Confessions of a baboon watcher: from inside to outside the paradigm.

In this "tale" I summarize the major landmarks of my 50-year career watching wild olive baboons (Papio anubis). I review some major discoveries, like baboon hunting and baboon social strategies of competition and defense, that only a creature with a "mind" could manage. My efforts expanded beyond science to include community-based conservation because quite early on these baboons experienced many of the threats of the Anthropocene. My research expanded to include studying crop-raiding by naïve groups of baboons, the first scientific translocation of a primate species, and a detour to study the invasion of a non-indigenous cactus, Opuntia stricta. Throughout I worked with local communities to find solutions to problems that the baboons created, and also to develop new options for their livelihoods. As the baboon research became a long-term project, it depended on a team of Kenyan research assistants who made possible the simultaneous monitoring of up to six baboon troops as well as extensive ecological monitoring. Knowing the ecology, including the impact of the sedentarization of pastoralists in the area, meant we could interpret the process of invasion by a non-indigenous cactus for the first time. Ecological periods allowed comparisons of the same troop over time and different baboon groups during the same ecological phase. Although I began my work before hypothesis testing was the preferred approach, once the paradigm changed, I continued to study and learn what matters to baboons from their perspective. As a result of observing them for 50 years, the baboons showed me that evolution often does not work the way that I had been taught, and it took all my detours and studies to convince me that anecdotes, when they are systematic and comparative, are not stories to be discounted, but evidence, much like Darwin's natural history. Natural history can reassemble the pieces that quantitative hypothesis testing has teased apart to provide its larger meaning. Today, the lone scientist, like me, is an anachronism because no one person has expertise in the many fields needed to understand and save the primates we care about.

Early life adversity has long-term effects on sociality and interaction style in female baboons.

Social bonds enhance fitness in many group-living animals, generating interest in the processes that create individual variation in sociality. Previous work on female baboons shows that early life adversity and temperament both influence social connectedness in adulthood. Early life adversity might shape sociality by reducing ability to invest in social relationships or through effects on attractiveness as a social partner. We examine how females' early life adversity predicts sociality and temperament in wild olive baboons, and evaluate whether temperament mediates the relationship between early life adversity and sociality. We use behavioural data on 31 females to quantify sociality. We measure interaction style as the tendency to produce grunts (signals of benign intent) in contexts in which the vocalization does not produce immediate benefits to the actor. Early life adversity was negatively correlated with overall sociality, but was a stronger predictor of social behaviours received than behaviours initiated. Females who experienced less early life adversity had more benign interaction styles and benign interaction styles were associated with receiving more social behaviours. Interaction style may partially mediate the association between early life adversity and sociality. These analyses add to our growing understanding of the processes connecting early life experiences to adult sociality.

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.

Bringing up baby: Maternal responsiveness, secondary attachments, and the development of infant social competence in wild olive baboons (Papio anubis).

Caregiver responsiveness and presence of secondary attachments play a crucial role in children's socio-cognitive and emotional development, but little is known of their effect on the development of non-human primates. Here we present the results of a 16-month behavioral study conducted on 22 wild infant olive baboons (Papio anubis) at the Uaso Ngiro Baboon Project, Kenya. This is the first study to examine the effects of maternal responsiveness and secondary attachments on the development of infant social behavior in a wild primate species that does not breed cooperatively. The data track maternal responsiveness and the rates of two behavioral indicators of infant social competence-orienting toward interactions and social play-over the course of the first year of life. Maternal responsiveness decreased as infants grew older, while infant orientation toward interactions and play behavior increased. Infants with poorly responsive mothers were more likely to have secondary attachments, and infants with secondary attachments to siblings oriented more frequently to social interactions than those with secondary attachments to adult/subadult males or with no secondary attachments. These findings indicate that variation in maternal responsiveness and presence of secondary attachments can influence the development of social competence in olive baboon infants.

Shifts in Male Reproductive Tactics over the Life Course in a Polygynandrous Mammal.

In polygynous and polygynandrous species, there is often intense male-male competition over access to females, high male reproductive skew, and more male investment in mating effort than parenting effort [1]. However, the benefits derived from mating effort and parenting effort may change over the course of males' lives. In many mammalian species, there is a ∩-shaped relationship between age, condition, and resource holding power as middle-aged males that are in prime physical condition outcompete older males [2-8] and sire more infants [9-12]. Thus, males might derive more benefits from parenting effort than mating effort as they age and their competitive abilities decline [13]. Alternatively, older males may invest more effort in making themselves attractive to females as mates [14]. One way that older males might do so is by developing relationships with females and providing care for their offspring [14, 15]. Savannah baboons provide an excellent opportunity to test these hypotheses. They form stable multi-male, multi-female groups, and males compete for high ranking positions. In yellow and chacma baboons (Papio cynocephalus and P. ursinus), there is a ∩-shaped relationship between male age and dominance rank [12], and high rank enhances paternity success [12, 16]. Lactating female baboons form close ties ("primary associations" hereafter) with particular males [15-20], who support them and their infants in conflicts [15, 19] and buffer their infants from rough handling [20]. Females' primary associates are often, but not always, the sires of their current infants [16, 20-22].

Male-female relationships in olive baboons (Papio anubis): Parenting or mating effort?

Long-term male-female bonds and bi-parental investment in offspring are hallmarks of human society. A key question is how these traits evolved from the polygynandrously mating multimale multifemale society that likely characterized the Pan-Homo ancestor. In all three species of savanna baboons, lactating females form strong ties (sometimes called "friendships") with one or more adult males. For yellow baboons (Papio cynocephalus) and chacma baboons (Papio ursinus), several lines of evidence suggest that these relationships are a form of male parenting effort. In olive baboons (Papio anubis), females are thought to preferentially mate with their "friends", and male-female bonds may thus function as a form of mating effort. Here, we draw on behavioral and genetic data to evaluate the factors that shape male-female relationships in a well-studied population of olive baboons. We find support for the parenting effort hypothesis in that sires have stronger bonds with their infants' mothers than do other males. These bonds sometimes persist past weaning age and, in many cases, the sire of the previous infant is still a close partner of the female when she nurses her subsequent offspring. We find that males who have the strongest bonds with females that have resumed cycling, but are not currently sexually receptive, are more likely to sire the female's next offspring but the estimate is associated with large statistical uncertainty. We also find that in over one third of the cases, a female's successive infants were sired by the same male. Thus, in olive baboons, the development of stable breeding bonds and paternal investment seem to be grounded in the formation of close ties between males and anestrous females. However, other factors such as male dominance rank also influence paternity success and may preclude stability of these bonds to the extent found in human societies.

To grunt or not to grunt: Factors governing call production in female olive baboons, Papio anubis.

Vocal signals often play an important role in synchronizing the activities of group members, coordinating decisions about when and where to travel, and facilitating social interactions in which there are potential conflicts of interest. Here, we show that when female olive baboons (Papio anubis) give low amplitude grunts after approaching other females, they are less likely to behave aggressively toward their partners and more likely to handle their partners' infants and interact affiliatively with them. In addition, females are more likely to grunt after they approach lower ranking females than after they approach higher ranking females and are less likely to grunt after they approach their own mothers and daughters than after they approach other females. These patterns, which are strikingly similar to patterns previously reported in chacma baboons (Papio ursinus) support the hypothesis that grunts function as signals of benign intent. Moreover, they suggest that actors' decisions about whether to grunt or remain silent are influenced by the social context, particularly their partners' likely response to their approach. Taken together, the patterning of grunts in olive and chacma baboon suggests that these vocalizations play an important in reducing uncertainty about actors' intentions and facilitate nonaggressive social interactions.

Darwin's monkey: why baboons can't become human.

Baboons were used in the past as models for human evolution. I utilize 40 years of data from my long-term study on baboons in Kenya to suggest that baboons are once again relevant for understanding human evolution, not as a referential model but to reset the starting conditions of the human experiment. The baboon data also offer a critique of widely held ideas about how natural selection might work by looking at real lives in real time. This situates competition in a matrix of collaboration and illustrates the critical role of chance, contingency, and history in baboon survival and success. I make three methodological moves to reach these conclusions. The first is to focus on process not just outcome. The second is to look at time scales longer than usual studies but shorter than evolutionary time as a way to open the black box that currently links behavior to evolutionary value. The third is to use comparative natural history, Darwin's method, as a way to capture and comprehend how complexity is generated and how baboons deal with it in their daily lives. These empirical and methodological turns lead to conclusions that run counter to widely held ideas about baboons, about primates, and about the determinism of natural selection. I follow my own research history to illustrate these points. The discussion ranges from alternative interpretations of the male and the female dominance hierarchies, to insights from a fission that happened when the foraging strategy of raiding and nonraiding baboons diverged, to evidence of adaptation after translocation, and finally to assessing two unusual fusions of baboon groups. Altogether, these natural histories yield baboon "principles of the social" with insights about cognition, cooperation, and culture and suggest why baboons can't become human. The data also support Weiss and Buchanan's framework (The Mermaid's Tale: Four Billion Years of Cooperation in the Making of Living Things. Cambridge, MA: Harvard University Press,2009. 305 p) with its alternative view of natural selection in which there is more slippage and tolerance, multiple solutions with larger acceptability spaces, and the possibility that an adaptive fit will be "good enough" rather than seamless. However, capturing behavioral complexity "in the wild" poses methodological challenges. Long-term field studies provide critical information but the current quantitative methods should be expanded also include natural history observations of behaviors and events across time, space, groups, and landscapes. Finally, the baboon natural histories illustrate how the evolutionary game has changed in the Anthropocene yielding a cautionary tale about the future for many primate species.

Maternal condition does not influence birth sex ratios in anubis baboons (Papio anubis).

Trivers and Willard predicted that when parental condition has differential effects on the fitness of male and female offspring, parents who are in good condition will bias investment toward the sex that benefits most from additional investment. Efforts to test predictions derived from Trivers and Willard's model have had mixed results, perhaps because most studies have relied on proxy measures of parental condition, such as dominance rank. Here, we examine the effects of female baboons condition on birth sex ratios and post-natal investment, based on visual assessments of maternal body condition. We find that local environmental conditions have significant effects on female condition, but maternal condition at conception has no consistent relationship with birth sex ratios. Mothers who are in poorer condition at the time of conception resume cycling significantly later than females who are in better condition, but the sex of their infants has no effect on the time to resumption of cycling. Thus, our findings provide strong evidence that maternal condition influences females' ability to reproduce, but females do not facultatively adjust the sex ratio of their offspring in relation to their dominance rank or current condition.

The Development of Primate Raiding: Implications for Management and Conservation.

Ecosystems and habitats are fast becoming human dominated, which means that more species, including primates, are compelled to exploit new human resources to survive and compete. Primate "pests" pose major management and conservation challenges. I here present the results from a unique opportunity to document how well-known individuals and groups respond to the new opportunity to feed on human foods. Data are from a long-term study of a single population in Kenya at Kekopey, near Gilgil, Kenya. Some of the naïve research baboons became raiders while others did not. I compare diet, activity budgets, and home range use of raiders and nonraiders both simultaneously, after the incursion of agriculture, and historically compared to the period before agriculture appeared. I present measures of the relative benefits (female reproduction) and costs (injuries, mortality, and survivorship) of incorporating human food into the diet and discuss why the baboons raid and their variations in raiding tendencies. Guarding and chasing are evaluated as control techniques. I also suggest conflict mitigation strategies by identifying the most likely options in different contexts. I end with a proposal for a rapid field assessment of human wildlife conflict involving primates.

Measuring success in primate translocation: a baboon case study.

Translocation of primates is still a rare event. The translocation in 1984 of two research groups of wild baboons that had been studied for 12 years prior to translocation and observed for 18 years afterwards offers a comprehensive set of data with which to evaluate success. A comparison with indigenous baboon troops at the release site provides an independent control for assessing performance in the release area. Two success criteria are developed with the use of indicator measures that include birth rate, death rate, patterns of mortality and survivorship, body condition, intestinal parasites, and group size. The baboon translocation succeeded according to both criteria: the two troops were saved by the translocation, and they did as well or better than could be expected in their new home. Their performance matched or exceeded that of translocated groups of other primate species.

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.

Variations in fecundity with age and environment in olive baboons (Papio anubis).

Ten years of reproductive data on a troop of savanna baboons (Papio anubis) demonstrated that females had an age-specific fecundity pattern similar to that of other mammals. Average yearly fecundity has also varied over the period of study and can be explained by variations in food abundance with interspecific competition from ungulate competitors, rather than by female age structure or density-dependent factors. The implications of age-specific fecundity for primate ecology, behavior, reproduction, and life-history strategies are discussed. The need to consider primate ecology within a broader community framework which includes human activity is also considered.