Yet Another Non-Unique Human Behaviour: Leave-Taking in Wild Chacma Baboons (Papio ursinus).

Leave taking is a common, possibly universal, feature of human social behaviour that has undergone very little empirical research. Although the importance remains unknown, it has been suggested to play an important role in managing separations, mitigating the risk, and increasing social bonding beyond the interaction itself. In nonhuman species, the literature is virtually absent, but identifying leave taking beyond humans may provide unique insights into the evolutionary history of this behaviour and shed light onto its proximate and ultimate function(s). Methods to study leave taking are not well-established, and the variation in definitions, measures, and control variables presented in past studies poses additional challenges. Baboons are a valuable model for investigating human behavioural evolution: as a flexible, highly adaptable, and social primate whose radiation is, similarly to humans, associated with the emergence of the African savannah biome. Using the framework and definition proposed by Baehren, we investigated the presence of leave taking in a wild, generalist primate and tested a range of candidate behaviours on prerecorded video footage: (1) self-scratching, (2) eye gaze, and (3) orientation in the direction of parting. Using multivariate analysis, controlling for interaction duration and individual variation, our results show that orientation in the direction of parting occurs predominantly before social separation events. These results indicate evidence of leave taking in a wild nonhuman population and contrast with previous ideas that this is a uniquely human behaviour. The presence of leave taking in baboons suggests a deep evolutionary history of this behaviour, warranting further investigation into its function and presence across other nonhuman primate species.

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.

A missing piece of the Papio puzzle: Gorongosa baboon phenostructure and intrageneric relationships.

Most authors recognize six baboon species: hamadryas (Papio hamadryas), Guinea (Papio papio), olive (Papio anubis), yellow (Papio cynocephalus), chacma (Papio ursinus), and Kinda (Papio kindae). However, there is still debate regarding the taxonomic status, phylogenetic relationships, and the amount of gene flow occurring between species. Here, we present ongoing research on baboon morphological diversity in Gorongosa National Park (GNP), located in central Mozambique, south of the Zambezi River, at the southern end of the East African Rift System. The park exhibits outstanding ecological diversity and hosts more than 200 baboon troops. Gorongosa National Park baboons have previously been classified as chacma baboons (P. ursinus). In accordance with this, two mtDNA samples from the park have been placed in the same mtDNA clade as the northern chacma baboons. However, GNP baboons exhibit morphological features common in yellow baboons (e.g., yellow fur color), suggesting that parapatric gene flow between chacma and yellow baboons might have occurred in the past or could be ongoing. We investigated the phenostructure of the Gorongosa baboons using two approaches: 1) description of external phenotypic features, such as coloration and body size, and 2) 3D geometric morphometric analysis of 43 craniofacial landmarks on 11 specimens from Gorongosa compared to a pan-African sample of 352 baboons. The results show that Gorongosa baboons exhibit a mosaic of features shared with southern P. cynocephalus and P. ursinus griseipes. The GNP baboon phenotype fits within a geographic clinal pattern of replacing allotaxa. We put forward the hypothesis of either past and/or ongoing hybridization between the gray-footed chacma and southern yellow baboons in Gorongosa or an isolation-by-distance scenario in which the GNP baboons are geographically and morphologically intermediate. These two scenarios are not mutually exclusive. We highlight the potential of baboons as a useful model to understand speciation and hybridization in early human evolution.

Isotopic assessment of marine food consumption by natural-foraging chacma baboons on the Cape Peninsula, South Africa.

OBJECTIVES: Stable isotope analysis has been used to investigate consumption of marine resources in a variety of terrestrial mammals, including humans, but not yet in extant nonhuman primates. We sought to test the efficacy of stable isotope analysis as a tool for such studies by comparing isotope- and observation-based estimates of marine food consumption by a troop of noncommensal, free-ranging chacma baboons. MATERIALS AND METHODS: We determined δ13 C and δ15 N values of baboon hair (n = 9) and fecal samples (n = 144), and principal food items (n = 362). These values were used as input for diet models, the outputs of which were compared to observation-based estimates of marine food consumption. RESULTS: Fecal δ13 C values ranged from -29.3‰ to -25.6‰. δ15 N values ranged from 0.9‰ to 6.3‰ and were positively correlated with a measure of marine foraging during the dietary integration period. Mean (± SD) δ13 C values of adult male and female baboon hairs were -21.6‰ (± 0.1) and -21.8‰ (± 0.3) respectively, and corresponding δ15 N values were 5.0‰ (± 0.3) and 3.9‰ (± 0.2). Models indicated that marine contributions were ≤10% of baboon diet within any season, and contributed ≤17% of dietary protein through the year. DISCUSSION: Model output and observational data were in agreement, both indicating that despite their abundance in the intertidal region, marine foods comprised only a small proportion of baboon diet. This suggests that stable isotope analysis is a viable tool for investigating marine food consumption by natural-foraging primates in temperate regions.

Description of a new species, Trichuris ursinus n. sp. (Nematoda: Trichuridae) from Papio ursinus Keer, 1792 from South Africa.

In the present work, we carried out a morphological, biometrical and molecular study of whipworms Trichuris Roederer, 1761 (Nematoda: Trichuridae) parasitizing Papio ursinus Keer 1792 (Chacma baboon). Biometrical and molecular data suggest a new species of Trichuris parasitizing baboons. In addition of main morphological features (spicule, spicule sheath, spicule tube, proximal cloacal tube, distal cloacal tube, vulva, vagina), the mean values of individual variables between Trichuris colobae, Trichuris suis, Trichuris trichiura examined by Student's t tests suggest that T. ursinus n. sp. constitutes a new species. The combined analysis of three markers (cox1, cob and ITS2) revealed a sister relationships between T. colobae and T. ursinus n. sp. Mitochondrial sequences revealed a higher inter-specific similarity between T. ursinus n. sp., T. suis and T. colobae. Phylogenetic hypotheses for both mitochondrial genes strongly supported distinct genetic lineages corresponding to different species of the genus Trichuris associated with certain hosts. Thus, T. suis, T. colobae and T. ursinus n. sp. appeared as a sister group and separated from Trichuris spp. from humans and other species of primates.

Sequential phenotypic constraints on social information use in wild baboons.

Social information allows the rapid dissemination of novel information among individuals. However, an individual's ability to use information is likely to be dependent on phenotypic constraints operating at three successive steps: acquisition, application, and exploitation. We tested this novel framework by quantifying the sequential process of social information use with experimental food patches in wild baboons (Papio ursinus). We identified phenotypic constraints at each step of the information use sequence: peripheral individuals in the proximity network were less likely to acquire and apply social information, while subordinate females were less likely to exploit it successfully. Social bonds and personality also played a limiting role along the sequence. As a result of these constraints, the average individual only acquired and exploited social information on.

The information trail.

The ability of a wild baboon to acquire and exploit social information depends on its individual characteristics and its position within various social networks.

Social effects on foraging behavior and success depend on local environmental conditions.

In social groups, individuals' dominance rank, social bonds, and kinship with other group members have been shown to influence their foraging behavior. However, there is growing evidence that the particular effects of these social traits may also depend on local environmental conditions. We investigated this by comparing the foraging behavior of wild chacma baboons, Papio ursinus, under natural conditions and in a field experiment where food was spatially clumped. Data were collected from 55 animals across two troops over a 5-month period, including over 900 agonistic foraging interactions and over 600 food patch visits in each condition. In both conditions, low-ranked individuals received more agonism, but this only translated into reduced foraging performances for low-ranked individuals in the high-competition experimental conditions. Our results suggest one possible reason for this pattern may be low-ranked individuals strategically investing social effort to negotiate foraging tolerance, but the rank-offsetting effect of this investment being overwhelmed in the higher-competition experimental environment. Our results also suggest that individuals may use imbalances in their social bonds to negotiate tolerance from others under a wider range of environmental conditions, but utilize the overall strength of their social bonds in more extreme environments where feeding competition is more intense. These findings highlight that behavioral tactics such as the strategic investment of social effort may allow foragers to mitigate the costs of low rank, but that the effectiveness of these tactics is likely to be limited in certain environments.

Personality predicts the propensity for social learning in a wild primate.

Social learning can play a critical role in the reproduction and survival of social animals. Individual differences in the propensity for social learning are therefore likely to have important fitness consequences. We asked whether personality might underpin such individual variation in a wild population of chacma baboons (Papio ursinus). We used two field experiments in which individuals had the opportunity to learn how to solve a task from an experienced conspecific demonstrator: exploitation of a novel food and a hidden item of known food. We investigated whether the (1) time spent watching a demonstrator and (2) changes in task-solving behaviour after watching a demonstrator were related to personality. We found that both boldness and anxiety influenced individual performance in social learning. Specifically, bolder and more anxious animals were more likely to show a greater improvement in task solving after watching a demonstrator. In addition, there was also evidence that the acquisition of social information was not always correlated with its use. These findings present new insights into the costs and benefits of different personality types, and have important implications for the evolution of social learning.

Occult hepatitis B virus infection in chacma baboons, South Africa.

During previous studies of susceptibility to hepatitis B virus (HBV) infection, HBV DNA was detected in 2/6 wild-caught baboons. In the present study, HBV DNA was amplified from 15/69 wild-caught baboons. All animals were negative for HBV surface antigen and antibody against HBV core antigen. Liver tissue from 1 baboon was immunohistochemically negative for HBV surface antigen but positive for HBV core antigen. The complete HBV genome of an isolate from this liver clustered with subgenotype A2. Reverse transcription PCR of liver RNA amplified virus precore and surface protein genes, indicating replication of virus in baboon liver tissue. Four experimentally naive baboons were injected with serum from HBV DNA-positive baboons. These 4 baboons showed transient seroconversion, and HBV DNA was amplified from serum at various times after infection. The presence of HBV DNA at relatively low levels and in the absence of serologic markers in the baboon, a nonhuman primate, indicates an occult infection.

Social relationships of mountain baboons: Leadership and affiliation in a non-female-bonded monkey.

Instead of close and differentiated relationships among adult females, the accepted norm for savanna baboons, groups of Drakensberg mountain baboons (Papio ursinus) showed strong affiliation of females towards a single male. The same male was usually the decision-making animal in controlling group movements. Lactating or pregnant females focused their grooming on this "leader" male, producing a radially patterned sociogram, as in the desert baboon (P. hamadryas); the leader male supported young animals in the group against aggression and protected them against external threats. Unlike typical savanna baboons, these mountain baboons rarely displayed approach-retreat or triadic interactions, and entirely lacked coalitions among adult females. Both groups studied were reproductively one-male; male-female relationships in one were like those in a unit of a hamadryas male at his peak, while the other group resembled the unit of an old hamadryas male, who still leads the group, with a male follower starting to build up a new unit and already monopolizing mating. In their mountain environment, where the low population density suggests conditions as harsh for baboons as in deserts, adults in these groups kept unusually large distances apart during ranging; kin tended to range apart, and spacing of adults was greatest at the end of the dry, winter season. These facts support the hypothesis that sparse food is responsible for convergence with hamadryas social organization. It is suggested that all baboons, though matrilocal, are better categorized as "cross-sex-bonded" than "female bonded".

Social relationships of mountain baboons: Leadership and affiliation in a non-female-bonded monkey.

Instead of close and differentiated relationship among adult females, the accepted norm for savanna baboons, groups of Drakensberg mountain baboons (Papio ursinus) showed strong affiliation of females towards a single male. The same male was usually the decision-making animal in controlling group movements. Lactating or pregnant females focused their grooming on this "leader" male, producing a radially patterned sociogram, as in the desert baboon (P. hamadryas); the leader male supported young animals in the group against aggression and protected them against external threats. Unlike typical savanna baboons, these mountain baboons rarely displayed approach-retreat or triadic interactions, and entirely lacked coalitions among adult females. Both groups studied were reproductively one-male; male-female relationships in one were like those in a unit of hamadryas male at his peak, while the other group resembled the unit of an old hamadryas male, who still led the group, with a male follower starting to build up a new unit and already monoplizing mating. In their mountain environment, where the low population density suggests conditions as harsh for baboons as in deserts, adults in these groups kept unusually large distances apart during ranging; kin tended to range apart, and spacing of adults was greatest at the end of the dry, winter season. These facts support the hypothesis that sparse food is responsible for convergence with hamadryas social organization. It is suggested that all baboons, though matrilocal, are better categorized as "cross-sex-bonded" than "female bonded".

Reactions to fear as a proximate factor in the sociospatial organization of baboon progressions.

The objective of this study was to test the hypothesis that fearfulness is a key proximate factor determining the nonrandom order repeatedly reported for baboon troops progressing from one location to another. According to this hypothesis, the most vulnerable troop members, the walking immatures, are expected in most circumstances to be cautious and to keep others between themselves and potential danger. The more confident adults, especially large powerful males, should tend toward the front and rear of progressing troops. The fear hypothesis predicts that in progressions toward a fear source, adult males should be near the front of the troop; on the other hand, when the troop is retreating from a frightening or tense situation, adult males should be found more toward the rear. Progressions of chacma baboons away from the location of a severe fright or in retreat from another troop were compared with other progressions. Adult males tended to be more rearward in these situations. The number of adults of either sex interposed between a fear source and the first walking immature was greater for retreating troops than for others. Some adult males continued to be near the front of the troop when retreating from tense situations.

Fishing baboons at desert waterholes.

Live fish capture by wild chacma baboons is described. Fish were captured from drying desert pools and then covered with sand to immobilize active fish or to facilitate handling. Possible reasons omnivorous primates elsewhere do not capture live fish are considered.

Solitary male chacma baboons in a desert canyon.

Solitary and paired adult (nine) and subadult (one) male chacma baboons, Papio ursinus, were observed over a period of years living in part of a wooded desert canyon not used by adjacent troops. These extratroop males were silent when alone and gave only one alarm vocalization, the "wa-hoo" call, when paired. The space occupied by them is unsuitable for use by troops according to criteria for adequate sleeping sites and access to water. But the foods available to them, especially figs, but also other fruits and fresh acacia seeds, were abundant. These foods are more highly preferred by baboons than those foods available to troop members. Troop members deplete these resources and shift to less preferred foods with lower water content and longer processing times. All of the adult members of the troop adjacent to these isolated males were infected with a skin disease. Isolated males were not so afflicted and so cannot have originated from, or ever been a part of, this troop. They probably moved to the space where they were observed from other inland troops, traveling to their current home range along the narrow canyon river course.

Diurnal variations in serum testosterone concentrations of captive adult male chacma baboons (Papio ursinus).

Captive adult male chacma baboons (Papio ursinus) housed with natural lighting exposure and blood sampled at 3-hr intervals showed significant diurnal variations in serum testosterone concentrations. Low mean concentrations were found at 0800 hr approximately 1 hr after sunrise and mean concentrations were their highest at 2000 hr approximately 1 » hr after sunset.