American Journal of Primatology 73:220–225 (2011)

COMMENTARY

Caring for Nonhuman Primates in Biomedical Research Facilities: Scientific,Moral and Emotional Considerations

KRISTINE COLEMAN�

Oregon National Primate Research Center, Beaverton, Oregon

Animal care for nonhuman primates (NHPs) in biomedical facilities has undergone major changes inthe past few decades. Today, most primate facilities have dedicated and highly trained animal caretechnicians who go to great efforts to ensure the physiological and psychological well being of theprimates in their charge. These caretakers work closely with the animals and, as a result, often developstrong relationships with them. Once discouraged and considered a potential threat to scientificobjectivity, such positive relationships are now seen as important components to animal care. Positiveinteractions between caretakers and primates can benefit the primates by reducing their stress andimproving their overall well being which can, in turn, help the scientific endeavor. Further, providingthe best possible care is our moral responsibility. However, there can also be emotional costs associatedwith caring for NHPs in research facilities, particularly when animals become ill or have to beeuthanized. Facilities can do much to help ease this conflict. High-quality and conscientious animal careis good for the animals, science, and public perception of research facilities. Am. J. Primatol.73:220–225, 2011. r 2010 Wiley-Liss, Inc.

Key words: animal care; positive reinforcement training; animal well-being; animal memorial

INTRODUCTION

Animal care for nonhuman primates [NHPs] inbiomedical facilities has undergone major changes inthe past few decades. At the start of the 20thcentury, there were few mandatory requirementsfor captive animals in research environments. Manyresearchers and veterinarians did not believe thatanimals had complex mental states or could feel pain.This attitude has changed, as the scientific commu-nity has learned more about animal behavior and theeffects of research and husbandry practices onbehavior and physiology of research subjects.

Today, animal care practice consists of morethan simply feeding animals and removing waste.Biomedical facilities have dedicated and highlytrained animal care technicians who are taught tonotice signs of pain and distress in animals. Mostprimate facilities have at least one full time veter-inarian; the larger primate centers typically haveseveral, some of whom are specialists in certainareas, such as dentistry or surgery. Furthermore, anincreasing number of primate facilities have one ormore behaviorists who attend to the psychologicalwell being of the primates. In many ways, the carethat is provided to NHPs at research facilities isanalogous to that enjoyed by well-insured citizens ofthe United States. Such high-quality care requiresthe dedication and devotion of those workingwith the primates, especially the caretakers whooften form very close relationships with these

animals. Although this level of care is vital to thescientific endeavor, there are inherent and undeniableethical and emotional challenges and dilemmas asso-ciated with forming close relationships with subjects ofanimal research. This commentary will discuss someof the scientific, moral, and emotional issues associatedwith caring for NHPs in research facilities.

SCIENTIFIC CONSIDERATIONS OF CARING

Simply put, high-quality science depends onhigh-quality animal care. It has long been estab-lished that animals who are sick or in pain or distressare not reliable subjects for most scientific studies.Psychosocial stressors can alter the hypothalamic–pituitary–adrenal axis as well as cardiovascularfunction [e.g. Gerber et al., 2002; von Holst, 1998]in NHPs and other laboratory animals. Reproductiveand immunological functions may also be compro-mised by emotional stress [Bethea et al., 2008;

Published online 23 June 2010 in Wiley Online Library (wileyonlinelibrary.com).

DOI 10.1002/ajp.20855

Received 28 January 2010; revised 25 May 2010; revisionaccepted 29 May 2010

Contract grant sponsor: NIH; Contract grant number: RR00163.

�Correspondence to: Kristine Coleman, Oregon National Pri-mate Research Center, 505 NW 185th Ave, Beaverton, OR97006. E-mail: colemank@ohsu.edu

rr 2010 Wiley-Liss, Inc.

Rogers et al., 1999]. These physiological and im-munological changes can affect a variety of researchoutcomes. Because individuals can vary widely intheir physiological and behavioral response to stress,stress can increase experimental variability [Schapiro,2000; Weed & Raber, 2005]. Additionally, stressed oremotionally compromised animals have a greaterrisk of developing maladaptive behaviors, such asself-directed aggressive behavior [e.g. Novak, 2003],which can also adversely affect research. Therefore,high-quality animal care, which includes identifyingand reducing distress, is important for optimalscientific validity.

There are many animal care practices in placetoday that can help decrease stress and increase wellbeing for NHPs in biomedical facilities. One suchpractice is promoting a strong, positive relationshipbetween the caretaker and NHPs [Reinhardt, 1997].This relationship can be formed through positivedaily interactions, such as providing enrichment[Bayne et al., 1993] or play [Baker, 2004; Mancioccoet al., 2009]. Positive interactions with caretakerscan reduce abnormal behavior, increase speciesappropriate behaviors, such as grooming, andimprove well being for a variety of primates,including marmosets, macaques, and chimpanzees[Baker, 2004; Bayne et al., 1993; Manciocco et al.,2009; Reinhardt, 1997; Waitt et al., 2002]. Theserelationships can also promote coping skills [Rennie& Buchanan-Smith, 2006] and help mitigate stressreactivity toward novel objects or situations. Forexample, Miller and co-workers [Miller et al., 1986]found that chimpanzees were less anxious whenconfronted with novelty in the presence of theirtrusted caretaker than when the caretaker wasabsent. Furthermore, such bonds can facilitate theresearch by allowing human observers to approachanimals easily and safely [Lehman, 1992]. Primatesare more likely to sit calmly in front of their cagewhen they trust their caretakers than when they donot. This relaxed response to the presence of humanscan facilitate daily observations and health checks aswell as research procedures.

Another practice that can improve well-being forNHPs is the use of positive reinforcement training(PRT) to train animals to cooperate with commonhusbandry and research procedures, such as remainingstationary for injection. PRT is a type of trainingin which the trainer reinforces desired behaviors(e.g. presenting a body part) by rewarding the subjectwhen it performs the behavior [e.g. Pryor, 1999].These techniques have been used to successfullytrain primates to perform various tasks, such aspresent a body part for injection [Priest, 1991;Schapiro et al., 2003], take oral medications [Klaiber-Schuh & Welker, 1997], and remain stationary forvenipuncture [Coleman et al., 2008; Laule et al.,1996]. PRT techniques can reduce stress and fearassociated with common management procedures

[e.g. Bassett et al., 2003; Laule et al., 2003], and thusreduce stress-related variability in data. In addition,training can reduce the need for pharmacologicalrestraint. Ketamine HCl, an anesthetic agent com-monly used to sedate primates, has been correlatedwith increased cortisol levels [Crockett et al., 2000],decreases in leukocytes [Hall & Everds, 2003], anddecreases in appetite after recovery [Crockett et al.,2000; Springer & Baker, 2007], all of which can affectvarious research paradigms.

Promoting positive interactions between humanand NHPs can help decrease stress and improve wellbeing of NHPs. However, it must be done in athoughtful and informed manner, as it can backfireeven with the most dedicated animal care techni-cians. Although caretakers generally have the bestinterest of the animals at heart, they sometimesmake decisions based on their own perception ofwhat animals want, which is not always good for theNHP or the science. One example of this issue occurswith favoritism. Most, if not all, caretakers developparticularly strong attachments to one or a fewselected animals in their care. They often spendmore time with these favorites, providing additionaltreats or toys. Not only can this favoritism lead to adecrease in technician attentiveness to other animals[Russow, 2002], it can also have consequences for thefavorite primate and, in turn, the research. Often,the favored animal has traits or characteristics thatmake it appealing to more than one caretaker. Ifeach of these caregivers provides extra treats to aparticular NHP, it can lead to unhealthy weight gain.In addition, playing favorites with one individual in aroom can upset the dynamics in that room. At ourfacility, a favorite monkey (‘‘Sammy’’) received extratreats from his caretakers. Sammy, a relatively lowranking monkey, was located across from a dominantanimal in the room. Every time Sammy receivedtreats, the dominant monkey, who had not receivedanything, threatened him. Unable to threaten backbecause of his subordinate status, Sammy respondedby biting himself. After figuring out these dynamics,we moved the monkeys and the self-biting stopped.We also cautioned the caretakers against providingextra treats to only their favorite animal, as it canhave unintended consequences for that individual.

There are other examples of how good intentionson the part of caretakers can result in untowardoutcomes. Research subjects may be prohibited fromreceiving particular items, such as food treats orother enrichment, on certain scientific protocols.Some caretakers ‘‘feel bad’’ for NHPs with theseprotocol restrictions and secretly provide them withprohibited items. The technicians generally do thisbecause of the sympathy they feel for the NHPs, butit can have repercussions for the research. Similarly,primate infants reared in the nursery are often givenexcessive human attention by well-meaning carestaff. However, this human interaction is sometimes

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provided at the expense of providing more species-appropriate interactions with conspecifics. Primatesreared without appropriate conspecific socializationearly in development are at a higher risk ofdeveloping behavioral problems later in life [e.g.Bellanca & Crockett, 2002; Novak, 2003; Rommecket al., 2009].

Facilities can help reduce these kinds of inap-propriate, though well-intentioned, interactions byteaching technicians and caretakers about primatebehavior and how to properly interact with captiveNHPs. At our facility, we talk about these issues withnew animal care staff. We also bring up the exampleof Sammy when we train new caregivers on how tointeract with monkeys. We remind them to payattention to all the animals in the room, not justtheir favorite. We have also found it very helpful forinvestigators to explain their research protocols tocaretakers, particularly if the study involves somesort of protocol restriction. Caretakers and othersare less likely to break the protocol (e.g. providerestricted items) if they understand why the restric-tion is important to the study.

MORAL CONSIDERATIONS OF CARING

In the past few decades, there has been growingdebate about the use of animals, particularly NHPs,in the laboratory. This debate is beyond the scope ofthis commentary. However, few would disagree thatwhen animals are used in research we have a moraland ethical responsibility to provide them withhumane, high-quality care and ensure that they arefree from unnecessary pain or distress. This idea isimplicit in policy statements or guidelines of manyprofessional organizations that deal with primates inresearch facilities, including the American Society ofPrimatology [ASP, 2001], the International Prima-tological Society [IPS, 2006], the American Psycho-logical Association [APA, 1992] and the AmericanAssociation of Laboratory Animal Science [AALAS,2007].

What constitutes morally acceptable practices inanimal care is defined by the institution as well asthe community in which the institution is located.Of course there are some practices, such as animalabuse, which are not acceptable at any institution.However, research facilities have different andunique cultures, and animal care and researchpractices morally acceptable in one facility may beunacceptable in others. This point is illustrated in astudy by sociologist Arnold Arluke [Arluke &Sanders, 1996] in which he interviewed animal careand research technicians at two primate facilities. Atone facility, the technicians viewed the primates asobjects and often used intimidation and physicalstrength to get the primates to perform certain tasks(e.g. move into a transfer box). The technicians at thesecond facility treated the primates with respect and

had a great deal of empathy for them. Thesetechnicians often spent their breaks with theprimates. Not surprisingly, the health and well beingof the primates was better in the second facility thanthe first [Arluke & Sanders, 1996]. Although animalcare practices, in general, have evolved since thepublication of this study, differences in technicianattitudes as well as acceptable practices acrossprimate facilities remain. For example, some facil-ities forbid technicians from naming their primateswhile others encourage this practice as a way toimprove the human–animal bond.

There are ways in which administrators andmanagers can foster a positive culture of animal carein their facilities. Managers and supervisors directlyinfluence the work force by their hiring practices.The managers at the second facility in Arluke’s study[Arluke & Sanders, 1996] hired people who consid-ered themselves ‘‘animal people’’ and showed inter-est in the primates during interviews. Many of theirhires also had some ambivalence about using animalsin research [Arluke & Sanders, 1996]. In addition,managers and supervisors can ensure that care-takers have adequate time to interact with theprimates in their care. This time could be spentproviding enrichment, training, or engaging in otherpositive interactions with the NHPs. Because it isoften not directly related to husbandry or researchtasks, this time is often skipped when technicians arebusy. However, this time should be protected andprioritized as a long-term investment that is neces-sary for developing bonds between caretakers andprimates. Furthermore, the Institutional AnimalCare and Use Committee (IACUC) has a significantrole in setting the moral tone for the facility. TheIACUC ensures that the facility meets its moral andethical responsibilities of animal care. In addition,the IACUC is responsible for making sure that allprotocols adhere to the ‘‘Three Rs’’: Reduction,Refinement, and Replacement [Russell & Burch,1959], and has the power to prevent protocols that donot follow these principals from proceeding. TheIACUC can, therefore, influence the culture of caringwithin the institution by supporting and promotingexemplary animal care practices.

Resolving the moral issues related to primates inresearch is at least as difficult for those who work inthe field as it is for the general public, because of therelationships that are formed with the animals.Although most caretakers agree, in principle, withthe need for animals in research, they may still feelmorally conflicted about their role in it. The dualityof working with animals that are used in researchmay result in feelings of guilt or uneasiness in carestaff [Arluke, 1999]. Caretakers may feel morallyconflicted by caring for the NHPs on the one handand participating in invasive studies on them on theother. They may feel particularly conflicted if they donot see how the study will advance human or animal

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health. Even with knowledge about a study’s greatergood, caretakers may still feel uneasy if a study is notethically acceptable to them, invasive, or involves aparticular individual (i.e., a favorite animal). Herzog[2002] proposed several ways in which researchinstitutions can help reduce the moral conflict facedby caretakers and others. First, institutions canpublically acknowledge that these moral conflictsexist. Second, scientists can explain the importanceof their studies, as well as the reasons why certainprocedures are necessary to those working closelywith the animals. Third, institutions can help reducemoral dilemmas faced by caretakers by providingthem a voice in ethical decisions. Sitting on commit-tees that oversee the use of animals, such as theIACUC, can help caretakers feel like their opinionsand moral concerns are being considered. Last,institutions can support the formation of strongbonds between caretakers and animals. Such bondsnot only help caretakers feel like they are doingsomething good for the animals which can helpassuage guilt, but they can also promote better care.

Providing excellent care not only helps the care-taker and science (as well as the primates), but is alsoone of the best ways we have to address the ethical andmoral concerns of the general public regarding the useof animals in research. At our facility, we find that thepublic is more accepting of the use of animals whenthey are comfortable with the care the animals arereceiving. We provide tours for more than 3,000persons each year, during which visitors learn aboutthe science that is being conducted and the care ouranimals receive. Several of these visitors are conflictedabout the need for animals in research, but aregenerally reassured when they learned how mucheffort is expended by the care staff on behalf of theanimals, and the extent to which laws protect researchanimals and provide for their welfare.

EMOTIONAL CONSIDERATIONS OF CARING

Benefits of caring: The majority of caretakers inbiomedical laboratories today chose that careerbecause they have a strong interest in animals[Chang & Hart, 2002]. As a result, most caretakersdevelop some sort of emotional connection to theanimals for whom they care [Arluke, 1999]. Theability to work closely with animals, particularlymonkeys or apes, is generally rewarding to care-takers. The opportunity to engage in positive inter-actions with the animals leads to increased moraleand job satisfaction, which in turn lead to better careand improved animal well being [Waitt et al., 2002].In addition, there are other emotional benefits tocaring for NHPs, including improved self-worth,increased knowledge about animals, and a sense ofdoing something for the greater good.

Costs of caring: There are also emotional costsassociated with caring for NHPs in research facilities.

It can be emotionally difficult for technicians whenanimals under their care become ill or have to beeuthanized for humane or scientific reasons. It isparticularly difficult for animals with whom theyhave developed a bond. Because of the emotionalinvestment, the loss of a NHP can be similar to theloss of a pet or a friend. Many caretakers reportfeeling depressed after a primate for whom theycared is euthanized.

An increasing number of institutions are takingsteps to help address the emotional consequences ofcaring for animals by providing their staff with theopportunity to pay tribute to the animals [Herzog,2002; Iliff, 2002]. These tributes can take severalforms, from memorial plaques to religious ceremo-nies. In Japan and other Asian countries, it is notuncommon for research facilities to have annualmemorial ceremonies as a way to pay respect to theanimals [Iliff, 2002]. These ceremonies are oftenreligious, but may be secular as well. For example,the Primate Research Institute (PRI) at KyotoUniversity, in Japan, has held a ‘‘Monkey MemorialService’’ every year since 1973 [Asquith, 1983]. Theseservices honor the monkeys who died of eithernatural or research-related causes at the PRI duringthe year. The attendees gather at a stone monumentand listen to various speakers, who may include PRIadministrators, veterinarians, and Buddhist priests.Speakers often talk about their own personal experi-ences with the primates. Flowers are then offered tothe spirits of the deceased monkeys. Less commonthan in Asia, such tributes are gaining popularityin the United States and Canada. In 1993, theUniversity of Guelph, Ontario, Canada, was the firstNorth American university to hold such a tribute.Their memorial was designed to acknowledge andraise awareness about the animals used for teachingand research [Taylor & Davis, 1993]. Other facilitiesthat have tributes to animals utilized in researchinclude Merck Research Laboratories [Iliff et al.,2000], University of Washington School of Medicine[Lynch & Slaughter, 2001], and State University ofNew York, Delhi [Iliff, 2002]. At the Oregon NationalPrimate Research Center, we are currently buildingan animal remembrance consisting of a plaquededicated to the animals and a private area in whichthe caretakers and others can go to reflect. Regard-less of its exact nature, this sort of tribute allowsanimal caretakers—as well as the scientists andothers—a way to recognize the loss as well as theimportant contributions the animals have made. Italso provides people with an opportunity to discussand share their feelings in a supportive environment.

CONCLUSIONS

One important outcome of high-quality animalcare is the close relationship that often formsbetween the caretaker and the primate. This

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relationship can be formed through positive dailyinteractions (e.g. providing enrichment; [Bayneet al., 1993], PRT [Bayne, 2002; Bloomsmith et al.,1997] or by unstructured interactions, such as play[Baker, 2004; Manciocco et al., 2009]. Once discour-aged and considered a potential threat to scientificobjectivity [Wolfle, 2002], such positive interactionsare now encouraged by many facilities. Studies haveshown that these sorts of relationships can benefitboth the caretaker as well as the research animal[Davis, 2002; Rennie & Buchanan-Smith, 2006].Of course, it is important to provide consistent careto animals on research studies. Finally, the moraland emotional consequences of caring for animalsshould not be ignored or minimized. Institutions andcaretakers benefit when grief associated with the lossof animals is acknowledged and supported. High-quality and conscientious animal care is good for theanimals, science, caretakers, and public perception ofresearch facilities.

ACKNOWLEDGMENTS

I am grateful to Diana Gordon, Ted Hobbs,Adriane Maier, Nicola Robertson, Greg Johnson,Jillann O’Connor, Steve Gordon, Jenny Manthe, andKatie Moore for useful discussions and comments onthis commentary. I also thank the dedicated animalcare staff at the Oregon National Primate ResearchCenter who work extremely hard for the monkeys.Funding was provided by NIH RR00163.

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