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Thinking Like a Monkey

What do our primate cousins know and when do they know it? Researcher Laurie Santos is trying to read their minds

• By Jerry Adler
• Photographs by Sylwia Kapuscinski
• Smithsonian magazine, January 2008

On a hot morning in early August, the primate census of Cayo Santiago, a 38-acre island just off the coast of Puerto Rico, numbers approximately 875. Of those, 861 are resident Macaca mulatta, commonly known as rhesus macaques, the descendants of a colony transported here from Calcutta in 1938 to provide a permanent breeding stock for medical researchers. The rest are Homo sapiens who have made the trip in a motorboat, including workers stocking the feeding bins with dun-colored biscuits of monkey chow, and researchers for whom the island provides a rare opportunity to study free-ranging primates without the drudgery of having to locate them deep in some remote forest.

The researchers comprise two distinct disciplines, with widely divergent interests and approaches. Ever since E. O. Wilson visited here in 1956 and came away with the ideas that would eventually become the foundation of a whole new field of research he called sociobiology, the island has been a mecca for ethologists, who study the monkeys' social hierarchies and interactions. It has also been discovered by experimental psychologists, who study the animals' thinking processes. Since the former try to stay as unobtrusive as possible, while the latter employ attention-getting constructions of colored posterboard and bags of fruit, there's a certain unavoidable tension between the disciplines. Trailed by three undergraduates toting armloads of gear up a path sodden with monkey droppings, Laurie Santos, a psychologist at Yale, is in the latter camp. "This is what we do," she says, "hike around looking for monkeys by themselves who are hungry and want to play. It's hard to find social creatures by themselves," she adds as she backs out of the field of view of a primatologist's video camera, "and even harder to find ones that aren't being followed by other researchers."

Santos has been coming to Cayo every year since 1993, when she was a freshman at Harvard and volunteered to work here with her psychology professor, Marc Hauser. She keeps that tradition alive with her own undergraduates. With her bright smile and mass of curly dark hair, Santos, 32, could pass for an undergraduate herself. Her boyfriend, Mark Maxwell, actually is an undergrad—albeit one who dropped out of MIT and supported himself for years by playing poker before returning this year to finish his degree at Yale. Santos teaches a class, "Sex, Evolution and Human Nature" with a course description ("Topics include...human mating strategies, the biology of warfare, sex differences in behavior, love and lust...") that all but guaranteed it would have to be held in the largest classroom on campus, the law school auditorium. She was embarrassed last year when her mother attended one of her lectures and by happenstance chose the day that she was discussing the female orgasm. "I had to cover it, but my mom was in the auditorium, so I kind of rushed through it," Santos says. "I hope the students didn't notice."

She has built a growing and impressive list of publications in cognitive neuroscience (mostly having to do with how primates understand physical objects and relations) and evolutionary psychology, the field that grew out of sociobiology. "If you see something in a primate," Santos reasons, "you can use it as a window into the evolutionary past of human beings."

On this summer day, if her undergraduate volunteers expected to be investigating the exuberant and promiscuous sex life of the rhesus macaque, they must be disappointed. Santos' interest here is in what psychologists call "theory of mind," the ability to impute thoughts and intentions to another individual, one of the cornerstones of human cognition. "Sitting here talking with you," Santos explains, "all I can see is your behavior, but I draw inferences about your desires and thoughts. The interesting question is, how far back in evolutionary time does that ability extend? Can it exist without language?" As recently as a decade ago, the conventional wisdom doubted that even chimpanzees, which are more closely related to human beings than are monkeys, possessed theory of mind. This view is changing, in large measure because of the work of Santos and her collaborators. With her students in tow and a small bag of grapes in her pocket, Santos is now out to demonstrate the phenomenon—if a Macaca mulatta can be induced to cooperate.

Trial 1: The experiment relies on one of the most predictable traits of rhesus monkeys: their tendency to steal food at every opportunity. Santos discovered this a few years ago when she and her colleagues were running experiments in cognition and tool use involving lemons, and frequently had to quit early because the animals stole all the fruit. The island's monkeys are supplied with food, of course, and they also forage, but to leave so much as a raisin unguarded is to invite larceny; the researchers eat their own lunches inside a locked cage of cyclone fencing.

The theory-of-mind experiment is designed to test whether the monkeys, who obsessively guard their own food, assume that people do the same. If so, Santos reasons, they should prefer to steal from people who are looking away. So Santos enlists Olivia Scheck and Katharine Jan, Yale student volunteers here for the month. They are dressed alike in blue slacks and white shirts to minimize any confounding effect from their appearance—although there are differences Santos cannot do anything about, because Olivia is several inches shorter than Katharine, and blond, where Katharine is dark-haired. In general, Santos has found, rhesus macaques prefer to steal from the shorter person, although top-ranking dominant males sometimes do the opposite, apparently just to show off.

The goal is to locate a monkey that isn't busy doing something else and isn't distracted by other monkeys. That's not always easy on this crowded island; monkeys who seem to be off by themselves are often low-ranking males skulking around a female in hopes of getting a quick copulation—out of sight of the dominant males. Once Santos has a monkey's attention, she holds up two grapes for it to see and impales each on a stick placed a few feet apart on the ground. Each student stands behind one of the grapes. Then Katharine turns her back on the monkey, while Olivia stares straight ahead. If the monkey doesn't fall asleep, wander off or lose interest, it will scamper, saunter or nervously edge over to one grape or the other and snatch it up. Based on published results, says Santos, nine times out of ten the person whose back is turned is the one who gets robbed.

This time, the monkey, who apparently hadn't read the literature, heads straight for Olivia's grape, grabs it from right under her nose and runs off.

Santos has traveled a long and (to her) unexpected path to this patch of tropical forest. She grew up in New Bedford, Massachusetts, the daughter of a high-school guidance counselor mother and a computer programmer father. She's French-Canadian on her mother's side, and on her father's is descended from Cape Verdean fishermen who settled in New England generations ago. In high school, all she knew about college was that she wanted to attend one in Boston; she chose Harvard because, taking financial aid into account, it was the least expensive. She enrolled in Hauser's psychology class, on which her own is modeled, because she was closed out of a course she'd needed for her intended career as a lawyer, and was won over by the charismatic professor and the intellectual challenge of a rapidly evolving field.

Santos did not originate the idea that has fueled several breakthroughs in the past decade, but she has been one of the most imaginative and successful in applying it. The concept, known as "domain specificity," holds that the cognitive abilities of primates evolved for particular tasks and can be tested only in a context that is meaningful to the animal itself. The early theory-of-mind experiments tried to enlist monkeys or chimps in begging for food, sharing it or cooperating to find it—behaviors, says Santos, that do not come naturally to them. As she and co-author and Yale colleague Derek E. Lyons put it in a recent paper in the journal Philosophy Compass, "though primates are social creatures, they are not exactly sociable ones." Colleagues say Santos has a talent for thinking like a monkey. Her experiments cleverly elicit and exploit primates' natural gifts for competitiveness, stealthiness, hoarding and deceit.

Trial 2: This time Olivia is the one facing away, and the monkey, better versed in theory-of-mind, makes a dash for her grape.

Rhesus macaques, especially juveniles, are capable of simulating cuteness, but it's not their defining characteristic. Scrappy and long-limbed, with pink hairless faces framed by gray or brown fur, they fight convincingly among themselves. At least two here appear to have lost limbs in their perpetual struggle for rank, and they will stand up to a human being if the stakes are high enough—a grape, for example. They have been known to carry a variety of herpes that can be fatal to human beings, and scattered around the island are first-aid stations holding disinfectant kits to be used in case of a bite. (On the other hand, a single human visitor with active tuberculosis could wipe out the entire colony.) Santos recognizes many of the individual monkeys here by sight or by the letter-and-number code tattooed on their chests, but she says she has never been even tempted to name them.

She has somewhat more affection for the 11 capuchin monkeys in her lab at Yale, who are named after characters in James Bond movies (Goldfinger, Jaws, Holly Goodhead). Her work with them involves experiments on "social decision-making." She equips them with tokens they can trade for food and studies the development of their rudimentary economy. Like human beings, they are loss-averse: if the going price is two grapes for a token, they prefer to trade with an experimenter who shows them one grape and then adds one, compared with one who shows three and takes one away. They are also sneaky. After swapping for an apple, she says, they will sometimes take a bite of it, then present the untouched side to the researcher and try to sell it back. And they have an entrepreneurial bent. At times they would offer their feces in exchange for a token, behavior that baffled the researchers until a student pointed out that every morning someone comes into the cage and scoops out the droppings—which may have given them the idea that people value them.

Trial 3: Katharine faces away again, and the monkey sidles up and grabs her grape, just as science would predict. Then it does a quick sideways dash and snatches up Olivia's as well. the experiments done so far are tests of first-order knowledge: the monkey sees the human experimenter either facing or facing away from the grape. Now Santos intends to test whether macaques possess the more sophisticated concept of "false belief"—the recognition that another individual may be mistaken. The classic test for this in people is the "Sally-Anne" experiment. The subject watches "Sally" put a ball in a box, then leave the room. While she's gone, "Anne" moves the ball to a different box. The experimenter asks the subject: Where will Sally look for the ball? The expected answer from adults is the first box, where Sally last saw it. Children younger than about 4, and those with autism, more often say the second box, where the ball actually is; they cannot conceive that Sally has a false belief.

To test if monkeys are capable of false belief, Santos has devised an experiment involving two grapes, three open boxes and four researchers, including Santos herself and someone to record the whole thing on video. Again, the premise is that the monkeys are more likely to steal things that, from their point of view, are unguarded. The protocol is as follows: the three boxes are arranged side by side on the ground with their open sides facing the monkey, and a student puts one grape in each of two boxes—B and C, say. Then she stands behind the boxes and turns her back, and a different student moves the grapes—into A and B. The monkey now knows where the grapes are, but the first student does not. When she turns and faces the monkey, which box is the monkey more likely to rob? If the monkey understands "false belief," it will expect the student to be guarding boxes B and C, and so will be more likely to steal from A.

"Make sure you don't both have your backs turned to the monkey at the same time," Santos warns the students. "Some of these monkeys will just rush the boxes."

Trial 1: After finally locating a suitable monkey, setting up the boxes and going through the pantomime with the grapes, Santos drifts back into the trees and watches as the monkey languidly scratches itself. Almost ostentatiously, it seems, the animal turns and looks out over the rocks to the sea.

Trials 2 and 3: No approach.

With her students, Santos tramps up and down the now-familiar hills, across a rocky isthmus, to the sounds of wind and crashing waves, chattering monkeys and the continual bang of metal lids slamming on the chow bins. Santos tries to enlist one young monkey gnawing a biscuit, only to be stared down by a nearby male that was about to mount a different female. "Don't worry," Santos says placatingly as she backs away, "she's gonna mate with you, I promise."

Trial 4: Boxes blow over, trial aborted.

Trial 5: As soon as the grapes are displayed, the monkey gets up and walks away.

Trial 6: Finally a monkey that seems interested. Actually, a little too interested. As the second student is approaching the boxes to move the grapes, the monkey gets off his haunches and walks swiftly toward her. "Turn around!" Santos calls. The student pivots, pulls herself up to her full height and stares right at the monkey. It snarls menacingly back at her; she shrieks and runs to hide behind a colleague. The monkey grabs both grapes and runs away, chewing.

Students must commit to a month in Puerto Rico, but it is the prerogative of the professor to fly home at the end of the first week. Before Santos leaves, she makes some modifications to the false-belief experiment, and by the end of the month she hears that it's working better. In the months after returning to New Haven, she begins to formulate some tentative conclusions about what she has found: monkeys can gauge the knowledge and intentions of others when they correspond to their own perceptions of reality, but they cannot make the leap to the concept of a false belief.

So is the mental gap between monkeys and human beings closing or widening? In a sense, both: if Santos is right, monkeys manage to navigate complex social hierarchies, hiding from and deceiving others as necessary, all without an ability that human beings develop by the age of 4. The more she works with monkeys, the more Santos is convinced that their abilities are limited to specific contexts and tasks, such as competing for food or establishing dominance. It's rather like the honeybee dance, a fantastically ingenious way to communicate geographic information. Still, honeybees can't use it to talk about their feelings. "My guess," says Hauser, "is that we will eventually come to see that the gap between human and animal cognition, even a chimpanzee, is greater than the gap between a chimp and a beetle." Perhaps, Santos says. Monkeys can reason quite competently about human beings' intentions with respect to grapes, but only by imputing to them what they themselves experience: a readiness to grab and hoard whenever possible. She speculates that it is our capacity for language that enables us to understand mental states different from our own. We may not be hungry now, but because we have a word for the concept we can imagine what it feels like. "The more you hang out with monkeys," she says, "the more you realize just how special people really are."

Jerry Adler is a Newsweek senior editor specializing in science and medicine.
Sylwia Kapuscinski usually photographs human primates, and focuses on immigrants.