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.     

Trends and developments in physical anthropology, 1990–91

The 1408 members of the American Association of Physical Anthropologists were surveyed by mail regarding professional background, training deficiencies, opinions regarding areas of future importance to the discipline, and teaching/research specializations. A total of 544 responses (39%) resulted; 71% were from professionals in the United States and 16% were from U.S. students. Survey results are compared to surveys done in 1971 and in 1978, and are broken into three cohorts: pre-1971 Ph.D.s, 1972–1978 Ph.D.s, and post-1979 Ph.D.s. Statistics and anatomy continue to be common training deficiencies across cohorts. Molecular/cell biology and writing are new training deficiencies that reflect contemporary concerns and trends in the discipline. Anatomy, genetics, ecology, and paleontology are still considered important to the future of physical anthropology; statistics, computer science, and the biomedical sciences are also thought to be of importance to its future. The most frequent teaching/research specializations are growth and development, evolutionary biology, and population studies. Genetics and primatology appear to be losing popularity; biomedical anthropology, statistics, and ecology appear to be gaining it. The survey results have implications for the future training of graduate students and for employment opportunities in physical anthropology.     

Sampling Effort in Neotropical Primate Diet Studies: Collective Gains and Underlying Geographic and Taxonomic Biases

Primates are among the most observable and best studied mammalian orders, yet the distribution of sampling effort by primatologists has inevitably concentrated on a few genera and a limited number of study sites. We present the first systematic review of sampling effort and associated biases in wild primate field research, focusing on dietary studies across the Neotropics. Our literature review of all 24 neotropical primate ecospecies spans 42 years (1969–2011) and covers 290 dietary studies at 164 study sites across 17 countries. We use a standardized measure of sampling effort to assimilate data sets derived from multiple methodologies and attempt to understand the distribution of effort (total equivalent to 193,804 h) using geographic variables and primate species traits. Results indicate that there are both geographic and taxonomic biases, with sampling effort generally skewed towards large-bodied species occupying large geographic ranges, and concentrated at a select few primatology research hubs. We also note that full primate assemblages at any given study site are rarely investigated. Our assessment thus reveals severely undersampled primate taxa and geographic regions that must be considered in future research. Current biases could be ameliorated by deliberately targeting poorly studied genera anywhere in their geographic distribution, well-studied genera in poorly studied regions, and striving to study multiple sympatric taxa within a single site. Although continued inequalities in sampling effort are probably inevitable, this study shows that this need not inhibit successful compilations and meta-analyses, provided that adequate data on feeding records and sampling effort can be made available.     

Solly Zuckerman: the making of a primatological career in Britain, 1925-1945

Solly Zuckerman's work has been largely dismissed or marginalized by both historians of primatology and primatologists. This paper, using archival and published materials, re-examines both his life and his research into primate sexuality and sociology in the 1920s, endocrinology in the 1930s, and the effects of bomb blast in the 1940s. Despite the many flaws in his work, which is now largely outdated, his career reveals a great deal about the audiences for primatological knowledge in pre-war and wartime Britain; the interlocking circles of the scientific community that impinged on primatology; and competing ideas of what constituted a scientifically correct methodology for the observation of primate behaviour. Also noted is the gap between Zuckerman's self-presentation as the scourge of anthropomorphism and the anthropomorphism of his remarks in private notebooks. Although his work well illustrates familiar themes of patriarchy, military and colonialism in the history of primatology, it also suggests another, underexplored dimension of that science: primatology as an example of cross-species social interaction.     

An academic genealogy on the history of American field primatologists

In this paper, we present the academic genealogy of American field primatologists. The genealogy has been compiled to formally document the historical record of this young field. Data have been collected from three main sources: 1) e-mail surveys, 2) library and Internet research, and 3) verbal communication through forums such as American Association of Physical Anthropology meetings. Lineages of primatologists have been graphically displayed using Microsoft Visio. As of September 2005, 672 names and 239 affiliated universities, organizations and institutions have been recorded in 19 lineages. Five hundred and thirty-eight of the 672 names, 80.1%, are field primatologists. The Hooton/Washburn lineage is the largest; 60.6% of the recorded field primatologists are linked to this lineage. In addition, four of the five professors who have mentored a comparable number of field primatologists at American universities since Washburn are linked to the Hooton/Washburn lineage; and the school where Washburn mentored a majority of his students, UC-Berkeley, continues to have the highest overall graduation record for this subdiscipline. However, the field of primatology has been diversifying since the 1960s, and different universities are now responsible for graduating a substantial number of primatologists. We conclude that while the Hooton/Washburn lineage has remained remarkably homogenous in its anthropological focus, the field is also becoming increasingly enriched by primatologists who have had training in fields such as zoology, psychology, and ecology both in the United States and abroad.     

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.     

Interspecific Interactions between Primates,Birds, Bats,and Squirrels May Affect Community Composition on Borneo

For several decades, primatologists have been interested in understanding how sympatric primate species are able to coexist. Most of our understanding of primate community ecology derives from the assumption that these animals interact predominantly with other primates. In this study, we investigate to what extent multiple community assembly hypotheses consistent with this assumption are supported when tested with communities of primates in isolation versus with communities of primates, birds, bats, and squirrels together. We focus on vertebrate communities on the island of Borneo, where we examine the determinants of presence or absence of species, and how these communities are structured. We test for checkerboard distributions, guild proportionality, and Fox's assembly rule for favored states, and predict that statistical signals reflecting interactions between ecologically similar species will be stronger when nonprimate taxa are included in analyses. We found strong support for checkerboard distributions in several communities, particularly when taxonomic groups were combined, and after controlling for habitat effects. We found evidence of guild proportionality in some communities, but did not find significant support for Fox's assembly rule in any of the communities examined. These results demonstrate the presence of vertebrate community structure that is ecologically determined rather than randomly generated, which is a finding consistent with the interpretation that interactions within and between these taxonomic groups may have shaped species composition in these communities. This research highlights the importance of considering the broader vertebrate communities with which primates co‐occur, and so we urge primatologists to explicitly consider nonprimate taxa in the study of primate ecology. Am. J. Primatol. 75:170‐185, 2013. © 2012 Wiley Periodicals, Inc.     

Primate Conservation: Unmet Challenges and the Role of the International Primatological Society

In the last 40 years, threats to the survival of wild primate populations have greatly increased. Primatologists have long been aware of these threats, and since 1978 have formulated plans to safeguard threatened species. Yet an increasing number of primate species face a high to extremely high risk of extinction. I asked 14 experienced field primatologists for their views on the most serious challenges to more effective primate conservation. They listed habitat loss and hunting as the major direct threats to primate survival, and noted that these activities are driven predominantly by the growth of human populations and the tendency of people to consume resources beyond their immediate survival needs. Two factors identified as most hindering effective action were a lack of political will and insufficient funding, while the main actions recommended to mitigate threats were to undertake more awareness-raising and make protected areas more effective. Such actions have long been recommended, so why have they not worked better? Perhaps the pressures on the natural world are too great to be countered, but I suggest also that too many of the various actors involved in conservation are overly driven by materialism and self-interest. I recommend more attention to the common good and a greater emphasis on the ethical and spiritual reasons for conservation. The International Primatological Society itself could have more vigorous debates on conservation policy at its congresses, and should consider the creation of regional chapters with the aim of promoting primatology in habitat countries.     

Complex societies

The complexity of human societies of the past few thousand years rivals that of social insect societies. We hypothesize that two sets of social “instincts” underpin and constrain the evolution of complex societies. One set is ancient and shared with other social primate species, and one is derived and unique to our lineage. The latter evolved by the late Pleistocene, and led to the evolution of institutions of intermediate complexity in acephalous societies. The institutions of complex societies often conflict with our social instincts. The complex societies of the past few thousand years can function only because cultural evolution has created effective “work-arounds” to manage such instincts. We describe a series of work-arounds and use the data on the relative effectiveness of WWII armies to test the work-around hypothesis. Richerson received his Ph.D. degree in zoology from UC Davis in 1969. He is currently a professor in the Department of Environmental Science and Policy. In addition to his work in cultural evolution, he has worked on the limnology of Lake Tahoe and Clear Lake in California, and on Lake Titicaca in Peru and Bolivia. Boyd received his Ph.D. degree in ecology from UC Davis in 1975, though his thesis work was a resource economics problem. He is currently a professor of anthropology at UCLA. His research interests besides cultural evolution are game theory and a small bit of primatology from time to time.     

Primatology: the beginning

The journal Primates was founded by Kinji Imanishi (1902–1992) in 1957: It is the oldest and longest-running international primatology journal in the world. In this series of dialogues between Tetsuro Matsuzawa, Editor-in-Chief of Primates and the General Director of the Japan Monkey Centre (JMC) and Juichi Yamagiwa, former Editor-in-Chief of Primates and the Museum Director of the JMC, we look back at the achievements of our spiritual ancestors in primate research and talk about the back story of Imanishi and his fellow primatologists: founding the JMC as a research institute focused on primates and launching this journal. What was their motivation? What challenges did they face? What is their continued influence on the field right up to the present? What will be the legacy of our influence on the discipline?     

Primatology in China

China is one of the countries with the greatest diversity of nonhuman primate species: 22 species with 30 subspecies, in 6 genera and 3 families. Primatology in China started in 1862, but fruitful study began only in the 1950s. More than 2,000 academic papers have been published, covering systematics, evolution, ecology, etho-ecology, conservation, reproduction and neuroscience. We review primatology in China over the past century, concentrating mostly on systematics, etho-ecology, conservation and reproduction. We aim to share this information with international colleagues and to seek possibilities for collaboration in the future.     

Identification of 13 Human Microsatellite Markers via Cross-species Amplification of Fecal Samples from Rhinopithecus bieti

Yunnan snub-nosed monkeys (Rhinopithecus bieti) are 1 of 3 snub-nosed monkey species endemic to China. Only ca. 1500 individuals remain in high-altitude forests 3000–4500 m above sea level on the Tibetan Plateau, making them the nonhuman primate living at the highest known elevation. It is one of the most endangered 25 primate species in the world. Proper knowledge of the population genetics and social system of Rhinopithecus bieti will contribute to more appropriate conservation management decisions. Cross-species amplification of human microsatellite loci has facilitated analysis of the population genetics and reproductive strategies of various primate species. We screened 72 human-derived markers to assess their utility in Yunnan snub-nosed monkeys. Thirteen of them produced reliable results and exhibited moderate levels of polymorphism.     

Being human and doing primatology: national, socioeconomic, and ethnic influences on primatological practice

The emerging manifesto, center of the essay collection this commentary is part of, points out that primatology is a primate's science and field of endeavor. It is about primates, and constructed and carried out by primates. But the relationships between different primates involved in primatology cannot be described merely as scientific, zoological, or conservatory. A main point emerging from this perspective is that the relationships amongst primates (as scientists and as subjects) are affected by primatologists' experiences outside of academic science and within the cultural schema that we acquire as members of human societies. My contribution focuses on the primatologists and their sometimes discussed, but too often ignored, cultural and ethnic contexts as influences on how they study, think about, and interact with other primates. In our views and bonds with other primates, do national, class, and ethnic factors count?     

Linking genotypes, phenotypes, and fitness in wild primate populations

In the decade since the first draft of the human genome was announced, genome sequencing projects have been initiated for an additional twenty-some primate species. Within the next several years, genome sequence data will likely become available for all primate genera and for most individuals within some primate populations. At the same time, gene mapping and association studies of humans and other organisms are rapidly advancing our understanding of the genetic bases of behavioral and morphological traits. Primatologists are especially well-placed to take advantage of this coming flood of genetic data. Here we discuss what this new era of primate genomics means for field primatology and highlight some of the unprecedented opportunities it will afford, particularly with regard to examining the genetic basis of primate adaptation and diversity.     

The what and where of primate field research may be failing primate conservation

With approximately 30% of nonhuman primate species listed as critically endangered, the window of opportunity to conserve primates is closing fast. In this article, we focus on the degree to which publications in field primatology are biased in favor of particular taxa and field sites. We examined more than 29,000 peer‐reviewed articles and identified 876 field visits to 349 field sites. We found a highly clumped distribution by site and species. We also examined publication ethical statements and the extent to which they acknowledged local human communities (<5%). Due to a lack of consistency across publications, we provide recommendations for improving ethical statements and for evaluating research impact. Given the plight of primate biodiversity, these results suggest broader coverage of primate species and geographies, as well as more attention to the local human communities whose support is necessary if the intent is to have primate species in the wild in the 22nd century.     

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.     

Reducing the primate pet trade: Actions for primatologists

This commentary emerged from a panel presentation at the International Primatological Society Congress in Nairobi, Kenya, 2018. The goal was to provide regional updates on the status of primate removal from habitat countries, especially for the pet trade, and develop guidelines that could help primatologists address this critical problem. The trade in live primates includes those used as pets, in entertainment, and as subjects of biomedical experimentation, but here we focus on those primates destined for the pet trade. Such transactions are a hugely lucrative business, impacting hundreds of thousands of individuals annually and affecting the survival of wild populations. Being intimately familiar with primate social behavior, life history and biology, primatologists, whether they work with captive or wild primates, are in a unique position to understand the nature of the trade and attempt to counter its effects. In addition to updating the status of the primate pet trade, we provide recommendations that may help primatologists formulate a plan to deal, locally and regionally, with illegal trafficking in live primates. General guidelines include increasing awareness of local customs, policies and laws; developing collaborative research opportunities for local people; engaging in training/informational opportunities; and instructing on how to take action when encountering illegally-trafficked primates.     

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.