Other Minds: The Octopus and the Evolution of Intelligent Life

This case illustrates a more general fact: octopuses have an ability to adapt to the special circumstances of captivity and their interaction with human keepers. Octopuses in the wild are fairly solitary animals. Their social life, in most species, is thought to be minimal (though later I’ll look at exceptions to this pattern). In the lab, however, they are often quick to get the hang of how life works in their new circumstances. For example, it has long appeared that captive octopuses can recognize and behave differently toward individual human keepers. Stories of this kind have been coming out of different labs for years. Initially it all seemed anecdotal. In the same lab in New Zealand that had the “lights-out” problem, an octopus took a dislike to one member of the lab staff, for no obvious reason, and whenever that person passed by on the walkway behind the tank she received a jet of half a gallon of water in the back of her neck. Shelley Adamo, of Dalhousie University, had one cuttlefish who reliably squirted streams of water at all new visitors to the lab, and not at people who were often around. In 2010, an experiment confirmed that giant Pacific octopuses can indeed recognize individual humans, and can do this even when the humans are wearing identical uniforms.

Stefan Linquist, a philosopher who once studied octopus behavior in the lab, puts it like this: “When you work with fish, they have no idea they are in a tank, somewhere unnatural. With octopuses it is totally different. They know that they are inside this special place, and you are outside it. All their behaviors are affected by their awareness of captivity.” Linquist’s octopuses would mess around with their tank, manipulating and testing it. Linquist had a problem with octopuses deliberately plugging the outflow valves on the tanks by poking in their arms, perhaps to increase the water level. Of course, this flooded the entire lab.

Another tale that illustrates Linquist’s point was told to me by Jean Boal, of Millersville University in Pennsylvania. Boal has a reputation as one of the most rigorous and critical of cephalopod researchers. She is known for her meticulous experimental designs, and her insistence that “cognition” or “thought” in these animals should be hypothesized only when experimental results cannot be explained in any simpler way. But like many researchers, she has a few tales of behaviors that are baffling in what they seem to show about the inner lives of these animals. One of these incidents has stayed in her mind for over a decade. Octopuses love to eat crabs, but in the lab they are often fed on thawed-out frozen shrimp or squid. It takes octopuses a while to get used to these second-rate foods, but eventually they do. One day Boal was walking down a row of tanks, feeding each octopus a piece of thawed squid as she passed. On reaching the end of the row, she walked back the way she’d come. The octopus in the first tank, though, seemed to be waiting for her. It had not eaten its squid, but instead was holding it conspicuously. As Boal stood there, the octopus made its way slowly across the tank toward the outflow pipe, watching her all the way. When it reached the outflow pipe, still watching her, it dumped the scrap of squid down the drain.

This story, along with all the tales of octopuses squirting experimenters, reminded me of something I’d seen myself. Captive octopuses often try to escape, and when they do, they seem unerringly able to pick the one moment you aren’t watching them. If you have an octopus in a bucket of water, for example, it will often look content enough in there, but if your attention strays for a second, when you look back there will be an octopus quietly crawling across the floor.

I thought I might be imagining this tendency, until I heard a talk a few years ago given by David Scheel, who works with octopuses full-time. He, too, said that octopuses seem to track in subtle ways whether he is watching them or not, and they make their move when he isn’t. I suppose this makes sense as a natural behavior in octopuses; you want to make a run for it when the barracuda is not looking at you, rather than when he is. But the fact that octopuses can so quickly do this with humans – both with scuba mask and without – is impressive.

As stories of this kind accumulate, an explanation suggests itself for the mixed results with octopuses in some standard learning experiments. It’s often said that they don’t do especially well in these experiments because the behaviors required are unnatural. (Hanlon and Messenger said this about the Dews experiment with the lever pulling, for example.) But octopus behavior in laboratory settings indicates that “unnatural” is often no problem for them. Octopuses can open screw-cap jars for food, and one has even been filmed opening such a jar from the inside. Behaviors don’t get much more unnatural than that. I think the problems with the old Peter Dews experiment, such as they were, came in part from the assumption that an octopus would be interested in pulling a lever repeatedly to get pieces of sardine, collecting piece after piece of this second-rate food. Rats and pigeons will do things like that, but octopuses take a while to deal with each item of food, probably can’t cram themselves, and tend to lose interest. For at least some of them, taking the lamp down from above the tank and hauling it back to the den – that is more interesting. So is squirting the experimenters.

In response to the difficulty of motivating the animals, some researchers, regrettably, have used negative reinforcement – electric shocks – more freely than they would with other animals. Quite a lot of the early work done in the Naples Zoological Station treated octopuses badly. Not only were electric shocks used, but many experiments included the removal of parts of the octopus’s brain, or the cutting of important nerves, just to see what the octopus would do when it woke up. Until recently, octopuses could also be operated on without anesthetic. As invertebrates, they were not covered by animal cruelty rules. Many of these early experiments make for distressing reading for someone who regards octopuses as sentient beings. Over the last decade, however, octopuses have often been listed as a kind of “honorary vertebrate” in rules governing their treatment in experiments, especially in the European Union. This is a step forward.

Another octopus behavior that has made its way from anecdote to experimental investigation is play – interacting with objects just for the sake of it. An innovator in cephalopod research, Jennifer Mather, along with Roland Anderson of the Seattle Aquarium, did the first studies of this behavior, and it’s now been investigated in detail. Some individual octopuses – and only some – will spend time blowing pill bottles around their tank with their jet, “bouncing” the bottle back and forth on the stream of water coming from the tank’s intake valve. In general, the initial interest an octopus takes in any new object is gustatory – can I eat it? But once an object is found to be inedible, that does not always mean it’s uninteresting. Recent work in the lab by Michael Kuba has confirmed that octopuses can quickly tell that some items are not food, and are often still quite interested in exploring and manipulating them.

~ Visiting Octopolis

In the first chapter I described Matthew Lawrence’s discovery of an octopus site on the east coast of Australia. Matt explored the bay by dropping an anchor off his small boat, swimming down to pick it up, and letting the drift of the boat guide his wandering over the sea floor. (I should add that diving alone is a bad idea. Matt takes down a second air supply that is completely independent of the first, in case things go wrong. Even then, it’s not recommended.) In 2009 he came across a shell bed with about a dozen octopuses living on it. They seemed unconcerned by his presence, roaming and wrestling with each other as he watched.

Matt marked the GPS coordinates of the spot and began visiting regularly. He’d watch and interact with the octopuses. They didn’t seem to mind his presence at all, and some were curious enough to play with him and explore his equipment. His camera and air hoses soon had octopuses roaming over them. Others were too busy dealing with each other. Sometimes he saw what looked like a kind of “bullying” behavior. An octopus would be sitting quietly in its den, and a larger one would come over, jump on top of the den, and wrestle furiously with the one below. After a great multicolored convulsion, the octopus below would come flying out like a rocket, its body pale, and land a few meters away, just off the shell bed. The aggressor octopus would wander back to its den.

As time passed, Matt became more and more accustomed to dealing with these animals, and to this day it seems to me that the octopuses treat Matt differently from anyone else. Once at a site close to this one, an octopus grabbed his hand and walked off with him in tow. Matt followed, as if he were being led across the sea floor by a very small eight-legged child. The tour went on for ten minutes, and ended at the octopus’s den.

Though he’s not a biologist, Matt had a sense that his site might be unusual. He posted some photos on a website that functions as an information center for cephalopod-inclined hobbyists and scientists. There they were seen by the biologist Christine Huffard, who asked me: Did I know this place? I was startled when I read about what he’d found, and Matt’s site is only a few hours from Sydney. I got in touch when I was next in town, and drove down to meet him.

Matt, I found, is a scuba fanatic. He keeps his own air compressor in a garage, where he concocts personalized mixes of enriched air to fill his tanks. Soon we were chugging out on his small boat to a spot in the middle of his bay, where he set the anchor and we swam down the line, observed by just a few small fish.

The site we now call Octopolis is about fifty feet down. It’s almost invisible until you get quite close, and the sea floor around it is nondescript. Scallops live scattered in little clumps, or on their own, and various kinds of seaweed waft about on the sand. My first trip to the site, in cold winter water, was quiet. We found just four octopuses, who were not doing much. But I could tell it was an unusual place. There was a bed of scallop shells, as Matt had said, a couple of yards in diameter. It seemed to contain shells of many ages. An encrusted rock-like object, a foot high or so, sat in the middle, with the largest octopus on the site using it as a den. I took measurements and photos, and began coming back whenever I could. Soon I was seeing the high concentrations of octopuses and complex behaviors that Matt had encountered on his first dives there.

If we had air enough and time, I don’t know how long we’d stay down there. When the site is active, it’s enthralling. The octopuses eye each other from their dens among the shells. They periodically haul themselves out and move over the shell bed or away onto the sand. Some will pass by others without incident, but an octopus might also send out an arm to poke or probe at another. An arm, or two, might come back in response, and this leads sometimes to a settling-down, with each octopus going on its way, but in other cases it prompts a wrestling match.

The first photo on the next page was taken just off the edge of the site, and it’s to give you a sense of how these animals look. The species is Octopus tetricus, a medium-size octopus found just in Australia and New Zealand. This is a fairly large individual; from the sea floor to the high spot at the end of its back would be a bit under two feet. It is rushing toward another octopus, off to the right.

The next scene is on the shell bed itself. The octopus on the left is leaping toward the one on the right, who is stretched out and starting to flee.

Frame from video taken by unmanned cameras (collaboration by Peter Godfrey-Smith, David Scheel, Matt Lawrence and Stefan Linquist).

And this is a more serious fight, on the sand just off the edge of the site:

In order to study changes in the shell bed, I once brought out some stakes and hammered them into the sea floor to mark the site’s approximate boundaries. The stakes, about seven inches long, were made of plastic, so I taped a heavy metal bolt to each one to give it more weight. I drove the stakes in so that only an inch or so of each one sat above the sand, and placed them at the four compass points. They’re very inconspicuous, hard to see unless you know exactly where to look. Some months later I went out to the site again, and found that one of the stakes had been hauled out and added to the pile of debris around one of the octopus dens, some distance away. The stake, I think, would have quickly been found inedible, and it was probably not especially useful as a barricade. But as with tape measures, cameras, and many other things we bring down to the site, the stake’s novelty seemed to make it interesting to an octopus.

Other octopus manipulations of foreign objects are done for more practical reasons. In 2009, a group of researchers in Indonesia were surprised to see octopuses in the wild carrying around pairs of half coconut shells to use as portable shelters. The shells, neatly halved, must have been cut by humans and discarded. The octopuses put them to good use. One half-shell would be nested inside another, and the octopus would carry the pair beneath its body as it “stilt-walked” across the sea bottom. The octopus would then assemble the halves into a sphere with itself inside. A wide range of animals use found objects for shelters (hermit crabs are an example), and some use tools for collecting food (including chimps and some crows). But to assemble and disassemble a “compound” object like this, and put it to use, is very rare. It’s not clear what to compare this behavior to, in fact. Many animals combine a variety of materials when making nests – a lot of nests are “compound” objects. But those are not disassembled, carried around, and put back together.

The coconut-house behavior illustrates what I see as the distinctive feature of octopus intelligence; it makes clear the way they have become smart animals. They are smart in the sense of being curious and flexible; they are adventurous, opportunistic. With this idea on the table I can add more to my picture of how octopuses fit into the range of animals and the history of life.

In the previous chapter, using some ideas from Michael Trestman, I said that across the wide range of animal body plans, only three groups contain some species with “complex active bodies.” Those are chordates (like us), arthropods (like insects and crabs), and a small group of mollusks, the cephalopods. The arthropods went down this road first, in the early Cambrian, over 500 million years ago. The way they did this may have initiated a process of evolutionary feedback that soon encompassed everyone else. Arthropods were first, and chordates and cephalopods followed.

Setting aside our own case, we can see a difference in the paths taken by the two other groups. Many arthropods specialize in social living and coordination. Not all of them do this – indeed, the majority of arthropod species don’t – but in the area of behavior, many of the great arthropod achievements are social. This is seen especially in ant and honeybee colonies, and in the air-conditioned cities built by termites.

Cephalopods are different. They never went onto land (though some other mollusks did), and while they probably started on the road toward complex behavior at a later date than the arthropods, they eventually evolved larger brains. (Here I think of an ant colony as many organisms with many brains, not as one.) In arthropods, very complex behaviors tend to be achieved through the coordination of many individuals. Some squid are social, but with nothing like the organization of ants and honeybees. Cephalopods, with the partial exception of squid, acquired a non-social form of intelligence. The octopus, most of all, would follow a path of lone idiosyncratic complexity.

~ Nervous Evolution

Let’s look more closely now at what’s inside an octopus, and how the nervous system behind these behaviors evolved.

The history of large brains has, very roughly, the shape of a letter Y. At the branching center of the Y is the last common ancestor of vertebrates and mollusks. From here, many paths run forward, but I single out two of them, one leading to us and one to cephalopods. What features were present at that early stage, available to be carried forward down both paths? The ancestor at the center of the Y certainly had neurons. It was probably a worm-like creature with a simple nervous system, though. It may have had simple eyes. Its neurons may have been partly bunched together at its front, but there wouldn’t have been much of a brain there. From that stage the evolution of nervous systems proceeds independently in many lines, including two that led to large brains of different design.

On our lineage, the chordate design emerges, with a cord of nerves down the middle of the animal’s back and a brain at one end. This design is seen in fish, reptiles, birds, and mammals. On the other side, the cephalopods’ side, a different body plan evolved, and a different kind of nervous system. These nervous systems are more distributed