Early maternal loss leads to short-but not long-term effects on diurnal cortisol slopes in wild chimpanzees

The biological embedding model (BEM) suggests that fitness costs of maternal loss arise when early-life experience embeds long-term alterations to hypothalamic-pituitary-adrenal (HPA) axis activity. Alternatively, the adaptive calibration model (ACM) regards physiological changes during ontogeny as short-term adaptations. Both models have been tested in humans but rarely in wild, long-lived animals. We assessed whether, as in humans, maternal loss had short-and long-term impacts on orphan wild chimpanzee urinary cortisol levels and diurnal urinary cortisol slopes, both indicative of HPA axis functioning. Immature chimpanzees recently orphaned and/or orphaned early in life had diurnal cortisol slopes reflecting heightened activation of the HPA axis. However, these effects appeared short-term, with no consistent differences between orphan and non-orphan cortisol profiles in mature males, suggesting stronger support for the ACM than the BEM in wild chimpan-zees. Compensatory mechanisms, such as adoption, may buffer against certain physiological effects of maternal loss in this species

Patterns of urinary cortisol levels during ontogeny appear population specific rather than species specific in wild chimpanzees and bonobos

Compared with most mammals, postnatal development in great apes is protracted, presenting both an extended period of phenotypic plasticity to environmental conditions and the potential for sustained mother-offspring and/or sibling conflict over resources. Comparisons of cortisol levels during ontogeny can reveal physiological plasticity to species or population specific socioecological factors and in turn how these factors might ameliorate or exaggerate mother-offspring and sibling conflict. Here, we examine developmental patterns of cortisol levels in two wild chimpanzee populations (Budongo and Taï), with two and three communities each, and one wild bonobo population (LuiKotale), with two communities. Both species have similar juvenile life histories. Nonetheless, we predicted that key differences in socioecological factors, such as feeding competition, would lead to interspecific variation in mother-offspring and sibling conflict and thus variation in ontogenetic cortisol patterns. We measured urinary cortisol levels in 1394 samples collected from 37 bonobos and 100 chimpanzees aged up to 12 years. The significant differences in age-related variation in cortisol levels appeared population specific rather than species specific. Both bonobos and Taï chimpanzees had comparatively stable and gradually increasing cortisol levels throughout development; Budongo chimpanzees experienced declining cortisol levels before increases in later ontogeny. These age-related population differences in cortisol patterns were not explained by mother-offspring or sibling conflict specifically; instead, the comparatively stable cortisol patterns of bonobos and Taï chimpanzees likely reflect a consistency in experience of competition and the social environment compared with Budongo chimpanzees, where mothers may adopt more variable strategies related to infanticide risk and resource availability. The clear population-level differences within chimpanzees highlight potential intraspecific flexibility in developmental processes in apes, suggesting the flexibility and diversity in rearing strategies seen in humans may have a deep evolutionary history.Publisher PDFPeer reviewe

Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees

Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.Additional co-authors: Klaus Zuberbuehler, Linda Vigilant, Tobias Deschner, Roman M. Wittig & Catherine Crockfor

Behavioral responses to injury and death in wild Barbary macaques (Macaca sylvanus)

The wounding or death of a conspecific has been shown to elicit varied behavioral responses throughout thanatology. Recently, a number of reports have presented contentious evidence of epimeletic behavior towards the dying and dead among non-human animals, a behavioral trait previously considered uniquely human. Here, we report on the behavioral responses of Barbary macaques, a social, non-human primate, to the deaths of four group members (one high-ranking adult female, one high-ranking adult male, one juvenile male, and one female infant), all caused by road traffic accidents. Responses appeared to vary based on the nature of the death (protracted or instant) and the age class of the deceased. Responses included several behaviors with potential adaptive explanations or consequences. These included exploration, caretaking (guarding, carrying, and grooming), and proximity to wounded individuals or corpses, and immediate as well as longer-lasting distress behaviors from other group members following death, all of which have been reported in other non-human primate species. These observations add to a growing body of comparative evolutionary analysis of primate thanatology and help to highlight the multifaceted impacts of human-induced fatalities on an endangered and socially complex primate. © 2016, Japan Monkey Centre and Springer Japan

Measuring personality in the field: An in situ comparison of personality quantification methods in wild Barbary Macaques (Macaca sylvanus)

Three popular approaches exist for quantifying personality in animals: behavioral coding in unconstrained and experimental settings and trait assessment. Both behavioral coding in an unconstrained setting and trait assessment aim to identify an overview of personality structure by reducing the behavioral repertoire of a species into broad personality dimensions, whereas experimental assays quantify personality as reactive tendencies to particular stimuli. Criticisms of these methods include that they generate personality dimensions with low levels of cross-study or cross-species comparability (behavioral coding in unconstrained and experimental settings) or that the personality dimensions generated are not ecologically valid, i.e. not reflecting naturally occurring behavior (trait assessment and experimental assays). Which method is best for comparative research is currently debated and there is presently a paucity of personality research conducted in wild subjects. In our study, all three described methods are used to quantify personality in a wild animal subject, the Barbary macaque (Macaca sylvanus). Our results show that the structures generated by unconstrained behavioral coding and trait assessment were not equivalent. Personality dimensions derived from both trait assessments and experimental assays demonstrated low levels of ecological validity, with very limited correlation with behaviors observed in non-manipulated circumstances. Our results reflect the methodological differences between these quantification methods. Based on these findings and the practical considerations of wild animal research, we suggest future comparative studies of quantification methods within similar methodological frameworks to best identify methods viable for future comparisons of personality structures in wild animals

Social thermoregulation as a potential mechanism linking sociality and fitness: Barbary macaques with more social partners form larger huddles [dataset]

This is the dataset attached to the paper "Social thermoregulation as a potential mechanism linking sociality and fitness: Barbary macaques with more social partners form larger huddles

The function of chimpanzee greeting calls is modulated by their acoustic variation

Signalling plays an important role in mediating social interactions in many animal species. For example, during approaches certain species produce ‘greetings’, which can take the form of vocal or visual signals, which reduce the probability of aggressive interactions and/or facilitate affiliation when approaching each other. However, in species where greetings comprise both vocal and visual signals, little is known about how the vocal component relates to the visual component or, in species with fission–fusion dynamics, to the time spent together by the dyad in the same subgroup prior to the approach. Similarly, in species with several acoustic variants of greeting calls, it is unclear whether different variants have different functions. We looked at the production of two acoustically distinct greeting call variants, low-fundamental frequency pant grunts and high-fundamental frequency pant barks, during approaches between two individuals in five communities of wild chimpanzees, Pan troglodytes, in Uganda and Ivory Coast. More specifically, we explored the relationship between greeting call production and (1) aggressive and submissive interactions during the approach and (2) preceding and subsequent proximity levels between the involved individuals. Calls were more likely to be produced during aggressive interactions and were associated with postures and gestures linked to submission; these patterns were stronger when the utterance contained a pant bark rather than a pant grunt alone. The production of greeting calls was more likely soon after party fusion and was negatively related to subsequent proximity levels between the caller and receiver. These results expand our knowledge of greeting calls and imply that these calls might be used to re-establish dominance relationships after a period of separation, and that the function of these calls can be modulated by their specific acoustic variants and by visual signals that often accompany them

Long-term repeatability in social behaviour suggests stable social phenotypes in wild chimpanzees

Core funding for the Taï Chimpanzee Project is provided by the Max Planck Society since 1997. P.J.T., C.C. and R.M.W. were supported by the European Research Council (ERC; grant agreement no. 679787). L.S. was supported by the Minerva Foundation. A.P. was supported by the Leakey Foundation. A.M. was supported by the Wenner-Gren Foundation and a British Academy Newton International Fellowship.Consistent individual differences in social phenotypes have been observed in many animal species. Changes in demographics, dominance hierarchies or ecological factors, such as food availability or disease prevalence, are expected to influence decision-making processes regarding social interactions. Therefore, it should be expected that individuals show flexibility rather than stability in social behaviour over time to maximize the fitness benefits of social living. Understanding the processes that create and maintain social phenotypes requires data encompassing a range of socioecological settings and variation in intrinsic state or life-history stage or strategy. Using observational data spanning up to 19 years for some individuals, we demonstrate that multiple types of social behaviour are repeatable over the long term in wild chimpanzees, a long-lived species with complex fission–fusion societies. We controlled for temporal, ecological and demographic changes, limiting pseudo-repeatability. We conclude that chimpanzees living in natural ecological settings have relatively stable long-term social phenotypes over years that may be independent of life-history or reproductive strategies. Our results add to the growing body of the literature suggesting consistent individual differences in social tendencies are more likely the rule rather than the exception in group-living animals.Publisher PDFPeer reviewe