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

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Network-based diffusion analysis demonstrates that a novel tool-use behavior, “moss-sponging”, spread via social learning in a wild East-African chimpanzee community.

          Abstract

          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.

          Author Summary

          Chimpanzees are widely considered as the most “cultural” of all animals, despite the lack of direct evidence for the spread of novel behaviors through social learning in the wild. Here, we present a novel, dynamic network-based diffusion analysis to describe the acquisition patterns of novel tool-use behavior in the Sonso chimpanzee community of Budongo Forest, Uganda. We find strong evidence for social transmission of “moss-sponging” (the production of a sponge consisting of moss) along the innovators' social network, demonstrating that wild chimpanzees learn novel tool-use behaviors from each other and supporting the more general claim that some of the observed behavioral diversity in wild chimpanzees should be interpreted as “cultural.” Our model also estimated that, for each new observation, naïve individuals enhanced their chances of developing moss-sponging by a factor of 15. We conclude that group-specific behavioral variants can be socially learned in wild chimpanzees, addressing an important critique of the claim of culture in our closest relatives.

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          Orangutan cultures and the evolution of material culture.

          Geographic variation in some aspects of chimpanzee behavior has been interpreted as evidence for culture. Here we document similar geographic variation in orangutan behaviors. Moreover, as expected under a cultural interpretation, we find a correlation between geographic distance and cultural difference, a correlation between the abundance of opportunities for social learning and the size of the local cultural repertoire, and no effect of habitat on the content of culture. Hence, great-ape cultures exist, and may have done so for at least 14 million years.
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            Social network analysis of animal behaviour: a promising tool for the study of sociality

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              Culture in whales and dolphins.

              Studies of animal culture have not normally included a consideration of cetaceans. However, with several long-term field studies now maturing, this situation should change. Animal culture is generally studied by either investigating transmission mechanisms experimentally, or observing patterns of behavioural variation in wild populations that cannot be explained by either genetic or environmental factors. Taking this second, ethnographic, approach, there is good evidence for cultural transmission in several cetacean species. However, only the bottlenose dolphin (Tursiops) has been shown experimentally to possess sophisticated social learning abilities, including vocal and motor imitation; other species have not been studied. There is observational evidence for imitation and teaching in killer whales. For cetaceans and other large, wide-ranging animals, excessive reliance on experimental data for evidence of culture is not productive; we favour the ethnographic approach. The complex and stable vocal and behavioural cultures of sympatric groups of killer whales (Orcinus orca) appear to have no parallel outside humans, and represent an independent evolution of cultural faculties. The wide movements of cetaceans, the greater variability of the marine environment over large temporal scales relative to that on land, and the stable matrilineal social groups of some species are potentially important factors in the evolution of cetacean culture. There have been suggestions of gene-culture coevolution in cetaceans, and culture may be implicated in some unusual behavioural and life-history traits of whales and dolphins. We hope to stimulate discussion and research on culture in these animals.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                September 2014
                30 September 2014
                : 12
                : 9
                : e1001960
                Affiliations
                [1 ]School of Psychology and Neuroscience, University of St. Andrews, Fife, United Kingdom
                [2 ]Budongo Conservation Field Station, Masindi, Uganda
                [3 ]Département de Biologie, Chimie et Géographie, Université du Québec à Rimouski, Rimouski, Québec, Canada
                [4 ]Québec Centre for Biodiversity Sciences, Montréal, Québec, Canada
                [5 ]Department of Comparative Cognition, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland
                [6 ]Animal and Environment Research Group, Anglia Ruskin University, Cambridge, United Kingdom
                Emory University, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: CH. Performed the experiments: CH. Analyzed the data: CH TG WH TP. Contributed reagents/materials/analysis tools: TP WH. Wrote the paper: TG CH KZ WH TP.

                Article
                PBIOLOGY-D-14-00902
                10.1371/journal.pbio.1001960
                4181963
                25268798
                c2a1edab-2532-4580-b2bc-8d525c381ab3
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 11 March 2014
                : 21 August 2014
                Page count
                Pages: 12
                Funding
                We are grateful to the Royal Zoological Society of Scotland for providing core funding for the Budongo Conservation Field Station. The fieldwork of CH was funded by the Leverhulme Trust, the Lucie Burgers Stichting, and the British Academy. TP was funded by the Canadian Research Chair in Continental Ecosystem Ecology, and received computational support from the Theoretical Ecosystem Ecology group at UQAR. The research leading to these results has received funding from the People Programme (Marie Curie Actions) and from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007–2013) REA grant agreement n°329197 awarded to TG, ERC grant agreement n° 283871 awarded to KZ. WH was funded by a BBSRC grant (BB/I007997/1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Neuroscience
                Cognitive Science
                Cognition
                Animal Cognition
                Zoology
                Mammalogy
                Primatology
                Animal Behavior
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction at Dryad Digital Repository. Openly available via http://dx.doi.org/10.5061/dryad.m6s21.

                Life sciences
                Life sciences

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