Are We Smart Enough to Know How Smart Animals Are

by Frans de Waal

  Neuroscience may one day resolve how planning takes place. The first hints are coming from the hippocampus, which has long been known to be vital both for memory and for future orientation. The devastating effects of Alzheimer’s typically begin with degeneration of this part of the brain. As with all major brain areas, however, the human hippocampus is far from unique. Rats have a similar structure, which has been intensely studied. After a maze task, these rodents keep replaying their experiences in this brain region, either during sleep or sitting still while awake. Using brain waves to detect what kind of maze paths the rats are rehearsing in their heads, scientists found that more is going on than a consolidation of past experiences. The hippocampus seems also engaged in the exploration of maze paths that the rats have not (yet) taken. Since humans, too, show hippocampal activity while imagining the future, it has been suggested that rats and humans relate to the past, present, and future in homologous ways.20 This realization, as well as the accumulated primate and bird evidence for future orientation, has swayed the opinion of several skeptics, who used to think that only humans show mental time travel. We are moving ever closer to Darwin’s continuity stance, according to which the human-animal difference is one of degree, not kind.21

  Animal Willpower

  A French politician accused of sexual assault was said to have acted like a “randy chimpanzee.”22 How insulting—to the ape! As soon as humans let their impulses run free, we rush to compare them with animals. But as the above descriptions show, rather than give in to sexual desires, chimps have sufficient emotional control to either refrain from them or to arrange privacy first. It all boils down to the social hierarchy, which is one giant behavioral regulator. If everyone were to act the way they wanted, any hierarchy would fall apart. It is built on restraint. Since social ladders are present in species from fish and frogs to baboons and chickens, self-control is an age-old feature of animal societies.

  A famous anecdote comes from the early days in Gombe Stream, when chimpanzees still received bananas from humans. The Dutch primatologist Frans Plooij observed an adult male approach the feeding box, which humans could unlock from a distance. Each individual chimpanzee had been put on a strict quota. The unlocking mechanism made a distinctive click, which announced the availability of fruits. But alas, at the very moment that this male heard the click and got lucky, a dominant male appeared on the scene. What to do now? The first male acted as if nothing were the matter. Rather than open the box—and lose his bananas—he sat down at a distance. No dummy either, the dominant male strolled away from the scene. But as soon as he was out of sight, he peeked around a tree trunk to see what the first male was up to. He thus noticed that the other opened the box and quickly relieved him of his prize.

  One reconstruction of this sequence is that the dominant male got suspicious since he felt that the other was acting odd. Hence his decision to keep an eye on him. Some have even suggested multiple layers of intentionality: first, that the dominant male suspected that the first male was trying to give the impression that the lid was still locked; second, that the dominant let the other think that he hadn’t noticed.23 If true, this would be a deceptive mind game more complex than most experts are willing to give apes credit for. For me, however, the interesting part is the patience and restraint both males showed. They suppressed the impulse to open the box in each other’s presence, even though it contained a highly desirable food that was rarely available.

  It is easy to see inhibitions at work in our pets, such as a cat who spots a chipmunk. Instead of going after the little rodent right away, she makes a wide detour, with her body sleekly pressed against the ground, to arrive at a hiding spot from which she can pounce on her unsuspecting prey. Or take the big dog who lets puppies jump all over him, bite his tail, and disturb his sleep without a single growl of protest. While restraint is apparent to anyone in daily contact with animals, Western thought hardly recognizes the ability. Traditionally, animals are depicted as slaves of their emotions. It all goes back to the dichotomy of animals as “wild” and humans as “civilized.” Being wild implies being undisciplined, crazy even, without holding back. Being civilized, in contrast, refers to exercising the well-mannered restraint that humans are capable of under favorable circumstances. This dichotomy lurks behind almost every debate about what makes us human, so much so that whenever humans behave badly, we call them “animals.”

  Desmond Morris once told me an amusing story to drive this point home. At the time Desmond was working at the London Zoo, which still held tea parties in the ape house with the public looking on. Gathered on chairs around a table, the apes had been trained to use bowls, spoons, cups, and a teapot. Naturally, this equipment posed no problem for these tool-using animals. Unfortunately, over time the apes became too polished and their performance too perfect for the English public, for whom high tea constitutes the peak of civilization. When the public tea parties began to threaten the human ego, something had to be done. The apes were retrained to spill the tea, throw food around, drink from the teapot’s spout, and pop the cups into the bowl as soon as the keeper turned his back. The public loved it! The apes were wild and naughty, as they were supposed to be.24

  In line with this misconception, the American philosopher Philip Kitcher labeled chimpanzees “wantons,” creatures vulnerable to whichever impulse hits them. The maliciousness and lasciviousness usually associated with this term was not part of his definition, which focused on a disregard of behavioral consequences. Kitcher went on to speculate that somewhere during our evolution we overcame this wantonness, which is what made us human. This process started with “awareness that certain forms of projected behavior might have troublesome results.”25 This awareness is key indeed but is obviously present in lots of animals, otherwise they’d run into all sorts of problems. Why do migrating wildebeest hesitate so long before jumping into the river they seek to cross? Why do juvenile monkeys wait until their playmate’s mother has moved out of sight before starting a fight? Why does your cat jump onto the kitchen counter only when you aren’t looking? Awareness of troublesome results is all around us.

  Behavioral inhibitions have rich ramifications, which extend to the origins of human morality and free will. Without impulse control, what would be the point of distinguishing right from wrong? The philosopher Harry Frankfurt defines a “person” as someone who does not just follow his desires but is aware of them and capable of wishing them to be different. As soon as an individual considers the “desirability of his desires,” he becomes a person with freedom of will.26 But while Frankfurt believes that animals and young children don’t monitor or judge their own desires, science is increasingly testing out this very capacity. Experiments on delayed gratification present apes and children with a temptation that they need to actively resist for the sake of future gain. Emotional control and future orientation are key, with free will not far behind.

  Most of us have seen the hilarious videos of children sitting alone behind a table desperately trying not to eat a marshmallow—secretly licking it, taking tiny bites from it, or looking the other way so as to avoid temptation. It is one of the most explicit tests of impulse control. The children have been promised a second marshmallow if they leave the first one alone while the experimenter is away. All they have to do is postpone gratification. But in order to do so, they have to go against the general rule that an immediate reward is more appealing than a delayed one. This is why we find it hard to save money for a rainy day, and why smokers find a cigarette more appealing than the prospect of lasting health. The marshmallow test measures how much weight children assign to the future. Children vary greatly on how well they do on the test, and their success predicts how they will fare later in life. Impulse control and future orientation are a major part of success in society.

  Many animals have trouble with a similar task and don’t hesitate to eat food right away, probably because in their natural habitat they might otherwise lose it. For other species, delay of grat
ification is very modest, such as in a recent experiment with capuchin monkeys. The monkeys saw a large rotating plate, like a lazy Susan, featuring one piece of carrot and one piece of banana. Capuchins favor the second food. They first saw one and a little later the second item move by, while sitting behind a window through which they were allowed to reach only once. The majority of monkeys ignored the carrot, letting it pass right in front of them, to hold out for the better reward. Even though the delay between the two was a mere fifteen seconds, they showed enough restraint to consume considerably more banana than carrot.27 Some species, however, show dramatic control that is more in line with that of our own. For example, a chimpanzee patiently stares at a container into which falls a candy every thirty seconds. He knows he can disconnect the container at any moment to swallow its contents but also that this will stop the candy flow. The longer he waits, the more candies he will gather. Apes do about as well as children on this task, delaying gratification for up to eighteen minutes.28

  Similar tests have been conducted with large-brained birds. We may not consider birds to need self-restraint, but think again. Many birds pick up food for their young that they could easily swallow themselves. In some species, males feed their mates during courtship while going hungry themselves. Birds that cache food inhibit immediate gratification for the sake of future need. There are many reasons to expect self-restraint in birds, therefore. The test results bear this out. Crows and ravens were given beans—a food they’d normally eat right away—after being taught that they could trade the beans later for a piece of sausage, which they liked better. The birds hung on to the beans for up to ten minutes.29 When Griffin, the African gray of Irene Pepperberg, was tested on a similar paradigm, he managed even longer waiting times. The parrot had the advantage that he understood the instruction “Wait!” So while Griffin was sitting on his perch, a cup with a less preferred food, such as cereal, was put in front of him, and he was asked to wait. Griffin knew that if he waited long enough, he might get cashew nuts or even candies. If the cereal was still in the cup after a random time interval—anywhere from ten seconds to fifteen minutes—Griffin would receive the better food. He was successful 90 percent of the time, including on the longest delays.30

  Most fascinating are the many ways in which children and animals cope with temptation. They are not passively sitting and staring at the object of desire but try to occupy themselves by creating distractions. Children avoid looking at the marshmallow, sometimes covering their eyes with their hands or putting their head into their arms. They talk to themselves, they sing, they invent games using their hands and feet, and they even fall asleep so as not to have to endure the terribly long wait.31 The behavior of apes is not so different, and one study found that if given toys, apes are able to hold out longer. Toys help them take their attention off the candy machine. Or take Griffin, who about one-third through one of his longest waits threw the cup with cereal across the room. This way he didn’t have to look at it. On other occasions, he moved the cup just out of reach, talked to himself, preened himself, shook his feathers, yawned extensively, or fell asleep (or at least closed his eyes). He also sometimes licked the treat without eating it, or shouted “Wanna nut!”

  Some of these behaviors don’t fit the situation at hand and fall under what ethologists call displacement activities, which occur when a drive is thwarted. This happens when two conflicting drives, such as fight and flight, arise at the same time. Since they cannot both be expressed, irrelevant behavior takes the pressure off. A fish spreading its fins to intimidate a rival may all of a sudden swim to the bottom to dig into the sand, or a rooster may interrupt a fight only to start pecking at some imaginary grains. In humans, a typical displacement activity is to scratch one’s head when asked a tough question. Scratching is also common in other primates during cognitive tests, especially challenging ones.32 Displacement activity occurs when motivational energy seeks an outlet and “sparks over” into extraneous behavior. The discoverer of this mechanism, the Dutch ethologist Adriaan Kortlandt, is still honored at the zoo in Amsterdam where he used to watch a colony of free-ranging cormorants. The wooden bench on which he spent hours following his birds is known as the “displacement bench.” I recently sat on it and obviously couldn’t resist yawning, fiddling, and scratching myself.

  But this is not the whole explanation of how animals cope with delayed gratification, and why they preen themselves or yawn. There are cognitive interpretations, too. Long ago the father of American psychology, William James, proposed “will” and “ego strength” as the basis of self-control. This is how the behavior of children usually is interpreted, as in the following description of the marshmallow test: “The subject can wait most stoically if he expects that he really will get the deferred larger outcome in the waiting paradigm, and wants it very much, but shifts his attention elsewhere and occupies himself internally with cognitive distractions.”33 The emphasis here is on a deliberate, conscious strategy. The child knows what the future holds and wills his mind off the temptation in front of him. Given how similarly children and some animals behave under the same conditions, it is logical to favor the same explanation. Demonstrating impressive willpower, animals too may be aware of their own desires and try to curb them.

  To explore this further, I visited Michael Beran, an American colleague at Georgia State University. Mike works at a lab in a large stretch of forest in Decatur, in the middle of the Atlanta area, with roomy accommodations for chimpanzees and monkeys. It is known as the Language Research Center, so named since Kanzi, the symbol-trained bonobo, was its first resident. At the same location, Charlie Menzel conducts tests of spatial memory on apes and Sarah Brosnan studies economic decision making by capuchins. The Atlanta area may well have the world’s highest concentration of primatologists, since they are also found at Zoo Atlanta, in nearby Athens, Georgia, and of course at the Yerkes Primate Center, which historically sparked all this interest. As a result, we have expertise on a wide range of topics.

  I asked Mike, who has worked extensively on self-control,34 why articles in this field so often start out with the connection to consciousness, then quickly move to actual behavior without ever returning to the issue of consciousness. Are the authors teasing us? The reason, Mike felt, is that the link with consciousness is rather speculative. Strictly speaking, the fact that animals achieve a better outcome by waiting doesn’t prove that they realize what will happen in the time ahead. On the other hand, their response doesn’t depend on gradual learning, since they generally show it right away. This is why Mike regards self-control decisions as being future-oriented and cognitive. We may not have proof beyond all doubt, but the assumption is that the apes make these decisions based on the anticipation of a better outcome: “To argue that the behavior of apes is entirely under external stimulus control is silly to me.”

  Another argument for a cognitive interpretation is their behavior during long waits, which last up to twenty minutes, while candies drop at regular intervals into a bowl. The waiting apes like to play with things during this time, which suggests recognition that they need self-control. Mike described some of the weird things they do to keep themselves busy. Sherman (an adult male chimpanzee) would pick up a candy from the bowl, inspect it, then put it back. Or Panzee would disconnect the tube through which the candies roll in. She’d look at it and shake it before putting it back onto the dispenser. Given toys, they would use them as a distraction to make the wait easier. Such behavior hints at anticipation and strategizing, both of which suggest conscious awareness.

  Mike’s interest in this topic was triggered by a legendary experiment on reversal pointing by the American primatologist Sarah Boysen with Sheba, a chimpanzee. Sheba was asked to choose between two cups with different amounts of candy. The catch, however, was that the cup that she’d point at would go to another chimp, leaving her with the alternative cup. Obviously, the smart strategy would be for Sheba to reverse her pointing, indicating the cup with the smaller
number of candies. Yet unable to overcome her desire for the fuller cup, she never learned to do so. When the candies were replaced by numbers, however, things changed. Sheba had learned the numbers 1 through 9, knowing the amounts of food associated with them. Presented with two different numbers, she never hesitated to point at the smaller one, showing that she understood how the reversals worked.35

  Mike was impressed by Sally’s research showing that chimps can’t get the reversal right with actual candies. This was obviously a matter of self-control. When he tried the same test on his own chimps, they didn’t pass either. Sally’s idea to replace the candies with numbers was brilliant. Whether it is the symbolizing or just the removal of the hedonic property, chimps trained with numerals were really good at it. When I asked if the same had ever been tried with children, Mike’s answer reflected the deep concern of students of animal cognition with fair comparisons: “It may have been tried, I don’t recall, but they probably explained it to the kids, and I would prefer that nothing is explained. We can’t explain it to the apes either.”

  Know What You Know

  The claim that only humans can mentally hop onto the time train, leaving all other species stranded on the platform, is tied to the fact that we consciously access past and future. Anything related to consciousness has been hard to accept in other species. But this reluctance is problematic: not because we know so much more about consciousness, but because we have growing evidence in other species for episodic memory, future planning, and delayed gratification. Either we abandon the idea that these capacities require consciousness, or we accept the possibility that animals may have it, too.

  The fourth spoke on this wheel is metacognition, which is literally cognition about cognition, also known as “thinking about thinking.” When the contestants in a game show are allowed to pick their topic, they obviously name the one they are most familiar with. This is metacognition in action, because it means they know what they know. In the same way, I may answer a question by saying “Wait, it’s on the tip of my tongue!” In other words, I suspect that I know the answer, even though it’s taking me time to recall it. A student raising her hand in class in reaction to a question is also relying on metacognition, because she only does so if she thinks she knows the solution. Metacognition rests on an executive function in the brain that allows one to monitor one’s own memory. Again, we associate these processes with consciousness, which is exactly why metacognition, too, was deemed unique to our species.