Enrichment and Primate Centers: Closing the Gap Between Research and Practice

A wealth of published research is available to guide environmental enrichment programs for nonhuman primates, but common practice may not consistently correspond to research findings. A 2003 survey to quantify common practice queried individuals overseeing enrichment programs about (a) social, feeding, structural, and manipulable enrichment; (b) human interaction and training; (c) general program administration; (d) the role of the institutional animal care and use committee (IACUC) in the enrichment program; and (e) the impetus for recent programmatic changes. Returned surveys provided information on the management of 35,863 primates and found social housing significantly more constrained than inanimate enrichment. Survey results suggest that social housing of macaques has not increased significantly over the past decade. The most commonly mentioned constraints related to research protocols. Facilities with thorough IACUC reviews of enrichment issues provided social housing for a significantly larger proportion of primates in biomedical research studies than did those with rare IACUC reviews. IACUC reviews prompted program enhancements much less often than did regulatory or accreditation inspections. These results suggest IACUC review is an underutilized mechanism for improving enrichment programs.     

Survey of environmental enhancement programs for laboratory primates

Animal welfare regulations in the United States require that nonhuman primate environmental enhancement plans be made in accordance with currently accepted professional standards; however, little information is available for quantifying common practice. Here we report the results of a 2003 survey that was sent to individuals overseeing enrichment programs at a variety of primate research institutions. The surveys requested information on program administration and management, implementation standards, procedures, and constraints pertaining to major categories of environmental enrichment, as well as intervention plans for animals exhibiting behavioral pathologies. Data were obtained on the management of 35,863 primates in 22 facilities. Behavioral scientists performed program oversight at the majority of facilities. Most programs reported recent changes, most commonly due to external site visits, and least commonly resulting from internal review. Most facilities' institutional animal care and use committees (IACUCs) included of individuals with behavioral expertise, and about two-thirds reported that enrichment issues could influence research protocol design. While most primates were reported to be housed socially (73%), social housing for indoor-housed primates appears to have changed little over the past 10 years. Research protocol issues and social incompatibility were commonly cited constraints. Implementation of feeding, manipulanda, and structural enrichment was relatively unconstrained, and contributions to these aspects of behavioral management generally included individuals in a wide variety of positions within a facility. In contrast, enrichment devices were used on a less widespread basis within facilities, and positive reinforcement programs that involved dedicated trainers were rare. We suggest that altering the role of the IACUC would be a productive avenue for increasing the implementation of social housing, and that an emphasis on prevention rather than intervention against behavioral pathology is warranted. The data from this survey may be useful for anticipating future program evaluations, establishing more effective internal evaluations, and assessing program progress and resource allocation.     

Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys

Certain types of inanimate environmental enrichment have been shown to positively affect the behavior of laboratory primates, as has housing them in appropriate social conditions. While social housing is generally advocated as an important environmental enhancement, few studies have attempted to measure the influence of social conditions on the effects of inanimate enrichment or to compare the relative merits of social and inanimate enhancements. In the present study, inanimate enrichment (predominately physical and feeding enhancements) resulted in increased species-typical behavior for socially restricted subjects. However, social enrichment (living in groups) appeared to be more beneficial for young rhesus monkeys, leading to increased species-typical activities and decreased abnormal activities. The behavior of one cohort of yearling rhesus monkeys (Macaca mulatta) housed in small peer groups was compared with the behavior of four yearling cohorts housed in single cages. Half the animals in each cohort received a three-phase enrichment program and the rest served as controls. Group-housed yearlings spent significantly more time feeding and exploring and significantly less time behaving abnormally, self-grooming, and drinking than did singly housed yearlings. Enriched subjects spent significantly more time playing by themselves, and significantly less time self-grooming and exploring than did controls. Among group-housed subjects only, there were no differences between enriched and control monkeys. Captive primates should be housed socially, whenever appropriate, as the first and most important step in an enrichment program, with the provision of inanimate enhancements being considerably less important. Limited resources for inanimate enrichment programs instead should be focused on those individuals who can not be housed socially. © 1996 Wiley-Liss, Inc.     

A Tail of Two Monkeys: Social Housing for Nonhuman Primates in the Research Laboratory Setting

Despite great adaptability, most nonhuman primates require regular tactile contact with conspecifics for their psychological well being. By illustrating the inherent value of social contact and by providing clues to the best ways of satisfying this need, behavioral studies are useful in designing social enrichment programs. Although group housing is ideal for most gregarious primates, space constraints and protocol requirements may preclude such environments for macaques housed indoors. Pair housing is an effective and practical alternative. Furthermore, such social experience facilitates integration into future social groups, including those in postresearch retirement facilities. This article references common research protocols that accommodate pair housing and includes scientific recommendations for institutional animal care and use committees (IACUCs) to facilitate providing physical social contact for nonhuman primates in laboratories.     

A tail of two monkeys: social housing for nonhuman primates in the research laboratory setting

Despite great adaptability, most nonhuman primates require regular tactile contact with conspecifics for their psychological well being. By illustrating the inherent value of social contact and by providing clues to the best ways of satisfying this need, behavioral studies are useful in designing social enrichment programs. Although group housing is ideal for most gregarious primates, space constraints and protocol requirements may preclude such environments for macaques housed indoors. Pair housing is an effective and practical alternative. Furthermore, such social experience facilitates integration into future social groups, including those in postresearch retirement facilities. This article references common research protocols that accommodate pair housing and includes scientific recommendations for institutional animal care and use committees (IACUCs) to facilitate providing physical social contact for nonhuman primates in laboratories.     

Comparing the relative benefits of grooming-contact and full-contact pairing for laboratory-housed adult female Macaca fascicularis

Tactile social contact is the most effective form of environmental enrichment for promoting normal behavior in captive primates. For laboratory macaques housed indoors, pair housing is the most common method for socialization. Pairs can be housed either in full contact (FC), or in protected contact (PC). At Washington National Primate Research Center, PC is provided by grooming-contact (GC) cages whereby two partners are housed individually in adjacent cages with access to each other through widely spaced vertical bars. Grooming-contact has been used to accommodate research protocol restrictions and improve the likelihood of compatibility for various pairings, in part by enabling male-female pairs. This study compares the benefits between the two housing types by video recording 14 pairs of adult female Macaca fascicularis in four sequential housing phases following an ABBA design: baseline grooming-contact, full contact shortly after introduction, 1-month-later full contact, and after reversion to grooming-contact. Prior to this study, pairs had been housed compatibly in GC. Twelve of the 14 long-term pairs transitioned successfully to full contact and data presented exclude the two failed pairs. Allogrooming increased significantly when pairs first switched from GC to FC (P = 0.018), but the effect did not last through the on 1-month-later FC phase suggesting that the initial improvement in affiliative behavior was a transitory novelty response that did not persist. Self-grooming significantly decreased between the first GC and first FC phases (P = 0.016), likely due to redirected allogrooming. Non-contact affiliative behavior towards partner or other conspecifics in the room did not differ, nor did agonism towards partner or others in the room. Occurrence of abnormal, tension, manipulation, miscellaneous active, and inactive behaviors did not differ significantly across housing phases. Proximity measurements indicated that pairs were significantly out of arm's reach more often in protected contact than when in full contact (P ≤ 0.02). Proportion of time spent in physical contact significantly increased between the first GC and first FC phases (P = 0.002), but subsequently declined. For both FC phases, partners chose to spend about 50% of their time in the same cage. Few behavioral improvements were seen after pairs switched to full contact and no negative effects came of reversion to grooming contact. This study suggests that tactile contact provided through widely spaced bars (grooming-contact) is a viable alternative to full contact housing for adult female longtailed macaques. It provides a degree of social housing while allowing both partners choice and control, key concepts in contemporary animal welfare guidelines.     

Environmental Enrichment for Laboratory Rodents: Animal Welfare and the Methods of Science

Because of the difficulty of' establishing objective measures of laboratory rodents' psychological well-being, developing environmental enrichment programs that are actually beneficial to rodents destined to participate in laboratory research is particularly challenging. Many studies of effects of environmental complexity, social housing, and increases in cage size suggest that professional judgments as to the impact of diverse types of environmental enrichment on rodent welfare are not a reliable basis for evaluating the outcomes of enrichment programs for laboratory rodents. Successful enrichment programs will vary from one rodent species to another, between sexes, as well as between age classes. There is a need for objective, measurable goals for proposed environmental enrichment programs for rodents, as well a s for empirical investigations of the beneficial and detrimental consequences of proposed environmental manipulations.     

Effects of environmental conditions on the psychological well-being of primates: a review of the literature

Amendments made to the Animal Welfare Act in 1985 require primate researchers to provide "a physical environment adequate to promote the psychological well-being of primates". Regulations have not yet been promulgated, in part because "the psychological well-being" of primates is extremely difficult to define. Ideally, those regulations would be based upon observable changes in behavior rather than assumed psychological changes. Regardless, new primate care regulations pertaining to social environment, cage size, exercise and other forms of environmental enrichment are anticipated. A review of the literature suggests that there is little scientific data to support changing existing regulations. For instance, although it is clear that total social isolation in very young primates can be behaviorally devastating in terms of normal social behaviors, there are few, if any, demonstrable adverse effects of individual housing in adult primates. On the other hand, group housing, particularly with groups changing frequently in composition, increases aggression, trauma and disease transmission. In addition, existing research suggests there are important species differences in terms of social preferences. It is impossible to justify an increase in cage size based upon the available literature. An additional practical consideration is that any change in cage size requirements will necessitate replacement of current primate housing on a national level, an enormously expensive proposition. Regarding environmental enrichment, research suggests that providing a naturalistic environment is not as critical as arranging dynamic events that are contingent upon behavior. However, new research is necessary to specify the types of environmental enrichment that are valuable and appropriate before useless, even damaging, and expensive changes are mandated.     

Environmental enrichment for laboratory rodents: animal welfare and the methods of science

Because of the difficulty of' establishing objective measures of laboratory rodents' psychological well-being, developing environmental enrichment programs that are actually beneficial to rodents destined to participate in laboratory research is particularly challenging. Many studies of effects of environmental complexity, social housing, and increases in cage size suggest that professional judgments as to the impact of diverse types of environmental enrichment on rodent welfare are not a reliable basis for evaluating the outcomes of enrichment programs for laboratory rodents. Successful enrichment programs will vary from one rodent species to another, between sexes, as well as between age classes. There is a need for objective, measurable goals for proposed environmental enrichment programs for rodents, as well a s for empirical investigations of the beneficial and detrimental consequences of proposed environmental manipulations.     

A sample postapproval monitoring program in academia

The primary goal of an animal care and use program (ACUP) should be to ensure animal well-being while fostering progressive science. Both the Animal Welfare Act (and associated regulations) and the Public Health Service (PHS) Policy require the institutional animal care and use committee (IACUC) to provide oversight of the animal program through continuing reviews to ensure that procedures are performed as approved by the committee. But for many committees the semiannual assessment does not provide an opportunity to observe research procedures being performed. Furthermore, IACUC members are typically volunteers with other full-time commitments and may not be able to dedicate sufficient time to observe protocol performance. Postapproval monitoring (PAM) is a tool that the IACUC can use to ensure that the institution fulfills its regulatory obligation for animal program oversight. When performed by attentive and observant individuals, PAM can extend the IACUC's oversight, management, training, and communication resources, regardless of program size or complexity. No defined PAM process fits all institutions or all situations; rather, the monitoring must match the program under review. Nonetheless, certain concepts, concerns, and conditions affect all PAM processes; they are described in this article. Regardless of the style or depth of PAM chosen for a given program, one thing is sure: failure of the IACUC to engage all available and effective oversight methods to ensure humane, compassionate, efficient, and progressive animal care and use is a disservice to the institution, to the research community and to the animals used for biomedical research, testing, or teaching.     

Behavioral effects of enrichment on singly-housed,yearling rhesus monkeys: An analysis including three enrichment conditions and a control group

Three cohorts of yearling rhesus monkeys (Macaca mulatta) were maintained in single cages for one year as part of a derivation program to produce a breeding colony of specific pathogen-free (SPF) monkeys. During this year of social restriction, subjects were provided with three different types of environmental enrichment (physical, feeding, and sensory) to counteract the known effects of social restriction and to quantify the effects of these different conditions of enhancement on their behavior. Focal animal observations were conducted on enriched and control subjects for all cohorts. Enrichment conditions were presented in a different order to each cohort. Monkeys provided with enrichment spent significantly more time playing and less time self-grooming than did control monkeys in unenriched cages, suggesting that the overall enrichment program was of some benefit to the monkeys, because these changes in behavior were in species-typical directions. Among enriched subjects only, there were significant differences in the amount of time spent drinking, grooming, feeding, playing, exploring, and using enrichment across the three enrichment conditions. Both the physical and feeding enrichment conditions led to species-appropriate changes in behavior, therefore enhancing psychological well-being as some define it. Sensory enrichment was of little benefit. The first cohort was housed indoors, received less stimulation from the environment outside of the single cage, and used enrichment more than did the other two cohorts housed outdoors. This suggests that the external environment influences behavior in the single cage and that enrichment may be most effective for animals housed indoors. © 1995 Wiley-Liss, Inc.     

Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys

Among captive primates, inanimate environmental enrichment can lead to measurable changes in behavior indicative of an improvement in psychological well-being. Although this has been demonstrated repeatedly for singly caged primates, the relationship is not as well studied for pairhoused animals. Study of the pair-housed setting has become increasingly relevant because of the social housing mandate of the Animal Welfare Act regulations. We therefore observed 68 juvenile rhesus monkeys born in 1988 and 1989 and living in mixed-sex pairs from the ages of 2 to 3 years. All pairs were compatible. Half of the pairs received two types of enrichment, while the remaining pairs served as controls. Enriched and control juvenile subjects differed in the amount of time that they spent being inactive, playing, and drinking, but did not differ in the amount of time they spent interacting with their partner. Grooming and play were the two most common socially directed activities in both groups, a species-appropriate pattern. Males played more and vocalized less than did females. Overall, enriched and control subjects spent equivalent amounts of time located within a social distance of one another, but there was some difference between groups in allocation of behaviors while near the pairmate. Environmental enhancers were frequently utilized, and led to relatively small changes in behavior between control and enriched subjects, suggesting that the presence of a partner for juvenile rhesus monkeys acts as a form of enrichment that may dilute the effects of inanimate environmental enhancements. © 1994 Wiley-Liss, Inc.     

Individual and collective responsibility to enhance regulatory compliance of the Three Rs

Investigators planning to use animals in their research and the Institutional Animal Care and Use Committee (IACUC) members who review the research protocols must take personal responsibility for ensuring that they have the skills and knowledge to perform their duties, applying the Three Rs principles of Russell and Burch. The two Korean laws introduced in 2008 and 2009 regulating animal use for scientific purposes in line with the Three Rs principles have been revised a total of 11 times over the last 6 years. Both regulatory agencies, e.g., the Animal and Plant Quarantine Agency and the Ministry of Food and Drug Safety, provide regular training based on the legal requirements. Based on the amended Animal Welfare Act, the IACUC appointment framework has been upgraded: appointments are now for two-year terms and require a qualified training certificate issued by the Animal and Plant Quarantine Agency since 2012. The authors reviewed the current curricular programs and types of training conducted by the two governing agencies through Internet searches. Our Internet survey results suggest that: a) diversity should be provided in training curricula, based on the roles, backgrounds and needs of the individual trainees; b) proper and continued educational programs should be provided, based on trainees’ experiences; and c) active encouragement by government authorities can improve the quality of training curricula. [BMB Reports 2014; 47(4): 179-183]     

Training strategies for IACUC members and the institutional official

Institutions are required by federal laws and regulations to oversee and evaluate their programs, facilities, and procedures for using animals in research, teaching, and/or testing activities. These responsibilities are specifically charged to an institutional official (IO) and an institutional animal care and use committee (IACUC). Initially, the individuals tasked with these responsibilities seldom have the requisite knowledge or experience to fulfill their charges effectively. Furthermore, simply reading the regulatory requirements does not prepare the novice IO and IACUC members to effectively monitor and guide the program. As a result, many new IOs and IACUC members are managing their responsibilities with insufficient understanding of the laws, regulations, standards, and policies. Specific training strategies for inexperienced IACUC members are needed to help them understand their responsibilities for ensuring animal welfare through an effective, high-quality, and compliant animal care and use program that supports the critical research needed to improve human and animal health. Likewise, most IOs would benefit from training to help them better understand their responsibility for enhancing or maintaining the quality of the institution's animal care and use program. Education and training should begin with an orientation to the laws, regulations, standards, and policies. Continuing training and education are also important to keep abreast of the changes in the interpretation of these laws and regulations as well as the changes in veterinary science. For both the IO and the IACUC, understanding and acceptance of their authority and responsibilities are significant factors in establishing and maintaining a quality animal care and use program.     

Social interaction in nonhuman primates: an underlying theme for primate research.

Social living is assumed to be a critical feature of nonhuman primate existence inasmuch as most primate species live in social groups in nature. Recent USDA legislation emphasizes the importance of social contact in promoting psychological well-being and recommends that laboratory primates be housed with companions when consistent with research protocols. Our goals were to examine the link between social housing and psychological well-being and to explore the idea that research may be compromised when primates are studied in environments that vary too greatly from their natural ecological setting (individual cage housing versus group housing). Three general points emerge from these examinations. First, providing companionship may be a very potent way in which to promote psychological well-being in nonhuman primates; however, social living is not synonymous with well-being. The extent to which social housing promotes psychological well-being can vary across species and among individual members of the same species (for example, high- and low-ranking monkeys). Secondly, housing conditions can affect research outcomes in that group-housed animals may differ from individually housed animals in response to some manipulation. Social interaction may be a significant variable in regulating the biobehavioral responses of nonhuman primates to experimental manipulations. Finally, a larger number of socially housed subjects than individually housed subjects may be necessary for some biomedical research projects to yield adequate data analysis. Thus, social living has significant benefits and some potential costs not only for the animals themselves, but for the research enterprise.     

Guidelines for developing and managing an environmental enrichment program for nonhuman primates.

Before implementing an environmental enrichment program for nonhuman primates, several issues should be considered. The assignment of enrichment tasks can be made to caretakers, a dedicated "enrichment technician," volunteers, students or individuals with training in behavioral science. Determining the enrichment techniques to be used must take into account personnel time available; the species, age, sex, and individual histories of the nonhuman primates; and experimental protocols for which animals are being maintained. Identifying the most beneficial way to use the available personnel time must be tailored for each institution. To meet federal regulations, records must be kept of the environmental enhancements available to each nonhuman primate. Good record-keeping will allow appropriate evaluation of the program. This evaluation should involve the animals' responses to the enrichment opportunity, cost and durability of enrichment items, human and nonhuman safety considerations, and personnel required. The well-being of captive nonhuman primates will be most improved if well-informed decisions are made in developing and managing environmental enrichment programs.     

Environmental enrichment for nonhuman primates: theory and application

Investigators have an obligation to promote the psychological well-being of nonhuman primates used in research. Considerable emphasis has been placed on providing nonhuman primates with enriched environments as a means to achieve this objective. A framework is provided that consists of a set of hypotheses about well-being, and the extent to which exposure to various enrichment devices and procedures actually promotes well-being is evaluated. Two hypotheses are concerned with fostering species-typical behavior: use (versus nonuse) of the enrichment, and whether use of enrichment helps normalize other aspects of the behavioral repertoire. Two additional hypotheses are concerned with abnormal behavior: whether currently existing enrichment lowers levels of abnormal behavior, and whether it prevents the behavior. This framework is applied to various enrichment strategies ranging from toys and foraging devices to social interaction. Most devices are used by nonhuman primates and thus constitute an important way to enrich the captive environment. However, enrichment devices vary as to their effectiveness in normalizing the behavioral repertoire and eliminating abnormal behavior. Only social contact satisfies the goal of promoting a wide variety of species-typical activities while at the same time reducing or preventing the development of abnormal behavior.     

Preference for social contact versus environmental enrichment in male laboratory mice

Due to their aggressive nature, male mice are less frequently used than female mice in biomedical research. When aggressive males are being used, individual housing is common practice. The question arises whether this is an acceptable housing for a social species. The present study was designed to gain more insight into the nature of inter-male social contact and into the potential of a form of environmental enrichment (nesting material) to compensate for the lack of social contact. In a series of tests, we analysed whether male mice of different ages preferred to spend time (1) near a familiar cage mate versus an empty cage, or (2) near to a familiar cage mate versus direct contact with nesting material (tissues). Dwelling time in each of the test cages and sleeping sites was recorded, as was the behaviour of the test mice. Results indicated that when other conditions were similar, male mice preferred to sleep in close proximity to their familiar cage mate. Furthermore, the need to engage in active social behaviour increased with age. Tissues were used to a large extent for sleeping and sleep-related behaviour. It is concluded that single housing in order to avoid aggression between male mice is a solution with evident negative consequences for the animals. When individual housing is inevitable due to excessive aggressive behaviour, the presence of nesting material could partly compensate for the deprivation of social contact.     

Interspecies pair housing of macaques in a research facility

The eighth edition of The Guide for the Care and Use of Laboratory Animals establishes social housing as the 'default' for social species including non-human primates. The advantages of social housing for primates have been well established, but small research facilities housing few primates in indoor cages have struggled with social housing as a result of limitations on appropriate housing and availability of compatible monkeys. Here, we report a novel approach to pair housing macaques - crossing species. We have successfully pair housed an intact male rhesus macaque with an intact male cynomolgus macaque, and an adult female rhesus macaque with numerous subadult female cynomolgus macaques. Monkeys in these pairs established dominant-subordinate relationships similar to same-species pairs. Rhesus and cynomolgus macaques can be successfully paired for the purpose of social housing in facilities with limited numbers of monkeys.     

Physical Environmental Effects on Infant Care and Development in Captive Callithrix jacchus

Environmental enrichment may affect infant care and development in captive primates. We investigated the effects of this factor in laboratory common marmosets (Callithrix jacchus). An enriched physical environment enhanced the social activities of the marmosets and elicited a greater repertoire of behaviors, without negatively affecting the provision of infant care. In addition, infants in enriched cages displayed certain behaviors sooner than infants in non-enriched cages did, which suggests an increased developmental rate. Infants in enriched cages also ate more solid food and engaged in solitary play and exploration more than ones in non-enriched cages did. Play and exploration probably improve spatial cognition and motor skills, which, together with a higher degree of independence, may allow infants to cope better with laboratory routines and general social interactions later in life than their counterparts reared in less complex enclosures. We conclude that laboratories can significantly increase the welfare of marmosets by providing a more complex physical environment.