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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.

      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,

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