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.

Mechanical properties of the Papio anubis tympanic membrane: Change significantly from infancy to adulthood.

Mechanical properties of the tympanic membrane (TM) are important for studying the transfer function of the auditory system. However, nearly all reported human data are limited to adults because of the unavailability of temporal bones from children. In this study, we used the baboon (Papio anubis), a genetically close human relative, as a model to address the occurrence of age-dependent changes of the human TM. Forty-five baboon TMs were characterized in five age groups: <1 year, 1 to <2 years, 2 to <3 years, 3 to <5, and >5 years of age, comparable to human ages ranging from newborn to adult. The elastic properties of the baboon TMs were characterized by a micro-fringe projection technique. Volume displacement of the TM under quasi-static pressure was first determined from its micro-fringe pattern. Subsequently, these displacement values were used in a finite element model to derive mechanical properties. The Young's modulus of the baboon TM exhibited a modest decrease from 29.1 MPa to 26.0 MPa over the age groups. The average Young's modulus was ∼1.4 times higher than that of the adult human TM. This is the first time that age-related TM mechanical properties of high primate are reported. These new findings may help to explore the potential value of the baboon as a new primate model for future age-related hearing research on the normal and diseased ear.

Segmental morphometrics of the olive baboon (Papio anubis): a longitudinal study from birth to adulthood.

The linear dimensions and inertial characteristics of the body are important in locomotion and they change considerably during the ontogeny of animals, including humans. This longitudinal and ontogenetic study has produced the largest dataset to date of segmental morphometrics in a Catarrhini species, the olive baboon. The objectives of the study were to quantify the changes in body linear and inertial dimensions and to explore their (theoretical) mechanical significance for locomotion. We took full-body measurements of captive individuals at regular intervals. Altogether, 14 females and 16 males were followed over a 7-year period, i.e. from infancy to adulthood. Our results show that individual patterns of growth are very consistent and follow the general growth pattern previously described in olive baboons. Furthermore, we obtained similar growth curve structures for segment lengths and masses, although the respective time scales were slightly different. The most significant changes in body morphometrics occurred during the first 2 years of life and concerned the distal parts of the body. Females and males were similar in size and shape at birth. The rate and duration of growth produced substantial size-related differences throughout ontogeny, while body shapes remained very similar between the sexes. We also observed significant age-related variations in limb composition, with a proximal shift of the centre of mass within the limbs, mainly due to changes in mass distribution and in the length of distal segments. Finally, we observed what we hypothesize to be 'early biomechanical optimization' of the limbs for quadrupedal walking. This is due to a high degree of convergence between the limbs' natural pendular periods in infants, which may facilitate the onset of quadrupedal walking. Furthermore, the mechanical significance of the morphological changes observed in growing baboons may be related to changing functional demands with the onset of autonomous (quadrupedal) locomotion. From a wider perspective, these data provide unique insights into questions surrounding both the processes of locomotor development in primates and how these processes might evolve.

Bipedality from locomotor autonomy to adulthood in captive olive baboon (Papio anubis): Cross-sectional follow-up and first insight into the impact of body mass distribution.

OBJECTIVE: Despite that the biomechanics of standing and walking bipedally has been extensively studied in nonhuman primates, the morphological features that may constrain, or facilitate, the control of balance and thus of the spontaneous occurrence of bipedal behavior are poorly known. We aim to test the relationship between body mass distribution and bipedal behavior using a nonhuman primate species, the olive baboon, Papio anubis, raised in captivity. MATERIALS AND METHODS: We collected quantitative data on the frequency and duration of bipedalism together with morphometrics on a sample of 22 individuals. We used ontogenetic changes as a natural experiment that provides insights into the impact of morphology. Specifically we focus on 1) quantifying how body mass distribution changes from infancy to adulthood in baboons; and 2) whether the different patterns of mass distribution influence the behavioral variables, i.e., a) the frequency and b) the duration of bouts of bipedal behavior realized in different activity contexts. RESULTS: With regard to assisted bipedal behaviors, the duration and frequency of bouts of standing, contrary to walking, are significantly related to age. With regard to unassisted bipedal behaviors, no correlation to age is observed; the bout duration of walking is strongly correlated to body mass and mass distribution, contrary to the frequency of walking as well as the bout duration and frequency of bipedal standing. DISCUSSION: Our results suggest a close relationship between the pattern of mass distribution and the mechanism of balance control in the spontaneous bipedal walking of baboons. The mechanical effects of the pattern of mass distribution on the ability to perform bipedally in extant nonhuman primates are discussed in the context of the evolution toward habitual bipedalism.

The relationship of accentuated lines in enamel to weaning stress in juvenile baboons (Papio hamadryas anubis).

Weaning conflict may represent an evolutionary conflict of interest between parent and offspring, an honest signal of need on the part of a weanling, or both. Accentuated lines visible in histological sections of teeth are indicators of stress during enamel formation and have been hypothesised to form in baboon teeth during weaning. We analysed growth increments in 5 tooth sections from 2 Ugandan baboons (Papio hamadryas anubis), using polarised light microscopy, to determine when stresses occurred during the weaning process. Dietary transitions were reconstructed using normalised strontium intensities (Sr/Ca) in enamel. Accentuated lines were cross-matched between teeth from the same animal and plotted by month. The highest frequency of stress was experienced at around 6 months in 1 baboon, coinciding with an inferred reduction in suckling frequency, and at 11 months in another, coinciding with the inferred cessation of suckling. Because accentuated lines appear to indicate weaning stress at dietary transitions, weaning conflict may represent an honest signal of need on the part of the weanling.

Irregular xenoantibodies against human red blood cells in Papio anubis, P ursinus, P hamadryas, P papio, Saimiri sciureus, and Macaca mulatta: possible effect on xenotransplantation results.

OBJECTIVE: To assess the presence of irregular xenoantibodies against human red blood cells (RBCs) in 6 primate species used in xenotransplantation and other experimental procedures. MATERIALS AND METHODS: Serum samples from 109 baboons of 4 different species (olive, chacma, sacred, and Guinea), 38 rhesus macaques, and 30 squirrel monkeys were tested for irregular xenoantibodies using an agglutination test using human RBCs of known phenotype for Rh, Kell, Kidd, Lewis, Lutheran, P1, and Duffy antigens, commercially available as RBC I, II, and III. RESULTS: We found hemagglutination for RBC I in 49%, 22%, 100%, 57%, 32%, and 33% of olive, chacma, sacred, and Guinea baboons, rhesus macaques, and squirrel monkey, respectively. The frequency for RBC II was 49%, 50%, 100%, 57%, 37%, and 33%, respectively, and for RBC III was 56%, 37%, 100%, 79%, 34%, and 33%, respectively. There were differences in frequency depending on the sex of the rhesus macaques; all 3 RBCs tested were higher in the females: 44% vs 0%, P = .008; 48% vs 1%, P = .02, and 44% vs 9.1%, P = .04 for RBC I, II, and III, respectively. There were differences due to age in only olive baboons, and a higher frequency in younger animals compared with juvenile, subadult, and adult animals for all 3 human RBCs. CONCLUSIONS: Assessment of irregular antibodies in the presence of primate serum should be taken into account during any experimental xenotransplantation protocol.

Living on the edge: life-history of olive baboons at Gashaka-Gumti National Park, Nigeria.

Baboons are the most successful and ubiquitous African primates, renowned for their behavioral and reproductive flexibility, which enable them to inhabit a wide variety of habitat types. Owing to a number of long-term field studies, comparative behavioral, developmental, demographic, and life-history data are available from several populations, but study sites show a heavy bias toward South and East African savannahs, with little research in West or Central Africa. Life-history data from such areas are important if we are fully to understand the nature of the environmental factors that limit baboon distribution. Here, we present demographic data for olive baboons at Gashaka-Gumti National Park (GGNP), Nigeria, collected from December 2000-February 2006, and use these data to test comparative models of baboon life-history. The GGNP habitat, which includes large areas of rainforest, is an environment in which baboons are little studied, and rainfall is much higher than at previous study sites. GGNP troop size data are presented from censuses, as well as life-history data for two troops, one of which is within the park and wild-feeding (Kwano troop), whereas the other dwells at the park edge, and supplements its diet by crop-raiding (Gamgam troop). Troop sizes at GGNP are small compared with other field sites, but fit within previously suggested ranges for baboons under these climatic conditions. Inter-birth intervals in Kwano troop were long compared with most studied populations, and values were not as predicted by comparative models. Consistent with known effects of food enhancement, Gamgam troop experienced shorter inter-birth intervals and lower infant mortality than Kwano troop. We indicate some possible factors that exclude baboons from true rainforest, and suggest that the clearing of forests in Central and West Africa for agricultural land may allow baboons to extend their range into regions from which they are currently excluded.

Age at maturity in wild baboons: genetic, environmental and demographic influences.

The timing of early life-history events, such as sexual maturation and first reproduction, can greatly influence variation in individual fitness. In this study, we analysed possible sources of variation underlying different measures of age at social and physical maturation in wild baboons in the Amboseli basin, Kenya. The Amboseli baboons are a natural population primarily comprised of yellow baboons (Papio cynocephalus) that occasionally hybridize with anubis baboons (Papio anubis) from outside the basin. We found that males and females differed in the extent to which various factors influenced their maturation. Surprisingly, we found that male maturation was most strongly related to the proportion of anubis ancestry revealed by their microsatellite genotypes: hybrid males matured earlier than yellow males. In contrast, although hybrid females reached menarche slightly earlier than yellow females, maternal rank and the presence of maternal relatives had the largest effects on female maturation, followed by more modest effects of group size and rainfall. Our results indicate that a complex combination of demographic, genetic, environmental, and maternal effects contribute to variation in the timing of these life-history milestones.