Styles of male social behavior and their endocrine correlates among high-ranking wild baboons

We have previously studied the relationship between dominance rank and physiology among male olive baboons (Papio anubis) living freely in a national park in Africa. In stable hierarchies, such males have distinctive secretory profiles of glucocorticoids and of testosterone. We find that these endocrine features are not, in fact, purely markers of social dominance; instead, they are found only among dominant males with particular stylistic traits of social behavior. One intercorrelated stylistic cluster revolved around the intensity with which the male is involved in sexual consortships (e.g., frequency of copulation, of grooming, degree to which feeding is suppressed by being in consortship). Males most involved in such consortships had the lowest basal cortisol concentrations and smaller cortisol stress-responses. A second stylistic cluster revolved around the degree of social affiliation (e.g., rate of grooming and interacting positively with non-estrus females and infants). Males who were highly affiliated had low basal cortisol concentrations and an attenuated cortisol stress-response. A third cluster revolved around the degree to which males could distinguish between highly threatening interactions with rivals and neutral or mildly threatening ones. Males most adept at this had lower basal cortisol concentrations. These behavioral/endocrine clusters were independent of each other. This suggests that the same adaptive physiological feature (e.g., low basal cortisol concentrations) may arise from different and independent personality styles. © 1992 Wiley-Liss, Inc.     

Rank-related differences in cardiovascular function among wild baboons: Role of sensitivity to glucocorticoids

In a population of wild baboons living in East Africa, we have observed endocrine differences among individuals as a function of dominance rank. Among these differences, we previously observed indirect evidence for dominant males being more. responsive to sympathetic catecholamines than were subordinate males. The present report tests this explicitly. Male baboons of known rank were anesthetized, and sympathetic and parasympathetic activity was pharmacologically inhibited. In experiment I, males were challenged with epinephrine; over a wide dose range, dominant males had the largest and fastest rises in systolic pressure, the greatest peak systolic pressure, and the most rapid recovery from the epinephrine challenge. Similar rank-related differences in heart rate response to epinephrine also occurred. Experiment II showed that this phenomenon probably reflects rank-related differences at both the heart and vasculature. As evidence, the same rank differences in systolic blood pressure responsiveness occurred when males were challenged with the alpha receptor agonist phenylephrine (which predominantly constricts systemic veins and arterioles), while the same rank differences in heart rate responses occurred following stimulation with the beta receptor agonist isoproterenol (which selectively works at the heart). These data were obtained from animals stressed by anesthetization, known to cause considerable glucocorticoid secretion in this population. Such steroids are well known for their capacity to augment catecholamine action. In experiment III, we blocked endogenous glucocorticoid secretion with the steroidogenesis inhibitor metyrapone, and repeated the epinephrine challenge. Under these conditions, the rank differences in epinephrine responsiveness were eliminated. Thus, dominant males are not so much preferentially sensitive to catecholamine action, as much as to the potentiating effects of glucocorticoids upon such action. In agreement, we have observed previously that dominant males are also more sensitive to glucocorticoid negative feedback regulation. © Wiley-Liss, Inc.     

Why should an aged male baboon ever transfer troops?

Dispersals by subadult or adult male baboons are common. In contrast, the occasional transfer of aged baboons is puzzling, given the physical dangers of transfer and the cognitive demands of mastering the ecological and social rules of a new troop. The present data suggest a possible explanation for such transfers in a study of two troops of olive baboons (Papio anubis) in Kenya. Aged males who remained in the troop in which they had been dominant were subjected to significantly higher rates of approach-avoid interactions by the current high-ranking cohort (i.e., the individuals they had dominated years past) when compared to males who had transferred into the troop in their old age. Thus, transfer in old age offers the advantage of relative anonymity. Of the 14 males who progressed into older adulthood in the same troop in which they were in their prime, seven ultimately transferred to a different troop. The seven who remained and the seven who transferred did not differ in the rate at which they were subjected to approach-avoid interactions. However, those who remained had significantly higher rates of various affiliative behaviors (copulations, consortships, grooming and contact with females, and positive interactions with infants). Thus, amid the disadvantages of an old age spent in the troop in which a male baboon was in his prime, a high degree of social affiliation might constitute a sufficient disincentive against transferring. © 1996 Wiley-Liss, Inc.     

Biochemical and hormonal correlates of dominance and social behavior in all-male groups of squirrel monkeys (Saimiri sciureus)

This study examined the relationship between dominance rank and several physiological and behavioral measures in stable, captive, all-male squirrel monkey groups. Four groups, each containing three males, were observed for 12 weeks during the breeding season. Relative dominance ranking among males in each group was based on the direction of agonistic behaviors displayed. For each subject, whole blood serotonin (WBS), plasma testosterone (T), and cortisol (C) were sampled 4 to 6 times over the course of the study. Samples were separated by 1- to 2-week intervals. Each group had a stable linear dominance hierarchy. WBS had small intraanimal variance and was positively related to dominance rank. In contrast, T and C were highly variable within subjects and were unrelated to dominance rank. Among alpha males, concentrations of T and C were positively correlated, and WBS and C were negatively correlated. The effect of dominance rank on the relationship between within-animal fluctuations in WBS, T, and C and behavior was also assessed. In dominant, but not subordinate subjects, intraanimal fluctuations in WBS correlated with agonistic behavior initiated, and fluctuations in C and T correlated with huddling. In beta and gamma males, C was related to agonism received, and in gamma males to food stealing received. Dominance status also affected endocrine response to the stress of capture but not the rate of sneezing. Sneezing was positively correlated with T concentrations irrespective of dominance rank. These results extend the association between WBS and dominance rank previously reported in Old World monkeys to a New World monkey species, support previous suggestions that mean T and C titers are not reflective of dominance rank in well-established groups, and indicate that dominance rank affects adrenocortical response to the stress associated with capture and anesthesia.     

Agonism,ranking, and the social behavior of adult male baboons

An ingrained technique in primatological analysis is to rank individual animals in a hierarchical system that is usually but not always based on the outcome of agonistic encounters. An explication of group structre and function is then sought by correlation these rankings with aspects of behavior. When the behavior of the adult males in a free-ranging troop of olive baboons is examined, ranking is found to be inadequate to represent the behavioral variability existing between individuals. The relationships maintained by these animals is analyzed, emphasizing amounts of time devoted to specific activities, and it is recommended that affiliative rather than agonistic behavior be stressed in future studies.     

The social contingency model and olive baboons

A theoretical and illustrative analysis of sequences of actions between pairs of olive baboons (Papio cynocephals anubis) is carried out using the social contingency model originally suggested by Jones and Gerard (1967) in social psychology. The model provides the basis for a step-by-step analysis and a typology. Signals from body postures, facial expressions, and vocalizations are subject to close study by using the model, in a similar fashion to its use in social skills analysis (Argyle, 1988). Sequences are categorized according to individual and joint strategies. Examples are given of three categories of contingency, reactive, mutual, and asymmetrical, which are adapted from their social psychological usage. The model is extended by a new category for competitive relationships between baboons: a conflictive category. The contingencies, as they are shown graphically, have a superficial resemblance to Tinbergen's (1951) zigzag diagrams, but their purpose is distinct in focusing on the detail of both infrequent and repeated interactions. The overall aim of the contingencies is to improve the analysis of social behavior at the proximate level and the model is potentially applicable to observation records at a level of detail that is often not utilized in reporting field studies.     

Male endocrine responses to females: Effects of social cues in cynomolgus macaques

This study tested the hypothesis that the hormonal responses of male macaques to sexually receptive females are mediated by specific socioenvironmental cues. Twelve, socially living male Macaca fascicularis were exposed to two-ovariectomized, estrogen-primed females under pair test, peer group, and peer group without dominant male conditions. Preexposure to postexposure changes in serum cortisol levels and testosterone levels were examined in relation to male dominance rank, age, and conditions of access to stimulus females. The males displayed significantly lower cortisol increases and greater testosterone increases with females under peer group than pair test conditions. Dominant males displayed greater testosterone increases than subordinate males under peer group conditions. The testosterone levels of subordinate males were greatly enhanced by removing the dominant male from each group. Adult males displayed greater cortisol responsivity to changes in conditions of access to females than did subadult males. Subadult males displayed greater testosterone responsivity to removal of the dominant male from the group than did adult males. It is concluded that specific social cues can greatly influence the endocrine responses of males to receptive females, and further, that there may be optimal socioenvironmental parameters for eliciting testosterone increases in male primates.     

The benefits of social capital: close social bonds among female baboons enhance offspring survival

Sociality has evolved in many animal taxa, but primates are unusual because they establish highly differentiated bonds with other group members. Such bonds are particularly pronounced among females in species like baboons, with female philopatry and male dispersal. These relationships seem to confer a number of short-term benefits on females, and sociality enhances infant survival in some populations. However, the long-term consequences of social bonds among adult females have not been well established. Here we provide the first direct evidence that social relationships among female baboons convey fitness benefits. In a group of free-ranging baboons, Papio cynocephalus ursinus, the offspring of females who formed strong social bonds with other females lived significantly longer than the offspring of females who formed weaker social bonds. These survival benefits were independent of maternal dominance rank and number of kin and extended into offspring adulthood. In particular, females who formed stronger bonds with their mothers and adult daughters experienced higher offspring survival rates than females who formed weaker bonds. For females lacking mothers or adult daughters, offspring survival was closely linked to bonds between maternal sisters. These results parallel those from human studies, which show that greater social integration is generally associated with reduced mortality and better physical and mental health, particularly for women.     

Odontometric variation among local populations of Kenyan olive baboons

This is a first report on a survey of local variations in genetic marker frequencies and morphometric features on Kenyan olive baboons. Data on dental casts of the upper dentitions of 207 baboons (115 males and 92 females) are analyzed with univariate and multivariate techniques. The materials represent 18 troops captured at 4 different localities. In general, levels of variability within and between localities are not great. The most marked variations present are in the premolar teeth. Females show greater variation than males. There are suggestive correlations between morphometric distance and geographic distance (positive) and morphometric distance and altitude difference (negative). There are some differences between this olive baboon sample and that of Swindler, McCoy & Hornbeck (1967) which lies close to a zone of olive-yellow baboon hybridization (Maples, 1972).     

Endocrine and behavioral correlates of drought in wild olive baboons (Papio anubis)

As part of a long-term study in behavioral endocrinology, wild olive baboons (Papio anubis) living in the Serengeti ecosystem of East Africa have been under study since 1978. The present report documents behavioral and endocrine changes associated with the severe drought of 1984. During this time, the annual rainy season failed and grassland biomass was severely reduced in the Serengeti. Baboons were able to maintain body weight but spent significantly more time foraging for food. In four prior years of study, basal testosterone concentrations were remarkably stable in adult and subadult males. In contrast, during the drought, there was a highly significant 60% decline in basal concentrations of the steroid. This testicular suppression was apparent in males of all ranks (by approach-avoidance criteria). Prior studies with this population, which examined the role of acute and chronic stressors in similarly suppressing testosterone concentrations, suggested that the present instance was in response to the stress of the drought. The drought was also associated with significant reductions in the rates of escalated aggression among males. However, the distribution of fights between high-ranking males, between low-ranking males, and between high- and low-ranking males did not change from prior years, nor was the dominance hierarchy inordinately unstable during this time. These findings agree with previous evidence that indicates that suppressed testosterone concentrations in males can be associated with lower rates of aggressive behaviors but that the steroid plays a predominantly facilitative rather than activational role. Finally, rates of approach-avoidance interactions and of male sexual behaviors were unchanged during the drought. These findings agree with an endocrine literature that indicates that reproductive behavior or physiology in primates is rarely disrupted by suppression of testosterone concentrations of the magnitude of the present case.     

Use of females by male olive baboons (Papio anubis)

Wild male olive baboons (Papio anubis) used females and infants as agonistic buffers. Male residency status determined whether a male used females or whether they were used against him. The success of the strategy depended on the cooperation of the female and the context of the interaction. Female cooperation correlated with preexisting social affiliation with the male user. Male choice of female or infant buffers represented a compromise between the potential effectiveness of each in different situations and the social and spatial availability of females and infants. Nonreproductive social relationships may provide long-term strategic benefits to the individuals who invest in them.     

Endocrine aspects of social instability in the olive baboon (Papio anubis)

The relationships among social status and the cortisol and testosterone stress-response were studied in the non-natal male members of a troop of olive baboons (Papio anubis) before and during a period of social instability. The unstable period was characterized by dominance interactions that were more frequent, more inconsistent, and produced less linear hierarchies than during the stable period. These changes occurred predominantly among the high-ranking males. Such males engaged in coalitions and consortship harassments at a higher rate during the unstable period than during the stable period. Finally, high-ranking males had the highest rates of involvement in and initiation of escalated fighting during the unstable period, in contrast with the stable period. A number of endocrine correlates of instability emerged. During the stable period, high-ranking males (by reproductive criteria) showed an endocrine profile different from that of subordinates. They had the lowest basal cortisol titers, the largest and fastest increases in cortisol titer during stress, and had elevated testosterone titers during stress. None of these attributes was found in high-ranking males during the unstable period. Males during the unstable period had elevated basal cortisol titers, suppressed cortisol responsiveness to stress, and no longer showed elevated testosterone titers during stress. When psychological advantages associated with social status in a stable social environment were lost, endocrine efficiency previously associated with social status was apparently also lost. Further, high-ranking males, who were most aggressive exclusively during the unstable period, had the highest absolute titers of testosterone exclusively during the unstable period. Thus, elevated testosterone and high levels of aggression were unrelated to social status during the period of social stability, but were traits associated with dominant individuals during the unstable period.     

Psychosocial and hormonal aspects of hierarchy formation in groups of male squirrel monkeys

Accounts of primate social dominance hierarchies often imply that the achievement of superior status is a “goal”, akin to a valued resource or commodity, and that hierarchies emerge in multimale groups from prolonged competitive conflicts over social status. This possibility is not consistent with our observations of five newly formed triads of adult male squirrel monkeys (Saimiri sciureus). Stable linear hierarchies based on clear asymmetries in the direction of intermale agonism and genital displays were established quickly, with virtually no reciprocal fighting, and in the absence of rank-related differences in plasma cortisol or testosterone. Although affiliative social overtures were initiated more often by high-ranking and middle-ranking males, affiliative overtures were directed equally often toward all members of each group. From the outset of the study all males, regardless of rank, spent an average of 33% of their time huddling in affiliative contact with male cagemates. These results suggest that in newly formed groups of adult male squirrel monkeys, social hierarchies reflect an expedient convention that reduces conflict and facilitates the formation of small cohesive groups. © 1994 Wiley-Liss, Inc.     

Intrasexual selection and male mating strategies in baboons and macaques

If baboon and macaque mating systems constitute a form of female defense polygyny, male mating strategies should be intrasexually selected and should vary in predictable ways with female defensibility, and demographic factors which affect the numbers of competing males per estrous female in populations. Substantial behavioral evidence exists for intrasexual selection of male mating strategies in baboons and macaques. Limited evidence also offers tentative support for theorybased predictions about the relationship between male mating strategy and female defensibility. Although male dominance rank generally predicts mating success, there are a number of factors which tend to increase the success of subordinate males above that expected from a simple dominance-based model of priority of access to mates.     

Endocrine and developmental correlates of unilateral cryptorchidism in a wild baboon

A wild, group-living 8.5-year-old adult baboon was found to have only a single palpable testicle, the only case of cryptorchidism found among more than 200 males that we have examined. This young adult had an unusually small body size for his age, one that was comparable to that of immature males two years younger, and during maturation his body mass was increasingly small for his age. As a young adult, he also had very low testosterone concentrations, which, in combination with his small size, history of impaired growth, and the absence of any obvious scars around the scrotum, suggest that this is a case of spontaneous unilateral cryptorchidism of unknown cause rather than one of monorchidism arising from injury. Despite striking differences in his growth, adult body size, and testosterone levels, the male's cryptorchidism seemed to have relatively little effect on his social and sexual maturation in his natal group. Nonetheless, it may be related to his inability to gain entry into another group after dispersal.     

Sex,social status and physiological stress in primates: the importance of social and glucocorticoid dynamics

Social status has been associated with health consequences, although the mechanisms by which status affects health are relatively unknown. At the physiological level, many studies have investigated the potential relationship between social behaviour/rank and physiological stress, with a particular focus on glucocorticoid (GC) production. GCs are of interest because of their experimentally established influence on health-related processes such as metabolism and immune function. Studies in a variety of species, in both naturalistic and laboratory settings, have led to complex outcomes. This paper reviews findings from primates and rodents and proposes a psychologically and physiologically relevant framework in which to study the relationship between social status and GC function. We (i) compare status-specific GC production between male and female primates, (ii) review the functional significance of different temporal patterns of GC production, (iii) propose ways to assess these temporal dynamics, and (iv) present novel hypotheses about the relationship between social status and GC temporal dynamics, and potential fitness and health implications. To understand whether GC production mediates social status-related fitness disparities, we must consider social contest conditions and the temporal dynamics of GC production. This framework will provide greater insights into the relationship between social status, physiological stress and health.     

Behavioural,endocrine and immune responses to repeated social stress in pregnant gilts

Pregnant sows are exposed to various stressors in intensive pig husbandry that may have negative consequences on their health, reproductive performances and welfare. Social stress is one of these challenges, because gestating sows have to be housed in groups according to EU guidelines (2001/88/CE). The purpose of this study was to determine the consequences of repeated social stress in pregnant female pigs on their behavioural, endocrine and immunological responses and on pregnancy outcome. Pregnant gilts were submitted to a repeated social stress procedure induced by housing unfamiliar gilts in pairs changed twice a week between days 77 and 105 of gestation (S group, n = 18). Control gilts were housed in stable pairs during the same period (C group, n = 18). Agonistic behaviour was observed during the first 3 h after each grouping. Skin lesions were numbered 2 h after each grouping. Salivary cortisol was measured before and repeatedly during the 4 weeks of grouping. Gilts were immunized against keyhole limpet haemocyanin (KLH) on days 81 and 95 of gestation. Immunoglobulins G against KLH, proliferative responses to concanavalin A, lipopolysaccharide, pokeweed mitogen and KLH and peripheral blood leukocyte numbers were evaluated 1 week before the first grouping and 3 days after the last one. Agonistic interactions and skin lesions were observed in S gilts at each grouping, although there was a decline between the first and the last grouping (P < 0.05). The repeated social stress induced a sustained endocrine response as shown by elevated salivary cortisol levels from 1 to 48 h after grouping in S gilts compared to C gilts. The cellular as well as the humoral immunity and the leukocyte numbers were not influenced by social stress. Gestation length tended to be shorter in S gilts (P = 0.09), but litter size, piglet weight or mortality at birth were not affected. Variability of the response of S gilts to groupings was partly explained by their average success value determined according to the outcome (defeat or win) of all the groupings. In conclusion, our study demonstrates that the application of repeated social stress to pregnant gilts during the last third of their gestation repeatedly activates their hypothalamo–pituitary–adrenal axis but does not impair their immune function and pregnancy outcome.     

Rank and grooming reciprocity among females in a mixed-sex group of captive hamadryas baboons

In a mixed-sex, captive group of hamadryas baboons (Papio hamadryas hamadryas) we investigated whether female grooming relationships are affected by their dominance ranks. Seyfarth's [1977] grooming for support model and Barrett et al.'s [1999] biological market model both predict that in primate groups where competition for monopolizable resources is high, grooming among females is based, at least partly, on the interchange of grooming for rank-related benefits, and that rank thus influences the distribution of grooming in females. Contrary to this prediction, our results show that despite the existence of a linear dominance hierarchy, rather strict dominance relationships, and high food-related aggression rates, grooming among female hamadryas baboons is not affected by rank and is only exchanged for itself. This is understandable since rank differences in our study group only result in differential access to limited, preferred food items that are not actively shared. Although some females are more likely to tolerate one another at the food pile, this tolerance is not determined by their grooming efforts and interchange of grooming for rank-related benefits does not occur. We conclude that female hamadryas baboons groom others in order to be groomed by them, which is supported by our observation that grooming reciprocity within a dyad increases when more grooming occurs in this dyad. Our results indicate that grooming is indeed a valuable commodity in itself, probably because of its stress- and tension-reducing effect. Based on our findings, the existing groom trade model is extended to include circumstances in which monopolizable resources are available but are not traded for grooming.     

Sex differences in the impact of social status on hair cortisol concentrations in rhesus monkeys (Macaca mulatta)

Social status impacts stress in primates, but the direction of the effect differs depending on species, social style, and group stability. This complicates our ability to identify broadly applicable principles for understanding how social status impacts health and fitness. One reason for this is the fact that social status is often measured as linear dominance rank, yet social status is more complex than simply high or low rank. Additionally, most research on social status and health ignores the effects of sex and sex-specific relationships, despite known differences in disease risk, coping strategies, and opposite-sex dominance interactions between males and females in many species. We examine the influence of social status, sex, and opposite-sex interactions on hair cortisol concentrations (HCC) in a well-studied species, rhesus macaques, where the literature predicts low ranking individuals would experience more chronic stress. Animals in three captive, seminaturalistic social groups (N = 252; 71 male) were observed for 6 weeks to obtain metrics of social status (rank and dominance certainty [DC]). DC is a measure of one's fit within the hierarchy. Hair samples were collected from each subject and analyzed for HCC. Generalized linear mixed models were used to examine (a) whether rank, DC, or sex predicted HCC; (b) whether same- or opposite-sex dominance relationships differentially impacted HCC; and (c) whether aggressive interactions initiated or received could explain any observed relationships. Results indicated that DC, not rank, predicted HCC in a sex-specific manner. For males, high HCC were predicted by receiving aggression from or having high DC with other males as well as having low DC with females. For females, only high DC with males predicted high HCC. These results likely relate to sex-specific life history pattern differences in inherited versus earned rank that are tied to female philopatry and male immigration.