Moving forward with the primate microbiome: Introduction to a special issue of the American Journal of Primatology

Primate microbiome research is a quickly growing field with exciting potential for informing our understanding of primate biology, ecology, and evolution as well as host‐microbe interactions more broadly. This introductory essay to a special section of the American Journal of Primatology provides a cross‐sectional snapshot of current activity in these areas by briefly summarizing the diversity of contributed papers and their relationships to key themes in host‐associated microbiome research. It then uses this survey as a foundation for consolidating a set of key research questions to broadly guide future research. It also argues for the importance of methods standardization to facilitate comparative analyses and the identification of generalizable patterns and relationships. While primatology will benefit greatly from the integration of microbial datasets, it is uniquely positioned to address important questions regarding microbiology and macro‐ecology and evolution more generally. We are eager to see where the primate microbiome leads us.     

Understanding primate communities: Recent developments and future directions

In 1999, the edited volume Primate Communities presented several studies that examined broad‐scale patterns of primate diversity.¹ Similar studies were being conducted on nonprimate taxa; advances in data availability and statistical approaches were allowing scientists to investigate a variety of new questions and to reexamine classical questions in novel ways. While such studies on nonprimate taxa have continued at a steady pace, they have only crept forward for primate species (Fig. 1 ). In the intervening time, the field of macroecology (Box 1) rapidly developed and has resulted in several books 2 - 4 and the establishment of new research institutes. We suggest that examining primate communities, especially in a macroecological context, is an important line of research for our field to embrace and an area where biological anthropologists can provide major contributions. We review the current state of research, describe new datasets and research tools, and suggest future research directions.     

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.     

Stable nitrogen isotope analysis of dentine serial sections elucidate sex differences in weaning patterns of wild chimpanzees (Pan troglodytes)

Offspring provisioning is one of the most energetically demanding aspects of reproduction for female mammals. Variation in lactation length and weaning strategies between chimpanzees (Pan troglodytes), our closest living relative, and modern human societies have been reported. When and why these changes occurred is frequently debated. Our study used stable nitrogen isotope data of tooth root dentine from wild Western chimpanzees (Pan troglodytes verus) in Taï National Park, Côte d'Ivoire, to quantify weaning in these chimpanzees and explore if infant sex plays a role in maternal investment. We analyzed serial sections of deciduous lateral incisor root dentine from four Taï chimpanzees to establish the δ¹⁵N signal of nursing infants; we then analyzed serial sections of first permanent mandibular molar root dentine from 12 Taï chimpanzees to provide quantitative δ¹⁵N data on weaning in this population. Up to 2 years of age both sexes exhibited dentine δ¹⁵N values ≈2–3‰ higher than adult female Taï chimpanzees, consistent with a nursing signal. Thereafter a steady decrease in δ¹⁵N values consistent with the onset, and progression, of weaning, was visible. Sex differences were also evident, where male δ¹⁵N values decreased at a significantly slower rate compared to females. Confirmation of sex differences in maternal investment among Taï chimpanzees, demonstrates the viability of using isotope analysis to investigate weaning in non‐human primates. Additionally, assuming that behaviors observed in the Taï chimpanzees are illustrative of the ancestral pattern, our results provide a platform to enable the trajectory of weaning in human evolution to be further explored. Am J Phys Anthropol 153:635–642, 2014. © 2013 Wiley Periodicals, Inc.     

The alpha factor and the conquest of Mexico: A study in ethological history

“Alpha behavior” affected human politics and social organization during the sixteenth-century conquest of Mexico by Spanish imperialists. The behavior of Spanish conquistadores is compared to that of other primates in the well-known studies of Jane Goodall and Frans de Waal. Parallels between Spanish and Aztec behavior are also noted so as to identify the shared patterns of behavior that cross human cultures and may be called primate universals. One of these universals is the alpha factor. It administers the social order through the ability to balance benevolence and brutality in order to maintain coalitions and the loyalty of subordinates. The alpha factor is expressed through display behaviors that vary with culture, but all cultures, including those of chimpanzees and bonobos, build around it. It may be tempered by the presence of female coalitions or of a bonobo alpha female, but it is a visible focal point of a society, thereby making display a necessary part of leadership.     

Are Animals Just Noisy Machines?: Louis Boutan and the Co-invention of Animal and Child Psychology in the French Third Republic

Historians of science have only just begun to sample the wealth of different approaches to the study of animal behavior undertaken in the twentieth century. To date, more attention has been given to Lorenzian ethology and American behaviorism than to other work and traditions, but different approaches are equally worthy of the historian’s attention, reflecting not only the broader range of questions that could be asked about animal behavior and the “animal mind” but also the different contexts in which these questions were important. One such approach is that represented by the work of the French zoologist Louis Boutan (1859–1934). This paper explores the intellectual and cultural history of Boutan’s work on animal language and the animal mind, and contextualizes the place of animal behavior studies within late-nineteenth-and early-twentieth-century French biology. I explore the ways in which Boutan addressed the philosophical issue of whether language was necessary for abstract thought and show how he shifted from the idea that animals were endowed with a purely affective language to the notion that of they were capable of “rudimentary” reasoning. I argue that the scientific and broader socio-cultural contexts in which Boutan operated played a role in this transition. Then I show how Boutan’s linguistic and psychological experiments with a gibbon and children provide insights into his conception of “naturalness.” Although Boutan reared his gibbon at home and studied it in the controlled environment of his laboratory, he continued to identify its behavior as “natural.” I specifically demonstrate the importance of the milieu of the French Third Republic in shaping Boutan’s understanding not only of animal intelligence and child education, but also his definition of nature. Finally, I argue that Boutan’s studies on the primate mind provide us with a lens through which we can examine the co-invention of animal and child psychology in early-twentieth-century France.     

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.     

Subsistence Technology of Nigerian Chimpanzees

A trademark of Homo sapiens is the enormous variation in behavioral patterns across populations. Insight into the development of human cultures can be aided by studies on communities of Pan across Africa that display unique combinations of social behavior and elementary technology. Only cross-population comparisons can reveal whether the diversity reflects differential genetics, environmental constraints, or is a cultural variant. However, the recently recognized and most endangered subspecies, Pan troglodytes vellerosus, remains completely unstudied in this respect. We report first evidence from a new long-term study of Nigerian chimpanzees at Gashaka. Their dietary composition is highly varied and they have to cope with high concentrations of antifeedant defenses of plants against consumption. Gashaka chimpanzees use a varied tool kit for extractive foraging. For example, they harvest insects throughout the year, via digging sticks and probes, to obtain honey from stingless-bee and honeybee nests, dipping wands to prey on army ants, and fishing rods to eat arboreal ants. Tools appeared to be custom-made with a considerable degree of standardization in length, diameter, and preferential use of distal ends. Moreover, compared to the rainy season, tools were longer during the dry season when insects retreat further into their nests. Many of the expressions of subsistence technology seem to be environmentally constrained. Most notably, the absence of termite-eating could reflect a low abundance of mounds. Other traits may represent cultural variation. For example, the chimpanzees did not hammer open 2 types of hard-shelled nuts with tools, unlike what occurs elsewhere in West Africa. The prevalence of elementary technology may indicate that the material culture of Gashaka chimpanzees is most related to core cultural tendencies of Central African populations.