Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Behavioral Variation in Gorillas: Evidence of Potential Cultural Traits

  • Martha M. Robbins ,

    robbins@eva.mpg.de

    Affiliation Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

  • Chieko Ando,

    Affiliation Kyoto Prefectural University, Graduate School of Life and Environmental Sciences, Kyoto, Japan

  • Katherine A. Fawcett,

    Affiliation Dian Fossey Gorilla Fund International, Atlanta, GA, United States of America

  • Cyril C. Grueter,

    Affiliations Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany, School of Anatomy, Physiology and Human Biology, The University of Western Australia, Crawley (Perth), WA 6009, Australia

  • Daniela Hedwig,

    Affiliation Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

  • Yuji Iwata,

    Affiliation Kyoto Prefectural University, Graduate School of Life and Environmental Sciences, Kyoto, Japan

  • Jessica L. Lodwick,

    Affiliation Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, New York, United States of America

  • Shelly Masi,

    Affiliation Muséum National d¹Histoire Naturelle, Musée de l’Homme, National Center for Scientific Research (CNRS), University Paris Diderot (Paris 7) Éco-anthropologie et Ethnobiologie, Paris, France

  • Roberta Salmi,

    Affiliation Department of Anthropology, University of Georgia, Athens, GA, United States of America

  • Tara S. Stoinski,

    Affiliation Dian Fossey Gorilla Fund International, Atlanta, GA, United States of America

  • Angelique Todd,

    Affiliation World Wildlife Fund-CAR, Bangui, Central African Republic

  • Veronica Vercellio,

    Affiliation Dian Fossey Gorilla Fund International, Atlanta, GA, United States of America

  • Juichi Yamagiwa

    Affiliation Kyoto University, Graduate School of Sciences, Kyoto, Japan

Behavioral Variation in Gorillas: Evidence of Potential Cultural Traits

  • Martha M. Robbins, 
  • Chieko Ando, 
  • Katherine A. Fawcett, 
  • Cyril C. Grueter, 
  • Daniela Hedwig, 
  • Yuji Iwata, 
  • Jessica L. Lodwick, 
  • Shelly Masi, 
  • Roberta Salmi, 
  • Tara S. Stoinski
PLOS
x

Abstract

The question of whether any species except humans exhibits culture has generated much debate, partially due to the difficulty of providing conclusive evidence from observational studies in the wild. A starting point for demonstrating the existence of culture that has been used for many species including chimpanzees and orangutans is to show that there is geographic variation in the occurrence of particular behavioral traits inferred to be a result of social learning and not ecological or genetic influences. Gorillas live in a wide variety of habitats across Africa and they exhibit flexibility in diet, behavior, and social structure. Here we apply the ‘method of exclusion’ to look for the presence/absence of behaviors that could be considered potential cultural traits in well-habituated groups from five study sites of the two species of gorillas. Of the 41 behaviors considered, 23 met the criteria of potential cultural traits, of which one was foraging related, nine were environment related, seven involved social interactions, five were gestures, and one was communication related. There was a strong positive correlation between behavioral dissimilarity and geographic distance among gorilla study sites. Roughly half of all variation in potential cultural traits was intraspecific differences (i.e. variability among sites within a species) and the other 50% of potential cultural traits were differences between western and eastern gorillas. Further research is needed to investigate if the occurrence of these traits is influenced by social learning. These findings emphasize the importance of investigating cultural traits in African apes and other species to shed light on the origin of human culture.

Introduction

Culture in non-human animals, defined as ‘group-typical behavioral patterns shared by community members that to some degree are reliant on socially learned and transmitted information [1,2], has sparked much interest among scientists for several reasons, but particularly because of the implications for understanding the origins of culture in humans [24]. Cultural traits may originate from innovation, followed by diffusion among individuals through social learning (i.e. ‘learning as a result of interacting with or observing another individual or its products’[5]. Several approaches have been used to address the challenge of demonstrating the existence of cultural traits and social learning in wild animals [6]. Observational studies providing evidence that within- and between- population variation in behavior is a result of social learning and transmission have argued that there are social traditions or culture in many species including chimpanzees [79], bonobos [10], orangutans [11], capuchin monkeys [12,13], spider monkeys [14,15], meerkats [16,17], dolphins [18,19], whales [20] and birds and fish [21]. Additionally, experiments in captivity and the wild have shown that different methods of solving complex tasks can be transmitted among group members (e.g. [2125].

Cultural traits in animals span the domains of diet [26,27], foraging techniques [8,16,28,29], tool use [7,30,31], and social interactions [13,14,32,33]. Cultural social interactions may include ‘social conventions’, which are defined as dyadic social behaviors or communicative behaviors which are unique to particular groups or cliques [13,34,35]. Behavioral traits considered to be cultural in non-human animals may result in improved nutritional intake, strengthened social bonds, or exhibit no obvious fitness advantage in some cases [12,36]. As a way to emphasize the complexity of cultural phenomena, some authors have restricted the presence of culture to those species with traditions in at least two different behavioral domains [35].

A commonly used starting point for demonstrating the existence of culture in wild animals is to use a geographic approach, or method of exclusion, in which researchers look for the presence/absence of particular behaviors in different social groups or populations (e. g. [9,11,13,14]). Following the method of exclusion, one can argue that a trait is cultural if a) a behavioral trait is customary (performed by most individuals of a particular age/sex class) or habitual (performed by several individuals of a particular age/sex class) in at least one site but absent in at least one site, b) if both ecological and genetic explanations can be inferred to be excluded as the explanation and c) if innovation and/or social learning can be inferred (ibid). This cross-site comparison approach has been criticized because conclusively eliminating any ecological or genetic influence on the behavioral variability is difficult, if not impossible, and because it relies on inference of social learning (e.g. [2], whereas some of the traits may be acquired through reinvention [37]). However, cultural traits are likely to be influenced by ecological conditions since ecology, genetics, and culture interact [38, 39].

To address the concern that ecological variation, not culture, may explain behavioral variation, detailed field studies in which behavioral variability was measured, while accounting for fine scale ecological variability, have provided more convincing evidence of cultural trait variation between populations [8] and between neighboring social units [7,17, 36]. Addressing whether or not there is a genetic influence on behavioral variability in wild populations is complicated. Langergraber et al. [40] found that levels of genetic and behavioral similarity were strongly correlated among chimpanzee populations and that only a few behaviors varied between genetically similar groups; yet these results do not eliminate the possibility that the traits are cultural because a) such a correlation does not mean that the occurrence of particular traits is solely genetically driven and causing the observed pattern of similarities and differences and b) some variation is still observed between genetically similar groups. Furthermore, according to the diffusion hypothesis, the spread (or diffusion) of a cultural trait is likely to radiate from its point of origin, such that behavioral similarity and geographic distance should be negatively correlated [11]. Geographic distance among populations is likely to be negatively correlated also to genetic similarity, making it difficult to disentangle the effects of social diffusion and genetic influence. Furthermore, the degree that a trait is acquired by individuals (via mechanisms such as stimulus enhancement or emulation learning or individual reinvention) may vary depending on the difficulty of the trait in relation to the ‘zone of latent solutions’ of the species [37]. Nonetheless, the method of exclusion is a useful approach for cataloguing behavioral variation of potential cultural traits for further study of causes of variation (hidden environmental and/or genetic), underlying mechanisms of social learning, and evidence of cultural variation [41].

Among the great apes, the least amount of evidence for culture and social learning is available for gorillas [42,43]. However, gorillas possess characteristics that are predicted to promote social learning and transmission such as a long developmental period, overlapping generations, and regular social interactions among group members living in stable social groups [44]. Gorillas live in a wide variety of habitats and they exhibit variability in morphology, diet, behavior, and social structure [4549]. The genus Gorilla was considered one species until 2001 when it was reclassified to be divided into two species, each having two subspecies [50]. Western gorillas (Gorilla gorilla) are found in seven central African countries and eastern gorillas (Gorilla beringei) are found in three, with the two species being separated by approximately 1000 km (Fig 1). The two species are believed to have initially split roughly 1.2–3 MYA, but with some gene flow until as recently as 80,000–200,000 years ago [5153]. Each species consists of two subspecies and this study examines only the subspecies Gorilla gorilla gorilla (western gorillas) and Gorilla beringei beringei (mountain gorillas).

thumbnail
Fig 1. Map of the five gorilla study sites.

Western Gorillas: 1. Moukalaba-Doudou National Park, Gabon 2. Bai Hokou, Dzanga-Ndoki National Park, Central African Republic 3. Mondika, located along the border of Dzanga-Sangha National Park, Central African Republic and Nouabale Ndoki National Park, Republic of Congo. Mountain Gorillas: 4. Bwindi Impenetrable National Park, Uganda 5. Karisoke Research Center, Volcanos National Park, Rwanda. Blue indicates the distribution of western gorillas (Gorilla gorilla) and green indicates the distribution of eastern gorillas (Gorilla beringei).

https://doi.org/10.1371/journal.pone.0160483.g001

Despite large variation in ecological conditions, the basic social structure of gorilla groups is consistent across all localities, with groups composed of an average of ten individuals with at least one adult male (silverback), several adult females and offspring [46,54]. However, group size may vary considerably, with groups containing more than one silverback and more than 20 individuals occurring almost exclusively in mountain gorillas [47]. Even after nearly five decades of research, the majority of our knowledge about gorillas comes from the Karisoke Research Center in Rwanda, which is located at an ecological extreme for primates with some groups living at over 3000m altitude. Our limited knowledge of other gorilla populations until recently stemmed largely from the difficulties of habituating western gorillas and hence an inability to collect detailed data on their behavioral patterns, and only limited efforts to study other populations of eastern gorillas. However, in the past decade additional study sites of habituated gorillas have developed, providing an opportunity to examine variability in their behavior.

The first goal of this paper is to generate a list of potential cultural traits in wild gorillas from five sites by examining variation in the occurrence of behavioral traits that could potentially be influenced by social learning and not due to ecological or genetic variation (using the method of exclusion). We then classify these traits according to behavioral domains (e.g. foraging, environment related, social, or gestural). Second, we quantify the degree of dissimilarity across sites and examine the relationship between geographic distance and behavioral dissimilarity. We expect behavioral dissimilarity to increase as the distance between study sites increases. Lastly, we discuss rarely observed behaviors that may reflect innovations [55] as well as behaviors that were present in all sites but varied in frequency of occurrence, as they may be potential universal cultural traits [15].

Methods

Ethics Statement

This study was conducted with wild free-ranging animals and was completely observational. Research was conducted in accordance with guidelines of the national authorities where the work occurred. Approval and permission to conduct research was granted by the Uganda Wildlife Authority, the Uganda National Council of Science and Technology, the Rwanda Development Board, Ministry of Education and Water and Forests of the government of Central African Republic for permission to work in Dzanga-Ndoki National Park, the Ministries of Scientific Research and Forest and Water in the Central African Republic and Republic of Congo for permission to conduct research at Mondika, and the Centre National de la Recherche Scientifique (CENAREST) and the Agence Nationale des Parcs Nationaux (ANPN) in Gabon.

Study Sites

Data were collected from five sites with habituated gorillas (Fig 1; Table 1). Gorilla groups were followed on a near daily basis at all sites, observed for a minimum of four hours per day, and observations of focal animals were conducted on a regular basis on various topics (i.e. diet, social interactions, communication [5666]). The three western gorilla sites are separated from the two mountain gorilla sites by approximately 1500–2100 km (see Table 2 for distance among all study sites). All the groups were monitored on a nearly daily by field assistants and we report the observation time (days) by the people contributing to this project (Table 1).

thumbnail
Table 1. Details of the observations made at the five study sites.

Total group size and the age sex classes include the range of number of individuals during the course of the study. Not all groups were observed for the entire duration of the study period for the sites with more than one group.

https://doi.org/10.1371/journal.pone.0160483.t001

thumbnail
Table 2. Overall behavioral dissimilarity between gorilla study sites using Manhattan distances (above diagonal; see methods for calculation) and geographic distance (below diagonal) in the ten pairs of study sites.

https://doi.org/10.1371/journal.pone.0160483.t002

Three groups of western gorillas (Gorilla gorilla gorilla) were observed at Bai Hokou, Dzanga-Ndoki National Park, in south-western Central African Republic (CAR), three groups were observed at the Mondika Research Center which straddles the border of the Central African Republic and the Republic of Congo, and one group was observed in Moukalaba-Doudou National Park, Gabon. Bai Hokou and Mondika are separated by only 60 km of contiguous rainforest. Both are composed primarily of low altitude (<400 m) mixed-species semi-evergreen forest [67,68]. The habitat of the gorillas in Bai Hokou includes open clearings, referred to as ‘bais’, whereas part of the home range of the groups in Mondika is swamp. Moukalaba-Doudou is located approximately 800 km away from those two sites and is composed of secondary forest, Musanga cecropioides forest, and savanna [69]. Observations of habituated gorillas were made by three observers at each of these sites spanning (not concurrently) a time period of over four years. All groups of western gorillas included in the study contained only one silverback, whereas both one-male and multimale mountain groups were observed.

The two populations of mountain gorillas (Gorilla beringei beringei) are located approximately 30 km apart from each other at the nearest point (study groups approximately 45 km apart), separated by an expanse of cultivated and developed land, preventing any migration between the two areas for at least the past several hundred years [70]. Three groups of mountain gorillas at the Karisoke Research Center, in the Volcanoes National Park, Rwanda were observed regularly for a period of three years (2006–2008) and following various group fissions and new group formations, an additional six groups were observed through 2014. The Virunga Volcanoes is the only location inhabited by gorillas that does not contain large fruiting trees. One group of gorillas was observed for 13 years in Bwindi Impenetrable National Park, Uganda.

Survey Procedure

First, based on our knowledge of gorilla behavior we generated a list of 41 behaviors that were likely to vary across sites. For each site, we categorized each behavior following [11], which is slightly modified from [9]. Numerical codes were assigned to each behavioral category following [40]. The categories and numerical codes used were as follows:

Customary (3): when the behavior occurred in all or most members of at least one age-sex class.

Habitual (2): when the behavior was observed repeatedly in several individuals, but was not customary.

Present (1): when the behavior was observed, but was neither customary nor habitual.

Absent (0): when the behavior was not observed and no ecological explanation is apparent.

Ecological Explanation: when the behavior was absent because of a local ecological feature, such as the presence or absence of a particular plant.

We then examined the results across sites and classified each trait as either variable across sites or universal among all sites. Finally, we were left with traits that varied among sites, excluding those with a straightforward ecological explanation. We considered traits that were classified as either customary or habitual in at least one population and absent in at least one other as potential cultural traits following Whiten et al. [9] and van Schaik et al. [11]. Behaviors that were neither customary nor habitual at any site (e.g. only present at one or more site) were not included as potential cultural variants (following previous studies) but are reported here as rare behaviors. We also categorized the traits as being foraging techniques, gestures, a component of social interactions among individuals, or environment related (those that involved a physical component of the environment and not another gorilla, but were not related to foraging). We next sorted potential cultural traits based on whether they differed within species, between species (i.e. western and eastern gorillas), or with no apparent pattern. Traits that were excluded for ecological explanations were those that could not occur at some sites due to ecological conditions, but occurred in all locations with suitable ecological conditions.

To test the prediction that behavioral dissimilarity increases as the distance between study sites increases, we used the numerical codes of the traits that were deemed as potential cultural variants to calculate the overall behavioral dissimilarity among the ten dyads of gorilla sites. Following Langergraber et al. [40], we used the Manhattan distance, which is the sum of the absolute values of the differences between the behavioral variants for a dyad of study sites (i.e. if the numerical code for a trait at one site is three, but one at another site is one, the absolute difference is two). Next, differences for all behavioral variants per dyad were then summed. The greater the difference between two study sites, the larger the difference in behavioral patterns. Because subtraction requires two numbers, behavioral variants with missing values (i.e. due to ecological explanations; for example, termites not present in mountain gorilla habitat) were excluded pairwise but not from the entire list. This does not bias the results because we are interested in the amount of behavioral dissimilarity that is due to potential cultural variation. We compared the behavioral dissimilarity among populations with geographic distance between locations using Pearson correlation coefficients calculated with a Mantel matrix permutation using 10,000 permutations to account for each population occurring multiple times in all the comparisons (ten dyadic comparisons among the five study sites).

Results

From the 41 behaviors examined, we identified 23 potential cultural traits (Table 3), which were habitual or customary at least at one site while absent from at least one other site. Of these, one was foraging related, nine were environment related, seven involved social interactions, five were gestures, and one was communication related. Roughly half (52%) of the potential cultural traits was variable within a species, whereas the other half (48^) distinguished the western from mountain gorillas. For the twelve traits that did not show clear differences between species, absence was recorded in at least one population and there were varying degrees of occurrence among the other populations with no clear pattern between the western and mountain gorillas. Comparing between the two mountain gorilla sites, of the 23 potential cultural traits, seven were absent at one site but occurred in the other, six were absent at both, eight occurred in both study sites, and two had ecological explanations for the absence at one location. Comparing among only the three western gorilla sites, ten behaviors were absent at one or two sites, four were absent at all three sites, and nine occurred at all three sites.

The remaining 18 traits could not be considered as potential cultural traits (Table 3). Three traits were observed in all populations but at varying degree of occurrence, so could be considered as universals. Five could be eliminated due to ecological explanations, with the trait occurring at all locations with suitable ecological conditions. Lastly, ten behaviors were rarely observed in one or more populations and were not observed to the level of habitual in any population.

The behavioral dissimilarities, quantified using the Manhattan distances, ranged between 16 and 48 (n = 10; Table 2; the highest possible score was 69). The four lowest Manhattan distances (having most behavioral similarity) were in the dyad containing the two mountain gorilla populations and dyads where both populations were western gorillas (Table 2). Geographic distances among the sites ranged from 45 to 2095 km (Table 2). The behavioral dissimilarities and geographic distance between sites were strongly correlated (Pearson’s r = 0.930; p = 0.008; Fig 2).

thumbnail
Fig 2. Behavioral dissimilarity (quantified as Manhattan distance; see methods for explanation) plotted against geographic distance among five gorilla study sties.

Each data point represents a dyad of two sites (two of the 10 dyads have the same value; hence only nine points are visible). As the geographic distance between sites increases, the dissimilarity in behavioral traits increases.

https://doi.org/10.1371/journal.pone.0160483.g002

Discussion

This study adds to the growing body of evidence of behavioral variants across many taxa that may be considered as potential cultural traits. We observed variation in occurrence of behaviors among gorillas at five field sites spanning behavioral domains of social interactions, gestural communication, environment related behaviors, and one foraging behavior. The strong correlation between the behavioral dissimilarity and geographic distance (a proxy for genetic similarity) indicates that a genetic influence cannot be ruled out as affecting the occurrence of the behavioral traits among the populations, particularly between the mountain gorillas and western gorillas, but it does not exclude the possibility of social learning. Alternatively, the correlation between the behavioral dissimilarity and geographic distance provides support for the behavioral diffusion hypothesis, in which there is more similarity in behavioral patterns among nearby populations and declines as distance increases because the trait has not spread further. However the low score between two western gorilla sites that are far from each other (Bai Hokou and Moukalaba), indicating that they have high similarity in the occurrence of traits, in comparison to Bai Hokou and Mondika, which are only 60 km apart from each other, would argue against both the genetic and diffusion hypotheses. Social learning and transmission may occur through a variety of processes including stimulus enhancement and emulation (see Whiten [71] for review). It is also possible that these traits were spontaneously reinvented at the different sites based on the ‘zone of latent solutions’ hypothesis [37].

We observed variation in the occurrence of half of the potential cultural traits between the two mountain gorilla sites, among the three western gorilla sites, and among all five sites (Table 3). Half of the behavioral variants reflected differences between western gorillas and mountain gorillas, which currently are classified as subspecies of two different species. We believe making a comparison on the species level is valid, as a similar approach was taken when examining culture in two species of orangutans [11,72], which diverged genetically 1.5 million years ago. Additionally, a large proportion of cultural variants observed in chimpanzees occur only in the most genetically divergent of the four subspecies [40,73], the West African Pan troglodytes verus, which has been proposed as a different species [74]. These examples emphasize the difficulty in observational studies of completely removing the possibility of genetic influences on the occurrence of traits [40,75]. Nonetheless, our results are consistent with evidence of potential cultural traits in both species of gorillas.

Only one trait involved food processing (rubbing fruit on arm to clean it) and nine of the 23 (39%) potential cultural traits were environment related. This diverges from studies of both chimpanzees and orangutans in which the majority of traits involved object manipulation and/or food processing [9,11,73]. In contrast to other ape species, potential tool use by wild gorillas has been observed only very rarely [58,76,77]. The question of why tool use in wild gorillas is so rare remains intriguing, especially given its frequency in captive gorillas. Wild bonobos also rarely use tools, which may be due to having less intrinsic motivation to manipulate objects compared to chimpanzees, rather than resulting from ecological conditions [78].

However, food processing techniques for several plants species consumed by mountain gorillas and termites eaten by western gorillas are seemingly complex and can be achieved through different methods [79]. The coarse level of defining these behaviors (termite eating and thistle processing) in this study resulted in no variation among sites where these behaviors occurred. Detailed, quantitative field studies on the variation among individuals and ontogeny of these behaviors are rare, but these traits are likely candidates for social learning [79], but see [80]. Two methods of termite eating have been observed in western gorillas, but both techniques were observed at the three sites in this study that have termites so it remains unclear if such techniques were individually acquired, reinvented, or socially learned. Similarly, the two methods of extractive foraging used by banded mongoose have been shown to be socially learned, even though most individuals use both methods [24]; see also [81] for extractive foraging by capuchin monkeys), stressing the importance of conducting social learning studies because the method of exclusion tends to conservatively eliminate traits for which multiple variants are found in all populations. Furthermore, research is needed to exclude the possibility that variation in environment related traits (e.g. bridge making, bare earth nests) are not a result of variation in environmental conditions (e.g. depth of water, mean temperature) on a finer scale than what was considered in this study (see [8,82]).

The social interactions, the gestures, and the communication related trait that varied in usage among the gorilla populations (13 of 23 traits) are difficult to exclude as cultural traits because they do not rely on particular components of the environment. Nonetheless, ecological variation could also play a role in the occurrence and frequency of social interactions. Social conventions, or variation in the occurrence of social behaviors, may be the result of differences in socialization during maturation or in the context of the social environment [33,81]. Of particular interest, grooming among adult females in wild western gorillas was never observed and grooming among adult females and a silverback was observed at only one site; although mother-offspring grooming was observed regularly at all sites. Given the ubiquity of grooming among primates, including both related and unrelated dyads of mountain gorillas [83], and its function in maintaining social relationships [84], this is a unique omission to the behavioral repertoire of wild western gorillas [85], or at least in these groups. Grooming among adult western gorillas in captivity has only rarely been mentioned in the published literature [86]. Observations of additional wild western gorillas are necessary to determine if this is a species-wide phenomena or if grooming is a social behavior that has gone extinct in these locations (for more on extinction of social conventions see [13,87].

Several gestures and social traits were observed in one population of mountain gorillas but not the other (e.g. play chase around tree, arms on back of gorilla in front while travelling, pseudo-feeding as part of display) or were not observed in all three western gorilla populations (silverback-adult female grooming, splash displays, immatures play on or with the silverback), which perhaps offer some of the strongest support for behavioral variants being cultural since these traits are by nature social (less likely to be environmentally influenced) and some of these populations (Bwindi and the Virungas; 70) have been isolated from one another only relatively recently. Hand clapping, which was observed in western but not mountain gorillas, has also been recorded regularly in captive western gorillas [88,89]. Genty et al.[89] suggest that a large majority of gorilla gestures are part of a species typical repertoire, but that their use may be based on contextual learning because they are used in a highly flexible manner; this could include the lack of using some gestures in some locations. This interpretation of gestural communication does not preclude the possibility that their use can be socially learned and transmitted and therefore be considered cultural rather than ecologically or genetically driven.

As observed in the great apes, variation in the propensity to use cultural traits in different behavioral domains (e.g. foraging techniques, tool use, and social context) is also apparent among New World monkeys and most likely reflects a combination of morphological, ecological, and social adaptations. Foraging behavior has been one focus of traditions in white-faced capuchins [29], although they only rarely use tools [12,29]. In contrast, a wide diversity of tool use has been observed in brown capuchins [31,90]. Social conventions occur regularly in white-faced capuchins, but not brown capuchins [12]. Spider monkeys are morphologically limited in their ability to manipulate objects which may explain their lack of material culture, and most of the traditions occurred within a social context [14]. The relative use of social learning for ecological and social traits among the great apes may reflect adaptive strategies to cope with different ecological and social constraints, resulting in different evolutionary cognitive pathways and niche construction [91,92].

Following other studies [9,11], we have listed a handful of behaviors that were observed rarely, because they could be potential innovations [72,87,93]. For example, thistle rolling was observed repeatedly by only one subadult female gorilla at Bwindi [94], but unfortunately she dispersed into an unhabituated group a few months after she started performing this behavior so we were unable to observe if it was passed on to her offspring. The behavior ‘covering lap with vegetation during rest’ was observed only four times in one group of Karisoke mountain gorillas. This group shifted their range to a very high altitude (>3300 m) in recent years so the occurrence of the behavior may be an adaptation to ecological conditions and may spread to more group members.

In contrast to behaviors observed rarely in only one population, several behavioral traits were observed in all populations, but with differing degrees of occurrence. By definition, the method of exclusion disregards such universal behaviors (those that are present in all populations), but such behaviors may still be the result of innovation and social learning [73]. Several cases of group- or community-preferred behavioral variants have been documented spanning a variety of social and foraging behaviors [15,27,33,81]. Examining the occurrence of universal traits using systematic data collection methods that estimate frequencies, rates of behavior and statistical comparisons may broaden the repertoire of cultural traits in gorillas, if reinforced with evidence of social learning.

To better understand the potential cultural variants among gorillas, future research should focus on detailed systematic inter-individual comparisons of behavioral patterns within field sites or at ecologically similar sites [15, 72, 95] to reduce the possibility of ecological or genetic influences on traits, help to avoid the possibility of false absences, and to provide a more quantitative assessment of frequency and distribution of behaviors among group members. Focusing on possible modes of social transmission can help confirm the most likely method of trait acquisition (e.g. [81, 96]). Conducting studies on gorillas at ecologically similar sites can be challenging because of the large ecological variation within and among gorilla habitats and the small number of habituated groups. For example, there is large variation in plant species composition and density between and within the habitats of the only two populations of mountain gorillas [97, 98]. Western gorillas are found across a much larger range and ongoing habituation efforts should make more comparisons possible in the future, but ecological variation between sites may remain a limitation in some cases given the differences in habitat and diet (e.g.[99, 100]). This study serves as a starting point for adding gorillas to the discussion of how animals may exhibit behavioral variation acquired through social learning as an additional mode of adapting to changing social and ecological landscapes [101].

Acknowledgments

We thank the following organizations for permission to work at the various field sites: Uganda Wildlife Authority, Uganda National Council of Science and Technology, Rwanda Development Board, Gabon National Center of Scientific Research and Technology, Gabon Agence Nationale des Parcs Nationaux, the Ministries of Education and Water and Forests of CAR and Republic of Congo for permission to work in Dzanga-Ndoki National Park. We also thank the administration of Dzanga-Sangha Protected Areas in CAR for logistic support. Special thanks go to Terence Fuh Neba for contributing to observations of the gorillas at Bai Hokou, the local Ba'Aka trackers of the Primate Habituation Program at Bai Hokou camp, Dzanga-Ndoki NP, and all for their irreplaceable help, great humour and courage. We thank WWF (CAR) and WCS for support and logistical assistance, the numerous field and research assistants, and the skilled BaAka trackers, without whom the habituation of gorillas would not have been possible at Mondika. In Gabon, we are also greatly indebted to all field assistants of Moukalaba-Doudou National Park and the people in the villages of Doussala, Konzi, and Mboungou for their kind support and hospitality. We also thank all the researchers and data technicians at Karisoke who helped with data collection as well as the field assistants of the Institute of Tropical Forest Conservation in Bwindi. Thanks to Jessica Junker and Nicole Seiler for help creating Fig 1. We appreciate useful comments from Claudio Tennie and two anonymous reviewers on a previous version of this manuscript. We thank Diane Doran-Sheehy, Kevin Langergraber, and Christophe Boesch for helpful discussions during the course of this project.

Author Contributions

  1. Conceived and designed the experiments: MMR.
  2. Performed the experiments: MMR.
  3. Analyzed the data: MMR.
  4. Contributed reagents/materials/analysis tools: MMR CA KF CCG DH YI JL SM RS TSS AT VV JY.
  5. Wrote the paper: MMR.

References

  1. 1. Laland KN, Hoppitt W. Do animals have culture? Evol Anthropol. 2003;12: 150–9.
  2. 2. Laland KN, Janik VM. The animal cultures debate. Trends Ecol Evol. 2006;21: 542–7. pmid:16806574
  3. 3. Boesch C. Is culture a golden barrier between human and chimpanzee? Evol Anthropol. 2003;12: 82–91.
  4. 4. Dean LG, Vale GL, Laland KN, Flynn E, Kendal RL. Human cumulative culture: a comparative perspective. Biol Rev. 2014;89: 284–301. pmid:24033987
  5. 5. Heyes CM. Social learning in animals: categories and mechanisms. Biol Rev. 1994;69: 207–31. pmid:8054445
  6. 6. Kendal RL, Galef BG, Van Schaik CP. Social learning research outside the laboratory: How and why? Learn Behav. 2010;38: 187–94. pmid:20628158
  7. 7. Luncz LV, Mundry R, Boesch C. Evidence for cultural differences between neighboring chimpanzee communities. Curr Biol. 2012;22: 922–6. pmid:22578420
  8. 8. Moebius Y, Boesch C, Koops K, Matsuzawa T, Humle T. Cultural differences in army ant predation by West African chimpanzees? A comparative study of microecological variables. Anim Behav. 2008;76: 37–45.
  9. 9. Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, et al. Cultures in chimpanzees. Nature. 1999;399: 682–5. pmid:10385119
  10. 10. Hohmann G, Fruth B. Culture in bonobos? Between-species and within-species variation in behavior. Curr Anthropol. 2003;44: 563–71.
  11. 11. van Schaik CP. Orangutan cultures and the evolution of material culture. Science. 2003;299: 102–5. pmid:12511649
  12. 12. Perry S. Social traditions and social learning in capuchin monkeys (Cebus). Philos Trans R Soc B Biol Sci. 2011;366: 988–96.
  13. 13. Perry S, Baker M, Fedigan L, Gros‐Louis J, Jack K, MacKinnon KC, et al. Social conventions in wild white‐faced capuchin monkeys: evidence for traditions in a neotropical primate. Curr Anthropol. 2003;44: 241–68.
  14. 14. Santorelli CJ, Schaffner CM, Campbell CJ, Notman H, Pavelka MS, Weghorst JA, et al. Traditions in spider monkeys are biased towards the social domain. PLoS ONE. 2011;6: e16863. pmid:21373196
  15. 15. Santorelli CJ, Schaffner CM, Aureli F. Universal behaviors as candidate traditions in wild spider monkeys. PloS One. 2011;6: e24400. pmid:21949715
  16. 16. Thornton A, Clutton-Brock T. Social learning and the development of individual and group behaviour in mammal societies. Philos Trans R Soc B Biol Sci. 2011;366: 978–87.
  17. 17. Thornton A, Samson J, Clutton-Brock T. Multi-generational persistence of traditions in neighbouring meerkat groups. Proc R Soc B Biol Sci. 2010;277: 3623–9.
  18. 18. Krützen M, Mann J, Heithaus MR, Connor RC, Bejder L, Sherwin WB. Cultural transmission of tool use in bottlenose dolphins. Proc Natl Acad Sci U S A. 2005;102:8939–43. pmid:15947077
  19. 19. Kopps AM, Sherwin WB. Modelling the emergence and stability of a vertically transmitted cultural trait in bottlenose dolphins. Anim Behav. 2012;84: 1347–62.
  20. 20. Allen J, Weinrich M, Hoppitt W, Rendell L. Network-based diffusion analysis reveals cultural transmission of lobtail feeding in humpback whales. Science. 2013;340: 485–8. pmid:23620054
  21. 21. Laland KN, Atton N, Webster MM. From fish to fashion: experimental and theoretical insights into the evolution of culture. Philos Trans R Soc B-Biol Sci. 2011;366: 958–68.
  22. 22. Dindo M, Thierry B, Whiten A. Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella). Proc R Soc B-Biol Sci. 2008;275: 187–93.
  23. 23. Whiten A, Spiteri A, Horner V, Bonnie KE, Lambeth SP, Schapiro SJ, et al. Transmission of multiple traditions within and between chimpanzee groups. Curr Biol. 2007;17: 1038–43. pmid:17555968
  24. 24. Müller CA, Cant MA. Imitation and traditions in wild banded mongooses. Curr Biol. 2010;20: 1171–5. pmid:20605459
  25. 25. Thornton A, Malapert A. Experimental evidence for social transmission of food acquisition techniques in wild meerkats. Anim Behav. 2009;78: 255–64.
  26. 26. Bastian ML, Zweifel N, Vogel ER, Wich SA, van Schaik CP. Diet traditions in wild orangutans. Am J Phys Anthropol. 2010;143: 175–87. pmid:20853473
  27. 27. Jaeggi AV, Dunkel LP, Van Noordwijk MA, Wich SA, Sura AAL, Van Schaik CP. Social learning of diet and foraging skills by wild immature Bornean orangutans: implications for culture. Am J Primatol. 2010;72: 62–71. pmid:19790189
  28. 28. Hirata S, Watanabe S, Kawai M. “Sweet potato washing” revisited. In: Matsuzawa T, editor. Primate origins of human behavior and cognition. Tokyo: Springer; 2001. p. 487–508.
  29. 29. Panger MA, Perry S, Rose L, Gros-Louis J, Vogel E, Mackinnon KC, et al. Cross-site differences in foraging behavior of white-faced capuchins (Cebus capucinus). Am J Phys Anthropol. 2002;119: 52–66. pmid:12209573
  30. 30. McGrew WC. Chimpanzee material culture: implications for human evolution. Cambridge: Cambridge University Press; 1992.
  31. 31. Ottoni EB, Izar P. Capuchin monkey tool use: Overview and implications. Evol Anthropol Issues News Rev. 2008;17: 171–8.
  32. 32. McGrew WC, Marchant LF, Scott SE, Tutin CEG. Intergroup differences in a social customof wild chimpanzees: the grooming hand-clasp of the Mahale Mountains. Curr Anthropol. 2001;42: 148–53.
  33. 33. Sapolsky RM, Share LJ. A Pacific Culture among Wild Baboons: Its Emergence and Transmission. PLoS Biol. 2004;2: e106. pmid:15094808
  34. 34. Leca JB, Gunst N, Huffman M. A. Indirect social influence in the maintenance of the stone-handling tradition in Japanese macaques, Macaca fuscata. Anim Behav. 2010: 117–26.
  35. 35. Nakamura M, McGrew WC, Marchant LF, Nishida T. Social scratch: another custom in wild chimpanzees? Primates. 2000;41: 237–48.
  36. 36. Whiten A, van Schaik CP. The evolution of animal “cultures” and social intelligence. Philos Trans R Soc B-Biol Sci. 2007;362: 603–20.
  37. 37. Tennie C, Call J, Tomasello M. Ratcheting up the ratchet: on the evolution of cumulative culture. Philos Trans R Soc B Biol Sci. 2009;364: 2405–15.
  38. 38. Koops K, McGrew WC, Matsuzawa T. Ecology of culture: do environmental factors influence foraging tool use in wild chimpanzees, Pan troglodytes verus? Anim Behav. 2013;85: 175–85.
  39. 39. Koops K, Schöning C, Isaji M, Hashimoto C. Cultural differences in ant-dipping tool length between neighbouring chimpanzee communities at Kalinzu, Uganda. Sci Rep. 2015;5: 12456. pmid:26198006
  40. 40. Langergraber KE, Boesch C, Inoue E, Inoue-Murayama M, Mitani JC, Nishida T, et al. Genetic and “cultural” similarity in wild chimpanzees. Proc R Soc B Biol Sci. 2011;278: 408–16.
  41. 41. van Schaik CP. The costs and benefits of flexibility as an expression of behavioural plasticity: a primate perspective. Philos Trans R Soc B Biol Sci. 2013;368: 20120339–20120339.
  42. 42. Byrne RW. Culture in great apes: using intricate complexity in feeding skills to trace the evolutionary origin of human technical prowess. Philos Trans R Soc B Biol Sci. 2007;362: 577–85.
  43. 43. Whiten A. The scope of culture in chimpanzees, humans and ancestral apes. R Soc Philos Trans Biol Sci. 2011;366: 997–1007.
  44. 44. van Schaik CP, Deaner RO, Merrill MY. The conditions for tool use in primates: implications for the evolution of material culture. J Hum Evol. 1999;36: 719–41. pmid:10330335
  45. 45. Doran DM, McNeilage A. Gorilla ecology and behavior. Evol Anthropol. 1998;6: 120–31.
  46. 46. Harcourt AH, Stewart KJ. Gorilla society: conflict, compromise, and cooperation between the sexes. Chicago: University of Chicago Press; 2007.
  47. 47. Robbins MM. Gorillas: Diversity in ecology and behavior. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder S, Stumpf RM, editors. Primates in Perspective. 2nd ed. Oxford: Oxford University Press; 2011. p. 326–39.
  48. 48. Taylor AB, Goldsmith ML. Gorilla Biology: A Multidisciplinary Perspective. Cambridge: Cambridge University Press; 2003.
  49. 49. Yamagiwa J, Basabose AK. Socioecological flexibility of gorillas and chimpanzees. In: Primates and Cetaceans: Field Reserach and Conesrvation of Complex Mammalian Societies. Tokyo: Springer; 2014.
  50. 50. Groves C. A history of gorilla taxonomy. In: Taylor AB, Goldsmith ML, editors. Gorilla Biology: A Multidisciplinary Approach. Cambridge: Cambridge University Press; 2003.
  51. 51. Thalmann O, Fischer A, Lankester F, Paabo S, Vigilant L. The Complex Evolutionary History of Gorillas: Insights from Genomic Data. Mol Biol Evol. 2006;24: 146–58. pmid:17065595
  52. 52. Langergraber KE, Pruefer K, Rowney C, Boesch C, Crockford C, Fawcett K, et al. Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc Natl Acad Sci USA. 2012;109: 15716–21. pmid:22891323
  53. 53. Xue Y, Prado-Martinez J, Sudmant PH, Narasimhan V, Ayub Q, Szpak M, et al. Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding. Science. 2015;348: 242–5. pmid:25859046
  54. 54. Yamagiwa J, Kahekwa J, Basabose AK. Intra-specific variation in social organization of gorillas: implications for their social evolution. Primates. 2003;44: 359–69. pmid:12942370
  55. 55. Ramsey G, Bastian ML, van Schaik CP. Animal innovation defined and operationalized. Behav Brain Sci. 2007;30: 1–45.
  56. 56. Doran-Sheeny DM, Fernandez D, Borries C. The Strategic Use of Sex in Wild Female Western Gorillas. Am J Primatol. 2009;71: 1011–20. pmid:19722225
  57. 57. Grueter CC, Ndamiyabo F, Plumptre AJ, Abavandimwe D, Mundry R, Fawcett KA, et al. Long-Term Temporal and Spatial Dynamics of Food Availability for Endangered Mountain Gorillas in Volcanoes National Park, Rwanda. Am J Primatol. 2013;75: 267–80. pmid:23208819
  58. 58. Grueter CC, Robbins MM, Ndagijimana F, Stoinski TS. Possible tool use in a mountain gorilla. Behav Processes. 2013;100: 160–2. pmid:24096185
  59. 59. Grueter CC, Deschner T, Behringer V, Fawcett K, Robbins MM. Socioecological correlates of energy balance using urinary C-peptide measurements in wild female mountain gorillas. Physiol Behav. 2014;127: 13–9. pmid:24472322
  60. 60. Hedwig D, Hammerschmidt K, Mundry R, Robbins MM, Boesch C. Acoustic structure and variation in mountain and western gorilla close calls: a syntactic approach. Behaviour. 2014;151: 1091–120.
  61. 61. Hedwig D, Mundry R, Robbins MM, Boesch C. Contextual correlates of syntactic variation in mountain and western gorilla close-distance vocalizations: Indications for lexical or phonological syntax? Anim Cogn. 2015;18: 423–35. pmid:25311802
  62. 62. Lodwick J. Links between foraging strategies, feeding competition, and female agonisticrelationships in wild western gorillas (Gorilla gorilla). [Stony Brook, NY]: Stony Brook University; 2014.
  63. 63. Robbins MM. Feeding competition and agonistic relationships among Bwindi Gorilla beringei. Int J Primatol. 2008;29: 999–1018.
  64. 64. Salmi R, Doran-Sheehy DM. The Function of Loud Calls (Hoot Series) in Wild Western Gorillas (Gorilla gorilla). Am J Phys Anthropol. 2014;155: 379–91. pmid:25059429
  65. 65. Salmi R, Hammerschmidt K, Doran-Sheehy DM. Western Gorilla Vocal Repertoire and Contextual Use of Vocalizations. Ethology. 2013;119: 831–47.
  66. 66. Masi S, Mundry R, Ortmann S, Cipolletta C, Boitani L, Robbins MM. The influence of seasonal frugivory on nutrient and energy intake in wild western gorillas. Plos One. 2015;10.
  67. 67. Doran-Sheehy D, Mongo P, Lodwick J, Conklin-Brittain NL. Male and Female Western Gorilla Diet: Preferred Foods, Use of Fallback Resources, and Implications for Ape versus Old World Monkey Foraging Strategies. Am J Phys Anthropol. 2009;140: 727–38. pmid:19890869
  68. 68. Cipolletta C. Effects of group dynamics and diet on the ranging patterns of a western gorilla group (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic. Am J Primatol. 2004;64: 193–205. pmid:15470747
  69. 69. Iwata Y, Ando C. Bed and bed-site reuse by western lowland gorillas (Gorilla g. gorilla) in Moukalaba-Doudou National Park, Gabon. Primates. 2006;48: 77–80. pmid:17106788
  70. 70. Roy J, Arandjelovic M, Bradley BJ, Guschanski K, Stephens CR, Bucknell D, et al. Recent divergences and size decreases of eastern gorilla populations. Biol Lett. 20141; 10.
  71. 71. Whiten A. Social learning, tradition, and culture. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB, editors. The Evolution of Primate Societies. Chicago: University of Chicago Press; 2012. p. 681–99.
  72. 72. Bastian ML, van Noordwijk MA, van Schalk CP. Innovative behaviors in wild Bornean orangutans revealed by targeted population comparison. Behaviour. 2012;149: 275–97.
  73. 73. Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, et al. Charting cultural variation in chimpanzees. Behaviour. 2001;138: 1481–516.
  74. 74. Gagneux P, Wills C, Gerloff U, Tautz D, Morin PA, Boesch C, et al. Mitochondrial sequences show diverse evolutionary histories of African hominoids. Proc Natl Acad Sci USA. 1999;96: 5077–82. pmid:10220421
  75. 75. Krützen M, Willems EP, van Schaik CP. Culture and geographic variation in orangutan behavior. Curr Biol. 2011;21: 1808–12. pmid:22018539
  76. 76. Breuer T, Ndoundou-Hockemba M, Fishlock V. First observation of tool use in wild gorillas. Plos Biol. 2005;3: 2041–3.
  77. 77. Kinani J-F, Zimmerman D. Tool use for food acquisition in a wild mountain gorilla (Gorilla beringei beringei): Tool use in a mountain gorilla. Am J Primatol. 2015;77: 353–7. pmid:25452208
  78. 78. Koops K, Furuichi T, Hashimoto C. Chimpanzees and bonobos differ in intrinsic motivation for tool use. Sci Rep. 2015;5: 11356. pmid:26079292
  79. 79. Byrne RW, Hobaiter C, Klailova M. Local traditions in gorilla manual skill: evidence for observational learning of behavioral organization. Anim Cogn. 2011;14: 683–93.
  80. 80. Tennie C, Hedwig D, Call J, Tomasello M. An experimental study of nettle feeding in captive gorillas. Am J Primatol. 2008;70: 584–93. pmid:18330896
  81. 81. Perry S. Conformism in the food processing techniques of white-faced capuchin monkeys (Cebus capucinus). Anim Cogn. 2009;12: 705–16. pmid:19455357
  82. 82. Schoening C, Humle T, Moebius Y, McGrew WC. The nature of culture: technological variation in chimpanzee predation on army ants revisited. J Hum Evol. 2008;55: 48–59. pmid:18275983
  83. 83. Watts DP. Social relationships of female mountain gorillas. In: Mountain gorillas: three decades of research at Karisoke. Cambridge: Cambridge University Press; 2001.
  84. 84. Silk JB. The adaptive value of sociality. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB, editors. The Evolution of Primate Societies. Chicago: University of Chicago Press; 2012. p. 552–64.
  85. 85. Masi S, Cipolletta C, Robbins MM. Western lowland gorillas (Gorilla gorilla gorilla) change their activity patterns in response to frugivory. Am J Primatol. 2009;71: 91–100. pmid:19021124
  86. 86. Scott J, Lockard JS. Competition coalitions and conflict interventions among captive female gorillas. Int J Primatol. 2007;28: 761–81.
  87. 87. Nishida T, Matsusaka T, McGrew WC. Emergence, propagation or disappearance of novel behavioral patterns in the habituated chimpanzees of Mahale: a review. Primates. 2009;50: 23–36. pmid:19137390
  88. 88. Pika S, Liebal K, Tomasello M. Gestural communication in young gorillas (Gorilla gorilla): Gestural repertoire, learning, and use. Am J Primatol. 2003;60: 95–111. pmid:12874841
  89. 89. Genty E, Breuer T, Hobaiter C, Byrne RW. Gestural communication of the gorilla (Gorilla gorilla): repertoire, intentionality and possible origins. Anim Cogn. 2009;12:527–46. pmid:19184669
  90. 90. Boinski S, Quatrone RP, Swartz H. Substrate and tool use by brown capuchins in Suriname: Ecological contexts and cognitive bases. Am Anthropol. 2000;102: 741–61.
  91. 91. Yamakoshi G. Dietary responses to fruit scarcity of wild chimpanzees at Bossou, Guinea: possible implications for ecological importance of tool use. Am J Phys Anthropol. 1998;106: 283–95. pmid:9696145
  92. 92. Laland KN, Brown GR. Niche construction, human behavior, and the adaptive-lag hypothesis. Evol Anthropol. 2006;15: 95–104.
  93. 93. van Schaik CP, van Noordwijk MA, Wich SA. Innovation in wild Bornean orangutans (Pongo pygmaeus wurmbii). Behaviour. 2006;143: 839–76.
  94. 94. Sawyer SC, Robbins MM. A Novel Food Processing Technique by a Wild Mountain Gorilla (Gorilla beringei beringei). Folia Primatol. 2009;80: 83–8. pmid:19420959
  95. 95. Byrne RW. Culture in great apes: using intricate complexity in feeding skills to trace the evolutionary origin of human technical prowess. Philos Trans R Soc B-Biol Sci. 2007;362: 577–85.
  96. 96. Lonsdorf EV, Eberly LE, Pusey AE. Sex differences in learning in chimpanzees. Nature. 2004;428: 715–6. pmid:15085121
  97. 97. Ganas J, Robbins MM, Nkurunungi JB, Kaplin BA, McNeilage A. Dietary variability of mountain gorillas in Bwindi Impenetrable National Park, Uganda. Int J Primatol. 2004:1043–72.
  98. 98. Wright E, Grueter CC, Seiler N, Abavandimwe D, Stoinski TS, Ortmann S, et al. Energetic responses to variation in food availability in the two mountain gorilla populations (Gorilla beringei beringei). Am J Phys Anthropol. 2015;158: 487–500. pmid:26174738
  99. 99. Head JS, Boesch C, Makaga L, Robbins MM. Sympatric Chimpanzees (Pan troglodytes troglodytes) and Gorillas (Gorilla gorilla gorilla) in Loango National Park, Gabon: dietary composition, seasonality, and intersite comparisons. Int J Primatol. 2011;32: 755–75.
  100. 100. Rogers ME, Abernethy K, Bermejo M, Cipolletta C, Doran D, McFarland K, et al. Western gorilla diet: A synthesis from six sites. Am J Primatol. 2004;64: 173–92. pmid:15470742
  101. 101. van Schaik CP, Burkart JM. Social learning and evolution: the cultural intelligence hypothesis. Philos Trans R Soc B Biol Sci. 2011;366: 1008–16.