Margaret C. Crofoot

Terrestrial animal tracking as an eye on life and planet

A brave new world with a wider view Researchers have long attempted to follow animals as they move through their environment. Until relatively recently, however, such efforts were limited to short distances and times in species large enough to carry large batteries and transmitters. New technologies have opened up new frontiers in animal tracking remote data collection. Hussey et al. review the unique directions such efforts have taken for marine systems, while Kays et al. review recent advances for terrestrial species. We have entered a new era of animal ecology, where animals act as both subjects and samplers of their environments. Science, this issue 10.1126/science.1255642, 10.1126/science.aaa2478 BACKGROUND The movement of animals makes them fascinating but difficult study subjects. Animal movements underpin many biological phenomena, and understanding them is critical for applications in conservation, health, and food. Traditional approaches to animal tracking used field biologists wielding antennas to record a few dozen locations per animal, revealing only the most general patterns of animal space use. The advent of satellite tracking automated this process, but initially was limited to larger animals and increased the resolution of trajectories to only a few hundred locations per animal. The last few years have shown exponential improvement in tracking technology, leading to smaller tracking devices that can return millions of movement steps for ever-smaller animals. Finally, we have a tool that returns high-resolution data that reveal the detailed facets of animal movement and its many implications for biodiversity, animal ecology, behavior, and ecosystem function. ADVANCES Improved technology has brought animal tracking into the realm of big data, not only through high-resolution movement trajectories, but also through the addition of other on-animal sensors and the integration of remote sensing data about the environment through which these animals are moving. These new data are opening up a breadth of new scientific questions about ecology, evolution, and physiology and enable the use of animals as sensors of the environment. High–temporal resolution movement data also can document brief but important contacts between animals, creating new opportunities to study social networks, as well as interspecific interactions such as competition and predation. With solar panels keeping batteries charged, “lifetime” tracks can now be collected for some species, while broader approaches are aiming for species-wide sampling across multiple populations. Miniaturized tags also help reduce the impact of the devices on the study subjects, improving animal welfare and scientific results. As in other disciplines, the explosion of data volume and variety has created new challenges and opportunities for information management, integration, and analysis. In an exciting interdisciplinary push, biologists, statisticians, and computer scientists have begun to develop new tools that are already leading to new insights and scientific breakthroughs. OUTLOOK We suggest that a golden age of animal tracking science has begun and that the upcoming years will be a time of unprecedented exciting discoveries. Technology continues to improve our ability to track animals, with the promise of smaller tags collecting more data, less invasively, on a greater variety of animals. The big-data tracking studies that are just now being pioneered will become commonplace. If analytical developments can keep pace, the field will be able to develop real-time predictive models that integrate habitat preferences, movement abilities, sensory capacities, and animal memories into movement forecasts. The unique perspective offered by big-data animal tracking enables a new view of animals as naturally evolved sensors of environment, which we think has the potential to help us monitor the planet in completely new ways. A massive multi-individual monitoring program would allow a quorum sensing of our planet, using a variety of species to tap into the diversity of senses that have evolved across animal groups, providing new insight on our world through the sixth sense of the global animal collective. We expect that the field will soon reach a transformational point where these studies do more than inform us about particular species of animals, but allow the animals to teach us about the world. Big-data animal tracking. The red trajectory shows how studies can now track animals with unprecedented detail, allowing researchers to predict the causes and consequences of movements, and animals to become environmental sensors. Multisensor tracking tags monitor movement, behavior, physiology, and environmental context. Geo- and biosciences merge now using a multitude of remote-sensing data. Understanding how social and interspecific interactions affect movement is the next big frontier. Moving animals connect our world, spreading pollen, seeds, nutrients, and parasites as they go about the their daily lives. Recent integration of high-resolution Global Positioning System and other sensors into miniaturized tracking tags has dramatically improved our ability to describe animal movement. This has created opportunities and challenges that parallel big data transformations in other fields and has rapidly advanced animal ecology and physiology. New analytical approaches, combined with remotely sensed or modeled environmental information, have opened up a host of new questions on the causes of movement and its consequences for individuals, populations, and ecosystems. Simultaneous tracking of multiple animals is leading to new insights on species interactions and, scaled up, may enable distributed monitoring of both animals and our changing environment.

Shared decision-making drives collective movement in wild baboons

Baboons follow the pack, not the leader How do groups of animals, including humans, make decisions that affect the entire group? Evidence collected from schooling animals suggests that the process is somewhat democratic, with nearest neighbors and the majority shaping overall collective behavior. In animals with hierarchical social structures such as primates or wolves, however, such democracy may be complicated by dominance. Strandburg-Peshkin et al. monitored all the individuals within a baboon troop continuously over the course of their daily activities. Even within this highly socially structured species, movement decisions emerged via a shared process. Thus, democracy may be an inherent trait of collective behavior. Science, this issue p. 1358 Democracy guides group decisions in baboons, even in the presence of strong social hierarchies. Conflicts of interest about where to go and what to do are a primary challenge of group living. However, it remains unclear how consensus is achieved in stable groups with stratified social relationships. Tracking wild baboons with a high-resolution global positioning system and analyzing their movements relative to one another reveals that a process of shared decision-making governs baboon movement. Rather than preferentially following dominant individuals, baboons are more likely to follow when multiple initiators agree. When conflicts arise over the direction of movement, baboons choose one direction over the other when the angle between them is large, but they compromise if it is not. These results are consistent with models of collective motion, suggesting that democratic collective action emerging from simple rules is widespread, even in complex, socially stratified societies.

Interaction location outweighs the competitive advantage of numerical superiority in Cebus capucinus intergroup contests

Numerical superiority confers a competitive advantage during contests among animal groups, shaping patterns of resource access, and, by extension, fitness. However, relative group size does not always determine the winner of intergroup contests. Smaller, presumably weaker social groups often defeat their larger neighbors, but how and when they are able to do so remains poorly understood. Models of competition between individuals suggest that location may influence contest outcome. However, because of the logistical difficulties of studying intergroup interactions, previous studies have been unable to determine how contest location and group size interact to shape relationships among groups. We address this question by using an automated radio telemetry system to study intergroup interactions among six capuchin monkey (Cebus capucinus) social groups of varying sizes. We find that the odds of winning increase with relative group size; one additional group member increases the odds of winning an interaction by 10%. However, this effect is not uniform across space; with each 100 m that a group moves away from the center of its home range, its odds of winning an interaction decrease by 31%. We demonstrate that contest outcome depends on an interaction between group size and location, such that small groups can defeat much larger groups near the center of their home range. The tendency of resident groups to win contests may help explain how small groups persist in areas with intense intergroup competition.

Social networks in primates: smart and tolerant species have more efficient networks

Network optimality has been described in genes, proteins and human communicative networks. In the latter, optimality leads to the efficient transmission of information with a minimum number of connections. Whilst studies show that differences in centrality exist in animal networks with central individuals having higher fitness, network efficiency has never been studied in animal groups. Here we studied 78 groups of primates (24 species). We found that group size and neocortex ratio were correlated with network efficiency. Centralisation (whether several individuals are central in the group) and modularity (how a group is clustered) had opposing effects on network efficiency, showing that tolerant species have more efficient networks. Such network properties affecting individual fitness could be shaped by natural selection. Our results are in accordance with the social brain and cultural intelligence hypotheses, which suggest that the importance of network efficiency and information flow through social learning relates to cognitive abilities.

Intergroup Aggression in Primates and Humans: The Case for a Unified Theory

Human warfare and intergroup aggression among primates have traditionally been considered to be largely unrelated phenomena. Recently, however, chimpanzee intergroup violence has been proposed to show evolutionary continuities with war among small-scale societies because both systems involve interactions among temporary subgroups, deliberate attempts to hunt and maim, and demographically significant death rates. Here, we ask whether the functional similarities between intergroup aggression among humans and chimpanzees can be extended to troop-living primates. In most primates, patterns of intergroup aggression involve brief encounters among stable troops, rare violence, and almost no killing. Although they, therefore, show little behavioral resemblance to warfare, growing evidence indicates that intergroup dominance is adaptively important in primates because it predicts long-term fitness. This suggests that in all primates, including humans, individuals use coalitions to maintain or expand access to resources by dominating their neighbors. Thus, while the style of coalitionary aggression depends on each species’ evolutionary ecology, we propose that the essential functional reasons for intergroup competition are consistent across group-living primates and humans: strength in numbers predicts long-term access to resources.

Mating and feeding competition in white-faced capuchins ( Cebus capucinus ): the importance of short- and long-term strategies

I investigate the ecological context of intergroup agonism (IGA) in white-faced capuchins ( Cebus capucinus ) to elucidate the roles of feeding and mating competition, explicitly exploring both long- and short-term competitive strategies. Short-term mating competition is not a major function of IGA in C. capucinus . Males were the primary participants in IGA, but did not attempt to prevent extra-group copulations by herding females, and there was no relationship between IGA rate and conception rate. Long-term mating competition, on the other hand, may be important: 41% of interactions were low intensity, as would be expected if males were assessing the composition of neighboring groups in anticipation of a takeover. However, 59% of intergroup interactions escalated to chases or physical contact and females were frequent participants in IGA, directing aggression at adults of both sexes and at juveniles. These findings are not consistent with male mating competition and, in conjunction with overlapping home ranges, high interaction rate, and a positive relationship between IGA rate and both food availability and fruit patch size, they indicate that intergroup feeding competition may be important for capuchins. However, interactions do not preferentially occur at food sources, suggesting that capuchins may gain long-term, rather than short-term, benefits from IGA.

Does watching a monkey change its behaviour? Quantifying observer effects in habituated wild primates using automated radiotelemetry

In studies of animal behaviour, researchers have long been concerned that their presence may change the conduct of their study subjects. To minimize observer effects, researchers often habituate their study animals. The premise of this method is that, with sufficient neutral exposure, animals will stop reacting to humans. While numerous studies demonstrate that negative responses to humans decrease over time, the fact that an animal does not flee from or behave aggressively towards observers cannot be taken as evidence that it is not altering its behaviour in other, more subtle ways. Because remotely monitoring the behaviour of wild animals is difficult, it has not been possible to answer the critical question: do habituated animals change their behaviour when researchers are present? Here, we use data from an automated radiotelemetry system that remotely monitored the movement and activity of radiocollared animals to test whether observers affected the behaviour of seven habituated white-faced capuchins, Cebus capucinus. We found no evidence that observers influenced the ranging behaviour or activity patterns of their study subjects. Capuchins did not move faster, stop to rest less frequently, or display higher levels of activity when they were being followed compared to when they were alone. It has been suggested that researchers may embolden habituated study subjects, artificially increasing their relative dominance, but we found no relationship between observer presence and proximity to neighbouring social groups. Although it remains possible that observer effects existed but were too subtle to be detected with the remote sensing technology we used, the results of this study nevertheless provide reassuring evidence that humans can observe habituated wild animals without overly influencing the animals’ activity and movement patterns.

Aggression, grooming and group-level cooperation in white-faced capuchins (Cebus capucinus): insights from social networks

The form of animal social systems depends on the nature of agonistic and affiliative interactions. Social network theory provides tools for characterizing social structure that go beyond simple dyadic interactions and consider the group as a whole. We show three groups of capuchin monkeys from Barro Colorado Island, Panama, where there are strong connections between key aspects of aggression, grooming, and proximity networks, and, at least among females, those who incur risk to defend their group have particular “social personalities.” Although there is no significant correlation for any of the network measures between giving and receiving aggression, suggesting that dominance relationships do not follow a simple hierarchy, strong correlations emerge for many measures between the aggression and grooming networks. At the local, but not global, scale, receiving aggression and giving grooming are strongly linked in all groups. Proximity shows no correlation with aggression at either the local or the global scale, suggesting that individuals neither seek out nor avoid aggressors. Yet, grooming has a global but not local connection to proximity. Extensive groomers who tend to direct their efforts at other extensive groomers also spend time in close proximity to many other individuals. These results indicate the important role that prosociality plays in shaping female social relationships. We also show that females who receive the least aggression, and thus pay low costs for group living, are most likely to participate in group defense. No consistent “social personality” traits characterize the males who invest in group defense. Am. J. Primatol. 73:821–833, 2011.

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. DOI: http://dx.doi.org/10.7554/eLife.19505.001

Non-random walks in monkeys and humans

Principles of self-organization play an increasingly central role in models of human activity. Notably, individual human displacements exhibit strongly recurrent patterns that are characterized by scaling laws and can be mechanistically modelled as self-attracting walks. Recurrence is not, however, unique to human displacements. Here we report that the mobility patterns of wild capuchin monkeys are not random walks, and they exhibit recurrence properties similar to those of cell phone users, suggesting spatial cognition mechanisms shared with humans. We also show that the highly uneven visitation patterns within monkey home ranges are not entirely self-generated but are forced by spatio-temporal habitat heterogeneities. If models of human mobility are to become useful tools for predictive purposes, they will need to consider the interaction between memory and environmental heterogeneities.