PART I
The Basics
CHAPTER 1
Introduction to the Handbook of Primate Behavioral Management
Steven J. Schapiro
The University of Texas MD Anderson Cancer Center and University of Copenhagen
CONTENTS
References
Welcome to the Handbook of Primate Behavioral Management (HPBM). This handbook contains 29 chapters divided into six parts, all of which focus on aspects of primate behavioral management. The overall goal of the HPBM is to provide those responsible for the development and/or implementation of behavioral management programs for nonhuman primates (NHPs) with a plethora of information, guidance, and data that will allow them to do everything within their power to guarantee that their animals are living in the best conditions possible. A more specific goal involves the presentation of the science of behavioral management, so that behavioral managers can base their decisions on relevant empirical evidence. If the data show that the subadult male offspring of high-ranking females cause social instability in large groups of rhesus macaques living in field cages (McCowan and Beisner 2017), then this information should be acted upon to prevent instability in large rhesus groups.
While the HPBM does include an entire part (Part IV; 7 chapters) on the behavioral management of specific taxonomic groups (macaques, chimpanzees, prosimians, etc.), I did not want this volume to simply be a collection of genera-specific or species-specific behavioral management plans. In my opinion, the value of presenting such plans is infinitely enhanced by the inclusion of the scientific underpinnings that drive the development and implementation of those plans. Hence, Parts II and III (“content” and “implementation,” described in more detail later) precede the discussion of behavioral management plans by taxonomic groups. Similarly, I wanted to take this opportunity to present their work to those who design, produce, and supply products, equipment, techniques, and services that facilitate behavioral management efforts (Part V).
Most of the chapter authors in this handbook work with nonhuman primates in “research” settings; so the information contained in their chapters is likely to be most relevant for primates living in such settings. However, many of the guidelines and recommendations contained in this volume will also be valuable to those managing nonhuman primates in other settings, including zoological parks and sanctuaries.
The HPBM coevolved with the Primate Behavioral Management Conference (PBMC) that we conduct at the Michale E. Keeling Center for Comparative Medicine and Research of The University of Texas MD Anderson Cancer Center in Bastrop, TX. Both the handbook and the conference arose from the ever-increasing importance of primate-focused, theoretical investigations to the applied behavioral management of nonhuman primates. Capitanio and colleagues (Capitanio et al. 2011, 2017; Gottlieb and Capitanio 2013; Gottlieb et al. 2013; Capitanio 2017) were conducting biobehavioral assays to study temperament, and the results of these investigations had important implications for pairing, grouping, and training rhesus macaques (Capitanio et al. 2017). Similarly, McCowan and colleagues (McCowan et al. 2008, 2011, 2016; Beisner et al. 2011; Beisner and McCowan 2013; McCowan and Beisner 2017) were performing social network analyses, the results of which had important practical applications to prevent deleterious aggression in large groups of rhesus monkeys. This handbook, and the PBMC, are filled with similar examples of science resulting in, and driving, applied behavioral management programs and decisions.
The scientific methods and findings included in Part II (Content Areas with Behavioral Management Implications) of the HPBM are concisely described and rigorous. It takes many hours of sophisticated observations and analysis to even partially understand the theory and meaning of biobehavioral assays (BBA; Capitanio 2017); stress (Novak et al. 2017), temperament (Coleman 2017), and depression (Shively 2017) assessments; antipredator behavior (Caine 2017); and social network analysis (McCowan and Beisner 2017). Those reading this handbook (and those attending the PBMC) are unlikely to have the time, skills, and/or resources to apply the relevant methods, conduct appropriate observations, and perform the statistical analyses. However, almost all of those reading this handbook should be able to apply specific findings from each of these research programs to enhance the welfare of the primates in their care. Therefore, most of the chapters are written in such a way that important assessment techniques and/or findings from each investigational approach (that should be applicable at any primate facility) have been identified.
Part I of the HPBM includes four chapters by Schapiro, Baker and colleagues, Hau and Bayne, and Bettinger and colleagues, respectively. Schapiro’s chapter, which you are currently reading, establishes the motivation for the handbook and describes the other chapters herein. The chapter by Baker and colleagues beautifully describes the Behavioral Management Consortium (BMC) of the National Primate Research Centers in the United States. The BMC is in the process of attempting to apply standard definitions and descriptions to many aspects (behaviors, abnormalities, therapies, etc.) of primate behavioral management, applicable not only at the National Primate Research Centers themselves, but should also be pertinent at most, if not all, primate facilities (e.g., academic laboratories, contract research organizations, zoological parks, sanctuaries, breeding “farms”). This chapter has much to offer those responsible for primate behavioral management. In Chapter 3, Hau and Bayne provide a brief description of the regulations and guidelines around the globe that are relevant when keeping primates in captivity, especially in research settings. Their chapter emphasizes those portions of The Guide (NRC 2011) and the European Directive (2010) that have the strongest implications for primate behavioral management. Part I closes with a general discussion by Bettinger and colleagues of the effects of the obvious, and not-so-obvious, aspects of the environment on primates in captivity, helping to establish a foundation for information contained in some of the later chapters.
Part II of the HPBM includes seven chapters by individuals/groups considered to be “content experts” in their respective fields. As already mentioned, the focus of the chapters in this part is the application of the theoretical findings from the work described to aspects of behavioral management. All of the chapters in Part II are written in a more or less similar format, with a description of the techniques used to study the “content” first, followed by descriptions of findings that are particularly relevant to address behavioral management questions, and concluding with recommendations and guidelines concerning the ways in which the methods and/or data from the content area can be directly applied to enhance behavioral management.
In Chapter 5, Capitanio describes his BBA program and the ways in which the data gathered when rhesus monkeys are 3 months old can provide valuable insight and guidance for multiple behavioral management decisions during the course of the animals’ lifetime. In many ways, the results of Capitanio’s work provided the stimulus for both the HPBM and the PBMC. Novak and colleagues, renowned experts in the study of abnormal behaviors in NHPs, discuss, in Chapter 6, abnormal behaviors and conditions in captive NHPs. As hair loss and self-injurious behavior can be extremely problematic for those working with NHPs, their empirical work should be applicable in many captive settings. Chapter 7, written by Coleman, describes her work on primate temperament and provides a set of simple, yet highly valuable, assessments that can be performed to help minimize incompatibility when forming pairs of macaques. These same simple temperament assessments can also be used to address questions related to trainability and a variety of other issues that inform behavioral management decisions. Shively, in Chapter 8, focuses on the behavior and physiology of depressed cynomolgus macaques. Her multifaceted research program has addressed many issues related to depression and its effects on scientific data, and she provides invaluable guidance for dealing with NHPs exhibiting depressed behaviors/postures. In Chapter 9, Caine describes primate antipredator behaviors and how these natural behavior patterns can impact behavioral management decisions. Responses to humans, appropriate sleeping sites, and the aftermath of simulated predatory events all must be considered if one is to achieve optimal behavioral management. Hopkins and Latzman, in Chapter 10, describe how noninvasive behavioral research procedures can positively affect the welfare of captive primates, especially chimpanzees. They strongly emphasize the need to continue to obtain valuable data from captive chimpanzees to benefit humans, captive chimpanzees, and even endangered wild chimpanzees. Part II closes with Chapter 11, which presents a discussion on social network analysis by McCowan and Beisner. This chapter contains a fair bit of “math,” which may put some readers off, but I strongly encourage you to read this chapter. As mentioned previously, and as will be discussed by Bloomsmith (2017) in the final chapter of the handbook, the types of “deep” analyses that are possible with network analysis are among the most important tools for the continuing evolution of primate behavioral management strategies and programs.
Part III of the HPBM includes seven chapters by individuals/groups considered to be “implementation experts” in their respective fields. The focus of these chapters is the application of specific techniques to behavioral management. Some of the techniques are experimental, some are procedural, and some emphasize communication and organizational strategies. However, all of the chapters include specific and useful guidance that can be used to enhance the behavioral management of captive primates.
In Chapter 12, Graham describes her inspiring work that incorporates positive reinforcement training (PRT) techniques into diabetes-related research. This chapter clearly demonstrates how refinements associated with the application of behavioral management techniques can significantly enhance the scientific research endeavor. Magden, in Chapter 13, discusses additional benefits associated with PRT, demonstrating how the application of these techniques can significantly enhance the health management of captive NHPs. Primates that voluntarily participate in their own health care are easier to treat, can be treated using additional modalities, and are likely to be healthier. In Chapter 14, Hutchinson discusses telos, the “primateness of the primate,” as well as the value of effective communication to the ultimate success of behavioral management programs. While he emphasizes communication among veterinarians and behavioral managers, effective communication involving all parties interested in the welfare of captive primates is essential. Hopper (Chapter 15) provides an insightful discussion of the ways in which findings related to social learning can be utilized to facilitate behavioral management. Understanding how socially housed primates learn from one another, and specifically, who learns from whom, can be extremely useful when making socialization-related decisions. Schapiro and colleagues, in Chapter 16, expand some of the ideas presented by Hopkins and Latzman (2017), specifically describing how collaborative research projects, especially those involving noninvasive and stimulating “cognitive” tasks, can positively affect the NHPs that participate. In Chapter 17, McGrew describes her techniques for pairing macaques, an issue that is of extremely high interest to those who manage primates in captivity. This chapter is based on the establishment of an extremely large number of successful pairs. Part III closes with Chapter 18, by Lambeth and Schapiro, which provides some straightforward guidance for building and supporting functional behavioral management programs.
Part IV of the HPBM is comprised of seven chapters describing behavioral management programs for different taxonomic groups of primates. Most of the chapters follow a similar format, beginning with a discussion of the natural behaviors of animals and ending with “expert recommendations” that you should be able to incorporate into your own behavioral management program. As Bloomsmith (2017) emphasizes in the final chapter of the handbook, understanding the natural behavior of the primates under our care is absolutely essential for the design and implementation of the highest quality behavioral management programs. The authors of these chapters have quite a bit of relevant experience, and so reading their work should provide you with useful ideas concerning strategies to implement as well as those to avoid.
Part IV begins with a fantastic chapter (Chapter 19) by Gottlieb and colleagues on the behavioral management of most macaque species. This chapter only casually deals with Macaca fascicularis, as Honess, in Chapter 20, deals specifically with this frequently utilized NHP. Those who manage macaques will learn a great deal from these two chapters. Jorgensen’s chapter (Chapter 21) is next, with a take-home message that Chlorocebus are not Macaca. Chapter 22, by Lutz and Nevill, describes behavioral management strategies for baboons, a large, potentially destructive, but ultimately manageable genus. Reamer and colleagues (Chapter 23) then discuss behavioral management strategies for Pan species (common and pygmy chimpanzees), another large, potentially destructive genus. The fact that Pan are both extremely intelligent and quite amenable to positive reinforcement training make them an especially important group for identifying techniques to take behavioral management to the next level. Behavioral management strategies for three genera (Aotus, Callithrix, Saimiri) of Neotropical p...