Nonhuman Primates in Biomedical Research || Behavioral Management, Enrichment, and Psychological...

Chapter 6

Behavioral Management, Enrichment,and Psychological Well-being ofLaboratory Nonhuman Primates

Kristine Coleman*, Mollie A. Bloomsmithy, Carolyn M. Crockettz, James L. Weedjj and Steven J. Schapiro{*Oregon National Primate Research Center, Beaverton, OR, yYerkes National Primate Research Center, Atlanta, GA, zWashington National Primate

Research Center, Seattle, WA, jjDivision of Veterinary Resources, National Institutes of Health, Bethesda, MD, {The University of Texas MD Anderson

Cancer Center, Bastrop, TX

No

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Chapter Outline

Introduction 149

Definitions of Terms 150

Why Perform Behavioral Management? 152

Regulatory Issues 152

Ethical Responsibilities 153

Enhancing the Research Endeavor 153

Managing Behavior 154

Colony Composition 154

Understanding Natural Behavior 154

Problem Cases 155

Threshold for Concern 155

Environmental Enrichment Plans 156

Overview 156

Examples of Enrichment 157

nhuman P

pyright �

Social Enrichment
157
Nonsocial Enrichment
159
rimates in Biomedical Research. DOI: 10.1016/B978-0-12-381365-7.00006-6

2012 Elsevier Inc. All rights reserved.

Assessing the Value of Enrichment 162

Safety Concerns 163

Documentation 163

Positive Reinforcement Training 164

PRT as Refinement 164

PRT and Husbandry, Veterinary and Research Procedures 166

PRT as Enrichment 167

Balancing Psychological Well-Being and Research Needs 168

Managing Behavioral Management Programs 169

Roles 169

Behavioral Management and the Institutional Animal Care

and Use Committee (IACUC) 169

Conclusions 169

Acknowledgments 170

References 170

INTRODUCTION

Animal care in biomedical facilities housing nonhumanprimates has undergone a dramatic transformation in thepast two decades, with increasing emphasis on behavioralmanagement, psychological well-being, and animalwelfare. In the early part of the 20th century, the need tomaintain the welfare of laboratory animals was largelyunrecognized. This situation changed as the scientificcommunity realized that nonhuman primates and otheranimals have many behavioral needs, which if not met canadversely affect the behavior, physical health, and researchutility of the animals. Prior to the 1985 amendments to theAnimal Welfare Act (also known as the Improved Stan-dards for Laboratory Animals Act; AWA, 1985), animal

care in general and the provision of enrichment in particularwas provided without real planning or effective evaluation.Toys, televisions, and other items were occasionallyprovided for animals on an ad hoc basis, primarily depen-dent upon the opinions of caretakers or veterinarians. Therewere few empirical studies demonstrating the efficacy ofparticular items or strategies intended as “enrichment.”

The 1985 amendment to the Animal Welfare Act(AWA) and passage of the 1991 Animal Welfare regula-tions inspired an increasing emphasis on empirical studiesaimed at examining the effects of enrichment and behav-ioral management practices, a major change that helpedshape modern animal care in biomedical facilities.Although the term “psychological well-being” for NHPs

149

150 Nonhuman Primates in Biomedical Research

did not come into common use until after enactment of theAWA and its regulations (see below), the academic roots forthe empirical evaluation of the welfare of captive primateswere evident many years earlier. Much of the early work onenrichment and behavioral management began in zoos andincluded nonprimates as well as primates. Hediger(Hediger, 1950, 1969) wrote of the need to occupy captiveanimals with play and training and the need for captiveanimals to behave in ways similar to their wild counter-parts. However, as early as the 1920s, Yerkes (Yerkes,1925) wrote about the need to design apparatus that wouldallow captive apes to work or play. Beginning in the 1970s,Markowitz initiated a series of empirical studies to improvezoo animal environments using what would now be calledenrichment techniques (Markowitz, 1975, 1982). In 1979,an edited volume, Captivity and Behavior: Primates inBreeding Colonies, Laboratories and Zoos (Erwin et al.,1979), focused on understanding a variety of behavioralissues affecting captive primates, including abnormalbehavior, attachment, aggression, and enrichment. Severalbooks and hundreds of peer-reviewed scientific articles onbehavioral management and enrichment have been pub-lished since that time. Some of these resources for envi-ronmental enrichment are provided in Table 6.1.

Today, providing for the psychological well-being ofnonhuman primates (NHPs) is an integral part of animalcare. Facilities housing NHPs for research or exhibitiondevote substantial resources in an effort to meet thebehavioral needs of their animals, and all such facilities inthe USA must by law have an Environmental EnhancementPlan in place (USDA, 1991). Many institutions, includingall of the National Primate Research Centers in the USA aswell as other breeding and research facilities, have behav-ioral management units dedicated to providing for thepsychological well-being of the NHPs. The majority ofthese units are overseen by PhD-level behavioral scientistsor veterinarians (Baker et al., 2007). These behavioralmanagement units typically are responsible for determiningthe enrichment plan for the facilities, socializing primates,training NHPs to cooperate with clinical or husbandry-related procedures, training caregivers, and conductingbehavioral assessments. Specialized positions in behavioralmanagement are now commonplace in research facilities,substantial budgets are devoted to the behavioral manage-ment of the NHPs, and commercially available productshave been designed and marketed to promote the psycho-logical well-being of NHPs.

This chapter summarizes a number of concepts that areintegral to the appropriate behavioral management oflaboratory primates and to the promotion of their psycho-logical well-being. We will focus on the NHPs mostcommonly utilized in biomedical research, includingmacaques (i.e. rhesus macaques (Macaca mulatta), cyn-omolgus macaques (M. fascicularis), and pigtailed

macaques (M. nemestrina)), baboons (Papio spp.), andNew World species, such as marmosets (e.g. Callithrixspp.), owl monkeys (Aotus spp.), and squirrel monkeys(Saimiri spp.). The concepts discussed here clearly apply toother NHP species as well.

DEFINITIONS OF TERMS

Four important terms used repeatedly throughout thischapter e environmental enrichment, behavioral manage-ment, psychological well-being, and welfare e are some-times used interchangeably; such usage is inappropriateand can be confusing. Enrichment has been defined as “ananimal husbandry principle that seeks to enhance thequality of captive animal care by identifying and providingthe environmental stimuli necessary for optimal psycho-logical and physiological well-being” (Shepherdson, 1998,p. 1). Enrichment should influence multiple aspects of anindividual’s behavioral repertoire. It is often classified intofive broad and overlapping categories (Bloomsmith et al.,1991; Keeling et al., 1991): social enrichment and fourtypes of nonsocial enrichment that typically consist ofphysical, sensory, food, and cognitive/occupationalcomponents. Although this definition implies a broad focuson multiple behavioral dimensions, in practice the term“enrichment” is sometimes simply used to refer to toys andobjects given to animals. Partly due to this misuse of theterm “enrichment,” many professionals working withcaptive nonhuman primates now prefer the broader term“behavioral management.”

Behavioral management is a comprehensive manage-ment strategy (Keeling et al., 1991) that includes usingenrichment (both social and nonsocial), positive reinforce-ment training, facilities and enclosure design, positivestaffeanimal interactions, and behavioral monitoring topromote psychological well-being (e.g. Bloomsmith andElse, 2005; Weed and Raber, 2005). Behavioral manage-ment is a holistic approach to captive care with the aim ofincreasing the animal’s opportunities to express species-typical behaviors and decreasing the occurrence ofabnormal behaviors. An important advantage of thisapproach is that the individual tools of enrichment, social-ization, training, and environmental design can be inte-grated to achieve behavioral goals for captive primates morecompletely than any single technique applied in isolation(Whittaker et al., 2001). The goals of behavioral manage-ment are to have animals that are in good physical condi-tion, display a variety of species-typical behaviors, areresilient to stress, and easily recover (behaviorally andphysiologically) from aversive stimuli (Novak and Suomi,1988). These goals should be addressed throughout theentire life span of the individual, and not just the timeduring periods in which the individual is a subject ofa research study.

TABLE 6.1 Helpful Resources Relevant to Nonhuman Primate Behavioral Management

Books on Enrichment:

Erwin, J, Maple. T.L., and Mitchell, G. (Eds). (1979). “Captivity and Behavior: Primates in Breeding Colonies, Laboratories and Zoos”. VanNostrand Reinhold Company, New York.

Segal, E.F. (1989). “Housing, Care and Psychological Well-being of Captive and Laboratory Primates”. Noyes Publications, Park Ridge, NJ.

National Research Council (1998). “The Psychological Well-Being of Nonhuman Primates”. National Academy Press, Washington, D.C.**This book is available online http://www.nap.edu/catalog/4909.html Accessed 4/20/2011.

Novak, M. and Petto, A. (1991). “Through the Looking Glass: Issues of PsychologicalWell-being in Captive Nonhuman Primates”. AmericanPsychological Association, Washington, D.C.

Shepherdson, D. J., Mellen, J. D., and Hutchins, M. (Eds) (1998). “Second Nature: Environmental Enrichment for Captive Animals”.Smithsonian Institution Press, Washington, D.C.

Wolfensohn, S. and Honess, P. (2005) “Handbook of Primate Husbandry and Welfare”. Blackwell Publishing, Oxford, U.K.

Young, R. J. (2003). “ Environmental Enrichment for Captive Animals”. Blackwell Publishing, Oxford, U.K.

Web Resources:

The National Institutes of Health (NIH) and Office of Laboratory Animal Welfare (OLAW) have published a six-booklet series on providingappropriate enrichment for baboons, capuchins, chimpanzees, macaques, marmosets and tamarins, and squirrel monkeys: http://grants.nih.gov/grants/olaw/Enrichment_for_Nonhuman_Primates.pdf

The Animal Welfare Information Center (through NIH and OLAW) maintains the Environmental Enrichment for Nonhuman PrimatesResource Guide, which contain information about US regulations as well as a bibliography: http://www.nal.usda.gov/awic/pubs/Primates2009/primates.shtml

The Animal Welfare Institute maintains an annotated bibliography of enrichment: http://labanimals.awionline.org/SearchResultsSite/enrich.aspx

European Primate Network: Advancing 3Rs and International Standards in Biological and Biomedical Research: EURPRIM-Net (http://www.euprim-net.eu/). This website has a number of useful links to enrichment and positive reinforcement training.

The Primate Info Net is maintained by the Library of the Wisconsin National Primate Research Center and is an invaluable resource on allaspects of primates and primatology, including enrichment: http://pin.primate.wisc.edu/

Workshops/Conferences:

Primate Training and Enrichment Workshop (PTEW; http://ptew.kccmr.org). This course, which meets for approximately one week, is anexcellent introduction to positive reinforcement training. A condensed version of this course is often offered at the annual meeting of theAmerican Association of Laboratory Animal Science (AALAS: www.aalas.org)

The International Conference on Environmental Enrichment (www.enrichment.org) meets every two years in locations around the world andhas a focus on environmental enrichment.

The Animal Behavior Management Alliance (www.theabma.org) is devoted to behavioral management of captive animals.

The American Society of Primatologists (www.asp.org) and the International Primatological Society (http://pin.primate.wisc.edu/ips/) meetannually and biennially respectively.

151Chapter | 6 Behavioral Management, Enrichment, and Psychological Well-being of Laboratory Nonhuman Primates

The term psychological well-being (PWB) became partof the general lexicon in the scientific community with thepassage of the 1985 amendment to the Animal Welfare Act(AWA, 1985) and 1991 USDA Animal Welfare Act regu-lations (USDA, 1991) mandating institutional environ-mental enhancement plans for nonhuman primates. ANational Research Council committee was formed soonafter to write a report on primate PWB, which was pub-lished in 1998. The committee concluded that PWB impliesa positive mental state and freedom from pain and distress,

both psychological and physiological (National ResearchCouncil, 1998). There is no single measurement that canaccurately assess PWB. The National Research Council(1998) suggested multiple criteria for the evaluation ofPWB, including the ability to cope with daily changes inthe environment, the ability to engage in beneficial species-typical behavior, the absence of maladaptive behaviorresulting in self-injury, and a balanced temperament (i.e.appropriate levels of aggression and passivity). In addition,animals in good psychological health should show signs of


physiological and behavioral adaptation to their environ-ment (Weed and Raber, 2005), including species-normalreproductive and appetitive behaviors (Novak and Suomi,1988; Crockett et al., 1995).

The fourth term, welfare, is typically discussed in waysthat are very similar to psychological well-being, althoughwelfare often encompasses considerations of the subject’shealth and biological function in addition to behavior(American College of Animal Welfare (ACAW), 2010).Welfare includes elements that contribute to the animal’squality of life, including those known as the “Five Free-doms” (Brambrell, 1965): freedom from hunger, thirst, andmalnutrition; freedom from fear and distress; freedom fromphysical and thermal discomfort; freedom from pain,injury, and disease; and freedom to express normal patternsof behavior (World Organisation for Animal Health, 2010).Welfare is often considered to be related to the long-termstatus of the animal, including how it is coping with itsliving conditions (American Veterinary Medical Associa-tion, 2011), whereas psychological well-being may beconsidered to relate to the current behavioral or mentalstatus of the animal (Morton and Hau, 2010). As anexample, giving a captive NHP an injection of a vaccinecan decrease the animal’s psychological well-being due tothe stress associated with the injection while enhancing itswelfare by providing immunity to a particular pathogen.

In general, behavioral management programs, whichinclude the use of environmental enrichment, have the goalof promoting the psychological well-being and welfare ofNHPs.

WHY PERFORM BEHAVIORALMANAGEMENT?

Regulatory Issues

There are several reasons for the dramatic increase in theamount of enrichment and other behavioral managementstrategies provided to laboratory primates over the pastfew decades. First, in some countries, including the USA,the UK, the European Union, and Japan, providingresearch animals with enrichment is required by variousregulatory agencies (Bayne and deGreeve, 2003; also seeChapter 2). In the USA, the Animal Welfare Act regula-tions mandate that research institutions must “develop,document, and follow an appropriate plan for environmentenhancement adequate to promote psychological well-being of nonhuman primates” (9CFR3.81; USDA, 1991).Furthermore, scientists receiving federal funding frommost US funding agencies must be compliant with theGuide for the Care and Use of Laboratory Animals (the“Guide”; National Research Council, 1996; 2011), whichspecifies that enrichment be provided for laboratoryanimals. Other nations have similar laws to those in the

USA. For nations within the European Union, providingfor the welfare of laboratory animals is mandated inDirective 2010/63/EU, protection of animals used forscientific purposes (European Parliament, 2010), and theUnited Kingdom provides such protection under theBritish Animal Welfare Act (British Parliament, 2006; seeChapter 2 for more information on international regula-tions about animal protection). Those facilities choosingto become accredited by the Association for the Assess-ment and Accreditation of Laboratory Animal Care,International (AAALACi), must also supply their primateswith suitable enrichment as detailed in the Guide(National Research Council, 1996, 2011). We discussthese regulations in greater detail below.

The 1985 Animal Welfare Act Amendment led to draftregulations published in 1989 for comment (USDA, 1989).The final rule (USDA, 1991) was criticized by animal rightsadvocates as being too performance based rather thanemphasizing rigid engineering standards (Crockett, 1993).The basic distinction between these two types of approachesis that engineering standards dictate specific minimumrequirements that would violate the law if not met, whereasperformance standards focus on end results, such asnormalized behavioral repertoires. Unlike engineeringstandards, performance standards allow for flexibility anddepend upon “professional input, sound judgment, anda team approach” to achieving specific outcome goals(National Research Council, 2011). Animal welfare regu-lations for NHPs in the USA and Europe are a mix of bothengineering and performance standards, with minimum cagesizes being the primary example of the application of engi-neering standards. An example of a performance standard isthe specification that the social needs of NHPs that normallylive in social groups in nature must be met in captivity (USAnimal Welfare Regulations, Section 3.81; USDA, 1991)instead of a defined specification of exactly how this shouldbe accomplished. Today’s behavioral managementapproaches emphasize implementing enrichment and otherstrategies that have positive impacts on psychological well-being. Further, there is a strong emphasis on utilizingapproaches that have been evaluated quantitatively. Theeffectiveness of enrichment is assessed by usage, thenormalization of behavioral repertoires, and the preventionor reduction of abnormal behaviors (Lutz and Novak, 2005).Specific recommendations on how to evaluate behavioralmanagement programs are detailed below. In addition toengineering and performance standards, practice standards(i.e. the application of professional judgment by experiencedand qualified individuals) may also be acceptable in therealm of animal care (National Research Council, 2011).However, in this chapter, we will emphasize performancestandards based on empirical data. Performance standardscan and should change as data accumulate within the field ofbehavioral management.


Ethical Responsibilities

As stewards for the NHPs in our care, we have a moral andethical responsibility to provide them with humane, highquality care that promotes both their physical andpsychological health. Societal expectations for this level ofcare have also risen in many countries, and it is importantthat biomedical research facilities be seen as institutionsthat care about the animals they house. In short, behavioralmanagement is a key component of promoting psycho-logical well-being and is therefore the “right thing to do.”

This ethical responsibility to provide for the psycho-logical and behavioral needs of captive primates is implicitin position statements by several veterinary and researchsocieties, including the American Veterinary MedicalAssociation (AVMA) (2011), the World Organization forAnimal Health (OIE) (2010), the American Collegeof Animal Welfare (ACAW) (2010), the American Societyof Primatologists (ASP) (2001), the American Society ofLaboratory Animal Science (AALAS) (2007), and severalothers. These position statements refer to the importance ofmanaging both physiological and psychological needs ofanimals in captivity.

Many modern animal care practices, including behav-ioral management, are based on the principle of the “threeRs”; refinement, reduction, and replacement (Russell andBurch, 1959). These principles are a part of the regulationsguiding animal care for several nations, including theEuropean Union’s Directive 2010/63/EU (EuropeanParliament, 2010) and Japan’s 2006 amendment to the Lawfor the Humane Treatment and Management of Animals(Japanese Parliament, 2006). Refinement is of particularimportance to psychological well-being, emphasizing waysto minimize the stress and distress experienced by theanimals while enhancing their well-being (Jennings et al.,2009). Many behavioral management practices representsignificant refinements insofar as they improve psycho-logical well-being and welfare and reduce stress forsubjects. Further, by decreasing stress-related variability inresearch-related dependent measures, behavioral manage-ment and improvements in psychological well-being canreduce the number of research subjects required for manyexperiments, resulting in a reduction in animal use as wellas an improvement in the reliability of the research datacollected. Primate behavior specialists can help facilitiesensure that true refinements in primate behavioralmanagement and psychological well-being are imple-mented (Jennings et al., 2009).

Enhancing the Research Endeavor

Another compelling reason to provide behavioralmanagement strategies for laboratory NHPs is to enhancethe research endeavor. High quality science depends on the

use of valid animal models. The value of most animalmodels is considerably improved when the subjects arehealthy, both physically and psychologically. Environ-mental and psychosocial stressors can alter many physio-logical parameters in nonhuman primates, including thereproductive axis (Norman et al., 1994; von Holst, 1998),immunological parameters (Rogers et al., 1998; Hickeyet al., 2003; Engler et al., 2004), cardiovascular variables(Schnell and Gerber, 1997), and brain function (Conrad andMcEwen, 2000). Common husbandry practices, such asfrequent moves (Capitanio and Lerche, 1998; Bethea et al.,2005), excessive noise (Peterson et al., 1981), and handlingfor venipuncture or injections (Reinhardt et al., 1990; Halland Everds, 2003; Reinhardt, 2003; Lambeth et al., 2005)can result in activation of the hypothalamic pituitarysystem, which can in turn affect research outcomes. Forexample, Capitanio and colleagues (Capitanio et al., 1998)found that rhesus macaques subjected to frequent housingrelocation and social separations around the time ofinfection with simian immunodeficiency virus (SIV) hadshorter survival times than did those not exposed to thesecommon stressors. These same procedures have been foundto disrupt menstrual cycles in some adult macaques (Betheaet al., 2005), an event that can negatively affect a variety ofresearch studies as well as breeding outcomes. Stress canalso result in the development of maladaptive behaviorssuch as self-injurious behavior (Novak, 2003), which cannegatively affect a variety of research outcomes. Further,because there can be vast differences in how individualsrespond to stress (Meaney et al., 1991; De Kloet, 2004;Bartolomucci et al., 2005), uncontrolled stressors can addvariability to studies. Behavioral management techniquescan reduce both the fear and anxiety associated withexperimental procedures and the development of stress-related problems and thereby can increase the validity ofexperimental results. As such, behavioral management isa key component of improving the quality of animal modelsfor research.

It is neither possible nor desirable to eliminate all of thestress experienced by laboratory primates. Stressors are notintrinsically detrimental (Novak and Suomi, 1988) and area natural part of the behavioral environment of manynonhuman primates (de Waal, 1991). Indeed, somestressors can be adaptive, as they relieve boredom and helpthe animal learn to cope with various factors in theirenvironment (Newberry, 1995). Enrichment and behavioralmanagement techniques can mitigate stress responses tosome aversive stimuli (Benaroya-Milshtein et al., 2004).Compared with animals in an impoverished environment,enriched animals show less fear and are less responsive tonegative events, such as exposure to predators or certainexperimental procedures (Klein et al., 1994; Moncek et al.,2004; Barbelivien et al., 2006). This increased resiliencywhen stressed is widely considered an important aspect of


well-being (Novak and Suomi, 1988; Overall and Dyer,2005).

Behavioral management can work in concert withresearch protocols directly to reduce stress and can improvethe research model. For example, primates are sometimesrestrained in primate chairs for certain research protocols inwhich animals must remain still for extended periods oftime. Subjects typically wear a specialized collar thatattaches to the restraint device and limits head movement.The chairs may also have restraints that limit movement ofarms or legs. This kind of restraint is stressful for manysubjects and can lead to agitation and frustration (Ruyset al., 2004), particularly initially. Behavioral managementtechniques can help reduce the stress associated with thisrestraint. McGuffey et al. (2002) found that providingmonkeys with unstructured play time in an activity cagereduced their anxiety toward the restraint chair. Further,training monkeys to sit in the primate chair using anapproach that emphasizes positive reinforcement training(see the section “Positive Reinforcement Training” below)can reduce stress associated with the chair and can increasethe ease of these kinds of research procedures (Rennie andBuchanan-Smith, 2006b). Other ways in which behavioralmanagement techniques can improve the scientificendeavor will be discussed throughout the chapter.

MANAGING BEHAVIOR

Colony Composition

While the ultimate goals of behavioral management plansare the same regardless of the species or size of the colony,in practice these plans have to take the size, composition,and purpose (e.g. research or breeding) of the colony intoaccount. There are different challenges associated withanimals housed in large, outdoor groups than there are withanimals housed in small, indoor cages. NHPs in cages areoften on active research protocols, whereas those in largegroups are often part of the breeding population. Althoughanimals in large breeding groups may be subjects inbehavioral studies, they are less frequently involved ininvasive protocols. Animals may also be kept in smallindoor or outdoor groups, either as study animals orbreeders.

Caged animals typically experience more threats totheir psychological well-being than do those housed inlarge groups. Caged primates have less space, less socialinteraction, and are more likely to be involved in stressfulresearch procedures than are those housed in large groups.Caged primates are at greater risk for developing behav-ioral problems than are primates in groups (see “Under-standing Natural Behavior” below). Because of theseheightened risks, behavioral management effort is oftengreater for caged primates than for those living in large

groups. Much of this behavioral management is focused onproviding caged primates with social opportunities,including pair housing. There has been considerableimprovement in the past ten years in the types of cagingavailable for social enrichment, including a variety ofpanels that allow social access to partners (see Chapter 9 formore details). Caging options currently exist that allowsmall groups of primates to live together (e.g. Erwin andLandon, 1992; Weed et al., 1995). Animals in cages are alsotypically provided with: (1) an enhanced schedule offeeding enrichment; (2) a variety of toys; (3) additionalstimulation from music (in some facilities); (4) videotapesof various types; (5) the use of destructible enrichment(e.g. paper, boxes); and (6) additional positive interactionwith humans to compensate for the lack of social partners.

Whereas NHPs housed in groups are less likely thanthose in cages to show behavioral problems (Schapiro et al.,1996a,b), other issues associated with this type of housingcan lead to diminished well-being and therefore must beconsidered. Aggression and social dynamics can negativelyaffect some individuals (Oates-O’Brien et al., 2010). It isuseful and often imperative to know which animals rank atthe top of the dominance hierarchy. For example, removalof the dominant female from a rhesus macaque group canlead to an increase in aggression in the group (Oates-O’Brien et al., 2010). Maternal behavior may also beproblematic in captive primate groups. Primiparous rhesusmacaque mothers are more likely than multiparous mothersto neglect or abuse their infants (McCormack et al., 2006),and infants are occasionally stolen by females other thanthe dam, requiring increased levels of observational vigi-lance by management staff during the birth season. Ingeneral, the ratio of enrichment personnel to animals islower (i.e. fewer enrichment staff per NHP) for facilitiesthat have a large number of group-housed primates than forfacilities that house NHPs primarily in cages (Baker et al.,2007). However, there is a great need for personnel trainedin primate behavior to observe group dynamics and monitorgroup stability.

Understanding Natural Behavior

In order for enrichment and the broader behavioralmanagement program to be effective, these need to betailored to the individual species of NHP (Lutz and Novak,2005; Jennings et al., 2009; National Research Council,2011). Thus, knowledge of the normal behavioral repertoireof the species is essential for the development of anappropriate behavioral management plan. While certainbehaviors, such as locomotion and climbing, are relativelyubiquitous across the various taxonomic groups ofprimates, others are not. Owl monkeys use nesting cavitiesand should be provided with the ability to nest. Someprosimian (Strepsirhine) and New World Monkey species


rely heavily on scent marking. Frequent cage cleaning caneliminate olfactory signals, the absence of which may thendisrupt social behavior and dominance hierarchies in thesespecies (National Research Council, 1998). Further,common behaviors such as locomotor or resting behaviormay be performed differently across taxonomic groups, andenrichment should address these adaptations. For example,squirrel monkeys perch with their hands and feet ratherthan sitting, and should be provided with round rather thanflat perching options (Williams et al., 1988). Even withinclosely related species, such as the macaques, it is impor-tant to understand species-specific patterns of behavior. Forexample, the dominance style of rhesus macaques isgenerally more aggressive and less tolerant than that ofstumptailed macaques (M. artoides) (de Waal and Luttrell,1989), a difference that can influence social enrichmentpractices (e.g. choice of partners).

Problem Cases

Ideally, behavioral management practices and techniquesreduce the risk of the occurrence of abnormal behaviors.Behavioral pathologies can vary by species. For example,repeated regurgitation and reingestion is a more commonpathology in apes than in macaques (Fritz et al., 1992).Within a species, there can be differences across age or sex.Adult male rhesus macaques are more prone to self-injurious behavior than are young female rhesus (Novak,2003). The following paragraphs detail some of the morecommon behavioral issues observed in NHPs housed inbiomedical facilities (also see Chapter 7).

The behavioral problem of greatest concern is self-injurious behavior (SIB). SIB includes behaviors such asself-biting, head banging, and damaging hair plucking(Novak, 2003). SIB can result in tissue or muscle injury aswell as infection. As with most other behavioral patholo-gies, the etiology of SIB is thought to involve an interactionof environmental and genetic/biological factors. Lack ofproper socialization early in life (e.g. rearing in a nursery orearly placement into single caging) has been found to be thebiggest risk factor for the development of SIB in macaques(Bellanca and Crockett, 2002; Novak, 2003; Rommecket al., 2009a,b; also see Chapter 7). Common husbandrypractices, such as relocating animals to new rooms, canexacerbate bouts of SIB in animals with a history of thebehavior (Davenport et al., 2008). There have been severalgenetic and/or biological factors implicated in the devel-opment of SIB, including dysregulation of the hypotha-lamic-pituitary-adrenal axis among subsets of individuals(Novak, 2003; Tiefenbacher et al., 2004) and alterations inserotonergic function (Henderson et al., 2008; Chen et al.,2010).

Stereotypic behavior (repetitive, habitual behaviorpatterns with no obvious function; Mason, 1991;

Shepherdson, 1993) is a widespread problem for captiveprimates in research laboratories across the USA (Laule,1993; Mason and Latham, 2004). Stereotypies can manifestthemselves in different ways, depending on the species orindividual (Wurbel, 2006) and can include whole-bodylocomotor behaviors, such as pacing, bouncing, somer-saulting, and rocking, as well as self-directed behaviors,such as hair pulling, eye poking, and digit sucking. Manyfactors have been implicated in the development ofstereotypic behavior (see Mason, 1991, for review),including genetics (Schoenecker and Heller, 2000;Schwaibold and Pillay, 2001) and adverse experiencesearly in life (Lutz et al., 2003; Novak, 2003; Novak et al.,2006; Latham and Mason, 2008). Still, the most commonlyposited etiology is suboptimal housing conditions, such asa barren environment with insufficient external stimuli(e.g. Meehan et al., 2004; Swaisgood and Shepherdson,2006) or the lack of appropriate socialization, particularlyearly in life (Bellanca and Crockett, 2002; Lutz et al., 2003;Novak, 2003).

Alopecia is a common problem in laboratory primates(Honess et al., 2005; Novak and Meyer, 2009). Despite itshigh prevalence, a “typical” etiology for this phenomenonhas yet to be identified (Reinhardt, 2005; Steinmetz et al.,2005, 2006). As summarized by Novak and Meyer (Novakand Meyer, 2009), NHPs can lose hair due to behavioral,seasonal, reproductive, or other physiological factors.Conditions such as bacterial infections, parasitic infesta-tions, fungal infections, compromised immune function,and nutritional deficiencies have been considered amongthe potential etiologies for this condition (Steinmetz et al.,2005; Kramer et al., 2010). Stress, in particular social orenvironmental stress, has also been hypothesized asa potential underlying factor in the development of alopecia(Reinhardt et al., 1986; Honess et al., 2005; Reinhardt,2005), although this is not a universal finding (Krameret al., 2010). Like stereotypy, alopecia (when confirmed tohave a behavioral cause) is often considered a maladaptivebehavior indicative of compromised well-being. However,whether alopecia truly is evidence of reduced well-being isnot clear, as it does not exclusively occur in conditionsotherwise associated with reduced well-being. Forexample, alopecia is seen in primates living in large socialgroups, not just among caged animals, and it is not moreprevalent among nursery-reared primates. Thus, under-standing the importance of alopecia represents a significantchallenge for laboratory animal management.

Threshold for Concern

One issue that becomes apparent in dealing with problemcases in captive colonies of NHPs is the point at which tointervene. In some situations, such as when NHPs areseriously injured, the decision is straightforward. However,


the threshold for intervention for other behavioral problems(e.g. alopecia or stereotypy) is less clear. As detailed inNovak et al. (see Chapter 7), it may not be necessary oruseful to try to treat every behavioral problem. Hair loss iscurrently one of the most common “problems” dealt withby NHP behavioral management staff. Because hair loss isoften viewed as an indicator of compromised well-being, itis a concern for many facilities (Novak and Meyer, 2009).However, as detailed above, not all hair loss has a behav-ioral etiology (Novak and Meyer, 2009). Some facilitiesintervene when primates lose more than a certain amount ofhair (e.g. 50%). While such a practice may be useful asa general rule, it may result in a certain portion of thepopulation being excluded from receiving potentiallyvaluable therapeutic interventions (e.g. animals with smallpatches of hair loss may respond well to certain behavioraltreatments). However, interventions intended to reducealopecia, such as grooming substrates, may be ineffectivefor many alopecia cases (Runeson et al., 2011). Further,significant time and effort may be spent providing inter-ventions to animals that will not benefit from them(e.g. monkeys that lose their hair coat due to pregnancy). Itis for this reason that empirical research to define behav-ioral problems and to evaluate potential “therapies” is socritical. As we learn more about the etiology and resultantphenotypes of various problems, we can develop hypoth-eses to determine when behavioral interventions will havethe most impact. As with any behavioral problem, imple-menting behavioral management strategies that prevent theproblem from developing is highly preferable to attemptingto “cure” the problem once the animal exhibits it, becausemany of these behavioral pathologies are resistant tochange.

It is clear that many factors have been identified thatcontribute to the development and expression of abnormalbehavior in captive NHPs. The nursery rearing of infants,other forms of social restriction later in life, and indoorhousing in relatively small cages are particularly influentialfactors. As described above, many of these abnormalbehaviors are resistant to change once they are established.However, even though the link between these factors andthe development of abnormal behavior has been welldocumented, some research facilities continue to manageNHPs in ways that may induce the expression of abnormalbehavior. While these management practices(e.g. individual housing) are often utilized to support thebiomedical research in which the animals participate,everyone should be aware that these practices can and oftendo cause behavioral problems. Reducing or eliminating theuse of these practices will help to significantly reduce theexpression of these behavioral problems in our laboratoryNHPs. For some facilities, these sorts of changes willrequire a shift in philosophy and/or infrastructure within theinstitution. Scientific investigators may need to be shown

that their studies can be performed with paired or group-housed NHPs. New cages that allow pairing or pens mayalso have to be purchased or built. It is the responsibility ofthose involved with behavioral management, as well as ofthe local IACUC, to advocate for these changes.

ENVIRONMENTAL ENRICHMENT PLANS

Overview

As previously mentioned, environmental enrichment ismore than toys; enrichment is one of the primary compo-nents of an effective behavioral management program,striving to functionally simulate in captivity the mostrelevant aspects of the species’ natural environment. Theefficacy of a facility’s environmental enhancement plan canbe maximized if it adheres to a number of well-establishedprinciples. Enrichment plans should be customized for eachspecies of nonhuman primate. Different species evolvedunder different environmental conditions, resulting inunique, species-specific behavioral repertoires. Successfulenrichment programs must take these specific behavioralpatterns into account in an effort to increase the biologicalfunctionality of the captive environment (Newberry, 1995).Enrichment programs that are appropriate for one speciesmay be inappropriate for another (Lutz and Novak, 2005;Jennings et al., 2009; National Research Council, 2011). Inaddition, whenever possible, enrichment plans should beappropriate not only for the species but also for the age andsex class of the animals involved. Juveniles of many speciestend to be more exploratory and active than adults andshould be provided with more opportunities to explore andto play. Individuals participating in some types of researchstudies (e.g. those that are more invasive or require singlehousing) may benefit from supplemental enrichment.Finally, to be effective, enrichment must be goal oriented.Whereas the goals of enrichment in general are to provideopportunities for animals to increase their time spent inspecies-typical behaviors and to reduce the amount of timespent in abnormal or undesirable behaviors, institutionsmay have additional goals that apply to the animals them-selves, including increases in reproductive output ordecreases in trauma due to aggression. Enrichment shouldbe provided with these goals in mind, and success must beevaluated and assessed on a regular basis. Items orapproaches that are not achieving appropriate outcomesshould be modified or eliminated.

Enrichment is often applied with the goal of reducingabnormal behavior. Foraging devices, such as puzzlefeeders or foraging boards, are common interventions forbehavioral issues such as stereotypies (Bayne, 1991; Lamet al., 1991; Lutz and Farrow, 1996). Because the perfor-mance of most stereotypies and other problem behaviorsare often incompatible with foraging from a device, the


undesired behavior may transiently decrease upon initialpresentation of the device (Lutz et al., 2003). However,once the foraging opportunity is gone, the animal oftenreturns to performing the behavior (Lutz and Farrow, 1996).Other enrichment strategies are more effective in reducingundesired behaviors over time. Benefits of specificenrichment are addressed below.

The decision to utilize particular behavioral manage-ment strategies should, whenever possible, be based on thescientific literature (National Research Council, 1998).There has been a tremendous increase in the number ofpublications that evaluate the effects of enrichment fornonhuman primates. Peer-reviewed studies of behavioralmanagement strategies for primates are routinely publishedin many journals serving the biomedical researchcommunity as well as in primate-specialty journals.However, studies have mainly focused on assessing thebehavioral effects of behavioral management procedures,with much less attention paid to the influence of theseprocedures on dependent measures relevant to biomedicalresearch studies (but see Schapiro et al., 2000 for anexception). Since studies in rodents have shown thatenrichment can cause neurological changes, includingincreased brain size and weight (Greenough, 1975),increased numbers of synapses per neuron (Benefiel andGreenough, 1998), and increased neurogenesis (Kemper-mann et al., 1997), enrichment itself could be a potentialvariable in studies (Bayne, 2005; Hubrecht, 2010). There isa strong need for additional research that attempts todocument the impact of behavioral management proce-dures on primates used in biomedical research.

Because enrichment can affect physiological variablesin NHPs, it is important that scientific staff be familiar withthe environmental enhancement plans approved for theirfacility. Further, investigators need to be aware of anyresearch protocol restrictions that may require exemptionsfrom the behavioral management plan and report these tothe Institutional Animal Care and Use Committee(IACUC). The process employed at one National PrimateResearch Center is described in detail by Thom andCrockett (Thom and Crockett, 2008).

Examples of Enrichment

Social Enrichment

Most species of nonhuman primates are social and haveevolved to live in complex societies. They form intricatesocial relationships in the wild, spending a great deal oftime engaged in social behaviors, including grooming andhuddling with other members of the troop. Providing socialhousing for NHPs affords them the opportunity to engage inspecies-specific social behaviors and to develop many ofthe cognitive and social skills necessary for group living

(de Waal, 1991), and as such is one of the best overallenrichment options for most captive NHPs (Crockett, 1990;de Waal, 1991; Lutz and Novak, 2005). However, of thedifferent types of enrichment, social enrichment requiresthe greatest amount of attention to the differences amongNHP species and the greatest expertise in understandingbehavior by those working with primates.

Social housing increases the opportunity for animals toengage in many species-typical behaviors, including play,feeding, and grooming (Schapiro et al., 1996a). It canreduce abnormal behaviors such as stereotypic behaviorand self-injurious behavior (Schapiro et al., 1996a; Weedet al., 2003). Importantly, social enrichment, particularlyearly in life, is also an effective tool for the prevention ofabnormal behaviors. As mentioned above, some of theprimary risk factors for developing self-injurious and otherabnormal behaviors in macaques involve being rearedwithout appropriate close social contact with conspecificsand living in single housing for extended periods whenyoung (Bellanca and Crockett, 2002; Novak, 2003;Rommeck et al., 2009a,b). In addition, the presence offamiliar companions can mitigate the effects of variousstressors and alter immune function, which can improvewell-being (Schapiro et al., 2000; Gilbert and Baker, 2011).Taken together, social enrichment is one of the mostimportant parts of an effective behavioral managementplan.

The importance of social housing is reflected by Euro-pean and US regulatory agencies, which require socialhousing for captive NHPs. The 2011 revision to the Guideunambiguously states that single housing for social animalsshould be the exception, acceptable only in situations inwhich there is either a behavioral or veterinary concern(e.g. the animal may cause harm to itself or others) or anexperimental requirement approved by the IACUC(National Research Council, 2011). Importantly, the Guidealso states that IACUC approval for such research-protocol-related social housing exemptions should be basedon currently accepted standards. Thus, as refinements aredeveloped that allow social housing of experimentalanimals, IACUC approval for single housing shoulddiminish. When animals are singly caged, they may requiremore cage space than is required for pair- or group-housedprimates, as well as the provision of additional enrichmentsuch as increased human contact, or periodic use of activitycages (National Research Council, 2011). The need forsingle housing should be reviewed by the attending veter-inarian and IACUC on a regular basis (National ResearchCouncil, 2011).

Options for social housing can vary from indoor cageshousing a pair of animals (i.e. pair housing) to large,outdoor enclosures containing many animals. Ideally,primates should be kept in housing that provides forexpression of their natural behavior. Unlike many other

FIGURE 6.1 Subadult (foreground) and adult (background) male

pigtailed macaques (Macaca nemestrina) in Washington National

Primate Research Center-style grooming-contact cages. (Photo by

Carolyn M. Crockett.)


species of NHPs, marmosets and tamarins live in cooper-ative breeding groups with a single breeding pair. Incaptivity, these primates are often kept in groups consistingof a breeding male and female and their subadult, juvenileand infant offspring (National Research Council, 1998).Macaques and chimpanzees as well as other primatespecies live in relatively large troops, and thus, living inlarge outdoor enclosures is often considered the best type ofhousing for them. Not only does living in a group providefor the most complex social environment, but it alsoprovides exercise and cognitive stimulation. However,group housing is not a viable option in all cases. Theconstraints of the facility and the “function” (i.e. assign-ment) of the animals are two factors that influence housingoptions. Some research procedures are more readilyaccomplished by housing NHPs in smaller cages ratherthan in a group setting. However, advances in technologyand in animal training techniques are making it morepractical to group house NHPs even when they are involvedin a variety of biomedical research projects. For example,implanting microchips as individual identifiers to be readby computers has allowed studies of cognition in group-housed macaques (Fagot and Bonte, 2010) as well asstudies of biological factors affecting eating and obesity(Arce et al., 2010). Training NHPs to cooperate withcommon research procedures such as leaving their groupbriefly for blood withdrawal (Blank et al., 1983) or vaginalswabbing for monitoring menses (Jensen et al., 2010) alsoallows the animals to benefit from living in social groupswhile contributing to biomedical science. As trainingbecomes a more pervasive element of behavioral manage-ment programs, there will be more opportunities like this inthe future, which will contribute to the well-being oflaboratory NHPs.

Caging should be selected to provide flexibility in thedegree and type of tactile and visual contact available to theanimals (see Chapter 9). Pair housing (i.e. housing twomonkeys in an appropriately sized cage) allows tactilesocial contact between the partners and is a common typeof social housing for NHPs living indoors in the USA(Baker et al., 2007). When full contact pair housing is notappropriate (e.g. for certain approved research protocols orfor maleefemale pairs), grooming contact panels (Crockettet al., 1997) between adjacent cages can be used in somecases (Figure 6.1). These panels are designed such that partof the panel consists of widely spaced bars or holes that areof sufficient diameter to permit the monkeys on oppositesides of the panel to groom one another. Grooming contactpanels afford individual monkeys privacy as well as choicein whether to engage in tactile social contact, includinggrooming with the neighboring monkey (Crockett et al.,1997). Interestingly, while the Guide calls for socialhousing of caged animals, what constitutes “pair housing”is not clearly defined. For two or more caged NHPs to be

considered socially housed, they should be in tactile contactto allow for touch and grooming. Therefore, as long as thebars or holes on the grooming panel are wide enough toallow the partners to put their hands through to groom oneanother, this kind of housing should be considered “social,”although it should not be preferred when full contactpairing can be achieved.

Assessments of the behavioral benefits of grooming-contact caging have found mixed results. Lee andcolleagues (in press) found few behavioral differencesbetween female longtailed macaque pairs when they werehoused in full contact versus when housed in grooming-contact cages. In contrast, Baker and colleagues (Bakeret al., 2008) found that abnormal behaviors of rhesusmacaques occurred at higher levels when the animals werehoused in protected-contact cages versus full-contact pairhousing. Although the empirical data are mixed, grooming-contact cages do provide opportunities for certain types ofsocial contact, including grooming, a behavior that couldnot happen in singly housed animals (Crockett et al., 1997).

Social housing is not a universally accepted behavioralmanagement panacea for NHPs, however. Social housingcan result in serious injury if individuals are not compatibleand if information concerning natural species-typical socialgroupings is not applied. Factors such as sex and age mayaffect how well individuals get along with each other.Given the xenophobic nature of some primate species,forming compatible pairs or groups can be challenging. Forthese species, keeping social units relatively stable can helpreduce aggression. When animals do need to be removedfrom the social group (e.g. for trauma or illness), it isimportant to return them to the group as quickly as possible.

FIGURE 6.2 Adult male vervet monkey (Chlorocebus aetheops) in

a “porch.” The porch is a small cage that attaches to the outside of the

home cage, providing the animals with a larger field of view. (Photo

courtesy of the Oregon National Primate Research Center.)


Not only does animal removal cause social disruption andpotential aggression, but also it can negatively impact thehealth of the individuals in the group (e.g. Capitanio andLerche, 1998). Even in the absence of overt aggression,living in a group can be stressful to individuals, particularlyin species with dominance hierarchies in which someanimals have greater access to resources than others. Inthese societies, individuals at the bottom of the hierarchyare more prone to stress and stress-related diseases, such asatherosclerosis and ulcers, than dominant individuals are(e.g. Sapolsky, 1990; Coe, 1991; Shively et al., 2009). Still,social stressors are not intrinsically detrimental to monkeys(Novak and Suomi, 1988), and behavioral strategies to copewith stressors are a natural part of the behavioral repertoireof most NHPs (de Waal, 1991).

Typically, NHPs are co-housed with conspecifics or,less commonly, with congenerics. In general, New Worldand Old World monkeys should not be co-housed in thesame room (Fortman et al., 2002). When possible, animalsco-housed with contraspecifics should also have access toconspecifics. For instance, infant chimpanzees have beenraised in the nursery with both a canine companion andother chimpanzee infants (Thompson et al., 1991). Whenpossible, NHPs should be in visual contact with conspe-cifics (Office of Animal Care and Use, National Institutesof Health (OACU), 2010).

Another form of social enrichment is the interactionbetween the caretaker and the primate. Positive interactionswith caretakers can reduce abnormal behavior (Bourgeoisand Brent, 2005) and increase species-appropriate behav-iors, such as grooming, in a variety of primates, includingmarmosets, macaques, and chimpanzees (Bayne et al.,1993a; Reinhardt, 1997; Waitt et al., 2002; Baker, 2004;Manciocco et al., 2009). Such relationships can alsopromote coping skills (Rennie and Buchanan-Smith,2006a) and help mitigate stress reactivity toward novelsituations. Miller and colleagues (Miller et al., 1986) foundthat chimpanzees were less anxious when confronted withnovelty in the presence of their trusted caretaker than whenthe caretaker was absent. Baker and Springer (2006) foundthat the frequency with which treats were fed affected thelikelihood of the treat being taken, and could improvemonkeys’ responses to unfamiliar people. Finally, Bloom-smith and colleagues (Bloomsmith et al., 1999) havedemonstrated that structured humaneprimate interaction(positive reinforcement training sessions) resulted in morepronounced increases in prosocial behavior than didunstructured humaneprimate interactions.

Nonsocial Enrichment

Physical Enrichment

Physical enrichment represents a broad category of envi-ronmental enhancements that are designed to provide the

animals with opportunities to explore or manipulate andincludes items such as toys, mirrors, logs, and branches.Physical enrichment can also include structural items, suchas perches, swings, play and resting structures, visualbarriers, pools or water baths, flooring substrates, nestboxes, and porches (a small cage hung on the outside of thehome cage; Figure 6.2). Again, physical enrichment isintended to afford individuals opportunities to expressspecies-normative behaviors, such as play, locomotion, andexploration.

Like other behavioral management practices, decisionsregarding the provision of physical enrichment itemsshould be based on the behavior of the species. Forexample, owl monkeys (Aotus spp.), unlike macaques,utilize nesting sites in the wild and should be providedwith some sort of nesting opportunity in captivity(Figure 6.3A). On the other hand, chimpanzees in the wildbuild a new nest each night, so captive chimpanzeesshould be provided with new nesting materials eachevening (Figure 6.3B). Physical enrichment optionsshould provide the animals with some degree of choice,control, challenge, and novelty (National ResearchCouncil, 2011). Items such as toys should be rotated ona regular basis to maximize their enrichment value

(A)

(B)

FIGURE 6.3 Nesting opportunities for (A) owl monkeys (Aotus

nancymaae) and (B) chimpanzees (Pan troglodytes). (Photos courtesy of

The University of Texas MD Anderson Cancer Center.)


(Rawlins et al., 2004). However, the handling and animalmanipulations related to changing items too frequentlycan be stressful for stress-sensitive or neophobic individ-uals (National Research Council, 2011).

Certain physical enrichment items have been found toprovide some benefits to some individuals. Manipulableitems such as toys have been found to reduce certainabnormal behaviors in some studies (Kessel and Brent,1998), while other studies found no discernible effect of thedevices on abnormal behavior (Line, 1991) or found thatthe benefit was limited to only those periods when theapparatus was present (Lutz and Novak, 2005). NHPs mayshow fairly rapid habituation to some types of physicalenrichment, but other types, such as destructible items, mayhave longer-lasting effects (Pruetz and Bloomsmith, 1992).Visual barriers can reduce aggression in group-housedanimals (Reinhardt, 1991), but in another study thesebarriers were found to have the opposite effect when adultfemale macaques were able to get out of sight of the adultmale (Erwin et al., 1979). Perches can also help to reduceaggression in group-housed NHPs (Nakamichi and Asa-numa, 1998), and flooring substrates, such as bedding orgrass, have reduced over-grooming behavior (Beisner andIsbell, 2008).

The biggest drawbacks associated with the imple-mentation of physical enrichment strategies are related tosafety; these strategies have the potential for increasing theprobability of injury or illness (see the section “SafetyConcerns” below). Physical enrichment can also lead toincreased trauma due to competitive aggression if onlylimited quantities of enrichment opportunities are providedto a group (Honess and Marin, 2006).

Habituation is another common drawback for manytypes of physical enrichment. Items such as toys are oftenused by the primates only for very short periods, typicallythe few moments immediately following their presentation.Items such as perches, nest boxes, and swings are less proneto habituation than are toys (Bayne et al., 1992). Frequentrotation of physical enhancements can maximize theirvalue while minimizing the probability that the subjectswill habituate to them. Concerns have also been expressedthat some physical enrichment items such as toys may actas fomites, which could have unintended consequences forresearch outcomes, particularly for studies of infectiousdiseases (Bayne et al., 1993b). A final and quite importantdrawback to the use of small, unattached physical enrich-ment devices (like toys, bedding, and nesting materials) inindoor rooms is that they can clog drains. Although mostfacilities have Standard Operating Procedures that requirethat items like toys and nesting materials NOT be washeddown the drain, in practice this occurs with problematicregularity. Appropriate personnel training must be in placeto ensure that such human behavior does not put unneces-sary restrictions on the provision of enrichment.


Sensory Enrichment

All primates in the wild are exposed to a variety of sensorystimuli, including visual, auditory, tactile, gustatory, andolfactory information. The diversity of such stimuli is oftendramatically reduced in laboratory conditions. Sensoryenrichment is a way to provide animals with opportunitiesto experience naturalistic stimulation of all five senses. Aswith most other types of enrichment, it is important to takethe species’ capabilities into account when providingsensory enrichment; olfactory stimuli are far more impor-tant to certain NHP species than they are to others.

Auditory enrichment often consists of music or naturalhabitat sounds (e.g. “jungle sounds”). The provision ofauditory stimuli can be considered as enrichment, but mayalso be used to mask other, assumedly stressful sounds(carts going down the hall, animal handling and/or cagecleaning procedures, etc.). Human studies have found thatcertain kinds of music can produce a calming effect onpeople (Wells, 2009). However, the results in NHP studiesare less clear. Certain types of music have been found toreduce aggression in gorillas (Wells, 2009) and chimpan-zees (Howell et al., 2003), yet when given a choice,chimpanzees, tamarins, and marmosets chose silence over“music” (Richardson et al., 2006). NHPs may prefernaturalistic sounds to human music; tamarins exposed tomusic based on species-specific affiliative vocalizationsresponded with calm behavior (Snowdon and Teie, 2010).

Visual enrichment can take a variety of forms,including videos, brightly colored mobiles, computerscreen savers and similar applications, or even somethingas simple as a window. Chimpanzees and several monkeyspecies will spend time watching videos (Platt and Novak,1997; Bloomsmith and Lambeth, 2000), with individuallyhoused primates spending more time “actively” watchingthan is the case with socially housed animals (Bloom-smith and Lambeth, 2000). Although NHPs will watchvideos, the presentation of uncontrollable video stimulihas not been shown to have a dramatic effect on eitherpromoting species-typical behavior or reducing abnormalbehavior (Platt and Novak, 1997; Bloomsmith and Lam-beth, 2000).

Olfactory enrichment, such as candles, scented oils, andsimilar items, are infrequently provided to Old Worldprimates and great apes, since these species are notparticularly sensitive to olfactory stimuli. New WorldMonkeys and prosimians, on the other hand, are quitesensitive to olfactory cues, and species-appropriate olfac-tory enrichment has been utilized with some of thesespecies (Andrews and Iliff, 2005; Ablard and Nekaris,2008). For “scent marking” species, this may include theleaving of dirty (i.e. scent marked) materials in otherwiseclean enclosures. It should be noted that some personnel areadversely affected by particular fragrances.

Food-related Enrichment

Most nonhuman primates spend much of their day in food-related activities, including foraging for, acquiring, pro-cessing, and eating their food. This time is greatly reducedin a laboratory setting, where food is typically providedonly once or twice a day. Food and foraging enrichment areways to provide laboratory NHPs with opportunities toincrease the amount of time they spend searching for,processing, and eating their diet, and is one of the mostcommonly utilized forms of enrichment (Baker et al.,2007).

Food-related enrichment encompasses a wide variety ofenhancements. Ideally, it should encourage foraging andincrease the amount of time primates spend in the searchfor food and its acquisition, processing, and/or consump-tion. Food-related enrichment appears to be less susceptibleto the effects of habituation than are many other types ofenrichment. Examples of ways to provide opportunities toincrease time spent in species-appropriate, food-relatedbehaviors include scattering food on substrates, hidingfood, and providing treats frozen in ice. This kind ofenrichment has been found to reduce aggression in a varietyof species, including macaques, tamarins, squirrelmonkeys, lemurs, marmosets, and chimpanzees (Baker,1997; Honess and Marin, 2006; Maloney et al., 2006).Another commonly used feeding enhancement strategy isto put food items in specially designed foraging devices,such as foraging boards or puzzle feeders, which requireNHPs to work to obtain the food (Crockett et al., 2001;Honess and Marin, 2006). These foraging devices havebeen found to decrease the occurrence of some undesirablebehaviors, including stereotypies and overgrooming(Bayne, 1991; Pyle et al., 2002), when kept on the cagescontinuously. However, these beneficial effects tend todissipate when the device is empty or removed from thecage (Lutz and Novak, 2005). Adding a small toy toa feeding device can increase the amount of time that theyare utilized (Rawlins et al., 2004).

There are relatively few problems associated with theprovision of feeding and foraging enrichment. Obviously,treats and/or high calorie food items should be provided inmoderation to prevent the development of nutritionalimbalances or obesity as a function of enrichment. Indi-vidual primates may have food allergies or bad reactions tospecific items (National Research Council, 2011), althoughthat is infrequent. Some foods may be incompatible withresearch protocols. For example, foods with phytoestrogensmight be contraindicated for animals participating inreproductive studies. Foraging devices may increaseaggression if provided in limited numbers to social groupsof animals (Honess and Marin, 2006). On the other hand,devices may be monopolized by dominant individuals asthey demonstrate their dominance status, and this reduces


the opportunity for other animals to benefit from theenrichment activity. When presenting foraging enrichmentopportunities for many animals within a group, multipledevices should be provided to reduce the chance formonopolization.

Occupational Enrichment

Occupational enrichment provides opportunities for theprimates to obtain physical and/or mental stimulation andincludes exercise and cognitive tasks. Exercise can beprovided by housing animals in large outdoor groups(e.g. corrals) with species-appropriate furnishings or byproviding access to exercise cages for NHPs living insmaller enclosures (Storey et al., 2000). Exercise or activitycages are commercially available or can be modified fromexisting cages. Additionally, many macaque speciesinteract with water sources in their natural environments,and therefore, providing water in pools, tubs, or tanks canbe utilized as occupational enrichment (Robins and Waitt,2011).

Cognitive tasks involving computers or related tech-nology are often used to collect data for hypothesis-drivenpsychological studies but can in certain circumstances beused for enrichment as well (Fagot and Paleressompoulle,2009; Fagot and Bonte, 2010). Primates can respond tosatisfy the experimental criteria, but they may also be ableto respond freely on the same or similar equipment, thusproviding them with the opportunity to control variousaspects of their treatment, one of the primary advantages ofoccupational enrichment. Computerized tasks can providemany enrichment opportunities, including “games” inwhich the subject uses a joystick to move the computer’scursor into a specific part of the screen to get a reward (Plattand Novak, 1997). These kinds of experimental procedurescan be viewed as enrichment opportunities when theyprovide a sense of control and choice. On the other hand,tests in which the animals are water or food restricted maynot be enriching to the animals (Prescott et al., 2010). Inorder to truly determine whether these sorts of tasks areenriching to the animal, the behavior of the animal shouldbe carefully documented and evaluated.

Compared with the number of studies on other forms ofenrichment, relatively few empirical studies have evaluatedthe efficacy of occupational enrichment. Access to exercisehas been shown to reduce behavioral problems in a varietyof species. Activity cages have also been shown to reduceabnormal behaviors, such as stereotypy (Storey et al.,2000). However, many of the behavioral problems returnedonce the animals were placed back in their home cage.Computer tasks have been found to influence levels ofstereotypies and other behavioral problems in rhesus andbonnet macaques (Washburn and Rumbaugh, 1992;Lincoln et al., 1995; Platt and Novak, 1997) and may be

useful as enrichment for zoo-housed orangutans (Tarouet al., 2004).

Assessing the Value of Enrichment

Enrichment should be empirically evaluated on a regularbasis to determine if it is achieving its intended goals.There are several ways to assess the efficacy of enrich-ment. One common method is to directly examine thebehavior of the subjects. Effective enrichment opportuni-ties should result in increased levels of species-typicalbehaviors, such as social grooming, foraging, and playing,while simultaneously resulting in decreased levels ofabnormal behaviors. Abnormal behaviors include behav-iors that do not occur in wild conspecifics and behaviorsthat occur at abnormal levels in captive NHPs (comparedwith their counterparts in the wild) (Poole, 1988). Forinstance, self-injurious behavior is virtually absent in wildprimates. While self-grooming occurs in wild populationsof rhesus, it is unlikely to comprise 20e30% of a wildrhesus’ activity profile as it may among singly cagedrhesus monkeys.

Additionally, one can examine indirect indicators ofbehavior. For example, if an animal is presented withenrichment (e.g. a grooming board) that is intended toprovide alternative activities to over-grooming, one cansimply monitor the quality of the hair coat (e.g. Runesonet al., 2011) rather than directly investing the time neces-sary to observe an increase in enrichment use and/ora decrease in self-grooming behavior. The same type ofapproach may be applied to enrichment strategies designedto minimize self-injurious behavior (e.g. look for fewerwounds).

Another way in which we can assess the value ofenrichment is to evaluate physiological parameters, such ascortisol, heart rate, and immune function. Effectiveenrichment opportunities should result in animals thatexhibit fewer physiological responses that are indicative ofthe adverse consequences of stress (see Chapter 7). It maybe valuable to focus such assessment efforts on the physi-ological indices that are most relevant to the experimentalrole of the animal. For instance, if an animal is to partici-pate in an experiment that assesses cell-mediated immuneresponses, it would be appropriate to assess the effects ofenrichment on those same parameters (Schapiro et al.,2000).

Finally, we can let the animals demonstrate the value ofenrichment opportunities. This can be done through choicetests in which the primates are provided with variousoptions and can choose whether or not they want toparticipate. Such choice tests are rare but can provideimportant information. In one such test (Crockett et al.,1997), adult M. fascicularis were trained to open a solidpanel to gain access to grooming-contact panels. Males in


this study were significantly more likely to open the panelwhen the other animal was female compared to a familiaror unfamiliar male. Thus, the social needs of malesappeared to be better met by female partners than malepartners. Additionally, consumer demand approaches canbe used to determine how hard primates are willing to workto gain access to specific enrichment opportunities(Schapiro and Lambeth, 2007).

It is important to point out that enrichment may notalways produce the results we want, such as an increase inspecies-typical behaviors. There can be a great deal ofvariation among individuals with respect to use of enrich-ment devices. Individual primates may not use certainenrichment devices because the devices are too challengingfor them, the object is simply not of interest to them, orsocial factors prevent them from accessing the device.However, providing the enrichment still affords theseindividuals the option of whether to use them. Along thesame lines, enrichment does not always reduce abnormalbehaviors. It can be very difficult to ameliorate manybehavioral problems, such as self-injurious behavior andstereotypies, once they have begun (see Chapter 7).Therefore, a key focus of behavioral management shouldbe on prevention. Behavioral management strategies thatfocus on prevention include appropriate rearing strategies(e.g. rearing infants with their mothers, preferably ina social group) and training staff to properly interact withthe primates.

There are costs and benefits associated with all behav-ioral management strategies. While some of these costs andbenefits are inherent, others are a function of the institutionand research project and may change over time. Costs areoften measured in terms of monetary expenditures associ-ated with purchasing the enrichment as well as personneltime. Other costs include the potential for injury or illness(Baer, 1998; Bayne, 2005). Benefits are typically discussedin terms of increased psychological well-being or welfarefor the subjects, although there can be other, less obviousbenefits from effective enrichment and behavioralmanagement. As is discussed below, training primates canreduce the time it takes to perform basic husbandry taskssuch as weighing or shifting animals between locations(Bassett et al., 2003; Veeder et al., 2009). If costebenefitanalyses reveal that the costs associated with the provisionof a particular enhancement outweigh the benefits of thatenhancement, then it is obvious that its use should bereconsidered. For example, many facilities utilizecommercially available foraging devices as part of theirenrichment program. Some of these devices are expensive,take a great deal of time to fill and clean (i.e. high cost), andare emptied by the NHPs within minutes of receiving them(i.e. low benefit). Behavioral management resources maybe better spent on other forms of enrichment, such assocializing animals (e.g. Baker et al., 2007).

Safety Concerns

Enrichment needs to be safe for the animals, for the care-givers, and for other staff (Baer, 1998; Young, 2003).Enrichment objects should not have sharp edges. Routinemonitoring of enrichment devices is required to ensurebroken enrichment items are removed. Chains or ropesutilized to hang objects should be short enough or of wideenough diameter to ensure that accidental choking orentrapment of a limb is extremely unlikely. They can alsobe covered with a length of PVC pipe or other hose-typematerial to reduce the risk of entrapment. Enrichmentobjects should be able to be properly cleaned and dis-infected to minimize the chance that they will act as fomites(Bayne et al., 1993b). Further, even simple toys can bedangerous if ingested. Some items used as enrichment haveresulted in an animal’s death from intestinal impaction(e.g. Hahn et al., 2000). Items that contain long fibers (suchas sisal rope or burlap) should be avoided and replaced withother materials, and animals should be observed to ensurethat they are not consuming these items. In general, newenrichment items should be observed in a sample of NHPsbefore widespread adoption to reduce the chance of injury.

In addition to considering safety concerns regarding theanimals, it is equally important to take safety concerns ofthe staff into account. Many enrichment and trainingpractices necessitate close proximity to nonhumanprimates, thus introducing the potential for scratches orbites (National Research Council, 1997). Therefore, allinstitutional safety protocols must be followed whenproviding enrichment. Proper personal protective equip-ment (PPE) including protective clothing, gloves and safetygoggles, or a face shield should be worn. Safety issuesrelated to the care of nonhuman primates are covered indetail elsewhere (see Chapter 18; National ResearchCouncil, 1997).

Documentation

Documentation is an important element of effectivebehavioral management programs for laboratory primates.Behavioral management “records” should include whatenrichment is given, how often it is given, and someassessment of whether it is used by the primates. Thisdocumentation should be routinely reviewed to ensure thatthe facility’s enhancement plan is being adequatelyimplemented. Documentation should be maintained onsocialization, particularly in situations where primates areliving in indoor cages. This documentation should includethe identities of primates that have been introduced to oneanother, the outcome of introduction attempts (i.e.successful or not), and the reason pairs or small groups havebeen separated from one another. For recording enrichmentthat has been provided, it may be practical to document


behavioral management efforts at the level of the animalhousing area/room, social group or the colony type(conventional, specific pathogen free (SPF), etc.), ratherthan having records for each individual. Figure 6.4 illus-trates an example of enrichment documentation at theUniversity of Texas, MD Anderson Cancer Center.

There are several ways in which documentation can beaccomplished. In some facilities, daily observation sheetsare used to document the provision of enrichment and otherbehavioral management strategies. Other facilities collectquantified, reliable observational behavioral data on indi-viduals, including information on both abnormal andnormal behavior. This information is then often used todocument behavioral problems among the NHPs and todetermine the effectiveness of therapeutic interventions.Handheld devices such as personal digital assistants(PDAs) or wireless computer tablets can allow behavioralobservations to be seamlessly integrated into databasescontaining the animal records. It is possible to maintaina “behavioral record” for each animal that is similar to and/or part of the animal’s medical record (Jennings et al.2009). While not every facility maintains these sorts ofrecords, most facilities are moving toward this goal (seeChapter 11). The National Primate Research Centers aremoving towards harmonizing animal care records so thatdata can be shared across facilities.

Because primates often behave differently in the pres-ence of human observers than they do when no humans arepresent (Line, 1995; Iredale et al., 2010), videocameras canbe an effective tool for documenting behavior. Behavioraldata recorded by videocameras and subsequently analyzedcan be effective for determining whether subjects are usingenrichment and if enrichment is altering behavior.However, videotaped behavioral data are often quite time-consuming and tedious to analyze. Further, videocameraequipment can be novel and even potentially aversive tosome individuals (e.g. camera lenses can look like a big eyeand power cords can appear similar to snakes), and there-fore, animals should be habituated to the presence of theseitems before they are used to collect data.

POSITIVE REINFORCEMENT TRAINING

Like environmental enrichment, positive reinforcementtraining (PRT) should be an important component ofa comprehensive behavioral management program. PRTtechniques take advantage of the stimulus-response-reinforcement contingency that is a principle of operantconditioning (Skinner, 1938). Positive reinforcement refersto the provision of a “reward” (reinforcement) that is likelyto increase the frequency of the target behavior (response)once a signal (stimulus) has been given. Primates trainedusing PRT techniques are typically asked to performa behavior (e.g. “present a thigh”) and are then given

a desired food item immediately after they present the thighto the trainer. There is no coercion or physical restraintused, and there is no consequence to the animal if theychoose not to participate. Laule and colleagues (Lauleet al., 2003) have presented a detailed description of theapplication of PRT for captive primates.

PRT as Refinement

Positive reinforcement training can reduce the stressassociated with common management and researchprocedures (Bassett et al., 2003; Laule et al., 2003;Schapiro et al., 2003), and as such represents a significantrefinement, according to the 3Rs presented by Russell andBurch (Russell and Burch, 1959). PRT desensitizes animalsto potentially stressful stimuli, such as injections (Schapiroet al., 2005), thereby reducing fear and anxiety related tothese procedures. In addition, by allowing individuals tocooperate with the procedures (i.e. they can choosewhether they want to participate), positive reinforcementtraining gives animals greater control over their environ-ment (Laule et al., 2003), a factor that typically reducesstress (Mineka et al., 1986). Studies have demonstratedreductions in both physiological and behavioral indices ofstress with the use of PRT. Chimpanzees trained tovoluntarily accept an injection of anesthetic (Telazol�) hadlower hematological indicators of stress (e.g. neutrophilsand white blood cells, glucose levels) than untrainedchimpanzees had (Lambeth et al., 2006). Training has alsobeen shown to reduce the animals’ stress for proceduresother than the task for which they were trained. Marmosetstrained to provide urine samples displayed fewer behav-ioral indices of stress (e.g. scratching) in response tocapture and weighing than untrained counterparts (Bassettet al., 2003). Savastano and colleagues (Savastano et al.,2003) reported a decrease in threat behavior toward care-takers after initiation of a PRT program for several speciesof New World monkeys. Results of these studies supportthe idea that PRT can promote overall well-being andwelfare.

There are other ways in which PRT is a useful refine-ment. Training can reduce the need for sedation forprocedures, such as venipuncture and weighing. Stressassociated with pharmacological agents such as ketamineHCl, commonly used for sedating monkeys, have beencorrelated with increased cortisol levels (Crockett et al.,1993, 2000), decreases in leukocytes (Hall and Everds,2003), and decreases in appetite after recovery (Crockettet al., 2000; Springer and Baker, 2007) in various macaquespecies. All of these changes can adversely affect variousresearch paradigms. Training can also allow researchanimals to be socially housed; trained animals are easier toaccess, even for biological sampling. By reducing the stressassociated with husbandry and handling procedures,

FIGURE 6.4 Example of a daily check sheet used to document the provision of enrichment. This sheet was developed for use with caged rhesus

macaques but can be adapted for use with other species as well as group-housed NHPs.


FIGURE 6.4 (continued).


interindividual variation may also be reduced, enhancingthe use of NHPs as research subjects. This increases thevalue of NHPs as biomedical models and can effectivelyreduce the number of NHPs required for certain investi-gations (which serves as a Reduction, another of the 3Rs(Russell and Burch, 1959)).

PRT and Husbandry, Veterinary andResearch Procedures

Primates have been successfully trained to perform varioushusbandry, veterinary, and research procedures. One of themost commonly trained behaviors is “shifting,” or moving

FIGURE 6.5 Adult male rhesus macaque (Macaca mulatta) with arm

in blood sleeve. The monkey was trained to put his arm in the blood

sleeve and hold onto the peg at the distal end until released by the trainer.

(Photo reprinted from Coleman et al. (2008, figure 1, p. 38) with

permission from the Journal of the American Association of Laboratory

Animal Science.)


animal(s) from one area to another. Shifting can take manyforms, including large groups moving on command fromtheir indoor enclosure to their outdoor enclosure or indi-vidual animals moving from their home cage to a transferbox. A variety of species have been trained to shift,including marmosets (McKinley et al., 2003), chimpanzees(Bloomsmith et al., 1998), and mangabeys (Veeder et al.,2009). Primates have also been trained to: (1) come to thefront of the cage or enclosure; (2) present a specific bodypart; and (3) remain stationary for veterinary or researchprocedures, such as an injection (Priest, 1991; Videan et al.,2005), a medical exam (Schapiro et al., 2005), or bloodpressure measurement (Turkkan, 1990). Primates havebeen trained to take oral medication (Klaiber-Schuh andWelker, 1997), and to give semen or urine samples(Schapiro et al., 2005). Both rhesus monkeys and chim-panzees have been trained to put an arm in a blood sleeveand remain stationary for venipuncture (Coleman et al.,2008, Figure 6.5). In this study, both the rhesus andchimpanzees reliably performed this task after approxi-mately 6 months of focused training.

Not only does training reduce stress for the animals, butit can also reduce stress for the people working with theanimals. Working with cooperative animals is safer and lesstime-consuming for caregivers and technicians than isworking with highly stressed and potentially reactiveanimals (Bloomsmith, 1992). While training can initiallybe time-consuming, the time invested is likely to berecovered once the animals are trained. For example,Veeder and colleagues (Veeder et al., 2009) found that

training mangabeys to shift on command saved approxi-mately one hour of technician time a day and that the initialtraining investment was recovered within about a month.Other procedures, such as weighing marmosets, takessignificantly less time with trained monkeys than untrainedmonkeys (McKinley et al., 2003).

PRT as Enrichment

Training can also be an effective form of occupationalenrichment. PRT was found to reduce the incidence ofstereotypies in several NHP species (Raper et al., 2002;Bourgeois and Brent, 2005; Coleman and Maier, 2010),although this is not a universal finding (Baker et al., 2009).Further, training can be used to decrease aggression ingroup-housed animals. Bloomsmith and colleagues(Bloomsmith et al., 1994) used cooperative feeding tech-niques to train dominant chimpanzees to remain stationaryduring feeding time and allow subordinates to feed, thusdecreasing food-related aggression. In this case, thedominant animals received extra treats for theircooperation.

Fewer studies have examined the efficacy of PRT onpromoting normal behavior. PRT has been shown toincrease prosocial behavior in group-housed chimpanzees(Pomerantz and Terkel, 2009) and baboons (Desmond,1994) in a zoo setting. It has also been used to promotesocial behavior (e.g. grooming and play) in group-housedrhesus macaques (Schapiro et al., 2001). In this study,female rhesus were categorized as either “high affiliators”or “low affiliators” based on their level of social interaction.PRT was used to successfully train the “low affiliators” tomove closer to and engage in social behavior with othergroup members. These effects extended to periods beyondthe actual training sessions (Schapiro et al., 2001).

While there are many benefits associated with estab-lishing a positive-reinforcement training program fornonhuman primates, there can be inherent difficulties aswell. Training often involves an initial investment of timeand monetary resources. In addition, there is a great deal ofvariation among individual NHPs with respect to theirtraining potential. Some subjects are relatively easy to trainand learn tasks quickly, whereas others require significantlymore time and effort. These differences may be especiallyproblematic if research protocols require all subjects to betrained. There are interspecific differences in behavior thatcan affect how individuals learn tasks (Savastano et al.,2003). In addition, there are also intraspecific differences inlearning abilities among individuals. Monkeys have uniquepersonalities, and strategies that work for one individualmay not work for all. For example, monkeys with relativelyshort attention spans may do better with shorter, morefrequent training sessions (Savastano et al., 2003). Shyanimals can be more difficult to train than more exploratory


animals (Coleman et al., 2005). Further, proper trainingrequires a great deal of practice, patience, and skill on thepart of the trainer. Consistency among all who are workingwith the animal is also important in training. If two trainersuse different methodologies when trying to train a subject,that will send mixed signals to the subject, making itdifficult for the subject to learn the task.

Animal training is becoming a more prominentcomponent of behavioral management programs atbiomedical facilities and is encouraged in the 2011 revi-sion to the Guide (National Research Council, 2011);however, formal training programs are still far fromuniversal. In their 2007 survey of 22 primate facilities,Baker and colleagues (Baker et al., 2007) found thatwhereas 55% of facilities reported utilizing PRT, only 9%had dedicated trainers. Further, training in the USA isoften focused on chimpanzees and rhesus macaques. Arecent study of training in the UK showed that themajority of training in research or breeding facilities in theUK also involved rhesus macaques (Prescott andBuchanan-Smith, 2007). However, training can benefitmany other laboratory-housed primates and should beextended to other species. Several resources for trainingare available (Table 6.1).

BALANCING PSYCHOLOGICALWELL-BEING AND RESEARCH NEEDS

An important goal of behavioral management programs inprimate laboratories is to balance the psychological well-being and welfare needs of the research subjects with theneeds of hypothesis-driven research studies. Althoughbehavioral management techniques generally improve thepsychological well-being of primates and thereby enhancethe value of the animals as research models, there are timeswhen research protocols may preclude the provision ofcertain types of behavioral management enhancements. Forexample, it may be difficult to provide some types offeeding enrichment to NHPs participating in studies inwhich food consumption or caloric intake is measuredprecisely. However, it may be possible to use noncaloricitems as part of the feeding enrichment program (e.g. icecubes, commercially available no calorie treats) and/or toprovide all of the animal’s daily food ration in foragingdevices. In addition, for nonhuman primates that may beparticipating in research projects conducted under theguidelines of Good Laboratory Practice (GLP), allenhancements, and especially food items, must be “certi-fied” to meet the quality control requirements of suchresearch projects.

Many biomedical research studies are completed whiletheir primate subjects are socially housed, but most primatelaboratories report that research protocols are a constraint

to implementing social housing (Baker et al., 2007).Providing captive primates with the opportunity to interactwith compatible conspecific(s) is one of the most beneficialcomponents of an effective behavioral managementprogram (Schapiro et al., 1996a,b). Therefore, it is imper-ative that any research project that could be accomplishedwith socially housed primate subjects, should be. Even ifsubjects cannot be housed in full contact at all times,socialization options still exist. For example, the use ofgrooming-contact caging (see the section “Social enrich-ment” above) allows some social interaction for primatesassigned to research protocols that preclude full socialcontact (Crockett et al., 1997). Intermittent full socialcontact is another option for studies that cannot beaccomplished with full-time, full-contact social housing.There are many different intermittent contact options,including continuous social contact for a specific portion ofeach day or night or continuous social contact during somephases of the study but not others (e.g. after inoculation orchallenge). Even though these strategies involve repeatedseparations and reunions, Baker and colleagues (Bakeret al., 2008) have found them to be beneficial for adultrhesus macaques. These options may be especially valuablewhen primates are participating in protocols that require theregular collection of biological samples (e.g. urine)(Crockett et al., 1994). Intermittent social housing may alsobe beneficial for nursery-reared infant NHPs (Ruppenthalet al., 1991; although see Rommeck et al., 2011 for draw-backs). While more work needs to be done to determinehow much contact time is necessary to benefit the monkeysin ways similar to continuous social housing, it is likely thatbeing together with a partner for part of the time is betterthan not having a partner at all (e.g. Baker et al., 2008).However, intermittent pair housing should only be used ifcontinuous full contact social housing options are notavailable.

The housing of infant and juvenile primates is anothersituation in which the requirements related to psychologicalwell-being and welfare must be carefully balanced withrequirements related to research projects. It is well estab-lished that social deprivation of young primates contributesto severe, lifelong behavioral problems for these animals.These behavioral problems include, but are not limited tothe performance of, stereotyped, self-injurious, and sociallyinappropriate behaviors (Novak and Sackett, 2006; seeChapter 7). For this reason, studies that purport to requiresingle housing for young, developing NHPs should beclosely scrutinized during the protocol review process thatin the USA is typically conducted by the InstitutionalAnimal Care and Use Committee (IACUC). The scientificjustification must be exceptionally strong for any protocolsto be approved that involve young, singly housed NHPs.This is consistent with the USDA requirement for specialattention to young primates (USDA, 1991).


As detailed above, PRT techniques can also be used toaddress the balance between the psychological needs ofprimates and the needs of the research protocol. Trainingcan reduce stress and fear associated with some experi-mental manipulations and can facilitate access to animalsfor research procedures. Other forms of training can also bebeneficial. Simple desensitization can be used to reduce thestress or fear primates experience in relation to certainhandling and research procedures (Clay et al., 2009). Othertraining processes that do not necessarily rely exclusivelyon positive reinforcement have been used to train primatesto briefly leave their large social groups for biologicalsampling (Blank et al., 1983). In this case, researchprocedures can be conducted while trained subjects arebenefiting from living in large, complex social groups.

The research protocol review process conducted by theIACUC is an important component in the process ofbalancing the psychological well-being and welfare needsof primates with their participation in biomedical researchstudies. Behavioral scientists with expertise in themanagement of primates are often members of the IACUC(Baker et al., 2007) and can objectively evaluate protocolsin terms of issues related to psychological well-being andwelfare, including enrichment, social housing, and animaltraining.

MANAGING BEHAVIORALMANAGEMENT PROGRAMS

Roles

The majority of behavioral management programs in largerprimate facilities are overseen by a behavioral scientistwith an advanced degree. At smaller facilities, enrichmentis often managed by veterinarians or colony managers.Regardless of who is overseeing the program, everyoneworking with the NHPs has a role in the behavioralmanagement process. Behavioral staff, if present, typicallyadminister the program (Baker et al., 2007). They may: (1)provide enrichment; (2) be responsible for training the staffto understand behavior and to interact appropriately withthe NHPs; and (3) be responsible for evaluating theprogram. The caregiving staff also play an important role inthe behavioral management program. Because caregiversoften spend more time with the animals than otheremployees, they provide important feedback on the way inwhich animals are responding to enrichment, a socialpartner, or another type of behavioral managementmanipulation. Caregivers are often the first to notice subtlechanges in animal behavior that might indicate compro-mised well-being and/or health. Caregivers may alsoparticipate in positive reinforcement training (Prescott andBuchanan-Smith, 2007). Therefore, anyone involvedin animal care (including veterinary, husbandry and

investigative staff) should receive training in the behaviorof the species with which they work (National ResearchCouncil, 2011). Such training should minimally includebehaviors that are normal for the species, behaviors that areabnormal for the species, and how humans can influencethose behaviors (e.g. how to work with monkeys). Carestaff should also receive information about how to identifypain or distress in their animals (Coleman, 2011). Thistraining should be repeated periodically. The Office ofLaboratory Animal Welfare (OLAW) through the NIH hasfreely available downloads about primate behavior (http://grants.nih.gov/grants/olaw/Enrichment_for_Nonhuman_Primates.pdf).

Behavioral Management and theInstitutional Animal Care and UseCommittee (IACUC)

As mentioned previously, the behavioral management plan(or environmental enrichment plan) and the IACUC ata facility housing NHPs should be strongly integrated. TheIACUC is empowered to exempt, for scientific reasons, anindividual primate from a specific part of a facility’sbehavioral management plan. It is therefore, the responsi-bility of the IACUC to determine whether or not requests forexemptions are scientifically valid (e.g. Thom and Crockett,2008). For example, requests to exempt animals from socialhousing simply for convenience should not be approved.Further, the IACUC is responsible for keeping up withcurrently accepted practices. IACUCs should promote theuse of PRT and other beneficial refinements wheneverappropriate.

Another role of the IACUC is to evaluate the enrichmentprogram. The Animal Welfare regulations mandate that theIACUC review the institution’s program for humane careand use of animals at least once every 6 months (USDA,1991). This evaluation should include the enrichmentprogram. This is echoed in the 2011 revisions to the Guide,which also states that the IACUC is “responsible for over-sight and evaluation of the entire [animal care] Program”(National Research Council, 2011). These IACUC reviewsshould ensure that enrichment programs are beneficial toanimal well-being (National Research Council, 2011).

CONCLUSIONS

The passage of the 1985 amendment to the Animal WelfareAct in the USA and similar regulations in other countrieshave resulted in significant refinements in the ways thatNHPs are handled and treated in captivity. Many of theseimprovements have occurred within the context of behav-ioral management. Prior to the implementation of theAnimal Welfare regulations in 1991, behavioral


management units at primate facilities in the USA wererare; today they are ubiquitous (Baker et al., 2007). Manyfacilities in the USA, Europe, and elsewhere currentlyhousing NHPs, devote substantial resources to enrichment,socialization, and training techniques that provide theanimals with opportunities to perform species-typicalbehaviors.

Primates will continue to play a key role in many typesof hypothesis-driven and applied research projects. Toprovide the most reliable and valid data from these animals,NHPs living in research facilities must be provided with thebest living conditions possible within the framework of theresearch endeavor. Behavioral management programs arean important component of addressing this critical need.

Providing enrichment and other behavioral manage-ment techniques is a dynamic process that must becontinuously evaluated and refined. There has beena dramatic increase in the number of rigorous scientificpapers addressing various aspects of behavioral manage-ment of captive primates since the Animal Welfare regu-lations were promulgated. This information should beincorporated into enrichment programs to the greatestextent possible. Empirically based and carefully evaluatedbehavioral management strategies may significantly refinethe scientific endeavor. Nonhuman primates whosepsychological well-being and welfare have been enhancedby an effective behavioral management program representa superior, better-defined NHP model for participation inresearch.

ACKNOWLEDGMENTS

Support is acknowledged from the Oregon National Primate Research

Center, RR 00163 (KC), the Yerkes National Primate Research

Center, RR-00165 (MAB), and the Washington National Primate

Research Center, RR-00166 (CMC). J.L.W. is supported by the

Intramural Research Program of the NIH Division of Veterinary

Resources. The views and opinions provided by J.L.W. do not reflect

the official policy or positions of the NIH, Department of Health and

Human Services, or United States Government.

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