Place,Practice and Primatology: Clarence Ray Carpenter,Primate Communication and the Development of Field Methodology, 1931–1945

Place, practice and status have played significant and interacting roles in the complex history of primatology during the early to mid-twentieth century. This paper demonstrates that, within the emerging discipline of primatology, the field was understood as an essential supplement to laboratory work. Founders argued that only in the field could primates be studied in interaction with their natural social group and environment. Such field studies of primate behavior required the development of existing and new field techniques. The practices and sites developed by American primatologist Clarence Ray Carpenter were used to demonstrate that scientific standards could be successfully applied to the study of primates in the field. In an environment in which many field biologists fought for higher scientific status, Carpenter gradually adopted increasingly interventionist techniques. These techniques raised epistemological problems for studies whose value rested on the naturalness of the behaviors observed. Thus, issues of status shaped field practices and subsequently altered Carpenter’s criteria for what constituted natural primate behavior. This article is part of a doctoral dissertation (in progress). This research was supported in part by a Doctoral Dissertation Research Grant and Doctoral Dissertation Fellowship from the University of Minnesota. Georgina (Hoptroff) Montgomery presented earlier versions of this paper at the ISHPSSB conference held in Vienna in July 2003 and at the HSS conference in Boston in November 2003.     

Personality research with non-human primates: theoretical formulation and methods

Since the earliest periods of primatology study, researchers have been aware of animals’ consistent individual differences in behavior or personality. Many papers have been published on this subject, but they lacked a common theoretical and methodological background. The present work is an attempt to provide such theoretical and methodological foundations to this field of biological science. In the theoretical formulation section, “biological study of personality” is first derived as an extension of the ethology paradigm, and non-human primate personality research is subsequently characterized as its strategic component. In the methodology section, brief reviews and discussions are presented on subjective and objective personality assessment methods with non-human primates with a reference to the reliability and validity concepts in human psychometrics. The work provides a theoretical framework and methodological suggestions for non-human primate personality research.     

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.     

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.     

Protein variations and primatology

We summarize work based on electrophoretic screening for protein variation within and between primate species. We consider serum proteins—albumins, haptoglobins, transferrins—and red cell proteins—carbonic anhydrases, hemoglobins. Using hemoglobin, cytochrome-c, and fibrinopeptides as examples, we discuss the value of using molecular data, i.e. protein structures, in evolutionary studies and in primatology.     

Of bonds and boundaries: what is the modern role of anthropomorphism in primatological studies?

Anthropomorphism (and its obverse, zoomorphism) continues to shift and propel us toward changing perspectives on ourselves and other animals. Discussions of anthropomorphism in primate behavior are ostensibly about our use and definition of terms, but ultimately reflect our views of what is unique to humans or unknowable in other animals. Primatologists doing long-term fieldwork report on the bonds that are inevitably formed through familiarity with their study subjects and how anecdotes and anthropomorphism help them to gain a contextualized view of animal lives. This fuller view of animal society serves as an aid to understanding different rationalities and provides a more effective modern role for anthropomorphism than does seeking to demonstrate isomorphic capacities in alloprimates. Although most ordinary language terms are accepted among primatologists, "primate culture" serves as an example of a term and a concept that overreached acceptable anthropomorphic limits when defined to accord with definitions of modern human culture. Comparing similar behavioral forms as the product of similar selective pressures acting on specific early traits, producing homoplasies through convergent evolution, provides a nonanthropomorphic basis for seeking similarities in human and alloprimate behavior.     

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.     

The promise of primatology fulfilled?

In 1972, Sherwood Washburn, one of the forerunners of biological anthropology, gave an invited address during the 4th Congress of the International Primatological Society in Portland, Oregon, in which he expounded his vision for the field of primatology. His address was published the following year in the American Journal of Physical Anthropology and titled: “The promise of primatology.” In this centennial commentary, we revisit Washburn's “promise”, 45 years on. His address and article discuss the constraints acting on the field, including a positioning of the discipline across different kinds of university departments, and within the social sciences, which he viewed as a mixed blessing. Prescient aspects of Washburn's address include a focus on the need to study communication multimodally, and a hope that the study of mechanisms would become foundational within the field. We discuss new promising aspects of primatology, focusing on technological advances in a number of areas highlighted by Washburn that have ushered in new eras of research, and the increasingly large number of long‐term field sites, which see the discipline well‐set for new developmental and longitudinal studies. We find much to admire in Washburn's keen foresight, and natural intuition. Washburn hoped that primatology would repudiate the notion that “the social should be studied without reference to the biological.” In this regard, we consider much of Washburn's promise fulfilled.     

Anthropomorphism,primatomorphism, mammalomorphism: understanding cross-species comparisons

The charge that anthropomorphizing nonhuman animals is a fallacy is itself largely misguided and mythic. Anthropomorphism in the study of animal behavior is placed in its original, theological context. Having set the historical stage, I then discuss its relationship to a number of other, related issues: the role of anecdotal evidence, the taxonomy of related anthropomorphic claims, its relationship to the attribution of psychological states in general, and the nature of the charge of anthropomorphism as a categorical claim. I then argue that the categorical reading of anthropomorphism cannot work and that it misrepresents what is being claimed when one claims that traits are shared between humans and nonhumans. We should think of such claims not as anthropomorphic per se– because that implies the trait is intrinsically human and only derivatively nonhuman. Instead, traits shared with mammals are mammalomorphic, for example, or primatomorphic when shared by primates.     

Extant primates and development of primatology in China: Publications,student training,and funding

China supports the richest non-human primate diversity in the northern hemisphere, providing an excellent opportunity for Chinese primatologists to take a leading role in advancing the study of primatology.Primatology in China began to flourish after 1979. To date, Chinese primatologists have published more than 1 000 papers in journals indexed by the Chinese Science Citation Database and the Web of Science Core Collection, and universities and academic institutions have trained 107 PhD students and 370 Masters students between 1984 and 2016. In total,the National Science Foundation of China has funded129 primate projects(RMB 71.7 million) supporting 59 researchers from 28 organizations. However, previous research has also shown obvious species bias.Rhinopithecus roxellana, Rhinopithecus bieti, and Macaca mulatta have received much greater research attention than other species. Researchers have also tended to continue to study the same species(55.2%)they studied during their Ph D training. To promote the development of primatology in China, we suggest(1)the need for a comprehensive primatology textbook written in Chinese,(2) continued training of more Ph D students, and(3) encouragement to study less well-known primate species.     

The road less traveled: Phylogenetic perspectives in primatology

Interest in phylogeny is increasing in many areas of evolutionary biology. One area of evolutionary anthropology that has not yet fully embraced this growth in phylogenetic thinking, however, is the study of primate behavior and ecology.¹ The predominant framework for behavioral studies of primates over the last three decades has been socioecological. The goals have been to identify broad correlations between species' behaviors and current environmental conditions. As such, the socioecological approach has been largely nonhistorical, taking little account of phylogeny. In contrast, phylogenetic approaches view the behavior of contemporary taxa within an explicitly historical framework. Although socioecology has proven extremely productive, there are many reasons to think that research in primatology could be profitably supplemented by a phylogenetic perspective.^2,3     

Primate Behavioral Ecology: From Ethnography to Ethology and Back

Nonhuman primates occupy a special niche in anthropology because of the comparative insights into humans they provide. Initial anthropological interest in primates targeted the apes for their close phylogenetic relationships with humans, and the semiterrestrial Old World monkeys for their ecological similarities with hominids adapting to life on the ground. From the earliest anecdotal reports of tool use and hunting to more contemporary quantitative analyses of local "cultural" traditions, nonhuman primates have challenged deep-rooted concepts of human uniqueness and redefined the boundaries between us and other animals. Yet, despite the long-standing influence of primate studies in anthropology, approaches to studying primates began diverging from those of earlier ethnographers. Advances in primatology, particularly during the 1990s, have included a much deeper understanding of how ecology, phylogeny, and demography affect behavior. Insights into intraspecific, population-level variation represent an important area of convergence between primatology, other areas of anthropology, and conservation biology. [Keywords: primate behavioral ecology, anthropocentrism, evolutionary theory, systematic methods, biology]     

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 subspecies concept in primatology: The case of mountain gorillas

The criteria for the application of subspecific units in living primate populations have received little attention relative to other vertebrate taxa, even though they have important implications for conservation strategies for many nonhuman primate populations. One of the most critically endangered primates is the mountain gorilla,Gorilla gorilla beringei, of which 600 animals exist in east-central Africa. FollowingSarmiento et al. (1996), taxonomists have proposed splitting these populations into two subspecies as part of a revised taxonomy of the genusGorilla. In this paper I review the application of the subspecies concept in primatology, using the gorillas of Bwindi Impenetrable National Park and the Virungas as case studies. An examination of genetic, morphological, biogeographic, ecological, and behavioral evidence indicates that reclassifying Bwindi gorillas as taxonomically distinct from those in the Virungas is not well supported and needs further study. Because taxonomy provides the basis of conservation management policies, a cautious and conservative approach to the subspecies question is warranted in the case of endangered primate populations.     

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?     

The importance of fallback foods in primate ecology and evolution

The role of fallback foods in shaping primate ranging, socioecology, and morphology has recently become a topic of particular interest to biological anthropologists. Although the use of fallback resources has been noted in the ecological and primatological literature for a number of decades, few attempts have been made to define fallback foods or to explore the utility of this concept for primate evolutionary biologists and ecologists. As a preface to this special issue of the American Journal of Physical Anthropology devoted to the topic of fallback foods in primate ecology and evolution, we discuss the development and use of the fallback concept and highlight its importance in primatology and paleoanthropology. AmJ Phys Anthropol 140:599–602, 2009. © 2009 Wiley-Liss, Inc.     

Adaptive signincance of infanticide in primates

Interpretation of the adaptive significance of infanticide has been one of the most controversial topics in recent primatology. Infanticide has so far been observed in natural populations of ten primate species. Accumulating evidence now suggests that it may have different functions in different species.     

The current status of evidence for and against postnatal oogenesis in mammals: a case of ovarian optimism versus pessimism?

Whether or not oogenesis continues in the ovaries of mammalian females during postnatal life was heavily debated from the late 1800s through the mid-1900s. However, in 1951 Lord Solomon Zuckerman published what many consider to be a landmark paper summarizing his personal views of data existing at the time for and against the possibility of postnatal oogenesis. In Zuckerman's opinion, none of the evidence he considered was inconsistent with Waldeyer's initial proposal in 1870 that female mammals cease production of oocytes at or shortly after birth. This conclusion rapidly became dogma, and remained essentially unchallenged until just recently, despite the fact that Zuckerman did not offer a single experiment proving that adult female mammals are incapable of oogenesis. Instead, 20 years later he reemphasized that his conclusion was based solely on an absence of data he felt would be inconsistent with the idea of a nonrenewable oocyte pool provided at birth. However, in the immortal words of Carl Sagan, an "absence of evidence is not evidence of absence." Indeed, building on the efforts of a few scientists who continued to question this dogma after Zuckerman's treatise in 1951, we reported several data sets in 2004 that were very much inconsistent with the widely held belief that germ cell production in female mammals ceases at birth. Perhaps not surprisingly, given the magnitude of the paradigm shift being proposed, this work reignited a vigorous debate that first began more than a century ago. Our purpose here is to review the experimental evidence offered in recent studies arguing support for and against the possibility that adult mammalian females replenish their oocyte reserve. "Never discourage anyone who continually makes progress, no matter how slow."-Plato (427-347 BC).     

A Global-Scale Evaluation of Primate Exposure and Vulnerability to Climate Change

Human-induced climate change poses many potential threats to nonhuman primate species, many of which are already threatened by human activities such as deforestation, hunting, and the exotic pet trade. Here, we assessed the exposure and potential vulnerability of all nonhuman primate species to projected future temperature and precipitation changes. We found that overall, nonhuman primates will experience 10 % more warming than the global mean, with some primate species experiencing >1.5 °C for every °C of global warming. Precipitation changes are likely to be quite varied across primate ranges (from >7.5 % increases per °C of global warming to >7.5 % decreases). We also identified individual endangered species with existing vulnerabilities (owing to their small range areas, specialized diet, or restricted habitat use) that are expected to experience the largest climate changes. Finally, we defined hotspots of primate vulnerability to climate changes as areas with many primate species, high concentrations of endangered species, and large expected climate changes. Although all primate species will experience substantial changes from current climatic conditions, our hotspot analysis suggests that species in Central America, the Amazon, and southeastern Brazil, as well as portions of East and Southeast Asia, may be the most vulnerable to the anticipated impacts of global warming. It is essential that impacts of human-induced climate change be a priority for research and conservation planning in primatology, particularly for species that are already threatened by other human pressures. The vulnerable species and regional hotspots that we identify here represent critical priorities for conservation efforts, as existing challenges are expected to become increasingly compounded by the impacts of global warming.