Marie Pelé

Calculated reciprocity after all: computation behind token transfers in orang-utans

Transfers and services are frequent in the animal kingdom. However, there is no clear evidence in animals that such transactions are based on weighing costs and benefits when giving or returning favours and keeping track of them over time (i.e. calculated reciprocity). We tested two orang-utans (Pongo pygmaeus abelii) in a token-exchange paradigm, in which each individual could exchange a token for food with the experimenter but only after first obtaining the token from the other orang-utan. Each orang-utan possessed tokens valuable to their partner but useless to themselves. Both orang-utans actively transferred numerous tokens (mostly partner-valuable) to their partner. One of the orang-utans routinely used gestures to request tokens while the other complied with such requests. Although initially the transfers were biased in one direction, they became more balanced towards the end of the study. Indeed, data on the last three series produced evidence of reciprocity both between and within trials. We observed an increase in the number and complexity of exchanges and alternations. This study is the first experimental demonstration of the occurrence of direct transfers of goods based on calculated reciprocity in non-human-primates.

Social networks in primates: smart and tolerant species have more efficient networks

Network optimality has been described in genes, proteins and human communicative networks. In the latter, optimality leads to the efficient transmission of information with a minimum number of connections. Whilst studies show that differences in centrality exist in animal networks with central individuals having higher fitness, network efficiency has never been studied in animal groups. Here we studied 78 groups of primates (24 species). We found that group size and neocortex ratio were correlated with network efficiency. Centralisation (whether several individuals are central in the group) and modularity (how a group is clustered) had opposing effects on network efficiency, showing that tolerant species have more efficient networks. Such network properties affecting individual fitness could be shaped by natural selection. Our results are in accordance with the social brain and cultural intelligence hypotheses, which suggest that the importance of network efficiency and information flow through social learning relates to cognitive abilities.

Token Transfers Among Great Apes (Gorilla gorilla, Pongo pygmaeus, Pan paniscus, and Pan troglodytes): Species Differences, Gestural Requests, and Reciprocal Exchange

Great apes appear to be the nonhuman primates most capable of recognizing trading opportunities and engaging in transfers of commodities with conspecifics. Spontaneous exchange of goods between them has not yet been reported. We tested gorillas (Gorilla gorilla), orangutans (Pongo pygmaeus), bonobos (Pan paniscus), and chimpanzees (Pan troglodytes) in a token-exchange task involving two conspecifics and a human experimenter. Tested in pairs, subjects had to exchange tokens with a partner to obtain food from the experimenter. We observed 4, 5, 264, and 328 transfers of tokens in gorillas, chimpanzees, orangutans, and bonobos, respectively. Most gifts were indirect in gorillas, chimpanzees, and bonobos, whereas most were direct in orangutans. The analysis showed no evidence of calculated reciprocity in interactions. A main finding of the study was the high rate of repeated gifts and begging gestures recorded in orangutans. This raises the question of the meaning of pointing in great apes and their ability to understand the communicative intent of others.

Fast and Accurate Decisions as a Result of Scale-Free Network Properties in Two Primate Species

The influence of particular individuals on others opinions and behaviours has long been studied by social and political scientists, and it is often suggested that certain individuals can act as leaders because they are socially connected, and have more ‘influence’ over others. However, this idea is difficult to test in a real-world (human or non-human) setting. Here, we present a study that describes the collective movements of two primate species: Macaca tonkeana and Macaca mulatta faced with the decision of when to stop resting and start foraging. We show that individuals that are central to the group’s social network elicit stronger follower behaviour and are crucial to the achievement of consensus decisions. This ‘embedded’ leader-follower dynamic improves the efficiency of the decision-making process, enabling faster decision times. Our data additionally suggest that a behavioural rule-of-thumb ‘follow my close affiliate’ can result in the most central individual leading decisions by virtue of the scale-free properties of the network. This may allow groups to utilise the knowledge of elder, dominant, or natal individuals (who are often central in social networks) whilst simultaneously maintaining bonds with highly social individuals which may bring indirect fitness benefits itself.

Monkeys fail to reciprocate in an exchange task.

Exchanges form the basis of human economies. Animals too can engage in reciprocal interactions but they do not barter goods like humans, which raises the question of the abilities necessary for trading to occur. Previous studies have shown that non-human primates can exchange food with human partners. Here, we tested the ability of brown capuchin monkeys and Tonkean macaques to reciprocate in a task requiring two conspecifics to exchange tokens in order to obtain rewards from an experimenter. We recorded 56 transfers between subjects in capuchin monkeys and 10 in Tonkean macaques. All transfers were passive in both species. Capuchins preferentially picked up tokens valuable for them in the partner’s compartment. They tended to manipulate the partner-valued tokens more often than the no-value ones, leading to more opportunities for these tokens to end up within reach of the partner. Despite optimal conditions where values of goods were defined and known by partners, however, none of the pairs tested engaged in short-term reciprocal interactions. These results indicate that calculated reciprocity was difficult if not impossible in the animals tested.

Decision-making theories: linking the disparate research areas of individual and collective cognition

In order to maximize their fitness, animals have to deal with different environmental and social factors that affect their everyday life. Although the way an animal behaves might enhance its fitness or survival in regard to one factor, it could compromise them regarding another. In the domain of decision sciences, research concerning decision making focuses on performances at the individual level but also at the collective one. However, between individual and collective decision making, different terms are used resulting in little or no connection between both research areas. In this paper, we reviewed how different branches of decision sciences study the same concept, mainly called speed-accuracy trade-off, and how the different results are on the same track in terms of showing the optimality of decisions. Whatever the level, individual or collective, each decision might be defined with three parameters: time or delay to decide, risk and accuracy. We strongly believe that more progress would be possible in this domain of research if these different branches were better linked, with an exchange of their results and theories. A growing amount of literature describes economics in humans and eco-ethology in birds making compromises between starvation, predation and reproduction. Numerous studies have been carried out on social cognition in primates but also birds and carnivores, and other publications describe market or reciprocal exchanges of commodities. We therefore hope that this paper will lead these different areas to a common decision science.

Different risk thresholds in pedestrian road crossing behaviour: A comparison of French and Japanese approaches

When crossing the road, pedestrians have to make a trade-off between saving time and avoiding any risk of injuries. Here, we studied how culture influences an individuals perception of risks when crossing a street, using survival analysis. This study is the first to use this analysis to assess cognitive mechanisms and optimality of decisions underlying road crossing behaviour. We observed pedestrian behaviour in two city centres: Inuyama (Japan) and Strasbourg (France). In each city, observations were made at a safe site consisting of a crosswalk and a street light and at an unsafe site (i.e. no crosswalk or street light). At the unsafe site, we measured the time needed by a pedestrian to take a decision (Tdec). During Tdec, a pedestrian estimates whether he can (Tsafe) or cannot (Trisk) cross the road. Using survival analysis, we studied the distributions of these three time variables and showed that French pedestrians took more risks than Japanese pedestrians, and that males took more risks than females, but only in Japan. More studies would considerably broaden our understanding on how culture may affect decision-making processes under risky circumstances.

Interspecies sexual behaviour between a male Japanese macaque and female sika deer

Interspecies sexual behaviour or ‘reproductive interference’ has been reported across a wide range of animal taxa. However, most of these occurrences were observed in phylogenetically close species and were mainly discussed in terms of their effect on fitness, hybridization and species survival. The few cases of heterospecific mating in distant species occurred between animals that were bred and maintained in captivity. Only one scientific study has reported this phenomenon, describing sexual harassment of king penguins by an Antarctic fur seal. This is the first article to report mating behaviour between a male Japanese macaque (Macaca fuscata yakui) and female sika deer (Cervus nippon yakushimae) on Yakushima Island, Japan. Although Japanese macaques are known to ride deer, this individual showed clearly sexual behaviour towards several female deer, some of which tried to escape whilst others accepted the mount. This male seems to belong to a group of peripheral males. Although this phenomenon may be explained as copulation learning, this is highly unlikely. The most realistic hypothesis would be that of mate deprivation, which states that males with limited access to females are more likely to display this behaviour. Whatever the cause for this event may be, the observation of highly unusual animal behaviour may be a key to understanding the evolution of heterospecific mating behaviour in the animal kingdom.

Social network and decision-making in primates: a report on Franco-Japanese research collaborations.

Sociality is suggested to evolve as a strategy for animals to cope with challenges in their environment. Within a population, each individual can be seen as part of a network of social interactions that vary in strength, type and dynamics (Sueur et al. 2011a). The structure of this social network can strongly impact upon not only on the fitness of individuals and their decision-making, but also on the ecology of populations and the evolution of a species. Our Franco-Japanese collaboration allowed us to study social networks in several species (Japanese macaques, chimpanzees, colobines, etc.) and on different topics (social epidemiology, social evolution, information transmission). Individual attributes such as stress, rank or age can affect how individuals take decisions and the structure of the social network. This heterogeneity is linked to the assortativity of individuals and to the efficiency of the flow within a network. It is important, therefore, that this heterogeneity is integrated in the process or pattern under study in order to provide a better resolution of investigation and, ultimately, a better understanding of behavioural strategies, social dynamics and social evolution. How social information affects decision-making could be important to understand how social groups make collective decisions and how information may spread throughout the social group. In human beings, road-crossing behaviours in the presence of other individuals is a good way to study the influence of social information on individual behaviour and decision-making, for instance. Culture directly affects which information — personal vs social — individuals prefer to follow. Our collaboration contributed to the understanding of the relative influence of different factors, cultural and ecological, on primate, including human, sociality.

Risk should be objectively defined: reply to Zentall and Smith

Zentall and Smith (2014) have published a comment on Pelé and Sueur (Anim Cogn 16:543–556, 2013) in which they raise two issues, one about the definition of risk and a second concerning the optimality of decisions. When making a choice, subjects are faced not only with several possible alternatives but also with the risk of opting for an unsuitable choice which depends on several variables (context, internal state, knowledge and perception). Although it is true that animals might learn about their environment and adapt their decisions to the context and to their experience, strong constraints make some behavioural traits stable over individual lifetime and even generations. We therefore consider that experience has limited impact on the variability of temporal discounting. These behavioural traits make the difference between perceived and actual risk. If the perceived risk strongly differs from the actual risk, a decision should be considered as suboptimal. If we want to lead individual and collective cognition to a common decision science, it is crucial to use the same definitions for terms implied in decision-making.