Thore J. Bergman

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 central importance of information in studies of animal communication

The concept of information plays a central role in studies of animal communication. Animals’ responses to the calls of different individuals, to food calls, alarm calls, and to signals that predict behaviour, all suggest that recipients acquire information from signals and that this information affects their response. Some scientists, however, want to replace the concept of information with one based on the ‘manipulation’ of recipients by signallers through the induction of nervous-system responses. Here we review both theory and data that argue against hypotheses based exclusively on manipulation or on a fixed, obligatory link between a signal’s physical features and the responses it elicits. Results from dozens of studies indicate that calls with ‘arousing’ or ‘aversive’ features may also contain information that affects receivers’ responses; that acoustically similar calls can elicit different responses; acoustically different calls can elicit similar responses; and ‘eavesdropping’ animals respond to the relationship instantiated by signal sequences. Animal signals encode a surprisingly rich amount of information. The content of this information can be studied scientifically.

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.

Chest color and social status in male geladas (Theropithecus gelada)

Conspicuous colored patches on animals often serve as sexually selected signals that advertise male quality. Such colored traits facilitate assessment of risks associated with a specific contest or benefits associated with a specific mate choice. Here, we investigate whether a colored patch of skin on the chests of male geladas (Theropithecus gelada) is a sexually selected signal. Specifically, we examine the relationship between color (redness), social status (a proxy for reproductive success), and age. We use observational data from known individuals from a population of wild geladas living in Ethiopia. We digitally quantified chest color using a previously-validated method for measuring color under field conditions. Results from this study are consistent with the hypothesis that redness is a quality signal in males. Baseline color correlates with status even when controlling for age. Indeed, males with redder chests were members of “better” groups: 1) leader males—the only males with reproductive access to females—had the reddest chests, and 2) within leader males, males with large units (>6 females) had redder chests than males with small units. At present, we are unable to address whether male chest color is directed at potential rivals or mates. Nevertheless, our data support the hypothesis that quality signals should prevail in large, fluid groups, where it is unlikely that individuals recognize all other group members. If individual recognition is limited in gelada society, this would favor the evolution of alternative means of assessment for making reproductive decisions.

A Bruce Effect in Wild Geladas

Avoiding Infanticide In male dominated hierarchies, newly dominant males will sometimes kill resident infants. In lab studies in mice conducted in the 1950s, Hilda Bruce showed that females introduced to an unfamiliar male will terminate their pregnancies, a process subsequently referred to as a Bruce Effect. Roberts et al. (p. 1222, published online 23 February) followed multiple dominance transitions within wild gelada baboons and showed that live birthrate among females previously identified as pregnant within unstable groups was much lower than within stable groups. Furthermore, females that terminated their pregnancies following transitions had a much shorter interbirth interval than those that did not, suggesting a higher overall reproductive success and fitness. Long-term field studies show female monkeys improve their fitness by terminating their pregnancies when a new male becomes dominant. Female rodents are known to terminate pregnancies after exposure to unfamiliar males (“Bruce effect”). Although laboratory support abounds, direct evidence for a Bruce effect under natural conditions is lacking. Here, we report a strong Bruce effect in a wild primate, the gelada (Theropithecus gelada). Female geladas terminate 80% of pregnancies in the weeks after a dominant male is replaced. Further, data on interbirth intervals suggest that pregnancy termination offers fitness benefits for females whose offspring would otherwise be susceptible to infanticide. Taken together, data support the hypothesis that the Bruce effect can be an adaptive strategy for females.