Are We Smart Enough to Know How Smart Animals Are

by Frans de Waal

  Like the scientist who gave us the mirror-anesthesia hypothesis, the one who wrote an entire article debunking the Koshima discovery was a nonprimatologist who, moreover, never bothered to set foot on Koshima or check his ideas with the fieldworkers who had camped for decades on the island. Again, I can’t help but wonder about the mismatch between conviction and expertise. Perhaps this attitude is a leftover of the mistaken belief that if you know enough about rats and pigeons, you know everything there is to know about animal cognition. It prompts me to propose the following know-thy-animal rule: Anyone who wishes to stress an alternative claim about an animal’s cognitive capacities either needs to familiarize him- or herself with the species in question or make a genuine effort to back his or her counterclaim with data. Thus, while I admire Pfungst’s work with Clever Hans and its eye-opening conclusions, I have great trouble with armchair speculations devoid of any attempt to check their validity. Given how seriously the field of evolutionary cognition takes variation between species, it is time to respect the special expertise of those who have devoted a lifetime getting to know one of them.

  The Thaw

  One morning at Burgers’ Zoo, we showed the chimpanzees a crate full of grapefruits. The colony was in the building where it spends the night, which adjoins a large island, where it spends the day. The apes seemed interested enough watching us carry the crate through a door onto the island. When we returned to the building with an empty crate, however, pandemonium broke out. As soon as they saw that the fruits were gone, twenty-five apes burst out hooting and hollering in a most festive mood, slapping one another’s backs. They must have inferred that grapefruits cannot vanish, hence must have remained on the island onto which the colony would soon be released. This kind of reasoning does not fall into any simple category of trial-and-error learning, especially since it was the first time we followed this procedure. The grapefruit experiment was a one-time event to study responses to cached food.

  One of the first tests of inferential reasoning was conducted by American psychologists David and Ann Premack, who presented Sadie, a chimpanzee, with two boxes. They placed an apple in one and a banana in the other. After a few minutes of distraction, Sadie saw one of the experimenters munching on either an apple or a banana. This experimenter then left, and Sadie was released to inspect the boxes. She faced an interesting dilemma, since she had not seen how the experimenter had gotten his fruit. Invariably, Sadie would go to the box with the fruit that the experimenter had not eaten. The Premacks ruled out gradual learning, because Sadie made this choice on the very first trial as well as all subsequent ones. She seemed to have reached two conclusions. First, that the eating experimenter had removed his fruit from one of the two boxes, even if she had not actually seen him do so. And second, that this meant that the other box must still hold the other fruit. The Premacks note that most animals don’t make any such assumptions: they just see an experimenter consume fruit, that’s all. Chimpanzees, in contrast, try to figure out the order of events, looking for logic, filling in the blanks.35

  Years later the Spanish primatologist Josep Call presented apes with two covered cups. They had learned that only one would be baited with grapes. If Call removed the tops and let them look inside the cups, the apes chose the one with grapes. Next, he kept the cups covered and shook first one, then the other. Only the cup with grapes made noise, which was the one they preferred. This was not too surprising. But making things harder, Call would sometimes shake only the empty cup, which made no noise. In this case, the apes would still pick the other one, thus operating on the basis of exclusion. From the absence of sound, they guessed where the grapes must be. Perhaps we are not impressed by this either, as we take such inferences for granted, but it is not all that obvious. Dogs, for example, flunk this task. Apes are special in that they seek logical connections based on how they believe the world works.36

  Here it gets interesting, because aren’t we supposed to go for the simplest possible explanation? If large-brained animals, such as apes, try to get at the logic behind events, could this be the simplest level at which they operate?37 It reminds me of Morgan’s provision to his canon, according to which we are allowed more complex premises in the case of more intelligent species. We most certainly apply this rule to ourselves. We always try to figure things out, applying our reasoning powers to everything around us. We go so far as to invent causes if we can’t find any, leading to weird superstitions and supernatural beliefs, such as sports fans wearing the same T-shirt over and over for luck, and disasters being blamed on the hand of God. We are so logic-driven that we can’t stand the absence of it.

  Evidently, the word simple is not as simple as it sounds. It means different things in relation to different species, which complicates the eternal battle between skeptics and cognitivists. In addition, we often get tangled up in semantics that aren’t worth the heat they generate. One scientist will argue that monkeys understand the danger posed by leopards, whereas another will say that monkeys have merely learned from experience that leopards sometimes kill members of their species. Both statements are really not that different, even though the first uses the language of understanding, and the second of learning. With the decline of behaviorism, debates on these issues have fortunately grown less fiery. By attributing all behavior under the sun to a single learning mechanism, behaviorism set up its own downfall. Its dogmatic overreach made it more like a religion than a scientific approach. Ethologists loved to slam it, saying that instead of domesticating white rats in order to make them suitable to a particular testing paradigm, behaviorists should have done the opposite. They should have invented paradigms that fit “real” animals.

  The counterpunch came in 1953, when Daniel Lehrman, an American comparative psychologist, sharply attacked ethology.38 Lehrman objected to simplistic definitions of innate, saying that even species-typical behavior develops from a history of interaction with the environment. Since nothing is purely inborn, the term instinct is in fact misleading and should be avoided. Ethologists were stung and dismayed by his unexpected critique, but once they got over their “adrenaline attack” (Tinbergen’s words), they discovered that Lehrman hardly fit the behaviorist bogeyman stereotype. He was an enthusiastic bird-watcher, for example, who knew his animals. This impressed the ethologists, and Baerends recalled that while meeting the “enemy” in person, they managed to resolve most misunderstandings, found common ground, and became “very good friends.”39 Once Tinbergen became acquainted with Danny, as they now knew Lehrman, he went so far as to call him more of a zoologist than a psychologist, which the latter took as a compliment.40

  Their bonding over birds went way beyond the way John F. Kennedy and Nikita Khrushchev bonded over Pushinka, a little dog that the Soviet leader sent to the White House. Despite this gesture, the Cold War continued unabated. In contrast, Lehrman’s harsh critique and the subsequent meeting of minds between comparative psychologists and ethologists set in motion a process of mutual respect and understanding. Tinbergen, in particular, acknowledged Lehrman’s influence on his later thinking. Apparently, they had needed a big spat to start a rapprochement, which was hastened by ongoing criticism within each camp of its own tenets. Within ethology, the younger generation grumbled about the rigid Lorenzian drive and instinct concepts, whereas comparative psychology had an even longer tradition of challenges to its own dominant paradigm.41 Cognitive approaches had been tried off and on, even as early as the 1930s.42 But ironically, the biggest blow to behaviorism came from within. It all started with a simple learning experiment conducted on rats.

  American psychologist Frank Beach lamented the narrow focus of behavioral science on the albino rat. His incisive critique featured a cartoon in which a Pied Piper rat is followed by a happy mass of white-coated experimental psychologists. Carrying their favorite tools—mazes and Skinner boxes—they are being led into a deep river. After S. J. Tatz in Beach (1950).

  Anyone who has tried to punish a dog or cat for problema
tic behavior knows that it is best to do so quickly, while the offense is still visible or at least fresh on the animal’s mind. If you wait too long, your pet doesn’t connect your scolding with the stolen meat or the droppings behind the couch. Since short intervals between behavior and consequence have always been regarded as essential, no one was prepared when, in 1955, the American psychologist John Garcia claimed he had found a case that broke all the rules: rats learn to refuse poisoned foods after just a single bad experience even if the resulting nausea takes hours to set in.43 Moreover, the negative outcome had to be nausea—electric shock didn’t have the same effect. Since toxic nutrition works slowly and makes you sick, none of this was particularly surprising from a biological standpoint. Avoiding bad food seems a highly adaptive mechanism. For standard learning theory, however, these findings came like a bolt out of the blue, due to the assumption that time intervals should be short while the kind of punishment is irrelevant. The findings were in fact devastating, and Garcia’s conclusions were so unwelcome that he had trouble getting them published. One imaginative reviewer contended that his data were less likely than finding bird shit in a cuckoo clock! The Garcia Effect is now well established, though. In our own lives, we remember food that has poisoned us so well that we gag at the mere thought of it or never set foot in a certain restaurant again.

  For readers who wonder about the fierce resistance to Garcia’s discovery despite the fact that most of us have firsthand experience with the power of nausea, it is good to realize that human behavior was (and still is) often seen as the product of reflection, such as an analysis of cause and effect, whereas animal behavior was supposedly free of such processes. Scientists were not ready to equate the two. Human reflection is chronically overrated, though, and we now suspect that our own reaction to food poisoning is in fact similar to that of rats. Garcia’s findings forced comparative psychology to admit that evolution pushes cognition around, adapting it to the organism’s needs. This became known as biologically prepared learning: each organism is driven to learn those things it needs to know in order to survive.. This realization obviously helped the rapprochement with ethology. Moreover, the geographic distance between both schools fell away. Once comparative psychology took hold in Europe—which is how I briefly ended up in a behaviorist lab—and ethology was being taught in North American zoology departments, students on both sides of the Atlantic could absorb the entire range of views and begin to integrate them. The synthesis between the two approaches did not take place just at international meetings or in the literature, therefore, but also in the classrooms.

  We entered a period of crossover scholars, which I’ll illustrate with just two examples. The first is the American psychologist Sara Shettleworth, who for most of her career taught at the University of Toronto, and who has been influential through her textbooks on animal cognition. She started out in the behaviorist corner but ended up advocating a biological approach to cognition that is sensitive to the ecological needs of each species. She remains as cautious in her interpretations of cognition as one would expect from someone of her background, yet her work gained a clear ethological flavor, which she attributes to certain professors when she was a student as well as involvement with her husband’s fieldwork on sea turtles. In an interview about her career, Shettleworth explicitly mentions Garcia’s work as a turning point that opened the eyes of her field to the evolutionary forces shaping learning and cognition.44

  At the other end of the scale is one of my heroes, Hans Kummer, a Swiss primatologist and ethologist. As a student, I avidly devoured every paper he wrote, mostly his field studies on hamadryas baboons in Ethiopia. Kummer did not just observe social behavior and relate it to ecology; he always puzzled about the cognition behind it and conducted field experiments on (temporarily) captured baboons. He later moved to captive work on long-tailed macaques at the University of Zürich. Kummer felt that the only way to test cognitive theories was by means of controlled experiments. Observation alone was not going to cut it, so primatologists should become more like comparative psychologists if they ever wished to unravel the puzzle of cognition.45

  I went through a similar transition from observation to experimentation and was greatly inspired by Kummer’s macaque lab when I set up my own lab for capuchin monkeys. The trick is to house the animals socially, hence build large indoor and outdoor areas, where the monkeys can spend most of the day playing, grooming, fighting, catching insects, and so on. We trained them to enter a test chamber where they could work on a touchscreen or a social task before we’d return them to the group. This arrangement had two advantages over traditional labs, which keep monkeys, rather like Skinner’s pigeons, in single cages. First of all, there is the quality of life issue. It is my personal feeling that if we are going to keep highly social animals in captivity, the very least we can do for them is permit them a group life. This is the best and most ethical way to enrich their lives and make them thrive.

  Second, it makes no sense to test monkeys on social skills without giving them a chance to express these skills in daily life. They need to be completely familiar with one another for us to investigate how they share food, cooperate, or judge one another’s situation. Kummer understood all this, having started out, like myself, as a primate watcher. In my opinion, anyone who intends to conduct experiments on animal cognition should first spend a couple thousand hours observing the spontaneous behavior of the species in question. Otherwise we get experiments uninformed by natural behavior, which is precisely the approach we should be leaving behind.

  Today’s evolutionary cognition is a blend of both schools, taking the best parts of each. It applies the controlled experimental methodology developed by comparative psychology combined with the blind testing that worked so well with Clever Hans, while adopting the rich evolutionary framework and observation techniques of ethology. For many young scientists, it is now immaterial whether we call them comparative psychologists or ethologists, since they integrate concepts and techniques from both. On top of this comes a third major influence, at least for work in the field. The impact of Japanese primatology is not always recognized in the West—which is why I have called it a “silent invasion”—but we routinely name individual animals and track their social careers across multiple generations. This allows us to understand the kinship ties and friendships at the core of group life. Begun by Imanishi right after World War II, this method has become standard in work on long-lived mammals, from dolphins to elephants and primates.

  Unbelievably, there was a time when Western professors warned their students away from the Japanese school because naming animals was considered too humanizing. There was of course also the language barrier, which made it hard for Japanese scientists to get heard. Junichiro Itani, Imanishi’s foremost student, was met with disbelief when he toured American universities in 1958 because no one believed that he and his colleagues were able to tell a hundred or more monkeys apart. Monkeys look so much alike that Itani obviously was making things up. He once told me that he was mocked to his face and had no one to defend him except the great American primatological pioneer Ray Carpenter, who did see the value of this approach.46 Nowadays, of course, we know that recognizing a large number of monkeys is possible, and we all do it. Not unlike Lorenz’s emphasis on knowing the whole animal, Imanishi urged us to empathize with the species under study. We need to get under its skin, he said, or as we would nowadays put it, try to enter its Umwelt. This old theme in the study of animal behavior is quite different from the misguided notion of critical distance, which has given us excessive worries about anthropomorphism.

  The eventual international embrace of the Japanese approach illustrates something else that we learned from the tale of two schools—ethology and comparative psychology—which is that the initial animosity between divergent approaches can be overcome if we realize that each has something to offer that the other lacks. We may weave them together into a new whole that is stronger than the sum of its parts. Th
e fusing of complementary strands is what makes evolutionary cognition the promising approach it is today. But sadly it took a century of misunderstandings and colliding egos before we got there.

  Beewolves

  Tinbergen was in tears when I last saw him. It was 1973, the year in which he, Lorenz, and von Frisch were honored with Nobel prizes. He had come to Amsterdam to receive a different medal and give a lecture. Speaking in Dutch, his voice quavering with emotion, he asked what we had done to his country. The magnificent little spot in the dunes where he had studied gulls and terns was no more. Decades earlier, while emigrating aboard a boat to England, he had pointed at the site—the eternal self-rolled cigarette in his hand—predicting that “it will all go, irrevocably.” Years later the place was swallowed up by the expansion of Rotterdam harbor, then the busiest in the world.47