Search

Funding: This study was financially supported by the Swiss National Science Foundation, grant number 31003A_156152, which was awarded to Michael Taborsky. One way to cooperate with others and avoid exploitation is reciprocal cooperation. Reciprocity is the selective helping of those who were cooperative before, which is commonly based on outcomes. Yet, outcomes may not reflect intentions, i.e., if an individual is unable but willing to help. Humans, including children, show such intention-based reciprocity. However, it is unclear whether other animals consider intentions in reciprocal settings. Here, I tested whether Norway rats (Rattus norvegicus) reciprocate help based on intentions by manipulating the outcome while keeping the partner’s cooperative inten-tions the same. Subjects experienced a partner that was able to help by providing food via a movable platform. In another condition, the same partner was unable to help because the platform was blocked. When the roles were exchanged afterwards, subjects provided food more often to ‘able’ than ‘unable’ partners, even though the latter attempted to help. I compare these findings to data using ‘willing’ and ‘unwilling’ partners that were able to help. Again, rats based their cooperative behaviour on outcomes rather than the intention to help. This suggests that rats reciprocate primarily based on outcomes and seem to not consider cooperative intentions. Although, subjects provided consistently less food to partners that did not help, they provided them with some help. Potentially, rats use a cognitively less demanding strategy by helping defectors a bit to maintain cooperation. Thereby, cooperation might be resistant to situations in which an apparent defector was actually unable to help, but had cooperative intentions, and might be a good cooperation partner in the future. Publisher PDF

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.

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.

Funding was provided by the Swiss National Science Foundation grants 31003A_156152 and 31003A 176174 to Michael Taborsky, and P2BEP3 175269 to Manon K. Schweinfurth. 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. Publisher PDF

Humans have a strong sense of fairness and are usually averse to unequal treatment for the same action. Ever since Brosnan and de Waal showed a similar effect in capuchin monkeys (Sapajus apella), numerous studies using different experimental methods have been conducted to investigate whether animals show inequity aversion like humans do. Capuchin monkeys have become one of the best-studied animals in this area. Our first aim in this chapter was to synthesise the findings in this literature. We found that there is mixed evidence for inequity aversion in capuchin monkeys. Our second aim was to understand this variation by focusing on the following factors: the type of task used, the feeding regime outside the experiment and the monkeys’ social environment. To obtain data on some of these factors, as they are not always reported in published studies, we contacted researchers in the main laboratories conducting this work. We found that responses to inequity systematically varied as a function of the task demands and the feeding regime, but not the social environment. Tasks, in particular pulling tasks, that required participants to expend effort to get the food were more likely to detect evidence of inequity aversion. Moreover, monkeys with access to food before or after testing, were more likely to show inequity aversion than those whose access to food was temporarily restricted. We note that our survey is an explorative approach to investigate the variation in reports on inequity aversion in capuchin monkeys. We hope this chapter raises awareness of the complexity of the concept and generates new testable hypotheses, which might advance our understanding of the theoretical foundations of inequity aversion.

In rats as in humans, nonhelping bystanders suppress helping whereas naive bystanders boost helping above individual levels., To investigate whether the classic bystander effect is unique to humans, the effect of bystanders on rat helping was studied. In the presence of rats rendered incompetent to help through pharmacological treatment, rats were less likely to help due to a reduction in reinforcement rather than to a lack of initial interest. Only incompetent helpers of a strain familiar to the helper rat exerted a detrimental effect on helping; rats helped at near control levels in the presence of incompetent helpers from an unfamiliar strain. Duos and trios of potential helper rats helped at superadditive rates, demonstrating that rats act nonindependently with helping facilitated by the presence of competent-to-help bystanders. Furthermore, helping was facilitated in rats that had previously observed other rats’ helping and were then tested individually. In sum, the influence of bystanders on helping behavior in rats features characteristics that closely resemble those observed in humans.

Funding was provided by SNF-grant 31003A_156152 to M.T. and P2BEP3 175269 to M.K.S. Theoretical models of cooperation typically assume that agents use simple rules based on last encounters, such as “tit-for-tat”, to reciprocate help. In 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 due 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. Postprint

This research was supported by the European Research Council (Synergy Grant 609819 SOMICS to Josep Call). Manon K. Schweinfurth was supported by the Swiss National Science Foundation (Grant P2BEP3 175269). 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. Postprint

Funding was provided by SNF-grant 31003A_156152 to M.T. Direct reciprocity can establish stable cooperation. Nevertheless, the significance of this mechanism is yet unclear. A frequent assumption is that both commodity and context should be the same when help is exchanged between social partners. Yet, an exchange of different favours appears more likely in a natural setting. This is assumed to be cognitively demanding, however, because experienced help in one context needs to change the motivation to help by different means or in a different context. We tested whether Norway rats, Rattus norvegicus, transfer help from one cooperative task to another. Individuals could provide food to previously either cooperating or defecting partners by using a different mechanism to produce food for their partner than the partner had used to help them. Test subjects indeed helped previously cooperative partners more often than defecting ones by using a different provisioning mechanism. This implies that rats realize the cooperative propensity of social partners, which they consequently reward by help of a different kind; hence, they do not merely copy experienced helping behaviour. Our results suggest that animals other than primates are capable of transferring help between different contexts, which highlights new possibilities for the occurrence of reciprocal altruism involving different commodities and services in nature. Postprint

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. Publisher PDF

Funding was provided by the Swiss National Science Foundation grants 31003A_156152 and 31003A 176174 to M.T. and P2BEP3 175269 to M.K.S. Reciprocal cooperation may evolve if the costs of help are reliably compensated for by delayed returns provided in future interactions. The associated probabilities and cost–benefit ratios may vary systematically between the sexes, which often display different dispersal strategies and interaction patterns. Whereas female Norway rats, Rattus norvegicus, are known to apply direct and generalized decision rules of reciprocal cooperation, the rules according to which males reciprocate favours are less well understood. Therefore, we investigated the cooperation propensity of male wild-type Norway rats. Male test rats experienced cooperating partners that provided food to them, or defecting partners that refused to provide help. Afterwards, test rats could donate food to previously experienced or unknown partners, resembling direct and generalized reciprocity paradigms, respectively. Male rats cooperated according to direct reciprocity, suggesting that this decision rule is similarly important for both sexes. However, whereas females additionally help according to generalized reciprocity, males did not apply this rule. These results suggest a sex difference in reciprocal decision rules, highlighting the potential importance of different interaction patterns and cost–benefit ratios between the sexes. Postprint

Funding was provided by SNF grants 310030B_138660 and 31003A_156152 to Michael Taborsky. Norway rats (Rattus norvegicus) cooperate according to indirect reciprocity, which implies the involvement of a reputation mechanism. Here, we test whether the rats employ such mechanism in repeated cooperative interactions. Focal subjects were first trained individually to pull food towards a social partner. During the experiment, the focal rats were confronted with two types of trained social partners: one always cooperated and the other one always defected, either in the presence or in the absence of an audience. Based on the hypotheses that the rats possess a reputation mechanism involving image scoring, we predicted them to be more helpful in the presence of an audience, independently of the partner's cooperative behaviour. If, in contrast, reputation involved a standing strategy, we predicted the rats to distinguish more between cooperators and defectors in the presence of an audience than in its absence. The rats helped cooperative partners more than defectors, but against both predictions the presence or absence of an audience did not influence their helping propensity. This indicates that either reputation is not included in the decision of rats to help an individual that has helped others, or that reputation is neither involving image scoring nor a standing strategy. Although the rats have been shown to modulate their decision to help a social partner based on its helpful behaviour towards others, they do not seem to adjust their behaviour strategically to the presence of an audience. Postprint

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.

Funding was provided by Swiss National Science Foundation (SNF) grants 310030B_138660 and 31003A_156152 to Michael Taborsky. 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. Postprint

Funding was provided by Swiss National Science Foundation grants 310030B_138660 and 31003A_ 156152 to M.T. 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. Postprint

Reciprocity can generate stable levels of cooperation among unrelated social partners. If individuals interact repeatedly, costs of altruistic acts can be compensated through an exchange of donor and receiver roles. Frequent interactions are conducive to attaining evolutionarily stable reciprocal exchange. High interaction frequencies are typical for group members maintaining close relationships among one another, which may thereby facilitate reciprocity. Norway rats (Rattus norvegicus) are highly social animals that were experimentally shown to reciprocally exchange food donations and allogrooming. Here, we tested experimentally the relationship between reciprocal cooperation and other social behaviours exchanged within dyads of wild-type Norway rats. In particular, we asked whether and how interactions differing in quality (characterised by affiliative and aggressive behaviours) influence reciprocal exchanges of different social services. Our experiment involved three steps: Focal individuals experienced social partners that were either providing them with food or not, via a learnt stick-pulling task. Thereafter, they could either interact physically with these partners, or not. Subsequently, we induced allogrooming among them by applying saltwater to an inaccessible part of the body, and tested for the reciprocation of allogrooming. When individuals were allowed to interact freely, previously cooperative food providers exhibited more aggression towards focal individuals than previously uncooperative partners, which might reflect an attempt to coercively demand a return of food provisioning from focal rats. Higher frequencies of affiliative behaviours and lower frequencies of aggressive behaviours experienced during the unrestricted interaction phase tended to increase the focal rats’ propensity to engage in grooming the partner in the subsequent induced allogrooming phase. This suggests that affiliative and aggressive behaviours affect the allogrooming propensity of rats. In particular, higher frequencies of received aggression decreased the propensity to reciprocate previously received cooperation. We provide experimental evidence that rats are more likely to groom partners that pulled a stick to deliver food to them. Reciprocal exchange of allogrooming depends apparently on experienced cooperation, but also on the quality of the social relationship. Close social relationships among individuals may enhance reciprocal exchange of services and thereby ensure long-term cooperation. Thus, we tested whether in unrelated and previously unfamiliar Norway rats, the quality of social interactions, that is, the amount of exchanged affiliative and aggressive behaviours, affects reciprocal cooperation, and whether received cooperation in turn predicts subsequent social behaviour. Our results show that focal individuals are generally more helpful to previously helpful partners, but that the quality of social interactions may modify their decision to cooperate. Received aggressive and affiliative behaviours affected the subsequent reciprocal exchange of hygienic behaviour. Moreover, received food provisioning affected the exchange of cooperative, affiliative and aggressive behaviours also outside of a food-provisioning context. These data reveal a close relationship between the exchange of social behaviours between individuals and their propensity to cooperate with one another.

Funding was provided by SNF-grant 31003A_156152 to Michael Taborsky. 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. Publisher PDF

Social bonds reflect specific and enduring relationships among conspecifics. In some group-living animals, they have been found to generate immediate and long-term fitness benefits. It is currently unclear how important and how widespread social bonds are in animals other than primates. It has been hypothesized that social bonds may help in establishing stable levels of reciprocal cooperation. Norway rats (Rattus norvegicus) reciprocate received help to an unrelated social partner. It is hitherto unknown, however, whether this cooperative behaviour is based on the establishment of social bonds among involved individuals. Norway rats live in social groups that can be very large; hence, without bonds, it may be difficult to keep track of other individuals and their previous behaviour, which is a precondition for generating evolutionarily stable levels of cooperation based on direct reciprocity. Here we tested whether wild-type female rats form bonds among each other, which are stable both over time and across different contexts. In addition, we scrutinized the potential influence of social rank on the establishment of bonds. Despite the fact that the hierarchy structure within groups remained stable over the study period, no stable social bonds were formed between group members. Apparently, social information from consecutive encounters with the same social partner is not accumulated. The lack of long-term social bonds might explain why rats base their decisions to cooperate primarily on the last encounter with a social partner, which may differ from other animals where cooperation is based on the existence of long-term social bonds. Social bonds have been hypothesized to favour reciprocal cooperation. Norway rats reciprocate help received from a social partner, but it is hitherto unclear whether they form social bonds that might further such cooperative behaviour. Here we tested whether female Norway rats engage in social relationships with a same-sex partner, which are stable over time and across contexts. In contrast to the hypothesized existence of bonds among long-term group members, our results provide no evidence that rats form specific social relationships. Rather than accumulating social information into social bonds, rats apparently base their decision to cooperate merely on the outcome of recent encounters.