Contrasting effects of male immigration and rainfall on rank-related patterns of miscarriage in female olive baboons.

In mammalian species with prolonged maternal investment in which high-ranking males gain disproportionate numbers of mating opportunities, males that quickly ascend the hierarchy may benefit from eliminating the dependent offspring of their competitors. In savanna baboons, high-ranking females are the most profitable targets of infanticide or feticide, because their offspring have higher survival rates and their daughters reach sexual maturity at a younger age. However, such patterns may be obscured by environmental stressors that are known to exacerbate fetal losses, especially in lower-ranking females. Using 30 years of data on wild olive baboons (Papio anubis) in Gombe National Park, Tanzania, we found evidence that rapidly-rising immigrant males induced miscarriages in high-ranking females outside of drought conditions. However, miscarriage rates were largely reversed during prolonged periods of low rainfall, suggesting that low-ranking females are particularly vulnerable to low food availability and social instability. Infanticide did not emerge as a recurrent male strategy in this population, likely because of the protective behavior of resident males towards vulnerable juveniles.

Influence of rainfall on sleeping site choice by a group of anubis baboons (Papio anubis).

For diurnal nonhuman primates, shifting among different sleeping sites may provide multiple benefits such as better protection from predators, reduced risk of parasitic infection, and closer proximity to spatially and temporally heterogeneous food and water. This last benefit may be particularly important in sleeping site selection by primates living in savanna-woodlands where rainfall is more limited and more seasonally pronounced than in rainforests. Here, we examined the influence of rainfall, a factor that affects food and water availability, on the use of sleeping sites by anubis baboons (Papio anubis) over two 13-month study periods that differed in rainfall patterns. We predicted that during wet periods, when food and water availability should be higher, the study group would limit the number of sleeping sites and would stay at each one for more consecutive nights than during dry periods. Conversely, we predicted that during dry periods the group would increase the number of sleeping sites and stay at each one for fewer consecutive nights as they searched more widely for food and water. We also predicted that the group would more often choose sleeping sites closer to the center of the area used during daytime (between 07:00 and 19:00) during wet months than during dry months. Using Global Positioning System data from collared individuals, we found that our first prediction was not supported on either monthly or yearly timescales, although past monthly rainfall predicted the use of the main sleeping site in the second study period. Our second prediction was supported only on a yearly timescale. This study suggests that baboons' choice of sleeping sites is fluid over time while being sensitive to local environmental conditions, one of which may be rainfall.

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.

A comparative perspective on the evolution of mammalian reactions to dead conspecifics.

In a variety of mammalian species, mothers and others care for and/or carry deceased newborns, and sometimes other conspecifics. The rationale for such behavior remains elusive. Based upon field observations of olive baboon (Papio anubis), African elephant (Loxodonta africana), and Thornicroft's giraffe (Giraffa camelopardalis) responses to recently dead conspecifics, combined with reports in the literature, a hypothesis is proposed to account for this activity. Among female mammals, lifetime reproductive success is more dependent upon rearing, than production, of offspring. The successful nurturing of progeny is associated with a strong maternal-offspring bond. One of the most important chemicals involved in both lactation and mother-infant bonding is oxytocin, a tiny molecule that has a lengthy evolutionary history and is implicated in the formation of social bonds across mammals. Evolution has extended the impact of oxytocin by adopting it beyond the original mother-infant bond to the establishment of social bonds that are required among group-living animals. Hence, sociality is a consequence of the same fundamental biological mediator of mother-offspring bonding, and this intricate connection between physiology and behavior has produced a situation where sometimes animals will care for or carry dead companions. Ways to test this hypothesis, as well as a potential way to refute it, are proposed.

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.

Manipulating social cues in baboon gesture learning: what does it tell us about the evolution of communication?

Reading the attentional state of an audience is crucial for effective intentional communication. This study investigates how individual learning experience affects subsequent ability to tailor gestural communication to audience visual attention. Olive baboons were atypically trained to request food with gestures by a human standing in profile, while not having access to her face. They were tested immediately after training, and then 1 year later in conditions that varied the human's cues to attention. In immediate testing, these baboons (profile group baboons) gestured towards untrained cues regardless of their relevance for visual communication. They were also less discriminant towards trained versus untrained cues than baboons trained by a human facing them (face group baboons, tested in Bourjade et al. Anim Behav 87:121-128; Bourjade et al., Anim Behav 87:121-128, 2014). In delayed testing, the number of gestures towards meaningful untrained cues increased and profile group baboons discriminated the orientation of the human body, a conspicuous proxy of visual attention. Our results provide support for the primary interplay between implicit learning and systematically reinforced associations made through explicit training in the scaffolding of intentional gesturing tuned to audience attention.

The effect of excluding juveniles on apparent adult olive baboons (Papio anubis) social networks.

In recent years there has been much interest in investigating the social structure of group living animals using social network analysis. Many studies so far have focused on the social networks of adults, often excluding younger, immature group members. This potentially may lead to a biased view of group social structure as multiple recent studies have shown that younger group members can significantly contribute to group structure. As proof of the concept, we address this issue by investigating social network structure with and without juveniles in wild olive baboons (Papio anubis) at Gashaka Gumti National Park, Nigeria. Two social networks including all independently moving individuals (i.e., excluding dependent juveniles) were created based on aggressive and grooming behaviour. We used knockout simulations based on the random removal of individuals from the network in order to investigate to what extent the exclusion of juveniles affects the resulting network structure and our interpretation of age-sex specific social roles. We found that juvenile social patterns differed from those of adults and that the exclusion of juveniles from the network significantly altered the resulting overall network structure. Moreover, the removal of juveniles from the network affected individuals in specific age-sex classes differently: for example, including juveniles in the grooming network increased network centrality of adult females while decreasing centrality of adult males. These results suggest that excluding juveniles from the analysis may not only result in a distorted picture of the overall social structure but also may mask some of the social roles of individuals belonging to different age-sex classes.

Antelope Predation by Nigerian Forest Baboons: Ecological and Behavioural Correlates.

Baboons are well studied in savannah but less so in more closed habitats. We investigated predation on mammals by olive baboons (Papio anubis) at a geographical and climatic outlier, Gashaka Gumti National Park (Nigeria), the wettest and most forested site so far studied. Despite abundant wildlife, meat eating was rare and selective. Over 16 years, baboons killed 7 bushbuck (Tragelaphus scriptus) and 3 red-flanked duiker (Cephalophus rufilatus), mostly still-lying 'parked' infants. Taking observation time into account, this is 1 predation per group every 3.3 months - far lower than at other sites. Some features of meat eating resemble those elsewhere; predation is opportunistic, adult males monopolize most prey, a targeted killing bite is lacking and begging or active sharing is absent. Carcass owners employ evasive tactics, as meat is often competed over, but satiated owners may tolerate others taking meat. Other features are unusual; this is only the second study site with predation records for bushbuck and the only one for red-flanked duiker. The atypical prey and rarity of eating mammals probably reflects the difficulty of acquiring prey animals when vegetation cover is dense. Our data support the general prediction of the socioecological model that environments shape behavioural patterns, while acknowledging their intraspecific or intrageneric plasticity.

Training experience in gestures affects the display of social gaze in baboons' communication with a human.

Gaze behaviour, notably the alternation of gaze between distal objects and social partners that accompanies primates' gestural communication is considered a standard indicator of intentionality. However, the developmental precursors of gaze behaviour in primates' communication are not well understood. Here, we capitalized on the training in gestures dispensed to olive baboons (Papio anubis) as a way of manipulating individual communicative experience with humans. We aimed to delineate the effects of such a training experience on gaze behaviour displayed by the monkeys in relation with gestural requests. Using a food-requesting paradigm, we compared subjects trained in requesting gestures (i.e. trained subjects) to naïve subjects (i.e. control subjects) for their occurrences of (1) gaze behaviour, (2) requesting gestures and (3) temporal combination of gaze alternation with gestures. We found that training did not affect the frequencies of looking at the human's face, looking at food or alternating gaze. Hence, social gaze behaviour occurs independently from the amount of communicative experience with humans. However, trained baboons-gesturing more than control subjects-exhibited most gaze alternation combined with gestures, whereas control baboons did not. By reinforcing the display of gaze alternation along with gestures, we suggest that training may have served to enhance the communicative function of hand gestures. Finally, this study brings the first quantitative report of monkeys producing requesting gestures without explicit training by humans (controls). These results may open a window on the developmental mechanisms (i.e. incidental learning vs. training) underpinning gestural intentional communication in primates.

Associations between spatial position, stress and anxiety in forest baboons Papio anubis.

Spatial position within a group affects the value of group-living benefits such as reduced predation risk and improved foraging. The threat of predation, poor nutrition or increased competition from conspecifics can all cause stress. In many species, central positions are known to be more beneficial than peripheral positions in terms of reduced predation, vigilance and foraging. In this study, we examine whether spatial position within a group is associated with stress and anxiety in a troop of olive baboons (Papio anubis). We predicted that the benefits of occupying central positions would be reflected by a reduction in stress and anxiety for animals who spent the most time in the centre of the group. The study subjects appeared to compete actively for the centre of the group. Physiological stress measures (faecal glucocorticoid concentrations) were positively correlated with time spent in central positions. Time spent in central positions was positively correlated with proximity but negatively correlated with vigilance behaviours (alarm barks). Vigilance rates were positively correlated with measures of anxiety (self-scratch frequency). It is suggested that individuals experience chronic stress due to proximity to conspecifics in central positions, whilst perceived predation risk causes anxiety, with perceived predation risk experienced more by individuals on the periphery.

Monkeys perform as well as apes and humans in a size discrimination task.

Whether the cognitive competences of monkeys and apes are rather similar or whether the larger-brained apes outperform monkeys in cognitive experiments is a highly debated topic. Direct comparative analyses are therefore essential to examine similarities and differences among species. We here compared six primate species, including humans, chimpanzees, bonobos, gorillas (great apes), olive baboons, and long-tailed macaques (Old World monkeys) in a task on fine-grained size discrimination. Except for gorillas, subjects of all taxa (i.e. humans, apes, and monkeys) were able to discriminate three-dimensional cubes with a volume difference of only 10 % (i.e. cubes of 50 and 48 mm side length) and performed only slightly worse when the cubes were presented successively. The minimal size discriminated declined further with increasing time delay between presentations of the cubes, highlighting the difficulty to memorize exact size differences. The results suggest that differences in brain size, as a proxy for general cognitive abilities, did not account for variation in performance, but that differential socio-ecological pressures may better explain species differences. Our study highlights the fact that differences in cognitive abilities do not always map neatly onto phylogenetic relationships and that in a number of cognitive experiments monkeys do not fare significantly worse than apes, casting doubt on the assumption that larger brains per se confer an advantage in such kinds of tests.

Olive baboons communicate intentionally by pointing.

A pointing gesture creates a referential triangle that incorporates distant objects into the relationship between the signaller and the gesture's recipient. Pointing was long assumed to be specific to our species. However, recent reports have shown that pointing emerges spontaneously in captive chimpanzees and can be learned by monkeys. Studies have demonstrated that both human children and great apes use manual gestures (e.g. pointing), and visual and vocal signals, to communicate intentionally about out-of-reach objects. Our study looked at how monkeys understand and use their learned pointing behaviour, asking whether it is a conditioned, reinforcement-dependent response or whether monkeys understand it to be a mechanism for manipulating the attention of a partner (e.g. a human). We tested nine baboons that had been trained to exhibit pointing, using operant conditioning. More specifically, we investigated their ability to communicate intentionally about the location of an unreachable food reward in three contexts that differed according to the human partner's attentional state. In each context, we quantified the frequency of communicative behaviour (auditory and visual signals), including gestures and gaze alternations between the distal food and the human partner. We found that the baboons were able to modulate their manual and visual communicative signals as a function of the experimenter's attentional state. These findings indicate that monkeys can intentionally produce pointing gestures and understand that a human recipient must be looking at the pointing gesture for them to perform their attention-directing actions. The referential and intentional nature of baboons' communicative signalling is discussed.

Baboon (Papio anubis) social complexity--a network approach.

Although many studies have analyzed the causes and consequences of social relationships, few studies have explicitly assessed how measures of social relationships are affected by the choice of behaviors used to quantify them. The use of many behaviors to measure social relationships in primates has long been advocated, but it was analytically difficult to implement this framework into primatological work. However, recent advances in social network analysis (SNA) now allow the comparison of multiple networks created from different behaviors. Here we use our database of baboon social behavior (Papio anubis, Gashaka Gumti National Park, Nigeria) to investigate (i) to what extent social networks created from different behaviors overlap, (ii) to what extent individuals occupy similar social positions in these networks and (iii) how sex affects social network position in this population of baboons. We used data on grooming, aggression, displacement, mounting and presenting, which were collected over a 15-month period. We calculated network parameters separately for each behavior. Networks based on displacement, mounting and presenting were very similar to each other, whereas grooming and aggression networks differed both from each other and from mounting, displacement and presenting networks. Overall, individual network positions were strongly affected by sex. Individuals central in one network tended to be central in most other networks as well, whereas other measures such as clustering coefficient were found to vary depending on the behavior analyzed. Thus, our results suggest that a baboon's social environment is best described by a multiplex network based on affiliative, aggressive and sexual behavior. Modern SNA provides a number of useful tools that will help us to better understand animals' social environment. We also discuss potential caveats related to their use.

Representational format determines numerical competence in monkeys.

A range of animal species possess an evolutionarily ancient system for representing number, which provides the foundation for simple arithmetical operations such as addition and numerical comparisons. Surprisingly, non-human primates tested in ecologically, highly valid quantity discrimination tasks using edible items often show a relatively low performance, suggesting that stimulus salience interferes with rational decision making. Here we show that quantity discrimination was indeed significantly enhanced when monkeys were tested with inedible items compared with food items (84 versus 69% correct). More importantly, when monkeys were tested with food, but rewarded with other food items, the accuracy was equally high (86%). The results indicate that the internal representation of the stimuli, not their physical quality, determined performance. Reward replacement apparently facilitated representation of the food items as signifiers for other foods, which in turn supported a higher acuity in decision making.

Informative breath: olfactory cues sought during social foraging among Old World monkeys (Mandrillus sphinx, M. Leucophaeus, and Papio anubis).

Sociality provides a unique opportunity for animals to acquire information and learn from others. Especially during foraging, where trial-and-error food selection might be fatal, conspecifics could act as valuable sources of information. During a six-year study across captive, semifree ranging, and wild Old World monkeys, I investigated whether individuals garnered olfactory-based information from their group mates that could guide their feeding decisions. Each of three study species [mandrills (Mandrillus sphinx), drills (M. leucophaeus), and olive baboons (Papio anubis)] performed a prominent muzzle-muzzle behavior, potentially enabling individuals to smell others' mouths and determine via olfaction what foods their conspecifics had chosen. This muzzle-muzzle behavior (1) was preferentially directed by naïve, younger individuals toward more experienced, older individuals, (2) occurred specifically while recipients were chewing and hence emitting the most potent chemical cues, (3) was typically followed by the actor consuming the very same food type the recipient had been eating, (4) was elicited most often in response to experiments involving novel foods, and (5) occurred less frequently as initially novel foods became more familiar. In contrast to this evidence for information acquisition, there was little support for previous proposals suggesting that muzzle-muzzle functions as a social display. Instead, the omnivorous diets and intensely social lifestyles of mandrills, drills, and baboons, may have each favored a convergent form of information acquisition: seeking out the breath of knowledgeable conspecifics to help decide what foods are safe to eat.

Contrast of hand preferences between communicative gestures and non-communicative actions in baboons: implications for the origins of hemispheric specialization for language.

Gestural communication is a modality considered in the literature as a candidate for determining the ancestral prerequisites of the emergence of human language. As reported in captive chimpanzees and human children, a study in captive baboons revealed that a communicative gesture elicits stronger degree of right-hand bias than non-communicative actions. It remains unclear if it is the communicative nature of this manual behavior which induces such patterns of handedness. In the present study, we have measured hand use for two uninvestigated behaviors in a group of captive olive baboons: (1) a non-communicative self-touching behavior ("muzzle wipe" serving as a control behavior), (2) another communicative gesture (a ritualized "food beg") different from the one previously studied in the literature (a species-specific threat gesture, namely "hand slap") in the same population of baboons. The hand preferences for the "food beg" gestures revealed a trend toward right-handedness and significantly correlated with the hand preferences previously reported in the hand slap gesture within the same baboons. By contrast, the hand preferences for the self-touching behaviors did not reveal any trend of manual bias at a group-level nor correlation with the hand preferences of any communicative gestures. These findings provide additional support to the hypothesized existence in baboons of a specific communicative system involved in the production of communicative gestures that may tend to a left-hemispheric dominance and that may differ from the system involved in purely motor functions. The hypothetical implications of these collective results are discussed within the theoretical framework about the origins of hemispheric specialization for human language.

Functional analysis and treatment of self-injury in a captive olive baboon.

Self-injurious behavior (SIB), such as self-biting and head banging, has been reported to occur in approximately 10% of captive, individually housed nonhuman primates. Accounts of the etiology of SIB in primates range from ecological to physiological. However, to date, no research has examined the possible influence of social consequences delivered by handlers and keepers in the maintenance of SIB in this population. The current study investigated the effects of social contact as a potentially reinforcing consequence for the SIB displayed by an olive baboon (Papio hamadryas anubis). Results indicated that the behavior was maintained by attention from humans. As treatment, reinforcement was arranged for an appropriate alternative response, resulting in increases in the appropriate alternative behavior and decreases in SIB.

Impact of social environment on variation in menstrual cycle length in captive female olive baboons (Papio anubis).

Factors affecting menstrual cycles and conception were explored for captive female olive baboons. We evaluated the relationship between the social environment and adequacy of the menstrual cycle in 55 non-conceptive and 21 conception cycles from 23 females. More abnormal cycles were expected for low-status females, and social stress levels were associated with variation in menstrual cycle length. Mean cycle length was 39.9 days (median=38) with a mean follicular phase duration of 23.7 (median=22) days. The duration of the follicular phase was more variable than that of the luteal phase (mean=15.8 days). The first cycle after postpartum resumption of cycling was not markedly different from subsequent cycles in terms of duration or probability of conception. Dominance rank was one significant factor affecting female fertility. Low-ranking females experienced more cycles prior to conception, longer cycles once cycling was well established and had smaller sexual swellings (anogenital area) than did high-ranking females. Both acute and chronic stresses may play important roles in fertility outcomes for these baboons and further research is needed to understand the role of stress and subtle menstrual cycle abnormalities in female mammal fertility.

Studies of reconciliation in anubis baboons.

Studies of post-conflict reconciliation were performed on anubis baboons living in corrals. Reconciliation was found to occur after more than a third of the conflicts observed; the mean reconciliatory tendency was 27.3 +/- 2.4. Different categories of conflict pairs showed similar reconciliation frequencies. In 75% of cases, reconciliation occurred within the first 2 min of completion of the conflict. The set of behavioral fragments demonstrated by participants in reconciliation depended on gender and role in the conflict. Differences were seen in the magnitudes of the reconciliatory tendencies of monkeys of high and low rankings.