Systematic mapping of developmental milestones in wild chimpanzees.

Postnatal development is protracted relative to lifespan in many primates, including modern humans (Homo sapiens), facilitating the acquisition of key motor, communication and social skills that can maximize fitness later in life. Nevertheless, it remains unclear what evolutionary drivers led to extended immature periods. While the developmental milestone literature is well established in humans, insight we can gain from one-species models is limited. By comparing the timing of relatable developmental milestones in a closely related species, the chimpanzee (Pan troglodytes), we can gain further understanding of the evolution of such an extended developmental phase. To date, few studies have specifically attempted to estimate developmental milestones in a manner comparable to the human literature, and existing studies lack sufficient sample sizes to estimate which milestones are more plastic with higher inter-individual variation in the timing of their emergence. Here, we describe the emergence of gross motor, fine motor, social interaction and communication traits from a longitudinal sample of 19 wild chimpanzee infants (8 females and 11 males), Taï National Park, Côte d'Ivoire. Gross motor traits emerged at a mean of 4 months, communication traits at 12 months, social interaction traits at 14 months and fine motor traits at 15 months, with later emerging milestones demonstrating greater inter-individual variation in the timing of the emergence. This pattern of milestone emergence is broadly comparable to observations in humans, suggesting selection for a prolonged infantile phase and that sustained skills development has a deep evolutionary history, with implications for theories on primate brain development.

Information transfer efficiency differs in wild chimpanzees and bonobos, but not social cognition.

Several theories have been generated to understand the socio-cognitive mechanisms underlying the unique cooperative abilities of humans. The 'interdependence hypothesis' posits first, that the cognitive dimension of human cooperation evolved in contexts when several individuals needed to act together to achieve a common goal, like when hunting large prey. Second, the more interdependent individuals are, the more likely they are to provide services to conspecifics in other contexts. Alternatively, the 'social tolerance hypothesis' proposes that higher social tolerance allows conspecifics to cooperate more efficiently and with a wider range of partners. We conducted the first field experimental evaluation of both hypotheses in our closest living relatives by contrasting chimpanzees to the less interdependent but more tolerant bonobos. We compared each species' performance during a cooperative task: informing conspecifics about a danger. We presented Gaboon viper models to 82 individuals from five wild communities. Chimpanzees arriving late at the snake were significantly more likely to have heard a call and less likely to startle, indicating that chimpanzees were better informed about the presence of the threat than bonobos. This stems from clear species differences in how individuals adjusted their calling decisions to the level of information already available. Chimpanzees were more likely to call and produced more alarm calls when they had not yet heard a call, whereas bonobos did so when they already heard a call. Our results confirm the link between interdependence and cooperation performance. These species differences were most likely driven by differences in motivation rather than in cognitive capacities because both species tended to consider audience knowledge in their decision to call. Our results inform theories on the evolution of human cooperation by linking inter-group competition pressure and in-group cooperative motivation and/or capability.

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.

Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (Pan troglodytes verus).

BACKGROUND: In animals with altricial offspring, most growth occurs after birth and may be optimized by post-natal maternal care. Maternal effects on growth may be influenced by individual characteristics of the mothers, such as social status, individual investment strategies and the length of association with offspring. The prolonged juvenile dependence seen in humans is a distinctive life history adaptation, which may have evolved to facilitate sustained somatic and brain growth.In chimpanzees, offspring are typically weaned at approximately 4 years old, yet immature individuals continue to associate with their mothers for up to 10 years beyond weaning. Whether this lengthy association or the individual characteristics of mothers influences growth patterns in this species is not clear.The relationship between urinary creatinine and specific gravity is an established non-invasive measure of muscle mass in humans and chimpanzees. We analysed the urinary creatinine and specific gravity of 1318 urine samples from 70 wild chimpanzees from the Taï Forest, Ivory Coast aged 4 to 15 years. RESULTS: We showed a clear increase in urinary creatinine levels with age in both males and females, replicating established growth curves in this species and reaffirming this measure as a reliable proxy for lean body mass. Comparing those who experience maternal loss (orphans) with non-orphan chimpanzees, maternal presence beyond weaning age and into late juvenility positively influenced offspring muscle mass throughout ontogeny such that orphans had significantly less muscle mass than age-matched non-orphans. In age-matched offspring with mothers, those with high-ranking mothers had greater muscle mass. Accounting for variation in muscle mass attributable to maternal presence, we found no effect of maternal investment (length of inter birth interval, from own birth to birth of following sibling) on offspring muscle mass. CONCLUSION: Chimpanzee mothers have an extended and multi-faceted influence on offspring phenotypes. Our results suggest that maternal investment extends beyond lactation and into early adulthood and has clear benefits to offspring physical development. Therefore, prolonged juvenile dependence, although unique in its form in human societies, may be a trait with deeper evolutionary origins.

Social uncertainty promotes signal complexity during approaches in wild chimpanzees (Pan troglodytes verus) and mangabeys (Cercocebus atys atys).

The social complexity hypothesis for the evolution of communication posits that complex social environments require greater communication complexity for individuals to effectively manage their relationships. We examined how different socially uncertain contexts, reflecting an increased level of social complexity, relate to variation in signalling within and between two species, which display varying levels of fission-fusion dynamics (sympatric-living chimpanzees and sooty mangabeys, Taï National Park, Ivory Coast). Combined signalling may improve message efficacy, notably when involving different perception channels, thus may increase in moments of high social uncertainty. We examined the probability of individuals to emit no signal, single or multisensory or combined (complex) signals, during social approaches which resulted in non-agonistic outcomes. In both species, individuals were more likely to use more combined and multisensory signals in post-conflict approaches with an opponent than in other contexts. The clearest impact of social uncertainty on signalling complexity was observed during chimpanzee fusions, where the likelihood of using complex signals tripled relative to other contexts. Overall, chimpanzees used more multisensory signals than mangabeys. Social uncertainty may shape detected species differences in variation in signalling complexity, thereby supporting the hypothesis that social complexity, particularly associated with high fission-fusion dynamics, promotes signalling complexity.

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.

Maternal effects on the development of vocal communication in wild chimpanzees.

Early-life experiences, such as maternal care received, influence adult social integration and survival. We examine what changes to social behavior through ontogeny lead to these lifelong effects, particularly whether early-life maternal environment impacts the development of social communication. Chimpanzees experience prolonged social communication development. Focusing on a central communicative trait, the "pant-hoot" contact call used to solicit social engagement, we collected cross-sectional data on wild chimpanzees (52 immatures and 36 mothers). We assessed early-life socioecological impacts on pant-hoot rates across development, specifically: mothers' gregariousness, age, pant-hoot rates and dominance rank, maternal loss, and food availability, controlling for current maternal effects. We found that early-life maternal gregariousness correlated positively with offspring pant-hoot rates, while maternal loss led to reduced pant-hoot rates across development. Males had steeper developmental trajectories in pant-hoot rates than females. We demonstrate the impact of maternal effects on developmental trajectories of a rarely investigated social trait, vocal production.

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 chimpanzees. Compensatory mechanisms, such as adoption, may buffer against certain physiological effects of maternal loss in this species.

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

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.

Maternal cannibalism in two populations of wild chimpanzees.

Maternal cannibalism has been reported in several animal taxa, prompting speculations that the behavior may be part of an evolved strategy. In chimpanzees, however, maternal cannibalism has been conspicuously absent, despite high levels of infant mortality and reports of non-maternal cannibalism. The typical response of chimpanzee mothers is to abandon their deceased infant, sometimes after prolonged periods of carrying and grooming the corpse. Here, we report two anomalous observations of maternal cannibalism in communities of wild chimpanzees in Uganda and Ivory Coast and discuss the evolutionary implications. Both infants likely died under different circumstances; one apparently as a result of premature birth, the other possibly as a result of infanticide. In both cases, the mothers consumed parts of the corpse and participated in meat sharing with other group members. Neither female presented any apparent signs of ill health before or after the events. We concluded that, in both cases, cannibalizing the infant was unlikely due to health-related issues by the mothers. We discuss these observations against a background of chimpanzee mothers consistently refraining from maternal cannibalism, despite ample opportunities and nutritional advantages. We conclude that maternal cannibalism is extremely rare in this primate, likely due to early and strong mother-offspring bond formation, which may have been profoundly disrupted in the current cases.

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, that is, 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 nonmanipulated 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. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Correction to: 'Behavioural thermoregulation via microhabitat selection of winter sleeping areas in an endangered primate: implications for habitat conservation'.

[This corrects the article DOI: 10.1098/rsos.181113.].

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

Individuals with more or stronger social bonds experience enhanced survival and reproduction in various species, though the mechanisms mediating these effects are unclear. Social thermoregulation is a common behaviour across many species which reduces cold stress exposure, body heat loss, and homeostatic energy costs, allowing greater energetic investment in growth, reproduction, and survival, with larger aggregations providing greater benefits. If more social individuals form larger thermoregulation aggregations due to having more potential partners, this would provide a direct link between sociality and fitness. We conducted the first test of this hypothesis by studying social relationships and winter sleeping huddles in wild Barbary macaques (Macaca sylvanus), wherein individuals with more social partners experience greater probability of winter survival. Precipitation and low temperature increased huddle sizes, supporting previous research that huddle size influences thermoregulation and energetics. Huddling relationships were predicted by social (grooming) relationships. Individuals with more social partners therefore formed larger huddles, suggesting reduced energy expenditure and exposure to environmental stressors than less social individuals, potentially explaining how sociality affects survival in this population. This is the first evidence that social thermoregulation may be a direct proximate mechanism by which increased sociality enhances fitness, which may be widely applicable across taxa.

Behavioural thermoregulation via microhabitat selection of winter sleeping areas in an endangered primate: implications for habitat conservation.

Strategic microhabitat selection allows animals in seasonally cold environments to reduce homeostatic energy costs, particularly overnight when thermoregulatory demands are greatest. Suitable sleeping areas may therefore represent important resources for winter survival. Knowledge of microhabitat use and potential impacts of anthropogenic habitat modification can aid species conservation through development of targeted habitat management plans. Wild, endangered Barbary macaques (Macaca sylvanus) in logged cedar-oak forest were studied to investigate (1) the hypothesis that macaques select winter sleeping areas with microhabitat characteristics that may reduce thermoregulatory costs, and, if so, (2) how to minimize damage to sleeping areas from logging. Macaques slept only in Atlas cedars (Cedrus atlantica). Consistent with predictions, macaques preferred sleeping in sheltered topography and dense vegetation, which may reduce exposure to wind, precipitation and cold, and preferred large trees that facilitate social huddling. This suggests that Barbary macaques employ strategic nocturnal microhabitat selection to reduce thermoregulatory costs and thus suitable sleeping areas may influence winter survival. To minimize negative impacts of logging on macaque sleeping areas, results suggest avoiding logging in topographical depressions and maintaining cedar densities greater than 250 ha-1 with average breast height greater than 60 cm. This study demonstrates how animal behaviour can be used to guide species-specific habitat management plans.

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.

Effect of Australian tea tree oil on Gyrodactylus spp. infection of the three-spined stickleback Gasterosteus aculeatus.

Gyrodactylus spp. infections of commercially farmed fishes are responsible for significant economic losses. Existing treatments have proved uneconomic, stressful to the fishes, and ecologically damaging. Essential oils are naturally occurring compounds that exhibit a wide range of anti-microbial and anti-fungal activities. This study explored the possibility of using Australian tea tree (Melaleuca alternifolia) oil (TTO) to treat Gyrodactylus spp. infection on the three-spined stickleback Gasterosteus aculeatus. In the presence of 0.01 % Tween 80 as an emulsifier, TTO treatments at concentrations between 3 and 30 ppmv (parts per million by volume) lowered the prevalence and significantly reduced the parasite burden of sticklebacks naturally infected with Gyrodactylus spp. In addition, Tween 80 alone exhibited parasiticidal activity against Gyrodactylus spp. These findings show the potential of TTO in combination with Tween 80 as an effective treatment of Gyrodactylus spp. infection of fishes.

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.