Biology subjects

Barrett, B. J.

Publications and source records attributed to Barrett, B. J..

13 recordsLinked to original sources

bioRxiv2026

Genetic and behavioural repertoires support olfactory communication in wild capuchin monkeys

Olfaction is a key sense for many mammals, but its role in the social lives of anthropoid primates (monkeys, apes, humans) is poorly understood. Studies of chemosensory receptor genes and olfactory behaviours can provide insight into the evolution and function of olfaction across social contexts. Vomeronasal receptor (VR) genes are especially relevant to social behaviour as they are specialized for the detection of pheromones and other cues involved in social signaling, reproductive behaviour, and individual recognition in mammals. Here, we examined the population genetics and gene repertoires of VR genes in wild white-faced capuchin monkeys (Cebus imitator) from Costa Rica and Panama using DNA sourced through both host tissues and through noninvasive fluorescence-activated cell sorting of fecal samples (fecalFACS). We compared VR diversity relative to putatively neutral reference loci (NRs) to investigate evidence of selection and potential effects of demography. To complement the genetic analysis, we also conducted a detailed observational study of capuchin olfactory behaviours. Combined, we find evidence of intact VRs subject to evolutionary constraint in capuchins, providing novel evidence that members of this gene family are maintained by evolutionary constraint in wild monkeys. We further document a rich and varied ethogram of olfactory behaviours that have clear potential for communication. Overall, our study provides compelling evidence for a role of olfaction in the complex social lives of capuchin monkeys, motivating future research on the contributions of olfaction to social communication and evolution in primates and other mammals.

animal behavior and cognition↗

bioRxiv2026

Maternal ranging strategies facilitate offspring social play at energetic cost in the most solitary ape

In most vertebrates, social play among peers is considered essential for behavioral development. Yet in solitary species bearing single offspring, opportunities for social play are inherently scarce. Whether mothers of such species actively facilitate play opportunities for their offspring, and at what cost, remains unknown. We used 15 years of behavioral and movement data ([~]30,000 observation hours) from 31 wild Bornean orangutan (Pongo pygmaeus wurmbii) mother-offspring pairs to test whether mothers adjust ranging behavior to increase their offsprings access to play with neighboring peers. Neighboring mothers with similarly aged offspring showed disproportionately high annual overlap in space use, independent of their relatedness or fruit availability. They intensified use of shared areas within existing range boundaries rather than shifting or expanding their ranges, indicating a fine-scaled ranging strategy. Mothers also incurred energetic costs; on days their offspring played with peers, mothers traveled farther and spent less time feeding. Travel distances were also elevated on the days before and after play, with mothers orienting movement toward play partners core areas before play and back toward their own core areas after play. This suggests these encounters are planned and actively pursued over multiple days rather than arising by chance. These findings reveal that orangutan mothers incorporate their infants social needs into daily ranging decisions, at a cost to their own energy budgets. This points toward an underappreciated form of maternal investment and illustrates how the social requirements of development can be met even near the solitary extreme of animal social organization.

ecology↗

bioRxiv2025

White-faced capuchins (Cebus capucinus imitator) exhibit selectivity for stone tools

Over the last few decades, the developing field of primate archaeology has used archaeological methods to reconstruct primate behaviors, especially tool use. We expand the possibilities of primate archaeology with an inverse approach: using living primates to address archaeological questions. In particular, we investigate tool selectivity, a phenomenon that not only represents a significant milestone for tool users, also for the emergence of stone tool technology in human evolution. Observing extant primate tool use can establish clear expectations for a percussion-based archaeological record across taxa. Here, we describe stone tools assemblages produced by two independent populations of white-faced capuchin monkeys (Cebus capucinus imitator) in Coiba National Park, Panama, and provide evidence of stone tool selectivity in both populations. We demonstrate that capuchins select for tool dimensions, and select different sizes for different tool functions. This selectivity analysis reveals that primate stone tool use results in assemblages of artifacts that are distinct from natural accumulations of unused material in the surrounding landscapes. These variations further suggest that stone tool use has a recognizable signature at the assemblage level, even where no lithic flaking occurs. The existence of such assemblage-level signatures offer new avenues for the archaeological identification of tool use both in unhabituated living primates and extinct taxa. The presence of selectivity in multiple capuchin populations suggests that, along with percussion, tool selectivity is ancestral to stone tool flaking, and is shared by phylogenetically distant branches of the primate tree.

animal behavior and cognition↗

bioRxiv2025

Between-group competitive advantage offsets foraging costs for bigger groups in harsher seasons

Larger animal groups are widely understood to require more space and expend more energy to mitigate the foraging costs of within-group competition. Yet between-group interactions and shifting resource distributions can obscure links between group size and behavior, making responses to demographic change difficult to predict. Using 33 years of observational data from 12 neighboring white-faced capuchin (Cebus imitator) groups in Costa Rica, combined with remotely sensed environmental data, we show that within- and between-group competition jointly shape space use, with their relative importance shifting with seasonal and interannual climate cycles. Larger groups compensated for reduced per-capita foraging efficiency by expanding into less-exploited areas over longer timescales rather than increasing daily travel. Notably, this expansion disproportionately encroached on smaller neighboring groups. In the dry season, resource confinement to riparian zones increased intergroup encounters and reduced overlap, with larger groups occupying the highest-quality areas. Climatic extremes linked to El Nino and La Nina exacerbated within-group foraging costs for large groups, whereas intermediate anomalies relaxed these constraints and amplified the benefits of between-group competitive ability. Our findings show that environmental variation shifts the trade-offs of within- and between-group competition, shaping how group-living animals adjust to changing social and ecological conditions.

ecology↗

bioRxiv2025

Development and social dynamics of stone tool use in white-faced capuchin monkeys

Percussive tool use for extractive foraging allows animals to access otherwise inaccessible resources and forage more efficiently, with potentially important implications for their fitness. The development of tool use proficiency has been well-documented in nut-cracking chimpanzees and robust capuchins, and in shellfish-cracking long-tailed macaques, where mothers and proficient tool users are the most important models for social learning. However, little is known about how tool use develops in populations where opportunities for social learning are scarce. White-faced capuchins (Cebus capucinus imitator) on Jicaron Island, Panama, provide a unique case to consider this question: stone tool use is entirely male-biased, meaning juveniles cannot learn from their mothers, and reduced group cohesion further limits social learning opportunities. Here, we investigate the acquisition and development of stone tool proficiency in this population using a year-long dataset from camera traps placed at two experimental anvils. We assess differences in proficiency between age classes, examine the development of tool use proficiency over time, and explore patterns of social attention during tool use. We show that juvenile capuchins are less proficient than subadults and adults, but their proficiency remains stable over the course of one year, suggesting that skill development may require prolonged practice or physical maturation. In contrast to other primates, social learning opportunities on Jicaron appear limited and scrounging is rare, yet when social attention occurs, we find robust patterns. Social attention to tool use mostly comes from juveniles too young to use tools themselves, who observe proficient subadults that tolerate scrounging. Our results contribute to the understanding of how complex tool use behaviours are acquired and maintained in primates. They highlight that even when tool use is largely solitary, directed social attention and social tolerance play an important role in the development of tool use proficiency. HighlightsO_LIJuvenile white-faced capuchins are less proficient tool users than (sub)adults C_LIO_LIDevelopment of capuchins tool use proficiency is a slow process C_LIO_LISocial learning opportunities on Jicaron island are limited and social attention rare C_LIO_LIAttention was selective, juveniles to proficient sub(adults) who tolerated scrounging C_LIO_LINon-tool-using juveniles paid most attention, so likely important for acquisition C_LI

animal behavior and cognition↗

bioRxiv2023

Male-biased stone tool use by wild white-faced capuchins (Cebus capucinus imitator)

Tool-using primates often show sex differences in both the frequency and efficiency of tool use. In species with sex-biased dispersal, such within-group variation likely shapes patterns of cultural transmission of tool-use traditions between groups. On the Panamanian islands of Jicaron and Coiba, a population of white-faced capuchins (Cebus capucinus imitator)--some of which engage in habitual stone tool use--provide an opportunity to test hypotheses about why such sex-biases arise. On Jicaron, we have only observed males engaging in stone tool use, whereas on Coiba, both sexes are known to use tools. Using 5 years of camera trap data, we show that this variation reflects a true sex difference in tool use rather than a sampling artefact, and then test hypotheses about the factors driving this pattern. Differences in physical ability or risk-aversion, and competition over access to anvils do not account for the sex-differences in tool-use we observe. Our data show that females are physically capable of stone tool use: females on Coiba and juveniles on Jicaron as small and smaller than adult females regularly engage in tool use. Females also have ample opportunity to use tools: the sexes are equally terrestrial, and competition over anvils is low. Finally, females rarely scrounge on left-over food items either during or after tool-using events, suggesting they are not being provisioned by males. Although it remains unclear why white-faced capuchin females on Jicaron do not use stone-tools, our results illustrate that such sex biases in socially learned behaviors can arise even in the absence of obvious physical, environmental and social constraints. This suggests that a much more nuanced understanding of the differences in social structure, diet and dispersal patterns are needed to explain why sex-biases in tool use arise in some populations but not in others.

animal behavior and cognition↗

bioRxiv2022

Coupling of Coastal Activity with Tidal Cycles is Stronger in Tool-using Capuchins (Cebus capucinus imitator)

Terrestrial mammals exploiting coastal resources must cope with the challenge that resource availability and accessibility fluctuate with tidal cycles. Tool use can improve foraging efficiency and provide access to structurally protected resources that are otherwise unavailable (e.g., mollusks and fruits). To understand how variable accessibility of valuable resources shapes behavioral patterns, and whether tool use aids in the efficient exploitation of intertidal resources, we compared the relationship between tidal cycles and activity patterns of tool-using vs. non-tool-using groups of white-faced capuchin monkeys on Jicaron Island in Coiba National Park, Panama. Although only a single group of capuchins on Jicaron uses tools, all coastal groups forage on intertidal resources. Using data from >3 years of camera trapping at varying distances from the coast, we found that capuchins on Jicaron showed increased coastal activity during specific parts of the tidal cycle, and that this relationship differed between tool-using and non-tool-using groups, as well as between seasons. Activity patterns of tool-using capuchins were more strongly and consistently tied to tidal cycles compared to non-tool-users, indicating that tool use might allow for more efficient exploitation of tidal resources. Our findings highlight the potential of tool use to aid niche expansion.

animal behavior and cognition↗

bioRxiv2021

Cultural diffusion dynamics depend on behavioural production rules

Culture is an outcome of both the acquisition of knowledge about behaviour through social transmission, and its subsequent production by individuals. Acquisition and production are often discussed interchangeably or modeled separately, yet to date, no study has accounted for both processes and explored their interaction. We present a generative model that integrates the two to explore how variation in production rules might shape cultural diffusion dynamics. Agents make behavioural choices that change as they learn from their productions. Their repertoires also change over time, and the social transmission of behaviours depends on their frequency. We diffuse a novel behaviour through social networks across a large parameter space to demonstrate how individual-level behavioural production rules influence population-level diffusion dynamics. We then investigate how linking transmission and production might affect the performance of two commonly used inferential models for social learning; Network-based Diffusion Analysis, and Experienced Weighted Attraction models. Clarifying the distinction between acquisition and production yields predictions for how production influences diffusion that are generalisable across species, and has consequences for how inferential methods are applied to empirical data. Our model illuminates the differences between social learning and social influence, demonstrates the overlooked role of reinforcement learning in cultural diffusions, and allows for clearer discussions about social learning strategies.

animal behavior and cognition↗

bioRxiv2020

Processing of novel food reveal payoff and rank-biased social learning in a wild primate

Social learning - learning from others - is the basis for behavioural traditions. Different social learning strategies (SLS), where individuals biasedly learn behaviours based on their content or who demonstrates them, may increase an individuals fitness and generate behavioural traditions. While SLS have been mostly studied in isolation, their interaction and the interplay between individual and social learning is less understood. We performed a field-based open diffusion experiment in a wild primate. We provided two groups of vervet monkeys with a novel food, unshelled peanuts, and documented how three different peanut opening techniques spread within the groups. We analysed data using hierarchical Bayesian dynamic learning models that explore the integration of multiple SLS with individual learning. We i) report evidence of social learning compared to strictly individual learning, ii) show that vervets preferentially socially learn the technique that yields the highest observed payoff and iii) also bias attention toward individuals of higher rank. This shows that behavioural preferences can arise when individuals integrate social information about the efficiency of a behaviour alongside cues related to the rank of a demonstrator. When these preferences converge to the same behaviour in a group, they may result in stable behavioural traditions.

animal behavior and cognition↗

bioRxiv2018

Rapid environmental change in games: complications and curiosities

Human-induced rapid environmental change (HIREC) has recently led to alterations in the fitness and behavior of many organisms. Game theory is an important tool of behavioral ecology for analyzing evolutionary situations involving multiple individuals. However, game theory bypasses the details by which behavioral phenotypes are determined, taking the functional perspective straight from expected payoffs to predicted frequencies of behaviors. In contrast with optimization approaches, we identify that to use existing game theoretic models to predict HIREC effects, additional mechanistic details (or assumptions) will often be required. We illustrate this in relation to the hawk-dove game by showing that three different mechanisms, each of which support the same ESS prior to HIREC (fixed polymorphism, probabilistic choice, or cue dependency), can have a substantial effect on behavior (and success) following HIREC. Surprisingly, an increase in the value of resources can lead to a reduction in payoffs (and vice versa), both in the immediate- and long-term following HIREC. An increase in expected costs also increases expected payoffs. Along with these counter-intuitive findings, this work shows that simply understanding the behavioral payoffs of existing games is insufficient to make predictions about the effects of HIREC.\n\nIts the little details that are vital. Little things make big things happen.\n\nJohn Wooden

animal behavior and cognition↗

bioRxiv2018

Habitual stone-tool aided extractive foraging in white-faced capuchins, Cebus capucinus

AO_SCPCAPBSTRACTC_SCPCAPHabitual 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.

animal behavior and cognition↗

bioRxiv2018

The Evolution of Bequeathal in Stable Habitats

Adults sometimes disperse while philopatric offspring inherit the natal site, a pattern known as bequeathal. Despite a decades-old empirical literature, little theoretical work has explored when natural selection may favor bequeathal. We present a simple mathematical model of the evolution of bequeathal in a stable environment, under both global and local dispersal. We find that natural selection favors bequeathal when adults are competitively advantaged over juveniles, baseline mortality is high, the environment is unsaturated, and when juveniles experience high dispersal mortality. However, frequently bequeathal may not evolve, because the fitness cost for the adult is too large relative to inclusive fitness benefits. Additionally, there are many situations for which bequeathal is an ESS, yet cannot invade the population. As bequeathal in real populations appears to be facultative, yet-to-be-modeled factors like timing of birth in the breeding season may strongly influence the patterns seen in natural populations.

evolutionary biology↗

bioRxiv2017

Payoff-biased social learning underlies the diffusion of novel extractive foraging traditions in a wild primate

AO_SCPLOWBSTRACTC_SCPLOWThe 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 payoff-biased learning, in 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 payoff-biased social learning 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.

animal behavior and cognition↗