Yerkes Researchers Discover Capuchin Monkeys Can Recognize Familiar Faces

Researchers at the Yerkes National Primate Research Center, Emory University, have discovered capuchin monkeys can recognize familiar individuals in photographs. The study, available in the current online edition of The Proceedings of the National Academy of Sciences, showed capuchins were able to recognize photographs of individuals living in their social group, an ability that helps to distinguish familiar individuals from outsiders. The research confirms the ability of monkeys not only to compare and recognize facial images, but the ability to connect faces with individuals they know or do not know, an ability shared with humans. The study also demonstrates capuchins understand the two-dimensional representational nature of photographs.

For the study, the capuchins viewed photographs of four different faces. One of the four pictures was of a capuchin from their own group, which they needed to tell apart from three strangers. They also needed to do the reverse, differentiating one stranger from three familiar individuals.

"This required monkeys to look at similar-looking faces and use their personal knowledge of group mates to solve the task," says lead researcher Jennifer Pokorny, PhD. "They readily performed the task and continued to do well when shown new pictures in color and in grayscale, as well as when presented with individuals they had never before seen in pictures, though with whom they were personally familiar, continues Pokorny.

Researchers often use two-dimensional images in experiments, yet there is little conclusive evidence to suggest nonhuman primates, particularly monkeys, truly understand the image represents individuals or items in real life.

"The study not only reveals that capuchin monkeys are able to individually recognize familiar faces, but it also convincingly demonstrates they understand the two-dimensional representational nature of photographs. The fact these monkeys correctly determined which faces belonged to in-group versus out-group members, corresponding to their personal experiences, validates the conclusion capuchin monkeys view images of faces as humans do - as individuals they do or do not know," says Pokorny.

Pokorny trained under world-renowned primatologist Frans de Waal, PhD, who says the study is the first to show face recognition in monkeys is fundamentally similar to that in humans, indicating that face recognition is an evolutionarily ancient ability. De Waal is director of the Living Links Center at the Yerkes Research Center.

For nearly eight decades, the Yerkes National Primate Research Center, Emory University, has been dedicated to conducting essential basic science and translational research to advance scientific understanding and to improve the health and well-being of humans and nonhuman primates. Today, the center, as one of only eight National-Institutes of Health-funded national primate research centers, provides leadership, training and resources to foster scientific creativity, collaboration and discoveries. Yerkes-based research is grounded in scientific integrity, expert knowledge, respect for colleagues, an open exchange of ideas and compassionate quality animal care.

Within the fields of microbiology, immunology, neuroscience and psychobiology, the center's research programs are seeking ways to: develop vaccines for infectious and noninfectious diseases, such as AIDS and Alzheimer's disease; treat cocaine addiction; interpret brain activity through imaging; increase understanding of progressive illnesses such as Parkinson's and Alzheimer's; unlock the secrets of memory; determine behavioral effects of hormone replacement therapy; address vision disorders; and advance knowledge about the evolutionary links between biology and behavior.

The goal of the Living Links Center at the Yerkes National Primate Research Center is to view great apes as a window to the human past by studying their behavior, cognition, neuroanatomy, genes and reproduction in a noninvasive manor. Another goal is to educate the public about apes and to help guarantee their continued existence in the wild.

Originally published Dec. 2, 2009

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Fish Vision Discovery Makes Waves in Natural Selection

Emory University researchers have identified the first fish known to have switched from ultraviolet vision to violet vision, or the ability to see blue light. The discovery is also the first example of an animal deleting a molecule to change its visual spectrum.

Their findings on scabbardfish, linking molecular evolution to functional changes and the possible environmental factors driving them, were published Oct. 13 in the Proceedings of the National Academy of Sciences.

"This multi-dimensional approach strengthens the case for the importance of adaptive evolution," says evolutionary geneticist Shozo Yokoyama, who led the study. "Building on this framework will take studies of natural selection to the next level."

The research team included Takashi Tada, a post-doctoral fellow in biology, and Ahmet Altun, a post-doctoral fellow in biology and computational chemistry.

Vision ‘like a painting'

For two decades, Yokoyama has done groundbreaking work on the adaptive evolution of vision in vertebrates. Vision serves as a good study model, since it is the simplest of the sensory systems. For example, only four genes are involved in human vision.

"It's amazing, but you can mix together this small number of genes and detect a whole color spectrum," Yokoyama says. "It's just like a painting."

The common vertebrate ancestor possessed UV vision. However, many species, including humans, have switched from UV to violet vision, or the ability to sense the blue color spectrum.

From the ocean depths

Fish provide clues for how environmental factors can lead to such vision changes, since the available light at various ocean depths is well quantified. All fish previously studied have retained UV vision, but the Emory researchers found that the scabbardfish has not. To tease out the molecular basis for this difference, they used genetic engineering, quantum chemistry and theoretical computation to compare vision proteins and pigments from scabbardfish and another species, lampfish. The results indicated that scabbardfish shifted from UV to violet vision by deleting the molecule at site 86 in the chain of amino acids in the opsin protein.

"Normally, amino acid changes cause small structure changes, but in this case, a critical amino acid was deleted," Yokoyama says.

More examples likely

"The finding implies that we can find more examples of a similar switch to violet vision in different fish lineages," he adds. "Comparing violet and UV pigments in fish living in different habitats will open an unprecedented opportunity to clarify the molecular basis of phenotypic adaptations, along with the genetics of UV and violet vision."

Scabbardfish spend much of their life at depths of 25 to 100 meters, where UV light is less intense than violet light, which could explain why they made the vision shift, Yokoyama theorizes. Lampfish also spend much of their time in deep water. But they may have retained UV vision because they feed near the surface at twilight on tiny, translucent crustaceans that are easier to see in UV light.

A framework for evolutionary biology

Last year, Yokoyama and collaborators completed a comprehensive project to track changes in the dim-light vision protein opsin in nine fish species, chameleons, dolphins and elephants, as the animals spread into new environments and diversified over time. The researchers found that adaptive changes occur by a small number of amino acid substitutions, but most substitutions do not lead to functional changes.

Their results provided a reference framework for further research, and helped bring to light the limitations of studies that rely on statistical analysis of gene sequences alone to identify adaptive mutations in proteins.

"Evolutionary biology is filled with arguments that are misleading, at best," Yokoyama says. "To make a strong case for the mechanisms of natural selection, you have to connect changes in specific molecules with changes in phenotypes, and then you have to connect these changes to the living environment."

From eScienceCommons

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The Secret Lives of Wild Primates

Ask any new dad, and he'll tell you — having a new baby in the house is no picnic.

Anthropology professor Patricia Whitten recently uncovered evidence that, in communities of the earliest primates, newborns stress out the guys. "I'm looking at different aspects of hormones and behavior in wild primates to understand humans better," says Whitten, who specializes in the links between behavior, biology and reproduction.

Whitten's lab at Emory has an international reputation for the analysis of steroid levels in fecal samples of wild primates. The data can help reveal all sorts of complex social dramas, from the emotional impact on baboons after a relative is killed by a lion, to the secrets of monkey mating strategies.

In 1998, she began collaborating with Diane Brockman of the University of North Carolina in a study of sifaka lemurs in Madagascar. Lemurs are prosimian primates –believed to be the forerunners of more advanced primates like apes and monkeys.

The study results, recently published by the Proceedings of the Royal Society B, found that male sifaka become more anxious during the annual birthing season. Whitten initially thought that the rise in glucocorticoid levels in males could be tied to an environmental factor. She was surprised that the data pointed instead to the presence of a new infant.

Males are Nurturing, but Stressed

Field observations revealed another surprise: male sifaka play a nurturing role with infants, grooming and caring for them. But the correlation between higher stress in males and the birthing season remains a mystery.

One hypothesis is that the males are worried about aggression by males from neighboring groups: Sifaka males roam and visit other groups of sifaka during the birthing season. Sometimes the visitors challenge the dominant male of a group. Occasionally, they will even kill infants.

For Whitten, the complex dramas revealed by the initial study raise more questions. For instance, why do the female sifaka sometimes allow visiting males to hold their newborns? "The females are dominant, so they are choosing which males are trustworthy – but sometimes they don't seem to be choosing that well," Whitten says.

Whitten is well-known for her groundbreaking studies of wild vervet monkeys, but the prosimian primates – believed to have originated 65 million years ago – offer her a glimpse further back.

"In anthropology, we commonly talk about one million years of evolution, or five million," Whitten says. "If we start looking at behavior going back 65 million years, think how much more deeply ingrained that may be."

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Giving Transcends Species in Yerkes Study

Researchers at the Yerkes National Primate Research Center, Emory University, have shown capuchin monkeys, just like humans, find giving to be a satisfying experience. This finding comes on the coattails of a recent imaging study in humans that documented activity in reward centers of the brain after humans gave to charity. Empathy in seeing the pleasure of another's fortune is thought to be the impetus for sharing, a trait this study shows transcends primate species.

The study is available online in the Early Edition of the Proceedings of the National Academy of Sciences.

Frans de Waal, PhD, director of the Living Links Center at the Yerkes Research Center, and Kristi Leimgruber, research specialist, led a team of researchers who exchanged tokens for food with eight adult female capuchins. Each capuchin was paired with a relative, an unrelated familiar female from her own social group or a stranger (a female from a different group). The capuchins then were given the choice of two tokens: the selfish option, which rewarded that capuchin alone with an apple slice; or the prosocial option, which rewarded both capuchins with an apple slice. The monkeys predominantly selected the prosocial token when paired with a relative or familiar individual but not when paired with a stranger.

"The fact the capuchins predominantly selected the prosocial option must mean seeing another monkey receive food is satisfying or rewarding for them," said de Waal. "We believe prosocial behavior is empathy based. Empathy increases in both humans and animals with social closeness, and in our study, closer partners made more prosocial choices. They seem to care for the welfare of those they know," continued de Waal.

de Waal and his research team next will attempt to determine whether giving is self-rewarding to capuchins because they can eat together or if the monkeys simply like to see the other monkey enjoying food.

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Anthropologists Examine Relatives and Friends, Seeking Both Sides of our Nature

To find out what makes us human, Brian Hare asks our closest relatives and best friends.

As a new and newsworthy assistant professor of biological anthropology and anatomy at Duke, he’s examining the social abilities of chimpanzees and bonobos, the two endangered species of ape with which we share about 99 percent of our genes.

This summer, the focus is on “xenophobia” (ZEE-no-phobia), the fear of strangers.

Bonobos “are extremely tolerant,” Hare says. “They’re very good at cooperating and much more egalitarian, like we are. Chimpanzees are a lot more hostile. They have a lot of problems. They can even kill each other.”

“What a fantastic opportunity! Here we have hallmarks of being human, and they differ between our two closest relatives.”

With his wife, scientist/journalist/blogger Vanessa Woods, Hare is again going to Africa in mid-June as he has for the last four years to study chimps and bonobos in orphanages.

Bonobos are not pets. These animals were orphaned by poachers.They’ll start at Point-Noire in the Republic of Congo, where three graduate students are already hard at work evaluating the behavior and thought processes of a group of orphaned chimpanzees at the Tchimpounga sanctuary. Then they’ll fly to Brazzaville and boat across the Congo River to Kinshasa in the Democratic Republic of Congo. There they will study a group of orphaned bonobos at the Lola Ya Bonobo Sanctuary.

This summer’s xenophobia testing will involve showing the apes photos of familiar and unfamiliar animals to see which they prefer looking at. “The prediction is that chimpanzees and bonobos will have different preferences,” Hare says. “Bonobos tend to be very peaceful with neighbors they don’t necessarily know very well. Chimpanzees do not.”

Meanwhile, Woods will continue evaluating “social-sexual behavior” among very young bonobos. Earlier research by Hare’s group and others documented that adult bonobos — unlike chimps — use simulated and real sexual activity to ward off tensions among group members. And Woods’ research has also found “2-and 3-year-old babies are already using these social-sexual behaviors.” Hare says. “The question is: does that require a lot of exposure to adults, or does it matter?”

The orphaned chimps and bonobos are the offspring of parents killed for food or trafficked as exotic pets. They’ve formed their own societies of primate peers at the three African wildlife sanctuaries where Hare has negotiated his group’s access to conduct research. At night the orphans can sleep in enclosures comfortably roofed-off from the rain. And by day they can “escape” from the gaze of human monitors within open, natural spaces of up to 100 acres filled with the plants they know.

“I want to see animals living in as rich an environment as possible, because I want to find out how they express their most sophisticated problem-solving abilities,” he says. “These are microcosms of what they would normally experience in the wild, but they’re up to 20 times larger than the world’s largest zoo facility. Not only that, they’re in primary tropical forests.” In such settings, the animals can develop normally despite being orphaned, he adds. “They show very few, if any, of the aberrant behaviors you see in laboratory animals.”

Hare does research with these subjects by their own invitation. “The idea is coming up with experiments that are fun for the animals, so they’ll volunteer to participate,” he says. “In the morning, we ask them if they would like to play games with us. If they’d like to play the games, then we’re doing our jobs well.” Doing such research on animals living in totally wild settings would be impossible as well as unethical, he adds.

Examples of fun and games include the “double rope” exercise in which animals are tested for their ability or inclination to work cooperatively by pulling on opposite ends of a rope connected to a food tray. Only by pulling together can they get a snack. The test highlights striking differences in the attitudes of chimps and bonobos, which split on our family tree about 2 million years ago. All in all, he has been working with apes for 14 years.

Bonobos play with the scientists only if they want to.Ingenious experiments on animal behavior have been Hare’s trademark since his undergraduate days at Emory University’s Yerkes Regional Primate Research Center in Atlanta. He first attracted attention there by taking up his professor’s challenge to prove that his family dogs could infer human thought in the way they followed a pointed finger to the correct Dixie cup where food was hidden.

“I found it interesting that dogs can do this but chimps can’t,” he recalls. “People think solving this pointing problem is also very important for young children as they develop the ability to think about the thoughts of others.”

Ironically, after graduating from Emory (summa cum laude) with anthropology and psychology degrees, Hare failed to be selected as a graduate student at Duke’s well-respected Department of Biological Anthropology and Anatomy. He ended up attending Harvard instead, which he calls “the Duke of the north for me.” At Harvard he expected to continue studying primates but found himself in Siberia evaluating an amazing breeding experiment that had “tamed” silver foxes.

By breeding only the animals that were least aggressive toward humans for 30 successive generations, scientists had turned them into “cute” foxes that behaved much like fawning retrievers. Hare’s experiments showed that they responded to human gestures — such as pointing — just like his dogs did back in Atlanta. Untamed silver foxes did not.

His Harvard advisor on the project – now a research colleague — thinks the same selection pressure is important in the evolution of the bonobos’ friendly behavior toward each other, says Hare.

Arriving at Duke this spring after making a name for himself as director of the Hominoid Psychology Research Group at the Max Planck Institute for Evolutionary Anthropology in Leipzig, Germany, Hare will be doing some chimpanzee research at North Carolina’s state zoo in Asheboro while also rekindling his canine research.

About 800 square feet of space in the Bioscience Building’s basement has been renovated as “a lab for people to bring their pet dogs in to play some fun games,” says Hare, who also has an appointment at Duke’s Center for Cognitive Neuroscience.

“We’ll be able to look at how dogs solve problems.” He explains. In the process, “we can also offer doggy day care.”

By Monte Basgall

Monte Basgall is senior science writer at Duke News and Communications.