Darwin argued that only humans blush. In the years since, the self-aware social emotions like shame, shyness, guilt, embarrassment, and self-consciousness—all feelings revolving around how the self is perceived by others—have usually been considered exclusively human. Yet there is evidence that many animals feel them, too, and shame may prove to be a surprisingly basic emotion.
Asked whether wild chimpanzees ever appear ashamed or embarrassed, Jane Goodall laughed. “They do, actually. In the wild you don’t see that very often. The best story I know of clear embarrassment was young Freud when he was about six years old. He was showing off—really, you could only describe it as showing off—in front of Uncle Figan, who was the alpha male. Figan was trying to groom Fifi, the new baby was there, and Freud was just prancing around and shaking branches and making a real big nuisance of himself. He went up into a tall plantain tree: they have a rather weak trunk like a banana. He was swaying it to and fro, to and fro, and suddenly it snapped!—and he crashed onto the ground. He just happened to land very close to me. I was able to see his face, and the first thing he did when he emerged from the grass was to take a quick little glance at Figan and then he crept quietly away and began feeding. That was quite clearly a big comedown for him.”
Shame is one of the most vividly remembered feelings. Recalling happiness or fear or anger, people do not usually experience the emotion again at the time of recalling it. But remembering an incident of embarrassment or shame can often bring a flood of shame sweeping back. Those who blush may blush again at a memory. In human psychology and psychotherapy, shame received little attention for years but has recently begun to be considered important. It has been called “the master emotion,” which societies use to enforce norms. Guilt refers to a particular event, but shame, which is more global, is said to refer to the individual’s entire being. Thus a person might feel guilt about going off their diet, and shame at being fat. Guilt can also result from a private event, while shame tends to require that others know or observe or are imagined to judge.
Some argue—not especially vigorously, as they have met little opposition—that only humans have self-conscious emotions. It is said that animals are intellectually incapable of self-consciousness—although this is generally meant to show the low level of animal intelligence rather than a lack of emotion.
But while it may seem logical to conclude that such emotions cannot exist without an intellectual comprehension of how one is viewed by other creatures, this need not be the case. There is no reason to suppose that an animal couldn’t feel shame without understanding why. As Darwin noted, mental confusion is a prominent symptom of shame. “I can’t think clearly in the moment of embarrassment, and I don’t know anybody else who can,” psychiatrist Donald Nathanson has written. Emotion can exist with or without understanding the reasons for it. One animal might be ashamed or embarrassed without being entirely conscious of the reason; another might be ashamed or embarrassed and understand the reason perfectly.
Self-consciousness denotes both emotional and intellectual states. Emotionally, it can be an uncomfortable feeling of being observed (or observing oneself)—a form of embarrassment. Intellectually, it is the reflective knowledge of one’s own mind, existence, and acts—a philosophical minefield.
Mirror studies with primates have been a focus of the debate over whether animals have or can have self-awareness. A chimpanzee allowed to become familiar with mirrors appears to learn that the image is its own. If such apes are anesthetized, dabbed on the face with a dot of paint, and given a mirror upon awakening, when they see the paint in their reflection they will touch their face with their fingers, examine their fingers, and then try to remove the paint. Orangutans also learn that the image in the mirror is of themselves; so far, monkeys have not done so. To some observers, this is evidence of self-consciousness. Others have sought to prove that it is nothing of the sort. John S. Kennedy follows some critics in arguing that it is more parsimonious to assume that the chimpanzee merely “forms a point-to-point association between the movements of the mirror image and his own movements.” This tortuous explanation assigns mental powers to the chimpanzee that are at least as complex as saying that it knows it is seeing itself in the mirror. Its appeal is simply that it denies the possibility of self-consciousness in a nonhuman being.
The chimpanzees Sherman and Austin, part of an ape language experiment in Atlanta, are monitored by video cameras that they have learned to use in a variety of ways. After several months of exposure to their own images on the video monitors, each ape appeared to suddenly realize that the image was of himself. They then used the monitor to observe themselves make faces, eat, or swirl water around in their mouths. Both have learned to distinguish between a live image and a taped image of themselves, by testing to see if their actions are duplicated on the screen. Sherman was using a hand mirror to guide his application of Crayola makeup one day, tired of the mirror and gestured to have the video camera aimed at his face instead. He used the image to apply the makeup and to locate and remove any that had stained his teeth. Austin made valiant attempts one day to use the monitor to look down his throat while simultaneously shining a flashlight into it.
The practice of saving face is another chimpanzee behavior that implies consciousness of self. At the zoo in Arnhem, the chimpanzee Yeroen was slightly injured in a fight with another chimp, Nikkie. To the astonishment of researchers, Yeroen spent the next week limping dramatically—but only in Nikkie’s view. A chimpanzee wishing to make peace with another sometimes will not approach directly, but will pretend to discover a nonexistent object and use the resulting gathering of many chimps to make contact with the former adversary, a strategy Frans de Waal thinks is used to save face.
In a diverse range of species, evidence that animals know when they are being observed suggests self-awareness. When a male baboon yawns, his impressive canine teeth are ostentatiously displayed. Observing wild baboons, biologist Craig Packer found that males with worn or broken teeth yawn less than males with teeth in good condition—unless there are no other males around, in which case they yawn just as often. Chimpanzees have been known to avoid glancing at a food source they know about but other chimps do not. On several occasions, lions in the Serengeti who had caught prey in high grass broke with the usual lion habit of beginning to eat at once. Instead the lion sat down and glanced around for as much as five minutes, as if it had caught nothing. When other nearby lions departed, the lion began to eat. A mountain goat who sees a predator will often walk away calmly and slowly and then, the moment it is out of the predator’s line of sight, take off, running at full speed. These animals act as if they were conscious of others perceiving their behavior and want to affect that perception. This level of self-consciousness might not permit a goat to look into a mirror and think, “That’s me,” but might show self-consciousness nonetheless. Self-awareness need not be all or nothing.
Embarrassment and shyness, also considered self-aware emotions, seem to be about being seen—in a bad light, or when one does not wish to be seen. Koko, the signing gorilla, has shown a rather touching form of embarrassment. Among her toys are a number of puppets and dolls. She was once seen signing “kiss” to her alligator puppet. On another occasion Koko signed “kiss” to her blue gorilla doll and “bad bad” to her pink gorilla doll. Then she signed “chase tickle,” slammed the dolls together, made them wrestle, and signed “good gorilla good good.” On each occasion, and other similar occasions, the moment she saw that she was being watched, she stopped playing.
Animals do not wear clothing to conceal parts of their bodies that humans in many cultures consider vital for adults to conceal. They do not hide many actions that correspond to actions people often prefer to hide. This does not necessarily mean that there is nothing they choose to hide or keep private. The courtship of one captive bird may be an example.
Alex, the verbally accomplished African grey parrot, may be imprinted on human beings. According to Irene Pepperberg, he attempts to court certain of her male students. When courting, Alex may regurgitate food and do a little ritualized dance. “If he is courting one of my students and I walk in, he immediately stops,” says Pepperberg. Perhaps Alex is embarrassed. If, on the other hand, he merely wants a little privacy, why does he want it? Perhaps he is trying to avoid competition. Is he shy? Shyness is an emotion that seems to shade into fear, the fear of being seen, and it may be that shame is also related to fear.
The essence of shame is the unpleasant feeling that one appears badly—weak, stupid, dirty, helpless, or inadequate—and the dread of appearing this way. At first sight, shame need have no connection with fear. At one oceanarium (where the animals were never punished) a bottle-nosed porpoise, Wela, was trained to jump out of the water and take a fish from a person’s hand. One day when this stunt was being photographed, trainer Karen Pryor was distracted and forgot to drop the fish as she usually did. As a result, when Wela grabbed the fish, she inadvertently bit Pryor’s hand. Wela, appearing “hideously embarrassed,” went to the bottom of the tank, put her snout in a corner, and would not come out until Pryor got in with her, petted her, and coaxed her into calmness.
Wela’s behavior is comparable to that of a dog who barks and threatens someone coming into the house—and suddenly realizes that the someone is its owner. From a barking, bristling, menacing creature, the dog suddenly deflates to a wriggling, whining, tail-wagging pup. It has been argued that the comic reversal of behavior in such a dog does not mean he or she is embarrassed, only seeking to appease a dominant animal—its owner—by showing submission. Whether this is accurate or not, it does not seem to describe Wela’s behavior, which looks more like embarrassment, a form of shame. The chimpanzee Washoe was seen to make a similar mistake, threatening an old friend (who had grown four or five inches since they had last met) before she recognized who it was and reacted with what would be called embarrassment if Washoe were human. One might say that such behavior is merely ritual submission, but then the same description could apply to an embarrassed human apology.
Dog trainers at Guide Dogs for the Blind say that old dogs who have lost bladder or sphincter control seem to be embarrassed or ashamed. One otherwise healthy sixteen-year-old dog in this condition refused to go indoors as she had always done.
One text on animal behavior evades acknowledging animal emotion by insisting, “It is certainly acceptable to say our misbehaving dog is acting as if embarrassed. It would be entirely without foundation to say it was embarrassed, even though we admit to the probable existence of emotions in animals.”
The blush is a primary evidence of shame in people. Charles Darwin, who investigated blushing at great length, seems to have been surrounded by people who blushed at the least provocation. He noted that it was usually accompanied by other signs of shame such as averting the eyes, the face, or the whole body. He had difficulty explaining the value of this phenomenon, and gave a rather Lamarckian explanation for it. Humans, he said, care about their personal appearance and the opinion of others. When people feel attention, especially critical attention, being directed at them, this “excite[s] into activity that part of the sensorium which receives the sensory nerves of the face; and this will react through the vaso-motor system on the facial capillaries. By frequent reiteration through numberless generations, the process will have become so habitual . . . that even a suspicion of . . . depreciation suffices to relax the capillaries, without any conscious thought about our faces.”
After questioning British missionaries stationed around the world on this subject, Darwin concluded that people of all races blush, and that it is not learned, since people who have been born blind also blush. (His data contradicted those defenders of slavery who alleged that Negroes did not blush because they were incapable of shame and hence not fully human.) He called blushing “the most peculiar and the most human of all expressions. Monkeys redden from passion, but it would require an overwhelming amount of evidence to make us believe that any animal could blush.”
It would have interested Darwin to know that animals other than monkeys also exhibit reddening skin. The ears of a Tasmanian devil (a small, carnivorous marsupial) in the Frankfurt Zoo turned red “during a state of excitement.” Some birds blush, as can be seen on featherless areas of skin. Like the turkey, the spangled honeyeater and the smoky honeyeater have unfeathered wattles that blush “when the bird is excited.” Macaws that have bare skin on their cheeks can be seen to blush. They do so when excited or enraged, and, according to parrot behaviorist Mattie Sue Athan, they have also been seen to do so if they fall accidentally while clambering down from a perch. This certainly looks like embarrassment. On the other hand the macaw might just be angry that it has fallen. Perhaps it will turn out to be true that humans are the only animals to blush self-consciously. Humans are unusually devoid of fur, feathers, and other coverings, after all, and so provide a large canvas for this effect.
On the other hand, it may be that the function of blushing is not, or not wholly, a visual one. The phenomenon of blushing need not be visible. Many people feel tingling skin—and shame—without visibly reddening. If people flushed, paled, and turned green with the frequency found in fiction, society would be a much more colorful place. Perhaps many species of animals blush unnoticed. No one has checked to see if, under the fur, a raccoon tingles with mortification or flushes with pride. Whether macaws also blush on the parts of their bodies covered by feathers or whether other parrots flush beneath their feathers is unknown. But even if they do not, it does not necessarily follow that if animals do not blush, they do not feel shame.
If shame proves to be widespread in the animal kingdom, the evolutionary approach would predict that it should confer some advantage. Just what might be adaptive about global self-accusation is not immediately apparent.
The self-conscious emotions seem to appear early in the lives of humans. In one series of experiments, researchers gave small children toys cunningly designed to fall apart and then videotaped their play. When a toy broke, some children cried; some looked for another toy; some appeared ashamed or guilty. Some children looked away, their bodies “collapsed” in what is considered a typical shame response. A child who appeared tense and averted its gaze, but then tried to fix the toy, was thought to be showing a guilt response. Helen Block Lewis, an early theorist in the field of shame and guilt, viewed human shame and guilt as regulators of social interactions that combat narcissism and punish transgressions of group mores. Blushing signals to other group members that the blusher recognizes such transgression and, therefore, recognizes the group rules.
Psychiatrist Donald Nathanson does not consider shame a social emotion. He cites an experiment in which three- to four-month-old infants could control a display of flashing colored lights by turning their heads. The babies apparently loved doing this and squealed with pleasure when the lights went on. When the experimenters changed the apparatus so that the babies’ efforts were unsuccessful, the infants’ heads and necks slumped, their breathing quickened, blood flow to their skin increased, and they turned their faces away. Nathanson and other theorists interpret this as a primitive shame response that was independent of whether or not other people were present, and hence argue that shame is not necessarily a social emotion. (It is not clear how disappointment and frustration can be excluded as possible explanations.) In Nathanson’s analysis, shame is “a biological system by which the organism controls its affective output so that it will not remain interested or content when it may not be safe to do so, or so that it will not remain in affective resonance with an organism that fails to match patterns stored in memory.” He believes that it evolved comparatively recently.
As for the advantages of global self-accusation, Nathanson argues: “If you were going to design a system capable of learning from experience and educating itself, you might as well build in the capacity to magnify failure. Shame augments our memory of failure and protects us from whatever danger might occur, when, in a moment of need, we might try something well beyond our capac ity.”
Another possibility is that shame might keep animals from attracting the attention of predators. Humans feel ashamed not only of their actual or perceived faults, but often of their differences from others, even when those differences are neutral or even positive. To be stared at can be unnerving, even when the stare is an admiring one. Often people are uncomfortable when praised. To be singled out in any way can be acutely embarrassing—and may also feel perilous.
Predators single out prey. Some predators select prey on the basis of physical condition, thus culling out sick and injured animals, as well as young animals. They may study herds of prey animals, chase some of them, and make an all-out effort to catch only a few. An examination of the bone marrow of wildebeest killed by lions revealed that a large percentage were in poor condition. Hyenas hunting make random passes at herds, or zigzag through, then stop and watch them run, switching their attention from animal to animal, apparently looking for potential weakness. One experimenter who was shooting wildebeest with anesthetic darts in order to measure and tag them found that, if he was not careful, these same animals would at once be killed by hyenas when he released them. Although they looked normal to humans, and seemed to be able to run as fast as ever, the hyenas noted some difference. He had to herd the hyenas away with his vehicle until the wildebeest had more time to recover.
Predators also notice other differences. A researcher once marked some wildebeest by painting their horns white. Within a few months, almost all of these animals had been killed by hyenas. Hans Kruuk has noted instances in which hyenas pursued animals who were presumably in good physical condition but were acting oddly and were then singled out by hyenas. At night, when dazzled by the headlights of a car, wildebeest ran in an odd way—and were instantly pursued by hyenas. Away from the headlights, the wildebeest quickly got their bearings and escaped.
Kruuk also saw a herd of several hundred wildebeest in which only one was rolling and showing territorial behavior. These actions, unremarkable in another context, instantly attracted a hyena’s pursuit. The wildebeest escaped easily. That the wildebeest escaped in these instances supports the idea that the hyenas were detecting difference rather than weakness.
Schooling or flocking behavior can baffle some predators in a very simple way: by preventing them from focusing on individual prey. When a few members of a school of small silver fish were dyed blue, not only were they more frequently attacked by predators, but so were the normal silver fish next to them. Faced by a cloud of identical fish, the predator could not pick out an individual, but it was able to pick out the blue one or the one next to the blue one.
Prey animals often seem aware of the assessment of predators. In Zaire, Paul Leyhausen saw two uneasy-looking male kobs (large antelope) near a river. Presently he saw two lions lurking near the kobs, moving from behind one bush to another. The kob closest to the lions appeared to grow calmer and began grazing, but the other began to run back and forth in alarm. It soon became clear from their movements, Leyhausen says, that the lions were stalking the farther kob—and that both kobs knew this well before the human observer figured out that the lions were not going for the closest prey.
Prey animals also seem able to tell when predators are hunting and when they are bent on other business entirely, and adjust their flight distance accordingly. A wish to conceal weakness and difference—behavior resulting from fear or dislike of being scrutinized—could lead animals to take actions to avoid predation. They could pretend not to be weak, minimize their difference, or hide from the view of predators.
Predators are not the only creatures who might take advantage of an animal’s display of vulnerability or weakness. Animals of the same species are all too likely to be alert to signs of such weakness and to exploit them. When lions in the Serengeti were shot with anesthetic darts, some of the other lions took the opportunity to attack them (and were driven off by the researchers). Thus, shame might motivate animals to hide weakness from members of their herd or pack. If a caribou appears visibly weak or lame, it will be the first in the herd to be attacked by wolves, but the wolf who appears weak or sick may lose status in the pack. This can have serious consequences in terms of having offspring.
To survive, then, an animal must not only be fit, it must look fit. The sense of shame, painful to experience, may provide an emotional reason to hide infirmity.
Sickness and injury are often concealed. To the despair of animal breeders and veterinarians, many captive animals will diligently conceal all signs of sickness until they are too far gone to be saved. Birds are particularly adept at this, sometimes hiding all symptoms and enduring secretly until the moment when they literally topple from their perches.
Scottish red deer leave the herd when they become sick or are injured. At one time it was suggested that they did this for the good of the herd, but it seems probable that a lone deer is less likely to be spotted by a predator than a herd of deer—and if a herd of deer is spotted, then the sick or injured one is most likely to be the first animal attacked. If the deer recovers, it returns to the herd. If predators zero in on difference, not merely weakness, animals might feel vulnerable or ashamed of things that attract the gaze of others.
It might seem odd that shame could lead to blushing. At first glance it seems counterproductive for an animal to blush visibly or physically show embarrassment: it does not look good, and isn’t the objective to look good or at least not to stand out? The tingle of the blush could conceivably signal the blusher to hide (or give them something to hide), which serves the purpose of concealing the original weakness that the blusher was embarrassed about. Most animals do not blush visibly, if at all, so it may be that humans (some of us) do have a small claim to distinction in being the most visible blushers, even if we do not prove unique in feeling shame.
Pet owners often say that their cat or dog hates to be laughed at. Elephant keepers have reported that elephants who are laughed at have responded by filling their trunks with water and spraying those who are mocking them. It seems curious that animals that do not laugh might recognize and resent laughter. But perhaps laughter should be considered the equivalent expression of something they do feel themselves, and they are better translators than we are.
Guilt—feeling remorse for a particular act—can be trickier to pin down than shame. An action that carries overtones of guilt usually does so because our culture has informed us that it is wrong. Guilt is easily confounded with fear of discovery and subsequent disapproval or punishment. The chimpanzee Nim Chimp-sky, as we saw, was taught the sign for “sorry” and used it when he had “misbehaved,” just as Alex the parrot has said “I’m sorry” after biting his trainer. The examples of Nim’s misdeeds that are cited—breaking a toy or jumping around too much—do not seem to be things that a chimpanzee would naturally regard as bad. Like human children, he knew it was misbehavior only because he had been taught so. Sometimes Nim signed “sorry” before his teachers noticed what he had done. Whether Nim felt something other than the desire to avert possible wrath is unclear. On the other hand, this is often unclear in humans, as well.
Washoe’s adopted son Loulis was teasing Roger Fouts one day, “just being a pill,” and poked him harder than usual, cutting Fouts with his nail. “I made a big deal of it, crying and so on. Later, whenever I showed him that, to make him feel guilty, if you will, to use it to exploit that, he would squeeze his eyes tight and turn away. He would refuse to look at me whenever I tried to show him or talk about this old, old scratch that he had given me.” There are a variety of possible interpretations for this extraordinarily familiar behavior, but guilt is very strongly suggested.
Dogs are the most familiar guilty animal for most people. Desmond Morris has argued persuasively that dogs do feel remorse for their actions at times. When a dog that has committed some misdeed greets a human in an unusually submissive manner before the person has any reason to guess what has happened, Morris says, it cannot be getting cues from human behavior. “It has an understanding that it has done something ‘wrong.’”
Human shame has only recently been deemed a respectable field of study. Donald Nathanson recounts how, early in his career, he organized a symposium on shame. When it was over a friend took him aside, complimented him on the success of the symposium, and urged him not to do any more work on shame, lest he get a reputation for it. “It was in that moment that I learned that the very idea of shame is embarrassing to most people,” Nathanson says. These are emotions to be hidden. Perhaps animals have been successful in hiding them from our gaze.
If social animals feel guilt and shame, other animals might learn to take advantage of this. When a young chimpanzee makes a fool of itself, as Freud did in the incident recounted by Jane Goodall, it would seem possible for other chimpanzees to ridicule the young animal, to draw the attention of their companions to the situation, and to exaggerate their reactions. There does not seem to be any evidence that they do in fact mock each other this way, and if so, in this they differ from human animals.