Erica van de Waal

Potent Social Learning and Conformity Shape a Wild Primate’s Foraging Decisions

Animal Culture Cultural transmission of information occurs when individuals learn from others with more experience or when individuals come to accept particular modes of behavior as the local norm. Such information transfer can be expected in highly social or long-lived species where contact and time for learning are maximized and are seen in humans (see the Perspective by de Waal). Using a network-based diffusion analysis on a long-term data set that includes tens of thousands of observations of individual humpback whales, Allen et al. (p. 485) show that an innovative feeding behavior has spread through social transmission since it first emerged in a single individual in 1980. The “lobtail” feeding has passed among associating individuals for more than three decades. Van de Waal et al. (p. 483), on the other hand, used a controlled experimental approach in vervet monkeys to show that individuals learn what to eat from more experienced individuals within their social group. Not only did young animals learn from observing older animals, but immigrating males switched their food preference to that of their new group. A natural experiment reveals that wild vervet migrants adopt local norms when it comes to choosing foods. [Also see Perspective by de Waal] Conformity to local behavioral norms reflects the pervading role of culture in human life. Laboratory experiments have begun to suggest a role for conformity in animal social learning, but evidence from the wild remains circumstantial. Here, we show experimentally that wild vervet monkeys will abandon personal foraging preferences in favor of group norms new to them. Groups first learned to avoid the bitter-tasting alternative of two foods. Presentations of these options untreated months later revealed that all new infants naïve to the foods adopted maternal preferences. Males who migrated between groups where the alternative food was eaten switched to the new local norm. Such powerful effects of social learning represent a more potent force than hitherto recognized in shaping group differences among wild animals.

Selective attention to philopatric models causes directed social learning in wild vervet monkeys

Human behaviour is often based on social learning, a mechanism that has been documented also in a variety of other vertebrates. However, social learning as a means of problem-solving may be optimal only under specific conditions, and both theoretical work and laboratory experiments highlight the importance of a potential models identity. Here we present the results from a social learning experiment on six wild vervet monkey groups, where models were either a dominant female or a dominant male. We presented ‘artificial fruit’ boxes that had doors on opposite, differently coloured ends for access to food. One option was blocked during the demonstration phase, creating consistent demonstrations of one possible solution. Following demonstrations we found a significantly higher participation rate and same-door manipulation in groups with female models compared to groups with male models. These differences appeared to be owing to selective attention of bystanders to female model behaviour rather than owing to female tolerance. Our results demonstrate the favoured role of dominant females as a source for ‘directed’ social learning in a species with female philopatry. Our findings imply that migration does not necessarily lead to an exchange of socially acquired information within populations, potentially causing highly localized traditions.

Social networks in primates: smart and tolerant species have more efficient networks

Network optimality has been described in genes, proteins and human communicative networks. In the latter, optimality leads to the efficient transmission of information with a minimum number of connections. Whilst studies show that differences in centrality exist in animal networks with central individuals having higher fitness, network efficiency has never been studied in animal groups. Here we studied 78 groups of primates (24 species). We found that group size and neocortex ratio were correlated with network efficiency. Centralisation (whether several individuals are central in the group) and modularity (how a group is clustered) had opposing effects on network efficiency, showing that tolerant species have more efficient networks. Such network properties affecting individual fitness could be shaped by natural selection. Our results are in accordance with the social brain and cultural intelligence hypotheses, which suggest that the importance of network efficiency and information flow through social learning relates to cognitive abilities.

Infant access and handling in sooty mangabeys and vervet monkeys

Access to one’s newborn infant is a commodity that can be traded for other benefits such as grooming in nonhuman primates. According to the biological market paradigm, the price paid should fluctuate with the number of newborns in the group. We investigated the grooming sessions between mothers with infants less than 3 months old and other adult females in free-ranging primates: one group of sooty mangabeys, Cercocebus atys, with 35 adult females (Ivory Coast) and two groups of vervet monkeys, Chlorocebus aethiops, with four and seven females, respectively (South Africa). Although many more infants were born per birth season in the mangabey group than in the vervet groups, interaction patterns involving infants showed many similarities: mothers did not reciprocate grooming received from nonmothers, but exchanged it directly for the opportunity to handle their infants, whereby obtaining access to infants required longer grooming bouts than reciprocating grooming in grooming sessions not involving infants. Low-ranking handlers needed to groom mothers for longer than their higher-ranking counterparts. The ‘value’ of an infant, in terms of grooming time received by the mother, decreased when infants grew older or when many infants were simultaneously present in the group. In vervets, infant availability affected handling times: females handled infants for longer when there were fewer infants. Furthermore, only frequent grooming partners of the mother could handle infants for longer and this familiarity was not kin related. This suggests that if the value of an infant varies with dominance, infant handling time may be determined by the quality of the females’ relationships.

Similarity in Food Cleaning Techniques within Matrilines in Wild Vervet Monkeys

Social learning and the formation of traditions rely on the ability and willingness to copy one another. A central question is under which conditions individuals adapt behaviour to social influences. Here, we demonstrate that similarities in food processing techniques emerge on the level of matrilines (mother – offspring) but not on the group level in an experiment on six groups of wild vervet monkeys that involved grapes covered with sand. Monkeys regularly ate unclean grapes but also used four cleaning techniques more similarly within matrilines: rubbing in hands, rubbing on substrate, open with mouth, and open with hands. Individual cleaning techniques evolved over time as they converged within matrilines, stabilised at the end and remained stable in a follow-up session more than one year later. The similarity within matrilines persisted when we analyzed only foraging events of individuals in the absence of other matriline members and matriline members used more similar methods than adult full sisters. Thus, momentary conversion or purely genetic causation are unlikely explanations, favouring social learning as mechanism for within matriline similarities. The restriction of traditions to matriline membership rather than to the group level may restrict the development of culture in monkeys relative to apes or humans.

Social learning and spread of alternative means of opening an artificial fruit in four groups of vervet monkeys

Two-action experiments, in which observer individuals watch models use one of two alternative methods to achieve the same goal, have become recognized as a powerful method for studying social learning. We applied this approach to vervet monkeys, Chlorocebus aethiops, using an artificial fruit (‘vervetable’) which could be opened by either lifting a door panel on its front, or alternatively by sliding the panel to the left or right. In each of two groups a model was trained to lift the door and in two others the model slid it to either the left or right. Members of each group could then watch their model before the group was given access to multiple baited vervetables. Over the course of 100 openings we found a significant tendency for the lift and slide approaches to spread preferentially in the groups in which they were seeded. The same was true for slide left versus slide right, indicating these monkeys can attend to and learn from a fine level of detail in what others do. This effect cannot be explained by mere local enhancement since monkeys grasped a knob centred in the door to perform all techniques. Instead, imitation or emulation is implicated. No significant diminution of the tendency to adopt the seeded technique occurred among individuals learning later rather earlier in the study. Our results show that vervet monkeys have the capacity to learn from others by either emulation or imitation and what they learn has the potential to spread across their group.

Spontaneous emergence, imitation and spread of alternative foraging techniques among groups of vervet monkeys.

Animal social learning has become a subject of broad interest, but demonstrations of bodily imitation in animals remain rare. Based on Voelkl and Hubers study of imitation by marmosets, we tested four groups of semi-captive vervet monkeys presented with food in modified film canisters (“aethipops’). One individual was trained to take the tops off canisters in each group and demonstrated five openings to them. In three groups these models used their mouth to remove the lid, but in one of the groups the model also spontaneously pulled ropes on a canister to open it. In the last group the model preferred to remove the lid with her hands. Following these spontaneous differentiations of foraging techniques in the models, we observed the techniques used by the other group members to open the canisters. We found that mouth opening was the most common technique overall, but the rope and hands methods were used significantly more in groups they were demonstrated in than in groups where they were not. Our results show bodily matching that is conventionally described as imitation. We discuss the relevance of these findings to discoveries about mirror neurons, and implications of the identity of the model for social transmission.

Social-learning abilities of wild vervet monkeys in a two-step task artificial fruit experiment

Social learning is the basis for the formation of traditions in both human and nonhuman animals. Field observations and experiments provide evidence for the existence of traditions in animals but they do not address the underlying social-learning mechanisms. We used an established laboratory experimental paradigm, the artificial fruit design, to test for copying of a sequence of actions and local enhancement in six groups of wild vervet monkeys, Chlorocebus aethiops. We introduced a two-step task where models had to remove a bar to untie a rope that blocked a single door of a box. The models were high-ranking individuals that monopolized the box early on and discovered by trial and error how to open it. We obtained successful models in three groups, while the other three groups acted as controls. After 20 successful demonstrations, we tested subjects with a box that had a rope in the same position but the rope was not functional. Under these conditions, sequential copying of the two-step opening did not occur. Only individuals that were exposed to models were likely to touch the bar if door opening was not immediately successful, providing evidence for local enhancement. When we presented the boxes with the functional rope, we found no effect of having been exposed to a model on the probability that subjects solved the task. We conclude that the social-learning abilities of wild vervet monkeys are relatively limited and discuss potential problems concerning the technical difficulty of the task.

Third-party ranks knowledge in wild vervet monkeys (Chlorocebus aethiops pygerythrus)

The Machiavellian/Social Intelligence Hypothesis proposes that a complex social environment selected for advanced cognitive abilities in vertebrates. In primates it has been proposed that sophisticated social strategies like obtaining suitable coalition partners are an important component of social intelligence. Knowing the rank relationships between group members is a basic requirement for the efficient use of coalitions and the anticipation of counter-coalitions. Experimental evidence for such knowledge currently exists in only few species. Here, we conducted rank reversal playback experiments on adult females belonging to three different groups of free-ranging vervet monkeys (Chlorocebus aethiops pygerythrus) to test their knowledge of the female hierarchy. Playbacks simulating rank reversals (subordinate aggressing a dominant) induced longer looking times than playbacks simulating a dominant aggressing a subordinate. Vervet monkey females therefore seem to compute the rank relationships between other females. Our results suggest that detailed social knowledge about rank relationships may be widespread in primates and potentially also in other species living in stable groups.

Wild vervet monkeys copy alternative methods for opening an artificial fruit

Experimental studies of animal social learning in the wild remain rare, especially those that employ the most discriminating tests in which alternative means to complete naturalistic tasks are seeded in different groups. We applied this approach to wild vervet monkeys (Chlorocebus aethiops) using an artificial fruit (‘vervetable’) opened by either lifting a door panel or sliding it left or right. In one group, a trained model lifted the door, and in two others, the model slid it either left or right. Members of each group then watched their model before being given access to multiple baited vervetables with all opening techniques possible. Thirteen of these monkeys opened vervetables, displaying a significant tendency to use the seeded technique on their first opening and over the course of the experiment. The option preferred in these monkeys’ first successful manipulation session was also highly correlated with the proportional frequency of the option they had previously witnessed. The social learning effects thus documented go beyond mere stimulus enhancement insofar as the same door knob was grasped for either technique. Results thus suggest that through imitation, emulation or both, new foraging techniques will spread across groups of wild vervet monkeys to create incipient foraging traditions.