The Many Emotions Of Animals

The following is an excerpt of Mama’s Last Hug by Frans de Waal.

Science often compares adult apes to children, as in “the chimpanzee has the mind of a four-year-old.” I never know what to do with such statements, though, given that I find it impossible to look at an adult chimpanzee as a child. A male is interested in power and sex and prepared to kill for it. If he is high-ranking, he may adopt a leadership role, which includes keeping order and defending the underdog. Males engaged in power struggles sometimes have a permanently furred-brow expression suggesting internal turmoil, and they are known to have high levels of stress. A female ape, on the other hand, is mainly interested in her offspring and the duties that come with motherhood, such as taking time to nurse, finding food, and deterring predators and aggressive members of her own species. She also works every day on her relationships, grooming her friends, consoling them after upheavals, and watching over their offspring if needed. The lives of adult apes center very much on adult concerns, therefore, and share little with a child’s insouciance.

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Juvenile apes squabble over food and hit each other screaming over the head, while adult apes politely beg and share, sometimes taking turns, while exchanging food for services received earlier in the day. Here, too, the best comparison is between ape and human juveniles or ape and human adults. This matters in relation to emotions, because some emotions are typical of adults, especially those that require a greater appreciation of time than is found in the young. Youngsters live in the moment, while adults don’t. Some emotions are future oriented, such as hope and worry, while others relate to the past, such as revenge, forgiveness, and gratitude. All these timeline emotions, as I like to call them, seem present in adult apes and in some other animals as well.

In chimpanzees, sharing food is part of a give-and-take economy that includes grooming, sex, support in fights, and other types of aid. All these favors are thrown into one big exchange basket glued together by the emotion of gratitude. Gratitude functions to maintain balance sheets of exchange: it prompts individuals to seek out those who have been good to them, and—if the occasion arises—return their favors. Based on thousands of observations, we have found that chimpanzees share food specifically with those who have been kind to them in the past. Every morning, when the apes gather in the climbing frame to patiently tend each other’s hair, we measure who grooms whom. In the afternoon, we provide them with shareable food, such as a few large watermelons. Melon owners allow anyone who has groomed them to remove pieces from their hands or mouth, but not individuals with whom they failed to interact in the morning—they may resist the latter individuals and sometimes even threaten them. Sharing patterns thus change from day to day depending on the distribution of earlier grooming. Since the time span between the two events is several hours, the sharing requires memory of past encounters and positive feelings about enjoyed services. We know this combination as gratitude.

Mark Twain once quipped, “If you pick up a starving dog and make him prosperous, he will not bite you. This is the principal difference between a dog and a man.” In my own home, adopted stray pets have always been most grateful for the warmth and food we offer. A scrawny kitten full of fleas, picked up in San Diego, grew into a gorgeous tomcat by the name of Diego. Diego purred excessively his entire fifteen-year-long life whenever he was fed—even when he barely ate anything. We interpreted his behavior as gratefulness, but it is hard to exclude mere happiness. Diego may just have enjoyed food more than your average spoiled pet.

In apes, signs of gratitude may be more obvious. Two chimps had been shut out of their shelter during a rainstorm. Wolfgang Köhler, the German pioneer of tool use studies, happened to walk by and found both apes soaking wet, shivering in the rain. He opened the door for them. Instead of hurrying past him to enter the dry area, however, the chimps hugged the professor in a frenzy of satisfaction.

Their reaction resembles that of Wounda, a chimpanzee who had been rescued from poachers, near death, and received medical care at the Tchimpounga Rehabilitation Center in Congo- Brazzaville. In 2013 she was released back into the forest. A video of this moment went viral because of the emotional interaction between Wounda and Jane Goodall, who attended her release. At first Wounda walked away, but she then hastily returned to hug the people who had taken care of her. She specifically turned to Goodall for a long mutual embrace before taking off. This was remarkable because Wounda had first been on her way, then seemed to correct herself and return, as if realizing it wouldn’t be very nice to just walk away from those who had saved her and nursed her back to health.

Similar accounts exist of netted or beached dolphins and whales that human divers cut loose from nets or pushed back into the ocean. The cetaceans returned to their rescuers and nudged them or lifted them half out of the water before swimming away. In all cases, the humans present, deeply moved, viewed these interactions as signs of gratitude.

I have already mentioned how Kuif, Mama’s best friend, was affected by my teaching her how to raise a baby on a bottle. From the moment we gave her permission to pick up Roosje, the adoptive baby we put in the straw of her bedroom, she treated me as family, something she’d never done before. I saw this as a sign of gratitude for changing her life for the better, from a mother who had lost several infants due to lactation failure to one who successfully raised Roosje and later applied the same bottle skills to her own offspring.

The ugly sister of gratitude is revenge, an emotion equally concerned with the squaring of accounts, but in a negative sense. Edvard Westermarck, the Finnish anthropologist who gave us the first ideas about the evolution of human morality, stressed the value of retribution in keeping people in line. He didn’t think we were the only species with this tendency, but in his time, there was little animal behavior research. So he relied on anecdotes, such as one he heard in Morocco about a camel that had been excessively beaten by a fourteen-year-old boy for turning the wrong way. The animal passively took his punishment, but a few days later, while unladen and alone on the road with the same conductor, it “seized the unlucky boy’s head in its monstrous mouth, and lifting him up in the air flung him down again on the earth with the upper part of the skull completely torn off, and his brains scattered on the ground.” Stories of resentful animals can often be heard at zoos, usually concerning elephants (with their proverbial memories) and apes. Every new student or caretaker working with apes needs to be told that they won’t be able to get away pestering or insulting them. An insulted ape remembers and will take all the time in the world for the right opportunity to get even. Sometimes it doesn’t take long. One day a woman came to the front desk of a zoo where I worked complaining that her son had been hit by a rock coming from the chimpanzees. The son was surprisingly subdued, however. Witnesses later told us he’d thrown the same rock first.

Among themselves as well, chimps retaliate. They support each other in fights, following the rule that one good turn deserves another; experiments have confirmed this tendency. Given a chance, many animals are prepared to do a partner a favor, such as by pulling a lever or selecting a token that produces food. They do so at a moderate level as long as their partner is a passive recipient, but they dramatically increase their generosity when the partner is allowed to return the favor. When both parties stand to gain, they move to a new stage. This is of course also how things work in real life. What may be unique for chimpanzees is that they apply similar tit-for-tat rules to negative acts. They tend to get even with those who have acted against them. For example, if a dominant female often attacks another female, the latter cannot retaliate on her own but will wait for the best occasion. As soon as her tormenter is involved in a brawl with others, she will join in to add to her troubles.

After Nikkie became the new alpha male in the chimpanzee colony of Burgers Zoo, he regularly practiced strategic retaliation. His dominance was not yet fully acknowledged, and subordinates would often pressure him, banding together and chasing him around, leaving him panting and licking his wounds. But Nikkie did not give up, and a few hours later he’d regain his composure. The rest of the day he’d go around the large island to single out members of the resistance, visiting them one by one while they were sitting alone minding their own business. He’d intimidate them or give them a beating, which likely made them think twice before opposing him again. This eye-for-an-eye tendency is so prominent in chimpanzees that it can be statistically demonstrated in thousands of observations in our database.

Retaliation is an “educational” reaction that attaches costs to undesirable behavior, but it is unclear if the apes themselves think along these lines. They probably just follow an urge to take revenge, a tendency we share with them. After all, we call revenge “sweet,” as if it were something delicious. When experimenters gave human subjects voodoo dolls representing people who had insulted them, their mood improved markedly when they were allowed to stick needles into those dolls. Our judicial systems take the longing to get even a step further: when the family of a murder victim or those who have been scammed out of money seek redress, they are undeniably driven by a deep desire to inflict harm on those who have done harm to them.

Chimpanzees do the same, thanks to their flexible hierarchy that offers room for retaliation. Rhesus macaques and baboons, in contrast, have such despotic hierarchies that it is almost suicidal for a subordinate to turn against a superior. Intimidation and punishments always flow down the hierarchy, which excludes opportunities for revenge. But even these monkeys know how to hit back: they rely on the kinship bonds that pervade their society. Grandmothers, mothers, and sisters spend extraordinary amounts of time together, forming tight units known as matrilines. A monkey who has become a victim of aggression will likely vent his feelings on a relative of the attacker. Instead of retaliating, which he can’t, he will look for a younger member of the attacker’s matriline, who will be easier to intimidate. They sometimes perform vindictive actions after quite a delay, suggesting they have excellent memories. This tactic obviously requires monkeys to be aware of the family to which every other monkey belongs, and we know they are. It would be as if I responded to a reprimand from my boss by yanking the hair of his young daughter. I don’t go against the pecking order, but I still punish my offender.

The final emotion concerning past events is forgiveness. Having studied primate reconciliation all my life, I have seen many times how chimpanzees kiss and embrace their former adversaries, how monkeys groom them, and how bonobos resolve social tensions with a little sex. This kind of behavior is not at all limited to primates: hundreds of reports find it in other social mammals and in birds, so much so that if anyone were to claim that a given species doesn’t make up after fights, we’d be baffled.

Conflict resolution is part and parcel of social life. The emotions involved are hard to pinpoint, but a minimum requirement is that anger and fear—the typical emotions during a confrontation—are toned down in order to permit a more positive attitude. This reversal is rather counterintuitive. Someone who has just lost a fight with a dominant attacker now needs to pluck up the courage to approach him or her for a friendly reunion. Meanwhile the aggressor must suddenly drop the enmity, which is illogical. But many animals undergo these emotional changes remarkably rapidly, as if a control knob in their mind were turned from hostile to friendly.

Humans become masters at turning the same emotional knob if we live in a conflict-prone environment, such as a large family or a workplace with lots of colleagues. These places require compromise and forgiveness every day. Forgiveness is never perfect, though, and even though we often say “Forgive and forget,” the forgetting part is problematic. We don’t erase the memory of a slight but simply decide to move on. Many group-living animals do the same because they, too, depend on peaceful coexistence and cooperation. Reconciliation is the observable process, whereas forgiveness is how it is internally experienced. Given the evolutionary antiquity of this mechanism, it is hard to imagine that the emotions involved are radically different between us and other species.

All three emotions—gratitude, revenge, and forgiveness—sustain social relationships based on years of interaction among individuals, sometimes going back to when they played together as youngsters. These emotions serve friendships and rivalries, enhance or harm trust, and keep the society functioning to everyone’s advantage. Animals are remarkably good at this balancing act, which requires them to exchange favors and resolve tensions. We know now that monkeys (and probably other animals as well) have dedicated brain networks that help them process social information. These neural networks have been tested: while monkeys watch televised scenes and see their fellows engage in social affairs, they are activated, but they remain inactive during physical or ecological scenes. Students of animal behavior have for a long time insisted on the special status of social intelligence: neuroscience is now backing us up.

Are there also emotions concerned with the future? It is well established that apes and some large- brained birds do not live purely in the present. Wild chimpanzees plan ahead by picking up tools hours before they arrive at the termite hill or beehive where they will use these implements. While collecting them, they must know where they are going. Similar planning has been demonstrated in primates and corvids, showing they may ignore immediate gratification to reap future benefits. Given a choice, apes will forgo a juicy grape placed right next to a tool that they can use only hours later for a better reward. This takes self-control. Planning is harder to prove in the social domain, even if the political battles among male chimpanzees are suggestive. When a young adult male challenges the established boss, he may lose about every confrontation and sustain frequent injuries. Yet he will keep going day after day without any immediate rewards. Only months later he may finally have a breakthrough and get support from others who help him topple his adversary. And even then, as was the case with Nikkie, the young male may still meet resistance before he is fully accepted. It may take years before his position is truly secure. Was this his plan all along? And if not, why go through this hell? It is hard to watch these strategies, as I have done so many times in my career, and not think that they are built on hope.

“Hope” is rarely attributed to animals, but the related idea of “expectation” was proposed already a century ago. The American psychologist Otto Tinklepaugh conducted an experiment in which a macaque watched a banana being placed under a cup. As soon as the monkey was given access to the room, she ran to the baited cup. If she found the banana, everything proceeded smoothly. But if the experimenter had surreptitiously replaced the banana with a piece of lettuce, the monkey could only stare at it. She’d frantically look around, inspecting the location over and over, while angrily shrieking at the sneaky experimenter. Only after a long pause would she settle for the disappointing vegetable. Tinklepaugh demonstrated that instead of a simple association between location and reward, the monkey recalled what she had seen being hidden. She had an expectation, the violation of which greatly upset her.

Primates and dogs react with similar surprise when human magicians make things miraculously disappear or conjure them out of thin air. Apes may laugh or look puzzled, while dogs madly search for the vanished treat, indicating that the reality they had in mind was different.

Expectations also feed tit-for-tat barter, which is well known among animals despite Adam Smith’s claim that “nobody ever saw a dog make a fair and deliberate exchange of one bone for another with another dog.”16 Smith may have been right about dogs, but wild chimpanzees in Guinea are known to raid papaya plantations in order to buy sex. Adult males usually steal large fruits, one for themselves, the other for a female with a genital swelling. The female waits at a quiet spot while the male risks the anger of farmers in order to bring her a delicious fruit, which he hands to her during or right after sex.

In another instance of tit for tat, the long-tailed macaques at some Balinese temples have a habit of stealing valuable objects from tourists. At temple entrances, written signs warn everyone to remove their glasses and take off their jewelry, but many tourists fail to do so, not realizing how incredibly fast the monkey mafia operates in these places. A monkey will jump onto their shoulder to snatch a pair of glasses or run off with a precious smartphone. They will steal flip-flops by literally removing them from the tourists’ feet. Instead of playing with these items or taking off with them, the monkeys sit down patiently nearby, but out of reach, to see how much their victim is willing to pay to get an item back. A few peanuts won’t do. The monkeys want at least a whole bag of crackers before they will drop the item. Primatologists who studied this extortion game found that the monkeys had a pretty good idea of which objects humans value the most.

Given the existence of future-oriented behavior, dogs have recently been classified as either “optimistic” or “pessimistic” while facing a given task. Dogs that get seriously upset when their owner leaves them alone at home—venting their frustration by destroying the house, relieving themselves, or furiously barking—are regarded as pessimistic. When presented with a food bowl of unknown content, they hesitate and approach slowly, perhaps expecting the bowl to be empty. Dogs that are less perturbed by separation, on the other hand, are considered more optimistic: they happily run toward the bowl, expecting it to be full. This so-called cognitive bias is also common in people. Cheery, easygoing people expect good things in life, whereas depressed ones believe that everything that can go wrong will go wrong.

Cognitive bias offers us a rare opportunity to test how farm animals feel about their living arrangements. After all, pigs that live under stress in small crates may expect few good things to happen to them. But those that live in a fun environment, with straw to burrow into while sleeping in piles, enjoying body heat and physical contact, may be in better spirits. In one study, groups of pigs were housed either in small pens with concrete floors or in larger pens with fresh straw every day and cardboard boxes to play with. All the pigs were trained on two different sounds: a positive sound would announce a slice of apple, and a negative sound announced only a plastic grocery bag waved in the pig’s face. Being intelligent, the pigs quickly learned to go for the positive sound.

After this training, the pigs were presented with an ambiguous sound, somewhere between the other two. What would they do? It depended entirely on their living conditions. The pigs in the enriched environment expected good things to happen and eagerly approached the ambiguous sound, but the ones kept in the barren environment did not see things the same way. They stayed away, perhaps expecting that stupid plastic bag again. If their housing was changed for better or worse, the pigs’ responses to the ambiguous sound followed suit, indicating that their daily life affected how they perceived the world. The cognitive bias test is informative, allowing us to verify the claims of companies that advertise their products as coming from happy animals, such as the well- known French spreadable cheese La vache qui rit (The Laughing Cow). The test can tell us if these animals really have anything to laugh about.

The condition of looking forward to something desirable is what we call “hope.” A monkey looking for a lucrative trade, a chimpanzee trying to improve his status, a dolphin searching the ocean for her lost calf, wolves setting out on a hunt, or a herd of elephants following an old matriarch who knows the last watering hole in the desert—all may well experience hope. It may be present or absent in farm animals as well. Like us, many animals evaluate everything that happens to them against a backdrop of past and future. Timeline emotions that transgress the present can no longer be denied, given the mounting evidence that animals hold memories of specific events, are forward- looking, exchange favors, and engage in an eye-for-an-eye.