Primate socio-ecology shapes the evolution of distinctive facial repertoires.

Primate facial musculature enables a wide variety of movements during bouts of communication, but how these movements contribute to signal construction and repertoire size is unclear. The facial mobility hypothesis suggests that morphological constraints shape the evolution of facial repertoires: species with higher facial mobility will produce larger and more complex repertoires. In contrast, the socio-ecological complexity hypothesis suggests that social needs shape the evolution of facial repertoires: as social complexity increases, so does communicative repertoire size. We tested these two hypotheses by comparing chimpanzees (Pan troglodytes) and gibbons (family Hylobatidae), two distantly related apes who vary in their facial mobility and social organization. While gibbons have higher facial mobility than chimpanzees, chimpanzees live in more complex social groups than gibbons. We compared the morphology and complexity of facial repertoires for both apes using Facial Action Coding Systems designed for chimpanzees and gibbons. Our comparisons were made at the level of individual muscle movements (action units [AUs]) and the level of muscle movement combinations (AU combinations). Our results show that the chimpanzee facial signaling repertoire was larger and more complex than gibbons, consistent with the socio-ecological complexity hypothesis. On average, chimpanzees produced AU combinations consisting of more morphologically distinct AUs than gibbons. Moreover, chimpanzees also produced more morphologically distinct AU combinations than gibbons, even when focusing exclusively on AUs present in both apes. Therefore, our results suggest that socio-ecological factors were more important than anatomical ones to the evolution of facial signaling repertoires in chimpanzees and gibbons. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Chimpanzees Use Least-Cost Routes to Out-of-Sight Goals.

While the ability of naturally ranging animals to recall the location of food resources and use straight-line routes between them has been demonstrated in several studies [1, 2], it is not known whether animals can use knowledge of their landscape to walk least-cost routes [3]. This ability is likely to be particularly important for animals living in highly variable energy landscapes, where movement costs are exacerbated [4, 5]. Here, we used least-cost modeling, which determines the most efficient route assuming full knowledge of the environment, to investigate whether chimpanzees (Pan troglodytes) living in a rugged, montane environment walk least-cost routes to out-of-sight goals. We compared the "costs" and geometry of observed movements with predicted least-cost routes and local knowledge (agent-based) and straight-line null models. The least-cost model performed better than the local knowledge and straight-line models across all parameters, and linear mixed modeling showed a strong relationship between the cost of observed chimpanzee travel and least-cost routes. Our study provides the first example of the ability to take least-cost routes to out-of-sight goals by chimpanzees and suggests they have spatial memory of their home range landscape. This ability may be a key trait that has enabled chimpanzees to maintain their energy balance in a low-resource environment. Our findings provide a further example of how the advanced cognitive complexity of hominins may have facilitated their adaptation to a variety of environmental conditions and lead us to hypothesize that landscape complexity may play a role in shaping cognition.

Differences in the mutual eye gaze of bonobos (Pan paniscus) and chimpanzees (Pan troglodytes).

Eye gaze is widespread in nonhuman primate taxa and important for social cognition and communicative signaling. Bonobos and chimpanzees, two closely related primate species, differ in social organization, behavior, and cognition. Chimpanzees' eye gaze and gaze following has been studied extensively, whereas less is known about bonobos' eye gaze. To examine species differences using a more ecologically relevant measure than videos or pictures, the current study compared bonobo and chimpanzee mutual eye gaze with a human observer. A multivariate analysis of variance revealed significant species differences in frequency and total duration, but not bout length, of mutual eye gaze (p < .001). Specifically, bonobos engage in mutual eye gaze more frequently and for longer total duration than chimpanzees. These results are likely related to species differences in social behavior and temperament and are consistent with eye-tracking studies in which bonobos looked at the eye region of conspecifics (in pictures and videos) longer than chimpanzees. Future research should examine the relationship between mutual eye gaze and gaze following, as well as examine its genetic and neurological correlates. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Bargaining in chimpanzees (Pan troglodytes): The effect of cost, amount of gift, reciprocity, and communication.

Humans routinely incur costs when allocating resources and reject distributions judged to be below/over an expected threshold. The dictator/ultimatum games (DG/UG) are two-player games that quantify prosociality and inequity aversion by measuring allocated distributions and rejection thresholds. Although the UG has been administered to chimpanzees and bonobos, no study has used both games to pinpoint their motivational substrate. We administered a DG/UG using preassigned distributions to four chimpanzee dyads controlling for factors that could explain why proposers' behavior varied substantially across previous studies: game order, cost for proposers, and amount for recipients. Moreover, players exchanged their roles (proposer/recipient) to test reciprocity. Our results show that proposers offered more in the DG than in the nonsocial baseline, particularly when they incurred no cost. In UG, recipients accepted all above-zero offers, suggesting absence of inequity aversion. Proposers preferentially chose options that gave larger amounts to the partner. However, they also decreased their offers across sessions, probably being inclined to punish their partner's rejections. Therefore, chimpanzees were not strategically motivated toward offering more generously to achieve ulterior acceptance from their partner. We found no evidence of reciprocity. We conclude that chimpanzees are generous rational maximizers that may not engage in strategic behavior. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

An assessment of the efficacy of camera traps for studying demographic composition and variation in chimpanzees (Pan troglodytes).

Demographic factors can strongly influence patterns of behavioral variation in animal societies. Traditionally, these factors are measured using longitudinal observation of habituated social groups, particularly in social animals like primates. Alternatively, noninvasive biomonitoring methods such as camera trapping can allow researchers to assess species occupancy, estimate population abundance, and study rare behaviors. However, measures of fine-scale demographic variation, such as those related to age and sex structure or subgrouping patterns, pose a greater challenge. Here, we compare demographic data collected from a community of habituated chimpanzees (Pan troglodytes verus) in the Taï Forest using two methods: camera trap videos and observational data from long-term records. By matching data on party size, seasonal variation in party size, measures of demographic composition, and changes over the study period from both sources, we compared the accuracy of camera trap records and long-term data to assess whether camera trap data could be used to assess such variables in populations of unhabituated chimpanzees. When compared to observational data, camera trap data tended to underestimate measures of party size, but revealed similar patterns of seasonal variation as well as similar community demographic composition (age/sex proportions) and dynamics (particularly emigration and deaths) during the study period. Our findings highlight the potential and limitations of camera trap surveys for estimating fine-scale demographic composition and variation in primates. Continuing development of field and statistical methods will further improve the usability of camera traps for demographic studies.

The costs of living at the edge: Seasonal stress in wild savanna-dwelling chimpanzees.

Adaptations associated with shifting from a predominately forested habitat to a more open environment are considered a crucial step in hominin evolution. Understanding how chimpanzees, one of our closest-living relatives, are exposed to the selection pressures associated with living in a relatively sparse, hot, and dry environment can inform us about the relative importance of potential environmental stressors involved in adaptations to drier environments. We investigated the extent to which chimpanzees living in an extreme savanna habitat experience seasonal variability in either energy balance or thermoregulation (dehydration and heat exposure), as well as whether these potential environmental constraints are taxing to chimpanzee individuals. Specifically, we tested the hypothesis that savanna environments impose seasonally-relevant costs to chimpanzees. To this end, we collected 368 urine samples from one community of chimpanzees at Fongoli, Senegal, and measured c-peptide, creatinine, and cortisol as measures of physiological responses to environmental food, water, and heat constraints, respectively. We then evaluated the influence of climatic and phenological factors on these indicators. Results illustrated significant seasonal variation in all biomarkers, which corresponded to relevant ecological correlates. Furthermore, creatinine but not c-peptide correlated with cortisol levels, suggesting that chimpanzees in this environment endure periods of heat and dehydration stress, but are able to avoid stressful levels of negative energy balance. Using savanna chimpanzees as a referential model, our research lends support to the notion that thermoregulatory challenges were a significant factor in hominin evolution, and suggests these challenges may have overshadowed the challenges of maintaining adequate energetic balance during the expansion of the hominin range from wetter to drier environments.

Sex-biased dispersal of human ancestors.

Some anthropologists and primatologists have argued that, judging by extant chimpanzees and humans, which are female-biased dispersers, the common ancestors of humans and chimpanzees were also female-biased dispersers. It has been thought that sex-biased dispersal patterns have been genetically transmitted for millions of years. However, this character has changed many times with changes in environment and life-form during human evolution and historical times. I examined life-form and social organization of nonhuman primates, among them gatherers (foragers), hunter-gatherers, agriculturalists, industrialists, and modern and extant humans. I conclude that dispersal patterns changed in response to environmental conditions during primate and human evolution.

Chimpanzees return favors at a personal cost.

Humans regularly provide others with resources at a personal cost to themselves. Chimpanzees engage in some cooperative behaviors in the wild as well, but their motivational underpinnings are unclear. In three experiments, chimpanzees (Pan troglodytes) always chose between an option delivering food both to themselves and a partner and one delivering food only to themselves. In one condition, a conspecific partner had just previously taken a personal risk to make this choice available. In another condition, no assistance from the partner preceded the subject's decision. Chimpanzees made significantly more prosocial choices after receiving their partner's assistance than when no assistance was given (experiment 1) and, crucially, this was the case even when choosing the prosocial option was materially costly for the subject (experiment 2). Moreover, subjects appeared sensitive to the risk of their partner's assistance and chose prosocially more often when their partner risked losing food by helping (experiment 3). These findings demonstrate experimentally that chimpanzees are willing to incur a material cost to deliver rewards to a conspecific, but only if that conspecific previously assisted them, and particularly when this assistance was risky. Some key motivations involved in human cooperation thus may have deeper phylogenetic roots than previously suspected.

A longitudinal assessment of vocabulary retention in symbol-competent chimpanzees (Pan troglodytes).

A number of studies from the 1960s to 1990s assessed the symbolic competence of great apes and other animals. These studies provided varying forms of evidence that some species were capable of symbolically representing their worlds, both through productive symbol use and comprehension of symbolic stimuli. One such project at the Language Research Center involved training chimpanzees (Pan troglodytes) to use lexigram symbols (geometric visual stimuli that represented objects, actions, locations, and individuals). Those studies now are more than 40 years old, and only a few of the apes involved in those studies are still alive. Three of these chimpanzees (and a fourth, control chimpanzee) were assessed across a 10-year period from 1999 to 2008 for their continued knowledge of lexigram symbols and, in the case of one chimpanzee, the continued ability to comprehend human speech. This article describes that longitudinal assessment and outlines the degree to which symbol competence was retained by these chimpanzees across that decade-long period. All chimpanzees showed retention of lexigram vocabularies, although there were differences in the number of words that were retained across the individuals. One chimpanzee also showed continual retention of human speech perception. These retained vocabularies largely consisted of food item names, but also names of inedible objects, locations, individuals, and some actions. Many of these retained words were for things that are not common in the daily lives of the chimpanzees and for things that are rarely requested by the chimpanzees. Thus, the early experiences of these chimpanzees in symbol-rich environments have produced long-lasting memories for symbol meaning, and those competencies have benefited research in a variety of topics in comparative cognition.

Chimpanzees trust conspecifics to engage in low-cost reciprocity.

Many of humans' most important social interactions rely on trust, including most notably among strangers. But little is known about the evolutionary roots of human trust. We presented chimpanzees (Pan troglodytes) with a modified version of the human trust game--trust in reciprocity--in which subjects could opt either to obtain a small but safe reward on their own or else to send a larger reward to a partner and trust her to reciprocate a part of the reward that she could not access herself. In a series of three studies, we found strong evidence that in interacting with a conspecific, chimpanzees show spontaneous trust in a novel context; flexibly adjust their level of trust to the trustworthiness of their partner and develop patterns of trusting reciprocity over time. At least in some contexts then, trust in reciprocity is not unique to humans, but rather has its evolutionary roots in the social interactions of humans' closest primate relatives.

From colour photographs to black-and-white line drawings: an assessment of chimpanzees' (Pan troglodytes') transfer behaviour.

Over two experiments, we investigated the ability of two adolescent and two adult chimpanzees to generalise a learnt, pictorial categorisation to increasingly degraded and abstract stimuli. In Experiment 2, we further assessed the ability of the adolescent chimpanzees to engage in open-ended categorisation of black-and-white line drawings. The current results confirmed and extended previous findings, showing that sub-adult chimpanzees outperform adult chimpanzees in the categorisation of pictorial stimuli, particularly when the stimuli are more degraded and abstract in nature. However, none of the four chimpanzees showed positive transfer of their category learning to a set of black-and-white line drawings, and neither of the adolescent chimpanzees evidenced reliable open-ended categorisation of the black-and-white line drawings. The latter findings suggest that both sub-adult and adult chimpanzees find it difficult to recognise black-and-white line drawings, and that open-ended categorisation of black-and-white line drawings is challenging for chimpanzees.

Why do chimpanzees hunt? Considering the benefits and costs of acquiring and consuming vertebrate versus invertebrate prey.

Understanding the benefits and costs of acquiring and consuming different forms of animal matter by primates is critical for identifying the selective pressures responsible for increased meat consumption in the hominin lineage. Chimpanzees (Pan troglodytes) are unusual among primates in the amount of vertebrate prey they consume. Still, surprisingly little is known about the nutritional benefits of eating meat for this species. In order to understand why chimpanzees eat vertebrates, it is critical to consider the relative benefits and costs of other types of faunivory - including invertebrates. Although we lack specific nutritional data on the flesh and organs of chimpanzee prey, the macronutrient profiles of insects and wild vertebrate meat are generally comparable on a gram-to-gram basis. There are currently very few data on the micronutrient (vitamin and mineral) content of meat consumed by chimpanzees. With few exceptions, the advantages of hunting vertebrate prey include year-round availability, rapid acquisition of larger packages and reduced handling/processing time (once prey are encountered or detected). The disadvantages of hunting vertebrate prey include high potential acquisition costs per unit time (energy expenditure and risk of injury) and greater contest competition with conspecifics. Acquiring an equivalent mass of invertebrates (to match even a small scrap of meat) is possible, but typically takes more time. Furthermore, in contrast to vertebrate prey, some insect resources are effectively available only at certain times of the year. Here we identify the critical data needed to test our hypothesis that meat scraps may have a higher (or at least comparable) net benefit:cost ratio than insect prey. This would support the 'meat scrap' hypothesis as an explanation for why chimpanzees hunt in groups even when doing so does not maximize an individual's energetic gain.

Assessment of landscape-scale distribution of sympatric great apes in African rainforests: concurrent use of nest and camera-trap surveys.

Information on the distribution and abundance of sympatric great apes (Pan troglodytes troglodytes and Gorilla gorilla gorilla) are important for effective conservation and management. Although much research has been done to improve the precision of nest-surveys, trade-offs between data-reliability and research-efficiency have not been solved. In this study, we used different approaches to assess the landscape-scale distribution patterns of great apes. We conducted a conventional nest survey and a camera-trap survey concurrently, and checked the consistency of the estimates. We divided the study area (ca. 500 km²), containing various types of vegetation and topography, into thirty 16-km² grids (4 km × 4 km) and performed both methods along 2-km transects centered in each grid. We determined the nest creator species according to the definitions by Tutin & Fernandez [Tutin & Fernandez, 1984, Am J Primatol 6:313-336] and estimated nest-site densities of each species by using the conventional distance-sampling approach. We calculated the mean capture rate of 3 camera traps left for 3 months at each grid as the abundance index. Our analyses showed that both methods provided roughly consistent results for the distribution patterns of the species; chimpanzee groups (parties) were more abundant in the montane forest, and gorilla groups were relatively homogeneously distributed across vegetation types. The line-transect survey also showed that the number of nests per nest site did not vary among vegetation types for either species. These spatial patterns seemed to reflect the ecological and sociological features of each species. Although the consistent results may be largely dependent on site-specific conditions (e.g., high density of each species, distinct distribution pattern between the two species), conventional nest-surveys and a subsequent check of their consistency with independent estimates may be a reasonable approach to obtain certain information on the species distribution patterns. Further analytical improvement is necessary for camera-traps to be considered a stand-alone method.

Skeletal evidence for variable patterns of handedness in chimpanzees, human hunter-gatherers, and recent British populations.

Previous studies have shown a strong correspondence between long bone bilateral asymmetry and reported handedness. Here, we compare the pattern of asymmetry in mechanical properties of the humerus and second metacarpal of Pan troglodytes, recent British industrial and medieval populations, and a broad range of human hunter-gatherers, to test whether technological variation corresponds with lateralization in bone function. The results suggest that P. troglodytes are left-lateralized in the morphology of the humerus and right-lateralized in the second metacarpal, while all human populations are predominantly right-biased in the morphology of these bones. Among human populations, the second metacarpals of 63% of hunter-gatherers show right-hand bias, a frequency similar to that found among chimpanzees. In contrast, the medieval and recent British populations show over 80% right-lateralization in the second metacarpal. The proportion of individuals displaying right-directional asymmetry is less than the expected 90% among all human groups. The variation observed suggests that the human pattern of right-biased asymmetry developed in a mosaic manner throughout human history, perhaps in response to technological development.

Vocal signature in wild infant chimpanzees.

A large array of communication signals supports the fission/fusion social organization in chimpanzees, and among them the acoustic channel plays a large part because of their forest habitat. Adult vocalizations convey social and ecological information to their recipients allowing them to obtain cues about an ongoing event from calls only. In contrast to adult vocalizations, information encoded in infant calls had been hardly investigated. Studies mainly focused on vocal development. The present article aims at assessing the acoustic cues that support individual identity coding in infant chimpanzees. By analyzing recordings performed in the wild from seven 3-year-old infant chimpanzees, we showed that their calls support a well-defined individual vocal signature relying on spectral cues. To assess the reliability of the signature across the calls of an individual, we defined two subsets of recordings on the basis of the characteristics of the frequency modulation (whimpers and screams) and showed that both call types present a reliable vocal signature. Early vocal signature may allow the mother and other individuals in the group to identify the infant caller when visual contact is broken. Chimpanzee mothers may have developed abilities to cope with changing vocal signatures while their infant, still vulnerable, gains in independence in close habitat.

Sociability of female bottlenose dolphins (Tursiops spp.) and chimpanzees (Pan troglodytes): Understanding evolutionary pathways toward social convergence.

On the northern tip of New Zealand's South Island, bottlenose dolphins (Tursiops truncatus) occasionally pass through Admiralty Bay in large, fast-traveling groups of 100 or so individuals. Watching such a group race and splash through the water is reminiscent of a stampeding herd of ungulates, cetaceans' closest terrestrial ancestors. At other times, smaller social groups of bottlenose dolphins appear in the bay and provide a glimpse of the behavioral complexity that dolphins share with their distant relatives, the primates (Fig. 1). Despite being evolutionarily separated for 95 million years and evolving in vastly different environments, cetaceans and primates share striking similarities in behavior, socioecological problem-solving, life-history patterns, and cognitive capacity. By comparing attributes shared by primates and cetaceans, distraction from phylogenetic "noise" is minimized and our understanding of evolutionary pathways is enhanced. In particular, cetaceans provide a powerful outgroup for studying the evolution of primate social organization.

Numerical judgments by chimpanzees (Pan troglodytes) in a token economy.

We presented four chimpanzees with a series of tasks that involved comparing two token sets or comparing a token set to a quantity of food. Selected tokens could be exchanged for food items on a one-to-one basis. Chimpanzees successfully selected the larger numerical set for comparisons of 1 to 5 items when both sets were visible and when sets were presented through one-by-one addition of tokens into two opaque containers. Two of four chimpanzees used the number of tokens and food items to guide responding in all conditions, rather than relying on token color, size, total amount, or duration of set presentation. These results demonstrate that judgments of simultaneous and sequential sets of stimuli are made by some chimpanzees on the basis of the numerousness of sets rather than other non-numerical dimensions. The tokens were treated as equivalent to food items on the basis of their numerousness, and the chimpanzees maximized reward by choosing the larger number of items in all situations.

Tolerant food sharing and reciprocity is precluded by despotism among bonobos but not chimpanzees.

Tolerant food sharing among human foragers can largely be explained by reciprocity. In contrast, food sharing among chimpanzees and bonobos may not always reflect reciprocity, which could be explained by different dominance styles: in egalitarian societies reciprocity is expressed freely, while in more despotic groups dominants may hinder reciprocity. We tested the degree of reciprocity and the influence of dominance on food sharing among chimpanzees and bonobos in two captive groups. First, we found that chimpanzees shared more frequently, more tolerantly, and more actively than bonobos. Second, among chimpanzees, food received was the best predictor of food shared, indicating reciprocal exchange, whereas among bonobos transfers were mostly unidirectional. Third, chimpanzees had a shallower and less linear dominance hierarchy, indicating that they were less despotic than bonobos. This suggests that the tolerant and reciprocal sharing found in chimpanzees, but not bonobos, was made possible by the absence of despotism. To investigate this further, we tested the relationship between despotism and reciprocity in grooming using data from an additional five groups and five different study periods on the main groups. The results showed that i) all chimpanzee groups were less despotic and groomed more reciprocally than bonobo groups, and ii) there was a general negative correlation between despotism and grooming reciprocity across species. This indicates that an egalitarian hierarchy may be more common in chimpanzees, at least in captivity, thus fostering reciprocal exchange. We conclude that a shallow dominance hierarchy was a necessary precondition for the evolution of human-like reciprocal food sharing.

Energetic costs of territorial boundary patrols by wild chimpanzees.

Chimpanzees are well known for their territorial behavior. Males who belong to the same community routinely patrol their territories, occasionally making deep incursions into those of their neighbors. Male chimpanzees may obtain several fitness benefits by participating in territorial boundary patrols, but patrolling is also likely to involve fitness costs. Patrollers risk injury or even death, and patrols may be energetically costly and may involve opportunity costs. Although territorial patrols have been reported at all long-term chimpanzee study sites, quantitative data on their energetic costs have not previously been available. I evaluated the energy costs of patrolling for male chimpanzees at Ngogo, Kibale National Park, Uganda during 14 months of observation. In 29 patrols and matched control periods, I recorded the distances covered and time spent traveling and feeding by chimpanzees. I found that male chimpanzees covered longer distances, spent more time traveling, and spent less time feeding during patrols than during control periods. These results support the hypothesis that chimpanzees incur energetic costs while patrolling and suggest that ecological factors may constrain the ability of chimpanzees to patrol.