Inter-individual coordination in walking chimpanzees.

Humans, like many other animals, live in groups and coordinate actions with others in social settings.1 Such interpersonal coordination may emerge unconsciously and when the goal is not the coordination of movements, as when falling into the same rhythm when walking together.2 Although one of our closest living relatives, the chimpanzee (Pan troglodytes), shows the ability to succeed in complex joint action tasks where coordination is the goal,3 little is known about simpler forms of joint action. Here, we examine whether chimpanzees spontaneously synchronize their actions with conspecifics while walking together. We collected data on individual walking behavior of two groups of chimpanzees under semi-natural conditions. In addition, we assessed social relationships to investigate potential effects on the strength of coordination. When walking with a conspecific, individuals walked faster than when alone. The relative phase was symmetrically distributed around 0° with the highest frequencies around 0, indicating a tendency to coordinate actions. Further, coordination was stronger when walking with a partner compared with two individuals walking independently. Although the inter-limb entrainment was more pronounced between individuals of similar age as a proxy for height, it was not affected by the kinship or bonding status of the walkers or the behaviors they engaged in immediately after the walk. We conclude that chimpanzees adapt their individual behavior to temporally coordinate actions with others, which might provide a basis for engaging in other more complex forms of joint action. This spontaneous form of inter-individual coordination, often called entrainment, is thus shared with humans.

Rats show direct reciprocity when interacting with multiple partners.

Direct reciprocity, where individuals apply the decision rule 'help someone who has helped you', is believed to be rare in non-human animals due to its high cognitive demands. Especially if previous encounters with several partners need to be correctly remembered, animals might either stop reciprocating favours previously received from an individual, or switch to the simpler generalized reciprocity mechanism. Here we tested the decision rules Norway rats apply when interacting with multiple partners before being able to return received help. In a sequential prisoner's dilemma situation, focal subjects encountered four different partners that were either helpful or not, on four consecutive days. On the fifth day, the focal subject was paired with one of the previous four partners and given the opportunity to provide it with food. The focal rats returned received help by closely matching the quantity of help their partner had previously provided, independently of the time delay between received and given help, and independently of the ultimate interaction preceding the test. This shows that direct reciprocity is not limited to dyadic situations in Norway rats, suggesting that cognitive demands involved in applying the required decision rules can be met by non-human animals even when they interact with multiple partners differing in helping propensity.

Anybody watching? How others affect helpful actions.

A new study by Havlik et al. (Science Advances, 6(28), eabb4205, 2020) reveals that rats are less likely to help a conspecific in need in the presence of passive bystanders, but that they are more likely to help when there are active bystanders that engage in helping. This study highlights the social skills of rats and the role of bystanders on cooperation, raising a range of interesting questions that should be explored both theoretically and empirically.

The smell of cooperation: rats increase helpful behaviour when receiving odour cues of a conspecific performing a cooperative task.

Reciprocity can explain cooperative behaviour among non-kin, where individuals help others depending on their experience in previous interactions. Norway rats (Rattus norvegicus) cooperate reciprocally according to direct and generalized reciprocity. In a sequence of four consecutive experiments, we show that odour cues from a cooperating conspecific are sufficient to induce the altruistic help of rats in a food-exchange task. When rats were enabled to help a non-cooperative partner while receiving olfactory information from a rat helping a conspecific in a different room, they helped their non-cooperative partner as if it was a cooperative one. We further show that the cues inducing altruistic behaviour are released during the act of cooperation and do not depend on the identity of the cue provider. Remarkably, olfactory cues seem to be more important for cooperation decisions than experiencing a cooperative act per se. This suggests that rats may signal their cooperation propensity to social partners, which increases their chances to receive help in return.

The social life of Norway rats (Rattus norvegicus).

The Norway rat has important impacts on our life. They are amongst the most used research subjects, resulting in ground-breaking advances. At the same time, wild rats live in close association with us, leading to various adverse interactions. In face of this relevance, it is surprising how little is known about their natural behaviour. While recent laboratory studies revealed their complex social skills, little is known about their social behaviour in the wild. An integration of these different scientific approaches is crucial to understand their social life, which will enable us to design more valid research paradigms, develop more effective management strategies, and to provide better welfare standards. Hence, I first summarise the literature on their natural social behaviour. Second, I provide an overview of recent developments concerning their social cognition. Third, I illustrate why an integration of these areas would be beneficial to optimise our interactions with them.

Rats play tit-for-tat instead of integrating social experience over multiple interactions.

Theoretical models of cooperation typically assume that agents use simple rules based on last encounters, such as 'tit-for-tat', to reciprocate help. By contrast, empiricists generally suppose that animals integrate multiple experiences over longer timespans. Here, we compared these two alternative hypotheses by exposing Norway rats to partners that cooperated on three consecutive days but failed to cooperate on the fourth day, and to partners that did the exact opposite. In additional controls, focal rats experienced cooperating and defecting partners only once. In a bar-pulling setup, focal rats based their decision to provide partners with food on last encounters instead of overall cooperation levels. To check whether this might be owing to a lack of memory capacity, we tested whether rats remember the outcome of encounters that had happened three days before. Cooperation was not diminished by the intermediate time interval. We conclude that rats reciprocate help mainly based on most recent encounters instead of integrating social experience over longer timespans.

Reciprocity: Different behavioural strategies, cognitive mechanisms and psychological processes.

Reciprocity is probably one of the most debated theories in evolutionary research. After more than 40 years of research, some scientists conclude that reciprocity is an almost uniquely human trait mainly because it is cognitively demanding. Others, however, conclude that reciprocity is widespread and of great importance to many species. Yet, it is unclear how these species reciprocate, given its apparent cognitive complexity. Therefore, our aim was to unravel the psychological processes underlying reciprocity. By bringing together findings from studies investigating different aspects of reciprocity, we show that reciprocity is a rich concept with different behavioural strategies and cognitive mechanisms that require very different psychological processes. We reviewed evidence from three textbook examples, i.e. the Norway rat, common vampire bat and brown capuchin monkey, and show that the species use different strategies and mechanisms to reciprocate. We continue by examining the psychological processes of reciprocity. We show that the cognitive load varies between different forms of reciprocity. Several factors can lower the memory demands of reciprocity such as distinctiveness of encounters, memory of details and network size. Furthermore, there are different information operation systems in place, which also vary in their cognitive load due to assessing the number of encounters and the quality and quantity of help. We conclude that many species possess the psychological processes to show some form of reciprocity. Hence, reciprocity might be a widespread phenomenon that varies in terms of strategies and mechanisms.

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.

Revisiting the possibility of reciprocal help in non-human primates.

Reciprocity is a ubiquitous and important human trait. Still, the evolutionary origin is largely unclear, partly because it is believed that our closest living relatives, other primates, do not reciprocate help. Consequently, reciprocity is suggested to have evolved in the human linage only. However, our systematic review of studies investigating reciprocity in non-human primates revealed that, contrary to common perception, there are more positive than negative findings in both experimental and observational studies. Furthermore, we argue that negative findings can provide important insights. We found that reciprocity is not confined to unrelated individuals. In addition, reciprocity can be influenced by the choice of experimental design, relationship quality, social services and temporal scales. Thus, negative findings should not be used as evidence of no reciprocity but as the building blocks for a more comprehensive theory. Based on our review, we conclude that reciprocity in primates is present but underestimated. We close by suggesting further steps that could pave the way for future research aimed at understanding the evolutionary origins of reciprocity.

Spontaneous social tool use in chimpanzees (Pan troglodytes).

Although there is good evidence that social animals show elaborate cognitive skills to deal with others, there are few reports of animals physically using social agents and their respective responses as means to an end-social tool use. In this case study, we investigated spontaneous and repeated social tool use behavior in chimpanzees (Pan troglodytes). We presented a group of chimpanzees with an apparatus, in which pushing two buttons would release juice from a distantly located fountain. Consequently, any one individual could only either push the buttons or drink from the fountain but never push and drink simultaneously. In this scenario, an adult male attempted to retrieve three other individuals and push them toward the buttons that, if pressed, released juice from the fountain. With this strategy, the social tool user increased his juice intake 10-fold. Interestingly, the strategy was stable over time, which was possibly enabled by playing with the social tools. With over 100 instances, we provide the biggest data set on social tool use recorded among nonhuman animals so far. The repeated use of other individuals as social tools may represent a complex social skill linked to Machiavellian intelligence. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Relatedness decreases and reciprocity increases cooperation in Norway rats.

Kin selection and reciprocity are two mechanisms underlying the evolution of cooperation, but the relative importance of kinship and reciprocity for decisions to cooperate are yet unclear for most cases of cooperation. Here, we experimentally tested the relative importance of relatedness and received cooperation for decisions to help a conspecific in wild-type Norway rats (Rattus norvegicus). Test rats provided more food to non-kin than to siblings, and they generally donated more food to previously helpful social partners than to those that had refused help. The rats thus applied reciprocal cooperation rules irrespective of relatedness, highlighting the importance of reciprocal help for cooperative interactions among both related and unrelated conspecifics.

Norway rats (Rattus norvegicus) communicate need, which elicits donation of food.

Reciprocal cooperation has been observed in a wide range of taxa, but the proximate mechanisms underlying the exchange of help are yet unclear. Norway rats reciprocate help received from partners in an iterated Prisoner's Dilemma game. For donors, this involves accepting own costs to the benefit of a partner, without obtaining immediate benefits in return. We studied whether such altruistic acts are conditional on the communication of the recipient's need. Our results show that in a 2-player mutual food-provisioning task, prospective recipients show a behavioral cascade reflecting increasing intensity. First, prospective receivers reach out for the food themselves, then they emit ultrasonic calls toward their partner, before finally showing noisy attention-grabbing behaviors. Food-deprived individuals communicate need more intensively than satiated ones. In return, donors provide help corresponding to the intensity of the recipients' communication. This indicates that rats communicate their need, which changes the helping propensity of potential donors. Communication of need and corresponding adjustment of cooperation may be a widespread proximate mechanism explaining the mutual exchange of services between animals. (PsycINFO Database Record

Reciprocal Trading of Different Commodities in Norway Rats.

The prevalence of reciprocal cooperation in non-human animals is hotly debated [1, 2]. Part of this dispute rests on the assumption that reciprocity means paying like with like [3]. However, exchanges between social partners may involve different commodities and services. Hitherto, there is no experimental evidence that animals other than primates exchange different commodities among conspecifics based on the decision rules of direct reciprocity. Here, we show that Norway rats (Rattus norvegicus) apply direct reciprocity rules when exchanging two different social services: food provisioning and allogrooming. Focal rats were made to experience partners either cooperating or non-cooperating in one of the two commodities. Afterward, they had the opportunity to reciprocate favors by the alternative service. Test rats traded allogrooming against food provisioning, and vice versa, thereby acting by the rules of direct reciprocity. This might indicate that reciprocal altruism among non-human animals is much more widespread than currently assumed.

Experimental evidence for reciprocity in allogrooming among wild-type Norway rats.

If individuals help more those who have previously helped them, stable cooperation may ensue through alternation of roles between donors and recipients. Allogrooming, which is costly to donors and beneficial to recipients, is often exchanged between social partners. Arguably, allogrooming and allopreening are the most frequently exchanged social services and have been used as a standard model of reciprocal cooperation. However, evidence for the application of reciprocity rules among social partners allogrooming each other hitherto is merely correlational. Here, we tested whether female Norway rats (Rattus norvegicus) apply the decision rule characterising direct reciprocity: help someone who has helped you before, by experimentally manipulating both the need for allogrooming and the behavioural response. Furthermore, we checked whether trading of grooming services is influenced by the rank of the social partner. We show that rats groom social partners reciprocally and prefer to do so up the hierarchy, i.e. they groom dominant partners more often than subordinates, while reciprocating with both. This provides experimental evidence that animals render a costly social service by applying reciprocity decision rules when showing a natural hygienic behaviour. The fact that allogrooming is more readily shown up the hierarchy may suggest an appeasing function.