Eye-tracking with nonhuman primates is now more accessible than ever before

Human and nonhuman primates rely almost exclusively on vision for social communication. Therefore, tracking eye movements and examining visual scan paths can provide a wealth of information about many aspects of primate social information processing. Although eye-tracking techniques have been utilized with humans for some time, similar studies in nonhuman primates have been less frequent over recent decades. This has largely been owing to the need for invasive manipulations, such as the surgical implantation of devices to limit head movement, which may not be possible in some laboratories or at some universities, or may not be congruent with some experimental aims (i.e., longitudinal studies). It is important for all nonhuman primate researchers interested in visual information processing or operant behavior to realize that such invasive procedures are no longer necessary. Here, we briefly describe new methods for fully noninvasive video eye-tracking with adult rhesus monkeys (Macaca mulatta). We also describe training protocols that require only ～30 days to accomplish and quality control measures that promote reliable data collection. It is our hope that this brief overview will reacquaint nonhuman primate researchers with the benefits of eye-tracking and promote expanded use of this powerful methodology.     

Methods in Primate Nutritional Ecology: A User’s Guide

An important goal of primatology is to identify the ecological factors that affect primate abundance, diversity, demography, and social behavior. Understanding the nutritional needs of primates is central to understanding primate ecology because adequate nutrition is a prerequisite for successful reproduction. Here, we review nutritional methods and provide practical guidelines to measure nutrient intake by primates in field settings. We begin with an assessment of how to estimate food intake by primates using behavioral observations. We then describe how to collect, prepare, and preserve food samples. Finally, we suggest appropriate nutritional assays for estimating diet nutritional quality and point to the merits and limitations of each. We hope this review will inspire primatologists to use nutritional ecology to answer many unresolved questions in primatology.     

Sex‐biased dispersal of human ancestors

Some anthropologists and primatologists have argued that, judging by extant chimpanzees and humans, which are female‐biased dispersers, the common ancestors of humans and chimpanzees were also female‐biased dispersers. It has been thought that sex‐biased dispersal patterns have been genetically transmitted for millions of years. However, this character has changed many times with changes in environment and life‐form during human evolution and historical times. I examined life‐form and social organization of nonhuman primates, among them gatherers (foragers), hunter‐gatherers, agriculturalists, industrialists, and modern and extant humans. I conclude that dispersal patterns changed in response to environmental conditions during primate and human evolution.     

Energetics of feeding,social behavior,and life history in non-human primates

Energy is a variable of key importance to a wide range of research in primate behavioral ecology, life history, and conservation. However, obtaining detailed data on variation in energetic condition, and its biological consequences, has been a considerable challenge. In the past 20 years, tremendous strides have been made towards non-invasive methods for monitoring the physiology of animals in their natural environment. These methods provide detailed, individualized data about energetic condition, as well as energy allocations to growth, reproduction, and somatic health. In doing so, they add much-needed resolution by which to move beyond correlative studies to research programs that can discriminate causes from effects and disaggregate multiple correlated features of the social and physical environment. In this review, I describe the conceptual and methodological approaches for studying primate energetics. I then discuss the core questions about primate feeding ecology, social behavior, and life history that can benefit from physiological studies, highlighting the ways in which recent research has done so. Among these are studies that test, and often refute, common assumptions about how feeding ecology shapes primate biology, and those that reveal proximate associations between energetics and reproductive strategies.     

The Maturation of Ethnoprimatology: Theoretical and Methodological Pluralism

Most remaining populations of primates live in environments that have been influenced in some way by humans (e.g., protected forests bisected by major roads, forest–farm edges, and urban centers). The field of ethnoprimatology has made these environments where humans and other primates interface its primary concern, recognizing that to fully understand primate behavior, our research objectives and practice cannot be disengaged from the human dimension. During the field’s initial years, scholars drew largely from theory and technique in primate ecology and sociocultural anthropology. The contributions to this Special Issue, which include empirical research and review papers, exemplify how the ethnoprimatologist’s toolkit has since expanded to include concepts, frameworks, and methods from the natural sciences (evolutionary biology, conservation ecology, epidemiology), and the social sciences and humanities (anthropology, geography, philosophy, and science studies). Moreover, the settings in which to examine the human–primate interface have diversified to include rural, urban, mixed-landscape, and captive spaces. In this introduction, I review the emergence and scope of ethnoprimatology. I then challenge some of the critiques leveled against ethnoprimatology and highlight its broader conceptual contributions, key elements of the field’s maturation, and recent trends in theoretically and methodologically integrative scholarship in ethnoprimatology. I conclude by offering a set of postulates to guide future ethnoprimatological work that is theoretically and methodological pluralistic and positioned to advance effective primate conservation efforts and facilitate sustainable human–primate coexistence.     

Where Next? Group Coordination and Collective Decision Making by Primates

Primate groups need to remain coordinated in their activities and collectively decide when and where to travel if they are to accrue the benefits and minimize the costs of sociality. The achievement of coordinated activity and group decision making therefore has important implications for individual survival and reproduction. The aim of this special issue is to bring together a collection of empirical, theoretical, and commentary articles by primatologists studying this rapidly expanding topic. In this article, we introduce the contributions within the special issue and provide a background to the topic. We begin by focusing on decisions that involve a collective transition between a resting and a moving state, a transition we term making the move. We examine whether specific predeparture behaviors seen during transitions represent intentional processes or more simple response facilitation. Next we classify decisions according to the contribution of individual group members, and describe how, and why, certain individuals can have a disproportionate influence over group-mates?? behavior. We then review how primate groups make decisions on the move. In particular, we focus on how variability in group size and spatial organization helps or hinders information transmission and coordination. We end with a discussion of new tools and methodology that will allow future investigators to address some outstanding questions in primate coordination and decision-making research. We conclude that a better integration of concepts and terminology, along with a focus on how individuals integrate environmental and social information, will be critical to developing a satisfactory understanding of collective patterns of behavior in primate systems.     

Bonding, biophilia, biosynergy, and the future of primates in the wild

Human and nonhuman primates bond with one another in countless ways, and the results are varied and vital to the individuals and species involved. The manifesto that is the basis for the collection of essays in which this commentary is included proposes that the "human/nonhuman bonds that arise in primatological research and practice deserve and demand study and research." An essential corollary of this proposal is that the primatologists themselves must be studied. The aim of this essay is to explore the influence of human/nonhuman primate bonding on conservation practice and on the future of primates in the wild. This commentary applies the author's professional experience as a conservation psychologist and his research on the impact of profound interspecies bonds on human worldviews, attitudes, and behavior. It examines two general categories of bonds: those driven by Biophilia (human fascination with life) and those influenced by Biosynergy (mutual enrichment of life). It is the author's premise that biosynergy promotes complex collaborative interspecies bonds that broaden the conservationist's desire to enhance synergy among all organisms in an ecosystem. Conversely, biophilia induces relatively simple unidirectional bonds between humans and other animals that deepen the conservationist's desire to understand and protect certain species. This contrast raises some crucial questions. Do biophilia-driven bonds between conservationists and their favorite primates blind them to the synergistic needs of all species and impair their ability to work for sustained preservation of threatened habitat? Does biosynergy-based human/nature bonding enhance focus on conservation as an ecological science and thus ignore species-specific factors crucial to assure survival of endangered primates? How can both types of bonds be optimally applied to the conservation of wildlife and wilderness?     

Stereotypies in Captive Primates and the Use of Inositol: Lessons from Obsessive–Compulsive Disorder in Humans

Animal stereotypies have long been used in the study of obsessive–compulsive disorder (OCD) in humans. These studies have led to the understanding of some of the molecular pathways in the disorder and the use of selective serotonin reuptake inhibitors and myo-inositol in the treatment of these conditions. If animal models, especially nonhuman primate models, were used to study human disorders and if the resulting treatments were successful, then conversely one should be able to treat nonhuman primate stereotypies with similar methods. We here summarize animal models of OCD (including nonhuman primate models) and human OCD treatments, and using successful human treatment by myo-inositol as models, recommend the use of myo-inositol in good captive management practice and the treatment of nonhuman primate stereotypies. We believe that this would be particularly useful in the treatment of stereotypies in nonhuman primates because they are physiologically so similar to humans.     

Humans as primates: The social relationships of Efe pygmy men in comparative perspective

The Efe are short-statured specialized hunger-gatherers living in the moist tropical forest in northeast Zaire. They live in small mobile groups averaging 18 individuals and practice viripatrilocal residence — what primatologists refer to as male philopatry and female dispersal. This study uses methods commonly employed by primatologists to study the social relationships of Efe men. It compares their association and affiliation patterns with those of two nonhuman primate species that show male philopatry and female transfer. The analyses of 376 hr of focal behavior observations on 16 Efe men reveal that the majority of their associations were with other adult men. Men associated preferentially with kin over non-kin, and with close kin more than with distant kin. Men's close relationships, or companionships,sensu Smuts' (1985) friendships among anubis baboons, were predominantly with other adult men; however, each man who cohabited with a woman had his strongestcompanionship by far with that woman. These quantitative measures of affinity are consistent with the Efe's pattern of viripatrilocal residence, where-by males remain in their natal group with their close male kin and females join or are recruited from other patriclans. The social relationships of Efe men are similar in some respects to those of hamadryas and chimpanzees; however, Efe men's social networks are larger and more fluid. We speculate that the explanation proposed for male philopatry and female dispersal among nonhuman primates also applies to the Efe.     

Advancing Primate Research and Conservation Through the Use of Camera Traps: Introduction to the Special Issue

Effective conservation and management of primates depend on our ability to accurately assess and monitor populations through research. Camera traps are proving to be useful tools for studying a variety of primate species, in diverse and often difficult habitats. Here, we discuss the use of camera traps in primatology to survey rare species, assess populations, and record behavior. We also discuss methodological considerations for primate studies, including camera trap research design, inherent biases, and some limitations of camera traps. We encourage other primatologists to use transparent and standardized methods, and when appropriate to consider using occupancy framework to account for imperfect detection, and complementary techniques, e.g., transect counts, interviews, behavioral observation, to ensure accuracy of data interpretation. In addition, we address the conservation implications of camera trapping, such as using data to inform industry, garner public support, and contributing photos to large-scale habitat monitoring projects. Camera trap studies such as these are sure to advance research and conservation of primate species. Finally, we provide commentary on the ethical considerations, e.g., photographs of humans and illegal activity, of using camera traps in primate research. We believe ethical considerations will be particularly important in future primate studies, although this topic has not previously been addressed for camera trap use in primatology or any wildlife species.     

A place that answers questions: primatological field sites and the making of authentic observations

The ideals and realities of field research have shaped the development of behavioural primatology over the latter half of the twentieth century. This paper draws on interviews with primatologists as well as a survey of the scientific literature to examine the idealized notion of the field site as a natural place and the physical environment of the field as a research space. It shows that what became standard field practice emerged in the course of wide ranging debate about the techniques, personal qualities and site conditions best suited to the scientific study of the natural behaviour of apes and monkeys. Although the laboratory was a constant presence in this debate, the export of techniques from the laboratory to the field was limited, due to concerns that experimental manipulation would destroy the naturalness of the behaviour. The paper goes on to demonstrate the central significance given by primatologists to the unique social, historical and ecological circumstances of particular field sites, and to sketch some of the complexities that fieldworkers contend with in trying to realize their ideals. Primatologists seek field sites that answer their questions; but once their studies become long term, they also need to find questions that answer to ever changing conditions at those sites.     

The human–primate interface in the New Normal: Challenges and opportunities for primatologists in the COVID-19 era and beyond

The emergence of SARS-CoV-2 in late 2019 and human responses to the resulting COVID-19 pandemic in early 2020 have rapidly changed many aspects of human behavior, including our interactions with wildlife. In this commentary, we identify challenges and opportunities at human–primate interfaces in light of COVID-19, focusing on examples from Asia, and make recommendations for researchers working with wild primates to reduce zoonosis risk and leverage research opportunities. First, we briefly review the evidence for zoonotic origins of SARS-CoV-2 and discuss risks of zoonosis at the human–primate interface. We then identify challenges that the pandemic has caused for primates, including reduced nutrition, increased intraspecific competition, and increased poaching risk, as well as challenges facing primatologists, including lost research opportunities. Subsequently, we highlight opportunities arising from pandemic-related lockdowns and public health messaging, including opportunities to reduce the intensity of problematic human–primate interfaces, opportunities to reduce the risk of zoonosis between humans and primates, opportunities to reduce legal and illegal trade in primates, new opportunities for research on human–primate interfaces, and opportunities for community education. Finally, we recommend specific actions that primatologists should take to reduce contact and aggression between humans and primates, to reduce demand for primates as pets, to reduce risks of zoonosis in the context of field research, and to improve understanding of human–primate interfaces. Reducing the risk of zoonosis and promoting the well-being of humans and primates at our interfaces will require substantial changes from “business as usual.” We encourage primatologists to help lead the way.     

Behavioral Aspects of Rodent Population Biology

Five approaches to the study of behavior as a factor in thepopulation biology of rodents are outlined. These approachesare: (1) genetics, (2) physiology, (3) chronobiology,(4) behavioralecology and sociobiology, and (5) the use of intra- and inter-specificcomparisons. For each approach selected examples from the recentliterature, from this symposium and from my own work are usedto illustrate the new directions that are emerging for analyzingbehavior as a factor affecting natality, mortality and emigration/immigrationin rodents. Areas where additional investigations are neededare noted including some questions to be tested by future experiments.A variety of new techniques that have been developed or areinnovative applications of existing techniques are incorporatedinto the examples. Most of the material presented concerns fourgenera of rodents, Microtus, Mus, Peromyscus, and Rattus. Thefollowing major conclusions emerge from an overview of theseapproaches: Most recent research on behavior as a factor inrodent population biology has been concerned primarily withnatality. Few investigators have dealt with mortality and onlya limited number have explored emigration/immigration. Fieldand laboratory studies on behavioral aspects of rodent populationbiology have become more integrated than they were several decadesago. Both proximate and ultimate questions about behavior andpopulation dynamics are now being tested by both laboratoryand field methods. In contrast to some earlier approaches thatoften viewed population control as involving a single factor,most emerging conceptual frameworks have, as a major assumption,that population regulation is a multi-factorial process includingmany behavioral components.     

Gestural communication in young gorillas (Gorilla gorilla): gestural repertoire,learning, and use

In the present study we investigated the gestural communication of gorillas (Gorilla gorilla). The subjects were 13 gorillas (1-6 years old) living in two different groups in captivity. Our goal was to compile the gestural repertoire of subadult gorillas, with a special focus on processes of social cognition, including attention to individual and developmental variability, group variability, and flexibility of use. Thirty-three different gestures (six auditory, 11 tactile, and 16 visual gestures) were recorded. We found idiosyncratic gestures, individual differences, and similar degrees of concordance between and within groups, as well as some group-specific gestures. These results provide evidence that ontogenetic ritualization is the main learning process involved, but some form of social learning may also be responsible for the acquisition of special gestures. The present study establishes that gorillas have a multifaceted gestural repertoire, characterized by a great deal of flexibility with accommodations to various communicative circumstances, including the attentional state of the recipient. The possibility of assigning Seyfarth and Cheney's [1997] model for nonhuman primate vocal development to the development of nonhuman primate gestural communication is discussed.     

Changing Assumptions in Primate Ecology

Ecological research on nonhuman primates developed separately from the discipline of ecology as a whole, and has in the past been characterized by a distinctive set of goals and assumptions. This paper examines some of the problems surrounding these assumptions. Recently, primate ecologists have begun to adopt the conceptual framework of other ecologists; it is argued here that this trend does not in fact solve all the old problems. Finally, the future of primate ecology is considered briefly . [Primates, ecology, adaptation, strategies, optimization]     

Preserving Preuss’s Red Colobus (<Emphasis Type="Italic">Piliocolobus preussi</Emphasis>): an Ethnographic Analysis of Hunting,Conservation, and Changing Perceptions of Primates in Ikenge-Bakoko,Cameroon

The futures of nonhuman primate species and human communities in shared landscapes rely on our ability to engage with and understand the complex histories and multiscalar aspects of human–animal relationships. We use the Critically Endangered Preuss’s red colobus (Piliocolobus preussi) as a case study to examine the important ways in which histories of multiscalar human–primate interactions play out in the village of Ikenge-Bakoko, Korup National Park, Cameroon. We contextualize ethnographic and catchment data from adult men (N?=?32) and women (N?=?31) within long-term diurnal primate monitoring datasets to better understand the relationships among hunting practices, local perceptions of diurnal primates, populations of P. preussi, and conservation management. Our data indicate a disconnect between local cultural definitions of “hunter” and Western assumptions as to the makeup and nature of this and other categories. We show that such contradictions can have negative outcomes for conservationists seeking to turn the science of establishing accurate off-take rates of prey species into practical management solutions. Using a single village as a focal point, we highlight the importance of an ethnoprimatological approach to understanding the intricate entanglements among conservation histories, subsistence strategies, and human and nonhuman primate lives. The application of ethnoprimatology is critical for twenty-first century primatologists who must navigate conservation concerns while also acknowledging and valuing the experiences of the human communities living alongside the primates we study.     

Primates got personality,too: Toward an integrative primatology of consistent individual differences in behavior

In recent years, research on animal personality has exploded within the field of behavioral ecology. Consistent individual differences in behavior exist in a wide range of species, and these differences can have fitness consequences and influence several aspects of a species' ecology. In comparison to studies of other animals, however, there has been relatively little research on the behavioral ecology of primate personality. This is surprising given the large body of research within psychology and biomedicine showing that primate personality traits are heritable and linked to health and life history outcomes. In this article, I bring together theoretical perspectives on the ecology and evolution of animal personality with an integrative review of what we know about primate personality from studies conducted on captive, free‐ranging, and wild primates. Incorporating frameworks that emphasize consistency in behavior into primate behavioral ecology research holds promise for improving our understanding of primate behavioral evolution.     

Nonhuman primate transgenesis: progress and prospects

The nonhuman primate is used extensively in biomedical research owing to its close similarities to human physiology and human disease pathophysiology. Recently, several groups have initiated efforts to genetically manipulate nonhuman primates to address complex questions concerning primate-specific development and physiological adaptation. Primates pose unique challenges to transgenesis and, although this field is still in its infancy, the potential for obtaining new insights into primate physiology and gene function is unprecedented. This review focuses on the methods and potential applications of genetically altered nonhuman primates in biomedical research.     

Investigating Niche Construction in Dynamic Human-Animal Landscapes: Bridging Ecological and Evolutionary Timescales

Human influence on the environment is evident at all landscape and ecological scales, from local to global, shaping both abiotic and biotic processes. Niche construction theory provides a means by which to investigate the consequences of these anthropogenic effects, but primatological research has been slow to integrate ecological and evolutionary timelines. We review methods that can be used to study how human niche construction influences nonhuman primates including phenological assessment, nonhuman primate behavioral observations, and ethnographic interview techniques. We argue that this approach provides a starting place to examine niche construction theory but that scholars of primate behavioral ecology must expand our methodologies to bridge the disconnect between ecological and evolutionary research time frames. We suggest areas of research and methods that have been underused but offer opportunities for integrative, innovative research. We conclude that an integrated, synthetic methodological approach is a major goal and that it will likely require a cross-disciplinary, collaborative effort.     

Network measures for dyadic interactions: stability and reliability

Social network analysis (SNA) is a general heading for a collection of statistical tools that aim to describe social interactions and social structure by representing individuals and their interactions as graph objects. It was originally developed for the social sciences, but more recently it was also adopted by behavioral ecologists. However, although SNA offers a full range of exciting possibilities for the study of animal societies, some authors have raised concerns about the correct application and interpretation of network measures. In this article, we investigate how reliable and how stable network measures are (i.e. how much variation they show under re-sampling and how much they are influenced by erroneous observations). For this purpose, we took a data set of 44 nonhuman primate grooming networks and studied the effects of re-sampling at lower re-sampling rates than the originally observed ones and the inclusion of two types of errors, "mis-identification" and "mis-classification," on six different network metrics, i.e. density, degree variance, vertex strength variance, edge weight disparity, clustering coefficient, and closeness centrality. Although some measures were tolerant toward reduced sample sizes, others were sensitive and even slightly reduced samples could yield drastically different results. How strongly a metric is affected seems to depend on both the sample size and the structure of the specific network. The same general effects were found for the inclusion of sampling errors. We, therefore, emphasize the importance of calculating valid confidence intervals for network measures and, finally, we suggest a rough research plan for network studies.