Prosocial behaviour emerges independent of reciprocity in cottontop tamarins

The cooperative breeding hypothesis posits that cooperatively breeding species are motivated to act prosocially, that is, to behave in ways that provide benefits to others, and that cooperative breeding has played a central role in the evolution of human prosociality. However, investigations of prosocial behaviour in cooperative breeders have produced varying results and the mechanisms contributing to this variation are unknown. We investigated whether reciprocity would facilitate prosocial behaviour among cottontop tamarins, a cooperatively breeding primate species likely to engage in reciprocal altruism, by comparing the number of food rewards transferred to partners who had either immediately previously provided or denied rewards to the subject. Subjects were also tested in a non-social control condition. Overall, results indicated that reciprocity increased food transfers. However, temporal analyses revealed that when the tamarins'' behaviour was evaluated in relation to the non-social control, results were best explained by (i) an initial depression in the transfer of rewards to partners who recently denied rewards, and (ii) a prosocial effect that emerged late in sessions independent of reciprocity. These results support the cooperative breeding hypothesis, but suggest a minimal role for positive reciprocity, and emphasize the importance of investigating proximate temporal mechanisms underlying prosocial behaviour.     

The role of social context and individual experience in novel task acquisition in cottontop tamarins, Saguinus oedipus

In socially tolerant settings, na?ve individuals may have opportunities to interact jointly with knowledgeable demonstrators and novel tasks. This process is expected to facilitate social learning. Individual experience may also be important for reinforcing and honing socially acquired behaviours. We examined the role of joint interaction and individual experience in the acquisition of a novel foraging task in captive cottontop tamarins. The task involved learning how to locate and access two hidden food rewards from among 10 differently cued forage sites. Tamarins were tested in three different conditions: (1) individually, (2) while interacting with a na?ve mate, and (3) while interacting with a mate trained as a knowledgeable demonstrator. For tamarins tested with mates present, we interspersed social input test days with exposure to the task while alone. Tamarins were tested again 17 months after their last exposure to the task, to assess long-term memory. All tamarins tested with knowledgeable demonstrators solved the task. In contrast, tamarins tested alone or with na?ve mates had similarly high levels of neophobia and low levels of task acquisition. We conclude that joint interaction occurs in mated pairs of cottontop tamarins and facilitates the spread of novel behaviour. Interspersing test days with a knowledgeable demonstrator present and test days alone with the task helped tamarins to achieve the ultimate goal of the task: obtaining food rewards. Tamarins performed similarly when tested 17 months later, regardless of their initial learning environment. Tamarins had memory deficits for the location of hidden food rewards, but retained memory of the necessary motor actions and solved the task.     

What chimpanzees (Pan troglodytes) learn in a cooperative task

To examine the development of cooperation in a captive group of chimpanzees (Pan troglodytes), we designed an apparatus which required the simultaneous traction by two animals to get a reward. Two chimpanzees, an adult male and an infant female in a group of six, produced most of the successful responses (pulling on two handles simultaneously). Visual behavior was used to try to determine what chimpanzees learned about the cooperative task. Propositions were made to investigate what kind of learning could be attributed to chimpanzees and were confronted with results. Both subjects learned the link between the presence of fruits on the apparatus and the possibility of getting a fruit. They also learned the importance of the partner at the apparatus to make a successful response. Only the adult male learned to take into account the behavior of the partner at the apparatus before pulling a handle. From a methodological point of view, the glances made by the animals can constitute a useful behavioral indicator of what the subjects learned in a given social situation.     

Blue-throated macaws (Ara glaucogularis) succeed in a cooperative task without coordinating their actions

Social complexity may select for socio-cognitive abilities. The “loose string” task has become a comparative benchmark paradigm for investigating cooperative problem-solving abilities in many species, thus enhancing our understanding of their evolution. It requires two individuals working together to solve a problem, specifically by pulling the two ends of a string simultaneously to move a reward towards them. A dyad's performance therefore depends on the individuals’ ability to coordinate their pulling action. Many species, including corvids and parrots, have been tested in this paradigm, but most appear insensitive to the exact cooperative nature of the task. We tested another parrot species, blue-throated macaws, to further our understanding of social cognition in psittacids. Five birds were tested with different partners in a dyadic setting. The study included two control conditions examining the cognitive mechanism underlying their seemingly cooperative behaviour. All birds were able to simultaneously pull the strings, but their performance did not drop when they were denied mutual visual access, and they failed to obtain food when they needed to wait for their partner. Moreover, the parrots decreased their latency to pull with increasing experience. These findings suggest that the birds may have applied an associatively learnt rule, or relied on acoustic cues, rather than coordinating their actions with the partner. This may not necessarily prove a lack of understanding the partner's role, given that their failure to wait in the delay control test might be explained by their poor inhibitory control abilities. Relationship quality (i.e. affiliation and food tolerance) did not influence dyadic success. Future studies are needed in order to disentangle macaws’ potentially limited cooperative abilities from their lack of inhibitory control.     

Behavioral and physiological response to inequity in bonobos (Pan paniscus)

Inequity aversion (IA), the affective, cognitive, and behavioral response to inequitable outcomes, allows individuals to avoid exploitation and therefore stabilizes cooperation. The presence of IA varies across animal species, which has stimulated research to investigate factors that might explain this variation, and to investigate underlying affective responses. Among great apes, IA is most often studied in chimpanzees. Here, we investigate IA in bonobos, a reputedly tolerant and cooperative species for which few IA studies are available. We describe how bonobos respond to receiving less preferred rewards than a partner in a token exchange task. We show that bonobos respond to receiving less preferred rewards by refusing tokens and rewards, and by leaving the experimental area. Bonobos never refused a trial when receiving preferred rewards, and thus showed no advantageous IA. We also investigate the variability in the disadvantageous IA response on a dyadic level, because the level of IA is expected to vary, depending on characteristics of the dyad. Like in humans and chimpanzees, we show that the tolerance towards inequity was higher in bonobo dyads with more valuable relationships. To study the affective component of IA, we included behavioral and physiological measures of arousal: a displacement behavior (rough self-scratching) and changes in salivary cortisol levels. Both measures of arousal showed large variability, and while analyses on rough self-scratching showed no significant effects, salivary cortisol levels seemed to be lower in subjects that received less than their partner, but higher in subjects that received more than their partner, albeit that both were not significantly different from the equity condition. This suggests that although overcompensated bonobos showed no behavioral response, they might be more aroused. Our data support the cooperation hypothesis on an interspecific and intraspecific level. They show inequity aversion in bonobos, a reputedly cooperative species, and suggest that the variability in IA in bonobos can be explained by their socioecology. Most successful cooperative interactions happen between mothers and their sons and among closely bonded females. The limited need to monitor the partners' investment within these dyads can result in a higher tolerance towards inequity. We therefore suggest future studies to consider relevant socioecological characteristics of the species when designing and analyzing IA studies.     

Ontogeny of tool use in cottontop tamarins, Saguinus oedipus: innate recognition of functionally relevant features

Adult cottontop tamarins are sensitive to the functionally relevant and irrelevant features of objects used as tools to gain access to food. We conducted four experiments designed to assess whether infant cottontop tamarins show comparable sensitivities to functionally relevant and irrelevant features. All subjects were reared in a species-typical social environment, but prior to the present studies had never participated in any experiments, and had no access to tools or other freely moving, manipulable objects with the exception of food. Despite their lack of experience, the pattern of object choice by infants precisely mirrored those obtained with adults. Specifically, having learned to use a hard blue cane to retrieve food (experiment 1), infant tamarins immediately generalized to other objects (experiments 2-4), recognizing that changes in colour and texture play no role in an object's functionality as a tool, whereas changes in size and shape do. These data suggest that for cottontop tamarins, a species that does not naturally use tools, and infrequently manipulates objects, that the capacity to distinguish between functionally relevant and irrelevant features develops in the absence of domain-specific experience.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Partner's behavior, not reward distribution, determines success in an unequal cooperative task in capuchin monkeys

It was recently demonstrated that capuchin monkeys notice and respond to distributional inequity, a trait that has been proposed to support the evolution of cooperation in the human species. However, it is unknown how capuchins react to inequitable rewards in an unrestricted cooperative paradigm in which they may freely choose both whether to participate and, within the bounds of their partner's behavior, which reward they will receive for their participation. We tested capuchin monkeys with such a design, using a cooperative barpull, which has been used with great success in the past. Contrary to our expectations, the equity of the reward distribution did not affect success or pulling behavior. However, the behavior of the partner in an unequal situation did affect overall success rates: pairs that had a tendency to alternate which individual received the higher-value food in unequal reward situations were more than twice as successful in obtaining rewards than pairs in which one individual dominated the higher-value food. This ability to equitably distribute rewards in inherently biased cooperative situations has profound implications for activities such as group hunts, in which multiple individuals work together for a single, monopolizable reward.     

Lack of prosociality in great apes,capuchin monkeys and spider monkeys: convergent evidence from two different food distribution tasks

Prosociality can be defined as any behaviour performed to alleviate the needs of others or to improve their welfare. Prosociality has probably played an essential role in the evolution of cooperative behaviour and several studies have already investigated it in primates to understand the evolutionary origins of human prosociality. Two main tasks have been used to test prosociality in a food context. In the Platforms task, subjects can prosocially provide food to a partner by selecting a prosocial platform over a selfish one. In the Tokens task, subjects can prosocially provide food to a partner by selecting a prosocial token over a selfish one. As these tasks have provided mixed results, we used both tasks to test prosociality in great apes, capuchin monkeys and spider monkeys. Our results provided no compelling evidence of prosociality in a food context in any of the species tested. Additionally, our study revealed serious limitations of the Tokens task as it has been previously used. These results highlight the importance of controlling for confounding variables and of using multiple tasks to address inconsistencies present in the literature.     

Adult Cleaner Wrasse Outperform Capuchin Monkeys,Chimpanzees and Orang-utans in a Complex Foraging Task Derived from Cleaner – Client Reef Fish Cooperation

The insight that animals'' cognitive abilities are linked to their evolutionary history, and hence their ecology, provides the framework for the comparative approach. Despite primates renowned dietary complexity and social cognition, including cooperative abilities, we here demonstrate that cleaner wrasse outperform three primate species, capuchin monkeys, chimpanzees and orang-utans, in a foraging task involving a choice between two actions, both of which yield identical immediate rewards, but only one of which yields an additional delayed reward. The foraging task decisions involve partner choice in cleaners: they must service visiting client reef fish before resident clients to access both; otherwise the former switch to a different cleaner. Wild caught adult, but not juvenile, cleaners learned to solve the task quickly and relearned the task when it was reversed. The majority of primates failed to perform above chance after 100 trials, which is in sharp contrast to previous studies showing that primates easily learn to choose an action that yields immediate double rewards compared to an alternative action. In conclusion, the adult cleaners'' ability to choose a superior action with initially neutral consequences is likely due to repeated exposure in nature, which leads to specific learned optimal foraging decision rules.     

Monkeys and apes: Are their cognitive skills really so different?

Differences in cognitive skills across taxa, and between monkeys and apes in particular, have been explained by different hypotheses, although these often are not supported by systematic interspecific comparisons. Here, we directly compared the cognitive performance of the four great apes and three monkey species (spider monkeys, capuchin monkeys, and long‐tailed macaques), differing in their phylogenetic‐relatedness and socioecology. We tested subjects on their ability to remember object locations (memory task), track object displacements (transposition task), and obtain out‐of‐reach rewards (support task). Our results showed no support for an overall clear‐cut distinction in cognitive skills between monkeys and apes as species performance varied substantially across tasks. Although we found differences in performance at tracking object displacements between monkeys and apes, interspecific differences in the other two tasks were better explained in terms of differential socioecology, especially differential levels of fission–fusion dynamics. A cluster analysis using mean scores of each condition of the three tasks for each species suggested that the only dichotomy might be between members of the genus Pan and the rest of the tested species. These findings evidence the importance of using multiple tasks across multiple species in a comparative perspective to test different explanations for the enhancement of specific cognitive skills. Am J Phys Anthropol 143:188–197, 2010. © 2010 Wiley‐Liss, Inc.     

The ecology and evolution of patience in two New World monkeys

Decision making often involves choosing between small, short-term rewards and large, long-term rewards. All animals, humans included, discount future rewards--the present value of delayed rewards is viewed as less than the value of immediate rewards. Despite its ubiquity, there exists considerable but unexplained variation between species in their capacity to wait for rewards--that is, to exert patience or self-control. Using two closely related primates--common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus)--we uncover a variable that may explain differences in how species discount future rewards. Both species faced a self-control paradigm in which individuals chose between taking an immediate small reward and waiting a variable amount of time for a large reward. Under these conditions, marmosets waited significantly longer for food than tamarins. This difference cannot be explained by life history, social behaviour or brain size. It can, however, be explained by feeding ecology: marmosets rely on gum, a food product acquired by waiting for exudate to flow from trees, whereas tamarins feed on insects, a food product requiring impulsive action. Foraging ecology, therefore, may provide a selective pressure for the evolution of self-control.     

Seed Swallowing in Tamarins: Evidence of a Curative Function or Enhanced Foraging Efficiency?

Nonhuman primates represent a major component of the frugivore biomass in several rain-forest communities. Although there is considerable evidence that prosimians, monkeys, and apes serve as dispersal agents for many tropical trees, little attention has been paid to the more basic questions of why certain species of primates swallow and void seeds, and what, if any, are the advantages to an animal of having a large, hard, bolus pass through its digestive tract. We examine patterns of fruit-eating and seed-swallowing in two species of free-ranging tamarins: Saguinus mystax and Saguinus geoffroyi. Fruits commonly eaten by tamarins contain large seeds surrounded by a fibrous and adhesive pulp or arilate seed coat. They generally swallow seeds and pulp together. Intact seeds are voided over a 1- to 3-h period. Measurements of 132 seeds naturally voided by Panamanian tamarins average 11.2 mm in length and 0.3 g. The greatest number of large seeds contained in the digestive tract of a single animal at one time was 13. In the case of moustached tamarins, we collected 220 seeds. Average seed length is 11.9 mm and average seed weight is 0.3 g. At the time of capture, one animal had 26 seeds in its digestive tract. In both tamarin species, there is evidence of sex-based differences in feeding behavior. Adult female moustached and Panamanian tamarins swallowed and voided seeds of larger size than adult males did. Seed size is positively correlated with pulp weight (p <. 001), therefore females were selecting food items with higher nutritional rewards than adult males did. Given their small body size and relatively short digestive tract, why do tamarins swallow such large seeds? Although several explanations are possible, we propose that the large number and size of undigested seeds continuously passing through the tamarin gut serve a curative role in mechanically dislodging and expelling intestinal parasites—Ancanthocephala (spiny-headed worms)—from their digestive tracts.     

Capuchins do cooperate: the advantage of an intuitive task

We used a cooperative pulling task to examine proximate aspects of cooperation in captive brown capuchin monkeys, Cebus apella. Specifically, our goal was to determine whether capuchins can learn the contingency between their partner's participation in a task and its successful completion. We examined whether the monkeys visually monitored their partners and adjusted pulling behaviour according to their partner's presence. Results on five same-sex pairs of adults indicate that (1) elimination of visual contact between partners significantly decreased success, (2) subjects glanced at their partners significantly more in cooperative tests than in control tests in which no partner-assistance was needed, and (3) they pulled at significantly higher rates when their partner was present rather than absent. Therefore, in contrast to a previous report by Chalmeau et al. (1997, Animal Behaviour, 54, 1215-1225), cooperating capuchins do seem able to take the role of their partner into account. However, the type of task used may be an important factor affecting the level of coordination achieved. Copyright 2000 The Association for the Study of Animal Behaviour.     

Cooperative Problem Solving by Orangutans (Pongo pygmaeus)

A captive pair of subadult male orangutans (Pongo pygmaeus) performed a cooperative task without training. Both partners had to pull a handle simultaneously in order for each to get food. They also learned the importance of the partner at the apparatus to make a successful response. The requirements of the cooperative task appear to have been understood by the orangutans, much like chimpanzees (Pan troglodytes) in the same situation. In contrast, capuchins (Cebus apella) succeeded in the cooperative task with a limited understanding of the requirement of the task and without taking into account the partner's role. These results gives further support to the hypothesis of a proximity of cognitive processes between chimpanzees and orangutans (in contrast to monkeys) though orangutans have not been seen to hunt cooperatively in the wild.     

Will travel for food: spatial discounting in two new world monkeys

Nonhuman animals steeply discount the future, showing a preference for small, immediate over large, delayed rewards. Currently unclear is whether discounting functions depend on context. Here, we examine the effects of spatial context on discounting in cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus), species known to differ in temporal discounting. We presented subjects with a choice between small, nearby rewards and large, distant rewards. Tamarins traveled farther for the large reward than marmosets, attending to the ratio of reward differences rather than their absolute values. This species difference contrasts with performance on a temporal task in which marmosets waited longer than tamarins for the large reward. These comparative data indicate that context influences choice behavior, with the strongest effect seen in marmosets who discounted more steeply over space than over time. These findings parallel details of each species' feeding ecology. Tamarins range over large distances and feed primarily on insects, which requires using quick, impulsive action. Marmosets range over shorter distances than tamarins and feed primarily on tree exudates, a clumped resource that requires patience to wait for sap to exude. These results show that discounting functions are context specific, shaped by a history of ecological pressures.     

A nonhuman primate's perception of object relations: experiments on cottontop tamarins, Saguinus oedipus

Objects in nature often have spatial and functional relationships with other objects. For example, fruit may be connected to tree branches, bushes sometimes function as landmarks for home, and stones are functionally associated with nuts when they are used to crack the nuts open. Although animals may use the spatial and functional relationships between specific objects, it is important for ethologists interested in cognitive mechanisms to ask whether animals understand the spatial relationship between objects in a more general and abstract way. In this experiment, we ask whether a small New World monkey, the cottontop tamarin, is capable of perceiving the abstract relational concept of ‘connectedness’. Using a traditional operant paradigm, subjects were required to press one button to images with connected objects, and another button to images with separated objects. In Phase 1 of the experiment, subjects received training with only one connected and one separated image. Following training, probe images were presented in which features such as colour, texture and shape were systematically manipulated to determine which features were more important in stimulus classification. Accuracies and reaction times of responses were recorded. On the basis of their performance, the tamarins appeared to recognize that changes in the colour or texture of two objects plays no functional role in determining whether such objects are connected or separated. In contrast, changes in the shape and distance between two objects does play an important functional role, and the tamarins appeared to be sensitive to such changes. In Phase 2, subjects received training with a larger set of images. After this training, classification accuracy remained significantly above chance with most probes, suggesting that the tamarins had acquired a more general connectedness concept. In Phase 3, novel images were presented. Classification accuracy was significantly above chance for many of the novel images. Overall, results suggest that tamarins perceive spatial relationships between stimuli to some extent and can classify images based in part on their spatial relationship. Other recent experiments have shown that cottontop tamarins respond to spatial relationships even better than in the current experiment when they have to act directly on the objects. The difference between these results suggests that tamarins perceive the spatial relationships between objects more readily in the context of an ecologically valid problem.     

Generalized reciprocity in rats

The evolution of cooperation among nonrelatives has been explained by direct, indirect, and strong reciprocity. Animals should base the decision to help others on expected future help, which they may judge from past behavior of their partner. Although many examples of cooperative behavior exist in nature where reciprocity may be involved, experimental evidence for strategies predicted by direct reciprocity models remains controversial; and indirect and strong reciprocity have been found only in humans so far. Here we show experimentally that cooperative behavior of female rats is influenced by prior receipt of help, irrespective of the identity of the partner. Rats that were trained in an instrumental cooperative task (pulling a stick in order to produce food for a partner) pulled more often for an unknown partner after they were helped than if they had not received help before. This alternative mechanism, called generalized reciprocity, requires no specific knowledge about the partner and may promote the evolution of cooperation among unfamiliar nonrelatives.     

Color discrimination by the cotton-top tamarin (Saguinus oedipus oedipus) and its relation to fruit coloration

Old World monkeys and apes have been reported to differ from New World monkeys in their abilities to discriminate colors across the visible spectrum. Old World monkeys and apes (Macaca, Pan, Pongo) discriminate colors quite accurately, while some New World monkeys studied (Saimiri, Cebus) have shown lower sensitivity to and poorer discrimination of long wavelength light. This study examined the color discrimination ability of another New World primate, the cotton-top tamarin, Saguinus oedipus oedipus (family Callitrichidae). The tamarins were trained to discriminate a set of Munsell color chips, both within the same hue category and from the 2 hue categories on either side of the training hue. Results indicated that the cotton-top tamarin can make accurate discriminations across the visible spectrum. Human subjects were tested under similar conditions in order to compare their color discrimination abilities to those of the tamarins. The tamarins and human subjects had the most difficulty discriminating the same hues. The discrimination abilities of the monkeys were assessed in relation to the coloration of fruits eaten in a natural environment. A list of the species of fruits commonly eaten by various species of New World monkeys was compiled and the coloration of fruits at maturity was noted. It was found that most New World primate species eat fruits whose mature coloration ranges across most of the spectrum.     

Social factors determine cooperation in marmosets

We investigated which factors determine cooperative behaviour of common marmosets, Callithrix jacchus, in an instrumental task. During the approach phase each of eight individuals of a family group learned in isolation to pull a handle moving a bowl with attractive food towards its reach. In the following two experimental phases we used 16 dyads. In a dyadic training phase we assessed whether the partners were willing to manipulate the apparatus and to share food. In the subsequent cooperation test we examined whether they were willing to cooperate at a slightly modified apparatus whose solution required one individual (the producer) to pull the handle and the other (the scrounger) to grasp the bowl. Although all individuals were willing to cooperate with at least one partner, only half of the dyads solved the task in the cooperation phase. Examination of the factors that correlated with success in this phase revealed that primarily those dyads cooperated in which the dominant subject took the role of the scrounger and the subordinate took the role of the producer. However, in these successful dyads the dominant animal did not force the subordinate partner to pull the handle. Rather, the partners of cooperative dyads shared the reward and pulled equally often in both the dyadic training and the cooperation test. Thus, cooperation of marmosets in an instrumental task seems to depend on a specific distribution of roles and the tolerance of higher-ranking individuals.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Cooperative problem solving in rooks (Corvus frugilegus)

Recent work has shown that captive rooks, like chimpanzees and other primates, develop cooperative alliances with their conspecifics. Furthermore, the pressures hypothesized to have favoured social intelligence in primates also apply to corvids. We tested cooperative problem-solving in rooks to compare their performance and cognition with primates. Without training, eight rooks quickly solved a problem in which two individuals had to pull both ends of a string simultaneously in order to pull in a food platform. Similar to chimpanzees and capuchin monkeys, performance was better when within-dyad tolerance levels were higher. In contrast to chimpanzees, rooks did not delay acting on the apparatus while their partner gained access to the test room. Furthermore, given a choice between an apparatus that could be operated individually over one that required the action of two individuals, four out of six individuals showed no preference. These results may indicate that cooperation in chimpanzees is underpinned by more complex cognitive processes than that in rooks. Such a difference may arise from the fact that while both chimpanzees and rooks form cooperative alliances, chimpanzees, but not rooks, live in a variable social network made up of competitive and cooperative relationships.