The type and variety of learning strategies used by individuals to acquire behaviours in the wild are poorly understood, despite the presence of behavioural traditions in diverse taxa. Social learning strategies such as conformity can be broadly adaptive, but may also retard the spread of adaptive innovations. Strategies like pay-off-biased learning, by contrast, are effective at diffusing new behaviour but may perform poorly when adaptive behaviour is common. We present a field experiment in a wild primate, Cebus capucinus, that introduced a novel food item and documented the innovation and diffusion of successful extraction techniques. We develop a multilevel, Bayesian statistical analysis that allows us to quantify individual-level evidence for different social and individual learning strategies. We find that pay-off-biased and age-biased social learning are primarily responsible for the diffusion of new techniques. We find no evidence of conformity; instead rare techniques receive slightly increased attention. We also find substantial and important variation in individual learning strategies that is patterned by age, with younger individuals being more influenced by both social information and their own individual experience. The aggregate cultural dynamics in turn depend upon the variation in learning strategies and the age structure of the wild population.

Habitual reliance on tool use is a marked behavioural difference between wild robust (genus Sapajus) and gracile (genus Cebus) capuchin monkeys. Despite being well studied and having a rich repertoire of social and extractive foraging traditions, Cebus sp. rarely use tools and have never been observed using stone tools. By contrast, habitual tool use by Sapajus is widespread. We review theory and discuss factors which might explain these differences in patterns of tool use between Cebus and Sapajus. We then report the first case of habitual stone tool use in a gracile capuchin: a population of white-faced capuchins (Cebus capucinus imitator) in Coiba National Park, Panama who habitually rely on hammerstone and anvil tool use to access structurally protected food items in coastal areas including Terminalia catappa seeds, hermit crabs, marine snails, terrestrial crabs and other items. This behaviour has persisted on one island in Coiba National Park since at least 2004. From 1 year of camera trapping, we found that stone tool use is strongly male-biased. Of the 205 camera trap days where tool use was recorded, adult females were never observed to use stone tools, although they were frequently recorded at the sites and engaged in scrounging behaviour. Stone tool use occurs year-round in this population; over half of all identifiable individuals were observed participating. At the most active tool use site, 83.2% of days where capuchins were sighted corresponded with tool use. Capuchins inhabiting the Coiba archipelago are highly terrestrial, under decreased predation pressure and potentially experience resource limitation compared to mainland populations—three conditions considered important for the evolution of stone tool use. White-faced capuchin tool use in Coiba National Park thus offers unique opportunities to explore the ecological drivers and evolutionary underpinnings of stone tool use in a comparative within- and between-species context.

An important extension to our understanding of evolutionary processes has been the discovery of the roles that individual and social learning play in creating recurring phenotypes on which selection can act. Cultural change occurs chiefly through invention of new behavioral variants combined with social transmission of the novel behaviors to new practitioners. Therefore, understanding what makes some individuals more likely to innovate and/or transmit new behaviors is critical for creating realistic models of culture change. The difficulty in identifying what behaviors qualify as new in wild animal populations has inhibited researchers from understanding the characteristics of behavioral innovations and innovators. Here, we present the findings of a long-term, systematic study of innovation (10 y, 10 groups, and 234 individuals) in wild capuchin monkeys (Cebus capucinus) in Lomas Barbudal, Costa Rica. Our methodology explicitly seeks novel behaviors, requiring their absence during the first 5 y of the study to qualify as novel in the second 5 y of the study. Only about 20% of 187 innovations identified were retained in innovators' individual behavioral repertoires, and 22% were subsequently seen in other group members. Older, more social monkeys were more likely to invent new forms of social interaction, whereas younger monkeys were more likely to innovate in other behavioral domains (foraging, investigative, and self-directed behaviors). Sex and rank had little effect on innovative tendencies. Relative to apes, capuchins devote more of their innovations repertoire to investigative behaviors and social bonding behaviors and less to foraging and comfort behaviors.innovation | Cebus capucinus | cultural evolution | phenotypic plasticity | learning B ehavioral innovation has long been a topic of interest for researchers dedicated to studying the evolution of culture, because it is a driver of cultural change (1, 2). The types of behavioral traditions that are of greatest interest to evolutionary modelers are those starting with an innovation that then spreads via social learning. Understanding the characteristics of (i) behavioral innovations (which are roughly analogous to genetic mutations) and (ii) the individuals who invent these behaviors is critical to understanding cultural evolution and its relationship to genetic evolution. Innovation is also of interest to evolutionary biologists who study the role that learning plays in macroevolution, because it is a type of phenotypic plasticity that can affect the direction of natural selection (3). Ability to innovate can enhance reproductive success (for example, by enabling individuals to exploit new resources) (4-6). Innovation can generate the Baldwin effect, in which learned traits create recurring phenotypes that select for morphological adaptations, eventually leading to speciation (3, 7). Innovation is also of interest as a correlate of intelligence more generally, and the ability to solve novel cognitive problems presented by experimenters can be positively ...

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Many animals respond well behaviorally to stimuli associated with human-induced rapid environmental change (HIREC), such as novel predators or food sources. Yet others make errors and succumb to evolutionary traps: approaching or even preferring low quality, dangerous or toxic options, avoiding beneficial stimuli, or wasting resources responding to stimuli with neutral payoffs. A common expectation is that learning should help animals adjust to HIREC; however, learning is not always expected or even favored in many scenarios that expose animals to ecological and evolutionary traps. We propose a conceptual framework that aims to explain variation in when learning can help animals avoid and escape traps caused by HIREC. We first clarify why learning to correct two main types of errors (avoiding beneficial options and approaching detrimental options) might be difficult (limited by constraints). We then identify and discuss several key behavioral mechanisms (adaptive sampling, generalization, habituation, reversal learning) that can be targeted to help animals learn to avoid traps. Finally, we discuss how individual differences in neophobia/neophilia and personality relate to learning in the context of HIREC traps, and offer some general guidance for disarming traps. Given how devastating traps can be for animal populations, any breakthrough in mitigating trap outcomes via learning could make the difference in developing effective solutions.

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Habitual reliance on tool use is a marked behavioral difference between wild robust (genus Sapajus) and gracile (genus Cebus) capuchin monkeys. Despite being well studied and having a rich repertoire of social and extractive foraging traditions, Cebus sp have rarely been observed engaging in tool use and have never been reported to use stone tools. In contrast, habitual tool use and stone-tool use by Sapajus is widespread. We discuss factors which might explain these differences in patterns of tool use between Cebus and Sapajus. We then report the first case of habitual stone-tool use in a gracile capuchin: a population of white-faced capuchins (Cebus capucinus imitator ) in Coiba National Park, Panama who habitually rely on hammerstone and anvil tool use to access structurally protected food items in coastal areas including Terminalia catappa seeds, hermit crabs, marine snails, terrestrial crabs, and other items. This behavior has persisted on one island in Coiba National Park since at least 2004. From one year of camera trapping, we found that stone tool use is strongly male-biased. Of the 205 unique camera-trap-days where tool use was recorded, adult females were never observed to use stone-tools, although they were frequently recorded at the sites and engaged in scrounging behavior. Stone-tool use occurs year-round in this population, and over half of all identifiable individuals were observed participating. At the most active tool use site, 83.2% of days where capuchins were sighted corresponded with tool use. Capuchins inhabiting the Coiba archipelago are highly terrestrial, under decreased predation pressure and potentially experience resource limitation compared to mainland populations-three conditions considered important for the evolution of stone tool use. White-faced capuchin tool use in Coiba National Park thus offers unique opportunities to explore the ecological drivers and evolutionary underpinnings of stone tool use in a comparative within-and between-species context.