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To determine if the presence of one or more familiar peers buffers the physiological effect of a stressor, 10 juvenile rhesus monkeys were removed from their natal group and placed together to form a new peer group. Six of the 10 juveniles were from the natal group of one or more others (companion subjects) whereas four juveniles came from entirely separate natal groups (alone subjects). Moreover, six matched juveniles remained in their natal group serving as controls. Two baseline blood samples were collected from all subjects, and then at 24 h, 1 week, and 4 weeks following the peer group formation. There was a significant interaction among the three study groups and sample times for absolute numbers of helper/inducer T lymphocytes, suppressor/cytotoxic T lymphocytes, and B lymphocytes, but not cortisol concentrations. Planned post hoc comparisons found that subjects introduced to the peer group, both those alone and those with companion(s), showed a significantly greater decline from baseline in lymphocyte subsets 24 h later compared to control subjects. It is of note that the alone subjects showed a significantly greater percent decline from baseline in helper/inducer T lymphocytes than companion subjects at 24 h, but not in suppressor/cytotoxic T lymphocytes or B lymphocytes, Planned post hoc comparisons for cortisol found that alone subjects showed significantly higher cortisol concentrations than those subjects with a companion only at the 1-week sample point. Proximity accounted for a significant portion of the variation (R = 0.66) in percent change in helper/inducer T lymphocytes at 24 h and this was a result of the companion subjects staying together. Results of this study confirm the stressful effect of removal from the natal group to a new social situation in juvenile rhesus monkeys and also adds to the growing body of human and nonhuman primate literature that the presence of companions can modulate the physiological effects of a stressor.

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Human epidemiological studies have suggested that social variables can modulate the effects of stress on the immune system, and this concept has been gaining increasing attention with positive results emerging from empirical studies using nonhuman primates over the last two decades. Results from a previous study in rhesus monkeys suggested that receiving grooming positively affected recovery of T-helper and T-suppressor cells following the initial stress associated with group formation, and this co-varied with high dominance rank. Thus, the present study was undertaken in order to determine: (1) if the stress effect of formation could be replicated in another species and (2) if social behaviors or dominance rank, given that formation is a stressor, might independently correlate with physiological recovery from the stressor. Eight adult female pigtail macaques were moved from individual cages and simultaneously introduced into an outdoor enclosure along with an adult male, while eight weight-matched controls remained in individual caging. Behavioral data were collected during the introduction and over 4 weeks thereafter. Blood samples were collected prior to and at intervals for 4 weeks following formation. Compared to control subjects, the test subjects showed an increase in basal cortisol secretion (+28.9%) and a significant decrease in T-helper cells (-33.6%), T-suppressor cells (-30.8%), and B cells (-22.5%), while there was a significant increase in white blood cells (+29.5%) 24 hr following formation. When dominance rank and seven behavioral categories were analyzed, only the frequency of receiving grooming significantly predicted change, with animals who received a greater frequency of grooms showing a lesser negative percent change from baseline in the absolute number of T-helper cells 1 week following formation. The establishment of a dominance hierarchy, apparent within 1 week, was accomplished with no serious fighting and a complete absence of wounding or trauma, suggesting that psychosocial stress was responsible for the physiological changes observed. © 1996 Wiley-Liss, Inc.

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Using a counterbalanced design, seven adult female rhesus monkeys were removed from their social group and housed in a novel environment both alone and with a companion chosen on the basis of quantitative affiliative behaviors. Blood samples (n = 2) were collected from all study animals before the exposure to the novel environment, then at 2, 24, and 96 h thereafter for cortisol and immunological analyses. During both conditions, subjects showed evidence of stress as indicated by elevated cortisol concentrations and decreases in absolute numbers of lymphocyte subsets. There was no significant interaction between condition (alone vs. companion) and time in cortisol percent change and further planned post hoc analyses showed no significant between-condition differences for any of the postseparation time points. Similarly, no significant interaction was found between conditions and time for the absolute number of CD4+CD8-T cells, CD8+CD4- T cells, or CD20+CD2- B cells. However, planned post hoc comparisons showed that subjects in the companion condition exhibited a significantly smaller percent change from baseline than in the alone condition at the 24 h and 96 h sample periods in absolute numbers of CD4+CD8- and CD8+CD4- T cells. Results showed that adult female rhesus monkeys exhibited a profound stress response when removed from their social group to a novel environment and that recovery time of T cell subsets was significantly enhanced by the presence of a preferred companion.

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The return of 6 juvenile mangabey monkeys to their social group following an absence of a year resulted in increased basal cortisol secretion for both the offspring and the mothers and in significant decrements in the absolute number of lymphocyte subsets for the offspring. Six 9-month-old sooty mangabeys were removed from their socially housed mothers, subsequently peer housed, and returned to the maternal social group 1 year later. Offspring showed a significant increase in cortisol levels 24 hr following reunion (48 +/- 6%) and this difference persisted through 1 month, while the mothers showed a significant increase only at the 24-hr sample point (18 +/- 3%). Moreover, the offspring, but not the mothers, showed a significant decrease in lymphocyte subsets which were evident through the 1-month sample point. Behavioral data revealed a significant positive correlation between the percent of total scan samples offspring were with their mothers (proximity, contact, huddle) the day of return and the offspring's percent change from baseline in total T cells 24 hr later, r = 0.84. All mother-offspring pairs with the exception of one exhibited frequent affiliative behaviors toward one another by 6 days following the return. These data demonstrate that the reunion of juvenile mangabeys with their mothers after a year's absence is an acute stressor for the mothers and a relatively longer term stressor for the offspring, and that behavioral interactions which characterize the return of individual subjects to the natal group can predict acute physiological responses.

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Psychosocial stress associated with the removal of six naive juvenile rhesus monkeys from their natal social group to peer housing resulted in increased basal cortisol secretion and significant decrements in the absolute numbers of the T lymphocyte subsets in the peripheral blood. Six subjects matched for age and social rank remained in the group of 80 animals serving as controls. Baseline immune and cortisol measurements were obtained before the six test subjects were removed from the group and housed together in an outdoor circular enclosure. Blood samples were taken 24 h following removal of the test subjects from the group and at intervals thereafter through 11 weeks. Compared to controls, test subjects showed a significant decrease in the absolute numbers of CD4+ (-56.9%) and CD8+ T cells (-57.6%) and a significant increase in basal cortisol levels (+43.9%) 24 h following removal to peer housing. Group difference in the absolute numbers of most immune cells persisted through 11 weeks, whereas cortisol differences lasted only through 2 weeks. These data, when compared to an earlier study employing an identical protocol, with the exception that subjects were housed in indoor individual cages following separation, fail to demonstrate a modulating effect of randomly chosen peer-mates on the stress effects produced by social separation.

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Removal of juvenile rhesus monkeys from their natal social group to indoor individual caging resulted in increased basal cortisol secretion and significant decrements in the frequency of lymphoid subpopulations. Fourteen juvenile rhesus monkeys, which had never been removed from the group, were studied. Baseline immune and cortisol measurements were obtained before seven of the subjects were removed from social housing to standard individual cages. The remaining seven subjects, matched for age, sex, weight, and rank, remained in the social group throughout the study serving as controls. Blood samples were taken 24 hours after removal of the test subjects from the group and at specific intervals thereafter through 11 weeks. At 24 hours after the separation test subjects showed a significant increase in basal cortisol levels (40%) and a significant decrease in several immune parameters, with absolute numbers of total T cells declining 72 +/- 12%. Significant group differences in immune parameters persisted through 11 weeks. Eighteen weeks following removal, the test subjects were returned to the group which produced a cortisol rise in both test and controls at the 24-hour postreturn sample. Although there were no group differences in the frequency of lymphoid subsets 24 hours after return, some test subjects showed marked decrements which were inversely related to cortisol and were predicted by behavioral events. These data demonstrate that the removal of naive juvenile rhesus monkeys from their natal social group to individual indoor caging is a potent psychosocial stressor and that the behavioral interactions which characterize the return of the individual subjects to the natal group may predict physiological response.

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Social stress associated with the formation of a new group of rhesus monkeys resulted in increased basal cortisol secretion and significant decreases in immunological parameters. Eight adult female rhesus monkeys, all of which had been raised in social groups, but with no common social history, were simultaneously introduced into an outdoor enclosure along with an adult male. Behavioral data were collected during the introduction and over 9 weeks thereafter. Blood samples were collected prior to and at intervals for 9 weeks following formation. The establishment of a dominance hierarchy, apparent within 48 h, was accomplished with no serious fighting and a complete absence of wounding or trauma. Overall, the group showed a significant increase in cortisol and a significant decrease in the absolute number of total lymphocytes and CD4+ and CD8+ T cells at 24 h postformation, but not thereafter. However, when partitioned into high and low dominance rank, differences in CD4+ and CD8+ T cells were evident for up to 9 weeks with low ranking subjects showing significantly lower values. The housing condition of the subjects immediately prior to introduction, either indoors in individual caging or outdoors in social groups, may have influenced behavior, rank acquisition, and possibly differences in immune parameters. These data demonstrate that social group formation is a potent psychosocial stressor in primates, since stress-sensitive changes were observed in the absence of serious aggression and wounding.

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One of 15 rhesus macaques infected with SIVsmm9 developed profound hemolysis with spherocytosis, reticulocytosis, and IgG and complement at the red blood cell surface. A female offspring born to this animal developed similar findings. Furthermore, cold agglutinins were noted in samples from both animals. Four of the 13 animals remaining in the cohort had weakly positive antiglobulin tests but were not anemic. Autoimmune hemolytic anemia may be an underrecognized cause of anemia in SIV infection.

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A panel of monoclonal antibody reagents has been identified that can be used for routine monitoring of subsets of peripheral blood mononuclear cells (PBMC) from Macaca mulatta (rhesus macaques), Macaca nemestrina (pig-tailed macaques), and Cercocebus atys (sooty mangabeys). The procedure uses fluorescein and phycoerythrin conjugates of the monoclonal antibodies in appropriate combinations, so that two-color microfluorometric analyses can be readily performed on as little as 1.2 ml of EDTA blood. PBMC from a total of 20 normal adult rhesus macaques, 21 normal adult pig-tailed macaques, 4 SIV- sooty mangabeys, and 16 SIV+ adult sooty mangabeys were analyzed with the panel of monoclonal reagents and flow microfluorometry. The mean frequency, absolute numbers, and range for each subset in these nonhuman primate species are described. Sooty mangabeys appeared markedly different from the other two primate species. The PBMCs from the mangabeys had a higher mean frequency and absolute number of total T cells, Leu-3a+/18- T cells, suppressor (Leu-2a+) T cells, which were HLA-DR+, and IL-2R+ cells. Functional helper, suppressor, natural killer (NK), lymphokine activated killer (LAK), and antigen-presenting cell studies were also performed to correlate phenotype with immune function. Data indicate that Leu-3a+ T cells (CD4+) and Leu-2a+ T cells (CD8+) in these primate species represent human equivalents of helper and suppressor T cells, respectively. NK and LAK effector cells in the rhesus and pig-tailed macaques appear to be predominantly Leu-19+. In contrast, Leu-2a+ cells appear to be the predominant NK and LAK effector cell in sooty mangabeys. These data provide a basis for routine evaluation of lymphocyte subsets in these nonhuman primate species, and provide a means to correlate phenotype with immune function.

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