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 Jicarón 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 Jicarón, 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 provide evidence that this variation likely reflects a sex difference in tool use rather than a sampling artifact, 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 adult females are physically capable of stone tool use: adult females on Coiba and juveniles on Jicarón 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 adult white-faced capuchin females on Jicarón 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.

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. molluscs and fruits). To understand how variable accessibility of valuable resources shapes behavioural 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 versus non-tool-using groups of white-faced capuchin monkeys on Jicarón Island in Coiba National Park, Panama. Although tool use on Jicarón is localized to a small stretch of coast (approx. 1 km), all coastal groups forage on intertidal resources. Using more than 5 years of camera trap data at varying distances from the coast, we found that capuchins on Jicarón 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 with 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.

Using optimal foraging theory to infer how groups make collective decisions.

Studying animal behavior as collective phenomena is a powerful tool for understanding social processes, including group coordination and decision-making. However, linking individual behavior during group decision-making to the preferences underlying those actions poses a considerable challenge. Optimal foraging theory, and specifically the marginal value theorem (MVT), can provide predictions about individual preferences, against which the behavior of groups can be compared under different models of influence. A major strength of formally linking optimal foraging theory to collective behavior is that it generates predictions that can easily be tested under field conditions. This opens the door to studying group decision-making in a range of species; a necessary step for revealing the ecological drivers and evolutionary consequences of collective decision-making.

Ecological and social pressures interfere with homeostatic sleep regulation in the wild.

Sleep is fundamental to the health and fitness of all animals. The physiological importance of sleep is underscored by the central role of homeostasis in determining sleep investment - following periods of sleep deprivation, individuals experience longer and more intense sleep bouts. Yet, most sleep research has been conducted in highly controlled settings, removed from evolutionarily relevant contexts that may hinder the maintenance of sleep homeostasis. Using triaxial accelerometry and GPS to track the sleep patterns of a group of wild baboons (Papio anubis), we found that ecological and social pressures indeed interfere with homeostatic sleep regulation. Baboons sacrificed time spent sleeping when in less familiar locations and when sleeping in proximity to more group-mates, regardless of how long they had slept the prior night or how much they had physically exerted themselves the preceding day. Further, they did not appear to compensate for lost sleep via more intense sleep bouts. We found that the collective dynamics characteristic of social animal groups persist into the sleep period, as baboons exhibited synchronized patterns of waking throughout the night, particularly with nearby group-mates. Thus, for animals whose fitness depends critically on avoiding predation and developing social relationships, maintaining sleep homeostasis may be only secondary to remaining vigilant when sleeping in risky habitats and interacting with group-mates during the night. Our results highlight the importance of studying sleep in ecologically relevant contexts, where the adaptive function of sleep patterns directly reflects the complex trade-offs that have guided its evolution.

Perspectives in machine learning for wildlife conservation.

Inexpensive and accessible sensors are accelerating data acquisition in animal ecology. These technologies hold great potential for large-scale ecological understanding, but are limited by current processing approaches which inefficiently distill data into relevant information. We argue that animal ecologists can capitalize on large datasets generated by modern sensors by combining machine learning approaches with domain knowledge. Incorporating machine learning into ecological workflows could improve inputs for ecological models and lead to integrated hybrid modeling tools. This approach will require close interdisciplinary collaboration to ensure the quality of novel approaches and train a new generation of data scientists in ecology and conservation.

Animal lifestyle affects acceptable mass limits for attached tags.

Animal-attached devices have transformed our understanding of vertebrate ecology. To minimize any associated harm, researchers have long advocated that tag masses should not exceed 3% of carrier body mass. However, this ignores tag forces resulting from animal movement. Using data from collar-attached accelerometers on 10 diverse free-ranging terrestrial species from koalas to cheetahs, we detail a tag-based acceleration method to clarify acceptable tag mass limits. We quantify animal athleticism in terms of fractions of animal movement time devoted to different collar-recorded accelerations and convert those accelerations to forces (acceleration × tag mass) to allow derivation of any defined force limits for specified fractions of any animal's active time. Specifying that tags should exert forces that are less than 3% of the gravitational force exerted on the animal's body for 95% of the time led to corrected tag masses that should constitute between 1.6% and 2.98% of carrier mass, depending on athleticism. Strikingly, in four carnivore species encompassing two orders of magnitude in mass (ca 2-200 kg), forces exerted by '3%' tags were equivalent to 4-19% of carrier body mass during moving, with a maximum of 54% in a hunting cheetah. This fundamentally changes how acceptable tag mass limits should be determined by ethics bodies, irrespective of the force and time limits specified.

Locomotor compromises maintain group cohesion in baboon troops on the move.

When members of a group differ in locomotor capacity, coordinating collective movement poses a challenge: some individuals may have to move faster (or slower) than their preferred speed to remain together. Such compromises have energetic repercussions, yet research in collective behaviour has largely neglected locomotor consensus costs. Here, we integrate high-resolution tracking of wild baboon locomotion and movement with simulations to demonstrate that size-based variation in locomotor capacity poses an obstacle to the collective movement. While all baboons modulate their gait and move-pause dynamics during collective movement, the costs of maintaining cohesion are disproportionately borne by smaller group members. Although consensus costs are not distributed equally, all group-mates do make locomotor compromises, suggesting a shared decision-making process drives the pace of collective movement in this highly despotic species. These results highlight the importance of considering how social dynamics and locomotor capacity interact to shape the movement ecology of group-living species.

Effects of body size on estimation of mammalian area requirements.

Accurately quantifying species' area requirements is a prerequisite for effective area-based conservation. This typically involves collecting tracking data on species of interest and then conducting home-range analyses. Problematically, autocorrelation in tracking data can result in space needs being severely underestimated. Based on the previous work, we hypothesized the magnitude of underestimation varies with body mass, a relationship that could have serious conservation implications. To evaluate this hypothesis for terrestrial mammals, we estimated home-range areas with global positioning system (GPS) locations from 757 individuals across 61 globally distributed mammalian species with body masses ranging from 0.4 to 4000 kg. We then applied block cross-validation to quantify bias in empirical home-range estimates. Area requirements of mammals <10 kg were underestimated by a mean approximately15%, and species weighing approximately100 kg were underestimated by approximately50% on average. Thus, we found area estimation was subject to autocorrelation-induced bias that was worse for large species. Combined with the fact that extinction risk increases as body mass increases, the allometric scaling of bias we observed suggests the most threatened species are also likely to be those with the least accurate home-range estimates. As a correction, we tested whether data thinning or autocorrelation-informed home-range estimation minimized the scaling effect of autocorrelation on area estimates. Data thinning required an approximately93% data loss to achieve statistical independence with 95% confidence and was, therefore, not a viable solution. In contrast, autocorrelation-informed home-range estimation resulted in consistently accurate estimates irrespective of mass. When relating body mass to home range size, we detected that correcting for autocorrelation resulted in a scaling exponent significantly >1, meaning the scaling of the relationship changed substantially at the upper end of the mass spectrum.

Efectos del Tamaño Corporal sobre la Estimación de los Requerimientos de Área de Mamíferos Resumen La cuantificación precisa de los requerimientos de área de una especie es un prerrequisito para que la conservación basada en áreas sea efectiva. Esto comúnmente implica la recolección de datos de rastreo de la especie de interés para después realizar análisis de la distribución local. De manera problemática, la autocorrelación en los datos de rastreo puede resultar en una subestimación grave de las necesidades de espacio. Con base en trabajos previos, formulamos una hipótesis en la que supusimos que la magnitud de la subestimación varía con la masa corporal, una relación que podría tener implicaciones serias para la conservación. Para probar esta hipótesis en mamíferos terrestres, estimamos las áreas de distribución local con las ubicaciones en GPS de 757 individuos de 61 especies de mamíferos distribuidas mundialmente con una masa corporal entre 0.4 y 4,000 kg. Después aplicamos una validación cruzada en bloque para cuantificar el sesgo en estimaciones empíricas de la distribución local. Los requerimientos de área de los mamíferos <10 kg fueron subestimados por una media ∼15% y las especies con una masa ∼100 kg fueron subestimadas en ∼50% en promedio. Por lo tanto, encontramos que la estimación del área estaba sujeta al sesgo inducido por la autocorrelación, el cual era peor para las especies de talla grande. En combinación con el hecho de que el riesgo de extinción incrementa conforme aumenta la masa corporal, el escalamiento alométrico del sesgo que observamos sugiere que la mayoría de las especies amenazadas también tienen la probabilidad de ser aquellas especies con las estimaciones de distribución local menos acertadas. Como corrección, probamos si la reducción de datos o la estimación de la distribución local informada por la autocorrelación minimizan el efecto de escalamiento que tiene la autocorrelación sobre las estimaciones de área. La reducción de datos requirió una pérdida de datos del ∼93% para lograr la independencia estadística con un 95% de confianza y por lo tanto no fue una solución viable. Al contrario, la estimación de la distribución local informada por la autocorrelación resultó en estimaciones constantemente precisas sin importar la masa corporal. Cuando relacionamos la masa corporal con el tamaño de la distribución local, detectamos que la corrección de la autocorrelación resultó en un exponente de escalamiento significativamente >1, lo que significa que el escalamiento de la relación cambió sustancialmente en el extremo superior del espectro de la masa corporal.

Increased terrestriality in a Neotropical primate living on islands with reduced predation risk.

An arboreal lifestyle is thought to be central to primate origins, and most extant primate species still live in the trees. Nonetheless, terrestrial locomotion is a widespread adaptation that has arisen repeatedly within the primate lineage. The absence of terrestriality among the New World monkeys (Platyrrhini) is thus notable and raises questions about the ecological pressures that constrain the expansion of platyrrhines into terrestrial niches. Here, we report the results of a natural experiment, comparing patterns of terrestrial behavior in white-faced capuchin monkeys (Cebus capucinus imitator) living on two islands off the Pacific coast of Panama that lack mammalian predators (island sites) with the behavior of capuchins at three sites in central Panama with more intact predator communities (mainland sites). Surveys with camera traps revealed increased terrestriality in island vs. mainland sites. Capuchin detection rates were higher, the range of party sizes observed was larger, and individuals engaged in a wider range of terrestrial behaviors on the islands lacking mammalian predators. Furthermore, females carrying infants were frequently photographed on the ground at the island sites, but never at the mainland sites. These findings support the long-standing hypothesis that predators constrain the exploitation of terrestrial niches by primates. These results are also consistent with the hypothesis that arboreal locomotion imposes costs that primates will avoid by walking on the ground when predation risk is low.

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

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.

Social tipping points in animal societies.

Animal social groups are complex systems that are likely to exhibit tipping points-which are defined as drastic shifts in the dynamics of systems that arise from small changes in environmental conditions-yet this concept has not been carefully applied to these systems. Here, we summarize the concepts behind tipping points and describe instances in which they are likely to occur in animal societies. We also offer ways in which the study of social tipping points can open up new lines of inquiry in behavioural ecology and generate novel questions, methods, and approaches in animal behaviour and other fields, including community and ecosystem ecology. While some behaviours of living systems are hard to predict, we argue that probing tipping points across animal societies and across tiers of biological organization-populations, communities, ecosystems-may help to reveal principles that transcend traditional disciplinary boundaries.

Understanding sources of variance and correlation among features of Bornean gibbon (Hylobates muelleri) female calls.

Acoustic signals serve important functions in mate choice, resource defense, and species recognition. Quantifying patterns and sources of variation in acoustic signals can advance understanding of the evolutionary processes that shape behavioral diversity more broadly. Animal vocalization datasets are inherently multivariate and hierarchical, wherein multiple features are estimated from calls of many individuals across different recording locations. Patterns of variation within different hierarchical levels-notwithstanding the challenges they present for modeling and inference-can provide insight into processes shaping vocal variation. The current work presents a multivariate, variance components model to investigate three levels of variance (within-female, between-female, and between-site) in Bornean gibbon calls. For six of the eight features estimated from call spectrograms, between-female variance was the most important contributor to total variance. For one feature, trill rate, there were site-level differences, which may be related to geographic isolation of certain gibbon populations. There was also a negative relationship between trill rate and duration of the introduction, suggesting trade-offs in the production of gibbon calls. Given substantial inter-individual variation in gibbon calls, it seems likely that there has been selection to confer information regarding caller identity, but mechanisms leading to site-level variation in trill rate remain to be determined.

Quantifying uncertainty due to fission-fusion dynamics as a component of social complexity.

Groups of animals (including humans) may show flexible grouping patterns, in which temporary aggregations or subgroups come together and split, changing composition over short temporal scales, (i.e. fission and fusion). A high degree of fission-fusion dynamics may constrain the regulation of social relationships, introducing uncertainty in interactions between group members. Here we use Shannon's entropy to quantify the predictability of subgroup composition for three species known to differ in the way their subgroups come together and split over time: spider monkeys (Ateles geoffroyi), chimpanzees (Pan troglodytes) and geladas (Theropithecus gelada). We formulate a random expectation of entropy that considers subgroup size variation and sample size, against which the observed entropy in subgroup composition can be compared. Using the theory of set partitioning, we also develop a method to estimate the number of subgroups that the group is likely to be divided into, based on the composition and size of single focal subgroups. Our results indicate that Shannon's entropy and the estimated number of subgroups present at a given time provide quantitative metrics of uncertainty in the social environment (within which social relationships must be regulated) for groups with different degrees of fission-fusion dynamics. These metrics also represent an indirect quantification of the cognitive challenges posed by socially dynamic environments. Overall, our novel methodological approach provides new insight for understanding the evolution of social complexity and the mechanisms to cope with the uncertainty that results from fission-fusion dynamics.

GPS-identified vulnerabilities of savannah-woodland primates to leopard predation and their implications for early hominins.

Predation is thought to have been a key selection pressure in primate evolution, especially in the savannah-woodland habitats where several early hominin species lived. However, predator-primate prey relationships are still poorly understood because human presence often deters predators, limiting our ability to quantify the impact of predation. Synchronized high-resolution tracking of leopards (Panthera pardus), vervets (Chlorocebus pygerythrus), and olive baboons (Papio anubis) during a 14-month study in Kenya revealed that increased vulnerability to leopard predation was not associated with higher encounter rates, smaller body size, smaller group size, or greater distance from refuges, contrary to long-standing inferences. Instead, the initiation, rate, timing, and duration of encounters, outcome of approaches, and predation events showed only a diel pattern of differential vulnerability. In the absence of human observers, vervets were more vulnerable during the day, whereas baboons were more vulnerable at night, but overall neither species was more vulnerable than the other. As our results show that leopards avoided baboons during the day and hunted them at night, we suggest that the same pattern would have applied to hominins-because they were even larger than baboons and bipedal, resulting in similarly offensive capability on the ground during the day but poorer agility in the trees at night, especially as they became committed bipeds. Drawing from hominid behavior and archaeopaleontological and ethnographic evidence, we hypothesize that ground-sleeping hominins initially dealt with this formidable threat by using stone tools to modify Acacia branches into 'bomas', thorny enclosures that provided nighttime shelter. The ability of hominins to create their own nightly refuges on the ground wherever Acacia spp. were available would have allowed them to range more widely, a crucial step in furthering the spread of hominins across Africa and beyond.

Inferring influence and leadership in moving animal groups.

Collective decision-making is a daily occurrence in the lives of many group-living animals, and can have critical consequences for the fitness of individuals. Understanding how decisions are reached, including who has influence and the mechanisms by which information and preferences are integrated, has posed a fundamental challenge. Here, we provide a methodological framework for studying influence and leadership in groups. We propose that individuals have influence if their actions result in some behavioural change among their group-mates, and are leaders if they consistently influence others. We highlight three components of influence (influence instances, total influence and consistency of influence), which can be assessed at two levels (individual-to-individual and individual-to-group). We then review different methods, ranging from individual positioning within groups to information-theoretic approaches, by which influence has been operationally defined in empirical studies, as well as how such observations can be aggregated to give insight into the underlying decision-making process. We focus on the domain of collective movement, with a particular emphasis on methods that have recently been, or are being, developed to take advantage of simultaneous tracking data. We aim to provide a resource bringing together methodological tools currently available for studying leadership in moving animal groups, as well as to discuss the limitations of current methodologies and suggest productive avenues for future research.This article is part of the theme issue 'Collective movement ecology'.

GPS-identified, low-level nocturnal activity of vervets (Chlorocebus pygerythrus) and olive baboons (Papio anubis) in Laikipia, Kenya.

OBJECTIVES: Except for owl monkeys (Aotus spp.), all anthropoid primates are considered strictly diurnal. Recent studies leveraging new technologies have shown, however, that some diurnal anthropoids also engage in nocturnal activity. Here we examine the extent to which vervets (Chlorocebus pygerythrus) and olive baboons (Papio anubis) are active at night. MATERIALS AND METHODS: We deployed GPS collars with tri-axial accelerometer data loggers on 18 free-ranging adult females: 12 vervets spread among 5 social groups, and 6 olive baboons spread among 4 groups. Their locations were recorded every 15 min, and their activity levels, for 3 s/min over 7.5 months. We also used camera traps that were triggered by heat and movement at seven sleeping sites. RESULTS: Travel was detected on 0.4% of 2,029 vervet-nights involving 3 vervets and 1.1% of 1,109 baboon-nights involving 5 baboons. Travel was mainly arboreal for vervets but mainly terrestrial for baboons. During the night, vervets and baboons were active 13% and 15% of the time, respectively. Activity varied little throughout the night and appeared unaffected by moon phase. DISCUSSION: Our results confirm the low nocturnality of vervets and olive baboons, which we suggest is related to living near the equator with consistent 12-hr days, in contrast to other anthropoids that are more active at night. Since anthropoid primates are thought to have evolved in northern latitudes, with later dispersal to tropical latitudes, our results may have implications for understanding the evolution of anthropoid diurnality.

Habitat and social factors shape individual decisions and emergent group structure during baboon collective movement.

For group-living animals traveling through heterogeneous landscapes, collective movement can be influenced by both habitat structure and social interactions. Yet research in collective behavior has largely neglected habitat influences on movement. Here we integrate simultaneous, high-resolution, tracking of wild baboons within a troop with a 3-dimensional reconstruction of their habitat to identify key drivers of baboon movement. A previously unexplored social influence - baboons' preference for locations that other troop members have recently traversed - is the most important predictor of individual movement decisions. Habitat is shown to influence movement over multiple spatial scales, from long-range attraction and repulsion from the troop's sleeping site, to relatively local influences including road-following and a short-range avoidance of dense vegetation. Scaling to the collective level reveals a clear association between habitat features and the emergent structure of the group, highlighting the importance of habitat heterogeneity in shaping group coordination.

Both Nearest Neighbours and Long-term Affiliates Predict Individual Locations During Collective Movement in Wild Baboons.

In many animal societies, groups of individuals form stable social units that are shaped by well-delineated dominance hierarchies and a range of affiliative relationships. How do socially complex groups maintain cohesion and achieve collective movement? Using high-resolution GPS tracking of members of a wild baboon troop, we test whether collective movement in stable social groups is governed by interactions among local neighbours (commonly found in groups with largely anonymous memberships), social affiliates, and/or by individuals paying attention to global group structure. We construct candidate movement prediction models and evaluate their ability to predict the future trajectory of focal individuals. We find that baboon movements are best predicted by 4 to 6 neighbours. While these are generally individuals' nearest neighbours, we find that baboons have distinct preferences for particular neighbours, and that these social affiliates best predict individual location at longer time scales (>10 minutes). Our results support existing theoretical and empirical studies highlighting the importance of local rules in driving collective outcomes, such as collective departures, in primates. We extend previous studies by elucidating the rules that maintain cohesion in baboons 'on the move', as well as the different temporal scales of social interactions that are at play.