Chimpanzees know what conspecifics do and do not see

We report a series of experiments on social problem solving in chimpanzees, Pan troglodytes. In each experiment a subordinate and a dominant individual were put into competition over two pieces of food. In all experiments dominants obtained virtually all of the foods to which they had good visual and physical access. However, subordinates were successful quite often in three situations in which they had better visual access to the food than the dominant, for example, when the food was positioned so that only the subordinate (and not the dominant) could see it. In some cases, the subordinate might have been monitoring the behaviour of the dominant directly and simply avoided the food that the dominant was moving towards (which just happened to be the one it could see). In other cases, however, we ruled out this possibility by giving subordinates a small headstart and forcing them to make their choice (to go to the food that both competitors could see, or the food that only they could see) before the dominant was released into the area. Together with other recent studies, the present investigation suggests that chimpanzees know what conspecifics can and cannot see, and, furthermore, that they use this knowledge to devise effective social-cognitive strategies in naturally occurring food competition situations. Copyright 2000 The Association for the Study of Animal Behaviour.     

Genetic differentiation and the evolution of cooperation in chimpanzees and humans

It has been proposed that human cooperation is unique among animals for its scale and complexity, its altruistic nature and its occurrence among large groups of individuals that are not closely related or are even strangers. One potential solution to this puzzle is that the unique aspects of human cooperation evolved as a result of high levels of lethal competition (i.e. warfare) between genetically differentiated groups. Although between-group migration would seem to make this scenario unlikely, the plausibility of the between-group competition model has recently been supported by analyses using estimates of genetic differentiation derived from contemporary human groups hypothesized to be representative of those that existed during the time period when human cooperation evolved. Here, we examine levels of between-group genetic differentiation in a large sample of contemporary human groups selected to overcome some of the problems with earlier estimates, and compare them with those of chimpanzees. We find that our estimates of between-group genetic differentiation in contemporary humans are lower than those used in previous tests, and not higher than those of chimpanzees. Because levels of between-group competition in contemporary humans and chimpanzees are also similar, these findings suggest that the identification of other factors that differ between chimpanzees and humans may be needed to provide a compelling explanation of why humans, but not chimpanzees, display the unique features of human cooperation.     

Spontaneous altruism by chimpanzees and young children

People often act on behalf of others. They do so without immediate personal gain, at cost to themselves, and even toward unfamiliar individuals. Many researchers have claimed that such altruism emanates from a species-unique psychology not found in humans' closest living evolutionary relatives, such as the chimpanzee. In favor of this view, the few experimental studies on altruism in chimpanzees have produced mostly negative results. In contrast, we report experimental evidence that chimpanzees perform basic forms of helping in the absence of rewards spontaneously and repeatedly toward humans and conspecifics. In two comparative studies, semi–free ranging chimpanzees helped an unfamiliar human to the same degree as did human infants, irrespective of being rewarded (experiment 1) or whether the helping was costly (experiment 2). In a third study, chimpanzees helped an unrelated conspecific gain access to food in a novel situation that required subjects to use a newly acquired skill on behalf of another individual. These results indicate that chimpanzees share crucial aspects of altruism with humans, suggesting that the roots of human altruism may go deeper than previous experimental evidence suggested.     

Context-dependent tool use in New Caledonian crows

Humans and chimpanzees both exhibit context-dependent tool use. That is, both species choose to use tools when food is within reach, but the context is potentially hazardous. Here, we show that New Caledonian crows used tools more frequently when food was positioned next to a novel model snake than when food was positioned next to a novel teddy bear or a familiar food bowl. However, the crows showed no significant difference in their neophobic reactions towards the teddy bear and the model snake. Therefore, the crows used tools more in response to a risky object resembling a natural predator than to a less-threatening object that provoked a comparable level of neophobia. These results show that New Caledonian crows, like humans and chimpanzees, are capable of context-dependent tool use.     

Unconstrained cranial evolution in Neandertals and modern humans compared to common chimpanzees

A variety of lines of evidence support the idea that neutral evolutionary processes (genetic drift, mutation) have been important in generating cranial differences between Neandertals and modern humans. But how do Neandertals and modern humans compare with other species? And how do these comparisons illuminate the evolutionary processes underlying cranial diversification? To address these questions, we used 27 standard cranial measurements collected on 2524 recent modern humans, 20 Neandertals and 237 common chimpanzees to estimate split times between Neandertals and modern humans, and between Pan troglodytes verus and two other subspecies of common chimpanzee. Consistent with a neutral divergence, the Neandertal versus modern human split-time estimates based on cranial measurements are similar to those based on DNA sequences. By contrast, the common chimpanzee cranial estimates are much lower than DNA-sequence estimates. Apparently, cranial evolution has been unconstrained in Neandertals and modern humans compared with common chimpanzees. Based on these and additional analyses, it appears that cranial differentiation in common chimpanzees has been restricted by stabilizing natural selection. Alternatively, this restriction could be due to genetic and/or developmental constraints on the amount of within-group variance (relative to effective population size) available for genetic drift to act on.     

Computer animations stimulate contagious yawning in chimpanzees

People empathize with fictional displays of behaviour, including those of cartoons and computer animations, even though the stimuli are obviously artificial. However, the extent to which other animals also may respond empathetically to animations has yet to be determined. Animations provide a potentially useful tool for exploring non-human behaviour, cognition and empathy because computer-generated stimuli offer complete control over variables and the ability to program stimuli that could not be captured on video. Establishing computer animations as a viable tool requires that non-human subjects identify with and respond to animations in a way similar to the way they do to images of actual conspecifics. Contagious yawning has been linked to empathy and poses a good test of involuntary identification and motor mimicry. We presented 24 chimpanzees with three-dimensional computer-animated chimpanzees yawning or displaying control mouth movements. The apes yawned significantly more in response to the yawn animations than to the controls, implying identification with the animations. These results support the phenomenon of contagious yawning in chimpanzees and suggest an empathic response to animations. Understanding how chimpanzees connect with animations, to both empathize and imitate, may help us to understand how humans do the same.     

Chimpanzees use self-distraction to cope with impulsivity

It is unknown whether animals, like humans, can employ behavioural strategies to cope with impulsivity. To examine this question, we tested whether chimpanzees (Pan troglodytes) would use self-distraction as a coping strategy in a situation in which they had to continually inhibit responses to accumulating candies in order to earn a greater amount of those rewards. We tested animals in three conditions in which they were sometimes given a set of toys and were sometimes allowed physical access to the accumulating candies. Chimpanzees allowed the rewards to accumulate longer before responding when they could divert their attention to the toys, and they manipulated the toys more when the candies were physically accessible. Thus, chimpanzees engaged in self-distraction with the toys when such behaviour was most beneficial as a coping mechanism.     

Raiding parties of male spider monkeys: Insights into human warfare?

Raids into neighboring territories may occur for different reasons, including the increase of foraging and mating opportunities directly or indirectly through the killing of neighboring rivals. Lethal raids have been mainly observed in humans and chimpanzees, with raiding males being reported to search purposefully for neighbors. Here we report on the first cases ever witnessed of raiding parties of male spider monkeys, a species expected to show such a behavioral tendency, given its similarity with humans and chimpanzees in critical socio-ecological characteristics, such as fission-fusion social dynamics and male-male bonding. Despite the high degree of arboreality of spider monkeys, all seven witnessed raids involved the males progressing single file on the ground in unusual silence. This is remarkably similar to the behavior of chimpanzees. The circumstances around the raids suggest that factors such as reduced mating opportunities, number of males relative to that in the neighboring community, and the strength of bonds among males could play a role in the timing of such actions. The raids did not appear to be aimed at finding food, whereas there is some indication that they may directly or indirectly increase reproductive opportunities. Although no killing was observed, we cannot exclude the possibility that spider monkey raids may be aimed at harming rivals if a vulnerable individual were encountered. The similarity of spider monkey raids with those of chimpanzees and humans supports the notion that lethal raiding is a convergent response to similar socio-ecological conditions.     

Endocranial shape changes during growth in chimpanzees and humans: A morphometric analysis of unique and shared aspects

Compared to our closest living and extinct relatives, humans have a large, specialized, and complex brain embedded in a uniquely shaped braincase. Here, we quantitatively compare endocranial shape changes during ontogeny in humans and chimpanzees. Identifying shared and unique aspects in developmental patterns of these two species can help us to understand brain evolution in the hominin lineage.Using CT scans of 58 humans and 60 chimpanzees varying in age from birth to adulthood, we generated virtual endocasts to measure and analyze 29 three-dimensional endocranial landmarks and several hundred semilandmarks on curves and the endocranial surface; these data were then analyzed using geometric morphometric methods.The ontogenetic shape trajectories are nonlinear for both species, which indicates several developmental phases. Endocranial shape is already distinct at birth and there is no overlap between the two species throughout ontogeny. While some aspects of the pattern of endocranial shape change are shared between humans and chimpanzees, the shape trajectories differ substantially directly after birth until the eruption of the deciduous dentition: in humans but not in chimpanzees, the parietal and cerebellar regions expand relatively (contributing to neurocranial globularity) and the cranial base flexes within the first postnatal year when brain growth rates are high. We show that the shape changes associated with this early “globularization phase” are unique to humans and do not occur in chimpanzees before or after birth.     

Chimpanzees Help Each Other upon Request

Background

The evolution of altruism has been explained mainly from ultimate perspectives. However, it remains to be investigated from a proximate point of view how and in which situations such social propensity is achieved. We investigated chimpanzees'' targeted helping in a tool transfer paradigm, and discuss the similarities and differences in altruism between humans and chimpanzees. Previously it has been suggested that chimpanzees help human experimenters by retrieving an object which the experimenter is trying to reach. In the present study, we investigated the importance of communicative interactions between chimpanzees themselves and the influence of conspecific partner''s request on chimpanzees'' targeted helping.

Methodology/Principal Findings

We presented two tool-use situations (a stick-use situation and a straw-use situation) in two adjacent booths, and supplied non-corresponding tools to paired chimpanzees in the two booths. For example, a chimpanzee in the stick-use situation was supplied with a straw, and the partner in the straw-use situation possessed a stick. Spontaneous tool transfer was observed between paired chimpanzees. The tool transfer events occurred predominantly following recipients'' request. Even without any hope of reciprocation from the partner, the chimpanzees continued to help the partner as long as the partner required help.

Conclusions/Significance

These results provide further evidence for altruistic helping in chimpanzees in the absence of direct personal gain or even immediate reciprocation. Our findings additionally highlight the importance of request as a proximate mechanism motivating prosocial behavior in chimpanzees whether between kin or non-kin individuals and the possible confounding effect of dominance on the symmetry of such interactions. Finally, in contrast to humans, our study suggests that chimpanzees rarely perform acts of voluntary altruism. Voluntary altruism in chimpanzees is not necessarily prompted by simple observation of another''s struggle to attain a goal and therefore an accurate understanding of others'' desires in the absence of communicative signals.     

The selfish nature of generosity: harassment and food sharing in primates

Animals may share food to gain immediate or delayed fitness benefits. Previous studies of sharing have concentrated on delayed benefits such as reciprocity, trade and punishment. This study tests an alternative model (the harassment or sharing-under-pressure hypothesis) in which a food owner immediately benefits because sharing avoids costly harassment from a beggar. I present an experiment that varies the potential ability of the beggar to harass, and of the owner to defend the food, to examine the effects of harassment on food sharing in two primate species: chimpanzees (Pan troglodytes) and squirrel monkeys (Saimiri boliviensis). For both species, high levels of harassment potential significantly increased both beggar harassment and sharing by the owner. Food defensibility did not affect harassment or sharing. Interestingly, squirrel monkeys and chimpanzees shared equally frequently with conspecifics despite a much higher natural sharing rate in chimpanzees. These results suggest that harassment can play a significant role in primate food sharing, providing a simple alternative to reciprocity. The selfish nature of harassment has implications for economic, psychological and evolutionary studies of cooperative systems.     

Rates of genomic divergence in humans,chimpanzees and their lice

The rate of DNA mutation and divergence is highly variable across the tree of life. However, the reasons underlying this variation are not well understood. Comparing the rates of genetic changes between hosts and parasite lineages that diverged at the same time is one way to begin to understand differences in genetic mutation and substitution rates. Such studies have indicated that the rate of genetic divergence in parasites is often faster than that of their hosts when comparing single genes. However, the variation in this relative rate of molecular evolution across different genes in the genome is unknown. We compared the rate of DNA sequence divergence between humans, chimpanzees and their ectoparasitic lice for 1534 protein-coding genes across their genomes. The rate of DNA substitution in these orthologous genes was on average 14 times faster for lice than for humans and chimpanzees. In addition, these rates were positively correlated across genes. Because this correlation only occurred for substitutions that changed the amino acid, this pattern is probably produced by similar functional constraints across the same genes in humans, chimpanzees and their ectoparasites.     

Do chimpanzees know what conspecifics know?

We conducted three experiments on social problem solving by chimpanzees, Pan troglodytes. In each experiment a subordinate and a dominant individual competed for food, which was placed in various ways on the subordinate's side of two opaque barriers. In some conditions dominants had not seen the food hidden, or food they had seen hidden was moved elsewhere when they were not watching (whereas in control conditions they saw the food being hidden or moved). At the same time, subordinates always saw the entire baiting procedure and could monitor the visual access of their dominant competitor as well. If subordinates were sensitive to what dominants did or did not see during baiting, they should have preferentially approached and retrieved the food that dominants had not seen hidden or moved. This is what they did in experiment 1 when dominants were either uninformed or misinformed about the food's location. In experiment 2 subordinates recognized, and adjusted their behaviour accordingly, when the dominant individual who witnessed the hiding was replaced with another dominant individual who had not witnessed it, thus demonstrating their ability to keep track of precisely who has witnessed what. In experiment 3 subordinates did not choose consistently between two pieces of hidden food, one of which dominants had seen hidden and one of which they had not seen hidden. However, their failure in this experiment was likely to be due to the changed nature of the competition under these circumstances and not to a failure of social-cognitive skills. These findings suggest that at least in some situations (i.e. competition with conspecifics) chimpanzees know what conspecifics have and have not seen (do and do not know), and that they use this information to devise effective social-cognitive strategies. Copyright 2001 The Association for the Study of Animal Behaviour.     

Response facilitation in the four great apes: is there a role for empathy?

Contagious yawning is a form of response facilitation found in humans and other primates in which observing a model yawning enhances the chance that the observer will also yawn. Because contagious yawning seems to be more easily triggered when models are conspecifics or have a strong social bond with the observer, it has been proposed that contagious yawning is linked to empathy. A possible way to test this hypothesis is to analyze whether individuals’ responses differ when they observe models yawning or performing different involuntary (i.e., nose wiping, scratching) and voluntary (i.e., hand closing, wrist shaking) actions that are not linked to empathy. In this study, we tested the four great ape species with two different setups by exposing them to a human experimenter repeatedly performing these actions online, and video-recorded conspecifics repeatedly performing these actions on a screen. We examined which behaviors were subject to response facilitation, whether response facilitation was triggered by both human models and video-recorded conspecifics, and whether all species showed evidence of response facilitation. Our results showed that chimpanzees yawned significantly more when and shortly after watching videos of conspecifics (but not humans) yawning than in control conditions, and they did not do so as a response to increased levels of anxiety. For all other behaviors, no species produced more target actions when being exposed to either model than under control conditions. Moreover, the individuals that were more “reactive” when watching yawning videos were not more reactive when exposed to other actions. Since, at least in chimpanzees, (1) subjects only showed response facilitation when they were exposed to yawning and (2) only if models were conspecifics, it appears that contagious yawning is triggered by unique mechanisms and might be linked to empathy.     

Age-related effects on malaria parasite infection in wild chimpanzees

Wild great apes are widely infected with a number of malaria parasites (Plasmodium spp.). Yet, nothing is known about the biology of these infections in the wild. Using faecal samples collected from wild chimpanzees, we investigated the effect of age on Plasmodium spp. detection rates. The data show a strong association between age and malaria parasite positivity, with significantly lower detection rates in adults. This suggests that, as in humans, individuals reaching adulthood have mounted an effective protective immunity against malaria parasites.     

Genetic and ‘cultural’ similarity in wild chimpanzees

The question of whether animals possess ‘cultures’ or ‘traditions’ continues to generate widespread theoretical and empirical interest. Studies of wild chimpanzees have featured prominently in this discussion, as the dominant approach used to identify culture in wild animals was first applied to them. This procedure, the ‘method of exclusion,’ begins by documenting behavioural differences between groups and then infers the existence of culture by eliminating ecological explanations for their occurrence. The validity of this approach has been questioned because genetic differences between groups have not explicitly been ruled out as a factor contributing to between-group differences in behaviour. Here we investigate this issue directly by analysing genetic and behavioural data from nine groups of wild chimpanzees. We find that the overall levels of genetic and behavioural dissimilarity between groups are highly and statistically significantly correlated. Additional analyses show that only a very small number of behaviours vary between genetically similar groups, and that there is no obvious pattern as to which classes of behaviours (e.g. tool-use versus communicative) have a distribution that matches patterns of between-group genetic dissimilarity. These results indicate that genetic dissimilarity cannot be eliminated as playing a major role in generating group differences in chimpanzee behaviour.     

Development of the visual preference of chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) for photographs of primates: effect of social experience

In a study by Tanaka (2003) five captive chimpanzees preferred photographs of humans to those of chimpanzees. All the subjects were raised by humans and lived in captivity for many years. This suggests their preference might have developed through social experience. In this study examined this hypothesis by using three young chimpanzees raised by their mothers in a captive chimpanzee community. The young chimpanzees were tested four times before six years of age. I also tested eight adult chimpanzees that had been in captivity for more than 20 years. Each subject was presented with digitized color photographs of different species of primates on a touch-sensitive screen. The subjects received a food reward when they touched a photograph, irrespective of which photograph they touched. All the adult chimpanzees touched photographs of humans more frequently than those of any other species of primate. Two of the young chimpanzees showed no species preference before reaching 5 years of age, when they started to show preference for humans. The remaining young chimpanzee consistently preferred chimpanzees. These results suggest that development of visual preference of chimpanzees is affected by social experience during infancy.     

Multi-generational persistence of traditions in neighbouring meerkat groups

Reports of socially transmitted traditions based on behavioural differences between geographically separated groups of conspecifics are contentious because they cannot exclude genetic or environmental causes. Here, we report persistent differences between neighbouring groups of meerkats (Suricata suricatta) where extensive gene flow precludes genetic differentiation. Over 11 years, some groups consistently emerged later from their sleeping burrows in the morning than others, despite complete turnovers in group membership and the influx of immigrants. Group territories overlapped and, in many cases, the same sleeping burrows were used by different groups. Differences persisted even after accounting for effects of group size, weather and burrow characteristics, and were unrelated to food availability within territories. These results provide compelling evidence that the emergence times of meerkat groups represent conservative traditions.     

Tokens improve capuchin performance in the reverse–reward contingency task

In humans and apes, one of the most adaptive functions of symbols is to inhibit strong behavioural predispositions. However, to our knowledge, no study has yet investigated whether using symbols provides some advantage to non-ape primates. We aimed to trace the evolutionary roots of symbolic competence by examining whether tokens improve performance in the reverse–reward contingency task in capuchin monkeys, which diverged from the human lineage approximately 35 Ma. Eight capuchins chose between: (i) two food quantities, (ii) two quantities of ‘low-symbolic distance tokens’ (each corresponding to one unit of food), and (iii) two ‘high-symbolic distance tokens’ (each corresponding to a different amount of food). In all conditions, subjects had to select the smaller quantity to obtain the larger reward. No procedural modifications were employed. Tokens did improve performance: five subjects succeeded with high-symbolic distance tokens, though only one succeeded with food, and none succeeded with low-symbolic distance tokens. Moreover, two of the five subjects transferred the rule to novel token combinations. Learning effects or preference reversals could not account for the successful performance with high-symbolic distance tokens. This is, to our knowledge, the first demonstration that tokens do allow monkeys to inhibit strong behavioural predispositions, as occurs in chimpanzees and children.     

Social benefits of non-kin food sharing by female vampire bats

Regurgitations of blood among vampire bats appear to benefit both direct and indirect fitness. To maximize inclusive fitness, reciprocal food sharing should occur among close kin. Why then do females with kin roost-mates help non-kin? We tested the hypothesis that helping non-kin increases a bat''s success at obtaining future donations by expanding its network of potential donors. On six occasions, we individually fasted 14 adult females and measured donations from 28 possible donors. Each female was fasted before, during and after a treatment period, when we prevented donations from past donors (including 10 close relatives) by simultaneously fasting or removing them. This experiment was designed to detect partner switching and yielded three main results. First, females received less food when we prevented donations from a past donor versus a control bat. Donors within a group are therefore not interchangeable. Second, the treatment increased the variance in donors'' contributions to food received by subjects, suggesting the possibility of alternative responses to a partner''s inability to reciprocate. Finally, bats that fed more non-kin in previous years had more donors and received more food during the treatment. These results indicate that a bat can expand its network of possible donors by helping non-kin.