Deborah A. Gust

A longitudinal investigation of gestural communication in young chimpanzees

A longitudinal study of chimpanzee gestural communication is reported. Subjects were seven 5- to 8-year-old members of a semi-natural group at the Yerkes Field Station. These were the same individuals observed byTomasello et al. (1985) four years previously. Nearly identical operational definitions and observational procedures were used in the two studies. Longitudinal comparisons between the two observation periods revealed that the development of chimpanzee gestural communication is best characterized as a series of ontogenetic adaptations: as particular social functions (e.g., nursing, playing, grooming, etc.) arise, decline, or change, gestural communication follows suit. Most gestures seem to be conventionalized by individuals in direct social interaction with conspecifics. Some gestures may be learned by “second-person imitation”—an individual copying a behavior directed to it by another individual. No evidence was found for “third-person imitation”—an individual copying a gesture used between two other individuals. Implications for the concept of chimpanzee “culture” are discussed.

Relationship between Social Factors and Pituitary-Adrenocortical Activity in Female Rhesus Monkeys (Macaca mulatta)

Psychosocial stress in humans has been related to the occurrence or progression of certain diseases and a positive social environment has been shown, in some cases, to ameliorate this effect. In many experimental studies changes in serum cortisol levels have been used as an endocrine-defined stress response, however, the variation in this measure under unchanging conditions in socially housed animals is not well documented. The present study was designed to examine the relationship between specific social behaviors and concentrations of serum cortisol in female rhesus monkeys. Subjects were members of one of two social groups. One was an established long-term (8 years) group with members which had from one to many kin, while the second was a group formed 5 months prior to the onset of the present study composed of initially unfamiliar animals. Blood samples were collected weekly and a total of 16 hr of behavioral data was collected on each subject. For purposes of analyses, the year-long study was organized according to calendar quarters (3 months) with cortisol concentrations averaged and behavioral categories cumulated. When regression techniques were applied, it is of note that neither group nor dominance rank was a predictor of cortisol levels. However, when a correlation analysis was applied to each group separately to assess the effect of dominance rank, rank significantly correlated with cortisol levels in the established but not in the recently formed group. In each quarter, analyses revealed behavioral categories which combined to account for a significant proportion of the variance in cortisol levels, but these behaviors were not identical over the four quarters. For three of the four quarters analyzed, and for the year as a whole, an affiliative behavioral category was predictive of cortisol levels in addition to agonistic behavioral categories. These data suggest that cortisol levels are influenced by not only negative interactions, such as receiving bites, but also by positive interactions such as receiving grooms. Results also showed that reconciliatory behaviors occurred significantly more frequently following dyadic agonistic episodes in the recently formed versus the long-term group. The higher rate of reconciliatory behaviors exhibited by the recently formed group may account for the lack of a dominance rank/cortisol relationship.

Formation of a new social group of unfamiliar female rhesus monkeys affects the immune and pituitary adrenocortical systems

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.

Effect of a preferred companion in modulating stress in adult female rhesus monkeys

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.

Social separation and reunion affects immune system in juvenile rhesus monkeys

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.

Effect of companions in modulating stress associated with new group formation in juvenile rhesus macaques

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.

Response to removal from and return to a social group in adult male rhesus monkeys

The removal of four adult rhesus monkeys from a large social group (n = 85) to peer housing resulted in no significant changes in basal cortisol levels or absolute numbers of T lymphocyte subsets 24 h later. However, the return of these males 1 year later to the same social group resulted in significant increases in cortisol levels (66 +/- 21%) and significant decreases in T-helper (-31.6 +/- 15.8%) and T-suppressor cells (-35.2 +/- 8.7%) 24 h later. Blood samples for immune and cortisol measurements were obtained before and 24 h following both the removal and the return 1 year later. Aggressive and sexual behavioral data were recorded on audiotape for 3.5 h following the reintroduction using an all occurrences of some behaviors sampling technique. Analyses revealed a negative correlation between percent change from baseline in T-helper cells 24 h following the return and the frequency of bites (nonwounding) and chases received during the 3.5 h following the return. The absence of a stress response to separation in adult males is in contrast to the presence of a stress response observed in infants, juveniles, and adult females and possibly is due to sex differences in group attachment in sexually mature males. On the other hand, the return to the social group did induce a psychosocial stress response in the males, and the degrees of the stress, as determined by cortisol and immune cell measures, was related to the agonistic interactions experienced by the individuals.

Removal from natal social group to peer housing affects cortisol levels and absolute numbers of T cell subsets in juvenile rhesus monkeys

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.

Group formation of female pigtail macaques (Macaca nemestrina)

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.

Alpha-male sooty mangabeys differentiate between females' fertile and their postconception maximal swellings

Alpha-male sooty mangabeys in four separate social groups discriminated between a female’s fertile and her postconception maximal swelling, confirming a previous finding that one alpha male, but not other males in the group, refrained from mounting females during the postconception maximum swelling. During a 3-hr observation session, the males mounted females an average of 2.2 ± 0.3 times during the females’ fertile maximal swelling, while there were no mounts by alpha males during the females’ postconception maximal swelling. Alpha males also showed higher durations of following and frequencies of genital inspection toward females during the fertile maximal swelling. Additionally, we collected blood samples from four females three times per week to monitor estradiol (E2), progesterone (P4), and luteinizing hormone (LH) changes during both swelling phases. Peak E2 concentrations preceded the maximal swelling during both the conception and the post-conception swelling, though to a greater extent during the latter period. Although 3×-weekly blood samples showed significantly greater E2 concentrations during the postconception swelling, daily samples to confirm the results revealed one instance of comparable concentrations of E2 during a fertile swelling. Thus, peak E2 concentrations may not differ during the conception and postconception swelling cycles, though the duration of the E2 elevation is longer during the postconception swelling. LH concentrations, corresponding to the conception and postconception maximal swelling, were significantly different, while P4concentrations were not. The behavioral results indicate that alpha males discriminate between a fertile swelling (associated with ovulation) and a nonfertile swelling (occurring approximately 49 days postconception); however, whether this discrimination is tied to the difference in the hormonal pattern has yet to be demonstrated.