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Do the quirks of capuchins make them creatures with culture?

Sorcha McDonagh

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 says.

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 monkey's 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 monkey's 
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 check 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: Available to subscribers 
athttp://www.sciencenews.org/articles/20000429/bob8.asp).

"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 Carel 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."

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.