Monkey business: do the quirks of capuchins make them creatures with culture?

It's not easy keeping up with pint-size monkeys in the jungle. The teams of researchers who've been doing it for the past 14 years have had to put up with a lot: barreling face-first into spider webs before sunrise, hacking through dense, bug-infested undergrowth, getting droppings in their hair, and being heckled by cantankerous little monkeys called capuchins. Still, there's no place Susan Perry would rather be than the forests of the Lomas Barbudal Biological Reserve in Costa Rica.

Perry is a primatologist at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany, and she's been studying white-faced capuchins (Cebus capucinus) at Lomas Barbudal since 1990. Each day in the field, she and her colleagues get to observe these monkeys' curious interactions, some of the quirkiest behavior in the animal kingdom.

For example, one game begins when one monkey bites a clump of hair from another monkey's face. The two monkeys use their teeth to pass the clump back and forth, dropping a little hair each time. When the hair runs out, the game begins again.

In another unusual duet, two monkeys sit together for long periods, swaying gently--with their fingers up each other's nose.

These are among the numerous social conventions that Perry and her colleagues call "traditions." The behaviors are so named because they don't appear to be an inherent part of the animals' biology; instead, the knee-high monkeys seem either to invent them or to learn them from each other.

Perry also observed that only certain individuals in certain cliques practice the behaviors. Moreover, the activities aren't necessarily perennial: They endure for various lengths of time and can be modified in the life of a monkey troop. They can become fashionable, fall out of use, and return some years later.

Innovative, learned, parochial, transient, flexible--these words describe some of the hallmarks of cultural behaviors, as set forth in numerous studies of nonhuman primates. Does this make capuchins a species with culture, as many researchers suggest that chimpanzees and other great apes are (SN: 6/19/99, p. 388)? And what do the strange high jinks mean to the capuchins?

ONE SMART MONKEY Perry and her colleague Joseph Manson, a cultural primatologist at the University of California, Los Angeles, decided to study capuchins in part because these feisty creatures have the highest brain-to-body-size ratio of any primate other than people. "I was interested in finding out what they were doing with these big brains," says Perry, who also has a position at the University of California, Los Angeles.

Their study is the first detailed observation of capuchins' social lives. In the April 2003 Current Anthropology, Perry, Manson, and their colleagues published their analysis of the monkeys' social behaviors. It's based on data collected over 13 years.

They had tracked 13 capuchin troops in four nature reserves, including Lomas Barbudal. Each troop contained 15 to 38 monkeys and had more females than males. More than half of each group was made up of juveniles. "Because they live in multimale, multifemale groups, they have a lot of potential for politics" Perry explains.

The groups selected were geographically close enough to each other to ensure only limited genetic variation from group to group, but they were far enough away so that they didn't ordinarily mix. By comparing notes, the researchers following different troops could check which behaviors were unique to their group. And within groups, they could trace the rise and fall of different behaviors.

"The most important aspect of a tradition is that it's transmitted to new practitioners via social learning," Perry explains.

In all, she and her colleagues nominated five conspicuous, lasting behaviors to be considered as social traditions in the monkeys. All of them were playful activities: the hair-in-mouth game; the fingers-in-noses pastime, which the scientists call hand-sniffing; the sucking of a companion's body parts, such as fingers, tails, or ears; a finger-in-mouth game; and a game in which a pair of monkeys use their teeth to pass an object, such as a stick or pebble, back and forth.

"We arbitrarily set a 6-month minimum for a behavior to be considered a tradition," Manson says. "This was a conservative cutoff to be sure that we didn't count as traditions behaviors that were tried only once or twice by a very small number of individuals."

When Perry started following her group, some of the capuchins were already practicing hand-sniffing. After grooming each other, the monkeys would stick their fingers up each other's nose, sometimes poking each other in the eye while doing so. They would then sit together, swaying gently, in what appears to some observers to be a trancelike state. The capuchins "have very long fingernails, and it's probably not very comfortable" Perry says. And having a finger in its nose can make a monkey sneeze. When that happens and a finger is ejected, the partner puts its finger back in place, and the pair continues swaying.

The researchers noticed the hand-sniffing behavior in different monkey groups and often with different practitioners. In some groups, all pairs were females; in others, all were males. "In one group, hand-sniffing faded out and then years later came back in, being performed by different individuals," Manson say.

In another type of behavior, monkeys lie side by side and suck on each other's tail. In a novel iteration of this social convention, one monkey would sit on another's head, and the monkey underneath would suck the top monkeys tail while giving the partner a foot massage. Once a pair of capuchins figured out a configuration they liked, the behavior became routine. Various monkeys have independently invented "funny little mutations of these behaviors," Perry says.

Finally, there's the game in which one monkey keeps another monkeys finger firmly gripped in its mouth. The trapped monkey uses its feet and other hand to pry open the captor-monkey's mouth and free the finger. "It's a very slow, methodical, relaxed interaction," Perry says. "They're working hard at getting the mouth open, but not in a frantic way. It's more like they're solving a puzzle."

TESTING THE BONDS What's behind all this curious conduct? Barbara Smuts, a psychologist and anthropologist at the University of Michigan in Ann Arbor and author of the book Sex and Friendship in Baboons (1999, Harvard University Press), says that the games are a form of social negotiation--a way for the capuchins to cheek where they stand with their cohorts.

"Play can establish a special context for individuals to negotiate their relationship with little risk of injury," she says.

But, Smuts points out, the capuchins' games have an edge. They all cause the monkeys some physical discomfort. Perry and Manson say that feature is important to understanding why these particular behaviors occur. The giver imposes stress on a receiver and then evaluates how well--or how badly--the latter reacts. In this way, the pair tests the bond between them.

This is, in fact, an old hypothesis about animal interactions--one put forward by biologist Amotz Zahavi of Tel Aviv University in 1977. "Zahavi's idea hasn't gotten much attention, which I don't understand, because it probably accounts for a lot of social behavior in animals; Manson says.

"Different groups develop different rituals that tell them about their relationships, and the general principle in these rituals is that they impose a cost," Zahavi explains. He cites an example from a bird species, Arabian babblers (Turdoides squamiceps), which he's studied for the past 33 years. "When birds come together for the first time, the male wants to be sure that the female is really coming to stay with him; he explains. "The simplest way to do it is to be aggressive. And if she stays, he knows she's serious."

Commenting on Perry and Manson's work, Zahavi says that the kind of aggressive testing he first described in birds probably motivates the capuchins' often-peculiar social interactions.

Smuts and her colleague John Watanabe of Dartmouth College in Hanover, N.H., described something similar in their 1990 and 1999 studies of baboons. The researchers theorized that male baboons are testing each other with their risky greetings: such effrontery as grabbing each other's testicles or mounting one another. Baboons that had successful encounters were more likely to team up later and act aggressively toward other baboons (SN: 4/29/00, p. 280).

"The greetings gave males a context for communicating about their relationships--a fairly neutral context set apart from the rest of their interactions, such as aggressive competition for a mate, Smuts says. A baboon presenting its genitals makes itself vulnerable, indicating a willingness to cooperate with a potential rival. The purpose of this kind of approach is "not to compete but to greet," Smuts says. What's acceptable in a greeting, however, would be dangerous in a competitive interaction.

Smuts argues that the baboon greeting behavior is similar to what the capuchins do. For a capuchin, consenting to having a cohort's finger up its nose is a good indication that the pair is on friendly terms. Perry predicts that such an affiliation will make it more likely the animals will later band together to make trouble for fellow group members or other animals.

Primatologist Card van Schaik of Duke University in Durham, N.C., says he hasn't seen "anything remotely similar to this in orangutans. But maybe we shouldn't expect it." Because different species have different social systems, observers must anticipate great variations in social behavior.

Nevertheless, there may be a human analog to some of the capuchin behaviors. "For lots of things that humans do, we expect to find precursors in animals," says Cheryl Knott, a primatologist at Harvard University.

Perry suggests that some young men's greeting ritual of roughing each other up might function as some of the monkeys' behaviors do.

CULTURE VULTURES? "One of the salient aspects of human culture is that a lot of cultural traditions have to do with negotiation of social relationships," Perry says.

Yet few studies of nonhuman primates have focused on such social traditions, commented Kevin N. Laland of Scotland's University of St. Andrews in a review accompanying Perry's 2003 report.

Instead, studies have focused largely on technology, such as tool use and foraging techniques, as evidence of culture. "What differentiates the [capuchin] traditions from most of the behaviors described for other nonhuman primates is that their proposed function is in the social realm rather than the material realm," Smuts says.

The landmark summary of cultural variation in chimpanzees appeared in 1999. Andrew Whiten, also of the University of St. Andrews, and his colleagues summarized data from a total of some 151 years of chimp observations at seven sites in Africa. Most of the 39 behavior patterns they listed had to do with variations in tool use, such as employing sticks to gather and eat ants (SN: 6/19/99, p. 388).

In 2001, however, William McGrew of Miami University in Oxford, Ohio described variations in an exclusively social custom among chimps. He analyzed a difference in the grooming activities of two chimpanzee groups. In one group, each chimp in a grooming pair would extend an arm overhead, and the pair would clasp hands. In the other group, grooming partners didn't clasp hands.

McGrew and his colleagues called these behaviors aspects of chimp "culture." But other researchers said that culture was too sophisticated a term to apply to such behaviors.

Manson and Perry try to avoid the whole debate. "Part of the reason why we don't use the word culture and [instead] call the behaviors 'traditions' is to sidestep the whole definitional argument and focus attention on the phenomena themselves--on their biological significance," Manson explains.

Whatever you want to call them, the behaviors are learned, Knott says. Animals develop ways of interacting, and the new behaviors that they exhibit get passed on." She agrees with Manson and Perry that this is what appears to be happening in the capuchin troops.

Knott suggests that there could be some sort of gradient of cultural behaviors across primate species. "I don't think that traditions start in the great apes" she says. "That's just the first place people start looking for them outside of humans."

However, she points out some differences between capuchin and ape traditions. For example, ape traditions often persist across generations and so are generally longer lasting than those of capuchins. Knott notes that researchers have already found species differences even among the great apes, such as more elaborate tool use in chimpanzees than in orangutans.

When it comes to social behavior, Smuts says that, so far, capuchins seem to be showing the greatest creativity among nonhuman primates. However, Manson says, "I'd be very. surprised if capuchins were highly unusual in this regard."

Smuts argues that the social realm is "really ripe for investigation." Manson agrees, and says he expects that researchers will now "start looking more at traditions in the area of social interactions."

RELATED ARTICLE: Mischievous monkey: cranky or cuddly? The many faces of the white-faced capuchin.

White-faced capuchins (Cebus capucinus) are a common species in forests from Honduras to Colombia. Widely regarded as the most intelligent monkeys in the Americas, capuchins get their name from Capuchin monks, an Italian order founded in the 1500s. The black, caplike section of hair on the monkeys' heads looks like the hood that those monks wore, but the resemblance stops there. The monks' solitary austerity was the antithesis of the rambunctious monkeys' way of life.

"They're really feisty, obnoxious animals. You don't want to mess with them," says Susan Perry of the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany. The limber, knee-high capuchins tend to gang up and pick fights with creatures that far outweigh them, including cows and people.

In a straight-up guide for prospective field workers on the capuchin project, Perry warns her new colleagues to steel themselves for some of the monkeys' behaviors. "You need to be able to stomach the sight of monkeys eating their cute, charismatic prey alive while the prey scream for help," she says, Among the victims are small vertebrates like squirrels, birds, and lizards--part of the omnivorous capuchins' diet.

Capuchins do have a sweet side. They're highly cooperative, indulging in mutual grooming sessions during periods of relaxation. They also act as surrogate parents, often nursing other monkeys' offspring, protecting them from predators, and ferrying infants across large tree gaps.--S. MCDONAGH