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Beyond Neutrality: the Human–Primate Interface During the Habituation Process

October 2018
International Journal of Primatology 39(6)

DOI:10.1007/s10764-017-0009-3

Authors:

Katherine T. Hanson

University of Texas at San Antonio

Erin P. Riley

San Diego State University

Ethnoprimatology explores the ecological, social, and cultural interconnections between humans and other primates. Since the field’s emergence, researchers have examined overlapping human–primate resource use and conflict, human–primate disease transmission, primate folklore and its influence on conservation status, and primate tourism. One facet of the human–primate interface that remains underexplored from an ethnoprimatological perspective is habituation. Habituation—defined as when wild animals accept a human observer as a neutral element of their environment—has long been considered a critical first step for successful primate fieldwork. Although primatologists have explored how to accomplish habituation, little attention has been paid to habituation as a mutually modifying process that occurs between human observers and their primate study subjects. By drawing on the ethnoprimatological approach and engaging with perspectives from human–animal studies, this manuscript examines habituation as a scientific and intersubjective process. Over seven months, we documented behavioral changes in moor macaques (Macaca maura) and human participants that occur during habituation. We also conducted interviews with researchers and local field assistants to track perceptions of habituation progress. Integrating ethological measures with ethnographic material enabled us to explore how and why quantitative markers of habituation “success” differ from subjective impressions, observe habituation—and primate fieldwork in general—as a bidirectional, intersubjective experience, and come to understand habituation as a dynamic spectrum of tolerance rather than a state to be “achieved.” Collectively, these findings have important implications for future work in ethnoprimatology and habituation methodology, as well as the practice of primate fieldwork.

Tower karst in the home range of an unhabituated group of moor macaques, Bantimurung–Bulusaraung National Park, South Sulawesi, Indonesia. (Photo: Indra Pradana).

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Park ranger sitting near a habituated study group (group B) of moor macaques in Bantimurung–Bulusaraung National Park, South Sulawesi, Indonesia. (Photo: Kate Jameson).

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Percentage of different types of encounters between moor macaques and observers across 138 h, divided into six equal time periods, Bantimurung–Bulusaraung National Park, July 14, 2014–January 25, 2015.

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Search time for a group of moor macaques across 138 h, divided into six equal time periods, Bantimurung–Bulusaraung National Park, July 14, 2014–January 25, 2015.

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Mean minimum distance (meters) between observers and two groups of moor macaques in Bantimurung–Bulusaraung National Park, South Sulawesi, Indonesia, July 14, 2014–January 25, 2015. Each period represents one-sixth of the total time spent in contact with each study group.

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Katherine T. Hanson

&Erin P. Riley

Received: 31 July 2017 / Accepted: 13 October 2017 / Published online: 27 December 2017

#Springer Science+Business Media, LLC, part of Springer Nature 2017

Abstract Ethnoprimatology explores the ecological, social, and cultural interconnec-

tions between humans and other primates. Since the field’s emergence, researchers

have examined overlapping human–primate resource use and conflict, human–primate

disease transmission, primate folklore and its influence on conservation status, and

primate tourism. One facet of the human–primate interface that remains underexplored

from an ethnoprimatological perspective is habituation. Habituation—defined as when

wild animals accept a human observer as a neutral element of their environment—has

long been considered a critical first step for successful primate fieldwork. Although

primatologists have explored how to accomplish habituation, little attention has been

paid to habituation as a mutually modifying process that occurs between human

observers and their primate study subjects. By drawing on the ethnoprimatological

approach and engaging with perspectives from human–animal studies, this manuscript

examines habituation as a scientific and intersubjective process. Over seven months, we

documented behavioral changes in moor macaques (Macaca maura) and human

participants that occur during habituation. We also conducted interviews with re-

searchers and local field assistants to track perceptions of habituation progress. Inte-

grating ethological measures with ethnographic material enabled us to explore how and

why quantitative markers of habituation Bsuccess^differ from subjective impressions,

observe habituation—and primate fieldwork in general—as a bidirectional, intersub-

jective experience, and come to understand habituation as a dynamic spectrum of

tolerance rather than a state to be Bachieved.^Collectively, these findings have

important implications for future work in ethnoprimatology and habituation method-

ology, as well as the practice of primate fieldwork.

Int J Primatol (2018) 39:852–877

https://doi.org/10.1007/s10764-017-0009-3

Handling Editor: Joanna M. Setchell

*Katherine T. Hanson

kth621@gmail.com

Department of Anthropology, San Diego State University, San Diego, CA 92182, USA

Beyond Neutrality: the Human–Primate Interface

During the Habituation Process

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Perspectives on the Continuum of Wild to Captive Behaviour

Chapter

Jan 2023

Historically, we have characterized the environments primates live in and that we observe them in as ‘wild’ and ‘captive’. We assumed that primates exhibited ‘natural’ behaviour in the ‘wild’, whereas ‘captive’ behaviour was an ‘unnatural’ artefact of human management. This view later expanded to consider the influence of anthropogenic activities on wild primates, and the distinctions of free-ranging, provisioned animals and enriched naturalistic environments. However, these dichotomies remain. Here, we suggest primate environments should be considered a continuum, ranging from intact primary forest to heavily managed captive environments. Across this continuum, the behaviour we observe is a flexible response to ecological conditions shaped by human presence. Rather than viewing wild behaviour as natural, and captive behaviour as an artificial reaction to human management, recognition of how humans shape primates’ environments across contexts improves our understanding of primate behaviour and evolution. Even the “wildest” primates’ lives are altered and influenced by humans, and the behaviour of intensely managed captive primates reflects species-level behavioural flexibility and individual responses. Beyond the indirect effects of anthropogenic pressures and management, the behaviour we observe is responsive to human observation and interaction. Whether the presence of researchers following primates, the presence of local people encountering primates in daily activity, or humans caring for primates in managed environments, these observer effects influence behaviour. Recognizing how observations are shaped by anthropogenic and observer effects across the continuum of primate habitats allows us to identify how co-evolutionary pressures shape the evolution of primate socioecology and socioecological flexibility of primates.

Encountering Sulawesi’s Endemic Primates: Considerations for Developing Primate Tourism in South Sulawesi, Indonesia

Chapter

Full-text available

Nov 2022

The island of Sulawesi, Indonesia is renowned as a birder and diver’s paradise, attracting tourists from around the globe who seek to encounter rare bird species or abundant and unusual marine life. In contrast to other areas of Indonesia (e.g., Bali and Kalimantan), Sulawesi is less known for its primate tourism opportunities, despite being home to at least 14 endemic primate species. In this chapter, we explore the possibilities and requisite considerations for developing primate tourism in South Sulawesi, a region of the island with minimal established tourism infrastructure. We argue that cautious, thoughtful, and collaborative development of primate tourism in South Sulawesi have the potential to raise awareness of local primate biodiversity and conservation issues, supplement and diversify local livelihoods, curb the acceleration of extractive industries, and provide a valuable contrast to other primate tourism sites across Indonesia. Though the aim of this chapter is to open a dialogue among local stakeholders and international practitioners regarding responsible development of primate tourism in South Sulawesi specifically, the considerations raised here are relevant in other regions where formal primate tourism remains underdeveloped. In particular, we encourage the consideration of existing dimensions of human-nonhuman primate coexistence (including conflict), tourism audiences, and the degree of local engagement from diverse stakeholders.

Detection of viruses from feces of wild endangered Macaca maura: a potential threat to moor macaque survival and for zoonotic infection

Article

Full-text available

Nov 2022
BMC Vet Res

Background To date, there is a scarcity of information and literature on Macaca maura health status relative to viral diseases. The objectives of the present study were to investigate on the potential spread of enteric and non-enteric viruses shed in the environment through a wild macaque feces and to understand the possible interrelation in the spread of zoonotic viruses in a poorly studied geographical area, the Sulawesi Island. This study will also contribute providing useful information on potential threats to the health of this endangered species. Methods The sampling was conducted between 2014 and 2016 in the Bantimurung Bulusaraung National Park, in the south of the Sulawesi Island and non-invasive sampling methods were used to collect fresh stools of the M. maura, one of the seven macaque species endemic to the island of Sulawesi, Indonesia. The population under study consisted in two wild, neighboring social macaque groups with partially overlapping home ranges; twenty-four samples were collected and examined using negative staining electron microscopy and a panel of PCR protocols for the detection of ten RNA and two DNA viruses. Results Viral particles resembling parvovirus (5 samples), picornavirus (13 samples) and calicivirus (13 samples) were detected by electron microscopy whereas the PCR panel was negative for the 12 viruses investigated, except for one sample positive for a mosquito flavivirus. The results did not correlate with animal sex; furthermore, because all of the animals were clinically healthy, it was not possible to correlate feces consistency with viral presence. Conclusions As information on viral infections in wild moor macaques remains limited, further studies are yet required to identify the fecal–oral and blood transmitted potentially zoonotic viruses, which may infect the moor macaque and other macaque species endemic to the South Sulawesi Island.

Primate Portrayals: Narratives and Perceptions of Primates in Entertainment

Chapter

Jan 2023

Across the globe and across time, primates have been used in live performances and depicted through imagery to entertain audiences and tell stories. Technological advances have led to a proliferation of ways in which we consume media and with that, audiences for primates in entertainment have flourished. Here we review some of the ways primates are used as entertainers and examine representations of primates in contemporary media. We provide an overview of the role of primates in the entertainment industry and discuss issues of animal welfare and conservation. An understanding of the history primates in media and entertainment is critical to regulating these practices and ensuring the health and welfare of both humans and animals.

Primate Tourism

Chapter

Jan 2023

Primate tourism, where people travel and see non-human primates, is a rapidly growing activity. This chapter introduces the history and the multidimensions of primate tourism across the world. We then focus on tourism associated with wild primate viewing and assess the costs and benefits of primate tourism related to habitat protection, revenue generation, co-existence with local communities, knowledge sharing, provisioning, health and habituation. Following this assessment, we explore the different drivers for human-primate interactions associated with primate tourism. This chapter concludes by summarising responsible primate tourism guidelines.

The Past, Present, and Future of the Primate Pet Trade

Chapter

Jan 2023

Pet primates are those kept typically for companionship, enjoyment, and status, although their uses as pets may extend beyond these parameters. The trade in pet primates is historically rooted, with many primates playing important roles in human cultures and religions. Thus, it is not surprising that current sociocultural trends reveal an ongoing fascination with primates and their purchase as status pets. Recent reports from various regions are presented in this chapter, demonstrating the need for drastic interventions to avoid further losses. Capture of animals for the pet trade may be intentional or opportunistic and is often exacerbated by internet trade and social media. This situation is complicated by the difficulty of obtaining accurate numbers of primates bought and sold illegally. The health and welfare of primates captured or kept as pets is another area of great concern. Long-term solutions will require attention from governmental, professional, and public actors on local and international levels.

Shared Ecologies, Shared Futures: Using the Ethnoprimatological Approach to Study Human-Primate Interfaces and Advance the Sustainable Coexistence of People and Primates

Chapter

Jan 2023

Ethnoprimatology is a research approach used to study the diverse ways that human and other primates’ lives and livelihoods intersect. Our objective in this chapter is to illustrate the use and value of ethnoprimatology in studying human-primate interfaces across both time and space. We begin by clarifying how human-primate interfaces occur across a gradient from rural to urban landscapes and illustrate how the ethnoprimatological approach is implemented. We showcase how ethnoprimatology’s theoretical and methodological landscape has expanded since its emergence in the late 1990s to include the integration of frameworks and tools from the natural and social sciences and the humanities. To illustrate the practice of ethnoprimatology, we highlight research conducted on the human-primate interface across three geographies of human-primate encounters: tourism sites, urban and peri-urban settings, and agroecosystems. We conclude by showing how the human-primate interconnections uncovered by ethnoprimatology have important implications for conservation, management of human-primate interfaces, and the sustainable coexistence of multispecies communities in the contemporary era.

Rethinking Tolerance to Tourism: Behavioral Responses by Wild Crested Macaques (Macaca nigra) to Tourists

Chapter

Nov 2022

There is an assumption that apparent tolerance of tourists at long-running primate tourism sites indicates habituation and that as a result primates no longer experience negative consequences of prolonged exposure to visitors. We examined effects of tourist presence on stress-related behavior in three groups of critically endangered, wild crested macaques (Macaca nigra) exposed to different intensities of tourism in Tangkoko Nature Reserve, Sulawesi, Indonesia. Group R2 has been exposed to research + intensive tourism for over 3 decades, R1 to research + less intensive tourism (1 decade), and PB1 to research only. Almost 740 h of data were collected from 33 adults via focal animal, all occurrence, and 1/0 sampling. All data were analyzed with general linear mixed models. Behavior appeared to be inhibited when tourists were in the forest, but not within groups; all groups vocalized less, exhibited fewer sexual behaviors and displayed fewer self-directed behaviors in months with greater numbers of tourists. When tourists were present vs. absent within groups, females displayed less affiliation, and males and females displayed more aggression, consistent with responses to uncertainty in the presence of tourists. Our results indicate that crested macaque groups exposed to tourism even for decades may not fully habituate to tourists. We tentatively suggest that their behavioral responses to tourists resemble typical responses of primates to perceived predators posing varying degrees of risk.

The Habit in Cohabitation: (Or, How to Meet a Tiger on the Path)

Article

Full-text available

Oct 2022

Kath Weston

As human and nonhuman animals increasingly share space, however enthusiastically or reluctantly, the concepts of habit, cohabitation, and habituation bear further scrutiny when applied to these makeshift arrangements. Even when researchers have critically examined the work these terms do in discussions of more-than-human relations, they have tended to ignore the temporalities embedded in "habit" and its cognates. A discourse of habit traps animals in an ethnographic present of the sort long critiqued within anthropology in its application to humans. One alternative is to approach more-than-human animals as what Mahesh Rangarajan calls "animals with histories," instead of treating them as members of species with fairly set characteristics who make cameo appearances in ecological histories, ethnographies, and field studies. Studies of human-tiger relations in Rajasthan, India, and auto-ethnographic material on human-bear relations in Alaska suggestively illustrate what a historical orientation has to offer by way of moving discussions of multispecies relations beyond a colonial discourse of encounter and the blurring of human/nonhuman boundaries. Acknowledgment that nonhuman animals have historically inflected backstories, even when their memories and experiences are not accessible to humans, is a step in the direction of more expansive possibilities for co-worlding.

Feral and out of control: a moral panic over free-roaming cats?

Chapter

Full-text available

Oct 2022

Kristine Hill

Lynn et al., (2019) accused fellow scientists of misrepresenting free-roaming cats (Felis catus) by framing them as a global threat to biodiversity, rather than a localised threat to specific ecosystems. These authors asserted that the narrative created a ‘moral panic’ over free-roaming cats, which is escalated by emotive journalistic pieces read by audiences around the world. To test this empirically, I performed a thematic discourse analysis of user comments responding to five news articles, a magazine, and a YouTube video related to the topic of freeroaming cats. The discourses examined flow between conservationists, the media, and the public, and reflect the confused and convoluted ways in which people think about cats. Here I discuss how well the data fits the moral panic theory. I analyse how labels such as ‘feral’ serve to ‘other’ cats, rendering them objects of distain and creating ‘folk devils’ that are deemed more killable than beloved companion animals of the same species.

Primates Watching Primates Watching Primates: An Ethnoprimatological Account of the Habituation Process in Moor Macaques (Macaca Maura)

Thesis

Full-text available

Jan 2017

Katherine T. Hanson

Ethnoprimatology is the study of the ecological and cultural interconnections between human and nonhuman primates. Since the field’s emergence, ethnoprimatologists have examined overlapping human-primate resource use and conflict, human-primate disease transmission, primate folklore and its impact on conservation status, and primate tourism. In order to address such multifaceted topics, ethnoprimatologists deploy diverse methods from ecology, ethology, and cultural anthropology. Similarly, the recent “animal turn” within cultural anthropology, sociology, and geography articulates the use of hybrid methodologies to shed light on the intertwined social realms of humans and other animals. By drawing on the ethnoprimatologial approach and engaging with perspectives from human-animal studies, this thesis examines habituation, a process by which wild animals learn to accept human observers as neutral elements in their environment. Primatologists have previously investigated appropriate habituation methods, observer effects on habituated primate behavior, and habituation’s ethical implications. However, despite habituation’s role as a hallmark of field primatology, it has received little empirical attention, particularly with regard to the intersubjective nature of the process; that is, as a mutually modifying experience for both primatologists and their study groups. My primary objective was therefore to explore habituation as both a scientific and subjective process by integrating quantitative behavioral measures with qualitative perceptions of habituation “success.” Accordingly, I assessed progress in habituating a group of wild moor macaques from two perspectives: 1) the observed behavioral changes in macaques and human observers that occur during habituation and 2) researcher and field assistant perceptions of habituation progress. Analysis of macaque behavioral data indicates that over the 7-month study period, the study group became more accustomed to human presence; rates of flight, avoidance, and display responses decreased while ignore responses increased. Significant changes in human-related habituation criteria also occurred; in particular, search times decreased and contact time ratios increased. Researchers’ and field assistants’ impressions of habituation progress, however, did not match these quantitative indicators; namely, most did not perceive the group to be fully habituated by the end of the study. These results suggest that “successful” habituation may be more nuanced than previously demonstrated in primate literature and should therefore be reexamined.

Primates in Mythology

Chapter

Full-text available

Apr 2017

People and nonhuman primates have shared different habitats since the beginning of human history. From early times, nonhuman primates have attracted people's attention and have inspired a number of myths in different parts of the world. This is not surprising considering the biological, phylogenetic, and behavioral similarities of nonhuman primates and humans. The prominent role of nonhuman primates in mythology is well evidenced in religious traditions, astronomy and astrology, and other diverse aspects of human life. As a result, depending on human culture, some people adopt a quasi-scientific view by considering nonhuman primates our close relatives, as respected and sacred beings, and mediators between deities and humans, while others consider them as evil creatures. These different views on nonhuman primates influence the way humans utilize primate by-products and interact with these animals, clearly demonstrating that understanding the mythology surrounding primates and their influence in the cultural and religious aspects of human populations is an important issue for primate conservation.

Habituating field scientists

Article

Full-text available

Oct 2016
SOC STUD SCI

Lys Alcayna-Stevens

This article explores the sensory dimensions of scientific field research in the only region in the world where free-ranging bonobos (Pan paniscus) can be studied in their natural environment; the equatorial rainforest of the Democratic Republic of Congo. If, as sensory anthropologists have argued, the senses are developed, grown and honed in a given cultural and environmental milieu, how is it that field scientists come to dwell among familiarity in a world which is, at first, unfamiliar? This article builds upon previous anthropological and philosophical engagements with habituation that have critically examined primatologists’ attempts to become ‘neutral objects in the environment’ in order to habituate wild apes to their presence. It does so by tracing the somatic modes of attention developed by European and North American researchers as they follow bonobos in these forests. The argument is that as environments, beings and their elements become familiar, they do not become ‘neutral’, but rather, suffused with meaning.

Habituation to Tourists: Protective or Harmful?

Chapter

Feb 2017

Jessica L. Westin

Ethnoprimatology, the combining of primatological and anthropological practice and the viewing of humans and other primates as living in integrated and shared ecological and social spaces, has become an increasingly popular approach to primate studies in the twenty-first century. Offering an insight into the investigation and documentation of human-nonhuman primate relations in the Anthropocene, this book guides the reader through the preparation, design, implementation, and analysis of an ethnoprimatological research project, offering practical examples of the vast array of methods and techniques at chapter level. With contributions from the world's leading experts in the field, Ethnoprimatology critically analyses current primate conservation efforts, outlines their major research questions, theoretical bases and methods, and tackles the challenges and complexities involved in mixed-methods research. Documenting the spectrum of current research in the field, it is an ideal volume for students and researchers in ethnoprimatology, primatology, anthropology, and conservation biology.

Kinship with Monkeys: The Guajá Foragers of Eastern Amazonia

Book

Oct 2003

Loretta A. Cormier

Primate Societies

Book

Jan 1986

In Quest of the Sacred Baboon: A Scientist's Journey

Book

Mar 2017

HANS KUMMER

Primates on display: Potential disease consequences beyond bushmeat: MUEHLENBEIN

Article

Jan 2017
AM J PHYS ANTHROPOL

Michael P Muehlenbein

Human interactions with nonhuman primates vary tremendously, from daily cultural engagements and food commodities, to pet ownership and tourist encounters. These interactions provide opportunities for the exchange of pathogenic organisms (both zoonoses and anthroponoses). As exposures are not limited to areas where bushmeat usage continues to be a major problem, we must work to understand better our motivations for engaging in activities like owning primates as pets and having direct physical contact with wild primates within the context of nature-based tourism. These topics, and the theoretical potential for pathogen transmission, are reviewed in the present manuscript. This is followed by a case study utilizing 3845 survey responses collected from four international locations known for primate-based tourism, with results indicating that while a majority of people understand that they can give/get diseases to/from wild primates, a surprising percentage would still touch or feed these animals if given the opportunity. Many people still choose to touch and/or own primates, as their drive to bond with animals outweighs some basic health behaviors. Desires to tame, control, or otherwise establish emotional connections with other species, combined with the central role of touch for exploring our environment, necessitate the development of better communication and educational campaigns to minimize risks of emerging infectious diseases.

Being-with-Animals : Modes of embodiment in human-Animal encounters

Chapter

Jan 2012

D. Dutton

Responses of wild chimpanzees and gorillas to the arrival of primatologists: behaviour observed during habituation

Chapter

Jan 1991

Wild primates show a variety of responses when primatologists arrive to study them. Some are very shy and flee rapidly, while others lack fear and are easy to approach and observe. Habituation is the term used to describe the acceptance by wild animals of a human observer as a neutral element in their environment. The process is rarely described, as it is commonly regarded as a means to an end; namely, the progression to a state that allows the natural behaviour of a species to be observed and documented.