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.     

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.     

A comparison of cell-mediated immune responses in rhesus macaques housed singly, in pairs, or in groups

A variety of psychosocial factors have been shown to influence immunological responses in laboratory primates. The present investigation examined the effects of social housing condition on cell-mediated immune responses, comparing rhesus macaques (Macaca mulatta) in three housing conditions (single, pair, and group). Subjects included 12 adults of both sexes in each housing condition (N=36). Multiple blood samples (0, 4, 8, and 12 months) were collected for immunological analyses, including lymphocyte subsets, lymphocyte proliferation to pathogens and nonspecific mitogens, natural killer cell activity, and cytokine production. CD4(+) to CD8(+) ratios differed significantly across housing conditions and singly caged subjects had significantly lower CD4(+)/CD8(+) after the 4-month timepoint than did socially housed (pair and group) subjects. CD4(+) to CD8(+) ratios were positively correlated within subjects, suggesting a trait-like aspect to this parameter. Lymphocyte proliferation responses to all four gastrointestinal pathogens differed across housing conditions (at least at the 0.08 level), as did proliferation responses to StaphA, and the production of cytokines (IFN-gamma, IL-2, and IL-10). Proliferation responses of singly caged monkeys did not differ from socially housed monkeys and the highest levels of both IFN-gamma and IL-10 were produced by group housed subjects. The data demonstrate that social housing condition affects immune responses. While not unidirectional, these effects generally suggest enhanced immune responses for socially housed animals. Since rhesus monkeys live socially in nature, and the immune responses of singly housed animals differed from those housed socially, there is considerable motivation and justification for suggesting that the use of singly housed rhesus macaques may complicate interpretations of normal immunological responses. This may have important implications for the management, treatment, and selection of primate subjects for immunological studies.     

Manipulating the affiliative interactions of group-housed rhesus macaques using positive reinforcement training techniques.

Social housing, whether continuous, intermittent, or partial contact, typically provides many captive primates with opportunities to express affiliative behaviors, important components of the species-typical behavioral repertoire. Positive reinforcement training techniques have been successfully employed to shape many behaviors important for achieving primate husbandry goals. The present study was conducted to determine whether positive reinforcement training techniques could also be employed to alter levels of affiliative interactions among group-housed rhesus macaques. Twenty-eight female rhesus were divided into high (n = 14) and low (n = 14) affiliators based on a median split of the amount of time they spent affiliating during the baseline phase of the study. During the subsequent training phase, half of the low affiliators (n = 7) were trained to increase their time spent affiliating, and half of the high affiliators (n = 7) were trained to decrease their time spent affiliating. Trained subjects were observed both during and outside of training sessions. Low affiliators significantly increased the amount of time they spent affiliating, but only during nontraining sessions. High affiliators on the other hand, significantly decreased the amount of time they spent affiliating, but only during training sessions. These data suggest that positive reinforcement techniques can be used to alter the affiliative behavior patterns of group-housed, female rhesus monkeys, although the two subgroups of subjects responded differently to the training process. Low affiliators changed their overall behavioral repertoire, while high affiliators responded to the reinforcement contingencies of training, altering their proximity patterns but not their overall behavior patterns. Thus, positive reinforcement training can be used not only as a means to promote species-typical or beneficial behavior patterns, but also as an important experimental manipulation to facilitate systematic analyses of the effects of psychosocial factors on behavior and potentially even immunology.     

The rehabilitation of captive baboons

Eleven baboons who had been singly housed indoors for an average of 5 years were moved to outdoor social groups in an attempt to provide a more species-typical environment and reduce high levels of abnormal behavior. Nine of the baboons were observed while in single housing and, over a 6-month period, while housed outdoors socially to document long-term changes in behavior. Abnormal behavior decreased significantly from an average of 14% of the observation time in the single cages to 3% in the sixth month of social housing. Cage manipulation and self-directed behaviors also significantly decreased, while social behavior, enrichment-directed behavior, and locomotion increased in social housing. Baboons that had been in long-term indoor single housing were able to reproduce and form stable social groups without injury. This study provides evidence that even behaviorally disturbed nonhuman primates can be successfully rehabilitated to live in social groups.     

Factors predicting increased incidence of abnormal behavior in male pigtailed macaques

To identify factors predicting abnormal behavior in laboratory monkeys, we observed all available singly housed 4- to 11-year-old male pigtailed macaques (Macaca nemestrina), the species/age/sex group most likely to be referred to the Washington National Primate Research Center's Psychological Well-Being Program for behavioral assessment. Of the 87 subjects, 29 had been referred to the program whereas 58 had not. Abnormal behavior was unrelated to the subject's housing location (biocontainment vs. other facility) or invasiveness of research. Nursery-reared subjects displayed more abnormal behavior than mother-reared subjects. Across and within rearing categories, the proportion of the first 48 months of life spent singly housed was positively related to the amount of abnormal behavior at maturity. This effect was stronger for subjects separated from the mother for clinical rather than experimental reasons, and least for mother-reared subjects. Locomotor stereotypy, by far the most frequent form of abnormal behavior, was positively related to time in single housing but was unrelated to rearing. These results reinforce the importance of tactile social contact during juvenility for the prevention of abnormal behavior in social primates. They also suggest that self-directed abnormal behaviors and locomotor stereotypies have different etiologies.     

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.     

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.     

Social buffering in adult male rhesus macaques (Macaca mulatta): Effects of stressful events in single vs. pair housing

Background The purpose of this study was to test whether long‐term pair housing of male rhesus macaques ameliorated negative responses to stressful events that can occur in the course of routine husbandry or research procedures. Methods Twelve singly housed individuals were videotaped during two potentially stressful events before and after social introduction into pairs. During each stressor, abnormal behavior and anxiety‐related behavior were quantified from videotape. Results When visually exposed to the restraint and anesthesia of other monkeys, subjects showed significantly reduced frequencies of abnormal behavior when pair‐housed in comparison to their reactions when housed singly. Noisy and disruptive conversation between technicians standing immediately in front of the subjects’ cage did not elicit the same reduction in abnormal behavior. Neither test showed a significant difference across housing settings for anxiety‐related behaviors. Conclusions These findings suggest that pair housing buffers adult male rhesus macaques against common stressors in the laboratory setting.     

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.     

Time budget of caged rhesus monkeys exposed to a companion,a PVC perch,and a piece of wood for an extended time

The present investigation assesses the percentage of time that rhesus monkeys (Macaca mulatta) are kept occupied by a more complex cage environment. Sixty animals were continuously exposed for at least 1.5 years to a compatible companion for social interaction, a suspended plastic pipe for perching, and a branch segment for gnawing. The behavior of the partners of each pair was recorded for 60 minutes when the animals were not distracted by human activities. Individuals spent an average of 23.5% of the time interacting with the companion, but only 10.4% with the plastic pipe and 4.8% with the branch segment. Differences were statistically significant. Females were socially more active than males. Subadult animals (3.5–4 years) used both inanimate objects significantly more than did adult animals (9–30 years). It was concluded that (1) a compatible companion, a suspended plastic pipe, and a loose branch segment remain effective stimuli for caged rhesus monkeys after more than 1 year of exposure and (2) a compatible companion is of greater stimulatory value–particularly for adults–than are inanimate objects.     

Old,socially housed rhesus monkeys manipulate objects

Recent research has indicated that old, individually housed monkeys show little interest in novel objects. Yet unanswered is whether this effect is caused primarily by age or housing condition. The purpose of this study was to assess the role of social living in promoting responsiveness to objects. We measured the rates of object manipulation in older animals, assessed responsiveness over time to particular objects as a measure of habituation, and examined social influences on object use. Several social groups of rhesus monkeys that contained older adults were studied. These groups were housed in indoor pens or in an outdoor enclosure, and all monkeys had continuous access to a variety of objects in their home environment. In contrast to previous studies of individually housed monkeys, our group-housed monkeys showed sustained interest in objects. Old monkeys manipulated objects extensively, and this response was all the more significant, given that the objects were not novel. Monkeys housed in an outdoor enclosure showed object manipulation patterns that were not different from monkeys housed in indoor pens. However, females exhibited much higher object-related responses than males. Social facilitation played a role in the reactions of some monkeys to objects. Patterns of social facilitation as well as avoidance were present in two of the three indoor groups that were observed. Failure to manipulate objects in rhesus macaques appears to be more a function of individual housing than of old age. Factors such as environmental complexity, social needs, and early experience should be considered in order to understand why individually housed rhesus monkeys are unresponsive to objects. © 1993 Wiley-Liss, Inc.     

A simple ethological monitoring system to assess social stress in group-housed laboratory rhesus macaques.

The increasing awareness of the importance of social housing of laboratory primates results in the establishment of group housing in many facilities. Our aim was to develop a set of manageable tools to allow continuous monitoring of social relations within groups and to establish an objective, scientific ground on which changes in group composition could be based. We studied 38 adult rhesus monkeys (Macaca mulatta) grouped as five one-male/multi-female groups using focal sampling. We recorded the occurrence and direction of aggressive and non-aggressive social interactions as well as time spent inactive in proportion to social contacts, feeding and other activities. The present analysis clearly identified low-ranking animals with none or few affiliative contacts and who also spent much time inactive and separated from other low-ranking animals. This suggests that the present approach results in useful information concerning compatibility between group members and enables identification of animals experiencing high social stress.     

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.     

Social segregation in male,but not female yearling rhesus macaques (Macaca mulatta)

Males and females of many species sex‐segregate, ranging from complete separation of habitats to social segregation within the same space, sometimes varying across seasons and lifespan development. Mechanisms for such segregation are not well understood, though some have suggested that sex differences in preferred juvenile behaviors lead to greater behavioral compatibility within than between sexes. This within‐sex behavioral compatibility may be the source of sex‐segregation. As juvenile behavioral sex differences are well‐documented in rhesus monkeys, we examined sex‐segregation patterns of yearling rhesus monkeys engaged in three different types of behavior: rough play, parallel play, and grooming. We observed male and female rhesus yearlings from five stable long‐term age‐graded social groups of 67–183 animals. Behavioral observations were designed to collect equal numbers of rough play, grooming, and parallel play bouts. In addition, sex composition and proximity to adults was recorded for each bout. Across all behaviors, more all‐male groups and fewer mixed sex‐groups were observed than expected by chance. All‐female groups occurred at the level expected by chance. Thus, males sex‐segregated regardless of type of behavior, while females did not sex‐segregate. Female groups were observed in proximity to adults more often than expected by chance. These results suggest that behavioral compatibility may produce sex‐segregation in male yearling rhesus monkeys, possibly preparing males and females for different social roles and segregation as adults. Am. J. Primatol. 72:87–92, 2010. © 2009 Wiley‐Liss, Inc.     

The effect of housing and environmental enrichment on stereotyped behavior of adult vervet monkeys (Chlorocebus aethiops)

Little information is available on the response of vervet monkeys to different housing conditions or on the suitability of enrichment devices or methods for vervet monkeys. In this study, the authors evaluated the occurrence of stereotyped behavior in adult vervet monkeys under various conditions of housing and enrichment. The variables included cage size, cage level (upper or lower), enrichment with a foraging log, enrichment with an exercise cage and presence of a mate. The authors first determined the incidence of stereotyped behavior in captive-bred, singly housed adult female and male vervet monkeys. They then exposed monkeys to different housing and enrichment situations and compared the incidence of stereotyped behavior among the monkeys. The authors found that more females than males engaged in stereotyped behavior and that females, on average, engaged in such behavior for longer periods of time than males. Stereotyped behavior was most often associated with a small, single cage. The average amount of observed stereotyped activity in monkeys housed in a small cage was significantly lower when the monkeys had access to either a foraging log or an exercise cage. Stereotyped behavior was also lower in female monkeys that were housed (either with a male or without a male) in a larger cage. The least amount of abnormal behavior was associated with the largest, most complex and enriched housing situation. Males and females housed in cages on the lower level of two-level housing engaged in more stereotyped behavior than did monkeys housed in the upper level, regardless of the presence or type of enrichment provided.     

Species differences in the interest shown in infants by juvenile female macaques (Macaca radiata andM. mulatta)

Using a focal animal technique, 16 juvenile female rhesus and bonnet macaques (2–3 years old) were observed with respect to the frequency and duration of their contacts with infants (0–1 year old). Each of these subjects was a member of one of four seminatural groups of macaques housed in 0.5-acre field cages at the California Primate Research Center. Rhesus juvenile females became very interested in infants when the latter were quite young, and maintained that interest throughout the study. When the infants were approximately 3–4 months old, the rhesus juveniles spent, on the average, 3.9 min/hr with those infants. By the time the infants were yearlings, the time spent with infants was approximately 6 min/hr. Relative to the rhesus, the bonnet juveniles showed less interest (about 2.2 min/hr) in young (3- to 4- month-old) infants, although by the time the infants were yearlings, the bonnets spent about 5.6 min/hr with them. Rhesus juveniles preferred sibling over nonsibling infants, but the presence of a sibling was not a necessary requirement for infant-directed behavior. The two bonnet juveniles who had infant siblings showed no preference for the latter. These data were interpreted within the framework of Quiatt’s [(1979) Am. Anthropol. 81: 310–319 conclusions about allomaternal behavior. Specifically, it was argued that, to the extent that there are species differences in maternal behavior, there should also be species differences in allomaternal behavior. The species differences in the maternal styles of rhesus and bonnet macaques provide a basis for an examination of this hypothesis.     

Assessing the effects of social environment on blood pressure and heart rates of baboons

The objective of this publication is to report on the feasibility of using a tether system for obtaining data on blood pressure and heart rates of socially housed primates and to evaluate the extent to which housing environment alters cardiovascular responses (mean arterial blood pressure and heart rate). Blood pressure and heart rates of adult male baboons (Papio cynocephalus hamadryas) were evaluated over a 6 week period under three different housing conditions: social companion, individual, and socially unfamiliar. Social environment was manipulated in a specially designed cage that incorporated removable panels of either woven wire or solid sheet metal. The design of the cage permitted nonhuman primates to engage in species-typical social behaviors such as grooming and aggression. Using a tether and catheter system, we monitored cardiovascular physiology. We tested the hypothesis that individual housing, housing with social companions, and housing with social strangers would produce different mean arterial blood pressure and heart rate responses. Individual housing and housing with strangers produced resting mean arterial blood pressures that were elevated relative to blood pressure responses with social companions. Individual housing and housing with social strangers produced different patterns of cardiovascular response. Individual housing resulted in lowered heart rates and elevated blood pressures relative to the social companion condition. Housing with social strangers resulted in both elevated blood pressure and elevated heart rate, relative to the social companion condition. Responses observed during this study demonstrated the sensitivity of blood pressure and heart rates to differences in social environment.     

Cage Toys Reduce Abnormal Behavior in Individually Housed Pigtail Macaques

As part of a behavioral intervention program that identifies and treats individual nonhuman primates exhibiting abnormal behavior, five individually housed pigtail macaques (Macaca nemestrina) were provided with multiple cage toys in an effort to reduce high levels of abnormal behavior. Ten 30-min observations of each subject were conducted during the baseline condition and again after novel toys were presented, both loose inside the cage and attached to the outside of the cage. The new toys were used during 27% of the observation time. Kong Toys were used most consistently by the macaques during the 5-week observation period. Significant decreases in abnormal behavior and cage-directed behavior, as well as significantly increased enrichment use, were evident after the toys were added. Several of the toys were destroyed quickly, and individual differences were evident in the levels of enrichment use and abnormal behavior. Providing multiple manipulable toys as enrichment for pigtail macaques was effective in reducing abnormal behavior and was an important part of an environmental enrichment program for monkeys who could not be housed socially.     

Cage toys reduce abnormal behavior in individually housed pigtail macaques

As part of a behavioral intervention program that identifies and treats individual nonhuman primates exhibiting abnormal behavior, five individually housed pigtail macaques (Macaca nemestrina) were provided with multiple cage toys in an effort to reduce high levels of abnormal behavior. Ten 30-min observations of each subject were conducted during the baseline condition and again after novel toys were presented, both loose inside the cage and attached to the outside of the cage. The new toys were used during 27% of the observation time. Kong Toys were used most consistently by the macaques during the 5-week observation period. Significant decreases in abnormal behavior and cage-directed behavior, as well as significantly increased enrichment use, were evident after the toys were added. Several of the toys were destroyed quickly, and individual differences were evident in the levels of enrichment use and abnormal behavior. Providing multiple manipulable toys as enrichment for pigtail macaques was effective in reducing abnormal behavior and was an important part of an environmental enrichment program for monkeys who could not be housed socially.