When and how do non-human great apes communicate to support cooperation?

Several scholars have long suggested that human language and remarkable communicative abilities originate from the need and motivation to cooperate and coordinate actions with others. Yet, little work has focused on when and how great apes communicate during joint action tasks, partly because of the widely held assumption that animal communication is mostly manipulative, but also because non-human great apes' default motivation seems to be competitive rather than cooperative. Here, we review experimental cooperative tasks and show how situational challenges and the degree of asymmetry in terms of knowledge relevant for the joint action task affect the likelihood of communication. We highlight how physical proximity and strength of social bond between the participants affect the occurrence and type of communication. Lastly, we highlight how, from a production point of view, communicators appear capable of calibrating their signalling and controlling their delivery, showing clear evidence of first-order intentionality. On the other hand, recipients appear to struggle in terms of making use of referential information received. We discuss different hypotheses accounting for this asymmetry and provide suggestions concerning how future work could help us unveil to what degree the need for cooperation has shaped our closest living relatives' communicative behaviour. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

Reduced risk-seeking in chimpanzees in a zero-outcome game.

A key component of economic decisions is the integration of information about reward outcomes and probabilities in selecting between competing options. In many species, risky choice is influenced by the magnitude of available outcomes, probability of success and the possibility of extreme outcomes. Chimpanzees are generally regarded to be risk-seeking. In this study, we examined two aspects of chimpanzees' risk preferences: first, whether setting the value of the non-preferred outcome of a risky option to zero changes chimpanzees' risk preferences, and second, whether individual risk preferences are stable across two different measures. Across two experiments, we found chimpanzees (Pan troglodytes, n = 23) as a group to be risk-neutral to risk-avoidant with highly stable individual risk preferences. We discuss how the possibility of going empty-handed might reduce chimpanzees' risk-seeking relative to previous studies. This malleability in risk preferences as a function of experimental parameters and individual differences raises interesting questions about whether it is appropriate or helpful to categorize a species as a whole as risk-seeking or risk-avoidant. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

How animals collaborate: Underlying proximate mechanisms.

Collaboration or social interactions in which two or more individuals coordinate their behavior to produce outcomes from which both individuals benefit are common in nature. Individuals from many species hunt together, defend their territory, and form coalitions in intragroup competition. However, we still know very little about the proximate mechanisms underlying these behaviors. Recent theories of human cognitive evolution have emphasized the role collaboration may have played in the selection of socio-cognitive skills. It has been argued that the capacity to form shared goals and joint intentions with others, is what allows humans to collaborate so flexibly and efficiently. Although there is no evidence that nonhuman animals are capable of shared intentionality, there is conceivably a wide range of proximate mechanisms that support forms of, potentially flexible, collaboration in other species. We review the experimental literature with the aim of evaluating what we know about how other species achieve collaboration; with a particular focus on chimpanzees. We structure the review with a new categorization of collaborative behavior that focuses on whether individuals intentionally coordinate actions with others. We conclude that for a wider comparative perspective we need more data from other species but the findings so far suggest that chimpanzees, and possibly other great apes, are capable of understanding the causal role of a partner in collaboration. This article is categorized under: Cognitive Biology > Evolutionary Roots of Cognition Psychology > Comparative Psychology.

Establishing an infrastructure for collaboration in primate cognition research.

Inferring the evolutionary history of cognitive abilities requires large and diverse samples. However, such samples are often beyond the reach of individual researchers or institutions, and studies are often limited to small numbers of species. Consequently, methodological and site-specific-differences across studies can limit comparisons between species. Here we introduce the ManyPrimates project, which addresses these challenges by providing a large-scale collaborative framework for comparative studies in primate cognition. To demonstrate the viability of the project we conducted a case study of short-term memory. In this initial study, we were able to include 176 individuals from 12 primate species housed at 11 sites across Africa, Asia, North America and Europe. All subjects were tested in a delayed-response task using consistent methodology across sites. Individuals could access food rewards by remembering the position of the hidden reward after a 0, 15, or 30-second delay. Overall, individuals performed better with shorter delays, as predicted by previous studies. Phylogenetic analysis revealed a strong phylogenetic signal for short-term memory. Although, with only 12 species, the validity of this analysis is limited, our initial results demonstrate the feasibility of a large, collaborative open-science project. We present the ManyPrimates project as an exciting opportunity to address open questions in primate cognition and behaviour with large, diverse datasets.

How chimpanzees (Pan troglodytes) share the spoils with collaborators and bystanders.

Chimpanzees hunt cooperatively in the wild, but the factors influencing food sharing after the hunt are not well understood. In an experimental study, groups of three captive chimpanzees obtained a monopolizable food resource, either via two individuals cooperating (with the third as bystander) or via one individual acting alone alongside two bystanders. The individual that obtained the resource first retained most of the food but the other two individuals attempted to obtain food from the "captor" by begging. We found the main predictor of the overall amount of food obtained by bystanders was proximity to the food at the moment it was obtained by the captor. Whether or not an individual had cooperated to obtain the food had no effect. Interestingly, however, cooperators begged more from captors than did bystanders, suggesting that they were more motivated or had a greater expectation to obtain food. These results suggest that while chimpanzee captors in cooperative hunting may not reward cooperative participation directly, cooperators may influence sharing behavior through increased begging.

Chimpanzees ( Pan troglodytes) coordinate by communicating in a collaborative problem-solving task.

Successful collaboration often relies on individuals' capacity to communicate with each other. Despite extensive research on chimpanzee communication, there is little evidence that chimpanzees are capable, without extensive human training, of regulating collaborative activities via communication. This study investigated whether pairs of chimpanzees were capable of communicating to ensure coordination during collaborative problem-solving. The chimpanzee pairs needed two tools to extract fruits from an apparatus. The communicator in each pair could see the location of the tools (hidden in one of two boxes), whereas only the recipient could open the boxes. The subjects were first successfully tested for their capacity to understand the pointing gestures of a human who indicated the location of the tools. In a subsequent conspecifics test, the communicator increasingly communicated the tools' location, by approaching the baited box and giving the key needed to open it to the recipients. The recipient used these signals and obtained the tools, transferring one of the tools to the communicator so that the pair could collaborate in obtaining the fruits. The study suggests that chimpanzees have the necessary socio-cognitive skills to naturally develop a simple communicative strategy to ensure coordination in a collaborative task.

The evolutionary roots of prosociality: the case of instrumental helping.

Comparative studies with closely related primate species are crucial to understand the origins of human prosociality. One type of prosocial behaviour that probably relies on evolutionary ancient skills and motivations is instrumental helping. Recent experimental studies have shown that bonobos and chimpanzees will help others achieve their action goals. Chimpanzees have shown to help others picking up and giving objects to a recipient, opening locked doors for conspecifics struggling to open them, and releasing stuck rewards that recipients were trying to reach. Recent studies have now replicated some of these results with bonobos. However, whereas chimpanzee's helping emerges mainly in response to recipients' signals of need, bonobos also help proactively. This difference could rely on bonobos' enhanced socio-cognitive skills.

The psychology of cooperation: Insights from chimpanzees and children.

Across all cultures, humans engage in cooperative activities that can be as simple as preparing a meal or sharing food with others and as complex as playing in an orchestra or donating to charity. Although intraspecific cooperation exists among many other animal species, only humans engage in such a wide array of cooperative interaction and participate in large-scale cooperation that extends beyond kin and even includes strangers.

One for You, One for Me: Humans' Unique Turn-Taking Skills.

Long-term collaborative relationships require that any jointly produced resources be shared in mutually satisfactory ways. Prototypically, this sharing involves partners dividing up simultaneously available resources, but sometimes the collaboration makes a resource available to only one individual, and any sharing of resources must take place across repeated instances over time. Here, we show that beginning at 5 years of age, human children stabilize cooperation in such cases by taking turns across instances of obtaining a resource. In contrast, chimpanzees do not take turns in this way, and so their collaboration tends to disintegrate over time. Alternating turns in obtaining a collaboratively produced resource does not necessarily require a prosocial concern for the other, but rather requires only a strategic judgment that partners need incentives to continue collaborating. These results suggest that human beings are adapted for thinking strategically in ways that sustain long-term cooperative relationships and that are absent in their nearest primate relatives.

Non-egalitarian allocations among preschool peers in a face-to-face bargaining task.

In face-to-face bargaining tasks human adults almost always agree on an equal split of resources. This is due to mutually recognized fairness and equality norms. Early developmental studies on sharing and equality norms found that egalitarian allocations of resources are not common before children are 5 or 6 years old. However, recent studies have shown that in some face-to face collaborative situations, or when recipients express their desires, children at much younger ages choose equal allocations. We investigated the ability of 3.5 and 5-year-olds to negotiate face-to-face, whether to collaborate to obtain an equal or an unequal distribution of rewards. We hypothesized that the face-to-face interaction and interdependency between partners would facilitate egalitarian outcomes at both ages. In the first experiment we found that 5-year-olds were more egalitarian than 3.5-year-olds, but neither of the age classes shared equally. In the second experiment, in which we increased the magnitude of the inequality, we found that children at both ages mostly agreed on the unequal distribution. These results show that communication and face-to-face interactions are not sufficient to guarantee equal allocations at 3-5 years of age. These results add to previous findings suggesting that in the context of non-collaboratively produced resources it is only after 5 years of age that children use equality norms to allocate resources.

Chimpanzees (Pan troglodytes) instrumentally help but do not communicate in a mutualistic cooperative task.

Chimpanzees cooperate in a variety of contexts, but communicating to influence and regulate cooperative activities is rare. It is unclear whether this reflects chimpanzees' general inability or whether they have found other means to coordinate cooperative activities. In the present study chimpanzees could help a partner play her role in a mutually beneficial food-retrieval task either by transferring a needed tool (transfer condition) or by visually or acoustically communicating the hiding-location of the needed tool (communication condition). Overall, chimpanzees readily helped their partner by delivering the needed tool, but none of them communicated the hiding location of the tool to their partner reliably across trials. These results demonstrate that although chimpanzees can coordinate their cooperative activities by instrumentally helping their partner in her role, they do not readily use communication with their partner for this same end.

Chimpanzees' (Pan troglodytes) strategic helping in a collaborative task.

Many animal species cooperate, but the underlying proximate mechanisms are often unclear. We presented chimpanzees with a mutualistic collaborative food-retrieval task requiring complementary roles, and tested subjects' ability to help their partner perform her role. For each role, subjects required a different tool, and the tools were not interchangeable. We gave one individual in each dyad both tools, and measured subjects' willingness to transfer a tool to their partner as well as which tool (correct versus incorrect) they transferred. Most subjects helped their partner and transferred the tool the partner needed. Thus, chimpanzees not only coordinate different roles, but they also know which particular action the partner needs to perform. These results add to previous findings suggesting that many of chimpanzees' limitations in collaboration are, perhaps, more motivational than cognitive.

The evolutionary roots of human collaboration: coordination and sharing of resources.

Humans' ability to collaborate to obtain otherwise inaccessible goals may be one main cause for our success as a species. Comparative psychological research with children and our closest primate relatives is starting to elucidate the phylogenetic roots as well as the unique psychological mechanisms that support our cooperative behavior. For mutually beneficial collaboration, individuals need (1) cognitive mechanisms to coordinate actions with partners and (2) mechanisms to distribute the acquired resources in a way that incentivizes partners to continue collaborating. Several recent studies suggest that we share with chimpanzees many of the cognitive mechanisms required for successful coordination: chimpanzees understand the need to act jointly with a partner, that is, recruiting the partner when the problem requires collaboration and even helping her to perform her role. However, in contrast to very young children, they do not seem well equipped to share resources obtained through joint effort. Chimpanzees' competitive nature around food constrains their sharing behavior, and because they do not share differently after individual or collaborative effort, partners lose motivation to continue collaborating. All this suggests that higher interindividual tolerance around food and mechanisms to counteract bullying behavior and share the spoils after a collaborative effort are probably derived human traits.

Allocation of resources to collaborators and free-riders in 3-year-olds.

Recent studies have shown that in situations where resources have been acquired collaboratively, children at around 3 years of age share mostly equally. We investigated 3-year-olds' sharing behavior with a collaborating partner and a free-riding partner who explicitly expressed her preference not to collaborate. Children shared more equally with the collaborating partner than with the free rider. These results suggest that young children are sensitive to the contributions made by others to a collaborative effort (and possibly their reasons for not collaborating) and distribute resources accordingly.

Assessing the psychological health of captive and wild apes: a response to Ferdowsian et al. (2011).

As many studies of cognition and behavior involve captive animals, assessing any psychological impact of captive conditions is an important goal for comparative researchers. Ferdowsian and colleagues (2011) sought to address whether captive chimpanzees show elevated signs of psychopathology relative to wild apes. They modified a checklist of diagnostic criteria for major depression and posttraumatic stress disorder in humans, and applied these criteria to various captive and wild chimpanzee populations. We argue that measures derived from human diagnostic criteria are not a powerful tool for assessing the psychological health of nonverbal animals. In addition, we highlight certain methodological drawbacks of the specific approach used by Ferdowsian and colleagues (2011). We propose that research should (1) focus on objective behavioral criteria that account for species-typical behaviors and can be reliably identified across populations; (2) account for population differences in rearing history when comparing how current environment impacts psychological health in animals; and (3) focus on how changes in current human practices can improve the well-being of both captive and wild animals.

Dogs (Canis familiaris) evaluate humans on the basis of direct experiences only.

Reputation formation is a key component in the social interactions of many animal species. An evaluation of reputation is drawn from two principal sources: direct experience of an individual and indirect experience from observing that individual interacting with a third party. In the current study we investigated whether dogs use direct and/or indirect experience to choose between two human interactants. In the first experiment, subjects had direct interaction either with a "nice" human (who played with, talked to and stroked the dog) or with an "ignoring" experimenter who ignored the dog completely. Results showed that the dogs stayed longer close to the "nice" human. In a second experiment the dogs observed a "nice" or "ignoring" human interacting with another dog. This indirect experience, however, did not lead to a preference between the two humans. These results suggest that the dogs in our study evaluated humans solely on the basis of direct experience.

How chimpanzees solve collective action problems.

We presented small groups of chimpanzees with two collective action situations, in which action was necessary for reward but there was a disincentive for individuals to act owing to the possibility of free-riding on the efforts of others. We found that in simpler scenarios (experiment 1) in which group size was small, there was a positive relationship between rank and action with more dominant individuals volunteering to act more often, particularly when the reward was less dispersed. Social tolerance also seemed to mediate action whereby higher tolerance levels within a group resulted in individuals of lower ranks sometimes acting and appropriating more of the reward. In more complex scenarios, when group size was larger and cooperation was necessary (experiment 2), overcoming the problem was more challenging. There was highly significant variability in the action rates of different individuals as well as between dyads, suggesting success was more greatly influenced by the individual personalities and personal relationships present in the group.

Young children share the spoils after collaboration.

Egalitarian behavior is considered to be a species-typical component of human cooperation. Human adults tend to share resources equally, even if they have the opportunity to keep a larger portion for themselves. Recent experiments have suggested that this tendency emerges fairly late in human ontogeny, not before 6 or 7 years of age. Here we show that 3-year-old children share mostly equally with a peer after they have worked together actively to obtain rewards in a collaboration task, even when those rewards could easily be monopolized. These findings contrast with previous findings from a similar experiment with chimpanzees, who tended to monopolize resources whenever they could. The potentially species-unique tendency of humans to share equally emerges early in ontogeny, perhaps originating in collaborative interactions among peers.

Chimpanzees help conspecifics obtain food and non-food items.

Chimpanzees (Pan troglodytes) sometimes help both humans and conspecifics in experimental situations in which immediate selfish benefits can be ruled out. However, in several experiments, chimpanzees have not provided food to a conspecific even when it would cost them nothing, leading to the hypothesis that prosociality in the food-provisioning context is a derived trait in humans. Here, we show that chimpanzees help conspecifics obtain both food and non-food items--given that the donor cannot get the food herself. Furthermore, we show that the key factor eliciting chimpanzees' targeted helping is the recipients' attempts to either get the food or get the attention of the potential donor. The current findings add to the accumulating body of evidence that humans and chimpanzees share the motivation and skills necessary to help others in situations in which they cannot selfishly benefit. Humans, however, show prosocial motives more readily and in a wider range of contexts.