Animal behavior: A tale of two apes.

A new paper shows that rates of aggression are higher, and rates of coalition formation are lower, among male bonobos than among male chimpanzees. These findings are noteworthy because they challenge the view that female bonobos' preferences for less aggressive males favored a reduction in male aggression and an increase in social tolerance.

Differences in expression of male aggression between wild bonobos and chimpanzees.

Researchers investigating the evolution of human aggression look to our closest living relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), as valuable sources of comparative data.1,2 Males in the two species exhibit contrasting patterns: male chimpanzees sexually coerce females3,4,5,6,7,8 and sometimes kill conspecifics,9,10,11,12 whereas male bonobos exhibit less sexual coercion13,14 and no reported killing.13 Among the various attempts to explain these species differences, the self-domestication hypothesis proposes negative fitness consequences of male aggression in bonobos.2,15,16 Nonetheless, the extent to which these species differ in overall rates of aggression remains unclear due to insufficiently comparable observation methods.17,18,19,20,21,22,23 We used 14 community-years of focal follow data-the gold standard for observational studies24-to compare rates of male aggression in 3 bonobo communities at the Kokolopori Bonobo Reserve, Democratic Republic of Congo, and 2 chimpanzee communities at Gombe National Park, Tanzania. As expected, given that females commonly outrank males, we found that bonobos exhibited lower rates of male-female aggression and higher rates of female-male aggression than chimpanzees. Surprisingly, we found higher rates of male-male aggression among bonobos than chimpanzees even when limiting analyses to contact aggression. In both species, more aggressive males obtained higher mating success. Although our findings indicate that the frequency of male-male aggression does not parallel species difference in its intensity, they support the view that contrary to male chimpanzees, whose reproductive success depends on strong coalitions, male bonobos have more individualistic reproductive strategies.25.

Chimpanzees demonstrate a behavioural signature of human joint action.

The strength of human society can largely be attributed to the tendency to work together to achieve outcomes that are not possible alone. Effective social coordination benefits from mentally representing a partner's actions. Specifically, humans optimize social coordination by forming internal action models adapted to joint rather than individual task demands. To what extent do humans share the cognitive mechanisms that support optimal human coordination and collaboration with other species? An ecologically inspired joint handover-to-retrieve task was systematically manipulated across several experiments to assess whether joint action planning in chimpanzees reflects similar patterns to humans. Chimpanzees' chosen handover locations shifted towards the location of the experimenter's free or unobstructed hand, suggesting they represent the constraints of the joint task even though their individual half of the task was unobstructed. These findings indicate that chimpanzees and humans may share common cognitive mechanisms or predispositions that support joint action.

May the force be with you: exploring force discrimination in chimpanzees using the force-feedback device.

While force-feedback devices have been developed in areas such as virtual reality, there have been very few comparative cognitive studies in nonhuman animals using these devices. In addition, although cross-modal perception between vision and touch has been actively studied in nonhuman primates for several decades, there have been no studies of their active haptic perception. In this study, we attempted to train force discrimination in chimpanzees using a force-feedback device modified from a trackball. Chimpanzees were given different levels of force feedback (8.0 vs. 0.5 N) when moving the on-screen cursor to the target area by manipulating the trackball and were required to select one of two choice stimuli based on the force cue. The experiment was conducted using a trial-block procedure in which the same force stimulus was presented for a fixed number of trials, and the force stimulus was changed between blocks. The block size was progressively reduced from ten trials. Four chimpanzees were trained, but none reached the learning criterion (80% or more correct responses under the condition that the force stimuli were presented randomly). However, a detailed analysis of the chimpanzees' performance before and after the trial-block switching revealed that their choice behavior could not be explained by a simple win-stay/lose-shift strategy, suggesting that the switching of the force stimuli affected the chimpanzees' choice behavior. It was also found that the chimpanzees performed better when switching from small to large force stimuli than when switching from large to small force stimuli. Although none of the chimpanzees in this study acquired force discrimination, future studies using such force-feedback devices will provide new insights for understanding haptic cognition in nonhuman primates from a comparative cognitive perspective.

Chimps remember faces of old friends and family for decades.

Recognition ability rivals all other animals, including humans.

Cooperation across social borders in bonobos.

Cooperation beyond familial and group boundaries is core to the functioning of human societies, yet its evolution remains unclear. To address this, we examined grooming, coalition, and food-sharing patterns in bonobos (Pan paniscus), one of our closest living relatives whose rare out-group tolerance facilitates interaction opportunities between groups. We show that, as in humans, positive assortment supports bonobo cooperation across borders. Bonobo cooperative attitudes toward in-group members informed their cooperative relationships with out-groups, in particular, forming connections with out-group individuals who also exhibited high cooperation tendencies. Our findings show that cooperation between unrelated individuals across groups without immediate payoff is not exclusive to humans and suggest that such cooperation can emerge in the absence of social norms or strong cultural dispositions.

Humans recognize affective cues in primate vocalizations: acoustic and phylogenetic perspectives.

Humans are adept at extracting affective information from vocalizations of humans and other animals. However, the extent to which human recognition of vocal affective cues of other species is due to cross-taxa similarities in acoustic parameters or the phylogenetic closeness between species is currently unclear. To address this, we first analyzed acoustic variation in 96 affective vocalizations, taken from agonistic and affiliative contexts, of humans and three other primates-rhesus macaques (Macaca mulatta), chimpanzees and bonobos (Pan troglodytes and Pan paniscus). Acoustic analyses revealed that agonistic chimpanzee and bonobo vocalizations were similarly distant from agonistic human voices, but chimpanzee affiliative vocalizations were significantly closer to human affiliative vocalizations, than those of bonobos, indicating a potential derived vocal evolution in the bonobo lineage. Second, we asked 68 human participants to categorize and also discriminate vocalizations based on their presumed affective content. Results showed that participants reliably categorized human and chimpanzee vocalizations according to affective content, but not bonobo threat vocalizations nor any macaque vocalizations. Participants discriminated all species calls above chance level except for threat calls by bonobos and macaques. Our results highlight the importance of both phylogenetic and acoustic parameter level explanations in cross-species affective perception, drawing a more complex picture to the origin of vocal emotions.

Similarity and structured representation in human and nonhuman apes.

How we judge the similarity between objects in the world is connected ultimately to how we represent those objects. It has been argued extensively that object representations in humans are 'structured' in nature, meaning that both individual features and the relations between them can influence similarity. In contrast, popular models within comparative psychology assume that nonhuman species appreciate only surface-level, featural similarities. By applying psychological models of structural and featural similarity (from conjunctive feature models to Tversky's Contrast Model) to visual similarity judgements from adult humans, chimpanzees, and gorillas, we demonstrate a cross-species sensitivity to complex structural information, particularly for stimuli that combine colour and shape. These results shed new light on the representational complexity of nonhuman apes, and the fundamental limits of featural coding in explaining object representation and similarity, which emerge strikingly across both human and nonhuman species.

Don't look back on failure: spontaneous uncertainty monitoring in chimpanzees.

During computer-controlled cognitive tasks, chimpanzees often look up at the food dispenser, which activates at the same time as feedback for the correct choice but not for feedback for the incorrect choice. Do these "looking back" behaviors also indicate signs of spontaneous monitoring of their confidence in their choices? To address this question, we delayed the feedback for 1 s after their choice responses and observed their look-back behaviors during the delay period. Two chimpanzees looked up at the food dispenser significantly less frequently when their choice was incorrect (but the feedback was not given) than when it was correct. These look-back behaviors have not been explicitly trained under experimental contexts. Therefore, these results indicate that chimpanzees spontaneously change the frequency of their look-back behaviors in response to the correctness or incorrectness of their own choices, even without external feedback, suggesting that their look-back behaviors may reflect the level of "confidence" or "uncertainty" of their responses immediately before.

Chimpanzee and Human Risk Preferences Show Key Similarities.

Risk preference impacts how people make key life decisions related to health, wealth, and well-being. Systematic variations in risk-taking behavior can be the result of differences in fitness expectations, as predicted by life-history theory. Yet the evolutionary roots of human risk-taking behavior remain poorly understood. Here, we studied risk preferences of chimpanzees (86 Pan troglodytes; 47 females; age = 2-40 years) using a multimethod approach that combined observer ratings with behavioral choice experiments. We found that chimpanzees' willingness to take risks shared structural similarities with that of humans. First, chimpanzees' risk preference manifested as a traitlike preference that was consistent across domains and measurements. Second, chimpanzees were ambiguity averse. Third, males were more risk prone than females. Fourth, the appetite for risk showed an inverted-U-shaped relation to age and peaked in young adulthood. Our findings suggest that key dimensions of risk preference appear to emerge independently of the influence of human cultural evolution.

Going forward: perceptual bias for forward-facing motion in chimpanzees.

When a row of objects surrounded by a frame suddenly shifts a certain distance so that part of the row is occluded by the frame, humans perceive ambiguous apparent motion either to the left or the right. However, when the objects have "directionality," humans perceive them as moving forward in the direction in which they are pointing, which is termed forward-facing motion bias. In the present study, five experiments were conducted to address whether, and if so how, physical properties or prior knowledge about the objects affected the perception of their apparent motion in two juvenile chimpanzees (Pan troglodytes). In experiment 1, the chimpanzees did not show a clear forward-facing bias in judging the direction of motion when directed triangles were presented, whereas the human participants did. In contrast, when pictures of the lateral view of chimpanzees with quadrupedal postures were shown, there was a clear bias for going "forward" with regards to the side with the head (experiment 2). We presented pictures of dogs looking back to explore what features caused the forward-facing motion bias (experiment 3). Chimpanzees did not show any bias for these stimuli, suggesting that the direction of the head and body interactively affected the perceptual bias. Experiment 4 tested the role of the head and found that only the lateral view of the heads of chimpanzees or humans caused the bias (experiment 4). Additional tests also showed that the chimpanzees could not solve the task based only on the direction of the stimuli without motion (experiment 5). These results indicate that the perception of motion in the chimpanzees was affected by the biological features of the stimuli, suggesting their prior knowledge of the "body" from a biological (morphological and kinetic) perspective.

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.

Do chimpanzees see a face on Mars? A search for face pareidolia in chimpanzees.

We sometimes perceive meaningful patterns or images in random arrangements of colors and shapes. This phenomenon is called pareidolia and has recently been studied intensively, especially face pareidolia. In contrast, there are few comparative-cognitive studies on face pareidolia with nonhuman primates. This study explored behavioral evidence for face pareidolia in chimpanzees using visual search and matching tasks. Faces are processed in a configural manner, and their perception and recognition are hampered by inversion and misalignment of top and bottom parts. We investigated whether the same effect occurs in a visual search for face-like objects. The results showed an effect of misalignment. On the other hand, consistent results were not obtained with the photographs of fruits. When only the top or bottom half of the face-like object was presented, chimpanzees showed better performance for the top-half condition, suggesting the importance of the eye area in face pareidolia. In the positive-control experiments, chimpanzees received the same experiment using human faces and human participants with face-like objects and fruits. As a result, chimpanzees showed an inefficient search for inverted and misaligned faces and humans for manipulated face-like objects. Finally, to examine the role of face awareness, we tested matching a human face to a face-like object in chimpanzees but obtained no substantial evidence that they saw the face-like object as a "face." Based on these results, we discussed the extents and limits of face pareidolia in chimpanzees.

I'll (not) take that: The reverse-reward contingency task as a test of self-control and inhibition.

While searching for more evidence of quantitative skills in chimpanzees to add to what she already had found, Boysen discovered something else. When training chimpanzees to point at what they would not get, and not pointing at what they would get, none could do this for piles of food items. Even when those items in the pointed-at set were given away to another chimpanzee, and even with experience in the task, failure persisted. This test, the reverse-reward contingency test, has now been used with many species, as a means of assessing inhibitory control and perhaps self-control in animals. Typically, the task is difficult, and only specific manipulations have worked to allow primates to overcome the reversed contingencies. This includes using symbolic stimuli, adding another layer to the story, and more value to the task itself as a measure perhaps of forms of cognitive control in other species. I will discuss some of these empirical results, including from other chimpanzees who were given variations of the task, and how these studies have influenced numerous areas within comparative cognitive science.

Chimpanzees organize their social relationships like humans.

Human relationships are structured in a set of layers, ordered from higher (intimate relationships) to lower (acquaintances) emotional and cognitive intensity. This structure arises from the limits of our cognitive capacity and the different amounts of resources required by different relationships. However, it is unknown whether nonhuman primate species organize their affiliative relationships following the same pattern. We here show that the time chimpanzees devote to grooming other individuals is well described by the same model used for human relationships, supporting the existence of similar social signatures for both humans and chimpanzees. Furthermore, the relationship structure depends on group size as predicted by the model, the proportion of high-intensity connections being larger for smaller groups.

Cognitive flexibility supports the development of cumulative cultural learning in children.

The scale of cumulative cultural evolution (CCE) is a defining characteristic of humans. Despite marked scientific interest in CCE, the cognitive underpinnings supporting its development remain understudied. We examined the role cognitive flexibility plays in CCE by studying U.S. children's (N = 167, 3-5-year-olds) propensity to relinquish an inefficient solution to a problem in favor of a more efficient alternative, and whether they would resist reverting to earlier versions. In contrast to previous work with chimpanzees, most children who first learned to solve a puzzlebox in an inefficient way switched to an observed, more efficient alternative. However, over multiple task interactions, 85% of children who switched reverted to the inefficient method. Moreover, almost all children in a control condition (who first learned the efficient method) switched to the inefficient method. Thus, children were keen to explore an alternative solution but, like chimpanzees, are overall conservative in reverting to their first-learned one.

Hierarchical object combination and tool use in the great apes and human children.

Object manipulation can be used as a comparative scale of cognitive development among primates, including humans. Combinatory object manipulation is a precursor of tool-using behavior that indicates material intelligence in primates. However, developmental data on it regarding the great apes other than chimpanzees is insufficient. We conducted a longitudinal investigation of humans and chimpanzees as well as a cross-sectional examination of other great-ape infants (two bonobos, three gorillas, and four orangutans) in captive settings by using two kinds of tasks that required either inserting or stacking combinatory action. The four species of great apes and humans demonstrated both types of combinatory object manipulation during infancy. However, the order of development in different types of combinatory object manipulations varied among the great apes. Furthermore, we applied a nesting-cup task to examine the hierarchical complexity in the combinatory strategies of human children and adult chimpanzees. Both of them exhibited highly hierarchical combinations in the nesting-cup task and employed the subassembly strategy, indicating that an action merge may exist not only in human children but also in adult chimpanzees. The results were discussed with reviews of the tool-use literature from the wild great apes. The early acquisition of an inserting action in the chimpanzees may explain the tool utilization commonality reported in wild chimpanzees. The combinatory object manipulation may have worked as an external enhancer to achieve an additional hierarchical complexity in cognition and behavior, eventually leading humans to develop a language system.

Dead-infant carrying by chimpanzee mothers in the Budongo Forest.

It has been suggested that non-human primates can respond to deceased conspecifics in ways that suggest they experience psychological states not unlike humans, some of which could indicate they exhibit a notion of death. Here, we report long-term demographic data from two East African chimpanzee groups. During a combined 40-year observation period, we recorded 191 births of which 68 died in infancy, mostly within the first year. We documented the post-mortem behaviour of the mothers and describe nine occasions where Budongo chimpanzee mothers carried infants for 1-3 days after their death, usually until the body started to decompose. We also observed three additional cases of extended carrying lasting for more than 2 weeks, one of which was followed by the unusual extended carrying of an object and another which lasted 3 months. In each case, the corpses mummified. In addition, we report four instances of recurring dead-infant carrying by mothers, three of whom carried the corpse for longer during the second instance. We discuss these observations in view of functional hypotheses of dead-infant carrying in primates and the potential proximate mechanisms involved in this behaviour.