ILAR J. 2017 Dec 1; 58(2):
295–307. More than a quarter of a century has elapsed since the Animal Welfare Act mandated that research facilities develop and follow a plan to promote the psychological well-being of captive primates. Since passage of this law, considerable effort and resources have been directed to designing environmental enrichment strategies in an effort to improve animal welfare. These plans typically consist of
environmental enrichment and socialization efforts. While environmental enhancement has undergone a great deal of improvement in the past 25 years, it should be viewed as a continual work in progress, which takes advantage of emergent and future technologies. In this review, we discuss the objectives of the environmental enhancement plan along with relevant outcome measures, as well as ongoing challenges, costs, and benefits. We then review various enrichment strategies and assess their efficacy
in meeting goals and objectives. Finally, we look forward to consider what the future might hold for environmental enrichment of nonhuman primates used in research. Keywords: animal welfare, nonhuman primate, psychological well-being, social housing More than a quarter of a century has elapsed since federal legislation was enacted to promote the psychological well-being of captive
nonhuman primates (NHP; Animal Welfare Act, USDA 2013). Initially spurred by a congressional mandate in 1986 to “provide a physical environment adequate to promote the psychological well-being of primates,” considerable effort has been directed to designing environmental enrichment strategies that achieve this mandate. In this review, we will first discuss the objectives of the
environmental enhancement plan along with relevant outcome measures. We will also identify ongoing challenges as well as costs and benefits. The second focus will be to review various enrichment strategies that have been employed during this period and assess their efficacy in meeting goals and objectives. Finally, we will look forward to consider what the future might hold for environmental enrichment of NHPs used in research. There are several interrelated terms we will use
throughout this paper: enrichment, environmental enhancement, behavioral management, and psychological well-being. Enrichment, or environmental enrichment, has been defined as “an animal husbandry principle that seeks to enhance the quality of captive animal care by identifying and providing the environmental stimuli necessary for optimal psychological and physiological well-being”
(Shepherdson 1998, 1). Broadly speaking, it refers to items or practices that promote the expression of species-typical behaviors for captive animals. These items are the foundation of environmental enhancement, or improvements to the living conditions of animals. Enrichment and environmental enhancement are parts of a comprehensive strategy known as behavioral
management, which addresses the behavioral needs and psychological well-being of individuals. Psychological well-being can be considered a positive mental state, in which individuals are free from pain and distress, both psychological and physiological (NRC 1998). The Animal Welfare Act (AWA) specifies that research facilities “must develop, document, and follow an appropriate plan for environment enhancement adequate to promote the psychological well-being of nonhuman primates” (USDA 2013, § 3.81). The plan must include information on social housing, environmental enrichment, and if relevant, sections on animals with special
considerations, use of restraint devices, and exemptions. The broad goal of an environmental enrichment plan is to detail the elements necessary for ensuring a complex environment that engages the animal’s senses, promotes interaction, and functionally simulates behavioral opportunities found in the animal’s natural habitat. The various elements of the plan should be species-specific and based on currently accepted professional standards and scientific evidence; thus they should be updated
regularly. Importantly, environmental enrichment plans should be delivered in a consistent and systematic manner so as not to become a source of uncontrolled variation. While there are many elements of an environmental enrichment plan, the focus of this review will be on environmental enrichment and social housing. This review will also emphasize Old World monkey species (including macaques and baboons) because of their common usage in biomedical research. However, most of the concepts are
universal and can be applied to other species as well. Information relevant to New World species (squirrel monkeys, marmosets, and owl monkeys) and apes (chimpanzees) will be specifically referenced in the text. A primary goal of this plan, as noted in the AWA, is to promote species-typical behavior. Various forms of enhancement have been adopted at NHP facilities to meet this goal, such as: (1) adding permanent
physical structures that include perches, porches, and primahedrons; (2) presenting passive forms of enrichment that include videos, sounds, odors, and food treats; (3) providing interactive devices such as toys, foraging devices, and iPADs; and (4) implementing exposure to conspecifics. The legal emphasis on psychological well-being has led to other possible objectives. Thus, environmental enrichment programs are often expected to minimize abnormal behavior, facilitate adaptation to
environmental change, reduce stress responses, and maintain physical health (Novak and Suomi 1988). Each of these objectives can be operationally defined and evaluated. Abnormal behavior can be quantified, stress responses can be measured, and basic standards of physical health are readily available for many species of NHPs. The above goals and objectives focus on the
behavior and physiology of captive NHPs as affected by a vigorous program of environmental enrichment. But an alternative approach is a consideration of the possible benefits from the perspective of the animals themselves. In this context, it may be desirable to select enhancement strategies that require problem solving, engage multiple sensory systems, provide stimulus variation, make cages more complex or interactive, and increase control over the environment. However, if not careful, this
approach is vulnerable to our anthropomorphic views of what is best for NHPs. For example, what is complexity or stimulus variation from the perspective of the individual and how do we assess it? This challenge can be met, in part, by understanding and using the species’ natural history and ecology as the driver for achieving these goals (e.g., importance of providing nesting materials for chimpanzees: chimpanzees in the wild build a new nest each night, thus captive chimpanzees should be
provided with new nesting material every evening; Videan 2006). Nonetheless, one cannot simply rely on species natural history. Empirical studies examining animals’ sensory, cognitive, and behavioral capacities are also an important part of this endeavor. Ideally, the implementation of
specific enrichment strategies will be based on scientific evidence derived from either the primary research literature or ongoing research studies. NHP facilities are the proving grounds for testing the efficacy of various strategies; however, it is important to note that assessment typically occurs in the context of the research environment. This has two scientific implications. For animals on research protocols, enrichment studies may occur in association with ongoing experimental research.
Even unassigned colony NHPs have varied experimental histories, which may differentially impact their response to enrichment. Several possible experimental designs can be used to evaluate various forms of enrichment. In the within-subject ABA design, all subjects receive the enrichment, and changes in behavior and physiology are assessed during the enrichment period and also during control periods both
before and after the enrichment (see Griffis et al. 2013 for an example). In the between-subject design, one or more groups receive forms of enrichment and another group serves as a control (see Doane et al. 2013 for an example of this approach). Both designs have strengths and
weaknesses. The within-subject design reduces variability because the same subjects are tested at all time points, but it is vulnerable to changes across time that can covary with the enrichment period. This problem can be partially overcome by a modification of the within-subject design, the cross-over design, in which one-half of the subjects receive enrichment with the remainder serving as controls during the first period followed by a second period in which the treated subjects become
controls and the controls now receive the enrichment. However, the cross-over design is vulnerable to order effects in that the control period occurred for some subjects before they received enrichment and for other subjects after they received enrichment. The between-subject design eliminates both the time problem and order effects, because both experimental and control groups are studied in the same period. However, it is vulnerable to increased variability and uncontrolled differences between
the experimental and control groups including, but not limited to, genetic factors, experimental history, room location, dominance status, and temperament. Depending on the objectives and the experimental design as outlined above, a number of behavioral, physiological, and cognitive outcome measures can be employed to assess the efficacy of particular types of environmental enrichment. If the objective of enrichment is to promote species-typical behavior and/or reduce abnormal behavior, then some form of behavioral assessment is necessary. For species-typical behavior, the goal is to determine how and when monkeys interact with the enrichment. Because NHPs do not use enrichment every hour of the day, a number of observations may be required to establish efficacy. This is particularly the case for
non-food-related enrichment (e.g., toys, perches). On the other hand, food-related enrichment can be studied at the time of provision. Additionally, some devices can be set to record usage (see Bennett et al. 2016 in which computer joystick activity was monitored). For abnormal behavior, the emphasis is on whether using the enrichment reduces the occurrence of abnormal
behavior such as stereotypical or self-injurious behavior. In this case, a stable base rate of abnormal behavior must be established against which one can compare the effects of environmental enrichment. This process can be labor intensive as many behavioral observations may be required to establish this rate. In one study designed to examine the effect of puzzle feeders on various forms of abnormal behavior in rhesus macaques, each subject was observed for fifty 5-min samples for 10 weeks (Novak et al. 1998). An alternative approach is to examine behaviors associated with abnormal behavior, such as anxiety, and evaluate how they change as a function of enrichment. For example, social enrichment reduces both abnormal behavior and anxiety in macaques (Baker et al. 2012).
There are standardized procedures available for assessing anxiety in NHPs, including the human intruder test and novel object test, which do not require extensive behavioral observations (see Coleman and Pierre 2014 for a review). If the objective is to reduce the stress of laboratory environments,
stress itself can be measured in several different systems. Most commonly, the focus is on the hypothalamic-pituitary adrenal (HPA) axis, one arm of the stress response system. The HPA axis consists of the hypothalamus, pituitary gland, and adrenal cortex. Each of these anatomical structures produces a hormone that theoretically could be measured as an indicator of the stress response. However, scientists typically assay the hormone cortisol as an indicator of increased HPA axis activity,
because it can be measured peripherally and is more stable than the other hormones (O’Connor et al. 2000). Cortisol is secreted by the adrenal gland into the blood stream. This hormone then moves into other fluid compartments such as saliva and sweat, becomes steadily incorporated into hair, and is excreted as cortisol and/or metabolites in urine and feces. Cortisol or
its metabolites can be sampled and assayed from any of these compartments. However, the interpretation of the results will vary depending on the compartment from which samples are obtained (Meyer and Novak 2012). Cortisol extracted from either blood or saliva represents activation of the HPA axis several minutes before the sample is obtained. Cortisol assayed in urine or feces represents
a period of time corresponding to hours or a day. In contrast, cortisol obtained from hair is considered a chronic measure of HPA axis activity integrated over several months. Issues about measuring HPA axis activity and in determining what constitutes stress have been reviewed previously (see ILAR Expert Report “Recognition and Alleviation of Distress in Research Animals”, 2008; and more specific NHP references,
Meyer and Novak 2012; Novak et al. 2013). Although the HPA axis is usually the target of inquiry in determining whether enrichment reduces stress, other related systems can also be studied. Stress hormones can have secondary effects on immune function, because
many immune cells have receptors for cortisol (Glaser and Kiecolt-Glaser 2005). Thus, a few studies have examined the effects of enrichment on cell-mediated immune responses (Lambeth et al. 2006;
Schapiro 2002; Schapiro et al. 2000). Cognitive bias.A novel approach to understanding environments and their impact on NHPs is the cognitive or judgment bias test (Harding et al. 2004; see Mendl et al. 2009 for review). This test is based on the premise that animals will be pessimistic in their judgments when exposed to adverse conditions. A number of studies have shown that rodents and NHPs show optimism after a positive event and pessimism after a negative event (Bethell et al. 2012; Brydges et al. 2011). There are several variants of the task, one of which is described here (see Pomerantz et al. 2012). In initial training, capuchin monkeys were exposed to rectangles (large vs. small) in association with two food wells, one covered with black and the other white. The large rectangle indicated a high value reward in the black-covered food well, whereas the small rectangle indicated a low value reward in the white-covered food well. Incorrect associations (e.g., selecting the white-covered well in the presence of the large rectangle) were not rewarded. During probe trials, monkeys saw an ambiguous stimulus, a medium-sized rectangle, and responses were scored. In this context, selection of the low-value white food well was considered a pessimistic choice. Despite its potential value, this procedure is labor intensive and requires extensive training. In recognition of this problem, Bethel and colleagues (Bethell et al. 2016) have introduced a modification that relies on species-typical stimuli (e.g., monkey faces) and measures differential reaction to direct and averted gazes following adverse events such as health exams. Nonetheless, this procedure still requires some training along with touch screens, feeders, computers, and software. Additionally, whereas the cognitive bias test may be useful in determining emotional responses to situational events such as health exams, it is not clear whether it is a useful tool for evaluating different forms of enrichment over the long term. An alternative approach has been to evaluate the presence of specific types of abnormal behavior and its possible association with pessimism. In one study, capuchin monkeys that engaged in pacing with head twirls, but not pacing alone, showed negative cognitive bias (Pomerantz et al. 2012). Challenges to Developing a PlanIn developing a plan for environmental enhancement, a number of issues must be considered. A standard plan wherein all NHPs receive the same kinds of enrichment may not succeed with every individual. Because of differential reactions across individuals, some form of evaluation may be needed. Various enrichments, while promoting species-typical behavior, also have potential risks that must be considered from the dual perspective of the caregiver and the NHP. Individual DifferencesIndividual NHPs vary considerably in temperament. Temperaments are derived from behavioral characteristics that can vary along a continuum, with some individuals consistently scoring low and other individuals consistently scoring high on those characteristics. Relevant temperamental factors as related to environmental enrichment include: (1) behavioral inhibition to novel stimuli (Chun and Capitanio 2016; Coleman 2012; Suomi 1991), (2) nervousness (Capitanio et al. 2017), (3) sociability (Sloan et al. 2008), and (4) impulsivity (Higley and Linnoila 1997; Mehlman et al. 1994). These highly consistent behavioral characteristics are associated with significant variation in biological parameters. Monkeys showing high levels of behavioral inhibition also exhibit exaggerated cortisol responses to novel stimuli; high impulsivity scores are correlated with low serotonin turnover; and monkeys low in sociability have weakened immune responses. Thus, it is not surprising that there may be wide individual differences in response to enrichment (Izzo et al. 2011). Whereas a particular enrichment may be used vigorously by some monkeys, other monkeys may actually show fear reactions or avoid the enrichment altogether. As an anecdote, eight individually housed rhesus macaques were given access to hammocks. Three monkeys used these hammocks a majority of the time both during the day and especially at night. The remaining monkeys avoided all contact with the hammocks and did not show any adaption after a year of exposure. Planning for Individual Differences.The presence of individual differences necessitates a monitoring program to ensure that the environmental enhancement plan produces positive experiences for as many NHPs as possible. Scientific studies are a useful resource for identifying enrichments that benefit individuals. However, they may not help in identifying those monkeys at a facility who do not benefit from a particular manipulation as noted in the hammock example above. Simple observations of usage at the time of implementation along with care staff queries may be sufficient to identify individuals with adverse reactions or whose usage is extremely limited. To overcome these problems, several options should be available within the general categories of enrichment. For example, monkeys who avoid hammocks may successfully use porches, or monkeys who are highly reactive in the presence of a companion may fare well in a protected contact environment. In this way, the environmental enhancement plan can be tailored to meet individual needs. Of course, such individualized plans might be more challenging in large facilities housing thousands of animals than in smaller facilities. Still, even in large facilities, caretakers and others tend to know the temperament and idiosyncrasies of the animals in their care and, to the degree possible, address them when providing enrichment. For example, older NHPs or those with limited use of digits are often provided with enrichment devices that do not require a high degree of dexterity. Risks of EnrichmentNearly every enrichment device has potential risks. For food-related enrichment (e.g., treats that are high in sugar), the risk is increased body weight, which can lead to health-related problems including insulin resistance, metabolic syndrome, and type 2 diabetes (Bremer et al. 2011). In one study, it was estimated that 4–15% of the diet was obtained through foraging devices (Bennett et al. 2016). Thus, even with species-appropriate treats, titration between the calories in chow and the calories obtained through foraging may be necessary to maintain a suitable, stable weight. Additionally, if too much of the diet consists of treats, regardless of their nutritive value, dietary imbalances may ensue. Thus, appropriate management of diet is an important consideration in developing an enrichment plan. Non-food enrichment can also have risks, particularly as pertains to manipulable objects. Dog toys, rope, and bedding can be chewed and ingested, thereby impacting gut motility and health (Etheridge and O’Malley 1996; Hahn et al. 2000). Monkeys can entrap limbs or even their heads in chain or ropes utilized to hang objects. Covering the chain with PVC pipe or other hose-type material can greatly reduce this risk. Certain enrichment objects such as kongs that are not properly cleaned and disinfected can act as fomites, spreading disease (Bayne et al. 1993a). Although social housing is arguably the most effective form of enrichment (Gilbert and Baker 2011), it also has potential risks because of incompatibility that can be manifested as aggressive altercations and/or food competition. The AWA places an emphasis on social housing, which is considered the default condition. For most laboratory-housed species, this means pair housing at the minimum, although larger, species-typical groups may be possible as well (see Enrichment Strategies: Social Housing below for current best practices). The AWA acknowledges conditions that may preclude socialization such as old age or hyper-aggressiveness. Several common assumptions are made when forming pairs or social groups of NHPs. First, the process of pairings or groupings will be relatively straightforward, and there are reliable ways to test for compatibility in advance of pairing. Second, if pairs or social groups are compatible in the beginning, they will remain compatible throughout. Finally, if incompatibility develops, there will be significant changes in behavior that will enable separation of such pairs prior to injury. However, the data do not fully support these assumptions. First, pairing success can vary widely. In one study of vervet monkeys, pairing success ranged from 20% to 98% across four facilities. This variability was attributed to differences in pairing procedure and whether monkeys were laboratory born or imported (Jorgensen et al. 2017). Additionally, there are many different factors to consider that may influence partner compatibility, including, but not limited to, sex, age, body weight, rearing history, temperament, and previous pairing history. Temperament may be one of the more salient dimensions to use for compatibility. In one study, temperamental characteristics as determined in infancy predicted successful pairings in adulthood for female pairs but not for male pairs (Capitanio et al. 2017). However, there is no blueprint at present that can be used reliably to ensure pairing success in most situations. The notion that successful pairings/groupings will remain compatible over the long term is uncertain. In a recent study examining pairing success in owl monkeys, a monogamous breeder, opposite sex pairings were more successful than male- or female-only pairings (80%, 62%, and 40%, respectively). More importantly, all pairs had a “finite lifespan” and had to be separated on average 1–7 years later due to incompatibility (Williams et al. 2017). Lastly, if animals can become incompatible after months of exposure, it is important to identify indicators of developing incompatibility that could be used to predict in advance the risk of serious aggression. In outdoor, corral-housed macaques, aggressive altercations (e.g., matrilineal overthrows) occur rapidly and can involve severe wounding and death (Dettmer et al. 2015; Ehardt and Bernstein 1986; Gygax et al. 1997; Herrington et al. 2016; Oates-O’Brien et al. 2010). In the past, it has proven difficult to predict such overthrows. However, recent evidence suggests that social network analysis might have value in assessing social stability in large species-typical groups (McCowan et al. 2008). On the other hand, further research is needed to identify factors that predict the development of incompatibility in long-term pair-housed NHPs. Enrichment StrategiesAs mentioned above, the AWA mandates that facilities housing NHPs have an environmental enhancement plan. The exact nature of the plan depends on the species of NHPs to be enriched, as well as facility and research constraints. Still, there are many commonalities among enrichment strategies, particularly with respect to the basic components. Below we provide a brief overview of common enrichment strategies. These strategies are not necessarily mutually exclusive; specific items may fall into one or more category. Physical Cage StructureOne of the most fundamental aspects of an enrichment plan involves the primary enclosure (e.g., cage, pen, corral). Prior to the implementation of the AWA, at many facilities, cages and pens were often bare, with solid sides and little else. Today, most primary enclosures contain various forms of structural enrichment, including perches, branches, swings, play and resting structures, nest boxes, pools of water, and visual barriers (Figure 1, A and B). This type of enrichment increases the complexity of the enclosure and provides animals with opportunities to express species-normal behaviors such as play, locomotion, and exploration. Decisions regarding the provision of these, and other, enrichment items should be based on the behavior of the species. For example, many New World monkeys utilize nesting sites in the wild and should be provided with nest boxes in captivity. Macaques, on the other hand, do not engage in nesting behavior in their natural habitats, and thus do not need that opportunity.  (A) Examples of toys and structures for climbing, resting, and hiding for group-housed rhesus macaques (photo courtesy of the Oregon National Primate Research Center). (B) Example of a hammock for a rhesus macaque (photo courtesy of the University of Massachusetts, Amherst). While not as stimulating as large, outdoor corrals, indoor caging can often be configured in ways that increase complexity. For example, many top-row cages have removable floors as well as removable sides, thus providing animals with additional vertical space and climbing opportunities. Many cages also contain porches, or cage extensions, which hang on the outside of the cage and are either permanent or removable (Figure 2). NHPs seem to spend a great deal of time in these cage extensions (K Coleman, personal observation), perhaps because they afford the animals a relatively wide field of view. Porches have been found to reduce the occurrence of some abnormal behaviors in macaques, including feces painting (Gottlieb et al. 2014) and stereotypy (K Coleman, personal observation). Similarly, tunnels that connect upper- and lower-row cages (Figure 3) are also used in enrichment programs. Not only do they promote social opportunities (i.e., four animals can occupy four connected cages), but they promote climbing while providing a wide field of view. Some of these tunnels are currently being manufactured with built-in scales, so that animals can be easily weighed as they sit in this enrichment device. Many cage manufacturers also make play or exercise cages (e.g., Griffis et al. 2013), which can attach directly to the primary enclosure and provide additional space for the animals. Caged rhesus macaque with a “porch” (photo reprinted from Gottlieb et al. 2014 [Figure 1, p 654] with permission from the Journal of the American Association of Laboratory Animal Science). Cynomolgus macaques with a tunnel connecting upper- and lower-level cages (photo courtesy of the Oregon National Primate Research Center). The floor of the enclosure can be configured to maximize enrichment opportunities. Substrate, such as straw or bedding material, placed on the floor of cages or pens is relatively common in facilities. Treats and other food can be scattered on the substrate, fostering foraging opportunities. Bedding material affords captive chimpanzees opportunities to build nests, a behavior their wild counterparts accomplish nightly. Not only does substrate increase the time NHPs spend engaged in species-typical behaviors, it decreases other, less desired behaviors, such as aggression and self-grooming (Bayne et al. 1992; Brent 1992; Doane et al. 2013; Novak et al. 1995). Macaques housed on natural substrate (e.g., grass) have lower levels of alopecia than those housed on concrete (Beisner and Isbell 2008). Further, substrate can help with temperature control, particularly in cooler environments. Multiple studies have shown that the use of bedding can dramatically decrease water use when compared to pens that are not bedded, while not increasing the time required to clean (Bennett et al. 2010; Doane et al. 2013). All of these physical adaptations to the cage provide a complex and challenging environment that promotes species-typical behavior, and many (e.g., porches, substrate) can help reduce abnormal behavior. NHPs tend to spend a significant amount of time using these devices and are less likely to habituate to them than other items such as toys (Bayne et al. 1992). However, there are potential risks associated with these enrichment items, mostly involving safety. If limited quantities of these items are provided to large groups, this can lead to competitive aggression. Because they tend to get a great deal of use, care must be taken to ensure that items do not become hazardous to the animals as they get worn out. Tactile StimulationMany of the most commonly utilized enrichment items provide tactile stimulation, including toys, foraging devices, wood, and destructible items such as paper or cardboard boxes. A recent survey of common enrichment practices at 27 facilities housing NHPs found that all provided their animals with this form of enrichment (Baker 2016). NHPs housed in cages are provided with at least one toy at all times; these toys are usually rotated on a regular basis (often when cages are changed for cleaning) in an effort to increase novelty. Foraging manipulanda such as puzzle feeders or similar items are also universal components of enrichment plans. Although the size and structure differs for various species, the devices are relatively similar and typically consist of small holes through which the animals can retrieve food items, promoting foraging behavior (Crockett et al. 2001; Honess and Marin 2006). Manipulable devices typically increase the expression of species-normal behaviors including foraging, exploration, and play, at least for a while. These foraging devices have been found to decrease the occurrence of some abnormal behaviors, including stereotypical behavior (Novak et al. 1998) and overgrooming (Schapiro and Bloomsmith 1995) in NHPs when they remain attached to the cage. However, the undesired behaviors tend to return after time (Lutz and Novak 2005), likely due to decreased interest in devices. Adding a simple toy to the feeding device can increase the amount of time primates utilize them (Rawlins et al. 2004). Similarly, interest in destructible items tends not to wane as much as foraging devices, in part because the items are usually quickly destroyed (Pruetz and Bloomsmith 1992). Visual StimulationMost NHP species rely heavily on vision and are exposed to a variety of visual stimuli in their natural environment. The diversity of visual stimulation is often reduced in a laboratory setting, particularly for animals housed indoors. Visual enrichment, including mirrors, videos, and brightly colored mobiles, is relatively common in enrichment plans. While there are few published reports on the benefits of mirrors as enrichment, they tend to get a great deal of use (Griffis et al. 2013). There is evidence to suggest that some NHPs will watch videos, although the presentation of uncontrollable video has not been shown to dramatically increase species-typical or decrease abnormal behavior (Bloomsmith and Lambeth 2000; Platt and Novak 1997). However, when visual stimuli changed frequently and could be controlled by the subjects it was found to reduce abnormal behavior in singly housed Japanese macaques (Ogura and Matsuzawa 2012). Auditory StimulationAuditory enrichment, consisting of music or natural sounds, is another relatively common component of enrichment plans. In addition to being used as enrichment, auditory stimuli may also be used to mask other, presumably stressful, sounds (e.g., animal handling and/or cage cleaning procedures). While certain kinds of music have been shown to be anxiolytic in humans and other species (Chikahisa et al. 2007; Wells 2009), their effect on NHPs is less clear. Music may help macaques and other NHPs habituate to noises and can lessen startle reflex (Jennings et al. 2009). It also has been shown to reduce aggression and agonistic behavior in chimpanzees (Howell et al. 2003). However, when given a choice, chimpanzees, tamarins, and marmosets typically chose silence over “music” (McDermott and Hauser 2007; Richardson et al. 2006). Although it is often assumed that “natural” sounds (i.e., those from an animal’s natural environment) are enriching, such sounds may not be meaningful to the animals, or may actually be stressful (Wells 2009). An additional consideration is the amplitude or loudness of the music, which should not inhibit or interfere with communication between animals. TasteNHPs in the wild are exposed to a variety of food options. Foraging, which includes searching for, procuring, and manipulating food (e.g., opening nuts or seeds), is a major part of the behavioral repertoire of most wild primates. Animals can spend upwards of 50% of their waking hours engaged in this behavior. This time is greatly reduced in a laboratory setting, where processed food items (biscuits, chow, pellets) are typically provided only once or twice a day. Feeding enrichment includes procedures and devices designed to increase time spent feeding and foraging (as indicated above), as well as provision of a diversity of treats and other food items. This kind of enrichment is ubiquitous (Baker 2016) and is almost universally utilized by animals. Effective food enrichment should be varied in taste, texture, and color. In an effort to meet the goal of encouraging species-typical foraging behaviors, food treats should be provided in ways that extend the time needed to find and procure food, and not simply handed to the animal. For example, food can be frozen in ice or hidden in substrate to promote foraging behaviors. However, food treats may have to be handed to pair-housed animals if they are highly competitive about food. With all feeding enrichment, care must be taken not to provide items that are high in “empty” calories. Weight gain and even obesity can be a problem for certain laboratory animals, particularly if they are not given ample opportunities to exercise. In addition, if too many treats are provided to animals, they may not consume the nutritionally balanced components of their diets. Cognitive StimulationOne of the more recent additions to many enrichment plans is provision for cognitive stimulation. This kind of cognitive-based enrichment, often accomplished with computers or tablets, provides NHPs with opportunities to solve problems. In particular, tablets provide NHPs access to a wide range of games, known as apps, which can be easily changed and updated (e.g., O’Connor et al. 2015; Figure 4). The apps can often be downloaded for free or can be created especially for NHPs (Sams CL, Hamel AF, Novak MA, unpublished data). In either case, the apps typically consist of some sort of reaction to touching of the screen (e.g., balloons pop or pictures appear). Unlike many touch screen programs, the apps provide no positive reinforcement other than the intrinsic reinforcing properties of the app itself; that is, there is no food or other palatable reward. There is currently a paucity of studies examining the effects of this kind of cognitive enrichment; however, a small number of studies have shown that tablets and apps positively affect welfare in NHPs. Computer tasks have been found to reduce levels of stereotypies and other behavioral problems in rhesus and bonnet macaques (Lincoln et al. 1995; Platt and Novak 1997; Washburn and Rumbaugh 1992). Even group-housed animals can benefit from this type of enrichment. A recent study found that voluntary access to touch screen computers reduced levels of stereotypic behavior and cortisol in group-housed baboons (Fagot et al. 2014). Rhesus macaque using iPad enrichment (photo courtesy of the University of Massachusetts, Amherst). This type of enrichment may be particularly sensitive to individual variation in temperament. Shy, inhibited animals are less likely to interact with tablets than less inhibited animals (Coleman 2017). However, for many individuals, tablets and computer games can be effective forms of enrichment. ExerciseExercise is clearly important to the well-being of most animals, including NHPs. Still, only since its use was recommended in the 8th edition of the Guide to the Care and Use of Laboratory Animals (the Guide; NRC 2011) has it received significant attention as an integral part of an enrichment plan. There are several ways in which exercise can be accomplished. Housing NHPs in large enclosures is one way to provide them with exercise. When this is not possible, activity cages can be utilized to provide exercise to NHPs (Wolff and Rupert 1991). These cages have been found to reduce abnormal behavior in baboons (Kessel and Brent 1995), vervet monkeys (Seier et al. 2011), and rhesus macaques (Griffis et al. 2013), at least during the time that the animals are able to use them. In addition, such enrichment may also help individuals cope with stressful procedures, an important aspect of psychological well-being. For example, providing monkeys with play time in an activity cage reduced anxiety towards restraint in a primate chair (McGuffey et al. 2002). Social HousingWhile environmental enrichment is a critical part of psychological enhancement plans, social enrichment is often at the center of these plans. Indeed, social housing is often posited as one of the most effective forms of enrichment for NHPs (Novak and Suomi 1991; Schapiro 2002). Options for social housing range from pairing in cages to large outdoor corrals with a hundred or so animals. The emphasis on social housing was underscored in the 8th edition of the Guide (NRC 2011). While the AWA has mandated social housing to be the default method for maintaining social species since its promulgation in 1991, site inspectors now look at issues surrounding social housing more closely. As a result, acceptance for singly housed animals has decreased in recent years. Indeed, in the recent survey of primate facilities (Baker 2016), 83% of rhesus and cynomolgus macaques were socially housed. This finding represents a significant increase over findings from a similar survey taken in 2003 (Baker et al. 2007), in which approximately 70% of these macaque species were socially housed. The kind of social housing provided to NHPs depends on factors such as the species of animal, their purpose (e.g., breeding or research), and facility constraints (e.g., location). Optimally, marmosets and tamarins would be housed in cooperative breeding groups consisting of a monogamous breeding pair and their offspring. Rhesus macaques, on the other hand, can be housed in pairs or large groups. While breeding colonies are typically housed in relatively large groups, animals on certain research projects are often pair-housed in cages. Certain research procedures are easier to accomplish when animals are housed in cages than pens, although positive reinforcement training (see below) can make it easier to access animals living in groups. In general, there are many benefits of social housing. Such housing affords NHPs opportunities to engage in grooming, play, and other species-typical behaviors. It has also been shown to reduce the occurrence of abnormal behaviors, including stereotypy, hair pulling, and self-injurious behavior (Lutz and Novak 2005; Weed et al. 2003). The process of forming groups can result in increased cortisol and decreased immune function initially, although these signs of stress usually dissipate relatively quickly (Schapiro et al. 2000). Importantly, the presence of familiar companions can help mitigate the effects of stressful events (Gerber et al. 2002). For example, marmosets relocated to a novel room with a familiar conspecific showed fewer physiological effects of stress compared to those moved by themselves (Smith et al. 1998). However, social housing is not without potential risks, as described above. Social introductions can lead to aggression, as individuals establish their place in the dominance hierarchy. A certain degree of aggression is to be expected, and the benefit of social companionship typically outweighs the cost of minor wounds to the individual. However, this may not be true for severe trauma or escalated aggression. The degree of “acceptable” aggression depends on many factors, including the species and the type of individuals. For example, aggression might be less tolerable when infants or frail animals are involved (Olsson and Westlund 2007). Even without overt aggression, social housing may cause stress for certain individuals, such as those at the bottom of the dominance hierarchy. Therefore, it is important to continuously monitor socially housed animals and to intervene when animals show signs of distress (e.g., showing excessive fear towards cagemate(s), etc). While social housing is considered the default condition by the AWA and the Guide, both recognize that there are situations in which it may not be appropriate. Single housing may be justified when there are clinical or behavioral concerns or when required by experimental protocols (NRC 2011; USDA 2013). Animals who are sick or debilitated due to injury, age, or conditions such as arthritis may be housed alone, as can those who are hyper-aggressive. Exemptions from social housing based on these well-being concerns should be reviewed by the attending veterinarian every 30 days. NHPs on certain research studies, such as infectious disease protocols in which viruses can be transmitted between partners, may also be singly housed. The scientific justification for single housing must be approved and reviewed at least annually by the Institutional Animal Care and Use Committee. Even when animals are singly housed, they should still have visual and audio contact with conspecifics. Human InteractionWhile socialization with conspecifics (or congenerics) is important for psychological well-being, NHPs can also benefit from positive interaction with humans. One such type of interaction is formed with positive reinforcement training (PRT). Positive reinforcement training is a form of operant conditioning in which subjects are rewarded with something desirable (e.g., a food treat) for performing specific behaviors on command (see Laule et al. 2003 for an overview of PRT). NHPs have been successfully trained to perform various husbandry or clinical tasks, including moving to a new part of an enclosure (Veeder et al. 2009), presenting a body part for an injection or another procedure (Priest 1991; Schapiro et al. 2003), and remaining stationary for blood sampling (Coleman et al. 2008; Laule et al. 1996). The use of PRT is gaining acceptance in the research community and is recognized as an important tool for promoting well-being for captive species. For example, in a 2003 survey of facilities housing NHPs, approximately one-half of the respondents reported utilizing PRT in their programs (Baker et al. 2007); in 2014, all facilities reported including training in their enrichment programs (Baker 2016). There are many benefits associated with PRT. By allowing individuals to cooperate with various procedures, PRT can reduce the stress associated with these procedures (Bassett et al. 2003; Laule et al. 2003; Schapiro et al. 2003). It can also increase well-being by decreasing boredom and increase mental stimulation for subjects (Laule et al. 2003). PRT has been found to reduce the incidence of stereotypies in several NHP species (Bourgeois and Brent 2005; Coleman and Maier 2010; Raper et al. 2002), although this is not a universal finding (Baker et al. 2009). Further, cooperative feeding training can be used to decrease aggression in group-housed animals. Bloomsmith and colleagues (Bloomsmith et al. 1994) trained dominant chimpanzees to remain stationary during feeding time and allow subordinates to feed, thus decreasing food-related aggression. For these reasons, positive reinforcement training is considered an effective enrichment strategy. Positive reinforcement training has many benefits but can also be time intensive. Other forms of positive interactions with humans can also be beneficial. Even unstructured human interaction, such as grooming, play, or provision of treats can improve welfare for laboratory NHPs (Baker 2004; Bayne et al. 1993b). Such interactions have been shown to reduce abnormal behavior, increase species-appropriate behaviors such as grooming, and improve well-being in marmosets (Manciocco et al. 2009), macaques (Bayne et al. 1993b; Reinhardt 1997; Waitt et al. 2002), and chimpanzees (Baker 2004). Importantly, these positive human-NHP relationships can also promote coping skills (Rennie and Buchanan-Smith 2006) and help mitigate stress reactivity towards novel objects or situations. Miller and colleagues (Miller et al. 1986) found that chimpanzees were less anxious when confronted with novel situations in the presence of their trusted caretaker than when the caretaker was absent. There can be indirect benefits of these relationships as well. NHPs are more likely to sit calmly in the front of their cage when they trust their caretakers than when they do not, allowing human observers to approach animals easily and safely (Lehman 1992). This relaxed response to the presence of humans can facilitate daily observations and health checks and can thus promote animal care. The time investment associated with positive interactions does not have to be great in order to have an effect. A preliminary study (Houser LA, Coleman K, unpublished data) found that when care staff spent 10–15 min per day, 3–4 days per week engaged in activities such as giving treats, blowing bubbles, and reading to rhesus macaques, it resulted in a decrease in aggression and fear and an increase in affiliative behavior towards observers. In a similar study, simply handing out treats for 5 minutes a day several times a week improved welfare and decreased variation in heart rate and blood pressure in cynomolgus macaques (Tasker and Buchanan-Smith 2016). Even sitting quietly in the room observing behavior and occasionally handing out treats has been found to reduce abnormal behavior in macaques (Markowitz and Line 1989). Thus, this kind of enrichment is not only effective, but relatively easy to implement. Enrichment for the FutureEnhancing the environment of captive primates should be viewed as a continual work in progress so as to take advantage of emergent and future technologies. These new applications will continue to revolutionize medical care and can be adapted for enhancing both the health and well-being of captive NHPs. Below are our thoughts on the future of environmental enrichment along with possible areas for new research initiatives. Colony Rooms and MonitoringCurrently, many colony rooms are not adapted for computer use and surveillance. In the future, improvements in health monitoring and provision of complex forms of enrichment can be achieved with WiFi, LED projectors, smart phones used to monitor implants, and surveillance cameras. The presence of WiFi allows for the expansion of cognitive and visual enrichment using computer devices such as iPads. It also enables the development of the technologies described below. LED projectors can be used to convert the typical barren white walls of the colony room environment to nature scenes that are rotated at some preselected interval. A considerable human literature on ecopsychology has demonstrated a strong relationship between exposure to nature (either in the form of windows that look out on nature or visual images) and psychological health (Kahn et al. 2008; Mayer et al. 2009). The effects of such exposure include decreased aggression (Kuo and Sullivan 2001), reduced autonomic activity (Parsons et al. 1998), and better surgical recovery along with reduced pain in a hospital setting (Ulrich 1984). Although extrapolations to NHPs should be considered carefully, it seems likely that nature scenes associated with the species-typical natural environment might have beneficial effects. This is a significant area of new research in NHPs for which beneficial effects are now well established in humans. Smart phones can now be employed to monitor different physiological variables (e.g., facial and external body temperatures). In the future, NHPs could have small implants that would provide information on internal body temperature, heart rate, etc., which could be downloaded remotely through WiFi to a computer or iPhone. Motion-activated surveillance cameras could monitor both daytime and nighttime activity and might be used to identify correlates of behavior problems and reduced physical health (Stanwicks LL, Novak MA, unpublished data). Cage DesignThe current cage environment consists of stainless steel mesh and solid walls. Although solid walls are important in maintaining visual separation between some animals in the colony room, new cage features could be used to promote both physical and psychological health. One part of cage might consist of an iPad holder. The iPad could be set up to produce videogames or videos that could be presented with or without subject control. Foraging devices that automatically record usage along with amount of food obtained could be set to release a small treat for performing a complex manipulation for which video instructions on the iPad were provided (e.g., videos of monkeys performing the manipulation); otherwise, standard extraction foraging would be present. Cages could be flexible and allow reconfiguration for the purpose of enrichment; for example, adding a porch, tunnel, or exercise area between two cages where pairs on either side could have access (not at the same time). The cage could also contain special training devices such as blood pressure and blood draw portals. Research would be needed to establish what worked and what did not and to answer several basic questions: Do monkeys exercise control when using an iPad; does control improve activity and health; and how is this impacted by pairs of monkeys. Can monkeys learn to solve tasks from video of monkeys solving these tasks? Do monkeys learn more quickly when provided with a visual depiction of training efforts (e.g., blood draws) prior to training? There is evidence that chimpanzees are able to learn complex tasks (i.e., operating a tool-use task) from watching a video display (Hopper et al. 2012). However, to date no such tests have been done examining whether such video instruction would work with macaques. Cage MaterialsAs new materials are developed, stainless steel cages could also include high impact plastic structures (e.g., perches). The advantages of plastic include increased surface warmth and reduction in noise. However, there are also disadvantages. At the present time, plastics appear not to be suitable for the exterior cage mesh, lacking structural integrity. Additionally, plastic can be scratched more readily than stainless steel and clear Plexiglas surfaces often used in sliding doors typically become translucent as a result of chemicals and heat associated with cage washers. As noted above, even if new plastic products appeared on the market that overcame these disadvantages, research would be necessary to evaluate whether plastic cages produced benefits in health, behavior, and well-being that exceeded stainless steel housing. Individualized Enrichment PlansIt is well established that effective behavioral management plans should be tailored to unique behavioral patterns of each individual species (Jennings et al. 2009; Lutz and Novak 2005; NRC 2011). However, for a given species, facilities often adopt a “one size fits all” approach, in which enrichment that has been found to be beneficial to some individuals is assumed to be good for all. Future enrichment plans should take individual differences into account. As detailed above, conspecifics vary with respect to a wide range of traits, including age, sex, and temperament, which can influence how they respond to enrichment practices. For example, young monkeys are generally more exploratory than older monkeys and are thus often provided with additional enrichment opportunities. Indeed, infant and juvenile NHPs are afforded special consideration with respect to environmental enrichment under the United States AWA (USDA 2013). Temperamental differences among individuals may also influence their behavioral needs. Highly fearful or inhibited NHPs may not benefit from certain enrichment options in the same way as others. The provision of novelty is an important part of most enrichment programs (Bloomsmith et al. 1990; Crockett et al. 1989); however, constant exposure to novel objects may be anxiogenic to highly shy or neophobic individuals (Coleman 2012). These individuals might do better with familiar, rather than novel, enrichment offerings. Similarly, while positive reinforcement training and other forms of human interaction are generally thought to improve well-being for NHPs, interacting with the trainer can actually increase, rather than decrease, stress for some shy animals (Coleman 2012). Most current enrichment plans deal with these sorts of individual differences in a reactive manner; animals that are fearful of certain enrichment items are not given those items, or animals that are wary of a trainer receive additional desensitization or habituation. However, these temperamental differences could be managed proactively. Relatively straightforward temperament tests can be performed on the entire colony (e.g., Coleman 2017), allowing animals to be categorized based on particular traits (e.g., fearful, aggressive, etc). Enrichment plans can then be developed for the various “subtypes” of NHP. For example, an enrichment plan for highly inhibited monkeys may involve less novelty and more habituation to humans than an enrichment plan for confident monkeys. Future research would need to be conducted to ensure that the enrichment plans for each subtype of monkey is meeting the needs of that animal. Having enrichment plans that are tailored, as much as possible, to the individual traits of animals should ultimately improve their well-being. Increased Human InteractionAs detailed above, positive interaction with humans can be an important part of an enrichment program. Yet, it is not utilized as often or consistently as other forms of enrichment. While Baker (2016) found that most facilities incorporated some sort of human interaction, this form of enrichment is not typically provided to all animals on a consistent basis. Rather, it tends to be carried out in a somewhat random fashion, often only occurring “when there is time.” Ideally, positive human interaction would be performed consistently and by multiple people, not just those tasked with providing enrichment (often husbandry, behavioral, or laboratory staff, depending on the size of the institution). Having veterinarians or investigators who rarely see the animals engage in positive interactions can help reduce the stress associated with their visits. Research should focus on the amount of human interaction needed to achieve benefits. Increased ControlEffective enrichment should provide animals with a sense of control over their environment. Yet, many of the items commonly provided to the animals do not provide much control, other than the choice of whether to use or not use them. In many situations, animals do not even have this level of control. For example, when television is provided to a room of animals, individuals rarely have the opportunity to turn it off. Perhaps not surprisingly, most studies have not found television to be a highly effective form of enrichment (e.g., Platt and Novak 1997). However, having the ability to change the video being played and/or turn it off altogether was found to reduce abnormal behavior in singly housed macaques (Ogura and Matsuzawa 2012). Thus, providing animals with additional control over this kind of enrichment may have positive benefits. Providing control over visual enrichment may be somewhat more difficult to accomplish with animals living in groups than those living in cages, since one animal will inevitably choose for the others. However, it may be possible to provide socially housed animals with multiple copies of certain enrichment items, such as tablets on which they can change apps. Not only can additional choice and control be provided with respect to enrichment items, but it can also be extended to pair housing. New caging exists which allows animals to choose whether or not they want to have social access to the monkey in the next cage by opening a window. Only when both monkeys have opened their windows (i.e., chosen to have access to the monkey in the next cage) do they get full social contact. While this method of partner selection may not be feasible in all circumstances, it provides an innovative option. SummaryEnvironmental enrichment plans designed to improve the psychological well-being of captive NHPs have evolved a great deal since passage of the 1991 AWA regulations. Broadly speaking, effective enrichment programs should encourage the expression of species-normal behavior and minimize abnormal behavior, reduce the stress response and mitigate the effects of environmental change, and promote physical health. They also need to achieve efficacy across individuals, who may vary in their response to enrichment, without compromising the integrity of research programs on which the animals participate. A wide variety of research options exist, the selection of which depends on specific goals as well as facility constraints. Enrichment is continually evolving, based in large part to increased research in the area of animal welfare. It is imperative that we keep up with and make use of new technologies as they become available. Equally important, we must also continue to empirically study new enrichment strategies, to ensure that they are actually meeting their goals and promoting well-being. AcknowledgmentsWe thank Dr. Daniel Gottlieb for kind use of the figure of the porch. We also thank Dr. Jack Harding and two anonymous reviewers for suggestions that greatly improved this review. Support is acknowledged from the Oregon National Primate Research Center, 8P51OD011092 (KC) and University of Massachusetts, R24OD11180 (MAN). References
Articles from ILAR Journal are provided here courtesy of Oxford University Press Which of the following is the most important reason for providing environmental enrichment to research animals?A major benefit of environmental enrichment is the reduction in stress in the animals with beneficial influences on the research projects they are involved in.
What is environmental enrichment animal welfare?Environmental enrichment is a term used to describe changing a captive animal's environment in a way that improves the animal's quality of life. Captive environments are often safer than the wild but can also be less challenging and stimulating.
Which of the following is considered an environmental enrichment?Environmental enrichment consists of introducing novel objects, social housing, and exercise opportunities to the home cage.
What is an environmental enrichment device?Environmental enrichment devices typically include interactive objects that promote natural behaviors, reduce negative effects, and improve biological functioning (Keeling et al., 2016; Zobel et al., 2017).
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Which one of the following is likely to provide the most effective enrichment for an animal?
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