Female Chacma Research Articles

More allogrooming is followed by higher physiological stress in wild female baboons.

Social bonds increase fitness in a range of mammals. One pathway by which social bonds may increase fitness is by reducing the exposure to physiological stress, i.e. glucocorticoid (GC) hormones, that can be detrimental to health and survival. This is achieved through downregulating hypothalamic-pituitary-adrenal (HPA)-axis activity. Indeed, long-term measures of social (grooming) bonds are often negatively correlated with HPA-axis activity. However, the proximate role of physical touch through allogrooming remains an open question in the sociality-health-fitness debate. Demonstrating the potential anxiolytic benefits of grooming in the wild is hindered by methodological limitations. Here, we match accelerometer-identified grooming in wild female chacma baboons (Papio ursinus) to non-invasive faecal GC metabolite concentrations (fGCs). Consistent with previous work, we found a negative (but statistically non-significant) overall relationship between individual averaged fGCs and grooming rates. However, when time-matching grooming to fGCs, we found that both more giving and receiving grooming were followed by higher fGCs. This upregulation of HPA-axis activity suggests that maintaining social bonds (and its ultimate fitness benefits) may come at a shorter-term physiological cost. This finding sheds new light on a ubiquitous social behaviour typically considered 'relaxing' and suggests that sociopositive contact can trigger physiological stress.

Cycle length flexibility: is the duration of sexual receptivity associated with changes in social pressures?

Research in social mammals has revealed the complexity of strategies females use in response to female-female reproductive competition and sexual conflict. One point at which competition and conflict manifests acutely is during sexual receptivity, indicated by swellings in some primates. Whether females can adjust their sexual receptivity from cycle to cycle to decrease reproductive competition and sexual conflict in response to social pressures has not been tested. As a first step, this study explores whether sexual receptivity duration is predicted by social pressures in wild female chacma baboons (Papio ursinus). Given that female baboons face intense reproductive competition and sexual coercion, we predicted that: females could shorten the duration of their sexual receptive period to reduce female-female aggression and male coercion or increase it to access multiple or their preferred male(s). We quantified 157 ovulatory cycles from 46 wild females living in central Namibia recorded over 15 years. We found no support for our hypothesis; however, our analyses revealed a negative correlation between maximal-swelling duration and group size, a proxy of within-group competition. This study provides further evidence that swelling is costly as well as a testable framework for future investigations of 'cycle length manipulation'.

Postpartum cessation of urban space use by a female baboon living at the edge of the City of Cape Town.

Species with slow life history strategies that invest in few offspring with extended parental care need to adapt their behavior to cope with anthropogenic changes that occur within their lifetime. Here we show that a female chacma baboon (Papio ursinus) that commonly ranges within urban space in the City of Cape Town, South Africa, stops using urban space after giving birth. This change of space use occurs without any significant change in daily distance traveled or social interactions that would be expected with general risk-sensitive behavior after birth. Instead, we suggest this change occurs because of the specific and greater risks the baboons experience within the urban space compared to natural space, and because leaving the troop (to enter urban space) may increase infanticide risk. This case study can inform methods used to manage the baboons' urban space use in Cape Town and provides insight into how life history events alter individuals' use of anthropogenic environments.

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.

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.

Strategic Use of Affiliative Vocalizations by Wild Female Baboons.

Although vocal production in non-human primates is highly constrained, individuals appear to have some control over whether to call or remain silent. We investigated how contextual factors affect the production of grunts given by wild female chacma baboons, Papio ursinus, during social interactions. Females grunted as they approached other adult females 28% of the time. Supporting previous research, females were much more likely to grunt to mothers with young infants than to females without infants. Grunts also significantly increased the likelihood of affiliative interactions among all partners. Notably, however, grunts did not simply mirror existing social bonds. Instead, they appeared to perform a very different function: namely, to serve as signals of benign intent between partners whose relationship is not necessarily close or predictable. Females were less likely to grunt to their mothers or adult daughters—the individuals with whom they shared the closest and least aggressive bonds—than to other females. In contrast, patterns of grunting between sisters were similar to those between nonkin, perhaps reflecting sisters’ more ambivalent relationships. Females grunted at higher rates to lower-ranking, than to higher-ranking, females, supporting the hypothesis that grunts do not simply signal the signaler’s level of arousal or anxiety about receiving aggression, but instead function as signals of benign intent. Taken together, results suggest that the grunts given by female baboons serve to reduce uncertainty about the likely outcome of an interaction between partners whose relationship is not predictably affiliative. Despite their limited vocal repertoire, baboons appear to be skilled at modifying call production in different social contexts and for different audiences.

The 2D:4D digit ratio and social behaviour in wild female chacma baboons (Papio ursinus) in relation to dominance, aggression, interest in infants, affiliation and heritability

Prenatal androgens are responsible for sex differences in behaviour and morphology in many species, causing changes in neural structure and function that persist throughout life. Some variation in the expression of behaviour between individuals of the same sex can also be attributed to differences in exposure to prenatal sex hormones. The ratio of the second and fourth digits (2D:4D ratio) is a proposed biomarker for prenatal androgen effects (PAE). Through assessment of 2D:4D ratios, this study aimed to investigate the relationship between inferred PAE and social behaviours in female chacma baboons (Papio ursinus). We validated a new method to measure 2D:4D indirectly using digital photographs and computer-assisted image analysis software. There was a strong correlation between 2D:4D ratio and dominance rank amongst female baboons. Low 2D:4D ratios were associated with high rank, lower submission rates and higher rates of non-contact and contact aggression. This is consistent with the hypothesis that prenatal androgens are linked to the expression of these behaviours in female baboons, although it was not possible to separate the effects of PAE and dominance rank on some rank-related behaviours. The 2D:4D ratio did not correlate with interest in infants or with the rate of affiliative behaviours, possibly because these behaviours are more affected by ovarian hormones in adult life than by PAE. Finally, mean 2D:4D ratios were positively correlated in six mother/infant pairs, consistent with a heritable basis for the 2D:4D ratio in primates. We suggest that PAE contribute significantly to the patterning of social relationships in female primates.

30 Days in the Life: Daily Nutrient Balancing in a Wild Chacma Baboon

For most animals, the ability to regulate intake of specific nutrients is vital to fitness. Recent studies have demonstrated nutrient regulation in nonhuman primates over periods of one observation day, though studies of humans indicate that such regulation extends to longer time frames. Little is known about longer-term regulation in nonhuman primates, however, due to the challenges of multiple-day focal follows. Here we present the first detailed study of nutrient intake across multiple days in a wild nonhuman primate. We conducted 30 consecutive all day follows on one female chacma baboon (Papio hamadryas ursinus) in the Cape Peninsula of South Africa. We documented dietary composition, compared the nutritional contribution of natural and human-derived foods to the diet, and quantified nutrient intake using the geometric framework of nutrition. Our focus on a single subject over consecutive days allowed us to examine daily dietary regulation within an individual over time. While the amounts varied daily, our subject maintained a strikingly consistent balance of protein to non-protein (fat and carbohydrate) energy across the month. Human-derived foods, while contributing a minority of the diet, were higher in fat and lower in fiber than naturally-derived foods. Our results demonstrate nutrient regulation on a daily basis in our subject, and demonstrate that she was able to maintain a diet with a constant proportional protein content despite wide variation in the composition of component foods. From a methodological perspective, the results of this study suggest that nutrient intake is best estimated over at least an entire day, with longer-term regulatory patterns (e.g., during development and reproduction) possibly requiring even longer sampling. From a management and conservation perspective, it is notable that nearly half the subject’s daily energy intake derived from exotic foods, including those currently being eradicated from the study area for replacement by indigenous vegetation.

Estrous synchrony in a nonseasonal breeder: adaptive strategy or population process?

The idea that female mammals can manipulate the duration of each other’s estrus in an effort to influence the degree of synchrony between their periods of sexual receptivity is a persistent and popularly held one. It is frequently cited as proof of pheromonal communication in humans and often invoked by models of female reproductive strategies more generally. Yet, to date, no tests of the evolutionary arguments put forward by proponents of the phenomenon have been undertaken. We addressed this deficit with an analysis of the reproductive demography of wild female chacma baboons, where variance in the temporal distribution of female receptivity is known to occur. Specifically, we tested the predictions that this variance will reflect female attempts to minimize 1) the risks of being monopolized by a single male or 2) the intensity of interfemale competition for males. Using model comparison, we found no evidence that male number or operational sex ratio had any influence on the distribution of female receptivity, the number of females in estrus, or the duration of female sexual swellings. Indeed, when modeling estrous overlap and cycling female number, we found that a simple nondeterministic model provided the best fit. We conclude, therefore, that variance in the temporal distribution of female receptivity is indicative of nothing more than a population process and that socially mediated synchrony is not a tangible adaptive phenomenon. Key words: female receptivity, population process, sexual selection, socially mediated synchrony. [Behav Ecol]

Strong and Consistent Social Bonds Enhance the Longevity of Female Baboons

Longevity is a major component of variation in fitness in long-lived iteroparous species [1-4]. Among female baboons, variation in breeding lifespan accounts for approximately 50% of the variation in lifetime fitness [5, 6]. However, we know little about the causes of variation in longevity in primates or other long-lived mammals. Savannah baboons form strong, equitable, and enduring relationships with specific female partners, particularly with close relatives and agemates [7-10]. The quality of females' social relationships influences their ability to cope with stressful events [11-13] and is associated with variation in female reproductive success [9, 14]. Here we show that dominance rank and the quality of close social bonds have independent effects on the longevity of female chacma baboons (Papio hamadryas ursinus). High-ranking females live longer than lower-ranking females. In addition, females who form stronger and more stable social bonds with other females live significantly longer than females who form weaker and less stable relationships. These data extend our understanding of the adaptive value of social bonds in baboons and complement a growing body of evidence that indicates that social bonds have adaptive value in a range of taxa, from mice to humans [9, 14-19].

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.

Hedging their bets? Male and female chacma baboons form friendships based on likelihood of paternity

In chacma baboons (Papio hamadryas ursinus), adult males and lactating females form preferential associations, or ‘friendships’, that provide protection against potentially infanticidal attacks. Little is known about the mechanisms by which males and females form friendships, or the function of friendships for males. We examined the relationship between mating activity, paternity and friendships over a 3-year period. A male’s proportion of consort activity with a female within and outside of her period of most likely conception, along with his dominance rank, each contributed importantly in models of paternity outcomes and formation of friendships. In 87% of births, the male that monopolized the greatest proportion of a female’s consort days during her last conceptive cycle was the father of her offspring. In 82% of the births where the female’s primary consort partner was present at parturition, he became her friend. When the primary consort partner was absent at parturition, females formed friendships with males that had monopolized the second or third greatest proportion of their previous consort days. Similarly, 78% of males became friends with females with whom they had obtained their greatest consort success. Such a flexible strategy based on probabilistic assessment of paternity may be adaptive for females, given unpredictable fluctuations in male presence within the group. In a mating system with high dominance-based reproductive skew, males may benefit by investing preferentially in those infants that they are most likely to have fathered.

Sexual conflict in chacma baboons, Papio hamadryas ursinus: absent males select for proactive females

We argue that, in the absence of an infanticidal threat from resident males, female chacma baboons favour polyandry because it may predispose multiple males to protect their infants from infanticide by immigrant males. This assumes that the most likely sire, or principal protector, of an infant may often be absent during its period of vulnerability, thereby creating the need for additional protection. Accordingly, we found that, on average, 47% of principal protectors were absent for at least part of an infant's vulnerable period. We predicted that, to secure additional protection, females should attempt to augment the paternity estimates of as many males as possible and, therefore, should seek to influence overall patterns of mating. In line with this prediction, we found that females actively solicited copulations from all guarding males and did so irrespective of their rank or the underlying probability of ovulation. By these means, females were able to elevate significantly the mating success, and presumably, in turn, the estimated total paternity probabilities, of these males. The apparently indiscriminate nature of the female strategy highlights how, in species where female choice is limited, females may be forced to maximize the potential of all mating opportunities afforded them by intermale competition.

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.

Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus)

In humans, bereavement is associated with an increase in glucocorticoid (GC) levels, though this increase can be mitigated by social support. We examined faecal GC levels and grooming behaviour of free-ranging female baboons to determine whether similar effects were also evident in a non-human species. Females who lost a close relative experienced a significant increase in GC levels in the weeks following their relative's death compared with the weeks before, whereas control females showed no such increase. Despite the fact that females concentrate much of their grooming on close kin, females who lost a close female relative did not experience a decrease in grooming rate and number of grooming partners; instead, both grooming rate and number of grooming partners increased after a relative's death. While the death of a close relative was clearly stressful over the short term, females appeared to compensate for this loss by broadening and strengthening their grooming networks. Perhaps as a result, females' GC levels soon returned to baseline. Even in the presence of familiar troop-mates and other relatives, females experienced a stress response when they lost specific companions, and they apparently sought to alleviate it by broadening and strengthening their social relationships.

Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors

Savannah baboons are one of the few mammalian species that do not exhibit seasonal reproduction patterns and are therefore ideally suited to study the effect of female reproductive states (cycling, pregnant, lactating) on cortisol levels independent of seasonal factors. Fecal samples from 10 free-ranging female chacma baboons ( Papio hamadryas ursinus), collected during a period of 17 months, were analyzed using a steroid-extraction method. Reproductive state had a significant effect on fecal cortisol, with lowest levels found in estrous females. Fertility was not related to fecal cortisol levels; we found no significant differences between samples collected on conceptive and nonconceptive cycles. Environmental factors explained most of the variance of fecal cortisol levels. Cortisol measures were strongly correlated with seasonal differences such as daylight duration, temperature and the amount of time that baboons spent resting. We measured higher cortisol levels during winter months and suggest that this could be related to shorter resting periods and to the cold minimum ambient temperatures at this study site. Finally, we found no relationship between social rank nor the rate of agonistic interactions with basal fecal cortisol levels.

A dynamic interaction between aggression and grooming reciprocity among female chacma baboons

We used data from a natural experiment on adult female chacma baboons, Papio cynocephalus ursinus, to test the hypothesis that variation in aggression through time influences patterns of grooming reciprocity within a social group. Owing to a change in the baboons' competitive regime, we were able to compare data from periods when aggression was high (period 1) and low (period 2). During period 2, the slope of the relationship between aggression and rank was significantly shallower than during period 1 and less aggression was directed at the lowest-ranking females suggesting there had been a reduction in the dominance gradient. We attributed this to reduced effectiveness of dominance as a means of excluding other females from feeding resources. The reduction in aggression during period 2 was accompanied by an increase in grooming reciprocity between dyads suggesting that high-ranking females no longer attracted grooming by subordinates in exchange for tolerance, and that grooming in period 2 was exchanged for its intrinsic benefits. The loss of rank-related effects on grooming reciprocity in period 2 compared with period 1 further confirmed this. These findings show that female baboons are able to respond flexibly and swiftly to changes in their social circumstances and that a dynamic approach to primate social interactions is worth pursuing. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Infants as a commodity in a baboon market

We used data from adult female chacma baboons, Papio cynocephalus ursinus, to provide the first test of hypotheses on interchange trading and the structure of a biological market (Noë & Hammerstein 1994, Behavioral Ecology and Sociobiology,35, 1–11) within a primate group. The interchange commodities selected were grooming and handling of infants less than 3 months of age. Patterns of grooming in relation to infant handling showed strong evidence for interchange. Grooming for infant access was initiated by potential handlers and was significantly likely to be nonreciprocated. More critically, the data show that infant ‘supply’ created a market effect: grooming bout duration (the price ‘paid’ for handling) was inversely related to the number of infants present in the group. In addition, there was an inverse relationship between grooming bout duration and the rank distance between mothers and handlers, suggesting that higher-ranking mothers could demand a higher price for infant handling. Where rank distance was high, females were able to handle infants without grooming. Dominance could thus be used to disrupt the infant market effect. If biological markets models are to be fully applicable to primate groups (and those of other social mammals) then the potentially distorting effect of dominance needs to be incorporated into the framework. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas.

Little is known about to what extent the sensitivity of the hypothalamic-pituitary-adrenal (HPA) axis may be state dependent and vary in the same species between environments. Here we tested whether the faecal corticosteroid concentrations of matrilineal adult female spotted hyenas are influenced by social and reproductive status in adjacent ecosystems and whether they vary between periods with and without social stress. Females in the Serengeti National Park frequently become socially subordinate intruders in other hyena territories by undertaking long-distance foraging trips to migratory herds, whereas in the Ngorongoro Crater they usually forage inside their own small territories on resident prey. The faecal corticosteroid concentrations in Serengeti females were significantly higher than in Ngorongoro females. Energy expenditure by lactation is exceptionally high in spotted hyenas and this may be reflected in their corticosteroid levels. The faecal corticosteroid levels in both populations were higher in lactating than in non-lactating females. During periods of social stability, faecal corticosteroid concentrations increased in non-lactating females but not in lactating females as social status declined. Lactating Serengeti females had significantly higher faecal corticosteroid concentrations during periods with acute severe social stress than during periods without, indicating that the HPA axis is sensitive to social stimuli even in lactating females. So far few studies have used non-invasive monitoring methods for assessing social stress in freeranging animals. This study demonstrates for the first time, to the authors' knowledge, that corticosteroid concentrations may differ between periods with and without social stress for a free-ranging female mammal and that the modulating effect of social status may depend on reproductive status.