Protracted development of stick tool use skills extends into adulthood in wild western chimpanzees.

Tool use is considered a driving force behind the evolution of brain expansion and prolonged juvenile dependency in the hominin lineage. However, it remains rare across animals, possibly due to inherent constraints related to manual dexterity and cognitive abilities. In our study, we investigated the ontogeny of tool use in chimpanzees (Pan troglodytes), a species known for its extensive and flexible tool use behavior. We observed 70 wild chimpanzees across all ages and analyzed 1,460 stick use events filmed in the Taï National Park, Côte d'Ivoire during the chimpanzee attempts to retrieve high-nutrient, but difficult-to-access, foods. We found that chimpanzees increasingly utilized hand grips employing more than 1 independent digit as they matured. Such hand grips emerged at the age of 2, became predominant and fully functional at the age of 6, and ubiquitous at the age of 15, enhancing task accuracy. Adults adjusted their hand grip based on the specific task at hand, favoring power grips for pounding actions and intermediate grips that combine power and precision, for others. Highly protracted development of suitable actions to acquire hidden (i.e., larvae) compared to non-hidden (i.e., nut kernel) food was evident, with adult skill levels achieved only after 15 years, suggesting a pronounced cognitive learning component to task success. The prolonged time required for cognitive assimilation compared to neuromotor control points to selection pressure favoring the retention of learning capacities into adulthood.

Chimpanzees make tactical use of high elevation in territorial contexts.

Tactical warfare is considered a driver of the evolution of human cognition. One such tactic, considered unique to humans, is collective use of high elevation in territorial conflicts. This enables early detection of rivals and low-risk maneuvers, based on information gathered. Whether other animals use such tactics is unknown. With a unique dataset of 3 years of simultaneous behavioral and ranging data on 2 neighboring groups of western chimpanzees, from the Taï National Park, Côte d'Ivoire, we tested whether chimpanzees make decisions consistent with tactical use of topography to gain an advantage over rivals. We show that chimpanzees are more likely to use high hills when traveling to, rather than away from, the border where conflict typically takes place. Once on border hills, chimpanzees favor activities that facilitate information gathering about rivals. Upon leaving hills, movement decisions conformed with lowest risk engagement, indicating that higher elevation facilitates the detection of rivals presence or absence. Our results support the idea that elevation use facilitated rival information gathering and appropriate tactical maneuvers. Landscape use during territorial maneuvers in natural contexts suggests chimpanzees seek otherwise inaccessible information to adjust their behavior and points to the use of sophisticated cognitive abilities, commensurate with selection for cognition in species where individuals gain benefits from coordinated territorial defense. We advocate territorial contexts as a key paradigm for unpicking complex animal cognition.

Characterization of Pan social systems reveals in-group/out-group distinction and out-group tolerance in bonobos.

Human between-group interactions are highly variable, ranging from violent to tolerant and affiliative. Tolerance between groups is linked to our unique capacity for large-scale cooperation and cumulative culture, but its evolutionary origins are understudied. In chimpanzees, one of our closest living relatives, predominantly hostile between-group interactions impede cooperation and information flow across groups. In contrast, in our other closest living relative, the bonobo, tolerant between-group associations are observed. However, as these associations can be frequent and prolonged and involve social interactions that mirror those within groups, it is unclear whether these bonobos really do belong to separate groups. Alternatively, the bonobo grouping patterns may be homologous to observations from the large Ngogo chimpanzee community, where individuals form within-group neighborhoods despite sharing the same membership in the larger group. To characterize bonobo grouping patterns, we compare the social structure of the Kokolopori bonobos with the chimpanzee group of Ngogo. Using cluster analysis, we find temporally stable clusters only in bonobos. Despite the large spatial overlap and frequent interactions between the bonobo clusters, we identified significant association preference within but not between clusters and a unique space use of each cluster. Although bonobo associations are flexible (i.e., fission-fusion dynamics), cluster membership predicted the bonobo fission compositions and the spatial cohesion of individuals during encounters. These findings suggest the presence of a social system that combines clear in-group/out-group distinction and out-group tolerance in bonobos, offering a unique referential model for the evolution of tolerant between-group interactions in humans.

Rethinking peace from a bonobo perspective.

Reconstructing pathways to human peace can be hampered by superficial evaluations of similar processes in nonhuman species. A deeper understanding of bonobo social systems allows us to reevaluate the preconditions for peace to gain a greater insight on the evolutionary timescale of peace emergence.

Tool use behavior in three wild bonobo communities at Kokolopori.

Comparative studies on tool technologies in extant primates, especially in our closest living relatives, offer a window into the evolutionary foundations of tool use in hominins. Whereas chimpanzee tool technology is well studied across populations, the scarcity of described tool technology in wild populations of our other closest living relative, the bonobo, is a mystery. Here we provide a first report of the tool use repertoire of the Kokolopori bonobos and describe in detail the use of leaf-umbrellas during rainfall, with the aim to improve our knowledge of bonobo tool use capacity in the wild. The tool use repertoire of the Kokolopori bonobos was most similar to that of the nearby population of Wamba and comprised eight behaviors, none in a foraging context. Further, over a 6-month period we documented 44 instances of leaf-umbrella use by 22 individuals from three communities, suggesting that this behavior is habitual. Most leaf-umbrella tool users were adult females, and we observed a nonadult using a leaf-umbrella on only a single occasion. While the study and theory of tool technologies is often based on the use of tools in foraging tasks, tool use in bonobos typically occurs in nonforaging contexts across populations. Therefore, incorporating both foraging and nonforaging contexts into our theoretical framework is essential if we wish to advance our understanding of the evolutionary trajectories of tool technology in humans.

Variation in aggression rates and urinary cortisol levels indicates intergroup competition in wild bonobos.

Intergroup competition is a widespread phenomenon across taxa and groups typically compete over access to limited resources, such as food and mates. Such competition may be quantified by changes in individuals' behavioral and physiological status in response to intergroup encounters (IGEs). Bonobos, one of our closest living relatives, are often regarded as xenophilic and exhibit high tolerance towards out-group individuals. This tolerance between groups may still be accompanied by intergroup competition over resources. We hereby compared variation in aggression rates and urinary cortisol levels of bonobos during and outside contexts of IGEs in the Kokolopori Bonobo Reserve and investigated whether food and mate availability influenced males' and females' aggression and cortisol levels, when controlling for dominance rank and the number of individuals present. We found that although females had higher aggression rates and urinary cortisol levels during than outside contexts of IGEs, these increases were not related to food availability or changes in between-group dynamics when maximally tumescent females were present, rather than absent. Furthermore, males showed higher aggression rates and urinary cortisol levels during than outside contexts of IGEs. However, males' responses during IGEs were not related to the presence of maximally tumescent females and food availability. Taken together, while competition intensified during seemingly tolerant IGEs in bonobos, such competition was unrelated to short-term changes in food and mate availability. Despite physical and physiological costs of aggression, bonobos associate with out-group individuals frequently and for extended periods. This suggests potential benefits of bonobo intergroup associations.

Increased sensitivity and signal-to-noise ratio in diffusion-weighted MRI using multi-echo acquisitions.

Post-mortem diffusion MRI (dMRI) enables acquisitions of structural imaging data with otherwise unreachable resolutions - at the expense of longer scanning times. These data are typically acquired using highly segmented image acquisition strategies, thereby resulting in an incomplete signal decay before the MRI encoding continues. Especially in dMRI, with low signal intensities and lengthy contrast encoding, such temporal inefficiency translates into reduced image quality and longer scanning times. This study introduces Multi Echo (ME) acquisitions to dMRI on a human MRI system - a time-efficient approach, which increases SNR (Signal-to-Noise Ratio) and reduces noise bias for dMRI images. The benefit of the introduced ME-dMRI method was validated using numerical Monte Carlo simulations and showcased on a post-mortem brain of a wild chimpanzee. The proposed Maximum Likelihood Estimation echo combination results in an optimal SNR without detectable signal bias. The combined strategy comes at a small price in scanning time (here 30% additional) and leads to a substantial SNR increase (here white matter: ~ 1.6x, equivalent to 2.6 averages, grey matter: ~ 1.9x, equivalent to 3.6 averages) and a general reduction of the noise bias.

Information transfer efficiency differs in wild chimpanzees and bonobos, but not social cognition.

Several theories have been generated to understand the socio-cognitive mechanisms underlying the unique cooperative abilities of humans. The 'interdependence hypothesis' posits first, that the cognitive dimension of human cooperation evolved in contexts when several individuals needed to act together to achieve a common goal, like when hunting large prey. Second, the more interdependent individuals are, the more likely they are to provide services to conspecifics in other contexts. Alternatively, the 'social tolerance hypothesis' proposes that higher social tolerance allows conspecifics to cooperate more efficiently and with a wider range of partners. We conducted the first field experimental evaluation of both hypotheses in our closest living relatives by contrasting chimpanzees to the less interdependent but more tolerant bonobos. We compared each species' performance during a cooperative task: informing conspecifics about a danger. We presented Gaboon viper models to 82 individuals from five wild communities. Chimpanzees arriving late at the snake were significantly more likely to have heard a call and less likely to startle, indicating that chimpanzees were better informed about the presence of the threat than bonobos. This stems from clear species differences in how individuals adjusted their calling decisions to the level of information already available. Chimpanzees were more likely to call and produced more alarm calls when they had not yet heard a call, whereas bonobos did so when they already heard a call. Our results confirm the link between interdependence and cooperation performance. These species differences were most likely driven by differences in motivation rather than in cognitive capacities because both species tended to consider audience knowledge in their decision to call. Our results inform theories on the evolution of human cooperation by linking inter-group competition pressure and in-group cooperative motivation and/or capability.

Patterns of urinary cortisol levels during ontogeny appear population specific rather than species specific in wild chimpanzees and bonobos.

Compared with most mammals, postnatal development in great apes is protracted, presenting both an extended period of phenotypic plasticity to environmental conditions and the potential for sustained mother-offspring and/or sibling conflict over resources. Comparisons of cortisol levels during ontogeny can reveal physiological plasticity to species or population specific socioecological factors and in turn how these factors might ameliorate or exaggerate mother-offspring and sibling conflict. Here, we examine developmental patterns of cortisol levels in two wild chimpanzee populations (Budongo and Taï), with two and three communities each, and one wild bonobo population (LuiKotale), with two communities. Both species have similar juvenile life histories. Nonetheless, we predicted that key differences in socioecological factors, such as feeding competition, would lead to interspecific variation in mother-offspring and sibling conflict and thus variation in ontogenetic cortisol patterns. We measured urinary cortisol levels in 1394 samples collected from 37 bonobos and 100 chimpanzees aged up to 12 years. The significant differences in age-related variation in cortisol levels appeared population specific rather than species specific. Both bonobos and Taï chimpanzees had comparatively stable and gradually increasing cortisol levels throughout development; Budongo chimpanzees experienced declining cortisol levels before increases in later ontogeny. These age-related population differences in cortisol patterns were not explained by mother-offspring or sibling conflict specifically; instead, the comparatively stable cortisol patterns of bonobos and Taï chimpanzees likely reflect a consistency in experience of competition and the social environment compared with Budongo chimpanzees, where mothers may adopt more variable strategies related to infanticide risk and resource availability. The clear population-level differences within chimpanzees highlight potential intraspecific flexibility in developmental processes in apes, suggesting the flexibility and diversity in rearing strategies seen in humans may have a deep evolutionary history.

Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (Pan troglodytes verus).

BACKGROUND: In animals with altricial offspring, most growth occurs after birth and may be optimized by post-natal maternal care. Maternal effects on growth may be influenced by individual characteristics of the mothers, such as social status, individual investment strategies and the length of association with offspring. The prolonged juvenile dependence seen in humans is a distinctive life history adaptation, which may have evolved to facilitate sustained somatic and brain growth.In chimpanzees, offspring are typically weaned at approximately 4 years old, yet immature individuals continue to associate with their mothers for up to 10 years beyond weaning. Whether this lengthy association or the individual characteristics of mothers influences growth patterns in this species is not clear.The relationship between urinary creatinine and specific gravity is an established non-invasive measure of muscle mass in humans and chimpanzees. We analysed the urinary creatinine and specific gravity of 1318 urine samples from 70 wild chimpanzees from the Taï Forest, Ivory Coast aged 4 to 15 years. RESULTS: We showed a clear increase in urinary creatinine levels with age in both males and females, replicating established growth curves in this species and reaffirming this measure as a reliable proxy for lean body mass. Comparing those who experience maternal loss (orphans) with non-orphan chimpanzees, maternal presence beyond weaning age and into late juvenility positively influenced offspring muscle mass throughout ontogeny such that orphans had significantly less muscle mass than age-matched non-orphans. In age-matched offspring with mothers, those with high-ranking mothers had greater muscle mass. Accounting for variation in muscle mass attributable to maternal presence, we found no effect of maternal investment (length of inter birth interval, from own birth to birth of following sibling) on offspring muscle mass. CONCLUSION: Chimpanzee mothers have an extended and multi-faceted influence on offspring phenotypes. Our results suggest that maternal investment extends beyond lactation and into early adulthood and has clear benefits to offspring physical development. Therefore, prolonged juvenile dependence, although unique in its form in human societies, may be a trait with deeper evolutionary origins.

Oxytocin reactivity during intergroup conflict in wild chimpanzees.

Intergroup conflict is evident throughout the history of our species, ubiquitous across human societies, and considered crucial for the evolution of humans' large-scale cooperative nature. Like humans, chimpanzee societies exhibit intragroup coordination and coalitionary support during violent intergroup conflicts. In both species, cooperation among group members is essential for individuals to gain access to benefits from engaging in intergroup conflict. Studies suggest that a contributive mechanism regulating in-group cooperation during intergroup conflicts in humans involves the neuropeptide hormone oxytocin, known to influence trust, coordination, and social cognition, although evidence from natural settings is lacking. Here, applying a noninvasive method, we investigate oxytocinergic system involvement during natural intergroup conflicts in wild chimpanzees. We found that chimpanzees of both sexes had significantly higher urinary oxytocin levels immediately before and during intergroup conflict compared with controls. Also, elevated hormone levels were linked with greater cohesion during intergroup conflicts, rather than with the level of potential threat posed by rival groups, intragroup affiliative social interactions, or coordinated behavior alone. Thus, the oxytocinergic system, potentially engendering cohesion and cooperation when facing an out-group threat, may not be uniquely human but rather a mechanism with evolutionary roots shared by our last common ancestor with chimpanzees, likely expediting fitness gains during intergroup conflict.

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.

Socially learned habituation to human observers in wild chimpanzees.

Habituation to human observers is an essential tool in animal behaviour research. Habituation occurs when repeated and inconsequential exposure to a human observer gradually reduces an animal's natural aversive response. Despite the importance of habituation, little is known about the psychological mechanisms facilitating it in wild animals. Although animal learning theory offers some account, the patterns are more complex in natural than in laboratory settings, especially in large social groups in which individual experiences vary and individuals influence each other. Here, we investigate the role of social learning during the habituation process of a wild chimpanzee group, the Waibira community of Budongo Forest, Uganda. Through post hoc hypothesis testing, we found that the immigration of two well-habituated, young females from the neighbouring Sonso community had a significant effect on the behaviour of non-habituated Waibira individuals towards human observers, suggesting that habituation is partially acquired via social learning.

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.

Social uncertainty promotes signal complexity during approaches in wild chimpanzees (Pan troglodytes verus) and mangabeys (Cercocebus atys atys).

The social complexity hypothesis for the evolution of communication posits that complex social environments require greater communication complexity for individuals to effectively manage their relationships. We examined how different socially uncertain contexts, reflecting an increased level of social complexity, relate to variation in signalling within and between two species, which display varying levels of fission-fusion dynamics (sympatric-living chimpanzees and sooty mangabeys, Taï National Park, Ivory Coast). Combined signalling may improve message efficacy, notably when involving different perception channels, thus may increase in moments of high social uncertainty. We examined the probability of individuals to emit no signal, single or multisensory or combined (complex) signals, during social approaches which resulted in non-agonistic outcomes. In both species, individuals were more likely to use more combined and multisensory signals in post-conflict approaches with an opponent than in other contexts. The clearest impact of social uncertainty on signalling complexity was observed during chimpanzee fusions, where the likelihood of using complex signals tripled relative to other contexts. Overall, chimpanzees used more multisensory signals than mangabeys. Social uncertainty may shape detected species differences in variation in signalling complexity, thereby supporting the hypothesis that social complexity, particularly associated with high fission-fusion dynamics, promotes signalling complexity.

Music production and its role in coalition signaling during foraging contexts in a hunter-gatherer society.

Music is a cultural activity universally present in all human societies. Several hypotheses have been formulated to understand the possible origins of music and the reasons for its emergence. Here, we test two hypotheses: (1) the coalition signaling hypothesis which posits that music could have emerged as a tool to signal cooperative intent and signal strength of alliances and (2) music as a strategy to deter potential predators. In addition, we further explore the link between tactile cues and the propensity of mothers to sing toward infants. For this, we investigated the singing behaviors of hunter-gatherer mothers during daily foraging trips among the Mbendjele BaYaka in the Republic of the Congo. Although singing is a significant component of their daily activities, such as when walking in the forest or collecting food sources, studies on human music production in hunter-gatherer societies are mostly conducted during their ritual ceremonies. In this study, we collected foraging and singing behavioral data of mothers by using focal follows of five BaYaka women during their foraging trips in the forest. In accordance with our predictions for the coalition signaling hypothesis, women were more likely to sing when present in large groups, especially when group members were less familiar. However, predictions of the predation deterrence hypothesis were not supported as the interaction between group size and distance from the village did not have a significant effect on the likelihood of singing. The latter may be due to limited variation in predation risk in the foraging areas, because of the intense bush meat trade, and hence, future studies should include foraging areas with higher densities of wild animals. Lastly, we found that mothers were more likely to sing when they were carrying infants compared to when infants were close, but carried by others, supporting the prediction that touch plays an important prerequisite role in musical interaction between the mother and child. Our study provides important insight into the role of music as a tool in displaying the intent between or within groups to strengthen potentially conflict-free alliances during joint foraging activities.

Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees.

Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.

Parochial cooperation in wild chimpanzees: a model to explain the evolution of parochial altruism.

Parochial altruism, taking individual costs to benefit the in-group and harm the out-group, has been proposed as one of the mechanisms underlying the human ability of large-scale cooperation. How parochial altruism has evolved remains unclear. In this review paper, we formulate a parochial cooperation model in small-scale groups and examine the model in wild chimpanzees. As suggested for human parochial altruism, we review evidence that the oxytocinergic system and in-group cooperation and cohesion during out-group threat are integral parts of chimpanzee collective action during intergroup competition. We expand this model by suggesting that chimpanzee parochial cooperation is supported by the social structure of chimpanzee groups which enables repeated interaction history and established social ties between co-operators. We discuss in detail the role of the oxytocinergic system in supporting parochial cooperation, a pathway that appears integral already in chimpanzees. The reviewed evidence suggests that prerequisites of human parochial altruism were probably present in the last common ancestor between Pan and Homo. This article is part of the theme issue 'Intergroup conflict across taxa'.

Flexibility in the social structure of male chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda.

Individuals of social species experience competitive costs and social benefits of group living. Substantial flexibility in humans' social structure and the combination of different types of social structure with fission-fusion dynamics allow us to live in extremely large groups-overcoming some of the costs of group living while capitalizing on the benefits. Non-human species also show a range of social strategies to deal with this trade-off. Chimpanzees are an archetypical fission-fusion species, using dynamic changes in day-to-day association to moderate the costs of within-group competition. Using 4 years of association data from two neighbouring communities of East African chimpanzees (Pan troglodytes schweinfurthii), we describe an unexplored level of flexibility in chimpanzee social structure. We show that males from the larger Waibira community (N = 24-31) exhibited additional structural levels of semi-stable core-periphery society, while males from the smaller Sonso community (N = 10-13) did not. This novel core-periphery pattern adds to previous results describing alternative modular social structure in other large communities of chimpanzees. Our data support the hypothesis that chimpanzees can incorporate a range of strategies in addition to fission-fusion to overcome costs of social living, and that their social structures may be closer to that of modern humans than previously described.

Evaluating the efficacy of a consumer-centric method for ecological sampling: Using bonobo (Pan paniscus) feeding patterns as an instrument for tropical forest characterization.

Characteristics of food availability and distribution are key components of a species' ecology. Objective ecological surveying used in animal behavior research does not consider aspects of selection by the consumer and therefore may produce imprecise measures of availability. We propose a method to integrate ecological sampling of an animal's environment into existing behavioral data collection systems by using the consumer as the surveyor. Here, we evaluate the consumer-centric method (CCM) of assessing resource availability for its ability to measure food resource abundance, distribution, and dispersion. This method catalogs feeding locations observed during behavioral observation and uses aggregated data to characterize these ecological metrics. We evaluated the CCM relative to traditional vegetation plot surveying using accumulated feeding locations across 3 years visited by a tropical frugivore, the bonobo (Pan paniscus), and compared it with data derived from over 200 vegetation plots across their 50 km2+ home ranges. We demonstrate that food species abundance estimates derived from the CCM are comparable to those derived from traditional vegetation plot sampling in less than 2 years of data collection, and agreement improved when accounting for aspects of consumer selectivity in objective vegetation plot sampling (e.g., tree size minima). Density correlated between CCM and plot-derived estimates and was relatively insensitive to home range inclusion and other species characteristics, however, it was sensitive to sampling frequency. Agreement between the methods in relative distribution of resources performed better across species than expected by chance, although measures of dispersion correlated poorly. Once tested in other systems, the CCM may provide a robust measure of food availability for use in relative food availability indices and can be incorporated into existing observational data collection. The CCM has an advantage over traditional sampling methods as it incorporates sampling biases relevant to the consumer, thereby serving as a promising method for animal behavioral research.