Other Minds: The Octopus and the Evolution of Intelligent Life

This is one possibility among many, though, and our imaginations, shaped by lives lived in modern bodies, underestimate the range of options. Possibilities abound. Here is one developed by the biologist Detlev Arendt and his colleagues. As they see it, nervous systems originated twice. But they don’t mean that they evolved in two kinds of animals; rather, they originated twice in the same animals, at different places in the animal’s body. Imagine a jellyfish-like animal shaped like a dome, with a mouth underneath. One nervous system evolves on the top, and tracks light, but not as a guide to action. Instead it uses light to control bodily rhythms and regulate hormones. Another nervous system evolves to control movement, initially just the movement of the mouth. And at some stage, the two systems begin to move within the body, coming into new relations with each other. Arendt sees this as one of the crucial events that took bilaterians forward in the Cambrian. A part of the body-controlling system moved up toward the top of the animal, where the light-sensitive system sat. This light-sensitive system, again, was only guiding chemical changes and cycles, not behavior. But the joining of the two nervous systems gave them a new role.

What an amazing image: in a long evolutionary process, a motion-controlling brain marches up through your head to meet there some light-sensitive organs, which become eyes.

~ The Fork

The bilaterian body plan arose before the Cambrian, in some small and unremarkable form, but it became the bodily scaffold on which a long series of increases in behavioral complexity was laid down. Early bilaterians also have another role in this book. Sometime soon after they appeared, probably still in the Ediacaran, there was a branching, one of the countless evolutionary forks that take place as the millennia pass. A population of these animals split into two. The animals who initially wandered off down the two paths might have looked like small flattened worms. They had neurons, and perhaps very simple eyes, but little of the complexity that was to come. Their scale was measured perhaps in millimeters.

After this innocuous split, the animals on each side diverged, and each became ancestor to a huge and persisting branch of the tree of life. One side led to a group that includes vertebrates, along with some surprising companions such as starfish, while the second side led to a huge range of other invertebrate animals. The point just before this split is the last point at which an evolutionary history is shared between ourselves and the big group of invertebrates that includes beetles, lobsters, slugs, ants, and moths.

Here is a diagram of this part of the tree of life. Lots of groups are omitted from the picture, both outside and inside the branches shown. The moment we’re talking about is labeled “the fork.”

On each path downstream of the fork, more branchings occurred. One side eventually sees fish appear, then dinosaurs and mammals. This is our side. On the other side, further branchings give rise to arthropods, mollusks, and others. On both sides, passing from the Ediacaran into the Cambrian and beyond, lives become entangled, the senses open, and nervous systems expand. Until, in one tiny example of this sensory and behavioral entangling, a rubber-encased mammal and a color-changing cephalopod find themselves staring at each other in the Pacific Ocean.

* (#ulink_cecea268-7b64-5a7d-b831-3fb128f67b74) If you’ve seen the word “sensorimotor” instead, please treat this as the same.

3

MISCHIEF AND CRAFT (#ulink_0847dd1a-97e2-5480-b2b5-082b2dc2198b)

Mischief and craft are plainly seen to be characteristics of this creature.

– Claudius Aelianus, third century A.D.,

writing about the octopus

In a Sponge Garden

Someone is watching you, intently, but you can’t see them. Then you notice, drawn somehow by their eyes.

You’re amid a sponge garden, the sea floor scattered with shrub-like clumps of bright orange sponge. Tangled in one of these sponges, and the gray-green seaweed around it, is an animal about the size of a cat. Its body, though, seems to be everywhere and nowhere. Much of the animal seems to have no definite shape at all. The only parts you can keep a fix on are a small head and the two eyes. As you make your way around the sponge, so too do those eyes, keeping their distance, keeping part of the sponge between the two of you. Its color matches – exactly, perfectly – the seaweed around it, except that some of its skin is folded into tiny tower-like peaks, and the tips of these peaks match – nearly as exactly – the orange of the sponge. You keep coming round its side of the sponge, and eventually it raises its head high, then rockets away under jet propulsion.

A second meeting with an octopus: this one is in a den. Shells are strewn in front, arranged with some pieces of old glass. You stop in front of its house and the two of you look at each other. This one is small, about the size of a tennis ball. You reach forward a hand and stretch out one finger, and one octopus arm slowly uncoils and comes out to touch you. The suckers grab your skin, and the hold is disconcertingly tight. Having attached the suckers, it tugs your finger, pulling you gently in. The arm is packed with sensors, hundreds of them in each of the dozens of suckers. It’s tasting your finger as it draws it in. The arm itself is alive with neurons, a nest of nervous activity. Behind the arm, large round eyes watch you the whole time. Hundreds of millions of years on from the events of chapter 2, this is one place the evolution of animals has landed.

~ Evolution of the Cephalopods

Octopuses and other cephalopods are mollusks – they belong to a large group of animals which also includes clams, oysters, and snails. Part of the story of the octopus, then, is the evolutionary history of mollusks. In the previous chapter we reached the Cambrian, the period in the history of life when a great range of animal body plans appear in the fossil record. Many of these animal groups, including mollusks, must pre-date the Cambrian, but in the Cambrian mollusks become noticeable, because of their shells.

Shells were the mollusks’ response to what looks like an abrupt change in the lives of animals: the invention of predation. There are various ways of dealing with the fact that you are suddenly surrounded by creatures who can see and would like to eat you, but one way, a molluscan specialty, is to grow a hard shell and live within or beneath it. The cephalopod line probably goes back to an early mollusk of this kind, crawling along the bottom of the sea under a hard shell peaked like a cap. This animal looked a bit like a limpet, one of those plain, cup-like shellfish that grip rocks in tide pools today. The cap grew, Pinocchio-like, over evolutionary time, slowly taking the shape of a horn. These animals were small – the “horn” was less than an inch long. Beneath the shell, as with other mollusks, a muscular “foot” anchored the animal and enabled it to crawl along the sea floor.

Then, at a stage later in the Cambrian, some of these animals rose from the sea floor and entered the water column. On dry land, no effortless move up into the air is possible for an animal; such a move requires the expense of wings or something similar. In the sea you can lift off easily, be carried, and see where you end up.

An upward-pointing shell which protects can be made into a buoyancy device, by filling it with gas. Early cephalopods seem to have done just that. Making the shell buoyant may have initially enabled easier crawling, and many of the old cephalopods might have moved by engaging in a half-crawl, half-swim on the bottom of the sea. Some, though, rose higher, and found a world of opportunity above. A small amount of gas, held within the shell, will turn a limpet into a zeppelin.

Once aloft, the “foot” is no use for crawling, so the zeppelin-cephalopods invented jet propulsion, by directing water through a tube-like siphon which could be pointed in several directions. The foot itself was freed up for grasping and manipulating objects, and part of it flowered into a cluster of tentacles. Talk of “flowering” would sound inappropriate, though, to the animals on the other end of these tentacles – the animals being grasped – as some of the tentacles sprouted dozens of sharp hooks. The opportunity the cephalopods were seizing by rising up into the water was the opportunity to feed on other animals, to become predators themselves. This they did with great evolutionary enthusiasm. Many forms appeared, with straight shells and coiled, and the largest reached sizes of eighteen feet or more. Beginning as diminutive limpets, cephalopods had become the most fearsome predators in the sea.

Figure by Ainsley Seago.

As well as zeppelins, a range of cephalopod hovercrafts and tanks probably prowled the sea floor – some of the shells from this time seem too unwieldy to carry in the open water. All these animals are now extinct, with one non-fearsome exception, the nautilus. Many of the losses occurred as part of the mass extinctions that punctuate the history of life, but it’s also likely that some predatory cephalopods were slowly outcompeted by fish, as those fish became larger and better armed. The zeppelins were challenged, and eventually vanquished, by airplanes.

The nautilus, however, made it through. No one knows why. At the start of this book I cited a Hawaiian creation myth that judges the octopus a “lone survivor” from an earlier world. The real survivor is indeed a cephalopod, but nautilus rather than octopus. Still living in the Pacific, present-day nautiluses are little changed from 200 million years ago. Living in coiled shells, they’re now scavengers. They have simple eyes and a cluster of tentacles, and they move up and down, from the deep sea to shallower water, in a rhythm that’s still being studied. They seem to stay higher in the water at night, deeper in the day.

Another shift was to come in the evolution of cephalopod bodies. Sometime before the age of the dinosaurs, it seems, some cephalopods began to give up their shells. The protective casings that had become buoyancy devices were abandoned, reduced, or internalized. This enabled more freedom of movement, but at the price of greatly increased vulnerability. It seems quite a gamble, but this was a path taken several times. The last common ancestor of “modern” cephalopods is not known, but at some stage the lineage split into two main branches, an eight-armed group including octopuses and a ten-armed group including cuttlefish and squid. These animals reduced their shells in different ways. In the cuttlefish, a shell was retained internally, and still helps the animal remain buoyant. In squid, a sword-shaped internal structure called a “pen” remains. Octopuses have lost their shell entirely. Many cephalopods began to live as soft-bodied, unprotected animals on reefs in shallow seas.

The oldest possible octopus fossil dates from 290 million years ago. I emphasize the uncertainty – it’s just one specimen, and little more than a smudge on a rock. After this there is a gap in the record, and then at around 164 million years ago there is a clearer case, a fossil that looks undeniably like an octopus, with eight arms and an octopus-like pose. The fossil record of octopuses remains skimpy because they don’t preserve well. But at some stage they radiated; around 300 species are known at present, including deep-sea as well as reef-dwelling forms. They range from less than an inch in length to the giant Pacific octopus, which weighs in at 100 pounds and spans twenty feet from arm tip to arm tip.

That’s the journey of the cephalopod body, a path from Ediacaran macaron through limpet-like shellfish to predatory hovercraft and zeppelin. The encumbrance of the external shell is then abandoned, as the shell is brought inside the body or, in an octopus, lost completely. With that step, the octopus loses almost all definite shape.

To completely forgo both skeleton and shell is an unusual evolutionary move for a creature of this size and complexity. An octopus has almost no hard parts at all – its eyes and beak are the largest – and as a result it can squeeze through a hole about the size of its eyeball and transform its body shape almost indefinitely. The evolution of cephalopods yielded, in the octopus, a body of pure possibility.

During the time I was writing an early version of this chapter, I spent a few days watching a pair of octopuses in the rocky shallows. I saw them mate once, and then spend much of the next afternoon just sitting, it seemed. The female moved off a little way, but returned to her den as the sun got low. The male had spent the day in a more exposed spot, less than a foot from her den. He was there when she came back.

I watched them, off and on, for two afternoons, and then storms came. Winds of sixty miles per hour lashed the coast, and waves rolled in from the south. The bay where the octopuses live has some protection from this onslaught, but not much. Waves swept around the entrance and turned the water into a boiling white soup. The shore was beaten by these storms for the next four days. Where do the octopuses go when the waves are pounding their rocks? It was impossible to get into the water to see. The cuttlefish have no problem. They disappear for weeks when the weather is bad. They fire up their jet propulsion and move off to some unknown deeper place. Perhaps the octopuses also move further out to sea, but more likely they climb into a crevice and hang on, for days at a stretch, recalling their ancestors who gripped rocks from inside cap-shaped shells.

Evolution of the Cephalopods: The figure is not to scale (far from it), and doesn’t represent actual descent relations between species. It presents a chronological sequence of forms seen in cephalopod evolution from over half a billion years ago to the present, with a few of the most important branchings marked along the way. I have included the controversial Kimberella as a possible early stage. The capped limpet-like shellfish is a monoplacophoran. The next animal, with a shell divided into compartments, is something like Tannuella. Opinion seems divided on whether the next in line, Plectronoceras, had lifted off the ground or was still on the sea floor, but this animal is often regarded as the first “true” cephalopod, because of various internal features. Cameroceras is the giant of the large predatory cephalopods, with conservative length estimates of up to eighteen feet. The octopus and squid are descended from unknown cephalopods that gave up their external shells and are now extinct, unlike the nautilus, which kept its shell and lived on. Figure by Eliza Jewett.

~ Puzzles of Octopus Intelligence

As the cephalopod body evolved toward its present-day forms, another transformation occurred: some of the cephalopods became smart.

“Smart” is a contentious term to use, so let’s begin cautiously. First, these animals evolved large nervous systems, including large brains. Large in what sense? A common octopus (Octopus vulgaris) has about 500 million neurons in its body. That’s a lot by almost any standard. Humans have many more – something like 100 billion – but the octopus is in the same range as various smaller mammals, close to the range of dogs, and cephalopods have much larger nervous systems than all other invertebrates.

Absolute size is important, but it is usually regarded as less informative than relative size – the size of the brain as a fraction of the size of the body. This tells us how much an animal is “investing” in its brain. This comparison is made by weight, and only counts the neurons in the brain. Octopuses also score high by this measure, roughly in the range of vertebrates, though not as high as mammals. Biologists regard all these assessments of size, though, as only a very rough guide to the brainpower an animal has. Some brains are organized differently from others, with more or fewer synapses, and those synapses can also be more or less complicated. The most startling finding in recent work on animal intelligence is how smart some birds are, especially parrots and crows. Birds have quite small brains in absolute terms, but very high-powered ones.

When we try to compare one animal’s brainpower with another’s, we also run into the fact that there is no single scale on which intelligence can be sensibly measured. Different animals are good at different things, as makes sense given the different lives they live. An analogy can be drawn with tool kits: brains are like tool kits for the control of behavior. As with human tool kits, there are some elements in common across many trades, but much diversity also. All the tool kits found in animals include some kind of perception, though different animals have very different ways of taking in information. All (or almost all) bilaterian animals have some form of memory and a means for learning, enabling past experiences to be brought to bear on the present. The tool kit sometimes includes capacities for problem solving and planning. Some tool kits are more elaborate and expensive than others, but they can be sophisticated in different ways. One animal might have better senses, while another may have more sophisticated learning. Different tool kits go with different ways of making a living.

When comparing cephalopods with mammals, the difficulties are acute. Octopuses and other cephalopods have exceptionally good eyes, and these are eyes built on the same general design as ours. Two experiments in the evolution of large nervous systems landed on similar ways of seeing. But the nervous systems beneath those eyes are organized very differently. When biologists look at a bird, a mammal, even a fish, they are able to map many parts of one animal’s brain onto another’s. Vertebrate brains all have a common architecture. When vertebrate brains are compared to octopus brains, all bets – or rather, all mappings – are off. There is no part-by-part correspondence between the parts of their brains and ours. Indeed, octopuses have not even collected the majority of their neurons inside their brains; most of the neurons are found in their arms. Given all this, the way to work out how smart octopuses are is to look at what they can do.

Here we quickly encounter puzzles. Perhaps the heart of the matter is a mismatch between the results of laboratory experiments on learning and intelligence, on one side, and a range of anecdotes and one-off reports, on the other. Mismatches like this are common in the world of animal psychology, but they are especially acute in the case of octopuses.

When tested in the lab, octopuses have done fairly well, without showing themselves to be Einsteins. They can learn to navigate simple mazes. They can use visual cues to determine which of two possible environments they have been placed in, and then take the correct route to a goal for that environment. They can learn to unscrew jars to obtain the food inside. But octopuses are slow learners in all these contexts. When you read the fine print of a “successful” experiment, progress often seems agonizingly slow. Against a background of mixed experimental results, though, there are anecdotes suggesting that a lot more is going on. What I find most intriguing is the octopus’s ability to adapt to new and unusual circumstances – confinement in a lab – and turn the apparatus around them to their own octopodean purposes.

A lot of early octopus work was done in Italy, at the Naples Zoological Station, in the middle of the twentieth century. Peter Dews was a Harvard scientist who worked mostly on the interaction between drugs and behavior. He had a general interest in learning, though, and his octopus experiment did not involve drugs at all. Dews was influenced by his Harvard colleague B. F. Skinner, whose work on “operant conditioning” – the learning of behaviors by reward and punishment – had revolutionized psychology. The idea that successful behaviors will be repeated and unsuccessful ones abandoned had been pioneered by Edward Thorndike around 1900, but Skinner developed the idea in great detail. Dews, with many others, was inspired by the way Skinner was able to make animal experiments rigorous and exact.

In 1959 Dews applied some standard experiments on learning and reinforcement to octopuses. Octopuses may be distantly related to vertebrates like us, but do they learn in similar ways? Can they learn, for example, that pulling and releasing a lever will get them a reward, and come to produce this behavior at will?

I first came across Dews’s work through a brief mention of his experiment in Roger Hanlon and John Messenger’s book Cephalopod Behaviour. Hanlon and Messenger comment that pulling and releasing a lever is surely something an octopus would never do in the sea, and they say that Dews’s experiment was not successful. I was curious about how things went, though, so I went back to the 1959 paper. The first thing I noticed is that the experiment was successful with respect to its main goals. Dews trained three octopuses, and found that all three of them did learn to operate the lever to obtain food. When they pulled the lever, a light came on and a small piece of sardine was given as a reward. Two of the octopuses, named Albert and Bertram, did this in a “reasonably consistent” manner, Dews said. The behavior of the third octopus, named Charles, was different. Though Charles did pass the test in a minimal way, his handling of the situation encapsulates much of the story with octopus behavior. Dews wrote:

1. Whereas Albert and Bertram gently operated the lever while free-floating, Charles anchored several tentacles on the side of the tank and others around the lever and applied great force. The lever was bent a number of times, and on the 11th day was broken, leading to a premature termination of the experiment.

2. The light, suspended a little above the level of the water, was not the subject of much “attention” by Albert or Bertram; but Charles repeatedly encircled the lamp with tentacles and applied considerable force, tending to carry the light into the tank. This behavior is obviously incompatible with lever-pulling behavior.

3. Charles had a high tendency to direct jets of water out of the tank; specifically, they were in the direction of the experimenter. The animal spent much time with eyes above the surface of the water, directing a jet of water at any individual who approached the tank. This behavior interfered materially with the smooth conduct of the experiments, and is, again, clearly incompatible with lever-pulling.

Dews comments dryly, “The variables responsible for the maintenance and strengthening of the lamp-pulling and squirting behavior in this animal were not apparent.” The language Dews is using here – the language of “variables responsible,” and so on – shows that he is thinking (or writing, at least) in line with the assumptions of mid-twentieth-century animal behavior experiments. He assumes that if Charles is squirting experimenters and absconding with the apparatus, this must be because something in Charles’s history has reinforced this behavior. Animals of a given species will start out the same, on this view, and if they diverge in behavior this must be because of rewarding (or unrewarding) experiences. That is the framework Dews is working within. However, one message of octopus experiments is that there is a great deal of individual variability. Charles, most likely, was not an octopus who started with the same behavioral routines as the others and was reinforced for squirting experimenters, but an octopus with a particularly feisty temperament.

This 1959 paper was one of the first encounters between a tightly controlled style of scientific work on animal behavior and the idiosyncrasies of the octopus. A great deal of work on animals has been done under the assumption that all animals of a given species (and perhaps of a given sex) will be very similar until they encounter different rewards, and will peck or run or pull a lever all day in order to get the same little morsels of food. Dews, like many others, wanted to work this way because he was determined to use what he called “objective, quantitative methods of study.” I am all for those, too. But octopuses, far more than rats and pigeons, have their own ideas: “mischief and craft,” as Aelianus, in this chapter’s epigraph, had it.

The most famous octopus anecdotes are tales of escape and thievery, in which octopuses in aquariums raid neighboring tanks at night for food. Those stories, despite their charm, are not especially indicative of high intelligence. Neighboring tanks are not so different from tide pools, even though the entrance and exit take more effort. Here is a behavior I find more intriguing. Octopuses in at least two aquariums have learned to turn off the lights by squirting jets of water at the bulbs when no one is watching, and short-circuiting the power supply. At the University of Otago in New Zealand, this became so expensive that the octopus had to be released back to the wild. A lab in Germany had the same problem. This seems very smart indeed. However, one can also sketch an explanation which may partially deflate the story. Octopuses don’t like bright lights, and they squirt jets of water at all sorts of things that annoy them (as Peter Dews discovered). So squirting water at lights might not be something that requires much explanation. Also, octopuses are more likely to roam far enough away from their dens to squirt at this particular target when no humans are around. On the other hand, both the stories of this kind that I’ve seen give the impression that the octopus learned very quickly how well this behavior works – that it’s worth getting into position and aiming right at the light, to turn it out. It should be possible to set up an experiment that tests some of the various possible explanations for the behavior.