Kristin E. Bonnie

Spread of arbitrary conventions among chimpanzees: a controlled experiment

Wild chimpanzees (Pan troglodytes) have a rich cultural repertoire—traditions common in some communities are not present in others. The majority of reports describe functional, material traditions, such as tool use. Arbitrary conventions have received far less attention. In the same way that observations of material culture in wild apes led to experiments to confirm social transmission and identify underlying learning mechanisms, experiments investigating how arbitrary habits or conventions arise and spread within a group are also required. The few relevant experimental studies reported thus far have relied on cross-species (i.e. human–ape) interaction offering limited ecological validity, and no study has successfully generated a tradition not involving tool use in an established group. We seeded one of two rewarded alternative endpoints to a complex sequence of behaviour in each of two chimpanzee groups. Each sequence spread in the group in which it was seeded, with many individuals unambiguously adopting the sequence demonstrated by a group member. In one group, the alternative sequence was discovered by a low ranking female, but was not learned by others. Since the action-sequences lacked meaning before the experiment and had no logical connection with reward, chimpanzees must have extracted both the form and benefits of these sequences through observation of others.

Prestige Affects Cultural Learning in Chimpanzees

Humans follow the example of prestigious, high-status individuals much more readily than that of others, such as when we copy the behavior of village elders, community leaders, or celebrities. This tendency has been declared uniquely human, yet remains untested in other species. Experimental studies of animal learning have typically focused on the learning mechanism rather than on social issues, such as who learns from whom. The latter, however, is essential to understanding how habits spread. Here we report that when given opportunities to watch alternative solutions to a foraging problem performed by two different models of their own species, chimpanzees preferentially copy the method shown by the older, higher-ranking individual with a prior track-record of success. Since both solutions were equally difficult, shown an equal number of times by each model and resulted in equal rewards, we interpret this outcome as evidence that the preferred model in each of the two groups tested enjoyed a significant degree of prestige in terms of whose example other chimpanzees chose to follow. Such prestige-based cultural transmission is a phenomenon shared with our own species. If similar biases operate in wild animal populations, the adoption of culturally transmitted innovations may be significantly shaped by the characteristics of performers.

Copying without rewards: socially influenced foraging decisions among brown capuchin monkeys

An individual’s foraging activity can be influenced by the choices made by nearby conspecifics. The interest shown in the location and characteristics of a feeding patch may depend on the feeding success of a conspecific there, a process that needs to be distinguished from choices guided by rewards to the observer itself. We investigated how rewards for both self and others influence the foraging choices of captive capuchin monkeys (Cebus apella). Thirteen adult capuchins observed familiar female conspecific models explore one of three opaque boxes under three conditions. In the first, there were no rewards available to either monkey; in the second, rewards were available to the model only; and in the third, both monkeys could retrieve a reward. Under all conditions, subjects more often explored the same box as the model than was expected by chance. Thus, without ever receiving a reward themselves or without seeing another receive rewards, subjects’ searches were directed at the box explored by another monkey. The tendency to match the model’s choice increased if the subject was rewarded. We compared these results to control conditions in which the model was either absent, or present but not allowed to demonstrate. Subjects’ located the reward less often in control conditions, than in the experimental conditions. We conclude that extrinsic rewards, while helpful, are not required for partners to influence the foraging choices of capuchins, and that the unrewarded copying of foraging choices demonstrated here may provide the basis for additional social influences on learning.

Opportunities and constraints when studying social learning: Developmental approaches and social factors.

Identifying social learning in wild populations is complicated by the relative lack of ability to conduct controlled experiments in natural habitats. Even in more controlled captive settings, tracking the innovation and spread of behavior among known individuals can be challenging, and these studies often suffer from a lack of ecological validity. In recent years, a host of new approaches have been undertaken to attempt to provide more quantitative control and empirical demonstration of social learning, both in the wild and in captive settings that more closely mimic natural contexts. Developmental approaches are being undertaken more regularly that allow us to study the ontogenetic trajectory of complex skills in a variety of taxa. Likewise, a spirited focus on the social context of social learning has emerged, and researchers have begun to meticulously analyze the influences of social systems and the characteristics of demonstrators and observers. Here, we provide a review of these studies and summarize the opportunities and constraints that exist when one attempts to study learning in social species. We suggest that although the study of social learning in nonhuman animals is becoming much more complex, addressing this complexity provides a fruitful model for understanding the evolution of human cultural behavior.

Flexibility and Persistence of Chimpanzee (Pan Troglodytes) Foraging Behavior in a Captive Environmentxht

As a result of environmental variability, animals may be confronted with uncertainty surrounding the presence of, or accessibility to, food resources at a given location or time. While individuals can rely on personal experience to manage this variability, the behavior of members of an individuals social group can also provide information regarding the availability or location of a food resource. The purpose of the present study was to measure how captive chimpanzees individually and collectively adjust their foraging strategies at an artificial termite mound, as the availability of resources provided by the mound varied over a number of weeks. As predicted, fishing activity at the mound was related to resource availability. However, chimpanzees continued to fish at unbaited locations on the days and weeks after a location had last contained food. Consistent with previous studies, our findings show that chimpanzees do not completely abandon previously learned habits despite learning individually and/or socially that the habit is no longer effective. Am. J. Primatol. 74:661–668, 2012.

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.

Seeding an arbitrary convention in capuchin monkeys: the effect of social context

The study of social learning in non-human animals has advanced beyond attempts to determine which animals are capable of learning socially to investigations of the factors that influence transmission. Capuchin monkeys (Sapajus sp.) are adept social learners of various behaviours including extractive foraging techniques and social customs. Here, we conducted an open diffusion experiment to determine whether capuchins would learn an arbitrary convention from a knowledgeable demonstrator. In addition, we investigated whether rank, sex and social context affected acquisition and expression of the behaviour. Participation in the experiment was strongly influenced by dominance rank in the group setting. However, when tested individually, the majority of individuals participated and faithfully copied the convention that was seeded into their group. Our findings demonstrate that capuchins can acquire an arbitrary convention via social learning, but that social context must be carefully considered in studies of social learning.

Captive chimpanzees share diminishing resources

Wild chimpanzees routinely share high-value resources such as meat obtained through hunting and fruit procured from raiding crops. Although it is predicted that the proximate mechanisms for sharing behaviour are the result of reciprocity, interchange and mutualism, examinations of these factors in captivity have not mirrored the degree to which they are found in the wild. The goal of the current study was to investigate how a group of seven captive chimpanzees responded when a highly desirable and monopolizable resource diminished over the course of eight months. To do this we measured the amount of time that was spent sharing food at an artificial termite mound as well as the relationship between dyads that spent time sharing. Our results contradicted our predictions that rates of aggression would increase and the number of individuals fishing at the termite mound would decrease when resources diminished, as we observed no difference in either variable over time. We did, though, find an increase in the amount of sharing as the number of baited holes decreased. We also found a correlation between the strength of dyadic relationships outside of the study and the amount of time that individuals spent sharing with each other.

Studying primate cognition in a social setting to improve validity and welfare: a literature review highlighting successful approaches

Background Studying animal cognition in a social setting is associated with practical and statistical challenges. However, conducting cognitive research without disturbing species-typical social groups can increase ecological validity, minimize distress, and improve animal welfare. Here, we review the existing literature on cognitive research run with primates in a social setting in order to determine how widespread such testing is and highlight approaches that may guide future research planning. Survey Methodology Using Google Scholar to search the terms “primate” “cognition” “experiment” and “social group,” we conducted a systematic literature search covering 16 years (2000–2015 inclusive). We then conducted two supplemental searches within each journal that contained a publication meeting our criteria in the original search, using the terms “primate” and “playback” in one search and the terms “primate” “cognition” and “social group” in the second. The results were used to assess how frequently nonhuman primate cognition has been studied in a social setting (>3 individuals), to gain perspective on the species and topics that have been studied, and to extract successful approaches for social testing. Results Our search revealed 248 unique publications in 43 journals encompassing 71 species. The absolute number of publications has increased over years, suggesting viable strategies for studying cognition in social settings. While a wide range of species were studied they were not equally represented, with 19% of the publications reporting data for chimpanzees. Field sites were the most common environment for experiments run in social groups of primates, accounting for more than half of the results. Approaches to mitigating the practical and statistical challenges were identified. Discussion This analysis has revealed that the study of primate cognition in a social setting is increasing and taking place across a range of environments. This literature review calls attention to examples that may provide valuable models for researchers wishing to overcome potential practical and statistical challenges to studying cognition in a social setting, ultimately increasing validity and improving the welfare of the primates we study.

Spatial learning deficits induced by muscimol and CL218,872: lack of effect of prenatal malnutrition.

Abstract The sensitivity of prenatal protein malnourished rats to the amnestic properties of the direct GABAA receptor agonist muscimol and the selective benzodiazepine (BZ) receptor agonist, CL218,872, was studied in the male offspring of rats provided with a protein deficient diet (6% casein) for 5 weeks prior to mating and throughout pregnancy. At postnatal day 90, rats were tested during acquisition of the submerged platform version of the Morris water maze task using four systemic doses of muscimol (0.1, 0.3, 1.0 and 1.8 mg/kg i.p.) or three systemic doses of CL218,872 (1.0, 3.2, and 5.6 mg/kg i.p.). In a dose dependent manner both drugs impaired acquisition of the task and impaired accuracy of the search pattern on the probe trial (platform removed). However, neither drug dissociated the performance of the two nutritional groups. These data are important in light of previous findings of differential behavioral effects of the non-specific BZ agonist, chlordiazepoxide (CDP), on spatial learning and on drug discrimination in prenatally malnourished rats and in the context of previous findings of reduced sensitivity to the anxiolytic effects of non-specific BZ receptor agonists across a wide variety of models of malnutrition. The present findings also support the concept that prenatal malnutrition does not affect the global functioning of the GABAA receptor, but fundamentally alters the way in which a subset of GABAA receptors (i.e. those containing the 2, 3 and/or the 5 but not the 1 subunit) is modulated by BZs.