Elevated glucocorticoids during the ovarian follicular phase predict conception in wild female chacma baboons.

Mating related behavior during ovarian cycling can be energetically demanding and constitute a significant stressor, requiring physiological responses to mediate investment in reproduction. To better understand the proximate mechanisms underlying these responses, we examine hormonal and behavioral variation across the ovarian cycle during conceptive and nonconceptive cycles in wild female chacma baboons (Papio ursinus). We quantified immunoreactive fecal estradiol, progesterone, and cortisol metabolites for 21 adult females, and calculated activity budgets and rates of received aggression from over 5000 15-min behavioral samples. We found conception to be associated with higher concentrations of both estradiol and cortisol during the follicular phase, but no difference in progesterone between conceptive and nonconceptive cycles for either the follicular or luteal phase. While females spent less time feeding during the follicular compared to the luteal phase, we found no difference in time spent feeding, moving, or copulating between conceptive and nonconceptive cycles of the same phase. Rates of received aggression also were similar across the ovarian cycle, with no difference between conceptive and nonconceptive cycles. Finally, we found positive associations between cortisol and estradiol, indicating that glucocorticoids (GCs) do not suppress hypothalamic-pituitary-gonadal (HPG) activity and reproductive function in this context. Overall, our results suggest that elevated GCs may play an adaptive role in mobilizing energy during sexually receptive periods of ovarian cycling.

Respect for males amid suppression of females: Selective use of aggression and fitness correlates in the male-dominated society of hamadryas baboons.

Hamadryas baboons (Papio hamadryas) are a useful model for human social evolution for multiple reasons, including their multilevel society, intense cross-sex bonds, and intermale tolerance. Their most stable social grouping, the one-male unit (OMU)-comprising a leader male, females, and sometimes follower males-is formed via successive takeovers of individual females by males. While takeovers occur via both aggressive and non-aggressive mechanisms, aggressive herding is common during and after takeovers and appears crucial in maintaining OMUs. Here we use behavioral and demographic data from Filoha, Ethiopia to examine the relationship between aggressive takeovers and fitness correlates. We found no relationship between a male's percentage of takeovers that were aggressive and his presumed number of infants sired, nor his number of females or followers. However, we did find that a leader male's average intensity of aggression toward both other males and females around the time of a takeover was negatively related to his presumed number of infants sired. In addition, a leader male's average intensity of aggression toward other males was negatively related to his maximum number of followers. Finally, leader males exhibited more intense aggression toward females in interband, compared to intraband, takeovers. Our findings suggest that (1) leader males who limit their aggression toward other males may have greater success in attracting followers, thereby increasing their fitness via enhanced defense of the OMU; (2) exceptionally aggressive takeovers may lead to lower birth rates via female reproductive suppression; and (3) the extent to which males use aggression toward females depends on the context in which the takeover occurs. Overall, these results both suggest that hamadryas males use aggression selectively and underscore the ubiquity of intermale tolerance and female suppression in the hamadryas social system. This study lends insight into the interplay between male-female and male-male social dynamics during human evolution.

Costs of seasonality at a southern latitude: Behavioral endocrinology of female baboons in the Cape Peninsula of South Africa.

Environmental challenges in the form of temperature extremes and unusual precipitation, which may lead to prolonged periods outside the thermoneutral zone, can be detrimental to animal physiology. Chacma baboons in the Cape Peninsula of South Africa, one of the highest latitudes at which nonhuman primates are found, experience extremes of both temperature and rainfall, as well as seasonal differences in day length that require animals to condense their daily routine into dramatically reduced daylight hours. Here we examine the effects of these climatic factors on the behavior (activity budgets and foraging patterns) and physiology (fecal glucocorticoid concentrations) of adult females (N = 33) in three groups of chacma baboons (Papio ursinus) inhabiting the Cape Peninsula, where temperatures ranged from 7 to 39 °C, monthly rainfall ranged from 2 to 158 mm, and day length varied by 4.5 h across seasons. Climatic variables showed a clear relationship to female baboon glucocorticoid concentrations, which significantly increased with lower temperatures, higher rainfall and shorter day lengths. Activity budgets also differed between summer and winter, with females generally spending less time socializing, moving and resting in the winter compared to summer, with some differences between troops in their feeding-related activities. Cold temperatures accompanied by rainfall and short day lengths may thus represent an ecological constraint for this population. This study highlights the potential impact of anthropogenic climate change on the physiology, behavior, and, ultimately, survival of wildlife populations.

The adaptive value of secondary males in the polygynous multi-level society of hamadryas baboons.

OBJECTIVES: One-male social systems are usually characterized by polygyny and reproductive exclusion by a single resident male. Sometimes, however, secondary males join these groups, and this may carry fitness costs and/or benefits to the resident male. In hamadryas baboons (Papio hamadryas hamadryas), which live in one-male units (OMUs) with female defense polygyny within a multi-level social system, secondary "follower" males often reside in OMUs. Our aim here is to examine possible benefits of these secondary males to hamadryas resident males. MATERIALS AND METHODS: Using 6 years of data from 65 OMUs in a band of wild hamadryas baboons in Ethiopia, we compared demographic and reproductive parameters of OMUs with and without secondary "follower" males to assess whether their presence conferred any reproductive benefits to resident "leader" males. RESULTS: Leaders with followers had tenure lengths almost twice as long, acquired more than twice as many females, retained females longer, and had three times as many infants during their tenure compared to leaders without followers. DISCUSSION: Hamadryas follower males enabled leaders to retain females for longer periods of time-likely through unit defense, social relationships with OMU members, and/or infant protection. Hamadryas leaders appear to be able to monopolize access to females despite the presence of followers, and as such any enhanced reproduction derived from the presence of followers likely increases the fitness of the leader rather than the follower. Thus the relationship between leaders and followers in hamadryas society appears to be a mutually beneficial one and tolerance of secondary males may be an adaptive reproductive strategy characterizing hamadryas leader males.

The rise and fall of leader males in a multi-level society: takeovers and tenures of male Hamadryas baboons.

As one means to maximize access to females, males of some species are intolerant of other males in social units, resulting in female defense polygyny, a mating system in which one male monopolizes mating access to as many females as he can for as long as possible. In such a system, the length of a male's tenure and the number of females he is able to acquire are important predictors of his reproductive success. Hamadryas baboons differ from many other taxa with female defense polygyny in that they acquire and lose females individually, thus patterns of acquisition and loss of females over time are additional factors contributing to a male's fitness. Here, we describe longitudinal patterns of female acquisition and loss over a 9-year period in a group of 250 wild hamadryas baboons. Complete tenures of leader males ranged from 310 to 2,160 days (N = 13) and results from a survival analysis yielded a median tenure length of 2,160 days, or 6 years (N = 49). The total number of females acquired, which increased with tenure length, ranged from 1 to 14 and averaged 3.5, and leader males acquired females both opportunistically and via challenging other males. The interval between acquisition of successive females ranged from 0 to 1,196 days with a median of 203, and males acquired all of their females less than halfway into their tenure. Females from outside of a leader male's social sphere (clan and band) were acquired relatively later in their tenure compared to females from within a male's social sphere. Leaders typically lost females gradually during the latter part of their tenure or all (or most) at once, suggesting an inverted U-shaped longitudinal arc of male competitive ability.

Predictors of helminth parasite infection in female chacma baboons (Papio ursinus).

Helminth parasite infection can impose major consequences on host fitness. Several factors, including individual characteristics of hosts, environmental conditions, and patterns of coinfection, are thought to drive variation in parasite risk. Here, we report on four key drivers of parasite infection-phase of reproduction, steroid hormone profiles, rainfall, and patterns of coinfection-in a population of wild female chacma baboons (Papio ursinus) in South Africa. We collected data on reproductive state and hormone profiles over a 3-year span, and quantified helminth parasite burdens in 2955 fecal samples from 24 female baboons. On a host level, we found that baboons are sensitive to parasite infection during the costliest phases of the reproductive cycle: pregnant females harbored higher intensities of Protospirura eggs than cycling and lactating females; lactating and cycling females had a higher probability of Oesophagostomum infection than pregnant females; and cycling females exhibited lower Trichuris egg counts than pregnant and lactating females. Steroid hormones were associated with both immunoenhancing and immunosuppressive properties: females with high glucocorticoid concentrations exhibited high intensities of Trichuris eggs but were at low risk of Oesophagostomum infection; females with high estrogen and progestagen concentrations exhibited high helminth parasite richness; and females with high progestagen concentrations were at high risk of Oesophagostomum infection but exhibited low Protospirura egg counts. We observed an interaction between host reproductive state and progestagen concentrations in infection intensity of Protospirura: pregnant females exhibited higher intensities and non-pregnant females exhibited lower intensities of Protospirura eggs with increasing progestagen concentrations. At a population level, rainfall patterns were dominant drivers of parasite risk. Lastly, helminth parasites exhibited positive covariance, suggesting that infection probability increases if a host already harbors one or more parasite taxa. Together, our results provide a holistic perspective of factors that shape variation in parasite risk in a wild population of animals.

Anthropogenic effects on the physiology and behaviour of chacma baboons in the Cape Peninsula of South Africa.

As animals increasingly occupy habitats in proximity to humans, with home ranges a mosaic of natural and anthropogenic landscapes, it becomes imperative from a conservation perspective to understand the impacts of human activities on wildlife. Many non-human primates share habitats with humans, an ability stemming largely from shared ecological needs due to our close evolutionary relationship. Such proximity, however, is often accompanied by direct conflict between humans and wildlife, leading to higher stress levels, injuries, mortality and behavioural changes, with detrimental effects on long-term health and fitness. Glucocorticoid (GC) hormones, which are released in response to ecological and social challenges, are increasingly employed to understand responses to anthropogenic disturbance. Here we investigate physiological and behavioural responses of female chacma baboons (Papio ursinus) to variation in spatial overlap and conflict with humans in their natural home range. The baboons resided in the Tokai Section of Table Mountain National Park in the Cape Peninsula of South Africa, where their home range included four types of habitats: protected, suburban, agricultural and mosaic areas. We studied the largest group of baboons in Tokai (70 individuals) and examined the effects of ranging in these different habitats on the faecal GCs and behaviour of all adult females in the troop (N = 16). We found time spent ranging in more anthropogenic habitats to be associated with higher levels of GCs, more aggression, less time socializing and shorter grooming bouts. Self-directed behaviour, however, varied and did not necessarily reflect physiological measures of stress. Taken together, the results of this study highlight the risks associated with ranging in anthropogenic environments and point to the need for a multifaceted approach to studying the negative impacts of human activities on animals so as to better inform conservation practices.