The Ape And The Sushi Master Reflections Of A Primatologist

by Franz De Waal

  The monkeys strongly remind me of stumptails, those noisy, smelly, congenial macaques I worked with for many years. Throughout my studies, I contrasted stumptails with rhesus monkeys, the quick-tempered, pugnacious New Yorkers of the primate world. Rhesus have a despotic dominance style, which means that dominants harshly punish transgressors, fiercely compete over food and water, and rarely make up after fights. It is a very one-sided relationship, with the dominant having lots of privileges, the subordinate almost none. The stumptail, in contrast, shows a high tolerance level and great concern about the state of its relationships. Stumptails reconcile with former opponents through elaborate "hold-bottom" rituals and lengthy grooming sessions. In stumptail society, inequality is mitigated, and whatever status differences are left do not seem to stand in the way of good relationships.

  Tibetan macaques share a long list of characteristics with the stumptail. They walk in the same stocky, bearlike manner (stumptails are known as "bear-macaques" in Dutch and German), utter the same excited shrieks and squeals when they embrace each other, teeth-chatter in friendly situations, lock together after copulation, know sexual harassment,212 and have brightly white babies that contrast with the dark-brown adults. The calls of both species differ from those of other macaques, yet are so similar to each other that I would be hard-pressed to tell stumptails and Tibetan macaques apart by ear. With so many behavioral similarities, it would be surprising if they weren't closely related. Probably, their temperaments and dominance styles are alike, too.

  Infant Bridges

  There are also differences between stumptails and Tibetan macaques, however. The most fascinating one concerns those tiny white infants. Stumptails are extremely attracted to infants in their troop, which are easy to spot due to their juvenile coat, yet they never pick them up the way Tibetan macaques do. Only in the latter species do adult males use infants as passports to get close to one another. On one occasion, an infant squealed, drawing attention to itself, when it saw the third-ranking male appear from behind a rock. The male didn't hesitate to grab the infant and turn around to take it to the second-ranking male. He approached the other male with a wide grin on his face, holding out the infant for so-called "bridging."213 While one male held its arms and the other its feet, the infant was stretched between them at eye level, literally bridging the gap between two huge, teeth-chattering faces. The males seemed focused mainly on the infant, but also looked each other in the eyes. One male briefly sucked the infant's erect penis. Both resumed their activities afterward as if nothing had happened. The subject of all this tugging ran straight back to its mom, who had followed the scene from a safe distance.

  I had to rely on Li, of course, for the males' identities and hierarchy; it takes a long time to gather such knowledge. Even the most experienced primate watcher sees only half of what is going on when he first encounters a troop. Li explained how one immigrant male, who had reached alpha status upon joining the troop, lost his rank through a social mistake: he punished a juvenile. Immediately, four high-ranking males banded together in defense to chase him off, seriously attacking him. It was as if this quick victory taught the others "Hey, we can beat this guy!" From that day on, they gave low-level repeat performances of their triumphant action and remained on top. In an attempt to gain acceptance with his victors, the former alpha male became the most frequent user of an infant passport to approach them.

  The lowest-ranking male while I was there was also a former alpha who had lost one testicle in the fight that deposed him. This one-balled male hung around the periphery of the troop, unable to join the others at the provisioning site. The park wardens helped him out with separate feedings directly from their hands.

  Their occasional battles notwithstanding, I was struck by the extraordinary tolerance among males. To see six big, heavily armed males (they have long, sharp canine teeth) moving about close together, almost touching each other, while collecting attractive food was a sight to behold. Yes, these males vie over females and status, but they are also perfectly capable of toning down food competition, and most of the time they get along fine. To keep the peace, they engage in excited mounts and embraces, mutual grooming, and infant-bridging. Away from the feeding site, I saw males pass each other calmly, without the nervous glances commonly seen in other species.

  Apart from chimpanzees, I had never seen primate males so intensely involved with each other. In chimpanzees, too, males are at the same time rivals and friends, and I would argue the same for human males.

  Social Culture

  The first time I heard about Tibetan macaques was many years ago at a zoo that had acquired three "specimens" (zoo lingo for individuals). The species is virtually nonexistent in captivity, so I was anxious to see them. I was told that when the males masturbate (which they do in the absence of females), they produce an incredible amount of semen, ejaculating over great distances.

  This sounds true in view of Li's observations at Huang Shan. The large testicles, the number of times a male can ejaculate in succession, the visible sperm plugs in the vaginas after copulation, the tendency of males to manually remove the plugs of other males when inspecting a female all hint at sperm competition. That is, males compete over chances to fertilize females not only through physical combat but also by dispatching as much sperm as possible toward the ovum. The injuries I saw on some males, and the tense guarding of one female by the alpha male, made it clear that aggressive competition has far from disappeared. Still, sperm competition may have partially taken its place. Whenever natural selection favors large testicles over nasty temperaments, male bonds are permitted to grow closer. The survival value of such an arrangement is as yet unclear, but one speculation is that Tibetan males collectively defend their troop. Perhaps big cats once roamed these mountains, driving the monkeys to cooperation.

  Such an adaptationist explanation does not preclude a role of learning in male-male affairs. For example, it is hard to believe that infant-bridging is a simple instinct, shown by each and every Tibetan male regardless of experience. To carry an infant to another male and engage in this peculiar tete-a-tete may well require that a male has seen this behavior before, or participated in it as a youngster. Imagine a Tibetan male raised by a macaque species in which males totally ignore infants: would he still develop the bridging habit?

  I raise this question because it is often assumed that behavior shown by all members of a species cannot be learned or cultural. "Species-typical" has become synonymous with "biologically determined." While not denying that biology is involved, we usually don't exclude the taming of fire from the cultural domain simply because it has been achieved by every human society. Some cultural inventions come naturally to us, such as building roofs over our heads, performing marriage rituals, or developing a classification system for close kin. There are plenty of ubiquitous cultural products.

  Returning to macaques, there is one feature shared by all members of this genus: the matrilineal hierarchy. As opposed to migratory males, females remain in their natal troop all their lives, forming stable, kin-based networks between mothers, daughters, granddaughters, sisters, and nieces. It is termed a hierarchy because the rank of each female derives from this network. Since its discovery by Japanese primatologists, hundreds of studies have shown how the future rank of a young macaque female can be predicted on the basis of her mother's rank. Females with relatives in high places are born with a silver spoon in their mouth, whereas others spend all their life at the bottom, being born to a lowly matriline.

  Despite its apparent rigidity, however, the system depends on learning. Early in life, the young female finds out against which opponents she can expect help from her mother and sisters. When sparring with peer A she may utter a barely audible squeak and yet receive massive support to defeat her. But against peer B she can scream her lungs out and nothing happens. Obviously, the young female will seek more and more confrontations with A-or A, who is equally smart, will learn to avoid her-whereas she will become
very careful with B, who eventually will rise above her in status.

  It is not that daughters of high-ranking females have blue blood; they are not inherently superior. Through adoption, for example, one can turn the infant of the lowest female into a successor to the throne, provided she is raised by the alpha female. Other experiments have manipulated the presence of family members and found that with dwindling support dominant females are unable to keep their positions.214 In other words, the hierarchy is maintained for generation after generation through social rather than genetic transmission.

  In my own work, I discovered that the same holds for social ties among female macaques. Together with my assistant, Lesleigh Luttrell, I closely followed the development of a large cohort of rhesus infants for many years, until they reached adulthood. We found that daughters copy their mothers' association preferences. Even when they have grown fully independent, and are approaching motherhood themselves, they spend much time with the daughters of their mothers' best friends.215 Thus, the friendship between two of our females, Ropey and Bizzy, led their daughters, Robin and Bubbles, to become good friends as well.

  We don't know exactly how friendships are being transmitted across the generations, but the simplest way I can think of is that when the mothers, Ropey and Bizzy, sat down to groom and relax, Robin and Bubbles would take the opportunity to play nearby. Being playmates early on, these youngsters then developed an association for the rest of their lives.

  Given these processes, imagine that females in a particular group begin to strengthen ties outside their own families. Over time, such a trend will become more and more deeply embedded because their daughters will start doing the same.216 Similarly, if mothers increasingly focus their attention on a narrow circle of kin, this will restrict the contact range of their offspring as well. If differently structured social networks are being transmitted, we may speak of different social cultures.

  So, even though the matrilineal hierarchy is a universal feature of macaque society, it is not purely inborn. Based on natural abilities and tendencies, the arrangement endures because it is passed on by nongenetic means from mother to offspring: it is a "cultural natural."217 Young monkeys are quick learners when it comes to kinship, friendship, support, and inequality, and then employ all of this knowledge when finding their place in society.

  Improved Monkeys

  My earlier suggestion of letting a Tibetan male grow up with a different macaque species is not as wild as it may sound. Two cross-species experiments have been conducted-one in the field, the other in the laboratory-with enlightening results.

  Hans Kummer once captured female hamadryas baboons in Ethiopia only to introduce them to a wild troop of savanna baboons living in the same region. These two kinds of baboons have strikingly different societies. Kummer spent a lifetime documenting the social organization of hamadryas baboons, in which males herd a small number of females by delivering a neck-bite whenever they stray. Calling these brutal arrangements "marriages" (a shocking choice of words for a scientist who has chided others for anthropomorphism), Kummer wondered about the contribution by each sex. This is why he released hamadryas females near a troop of savanna baboons, a species that has none of this harem business. Here is what happened:

  Although no male took possession of them, each of them attached herself to a particular anubis male and groomed him. But when the female noticed that she was neither herded by the selected male nor protected from other group members by him, she behaved as freely as her savanna baboon ancestors must have done before the evolution of marriage.218

  Hamadryas females apparently love freedom, which must mean that the social organization typical of their species is imposed upon them by the males. Conversely, when Kummer released savanna baboon females near a hamadryas troop, these females were quickly claimed by males, who trained them to stay close. The females learned that in order to avoid neck-bites, they had to act like hamadryas females, who never leave their master. They acquired this habit in a very short time, often within an hour, but never as perfectly as their hamadryas sisters. Lack of motivation to stay with a single male made them break the rules: ". . . the anubis females made life hard for their husbands. After days together they still had to be herded so often that their males finally gave up and let them go." As a result, the anubis females never achieved full integration in hamadryas society.

  In another attempt to gauge the role of learning, I myself mixed rhesus and stumptail monkeys. Juveniles of the two species were placed together, day and night, for a period of five months. Having described this experiment before, here I will just mention its most conspicuous result. The rhesus monkeys, normally a quarrelsome, nonconciliatory bunch, developed peacemaking skills on a par with those of their more tolerant counterparts. Even after permanent separation from the stumptails, the rhesus showed three to four times more friendly reunions and grooming after fights than is typical of their species.219

  Our new and improved rhesus monkeys demonstrate the power of social learning. True, all macaques know reconciliation, but at the same time the behavior is an acquired social skill. How could it be otherwise with animals that take four to five years to mature? A slow development leaves ample room for the environment to exert its influence. Similarly, even though all hamadryas baboon troops show the typical harem structure, it is the product of learning. Females of this species respond to social rules enforced by the much larger males.

  Primates thus form cultures in which social arrangements are taught and acquired. Most of the time we barely notice the degree to which this happens, except when we mix species, switch infants, or create new environments. Sometimes, however, cultural developments result in dramatic differences between groups. For example, the Wisconsin Primate Center used to keep two large rhesus groups in identical enclosures. When I worked there, I could see, side by side, one group in which males fiercely competed every mating season and another group in which they did not. In the first group, the alpha male would not allow any other male in his sight to mount a female. This didn't stop the other males from mating; they seized every opportunity when the old leader had his back turned. Other high-ranking males were equally intolerant, however, prohibiting matings by males below them.

  In the other group, five adult males might each be consorting with a female in plain view of the others without any interference. Of course, the alpha male had first pick, but he tolerated the others' sexual activity. Both groups had many more females than males, so the difference cannot be attributed to the relative availability of females.

  I studied these groups for a decade, and the contrasting male relations persisted despite changes in the hierarchy. Probably, young males growing up in each group received quite contrary lessons about how to act during the mating season.

  The Welcome Tree

  Cultural naturals defy the traditional dualism between culture and nature. They are not cultural products, in the strict sense; nor do they conflict with biology. Thus, the matrilineal hierarchy of macaques arises automatically out of natural tendencies, such as the inclination to support kin, but these tendencies need to be supplemented with learning; otherwise a stable structure can never emerge. Similarly, the human incest taboo, long held up as a prime example of our ability to subjugate nature, is now considered a cultural fortification of a natural tendency. Like many animals, people tend to avoid sexual relations with individuals with whom they grew up. The universality of the incest taboo reflects a happy marriage between nature and culture.22°

  Cultural naturals are not to be taken lightly. Although the role of learning may create the illusion of flexibility, it is impossible for our species to get around certain cultural institutions. In the same way that communism floundered because it went against human economic nature, rules against stable family arrangements tend to backfire. The hippie communities of the sixties, based on a denial of sexual jealousy, evidently didn't last. And attempts to break the oldest mammalian union, the mother-child bond, have been
equally unsuccessful. The kibbutzim in Israel have largely abandoned their communal child-rearing practices in recognition that parents and children belong together. And after a flirtation in U.S. maternity wards with purely physical medical care and incubators-resulting in the swift removal of newborns from their mothers lest they might catch infections-there is now a growing awareness of the importance of early body contact and attachment: "After a period of about ninety years during which that bond was ignored, dismissed, shattered, and fully re-examined `scientifically,' Western culture has now returned to accepting that babies and mothers are a natural pair."22'

  I had to think of the importance of family arrangements, including the human pair-bond, when visiting Huang Shan. Somewhere on the tallest mountain there is an ancient, knotty tree, a member of Pinus hwangshanensis (the pine tree of this region), which is so familiar in this nation of a billion people that when foreign dignitaries visit they are often photographed in front of a large watercolor of the tree.

  The image behind them does not show the tree species in general, but this particular tree, known as the "Welcome Tree." The poor old pine is propped up by a metal frame so that it can serve for another century. Approach to the tree is obstructed by heavy chains, weighed down by thousands of padlocks. No lock on the chain is single. All of them hang in pairs, each pair permanently hooked together. Chinese lovers and newlyweds visit this site, link their padlocks together, then throw the keys down the mountain.

  Their gesture may not be universal, but it is universally understood. The large number of customs that people don't need to explain to members of other cultures indicates how much our societies are constructed around a shared humanity.