Bystanders, parcelling, and an absence of trust in the grooming interactions of wild male chimpanzees

The evolution of cooperation remains a central issue in socio-biology with the fundamental problem of how individuals minimize the risks of being short-changed (‘cheated’) should their behavioural investment in another not be returned. Economic decisions that individuals make during interactions may depend upon the presence of potential partners nearby, which o ers co operators a temptation to defect from the current partner. The parcelling model posits that donors subdivide services into parcels to force cooperation, and that this is contingent on opportunities for defection; that is, the presence of bystanders. Here we test this model and the e ect of bystander presence using grooming interactions of wild chimpanzees. We found that with more bystanders, initiators gave less grooming at the beginning of the bout and were more likely to abandon a grooming bout, while bouts were less likely to be reciprocated. We also found that the groomer’s initial investment was not higher among frequent groomers or stronger reciprocators, suggesting that contrary to current assumptions, grooming decisions are not based on trust, or bonds, within dyads. Our work highlights the importance of considering immediate social context and the in uence of bystanders for understanding the evolution of the behavioural strategies that produce cooperation

Anogenital scent-marking signals fertility in a captive female Alaotran gentle lemur

The Lake Alaotra gentle lemur (Hapalemur alaotrensis) is one of the 25 most endangered primates in the world and shows low success rate in captive breeding programmes. It is therefore vital to further understand its reproductive biology. We studied a captive troop consisting of five individuals hosted at Jersey Zoo during breeding and non-breeding periods over 1 year. We collected behavioural data (n = 318 h) using all occurrence of some behaviours and ad libitum sampling methods, as well as faecal (n = 54) and anogenital scent (n = 35) samples of the breeding female. We measured sex hormone levels using enzyme immunoassay technique and investigated the volatile component of odour signals using solid-phase microextraction and gas chromatography-mass spectrometry. We observed sexual and aggressive behaviours occasionally during the breeding period. Our regression analysis showed that only period significantly predicted rates of female anogenital scent-marking, whereby the female performed anogenital scent-marking more frequently during the breeding rather than the non-breeding period. In contrast, female hormone levels did not significantly explain variation in rates of neither male nor female olfactory, sexual and affiliative behaviours, suggesting that individuals' behaviour alone is not an effective indicator of the ovulation window. The volatile chemical profile of anogenital odour secretions changed over the study, with four compounds distinguishing the fertile window during the breeding period. In conclusion, our findings suggest that anogenital scent-marking may signal the reproductive status of captive female gentle lemurs

Relationships between affiliative social behavior and hair cortisol concentrations in semi-free ranging rhesus monkeys

Sociality is a fundamental aspect of human behavior and health. One benefit of affiliative social relationships is reduced short-term levels of glucocorticoids (GCs), which are indicative of physiological stress. Less is known, however, about chronic GC production in relation to affiliative social behavior. To address this issue, we studied a semi-free ranging troop of rhesus macaques (Macaca mulatta) and collected hair samples to measure hair cortisol concentrations (HCCs), as a measure of chronic GC production, during routine biannual exams. We collected social behavior (both aggressive and affiliative) and hair samples for 32 adult female rhesus macaques over one year (Experiment 1). Our results indicated that adult females who initiated higher levels of social affiliation had significantly lower levels of HCCs. Neither the initiation nor the receipt of aggression were significantly related to HCCs in this study. In a second experiment we studied 28 mother-infant dyads for the first 90 days postpartum to examine mother-infant facial interactions (i.e. mutual gazing). We analyzed HCCs during weaning approximately one year later, which is a major transitional period. We found that infants that engaged in higher levels of mutual gazing in the first 90 days postpartum had significantly lower levels of HCCs during weaning. Finally, we studied 17 infant rhesus macaques (13 males) to examine whether social behavior (such as play) in the first five months of life correlated with infant HCCs over those months (Experiment 3). We found that infant males that engaged in more social play had significantly lower levels of HCCs. By relying on an animal model, our study shows that affiliative social traits are associated with lower long-term GC production. Future research should address the complex interactions between social behavior, chronic GC production, and mental and physical health

Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys

In primates, including humans, mothers engage in face-to-face interactions with their infants, with frequencies varying both within and across species. However, the impact of this variation in face-to-face interactions on infant social development is unclear. Here we report that infant monkeys (Macaca mulatta) who engaged in more neonatal face-to-face interactions with mothers have increased social interactions at 2 and 5 months. In a controlled experiment, we show that this effect is not due to physical contact alone: monkeys randomly assigned to receive additional neonatal face-to-face interactions (mutual gaze and intermittent lip-smacking) with human caregivers display increased social interest at 2 months, compared with monkeys who received only additional handling. These studies suggest that face-to-face interactions from birth promote young primate social interest and competenc

Interactions with humans impose time constraints on urban-dwelling rhesus macaques (Macaca mulatta)

Time is a valuable but limited resource, and animals’ survival depends on their ability to carefully manage the amount of time they allocate to each daily activity. While existing research has examined the ecological factors affecting animals’ activity budgets, the impact of anthropogenic factors on urban dwelling animals’ time budgets remains understudied. Here we collected data through focal animal sampling from three groups of rhesus macaques in Northern India to examine whether interactions with humans decrease macaques’ resting and social time (time constraints hypothesis), or whether, by contrast, foraging on anthropogenic food, that is potentially high in calories, leads macaques to spend more time resting and in social interactions (free time hypothesis). We found that macaques who interacted more frequently with people spent significantly less time resting and grooming, supporting the time constraints hypothesis. We argue that these time constraints are likely caused by the unpredictability of human behavior.National Science Foundatio

Matrilineal behavioral and physiological changes following the death of a non-alpha matriarch in rhesus macaque

In many species, the loss of alpha matriarchs is associated with a number of negative outcomes such as troop fission, eviction, wounding, and reduced vitality. However, whether the dramatic consequences of their loss are due to their role as an old experienced figure or to their alpha status remains unclear. In a retrospective study, we tested that in a semi-free ranging colony of rhesus macaques (Macaca mulatta), the removal of a non-alpha matriarch, who had a large set of kin, led to changes in behavior and physiological stress within her matriline. Following her removal, her matriline increased in aggression, vigilance, and social grooming. Additionally, hierarchical stability, measured by levels of rank changes, decreased within her matriline, and levels of intense aggression by high-ranking animals were more frequent, as well as matrilineal wounding. Although ordinal rank was positively associated with higher chronic hair cortisol concentrations (HCCs) in the months before the matriarch’s removal, following her removal, only those who experienced large increases in rank within her matriline displayed higher HCCs. Changes in matrilineal stability, aggression, behavior, and HCCs within the other two matrilines in the troop were not evident, although caution is needed due to the small sample sizes. We conclude that the removal of the non-alpha matriarch led to matrilineal instability, characterized by higher levels of aggression and subsequent vigilance, rank changes, physiological stress, and grooming. We suggest that non-alpha matriarchs with a large number of kin and social support can be integral to the stability of matrilines.Division of Intramural Research, National Institute of Child Health and Human Development, 1ZIAHD001107- 3

Trading or coercion? Variation in male mating strategies between two communities of East African chimpanzees

Across taxa, males employ a variety of mating strategies, including sexual coercion and the provision, or trading, of resources. Biological Market theory (BMT) predicts that trading of commodities for mating opportunities should exist only when males cannot monopolise access to females and/or obtain mating by force, in situations where power differentials between males are low; both coercion and trading have been reported for chimpanzees (Pan troglodytes). Here, we investigate whether the choice of strategy depends on the variation in male power differentials, using data from two wild communities of East African chimpanzees (P.t. schweinfurthii): the structurally despotic Sonso community (Budongo, Uganda) and the structurally egalitarian M-group (Mahale, Tanzania). We found evidence of sexual coercion by male Sonso chimpanzees, and of trading—of grooming for mating—by M-group males; females traded sex for neither meat nor protection from male aggression. Our results suggest that the despotism–egalitarian axis influences strategy choice: male chimpanzees appear to pursue sexual coercion when power differentials are large and trading when power differentials are small and coercion consequently ineffective. Our findings demonstrate that trading and coercive strategies are not restricted to particular chimpanzee subspecies; instead, their occurrence is consistent with BMT predictions. Our study raises interesting, and as yet unanswered, questions regarding female chimpanzees’ willingness to trade sex for grooming, if doing so represents a compromise to their fundamentally promiscuous mating strategy. It highlights the importance of within-species cross-group comparisons and the need for further study of the relationship between mating strategy and dominance steepness

Object manipulation and tool use in Nicobar long-tailed macaques (Macaca fascicularis umbrosus)

This is an accepted manuscript of an article published by Springer in International Journal of Primatology on 08/09/2020, available online: https://link.springer.com/article/10.1007%2Fs10764-020-00141-y The accepted version of the publication may differ from the final published version.Object manipulation and tool use by non-human primates have received considerable attention from primatologists and anthropologists, because of their broad implications for understanding the evolution of tool use in humans. To date, however, most of the studies on this topic have focused on apes, given their close evolutionary relationship with humans. In contrast, fewer studies on tool use and object manipulation have been conducted on monkeys. Documenting and studying object manipulation and tool use in species that are more distantly related to humans can provide a broader perspective on the evolutionary origins of this behaviour. We present a detailed description of toolaided behaviours and object manipulation by Nicobar long-tailed macaques ( Macaca fascicularis umbrosus ) living along the coastlines of Great Nicobar Island. We made observations from December 2018 to March 2019, using ad libitum and focal sampling methods. We observed behaviours related to object manipulation and tool use in six different behavioural contexts (foraging, hygiene, communication, play, selfdirected and self-hygiene behaviour) involving eight different types of objects, namely resonance rod, play object, rolling platform, scraping tool, dental groom, pounding substrate, leaves as grip pads and wipers, and stimulation tool. We observed that males were involved in tool use and object manipulation more frequently than females. Our results add to existing records of object manipulation, tool-use behaviour and tool variants displayed by non-human primates, showing that Nicobar macaques perform multiple and diverse tool-aided behaviours

Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques

Rationale: Exogenous oxytocin administration is widely reported to improve social cognition in human and nonhuman primate adults. Risk factors of impaired social cognition, however, emerge in infancy. Early interventions—when plasticity is greatest—are critical to reverse negative outcomes. Objective: We tested the hypothesis that oxytocin may exert similar positive effects on infant social cognition, as in adults. To test this idea, we assessed the effectiveness of acute, aerosolized oxytocin on two foundational social cognitive skills: working memory (i.e., ability to briefly hold and process information) and social gaze (i.e., tracking the direction of others’ gaze) in 1-month-old nursery-reared macaque monkeys (Macaca mulatta). We did not predict sex differences, but we included sex as a factor in our analyses to test whether our effects would be generalizable across both males and females. Results: In a double-blind, placebo-controlled design, we found that females were more socially skilled at baseline compared to males, and that oxytocin improved working memory and gaze following, but only in males. Conclusions: These sex differences, while unexpected, may be due to interactions with gonadal steroids and may be relevant to sexually dimorphic disorders of social cognition, such as male-biased autism spectrum disorder, for which oxytocin has been proposed as a potential treatment. In sum, we report the first evidence that oxytocin may influence primate infant cognitive abilities. Moreover, these behavioral effects appear sexually dimorphic, highlighting the importance of considering sex differences. Oxytocin effects observed in one sex may not be generalizable to the other sex