Jacinta C. Beehner

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.

Factors Affecting Reproduction and Mortality Among Baboons in the Okavango Delta, Botswana

We present results of a 10-year study of free-ranging gray-footed chacma baboons (Papio ursinus griseipes) in the Okavango Delta of Botswana. The majority of deaths among adult females and juveniles were due to predation, while infants were more likely to die of infanticide. There were strong seasonal effects on birth and mortality, with the majority of conceptions occurring during the period of highest rainfall. Mortality due to predation and infanticide was highest during the 3-mo period when flooding was at its peak, when the group was more scattered and constrained to move along predictable routes. The reproductive parameters most likely to be associated with superior competitive ability—interbirth interval and infant growth rates—conferred a slight fitness advantage on high-ranking females. However, it was counterbalanced by the effects of infanticide and predation. Infanticide affected high- and low-ranking females more than middle-ranking females, while predation affected females of all ranks relatively equally. As a result, there were few rank-related differences in estimated female lifetime reproductive success.

Female chacma baboons form strong, equitable, and enduring social bonds

Analyses of the pattern of associations, social interactions, coalitions, and aggression among chacma baboons (Papio hamadryas ursinus) in the Okavango Delta of Botswana over a 16-year period indicate that adult females form close, equitable, supportive, and enduring social relationships. They show strong and stable preferences for close kin, particularly their own mothers and daughters. Females also form strong attachments to unrelated females who are close to their own age and who are likely to be paternal half-sisters. Although absolute rates of aggression among kin are as high as rates of aggression among nonkin, females are more tolerant of close relatives than they are of others with whom they have comparable amounts of contact. These findings complement previous work which indicates that the strength of social bonds enhances the fitness of females in this population and support findings about the structure and function of social bonds in other primate groups.

The effect of new alpha males on female stress in free-ranging baboons

In chacma baboons, Papio hamadryas ursinus, young adult males often rise to the top of the dominance hierarchy shortly after immigrating to a new group. Such events are potentially disruptive for pregnant and lactating females because high-ranking immigrant males often commit infanticide. In this preliminary study, we assessed the effects of upheavals in the male hierarchy on the physiology of 18 females in a baboon group living in the Moremi Game Reserve, Botswana. We collected behavioural and hormonal data to examine the effects of two separate events, a natal male take-over and an immigrant male take-over, on female faecal glucocorticoids (fGC). While few females had elevated fGC concentrations in response to the natal male take-over, following the immigrant male take-over there was a significant rise in fGCs, but only among lactating and pregnant females. Analysis of behavioural data indicated that elevated fGC concentrations were unrelated to male aggression towards females, female–female aggression, or rates of female–female grooming. Furthermore, lactating females with a male ‘friend’ during the immigrant male take-over period had a less marked increase in fGCs and lower fGC concentrations overall than females without a male friend. Taken together, these results suggest that male social instability itself does not necessarily elicit a stress response from females. Rather, it is the specific male that rises to the alpha position that prompts a stress response, and only from the females at risk for infanticide. Finally, females with a male friend may perceive themselves to be at a reduced risk of infanticide.

Testosterone predicts future dominance rank and mating activity among male chacma baboons

Despite the many benefits that testosterone has on male reproduction, sustaining high levels of testosterone for long periods can be costly. The challenge hypothesis predicts that males will show temporarily sustained elevations of testosterone at critical periods, counterbalanced by decreased levels during noncritical periods. We investigated male testosterone measures extracted from fecal samples in a group of chacma baboons (Papio hamadryas ursinus) living in the Okavango Delta, Botswana. Because rank serves as a proxy for competition for mates, we examined how male testosterone was related to dominance rank, age, aggression, and mating activity. Males showed an elevation in testosterone at maturity; young adult males had the highest testosterone levels followed by a steady decline with age. Among dispersing males, testosterone was temporarily elevated in the month following dispersal. After controlling for age, testosterone and rank were unrelated, but testosterone and changes in rank were positively correlated, such that males rising in rank had higher testosterone than males falling in rank. Thus, for males in this group, testosterone was predictive of a males rank trajectory, or future rank. Similarly, male testosterone levels predicted future, rather than current, mating activity. Finally, male testosterone and aggression rates were unrelated during stable periods in the dominance hierarchy but positively related during unstable periods when high ranks were being contested. In general, our results support the challenge hypothesis with males exhibiting elevated testosterone in association with the acquisition of high rank (ensuring access to mates), rather than with mating itself.

Female hierarchy instability, male immigration and infanticide increase glucocorticoid levels in female chacma baboons

Female baboons (Papio hamadryas spp.) must contend with myriad potential stressors on a daily basis. In a previous study on female chacma baboons, Papio hamadryas ursinus, living in the Okavango Delta of Botswana, increases in glucocorticoid (GC) concentrations were associated with female reproductive stage, male immigration and the threat of infanticide. Here, we extend this previous analysis to a larger data set with several additional potential stressors, including actual infanticide and instability in the female dominance hierarchy. A general linear mixed model showed that reproductive state, male immigration, infanticide, female rank instability and predation all had significant effects on GC levels. Lactating females’ GC levels increased in response to the arrival of immigrant males and increased even further when infanticide occurred. In contrast, cycling and pregnant females’ GC levels did not change. Females also showed elevated GCs in response to instability within their own dominance hierarchy, especially if their own ranks were at risk. Females’ stress responses were frequent, but specific to events that threatened their own lives, the lives of their offspring, or their dominance ranks.

Correlates of stress in free-ranging male chacma baboons, Papio hamadryas ursinus

In male baboons, social instability is known to increase concentrations of glucocorticoids (GCs), a class of steroid hormones associated with the vertebrate stress response. The stress response may be particularly marked among male chacma baboons, whose social groups often demonstrate a strong mating skew and high rates of infanticide. Here we test this prediction and explore additional correlates of variation in concentrations of GCs measured in faeces. We collected 482 faecal samples from 13 males over 14 months. Changes in the male hierarchy were the major source of GC variation. Such instability occurred as the result of a new immigrant male’s take-over of the alpha position, a resident male’s rise to the alpha position, and the rise in rank of a young natal male. All three events were correlated with elevated GCs among all males and higher rates of male–male aggression than were found during periods of stability. The interaction between rank and instability had a significant effect on GC concentrations; low-ranking males had higher GCs during stable periods, whereas high-ranking males had higher GCs during unstable periods. Males that dispersed had elevated GCs in the month following immigration but not at other times, including the month preceding emigration. Finally, entering into a sexual consortship led to a temporary increase in a male’s GC measures. By contrast, seasonal changes and a male’s age were unrelated to GCs. GC variation in chacma males was primarily explained by temporary elevations following events that relate to reproductive fitness.

Factors affecting individual participation in group-level aggression among non-human primates

Summary Group members do not always act cohesively when facing extra-group rivals. When benefits such as group-defence are not monopolizable, it poses an economics problem: who should contribute to public goods and who should freeload? A collective action framework compliments existing theoretical explanations for cooperation, and provides testable hypotheses about group-level behaviour based on individual costs and benefits. Using this approach, we review research on intergroup encounters in non-human primates published over the last 20 years, focusing on participation by different classes of individuals. While food- and matedefence explain much between-sex variation in participation, rank and reproductive access frequently explain within-sex variation. In some species, individuals may use intergroup interactions to survey potential transfer locations and mating options, which might coincidently intimidate rivals. Experimental evidence suggests that when intergroup dominance is based on relative number of fighters, individual participation still varies with sex, rank, companion behaviour and dependent offspring presence. Relatively few studies have examined how factors such as relationships within and between groups or individual temperament mediate aggression. Long-term studies of multiple habituated groups and methodological advances (e.g., playback experiments) will continue to improve our understanding of how complex group-level patterns are predictable when viewed from an individual perspective.

Modifications of a field method for fecal steroid analysis in baboons

By extracting steroid metabolites from feces, researchers can track endocrine activity noninvasively in free-ranging animals. Sample preservation is a critical component of such methods because steroid metabolites rapidly decompose. Here, we describe a method for preservation, field extraction, and radioimmunoassay of steroid metabolites (estradiol, progesterone, glucocorticoids, and testosterone) from the feces of wild female baboons (Papio spp.). This method is a modification of that developed by Stavisky [Socioendocrinology: noninvasive techniques for monitoring reproductive function in captive and free-ranging primates. PhD, Emory University, 1994.], which employs reversed-phase octadecylsilane cartridges to extract steroids from feces. In addition to providing physiological validation for this method, we examine variation in steroid concentration across different (1) collection times (morning vs. afternoon), (2) methanol extraction treatments (homogenized vs. hand-mixed), and (3) solid-phase extraction times (2 vs. 10 h after collection). We then examine the stability of sample storage at ambient and subzero temperatures to determine whether storage time significantly alters steroid concentrations. Our results show that hormone concentrations do not differ between morning and afternoon samples, homogenization yields significantly higher fecal steroid concentrations, and fecal steroids are stable in a methanol/acetone solution for up to 10 h. When stored at ambient temperatures, only glucocorticoid metabolites had some degradation over a period of up to 40 days. However, when stored at -10 degrees C, no significant steroid changes were observed for up to 400 days. This method is particularly suited for behavioral research because it permits delays between sample collection and sample processing, thus allowing behavioral observations to continue.

The Endocrinology Of Pregnancy And Fetal Loss In Wild Baboons.

An impressive body of research has focused on the mechanisms by which the steroid estrogens (E), progestins (P), and glucocorticoids (GC) ensure successful pregnancy. With the advance of non-invasive techniques to measure steroids in urine and feces, steroid hormones are routinely monitored to detect pregnancy in wild mammalian species, but hormone data on fetal loss have been sparse. Here, we examine fecal steroid hormones from five groups of wild yellow baboons (Papio cynocephalus) in the Amboseli basin of Kenya to compare the hormones of successful pregnancies to those ending in fetal loss or stillbirth. Using a combination of longitudinal and cross-sectional data, we analyzed three steroid hormones (E, P, GC) and related metabolites from 5 years of fecal samples across 188 pregnancies. Our results document the course of steroid hormone concentrations across successful baboon pregnancy in the wild and demonstrate that fecal estrogens predicted impending fetal loss starting 2 months before the externally observed loss. By also considering an additional 450 pregnancies for which we did not have hormonal data, we determined that the probability for fetal loss for Amboseli baboons was 13.9%, and that fetal mortality occurred throughout gestation (91 losses occurred in 656 pregnancies; rates were the same for pregnancies with and without hormonal data). These results demonstrate that our longstanding method for early detection of pregnancies based on observation of external indicators closely matches hormonal identification of pregnancy in wild baboons.