A new approach to geostatistical synthesis of historical records reveals capuchin spatial responses to climate and demographic change.

Recent proliferation of GPS technology has transformed animal movement research. Yet, time-series data from this recent technology rarely span beyond a decade, constraining longitudinal research. Long-term field sites hold valuable historic animal location records, including hand-drawn maps and semantic descriptions. Here, we introduce a generalised workflow for converting such records into reliable location data to estimate home ranges, using 30 years of sleep-site data from 11 white-faced capuchin (Cebus imitator) groups in Costa Rica. Our findings illustrate that historic sleep locations can reliably recover home range size and geometry. We showcase the opportunity our approach presents to resolve open questions that can only be addressed with very long-term data, examining how home ranges are affected by climate cycles and demographic change. We urge researchers to translate historical records into usable movement data before this knowledge is lost; it is essential to understanding how animals are responding to our changing world.

Sharing sleeping sites disrupts sleep but catalyses social tolerance and coordination between groups.

Sleeping refuges-like other important, scarce and shareable resources-can serve as hotspots for animal interaction, shaping patterns of attraction and avoidance. Where sleeping sites are shared, individuals balance the opportunity for interaction with new social partners against their need for sleep. By expanding the network of connections within animal populations, such night-time social interactions may have important, yet largely unexplored, impacts on critical behavioural and ecological processes. Here, using GPS and tri-axial accelerometry to track the movements and sleeping patterns of wild olive baboon groups (Papio anubis), we show that sharing sleeping sites disrupts sleep but appears to catalyse social tolerance and coordinated movement between groups. Individual baboons experienced shorter and more fragmented sleep when groups shared a sleeping site. After sharing sleeping sites, however, otherwise independent groups showed a strong pattern of spatial attraction, moving cohesively for up to 3 days. Our findings highlight the influence of night-time social interactions on daytime social relationships and demonstrate how a population's reliance on, and need to share, limiting resources can drive the emergence of intergroup tolerance.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

How to treat mixed behavior segments in supervised machine learning of behavioural modes from inertial measurement data.

The application of supervised machine learning methods to identify behavioural modes from inertial measurements of bio-loggers has become a standard tool in behavioural ecology. Several design choices can affect the accuracy of identifying the behavioural modes. One such choice is the inclusion or exclusion of segments consisting of more than a single behaviour (mixed segments) in the machine learning model training data. Currently, the common practice is to ignore such segments during model training. In this paper we tested the hypothesis that including mixed segments in model training will improve accuracy, as the model would perform better in identifying them in the test data. We test this hypothesis using a series of data simulations on four datasets of accelerometer data coupled with behaviour observations, obtained from four study species (Damaraland mole-rats, meerkats, olive baboons, polar bears). Results show that when a substantial proportion of the test data are mixed behaviour segments (above ~ 10%), including mixed segments in machine learning model training improves the accuracy of classification. These results were consistent across the four study species, and robust to changes in segment length, sample size, and degree of mixture within the mixed segments. However, we also find that in some cases (particularly in baboons) models trained with mixed segments show reduced accuracy in classifying test data containing only single behaviour (pure) segments, compared to models trained without mixed segments. Based on these results, we recommend that when the classification model is expected to deal with a substantial proportion of mixed behaviour segments (> 10%), it is beneficial to include them in model training, otherwise, it is unnecessary but also not harmful. The exception is when there is a basis to assume that the training data contains a higher rate of mixed segments than the actual (unobserved) data to be classified-such a situation may occur particularly when training data are collected in captivity and used to classify data from the wild. In this case, excess inclusion of mixed segments in training data should probably be avoided.

The sociality of sleep in animal groups.

Group-living animals sleep together, yet most research treats sleep as an individual process. Here, we argue that social interactions during the sleep period contribute in important, but largely overlooked, ways to animal groups' social dynamics, while patterns of social interaction and the structure of social connections within animal groups play important, but poorly understood, roles in shaping sleep behavior. Leveraging field-appropriate methods, such as direct and video-based observation, and increasingly common on-animal motion sensors (e.g., accelerometers), behavioral indicators can be tracked to measure sleep in multiple individuals in a group of animals simultaneously. Sleep proximity networks and sleep timing networks can then be used to investigate the collective dynamics of sleep in wild group-living animals.

The cost of defeat: Capuchin groups travel further, faster and later after losing conflicts with neighbors.

Although competition between social groups is central to hypotheses about the evolution of human social organization, competitive interactions among group-mates are thought to play a more dominant role in shaping the behavior and ecology of other primate species. However, few studies have directly tested the impact of intergroup conflicts in non-human primates. What is the cost of defeat? To address this question, the movements of six neighboring white-faced capuchin (Cebus capucinus) social groups living on Barro Colorado Island, Panama were tracked simultaneously using an Automated Radio Telemetry System (ARTS), for a period of six months. Groups moved 13% (441 m) further on days they lost interactions compared with days they won interactions. To cover these larger distances, they traveled faster, stopped less frequently, and remained active later in the evening. Defeat also caused groups to alter their patterns of space use. Losing groups had straighter travel paths than winning groups, larger net displacements and were more likely to change their sleeping site. These results demonstrate that losing groups pay increased travel costs and suggest that they forage in low-quality areas. They provide some of the first direct evidence that intergroup conflicts have important energetic consequences for members of competitively unsuccessful primate social groups. A better understanding of how intergroup competition impacts patterns of individual fitness is thus needed to clarify the role that this group-level process plays in shaping the evolution of human- and non-human primate behavior.

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.

Why mob? Reassessing the costs and benefits of primate predator harassment.

While some primate species attempt to avoid predators by fleeing, hiding or producing alarm calls, others actually approach, harass and sometimes attack potential threats, a behavior known as 'mobbing'. Why individuals risk their safety to mob potential predators remains poorly understood. Here, I review reports of predator harassment by primates to (1) determine the distribution of this behavior across taxa, (2) assess what is known about the costs of mobbing, and (3) evaluate hypotheses about its function. Mobbing is taxonomically widespread and is used against a wide range of predator species. However, inconsistent use of the term 'mobbing' within the primate literature, the lack of systematic studies of primate mobbing, and the likelihood of systematic biases in the existing data pose significant obstacles to understanding this puzzling behavior. Although difficult to quantify, the costs associated with harassing predators appear nontrivial. Many benefits that have been proposed to explain mobbing in birds may also be important in primate systems. There are puzzling aspects of primate mobbing, however, that existing hypotheses cannot explain. Future research should consider the within-group signaling potential of this costly behavior, as well as the ability of behavioral syndromes to explain the distribution of mobbing in primates.

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.