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What is time? Leave now for dogs and apes! Man has forever!

—Robert Browning (1896)1

Judging the gap between two trees, a monkey relies on its memory of past jumps to calculate the next one. Is there a landing spot on the other side? Is it within jumping distance? Can the branch handle its impact? These life-and-death decisions take a great deal of experience to make and show how past and future intertwine in a species’s behavior. The past provides the required practice, whereas the future is where the next move will take place. Long-range future orientation is also common, such as when during a drought the matriarch of an elephant herd remembers a drinking hole miles away that no one else knows about. The herd sets out on a long trek, taking days to reach precious water. While the matriarch operates on the basis of knowledge, the rest of the herd operates on the basis of trust. Whether it is a matter of seconds or days, animal behavior is not only goal- but also future-oriented.

So it is curious to me that animals are often thought to be stuck in the present. The present is ephemeral. One moment it is here, the next it is gone. Whether you are a thrush picking up a worm for your chicks in a distant nest or a dog setting out in the morning to patrol your territory and dribble urine at strategic locations, animals have jobs to do, which imply the future. True, most of the time it is the near future, and it remains unclear how aware they are of it. Yet their behavior would make no sense if they lived entirely in the present.

We ourselves consciously reflect on the past and the future, so it was perhaps unavoidable that whether animals do or don’t would become a battleground. Isn’t consciousness what sets humans apart? Some claim that we are the only ones to actively recall the past and imagine the future, but others have been busy gathering evidence to the contrary. Since no one can prove conscious reflection without verbal reports, the debate skirts subjective experience as something that—at least for now—we can’t put our finger on. There has been genuine progress, though, in the exploration of how animals relate to the time dimension. Of all areas of evolutionary cognition, this one is perhaps the most esoteric and the hardest to get a handle on. The terminology shifts regularly, and debates are fierce. For this reason, I have visited two experts to ask them where we currently stand, which opinions will be presented at the end of this chapter.

In Search of Lost Time

Perhaps the controversy started earlier than we think, because in the 1920s an American psychologist, Edward Tolman, bravely and controversially asserted that animals are capable of more than the mindless linking between stimulus and response. He rejected the idea of them as purely incentive-driven. He dared use the term cognitive (he was famous for his studies of cognitive maps in maze-learning rats) and called animals “purposive,” guided by goals and expectations, both of which reference the future.

While Tolman—in a bow to the suffocating grip of the era’s classical behaviorism—shied away from the stronger term purposeful, his student Otto Tinklepaugh designed an experiment in which a macaque watched either a lettuce leaf or a banana being placed under a cup. As soon as the monkey was given access, she ran to the baited cup. If she found the food that she had seen being hidden, everything proceeded smoothly. But if the experimenter had replaced the banana with lettuce, the monkey only stared at the reward. She’d frantically look around, inspecting the location over and over, while angrily shrieking at the sneaky experimenter. Only after a long delay would she settle for the disappointing vegetable. From a behaviorist perspective, her attitude was bizarre since animals are supposed to merely connect behavior with rewards, any rewards. The nature of the reward shouldn’t matter. Tinklepaugh, however, demonstrated that there is more going on. Guided by a mental representation of what she had seen being hidden, the monkey had developed an expectation, the violation of which deeply upset her.2

Instead of merely preferring one behavior over another, or one cup over another, the monkey recalled a specific event. It was as if she were saying “Hey, I swear I saw them put a banana under that cup!” Such precise recall of events is known as episodic memory, which was long thought to require language, hence to be uniquely human. Animals were thought to be good at learning the general consequences of behavior without retaining any specifics. This position has become shaky, though. Let me give an example that is a bit more striking since it involves a much longer time frame than the monkey experiment.

We once applied a Menzel-type test to Socko, when he was still an adolescent chimpanzee. Through a small window, Socko watched my assistant hide an apple in a large tractor tire in the outdoor enclosure, while the rest of the colony was kept behind closed doors. Then we released the colony, holding Socko back until last. The first thing he did after coming out the door was to climb onto the tire and peek into it, checking on the apple. He left it alone, though, and nonchalantly walked away from the scene. He waited for more than twenty minutes, until everyone was otherwise occupied, and then went to collect the fruit. This was clever, since he might otherwise have lost his prize.

The truly interesting twist came years later, however, when we repeated this experiment. Socko had been tested only once, and we showed the video to a visiting camera crew. But as is typical, the crew trusted its own filming better and insisted on redoing the whole test. By this time Socko was the alpha male and hence could not be used anymore. Being of high rank, he would have had no reason to conceal what he knew about hidden food. So instead we selected a low-ranking female named Natasha and did everything nearly same. We locked up all the chimps and let Natasha watch through the window while we hid an apple. This time we dug a hole in the ground, put the apple into it, and covered it with sand and leaves. We did this so well that afterward we barely knew where we’d put the fruit.

After the others were released, Natasha finally entered the enclosure. We waited anxiously, following her with several cameras. She showed a pattern similar to Socko’s and moreover displayed a far better sense of location than we did. She passed slowly over to the precise hiding spot, then returned ten minutes later to confidently dig up the fruit. While she did so, Socko stared at her with apparent surprise. It is not every day that someone pulls an apple out of the ground! I worried that Socko might punish her for snacking right in front of him, but no, Socko ran straight to the tractor tire! He looked into it from several angles, but obviously it was empty. It was as if he had concluded that we were hiding fruit again—and he recalled the exact location we’d used before. This was most remarkable since I am pretty sure Socko had had only one experience of this kind in his whole life, which had occurred five years earlier.

Was this mere coincidence? It is hard to tell based on a single event, but fortunately a Spanish scientist, Gema Martin-Ordas, has been testing out this sort of memory. Working with a large number of chimpanzees and orangutans, she tested the apes on what they remembered of past events. Previously, the apes had been given a task that required them to find the right tool to fetch either a banana or frozen yogurt. The apes had watched tools being hidden in boxes, after which they needed to pick the right box to get a tool for the task. This being easy for apes, all went well. But three years later, after the apes had gone through scores of other events and tests, they all of a sudden encountered the same person, Martin-Ordas, presenting the same setup in the same rooms of the building. Would the presence of the same investigator and situation cue the apes about the challenge they faced? Would they know right away what tool to use and where to look for it? They did, or at least those with previous experience did. Naïve apes did nothing of the kind, thus confirming the role of memory. And not only that, the apes did not hesitate: they solved the problem in a matter of seconds.3

Most animal learning is of a rather vague kind, similar to how I have learned to avoid some Atlanta highways at certain times of the day. Having gotten stuck in traffic often enough, I will look for a better, faster route, without any specific memory of what happened on my previous commutes. This is also how a rat in a maze learns to turn one way and not another, and how a bird learns at what time of day to find bread crumbs at my parents’ balcony. This kind of learning is all around us. What we deem a special kind, the one at issue here, is the recall of particulars, the way the French novelist Marcel Proust, in In Search of Lost Time dwelled on the taste of a petite madeleine. The little tea-soaked biscuit made him relive his childhood visits to Aunt Leonie: “No sooner had the warm liquid mixed with the crumbs touched my palate than a shudder ran through me and I stopped, intent upon the extraordinary thing that was happening to me.”4 The power of autobiographical memories lies in their specificity. Colorful and alive, they can be actively called up and dwelled upon. They are reconstructions—which is why they are sometimes false—yet so powerful that they are accompanied by an extraordinary sense of their correctness. They fill us with emotions and sensations, as happened to Proust. You mention someone’s wedding day, or Dad’s funeral, and all sorts of memories about the weather, the guests, the food, the happiness, or the sadness will flood the mind.

This kind of memory must be at work when apes react to cues connected to events from years back. The same memory serves foraging wild chimpanzees, which visit about a dozen fruit-bearing trees per day. How do they know where to go? The forest has far too many trees to go about it randomly. Working in Taï National Park, in Ivory Coast, the Dutch primatologist Karline Janmaat found apes to have an excellent recall of previous meals. They mostly checked trees at which they had eaten in previous years. If they ran into copious ripe fruit, they’d gorge on it while grunting contentedly and make sure to return a couple of days later.

Janmaat describes how the chimps would build their daily nests (in which they sleep for only one night) en route to such trees and get up before dawn, something they normally hate to do. The intrepid primatologist followed the traveling party on foot, but whereas the chimps typically ignored her tripping or stepping on a noisy branch, now they all would turn around and stare pointedly at her, making her feel bad. Sounds draw attention, and the chimps were on edge in the dark. This was understandable since one of the females had recently lost her infant to a leopard.

Despite their deep-seated fear, the apes would set out on a long trek to a specific fig tree where they had recently eaten. Their goal was to beat the early fig rush. These soft, sweet fruits are favored by many forest animals, from squirrels to flocks of hornbills, so that an early arrival would be the only way to take advantage of the abundance. Remarkably, the chimps would get up earlier for trees far from their nests than for those nearby, arriving at about the same time at both. This suggests calculation of travel time based on expected distances. All this makes Janmaat believe that the Taï chimpanzees actively recall previous experiences in order to plan for a plentiful breakfast.5

The Estonian-Canadian psychologist Endel Tulving defined episodic memory as the recall of what happened at which place and at what time. This has prompted research into memory of the three W’s of events: their what, when, and where.6 While the above ape examples seem to fit the bill, we need more tightly controlled experiments. The first challenge to Tulving’s claim that episodic memory is limited to humans came from precisely such an experiment, not on apes, but on birds. Together with Anthony Dickinson, Nicky Clayton took advantage of the hoarding tendency of her western scrub jays to see what they remembered about cached foods. The birds were given different items to hide, some perishable (waxworms), others durable (peanuts). Four hours later the jays looked for the worms—their favorite food—before they looked for nuts, but five days later their response was reversed. They didn’t even bother to find the worms, which by that time would have spoiled and become distasteful. They did remember the peanut locations after this long interval, though. Odor could be ruled out as a factor, because by the time they were tested, the scientists recorded search patterns in the absence of food. This study was quite ingenious and included a few additional controls, leading the authors to conclude that jays recall what items they have put where and at what point in time. They remembered the three W’s of their actions.7

The case for episodic memory in animals was further strengthened when the American psychologists Stephanie Babb and Jonathon Crystal let rats run around in an eight-armed radial maze. The rodents learned that once they had visited an arm and eaten the food in it, it would be permanently gone, so there would be no point returning to it. There was one exception, though. They occasionally found chocolate-flavored pellets, which would be replenished after long time intervals. The rats formed an expectation about this delicious food based on where and when they had encountered it. They did return to those specific arms, but only after long intervals. In other words, the rodents kept track of the when, what, and where of chocolate surprises.8

Tulving and a few other scholars were hardly satisfied with these results, however. They fail to tell us—the way Proust did so eloquently—how aware the birds, rats or apes are of their own memories. What kind of consciousness, if any, is involved? Do they view their past as a piece of personal history? Since such questions are unanswerable, some have weakened the terminology by endowing animals only with “episodic-like” memory. I don’t agree with this retreat, however, since it gives weight to an ill-defined aspect of human memory known only through introspection and language. While language is helpful to communicate memories, it is hardly what produces them. My preference would be to turn the burden of proof around, especially when it comes to species close to us. If other primates recall events with equal precision as humans do, the most economic assumption is that they do so in the same way. Those who insist that human memory rests on unique levels of awareness have their work cut out for them to substantiate such a claim.

It may, literally, be all in our heads.

The Cat’s Umbrella

The debate about how animals experience the time dimension heated up even further in relation to the future. Who’d ever heard of them contemplating events that lay ahead? Tulving drew on what he knew about Cashew, his cat. Cashew seems capable of predicting rain, he said, and is good at finding places to take cover, yet “never thinks ahead and packs an umbrella.”9 Generalizing this astute observation to the entire animal kingdom, the eminent scientist explained that while animals adapt to their present environment, they sadly fail to imagine the future.

Another human uniqueness proponent noted that “there is no obvious evidence that animals have ever agreed on a five-year plan.”10 True, but how many humans have? I associate five-year plans with central government and prefer examples drawn from the way both humans and animals go about their daily business. For example, I may plan to buy groceries on my way home, or decide to surprise my students with a quiz next week. This is the nature of our planning. It is not unlike the story with which I opened this book regarding Franje, the chimpanzee who gathered all the straw from her night cage to build a warm nest outdoors. That she took this precaution while still indoors, before actually feeling the cold outside, is significant because it fits Tulving’s so-called spoon test. In an Estonian children’s story, a girl dreams of a friend’s chocolate pudding party where she can only watch other children eat, because everyone has brought their own spoon, and she has not. To prevent this from happening again, she goes to bed that night clutching a spoon. Tulving proposed two criteria to recognize future planning. First, the behavior should not follow directly from present needs and desires. Second, it should prepare the individual for a future situation in a different context than the current one. The girl needed a spoon not in bed, but at the chocolate pudding party she expected in her dream.11

When Tulving came up with the spoon test, he wondered if it was perhaps unfair. Wasn’t it too demanding for animals? He proposed this test in 2005, well before most experiments on future planning were conducted, apparently unaware that apes pass the spoon test every day in their spontaneous behavior. Franje did so when she gathered straw in a different location and under different circumstances than where it was needed. At the Yerkes Primate Center, we also have a male chimp, Steward, who never enters our testing room without first looking around outdoors for a stick or branch that he uses to point at the various items in our experiments. Even though we have tried to discourage this behavior, by removing the stick from his hands so that he’ll point with a finger like everyone else, Steward is stubborn. He prefers to point with a stick and will go out of his way to bring one with him, thus anticipating our test and his self-invented need for a tool.

But perhaps the nicest illustration, out of dozens I could offer, is a bonobo named Lisala, who lives at Lola ya Bonobo, a jungle sanctuary near Kinshasa where we conducted studies of empathy. The observation in question was unrelated to this topic, however, and was made by my coworker Zanna Clay when she unexpectedly saw Lisala pick up an enormous fifteen-pound rock and lift it onto her back. Lisala carried this heavy load on her shoulders while her baby clung to her lower back. It was rather ridiculous, of course, since it impeded her travel and required extra energy. Zanna turned on her video camera and followed the bonobo to see what the rock might be for. Like any true ape expert, she immediately assumed that Lisala had a goal in mind, because, as K?hler had noted, ape behavior is “unwaveringly purposeful.” The same holds for human behavior. If we see a man walking in the street with a ladder, we automatically assume that he wouldn’t be carrying such a heavy tool for no reason.

Lisala, a bonobo, carries a heavy rock on a long trek toward a place where she knows there are nuts. After collecting the nuts, she continues her trek to the only large slab of rock in the area, where she employs her rock as a hammer to crack the nuts. Picking up a tool so long in advance suggests planning.

Zanna filmed Lisala’s trek of about half a kilometer. It was interrupted only once when she put down the rock and picked up some items that were hard to identify. Then she put the rock back onto her back and continued her travels. She walked all told almost ten minutes before she reached her destination, which was a large slab of hard rock. She cleared it of debris with a few swipes of her hand, then put down her rock, her infant, and the collected items, which turned out to be a handful of palm nuts. She set out to crack these extremely tough nuts, placing them on the large anvil while banging them with her fifteen-pound rock as a hammer. She spent about fifteen minutes on this activity, then left her tool behind. It is hard to imagine that Lisala had gone through all this trouble without a plan, which she must have had well before she picked up the nuts. She probably knew where to find those, hence planned her route via this location, to end up at a point that she knew had a hard enough surface for successful cracking. In a nutshell, Lisala fulfilled all of Tulving’s criteria. She picked up a tool to be used at a distant location for the processing of food that she could only have imagined.

Another remarkable instance of future-oriented behavior was documented at a zoo by the Swedish biologist Mathias Osvath, this time involving a male chimpanzee, Santino. Every morning before visitors arrived, Santino would leisurely collect rocks from the moat surrounding his enclosure, stacking them up in neat little piles hidden from view. This way he’d have an arsenal of weapons when the zoo opened its gates. Like so many male chimps, Santino would several times a day rush around with all his hair on end to impress the colony and the public. Throwing stuff around was part of the show, including projectiles aimed at the watching masses. Whereas most chimps find themselves empty-handed at the critical moment, Santino prepared his rock piles for these occasions. He did so at a quiet time of the day, when he was not yet in the adrenaline-filled mood to produce his usual spectacle.12

Such cases deserve attention since they show that apes do not have to be prompted by experimental conditions concocted by us humans to plan for the future. They do so of their own accord. Their accomplishments are quite different from the way many other animals orient to upcoming events. We all know that squirrels collect nuts in the fall and hide them for retrieval in winter and spring. Their hoarding is triggered by the shortening of day length and the presence of nuts, regardless of whether the animals know what winter is. Young squirrels naïve about the seasons do exactly the same. Whereas this activity does serve future needs and requires quite a bit of cognition regarding what nuts to store and how to find them again, the seasonal preparations of squirrels are unlikely to reflect actual planning.13 It is an evolved tendency found in all members of their species and limited to only one context.

The planning of apes, in contrast, adjusts to the circumstances and is flexibly expressed in myriad ways. That it is based on learning and understanding is hard to prove from observation alone, however. It requires subjecting apes to conditions that they have never met before. What happens, for example, if we create a situation in which clutching a spoon, so to speak, is advantageous later on?

The first such study was conducted in Germany by Nicholas Mulcahy and Josep Call, who let orangutans and bonobos select a tool that they couldn’t use right away even though the rewards were visible. The apes were moved away to a waiting room to see if they would hold on to their tool for later use even if the right occasion would arise only fourteen hours later. The apes did so, yet it could be (and has been) argued that they might have developed positive associations with certain tools, hence valued them regardless of what they knew about the future.14

This issue was addressed by a similar experiment in which apes selected tools, but this time the rewards were kept out of sight. The apes preferred a tool they could use in the future over a grape placed right next to it. They suppressed their desire for an immediate benefit to gamble on a future one. Once they had the right tool in hand, however, and got a second presentation of the same set of tools, they did pick the grape. Clearly, they didn’t value the tool over anything else, because if they did, their second choice should have replicated the first. The apes must have realized that once they had the right tool in hand, there was no point having a second one of the same kind, and that the grape was a better choice.15

These clever experiments were foreshadowed by Tulving’s proposal as well as by K?hler, who was the first to speculate about future planning in animals. There is now even a test in which, instead of presenting apes with actual tools, they are given an opportunity to fabricate them in advance. Apes learned to break a board of soft wood into smaller pieces to produce sticks with which they could reach grapes. Anticipating the need for sticks, they worked hard on having them ready in time.16 Their preparations resembled the behavior of wild apes, which travel long distances with raw materials that they turn on the spot into tools by modifying, sharpening, or fraying them. They sometimes bring more than one type of tool to a task in the forest. Chimps carry toolkits of up to five different sticks and twigs to hunt for underground ants or raid bee nests for honey. It is hard to imagine an ape searching for and traveling with multiple instruments without a plan. Just so, Lisala picked up a heavy rock that by itself was useless and that could serve its purpose only in combination with nuts that she had yet to collect as well as a hard surface located far away. Attempts to explain this kind of behavior without foresight invariably sound cumbersome and far-fetched.

The question now is whether similar evidence can be produced without reliance on tools such as spoons, umbrellas, or sticks. What if we consider a wider spectrum of behavior? How this might be done was again demonstrated by Clayton’s scrub jays. These birds routinely cache food, and although some scientists complain that this behavior offers a rather narrow window on cognition, it is a window nonetheless and one that differs radically from the one used for primates. It exploits an activity that corvids are particularly good at, just as tool studies exploit specialized primate skills. The outcome has been most remarkable.

Caroline Raby offered jays an opportunity to store food in two compartments of their cage that would be closed off during the night. The next morning they would get a chance to visit only one of the two compartments. One compartment had become associated with hunger, since the birds had spent mornings there without breakfast. The second compartment, on the other hand, was known as the “breakfast room” because it was stocked with food every morning. Given a chance in the evening to cache pine nuts, the birds put three times as many nuts in the first room as in the second, thus anticipating the hunger they might suffer there. In another experiment, the birds had learned to associate both compartments with different kinds of food. Once they knew what kind to expect, they tended to store a different food in each compartment in the evening. This guaranteed a more varied breakfast if they ended up in one of those compartments next morning. All in all, when scrub jays stash away food, they do not seem guided by their present needs and desires but rather by the ones they anticipate in the future.17

In thinking of primate examples without tools, the ones that come to mind are social situations in which it helps to be diplomatic. For example, chimpanzees sometimes arrange a secret rendezvous with the opposite sex. Bonobos don’t need to do so, since others rarely interrupt their sexual escapades, but chimpanzees are far less tolerant. High-ranking males don’t allow rivals near females with an attractive genital swelling. Nevertheless, the alpha male cannot always be awake and alert, hence occasions do arise for young males to invite a female to get away to a quiet spot. Typically, the young male spreads his legs to show his erection—a sexual invitation—making sure that his back is turned to the other males or that, with his underarm leaning on his knee, one of his hands loosely dangles right next to his penis so that only the wooed female can see it. After this display, the male nonchalantly wanders off in a given direction and sits down out of view of dominant males. Now it is up to the female, who may or may not follow. So as to give nothing away, she usually takes off in a different direction, only to arrive, via a detour, at the same spot as the young male. What a coincidence! The two of them then engage in a quick copulation, making sure to stay silent. It all gives the impression of a well-planned arrangement.

Even more striking are the tactics of adult males challenging each other for status. Given that confrontations are almost never decided between two rivals on their own but involve support for one or the other by third parties, it is to their advantage to influence public opinion beforehand. The males commonly groom high-ranking females or one of their male buddies before launching into a display, with all their hair on end, to provoke a rival. The grooming gives the impression of them currying favors in advance, knowing full well what the next step will be. In fact, there has been a systematic study on this issue. At Chester Zoo in the United Kingdom, Nicola Koyama recorded for over two thousand hours who groomed whom in a large chimpanzee colony. She also noted what kinds of conflicts arose among the males, and who allied with whom. When she compared records on both behaviors—grooming and alliances—from one day to the next, she discovered that males received more support from the individuals they had groomed the day before. This is the sort of tit-for-tat that we are used to in chimpanzees. But since this connection held only for the aggressors, and not for their victims, the explanation was not simply that grooming promotes support. Koyama viewed the connection as part of an active strategy. Males know beforehand which confrontations they are going to incite, and they pave the way for them by grooming their friends a day in advance. This way they make sure to have their backing.18 It reminds me of the politics at university departments, where colleagues come to my office in the days leading up to an important faculty meeting to influence my vote.

Observations are suggestive yet rarely conclusive. They do, however, give an idea under what circumstances future planning might be useful. If naturalistic observations and experiments point in the same direction, we must be on the right track. For example, a recent study suggested that wild orangutans communicate future travel routes. Orangutans are such loners that their encounters in the canopy have been described as ships passing in the night. They often travel on their own, accompanied only by their dependent offspring, and remain visually isolated for long stretches of time. Auditory information about one another’s whereabouts is often all they have.

Carel van Schaik—a Dutch primatologist who once was a fellow student of mine and whose field site on Sumatra I visited—followed wild males right before they went to bed in their self-made nests high up in the trees. He recorded over a thousand whooping calls made by these males before nightfall. These loud calls may last for up to four minutes, and all orangs around pay close attention, because the dominant male (the only fully grown male with well-developed cheek pads, or flanges) is a figure to be reckoned with. There is usually only one such male in a given area of the forest.

Carel found that the direction in which adult males call before going to sleep predicts their travel path the next day. The calls contain this information even if the direction changes from day to day. Females adjust their own routes to the male’s, such that sexually receptive females may approach him, and other females know where to find him in case they are being harassed by adolescent males. (Female orangutans generally prefer the dominant male.) Although Carel recognizes the limitations of a field study, his data imply that orangutans know where they will be going and vocally announce their plan at least twelve hours before its execution.19

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 gratification 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.

Animal research in this area began perhaps with the uncertainty response noticed by Tolman in the 1920s. His rats seemed to hesitate before a difficult task as reflected in their “lookings or runnings back and forth.”36 This was most remarkable, since at the time animals were thought to simply respond to stimuli. Absent an inner life, why be in turmoil about a decision? Decades later the American psychologist David Smith gave a bottlenose dolphin the task to tell the difference between high and low tones. The dolphin was an eighteen-year-old male named Natua, in a pool at the Dolphin Research Center in Florida. As in Tolman’s rats, Natua’s level of confidence was quite manifest. He swam at different speeds toward the response, depending on how easy or hard it was to tell both tones apart. When they were very different, the dolphin arrived with such speed that his bow wave threatened to soak the electronics of the apparatus. They had to be covered with plastic. If the tones were similar, though, Natua slowed down, waggled his head, and wavered between the two paddles that he needed to touch in order to indicate a high or low sound. He didn’t know which one to pick. Smith decided to make a study of Natua’s uncertainty, mindful of Tolman’s suggestion that it might reflect consciousness. The investigator created a way for the animal to opt out. A third paddle was added, which Natua could touch if he wanted a fresh trial with an easier distinction. The tougher the choice, the more Natua went for the third paddle, apparently realizing when he had trouble coming up with the right answer. Thus the field of animal metacognition was born.37

Investigators have essentially followed two approaches. One is to explore the uncertainty response, as in the dolphin study, while the other is to see if animals realize when they need more information. The first approach has been successful with rats and macaques. Robert Hampton, now a colleague at Emory University, gave monkeys a memory task on a touchscreen. They would first see one particular image, say a pink flower, then face a delay before being presented with several pictures, including the pink flower. The delay varied in length. Before each test, the monkeys had the choice to either take it or decline it. If they took the test and correctly touched the pink flower, they gained a peanut. But if they declined, they only got a monkey pellet, a boring everyday food. The longer the delay, the more the monkeys declined taking the test despite its better reward. They seemed to realize that their memory had faded. Occasionally, they were forced to take a trial without a chance of escape. In those cases they fared rather poorly. In other words, they opted out for a reason, doing so when they couldn’t count on their memory.38 A similar test with rats gave similar results: the rats performed best on tests that they had deliberately chosen to take.39 In other words, both macaques and rats volunteer for tests only when they feel confident, suggesting that they know their own knowledge.

A rhesus macaque knows that food has been hidden in one of four tubes, but he has no idea which one. He is not allowed to try every tube and will get only one pick. By bending down to first peek into the tubes, he demonstrates that he knows he doesn’t know, which is a sign of metacognition.

The second approach concerns information seeking. For example, jays placed at peepholes were given an opportunity to watch food—waxworms—being hidden before they were allowed to enter the area to find it. They could look through one peephole to see an experimenter put a waxworm in one of four open cups, or they could look through another to see another experimenter with three covered cups plus one open one. In the second case, it was obvious where the worm would end up. Before entering the area to find the worm, the birds spent more time watching the first experimenter. They seemed to realize that this was the information they needed most.40

In monkeys and apes, the same sort of test has been done by having them watch an experimenter hide food in one of several horizontal pipes. Obviously, the primates remembered where he had put the food and confidently selected the correct pipe. If the food hiding had taken place in secret, however, they were not sure which pipe to pick. They peeked into the pipes, bending down to get a good look, before selecting one. They realized that they needed more information to succeed.41

As a result of these studies, some animals are now believed to track their own knowledge and to realize when it is deficient. It all fits Tolman’s insistence that animals are active processors of the cues around them, with beliefs, expectations, perhaps even consciousness. This viewpoint being on the rise, I asked my colleague Rob Hampton about the state of affairs in this field. The two of us have offices on the same floor of Emory’s psychology department. While sitting in mine, we first watched the video of Lisala carrying her huge rock. Like a real scientist, Rob immediately began to imagine how to turn this situation into a controlled experiment by varying the locations of the nuts and the tools, even though for me the beauty of the whole sequence was Lisala’s spontaneity. We had nothing to do with it. Rob was impressed.

I asked him if his work on metacognition had been inspired by the dolphin study, but he rather saw this as a case of convergent interests. The dolphin study did come out first, but it wasn’t about memory, which was Rob’s focus. He was inspired by the ideas of Alastair Inman, a postdoc in Sara Shettleworth’s Toronto lab, where Rob worked at the time. Alastair wondered about the cost of memorizing things. What is the price of holding information in mind? He set up an experiment on pigeon memory that was similar to the metacognition test for monkeys that Rob developed.42

When I asked what he thought of people who draw a sharp line between humans and other animals, such as Endel Tulving’s shifting definitions, Rob exclaimed: “Tulving! He loves to do that. He has done a great service to the animal research community.” Tulving says those things, Rob believes, because he thinks it’s fun to set a high bar. He knows that others will go after it, so he pushes them to come up with clever experiments. In his first monkey paper, Rob thanked Tulving for his “incitement.” Meeting the senior scientist not long thereafter at a conference, Tulving told Rob, “I have seen what you wrote, thank you!”

For Rob, the big question in relation to consciousness is why we actually need it. What is it good for? After all, there are lots of things we can do unconsciously. For example, amnesic patients are able to learn without knowing what they have learned. They may learn to make inverse drawings guided by a mirror. They acquire the hand-eye coordination at about the same rate as any other person, but every time you test them, they’ll tell you that they’ve never done it before. It is all new to them. In their behavior, though, it is obvious that they have experience with the task and have acquired the required skill.

While consciousness has evolved at least once, it is unclear why and under which conditions. Rob considers it such a messy word that he is reluctant to use it. He adds, “Anyone who thinks they have solved the problem of consciousness hasn’t been thinking about it carefully enough.”


When in 2012 a group of prominent scientists came out with The Cambridge Declaration on Consciousness, I was skeptical.43 The media described it as asserting once and for all that nonhuman animals are conscious beings. Like most scientists studying animal behavior, I really don’t know what to say to this. Given how ill-defined consciousness is, it is not something we can affirm by majority vote or by people saying “Of course, they are conscious—I can see it in their eyes.” Subjective feelings won’t get us there. Science goes by hard evidence.

But in reading the actual declaration, I calmed down, because it is a reasonable document. It doesn’t actually claim animal consciousness, whatever that is. It only says that given the similarities in behavior and nervous systems between humans and other large-brained species, there is no reason to cling to the notion that only humans are conscious. As the document puts it, “The weight of evidence indicates that humans are not unique in possessing the neurological substrates that generate consciousness.” I can live with that. As you can see from this chapter, there is sound evidence that mental processes associated with consciousness in humans, such as how we relate to the past and future, occur in other species as well. Strictly speaking, this doesn’t prove consciousness, but science is increasingly favoring continuity over discontinuity. This is certainly true for comparisons between humans and other primates, but extends to other mammals and birds, especially since bird brains turn out to resemble those of mammals more than previously thought. All vertebrate brains are homologous.

Although we cannot directly measure consciousness, other species show evidence of having precisely those capacities traditionally viewed as its indicators. To maintain that they possess these capacities in the absence of consciousness introduces an unnecessary dichotomy. It suggests that they do what we do but in fundamentally different ways. From an evolutionary standpoint, this sounds illogical. And logic is one of those other capacities we pride ourselves on.

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