Lydia M. Hopper

'Ghost' experiments and the dissection of social learning in humans and animals

The focus of this review is the experimental techniques used to identify forms of social learning shown by humans and nonhuman animals. Specifically, the ‘ghost display’ and ‘end‐state’ conditions, which have been used to tease apart imitative and emulative learning are evaluated. In a ghost display, the movements of an apparatus are demonstrated, often through the discrete use of fishing‐line or hidden mechanisms, without a live model acting directly upon the apparatus so that the apparatus appears to be operated as if by a ‘ghostly’ agent. In an end‐state condition, an observing individual is shown the initial state of the test apparatus, the apparatus is then manipulated out‐of‐sight and then represented to the individual in its final state. The aim of the ghost display condition is to determine whether individuals are able to emulate by replicating the movements of an apparatus, or perform a task, without requiring information about the bodily movements required to do so (imitation). The end‐state condition is used to identify goal‐emulation by assessing whether the observer can replicate the steps required to solve the task without having been shown the required body actions or task movements. The responses of individuals tested with either the ghost display and/or end‐state conditions are compared to those of further individuals who have observed a full demonstration by either a human experimenter or a conspecific. The responses of a control group, to whom no information has been provided about the test apparatus or required actions, are also compared and evaluated. The efficacy of these experimental techniques employed with humans, nonhuman primates, dogs, rats and birds are discussed and evaluated. The experiments reviewed herein emphasise the need to provide ghost displays and end‐state conditions in combination, along with full live demonstrations and a no‐information control. Future research directions are proposed.

Developing a Comprehensive and Comparative Questionnaire for Measuring Personality in Chimpanzees Using a Simultaneous Top-Down/Bottom-Up Design

One effective method for measuring personality in primates is to use personality trait ratings to distill the experience of people familiar with the individual animals. Previous rating instruments were created using either top‐down or bottom‐up approaches. Top‐down approaches, which essentially adapt instruments originally designed for use with another species, can unfortunately lead to the inclusion of traits irrelevant to chimpanzees or fail to include all relevant aspects of chimpanzee personality. Conversely, because bottom‐up approaches derive traits specifically for chimpanzees, their unique items may impede comparisons with findings in other studies and other species. To address the limitations of each approach, we developed a new personality rating scale using a combined top‐down/bottom‐up design. Seventeen raters rated 99 chimpanzees on the new 41‐item scale, with all but one item being rated reliably. Principal components analysis, using both varimax and direct oblimin rotations, identified six broad factors. Strong evidence was found for five of the factors (Reactivity/Undependability, Dominance, Openness, Extraversion, and Agreeableness). A sixth factor (Methodical) was offered provisionally until more data are collected. We validated the factors against behavioral data collected independently on the chimpanzees. The five factors demonstrated good evidence for convergent and predictive validity, thereby underscoring the robustness of the factors. Our combined top‐down/bottom‐up approach provides the most extensive data to date to support the universal existence of these five personality factors in chimpanzees. This framework, which facilitates cross‐species comparisons, can also play a vital role in understanding the evolution of personality and can assist with husbandry and welfare efforts. Am. J. Primatol. 75:1042–1053, 2013.

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.

Social comparison mediates chimpanzees’ responses to loss, not frustration

Abstract Why do chimpanzees react when their partner gets a better deal than them? Do they note the inequity or do their responses reflect frustration in response to unattainable rewards? To tease apart inequity and contrast, we tested chimpanzees in a series of conditions that created loss through individual contrast, through inequity, or by both. Chimpanzees were tested in four social and two individual conditions in which they received food rewards in return for exchanging tokens with an experimenter. In conditions designed to create individual contrast, after completing an exchange, the chimpanzees were given a relatively less-preferred reward than the one they were previously shown. The chimpanzees’ willingness to accept the less-preferred rewards was independent of previously offered foods in both the social and individual conditions. In conditions that created frustration through inequity, subjects were given a less-preferred reward than the one received by their partner, but not in relation to the reward they were previously offered. In a social context, females were more likely to refuse to participate when they received a less-preferred reward than their partner (disadvantageous inequity), than when they received a more-preferred reward (advantageous inequity). Specifically, the females’ refusals were typified by refusals to exchange tokens rather than refusals to accept food rewards. Males showed no difference in their responses to inequity or individual contrast. These results support previous evidence that some chimpanzees’ responses to inequity are mediated more strongly by what others receive than by frustration effects.

Different Responses to Reward Comparisons by Three Primate Species

Background Recently, much attention has been paid to the role of cooperative breeding in the evolution of behavior. In many measures, cooperative breeders are more prosocial than non-cooperatively breeding species, including being more likely to actively share food. This is hypothesized to be due to selective pressures specific to the interdependency characteristic of cooperatively breeding species. Given the high costs of finding a new mate, it has been proposed that cooperative breeders, unlike primates that cooperate in other contexts, should not respond negatively to unequal outcomes between themselves and their partner. However, in this context such pressures may extend beyond cooperative breeders to other species with pair-bonding and bi-parental care. Methods Here we test the response of two New World primate species with different parental strategies to unequal outcomes in both individual and social contrast conditions. One species tested was a cooperative breeder (Callithrix spp.) and the second practiced bi-parental care (Aotus spp.). Additionally, to verify our procedure, we tested a third confamilial species that shows no such interdependence but does respond to individual (but not social) contrast (Saimiri spp.). We tested all three genera using an established inequity paradigm in which individuals in a pair took turns to gain rewards that sometimes differed from those of their partners. Conclusions None of the three species tested responded negatively to inequitable outcomes in this experimental context. Importantly, the Saimiri spp responded to individual contrast, as in earlier studies, validating our procedure. When these data are considered in relation to previous studies investigating responses to inequity in primates, they indicate that one aspect of cooperative breeding, pair-bonding or bi-parental care, may influence the evolution of these behaviors. These results emphasize the need to study a variety of species to gain insight in to how decision-making may vary across social structures.

Dissecting the mechanisms of squirrel monkey (Saimiri boliviensis) social learning

Although the social learning abilities of monkeys have been well documented, this research has only focused on a few species. Furthermore, of those that also incorporated dissections of social learning mechanisms, the majority studied either capuchins (Cebus apella) or marmosets (Callithrix jacchus). To gain a broader understanding of how monkeys gain new skills, we tested squirrel monkeys (Saimiri boliviensis) which have never been studied in tests of social learning mechanisms. To determine whether S. boliviensis can socially learn, we ran “open diffusion” tests with monkeys housed in two social groups (N = 23). Over the course of 10 20-min sessions, the monkeys in each group observed a trained group member retrieving a mealworm from a bidirectional task (the “Slide-box”). Two thirds (67%) of these monkeys both learned how to operate the Slide-box and they also moved the door significantly more times in the direction modeled by the trained demonstrator than the alternative direction. To tease apart the underlying social learning mechanisms we ran a series of three control conditions with 35 squirrel monkeys that had no previous experience with the Slide-box. The first replicated the experimental open diffusion sessions but without the inclusion of a trained model, the second was a no-information control with dyads of monkeys, and the third was a ‘ghost’ display shown to individual monkeys. The first two controls tested for the importance of social support (mere presence effect) and the ghost display showed the affordances of the task to the monkeys. The monkeys showed a certain level of success in the group control (54% of subjects solved the task on one or more occasions) and paired controls (28% were successful) but none were successful in the ghost control. We propose that the squirrel monkeys’ learning, observed in the experimental open diffusion tests, can be best described by a combination of social learning mechanisms in concert; in this case, those mechanisms are most likely object movement reenactment and social facilitation. We discuss the interplay of these mechanisms and how they related to learning shown by other primate species.

An Evaluation of the Efficacy of Video Displays for Use With Chimpanzees (Pan troglodytes)

Video displays for behavioral research lend themselves particularly well to studies with chimpanzees (Pan troglodytes), as their vision is comparable to humans’, yet there has been no formal test of the efficacy of video displays as a form of social information for chimpanzees. To address this, we compared the learning success of chimpanzees shown video footage of a conspecific compared to chimpanzees shown a live conspecific performing the same novel task. Footage of an unfamiliar chimpanzee operating a bidirectional apparatus was presented to 24 chimpanzees (12 males, 12 females), and their responses were compared to those of a further 12 chimpanzees given the same task but with no form of information. Secondly, we also compared the responses of the chimpanzees in the video display condition to responses of eight chimpanzees from a previously published study of ours, in which chimpanzees observed live models. Chimpanzees shown a video display were more successful than those in the control condition and showed comparable success to those that saw a live model. Regarding fine‐grained copying (i.e. the direction that the door was pushed), only chimpanzees that observed a live model showed significant matching to the models methods with their first response. Yet, when all the responses made by the chimpanzees were considered, comparable levels of matching were shown by chimpanzees in both the live and video conditions. Am. J. Primatol. 74:442‐449, 2012.

When given the opportunity, chimpanzees maximize personal gain rather than “level the playing field”

We provided chimpanzees (Pan troglodytes) with the ability to improve the quality of food rewards they received in a dyadic test of inequity. We were interested to see if this provision influenced their responses and, if so, whether it was mediated by a social partner’s outcomes. We tested eight dyads using an exchange paradigm in which, depending on the condition, the chimpanzees were rewarded with either high-value (a grape) or low-value (a piece of celery) food rewards for each completed exchange. We included four conditions. In the first, “Different” condition, the subject received different, less-preferred, rewards than their partner for each exchange made (a test of inequity). In the “Unavailable” condition, high-value rewards were shown, but not given, to both chimpanzees prior to each exchange and the chimpanzees were rewarded equally with low-value rewards (a test of individual contrast). The final two conditions created equity. In these High-value and Low-value “Same” conditions both chimpanzees received the same food rewards for each exchange. Within each condition, the chimpanzees first completed ten trials in the Baseline Phase, in which the experimenter determined the rewards they received, and then ten trials in the Test Phase. In the Test Phase, the chimpanzees could exchange tokens through the aperture of a small wooden picture frame hung on their cage mesh in order to receive the high-value reward. Thus, in the Test Phase, the chimpanzees were provided with an opportunity to improve the quality of the rewards they received, either absolutely or relative to what their partner received. The chimpanzees responded in a targeted manner; in the Test Phase they attempted to maximize their returns in all conditions in which they had received low-value rewards during the Baseline Phase. Thus, the chimpanzees were apparently motivated to increase their reward regardless of their partners’, but they only used the mechanism provided when it afforded the opportunity for them to increase their rewards. We also found evidence that the chimpanzees’ responses were enhanced by social facilitation. Specifically, the chimpanzees were more likely to exchange their tokens through the frame when their test partner also did so, even in circumstances in which their reward value could not be improved. Our paradigm provided the chimpanzees with the possibility to improve the quality of rewards they received in the Test Phase. We found that refusals – to exchange tokens or to eat rewards – decreased significantly in the Test Phase compared to the Baseline Phase, where no such opportunity for improvement of outcomes existed. Thus, the chimpanzees participated more when they could improve the rewards they received.

Captive chimpanzee foraging in a social setting: a test of problem solving, flexibility, and spatial discounting

In the wild, primates are selective over the routes that they take when foraging and seek out preferred or ephemeral food. Given this, we tested how a group of captive chimpanzees weighed the relative benefits and costs of foraging for food in their environment when a less-preferred food could be obtained with less effort than a more-preferred food. In this study, a social group of six zoo-housed chimpanzees (Pan troglodytes) could collect PVC tokens and exchange them with researchers for food rewards at one of two locations. Food preference tests had revealed that, for these chimpanzees, grapes were a highly-preferred food while carrot pieces were a less-preferred food. The chimpanzees were tested in three phases, each comprised of 30 thirty-minute sessions. In phases 1 and 3, if the chimpanzees exchanged a token at the location they collected them they received a carrot piece (no travel) or they could travel ≥10 m to exchange tokens for grapes at a second location. In phase 2, the chimpanzees had to travel for both rewards (≥10 m for carrot pieces, ≥15 m for grapes). The chimpanzees learned how to exchange tokens for food rewards, but there was individual variation in the time it took for them to make their first exchange and to discover the different exchange locations. Once all the chimpanzees were proficient at exchanging tokens, they exchanged more tokens for grapes (phase 3). However, when travel was required for both rewards (phase 2), the chimpanzees were less likely to work for either reward. Aside from the alpha male, all chimpanzees exchanged tokens for both reward types, demonstrating their ability to explore the available options. Contrary to our predictions, low-ranked individuals made more exchanges than high-ranked individuals, most likely because, in this protocol, chimpanzees could not monopolize the tokens or access to exchange locations. Although the chimpanzees showed a preference for exchanging tokens for their more-preferred food, they appeared to develop strategies to reduce the cost associated with obtaining the grapes, including scrounging rewards and tokens from group mates and carrying more than one token when travelling to the farther exchange location. By testing the chimpanzees in their social group we were able to tease apart the social and individual influences on their decision making and the interplay with the physical demands of the task, which revealed that the chimpanzees were willing to travel farther for better.

Social Models Enhance Apes' Memory for Novel Events.

Nonhuman primates are more likely to learn from the actions of a social model than a non-social “ghost display”, however the mechanism underlying this effect is still unknown. One possibility is that live models are more engaging, drawing increased attention to social stimuli. However, recent research with humans has suggested that live models fundamentally alter memory, not low-level attention. In the current study, we developed a novel eye-tracking paradigm to disentangle the influence of social context on attention and memory in apes. Tested in two conditions, zoo-housed apes (2 gorillas, 5 chimpanzees) were familiarized to videos of a human hand (social condition) and mechanical claw (non-social condition) constructing a three-block tower. During the memory test, subjects viewed side-by-side pictures of the previously-constructed block tower and a novel block tower. In accordance with looking-time paradigms, increased looking time to the novel block tower was used to measure event memory. Apes evidenced memory for the event featuring a social model, though not for the non-social condition. This effect was not dependent on attention differences to the videos. These findings provide the first evidence that, like humans, social stimuli increase nonhuman primates’ event memory, which may aid in information transmission via social learning.