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.     

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.     

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.     

The effect of cage size and enrichment on core temperature and febrile response of the golden hamster

The aim of this study is to determine the effect of cage size and cage enrichment. Golden hamsters were individually housed in standard cages of four different sizes and in enriched cages of three different sizes since 3 weeks of age. Each of the seven housing groups consisted of 12 hamsters. After 14 weeks of housing in their respective environments the measurements started. The mean baseline rectal temperature was significantly higher in hamsters housed in small cages than in hamsters housed in large cages. After the injection of fever-inducing lipopolysaccharide rectal temperature increased by 1 to 2 degrees C. The increase of rectal temperature and the fever index were the highest in animals housed in large cages and the smallest in animals housed in small cages. Through cage enrichment and increasing cage size the mean febrile response increased while the mean baseline rectal temperature decreased. Cage size and cage enrichment had no effect on the dispersion of the measured values. The differences in microclimate between large and small cages were too small to have an effect on thermoregulation. The results indicate that housing in small cages induce chronic stress which obviously affects thermoregulation. The findings demonstrate that the results of some physiological experiments are significantly influenced by the pre-experimental housing conditions.     

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.     

Heterosexual housing increases the retention of courtship behavior following castration and elevates metabolic capacity in limbic brain nuclei in male whiptail lizards,Cnemidophorus inornatus

In male vertebrates the display of courtship behavior depends on the presence of testicular androgens. However, social experiences in adulthood can alter the hormonal dependence of courtship behavior in a variety of species, and we have previously proposed that these behavioral changes are linked to changes in neural metabolic capacity (cytochrome oxidase activity). Here we investigated the effects of prior social experience (housing with females vs housing in isolation) on the retention of courtship behavior following gonadectomy and on cytochrome oxidase (CO) activity in male little striped whiptail lizards, Cnemidophorus inornatus. In Experiment 1, we found that males that were previously housed with females (HWF males) continued to display courtship behavior longer after castration than males previously housed in isolation (ISOLATE males). This is similar to the behavioral plasticity found in rodents and cats. On the other hand, courtship behavior while gonadally intact was indistinguishable between HWF and ISOLATE males. Because all males were housed individually following castration, the difference is due to different social experiences prior to castration. In Experiment 2, we found that gonadally intact HWF males had significantly elevated CO activity in the preoptic area, amygdala, and anterior and ventromedial hypothalamic areas relative to intact ISOLATE males. No significant differences in metabolism were found in the lateral septum, lateral hypothalamus, and habenula or in hindlimb muscle, suggesting that the increase in metabolism is specific to brain nuclei involved in courtship behavior. Altogether, this demonstrates that elevations in metabolic capacity correlate with experience-dependent increases in robustness to castration.     

Development of a system for individual feeding of baboons maintained in an outdoor group social environment

We developed a system that allows individual feeding of adult baboons, 8-15 years of age, maintained in an outdoor group social environment. The purpose of the system is to allow careful monitoring and control of individual diet. Baboons were housed in two group cages, 16 females and a single male in one and 12 females and a single male in the other. Baboons exited the group cage once daily and passed along a chute and over a scale into individual cages where they received their individual diets. Food intake was monitored during their 2-hour stay in the individual cages. Baboons rapidly learned to use this system. Food intake and weight were stable within 20 days. Food consumed decreased during the period of sexual receptivity. The maintenance of the group social environment allowed observations on the group's dominance structure and the relationship of dominance to food consumption. Speed of food access in the group cage was related to dominance. Dominance was not related to food consumed in individual cages. The system permits study of many variables related to behavior and food intake while still retaining critical social interactions.     

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.     

The effects of cage size and pair housing on exercise of beagle dogs

One of the requirements of the 1985 amendments to the Animal Welfare Act is the establishment of an exercise program for dogs. Assumptions have been made by some that larger cages or the presence of a companion animal will motivate exercise. To examine how cage size, pair housing and human contact affect exercise, a study was conducted using a computerized video-data acquisition system that measured distance traveled and time spent moving in 1 x 1 m, (single only) and 1 x 2 m (single and paired) and 1 x 1.5 m cage (paired only) cages. Male beagle dogs (n = 6) housed singly in the 1 m2 cage traveled an average of 55 m/hr spending only 8% (57 min) of the 12 h photo period in motion. When the cage size was doubled, the average distance traveled decreased to 13 m/hr and the time spent moving increased to 11% (77 min/day). When dogs were pair housed in a regulation size cage, the average distance traveled decreased to 8.6 m/hr and they spent less than 6% of the day in exercising (42 min/12 hrs). The greatest amount of exercise was seen when dogs were housed as a pair in a cage less than recommended size (an average of 109 m/hr and 8.8 min/hr). Therefore, these data indicate that larger cages or pair housing in regulation size cages have little or no effect on the activity of purpose bred male beagle dogs. There was, however, a direct correlation between activity, time and distance, and the presence of humans in the animal room.(ABSTRACT TRUNCATED AT 250 WORDS)     

Long-term isolated housing causes anxiety in C57BL/6J female mice

Behaviour of female C57BL/6J strain mice was studied in the elevated plus-maze and Porsolt's tests after either long-lasting individual housing or keeping with daily shifting group-housed females (social instability). After 2-3 months, an increased level of anxiety in the individually housed females was revealed in the elevated plus-maze. However, in 3 months the least passive behaviour in the Porsolt's was in the individually housed females. No changes were found in behaviour of females individually housed at 3 weeks of age for 4 months. Also, females with preliminary social contacts with males and following individual housing for one month had not any abnormalities in the used behavioural tests. Social instability conditions did not significantly influence the females' plus-maze behaviour, but decreased the passive behaviour in the Porsolt's test.     

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.     

Cooperative social coordination and aggression in male laboratory rats: effects of housing and testosterone

A cooperative behavior, coordinated shuttling by pairs of laboratory rats in a rectangular chamber, can be influenced strongly by an interaction between housing and sex. Males and females learn readily when housed together socially, but individual housing ("isolation") causes severe deficits selectively in males. The aim of the present study was to examine the role of testosterone in the differential effects of housing on cooperation learning. Males of a Sprague-Dawley derived strain were housed socially or individually and treated daily in one of three ways (six groups, n = 6 per group): (1) castrated, injected with oil vehicle (without testosterone); (2) castrated, injected with 500 micrograms testosterone propionate (exogenous TP); and (3) sham operated, injected with oil (intact, endogenous testosterone). Socially housed pairs learned readily in all treatment groups, using strategies of coordination in which stereotyped contact or aggressive interactions were interpolated. Individual housing was associated with a deficit, but only in the TP-treated and intact groups in which some pairs either did not learn or performed poorly. The deficit was associated with violent fighting and extreme and stable differentiation into dominants and subordinates, the latter exhibiting prolonged freezing. Oil-treated castrates, when housed individually, were unimpaired and actually surpassed their socially housed counterparts on some measures. Their success was associated with an increase only in low-level aggression. The housing-hormone interaction in male rats suggests that testosterone influences the capacity to develop cooperative behavior by modulating both aggression and its consequences for the relationship between partners. The use of social interaction models, including cooperation, for the study of behavior-hormone interactions was also discussed.     

Pair-housing of male and female rats during chronic stress exposure results in gender-specific behavioral responses

Social support has a positive influence on the course of a depression and social housing of rats could provide an animal model for studying the neurobiological mechanisms of social support. Male and female rats were subjected to chronic footshock stress for 3 weeks and pair-housing of rats was used to mimic social support. Rats were isolated or housed with a partner of the opposite sex. A plastic tube was placed in each cage and subsequently used as a 'safe' area in an open field test. Time spent in the tube was used as a measurement of anxiety levels. Chronic stress increased adrenal weights in all groups, except for isolated females who showed adrenal hypertrophy in control conditions. In isolated males, chronic stress resulted in an increase in the time the animals spent in the tube. While stress did not affect this parameter in socially housed males, males with a stressed partner showed a similar response as isolated stressed males. Even though adrenal weights showed that isolated females were more affected by stress, after chronic stress exposure, they spent less time in the tube than socially housed females. Socially housed stressed females spent less time in the 'safe' tube compared to control counterparts, indicating that stress has a gender-specific behavioral effect. In conclusion: pair-housing had a stress-reducing effect on behavior in males. Isolation of females was stressful by itself. Pair housing of females was not able to prevent stress-induced behavioral changes completely, but appeared to reduce the effects of chronic stress.     

The physiological and behavioral impact of sensory contact among unfamiliar adult mice in the laboratory

Housing mice in the laboratory in groups enables social interaction and is the way a laboratory should house mice. However, adult males show reciprocal aggression and are therefore frequently housed individually. Alternatively, a grid divider, which allows sensory contact by sight and smell but prevents fighting and injuries, can separate mice within 1 cage. This study examined the influence of this housing method on various physiological and behavioral parameters. Adult male mice housed for 10 days with sensory contact to an unfamiliar male displayed significant increases in heart rate (HR), body core temperature (BT), and motor activity (ACT). Furthermore, the mice suffered impaired nest-building behavior and significantly reduced body weight. Conversely, males housed in a similar manner with a female companion showed only a transient elevation of ACT, BT, and HR. Although no clear beneficial effect of housing males with sensory contact to females was evident, this study could not exclude it. On the other hand, housing of mature males in this way leads to sustained detrimental alterations of physiology and behavior, thus implying severe impairment of animal well-being.     

Infant behaviors in mother-reared and harem-reared baboons (Papio cynocephalus)

Seven groups of socially living baboons between the ages of 0 and three months were observed at the Southwest Foundation for Research and Education, San Antonio, Texas. Six groups were harems containing one adult male (the biological father), the nursing mothers and their infants, and adult females without offspring. The other group consisted only of nursing mothers and their infants. All seven groups were housed in identical outdoor enclosures 45 m × 27 m × 23 m. Fourteen behavioral categories were tested. The hypothesis that behavioral sex differences in infant baboons are influenced by the presence of an adult male was not supported by the test results. Sex differences were not detected in either the mother-reared infants or in harem-reared infants. Mother-reared infants (n=13) had significantly greater scores for contact aggression and non-contact aggression categories, whereas harem-reared infants (n=12) scored significantly higher for locomotion, non-aggressive social behaviors, exploration, and rough-and-tumble play.     

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.     

The effect of prior housing conditions on the sexual receptivity of females of the blowfly,Lucilia cuprina

Sexual receptivity in sugar-and-water-fed females of the anautogenous blowfly Lucilia cuprinawas low when they had been housed in groups but high when they had been housed singly. Females were completely unreceptive on the second and third days after emergence, irrespective of housing conditions. There after receptivity increased but more rapidly in the singly housed females. Experiments in which females were housed singly for some days and then in groups, or vice versa, showed that receptivity could be influenced by housing conditions experienced both over the first 5 days after emergence and later in life.     

Baboons (Papio anubis) living in larger social groups have bigger brains

The evolutionary origin of Primates' exceptionally large brains is still highly debated. Two competing explanations have received much support: the ecological hypothesis and the social brain hypothesis (SBH). We tested the SBH in (n = 82) baboons (Papio anubis) belonging to the same research centre but housed in groups with size ranging from 2 to 63 individuals. We found that baboons living in larger social groups had larger brains. This effect was driven mainly by white matter volume and to a lesser extent by grey matter volume but not by the cerebrospinal fluid. In comparison, the size of the enclosure, an ecological variable, had no such effect. In contrast to the current re-emphasis on potential ecological drivers of primate brain evolution, the present study provides renewed support for the social brain hypothesis and suggests that the social brain plastically responds to group size. Many factors may well influence brain size, yet accumulating evidence suggests that the complexity of social life might be an important determinant of brain size in primates.     

Social housing influences the composition of volatile compounds in the preputial glands of male rats

In rodents the preputial glands are one of the major sources of pheromones. These volatile chemosignaling compounds are known to elicit specific behavioral and physiological effects in their conspecifics. While social stress can alter both the behavior and hormonal status of rodents, little is known about its influence on the volatile constituents of the preputial glands. We have examined the composition of volatile compounds in the preputial glands of gonadally intact male rats housed for 70 days in either unisex triads (three/cage) or singly. The rank status of triad-housed rats was based on quantitative behavioral assessments taken during the initial 30 min of triad housing. Dominant rats had heavier preputial glands compared to subdominant and subordinate rats. Capillary gas chromatography-mass spectrometry identified 56 volatile preputial compounds, of these 17 did not differ between groups while 26 compounds were significantly higher in the single-housed compared to the triad-housed rats. Six additional volatile compounds were higher in the dominant compared to the other 3 groups, while another six compounds were higher in both the dominant and single-housed rats compared to the subdominant and subordinate rats. It can be concluded that both housing condition and social rank status have significant but different effects on the composition of volatile compounds found in preputial glands of male rats. The physiological and behavioral significance of these changes in preputial gland volatile compound composition in rats remain to be investigated.