Frans de Waal - US grants

Research institutions have recently come under attack for trauma in their rhesus monkeys (Macaca mulatta). The fighting is blamed on crowded housing conditions. The literature, however, suggest a more complex relation between space and aggression. A comparison between free-ranging temple monkeys in Kathmandu, monkeys in a large corral, and caged monkeys with a relatively high population density yields and average rate of between 1.6 and 2.2 aggressive acts performed per adult female per hour. In addition to this small variability, the highest rate is not found under the most crowded condition. For males, the variation is greater, with by the highest aggression rate in the free-ranging population. Nonaggressive behavior can also be affected by spatial conditions. Patterns which increase under crowding (e.g. grooming) may serve to regulate social tensions. Buffering mechanisms are expected to be particularly well- developed in groups of monkeys with a long history of captive housing. The proposed research aims at an investigation of 1) the relation between population density and the rate of aggressive behavior in well-established, provisioned rhesus monkey groups under a wide range of spatial conditions, and 2) the role of affiliative behavior in social adjustment to environmental conditions. For this purpose, rhesus monkeys will be observed in social groups housed in laboratory cages, in medium to large pens, and in spacious corrals at two Regional Primate Research Centers. These observations will be compared with those on Free-ranging, provisioned groups of the same species. Except for one experimental manipulation, the study will be of an observational nature. Subjects will be observed in the environment in which they have lived for many years, surrounded by familiar individuals. The social behavior of one individual at a time will be recorded on a portable computer during ten-minute intervals. Besides aggressive acts of various intensities, records will include the context of aggression, the direction and duration of affiliative behavior, and the probability of inter-opponent reunion following an aggressive incident. Over a 3 year period data will be collected on 42 adult males and 150 adult females. The proposed experiment consists of confining an entire monkey group for eight hours to a familiar space that is smaller than their normal enclosure. Such acute crowding is expected to have a greater effect on aggression than chronic crowding. The study is intended to illuminate some of the pros and cons of social housing; an important issue in the ongoing debate about laboratory animal well-being.

In nature, young rhesus monkey females are integrated for life into their natal group, whereas males transfer during puberty. The social position that young females attain in their group depends very much on that of their mother. When adult, a female's place in the rank-order is usually at about the same level as that of her mother and sisters. There are strong indications that this inheritance of status is mainly a social (as opposed to genetic) process, brought about by the young female's association with her kin. Not only a young female's future rank, but also her future friends in the group are to some extent predictable; she will form bonds with other females of her age and status level, both kin and nonkin. Whereas these outcomes of social development are now fairly well known, the details of the process are not. There are many ways in which mothers, actively or passively, may guide their daughters' development, for example, by supporting them against particular opponents, by bringing them into contact with the offspring of their kin and friends, or by preventing the development of certain other contacts. The purpose of this research project is to continue an investigation of the way rhesus mothers shape the social environment of their daughters. Data will be collected on a wide range of behaviors of young monkeys and their mothers in two large groups. For the first time, social development will be followed over the entire developmental period, from birth to adulthood, in order to investigate the extent to which social interactions at early stages of development predict relationships formed at later stages. Because this project considers socially positive behaviors (e.g., bonding, social tolerance) along with socially disruptive behaviors (e.g., aggression, rank acquisition), the study may be able to integrate these behaviors into a single theoretical model of social relationships.

The proposed research is part of a continuing effort to map nonhuman primate social cognition. It marks a shift in PI's methodology from observation of spontaneous behavior to noninvasive experimental manipulation. The aspect selected for study is social reciprocity, which is considered a key element of human social functioning and morality. A previous study of captive chimpanzees (Pan troglodytes) suggested food- sharing as a promising dependent variable in this species. An outdoor-housed group of captive chimpanzees will be subjected to food trials in which all individuals are present, as well as to experiments designed to increase the optimal character of food sharing. This will be achieved by temporary separation of particular individuals during which time they will discover food and subsequently be given the choice to either rejoin the group or consume the food undisturbed. In a variation on this experiment, subjects can consume the food on their own but conspecifics will be allowed to watch. A comparison of behavior across the various conditions will test the prediction that chimpanzees take the perceptions of conspecifics into account. Because of the close taxonomic relation between humans and chimpanzees, the reciprocity system of chimpanzees may depend on emotions, social pressures, and cognitive evaluations that are fundamentally similar to those underlying human reciprocity. Investigation of how individuals judge and influence one another may increase understanding of misjudgments underlying social dysfunction.

DESCRIPTION (Adapted from the applicant's abstract): The purpose of this interdisciplinary project is to accumulate information on the relation between physical and psychological health of captive primates and their social housing conditions. This information is needed to successfully manage existing colonies of AIDS animal models, such as the chimpanzee (Pan troglodytes), rhesus macaque (Macaca mulatta), and pigtail macaque (M. nemestrina). Data collected on nonhuman primates under a variety of conditions will be supplemented with a unique data base accumulated during previous research. Standardized behavioral protocols and a computerized data base will enhance the ability of national breeding programs to justify existing housing conditions and/or provide an empirical basis for the design of future facilities. One of the envisaged end-products is a guide with behavioral data collection techniques, basal levels of easy-to-observe behavior patterns, as well as general health information. At the same time, the proposed research is part of an ongoing effort to develop a new theoretical model of environmental effects on aggressive behavior. The existing model, which attributes aggression levels to crowding, has serious flaws. Nonhuman primates have many checks and balances on aggression and violence, and appear to effectively cope and neutralize social tensions related to high population densities through appeasement and peacemaking. Research on chimpanzees will concern three main conditions: small groups in indoor/outdoor runs; larger groups in outdoor compounds; and, zoo groups in naturalistic enclosures. The chimpanzees will be observed with existing, detailed methods to determine the frequency of aggressive behavior, affiliation patterns, play, reproductive behavior, etc. The proposed study seeks to integrate behavioral and veterinary measures of well-being while paying special attention to measures of environmentally induced stress, ranging from behavioral stress measures to fecal cortisol levels, and immunological data. Research on pigtail macaques will be modeled after a previous large-scale study of rhesus monkeys. It will involve corral-housed groups as well as small harem groups. The study of pigtail macaques will be entirely observational and behavioral.

Reciprocal exchange of goods and services is a universal characteristic of human society. In animals, so-called "reciprocal altruism" is a much-discussed yet much less investigated issue. Evidence accumulated over the past two decades is based almost exclusively on observational research. Food sharing among capuchin monkeys (Cebus apella) - one of the few primate species in which this behavior is well-developed - may provide a handle on reciprocal exchange as this behavior lends itself uniquely to experimentation. Available are thirteen adult subjects (4 males and 9 females), group housed in two separate indoor/outdoor enclosures. Trained for temporary separation from their group, the monkeys have shown high rates of food transfer through a mesh partition during pair tests in which one subject received food and the other did not. The proposed study employs this paradigm to determine the voluntary character of food transfers, and the degree of reciprocity. Data will concern: (1) spontaneous social interactions, including interactions over food, in the group context; and (2) the outcome of pair tests in which partner combination, food type and quality, and other conditions are systematically varied. Behavior in the social group and in the test situation will be compared in detail. Results from this study will show to what extent a non human species can keep track of given and received favors, and develop the sort of expectations and sense of obligation that underlie human economic activity. As such, the study may shed light on the origin of a give-and-take mentality, and the psychological mechanisms guiding its expression.

Nontechnical Abstract Measuring Emotion in Chimpanzees Using Cognitive Tasks This project aims to establish a new, pioneering direction of research to measure the subjective experience of emotion in chimpanzees, the closest living relative of humans. The technique combines experimental and physiological techniques to provide an objective measure of emotional responses in a nonverbal animal. Changes in psychophysiological responses, such as changes in electronic conduction of facial muscles and skin will be measured when subjects view emotion-eliciting videos, and when required to categorize these videos according to their emotional valence. Categorization involves matching positive, negative and neutral facial expressions with videos of social scenes presented on a computer monitor by contacting them with a joystick-controlled cursor. Traditionally, students of nonhuman primates have investigated social behavior and social cognition while ignoring the emotional aspects. Emotion is considered inaccessible in a nonverbal species. Psychophysiological responses, such as those noted above, have an inherent correlation with autonomic nervous system functions that have been associated with the experience of emotion in humans. Measuring psychophysiological parameters in nonverbal organisms will provide an objective measure of what are often covert, unconscious responses. Applying an objective, empirical measure of emotion to chimpanzees will broaden an understanding of the evolution of emotional responses and empathy in humans.

This subproject is one of many research subprojects utilizing the resources provided by a Center grant funded by NIH/NCRR. Primary support for the subproject and the subproject's principal investigator may have been provided by other sources, including other NIH sources. The Total Cost listed for the subproject likely represents the estimated amount of Center infrastructure utilized by the subproject, not direct funding provided by the NCRR grant to the subproject or subproject staff. The Living Links Center is a research and educational center for the study of ape and human evolution, using behavioral, cognitive, anatomic, and molecular approaches. The LLC was formed in response to three developments. The first was the intellectual convergence of the fields of evolutionary psychology, comparative cognition, and field primatology around the importance of using extant species to understand extinct hominid ancestors. Second, technical developments in brain imaging and genomic sequencing provided new non-invasive approaches to study similarities and differences between great apes and humans. The LLC utilizes an ape colony in non-invasive comparative research and provides a base for philanthropic fund raising for both scientific and colony support. Major activities over the past years have been 1) organization of a hugely successful symposium on human origins that drew nearly 2,000 people from Emory and beyond and 2) an international conference with the Chicago Academy of Sciences, in Chicago that has just been turned into a published volume. Currently, we are exploring a joint operation with St. Andrews University, in Scotland, where a center with the same name is being opened at the Edinburgh Zoo.

Reciprocal exchange of goods and services is a universal human economic activity. In animals, so-called "reciprocal altruism" or "tit-for-tat" is much discussed yet less investigated. It has been theorized that such behavior should occur in animals, at least to some degree: otherwise they could not build the highly cooperative societies that we see. This investigator will investigate cooperation in capuchins (Cebus apella), small monkeys known for their large brains and high intelligence. An apparatus will be installed from which two or more monkeys can obtain food through cooperative effort. Tested in small subgroups, the monkeys can team up with any others present. The development of cooperative partnerships will be followed in detail as well as the tendency to preferentially share pay-offs with helpers. By manipulating partner availability, the investigator be able to measure the long-term impact of cooperation in the larger social group.

The proposed experiments seek to illuminate how cooperation arises between individuals, and to what degree it is regulated by tit-for-tat rules. Although the processes are undoubtedly simpler than those underlying the transactions and obligations in human society are, the underlying assumption is that there is a shared psychology that regulates many different kinds of cooperation in a great variety of species.

This study will provide a better understanding of how social relationships foster cooperation, and how cooperation affects subsequent social relationships.

Frans B. M. de Waal, Ph. D.
Reactions to (In)Equality in Monkeys

Social emotions, known by economists as passions, guide human reactions to the efforts, gains, and losses of others. Reactions such as envy, retaliation, and punishment, are sometimes seen as irrational, but may have evolved to promote cooperation. The present study seeks to determine the same reactions in a large-brained, highly cooperative primate, the capuchin monkey (Cebus apella). In previous research these monkeys reacted negatively if a partner received a better reward for equal or less effort. The study will experimentally address the degree to which monkeys monitor the efforts and pay-offs of others, and how they react to (un)equal reward division. Available is a colony of 28 capuchins in an indoor/outdoor enclosure, trained for temporary separation for testing. Monkeys will pull in a tray that rewards their partner at the same time that it rewards themselves. An individual's pulling activity is expected to decline if the partner's rewards substantially exceed those for itself. Females are expected to be more sensitive to reward division than males. This sex difference will be tested in two further paradigms, one that measures the feeding speed of two monkeys eating side by side from different foods. Second, in a task of imitation, in which food rewards play a role.

This subproject is one of many research subprojects utilizing the resources provided by a Center grant funded by NIH/NCRR. Primary support for the subproject and the subproject's principal investigator may have been provided by other sources, including other NIH sources. The Total Cost listed for the subproject likely represents the estimated amount of Center infrastructure utilized by the subproject, not direct funding provided by the NCRR grant to the subproject or subproject staff. In collaboration with Dr. Andrew Whiten of St. Andrews University in Scotland (a world renowned specialist in this field), and two postdoctoral associates, we study the process of social learning in outdoor housed groups of chimpanzees. The most recent progress came from a study on the "prestige effect," which asked if chimpanzees, like humans, tend to follow high status models more than low status ones. Comparing two groups in a counterbalanced design, the study found indeed that high status models attract more followers (Horner et al. 2010). The unique feature of these studies, compared to all studies done before, is that some of the models from which the chimpanzees can learn are conspecifics. The first signs are that chimpanzees are much better at learning from other chimpanzees than from humans, which of course puts question marks behind all previously obtained results in the literature.

Dr. Frans B. M. de Waal
Proposal # IOS-0718010
Social Modification of Primate Behavior

For social animals to react appropriately to each other they need to know about each others'' gender, social status, and the state they are in (such as whether they are hungry, distressed, fearful, or aggressive). This project seeks to establish what brown capuchin monkeys (Cebus apella) know about their group mates. It asks them to indicate, on the basis of portraits projected on a computer screen, which individual monkey belongs to their group. It asks them to rate calls as either aversive or attractive, dependent on the identity of the caller (for example, does a female find the distress calls of her own offspring more aversive than such calls by unrelated juveniles?). And it will ask monkeys to share food with others based on what they know about their hunger state to see if they take the needs of others into account. Available are 30 capuchin monkeys, kept in indoor/outdoor enclosures, trained for temporary separation for experiments. The proposed study will illuminate basic social cognition that is often taken for granted. The laboratory at the Yerkes Primate Center serves the education of a great many undergraduate and graduate students, who obtain valuable training in combination with classes they take. Through his popular books and lectures, the Principal Investigator is at the forefront in communicating findings in animal behavior to a wider public, both academic and nonacademic.

This subproject is one of many research subprojects utilizing the resources provided by a Center grant funded by NIH/NCRR. Primary support for the subproject and the subproject's principal investigator may have been provided by other sources, including other NIH sources. The Total Cost listed for the subproject likely represents the estimated amount of Center infrastructure utilized by the subproject, not direct funding provided by the NCRR grant to the subproject or subproject staff. How do brown capuchin monkeys (Cebus apella) react to their group mates in terms of the knowledge they have and prosocial vs. competitive tendencies? In the last year we published several papers (first author: Pokorny) on face recognition, since we found that capuchin monkeys have a very acute recognition, and are able to tell group mates from non group mates from portraits alone, which is the first such evidence for monkeys. We also found evidence for cooperation and prosocial choice, especially the increase of such choice under conditions that allow reciprocity These projects are currently being written up (Suchak as first author). Another recent projects concerns cultural learning (i.e. how monkeys learn from each other and how habits spread in a group), which have been quite successful (first author: Dindo). Available are 30 capuchin monkeys, kept in indoor/outdoor enclosures, trained for temporary separation for experiments. Our studies illuminate basic social cognition that is often taken for granted. The laboratory at the Yerkes primate Center serves the education of a great many undergraduate and graduate students, who obtain valuable training in combination with classes they take. Through his popular books and lectures, the Principal Investigator is at the forefront in communicating findings in animal behavior to a wider public, both academic and nonacademic.