Age-Related Tooth Wear Differs between Forest and Savanna Primates

Tooth wear in primates is caused by aging and ecological factors. However, comparative data that would allow us to delineate the contribution of each of these factors are lacking. Here, we contrast age-dependent molar tooth wear by scoring percent of dentine exposure (PDE) in two wild African primate populations from Gabonese forest and Kenyan savanna habitats. We found that forest-dwelling mandrills exhibited significantly higher PDE with age than savanna yellow baboons. Mandrills mainly feed on large tough food items, such as hard-shell fruits, and inhabit an ecosystem with a high presence of mineral quartz. By contrast, baboons consume large amounts of exogenous grit that adheres to underground storage organs but the proportion of quartz in the soils where baboons live is low. Our results support the hypothesis that not only age but also physical food properties and soil composition, particularly quartz richness, are factors that significantly impact tooth wear. We further propose that the accelerated dental wear in mandrills resulting in flatter molars with old age may represent an adaptation to process hard food items present in their environment.     

Canine Length in Wild Male Baboons: Maturation,Aging and Social Dominance Rank

Canines represent an essential component of the dentition for any heterodont mammal. In primates, like many other mammals, canines are frequently used as weapons. Hence, tooth size and wear may have significant implications for fighting ability, and consequently for social dominance rank, reproductive success, and fitness. We evaluated sources of variance in canine growth and length in a well-studied wild primate population because of the potential importance of canines for male reproductive success in many primates. Specifically, we measured maxillary canine length in 80 wild male baboons (aged 5.04–20.45 years) from the Amboseli ecosystem in southern Kenya, and examined its relationship with maturation, age, and social dominance rank. In our analysis of maturation, we compared food-enhanced baboons (those that fed part time at a refuse pit associated with a tourist lodge) with wild-feeding males, and found that food-enhanced males achieved long canines earlier than wild-feeding males. Among adult males, canine length decreased with age because of tooth wear. We found some evidence that, after controlling for age, longer canines were associated with higher adult dominance rank (accounting for 9% of the variance in rank), but only among relatively high-ranking males. This result supports the idea that social rank, and thus reproductive success and fitness, may depend in part on fighting ability mediated by canine size.     

Life history and the competitive environment: trajectories of growth,maturation, and reproductive output among chacma baboons

The social environment is a key feature influencing primate life histories. Chacma baboons (Papio hamadryas ursinus) are a female-bonded species with a strict linear dominance hierarchy. In this species, the allocation of energy to competing demands of growth and reproduction is hypothesized to vary as a function of competitive ability, which in turn increases with social rank. Since growth rate is a major component of life history models, measures of age-specific growth were used to analyze variation in life history traits across social ranks. Weights of 42 immature baboons were obtained without sedation or baiting from a troop of well-habituated chacma baboons in the Okavango Delta, Botswana. Using demographic and weight data from this wild population, five main findings emerged: 1) Weight for age and growth rate of infant and juvenile females are positively associated with maternal rank. 2) Male growth is not influenced by maternal rank. 3) Female growth shows smaller variation across feeding conditions than male growth. 4) Low-ranking adult females continue investment in offspring through prolonged lactation until they reach a weight comparable to that of high-ranking infants. 5) The benefit of rank to reproductive success shown in this study is 0.83 additional offspring. Reproductive span determined predominantly by age at maturation contributes 27-38% to the difference in expected number of offspring by rank, vs. 62-73% due to reproductive rate. These findings have major implications for understanding the role of social environment in phenotypic plasticity of life history traits, and in the evolution of primate life histories.     

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.     

Persistence of maternal effects in baboons: Mother's dominance rank at son's conception predicts stress hormone levels in subadult males

Dominance status and reproductive experience are maternal characteristics that affect offspring traits in diverse taxa, including some cercopithecine primates. Maternal effects of this sort are widespread and are sources of variability in offspring fitness. We tested the hypothesis that maternal dominance rank and reproductive experience as well as a male's own age and dominance rank predicted chronic fecal glucocorticoid (fGC) concentrations in 17 subadult wild male baboons, Papio cynocephalus (median age 6.5 years), in the Amboseli basin, Kenya. Among these variables, maternal dominance rank at a subadult male's conception was the sole significant predictor of the male's fGC and accounted for 42% of fGC variance; sons of lower ranking mothers had higher fGC than did those of high-ranking mothers. This result is striking because subadult male baboons are approximately 4-6 years past the period of infant dependence on their mothers, and are larger than and dominant to all adult females. In addition, many males of this age have survived their mothers' death. Consequently, the influence of maternal dominance rank persisted well beyond the stage at which direct maternal influence on sons is likely. Persistence of these major maternal influences from the perinatal period may signal organizational effects of mothers on sons' HPA axis. Although short-term, acute, elevations in GC are part of adaptive responses to challenges such as predators and other emergencies, chronically elevated GC are often associated with stress-related pathologies and, thereby, adverse effects on fitness components.     

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.     

Patterns of coalition formation by adult female baboons in Amboseli, Kenya

Coalitionary support in agonistic interactions is generally thought to be costly to the actor and beneficial to the recipient. Explanations for such cooperative interactions usually invoke kin selection, reciprocal altruism or mutualism. We evaluated the role of these factors and individual benefits in shaping the pattern of coalitionary activity among adult female savannah baboons, Papio cynocephalus, in Amboseli, Kenya. There is a broad consensus that, when ecological conditions favour collective defence of resources, selection favours investment in social relationships with those likely to provide coalitionary support. The primary features of social organization in female-bonded groups, including female philopatry, linear dominance hierarchies, acquisition of maternal rank and well-differentiated female relationships, are thought to be functionally linked to the existence of alliances between females. Female savannah baboons display these characteristics, but the frequency and function of their coalitionary aggression is disputed. In our five study groups, 4-6% of all disputes between females led to intervention by third parties. Adult females selectively supported close maternal kin. There was no evidence that females traded grooming for support or reciprocated support with nonkin. High-ranking females participated in coalitionary aggression most frequently, perhaps because they derived more benefits from group membership than other females did or could provide support at lower cost. Females typically supported the higher ranking of two contestants when they intervened in disputes between subordinates, so most coalitions reinforced the existing dominance hierarchy. Results indicate that female baboons participate in coalitionary aggression in a manner strongly influenced by nepotism and individual benefits.     

Tail carriage in baboons (Papio cynocephalus): relationship to dominance rank and age.

Several metric and categorical variables were used to assess tail carriage in 717 photographs of 54 yellow baboons (Papio cynocephalus) of known identity, sex, dominance rank, and estimated or known age. Analyses of these data demonstrated that age was the primary factor, influencing tail carriage of baboons not engaged in social interaction. Specifically, the proximal segment of the tail was carried increasingly close to the vertical with increasing age; other changes in tail angles and segment curvature were also correlated with age. There was no relationship between dominance rank and neutral tail carriage in adult male or female baboons, nor was the neutral tail carriage of the first-ranking male or female either distinctive or characteristic. The morphological basis of ontogenetic changes in neutral tail carriage in baboons is also discussed.     

Allogrooming, partner choice, and dominance in male anubis baboons

This study was designed to test the hypothesis that among unrelated male baboons (Papio cynocephalus anubis) in single-gender social groups there is no significant association between dominance status and allogrooming performance. The hypothesis was tested using behavioral measures obtained by focal animal sampling techniques. The results indicate that unrelated male baboons established well-defined linear dominance hierarchies, formed allogrooming relationships with one another, and exhibited a nonrandom distribution of allogrooming; however, there were no significant relationships between dominance rank and the frequency of allogrooming. We further tested our results by grouping individuals into three dominance status classes (high, middle, and low) and comparing the classes. Analysis of variance demonstrated no significant differences in rates of allogrooming by dominance class. These results suggest that dominance did not account for the variation in observed allogrooming behavior: Dominance status did not appear to determine the frequency with which animals groomed others, the number of grooming partners, or frequency of grooming that any individual received in comparison to that performed. High-ranking animals did not have significantly more grooming partners than low-ranking animals, and there appeared to be little competition within the groups for subordinates to groom high-ranking animals. When age, kinship, and group tenure are controlled, performance and reception of allogrooming are not strongly associated with dominance in single-gender social groups of male anubis baboons.     

Body mass and growth rates in a wild primate population

Summary We obtined data on body mass and growth rates for the immature members of two groups of wild baboons in Amboseli National Park, Kenya. Data were collected without feeding, trapping, or handling. The data were separated into cross-sectional and longitudinal components, allowing both the examination of body mass-age relationships and the calculation of growth rates for individuals. For animals less than three years old, body mass was wellperedicted from age by a linear model. Differences based on social group membership were small but consistent, and their origins are discussed. We detected no differences in body mass based on sex or on maternal dominance rank. For older juveniles, those three to seven years of age, a better fit was obtained from log of mass than by mass in a linear model. This was also true for the cross-sectional data set over the whole age range (zero to seven years). For older juveniles, samples were too small for quantitative analysis of differences based on sex, rank, or group membership, but trends in the data are indicated. Growth rates derived from repeat measures of body mass for 38 animals are presented and discussed.The growth rate values obtained in this study are consistent with data from cross-sectional studies of other wild baboon populations; these values for wild baboons are consistently one-half to one-third lower than growth rate values for well-provisioned captive baboons and equivalent to captive baboons fed a low-protein diet. Comparisons between primates and other mammals in the primate size range raise questions concerning ecological and behavioral constraints on primate growth rates; some possible mechanisms of constraint are suggested.     

Distribution of Affiliative Behavior Across Kin Classes and Their Fitness Consequences in Mandrills

Multimale–multifemale primate groups are ideal models to study the impact of kinship on the evolution of sociality. Indeed, the frequent combination of female philopatry and male reproductive skew produces social systems where both maternal and paternal kin are co‐resident. Several primates are known to bias their behavior toward both maternal and paternal kin. Moreover, allocation of affiliation toward paternal kin has been shown to depend on the availability in maternal kin: Female baboons invest more in paternal kin after the loss of preferred maternal kin. Here, we examined how affiliation co‐varies across kin classes in juvenile mandrills (Mandrillus sphinx), an Old World primate living in a multimale–multifemale society. While affiliation levels observed with the mother and with maternal half‐sibs co‐varied positively, especially in young females, we found that levels of affiliation among paternal half‐sibs correlated negatively with levels of affiliation among individuals from the same matriline (distant kin), possibly as a result of kin availability. In addition, in social species, social bonds between individuals have been linked to differentiated fitness consequences: More socially integrated individuals generally enjoy higher fitness. We therefore also tested whether affiliation during early life impacts fitness. We showed that the global amount of affiliation during juvenescence translated into possible reproductive benefits: Females who were more socially integrated gave birth on average a year before females that were less socially integrated. However, age at first reproduction was not predicted by the amount of affiliation exchanged with any particular kin class. These results add to the growing body of evidence demonstrating differential investment in bonding and possible social adjustments among different kin categories and emphasizing once more the adaptive value of sociality.     

Growth in colony living anubis baboon infants and its relationship with maternal activity budgets and reproductive status

Early growth is of interest because it is susceptible to maternal effects and linked to fitness components for a range of species. Here we present anthropometric measurements on 23 infant olive baboons born into a captive colony in order to describe growth over the first 2 years of life, to explore maternal influences on growth, and to assess the impact of growth profiles on maternal reproduction. Six main findings emerged: 1) Infant growth rates in our colony were higher than those reported for wild populations but comparable to those observed for food-enhanced animals. 2) The ratio of infant mass to maternal mass was positively associated with reproductive parameters, such as duration of post-partum amenorrhea and interbirth interval. 3) Mothers resumed cycling and reconceived when their infants attained a relatively consistent threshold mass. 4) Infant mass-for-age was associated with maternal rank and, independently, with maternal mass such that females of high dominance rank and heavy females had relatively large infants at their resumption of cycling. 5) Low-ranking and lighter females had longer investment periods but smaller infants. They continued investment in infant through prolonged lactation until their infants reached a mass similar to that of infants of high-ranking/heavy mothers, suggesting that the lengthening of investment is essentially compensatory for slow early growth. 6) There was no relationship between infant growth and maternal activity budgets. Maternal physical and social factors, not energetics, contributed to differences among infants in growth trajectories, and infant growth temporally influenced successive reproductive events.     

Status change during adulthood: life-history by-product or kin selection based on reproductive value?

When dominance status predicts fitness, most adaptive models of dominance relationships among cercopithecine primate females predict lifetime maintenance of status. These models and alternative ones positing rank decline as a non-adaptive by-product have remained largely untested, however, because lifetime status of older adults has been virtually unknown for natural populations. In a 25-year study of adult female savannah baboons (Papio cynocephalus), in each of three social groups, rank losses were common among the 66 females that lived past median adult age. These losses were not accounted for by loss in relative rank from group growth or by loss in absolute rank from reversals in rank between members of different maternal families or between sisters. Rather, females that had mature daughters experienced loss of dominance status to these offspring, a characteristic of all but the top-ranking matriline of each group. Among proposed hypotheses for rank reversals between adults, that of kin selection based on relative reproductive value is most clearly supported by these data. In contrast, observed patterns of rank loss are not consistent with alternative models that postulate that changes during adult lifespan are a product of accumulated risk, physical decline during ageing, or coalitionary support among females within or between matrilines.     

Contrasting the Effects of Maternal and Behavioral Characteristics on Fawn Birth Mass in White-Tailed Deer

Maternal care influences offspring quality and can improve a mother’s inclusive fitness. However, improved fitness may only occur when offspring quality (i.e., offspring birth mass) persists throughout life and enhances survival and/or reproductive success. Although maternal body mass, age, and social rank have been shown to influence offspring birth mass, the inter-dependence among these variables makes identifying causation problematic. We established that fawn birth mass was related to adult body mass for captive male and female white-tailed deer (Odocoileus virginianus), thus maternal care should improve offspring fitness. We then used path analysis to identify which maternal characteristic(s) most influenced fawn birth mass of captive female white-tailed deer. Maternal age, body mass and social rank had varying effects on fawn birth mass. Maternal body mass displayed the strongest direct effect on fawn birth mass, followed by maternal age and social rank. Maternal body mass had a greater effect on social rank than age. The direct path between social rank and fawn birth mass may indicate dominance as an underlying mechanism. Our results suggest that heavier mothers could use dominance to improve access to resources, resulting in increased fitness through production of heavier offspring.     

Primate Rituals: The Function of Greetings between Male Guinea Baboons

The bond‐testing hypothesis suggests that social animals can obtain honest information about the quality of their dyadic relationships by exchanging costly, high‐risk signals (Zahavi & Zahavi 1997). We evaluated this hypothesis by investigating whether adult male baboons use intense greeting interactions to test the quality and strength of their social bonds. Intense greetings involve intimate and risky behaviors such as embracing and the diddling of the penis and/or scrotum. Data were collected on a colony of 40 Guinea baboons (Papio papio) at the Brookfield Zoo in Chicago. Fifteen adult male baboons were focally observed for 30‐min sessions over a 6‐mo period, resulting in 195 h of observation. We assessed the quality of male–male relationships using measures of affiliation, aggression, and social tolerance. As predicted by the bond‐testing hypothesis, dyads with strong social bonds exchanged a higher frequency of intense greetings than did pairs with poor relationships. We found no support for the competing hypotheses, that suggest that greetings have an aggressive or submissive function or are used as a form of post‐conflict reconciliatory behavior. Neither dominance relationships nor contextual variables were predictive of intense greeting patterns. We suggest that by imposing on his partner, a male baboon is able to obtain reliable information about this individual's current willingness to cooperate and invest in the relationship.     

Life history in male mandrills (Mandrillus sphinx): physical development, dominance rank, and group association

We assess life history from birth to death in male mandrills (Mandrillus sphinx) living in a semifree-ranging colony in Gabon, using data collected for 82 males that attained at least the age of puberty, including 33 that reached adulthood and 25 that died, yielding data for their entire lifespan. We describe patterns of mortality and injuries, dominance rank, group association, growth and stature, and secondary sexual character expression across the male lifespan. We examine relationships among these variables and investigate potential influences on male life history, including differences in the social environment (maternal rank and group demography) and early development, with the aim of identifying characteristics of successful males. Sons of higher-ranking females were more likely to survive to adulthood than sons of low-ranking females. Adolescent males varied consistently in the rate at which they developed, and this variation was related to a male's own dominance rank. Males with fewer peers and sons of higher-ranking and heavier mothers also matured faster. However, maternal variables were not significantly related to dominance rank during adolescence, the age at which males attained adult dominance rank, or whether a male became alpha male. Among adult males, behavior and morphological development were related to a male's own dominance rank, and sons of high-ranking females were larger than sons of low-ranking females. Alpha males were always the most social, and the most brightly colored males, but were not necessarily the largest males present. Finally, alpha male tenure was related to group demography, with larger numbers of rival adult males and maturing adolescent males reducing the time a male spent as alpha male. Tenure did not appear to be related to characteristics of the alpha male himself.     

Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus

In many animals, variance in male mating success is strongly correlated with male dominance rank or some other measure of fighting ability. Studies in primates, however, have varied greatly in whether they detect a relationship between male dominance rank and mating success. This variability has led to debate about the nature of the relation between rank and mating success in male primates. We contribute to the resolution of this debate by presenting an analysis of the relationship between dominance rank and male mating success over 32 group-years in a population of wild savannah baboons. When data were pooled over the entire period, higher-ranking males had greater access to fertile females. However, when we examined successive 6-month blocks, we found variance in the extent to which rank predicted mating success. In some periods, the dominance hierarchy functioned as a queue in which males waited for mating opportunities, so that rank predicted mating success. In other periods, the queuing system broke down, and rank failed to predict mating success when many adult males were in the group, when males in the group differed greatly in age, and when the highest-ranking male maintained his rank for only short periods. The variance within this single population is similar to the variance observed between populations of baboons and between species of primates. Our long-term results provide strong support for the proposition that this variance is not an artefact of methodological differences between short-term studies, but is due to true variance in the extent to which high-ranking males are able to monopolize access to females. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.     

Sex-specific strategies of dentine depletion in red deer

Worn teeth in herbivore ungulates may be related to lower efficiency in mastication and hence lower performance. However, selection should favour maximal performance in terms of body mass and reproductive capacity during reproductive lifespan, when permanent teeth are already partially worn. We hypothesize that wear rate may respond to a strategy of use of tooth materials (notably dentine), which balances instantaneous wear rate and performance against tooth preservation for future performance and reproduction. In the present study, we investigated 4151 carcasses of Iberian red deer Cervus elaphus hispanicus and show that more worn molars were not related to lower performance throughout age. By comparing between sexes, tooth wear rates were smaller in females than in males, but the relationship between tooth wear and body performance also differed between the sexes: females did not show a significant relationship between tooth wear and performance but males with more worn teeth were in general heavier and had larger antlers until senile age, when more depleted teeth were related to smaller antlers. These results reveal, for the first time, sex-specific lifetime strategies of dentine expenditure: maintenance of performance ability throughout a longer reproductive lifespan in females, compared with maximizing current performance by depleting dentine reserves within a shorter lifespan in males.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 487–497.     

Hormonal correlates of changes in interest in unrelated infants across the peripartum period in female baboons (Papio hamadryas anubis sp.)

In past research on human and nonhuman primates, maternal responsiveness and behavior has been thought of as an experiential, cognitive mechanism; however, recent findings have shown that maternal motivation and behavior may not be entirely divorced from the endocrine system. To investigate the relationship between interest in infants and the hormonal changes related to pregnancy, we examined the nature of social interactions across parturition between a large sample (n = 133) of adult female baboons (Papio hamadryas anubis sp.) and unrelated infants. Prepartum data were collected during ten 30-min focal observations for each subject. Each mother-infant pair was then observed through the infant's first 8 weeks of life. A total of 2325 h of observation was recorded. Urine was collected on 65 subjects, starting 5 weeks before the expected date of parturition and ending 4 weeks after parturition. Evidence for a connection between endocrine function and responsiveness toward infants was found. Affiliative behaviors during the prepartum period were positively correlated to the estrogen/cortisol ratio and high dominance rank. In the postpartum period, affiliative behaviors were positively correlated with prepartum progesterone and dominance rank, and negatively correlated with postpartum cortisol levels. Finally, a positive correlation was recorded during the postpartum period between prepartum progesterone and aggression, and a negative correlation between postpartum cortisol and aggression and submission. Our data suggest that the endocrine changes that may help regulate maternal care of offspring also influence the way in which pre- and postpartum female baboons interact with unrelated infants in their social group.     

Paternal Relatedness Predicts the Strength of Social Bonds among Female Rhesus Macaques

Forming strong, equitable, and enduring social bonds with a few individuals in a group carries adaptive benefits in terms of increased longevity, offspring survival and paternity success in birds and mammals, including humans. These recent insights generated a new interest in the factors creating variation in the strength of social relationships. Whether and how animals discriminate paternal kin from non-kin and bias their social behavior accordingly is being debated. This study explores the relative importance of dominance rank, age, maternal and paternal relatedness in shaping dyadic affiliative relationships in a group of 30 captive rhesus macaque females. The strength of social relationships, measured by the composite sociality index from observational data, was independently predicted in GLMMs by both maternal and paternal relatedness as well as rank similarity. In addition, social bonds between paternal half-sisters were stronger than between distantly related kin suggesting that females biased their affiliative effort towards paternal relatives. Despite identical relatedness coefficients bonds between mothers and their daughters were three times as strong as those between full sisters. Together these results add to the growing body of evidence for paternal kin biases in affiliative behavior and highlight that females prefer descendent over lateral kin.