Chimpanzee tool technology in the Goualougo Triangle, Republic of Congo

With the exception of humans, chimpanzees show the most diverse and complex tool-using repertoires of all extant species. Specific tool repertoires differ between wild chimpanzee populations, but no apparent genetic or environmental factors have emerged as definitive forces shaping variation between populations. However, identification of such patterns has likely been hindered by a lack of information from chimpanzee taxa residing in central Africa. We report our observations of the technological system of chimpanzees in the Goualougo Triangle, located in the Republic of Congo, which is the first study to compile a complete tool repertoire from the Lower Guinean subspecies of chimpanzee (Pan troglodytes troglodytes). Between 1999 and 2006, we documented the tool use of chimpanzees by direct observations, remote video monitoring, and collections of tool assemblages. We observed 22 different types of tool behavior, almost half of which were habitual (shown repeatedly by several individuals) or customary (shown by most members of at least one age-sex class). Several behaviors considered universals among chimpanzees were confirmed in this population, but we also report the first observations of known individuals using tools to perforate termite nests, puncture termite nests, pound for honey, and use leafy twigs for rain cover. Tool behavior in this chimpanzee population ranged from simple tasks to hierarchical sequences. We report three different tool sets and a high degree of tool-material selectivity for particular tasks, which are otherwise rare in wild chimpanzees. Chimpanzees in the Goualougo Triangle are shown to have one of the largest and most complex tool repertoires reported in wild chimpanzee populations. We highlight new insights from this chimpanzee population to our understanding of ape technological systems and evolutionary models of tool-using behavior.     

Social Network Analysis Shows Direct Evidence for Social Transmission of Tool Use in Wild Chimpanzees

Social network analysis methods have made it possible to test whether novel behaviors in animals spread through individual or social learning. To date, however, social network analysis of wild populations has been limited to static models that cannot precisely reflect the dynamics of learning, for instance, the impact of multiple observations across time. Here, we present a novel dynamic version of network analysis that is capable of capturing temporal aspects of acquisition—that is, how successive observations by an individual influence its acquisition of the novel behavior. We apply this model to studying the spread of two novel tool-use variants, “moss-sponging” and “leaf-sponge re-use,” in the Sonso chimpanzee community of Budongo Forest, Uganda. Chimpanzees are widely considered the most “cultural” of all animal species, with 39 behaviors suspected as socially acquired, most of them in the domain of tool-use. The cultural hypothesis is supported by experimental data from captive chimpanzees and a range of observational data. However, for wild groups, there is still no direct experimental evidence for social learning, nor has there been any direct observation of social diffusion of behavioral innovations. Here, we tested both a static and a dynamic network model and found strong evidence that diffusion patterns of moss-sponging, but not leaf-sponge re-use, were significantly better explained by social than individual learning. The most conservative estimate of social transmission accounted for 85% of observed events, with an estimated 15-fold increase in learning rate for each time a novice observed an informed individual moss-sponging. We conclude that group-specific behavioral variants in wild chimpanzees can be socially learned, adding to the evidence that this prerequisite for culture originated in a common ancestor of great apes and humans, long before the advent of modern humans.     

Are behavioral differences among wild chimpanzee communities genetic or cultural? An assessment using tool‐use data and phylogenetic methods

Over the last 30 years it has become increasingly apparent that there are many behavioral differences among wild communities of Pan troglodytes. Some researchers argue these differences are a consequence of the behaviors being socially learned, and thus may be considered cultural. Others contend that the available evidence is too weak to discount the alternative possibility that the behaviors are genetically determined. Previous phylogenetic analyses of chimpanzee behavior have not supported the predictions of the genetic hypothesis. However, the results of these studies are potentially problematic because the behavioral sample employed did not include communities from central Africa. Here, we present the results of a study designed to address this shortcoming. We carried out cladistic analyses of presence/absence data pertaining to 19 tool‐use behaviors in 10 different P. troglodytes communities plus an outgroup (P. paniscus). Genetic data indicate that chimpanzee communities in West Africa are well differentiated from those in eastern and central Africa, while the latter are not reciprocally monophyletic. Thus, we predicted that if the genetic hypothesis is correct, the tool‐use data should mirror the genetic data in terms of structure. The three measures of phylogenetic structure we employed (the Retention Index, the bootstrap, and the Permutation Tail Probability Test) did not support the genetic hypothesis. They were all lower when all 10 communities were included than when the three western African communities are excluded. Hence, our study refutes the genetic hypothesis and provides further evidence that patterns of behavior in chimpanzees are the product of social learning and therefore meet the main condition for culture. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

Oil Palm Use by Adjacent Communities of Chimpanzees at Bossou and Nimba Mountains,West Africa

We investigated oil palm (Elaeis guineensis) use for feeding in 3 chimpanzee communities: Bossou and Seringbara in Guinea and Yealé in Côte d'Ivoire. Bossou was used as the benchmark for comparison. Bossou chimpanzees (Pan troglodytes verus) exhibit a wide range of oil palm targeted behaviors. We used direct observations of their two tool use, i.e., nut-cracking and pestle pounding, to establish strict and reliable criteria to ascertain the presence of comparable behaviors at the two adjacent Nimba sites. Based on monthly surveys of oil palms across the three sites, significant differences in patterns of use emerged. Bossou chimpanzees demonstrated the greatest frequency of oil palm use, while Seringbara chimpanzees, 6 km away, failed to exhibit any use and Yealé chimpanzees, 12 km away, showed all uses comparable to Bossou chimpanzees except pestle pounding and mature leaf pith-feeding. We examined the density and distribution of oil palms, tool availability for nut-cracking and pestle pounding, fruit, flower and nut availability, competition with sympatric species for fruit and nuts and the diversity of fruit species in the diet across the 3 sites. We found no clear difference in proximate environmental variables underlying observed variations in oil palm use among the 3 sites, yielding the conclusion that the differences are cultural. Assuming individual interchange between communities and the involvement of social learning in the intracommunity transmission and maintenance of oil palm uses, the result raises interesting questions about diffusion of behavior between neighboring chimpanzee communities.     

The influence of AVPR1A genotype on individual differences in behaviors during a mirror self‐recognition task in chimpanzees (Pan troglodytes)

The mark/rouge test has been used to assess mirror self‐recognition (MSR) in many species. Despite consistent evidence of MSR in great apes, genetic or non‐genetic factors may account for the individual differences in behavioral responses that have been reported. We examined whether vasopressin receptor gene (AVPR1A) polymorphisms are associated with MSR‐related behaviors in chimpanzees since vasopressin has been implicated in the development and evolution of complex social relations and cognition and chimpanzees are polymorphic for the presence of the RS3‐containing DupB region. We compared a sample of DupB+/? and DupB?/? chimpanzees on a mark test to assess its role on social behavior toward a mirror. Chimpanzees were administered two, 10‐min sessions where frequencies of mirror‐guided self‐directed behaviors, contingent actions and other social behaviors were recorded. Approximately one‐third showed evidence of MSR and these individuals exhibited more mirror‐guided self‐exploratory behaviors and mouth contingent actions than chimpanzees not classified as passers. Moreover, DupB+/? males exhibited more scratching and agonistic behaviors than other male and female cohorts. Our findings support previous studies demonstrating individual differences in MSR abilities in chimpanzees and suggest that AVPR1A partly explains individual differences in MSR by influencing the behavioral reactions of chimpanzees in front of a mirror.     

Transmission of multiple traditions within and between chimpanzee groups

Field reports provide increasing evidence for local behavioral traditions among fish, birds, and mammals. These findings are significant for evolutionary biology because social learning affords faster adaptation than genetic change and has generated new (cultural) forms of evolution. Orangutan and chimpanzee field studies suggest that like humans, these apes are distinctive among animals in each exhibiting over 30 local traditions. However, direct evidence is lacking in apes and, with the exception of vocal dialects, in animals generally for the intergroup transmission that would allow innovations to spread widely and become evolutionarily significant phenomena. Here, we provide robust experimental evidence that alternative foraging techniques seeded in different groups of chimpanzees spread differentially not only within groups but serially across two further groups with substantial fidelity. Combining these results with those from recent social-diffusion studies in two larger groups offers the first experimental evidence that a nonhuman species can sustain unique local cultures, each constituted by multiple traditions. The convergence of these results with those from the wild implies a richness in chimpanzees' capacity for culture, a richness that parsimony suggests was shared with our common ancestor.     

Social learning and evolution: the cultural intelligence hypothesis

If social learning is more efficient than independent individual exploration, animals should learn vital cultural skills exclusively, and routine skills faster, through social learning, provided they actually use social learning preferentially. Animals with opportunities for social learning indeed do so. Moreover, more frequent opportunities for social learning should boost an individual's repertoire of learned skills. This prediction is confirmed by comparisons among wild great ape populations and by social deprivation and enculturation experiments. These findings shaped the cultural intelligence hypothesis, which complements the traditional benefit hypotheses for the evolution of intelligence by specifying the conditions in which these benefits can be reaped. The evolutionary version of the hypothesis argues that species with frequent opportunities for social learning should more readily respond to selection for a greater number of learned skills. Because improved social learning also improves asocial learning, the hypothesis predicts a positive interspecific correlation between social-learning performance and individual learning ability. Variation among primates supports this prediction. The hypothesis also predicts that more heavily cultural species should be more intelligent. Preliminary tests involving birds and mammals support this prediction too. The cultural intelligence hypothesis can also account for the unusual cognitive abilities of humans, as well as our unique mechanisms of skill transfer.     

Social influences on foraging behavior in young nonhuman primates: Learning what,where, and how to eat

Human infants rely on social interactions to acquire food‐related information. 1 , 2 Adults actively teach children about food through culturally diverse feeding practices. Characteristics we share with the other primates, such as complex diets, highly social lives, and extended juvenile periods, suggest that social learning may be important during ontogeny throughout the order. Although all young primates typically pay attention to feeding adults, great apes and callitrichids, in particular, acquire new foraging techniques through abilities unknown in other nonhuman primates; that is, they learn by imitation. However, ape social learning is almost exclusively infant‐initiated, while adult callitrichids actively teach their young. It is unlikely that the same selective forces have acted to favor sophisticated social‐learning mechanisms in both taxa. 3 , 4 Equipped with an ape brain, complex foraging methods, and a cooperative infant‐care system, early hominins were uniquely poised to take social learning about food and foraging techniques to a new level.     

Implementing long‐term baselines into primate tool‐use studies

Studies on primate tool‐use often involve the use of baseline conditions, as they allow for the examination of any differences in the subjects' behavior before and after the introduction of a tool‐use task. While these baseline conditions can be powerful for identifying the relative contributions of individual and social learning for the acquisition of tool‐use behaviors in naïve (usually captive) subjects, many have criticized them for being too short, and not allowing enough time for the behavior to develop spontaneously. Furthermore, some wild tool‐use behaviors such as chimpanzee nut‐cracking require animals to manipulate and familiarize themselves with the materials of the behavior within a “sensitive learning period” before it develops later on in life. One solution to this problem is to implement long‐term baselines, in which, with collaboration with zoological institutions, the materials of the behavior are left in the enclosure for an extended period. The keepers would then be asked not to demonstrate or train the animals in the target behavior, but to report back to the researchers if they observe the behavior emerge during this extended period. Alongside keeper reports, video cameras could be installed in the enclosure to minimize the chance of false negatives and to allow for coding and inter‐rater reliability to be carried out on the videos. These long‐term baselines therefore provide extended enrichment opportunities for the animals, alongside allowing the zoological institution to publicize their involvement with the study and guests to observe animals interacting with different testing apparatuses and tools. Finally, long‐term baselines can provide invaluable insight on the individual and social learning abilities of primates as well as the potential development stages and sensitive learning periods required for specific behaviors.     

“Stepping-sticks” and “seat-sticks”: New types of tools used by wild chimpanzees (Pan troglodytes) in Sierra Leone

In Tenkere, Sierra Leone, a community of wild chimpanzees (Pan troglodytes verus) spent long hours eating the fruits and flowers of the Kapok (Ceiba pentandra) tree. The branches of this species are covered in sharp thorns which make movement in their high canopies problematic for the chimpanzees. In an apparent attempt to increase their mobility and to ease the discomfort of lengthy bouts of eating in these trees, some of the Tenkere chimpanzees have been observed using stick tools as foot (“stepping-sticks”) and body (“seat-sticks”) protection against the painful thorns. This form of tool-using is culturally unique to the Tenkere chimpanzees, as at other sites where these apes have been observed eating parts of kapok trees, there are no published records of this tool technology. In three of the stepping-stick tool use incidents, the chimpanzee used the tool(s), held between their greater and lesser toes, in locomotion. This form of tool use is the first recorded case of habitually used tools that can be justifiably categorized as being “worn” by any known wild population of Pan troglodytes. Am J Primatol 41:45–52, 1997. © 1997 Wiley-Liss, Inc.     

Is culture a golden barrier between human and chimpanzee?

Culture pervades much of human existence. Its significance to human social interaction and cognitive development has convinced some researchers that the phenomenon and its underlying mechanisms represent a defining criterion for humankind. However, care should be taken not to make hasty conclusions in light of the growing number of observations on the cultural abilities of different species, ranging from chimpanzees and orangutans to whales and dolphins. The present review concentrates on wild chimpanzees and shows that they all possess an extensive cultural repertoire. In the light of what we know from humans, I evaluate the importance of social learning leading to acquisition of cultural traits, as well as of collective meaning of communicative traits. Taking into account cross‐cultural variations in humans, I argue that the cultural abilities we observe in wild chimpanzees present a broad level of similarity between the two species.     

Dominance rank and fecal testosterone levels in adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda

In an attempt to describe hormone-behavior interactions in a sample of wild male chimpanzees, we quantified testosterone in 67 fecal samples obtained from 22 adult male chimpanzees at Ngogo, Kibale National Park, Uganda. A mixed-model methodology that controlled for age-class identified a significant positive association between testosterone levels and dominance rank. The results are consistent with those reported from a separate, smaller chimpanzee community in the same population in a study that analyzed testosterone levels in urine [Muller & Wrangham, 2004]. As in that earlier study, our results held during a period of social stability, which is not consistent with predictions of the "challenge hypothesis." We concur with Muller and Wrangham [2004] that the challenge hypothesis requires modification to explain the chimpanzee data, because fission-fusion sociality in chimpanzees makes challenges unpredictable. We also discuss the utility of fecal samples and a mixed-model statistical method for behavioral endocrinology studies.     

Nutritional composition of actual and potential insect prey for the Kasekela chimpanzees of Gombe National Park,Tanzania

Humans, all great ape species, and some lesser apes consume insects. Insects can provide comparable nutritional yields to meat on a gram‐for‐gram basis and may serve as an important source of energy, fat, protein, minerals, and vitamins for hominoids. Although potential insect prey are abundant in ape habitats, patterns of insectivory are not consistent across species or populations. Efforts to understand these patterns are complicated by a lack of nutritional data. We collected samples of insects consumed by the Kasekela chimpanzee community of Gombe National Park, Tanzania, as well as of some insects found within the community range and ignored by these chimpanzees but known to be preyed upon by Pan elsewhere. We determined the gross energy (GE), estimated metabolizable energy (ME), fat, protein, fiber, and ash content of these samples following standard methodologies. We use these data to test the hypothesis that Kasekela chimpanzees choose insect prey (at least in part) based on energy and/or macronutrient content. On a fresh‐weight, per‐gram basis, the insect prey consumed by Kasekela chimpanzees had significantly higher fat and lower ash content than other assayed insects, and on a fresh‐weight, per‐foraging‐unit (“per‐insect,” “per‐dip,” or “per‐nest”) basis were significantly higher in GE, fat, and protein. On a per‐gram basis, the assayed insects were generally comparable in energy and macronutrients to wild vertebrate meat. We conclude that Kasekela chimpanzees do favor insects that are high in energy, fat, and protein, and that the potential macronutrient yields from some forms of insectivory are not trivial. © 2012 Wiley Periodicals, Inc.     

Innovative social behavior in chimpanzees (Pan troglodytes)

We present evidence of agonistic buffering in captive chimpanzees, recorded from 1993 until 2005, mainly from ad libitum sampling in over 2000 hr of observation. A total of 33 agonistic buffering episodes were analyzed for context and effects of this complex social behavior. Agonistic buffering was directed at the whole chimpanzee colony as they supported an individual who initially received aggression from the alpha male, independently of the victim's age, sex or social rank. Chimpanzee agonistic buffering behavior is compared with that in other nonhuman primate species, and we describe some particularities of chimpanzee agonistic buffering: the status of the buffers used-socially important offspring such as those from the alpha female-and the social rank of the adult male responsible for the buffering episode-alpha male. Possible functions for this behavior in chimpanzees are suggested as appeasement of group members in a particularly crowded captive setting, and/or as a "forced reconciliation" mechanism. Chimpanzees exhibit behavioral flexibility by adapting themselves to new social and physical situations and use novel behavior to achieve social benefits.     

Vocal responsiveness in male wild chimpanzees: implications for the evolution of language

Several captive chimpanzees and bonobos have learned to use symbols and to comprehend syntax. Thus, compared with other nonhumans, these animals appear to have unusual cognitive powers that can be recruited for communicative behavior. This raises the possibility that wild chimpanzee vocal communication is more complex than heretofore demonstrated. To examine this possibility, I investigated whether wild chimpanzee vocal exchanges exhibit uniquely human conversational attributes. The results indicate that wild chimpanzees vocalize at low rates, tend not to respond to calls that they hear, and, when they do respond, tend to give calls that are similar to the ones they have heard. Thus, chimpanzee vocal interactions resemble those of other primate species, and show no special similarity to human conversations. The results support the view that we need to explore cognitive and social continuities and discontinuities with nonhuman primates to understand the origin and evolution of language, but also emphasize the need for fine-grained analyses of wild chimpanzee vocal interactions.     

A model for tool-use traditions in primates: implications for the coevolution of culture and cognition

Inspired by the demonstration that tool-use variants among wild chimpanzees and orangutans qualify as traditions (or cultures), we developed a formal model to predict the incidence of these acquired specializations among wild primates and to examine the evolution of their underlying abilities. We assumed that the acquisition of the skill by an individual in a social unit is crucially controlled by three main factors, namely probability of innovation, probability of socially biased learning, and the prevailing social conditions (sociability, or number of potential experts at close proximity). The model reconfirms the restriction of customary tool use in wild primates to the most intelligent radiation, great apes; the greater incidence of tool use in more sociable populations of orangutans and chimpanzees; and tendencies toward tool manufacture among the most sociable monkeys. However, it also indicates that sociable gregariousness is far more likely to produce the maintenance of invented skills in a population than solitary life, where the mother is the only accessible expert. We therefore used the model to explore the evolution of the three key parameters. The most likely evolutionary scenario is that where complex skills contribute to fitness, sociability and/or the capacity for socially biased learning increase, whereas innovative abilities (i.e., intelligence) follow indirectly. We suggest that the evolution of high intelligence will often be a byproduct of selection on abilities for socially biased learning that are needed to acquire important skills, and hence that high intelligence should be most common in sociable rather than solitary organisms. Evidence for increased sociability during hominin evolution is consistent with this new hypothesis.     

Effects of early rearing conditions on problem‐solving skill in captive male chimpanzees (Pan troglodytes)

Early rearing conditions of captive chimpanzees characterize behavioral differences in tool use, response to novelty, and sexual and maternal competence later in life. Restricted rearing conditions during early life hinder the acquisition and execution of such behaviors, which characterize the daily life of animals. This study examined whether rearing conditions affect adult male chimpanzees' behavior skills used for solving a problem with acquired locomotion behavior. Subjects were 13 male residents of the Chimpanzee Sanctuary Uto: 5 wild‐born and 8 captive‐born. A pretest assessed bed building and tool use abilities to verify behavioral differences between wild‐ and captive‐born subjects, as earlier reports have described. Second, a banana‐access test was conducted to investigate the problem‐solving ability of climbing a bamboo pillar for accessing a banana, which might be the most efficient food access strategy for this setting. The test was repeated in a social setting. Results show that wild‐born subjects were better able than captive‐born subjects to use the provided materials for bed building and tool use. Results of the banana‐access test show that wild‐born subjects more frequently used a bamboo pillar for obtaining a banana with an efficient strategy than captive‐born subjects did. Of the eight captive‐born subjects, six avoided the bamboo pillars to get a banana and instead used, sometimes in a roundabout way, an iron pillar or fence. Results consistently underscored the adaptive and sophisticated skills of wild‐born male chimpanzees in problem‐solving tasks. The rearing conditions affected both the behavior acquisition and the execution of behaviors that had already been acquired. Am. J. Primatol. 72:626–633, 2010. © 2010 Wiley‐Liss, Inc.     

Acquisition of a socially learned tool use sequence in chimpanzees: Implications for cumulative culture

Cumulative culture underpins humanity's enormous success as a species. Claims that other animals are incapable of cultural ratcheting are prevalent, but are founded on just a handful of empirical studies. Whether cumulative culture is unique to humans thus remains a controversial and understudied question that has far-reaching implications for our understanding of the evolution of this phenomenon. We investigated whether one of human's two closest living primate relatives, chimpanzees, are capable of a degree of cultural ratcheting by exposing captive populations to a novel juice extraction task. We found that groups (N = 3) seeded with a model trained to perform a tool modification that built upon simpler, unmodified tool use developed the seeded tool method that allowed greater juice returns than achieved by groups not exposed to a trained model (non-seeded controls; N = 3). One non-seeded group also discovered the behavioral sequence, either by coupling asocial and social learning or by repeated invention. This behavioral sequence was found to be beyond what an additional control sample of chimpanzees (N = 1 group) could discover for themselves without a competent model and lacking experience with simpler, unmodified tool behaviors. Five chimpanzees tested individually with no social information, but with experience of simple unmodified tool use, invented part, but not all, of the behavioral sequence. Our findings indicate that (i) social learning facilitated the propagation of the model-demonstrated tool modification technique, (ii) experience with simple tool behaviors may facilitate individual discovery of more complex tool manipulations, and (iii) a subset of individuals were capable of learning relatively complex behaviors either by learning asocially and socially or by repeated invention over time. That chimpanzees learn increasingly complex behaviors through social and asocial learning suggests that humans' extraordinary ability to do so was built on such prior foundations.