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]     

Introduction to the special section: "the effects of bonds between human and nonhuman primates on primatological research and practice"

This commentary introduces this special section on ‘‘the Effects of Bonds Between Human and Nonhuman Primates on Primatological Research and Practice.’’ The aim is to explore the different causes and consequences of bonding experiences between observers and observed in different primatological contexts. In the first contribution, Vitale asks what are the possible consequences of such bonding in behavioral primatology. Examples of beneficial consequences of this kind of relationship come fromstudies on cognitive abilities of great apes. Furthermore, an empathic attitude with the experimental animals leads to better care and attention toward individual welfare needs. Coleman discusses the particular case of nonhuman primates housed in research laboratories. Care-giving practices arediscussed in relation to scientific, ethical and emotional issues. Morimura et al. present the case of the first Japanese sanctuary for retiring chimpanzees from research where, in order to facilitate the social living of re-located chimpanzees, face-to-face interactions between caregivers and chimpanzees areessential. Asquith discusses the role of an thropomorphism, and proposes that this attitude can help to better understand the lives of primates, in more contextualized scenarios. In relation to this view, sheemphasizes how the term ‘‘primate culture’’ accords with some definition of the term ‘‘human culture.’’Fuentes, in his article asks whether national, class and ethnic characteristics can influence bonding between human and nonhuman primates, and calls for focused quantitative studies. Finally, Rose calls for the application of the concept of biosynergy, explained as promoting the formation of healthy and sustainable bonding relationships among living creatures. One of the most important aspects emerging from these papers is the need to better understand whether the issue of bonding in primatological studiescan be generalized to other areas of research such as conservation, behavior, captive care, or whether each of these disciplines needs to develop their own understanding of the effects of bonding in ‘‘producing science.’’     

Jane goodall and the chimpanzees of gombe: An analysis of publications and their impact on teaching science

Five types of introductory university textbooks (N=37) were analyzed for references and citations pertaining to research on wild chimpanzees. Jane Goodall's publications were cited about three times as often as the publications from field sites other than Gombe and approximately five times more often than other Gombe researchers. Biological anthropology textbooks cited Goodall's work most often, followed by textbooks in general anthropology and cultural anthropology. Psychology and biology textbooks cited Goodall least often. Goodall's most comprehensive work, The Chimpanzees of Gombe: Patterns of Behavior (1986), was the most often cited publication about Gombe's apes, and tool-use was the most cited topic. The number of citations to wild chimpanzees tripled from publications in the 1960s to those in the 1980s, suggesting a growing recognition of primatology in the teaching of science.     

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.     

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.     

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.     

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.     

Racism,disadvantage and multiculturalism: towards effective anti-racist praxis

Measuring ethnicity in any society is a challenge. Given world immigration patterns, many countries face a growing dilemma in determining the cultural antecedents of their populations. A further complication is the reality that such determination occurs within the political and nationalistic settings where ethnic‐cultural groups may be potent forces in their own right. As societies mature and evolve, there is an increasing tendency for populations, especially those with many generations of residence in the country, to see themselves as ‘indigenous’ to the society in which they live. Canada is not alone in having to deal with the fluidity of the concept, ‘Canadian’, ‘American’, ‘Australian’, ‘Yugoslav’, and ‘Soviet’ are parallel concepts in other countries of multiple ethnic composition. Using 1991 National Census Test results, the article explores some of the parameters of the indigenous category ‘Canadian’. In particular, the location in Canada and mother tongue of respondents reporting ‘Canadian’ as the ethnic origin of their parents and grandparents or as their own ethnic identity are important indicators for this emerging ethnic category.     

Extending Ethnoprimatology: Human–Alloprimate Relationships in Managed Settings

The majority of studies in ethnoprimatology focus on areas of sympatry where humans and nonhuman primates (hereafter, primates) naturally coexist. We argue that much can be gained by extending the field’s scope to incorporate settings where humans manage most aspects of primates’ lives, such as zoos, laboratories, sanctuaries, and rehabilitation centers (hereafter, managed settings). We suggest that the mixed-methods approach of ethnoprimatology, which facilitates examination of both humans’ and primates’ responses to one another, can reveal not only how humans’ ideas about primates shape management strategies, but also how those management strategies affect primates’ lives. Furthermore, we note that a greater focus on managed settings will strengthen links between ethnoprimatology and primate rights/welfare approaches, and will introduce new questions into discussions of ethics in primatology. For example, managed settings raise questions about when it might be justifiable to restrict primates’ freedom for a “greater good,” and the desirability of making primates’ lives more “natural” even if this would decrease their well-being. Finally, we propose that because ethnoprimatology is premised on challenging false dichotomies between categories of field site—specifically, between “natural” and “unnatural” free-ranging populations—it makes sense for ethnoprimatologists to examine settings in which humans exert considerable control over primates’ lives, given that the distinction between “wild” and “captive” is similarly unclear.     

Origins,Diversity and Relationships of Lemurs

I review new evidence on origins and adaptive radiation of Malagasy lemurs, a remarkably diverse group containing 13% of living primate species. The number of recognized lemur species has increased significantly, partly due to research revealing specific subdivisions within known populations but mainly because of discovery of new populations through fieldwork. Some species feared to be extinct have also been rediscovered. Specific numbers have increased particularly in small-bodied, cryptic genera for which continued research will surely reveal even more species.Adaptative radiation of lemurs has been essentially confined to Madagascar. The high density of lemur species on that island, associated with very small geographical ranges, has major implications both for their evolutionary divergence and for conservation. Reconstructions of phylogenetic relationships among primates have been considerably enhanced by DNA sequence data. Sufficient data are now available from both nuclear and mitochondrial sequences to examine relationships among and within the major groups of living primates. Most studies have confirmed that lemurs constitute a monophyletic sister-group of the lorisiform clade and all exclude a specific relationship between cheirogaleids and lorisiforms repeatedly inferred from morphological evidence. However, some analyses indicate that the aye-aye may have branched away before the divergence between other lemurs and lorisiforms. DNA sequence analyses have also yielded a broad consensus for relationships between Eulemur, Hapalemur, Lemur and Varecia: Varecia branched away first, while Lemur is more closely related to Hapalemur than to Eulemur. As debate about phylogenetic relationships among lemurs and other primates seems to have been settled in favor of lemur monophyly (possibly excluding the aye-aye), only a single invasion of Madagascar is required; but it must still be explained how ancestral lemurs could have migrated there at an appropriate time. Separation between Madagascar and Africa was apparently complete by about 120 Ma, too far in the past for direct overland migration. A recent hypothesis suggested that uplifted land in the Mozambique Channel assisted colonization of Madagascar 26-45 Ma, seemingly agreeing with an estimated date of about 40 Ma for divergence of lemurs from other primates. However, mounting evidence suggests that divergence occurred significantly earlier. Because the earliest known fossil representatives of several modern orders of placental mammals (including primates) are dated no earlier than the early Tertiary, it is widely accepted that their divergence took place after the Cretaceous/Tertiary mass extinction. Yet the known fossil record can only yield minimum divergence times; if sampling is poor and/or biased there may be a considerable discrepancy between minimum and actual dates. There is, for example, virtually no known fossil record for lemurs in Madagascar and the earliest known representatives are subfossil lemurs, so in this case a direct reading of the fossil record would indicate that the lemurs first originated just a few thousand years ago! Examination of underestimation of times of origin because of poor sampling in the fossil record has confirmed previous suggestions that primates originated considerably earlier than generally believed. Several recent phylogenetic reconstructions based on DNA sequence data and using calibration dates derived from groups other than primates provide independent support for this inference. Overall, it now seems that primates originated at around 90 Ma rather than the 55 Ma indicated by direct reading of the known fossil record. Hence, colonization of Madagascar by lemurs would have taken place at about 80 Ma, double the date usually accepted, and should be interpreted in terms of contemporary continental relationships.     

Chemical and physical restraint of nonhuman primates.

Numerous publications on primate restraint and anesthesiology have appeared in recent years. This reflects the striking growth of interest in medical primatology and of efforts to improve restraint agents and methods to facilitate humane use of primates in research. For access to earlier literature, readers should consult recent textbooks [12; 29, pp. 469--474], reviews on chemical or physical restraint [3, 4, 16, 27, 30, 37], and other valuable publications on these subjects that have appeared since 1965 [1, 20, 23, 36, 40, 42]. In this brief review we consider publications, principally since 1971, that deal with chemical or physical restraint. We also present previously unpublished data on the clinical use in primates of CI 744 (Telazol), a new dissociative anesthetic that until recently has been available only for investigational use.     

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.     

The relationships among physical,geometrical and mechanical properties of bone,with a note on the properties of nonhuman primate bone

Since bone reacts to imposed loads by formation and resorption of tissue, analysis of tissue distribution within a bone provides evidence of the adaptation of that bone to a given mechanical function. Definition of these structure-function relationships permits the physical anthropologist to clarify the wide variety of behavioral/morphological adaptations to specific ecological niches in extant primates. From this information, behavior and locomotor function can ultimately be inferred in fossil primates. This paper reviews research which shows the relationships between the physical, geometrical and mechanical properties of bone, so that researchers who are investigating the properties of bone are aware of the numerous interpretations which may be made about structure and function from basic data. In addition, this paper is an attempt to apprise investigators working with primates that comparative data on the properties of primate bone are available, though sparse.     

Yerkes, Hamilton and the experimental study of the ape mind: from evolutionary psychiatry to eugenic politics

Robert Yerkes is a pivotal figure in American psychology and primatology in the first half of the twentieth century. As is well known, Yerkes first studied ape intelligence in 1915, on a visit to the private California laboratory of the psychiatrist Gilbert Hamilton, a former student. Less widely appreciated is how far the work done at the Hamilton lab, in its aims and ambitions as well as its techniques, served as a template for much of Yerkes's research thereafter. This paper uses the Hamilton-Yerkes relationship to re-examine Yerkes's career and, more generally, that of American psychology in the early twentieth century. Three points especially are emphasized: first, the role of Freudian psychoanalysis as a spur to Hamilton's experimental studies of ape intelligence; second, the importance of Hamilton's laboratory, with its semi-wild population of monkeys and ape, as a model for Yerkes's efforts to create a laboratory of his own; and third, the influence on Yerkes of Hamilton's optimism about experimental psychological studies of nonhuman primates as a source of lessons beneficial to a troubled human world.     

灵长类家域的研究

灵长类家域的研究李保国刘安宏（西北大学生物学系,西安７１００６９）（西安市林业局,７１０００３）ＨｏｍｅＲａｎｇｅＳｔｕｄｙｏｆＰｒｉｍａｔｅｓ．￥ＬｉＢａｏｇｕｏ（ＤｅｐａｒｔｍｅｎｔｏｆＢｉｏｌｇｙ,ＮｏｒｔｈｗｅｓｔＵｎｉｖｅｒｓｉｔｙ,Ｘｉａ...     

The Politics Of Resemblance: Ethnicity, Trademarks, Head-Hunting

This article questions the assumption that shared culture, or affiliation to shared cultural symbols, is necessarily a source of social cohesion, and that ethnic divisions are associated specifically with perceptions or attributions of difference. I argue that shared cultural symbolism can give rise to competition over its ownership or use, and that this competition can play an important role in defining ethnic boundaries, by creating what might be called relationships of conflictual resemblance between the two sides. Such conflicts are analogous in a number of respects to disputes over the ownership and use of commercial trademarks, and reveal the same underlying conceptions of 'proprietary' identity.     

The evolution and cultural transmission of percussive technology: integrating evidence from palaeoanthropology and primatology

We bring together the quite different kinds of evidence available from palaeoanthropology and primatology to better understand the origins of Plio-Pleistocene percussive technology. Accumulated palaeoanthropological discoveries now document the Oldowan Complex as the dominant stone tool making culture between 2.6–1.4 Ma, the earlier part of this contemporaneous with pre-Homo hominins. The principal types of artefacts and other remains from 20 Early Stone Age (Oldowan and earliest Acheulean) localities in Africa and elsewhere are reviewed and described. To better understand the ancestral behavioural foundations of this early lithic culture, we examine a range of recent findings from primatology. In particular, we attempt to identify key shared characteristics of Homo and Pan that support inferences about the preparedness of our common ancestor for the innovation of stone tool culture. Findings of particular relevance include: (i) the discovery of an expanding repertoire of percussive and other tool use based on directed use of force among wild chimpanzees, implicating capacities that include significant innovatory potential and appreciation of relevant causal factors; (ii) evidence of material cultural diversity among wild chimpanzees, indicating a readiness to acquire and transmit tool use innovations; and (iii) experimental studies of social learning in chimpanzees and bonobos that now encompass the acquisition of nut cracking through observation of skilled use of hammers and anvils by conspecifics, the diffusion within and between groups of alternative styles of tool use, and the adoption of free-hand stone-to-stone percussion to create useful flakes for cutting to gain access to food resources. We use the distributions of the inferred cultural traits in the wild to assess how diffusion relates to geographic distances, and find that shared traits drop by 50% from the approximately eight characteristic of close neighbours over a distance of approximately 700 km. This pattern is used to explore the implications of analogous processes operating in relation to Early Stone Age sites.     

Primate microbial endocrinology: An uncharted frontier

Gut microbial communities communicate bidirectionally with the brain through endocrine, immune, and neural signaling, influencing the physiology and behavior of hosts. The emerging field of microbial endocrinology offers innovative perspectives and methods to analyze host‐microbe relationships with relevance to primate ecology, evolution, and conservation. Herein we briefly summarize key findings from microbial endocrinology and explore how applications of a similar framework could inform our understanding of primate stress and reproductive physiology and behavior. We conclude with three guiding hypotheses to further investigate endocrine signaling between gut microbes and the host: (a) host‐microbe communication systems promote microbe‐mediated stability, in which the microbes are using endocrine signaling from the host to maintain a functioning habitat for their own fitness, (b) host‐microbe communication systems promote host‐mediated stability, in which the host uses the endocrine system to monitor microbial communities and alter these communities to maintain stability, or (c) host‐microbe systems are simply the product of coincidental cross‐talk between the host and microbes due to similar molecules from shared ancestry. Utilizing theory and methodology for studying relationships between the microbiome, hormones, and behavior of wild primates is an uncharted frontier with many promising insights when applied to primatology.     

Breaking Through Disciplinary Barriers: Human–Wildlife Interactions and Multispecies Ethnography

One of the main challenges when integrating biological and social perspectives in primatology is overcoming interdisciplinary barriers. Unfamiliarity with subject-specific theory and language, distinct disciplinary-bound approaches to research, and academic boundaries aimed at “preserving the integrity” of subject disciplines can hinder developments in interdisciplinary research. With growing interest in how humans and other primates share landscapes, and recognition of the importance of combining biological and social information to do this effectively, the disparate use of terminology is becoming more evident. To tackle this problem, we dissect the meaning of what the biological sciences term studies in “human–wildlife conflict” or more recently “human–wildlife interactions” and compare it to what anthropology terms “multispecies ethnography.” In the biological sciences, human–wildlife interactions are the actions resulting from people and wild animals sharing landscapes and resources, with outcomes ranging from being beneficial or harmful to one or both species. In the social sciences, human–nonhuman relationships have been explored on a philosophical, analytical, and empirical level. Building on previous work, we advocate viewing landscapes through an interdisciplinary “multispecies lens” in which humans are observed as one of multiple organisms that interact with other species to shape and create environments. To illustrate these interconnections we use the case study of coexistence between people of the Nalu ethnic group and Critically Endangered western chimpanzees (Pan troglodytes verus) at Cantanhez National Park in Guinea-Bissau, to demonstrate how biological and social research approaches can be complementary and can inform conservation initiatives at the human–primate interface. Finally, we discuss how combining perspectives from ethnoprimatology with those from multispecies ethnography can advance the study of ethnoprimatology to aid productive discourse and enhance future interdisciplinary research.