Assignment
In the Minds of Monkeys
What do they know--and do they know they know it?
It was early morning, and the vervet monkeys had moved out of their yellow-barked acacia sleeping trees to forage on the open plains of the East African savanna. While the adults fed, the juveniles played in a nearby bush. Macaulay, the rambunctious son of a low-ranking female, wrestled Carlyle, the juvenile daughter of the highest-ranking female in the group, to the ground. Carlyle screamed, chased Macaulay away, and went to forage next to her mother. The fight had lasted no more than a few seconds, but it had not gone unnoticed: twenty minutes later, Shelley, Carlyle's sister, approached Austen, Macaulay's sister, and without provocation bit her on the tail.
This kind of anecdote sets the stage for the typical article on nonhuman primates. Read any description of a long-term study of monkeys or apes and you will find an account of complex kinship networks, friendships, struggles for dominance, and shifting alliances. For most human observers, what makes these animals so fascinating is their social structure, which often seems as rich and complex as our own. When we read Shakespeare's account of the blood feud between the Capulets and the Montagues, we take it for granted that the members of these two families had a well-developed sense of their own and other peoples' social relationships. If they didn't, there would have been no feud and no ironic or tragic elements to Romeo and Juliet's romance. Monkeys, like Shelley in the anecdote above, apparently also recognize relationships in families other than their own, and they use this knowledge to retaliate against their opponents. For monkeys, as for humans, the enemy of my kin and the kin of my enemy are my enemies too.
Highly social creatures, monkeys and apes have often impressed observers with their ability to predict the behavior of other animals and to recognize their relatives and allies. This has led some scientists to speculate that primate, including human, intelligence originally evolved to solve social problems. According to this theory, natural selection has acted with particular force in the social domain, making monkeys and apes especially sensitive to the behavior and relations of others.
But what sort of social knowledge really exists in the minds of monkeys? How is their intelligence similar to our own, and how is it different? For the past thirteen years, we and our colleagues have attempted to tackle some of these questions by studying the East African vervet monkey in Kenya's Amboseli National Park. Vervets are members of the largest family of Old World monkeys, which includes baboons, macaques, and many forest-dwelling monkeys, and they are among the most common primates in sub-Saharan Africa. As primates, they are relatives of ours, but they are by no means our closest relatives. Humans and chimpanzees, for example, seem to have shared a common ancestor only 5 million years ago, while the common ancestor of Old World monkeys and humans lived roughly 20 million years ago.
In Amboseli--an arid savanna woodland punctuated by swamps at the foot of Kilimanjaro--vervets live in groups of ten to thirty monkeys that include anywhere from one to eight adult males and two to eight adult females. As in other Old World monkey societies, females remain in their natal groups throughout their lives, maintaining close bonds with their matrilineal kin; males transfer to neighboring groups at sexual maturity. Social life in the group is far from democratic. Each male and female occupies a specific rank, dominating all those further down the ladder. Offspring assume their mother's rank, so the dominance hierarchy is in fact a hierarchy of families, with all the members of family A outranking all the members of family B, and so on down the line. Even a male assumes his mother's rank until he migrates to another group. After that, a male's rank depends on more subtle factors, including fighting ability, age, and his acceptance by his adopted group's adult females.
While each vervet female inherits her high or low status, this does not mean that she accepts her lot in life without protest. Quite the contrary. Vervets, macaques, and baboons are--it must be said--dreadful social climbers. They constantly compete for the opportunity to groom highranking females, sit near them, and play or groom with their infants. Animals that groom together also tend to feed together and form alliances, and high-ranking females have access to the best food,the best resting places, and win almost all the disputes they enter. By establishing a close bond with a high-ranking female, low- and middle-ranking females may be able to enjoy some of the benefits of high rank, even if they never actually increase their status. In sum, vervet monkeys--like characters in a Jane Austen novel--organize their lives around two principles: to maintain close bonds with kin and to establish good relations with the members of high-ranking families.
Time and time again, we have seen the practical value of alliances. In a typical encounter, one female, Newton, may lunge at another, Tycho, while competing for a fruit. As Tycho moves off, Newton's sister Charing Cross runs up to aid in the chase. In the meantime, Wormwood Scrubs, another of Newton's sisters, runs over to Tycho's sister Holborn, who is feeding sixty feet away, and hits her on the head. Hostility between two animals often expands to include whole families, so not only must monkeys predict one another's behavior but they must also assess one another's relationships. A monkey confronted with all this nonrandom turmoil cannot be content with learning simply who is dominant or subordinate to herself; she must also know who is allied to whom and who is likely to aid an opponent.
We tested the vervets' ability to recognize the kin relations of others by playing the scream of a two-year-old juvenile through a concealed loudspeaker. The subjects for each experiment were three females, one of whom was the juvenile's mother. In a typical experiment, we would play the scream of Emerson to three females: Teapot Dome (Emerson's mother), Profumo, and Suez. Our original purpose was simply to determine whether or not mothers recognized their offspring's screams. But when we analyzed the films of the playback experiments, we found that the screams often caused the other two females to look at the mother. It was as if they were thinking, "That scream goes with Emerson, and Emerson goes with Teapot Dome. What's she going to do about it?"
Humans, obviously, do more than simply recognize the relationships of others; we also compare different sorts of relationships, classifying them and giving them labels that are independent of the particular individuals involved. When a friend mentions a sister or a lover, images of a particular type of relationship are conjured up in our minds, even if we have never met the person being discussed. Monkeys don't have words for particular types of relationships, but they do seem to evaluate and compare one another's social relationships. Vervets apparently recognize parallels between their own kinship bonds and those of others. A fight between Carlyle and Macaulay increases the probability that Carlyle's relative will later threaten Macaulay's relative.
While monkeys may know a lot about one another's social relationships, they seem to know much less about one another's minds. Consider deception, for example. Among humans, successful deception demands that the liar identify what another person believes to be true and then attempt to hide or falsify relevant information. In other words, the liar must recognize the distinction between his or her own beliefs and the beliefs of others. Many animal species, including insects occasionally give false signals to others, but these signals are typically inflexible and occur only in a narrow range of contexts. Male scorpion flies, for instance, sometimes steal dead insects from other males by mimicking the behavior of a female, but as far as we know, they never attempt to deceive one another in any other context or in any other way.
Monkeys and apes, in contrast, attempt to hide or falsify a variety of signals and patterns of behavior, and they do so in a variety of contexts. For example, dominant male vervet monkeys often chase subordinate males from sexually receptive females. To counteract this tactic, a subordinate male will lead a female behind a bush or tree, out of sight of more dominant males, before attempting to copulate with her. Nevertheless, monkeys' lies often seem oddly incomplete. To cite one example, when vervet males spot a leopard, one of their primary predators, they give loud barking alarm calls that cause other vervets to run up into trees for safety. Most of the monkeys' alarm calls are reliable, signaling the true presence of a predator. Over the years, though, we have observed cases in which a male gave apparently false alarm calls just as a new male was attempting to transfer into his group. Normally, males are hostile to solitary males that approach their groups, since such males are almost invariably migrants in search of a group to join. Resident males are not always successful, however, in driving away these migrants, particularly when the migrants are younger and stronger than themselves. The primary perpetrator of false alarm calls during our study was Kitui, a perpetually low-ranking male that could reasonably have expected to become subordinate to any rival that successfully transferred into the group. Kitui's false alarms were effective because they caused his rival to run up into a tree and prevented him from approaching the group.
So far, so good. The alarm calls appeared to be deceitful, signaling a danger that Kitui, but not the rival, knew to be false, and they kept the rival temporarily at bay. But was Kitui actually trying to make his rival believe a leopard was nearby?
We can never know for certain what goes on in the mind of a monkey when he gives an incorrect alarm call. Even if the call functions to mislead, it may not be at all appropriate to conclude that the signaler attributes mental states to others. Here the issue becomes murky, because Kitui's subsequent behavior was often puzzling. As if to convince his rival of the importance of his calls, on three occasions Kitui left his own tree, walked across the plain in full view of the imaginary leopard, and entered a tree next to his rival's, alarm calling all the while. He seemed to have gotten only half the story right: he acted as if he knew that his alarm calls caused others to believe there was a leopard nearby, but he didn't seem to realize that he should behave as if he also believed in the leopard.
Numerous psychological studies have demonstrated that, like Kitui, young children also have difficulty in distinguishing their own knowledge from that of others. As any parent of a small child will readily attest, children cannot easily recognize or create false beliefs in others. Perhaps this iswhat makes them such poor liars. A child of three will deny having been to the cookie jar when there are still telltale crumbs on his or her face; only later do children learn to wipe the crumbs off before pleading innocence.
Other anecdotes are equally difficult to interpret. Subordinate female baboons often raise their tails when approaching or interacting with more dominant animals. Raised tails seem to reflect anxiety and are usually accompanied by other signs of subordination, such as grimacing or presenting the hindquarters. In an earlier study of baboons, we once watched a female attempt to suppress this sign of subordination. The female, known to us as the Lady from Philadelphia, was attempting to follow her daughter on a narrow rock ledge, and the path led her within two feet of the resting place of the group's dominant male, Rocky. As she approached Rocky, the Lady from Philadelphia's tail began to rise. Looking back at her tail, she pressed it down and held it until she had passed him, as if she recognized that her raised tail would reveal an anxiety she wanted to conceal.
Watching this behavior, we were tempted to conclude that the Lady from Philadelphia was aware of the distinction between her actual state of mind and the state of mind she wished to convey to Rocky. Even if her actions represented a true deceptive tactic, her behavior was difficult to interpret, at least for human observers. Didn't she realize that by pushing her tail down in full view of Rocky, she was less likely to fool him? Or was Rocky's ability to detect deception also so incomplete that it didn't matter how conspicuous her act of deception was?
Many anecdotes suggest that apes may be better than monkeys at attributing beliefs to others and at recognizing the effects of their own behavior on others. To give one example, Luit and Nikki, two adult males in a captive group of chimpanzees studied by Frans de Waal, were engaged in a prolonged struggle for dominance. During one fight, Luit chased Nikki into a tree and then took up a position of vigilance at its base. As he sat, Luit began to bare his teeth in a nervous "fear grin"--a sign of anxiety. Quickly, Luit turned his back to Nikki, put his hand over his mouth, and pressed his lips together, apparently to hide this sign of submission. Only after three attempts, when he had succeeded in wiping the fear grin from his face, did Luit turn to face Nikki again. Luit's actions suggested that he was aware of his nervousness, of the external manifestation of his fear, and of the need to hide this sign from his rival. Luit appeared to be attempting to manipulate Nikki's beliefs, but until definitive experiments are designed to test this hypothesis, simpler explanations are also possible. For example, Luit might have learned that whenever he showed a particular facial expression, Nikki chased him.
Many observers have suggested that nonhuman primates seem to show much greater intelligence when manipulating one another than when manipulating objects. According to this "social intelligence" hypothesis, the reason that monkeys in the laboratory can be taught to classify objects according to some criterion, such as color or shape, is that they do this sort of thingnaturally in the context of social interactions: placing objects X, Y, and Z into a particular class comes easily to animals used to classifying one another as members of different matrilines. Similarly, when monkeys solve problems of transitive inference in the laboratory (if A is bigger than B, and B is bigger than C, then A must be bigger than C), they are merely duplicating an ability they use daily in assessing other animals' dominance ranks.
The idea that a given ability may be manifested more in one context than in another is not new. Many food-caching birds, for instance, exhibit striking spatial memory when it comes to finding seeds, but it is not clear whether they extend this ability to nonforaging contexts. Similarly, although the honeybee's dance conveys extraordinarily precise information about the location, direction, and quality of food, honeybees do not seem to use their dance to communicate, for example, about their nest mates.
Do monkeys in fact exhibit more skills in social interactions than in nonsocial contexts? Our investigations are still preliminary, but they suggest that vervets sometimes show surprising gaps in their knowledge of the external world. Consider the monkeys' understanding of their predators. In Amboseli, predation accounts for more than 70 percent of all vervet deaths. The monkeys are preyed upon by leopards, smaller cats, martial eagles, pythons, and baboons. In some respects, the vervets have an impressive battery of responses to these many predators. They have at least six acoustically different alarm calls for these different classes of predators, and each type of alarm call evokes a different escape response. The loud, barklike leopard alarm call, for instance, causes monkeys to run up into trees, while their more gruntlike eagle alarm call causes them to look up into the air.
Vervets also recognize the various alarm calls of other species. The superb starling, one of the most common bird species in Amboseli, has two distinct alarm calls: one for terrestrial predators (including vervets, which steal their eggs); the other for hawks and eagles. When we played recordings of starling alarm calls to vervets, we found that the monkeys responded appropriately: the starling's terrestrial predator alarm call caused the monkeys to run toward trees, while the starling's eagle alarm call caused them to look up into the air.
In contrast to their skill at recognizing the alarm calls of other species, however, vervets seem remarkably poor at identifying the many kinds of visual cues left by predators. Leopards, for example, are the only predators that cache carcasses in trees, and vervets invariably alarm call when they spot a leopard in a tree with a carcass. Nevertheless, the monkeys show no sign of anxiety or increased vigilance when they spot a carcass in a tree in the absence of a leopard; they never seem to realize that a carcass in a tree may mean that a leopard is nearby.
Vervets are similarly blind to visual evidence of pythons. These snakes hunt vervets by lying in wait for them in bushes or at the base of trees. The snakes leave straight, wide tracks(reminiscent of a wide-wheeled bicycle) that cannot be mistaken for those of any other species, and humans quickly learn to avoid bushy areas where there are fresh python tracks that haven't yet been disturbed by wind or other animal footprints. The vervets, though, never seem to learn that a python track denotes the proximity of a python. We have often watched in utter mystification as a vervet monkey walked calmly into a bush to feed, ignoring the python track that led directly into it, only to leap away in shocked horror when it encountered the snake there.
Finally, vervet monkeys flee from Masai herdsmen and their cattle, and they also respond to the mooing of cows and the ringing of cowbells with vigilance and flight. Nevertheless, they don't seem to recognize the distinctive clouds of dust that herald the approach of cattle and Masai. Livestock herds produce thick, dense clouds of dust that are readily distinguished (at least by humans) from the more diffuse dust clouds produced by zebras, wildebeest, and elephants. Day after day, however, the monkeys will sit impassively in the midst of the livestock dust clouds, only to give surprised alarm calls when the cows invariably emerge.
Why should vervets fail to recognize the visual evidence of predators? One possible explanation may be that visual and auditory cues first evolved to deal with social problems. Vervets do use visual signals in face-to-face interactions with other monkeys but do not respond to visual evidence of an absent object or individual. They do not, for example, follow one another's tracks when foraging, look for the tracks made by other groups when patrolling a territorial boundary, or visually alter aspects of their physical environment to denote rank or group membership. Auditory cues, in the form of their many vocalizations, however, are abundant in these sorts of situations. Monkeys frequently call when out of sight of one another. If monkeys are foraging in dense brush, a vocalization is enough to signal that a dominant animal is approaching or another group has been spotted. In the social context, vervets may never have needed to recognize that a visual cue can denote some absent object or individual. Perhaps as a result, when they confront a python's tracks or a carcass in a tree, the monkeys do not make the connection between these objects and the predators that put them there.
Apes may be better than vervet monkeys at recognizing the visual cues left by other animals. In the wild, for instance, chimpanzees make sleeping nests each night. When the members of one group make raiding patrols into the range of another group, they sometimes give aggressive displays upon encountering their neighbors' empty nests. It would be interesting to determine if chimpanzees were better than vervets at recognizing the visual clues left by predators. The superior performance of chimpanzees in many laboratory tests does suggest that their intelligence may be less constrained and less context specific than that of monkeys.
One of the most important features of human intelligence is our ability to take a skill we have acquired in one context and extend, or generalize, it to another. Humans can use analogical reasoning not just to evaluate the similarity between our own and other people's familiarelationships but also to recognize, for example, that cat doors and the valves of a heart operate according to the same general principles. One of the primary distinctions between our intelligence and that of other primates may lie not so much in any specific skill as in our ability to extend knowledge gained in one context to new and different ones.
Answer the following seven questions.
1. What is the dental formula of vervetmonkeys (hint: what kind of primate are they)?
2.Since vervet monkeys and humans last shared a common ancestor 20 million years ago, do you think primatologists can learn useful information about human behavior and intelligence from studying them?
3.Describe vervet monkey social structures. Why do vervet monkeys need to keep track of so many other individuals and their relationships? How do they use vocalizations to do this?
4.What are several ways primates use deception?
5.Define the social intelligence hypothesis. Why are monkeys better at manipulating each other than objects?
6.What are vervets better at - interpreting visual information about predators, or auditory information about predators? Why?
7.What distinctions do the authors draw between human and non-human primate intelligence?