The Soul of an Octopus

by Sy Montgomery

  It’s getting dark and cold. During the hour we wait topside, off-gassing the nitrogen built up in our blood, Big D and I huddle beneath a shared towel, shivering and giggling. Now I’m nervous. I think: My ears; the dark; it’s night, and this is the ocean.

  Francisco convenes the dive briefing. “We are almost there,” he says. “Paradise: this place is called Paradiso. Of all the places in Cozumel, this is the place of the night dive. I am thinking we are going to see octopus and shark. But every night you are here is different. One night there will be lots of octopus. On the full moon, the octopus is out because he is a predator and the moon is his strobe. But lobsters stay in their hole. You may see huge crabs. You may see large squid, too. There are eels, the sharp-tailed eel who looks like a snake. You find him on the side of the reef.

  “We’ll meet at the surface first, at the back of the boat, and go down together. Get your light on. When you use hand signals, light your hand. And when you surface, when you come up, shine the light on your head so the boat can find you.

  “I have an orange-brown light and a green one. If you see that, that’s me. Okay—let’s go!”

  We each have two lights: a flashlight and a glow-stick on our backs. I stride in right after Rob. Because of the problems with the shore night dive, he decides to hold my right hand throughout the dive. We descend together slowly. At three feet I start equalizing. I feel a squeeze. I blow and blow and descend some more. At ten feet, I signal Rob “trouble with ears.” We rise, together, a foot or two. I Frenzel. I Valsalva. I tip my head to one shoulder, then the other. That’s better. I shine my light on my left hand, signaling “okay.” I drop a foot, two, three. My ears squeal. But unless the pain is shattering, I am going to continue.

  Finally Rob and I are on the bottom with the others. We proceed along the reef in the dark. I am so glad he is holding my hand, because I am finding it very difficult to adjust my buoyancy, use my flashlight to see my depth gauge, clear my ears and sometimes my mask, and look for animals in the small disk of light from my flashlight all at once. It feels as if I am traveling in a small capsule in outer space. Around me the darkness is heavy and enveloping. My senses have constricted and intensified to focus only on this tiny circle of light. And here it reveals a huge crab—a tall purple turret of coral—a bright blue angelfish! A school of snapper mass beneath a coral. A spiny lobster waves its antennae. Ahead there are flashes of light, like heat lightning, from my friends’ cameras, contrails of light trailing from their BCDs. And then: an octopus! I squeeze Rob’s hand, but he has already seen it, oozing from its hole. It’s brown with white stripes, then becoming lighter as its arms boil out of its lair. Three arms walk forward, and then it turns its head, its eyes looking directly into our faces, turns green, then brown, then disappears.

  Yellow coral animals are extending their feeding tentacles. Purple and orange sponges heave into view. A second octopus! Its eyes pop up, then down. The area surrounding the eye seems yellow, the pupil a slit. In an instant, it flashes speckles on its skin, a starscape, and then pours itself back down its lair.

  Ahead, my flashlight reveals that Francisco is playing with a puffer fish, who for some reason allows him to gently palm its belly. But Rob is twirling his light to catch my attention. Directly below us is a third octopus. I flip head down, feet up, to observe it. This octopus is larger than the other two, and the animal doesn’t seem as alarmed. Its funnel faces away from me as it crawls toward me. It flashes stripes, then dots. I feel as if it’s testing me, like a scientist conducting an experiment, to see what I’ll do. I want to stay, but the current is sweeping me away, and so is Rob, who must not let us get separated from the others in the dark. I feel like Dr. Zhivago having just spotted his long-lost Lara in the busy city at the end of the eponymous movie—but I am in the ocean’s grip and its currents propel me forward.

  Marvels flash before me in the circle of my light: a sharp-tailed eel, its tail a flat paddle, pointed at the tip. Striped grunts, so named for the grinding sound they make with their teeth. A bright blue angelfish. A huge crab. But the pressure in my ears is building. I am having trouble focusing my attention. I constantly blow out my nose, trying to equalize, but instead create a bizarre underwater sound track inside my head, squeals and bubblings accompanying the Darth Vader hissing of my regulator. If it were not for Rob’s hand holding mine, I would be completely disoriented.

  And then, a fourth octopus, this time on a reef wall! This one is quite small and shy, and all I see are eyes and suckers peering from a hole in the corals. My ears are screaming as Rob gives the thumbs-up sign that it’s time to surface. I ascend with him slowly, like a dying soul reluctant to leave its body, and we watch the silver trail of our bubbles rising above us like shooting stars.

  CHAPTER SIX

  Exit

  Freedom, Desire, and Escape

  Upon my return, the elderly Octavia is still going strong. She is very active, swirling her suckers, turning her mouth toward the glass. Then she flips back, her body hanging below her head. She makes an eyebar, then mottles, then runs three arms across her brow. Gaping her gill opening wide as a pitcher, she inserts one arm into its entrance and then pokes the tip of her arm out her funnel, waving it like a person hailing a cab. She pulls that arm out, then sticks in another arm. Now she grows paler, expanding hugely with each breath and exhaling forcefully through her funnel. Her pupil is a fat bar, giving her an intense expression. Then she rotates her funnel, more flexible than a tongue, out of my sight. She continues to modify her coloring: Her eyebar gone, now she creates a starburst pattern. Her mottling is as rich and varied as a plush Persian carpet as she fluffs the eggs toward the back of her lair with one arm. She turns and I see that the eggs extend two feet back—there are not just thousands, but tens of thousands of them. I point them out to two children and their mom, and they gasp.

  Half a flight above us, opening the top of the tank, Wilson offers Octavia first one squid, then another, in the long tongs. I watch downstairs with the transfixed children. As the octopus eagerly eats the squid, the sunflower sea star stretches the tube feet at the tip of one arm toward Wilson. “He’s begging for a fish,” I tell the kids. “He’s got no brain, but he’s not stupid. Watch!” Wilson obligingly gives him a capelin, and the star, his stomach side plastered to the glass at eye level to the kids, begins to pass the food from one thin, stalklike foot to the next. While the children watch in slack-jawed wonder, the star slowly conveys the food the full nine inches from the tip of his arm to his mouth—through which he then extrudes his stomach. “He can drool acid right out of his stomach to dissolve his food!” I tell the kids. They squeal with delight as the fish melts away like a cough drop in a person’s mouth.

  Kali is nearly as big as Octavia now, and the problem of where to put her is pressing. Last week, Christa and Wilson tell me, when they fed her, her arms came gushing out of the barrel with such force it was all they could do to peel her suckers away in time to keep her from escaping. “She seemed desperate to get out,” Christa tells me. Today, though, Kali is not at all agitated, but seems friendly and calm, and her cold, wet embrace feels like a warm welcome.

  Perhaps last week’s ruckus was due to her new neighbors. A sick surf perch who shares the sump’s water is being treated with Praziquantel, a drug whose effects on octopuses are unknown, so Bill moved Kali’s barrel to a huge open tank with a different water source, just a few yards away. The tank in which the barrel now floats is occupied by animals he collected on the Gulf of Maine expedition: anemones; orange-footed sea cucumbers who look like Technicolor pickles; stalked tunicates, sea squirts shaped like ginger roots; and lumpfish, battleship gray, appealing and chubby, with mouths shaped in an O of perpetual surprise. The lumpfish is equipped with an adaptation to surf: a single suction cup on the belly, allowing it to adhere to any surface like a window decoration. And lumpfish are smart. A 2009 video records the feats of one named Blondie who, working with one of the marine mammal trainers at the aqua
rium, learned to swim through hoops, blow bubbles on command, hold still for veterinary skin scrapes, and swim in tight circles at the surface. In an obedience-school class my border collie Sally and I once took together, the command for this last behavior was “spin”—a trick which I, even though working with a dog breed famed for its intelligence, failed to teach her.

  One of the new lumpfish seems curious about Kali. Yesterday, Bill tells me, while he was feeding the octopus, the fish came over to investigate the tips of Kali’s arms.

  “Maybe it makes things more interesting for her,” Christa suggests. “I hope so,” says Wilson. “She could use some fun.”

  Even without touching her neighbors, Kali can taste them. Her chemoreceptors can pick up chemical information from a distance of at least 30 yards. One researcher found that octopus suckers were 100 times more sensitive tasting chemicals dissolved in seawater than a human tongue tasting flavors dissolved in distilled water. Perhaps Kali knows her tank mates’ species, their sex, their health.

  Although octopuses are generally asocial with others of their kind, very little is known about their relationships with animals of other species, other than hunting prey or hiding from predators. Experts on home ceph-keeping advise the amateur against housing octopuses with other animals, because the octopus may kill and eat them. But not all interactions with tank mates are necessarily hostile. At British Columbia Waters at the Vancouver Aquarium, curator Danny Kent found that “some individuals can live with schools of rockfish for years and not eat them, while others rapidly pick off all of their tank mates in no time.” One octopus who lived in the aquarium’s 65,000-gallon Strait of Georgia exhibit liked to crawl up the side of the rockwork near the water’s surface and trail one arm into the water column. Kent discovered the octopus was using his arm as a fishing rod, waiting for a herring to bump into it, whereupon he’d seize the fish and eat it.

  Relationships with tank mates may be complicated. In 2000, the Seattle Aquarium made the risky decision to house a giant Pacific octopus in its 400,000-gallon tank with several four- to five-foot dogfish sharks, believing the octopus would hide when threatened. They were wrong. To their astonishment (and to the amazement of 2.9 million viewers, when a video re-creating the incident was posted in 2007 and went viral), the octopus instead began systematically murdering the sharks. The sharks were not missing, but were found dead, uneaten, in the tank. This was not predation, nor an immediate reaction to direct threat. According to the original news reports and the text accompanying the video, the shark-killing spree comprised a series of preemptive strikes, with the octopus taking out potential predators before the sharks even had a chance to threaten it.

  In Cozumel, I had witnessed a peculiar scene which may have been evidence of a different kind of interspecies relationship, the likes of which I had never seen reported before. On my last dive of the trip, we had visited a low-profile reef with relatively few big coral heads and long ledges and overhangs. About half an hour into the dive, at a depth of about 30 feet, we spotted a Caribbean reef octopus on white sand beneath a rocky overhang. I approached to within six feet of the animal and saw to my astonishment that about a dozen live crabs, some reddish and some greenish, with carapaces between two to three inches long, were gathered just inches in front of the octopus. The crabs seemed remarkably calm, considering the predicament they were in. Some were crawling slowly, but when one seemed to be venturing too far away from the octopus, the octopus would extend an arm and (rather gently, I thought) sweep the crab back in closer.

  Everything about this was strange. The octopus was not bright red with excitement, as you would think it would be surrounded with a living buffet of its favorite food; it was white, with an iridescent turquoise sheen. The octopus did not seem to be using its suckers to retrieve errant crabs but instead was sweeping them toward itself with its arms. The crabs, oddly, did not scuttle. And I did not see shell or crab remains, which you usually see outside an octopus den. But perhaps this was not a den. Regardless, there were so many crabs, possibly they were standing on the exoskeletons of former companions but I just couldn’t see them. The octopus looked at me briefly but then turned its attention back to wrangling crabs. It did not retreat at our approach, even as I came as close as three feet.

  I had wanted to stay there longer, but the current was strong, and this was a drift dive. I ask my aquarium friends: What were all those crabs doing there? Why didn’t they all run away? What was the octopus planning to do with the crabs? Was the octopus running a crab ranch? I am only half joking. I throw out another idea: Was it possible the octopus had drugged them with ink?

  American marine zoologists G. E. and Nettie MacGinitie occasionally put a moray eel into a tank containing a mudflat octopus. The moray began to search for the octopus, and when it came too close, the octopus inked. The moray would continue to hunt, but it would not attack the octopus. Even if the moray actually touched the octopus, it showed no interest in attacking or eating it. The same thing happened every time.

  Octopus ink, in addition to the pigment melanin, contains several other biologically important substances. One is tyrosinase, an enzyme that irritates the eyes and clogs the gills. But it may also have other effects. A 1962 article in the British Journal of Pharmacology reports that in experiments on mammals, the enzyme blocks the action of the hormones oxytocin (the “cuddle hormone”) and vasopressin (an antidiuretic hormone that affects circulation). Fish, birds, reptiles, and invertebrates, including octopuses, have their own version of both these hormones. And, as in mammals, oxytocin has been found, in experiments with fish, to affect social interactions. If the natural level of this hormone were altered, might a normally solitary creature like a crab feel unusually calm in a crowd—even a crowd that included a major predator?

  Another substance in octopus ink is dopamine, a neurotransmitter known as the “reward hormone.” I had recently seen an entry mentioning dopamine in one of my favorite octopus blogs, Cephalove, an inquiry into the biology and psychology of cephalopods, started in May 2010 by then Buffalo University psychology major Mike Lisieski. Citing papers by researchers Mary Lucero, W. F. Gilly, and H. Farrington on squid ink, Lisieski speculated, “Squid ink might trick predators into ‘thinking’ they’d caught the squid and were eating it. . . . If a predator gets a mouthful of ink, if they can sense the amino acids that normally tell them they are eating flesh, they may behave as if they have already caught and/or eaten their prey and give up pursuit.” Maybe, I suggest, the crabs were hanging out sedately because they’d been drugged into feeling happy and sated.

  “I think you are reading too much into this,” warns Wilson.

  “What?! You think octopuses running crab ranches, corralling the crab herd by drugging them with ink is crazy?” I reply. “Then listen to this.”

  I relate my conversations with Peter Godfrey-Smith, a philosopher who spends his summers diving around Sydney Harbor among giant cuttlefish and octopus. He describes these encounters as “like meeting an intelligent alien.”

  Like humans, the cephs he met were intelligent and aware. “But look at all those neurons in the arms!” he said. “They may have a radically different style of psychological organization from us. Perhaps in octopus we see intelligence without a centralized self. If you have the design of an octopus,” Peter asked, “is there a sense of self at all, a center of experience? If not, that involves imagining something so different from us it might be impossible to think of.”

  If there is no central consciousness, does an octopus have a “collaborative, cooperative, but distributed mind,” as Peter suggests? Does it have a sense of multiple selves? Does each arm literally have a mind of its own?

  It’s even possible that octopuses have some shy arms and some bold arms. University of Vienna researcher Ruth Byrne reported that her captive octopuses always choose a favorite arm to explore new objects or mazes—even though all their limbs are equally dexterous. She looked at eight octopuses, all of whom would jump on pre
y with all their arms, curling both the interbrachial web and arms around whatever food item they would find. But they all used combinations of one, two, or three favorite arms when manipulating objects. Her team counted the octopuses using only forty-nine different combinations of one, two, or three arms for manipulating objects, when, according to her calculations, 448 combinations were actually possible if all eight arms were involved.

  This could simply be an instance of handedness. Tank-bound octopuses, at least, are known to have a dominant eye, and Byrne thinks this dominance might be transferred to the front limb nearest the favored eye.

  But the bold versus shy arms could be something quite different. While arms can be employed for specialized tasks—for example, as your left hand holds the nail while your right hand wields the hammer—each arm may have its own personality, almost like a separate creature. Researchers have repeatedly observed that when an octopus is in an unfamiliar tank with food in the middle, some of its arms may walk toward the food—while some of its other arms seem to cower in a corner, seeking safety.

  Each octopus arm enjoys a great deal of autonomy. In experiments, a researcher cut the nerves connecting an octopus’s arm to the brain, and then stimulated the skin on the arm. The arm behaved perfectly normally—even reaching out and grabbing food. The experiment demonstrated, as one colleague told National Geographic News, “there is a lot of processing of information in the arms that never makes it to the brain.” As science writer Katherine Harmon Courage put it, the octopus may be able to “outsource much of the intelligence analysis [from the outside world] to individual body parts.” Further, it seems “that the arms can get in touch with one another without having to go through the central brain.”