show how this creature thinks. We don’t even understand them enough to test them. Maybe mazes aren’t the way to study them. Science can only say so much. I know they watched me. They followed me. But proving that intelligence is so difficult. There’s nothing as peculiar as an octopus.”

  A week after Octavia nearly pulled me into her tank, I was back at the aquarium.

  Sparked by an article I had written for Orion magazine, friends at the national environmental radio show Living on Earth wanted to record a segment with me on octopus intelligence. They hoped to interact with Octavia. I had no idea what to tell them to expect.

  I came in early to visit with Scott, Wilson, and Bill. What kind of reception might Octavia give my radio friends? Bill, who had worked with five octopuses over his eight years at the aquarium, characterized her personality this way: “Aggressive and standoffish.”

  “This one,” agreed Wilson, “isn’t playful.” Unlike all the others, he said, about half the time he tried to interact with her, she completely ignored him.

  Octavia was different from the other octopuses Wilson had known in another important way: She camouflaged. Previous octopuses, who had all come as young pups, had lived behind the scenes in tanks or barrels that were completely barren—no hiding places, no rocks or sand or tank mates. And though these octopuses could turn color—growing red when excited, pale or white when calm, and showing shades of brown and white and mottling in between—they didn’t camouflage to match their background. There was nothing much to match. Wilson noticed that even when they were transferred to the public display tank, they still didn’t camouflage.

  But Octavia did.

  The ability of the octopuses and their kin to camouflage themselves is unmatched in both speed and diversity. Octopuses and their relatives put chameleons to shame. Most animals gifted with the ability to camouflage can assume only a tiny handful of fixed patterns. The cephalopods have a command of thirty to fifty different patterns per individual animal. They can change color, pattern, and texture in seven tenths of a second. On a Pacific coral reef, a researcher once counted an octopus changing 177 times in a single hour. At Woods Hole Oceanographic Institution, cephalopods put on laboratory checkerboards virtually disappear. They don’t make checks, of course; but they can create a pattern of light and dark that makes them invisible on virtually any background, to virtually any eye.

  Octopuses and their relatives have what Woods Hole researcher Roger Hanlon calls electric skin. For its color palette, the octopus uses three layers of three different types of cells near the skin’s surface—all controlled in different ways. The deepest layer, containing the white leucophores, passively reflects background light. This process appears to involve no muscles or nerves. The middle layer contains the tiny iridophores, each 100 microns across. These also reflect light, including polarized light (which humans can’t see, but a number of octopuses’ predators, including birds, do). The iridophores create an array of glittering greens, blues, golds, and pinks. Some of these little organs seem to be passive, but other iridophores appear to be controlled by the nervous system. They are associated with the neurotransmitter acetylcholine, the first neurotransmitter to be identified in any animal. Acetylcholine helps with contraction of muscles; in humans, it is also important in memory, learning, and REM sleep. In octopuses, more of it “turns on” the greens and blues; less creates pinks and golds. The topmost layer of the octopus’s skin contains chromatophores, tiny sacks of yellow, red, brown, and black pigment, each in an elastic container that can be opened or closed to reveal more or less color. Camouflaging the eye alone—with a variety of patterns including a bar, a bandit’s mask, and a starburst pattern—can involve as many as 5 million chromatophores. Each chromatophore is regulated via an array of nerves and muscles, all under the octopus’s voluntary control.

  To blend with its surroundings, or to confuse predators or prey, an octopus can produce spots, stripes, and blotches of color anywhere on its body except its suckers and the lining of its funnel and mantle openings. It can create a light show on its skin. One of several moving patterns the animal can create is called “Passing Cloud” because it’s like a dark cloud passing over the landscape—making the octopus look like it’s moving when it’s not. And of course the octopus can also voluntarily control its skin texture—raising and lowering fleshy projections called papillae—as well as change its overall shape and posture. The sand-dwelling mimic octopus, an Atlantic species, is particularly adept at this. One online video shows the animal altering its body position, color, and skin texture to morph into a flatfish, then several sea snakes, and finally a poisonous lionfish—all in a matter of seconds.

  No researcher today suggests that all of this is purely instinctive. An octopus must choose the display it needs to produce for the occasion, then change accordingly, then monitor the results—and, if necessary, change again. Octavia’s camouflage abilities were superior to those of her predecessors because, living longer in the ocean among wild predators and prey, she had learned them.

  This is more evidence of the octopus’s alien, invertebrate intelligence. But I feared my friends from the radio show might not get to see even a glimmer of Octavia’s sparkling mind, and would witness only a baggy, boneless body balled up in its lair. “If she doesn’t want to come,” Wilson reminded me, “forget it.”

  So I was completely unprepared for what happened when Bill opened the top of her tank that afternoon. As host Steve Curwood, his producer, and his sound crew stood by, Wilson fished a capelin out of the small plastic bucket of fish he had positioned at the lip of Octavia’s tank. Flushed with excitement, Octavia flowed immediately over to him—not just extending an arm or two, but rushing toward him with her whole body. Her head bobbed to the surface so she could look into our faces. She looked us both directly in the eyes and then accepted the capelin. As she conveyed it toward her mouth, three of her arms rose from the water, and she grabbed Wilson’s free hand with some of her largest suckers. I plunged my hands and arms in and she grabbed me, too. One arm, two, then a third, attached to me. I could feel the suction of the suckers, but her arms did not pull me.

  “Steve, meet Octavia.” Bill invited Steve to let her touch him, too. “Roll up your sleeves; take off your watch,” he instructed. “We al
ways joke that they’re very sticky fingered, so they could probably slip off a ring or a watch without you realizing it, but also, we don’t want anything sharp on ourselves that would hurt them.”

  Steve obliged and extended his fingers. Octavia uncurled an arm to taste him.

  “Oh!” cried Steve. “She’s grabbing ahold, here—”

  Wilson handed Octavia another capelin.

  “Yup, feel the suckers!” said Steve. Bill explained that she could control each sucker individually. “Wow!” said Steve. “So she’d be amazing playing the piano—can you imagine?”

  We were drowning in sensation: the feel of Octavia’s suckers on our skin, the spectacle of her subtly changing color, the procession of the capelin as they were passed forward to her mouth, the unconstrained acrobatics of her many unjointed arms. Six of us were watching her, and three of us had arms in the tank, before anyone noticed what had happened: She had managed to steal the bucket of fish right out from under us. She was holding the bucket fast with some of her strongest, biggest suckers while using hundreds of other suckers to explore Wilson, Steve, and me.

  Octavia wasn’t interested in the fish. They were still in the bucket. She was holding it in such a way that the fish, in the bucket’s bowl, faced away from her. She drew the webbing between her arms around the bucket almost like a hawk hides its captured prey with its wings. As she had been with the tongs she grabbed from Scott the week before, Octavia was more interested in the object that held the food than in even the food itself.

  Apparently the six of us were not sufficiently interesting to occupy her vast capacity for attention. And unlike the guest who texts and checks his e-mail while eating and carrying on a conversation at a dinner party, Octavia did not seem distracted as she multitasked; she was able to focus on each of her many, simultaneous efforts. This stunned us all the more, because we had clearly been overcome by our single—and, one would think, simple—task: watching what the animal, who we were actually touching, was doing.