Foraging in a social setting: a comparative analysis of captive gorillas and chimpanzees.

This study was designed to investigate the foraging behavior of zoo-housed western lowland gorillas (Gorilla gorilla gorilla) and compare it with that of zoo-housed chimpanzees (Pan trogloydytes) tested previously in a similar paradigm. Specifically, we aimed to document how a group of zoo-housed gorillas foraged within a familiar environment to discover novel food sources and whether they sought out more preferred foods, even if they had to travel further to reach them, as they do in the wild. Gorillas were provided plastic tokens to exchange with researchers at two locations-at the same location as the tokens (close) for carrot pieces and another 6.5 m away (far) for grapes. Over the course of 30 sessions, a single individual-the silverback male-accounted for 96% of the 1546 tokens exchanged, all of which took place at the far location. Inter-individual distance measures collected during each session, as well as during matched control sessions, showed that while both gorillas and chimpanzees express similar patterns of social association across the two conditions, the average dyadic association for chimpanzees was stronger than that for gorillas. Together, these findings provide an example of the value of employing identical methodologies to compare cognition and behavior across species as well highlight the importance of the social context in which studies take place.

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.

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.

The interplay between individual, social, and environmental influences on chimpanzee food choices.

The foraging activity of chimpanzees requires individuals to balance personal preferences with nutrient requirements, food availability, and interactions with members of their social group. To determine whether chimpanzee food preferences are fixed or malleable across varying socio-ecological contexts, we presented six zoo-housed chimpanzees with pairwise combinations of four different foods under two experimental conditions. First, we individually tested each chimpanzee's choices for the four foods to ascertain individual preferences. Second, we tested the chimpanzees in a situation which more-closely mimicked the foraging pressures experienced by wild chimpanzees. In this second condition, the chimpanzees were tested in a group setting and the food availability was less predictable, such as in a patchy foraging environment. Subjects expressed significant variation in their selection of which foods to consume in the two different contexts and also appeared more willing to consume less-preferred foods in the unpredictable, social environment. These results suggest that chimpanzees' food preferences are not fixed, but change with context and are likely mediated by social facilitation. This is not only important to understand chimpanzees' foraging patterns and dietary requirements, but also has implications for experimental paradigms that rely on food preferences.

Flexibility and persistence of chimpanzee (Pan troglodytes) foraging behavior in a captive environment.

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 individual's 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.

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.

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.

Transmission of multiple traditions within and between chimpanzee groups.

Field reports provide increasing evidence for local behavioral traditions among fish, birds, and mammals. These findings are significant for evolutionary biology because social learning affords faster adaptation than genetic change and has generated new (cultural) forms of evolution. Orangutan and chimpanzee field studies suggest that like humans, these apes are distinctive among animals in each exhibiting over 30 local traditions. However, direct evidence is lacking in apes and, with the exception of vocal dialects, in animals generally for the intergroup transmission that would allow innovations to spread widely and become evolutionarily significant phenomena. Here, we provide robust experimental evidence that alternative foraging techniques seeded in different groups of chimpanzees spread differentially not only within groups but serially across two further groups with substantial fidelity. Combining these results with those from recent social-diffusion studies in two larger groups offers the first experimental evidence that a nonhuman species can sustain unique local cultures, each constituted by multiple traditions. The convergence of these results with those from the wild implies a richness in chimpanzees' capacity for culture, a richness that parsimony suggests was shared with our common ancestor.

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.

Affiliation promotes the transmission of a social custom: handclasp grooming among captive chimpanzees.

Handclasp grooming is a unique social custom, known to occur regularly among some, but not all populations of chimpanzees (Pan troglodytes). As with other cultural behaviors, it is assumed that this distinctive grooming posture is learned socially by one individual from another. However, statistical comparisons among factors thought to influence how a behavior spreads within a group have never, to our knowledge, been conducted. In the present study, the origination and spread of handclasp grooming in a group of captive chimpanzees was followed throughout more than 1,500 h of observation over a period of 12 years. We report on the frequency, bout duration, and number and demography of performers throughout the study period, and compare these findings to those reported for wild populations. We predicted that dyads with strong affiliative ties, measured by time spent in proximity to and grooming one another, were likely to develop a handclasp grooming partnership during the study period. A quadratic assignment procedure was used to compare correlations among observed frequencies of grooming and proximity with handclasp grooming in all possible dyads within the group. As predicted, the formation of new handclasp grooming dyads was positively correlated with the rate of overall grooming and proximity within a dyad. In addition, in nearly all dyads formed, at least one individual had been previously observed to handclasp groom. We concluded that affiliation and individual experience determines the transmission of handclasp grooming among captive chimpanzees.

Ultrasonic call characteristics of rat pups are altered following prenatal malnutrition.

The male offspring of rats provided with a protein deficient diet (6% casein) for 5 weeks prior to mating and throughout pregnancy were subjected to a brief period of isolation and cooling at postnatal Days (P)7, 9, and 11, and their ultrasonic vocalizations were compared with those of well-nourished pups. Calls were categorized into 12 different types based upon their sonographic patterns. Although call rates were equal, the call characteristics of the prenatally malnourished pups differed significantly from those of well-nourished controls. At P7, their mean peak sound frequency (irrespective of call type) was significantly higher, and constant frequency calls were of both higher frequency and longer duration. Over the age range studied, prenatally malnourished pups emitted a smaller variety of calls, with significantly fewer ascending frequency vocalizations while producing either significantly fewer (P9) or greater (P11) descending frequency calls. Altered crying patterns have been related to brain damage in human babies, with more abnormal cries being associated with more severe neurological impairment. Therefore, the present results most likely reflect altered central nervous system development and function. Ultrasonic vocalization characteristics in rat pups may provide a useful early marker of the severity of disturbance to the development of the central nervous system following an insult, and offer the potential for predicting the degree of functional and behavioral deficits later in life.