Researchers' ethical concerns regarding habituating wild-nonhuman primates and perceived ethical duties to their subjects: Results of an online survey.

While the process of habituation is essential for researchers to observe primates in their natural habitats, ethical dilemmas may arise from its consequences. We collected data from 286 participants via an online survey to investigate: (a) how primatologists perceive their ethical duties toward their subjects; (b) the extent to which primatologists are concerned about the potential ethical consequences of habituation; and (c) the methods primatologists use to reduce potential harms caused by habituation. Overall, primatologists felt an extremely strong duty to mitigate harms that they may cause (e.g., to not stress individuals during observation, treat injuries, and reunite separated individuals) and expressed very high concern for habituation's potential to increase the vulnerability of their subjects to poaching and disease transfer. Ratings for those items were so high that they could not be included in subsequent exploratory factor analyses that were designed to reveal constructs underlying respondents' ratings of their ethical duties and concerns. Factor analysis of ratings of ethical duties revealed that primatologists reported a strong duty to mitigate harms caused by other humans and a lower perceived duty to mitigate naturally occurring harmful events. Factor analysis on ethical concern ratings revealed that respondents were concerned about harms during the habituation process, the presence of unhabituated behavior after habituation had been established, and indirect harms of habituation. Concerns for unhabituated behavior and indirect harms were rated slightly higher than concern for harms during the habituation process. To mitigate potential harms, primatologists primarily reported engaging in strategies to reduce stress in their subjects. Our findings reveal a disconnect between primatologists' ratings of their ethical concerns and their reported mitigation practices that may, in part, stem from gaps in knowledge about the true impacts of habituation. We suggest areas of discussion and research in the field necessary to address those gaps.

Fundamental differences between wildlife and biomedical research.

Non-human animals have starred in countless productions of biological research. Whether they play the lead or supporting role depends on the nature of the investigation. These differences in the roles of animals affect nearly every facet of animal involvement, including: the choice of species, the sample size, the source of individuals, and the settings in which the animals are used. These roles establish different baselines for animal use that require substantially different ethical considerations. Efficient and appropriate oversight of wildlife research benefits the animals and their investigators. Toward that end, Institutional Animal Care and Use Committee (IACUCs) must appreciate the profound differences between biomedical and wildlife research and recognize the value of the state and federal permitting processes required for wildlife studies. These processes assure us that potential impacts beyond the level of the individual are minimal or are justified. Most importantly, IACUCs must recognize that they, and their investigators, have an obligation to use appropriate guidelines for evaluating wildlife research.

Ethical issues in African great ape field studies.

Great apes have been systematically studied in the wild for over half a century. Great apes are now critically endangered and this raises significant ethical issues for field primatologists who study and work to conserve these primates and their habitats. The most immediate ethical concerns involve the well-being of the subjects, but there are also important ethical considerations involved in researchers' interactions with local human populations and extracting industry representatives. This essay will discuss some of the ethical issues raised by African great ape research, with the hope of generating greater dialogue about best practices. After briefly presenting the history of great ape fieldwork, the ethical issues associated with habituation, intervention, and conservation will be discussed. This text will end with specific proposals that focus on the ethical concerns in great ape field studies.

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.''

Bonding, biophilia, biosynergy, and the future of primates in the wild.

Human and nonhuman primates bond with one another in countless ways, and the results are varied and vital to the individuals and species involved. The manifesto that is the basis for the collection of essays in which this commentary is included proposes that the "human/nonhuman bonds that arise in primatological research and practice deserve and demand study and research." An essential corollary of this proposal is that the primatologists themselves must be studied. The aim of this essay is to explore the influence of human/nonhuman primate bonding on conservation practice and on the future of primates in the wild. This commentary applies the author's professional experience as a conservation psychologist and his research on the impact of profound interspecies bonds on human worldviews, attitudes, and behavior. It examines two general categories of bonds: those driven by Biophilia (human fascination with life) and those influenced by Biosynergy (mutual enrichment of life). It is the author's premise that biosynergy promotes complex collaborative interspecies bonds that broaden the conservationist's desire to enhance synergy among all organisms in an ecosystem. Conversely, biophilia induces relatively simple unidirectional bonds between humans and other animals that deepen the conservationist's desire to understand and protect certain species. This contrast raises some crucial questions. Do biophilia-driven bonds between conservationists and their favorite primates blind them to the synergistic needs of all species and impair their ability to work for sustained preservation of threatened habitat? Does biosynergy-based human/nature bonding enhance focus on conservation as an ecological science and thus ignore species-specific factors crucial to assure survival of endangered primates? How can both types of bonds be optimally applied to the conservation of wildlife and wilderness?

Primatology between feelings and science: a personal experience perspective.

The aim of this article is to discuss some aspects of the relationship between feelings and primatological science, and how this relationship can influence this particular scientific practice. This point of view is based on the author's personal experience. A sentimental reason to study primatology in the first place will be discussed, and then the existence of a bond between the observer and the observed will be presented as a possible by-product of primatology. The following question is whether a sentimental attitude toward primates is detrimental for good science or is, alternatively, actually leading to better primatological science. As an example, the practice of naming individual monkeys is considered. It is argued that naming monkeys can help by characterizing individuality, and this is likely to improve planning of behavioural observations and welfare of captive individuals. The relationship between the researcher and study subject in biomedical studies is discussed in terms of hierarchy of moral status. Finally, primatology is not unique in the existence of bonds between the observer and the observed, at least from the point of view of the observer. However, primatology is unique because, more than in other cases, it gives greater opportunity for reasoning about different factors surrounding "doing science with animals." This is most probably owing to the phylogenetic closeness primatologists have with their study subjects. Among the different factors involved in making science using animals, the sentimental bond developing between the researcher and study animal can be very influential.

Field primatology of today: current ethical issues.

As members of professional organizations such as American Society of Primatologists (ASP) and the International Primatological Society (IPS), primatologists must adhere to a set of nonhuman primate-focused principles outlined in resolutions and policy statements on, for example, the ethical treatment of nonhuman primates. Those of us that work in the field must also address issues such as the protection of primate health in the wild and the conservation of wild primate populations. Moreover, we increasingly find ourselves in complex situations where we must balance human and nonhuman primate needs and interests. The selection of commentary pieces in this edition of the American Journal of Primatology originated from presentations given in the symposium, Field Primatology of Today: Navigating the Ethical Landscape, held at the 32nd Annual Meeting of the American Society of Primatologists (ASP) in September 2009. The goals of that symposium and these resulting commentary pieces are threefold: (1) to revive a discussion of key contemporary ethical issues faced by field primatologists, (2) to highlight the need for centrally placed ethical considerations in various facets of our professional lives, particularly research and teaching, and (3) to consider what a comprehensive ethical code that addresses all of these issues might look like.

Ethics commentary: subjects of knowledge and control in field primatology.

Our primate kin are routinely displaced from their habitats, hunted for meat, captured for trade, housed in zoos, made to perform for our entertainment, and used as subjects in biomedical testing. They are also the subjects of research inquiries by field primatologists. In this article, we place primate field studies on a continuum of human and alloprimate relationships as a heuristic device to explore the unifying ethical implications of such inter-relationships, as well as address specific ethical challenges arising from common research protocols "in the field" (e.g. risks associated with habituation, disease transmission, invasive collection of biological samples, etc.). Additionally, we question the widespread deployment of conservation- and/or local economic development-based justifications for field-based primatological pursuits. Informed by decades of combined fieldwork experience in Indonesia and the Democratic Republic of Congo, we demonstrate the process by which the adherence to a particular ethical calculus can lead to unregulated and ethically problematic research agendas. In conclusion, we offer several suggestions to consider in the establishment of a formalized code of ethics for field primatology.

Putting the community back in community ecology and education: the role of field schools and private reserves in the ethical training of primatologists.

In 1993 and 1999, with the assistance of a Nicaraguan family, we founded La Suerte Biological Research Station in northeastern Costa Rica and Ometepe Biological Research Station in southern Nicaragua as a privately owned conservation-oriented business. Our goal was to develop a program of sustainable community ecology focused on education, research, and the conservation of primates and tropical forests. In order to accomplish this we developed field courses in which undergraduate and graduate students conduct scientific research, experience local cultures, and learn about conservation. Over 120 of these students have received doctoral degrees or are currently in graduate programs. Four doctoral dissertations, several MA theses, and some 20 scientific articles have been published based on research conducted at our field stations. In order to achieve our long-term goals of preserving the environment, we also needed to engage directly with local communities to address their needs and concerns. To this end, we developed a series of community-based initiatives related to health care, bilingual education, and conservation education using traditional and on-line teaching tools. In this article, we describe our efforts in Costa Rica and Nicaragua teaching conservation-oriented field courses and working with the local human communities. Building upon these experiences, we outline a set of ethical considerations and responsibilities for private reserves, conservation-oriented businesses, NGOs, and conservancies that help integrate members of the local community as stakeholders in conservation.

Ethical issues faced by field primatologists: asking the relevant questions.

Field primatologists face unusual ethical issues. We study animals rather than people and receive research approval from animal care rather than ethics committees. However, animal care evaluation forms are developed from concerns about laboratory animal research and are based on the "Three R's" for humane treatment of captive experimental subjects (replacement, reduction and refinement), which are only debatably relevant to field research. Scientists who study wild, free-ranging primates in host countries experience many ethical dilemmas seldom dealt with in animal care forms. This paper reviews the ethical issues many field primatologists say they face and how these might be better addressed by animal care forms. The ethical issues arising for field researchers are divided into three categories: "Presence, Protocols and People" and for each the most frequent issues are described. The most commonly mentioned ethical concern arising from our presence in the field is the possibility of disease transmission. Although most primate field studies employ only observational protocols, the practice of habituating our study animals to close human presence is an ethical concern for many since it can lessen the animals' fear of all humans, thereby facilitating undesirable behaviors (e.g., crop-raiding) and rendering them vulnerable to harm. Field primatologists who work in host countries must observe national laws and local traditions. As conservationists, primatologists must often negotiate between the resource needs and cultural practices of local people and the interests of the nonhuman primates. Many say they face more ethical dilemmas arising from human interactions than from research on the animals per se. This review concludes with suggestions for relevant questions to ask on animal care forms, and actions that field primatologists can take to better inform animal care committees about the common ethical issues we experience as well as how to develop guidelines for addressing them.

Controlling life: from Jacques Loeb to regenerative medicine.

In his 1987 book Controlling Life: Jacques Loeb and the Engineering Ideal in Biology, Philip Pauly presented his readers with the biologist Jacques Loeb and his role in developing an emphasis on control of life processes. Loeb's work on artificial parthenogenesis, for example, provided an example of bioengineering at work. This paper revisits Pauly's study of Loeb and explores the way current research in regenerative medicine reflects the same tradition. A history of regeneration research reveals patterns of thinking and research methods that both echo Loeb's ideology and point the way to modern studies. Pauly's work revealed far more than we readers realized at the time of its publication.